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Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Review

Reactive oxygen species and male reproductive hormones

Authors: Mahsa Darbandi, Sara Darbandi, Ashok Agarwal, Pallav Sengupta, Damayanthi Durairajanayagam, Ralf Henkel, Mohammad Reza Sadeghi

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

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Abstract

Reports of the increasing incidence of male infertility paired with decreasing semen quality have triggered studies on the effects of lifestyle and environmental factors on the male reproductive potential. There are numerous exogenous and endogenous factors that are able to induce excessive production of reactive oxygen species (ROS) beyond that of cellular antioxidant capacity, thus causing oxidative stress. In turn, oxidative stress negatively affects male reproductive functions and may induce infertility either directly or indirectly by affecting the hypothalamus-pituitary-gonadal (HPG) axis and/or disrupting its crosstalk with other hormonal axes. This review discusses the important exogenous and endogenous factors leading to the generation of ROS in different parts of the male reproductive tract. It also highlights the negative impact of oxidative stress on the regulation and cross-talk between the reproductive hormones. It further describes the mechanism of ROS-induced derangement of male reproductive hormonal profiles that could ultimately lead to male infertility. An understanding of the disruptive effects of ROS on male reproductive hormones would encourage further investigations directed towards the prevention of ROS-mediated hormonal imbalances, which in turn could help in the management of male infertility.
Literature
1.
2.
go back to reference Swan SH, Elkin EP, Fenster L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect. 2000;108(10):961.PubMedPubMedCentralCrossRef Swan SH, Elkin EP, Fenster L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect. 2000;108(10):961.PubMedPubMedCentralCrossRef
3.
go back to reference Rolland M, Le Moal J, Wagner V, Royère D, De Mouzon J. Decline in semen concentration and morphology in a sample of 26 609 men close to general population between 1989 and 2005 in France. Hum Reprod. 2012;28(2):462–70.PubMedPubMedCentralCrossRef Rolland M, Le Moal J, Wagner V, Royère D, De Mouzon J. Decline in semen concentration and morphology in a sample of 26 609 men close to general population between 1989 and 2005 in France. Hum Reprod. 2012;28(2):462–70.PubMedPubMedCentralCrossRef
4.
go back to reference Sengupta P, Dutta S, Krajewska-Kulak E. The disappearing sperms: analysis of reports published between 1980 and 2015. Am J Mens Health. 2017;11(4):1279–1304. Sengupta P, Dutta S, Krajewska-Kulak E. The disappearing sperms: analysis of reports published between 1980 and 2015. Am J Mens Health. 2017;11(4):1279–1304.
5.
go back to reference Sikka SC. Relative impact of oxidative stress on male reproductive function. Curr Med Chem. 2001;8(7):851–62.PubMedCrossRef Sikka SC. Relative impact of oxidative stress on male reproductive function. Curr Med Chem. 2001;8(7):851–62.PubMedCrossRef
6.
go back to reference Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J Exp Biol. 2005;43(11):963–74.PubMed Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J Exp Biol. 2005;43(11):963–74.PubMed
7.
go back to reference Rakhit M, Gokul SR, Agarwal A, du Plessis SS. Antioxidant strategies to overcome OS in IVF-embryo transfer. In: Studies on Women’s Health. Editors: Agarwal, A., Aziz, N. and Rizk, B. Humana Press, Springer Science+Business Media, New York; 2013. p. 237–262. Rakhit M, Gokul SR, Agarwal A, du Plessis SS. Antioxidant strategies to overcome OS in IVF-embryo transfer. In: Studies on Women’s Health. Editors: Agarwal, A., Aziz, N. and Rizk, B. Humana Press, Springer Science+Business Media, New York; 2013. p. 237–262.
8.
go back to reference Barazani Y, Katz BF, Nagler HM, Stember DS. Lifestyle, environment, and male reproductive health. Urol Clin North Am. 2014;41(1):55–66.PubMedCrossRef Barazani Y, Katz BF, Nagler HM, Stember DS. Lifestyle, environment, and male reproductive health. Urol Clin North Am. 2014;41(1):55–66.PubMedCrossRef
10.
go back to reference Darbandi S, Darbandi M. Lifestyle modifications on further reproductive problems. Cresco J Reprod Sci. 2016;1(1):1–2. Darbandi S, Darbandi M. Lifestyle modifications on further reproductive problems. Cresco J Reprod Sci. 2016;1(1):1–2.
11.
go back to reference Hardy MP, Gao H-B, Dong Q, Ge R, Wang Q, Chai WR, et al. Stress hormone and male reproductive function. Cell Tissue Res. 2005;322(1):147–53.PubMedCrossRef Hardy MP, Gao H-B, Dong Q, Ge R, Wang Q, Chai WR, et al. Stress hormone and male reproductive function. Cell Tissue Res. 2005;322(1):147–53.PubMedCrossRef
12.
go back to reference Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS, Soto AM, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30(4):293–342.PubMedPubMedCentralCrossRef Diamanti-Kandarakis E, Bourguignon J-P, Giudice LC, Hauser R, Prins GS, Soto AM, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30(4):293–342.PubMedPubMedCentralCrossRef
13.
go back to reference Spiers JG, Chen HJ, Sernia C, Lavidis NA. Activation of the hypothalamic-pituitary-adrenal stress axis induces cellular oxidative stress. Front Neurosci. 2014;8:456.PubMed Spiers JG, Chen HJ, Sernia C, Lavidis NA. Activation of the hypothalamic-pituitary-adrenal stress axis induces cellular oxidative stress. Front Neurosci. 2014;8:456.PubMed
14.
go back to reference Appasamy M, Muttukrishna S, Pizzey A, Ozturk O, Groome N, Serhal P, et al. Relationship between male reproductive hormones, sperm DNA damage and markers of oxidative stress in infertility. Reprod BioMed Online. 2007;14(2):159–65.PubMedCrossRef Appasamy M, Muttukrishna S, Pizzey A, Ozturk O, Groome N, Serhal P, et al. Relationship between male reproductive hormones, sperm DNA damage and markers of oxidative stress in infertility. Reprod BioMed Online. 2007;14(2):159–65.PubMedCrossRef
15.
go back to reference Baker H, Burger H, de Kretser D, Hudson B (1986) Relative incidence of etiologic disorders in male infertility. In: Santen RJ, Swerdloff RS (eds) Male reproductive dysfunction: diagnosis and management of hypogonadism, infertility and impotence. Marcel Dekker, New York, pp 341–372. Baker H, Burger H, de Kretser D, Hudson B (1986) Relative incidence of etiologic disorders in male infertility. In: Santen RJ, Swerdloff RS (eds) Male reproductive dysfunction: diagnosis and management of hypogonadism, infertility and impotence. Marcel Dekker, New York, pp 341–372.
16.
go back to reference Santen R, Paulsen C. Hypogonadotropic eunuchoidism. I. Clinical study of the mode of inheritance. J Clin Endocrinol Metab. 1973;36(1):47–54.PubMedCrossRef Santen R, Paulsen C. Hypogonadotropic eunuchoidism. I. Clinical study of the mode of inheritance. J Clin Endocrinol Metab. 1973;36(1):47–54.PubMedCrossRef
17.
go back to reference Kavoussi P, Costabile RA, Salonia A. Clinical urologic endocrinology: principles for Men’s health. London: Springer; 2012. Kavoussi P, Costabile RA, Salonia A. Clinical urologic endocrinology: principles for Men’s health. London: Springer; 2012.
18.
go back to reference Jameson JL. Harrison’s endocrinology, 4E. New York: McGraw-Hill Education; 2016. Jameson JL. Harrison’s endocrinology, 4E. New York: McGraw-Hill Education; 2016.
19.
go back to reference Patton PE, Battaglia DE. Office andrology. New York: Humana Press; 2007. Patton PE, Battaglia DE. Office andrology. New York: Humana Press; 2007.
20.
go back to reference Byrd W, Bennett MJ, Carr BR, Dong Y, Wians F, Rainey W. Regulation of biologically active dimeric inhibin a and B from infancy to adulthood in the male. J Clin Endocrinol Metab. 1998;83(8):2849–54.PubMedCrossRef Byrd W, Bennett MJ, Carr BR, Dong Y, Wians F, Rainey W. Regulation of biologically active dimeric inhibin a and B from infancy to adulthood in the male. J Clin Endocrinol Metab. 1998;83(8):2849–54.PubMedCrossRef
21.
go back to reference Raivio T, Perheentupa A, McNeilly AS, Groome NP, Anttila R, Siimes MA, et al. Biphasic increase in serum inhibin B during puberty: a longitudinal study of healthy Finnish boys. Pediatr Res. 1998;44(4):552–6.PubMedCrossRef Raivio T, Perheentupa A, McNeilly AS, Groome NP, Anttila R, Siimes MA, et al. Biphasic increase in serum inhibin B during puberty: a longitudinal study of healthy Finnish boys. Pediatr Res. 1998;44(4):552–6.PubMedCrossRef
22.
go back to reference Mancini A, Festa R, Silvestrini A, Nicolotti N, Di Donna V, La Torre G, et al. Hormonal regulation of total antioxidant capacity in seminal plasma. J Androl. 2009;30(5):534–40.PubMedCrossRef Mancini A, Festa R, Silvestrini A, Nicolotti N, Di Donna V, La Torre G, et al. Hormonal regulation of total antioxidant capacity in seminal plasma. J Androl. 2009;30(5):534–40.PubMedCrossRef
23.
go back to reference Parker CR. Dehydroepiandrosterone and dehydroepiandrosterone sulfate production in the human adrenal during development and aging. Steroids. 1999;64(9):640–7.PubMedCrossRef Parker CR. Dehydroepiandrosterone and dehydroepiandrosterone sulfate production in the human adrenal during development and aging. Steroids. 1999;64(9):640–7.PubMedCrossRef
24.
go back to reference Jacob MH, DdR J, Belló-Klein A, Llesuy SF, Ribeiro MF. Dehydroepiandrosterone modulates antioxidant enzymes and Akt signaling in healthy Wistar erat hearts. J Steroid Biochem Mol Biol. 2008;112(1):138–44.PubMedCrossRef Jacob MH, DdR J, Belló-Klein A, Llesuy SF, Ribeiro MF. Dehydroepiandrosterone modulates antioxidant enzymes and Akt signaling in healthy Wistar erat hearts. J Steroid Biochem Mol Biol. 2008;112(1):138–44.PubMedCrossRef
25.
go back to reference Lu C, Yang W, Chen M, Liu T, Yang J, Tan P, et al. Inhibin a inhibits follicle-stimulating hormone (FSH) action by suppressing its receptor expression in cultured rat granulosa cells. Mol Cell Endocrinol. 2009;298(1–2):48–56.PubMedCrossRef Lu C, Yang W, Chen M, Liu T, Yang J, Tan P, et al. Inhibin a inhibits follicle-stimulating hormone (FSH) action by suppressing its receptor expression in cultured rat granulosa cells. Mol Cell Endocrinol. 2009;298(1–2):48–56.PubMedCrossRef
27.
go back to reference Awad H, Halawa F, Mostafa T, Atta H. Melatonin hormone profile in infertile males. Int J Androl. 2006;29(3):409–13.PubMedCrossRef Awad H, Halawa F, Mostafa T, Atta H. Melatonin hormone profile in infertile males. Int J Androl. 2006;29(3):409–13.PubMedCrossRef
28.
go back to reference La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio AC, et al. Anti-Müllerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010;16(2):113–30.PubMedCrossRef La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio AC, et al. Anti-Müllerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update. 2010;16(2):113–30.PubMedCrossRef
29.
30.
go back to reference Trigo RV, Bergadá I, Rey R, Ballerini MG, Bedecarrás P, Bergadá C, et al. Altered serum profile of inhibin B, pro-αC and anti-Müllerian hormone in prepubertal and pubertal boys with varicocele. Clin Endocrinol. 2004;60(6):758–64.CrossRef Trigo RV, Bergadá I, Rey R, Ballerini MG, Bedecarrás P, Bergadá C, et al. Altered serum profile of inhibin B, pro-αC and anti-Müllerian hormone in prepubertal and pubertal boys with varicocele. Clin Endocrinol. 2004;60(6):758–64.CrossRef
31.
go back to reference Castañeda Cortés DC, Langlois VS, Fernandino JI. Crossover of the hypothalamic pituitary–adrenal/Interrenal, –thyroid, and –gonadal axes in testicular development. Front Endocrinol. 2014;5:139. Castañeda Cortés DC, Langlois VS, Fernandino JI. Crossover of the hypothalamic pituitary–adrenal/Interrenal, –thyroid, and –gonadal axes in testicular development. Front Endocrinol. 2014;5:139.
32.
go back to reference Bisht S, Faiq M, Tolahunase M, Dada R. Oxidative stress and male infertility. Nat Rev Urol. 2017;14(8):470–85.PubMedCrossRef Bisht S, Faiq M, Tolahunase M, Dada R. Oxidative stress and male infertility. Nat Rev Urol. 2017;14(8):470–85.PubMedCrossRef
33.
go back to reference Gosalvez J, Tvrda E, Agarwal A. Free radical and superoxide reactivity detection in semen quality assessment: past, present, and future. J Assist Reprod Genet. 2017;34:697–707.PubMedPubMedCentralCrossRef Gosalvez J, Tvrda E, Agarwal A. Free radical and superoxide reactivity detection in semen quality assessment: past, present, and future. J Assist Reprod Genet. 2017;34:697–707.PubMedPubMedCentralCrossRef
34.
go back to reference Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Men’s Health. 2014;32(1):1–17.CrossRef Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Men’s Health. 2014;32(1):1–17.CrossRef
35.
go back to reference Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update. 2009;15(5):553–72.PubMedCrossRef Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update. 2009;15(5):553–72.PubMedCrossRef
36.
go back to reference Kussmaul L, Hirst J. The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci U S A. 2006;103(20):7607–12.PubMedPubMedCentralCrossRef Kussmaul L, Hirst J. The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci U S A. 2006;103(20):7607–12.PubMedPubMedCentralCrossRef
37.
go back to reference Vinogradov AD, Grivennikova VG. Generation of superoxide-radical by the NADH:ubiquinone oxidoreductase of heart mitochondria. Biochem Mosc. 2005;70(2):120–7.CrossRef Vinogradov AD, Grivennikova VG. Generation of superoxide-radical by the NADH:ubiquinone oxidoreductase of heart mitochondria. Biochem Mosc. 2005;70(2):120–7.CrossRef
38.
39.
go back to reference Blaylock MG, Cuthbertson BH, Galley HF, Ferguson NR, Webster NR. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Radic Biol Med. 1998;25(6):748–52.PubMedCrossRef Blaylock MG, Cuthbertson BH, Galley HF, Ferguson NR, Webster NR. The effect of nitric oxide and peroxynitrite on apoptosis in human polymorphonuclear leukocytes. Free Radic Biol Med. 1998;25(6):748–52.PubMedCrossRef
40.
go back to reference Sabeur K, Ball B. Characterization of NADPH oxidase 5 in equine testis and spermatozoa. Reprod. 2007;134(2):263–70.CrossRef Sabeur K, Ball B. Characterization of NADPH oxidase 5 in equine testis and spermatozoa. Reprod. 2007;134(2):263–70.CrossRef
41.
go back to reference Petrushanko IY, Lobachev VM, Kononikhin AS, Makarov AA, Devred F, Kovacic H, et al. Oxidation of capital ES, Cyrillicsmall a, Cyrillic2+-binding domain of NADPH oxidase 5 (NOX5): toward understanding the mechanism of inactivation of NOX5 by ROS. PLoS One. 2016;11(7):e0158726.PubMedPubMedCentralCrossRef Petrushanko IY, Lobachev VM, Kononikhin AS, Makarov AA, Devred F, Kovacic H, et al. Oxidation of capital ES, Cyrillicsmall a, Cyrillic2+-binding domain of NADPH oxidase 5 (NOX5): toward understanding the mechanism of inactivation of NOX5 by ROS. PLoS One. 2016;11(7):e0158726.PubMedPubMedCentralCrossRef
42.
go back to reference Rengan AK, Agarwal A, van der Linde M, du Plessis SS. An investigation of excess residual cytoplasm in human spermatozoa and its distinction from the cytoplasmic droplet. Reprod Biol Endocrinol. 2012;10(1):92.PubMedPubMedCentralCrossRef Rengan AK, Agarwal A, van der Linde M, du Plessis SS. An investigation of excess residual cytoplasm in human spermatozoa and its distinction from the cytoplasmic droplet. Reprod Biol Endocrinol. 2012;10(1):92.PubMedPubMedCentralCrossRef
43.
go back to reference Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, Meyer A, et al. Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril. 2003;79:1597–605.PubMedCrossRef Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, Meyer A, et al. Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril. 2003;79:1597–605.PubMedCrossRef
44.
go back to reference Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod. 2011;26(7):1628–40.PubMedCrossRef Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy. Hum Reprod. 2011;26(7):1628–40.PubMedCrossRef
45.
go back to reference Lavranos G, Balla M, Tzortzopoulou A, Syriou V, Angelopoulou R. Investigating ROS sources in male infertility: a common end for numerous pathways. Reprod Toxicol. 2012;34(3):298–307.PubMedCrossRef Lavranos G, Balla M, Tzortzopoulou A, Syriou V, Angelopoulou R. Investigating ROS sources in male infertility: a common end for numerous pathways. Reprod Toxicol. 2012;34(3):298–307.PubMedCrossRef
46.
go back to reference Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003;79(4):829–43.PubMedCrossRef Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril. 2003;79(4):829–43.PubMedCrossRef
47.
48.
go back to reference World Health Organization. WHO laboratory manual for the examination and processing of human semen. Fifth Edition. WHO: Geneva, 2010. World Health Organization. WHO laboratory manual for the examination and processing of human semen. Fifth Edition. WHO: Geneva, 2010.
49.
go back to reference Agarwal A, Prabakaran S, Allamaneni SS. Relationship between oxidative stress, varicocele and infertility: a meta-analysis. Reprod BioMed Online. 2006;12(5):630–3.PubMedCrossRef Agarwal A, Prabakaran S, Allamaneni SS. Relationship between oxidative stress, varicocele and infertility: a meta-analysis. Reprod BioMed Online. 2006;12(5):630–3.PubMedCrossRef
50.
go back to reference Shiraishi K, Matsuyama H, Takihara H. Pathophysiology of varicocele in male infertility in the era of assisted reproductive technology. Int J Urol. 2012;19(6):538–50.PubMedCrossRef Shiraishi K, Matsuyama H, Takihara H. Pathophysiology of varicocele in male infertility in the era of assisted reproductive technology. Int J Urol. 2012;19(6):538–50.PubMedCrossRef
51.
go back to reference Clarke RN, Klock SC, Geoghegan A, Travassos DE. Relationship between psychological stress and semen quality among in-vitro fertilization patients. Hum Reprod. 1999;14(3):753–8.PubMedCrossRef Clarke RN, Klock SC, Geoghegan A, Travassos DE. Relationship between psychological stress and semen quality among in-vitro fertilization patients. Hum Reprod. 1999;14(3):753–8.PubMedCrossRef
52.
go back to reference Lampiao F. Variation of semen parameters in healthy medical students due to exam stress. Malawi Med J. 2009;21(4):166–7.PubMedPubMedCentral Lampiao F. Variation of semen parameters in healthy medical students due to exam stress. Malawi Med J. 2009;21(4):166–7.PubMedPubMedCentral
53.
go back to reference Gollenberg AL, Liu F, Brazil C, Drobnis EZ, Guzick D, Overstreet JW, et al. Semen quality in fertile men in relation to psychosocial stress. Fertil Steril. 2010;93(4):1104–11.PubMedCrossRef Gollenberg AL, Liu F, Brazil C, Drobnis EZ, Guzick D, Overstreet JW, et al. Semen quality in fertile men in relation to psychosocial stress. Fertil Steril. 2010;93(4):1104–11.PubMedCrossRef
54.
go back to reference Flaherty RL, Owen M, Fagan-Murphy A, Intabli H, Healy D, Patel A, et al. Glucocorticoids induce production of reactive oxygen species/reactive nitrogen species and DNA damage through an iNOS mediated pathway in breast cancer. Breast Cancer Res. 2017;19(1):35.PubMedPubMedCentralCrossRef Flaherty RL, Owen M, Fagan-Murphy A, Intabli H, Healy D, Patel A, et al. Glucocorticoids induce production of reactive oxygen species/reactive nitrogen species and DNA damage through an iNOS mediated pathway in breast cancer. Breast Cancer Res. 2017;19(1):35.PubMedPubMedCentralCrossRef
55.
go back to reference Bakunina N, Pariante CM, Zunszain PA. Immune mechanisms linked to depression via oxidative stress and neuroprogression. Immunol. 2015;144(3):365–73.CrossRef Bakunina N, Pariante CM, Zunszain PA. Immune mechanisms linked to depression via oxidative stress and neuroprogression. Immunol. 2015;144(3):365–73.CrossRef
56.
go back to reference O'Hara L, McInnes K, Simitsidellis I, Morgan S, Atanassova N, Slowikowska-Hilczer J, et al. Autocrine androgen action is essential for Leydig cell maturation and function, and protects against late-onset Leydig cell apoptosis in both mice and men. FASEB J. 2015;29(3):894–910.PubMedCrossRef O'Hara L, McInnes K, Simitsidellis I, Morgan S, Atanassova N, Slowikowska-Hilczer J, et al. Autocrine androgen action is essential for Leydig cell maturation and function, and protects against late-onset Leydig cell apoptosis in both mice and men. FASEB J. 2015;29(3):894–910.PubMedCrossRef
57.
go back to reference Gao HB, Tong MH, Hu YQ, Guo QS, Ge R, Hardy MP. Glucocorticoid induces apoptosis in rat leydig cells. Endocrinol. 2002;143(1):130–8.CrossRef Gao HB, Tong MH, Hu YQ, Guo QS, Ge R, Hardy MP. Glucocorticoid induces apoptosis in rat leydig cells. Endocrinol. 2002;143(1):130–8.CrossRef
58.
go back to reference MacAdams MR, White RH, Chipps BE. Reduction of serum testosterone levels during chronic glucocorticoid therapy. Ann Intern Med. 1986;104(5):648–51.PubMedCrossRef MacAdams MR, White RH, Chipps BE. Reduction of serum testosterone levels during chronic glucocorticoid therapy. Ann Intern Med. 1986;104(5):648–51.PubMedCrossRef
59.
go back to reference Norman R. Effects of corticotropin-releasing hormone on luteinizing hormone, testosterone, and cortisol secretion in intact male rhesus macaques. Biol Reprod. 1993;49(1):148–53.PubMedCrossRef Norman R. Effects of corticotropin-releasing hormone on luteinizing hormone, testosterone, and cortisol secretion in intact male rhesus macaques. Biol Reprod. 1993;49(1):148–53.PubMedCrossRef
60.
go back to reference Orr T, Taylor M, Bhattacharyya A, Collins D, Mann D. Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17α-hydroxylase and 17, 20-Lyase without affecting the binding of LH/hCG receptors. J Androl. 1994;15(4):302–8.PubMed Orr T, Taylor M, Bhattacharyya A, Collins D, Mann D. Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17α-hydroxylase and 17, 20-Lyase without affecting the binding of LH/hCG receptors. J Androl. 1994;15(4):302–8.PubMed
61.
go back to reference Gao H-B, Tong M-H, Hu Y-Q, You H-Y, Guo Q-S, Ge R-S, et al. Mechanisms of glucocorticoid-induced Leydig cell apoptosis. Mol Cell Endocrinol. 2003;199(1):153–63.PubMedCrossRef Gao H-B, Tong M-H, Hu Y-Q, You H-Y, Guo Q-S, Ge R-S, et al. Mechanisms of glucocorticoid-induced Leydig cell apoptosis. Mol Cell Endocrinol. 2003;199(1):153–63.PubMedCrossRef
62.
go back to reference Almeida S, Anselmo-Franci J, Silva AR e, Carvalho TL. Chronic intermittent immobilization of male rats throughout sexual development: a stress protocol. Exp Physiol. 1998;83(05):701–4.PubMedCrossRef Almeida S, Anselmo-Franci J, Silva AR e, Carvalho TL. Chronic intermittent immobilization of male rats throughout sexual development: a stress protocol. Exp Physiol. 1998;83(05):701–4.PubMedCrossRef
63.
go back to reference Wagenmaker ER, Breen KM, Oakley AE, Tilbrook AJ, Karsch FJ. Psychosocial stress inhibits amplitude of gonadotropin-releasing hormone pulses independent of cortisol action on the type II glucocorticoid receptor. Endocrinol. 2009;150(2):762–9.CrossRef Wagenmaker ER, Breen KM, Oakley AE, Tilbrook AJ, Karsch FJ. Psychosocial stress inhibits amplitude of gonadotropin-releasing hormone pulses independent of cortisol action on the type II glucocorticoid receptor. Endocrinol. 2009;150(2):762–9.CrossRef
65.
go back to reference Paul C, Murray AA, Spears N, Saunders PT. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reprod. 2008;136(1):73–84.CrossRef Paul C, Murray AA, Spears N, Saunders PT. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reprod. 2008;136(1):73–84.CrossRef
66.
go back to reference Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod. 2009;80(5):913–9.PubMedPubMedCentralCrossRef Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod. 2009;80(5):913–9.PubMedPubMedCentralCrossRef
67.
go back to reference Yaeram J, Setchell BP, Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev. 2006;18(6):647–53.PubMedCrossRef Yaeram J, Setchell BP, Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev. 2006;18(6):647–53.PubMedCrossRef
68.
go back to reference Moon EJ, Sonveaux P, Porporato PE, Danhier P, Gallez B, Batinic-Haberle I, et al. NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci. 2010;107(47):20477–82.PubMedCrossRef Moon EJ, Sonveaux P, Porporato PE, Danhier P, Gallez B, Batinic-Haberle I, et al. NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci. 2010;107(47):20477–82.PubMedCrossRef
69.
go back to reference Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. Rev Int J Hyperthermia. 2014;30(7):513–23.CrossRef Belhadj Slimen I, Najar T, Ghram A, Dabbebi H, Ben Mrad M, Abdrabbah M. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. Rev Int J Hyperthermia. 2014;30(7):513–23.CrossRef
70.
go back to reference Jung A, Schuppe HC. Influence of genital heat stress on semen quality in humans. Andrologia. 2007;39(6):203–15.PubMedCrossRef Jung A, Schuppe HC. Influence of genital heat stress on semen quality in humans. Andrologia. 2007;39(6):203–15.PubMedCrossRef
71.
go back to reference Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, et al. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod. 2013;28(4):877–85.PubMedCrossRef Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, et al. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod. 2013;28(4):877–85.PubMedCrossRef
72.
go back to reference Aggarwal A, Upadhyay R. Heat stress and hormones, in heat stress and animal productivity. India: Springer; 2013. p. 27–51. Aggarwal A, Upadhyay R. Heat stress and hormones, in heat stress and animal productivity. India: Springer; 2013. p. 27–51.
73.
go back to reference Rhynes W, Ewing L. Testicular endocrine function in Hereford bulls exposed to high ambient temperature 1. Endocrinology. 1973;92(2):509–15.PubMedCrossRef Rhynes W, Ewing L. Testicular endocrine function in Hereford bulls exposed to high ambient temperature 1. Endocrinology. 1973;92(2):509–15.PubMedCrossRef
74.
go back to reference Hansen PJ. Effects of heat stress on mammalian reproduction. Philosophical transactions of the Royal Society of London B. Biol Sci. 2009;364(1534):3341–50.CrossRef Hansen PJ. Effects of heat stress on mammalian reproduction. Philosophical transactions of the Royal Society of London B. Biol Sci. 2009;364(1534):3341–50.CrossRef
75.
go back to reference Li Z, Tian J, Cui G, Wang M, Yu D. Effects of local testicular heat treatment on Leydig cell hyperplasia and testosterone biosynthesis in rat testes. Reproduction, fertility. Development. 2016;28(9):1424–32. Li Z, Tian J, Cui G, Wang M, Yu D. Effects of local testicular heat treatment on Leydig cell hyperplasia and testosterone biosynthesis in rat testes. Reproduction, fertility. Development. 2016;28(9):1424–32.
76.
go back to reference Hagenas L, Ritzen EM, Svensson J, Hansson V, Purvis K. Temperature dependence of Sertoli cell function. Int J Androl. 1978;1(Supplement 2):449–58.CrossRef Hagenas L, Ritzen EM, Svensson J, Hansson V, Purvis K. Temperature dependence of Sertoli cell function. Int J Androl. 1978;1(Supplement 2):449–58.CrossRef
77.
go back to reference Megahed G, Anwar M, Wasfy S, Hammadeh M. Influence of heat stress on the cortisol and oxidant-antioxidants balance during Oestrous phase in buffalo-cows (Bubalus bubalis): Thermo-protective role of antioxidant treatment. Reprod Domest Anim. 2008;43(6):672–7.PubMedCrossRef Megahed G, Anwar M, Wasfy S, Hammadeh M. Influence of heat stress on the cortisol and oxidant-antioxidants balance during Oestrous phase in buffalo-cows (Bubalus bubalis): Thermo-protective role of antioxidant treatment. Reprod Domest Anim. 2008;43(6):672–7.PubMedCrossRef
78.
go back to reference Coutts SM, Fulton N, Anderson RA. Environmental toxicant-induced germ cell apoptosis in the human fetal testis. Hum Reprod. 2007;22(11):2912–8.PubMedCrossRef Coutts SM, Fulton N, Anderson RA. Environmental toxicant-induced germ cell apoptosis in the human fetal testis. Hum Reprod. 2007;22(11):2912–8.PubMedCrossRef
79.
go back to reference Wong W, Yan H, Li W, Lie P, Mruk D, Cheng C. Cell junctions in the testis as targets for toxicants. In: Richburg J, Hoyer P, editors. Comprehensive toxicology. Oxford: Elsevier; 2010. p. 167–88.CrossRef Wong W, Yan H, Li W, Lie P, Mruk D, Cheng C. Cell junctions in the testis as targets for toxicants. In: Richburg J, Hoyer P, editors. Comprehensive toxicology. Oxford: Elsevier; 2010. p. 167–88.CrossRef
80.
go back to reference Benoff S, Hauser R, Marmar JL, Hurley IR, Napolitano B, Centola GM. Cadmium concentrations in blood and seminal plasma: correlations with sperm number and motility in three male populations (infertility patients, artificial insemination donors, and unselected volunteers). Mol Med. 2009;15(7–8):248–62.PubMedPubMedCentral Benoff S, Hauser R, Marmar JL, Hurley IR, Napolitano B, Centola GM. Cadmium concentrations in blood and seminal plasma: correlations with sperm number and motility in three male populations (infertility patients, artificial insemination donors, and unselected volunteers). Mol Med. 2009;15(7–8):248–62.PubMedPubMedCentral
81.
go back to reference Luparello C, Sirchia R, Longo A. Cadmium as a transcriptional modulator in human cells. Crit Rev Toxicol. 2011;41(1):75–82.PubMedCrossRef Luparello C, Sirchia R, Longo A. Cadmium as a transcriptional modulator in human cells. Crit Rev Toxicol. 2011;41(1):75–82.PubMedCrossRef
82.
go back to reference Choy CM, Yeung QS, Briton-Jones CM, Cheung CK, Lam CW, Haines CJ. Relationship between semen parameters and mercury concentrations in blood and in seminal fluid from subfertile males in Hong Kong. Fertil Steril. 2002;78(2):426–8.PubMedCrossRef Choy CM, Yeung QS, Briton-Jones CM, Cheung CK, Lam CW, Haines CJ. Relationship between semen parameters and mercury concentrations in blood and in seminal fluid from subfertile males in Hong Kong. Fertil Steril. 2002;78(2):426–8.PubMedCrossRef
83.
go back to reference Mocevic E, Specht IO, Marott JL, Giwercman A, Jonsson BA, Toft G, et al. Environmental mercury exposure, semen quality and reproductive hormones in Greenlandic Inuit and European men: a cross-sectional study. Asian J Androl. 2013;15(1):97–104.PubMedCrossRef Mocevic E, Specht IO, Marott JL, Giwercman A, Jonsson BA, Toft G, et al. Environmental mercury exposure, semen quality and reproductive hormones in Greenlandic Inuit and European men: a cross-sectional study. Asian J Androl. 2013;15(1):97–104.PubMedCrossRef
84.
go back to reference Welshons WV, Nagel SC, Vom Saal FS. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol a at levels of human exposure. Endocrinology. 2006;147(6 Suppl):S56–69.PubMedCrossRef Welshons WV, Nagel SC, Vom Saal FS. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol a at levels of human exposure. Endocrinology. 2006;147(6 Suppl):S56–69.PubMedCrossRef
85.
go back to reference Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol a and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect. 2008;116(1):39–44.PubMedCrossRef Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol a and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect. 2008;116(1):39–44.PubMedCrossRef
86.
go back to reference Galimova EF, Amirova ZK, Galimov Sh N. Dioxins in the semen of men with infertility. Environ Sci Pollut Res Int. 2015;22(19):14566–9.PubMedCrossRef Galimova EF, Amirova ZK, Galimov Sh N. Dioxins in the semen of men with infertility. Environ Sci Pollut Res Int. 2015;22(19):14566–9.PubMedCrossRef
87.
go back to reference Lodovici M, Bigagli E. Oxidative stress and air pollution exposure. Journal of toxicology. 2011;2011:1–9. Lodovici M, Bigagli E. Oxidative stress and air pollution exposure. Journal of toxicology. 2011;2011:1–9.
88.
go back to reference Pacey A. Environmental and lifestyle factors associated with sperm DNA damage. Hum Fertil. 2010;13(4):189–93.CrossRef Pacey A. Environmental and lifestyle factors associated with sperm DNA damage. Hum Fertil. 2010;13(4):189–93.CrossRef
89.
go back to reference Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab. 2010;21(4):214–22.PubMedPubMedCentralCrossRef Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab. 2010;21(4):214–22.PubMedPubMedCentralCrossRef
90.
go back to reference Sengupta P, Dutta S. Metals. In M. K. Skinner (Ed.), Encyclopedia of Reproduction. vol. 1, pp. 579–587. Academic Press: Elsevier, Cambridge, Massachusetts, United States. Sengupta P, Dutta S. Metals. In M. K. Skinner (Ed.), Encyclopedia of Reproduction. vol. 1, pp. 579–587. Academic Press: Elsevier, Cambridge, Massachusetts, United States.
91.
go back to reference Güven M, Bayram F, Ünlühizarci K, Kelestimur F. Endocrine changes in patients with acute organophosphate poisoning. Hum Exp Toxicol. 1999;18(10):598–601.PubMedCrossRef Güven M, Bayram F, Ünlühizarci K, Kelestimur F. Endocrine changes in patients with acute organophosphate poisoning. Hum Exp Toxicol. 1999;18(10):598–601.PubMedCrossRef
92.
go back to reference Herath CB, Jin W, Watanabe G, Arai K, Suzuki AK, Taya K. Adverse effects of environmental toxicants, octylphenol and bisphenol a, on male reproductive functions in pubertal rats. Endocrine. 2004;25(2):163–72.PubMedCrossRef Herath CB, Jin W, Watanabe G, Arai K, Suzuki AK, Taya K. Adverse effects of environmental toxicants, octylphenol and bisphenol a, on male reproductive functions in pubertal rats. Endocrine. 2004;25(2):163–72.PubMedCrossRef
93.
go back to reference Meeker JD, Rossano MG, Protas B, Padmanahban V, Diamond MP, Puscheck E, et al. Environmental exposure to metals and male reproductive hormones: circulating testosterone is inversely associated with blood molybdenum. Fertil Steril. 2010;93(1):130–40.PubMedCrossRef Meeker JD, Rossano MG, Protas B, Padmanahban V, Diamond MP, Puscheck E, et al. Environmental exposure to metals and male reproductive hormones: circulating testosterone is inversely associated with blood molybdenum. Fertil Steril. 2010;93(1):130–40.PubMedCrossRef
94.
go back to reference Shimon I, Lubina A, Gorfine M, Ilany J. Feedback inhibition of gonadotropins by testosterone in men with hypogonadotropic hypogonadism: comparison to the intact pituitary-testicular axis in primary hypogonadism. J Androl. 2006;27(3):358–64.PubMedCrossRef Shimon I, Lubina A, Gorfine M, Ilany J. Feedback inhibition of gonadotropins by testosterone in men with hypogonadotropic hypogonadism: comparison to the intact pituitary-testicular axis in primary hypogonadism. J Androl. 2006;27(3):358–64.PubMedCrossRef
95.
go back to reference Sharma RP, Schuhmacher M, Kumar V. Review on crosstalk and common mechanisms of endocrine disruptors: scaffolding to improve PBPK/PD model of EDC mixture. Environ Int. 2017;99:1–14.PubMedCrossRef Sharma RP, Schuhmacher M, Kumar V. Review on crosstalk and common mechanisms of endocrine disruptors: scaffolding to improve PBPK/PD model of EDC mixture. Environ Int. 2017;99:1–14.PubMedCrossRef
96.
go back to reference Sengupta P, Banerjee R. Environmental toxins: alarming impacts of pesticides on male fertility. Hum Exp Toxicol. 2014;33(10):1017–39.PubMedCrossRef Sengupta P, Banerjee R. Environmental toxins: alarming impacts of pesticides on male fertility. Hum Exp Toxicol. 2014;33(10):1017–39.PubMedCrossRef
97.
go back to reference Vignera S, Condorelli RA, Vicari E, D'Agata R, Calogero AE. Effects of the exposure to mobile phones on male reproduction: a review of the literature. J Androl. 2012;33(3):350–6.PubMedCrossRef Vignera S, Condorelli RA, Vicari E, D'Agata R, Calogero AE. Effects of the exposure to mobile phones on male reproduction: a review of the literature. J Androl. 2012;33(3):350–6.PubMedCrossRef
98.
go back to reference Darbandi M, Darbandi S, Agarwal A, Henkle R, Sadeghi MR. The effects of exposure to low frequency electromagnetic fields on male fertility. Altern Ther Health Med. 2017;23 Darbandi M, Darbandi S, Agarwal A, Henkle R, Sadeghi MR. The effects of exposure to low frequency electromagnetic fields on male fertility. Altern Ther Health Med. 2017;23
99.
go back to reference Agarwal A, Singh A, Hamada A, Kesari K. Cell phones and male infertility: a review of recent innovations in technology and consequences. Int Braz J Urol. 2011;37(4):432–54.PubMedCrossRef Agarwal A, Singh A, Hamada A, Kesari K. Cell phones and male infertility: a review of recent innovations in technology and consequences. Int Braz J Urol. 2011;37(4):432–54.PubMedCrossRef
100.
go back to reference Yildirim ME, Kaynar M, Badem H, Cavis M, Karatas OF, Cimentepe E. What is harmful for male fertility: cell phone or the wireless internet? Kaohsiung J Med Sci. 2015;31(9):480–4.PubMedCrossRef Yildirim ME, Kaynar M, Badem H, Cavis M, Karatas OF, Cimentepe E. What is harmful for male fertility: cell phone or the wireless internet? Kaohsiung J Med Sci. 2015;31(9):480–4.PubMedCrossRef
101.
go back to reference Al-Quzwini OF, Al-Taee HA, Al-Shaikh SF. Male fertility and its association with occupational and mobile phone towers hazards: an analytic study. Middle East Fertil Soc J. 2016;21(4):236–40.CrossRef Al-Quzwini OF, Al-Taee HA, Al-Shaikh SF. Male fertility and its association with occupational and mobile phone towers hazards: an analytic study. Middle East Fertil Soc J. 2016;21(4):236–40.CrossRef
102.
go back to reference Agarwal A, Deepinder F, Sharma RK, Ranga G, Li J. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril. 2008;89(1):124–8.PubMedCrossRef Agarwal A, Deepinder F, Sharma RK, Ranga G, Li J. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril. 2008;89(1):124–8.PubMedCrossRef
103.
go back to reference Agarwal A, Desai NR, Makker K, Varghese A, Mouradi R, Sabanegh E, et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril. 2009;92(4):1318–25.PubMedCrossRef Agarwal A, Desai NR, Makker K, Varghese A, Mouradi R, Sabanegh E, et al. Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril. 2009;92(4):1318–25.PubMedCrossRef
104.
go back to reference Mahdavi SM, Sahraei H, Yaghmaei P, Tavakoli H. Effects of electromagnetic radiation exposure on stress-related behaviors and stress hormones in male wistar rats. Biomolecules Ther. 2014;22(6):570.CrossRef Mahdavi SM, Sahraei H, Yaghmaei P, Tavakoli H. Effects of electromagnetic radiation exposure on stress-related behaviors and stress hormones in male wistar rats. Biomolecules Ther. 2014;22(6):570.CrossRef
105.
go back to reference Meo SA, Al-Drees AM, Husain S, Khan MM, Imran MB. Effects of mobile phone radiation on serum testosterone in Wistar albino rats. Saudi Med J. 2010;31(8):869–73.PubMed Meo SA, Al-Drees AM, Husain S, Khan MM, Imran MB. Effects of mobile phone radiation on serum testosterone in Wistar albino rats. Saudi Med J. 2010;31(8):869–73.PubMed
107.
go back to reference Stevens RG, Davis S. The melatonin hypothesis: electric power and breast cancer. Environ Health Perspects. 1996;104(Suppl 1):135.CrossRef Stevens RG, Davis S. The melatonin hypothesis: electric power and breast cancer. Environ Health Perspects. 1996;104(Suppl 1):135.CrossRef
108.
go back to reference Malpaux B, Daveau A, Maurice F, Gayrard V, Thiery J-C. Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod. 1993;48(4):752–60.PubMedCrossRef Malpaux B, Daveau A, Maurice F, Gayrard V, Thiery J-C. Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod. 1993;48(4):752–60.PubMedCrossRef
109.
go back to reference Adefuye AO, Adeola HA, Sales KJ, Katz AA. Seminal fluid-mediated inflammation in physiology and pathology of the female reproductive tract. J Immunol Res. 2016;2016:1–13. Adefuye AO, Adeola HA, Sales KJ, Katz AA. Seminal fluid-mediated inflammation in physiology and pathology of the female reproductive tract. J Immunol Res. 2016;2016:1–13.
110.
go back to reference Vaamonde D, Da Silva-Grigoletto ME, García-Manso JM, Barrera N, Vaamonde-Lemos R. Physically active men show better semen parameters and hormone values than sedentary men. Eur J Appl Physiol. 2012;112(9):3267–73.PubMedCrossRef Vaamonde D, Da Silva-Grigoletto ME, García-Manso JM, Barrera N, Vaamonde-Lemos R. Physically active men show better semen parameters and hormone values than sedentary men. Eur J Appl Physiol. 2012;112(9):3267–73.PubMedCrossRef
111.
go back to reference Grandys M, Majerczak J, Duda K, Zapart-Bukowska J, Kulpa J, Zoladz J. Endurance training of moderate intensity increases testosterone concentration in young, healthy men. Int J Sports Med. 2009;30(07):489–95.PubMedCrossRef Grandys M, Majerczak J, Duda K, Zapart-Bukowska J, Kulpa J, Zoladz J. Endurance training of moderate intensity increases testosterone concentration in young, healthy men. Int J Sports Med. 2009;30(07):489–95.PubMedCrossRef
112.
go back to reference Fahrner C, Hackney AC. Effects of endurance exercise on free testosterone concentration and the binding affinity of sex hormone binding globulin (SHBG). Int J Sports Med. 1998;19(01):12–5.PubMedCrossRef Fahrner C, Hackney AC. Effects of endurance exercise on free testosterone concentration and the binding affinity of sex hormone binding globulin (SHBG). Int J Sports Med. 1998;19(01):12–5.PubMedCrossRef
113.
go back to reference Flynn M, Pizza F, Brolinson P. Hormonal responses to excessive training: influence of cross training. Int J Sports Med. 1997;18(03):191–6.PubMedCrossRef Flynn M, Pizza F, Brolinson P. Hormonal responses to excessive training: influence of cross training. Int J Sports Med. 1997;18(03):191–6.PubMedCrossRef
114.
go back to reference Safarinejad MR, Azma K, Kolahi AA. The effects of intensive, long-term treadmill running on reproductive hormones, hypothalamus–pituitary–testis axis, and semen quality: a randomized controlled study. J Endocrinol. 2009;200(3):259–71.PubMedCrossRef Safarinejad MR, Azma K, Kolahi AA. The effects of intensive, long-term treadmill running on reproductive hormones, hypothalamus–pituitary–testis axis, and semen quality: a randomized controlled study. J Endocrinol. 2009;200(3):259–71.PubMedCrossRef
115.
go back to reference Kindermann W, Schnabel A, Schmitt W, Biro G, Cassens J, Weber F. Catecholamines, growth hormone, cortisol, insulin, and sex hormones in anaerobic and aerobic exercise. Eur J Appl Physiol Occup Physiol. 1982;49(3):389–99.PubMedCrossRef Kindermann W, Schnabel A, Schmitt W, Biro G, Cassens J, Weber F. Catecholamines, growth hormone, cortisol, insulin, and sex hormones in anaerobic and aerobic exercise. Eur J Appl Physiol Occup Physiol. 1982;49(3):389–99.PubMedCrossRef
116.
go back to reference Jurimae J, Jurimae T. Responses of blood hormones to the maximal rowing ergometer test in college rowers. J Sports Med Phys Fitness. 2001;41(1):73.PubMed Jurimae J, Jurimae T. Responses of blood hormones to the maximal rowing ergometer test in college rowers. J Sports Med Phys Fitness. 2001;41(1):73.PubMed
117.
go back to reference Kopelman PG. Hormones and obesity. Baillieres Clin Endocrinol Metab. 1994;8(3):549–75. Kopelman PG. Hormones and obesity. Baillieres Clin Endocrinol Metab. 1994;8(3):549–75.
119.
go back to reference Álvarez-Castro P, Pena L, Cordido F. Ghrelin in obesity, physiological and pharmacological considerations. Mini Rev Med Chem. 2013;13(4):541–52.PubMedCrossRef Álvarez-Castro P, Pena L, Cordido F. Ghrelin in obesity, physiological and pharmacological considerations. Mini Rev Med Chem. 2013;13(4):541–52.PubMedCrossRef
120.
go back to reference Kawano J, Arora R. The role of adiponectin in obesity, diabetes, and cardiovascular disease. J Cardiometab Syndr. 2009;4(1):44–9.PubMedCrossRef Kawano J, Arora R. The role of adiponectin in obesity, diabetes, and cardiovascular disease. J Cardiometab Syndr. 2009;4(1):44–9.PubMedCrossRef
121.
go back to reference Perez-Leighton C, Butterick-Peterson T, Billington C, Kotz C. Role of orexin receptors in obesity: from cellular to behavioral evidence. Int J Obes. 2013;37(2):167–74.CrossRef Perez-Leighton C, Butterick-Peterson T, Billington C, Kotz C. Role of orexin receptors in obesity: from cellular to behavioral evidence. Int J Obes. 2013;37(2):167–74.CrossRef
122.
go back to reference Ren A-J, Guo Z-F, Wang Y-K, Lin L, Zheng X, Yuan W-J. Obestatin, obesity and diabetes. Peptides. 2009;30(2):439–44.PubMedCrossRef Ren A-J, Guo Z-F, Wang Y-K, Lin L, Zheng X, Yuan W-J. Obestatin, obesity and diabetes. Peptides. 2009;30(2):439–44.PubMedCrossRef
123.
go back to reference Bouloumie A, Marumo T, Lafontan M, Busse R. Leptin induces oxidative stress in human endothelial cells. FASEB J. 1999;13(10):1231–8.PubMedCrossRef Bouloumie A, Marumo T, Lafontan M, Busse R. Leptin induces oxidative stress in human endothelial cells. FASEB J. 1999;13(10):1231–8.PubMedCrossRef
124.
go back to reference Yamagishi SI, Edelstein D, Du XL, Kaneda Y, Guzman M, Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase a. J Biol Chem. 2001;276(27):25096–100.PubMedCrossRef Yamagishi SI, Edelstein D, Du XL, Kaneda Y, Guzman M, Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase a. J Biol Chem. 2001;276(27):25096–100.PubMedCrossRef
125.
go back to reference Wauters M, Considine RV, Van Gaal LF. Human leptin: from an adipocyte hormone to an endocrine mediator. Eur J Endocrinol. 2000;143(3):293–311.PubMedCrossRef Wauters M, Considine RV, Van Gaal LF. Human leptin: from an adipocyte hormone to an endocrine mediator. Eur J Endocrinol. 2000;143(3):293–311.PubMedCrossRef
126.
go back to reference Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. Ghrelin expression in human testis and serum testosterone level. J Androl. 2007;28(2):320–4.PubMedCrossRef Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. Ghrelin expression in human testis and serum testosterone level. J Androl. 2007;28(2):320–4.PubMedCrossRef
127.
go back to reference Wang L, Fang F, Li Y, Zhang Y, Pu Y, Zhang X. Role of ghrelin on testosterone secretion and the mRNA expression of androgen receptors in adult rat testis. Systems Biol Reprod Med. 2011;57(3):119–23.CrossRef Wang L, Fang F, Li Y, Zhang Y, Pu Y, Zhang X. Role of ghrelin on testosterone secretion and the mRNA expression of androgen receptors in adult rat testis. Systems Biol Reprod Med. 2011;57(3):119–23.CrossRef
128.
go back to reference Greenman Y, Rouach V, Limor R, Gilad S, Stern N. Testosterone is a strong correlate of ghrelin levels in men and postmenopausal women. Neuroendocrinology. 2009;89(1):79–85.PubMedCrossRef Greenman Y, Rouach V, Limor R, Gilad S, Stern N. Testosterone is a strong correlate of ghrelin levels in men and postmenopausal women. Neuroendocrinology. 2009;89(1):79–85.PubMedCrossRef
130.
go back to reference Page ST, Herbst KL, Amory JK, Coviello AD, Anawalt BD, Matsumoto AM, et al. Testosterone administration suppresses adiponectin levels in men. J Androl. 2005;26(1):85–92.PubMed Page ST, Herbst KL, Amory JK, Coviello AD, Anawalt BD, Matsumoto AM, et al. Testosterone administration suppresses adiponectin levels in men. J Androl. 2005;26(1):85–92.PubMed
131.
go back to reference Yuan F, Li Y-N, Liu Y-H, Yi B, Tian J-W, Liu F-Y. Adiponectin inhibits the generation of reactive oxygen species induced by high glucose and promotes endothelial NO synthase formation in human mesangial cells. Mol Med Rep. 2012;6(2):449–53.PubMedCrossRef Yuan F, Li Y-N, Liu Y-H, Yi B, Tian J-W, Liu F-Y. Adiponectin inhibits the generation of reactive oxygen species induced by high glucose and promotes endothelial NO synthase formation in human mesangial cells. Mol Med Rep. 2012;6(2):449–53.PubMedCrossRef
132.
go back to reference Zheng D, Zhao Y, Shen Y, Chang X, Ju S, Guo L. Orexin A-mediated stimulation of 3β-HSD expression and testosterone production through MAPK signaling pathways in primary rat Leydig cells. J Endocrinol Investig. 2014;37(3):285–92.CrossRef Zheng D, Zhao Y, Shen Y, Chang X, Ju S, Guo L. Orexin A-mediated stimulation of 3β-HSD expression and testosterone production through MAPK signaling pathways in primary rat Leydig cells. J Endocrinol Investig. 2014;37(3):285–92.CrossRef
133.
134.
go back to reference Aggerholm AS, Thulstrup AM, Toft G, Ramlau-Hansen CH, Bonde JP. Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil Steril. 2008;90(3):619–26.PubMedCrossRef Aggerholm AS, Thulstrup AM, Toft G, Ramlau-Hansen CH, Bonde JP. Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil Steril. 2008;90(3):619–26.PubMedCrossRef
135.
go back to reference Al-Ali B M, Gutschi T, Pummer K, Zigeuner R, Brookman-May S, Wieland W, et al. Body mass index has no impact on sperm quality but on reproductive hormones levels. Andrologia. 2014;46(2):106–11.CrossRef Al-Ali B M, Gutschi T, Pummer K, Zigeuner R, Brookman-May S, Wieland W, et al. Body mass index has no impact on sperm quality but on reproductive hormones levels. Andrologia. 2014;46(2):106–11.CrossRef
136.
go back to reference Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: impact on human health. Pharmacognosy Rev. 2010;4(8):118.CrossRef Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: impact on human health. Pharmacognosy Rev. 2010;4(8):118.CrossRef
137.
go back to reference Chavarro JE, Toth TL, Sadio SM, Hauser R. Soy food and isoflavone intake in relation to semen quality parameters among men from an infertility clinic. Hum Reprod. 2008;23(11):2584–90.PubMedPubMedCentralCrossRef Chavarro JE, Toth TL, Sadio SM, Hauser R. Soy food and isoflavone intake in relation to semen quality parameters among men from an infertility clinic. Hum Reprod. 2008;23(11):2584–90.PubMedPubMedCentralCrossRef
138.
go back to reference Mendiola J, Torres-Cantero AM, Moreno-Grau JM, Ten J, Roca M, Moreno-Grau S, et al. Food intake and its relationship with semen quality: a case-control study. Fertil Steril. 2009;91(3):812–8.PubMedCrossRef Mendiola J, Torres-Cantero AM, Moreno-Grau JM, Ten J, Roca M, Moreno-Grau S, et al. Food intake and its relationship with semen quality: a case-control study. Fertil Steril. 2009;91(3):812–8.PubMedCrossRef
139.
go back to reference Ruggiero C, Ehrenshaft M, Cleland E, Stadler K. High-fat diet induces an initial adaptation of mitochondrial bioenergetics in the kidney despite evident oxidative stress and mitochondrial ROS production. Am J Physiol Endocrinol Metab. 2011;300(6):8.CrossRef Ruggiero C, Ehrenshaft M, Cleland E, Stadler K. High-fat diet induces an initial adaptation of mitochondrial bioenergetics in the kidney despite evident oxidative stress and mitochondrial ROS production. Am J Physiol Endocrinol Metab. 2011;300(6):8.CrossRef
140.
go back to reference Kolodziej U, Maciejczyk M, Niklinska W, Waszkiel D, Zendzian-Piotrowska M, Zukowski P, et al. Chronic high-protein diet induces oxidative stress and alters the salivary gland function in rats. Arch Oral Biol. 2017;84:6–12.PubMedCrossRef Kolodziej U, Maciejczyk M, Niklinska W, Waszkiel D, Zendzian-Piotrowska M, Zukowski P, et al. Chronic high-protein diet induces oxidative stress and alters the salivary gland function in rats. Arch Oral Biol. 2017;84:6–12.PubMedCrossRef
141.
go back to reference Kahle M, Schafer A, Seelig A, Schultheiss J, Wu M, Aichler M, et al. High fat diet-induced modifications in membrane lipid and mitochondrial-membrane protein signatures precede the development of hepatic insulin resistance in mice. Mol Metab. 2014;4(1):39–50.PubMedPubMedCentralCrossRef Kahle M, Schafer A, Seelig A, Schultheiss J, Wu M, Aichler M, et al. High fat diet-induced modifications in membrane lipid and mitochondrial-membrane protein signatures precede the development of hepatic insulin resistance in mice. Mol Metab. 2014;4(1):39–50.PubMedPubMedCentralCrossRef
142.
go back to reference Chakraborty TR, Donthireddy L, Adhikary D, Chakraborty S. Long-term high fat diet has a profound effect on body weight, hormone levels, and estrous cycle in mice. Med Sci Monit. 2016;22:1601–8. Chakraborty TR, Donthireddy L, Adhikary D, Chakraborty S. Long-term high fat diet has a profound effect on body weight, hormone levels, and estrous cycle in mice. Med Sci Monit. 2016;22:1601–8.
143.
go back to reference Attaman JA, Toth TL, Furtado J, Campos H, Hauser R, Chavarro JE. Dietary fat and semen quality among men attending a fertility clinic. Hum Reprod. 2012; 27(5):1466–74. Attaman JA, Toth TL, Furtado J, Campos H, Hauser R, Chavarro JE. Dietary fat and semen quality among men attending a fertility clinic. Hum Reprod. 2012; 27(5):1466–74.
144.
go back to reference Agarwal A, Sekhon LH. The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb). 2010;13(4):217–25.CrossRef Agarwal A, Sekhon LH. The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb). 2010;13(4):217–25.CrossRef
145.
go back to reference Ahmadi S, Bashiri R, Ghadiri-Anari A, Nadjarzadeh A. Antioxidant supplements and semen parameters: an evidence based review. Int J Reprod Biomed. 2016;14(12):729–36.CrossRef Ahmadi S, Bashiri R, Ghadiri-Anari A, Nadjarzadeh A. Antioxidant supplements and semen parameters: an evidence based review. Int J Reprod Biomed. 2016;14(12):729–36.CrossRef
146.
go back to reference Wu D, Cederbaum AI. Alcohol, oxidative stress, and free radical damage. Alcohol Res Health. 2003;27:277–84.PubMed Wu D, Cederbaum AI. Alcohol, oxidative stress, and free radical damage. Alcohol Res Health. 2003;27:277–84.PubMed
147.
go back to reference Qureshi GA, Memon SA, Memon AB, Ghouri RA, Memon JM, Parvez SH. The emerging role of iron, zinc, copper, magnesium and selenium and oxidative stress in health and diseases. Brill Online. 2005;19(2):147–69. Qureshi GA, Memon SA, Memon AB, Ghouri RA, Memon JM, Parvez SH. The emerging role of iron, zinc, copper, magnesium and selenium and oxidative stress in health and diseases. Brill Online. 2005;19(2):147–69.
148.
go back to reference Whitfield JB, Zhu G, Heath AC, Powell LW, Martin NG. Effects of alcohol consumption on indices of iron stores and of iron stores on alcohol intake markers. Alcohol Clin Exp Res. 2001;25(7):1037–45.PubMedCrossRef Whitfield JB, Zhu G, Heath AC, Powell LW, Martin NG. Effects of alcohol consumption on indices of iron stores and of iron stores on alcohol intake markers. Alcohol Clin Exp Res. 2001;25(7):1037–45.PubMedCrossRef
149.
go back to reference Emanuele MA, Emanuele N. Alcohol and the male reproductive system. Alcohol Res Health. 2001;25(4):282–7.PubMed Emanuele MA, Emanuele N. Alcohol and the male reproductive system. Alcohol Res Health. 2001;25(4):282–7.PubMed
150.
go back to reference Maneesh M, Dutta S, Chakrabarti A, Vasudevan D. Alcohol abuse-duration dependent decrease in plasma testosterone and antioxidants in males. Indian J Physiol Pharmacol. 2006;50(3):291.PubMed Maneesh M, Dutta S, Chakrabarti A, Vasudevan D. Alcohol abuse-duration dependent decrease in plasma testosterone and antioxidants in males. Indian J Physiol Pharmacol. 2006;50(3):291.PubMed
151.
go back to reference Uddin S, Wilson T, Emanuele M, Williams D, Kelley M, Emanuele N. Ethanol-induced alterations in the posttranslational processing, but not secretion of luteinizing hormone-releasing hormone in vitro. Alcohol Clin Exp Res. 1996;20(3):556–60.PubMedCrossRef Uddin S, Wilson T, Emanuele M, Williams D, Kelley M, Emanuele N. Ethanol-induced alterations in the posttranslational processing, but not secretion of luteinizing hormone-releasing hormone in vitro. Alcohol Clin Exp Res. 1996;20(3):556–60.PubMedCrossRef
152.
go back to reference Kim JH, Kim HJ, Noh HS, Roh GS, Kang SS, Cho GJ, et al. Suppression by ethanol of male reproductive activity. Brain Res. 2003;989(1):91–8.PubMedCrossRef Kim JH, Kim HJ, Noh HS, Roh GS, Kang SS, Cho GJ, et al. Suppression by ethanol of male reproductive activity. Brain Res. 2003;989(1):91–8.PubMedCrossRef
153.
go back to reference Salonen I, Huhtaniemi I. Effects of chronic ethanol diet on pituitary-testicular function of the rat. Biol Reprod. 1990;42(1):55–62.PubMedCrossRef Salonen I, Huhtaniemi I. Effects of chronic ethanol diet on pituitary-testicular function of the rat. Biol Reprod. 1990;42(1):55–62.PubMedCrossRef
154.
go back to reference Zhu Q, Van Thiel DH, Gavaler JS. Effects of ethanol on rat Sertoli cell function: studies in vitro and in vivo. Alcohol Clin Exp Res. 1997;21(8):1409–17.PubMed Zhu Q, Van Thiel DH, Gavaler JS. Effects of ethanol on rat Sertoli cell function: studies in vitro and in vivo. Alcohol Clin Exp Res. 1997;21(8):1409–17.PubMed
155.
go back to reference Zhu Q, Meisinger J, Emanuele NV, Emanuele MA, LaPaglia N, Thiel DH. Ethanol exposure enhances apoptosis within the testes. Alcohol Clin Exp Res. 2000;24(10):1550–6.PubMedCrossRef Zhu Q, Meisinger J, Emanuele NV, Emanuele MA, LaPaglia N, Thiel DH. Ethanol exposure enhances apoptosis within the testes. Alcohol Clin Exp Res. 2000;24(10):1550–6.PubMedCrossRef
156.
go back to reference Pajarinen J, Karhunen PJ, Savolainen V, Lalu K, Penttilä A, Laippala P. Moderate alcohol consumption and disorders of human spermatogenesis. Alcohol Clin Exp Res. 1996;20(2):332–7.PubMedCrossRef Pajarinen J, Karhunen PJ, Savolainen V, Lalu K, Penttilä A, Laippala P. Moderate alcohol consumption and disorders of human spermatogenesis. Alcohol Clin Exp Res. 1996;20(2):332–7.PubMedCrossRef
157.
158.
go back to reference Brown TT, Wisniewski AB, Gonadal DAS. Adrenal abnormalities in drug users: cause or consequence of drug use behavior and poor health outcomes. Am J Infect Dis. 2006;2(3):130–5.PubMedPubMedCentralCrossRef Brown TT, Wisniewski AB, Gonadal DAS. Adrenal abnormalities in drug users: cause or consequence of drug use behavior and poor health outcomes. Am J Infect Dis. 2006;2(3):130–5.PubMedPubMedCentralCrossRef
159.
go back to reference Sarafian TA, Magallanes JAM, Shau H, Tashkin D, Roth MD. Oxidative stress produced by marijuana smoke: an adverse effect enhanced by cannabinoids. Am J Respir Cell Mol Biol. 1999;20(6):1286–93.PubMedCrossRef Sarafian TA, Magallanes JAM, Shau H, Tashkin D, Roth MD. Oxidative stress produced by marijuana smoke: an adverse effect enhanced by cannabinoids. Am J Respir Cell Mol Biol. 1999;20(6):1286–93.PubMedCrossRef
160.
go back to reference Kim HR, Son BH, Lee SY, Chung KH, Oh SM. The role of p53 in marijuana smoke condensates-induced genotoxicity and apoptosis. Environ Health Toxicol. 2012;27:e2012017. Kim HR, Son BH, Lee SY, Chung KH, Oh SM. The role of p53 in marijuana smoke condensates-induced genotoxicity and apoptosis. Environ Health Toxicol. 2012;27:e2012017.
161.
go back to reference Faux SP, Tai T, Thorne D, Xu Y, Breheny D, Gaca M. The role of oxidative stress in the biological responses of lung epithelial cells to cigarette smoke. Biomarkers. 2009;1:90–6.CrossRef Faux SP, Tai T, Thorne D, Xu Y, Breheny D, Gaca M. The role of oxidative stress in the biological responses of lung epithelial cells to cigarette smoke. Biomarkers. 2009;1:90–6.CrossRef
162.
go back to reference Abs R, Verhelst J, Maeyaert J, Van Buyten J-P, Opsomer F, Adriaensen H, et al. Endocrine consequences of long-term intrathecal administration of opioids. J Clin Endocrinol Metab. 2000;85(6):2215–22.PubMedCrossRef Abs R, Verhelst J, Maeyaert J, Van Buyten J-P, Opsomer F, Adriaensen H, et al. Endocrine consequences of long-term intrathecal administration of opioids. J Clin Endocrinol Metab. 2000;85(6):2215–22.PubMedCrossRef
163.
go back to reference Daniell HW. Hypogonadism in men consuming sustained-action oral opioids. J Pain. 2002;3(5):377–84.PubMedCrossRef Daniell HW. Hypogonadism in men consuming sustained-action oral opioids. J Pain. 2002;3(5):377–84.PubMedCrossRef
164.
go back to reference Fronczak CM, Kim ED, Barqawi AB. The insults of illicit drug use on male fertility. J Androl. 2012;33(4):515–28.PubMedCrossRef Fronczak CM, Kim ED, Barqawi AB. The insults of illicit drug use on male fertility. J Androl. 2012;33(4):515–28.PubMedCrossRef
165.
go back to reference Park B, McPartland JM, Glass M. Cannabis, cannabinoids and reproduction. Prostaglandins Leukot Essent Fatty Acids. 2004;70(2):189–97.PubMedCrossRef Park B, McPartland JM, Glass M. Cannabis, cannabinoids and reproduction. Prostaglandins Leukot Essent Fatty Acids. 2004;70(2):189–97.PubMedCrossRef
166.
go back to reference Patra P, Wadsworth R. Quantitative evaluation of spermatogenesis in mice following chronic exposure to cannabinoids. Andrologia. 1991;23(2):151–6.PubMedCrossRef Patra P, Wadsworth R. Quantitative evaluation of spermatogenesis in mice following chronic exposure to cannabinoids. Andrologia. 1991;23(2):151–6.PubMedCrossRef
167.
go back to reference Heesch CM, Negus BH, Bost JE, Keffer JH, Snyder RW 2nd, Eichhorn EJ. Effects of cocaine on anterior pituitary and gonadal hormones. J Pharmacol Exp Ther. 1996;278(3):1195–200.PubMed Heesch CM, Negus BH, Bost JE, Keffer JH, Snyder RW 2nd, Eichhorn EJ. Effects of cocaine on anterior pituitary and gonadal hormones. J Pharmacol Exp Ther. 1996;278(3):1195–200.PubMed
168.
go back to reference Meri ZB, Irshid IB, Migdadi M, Irshid AB, Mhanna SA. Does cigarette smoking affect seminal fluid parameters? A comparative study. Oman Med J. 2013;28(1):12–6.PubMedPubMedCentralCrossRef Meri ZB, Irshid IB, Migdadi M, Irshid AB, Mhanna SA. Does cigarette smoking affect seminal fluid parameters? A comparative study. Oman Med J. 2013;28(1):12–6.PubMedPubMedCentralCrossRef
169.
go back to reference Sheynkin Y, Gioia K. Environmental and lifestyle considerations for the infertile male. AUA Update Ser. 2013;32(4):30–8. Sheynkin Y, Gioia K. Environmental and lifestyle considerations for the infertile male. AUA Update Ser. 2013;32(4):30–8.
170.
go back to reference Tostes RC, Carneiro FS, Lee AJ, Giachini FR, Leite R, Osawa Y, et al. Cigarette smoking and erectile dysfunction: focus on NO bioavailability and ROS generation. J Sex Med. 2008;5(6):1284–95.PubMedPubMedCentralCrossRef Tostes RC, Carneiro FS, Lee AJ, Giachini FR, Leite R, Osawa Y, et al. Cigarette smoking and erectile dysfunction: focus on NO bioavailability and ROS generation. J Sex Med. 2008;5(6):1284–95.PubMedPubMedCentralCrossRef
171.
go back to reference Halmenschlager G, Rossetto S, Lara GM, Rhoden EL. Endocrinology: evaluation of the effects of cigarette smoking on testosterone levels in adult men. J Sex Med. 2009;6(6):1763–72.PubMedCrossRef Halmenschlager G, Rossetto S, Lara GM, Rhoden EL. Endocrinology: evaluation of the effects of cigarette smoking on testosterone levels in adult men. J Sex Med. 2009;6(6):1763–72.PubMedCrossRef
172.
go back to reference Shiels MS, Rohrmann S, Menke A, Selvin E, Crespo CJ, Rifai N, et al. Association of cigarette smoking, alcohol consumption, and physical activity with sex steroid hormone levels in US men. Cancer Causes Control. 2009;20(6):877–86.PubMedPubMedCentralCrossRef Shiels MS, Rohrmann S, Menke A, Selvin E, Crespo CJ, Rifai N, et al. Association of cigarette smoking, alcohol consumption, and physical activity with sex steroid hormone levels in US men. Cancer Causes Control. 2009;20(6):877–86.PubMedPubMedCentralCrossRef
173.
go back to reference Trummer H, Habermann H, Haas J, Pummer K. The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 2002;17(6):1554–9.PubMedCrossRef Trummer H, Habermann H, Haas J, Pummer K. The impact of cigarette smoking on human semen parameters and hormones. Hum Reprod. 2002;17(6):1554–9.PubMedCrossRef
174.
go back to reference Kapoor D, Jones TH. Smoking and hormones in health and endocrine disorders. Eur J Endocrinol. 2005;152(4):491–9.PubMedCrossRef Kapoor D, Jones TH. Smoking and hormones in health and endocrine disorders. Eur J Endocrinol. 2005;152(4):491–9.PubMedCrossRef
175.
go back to reference Neri M, Bello S, Bonsignore A, Cantatore S, Riezzo I, Turillazzi E, et al. Anabolic androgenic steroids abuse and liver toxicity. Mini Rev Med Chemist. 2011;11(5):430–7.CrossRef Neri M, Bello S, Bonsignore A, Cantatore S, Riezzo I, Turillazzi E, et al. Anabolic androgenic steroids abuse and liver toxicity. Mini Rev Med Chemist. 2011;11(5):430–7.CrossRef
176.
177.
go back to reference de Souza GL, Hallak J. Anabolic steroids and male infertility: a comprehensive review. BJU Int. 2011;108(11):1860–5.PubMedCrossRef de Souza GL, Hallak J. Anabolic steroids and male infertility: a comprehensive review. BJU Int. 2011;108(11):1860–5.PubMedCrossRef
178.
go back to reference El Osta R, Almont T, Diligent C, Hubert N, Eschwege P, Hubert J. Anabolic steroids abuse and male infertility. Basic Clin Androl. 2016;26:1–8. El Osta R, Almont T, Diligent C, Hubert N, Eschwege P, Hubert J. Anabolic steroids abuse and male infertility. Basic Clin Androl. 2016;26:1–8.
179.
go back to reference Foster ZJ, Housner JA. Anabolic-androgenic steroids and testosterone precursors: ergogenic aids and sport. Curr Sports Med Rep. 2004;3(4):234–41.PubMedCrossRef Foster ZJ, Housner JA. Anabolic-androgenic steroids and testosterone precursors: ergogenic aids and sport. Curr Sports Med Rep. 2004;3(4):234–41.PubMedCrossRef
180.
go back to reference Fujii J, Iuchi Y, Matsuki S, Ishii T. Cooperative function of antioxidant and redox systems against oxidative stress in male reproductive tissues. Asian J Androl. 2003;5(3):231–42.PubMed Fujii J, Iuchi Y, Matsuki S, Ishii T. Cooperative function of antioxidant and redox systems against oxidative stress in male reproductive tissues. Asian J Androl. 2003;5(3):231–42.PubMed
181.
go back to reference Allen JA, Shankara T, Janus P, Buck S, Diemer T, Held Hales K, et al. Energized, polarized, and actively respiring mitochondria are required for acute Leydig cell steroidogenesis. Endocrinology. 2006;147(8):3924–35.PubMedCrossRef Allen JA, Shankara T, Janus P, Buck S, Diemer T, Held Hales K, et al. Energized, polarized, and actively respiring mitochondria are required for acute Leydig cell steroidogenesis. Endocrinology. 2006;147(8):3924–35.PubMedCrossRef
182.
go back to reference Chen H, Zhou L, Lin C-Y, Beattie MC, Liu J, Zirkin BR. Effect of glutathione redox state on Leydig cell susceptibility to acute oxidative stress. Mol Cell Endocrinol. 2010;323(2):147–54.PubMedPubMedCentralCrossRef Chen H, Zhou L, Lin C-Y, Beattie MC, Liu J, Zirkin BR. Effect of glutathione redox state on Leydig cell susceptibility to acute oxidative stress. Mol Cell Endocrinol. 2010;323(2):147–54.PubMedPubMedCentralCrossRef
183.
go back to reference Veldhuis JD. Recent insights into neuroendocrine mechanisms of aging of the human male hypothalamic-pituitary-gonadal Axis. J Androl. 1999;20(1):1–18.PubMed Veldhuis JD. Recent insights into neuroendocrine mechanisms of aging of the human male hypothalamic-pituitary-gonadal Axis. J Androl. 1999;20(1):1–18.PubMed
184.
go back to reference Diemer T, Allen JA, Hales KH, Hales DB. Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology. 2003;144(7):2882–91.PubMedCrossRef Diemer T, Allen JA, Hales KH, Hales DB. Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology. 2003;144(7):2882–91.PubMedCrossRef
185.
go back to reference Koksal I, Usta M, Orhan I, Abbasoglu S, Kadioglu A. Potential role of reactive oxygen species on testicular pathology associated with infertility. Asian J Androl. 2003;5(2):95–100.PubMed Koksal I, Usta M, Orhan I, Abbasoglu S, Kadioglu A. Potential role of reactive oxygen species on testicular pathology associated with infertility. Asian J Androl. 2003;5(2):95–100.PubMed
186.
go back to reference Hanukoglu I. Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev. 2006;38(1–2):171–96.PubMedCrossRef Hanukoglu I. Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev. 2006;38(1–2):171–96.PubMedCrossRef
187.
go back to reference Peltola V, Huhtaniemi I, Metsa-Ketela T, Ahotupa M. Induction of lipid peroxidation during steroidogenesis in the rat testis. Endocrinology. 1996;137(1):105–12.PubMedCrossRef Peltola V, Huhtaniemi I, Metsa-Ketela T, Ahotupa M. Induction of lipid peroxidation during steroidogenesis in the rat testis. Endocrinology. 1996;137(1):105–12.PubMedCrossRef
188.
go back to reference Perheentupa A, De Jong F, Huhtaniemi I. Biphasic effect of exogenous testosterone on follicle-stimulating hormone gene expression and synthesis in the male rat. Mol Cell Endocrinol. 1993;93(2):135–41.PubMedCrossRef Perheentupa A, De Jong F, Huhtaniemi I. Biphasic effect of exogenous testosterone on follicle-stimulating hormone gene expression and synthesis in the male rat. Mol Cell Endocrinol. 1993;93(2):135–41.PubMedCrossRef
189.
go back to reference Perheentupa A, Huhtaniemi I. Gonadotropin gene expression and secretion in gonadotropin-releasing hormone antagonist-treated male rats: effect of sex steroid replacement. Endocrinology. 1990;126(6):3204–9.PubMedCrossRef Perheentupa A, Huhtaniemi I. Gonadotropin gene expression and secretion in gonadotropin-releasing hormone antagonist-treated male rats: effect of sex steroid replacement. Endocrinology. 1990;126(6):3204–9.PubMedCrossRef
190.
go back to reference Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxidative Med Cell Longev. 2008;1(1):15–24.CrossRef Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Oxidative Med Cell Longev. 2008;1(1):15–24.CrossRef
191.
go back to reference Chigurupati S, Son TG, Hyun D-H, Lathia JD, Mughal MR, Savell J, et al. Lifelong running reduces oxidative stress and degenerative changes in the testes of mice. J Endocrinol. 2008;199(2):333–41.PubMedPubMedCentralCrossRef Chigurupati S, Son TG, Hyun D-H, Lathia JD, Mughal MR, Savell J, et al. Lifelong running reduces oxidative stress and degenerative changes in the testes of mice. J Endocrinol. 2008;199(2):333–41.PubMedPubMedCentralCrossRef
192.
go back to reference Loveland KL, Klein B, Pueschl D, Indumathy S, Bergmann M, Loveland BE, et al. Cytokines in male fertility and reproductive pathologies: Immunoregulation and beyond. Front Endocrinol. 2017;8:1–16. Loveland KL, Klein B, Pueschl D, Indumathy S, Bergmann M, Loveland BE, et al. Cytokines in male fertility and reproductive pathologies: Immunoregulation and beyond. Front Endocrinol. 2017;8:1–16.
193.
go back to reference Maegawa M, Kamada M, Irahara M, Yamamoto S, Yoshikawa S, Kasai Y, et al. A repertoire of cytokines in human seminal plasma. J Reprod Immunol. 2002;54(1–2):33–42.PubMedCrossRef Maegawa M, Kamada M, Irahara M, Yamamoto S, Yoshikawa S, Kasai Y, et al. A repertoire of cytokines in human seminal plasma. J Reprod Immunol. 2002;54(1–2):33–42.PubMedCrossRef
194.
go back to reference Joki-Korpela P, Sahrakorpi N, Halttunen M, Surcel HM, Paavonen J, Tiitinen A. The role of Chlamydia trachomatis infection in male infertility. Fertil Steril. 2009;91(4 Suppl):1448–50. Joki-Korpela P, Sahrakorpi N, Halttunen M, Surcel HM, Paavonen J, Tiitinen A. The role of Chlamydia trachomatis infection in male infertility. Fertil Steril. 2009;91(4 Suppl):1448–50.
195.
go back to reference Ochsendorf F. Infections in the male genital tract and reactive oxygen species. Hum Reprod Update. 1999;5(5):399–420.PubMedCrossRef Ochsendorf F. Infections in the male genital tract and reactive oxygen species. Hum Reprod Update. 1999;5(5):399–420.PubMedCrossRef
196.
go back to reference Dejucq N, Jegou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65(2):208–31.PubMedPubMedCentralCrossRef Dejucq N, Jegou B. Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev. 2001;65(2):208–31.PubMedPubMedCentralCrossRef
197.
go back to reference Aiman J, Brenner PF, MacDonald PC. Androgen and estrogen production in elderly men with gynecomastia and testicular atrophy after mumps orchitis. J Clin Endocrinol Metab. 1980;50(2):380–6.PubMedCrossRef Aiman J, Brenner PF, MacDonald PC. Androgen and estrogen production in elderly men with gynecomastia and testicular atrophy after mumps orchitis. J Clin Endocrinol Metab. 1980;50(2):380–6.PubMedCrossRef
198.
go back to reference Adamopoulos DA, Lawrence DM, Vassilopoulos P, Contoyiannis PA, Swyer GI. Pituitary-testicular interrelationships in mumps orchitis and other viral infections. Br Med J. 1978;1(6121):1177–80.PubMedPubMedCentralCrossRef Adamopoulos DA, Lawrence DM, Vassilopoulos P, Contoyiannis PA, Swyer GI. Pituitary-testicular interrelationships in mumps orchitis and other viral infections. Br Med J. 1978;1(6121):1177–80.PubMedPubMedCentralCrossRef
199.
go back to reference Dimitrakov J, Joffe HV, Soldin SJ, Bolus R, Buffington CT, Nickel JC. Adrenocortical hormone abnormalities in men with chronic prostatitis/chronic pelvic pain syndrome. Urology. 2008;71(2):261–6.PubMedPubMedCentralCrossRef Dimitrakov J, Joffe HV, Soldin SJ, Bolus R, Buffington CT, Nickel JC. Adrenocortical hormone abnormalities in men with chronic prostatitis/chronic pelvic pain syndrome. Urology. 2008;71(2):261–6.PubMedPubMedCentralCrossRef
201.
go back to reference Zirkin BR, Chen H. Regulation of Leydig cell steroidogenic function during aging. Biol Reprod. 2000;63(4):977–81.PubMedCrossRef Zirkin BR, Chen H. Regulation of Leydig cell steroidogenic function during aging. Biol Reprod. 2000;63(4):977–81.PubMedCrossRef
202.
go back to reference Turner TT, Bang HJ, Lysiak JJ. Experimental testicular torsion: reperfusion blood flow and subsequent testicular venous plasma testosterone concentrations. Urology. 2005;65(2):390–4.PubMedCrossRef Turner TT, Bang HJ, Lysiak JJ. Experimental testicular torsion: reperfusion blood flow and subsequent testicular venous plasma testosterone concentrations. Urology. 2005;65(2):390–4.PubMedCrossRef
203.
go back to reference Luo L, Chen H, Trush MA, Show MD, Anway MD, Zirkin BR. Aging and the brown Norway rat leydig cell antioxidant defense system. J Androl. 2006;27(2):240–7.PubMedCrossRef Luo L, Chen H, Trush MA, Show MD, Anway MD, Zirkin BR. Aging and the brown Norway rat leydig cell antioxidant defense system. J Androl. 2006;27(2):240–7.PubMedCrossRef
204.
go back to reference Aitken RJ, Baker MA, Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod BioMed Online. 2003;7(1):65–70.PubMedCrossRef Aitken RJ, Baker MA, Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod BioMed Online. 2003;7(1):65–70.PubMedCrossRef
205.
go back to reference Agarwal A, Said TM. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update. 2003;9(4):331–45.PubMedCrossRef Agarwal A, Said TM. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update. 2003;9(4):331–45.PubMedCrossRef
206.
go back to reference Meucci E, Milardi D, Mordente A, Martorana GE, Giacchi E, De Marinis L, et al. Total antioxidant capacity in patients with varicoceles. Fertil Steril. 2003;79:1577–83.PubMedCrossRef Meucci E, Milardi D, Mordente A, Martorana GE, Giacchi E, De Marinis L, et al. Total antioxidant capacity in patients with varicoceles. Fertil Steril. 2003;79:1577–83.PubMedCrossRef
207.
go back to reference Mancini A, Leone E, Festa R, Grande G, Silvestrini A, Marinis L, et al. Effects of testosterone on antioxidant systems in male secondary hypogonadism. J Androl. 2008;29(6):622–9.PubMedCrossRef Mancini A, Leone E, Festa R, Grande G, Silvestrini A, Marinis L, et al. Effects of testosterone on antioxidant systems in male secondary hypogonadism. J Androl. 2008;29(6):622–9.PubMedCrossRef
208.
go back to reference Chainy G, Samantaray S, Samanta L. Testosterone-induced changes in testicular antioxidant system. Andrologia. 1997;29(6):343–9.PubMedCrossRef Chainy G, Samantaray S, Samanta L. Testosterone-induced changes in testicular antioxidant system. Andrologia. 1997;29(6):343–9.PubMedCrossRef
209.
go back to reference Shang X, Huang Y, Ye Z, Yu X, Gu W. Protection of melatonin against damage of sperm mitochondrial function induced by reactive oxygen species. Zhonghua Nan Ke Xue. 2004;10(8):604–7.PubMed Shang X, Huang Y, Ye Z, Yu X, Gu W. Protection of melatonin against damage of sperm mitochondrial function induced by reactive oxygen species. Zhonghua Nan Ke Xue. 2004;10(8):604–7.PubMed
210.
go back to reference Lakpour N, Mahfouz RZ, Akhondi MM, Agarwal A, Kharrazi H, Zeraati H, et al. Relationship of seminal plasma antioxidants and serum male hormones with sperm chromatin status in male factor infertility. Syst Biol Reprod Med. 2012;58(5):236–44.PubMedCrossRef Lakpour N, Mahfouz RZ, Akhondi MM, Agarwal A, Kharrazi H, Zeraati H, et al. Relationship of seminal plasma antioxidants and serum male hormones with sperm chromatin status in male factor infertility. Syst Biol Reprod Med. 2012;58(5):236–44.PubMedCrossRef
211.
go back to reference Oluboyo A, Adijeh R, Onyenekwe C, Oluboyo B, Mbaeri T, Odiegwu C, et al. Relationship between serum levels of testosterone, zinc and selenium in infertile males attending fertility clinic in Nnewi, south East Nigeria. Afr J Med Med Sci. 2012;41:51–4.PubMed Oluboyo A, Adijeh R, Onyenekwe C, Oluboyo B, Mbaeri T, Odiegwu C, et al. Relationship between serum levels of testosterone, zinc and selenium in infertile males attending fertility clinic in Nnewi, south East Nigeria. Afr J Med Med Sci. 2012;41:51–4.PubMed
212.
go back to reference Safarinejad MR. Efficacy of coenzyme Q10 on semen parameters, sperm function and reproductive hormones in infertile men. J Urol. 2009;182(1):237–48.PubMedCrossRef Safarinejad MR. Efficacy of coenzyme Q10 on semen parameters, sperm function and reproductive hormones in infertile men. J Urol. 2009;182(1):237–48.PubMedCrossRef
213.
go back to reference Richthoff J, Spano M, Giwercman Y, Frohm B, Jepson K, Malm J, et al. The impact of testicular and accessory sex gland function on sperm chromatin integrity as assessed by the sperm chromatin structure assay (SCSA). Hum Reprod. 2002;17(12):3162–9.PubMedCrossRef Richthoff J, Spano M, Giwercman Y, Frohm B, Jepson K, Malm J, et al. The impact of testicular and accessory sex gland function on sperm chromatin integrity as assessed by the sperm chromatin structure assay (SCSA). Hum Reprod. 2002;17(12):3162–9.PubMedCrossRef
214.
go back to reference Meeker JD, Singh NP, Hauser R. Serum concentrations of estradiol and free T4 are inversely correlated with sperm DNA damage in men from an infertility clinic. J Androl. 2008;29(4):379–88.PubMedPubMedCentralCrossRef Meeker JD, Singh NP, Hauser R. Serum concentrations of estradiol and free T4 are inversely correlated with sperm DNA damage in men from an infertility clinic. J Androl. 2008;29(4):379–88.PubMedPubMedCentralCrossRef
215.
go back to reference Dobrzyńska MM, Baumgartner A, Anderson D. Antioxidants modulate thyroid hormone-and noradrenaline-induced DNA damage in human sperm. Mutagenesis. 2004;19(4):325–30.PubMedCrossRef Dobrzyńska MM, Baumgartner A, Anderson D. Antioxidants modulate thyroid hormone-and noradrenaline-induced DNA damage in human sperm. Mutagenesis. 2004;19(4):325–30.PubMedCrossRef
216.
go back to reference Palomba S, Falbo A, Espinola S, Rocca M, Capasso S, Cappiello F, et al. Effects of highly purified follicle-stimulating hormone on sperm DNA damage in men with male idiopathic subfertility: a pilot study. J Endocrinol Investig. 2011;34(10):747–52. Palomba S, Falbo A, Espinola S, Rocca M, Capasso S, Cappiello F, et al. Effects of highly purified follicle-stimulating hormone on sperm DNA damage in men with male idiopathic subfertility: a pilot study. J Endocrinol Investig. 2011;34(10):747–52.
217.
go back to reference Colacurci N, Monti MG, Fornaro F, Izzo G, Izzo P, Trotta C, et al. Recombinant human FSH reduces sperm DNA fragmentation in men with idiopathic oligoasthenoteratozoospermia. J Androl. 2012;33(4):588–93.PubMedCrossRef Colacurci N, Monti MG, Fornaro F, Izzo G, Izzo P, Trotta C, et al. Recombinant human FSH reduces sperm DNA fragmentation in men with idiopathic oligoasthenoteratozoospermia. J Androl. 2012;33(4):588–93.PubMedCrossRef
218.
go back to reference Tesarik J, Martinez F, Rienzi L, Iacobelli M, Ubaldi F, Mendoza C, et al. In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Hum Reprod. 2002;17(7):1811–9.PubMedCrossRef Tesarik J, Martinez F, Rienzi L, Iacobelli M, Ubaldi F, Mendoza C, et al. In-vitro effects of FSH and testosterone withdrawal on caspase activation and DNA fragmentation in different cell types of human seminiferous epithelium. Hum Reprod. 2002;17(7):1811–9.PubMedCrossRef
219.
go back to reference Nematollahi-Mahani SN, Azizollahi GH, Baneshi MR, Safari Z, Azizollahi S. Effect of folic acid and zinc sulphate on endocrine parameters and seminal antioxidant level after varicocelectomy. Andrologia. 2014;46(3):240–5.PubMedCrossRef Nematollahi-Mahani SN, Azizollahi GH, Baneshi MR, Safari Z, Azizollahi S. Effect of folic acid and zinc sulphate on endocrine parameters and seminal antioxidant level after varicocelectomy. Andrologia. 2014;46(3):240–5.PubMedCrossRef
220.
go back to reference Manna PR, Tena-Sempere M, Huhtaniemi IT. Molecular mechanisms of thyroid hormone-stimulated steroidogenesis in mouse Leydig tumor cells involvement of the steroidogenic acute regulatory (StAR) protein. J Biol Chem. 1999;274(9):5909–18.PubMedCrossRef Manna PR, Tena-Sempere M, Huhtaniemi IT. Molecular mechanisms of thyroid hormone-stimulated steroidogenesis in mouse Leydig tumor cells involvement of the steroidogenic acute regulatory (StAR) protein. J Biol Chem. 1999;274(9):5909–18.PubMedCrossRef
Metadata
Title
Reactive oxygen species and male reproductive hormones
Authors
Mahsa Darbandi
Sara Darbandi
Ashok Agarwal
Pallav Sengupta
Damayanthi Durairajanayagam
Ralf Henkel
Mohammad Reza Sadeghi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0406-2

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