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Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Research

Exogenous leptin affects sperm parameters and impairs blood testis barrier integrity in adult male mice

Authors: Xiaotong Wang, Xiaoke Zhang, Lian Hu, Honggang Li

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

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Abstract

Background

Serum leptin levels are augmented in obese infertile men and in men with azoospermia. They also correlate inversely with sperm concentration, motility and normal forms. The mechanisms underlying the adverse effects of excess leptin on male reproductive function remain unclear. The present study aimed to evaluate the effects of exogenous leptin on sperm parameters in mice and to explore the underlying mechanisms.

Methods

We treated normal adult male mice with saline, 0.1, 0.5 or 3 mg/kg leptin daily for 2 weeks. After treatment, serum leptin levels, serum testosterone levels, sperm parameters and testicular cell apoptosis were evaluated. Blood testis barrier integrity and the expression of tight junction-associated proteins in testes were also assessed. We further verified the direct effects of leptin on tight junction-associated proteins in Sertoli cells and the possible leptin signaling pathways involved in this process.

Results

After treatment, there were no significant differences in body weights, reproductive organ weights, serum leptin levels and serum testosterone levels between leptin-treated mice and control mice. Administration of 3 mg/kg leptin reduced sperm concentration, motility and progressive motility while increasing the percentage of abnormal sperm and testicular cell apoptosis. Mice treated with 3 mg/kg leptin also had impaired blood testis barrier integrity, which was related to decreased tight junction-associated proteins in testes. Leptin directly reduced tight junction-associated proteins in Sertoli cells, JAK2/STAT, PI3K and ERK pathways were suggested to be involved in this process.

Conclusions

Exogenous leptin negatively affects sperm parameters and impairs blood testis barrier integrity in mice. Leptin reduced tight junction-associated proteins in Sertoli cells, indicating that leptin has a direct role in impairing blood testis barrier integrity. Given the function of blood testis barrier in maintaining normal spermatogenesis, leptin-induced blood testis barrier impairment may be one of the mechanisms contributing to male subfertility and infertility.
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Literature
1.
go back to reference González RR, Simón C, Caballero-Campo P, Norman R, Chardonnens D, Devoto L, Bischof P. Leptin and reproduction. Hum Reprod Update. 2000;6(3):290–330.CrossRefPubMed González RR, Simón C, Caballero-Campo P, Norman R, Chardonnens D, Devoto L, Bischof P. Leptin and reproduction. Hum Reprod Update. 2000;6(3):290–330.CrossRefPubMed
4.
go back to reference Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB, Kuijper JL, Clifton DK, Steiner RA. Leptin is a metabolic signal to the reproductive system. Endocrinology. 1996;137(7):3144–7.CrossRefPubMed Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB, Kuijper JL, Clifton DK, Steiner RA. Leptin is a metabolic signal to the reproductive system. Endocrinology. 1996;137(7):3144–7.CrossRefPubMed
5.
go back to reference Mounzih K, Lu R, Chehab FF. Leptin treatment rescues the sterility of genetically obese Ob/Ob males. Endocrinology. 1997;138(3):1190–3.CrossRefPubMed Mounzih K, Lu R, Chehab FF. Leptin treatment rescues the sterility of genetically obese Ob/Ob males. Endocrinology. 1997;138(3):1190–3.CrossRefPubMed
6.
go back to reference Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334(5):292–5.CrossRefPubMed Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334(5):292–5.CrossRefPubMed
7.
go back to reference Handjieva-Darlenska T, Boyadjieva N. The effect of high-fat diet on plasma ghrelin and leptin levels in rats. J Physiol Biochem. 2009;65(2):157–64.CrossRefPubMed Handjieva-Darlenska T, Boyadjieva N. The effect of high-fat diet on plasma ghrelin and leptin levels in rats. J Physiol Biochem. 2009;65(2):157–64.CrossRefPubMed
8.
go back to reference Leisegang K, Bouic PJ, Menkveld R, Henkel RR. Obesity is associated with increased seminal insulin and leptin alongside reduced fertility parameters in a controlled male cohort. Reprod Biol Endocrinol. 2014;12:34.CrossRefPubMedPubMedCentral Leisegang K, Bouic PJ, Menkveld R, Henkel RR. Obesity is associated with increased seminal insulin and leptin alongside reduced fertility parameters in a controlled male cohort. Reprod Biol Endocrinol. 2014;12:34.CrossRefPubMedPubMedCentral
9.
go back to reference Einollahi N, Dashti N, Emamgholipour S, Zarebavani M, Sedighi-Gilani MA, Choobineh H. Evidence for alteration in serum concentrations of leptin in infertile men categorized based on BMI. Clin Lab. 2016;59:2361–6. Einollahi N, Dashti N, Emamgholipour S, Zarebavani M, Sedighi-Gilani MA, Choobineh H. Evidence for alteration in serum concentrations of leptin in infertile men categorized based on BMI. Clin Lab. 2016;59:2361–6.
10.
go back to reference Hofny ER, Ali ME, Abdel-Hafez HZ, Eel-D K, Mohamed EE, Abd El-Azeem HG, Mostafa T. Semen parameters and hormonal profile in obese fertile and infertile males. Fertil Steril. 2010;94(2):581–4.CrossRefPubMed Hofny ER, Ali ME, Abdel-Hafez HZ, Eel-D K, Mohamed EE, Abd El-Azeem HG, Mostafa T. Semen parameters and hormonal profile in obese fertile and infertile males. Fertil Steril. 2010;94(2):581–4.CrossRefPubMed
11.
go back to reference Steinman N, Gamzu R, Yogev L, Botchan A, Schreiber L, Yavetz H. Serum leptin concentrations are higher in azoospermic than in normozoospermic men. Fertil Steril. 2001;75(4):821–2.CrossRefPubMed Steinman N, Gamzu R, Yogev L, Botchan A, Schreiber L, Yavetz H. Serum leptin concentrations are higher in azoospermic than in normozoospermic men. Fertil Steril. 2001;75(4):821–2.CrossRefPubMed
12.
go back to reference Yuan M, Huang G, Li J, Zhang J, Li F, Li K, et al. Hyperleptinemia directly affects testicular maturation at different sexual stages in mice, and suppressor of cytokine signaling 3 is involved in this process. Reprod Biol Endocrinol. 2014;12:15.CrossRefPubMedPubMedCentral Yuan M, Huang G, Li J, Zhang J, Li F, Li K, et al. Hyperleptinemia directly affects testicular maturation at different sexual stages in mice, and suppressor of cytokine signaling 3 is involved in this process. Reprod Biol Endocrinol. 2014;12:15.CrossRefPubMedPubMedCentral
13.
go back to reference Giovambattista A, Suescun MO, Nessralla CC, França LR, Spinedi E, Calandra RS. Modulatory effects of leptin on leydig cell function of normal and hyperleptinemia rats. Neuroendocrinology. 2003;78(5):270–9.CrossRefPubMed Giovambattista A, Suescun MO, Nessralla CC, França LR, Spinedi E, Calandra RS. Modulatory effects of leptin on leydig cell function of normal and hyperleptinemia rats. Neuroendocrinology. 2003;78(5):270–9.CrossRefPubMed
14.
go back to reference Haron MN, D'Souza UJ, Jaafar H, Zakaria R, Singh HJ. Exogenous leptin administration decreases sperm count and increases the fraction of abnormal sperm in adult rats. Fertil Steril. 2010;93(1):322–4.CrossRefPubMed Haron MN, D'Souza UJ, Jaafar H, Zakaria R, Singh HJ. Exogenous leptin administration decreases sperm count and increases the fraction of abnormal sperm in adult rats. Fertil Steril. 2010;93(1):322–4.CrossRefPubMed
15.
go back to reference Abbasihormozi S, Shahverdi A, Kouhkan A, Cheraghi J, Akhlaghi AA, Kheimeh A. Relationship of leptin administration with production of reactive oxygen species, sperm DNA fragmentation, sperm parameters and hormone profile in the adult rat. Arch Gynecol Obstet. 2013;287(6):1241–9.CrossRefPubMed Abbasihormozi S, Shahverdi A, Kouhkan A, Cheraghi J, Akhlaghi AA, Kheimeh A. Relationship of leptin administration with production of reactive oxygen species, sperm DNA fragmentation, sperm parameters and hormone profile in the adult rat. Arch Gynecol Obstet. 2013;287(6):1241–9.CrossRefPubMed
16.
go back to reference Almabhouh FA, Osman K, Ibrahim SF, Gupalo S, Gnanou J, Ibrahim E, Singh HJ. Melatonin ameliorates the adverse effects of leptin on sperm. Asian J Androl. 2016;19(6):647–54.PubMedCentral Almabhouh FA, Osman K, Ibrahim SF, Gupalo S, Gnanou J, Ibrahim E, Singh HJ. Melatonin ameliorates the adverse effects of leptin on sperm. Asian J Androl. 2016;19(6):647–54.PubMedCentral
17.
go back to reference Almabhouh FA, Singh HJ. Adverse effects of leptin on histone- to- protamine transition during spermatogenesis are prevented by melatonin in Sprague- Dawley rats. Andrologia. 2018;50(1):e12814.CrossRef Almabhouh FA, Singh HJ. Adverse effects of leptin on histone- to- protamine transition during spermatogenesis are prevented by melatonin in Sprague- Dawley rats. Andrologia. 2018;50(1):e12814.CrossRef
18.
go back to reference Fernandez CD, Fernandes GS, Favareto AP, Perobelli JE, Sanabria M, Kempinas WD. Decreased implantation number after in utero artificial insemination can reflect an impairment of fertility in adult male rats after exogenous leptin exposure. Reprod Sci. 2017;24(2):234–41.CrossRefPubMed Fernandez CD, Fernandes GS, Favareto AP, Perobelli JE, Sanabria M, Kempinas WD. Decreased implantation number after in utero artificial insemination can reflect an impairment of fertility in adult male rats after exogenous leptin exposure. Reprod Sci. 2017;24(2):234–41.CrossRefPubMed
19.
go back to reference Almabhouh FA, Osman K, Siti Fatimah I, Sergey G, Gnanou J, Singh HJ. Effects of leptin on sperm count and morphology in Sprague-Dawley rats and their reversibility following a 6-week recovery period. Andrologia. 2015;47(7):751–8.CrossRefPubMed Almabhouh FA, Osman K, Siti Fatimah I, Sergey G, Gnanou J, Singh HJ. Effects of leptin on sperm count and morphology in Sprague-Dawley rats and their reversibility following a 6-week recovery period. Andrologia. 2015;47(7):751–8.CrossRefPubMed
20.
go back to reference Kim CY, Kim KH. Curcumin prevents leptin-induced tight junction dysfunction in intestinal Caco-2 BBe cells. J Nutr Biochem. 2014;25(1):26–35.CrossRefPubMed Kim CY, Kim KH. Curcumin prevents leptin-induced tight junction dysfunction in intestinal Caco-2 BBe cells. J Nutr Biochem. 2014;25(1):26–35.CrossRefPubMed
21.
go back to reference Le Dréan G, Haure-Mirande V, Ferrier L, Bonnet C, Hulin P, de Coppet P, Segain JP. Visceral adipose tissue and leptin increase colonic epithelial tight junction permeability via a RhoA-ROCK-dependent pathway. FASEB J. 2014;28(3):1059–70.CrossRefPubMed Le Dréan G, Haure-Mirande V, Ferrier L, Bonnet C, Hulin P, de Coppet P, Segain JP. Visceral adipose tissue and leptin increase colonic epithelial tight junction permeability via a RhoA-ROCK-dependent pathway. FASEB J. 2014;28(3):1059–70.CrossRefPubMed
24.
go back to reference Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev. 2004;25(5):747–806.CrossRefPubMed Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev. 2004;25(5):747–806.CrossRefPubMed
25.
go back to reference Morrow CM, Mruk D, Cheng CY, Hess RA. Claudin and occludin expression and function in the seminiferous epithelium. Philos Trans R Soc Lond Ser B Biol Sci. 2010;365(1546):1679–96.CrossRef Morrow CM, Mruk D, Cheng CY, Hess RA. Claudin and occludin expression and function in the seminiferous epithelium. Philos Trans R Soc Lond Ser B Biol Sci. 2010;365(1546):1679–96.CrossRef
26.
go back to reference Cao XN, Shen LJ, Wu SD, Yan C, Zhou Y, Xiong G, et al. Urban fine particulate matter exposure causes male reproductive injury through destroying blood-testis barrier (BTB) integrity. Toxicol Lett. 2017;266:1–12.CrossRefPubMed Cao XN, Shen LJ, Wu SD, Yan C, Zhou Y, Xiong G, et al. Urban fine particulate matter exposure causes male reproductive injury through destroying blood-testis barrier (BTB) integrity. Toxicol Lett. 2017;266:1–12.CrossRefPubMed
27.
go back to reference Zhang J, Li Z, Qie M, Zheng R, Shetty J, Wang J. Sodium fluoride and sulfur dioxide affected male reproduction by disturbing blood-testis barrier in mice. Food Chem Toxicol. 2016;94:103–11.CrossRefPubMed Zhang J, Li Z, Qie M, Zheng R, Shetty J, Wang J. Sodium fluoride and sulfur dioxide affected male reproduction by disturbing blood-testis barrier in mice. Food Chem Toxicol. 2016;94:103–11.CrossRefPubMed
28.
go back to reference Qiu L, Zhang X, Zhang X, Zhang Y, Gu J, Chen M, et al. Sertoli cell is a potential target for perfluorooctane sulfonate-induced reproductive dysfunction in male mice. Toxicol Sci. 2013;135(1):229–40.CrossRefPubMed Qiu L, Zhang X, Zhang X, Zhang Y, Gu J, Chen M, et al. Sertoli cell is a potential target for perfluorooctane sulfonate-induced reproductive dysfunction in male mice. Toxicol Sci. 2013;135(1):229–40.CrossRefPubMed
29.
go back to reference Ahn JH, Choi YS, Choi JH. Leptin promotes human endometriotic cell migration and invasion by up-regulating MMP-2 through the JAK2/STAT3 signaling pathway. Mol Hum Reprod. 2015;21(10):792–802.CrossRefPubMed Ahn JH, Choi YS, Choi JH. Leptin promotes human endometriotic cell migration and invasion by up-regulating MMP-2 through the JAK2/STAT3 signaling pathway. Mol Hum Reprod. 2015;21(10):792–802.CrossRefPubMed
30.
go back to reference Rossi SP, Windschüttl S, Matzkin ME, Rey-Ares V, Terradas C, Ponzio R, et al. Reactive oxygen species (ROS) production triggered by prostaglandin D2 (PGD2) regulates lactate dehydrogenase (LDH) expression/activity in TM4 Sertoli cells. Mol Cell Endocrinol. 2016;434:154–65.CrossRefPubMed Rossi SP, Windschüttl S, Matzkin ME, Rey-Ares V, Terradas C, Ponzio R, et al. Reactive oxygen species (ROS) production triggered by prostaglandin D2 (PGD2) regulates lactate dehydrogenase (LDH) expression/activity in TM4 Sertoli cells. Mol Cell Endocrinol. 2016;434:154–65.CrossRefPubMed
31.
go back to reference Choi MS, Park HJ, Oh JH, Lee EH, Park SM, Yoon S. Nonylphenol-induced apoptotic cell death in mouse TM4 Sertoli cells via the generation of reactive oxygen species and activation of the ERK signaling pathway. J Appl Toxicol. 2014;34(6):628–36.CrossRefPubMed Choi MS, Park HJ, Oh JH, Lee EH, Park SM, Yoon S. Nonylphenol-induced apoptotic cell death in mouse TM4 Sertoli cells via the generation of reactive oxygen species and activation of the ERK signaling pathway. J Appl Toxicol. 2014;34(6):628–36.CrossRefPubMed
32.
go back to reference World Health Organization, editor. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World Health Organization; 2010. World Health Organization, editor. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World Health Organization; 2010.
33.
go back to reference Ward MA. Intracytoplasmic sperm injection effects in infertile azh mutant mice. Biol Reprod. 2005;73(1):193–200.CrossRefPubMed Ward MA. Intracytoplasmic sperm injection effects in infertile azh mutant mice. Biol Reprod. 2005;73(1):193–200.CrossRefPubMed
34.
go back to reference Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE. Androgens regulate the permeability of the blood–testis barrier. Proc Natl Acad Sci. 2005;102(46):16696–700.CrossRefPubMedPubMedCentral Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE. Androgens regulate the permeability of the blood–testis barrier. Proc Natl Acad Sci. 2005;102(46):16696–700.CrossRefPubMedPubMedCentral
35.
go back to reference El-Hefnawy T, Ioffe S, Dym M. Expression of the leptin receptor during germ cell development in the mouse testis. Endocrinology. 2000;141(7):2624–30.CrossRefPubMed El-Hefnawy T, Ioffe S, Dym M. Expression of the leptin receptor during germ cell development in the mouse testis. Endocrinology. 2000;141(7):2624–30.CrossRefPubMed
36.
go back to reference Woods DC, White YA, Niikura Y, Kiatpongsan S, Lee HJ, Tilly JL. Embryonic stem cell–derived granulosa cells participate in ovarian follicle formation in vitro and in vivo. Reprod Sci. 2013;20(5):524–35.CrossRefPubMedPubMedCentral Woods DC, White YA, Niikura Y, Kiatpongsan S, Lee HJ, Tilly JL. Embryonic stem cell–derived granulosa cells participate in ovarian follicle formation in vitro and in vivo. Reprod Sci. 2013;20(5):524–35.CrossRefPubMedPubMedCentral
37.
go back to reference Hoffmann A, Manjowk GM, Wagner IV, Klöting N, Ebert T, Jessnitzer B, et al. Leptin within the subphysiological to physiological range dose-dependently improves male reproductive function in an obesity mouse model. Endocrinology. 2016;157(6):2461–8.CrossRefPubMed Hoffmann A, Manjowk GM, Wagner IV, Klöting N, Ebert T, Jessnitzer B, et al. Leptin within the subphysiological to physiological range dose-dependently improves male reproductive function in an obesity mouse model. Endocrinology. 2016;157(6):2461–8.CrossRefPubMed
38.
go back to reference Fan Y, Liu Y, Xue K, Gu G, Fan W, Xu Y, Ding Z. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PLoS One. 2015;10(4):e0120775.CrossRefPubMedPubMedCentral Fan Y, Liu Y, Xue K, Gu G, Fan W, Xu Y, Ding Z. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PLoS One. 2015;10(4):e0120775.CrossRefPubMedPubMedCentral
39.
go back to reference Tena-Sempere M, Manna PR, Zhang FP, Pinilla L, González LC, Diéguez C, Huhtaniemi I, Aguilar E. Molecular mechanisms of leptin action in adult rat testis: potential targets for leptin-induced inhibition of steroidogenesis and pattern of leptin receptor messenger ribonucleic acid expression. J Endocrinol. 2001;170(2):413–23.CrossRefPubMed Tena-Sempere M, Manna PR, Zhang FP, Pinilla L, González LC, Diéguez C, Huhtaniemi I, Aguilar E. Molecular mechanisms of leptin action in adult rat testis: potential targets for leptin-induced inhibition of steroidogenesis and pattern of leptin receptor messenger ribonucleic acid expression. J Endocrinol. 2001;170(2):413–23.CrossRefPubMed
40.
go back to reference Martins AD, Moreira AC, Sá R, Monteiro MP, Sousa M, Carvalho RA, et al. Leptin modulates human Sertoli cell acetate production and glycolytic profile: a novel mechanism of obesity-induced male infertility? Biochim Biophys Acta. 2015;1852(9):1824–32.CrossRefPubMed Martins AD, Moreira AC, Sá R, Monteiro MP, Sousa M, Carvalho RA, et al. Leptin modulates human Sertoli cell acetate production and glycolytic profile: a novel mechanism of obesity-induced male infertility? Biochim Biophys Acta. 2015;1852(9):1824–32.CrossRefPubMed
41.
go back to reference Peelman F, Zabeau L, Moharana K, Savvides SN, Tavernier J. 20 years of leptin: insights into signaling assemblies of the leptin receptor. J Endocrinol. 2014;223(1):T9–23.CrossRefPubMed Peelman F, Zabeau L, Moharana K, Savvides SN, Tavernier J. 20 years of leptin: insights into signaling assemblies of the leptin receptor. J Endocrinol. 2014;223(1):T9–23.CrossRefPubMed
42.
go back to reference Wu D, Huang CJ, Khan FA, Jiao XF, Liu XM, Pandupuspitasari NS, Brohi RD, Huo LJ. SENP3 grants tight junction integrity and cytoskeleton architecture in mouse Sertoli cells. Oncotarget. 2017;8(35):58430–42.PubMedPubMedCentral Wu D, Huang CJ, Khan FA, Jiao XF, Liu XM, Pandupuspitasari NS, Brohi RD, Huo LJ. SENP3 grants tight junction integrity and cytoskeleton architecture in mouse Sertoli cells. Oncotarget. 2017;8(35):58430–42.PubMedPubMedCentral
43.
go back to reference Donahoo WT, Stob NR, Ammon S, Levin N, Eckel RH. Leptin increases skeletal muscle lipoprotein lipase and postprandial lipid metabolism in mice. Metabolism. 2011;60(3):438–43.CrossRefPubMed Donahoo WT, Stob NR, Ammon S, Levin N, Eckel RH. Leptin increases skeletal muscle lipoprotein lipase and postprandial lipid metabolism in mice. Metabolism. 2011;60(3):438–43.CrossRefPubMed
44.
go back to reference Burnett LC, Skowronski AA, Rausch R, LeDuc CA, Leibel RL. Determination of the half-life of circulating leptin in the mouse. Int J Obes. 2017;41(3):355–9.CrossRef Burnett LC, Skowronski AA, Rausch R, LeDuc CA, Leibel RL. Determination of the half-life of circulating leptin in the mouse. Int J Obes. 2017;41(3):355–9.CrossRef
45.
go back to reference Luukkaa V, Pesonen U, Huhtaniemi I, Lehtonen A, Tilvis R, Tuomilehto J, Koulu M, Huupponen R. Inverse correlation between serum testosterone and leptin in men. J Clin Endocrinol Metab. 1998;83(9):3243–6.PubMed Luukkaa V, Pesonen U, Huhtaniemi I, Lehtonen A, Tilvis R, Tuomilehto J, Koulu M, Huupponen R. Inverse correlation between serum testosterone and leptin in men. J Clin Endocrinol Metab. 1998;83(9):3243–6.PubMed
46.
go back to reference Söderberg S, Olsson T, Eliasson M, Johnson O, Brismar K, Carlström K, Ahrén B. A strong association between biologically active testosterone and leptin in non-obese men and women is lost with increasing (central) adiposity. Int J Obes Relat Metab Disord. 2001;25(1):98–105.CrossRefPubMed Söderberg S, Olsson T, Eliasson M, Johnson O, Brismar K, Carlström K, Ahrén B. A strong association between biologically active testosterone and leptin in non-obese men and women is lost with increasing (central) adiposity. Int J Obes Relat Metab Disord. 2001;25(1):98–105.CrossRefPubMed
47.
go back to reference Vigueras-Villaseñor RM, Rojas-Castañeda JC, Chávez-Saldaña M, Gutiérrez-Pérez O, García-Cruz ME, Cuevas-Alpuche O, et al. Alterations in the spermatic function generated by obesity in rats. Acta Histochem. 2011;113(2):214–20.CrossRefPubMed Vigueras-Villaseñor RM, Rojas-Castañeda JC, Chávez-Saldaña M, Gutiérrez-Pérez O, García-Cruz ME, Cuevas-Alpuche O, et al. Alterations in the spermatic function generated by obesity in rats. Acta Histochem. 2011;113(2):214–20.CrossRefPubMed
48.
go back to reference Landry DA, Sormany F, Haché J, Roumaud P, Martin LJ. Steroidogenic genes expressions are repressed by high levels of leptin and the JAK/STAT signaling pathway in MA-10 Leydig cells. Mol Cell Biochem. 2017;433(1–2):79–95.CrossRefPubMed Landry DA, Sormany F, Haché J, Roumaud P, Martin LJ. Steroidogenic genes expressions are repressed by high levels of leptin and the JAK/STAT signaling pathway in MA-10 Leydig cells. Mol Cell Biochem. 2017;433(1–2):79–95.CrossRefPubMed
Metadata
Title
Exogenous leptin affects sperm parameters and impairs blood testis barrier integrity in adult male mice
Authors
Xiaotong Wang
Xiaoke Zhang
Lian Hu
Honggang Li
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/s12958-018-0368-4

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