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Published in:

01-03-2007

Effects of Tumour Necrosis Factor-α on Human Sperm Motility and Apoptosis

Authors: Anna Perdichizzi, Ferdinando Nicoletti, Sandro La Vignera, Nunziata Barone, Rosario D’Agata, Enzo Vicari, Aldo E. E. Calogero

Published in: Journal of Clinical Immunology | Issue 2/2007

Abstract

The aim of this study was to evaluate the effects of tumour necrosis factor-α (TNF-α) on sperm motility, mitochondrial membrane potential (ΔΨ), phosphatidylserine (PS) externalization, sperm chromatin packaging quality, and DNA fragmentation. Motile spermatozoa, obtained from 10 normozoospermic men, were incubated with increasing concentrations of TNF-α and analyzed 1, 3, 6, and 24 h after incubation by flow cytometry. TNF-α decreased total motility 24 h after incubation at 10 ng/mL and progressive motility 3 h after incubation. Accordingly, TNF-α reduced sperm ΔΨ in a concentration- and time-dependent manner. TNF-α increased the percentage of spermatozoa with PS externalization from the concentration of 1 ng/mL 1 h after incubation. TNF-α produced sperm chromatin and DNA damage in a concentration- and time-dependent manner. In conclusion, these findings may explain the reduction of fertility, secondary to upregulated production of TNF-α, in men with urogenital infections.

Bingham CO III: The pathogenesis of rheumatoid arthritis: Pivotal cytokines involved in bone degradation and inflammation. J Rheumatol 65(Suppl):3–9, 2002

Lowes MA, Lew W, Krueger JG: Current concepts in the immunopathogenesis of psoriasis. Dermatol Clin 22:349–369, 2004PubMedCrossRef

Rabinovitch A, Suarez-Pinzon WL: Role of cytokines in the pathogenesis of autoimmune diabetes mellitus. Rev Endocrinol Metab Disord 4:291–299, 2003CrossRef

Romagnani S: Th1 and Th2 in human diseases. Clin Immunol Immunopathol 80(3 Pt 1):225–235, 1996PubMedCrossRef

Anderson DJ, Hill JA: Cell-mediated immunity in infertility. Am J Reprod Immunol Microbiol 17:22–30, 1988PubMed

Cohen J, Edwards R, Fehilly C, Fishel S, Hewitt J, Purdy J, Rowland G, Steptoe P, Webster J: In vitro fertilization: A treatment for male infertility. Fertil Steril 43:422–432, 1985PubMed

Talbert LM, Hammond MG, Halme J, O’Rand M, Fryer JG, Ekstrom RD: Semen parameters and fertilization of human oocytes in vitro: A multivariable analysis. Fertil Steril 48:270–277, 1987PubMed

Wolf JP, Bulwa S, Ducot B, Rodrigues D, Jouannet P: Fertilizing ability of sperm with unexplained in vitro fertilization failures, as assessed by the zona-free hamster egg penetration assay: Its prognostic value for sperm-oolemma interaction. Fertil Steril 65:1196–1201, 1996PubMed

Krause W, Bohring C, Gueth A, Horster S, Krisp A, Skrzypek J: Cellular and biochemical markers in semen indicating male accessory gland inflammation. Andrologia 35:279–282, 2003PubMedCrossRef

10.

Billig H, Furuta I, Rivier C, Tapanainen J, Parvinen M, Hsueh AJ: Apoptosis in testis germ cells: Developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136:5–12, 1995PubMedCrossRef

11.

Aitken RJ, Buckingham D: Enhanced detection of reactive oxygen species produced by human spermatozoa with 7-dimethyl amino-naphthalin-1, 2-dicarbonic acid hydrazide. Int J Androl 15:211–219, 1992PubMed

12.

Barroso G, Morshedi M, Oehninger S: Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Hum Reprod 15:1338–1344, 2000PubMedCrossRef

13.

Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, Evenson D, Thomas AJ Jr, Alvarez JG: Characterization of subsets of human spermatozoa at different stages of maturation: Implications in the diagnosis and treatment of male infertility. Hum Reprod 16:1912–1921, 2001PubMedCrossRef

14.

Aitken RJ, Clarkson JS, Fishel S: Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 41:183–197, 1989PubMedCrossRef

15.

Sun JG, Jurisicova A, Casper RF: Detection of deoxyribonucleic acid fragmentation in human sperm: Correlation with fertilization in vitro. Biol Reprod 56:602–607, 1997PubMedCrossRef

16.

Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS: Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 59:1037–1046, 1998PubMedCrossRef

17.

Lopes S, Jurisicova A, Casper RI: Gamete-specific DNA fragmentation in unfertilized human oocytes after intracytoplasmic sperm injection. Hum Reprod 13:703–708, 1998PubMedCrossRef

18.

Twigg J, Fulton N, Gomez E, Irvine DS, Aitken RJ: Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: Lipid peroxidation, DNA fragmentation and effectiveness of antioxidants. Hum Reprod 13:1429–1436, 1998PubMedCrossRef

19.

Gruschwitz MS, Brezinschek R, Brezinschek HP: Cytokine levels in the seminal plasma of infertile males. J Androl 17:158–163, 1996PubMed

20.

Besset V, Le Magueresse-Battistoni B, Collette J, Benahmed M: Tumor necrosis factor alpha stimulates insulin-like growth factor binding protein 3 expression in cultured porcine Sertoli cells. Endocrinology 137:296–303, 1996PubMedCrossRef

21.

Grataroli R, Boussouar F, Benahmed M: Role of sphingosine in the tumor necrosis factor alpha stimulatory effect on lactate dehydrogenase A expression and activity in porcine Sertoli cells. Biol Reprod 63:1473–1481, 2000PubMedCrossRef

22.

Said TM, Agarwal A, Falcone T, Sharma RK, Bedaiwy MA, Li L: Infliximab may reverse the toxic effects induced by tumor necrosis factor alpha in human spermatozoa: An in vitro model. Fertil Steril 83:1665–1673, 2005PubMedCrossRef

23.

Erenpreiss J, Spano M, Erenpreisa J, Bungum M, Giwercman A: Sperm chromatin structure and male fertility: Biological and clinical aspects. Asian J Androl 8:11–29, 2006PubMedCrossRef

24.

World Health Organization: WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th edn. Cambridge, UK, Cambridge University Press, 1999

25.

Calogero AE, Burrello N, Ferrara E, Hall J, Fishel S, D’Agata R: Gamma-aminobutyric acid (GABA) A and B receptors mediate the stimulatory effects of GABA on the human sperm acrosome reaction: Interaction with progesterone. Fertil Steril 71:930–936, 1999PubMedCrossRef

26.

Vicari E, Perdichizzi A, De Palma A, Burrello N, D’Agata R, Calogero AE: Globozoospermia is associated with chromatin structure abnormalities: Case report. Hum Reprod 17:2128–2133, 2002PubMedCrossRef

27.

Hussenet F, Dousset B, Cordonnier JL, Jacob C, Foliguet B, Grignon G, Nabet P: Tumour necrosis factor alpha and interleukin 2 in normal and infected human seminal fluid. Hum Reprod 8:409–411, 1993PubMed

28.

Omu AE, Al-Qattan F, Al-Abdul-Hadi FM, Fatinikun MT, Fernandes S: Seminal immune response in infertile men with leukocytospermia: Effect on antioxidant activity. Eur J Obstet Gynecol Reprod Biol 86:195–202, 1999PubMedCrossRef

29.

Sikorski R, Kapec E, Krzeminski A, Zaleska W: Levels of proinflammatory cytokines (IL-1 alpha, IL-6, TNF-alpha) in the semen plasma of male partners of infertile couples. Ginekol Pol 72:1325–1328, 2001PubMed

30.

Wincek TJ, Meyer TK, Meyer MR, Kuehl TJ: Absence of a direct effect of recombinant tumor necrosis factor-alpha on human sperm function and murine preimplantation development. Fertil Steril 56:332–339, 1991PubMed

31.

Haney AF, Hughes SF, Weinberg JB: The lack of effect of tumor necrosis factor-alpha, interleukin-1-alpha, and interferon-gamma on human sperm motility in vitro. J Androl 13:249–253, 1992PubMed

32.

Fedder J, Ellerman-Eriksen S: Effect of cytokines on sperm motility and ionophore-stimulated acrosome reaction. Arch Androl 35:173–185, 1995PubMed

33.

Lewis SE, Donnelly ET, Sterling ES, Kennedy MS, Thompson W, Chakravarthy U: Nitric oxide synthase and nitrite production in human spermatozoa: Evidence that endogenous nitric oxide is beneficial to sperm motility. Mol Hum Reprod 2:873–878, 1996PubMedCrossRef

34.

Kocak I, Yenisey C, Dundar M, Okyay P, Serter M: Relationship between seminal plasma interleukin-6 and tumor necrosis factor alpha levels with semen parameters in fertile and infertile men. Urol Res 30:263–267, 2002PubMedCrossRef

35.

Estrada LS, Champion HC, Wang R, Rajasekaran M, Hellstrom WJ, Aggarwal B, Sikka SC: Effect of tumour necrosis factor-alpha (TNF-alpha) and interferon-gamma (IFN-gamma) on human sperm motility, viability and motion parameters. Int J Androl 20:237–242, 1997PubMedCrossRef

36.

Eisermann J, Register KB, Strickler RC, Collins JL: The effect of tumor necrosis factor on human sperm motility in vitro. J Androl 10:270–274, 1989PubMed

37.

Bian J, Guo X, Xiong C, Li J, Tian Y, Ma H, Zhang Y, Nie Y, Yu L, Xiao L: Experimental study of the effect of rhTNF-alpha on human sperm mitochondrial function and motility in vitro. Zhonghua Nan Ke Xue 10:415–419, 2004PubMed

38.

Matsuda Y, Tobari I: Chromosomal analysis in mouse eggs fertilized in vitro with sperm exposed to ultraviolet light (UV) and methyl and ethyl methanesulfonate (MMS and EMS). Mutat Res 198:131–144, 1988PubMed

39.

Genesca A, Caballin MR, Miro R, Benet J, Germa JR, Egozcue J: Repair of human sperm chromosome aberrations in the hamster egg. Hum Genet 89:181–186, 1992PubMedCrossRef

40.

Ahmadi A, Ng SC: Developmental capacity of damaged spermatozoa. Hum Reprod 14:2279–2285, 1999PubMedCrossRef

41.

Aitken RJ, Buckingham D: Oxidative stress, DNA damage and the Y chromosome. Reproduction 122:497–506, 2001PubMedCrossRef

42.

Sakkas D, Manicardi G, Bianchi PG, Bizzaro D, Bianchi U: Relationship between the presence of endogenous nicks and sperm chromatin packaging in maturing and fertilizing mouse spermatozoa. Biol Reprod 52:1149–1155, 1995PubMedCrossRef

43.

Gorczyca W: Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: Analogy to apoptosis of somatic cells. Exp Cell Res 207:202–205, 1993PubMedCrossRef

44.

Sakkas D, Mariethoz E, St John JC: Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fas-mediated pathway. Exp Cell Res 251:350–355, 1999PubMedCrossRef

45.

Gandini L, Lombardo F, Paoli D, Caponecchia L, Familiari G, Verlengia C, Dondero F, Lenzi A: Study of apoptotic DNA fragmentation in human spermatozoa. Hum Reprod 15:830–839, 2000PubMedCrossRef

46.

Blanco-Rodriguez J, Martinez-Garcia C: Apoptosis is physiologically restricted to a specialized cytoplasmic compartment in rat spermatids. Biol Reprod 61:1541–1547, 1999PubMedCrossRef

47.

Weng SL, Taylor SL, Morshedi M, Schuffner A, Duran EH, Beebe S, Oehninger S: Caspase activity and apoptotic markers in ejaculated human sperm. Mol Hum Reprod 8:984–991, 2002PubMedCrossRef

48.

Paasch U, Grunewald S, Fitzl G, Glander HJ: Deterioration of plasma membrane is associated with activated caspases in human spermatozoa. J Androl 24:246–252, 2003PubMed

49.

Yule TD, Tung KS: Experimental autoimmune orchitis induced by testis and sperm antigen-specific T cell clones: An important pathogenic cytokine is tumor necrosis factor. Endocrinology 133:1098–1107, 1993PubMedCrossRef

50.

Weinberg JM, Bottino CJ, Lindholm J, Buchholz R: Biologic therapy for psoriasis: An update on the tumor necrosis factor inhibitors infliximab, etanercept, and adalimumab, and the T-cell-targeted therapies efalizumab and alefacept. J Drugs Dermatol 4:544–555, 2005PubMed

51.

Puppo F, Murdaca G, Ghio M, Indiveri F: Emerging biologic drugs for the treatment of rheumatoid arthritis. Autoimmun Rev 4:537–541, 2005PubMedCrossRef

52.

Chang JT, Lichtenstein GR. Drug Insight: Antagonists of tumor-necrosis factor-alpha in the treatment of inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol 3:220–228, 2006PubMedCrossRef

Title: Effects of Tumour Necrosis Factor-α on Human Sperm Motility and Apoptosis
Authors: Anna Perdichizzi
Ferdinando Nicoletti
Sandro La Vignera
Nunziata Barone
Rosario D’Agata
Enzo Vicari
Aldo E. E. Calogero
Publication date: 01-03-2007
Publisher: Springer US
Published in: Journal of Clinical Immunology / Issue 2/2007
Print ISSN: 0271-9142
Electronic ISSN: 1573-2592
DOI: https://doi.org/10.1007/s10875-007-9071-5

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