Role of zinc trafficking in male fertility: From germ to sperm

Human Reproduction

Volumn 29, Issue 6, 2014, Pages 1134-1145

  Foresta, Carlo ^a   Garolla, Andrea ^a   Cosci, Ilaria ^a   Menegazzo, Massimo ^a   Ferigo, Marco ^a   Gandin, Valentina ^a   De Toni, Luca ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

Capacitation; Male infertility; Sperm motility; Zinc; Zinc transporters

Indexed keywords

CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ZINC; ZINC TRANSPORTER; CARRIER PROTEIN; ZINC-BINDING PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ZIP1 PROTEIN; ZIP5 PROTEIN; ZIP6 PROTEIN; ZIP8 PROTEIN;

ACROSOME REACTION; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; AUTOMETALLOGRAPHY; AZOOSPERMIA; CLINICAL ARTICLE; CONTROLLED STUDY; EJACULATION; EPIDIDYMIS; EPIDIDYMIS BIOPSY; FINE NEEDLE ASPIRATION BIOPSY; FLOW CYTOMETRY; GENE MUTATION; GERM CELL; GERM CELL TUMOR; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; INFERTILITY THERAPY; MALE; MALE FERTILITY; MALE INFERTILITY; PREGNANCY OUTCOME; PROSTATE SECRETION; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERM; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; TESTIS; ADOLESCENT; ADULT; METABOLISM; SPERM RETRIEVAL; YOUNG ADULT; BASEMENT MEMBRANE; CELL MEMBRANE; CELL VIABILITY; ION TRANSPORT; LIMIT OF DETECTION; TESTIS BIOPSY;

ADOLESCENT; ADULT; CARRIER PROTEINS; HUMANS; INFERTILITY, MALE; MALE; SPERM RETRIEVAL; SPERMATOZOA; YOUNG ADULT; ZINC;

EID: 84900825559     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu075     Document Type: Article

References (40)

1. Adinolfi A, Moratti R, Olezza S, Ruffo A. Control of the citric acid cycle by glyoxylate. The mechanism of inhibition of oxoglutarate dehydrogenase, isocitrate dehydrogenase and aconitate hydratase. Biochem J 1969; 114:513-518.
2. Aoki VW, Emery BR, Liu L, Carrell DT. Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J Androl 2006;27:890-898.
3. Behne D, Gessner H, Wolters G, Brotherton J. Selenium, rubidium and zinc in human semen and semen fractions. Int J Androl 1988;11:415-423.
4. Bettella A, Ferlin A, Menegazzo M, Ferigo M, Tavolini IM, Bassi PF, Foresta C. Testicular fine needle aspiration as a diagnostic tool in non-obstructive azoospermia. Asian J Androl 2005;7:289-294.
5. Carlson AE, Westenbroek RE, Quill T, Ren D, Clapham DE, Hille B, Garbers DL, Babcock DF. CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci USA 2003; 100:14864-14868.
6. Colagar AH, Marzony ET, Chaichi MJ. Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 2009; 29:82-88.
7. Costello LC, Liu Y, Franklin RB, Kennedy MC. Zinc inhibition of mitochondrial aconitase and its importance in citrate metabolism of prostate epithelial cells. J Biol Chem 1997;272:28875-28881.
8. Dickens CJ, Maguiness SD, Comer MT, Palmer A, Rutherford AJ, Leese HJ. Human tubal fluid: Formation and composition during vascular perfusion of the fallopian tube. Hum Reprod 1995;10:505-508.
9. Eide DJ. Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 2006;1763:711-722.
10. Foresta C, De Carlo E, Zorzi M, Rossato M, Finelli L. Possible significance of seminal zinc on human spermatozoa functions. Acta Eur Fertil 1990; 21:305-308.
11. Franca LR, Avelar GF, Almeida FF. Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 2005;63:300-318.
12. Garcia-Macias V, Martinez-Pastor F, Alvarez M, Garde JJ, Anel E, Anel L, De Paz P. Assessment of chromatin status (SCSA) in epididymal and ejaculated sperm in Iberian red deer, ram and domestic dog. Theriogenology 2006;66:1921-1930.
13. Garolla A, Lenzi A, Palu G, Pizzol D, Bertoldo A, De Toni L, Foresta C. Human papillomavirus sperm infection and assisted reproduction: A dangerous hazard with a possible safe solution. Hum Reprod 2012; 27:967-973.
14. Golan R, Cooper TG, Oschry Y, Oberpenning F, Schulze H, Shochat L, Lewin LM. Changes in chromatin condensation of human spermatozoa during epididymal transit as determined by flow cytometry. Hum Reprod 1996;11:1457-1462.
15. Grunewald S, Baumann T, Paasch U, Glander HJ. Capacitation and acrosome reaction in nonapoptotic human spermatozoa. Ann N Y Acad Sci 2006; 1090:138-146.
16. Hagenfeldt K, Plantin LO, Diczfalusy E. Trace elements in the human endometrium. 2. Zinc, copper and manganese levels in the endometrium, cervical mucus and plasma. Acta Endocrinol (Copenh) 1973;72:115-126.
17. Henkel R, Bittner J, Weber R, Hüther F, Miska W. Relevance of zinc in human sperm flagella and its relation to motility. Fertil Steril 1999; 71:1138-1143.
18. Henkel R, Maass G, Schuppe HC, Jung A, Schubert J, Schill WB. Molecular aspects of declining sperm motility in older men. Fertil Steril 2005; 84:1430-1437.
19. Jaiswal BS, Cohen-Dayag A, Tur-Kaspa I, Eisenbach M. Sperm capacitation is, after all, a prerequisite for both partial and complete acrosome reaction. FEBS Lett 1998;8:309-313.
20. Kirichok Y, Navarro B, Clapham DE. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-Activated Ca2+ channel. Nature 2006; 439:737-740.
21. Kvist U, Björndahl L, Roomans GM, Lindholmer C. Nuclear zinc in human epididymal and ejaculated spermatozoa. Acta Physiol Scand 1985; 125:297-303.
22. Kvist U, Björndahl L, Kjellberg S. Sperm nuclear zinc, chromatin stability, and male fertility. Scanning Microsc 1987;1:1241-1247.
23. Kvist U, Kjellberg S, Björndahl L, Hammar M, Roomans GM. Zinc in sperm chromatin and chromatin stability in fertile men and men in barren unions. Scand J Urol Nephrol 1988;22:1-6.
24. Lachance C, Goupil S, Leclerc P. Stattic V, a STAT3 inhibitor, affects human spermatozoa through regulation of mitochondrial activity. Cell Physiol 2013; 228:704-713.
25. Lishko PV, Botchkina IL, Fedorenko A, Kirichok Y. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell 2010;140:327-337.
26. Oldereid NB, Thomassen Y, Attramadal A, Olaisen B, Purvis K. Concentrations of lead, cadmium and zinc in the tissues of reproductive organs of men. J Reprod Fertil 1993;99:421-425.
27. Prieto MC, Maki AH, Balhorn R. Analysis of DNA-protamine interactions by optical detection of magnetic resonance. Biochemistry 1997; 36:11944-11951.
28. Riffo M, Leiva S, Astudillo J. Effect of zinc on human sperm motility and the acrosome reaction. Int J Androl 1992;15:229-237.
29. Sandström B, Cederblad A. Zinc absorption from composite meals. II. Influence of the main protein source. Am J Clin Nutr 1980;33:1778-1783.
30. Schneider M, Förster H, Boersma A, Seiler A, Wehnes H, Sinowatz F, Neumüller C, Deutsch MJ, Walch A, Hrabé de Angelis M et al. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J 2009;23:3233-3242.
31. Siciliano L, De Stefano C, Petroni MF, Vivacqua A, Rago V, Carpino A. Prostatic origin of a zinc binding high molecular weight protein complex in human seminal plasma. Mol Hum Reprod 2000;6:215-218.
32. Smith AF, Longpre J, Loo G. Inhibition by zinc of deoxycholate-induced apoptosis in HCT-116 cells. J Cell Biochem 2012;113:650-657.
33. Stoltenberg M, Sorensen MB, Danscher G, Juhl S, Andreasen A, Ernst E. Autometallographic demonstration of zinc ions in rat sperm cells. Mol Hum Reprod 1997;3:763-776.
34. Tesarik J, Kopecny V. Development of human male pronucleus: Ultrastructure and timing. Gamete Res 1989;24:135-149.
35. Vera-Gil A, Pérez Castejón MC, Barral MJ, Recreo P, Pérez Castejón MJ. Location of Zn in the testicle of the rat. Acta Anat (Basel) 1991;141:70-73.
36. World Health Organization.WHOLaboratory Manual for the Examination and Processing of Human Semen. 5th edn. Geneva:World Health Organization, 2010.
37. Yamaguchi S, Miura C, Kikuchi K, Celino FT, Agusa T, Tanabe S, MiuraT. Zinc is an essential trace element for spermatogenesis. Proc Natl Acad Sci USA 2009;106:10859-10864.
38. Yang J, Zhang Y, Cui X, Yao W, Yu X, Cen P, Hodges SE, Fisher WE, Brunicardi FC, Chen C et al. Gene profile identifies zinc transporters differentially expressed in normal human organs and human pancreatic cancer. Curr Mol Med 2013;13:401-409.
39. Yu J, Chen Z, Ni Y, Li Z. CFTR mutations in men with congenital bilateral absence of the vas deferens (CBAVD): A systemic review and meta-Analysis. Hum Reprod 2012;27:25-35.
40. Zuccarello D, Ferlin A, Garolla A, Menegazzo M, Perilli L, Ambrosini G, Foresta C. How the human spermatozoa sense the oocyte: A new role of SDF1-CXCR4 signalling. Int J Androl 2011;34:554-565.