Role of copper in the process of spermatogenesis
Mateusz Ogórek 1 , Łukasz Gąsior 1 , Olga Pierzchała 1 , Regina Daszkiewicz 1 , Małgorzata Lenartowicz 1Abstract
Copper (Cu) is an essential trace element required for the normal development of living organisms. Due to its redox potential, copper is a cofactor in many enzymes responsible for important processes in cells. Copper deficiency has a significant influence on the reduction or the total eradication of copper-dependent enzymes in the body, thereby inhibiting cell life processes. On the other hand, copper is a very reactive element and in its free state, it can trigger the production of large amounts of free radicals, which will consequently lead to the damage of proteins and DNA. Because of those reasons, living organisms have developed precise mechanisms regulating the concentration of copper in cells. Copper also plays a very important role in male fertility. It is an essential element for the production of male gametes. The significant role of copper is also described in the processes of cell division – mitotic and meiotic. Copper-dependent enzymes such as ceruloplasmin, superoxide dismutase SOD1 and SOD3, group of metallothionein and cytochrome c oxidase are present at all stages of gametogenesis as well as in the somatic cells of the testis and in the somatic cells of epididymis. Substantial amounts of copper can also be found in liquids associated with sperm in the epididymis and prostate. Copper also affects the integral androgen distribution in terms of fertility on the line hypothalamic-pituitary-testis. Both copper increase and deficiency leads to a significant reduction in male fertility, which spans the entire spectrum of abnormalities at the sperm level, male gonad, production of hormones and distribution of micronutrients such as zinc and iron. Nowadays, the effects of copper on gametes production have become more important and are connected with the increasing levels of pollution with heavy metals in environment.
References
- 1. Agrawal R., Bedwal R.S.: Effect of dietary zinc deficiency on metallothionein concentration of epididymal luminal fluids of weanling Wistar albino rats. Indian J. Exp. Biol., 2003; 41: 118-122
Google Scholar - 2. Aitken R.J., Curry B.J.: Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid. Redox Signal., 2011; 14: 367-381
Google Scholar - 3. Aitken R.J., Roman S.D.: Antioxidant systems and oxidative stress in the testes. Adv. Exp. Med. Biol., 2008; 636: 154-171
Google Scholar - 4. Aydemir B., Kiziler A.R., Onaran I., Alici B., Ozkara H., Akyolcu M.C.: Impact of Cu and Fe concentrations on oxidative damage in male infertility. Biol. Trace Elem. Res., 2006; 112: 193-203
Google Scholar - 5. Aydilek N., Varisli O., Kocyigit A., Taskin A., Kaya M.S.: Effect of dietary restriction on sperm characteristic and oxidative status on testicular tissue in young rats exposed to long-term heat stress. Andrologia, 2015; 47: 1055-1061
Google Scholar - 6. Babaei H., Kheirandish R., Ebrahimi L.: The effects of copper toxicity on histopathological and morphometrical changes of the rat testes. Asian Pac. J. Trop. Biomed., 2012; 2: S1615-S1619
Google Scholar - 7. Beaudoin J., Ioannoni R., López-Maury L., Bähler J., Ait-Mohand S., Guérin B., Dodani S.C., Chang C.J., Labbé S.: Mfc1 is a novel forespore membrane copper transporter in meiotic and sporulating cells. J. Biol. Chem., 2011; 286: 34356-34372
Google Scholar - 8. Beaudoin J., Ioannoni R., Mailloux S., Plante S., Labbé S.: Transcriptional regulation of the copper transporter Mfc1 in meiotic cells. Eukaryot. Cell., 2013; 12: 575-590
Google Scholar - 9. Benagiano G., Gabelnick H., Farris M.: Contraceptive devices: intravaginal and intrauterine delivery systems. Expert Rev. Med. Devices, 2008; 5: 639-654
Google Scholar - 10. Bonda E., Włostowski T., Krasowska A.: Testicular toxicity induced by dietary cadmium is associated with decreased testicular zinc and increased hepatic and renal metallothionein and zinc in the bank vole (Clethrionomys glareolus). Biometals, 2004; 17: 615-624
Google Scholar - 11. Brown M.A., Stenberg L.M., Mauk A.G.: Identification of catalytically important amino acids in human ceruloplasmin by sitedirected mutagenesis. FEBS Lett., 2002; 520: 8-12
Google Scholar - 12. Celino F.T., Yamaguchi S., Miura C., Ohta T., Tozawa Y., Iwai T., Miura T.: Tolerance of spermatogonia to oxidative stress is due to high levels of Zn and Cu/Zn superoxide dismutase. PLoS One, 2011; 6: e16938
Google Scholar - 13. Chattopadhyay A., Sarkar M., Sengupta R., Roychowdhury G., Biswas N.M.: Antitesticular effect of copper chloride in albino rats. J. Toxicol. Sci., 1999; 24: 393-397
Google Scholar - 14. Chia S.E., Ong C.N., Chua L.H., Ho L.M., Tay S.K.: Comparison of zinc concentrations in blood and seminal plasma and the various sperm parameters between fertile and infertile men. J. Androl., 2000; 21: 53-57
Google Scholar - 15. Culotta V.C., Klomp L.W.J., Strain J., Casareno R.L.B., Krems B., Gitlin J.D.: The copper chaperone for superoxide dismutase. J. Biol. Chem., 1997; 272: 23469-23472
Google Scholar - 16. Cyr D.G., Dufresne J., Pillet S., Alfieri T.J., Hermo L.: Expression and regulation of metallothioneins in the rat epididymis. J. Androl., 2001; 2: 124-135
Google Scholar - 17. De S.K., Enders G.C., Andrews G.K.: High levels of metallothionein messenger RNAs in male germ cells of the adult mouse. Mol. Endocrinol., 1991; 5: 628-636
Google Scholar - 18. De Domenico I., Ward D.M., di Patti M.C.B., Jeong S.Y., David S., Musci G., Kaplan J.: Ferroxidase activity is required for the stability of cell surface ferroportin in cells expressing GPI-ceruloplasmin. EMBO J., 2007; 26: 2823-2831
Google Scholar - 19. de Lamirande E., Leclerc P., Gagnon C.: Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod., 1997; 3: 175-194
Google Scholar - 20. Desai V., Kaler S.G.: Role of copper in human neurological disorders. Am. J. Clin. Nutr., 2008; 88: 855S-858S
Google Scholar - 21. DiDonato M., Sarkar B.: Copper transport and its alterations in Menkes and Wilson diseases. Biochim. Biophys. Acta, 1997; 1360: 3-16
Google Scholar - 22. Esakky P., Hansen D.A., Drury A.M., Moley K.H.: Molecular analysis of cell type-specific gene expression profile during mouse spermatogenesis by laser microdissection and qRT-PCR. Reprod. Sci., 2012; 20: 238-252
Google Scholar - 23. Formigari A., Irato P., Santon A.: Zinc, antioxidant systems and metallothionein in metal mediated-apoptosis: biochemical and cytochemical aspects. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 2007; 146: 443-459
Google Scholar - 24. Fortna R.R., Watson H.A., Nyquist S.E.: Glycosyl phosphatidylinositol-anchored ceruloplasmin is expressed by rat Sertoli cells and is concentrated in detergent-insoluble membrane fractions. Biol. Reprod., 1999; 61: 1042-1049
Google Scholar - 25. Fridovich I.: Superoxide anion radical (O2 – ), superoxide dismutases, and related matters. J. Biol. Chem., 1997; 272: 18515-18517
Google Scholar - 26. Frydman M., Kauschansky A., Bonne‐Tamir B., Nassar F., Homburg R.: Assessment of the hypothalamic‐pituitary‐testicular function in male patients with Wilson’s disease. J. Androl., 1991; 12: 180- 184
Google Scholar - 27. Gancarczyk M., Paziewska-Hejmej A., Carreau S., Tabarowski Z., Bilińska B.: Dose – and photoperiod-dependent effects of 17β-estradiol and the anti-estrogen ICI 182,780 on testicular structure, acceleration of spermatogenesis, and aromatase immunoexpression in immature bank voles. Acta Histochem., 2004; 106: 269-278
Google Scholar - 28. Garratt M., Bathgate R., de Graaf S.P., Brooks R.C.: Copper-zinc superoxide dismutase deficiency impairs sperm motility and in vivo fertility. Reproduction, 2013; 146: 297-304
Google Scholar - 29. Gu W., Hecht N.R.: Translation of a testis-specific Cu/Zn superoxide dismutase (SOD-1) mRNA is regulated by a 65-kilodalton protein which binds to its 5’ untranslated region. Mol. Cell. Biol., 1996; 16: 4535-4543
Google Scholar - 30. Guo Y., Smith K., Lee J., Thiele D.J., Petris M.J.: Identification of methionine-rich clusters that regulate copper-stimulated endocytosis of the human Ctr1 copper transporter. J. Biol. Chem., 2004; 279: 17428-17433
Google Scholar - 31. Gupta A., Lutsenko S.: Human copper transporters: mechanism, role in human diseases and therapeutic potential. Future Med. Chem., 2009; 1: 1125-1142
Google Scholar - 32. Halliwell B.: Biochemistry of oxidative stress. Biochem. Soc. Trans., 2007; 35: 1147-1150
Google Scholar - 33. Hatori Y., Lutsenko S.: An expanding range of functions for the copper chaperone/antioxidant protein Atox1. Antioxid. Redox Signal., 2013; 19: 945-957
Google Scholar - 34. Hecht N.B.: Molecular mechanisms of male germ cell differentiation. Bioessays, 1998; 20: 555-561
Google Scholar - 35. Huster D., Lutsenko S.: Wilson disease: not just a copper disorder. Analysis of a Wilson disease model demonstrates the link between copper and lipid metabolism. Mol. Biosyst., 2007; 3: 816-824
Google Scholar - 36. Hüttemann M., Jaradat S., Grossman L.I.: Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb – the counterpart to testes-specific cytochrome c? Mol. Reprod. Dev., 2003; 66: 8-16
Google Scholar - 37. Ioannoni R., Beaudoin J., Lopez-Maury L., Codlin S., Bahler J., Labbe S.: Cuf2 is a novel meiosis-specific regulatory factor of meiosis maturation. PLoS One, 2012; 7: e36338
Google Scholar - 38. Itoh S., Kim H.W., Nakagawa O., Ozumi K., Lessner S.M., Aoki H., Akram K., McKinney R.D., Ushio-Fukai M., Fukai T.: Novel role of antioxidant-1 (Atox1) as a copper-dependent transcription factor involved in cell proliferation. J. Biol. Chem., 2008; 283: 9157-9167
Google Scholar - 39. Itoh S., Ozumi K., Kim H.W., Nakagawa O., McKinney R.D., Folz R.J., Zelko I.N., Ushio-Fukai M., Fukai T.: Novel mechanism for regulation of extracellular SOD transcription and activity by copper: role of antioxidant-1. Free Radic. Biol. Med., 2009; 46: 95-104
Google Scholar - 40. Jow W.W., Schlegel P.N., Cichon Z., Phillips D., Goldstein M., Bardin C.W.: Identification and localization of copper-zinc superoxide dismutase gene expression in rat testicular development. J. Androl., 1993; 14: 439-447
Google Scholar - 41. Kantsler V., Dunkel J., Blayney M., Goldstein R.E.: Rheotaxis facilitates upstream navigation of mammalian sperm cells. Elife, 2014; 3: e02403
Google Scholar - 42. Kehr S., Malinouski M., Finney L., Vogt S., Labunskyy V.M., Kasaikina M.V., Carlson B.A., Zhou Y., Hatfield D.L., Gladyshev V.N.: X-ray fluorescence microscopy reveals the role of selenium in spermatogenesis. J. Mol. Biol., 2009; 389: 808-818
Google Scholar - 43. Kelly E.J., Palmiter R.D.: A murine model of Menkes disease reveals a physiological function of metallothionein. Nat. Genet., 1996; 13: 219-222
Google Scholar - 44. Khan R.U., Laudadio V., Tufarelli V.: Semen traits and seminal plasma biochemical parameters in white leghorn layer breeders. Reprod. Domest. Anim., 2012; 47: 190-195
Google Scholar - 45. Knazicka Z., Tvrda E., Bardos L., Lukac N.: Dose – and time-dependent effect of copper ions on the viability of bull spermatozoa in different media. J. Environ. Sci. Health. A. Tox. Hazard. Subst. Environ. Eng., 2012; 47: 1294-1300
Google Scholar - 46. Kodama H., Kuribayashi Y., Gagnon C.: Effect of sperm lipid peroxidation on fertilization. J. Androl., 1996; 17: 151-157
Google Scholar - 47. Kotula-Balak M., Lenartowicz M., Kowal M., Styrna J., Bilińska B.: Testicular morphology and expression of aromatase in testes of mice with the mosaic mutation (Atp7a mo-ms). Theriogenology, 2007; 67: 423-434
Google Scholar - 48. Kowal M., Lenartowicz M., Pecio A., Gołas A., Błaszkiewicz T., Styrna J.: Copper metabolism disorders affect testes structure and gamete quality in male mice. Syst. Biol. Reprod. Med., 2010; 56: 431-444
Google Scholar - 49. Kusakabe T., Nakajima K., Suzuki K., Nakazato K., Takada H., Satoh T., Oikawa M., Kobayashi K., Koyama H., Arakawa K., Nagamine T.: The changes of heavy metal and metallothionein distribution in testis induced by cadmium exposure. Biometals, 2008; 21: 71-81
Google Scholar - 50. Lara-Torre E., Spotswood L., Correia N., Weiss P.M.: Intrauterine contraception in adolescents and young women: a descriptive study of use, side effects, and compliance. J. Pediatr. Adolesc. Gynecol., 2011; 24: 39-41
Google Scholar - 51. Larson C.A., Blair B.G., Safaei R., Howell S.B.: The role of the mammalian copper transporter 1 in the cellular accumulation of platinum-based drugs. Mol. Pharmacol., 2009; 75: 324-330
Google Scholar - 52. Lassi K.C., Prohaska J.R.: Erythrocyte copper chaperone for superoxide dismutase is increased following marginal copper deficiency in adult and postweanling mice. J. Nutr., 2012; 142: 292-297
Google Scholar - 53. Lee Y.Y., Choi C.H., Do I.G., Song S.Y., Lee W., Park H.S., Song T.J., Kim M.K., Kim T.J., Lee J.W., Bae D.S., Kim B.G.: Prognostic value of the copper transporters, CTR1 and CTR2, in patients with ovarian carcinoma receiving platinum-based chemotherapy. Gynecol. Oncol., 2011; 122: 361-365
Google Scholar - 54. Leichtmann-Bardoogo Y., Cohen L.A., Weiss A., Marohn B., Schubert S., Meinhardt A., Meyron-Holtz E.G.: Compartmentalization and regulation of iron metabolism proteins protect male germ cells from iron overload. Am. J. Physiol. Endocrinol. Metab., 2012; 302: E1519-E1530
Google Scholar - 55. Lenartowicz M., Grzmil P., Shoukier M., Starzyński R., Marciniak M., Lipiński P.: Mutation in the CPC motif-containing 6th transmembrane domain affects intracellular localization, trafficking and copper transport efficiency of ATP7Aprotein in mosaic mutant mice – an animal model of Menkes disease. Metallomics, 2012; 4: 197-204
Google Scholar - 56. Lenartowicz M., Krzeptowski W.: Structure and function of ATP7A and ATP7B proteins – Cu-transporting ATPases. Postępy Biochem., 2010; 56: 317-327
Google Scholar - 57. Lenartowicz M., Sasuła K.: Altered copper metabolism in the mosaic mutant mice. Nutr. Res., 2000; 20: 1467-1471
Google Scholar - 58. Lenartowicz M., Starzyński R.R., Krzeptowski W., Grzmil P., Bednarz A., Ogórek M., Pierzchała O., Staroń R., Gajowiak A., Lipiński P.: Haemolysis and perturbations in the systemic iron metabolism of suckling, copper-deficient mosaic mutant mice – an animal model of Menkes disease. PLoS One, 2014; 9: e107641
Google Scholar - 59. Lenartowicz M., Wieczerzak K., Krzeptowski W., Dobosz P., Grzmil P., Starzyński R., Lipiński P.: Developmental changes in the expression of the Atp7a gene in the liver of mice during the postnatal period. J. Exp. Zool. A Ecol. Genet. Physiol., 2010; 313: 209-217
Google Scholar - 60. Lenartowicz M., Windak R., Tylko G., Kowal M., Styrna J.: Effects of copper supplementation on the structure and content of elements in kidneys of mosaic mutant mice. Biol. Trace Elem. Res., 2010; 136: 204-220
Google Scholar - 61. Letelier M.E., Sánchez-Jofré S., Peredo-Silva L., Cortés-Troncoso J., Aracena-Parks P.: Mechanisms underlying iron and copper ions toxicity in biological systems: Pro-oxidant activity and protein-binding effects. Chem. Biol. Interact., 2010; 188: 220-227
Google Scholar - 62. Liang G., Zhang X.D., Wang L.J., Sha Y.S., Zhang J.C., Miao S.Y., Zong S.D., Wang L.F., Koide S.S.: Identification of differentially expressed genes of primary spermatocyte against round spermatid isolated from human testis using the laser capture microdissection technique. Cell Res., 2004; 14: 507-512
Google Scholar - 63. Lindley P.F., Card G., Zaitseva I., Zaitsev V., Reinhammar B., Selin-Lindgren E., Yoshida K.: An X-ray structural study of human ceruloplasmin in relation to ferroxidase activity. J. Biol. Inorg. Chem., 1997; 2: 454-463
Google Scholar - 64. Liu N., Lo L.S., Askary S.H., Jones L., Kidane T.Z., Trang T., Nguyen M., Goforth J., Chu Y.H., Vivas E., Tsai M., Westbrook T., Linder M.C.: Transcuprein is a macroglobulin regulated by copper and iron availability. J. Nutr. Biochem., 2007; 18: 597-608
Google Scholar - 65. Løvstad R.A.: Copper catalyzed oxidation of ascorbate (vitamin C). Inhibitory effect of catalase, superoxide dismutase, serum proteins (ceruloplasmin, albumin, apotransferrin) and amino acids. Int. J. Biochem., 1987; 19: 309-313
Google Scholar - 66. Lutsenko S., Barnes N.L., Bartee M.Y., Dmitriev O.Y.: Function and regulation of human copper-transporting ATPases. Physiol. Rev., 2007; 87: 1011-1046
Google Scholar - 67. Maeda Y., Kinoshita T.: Structural remodeling, trafficking and functions of glycosylphosphatidylinositol-anchored proteins. Prog. Lipid Res., 2011; 50: 411-424
Google Scholar - 68. Mansour D., Gemzell-Danielsson K., Inki P., Jensen J.T.: Fertility after discontinuation of contraception: a comprehensive review of the literature. Contraception, 2011; 84: 465-477
Google Scholar - 69. Marklund S.L.: Extracellular superoxide dismutase and other superoxide dismutase isoenzymes in tissues from nine mammalian species. Biochem. J., 1984; 222: 649-655
Google Scholar - 70. Marzec-Wróblewska U., Kamiński P., Lakota P., Szymański M., Wasilow K., Ludwikowski G., Kuligowska-Prusińska M., Odroważ- -Sypniewska G., Stuczyński T., Michałkiewicz J.: Zinc and iron concentration and SOD activity in human semen and seminal plasma. Biol. Trace Elem. Res., 2011; 143: 167-177
Google Scholar - 71. Milani P., Gagliardi S., Cova E., Cereda C.: SOD1 transcriptional and posttranscriptional regulation and its potential implications in ALS. Neurol. Res. Int., 2011; 2011: 458427
Google Scholar - 72. Miska-Schramm A., Kruczek M., Kapusta J.: Effect of copper exposure on reproductive ability in the bank vole (Myodes glareolus). Ecotoxicology, 2014; 23: 1546-1554
Google Scholar - 73. Morales C., Sylvester S.R., Griswold M.D.: Transport of iron and transferrin synthesis by the seminiferous epithelium of the rat in vivo. Biol. Reprod., 1987; 37: 995-1005
Google Scholar - 74. Mruk D., Cheng C.H., Cheng Y.H., Mo M.Y., Grima J., Silvestrini B., Lee W.M., Cheng C.Y.: Rat testicular extracellular superoxide dismutase: its purification, cellular distribution, and regulation. Biol. Reprod., 1998; 59: 298-308
Google Scholar - 75. Mukai C., Travis A.J.: What sperm can teach us about energy production. Reprod. Domest. Anim., 2012; 47: 164-169
Google Scholar - 76. Murawski M., Saczko J., Marcinkowska A., Chwiłkowska A., Gryboś M., Banaś T.: Evaluation of superoxide dismutase activity and its impact on semen quality parameters of infertile men. Folia Histochem. Cytobiol., 2007; 45: S123-S126
Google Scholar - 77. Narisawa S., Hecht N.B., Goldberg E., Boatright K.M., Reed J.C., Millán J.L.: Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy. Mol. Cell. Biol., 2002; 22: 5554-5562
Google Scholar - 78. Nevitt T., Ohrvik H., Thiele D.J.: Charting the travels of copper in eukaryotes from yeast to mammals. Biochim. Biophys. Acta, 2012; 1823: 1580-1593
Google Scholar - 79. Nishimura H., Nishimura N., Tohyama C.: Localization of metallothionein in the genital organs of the male rat. J. Histochem. Cytochem., 1990; 38: 927-933
Google Scholar - 80. Nodera M., Yanagisawa H., Wada O.: Increased apoptosis in a variety of tissues of zinc-deficient rats. Life Sci., 2001; 69: 1639-1649
Google Scholar - 81. Nose Y., Rees E.M., Thiele D.J.: Structure of the Ctr1 copper trans’PORE’ter reveals novel architecture. Trends Biochem. Sci., 2006; 31: 604-607
Google Scholar - 82. O’Halloran T.V, Culotta V.C.: Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem., 2000; 275: 25057-25060
Google Scholar - 83. Öhrvik H., Thiele D.J.: The role of Ctr1 and Ctr2 in mammalian copper homeostasis and platinum-based chemotherapy. J. Trace Elem. Med. Biol., 2015; 31: 178-182
Google Scholar - 84. Orlando C., Caldini A.L., Barni T., Wood W.G., Strasburger C.J., Natali A., Maver A., Forti G., Serio M.: Ceruloplasmin and transferrin in human seminal plasma: are they an index of seminiferous tubular function? Fertil. Steril., 1985; 43: 290-294
Google Scholar - 85. Ozawa N., Goda N., Makino N., Yamaguchi T., Yoshimura Y., Suematsu M.: Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J. Clin. Invest., 2002; 109: 457-467
Google Scholar - 86. Park K., Jeon S., Song Y.J., Yi L.S.: Proteomic analysis of boar spermatozoa and quantity changes of superoxide dismutase 1, glutathione peroxidase, and peroxiredoxin 5 during epididymal maturation. Anim. Reprod. Sci., 2012; 135: 53-61
Google Scholar - 87. Patel B.N., Dunn R.J., David S.: Alternative RNA splicing generates a glycosylphosphatidylinositol-anchored form of ceruloplasmin in mammalian brain. J. Biol. Chem., 2000; 275: 4305-4310
Google Scholar - 88. Peeker R., Abramsson L., Marklund S.L.: Superoxide dismutase isoenzymes in human seminal plasma and spermatozoa. Mol. Hum. Reprod., 1997; 3: 1061-1066
Google Scholar - 89. Penkowa M., Florit S., Giralt M., Quintana A., Molinero A., Carrasco J., Hidalgo J.: Metallothionein reduces central nervous system inflammation, neurodegeneration, and cell death following kainic acid-induced epileptic seizures. J. Neurosci. Res., 2005; 79: 522-534
Google Scholar - 90. Piasecka M., Gaczarzewicz D., Kurzawa R., Laszczyńska M., Kram A.: Diagnostic evaluation of oxidoreductive capability of sperm mitochondria. Rocz. Akad. Med. w Białymst., 2004; 49: 108-110
Google Scholar - 91. Plante S., Ioannoni R., Beaudoin J., Labbé S.: Characterization of Schizosaccharomyces pombe copper transporter proteins in meiotic and sporulating cells. J. Biol. Chem., 2014; 289: 10168-10181
Google Scholar - 92. Qin Z., Itoh S., Jeney V., Ushio-Fukai M., Fukai T.: Essential role for the Menkes ATPase in activation of extracellular superoxide dismutase: implication for vascular oxidative stress. FASEB J., 2005; 20: 334-336
Google Scholar - 93. Roblero L., Guadarrama A., Lopez T., Zegers-Hochschild F.: Effect of copper ion on the motility, viability, acrosome reaction and fertilizing capacity of human spermatozoa in vitro. Reprod. Fertil. Dev., 1996; 8: 871-874
Google Scholar - 94. Roy D., Dey S., Majumder G.C., Bhattacharyya D.: Copper: a biphasic regulator of caprine sperm forward progression. Syst. Biol. Reprod. Med., 2014; 60: 52-57
Google Scholar - 95. Rytka J., Palamarczyk G.: Yeast model of an eucaryotic organism in molecular biology. Postępy Biochem., 1993; 39: 152-155
Google Scholar - 96. Safaei R.: Role of copper transporters in the uptake and efflux of platinum containing drugs. Cancer Lett., 2006; 234: 34-39
Google Scholar - 97. Sakhaee E., Abshenas J., Emadi L., Azari O., Kheirandish R., Samaneh A.: Effects of vitamin C on epididymal sperm quality following experimentally induced copper poisoning in mice. Comp. Clin. Path., 2014; 23: 181-186
Google Scholar - 98. Salsabili N., Mehrsai A.R., Jalaie S.: Concentration of blood and seminal plasma elements and their relationships with semen parameters in men with spinal cord injury. Andrologia, 2009; 41: 24-28
Google Scholar - 99. Saunders P.T., Millar M.R., West A.P., Sharpe R.M.: Mitochondrial cytochrome C oxidase II messenger ribonucleic acid is expressed in pachytene spermatocytes at high levels and in a stage-dependent manner during spermatogenesis in the rat. Biol. Reprod., 1993; 48: 57-67
Google Scholar - 100. Sharma M.C., Joshi C., Pathak N.N., Kaur H.: Copper status and enzyme, hormone, vitamin and immune function in heifers. Res. Vet. Sci., 2005; 79: 113-123
Google Scholar - 101. Skandhan K.P.: Review on copper in male reproduction and contraception. Rev. Fr. Gynecol. Obstet., 1992; 87: 594-598
Google Scholar - 102. Skrzycki M., Czeczot H.: Extracellular superoxide dismutase (EC-SOD) – structure, properties and functions. Postępy Hig. Med. Dośw., 2004; 58: 301-311
Google Scholar - 103. Sohal R.S., Toy P.L., Allen R.G.: Relationship between life expectancy, endogenous antioxidants and products of oxygen free radical reactions in the housefly, Musca domestica. Mech. Ageing Dev., 1986; 36: 71-77
Google Scholar - 104. Srinivasan S., Avadhani N.G.: Cytochrome c oxidase dysfunction in oxidative stress. Free Radic. Biol. Med., 2012; 53: 1252-1263
Google Scholar - 105. Steiger D., Fetchko M., Vardanyan A., Atanesyan L., Steiner K., Turski M.L., Thiele D.J., Georgiev O., Schaffner W.: The Drosophila copper transporter Ctr1C functions in male fertility. J. Biol. Chem., 2010; 285: 17089-17097
Google Scholar - 106. Suzuki T., Nakajima K., Yamamoto A., Yamanaka H.: Metallothionein binding zinc inhibits nuclear chromatin decondensation of human spermatozoa. Andrologia, 1995; 27: 161-164
Google Scholar - 107. Sylvester S.R., Griswold M.D.: Localization of transferrin and transferrin receptors in rat testes. Biol. Reprod., 1984; 31: 195-203
Google Scholar - 108. Sylvester S.R., Griswold M.D.: The testicular iron shuttle: a “nurse” function of the Sertoli cells. J. Androl., 1994; 15: 381-385
Google Scholar - 109. Tarnacka B., Rodo M., Cichy S., Członkowska A.: Procreation ability in Wilson’s disease. Acta Neurol. Scand., 2000; 101: 395-398
Google Scholar - 110. Telianidis J., Hung Y.H., Materia S., La Fontaine S.: Role of the P-type ATPases, ATP7A and ATP7B in brain copper homeostasis. Front. Aging Neurosci., 2013; 5: 44
Google Scholar - 111. Tohyama C., Nishimura N., Suzuki J.S., Karasawa M., Nishimura H.: Metallothionein mRNA in the testis and prostate of the rat detected by digoxigenin-labeled riboprobe. Histochemistry, 1994; 101: 341-346
Google Scholar - 112. Tsunoda S., Kawano N., Miyado K., Kimura N., Fujii J.: Impaired fertilizing ability of superoxide dismutase 1-deficient mouse sperm during in vitro fertilization. Biol. Reprod., 2012; 87: 121
Google Scholar - 113. Tümer Z., Møller L.B.: Menkes disease. Eur. J. Hum. Genet., 2010; 18: 511-518
Google Scholar - 114. Uriu-Adams J.Y., Keen C.L.: Copper, oxidative stress, and human health. Mol. Aspects Med., 2005; 26: 268-298
Google Scholar - 115. van den Berghe P.V., Klomp L.W.: Posttranslational regulation of copper transporters. J. Biol. Inorg. Chem., 2010; 15: 37-46
Google Scholar - 116. Vasák M.: Advances in metallothionein structure and functions. J. Trace Elem. Med. Biol., 2005; 19: 13-17
Google Scholar - 117. Vonk W.I., Klomp L.W.: Role of transition metals in the pathogenesis of amyotrophic lateral sclerosis. Biochem. Soc. Trans., 2008; 36: 1322-1328
Google Scholar - 118. Walczak-Jedrzejowska R., Wolski J.K., Slowikowska-Hilczer J.: The role of oxidative stress and antioxidants in male fertility. Cent. Eur. J. Urol., 2013; 66: 60-67
Google Scholar - 119. Walter C.A., Intano G.W., McCarrey J.R., McMahan C.A., Walter R.B.: Mutation frequency declines during spermatogenesis in young mice but increases in old mice. Proc. Natl. Acad. Sci. USA, 1998; 95: 10015-10019
Google Scholar - 120. Wee N.K., Weinstein D.C., Fraser S.T., Assinder S.J.: The mammalian copper transporters CTR1 and CTR2 and their roles in development and disease. Int. J. Biochem. Cell Biol., 2013; 45: 960-963
Google Scholar - 121. West E.C., Prohaska J.R.: Cu,Zn-superoxide dismutase is lower and copper chaperone CCS is higher in erythrocytes of copper-deficient rats and mice. Exp. Biol. Med., 2004; 229: 756-764
Google Scholar - 122. Wierzbicka D., Gromadzka G.: Ceruloplasmin, hephaestin and zyklopen: the three multicopper oxidases important for human iron metabolism. Postępy Hig. Med. Dośw., 2014; 68: 912-924
Google Scholar - 123. Wijmenga C., Klomp L.W.: Molecular regulation of copper excretion in the liver. Proc. Nutr. Soc., 2004; 63: 31-39
Google Scholar - 124. Williams M.S., Kwon J.: T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic. Biol. Med., 2004; 37: 1144-1151
Google Scholar - 125. Wright W.W., Musto N.A., Mather J.P., Bardin C.W.: Sertoli cells secrete both testis-specific and serum proteins. Proc. Natl. Acad. Sci. USA, 1981; 78: 7565-7569
Google Scholar - 126. Xia B., Chen H., Hu G., Wang L., Cao H., Zhang C.: The co-induced effects of molybdenum and cadmium on the trace elements and the mRNA expression levels of CP and MT in duck testicles. Biol. Trace Elem. Res., 2016; 169: 331-340
Google Scholar - 127. Yamaguchi S., Miura C., Kikuchi K., Celino F.T., Agusa T., Tanabe S., Miura T.: Zinc is an essential trace element for spermatogenesis. Proc. Natl. Acad. Sci. USA, 2009; 106: 10859-10864
Google Scholar - 128. Yamashita Y.M., Fuller M.T., Jones D.L.: Signaling in stem cell niches: lessons from the Drosophila germline. J. Cell Sci., 2005; 118: 665-672
Google Scholar - 129. Yuan D., Wang H., He H., Jia L., He Y., Wang T., Zeng X., Li Y., Li S., Zhang C.: Protective effects of total flavonoids from epimedium on the male mouse reproductive system against cyclophosphamide- -induced oxidative injury by up-regulating the expressions of SOD3 and GPX1. Phytother. Res., 2014; 28: 88-97
Google Scholar