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Human Fertility
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Volume 23, 2020 - Issue 1
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Review Article

Effects of zinc deficiency on impaired spermatogenesis and male infertility: the role of oxidative stress, inflammation and apoptosis

, , , &
Pages 5-16 | Received 09 Aug 2017, Accepted 16 May 2018, Published online: 21 Aug 2018

References

  • Abbasi, A.A., Prasad, A.S., & Rabbani, P.R. (1979). Experimental zinc deficiency in man: Effect on spermatogenesis. Transactions of the Association of American Physicians, 92, 292–302. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/549254.
  • Agarwal, A., Robo, R., Jain, N., Gutch, M., Consil, S., & Kumar, S. (2014). Oxidative stress determined through the levels of antioxidant enzymes and the effect of N-acetylcysteine in aluminum phosphide poisoning. Indian Journal of Critical Care Medicine, 18, 666–671. doi: 10.4103/0972-5229.142176.
  • Agarwal, A., & Said, T.M. (2005). Oxidative stress, DNA damage and apoptosis in male infertility: A clinical approach. BJU International, 95, 503–507. doi: 10.1111/j.1464-410X.2005.05328.x.
  • Agarwal, A., & Sekhon, L.H. (2011). Oxidative stress and antioxidants for idiopathic oligoasthenoteratospermia: Is it justified? Indian Journal of Urology, 27, 74–85. doi: 10.4103/0970-1591.78437.
  • Agarwal, A., Tvrda, E., & Sharma, R. (2014). Relationship amongst teratozoospermia, seminal oxidative stress and male infertility. Reproductive Biology and Endocrinology, 12, 45. doi: 10.1186/1477-7827-12-45.
  • Agarwal, A., & Wang, S.M. (2017). Clinical relevance of oxidation-reduction potential in the evaluation of male infertility. Urology, 104, 84–89. doi: 10.1016/j.urology.2017.02.016.
  • Ahmad, G., Agarwal, A., Esteves, S.C., Sharma, R., Almasry, M., Al-Gonaim, A., … Sabanegh, E. (2017). Ascorbic acid reduces redox potential in human spermatozoa subjected to heat-induced oxidative stress. Andrologia, 49, e12773. doi: 10.1111/and.12773.
  • Ajina, T., Sallem, A., Haouas, Z., & Mehdi, M. (2017). Total antioxidant status and lipid peroxidation with and without in vitro zinc supplementation in infertile men. Andrologia, 49, e12703. doi: 10.1111/and.12703.
  • Al-Bader, A., Omu, A.E., & Dashti, H. (1999). Chronic cadmium toxicity to sperm of heavy cigarette smokers: Immunomodulation by zinc. Archives of Andrology, 43, 135–140. doi: 10.1080/014850199262643.
  • Atig, F., Raffa, M., Habib, B.A., Kerkeni, A., Saad, A., & Ajina, M. (2012). Impact of seminal trace element and glutathione levels on semen quality of Tunisian infertile men. BMC Urology, 12, 6. doi: 10.1186/1471-2490-12-6.
  • Azenabor, A., Ekun, A.O., & Akinloye, O. (2015). Impact of inflammation on male reproductive tract. Journal of Reproduction & Infertility, 16, 123–129. Retrieved from https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4508350/.
  • Babaei, H., & Abshenas, J. (2013). Zinc therapy improves adverse effects of long term administration of copper on epididymal sperm quality of rats. Iranian Journal of Reproductive Medicine, 11, 577–582. Retrieved from http://www.sid.ir/en/journal/ViewPaper.aspx?ID=453605.
  • Bagchi, D., Vuchetich, P.J., Bagchi, M., Tran, M.X., Krohn, R.L., Ray, S.D., & Stohs, S.J. (1998). Protective effects of zinc salts on TPA-induced hepatic and brain lipid peroxidation, glutathione depletion, DNA damage and peritoneal macrophage activation in mice. General Pharmacology, 30, 43–50. doi: 10.1016/S0306-3623(97)00072-4.
  • Barbato, V., Talevi, R., Braun, S., Merolla, A., Sudhakaran, S., Longobardi, S., & Gualtieri, R. (2017). Supplementation of sperm media with zinc, D-aspartate and co-enzyme Q10 protects bull sperm against exogenous oxidative stress and improves their ability to support embryo development. Zygote, 25, 168–175. doi: 10.1017/S0967199416000459.
  • Boukhris, R. (1971). [Syndrome of hypogonadism, growth retardation and zinc deficiency: review, discussion and research prospects]. La Tunisie Médicale, 3, 145–151. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/4946486.
  • Caggiano, V., Schnitzler, R., Strauss, W., Baker, R.K., Carter, A.C., Josephson, A.S., & Wallach, S. (1969). Zinc deficiency in a patient with retarded growth, hypogonadism, hypogammaglobulinemia and chronic infection. American Journal of the Medical Sciences, 257, 305–319. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/5786695 doi: 10.1097/00000441-196905000-00003.
  • Cavalieri, J., & Wang, M. (2015). Chemical sterilisation of Bos indicus bull calves following intratesticular injection of zinc acetate: Effects on growth and concentrations of testosterone. Animal Reproduction Science, 159, 163–171. doi: 10.1016/j.anireprosci.2015.06.012.
  • Chesters, J.K., Petrie, L., & Lipson, K.E. (1993). Two zinc-dependent steps during G1 to S phase transition. Journal of Cellular Physiology, 155, 445–451. doi: 10.1002/jcp.1041550303.
  • Chia, S.E., Ong, C.N., Chua, L.H., Ho, L.M., & Tay, S.K. (2000). Comparison of zinc concentrations in blood and seminal plasma and the various sperm parameters between fertile and infertile men. Journal of Andrology, 21, 53–57. doi: 10.1002/j.1939-4640.2000.tb03275.x.
  • Chu, Q., Chi, Z.H., Zhang, X., Liang, D, Wang, X., Zhao, Y., … Zhang, P. (2016). A potential role for zinc transporter 7 in testosterone synthesis in mouse Leydig tumor cells. International Journal of Molecular Medicine, 37, 1619–1626. doi: 10.3892/ijmm.2016.2576.
  • Close, C.E., Roberts, P.L., & Berger, R.E. (1990). Cigarettes, alcohol and marijuana are related to pyospermia in infertile men. Journal of Urology, 144, 900–903. doi: 10.1016/S0022-5347(17)39618-0.
  • Colagar, A.H., Jorsaraee, G.A., & Marzony, E.T. (2007). Cigarette smoking and the risk of male infertility. Pakistan Journal of Biological Sciences, 10, 3870–3874. doi: 10.3923/pjbs.2007.3870.3874.
  • Colagar, A.H., & Marzony, E.T. (2009). Ascorbic Acid in human seminal plasma: Determination and its relationship to sperm quality. Journal of Clinical Biochemistry and Nutrition, 45, 144–149. doi: 10.3164/jcbn.08-251.
  • Colagar, A.H., Marzony, E.T., & Chaichi, M.J. (2009). Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutrition Research, 29, 82–88. doi: 10.1016/j.nutres.2008.11.007.
  • Correia, J., Michelangeli, F., & Publicover, S. (2015). Regulation and roles of Ca2+ stores in human sperm. Reproduction, 150, R65–R76. doi: 10.1530/REP-15-0102.
  • Croxford, T.P., McCormick, N.H., & Kelleher, S.L. (2011). Moderate zinc deficiency reduces testicular Zip6 and Zip10 abundance and impairs spermatogenesis in mice. Journal of Nutrition, 141, 359–365. doi: 10.3945/jn.110.131318.
  • Daniel, A.G., Peterson, E.J., & Farrell, N.P. (2014). The bioinorganic chemistry of apoptosis: Potential inhibitory zinc binding sites in caspase-3. Angewandte Chemie International Edition English, 53, 4098–4101. doi: 10.1002/anie.201311114.
  • Deng, C.H., Zheng, B., & She, S.F. (2005). [A clinical study of biological zinc for the treatment of male infertility with chronic prostatitis]. Zhonghua Nan Ke Xue, 11, 127–129. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/15755033.
  • Dissanayake, D., Wijesinghe, P., Ratnasooriya, W., & Wimalasena, S. (2010). Relationship between seminal plasma zinc and semen quality in a subfertile population. Journal of Human Reproductive Sciences, 3, 124–128. doi: 10.4103/0974-1208.74153.
  • Dorostkar, K., Alavi Shoushtari, S.M., & Khaki, A. (2014). Effects of in vitro zinc sulphate additive to the semen extender on water buffalo (Bubalus bubalis) spermatozoa before and after freezing. International Journal of Fertility and Sterility, 8, 325–332. Retrieved from http://www.sid.ir/en/journal/ViewPaper.aspx?ID=405367.
  • Ebisch, I.M., Thomas, C.M., Peters, W.H., Braat, D.D., & Steegers-Theunissen, R.P. (2007). The importance of folate, zinc and antioxidants in the pathogenesis and prevention of subfertility. Human Reproduction Update, 13, 163–174. doi: 10.1093/humupd/dml054.
  • Egwurugwu, J.N., Ifedi, C.U., Uchefuna, R.C., Ezeokafor, E.N., & Alagwu, E.A. (2013). Effects of zinc on male sex hormones and semen quality in rats. Nigerian Journal of Physiological Sciences, 28, 17–22. Retrieved from https://www.ajol.info/index.php/njps/article/view/95096
  • Erdem, M., Yuceturk, A., Cetinkaya, T., Erdem, A., & Himmetoglu, O. (2013). Comparison of serum and seminal plasma zinc levels on sperm parameters in patients with unexplained and male factor infertility. Fertility and Sterility, 100, S442. doi: 10.1016/j.fertnstert.2013.07.565.
  • Fatima, P., Begum, N., Lshrat, S., Banu, J., Anwary, S.A., Rolly, S.J., … Hossain, H.N. (2015). Zinc supplementation in male infertility. Bangabandhu Sheikh Mujib Medical University Journal, 8, 9–13. doi: 10.3329/bsmmuj.v8i1.28913.
  • Foresta, C., Garolla, A., Cosci, I., Menegazzo, M., Ferigo, M., Gandin, V., & De Toni, L. (2014). Role of zinc trafficking in male fertility: From germ to sperm. Human Reproduction, 29, 1134–1145. doi: 10.1093/humrep/deu075.
  • Freedman, L.P. (1992). Anatomy of the steroid receptor zinc finger region. Endocrine Reviews, 13, 129–145. doi: 10.1210/edrv-13-2-129.
  • Fukamachi, Y., Karasaki, Y., Sugiura, T., Itoh, H., Abe, T., Yamamura, K., & Higashi, K. (1998). Zinc suppresses apoptosis of U937 cells induced by hydrogen peroxide through an increase of the Bcl-2/Bax ratio. Biochemical and Biophysical Research Communications, 246, 364–369. doi: 10.1006/bbrc.1998.8621.
  • Ganger, R., Garla, R., Mohanty, B.P., Bansal, M.P., & Garg, M.L. (2016). Protective effects of zinc against acute arsenic toxicity by regulating antioxidant defense system and cumulative metallothionein expression. Biological Trace Element Research, 169, 218–229. doi: 10.1007/s12011-015-0400-x.
  • Gavella, M., & Lipovac, V. (1998). In vitro effect of zinc on oxidative changes in human semen. Andrologia, 30, 317–323. doi: 10.1111/j.1439-0272.1998.tb01177.x.
  • Gruschwitz, M.S., Brezinschek, R., & Brezinschek, H.P. (1996). Cytokine levels in the seminal plasma of infertile males. Journal of Andrology, 17, 158–163. doi: 10.1002/j.1939-4640.1996.tb01765.x.
  • Guzikowski, W., Szynkowska, M.I., Motak-Pochrzęst, H., Pawlaczyk, A., & Sypniewski, S. (2015). Trace elements in seminal plasma of men from infertile couples. Archives of Medical Science, 3, 591–598. doi: 10.5114/aoms.2015.52363.
  • Hamdi, S.A., Nassif, O.I., & Ardawi, M.S. (1997). Effect of marginal or severe dietary zinc deficiency on testicular development and functions of the rat. Archives of Andrology, 38, 243–253. doi: 10.3109/01485019708994883.
  • Ho, L.H., Ruffin, R.E., Murgia, C., Li, L., Krilis, S.A., & Zalewski, P.D. (2004). Labile zinc and zinc transporter ZnT4 in mast cell granules: Role in regulation of caspase activation and NF-kappaB translocation. Journal of Immunology, 172, 7750–7760. doi: 10.4049/jimmunol.172.12.7750.
  • Hong, C.Y., Chiang, B.N., & Turner, P. (1984). Calcium ion is the key regulator of human sperm function. Lancet, 324, 1449–1451. doi: 10.1016/S0140-6736(84)91634-9.
  • Hosseinzadeh Colagar, A., Pouramir, M., Tahmasbpour Marzony, E., & Jorsaraei, E.G.A. (2009). Relationship between seminal malondialdehyde levels and sperm quality in fertile and infertile men. Brazilian Archives of Biology and Technology, 52, 1387–1392. doi: 10.1590/S1516-89132009000600010.
  • Hyun, H.J., Sohn, J., Ahn, Y.H., Shin, H.C., Koh, J.Y., & Yoon, Y.H. (2000). Depletion of intracellular zinc induces macromolecule synthesis- and caspase-dependent apoptosis of cultured retinal cells. Brain Research, 869, 39–48. doi: 10.1016/S0006-8993(00)02340-4.
  • Inaba, K., Dreanno, C., & Cosson, J. (2003). Control of flatfish sperm motility by CO2 and carbonic anhydrase. Cell Motility and the Cytoskeleton, 55, 174–187. doi: 10.1002/cm.10119.
  • Inoue, A., Ishiji, A., Kasagi, S., Ishizuka, M., Hirose, S., Baba, T., & Hagiwara, H. (2000). The transcript for a novel protein with a zinc finger motif is expressed at specific stages of mouse spermatogenesis. Biochemical and Biophysical Research Communications, 273, 398–403. doi: 10.1006/bbrc.2000.2953.
  • Ishizuka, M., Ohshima, H., Tamura, N., Nakada, T., Inoue, A., Hirose, S., & Hagiwara, H. (2003). Molecular cloning and characteristics of a novel zinc finger protein and its splice variant whose transcripts are expressed during spermatogenesis. Biochemical and Biophysical Research Communications, 301, 1079–1085. doi: 10.1016/S0006-291X(03)00085-8.
  • Ishizuka, M., Ohtsuka, E., Inoue, A., Odaka, M., Ohshima, H., Tamura, N., … Hagiwara, H. (2016). Abnormal spermatogenesis and male infertility in testicular zinc finger protein Zfp318-knockout mice. Development, Growth & Differentiation, 58, 600–608. doi: 10.1111/dgd.12301.
  • Jalali, G.R., Roozbeh, J., Mohammadzadeh, A., Sharifian, M., Sagheb, M.M., Jahromi, A.H., … Afshariani, R. (2010). Impact of oral zinc therapy on the level of sex hormones in male patients on hemodialysis. Renal Failure, 32, 417–419. doi: 10.3109/08860221003706958.
  • Jemai, H., Lachkar, H.A., Messaoudi, I., & Kerkeni, A. (2010). Effects of zinc pre-treatment on blood glutathione, serum zinc and kidney histological organisation in male rats exposed to cadmium. Journal of Trace Elements in Medicine and Biology, 24, 277–282. doi: 10.1016/j.jtemb.2010.07.001.
  • Kehinde, E.O., Anim, J.T., Oriowo, M.A., Memon, A., Omu, A.E., Al-Azemi, M.K., … Omu, F.E. (2015). Molecular basis for the effects of zinc deficiency on spermatogenesis: An experimental study in the Sprague-Dawley rat model. Indian Journal of Urology, 31, 57–64. doi: 10.4103/0970-1591.139570.
  • Kendall, N.R., McMullen, S., Green, A., & Rodway, R.G. (2000). The effect of a zinc, cobalt and selenium soluble glass bolus on trace element status and semen quality of ram lambs. Animal Reproduction Science, 62, 277–283. doi: 10.1016/S0378-4320(00)00120-2.
  • Khan, M.S., Zaman, S., Sajjad, M., Shoaib, M., & Gilani, G. (2011). Assessment of the level of trace element zinc in seminal plasma of males and evaluation of its role in male infertility. International Journal of Applied and Basic Medical Research, 1, 93–96. doi: 10.4103/2229-516X.91152.
  • Kocak, I., Yenisey, C., Dündar, M., Okyay, P., & Serter, M. (2002). Relationship between seminal plasma interleukin-6 and tumor necrosis factor alpha levels with semen parameters in fertile and infertile men. Urological Research, 30, 263–267. doi: 10.1007/s00240-002-0269-y.
  • Kothari, R.P., & Chaudhari, A.R. (2016). Zinc levels in seminal fluid in infertile males and its relation with serum free testosterone. Journal of Clinical and Diagnostic Research, 10, CC05–CC08. doi: 10.7860/JCDR/2016/14393.7723.
  • Kumar, N., & Kant Singh, A. (2016). Role of zinc in male infertility: Review of literature. Indian Journal of Obstetrics and Gynecology Research, 3, 167–171. Retrieved from https://www.innovativepublication.com/view-article.php?article_id =1954&jid =28&issue_id =199&volume_id =75 doi: 10.5958/2394-2754.2016.00028.X.
  • Kumar, N., Verma, R.P., Singh, L.P., Varshney, V.P., & Dass, R.S. (2006). Effect of different levels and sources of zinc supplementation on quantitative and qualitative semen attributes and serum testosterone level in crossbred cattle (Bos indicus x Bos taurus) bulls. Reproduction Nutrition Development, 46, 663–675. doi: 10.1051/rnd:2006041.
  • Kumari, D., Nair, N., & Bedwal, R.S. (2011). Testicular apoptosis after dietary zinc deficiency: Ultrastructural and TUNEL studies. Systems Biology in Reproductive Medicine, 57, 233–243. doi: 10.3109/19396368.2011.584500.
  • Liu, D.Y., Sie, B.S., Liu, M.L., Agresta, F., & Baker, H.W. (2009). Relationship between seminal plasma zinc concentration and spermatozoa-zona pellucida binding and the ZP-induced acrosome reaction in subfertile men. Asian Journal of Andrology, 11, 499–507. doi: 10.1038/aja.2009.23.
  • Ludwig, M., Vidal, A., Huwe, P., Diemer, T., Pabst, W., & Weidner, W. (2003). Significance of inflammation on standard semen analysis in chronic prostatitis/chronic pelvic pain syndrome. Andrologia, 35, 152–156. doi: 10.1046/j.1439-0272.2003.00553.x.
  • MacDonald, R.S. (2000). The role of zinc in growth and cell proliferation. The Journal of Nutrition, 130, 1500S–1508S. doi: 10.1093/jn/130.5.1500S.
  • Meerarani, P., Ramadass, P., Toborek, M., Bauer, H.C., Bauer, H., & Hennig, B. (2000). Zinc protects against apoptosis of endothelial cells induced by linoleic acid and tumor necrosis factor alpha. The American Journal of Clinical Nutrition, 71, 81–87. doi: 10.1093/ajcn/71.1.81.
  • Merker, H.J., & Günther, T. (1997). Testis damage induced by zinc deficiency in rats. Journal of Trace Elements in Medicine and Biology, 11, 19–22. doi: 10.1016/S0946-672X(97)80004-1.
  • Merrells, K.J., Blewett, H., Jamieson, J.A., Taylor, C.G., & Suh, M. (2009). Relationship between abnormal sperm morphology induced by dietary zinc deficiency and lipid composition in testes of growing rats. British Journal of Nutrition, 102, 226–232. doi: 10.1017/S0007114508159037.
  • Michalska-Mosiej, M., Socha, K., Soroczyńska, J., Karpińska, E., Łazarczyk, B., & Borawska, M.H. (2016). Selenium, zinc, copper, and total antioxidant status in the serum of patients with chronic tonsillitis. Biological Trace Element Research, 173, 30–34. doi: 10.1007/s12011-016-0634-2.
  • Nunes, R., Pasko, P., Tyszka-Czochara, M., Szewczyk, A., Szlosarczyk, M., & Carvalho, I.S. (2017). Antibacterial, antioxidant and anti-proliferative properties and zinc content of five south Portugal herbs. Pharmaceutical Biology, 55, 114–123. doi: 10.1080/13880209.2016.1230636.
  • Omu, A.E., Al-Azemi, M.K., Al-Maghrebi, M., Mathew, C.T., Omu, F.E., Kehinde, E.O., … Memon, A. (2015). Molecular basis for the effects of zinc deficiency on spermatogenesis: An experimental study in the Sprague-dawley rat model. Indian J Urol, 31, 57–64. doi: 10.4103/0970-1591.139570.
  • Omu, A.E., Al-Azemi, M.K., Kehinde, E.O., Anim, J.T., Oriowo, M.A., & Mathew, T.C. (2008). Indications of the mechanisms involved in improved sperm parameters by zinc therapy. Medical Principles and Practice, 17, 108–116. doi: 10.1159/000112963.
  • Omu, A.E., Al-Bader, A.A., Dashti, H., & Oriowo, M.A. (2001). Magnesium in human semen: Possible role in premature ejaculation. Archives of Andrology, 46, 59–66. doi: 10.1080/01485010121440.
  • Omu, A.E., Al-Qattan, F., Al-Abdul-Hadi, F.M., Fatinikun, M.T., & Fernandes, S. (1999). Seminal immune response in infertile men with leukocytospermia: Effect on antioxidant activity. European Journal of Obstetrics, Gynecology and Reproductive Biology, 86, 195–202. doi: 10.1016/S0301-2115(99)00073-1.
  • Oteiza, P.I., Adonaylo, V.N., & Keen, C.L. (1999). Cadmium-induced testes oxidative damage in rats can be influenced by dietary zinc intake. Toxicology, 137, 13–22. doi: 10.1016/S0300-483X(99)00067-0.
  • Oteiza, P.I., Olin, K.L., Fraga, C.G., & Keen, C.L. (1995). Zinc deficiency causes oxidative damage to proteins, lipids and DNA in rat testes. The Journal of Nutrition, 125, 823–829. doi: 10.1093/jn/125.4.823.
  • Oztürk, A., Baltaci, A.K., Bediz, C.S., Mogulkoc, R., & Güngör, S. (2003). Effects of zinc and melatonin deficiency on testicular tissue of rats. Biological Trace Element Research, 96, 255–262. doi: 10.1385/BTER:96:1-3:255.
  • Pandy, V.K., Parmeshwaran, M., Soman, S.D., & Dacosta, J.C. (1983). Concentrations of morphologically normal, motile spermatozoa: Mg, Ca and Zn in the semen of infertile men. Science of the Total Environment, 27, 49–52. doi: 10.1016/0048-9697(83)90122-5.
  • Perry, D.K., Smyth, M.J., Stennicke, H.R., Salvesen, G.S., Duriez, P., Poirier, G.G., & Hannun, Y.A. (1997). Zinc is a potent inhibitor of the apoptotic protease, caspase-3. A novel target for zinc in the inhibition of apoptosis. Journal of Biological Chemistry, 272, 18530–18533. doi: 10.1074/jbc.272.30.18530.
  • Powell, S.R. (2000). The antioxidant properties of zinc. The Journal of Nutrition, 130, 1447S–1454S. doi: 10.1093/jn/130.5.1447S.
  • Prasad, A.S. (1991). Discovery of human zinc deficiency and studies in an experimental human model. The American Journal of Clinical Nutrition, 53, 403–412. doi: 10.1093/ajcn/53.2.403.
  • Prasad, A.S. (2003). Zinc deficiency. BMJ, 326, 409–410. doi: 10.1136/bmj.326.7386.409.
  • Rafique, M., Khan, N., Perveen, K., & Naqvi, A. (2009). The effects of lead and zinc on the quality of semen of albino rats. Journal of the College of Physicians and Surgeons-Pakistan, 19, 510–513. doi: 08.2009/JCPSP.510513.
  • Rahman, H.U., Qureshi, M.S., & Khan, R.U. (2014). Influence of dietary zinc on semen traits and seminal plasma antioxidant enzymes and trace minerals of Beetal bucks. Reproduction in Domestic Animals, 49, 1004–1007. doi: 10.1111/rda.12422.
  • Ruwanpura, S.M., McLachlan, R.I., & Meachem, S.J. (2010). Hormonal regulation of male germ cell development. Journal of Endocrinology, 205, 117–131. doi: 10.1677/JOE-10-0025.
  • Saeed, S., Khan, F.A., Rahman, S.B., Khan, D.A., & Ahmad, M. (1994). Biochemical parameters in evaluation of oligospermia. Journal of the Pakistan Medical Association, 44, 137–140. Retrieved from http://www.jpma.org.pk/full_article_text.php?article_id =4769.
  • Sanocka, D., Jędrzejczak, P., Szumała-Kaękol, A., Frączek, M., & Kurpisz, M. (2003). Male genital tract inflammation: The role of selected interleukins in regulation of pro-oxidant and antioxidant enzymatic substances in seminal plasma. Journal of Andrology, 24, 448–455. doi: 10.1002/j.1939-4640.2003.tb02693.x.
  • Sørensen, M.B., Stoltenberg, M., Henriksen, K., Ernst, E., Danscher, G., & Parvinen, M. (1998). Histochemical tracing of zinc ions in the rat testis. Molecular Human Reproduction, 4, 423–428. doi: 10.1093/molehr/4.5.423.
  • Supuran, C.T., Scozzafava, A., & Casini, A. (2003). Carbonic anhydrase inhibitors. Medicinal Research Reviews, 23, 146–189. doi: 10.1002/med.10025.
  • Tahmasbpour, E., Balasubramanian, D., & Agarwal, A. (2014). A multi-faceted approach to understanding male infertility: Gene mutations, molecular defects and assisted reproductive techniques (ART). Journal of Assisted Reproduction and Genetics, 31, 1115–1137. doi: 10.1007/s10815-014-0280-6.
  • Tahmasbpour, E., Ghanei, M., & Panahi, Y. (2016). Relationship of oxidative stress with male infertility in sulfur mustard-exposed injuries. Asian Pacific Journal of Reproduction, 5, 1–9. doi: 10.1016/j.apjr.2015.12.001.
  • Tahmasbpour, E., Reza Emami, S., Ghanei, M., & Panahi, Y. (2015). Role of oxidative stress in sulfur mustard-induced pulmonary injury and antioxidant protection. Inhalation Toxicology, 27, 659–672. doi: 10.3109/08958378.2015.1092184.
  • Talevi, R., Barbato, V., Fiorentino, I., Braun, S., Longobardi, S., & Gualtieri, R. (2013). Protective effects of in vitro treatment with zinc, d-aspartate and coenzyme q10 on human sperm motility, lipid peroxidation and DNA fragmentation. Reproductive Biology and Endocrinology, 11, 81. doi: 10.1186/1477-7827-11-81.
  • Truong-Tran, A.Q., Carter, J., Ruffin, R.E., & Zalewski, P.D. (2001). The role of zinc in caspase activation and apoptotic cell death. Biometals, 14, 315–330. doi: 10.1023/A:1012993017026.
  • Villanueva, O., Vigueras, R.M., Hernandez, R., Chavira, R., Cardenas, M., Villa, A., & Murphy, E. (2005). Zinc-induced survival of Leydig cells in Fischer rats (Rattus norvegicus) treated with cadmium chloride. Comparative Medicine, 55, 533–538. Retrieved from http://www.ingentaconnect.com/content/aalas/cm/2005/00000055/00000006/art00008;jsessionid =5525ojt2mtani.x-ic-live-02.
  • Wandernoth, P.M., Raubuch, M., Mannowetz, N., Becker, H.M., Deitmer, J.W., Sly, W.S., & Wennemuth, G. (2010). Role of carbonic anhydrase IV in the bicarbonate-mediated activation of murine and human sperm. PLoS One, 5, e15061. doi: 10.1371/journal.pone.0015061.
  • Wang, X., Sharma, R.K., Sikka, S.C., Thomas, A.J., Jr., Falcone, T., & Agarwal, A. (2003). Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility. Fertility and Sterility, 80, 531–535. doi: 10.1016/S0015-0282(03)00756-8.
  • Wei, S., Zhang, L., Zhou, X., Du, M., Jiang, Z., Hausman, G.J., … Dodson, M.V. (2013). Emerging roles of zinc finger proteins in regulating adipogenesis. Cellular and Molecular Life Sciences, 70, 4569–4584. doi: 10.1007/s00018-013-1395-0.
  • Weissig, H., Narisawa, S., Sikström, C., Olsson, P.G., McCarrey, J.R., A. Tsonis, P., … Millán, J.L. (2003). Three novel spermatogenesis-specific zinc finger genes. FEBS Letters, 547, 61–68. doi: 10.1016/S0014-5793(03)00669-0.
  • Wuehler, S.E., Peerson, J.M., & Brown, K.H. (2005). Use of national food balance data to estimate the adequacy of zinc in national food supplies: Methodology and regional estimates. Public Health Nutrition, 8, 812–819. doi: 10.1079/PHN2005724.
  • Yamaguchi, S., Miura, C., Kikuchi, K., Celino, F.T., Agusa, T., Tanabe, S., & Miura, T. (2009). Zinc is an essential trace element for spermatogenesis. Proceedings of the National Academy of Sciences USA, 106, 10859–10864. doi: 10.1073/pnas.0900602106.
  • You, X., Wei, L., Fan, S., Yang, W., Liu, X., Wang, G., … Feng, W. (2017). Expression pattern of Zinc finger protein 185 in mouse testis and its role in regulation of testosterone secretion. Molecular Medicine Reports, 16, 2101–2106. doi: 10.3892/mmr.2017.6797.
  • Zago, M.P., & Oteiza, P.I. (2001). The antioxidant properties of zinc: Interactions with iron and antioxidants. Free Radical Biology and Medicine, 31, 266–274. doi: 10.1016/S0891-5849(01)00583-4.
  • Zhao, J., Dong, X., Hu, X., Long, Z., Wang, L., Liu, Q., … Li, L. (2016). Zinc levels in seminal plasma and their correlation with male infertility: A systematic review and meta-analysis. Scientific Reports, 6, 22386. doi: 10.1038/srep22386.
  • Zhao, R.P., & Xiong, C.L. (2005). Zinc content analysis in serum, seminal plasma and spermatozoa of asthenozoospermic and oligoasthenozoospermic patients. Zhonghua Nan Ke Xue, 11, 680–682. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/16209210.

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