1,011
Views
21
CrossRef citations to date
0
Altmetric
RESEARCH ARTICLE

Testicular apoptosis after dietary zinc deficiency: Ultrastructural and TUNEL studies

, &
Pages 233-243 | Received 30 Jul 2010, Accepted 05 Mar 2011, Published online: 07 Jun 2011

References

  • Adamo, A.M., Oteiza and P.I. (2010) Zinc deficiency and neurodevelopment: The case of neurons. Biofactors 36:117–124.
  • Aitken, R.J., Harkiss, D. and Buckingham, D.W. (1993) Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol Reprod Dev 35:302–315.
  • Ali, H., Ahmed, M., Baig, M. and Ali, M. (2007) Relationship of zinc concentrations in blood and seminal plasma with various semen parameters in infertile subjects. Pak J Med Sci 23:111–114.
  • Al-Timimi, D.J. (2009) Marginal zinc deficiency: A significant but unrecognized public health problem in Iraq. Duhok Med J 3:1–3.
  • Auld, D.S. (2009) The ins and outs of biological zinc sites. Biometals 22:141–148.
  • Bahuguna, A. and Bedwal, R.S. (1998) Effects of zinc deficiency on boundary layers of seminiferous tubules of testes of Wistar rats. Curr Sci 75:611–616.
  • Barney, G.H., Orgebin-Crist, M.C. and Macapinalac, M.P. (1968) Genesis of esophageal parakeratosis and histologic changes in the testes of the zinc-deficient rat and their reversal by zinc repletion. J Nutr 95:526–534.
  • Bedwal, R.S., Nair, N. and Mathur, R.S. (1991) Effects of zinc deficiency and toxicity on reproductive organs, pregnancy and lactation - A review. Trace Elem Med 8:89–100.
  • Bedwal, R.S. and Bahuguna, A. (1994) Zinc, Copper and Selenium in reproduction. Experientia 50:626–640.
  • Billig, H., Furuta, I., Rivier, C., Tapanainen, J., Parvinen, M. and Hsueh, A.J. (1995) Apoptosis in testis germ cells: Developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 136:5–12.
  • Björndahl, L. and Kvist, U. (2010) Human sperm chromatin stabilization: A proposed model including zinc bridges. Mol Human Reprod 16:23–29.
  • Björndahl, L. and Kvist, U. (2011) A model for the importance of zinc in the dynamics of human sperm chromatin stabilization after ejaculation in relation to sperm DNA vulnerability. Syst Biol Reprod Med 57(1–2):86–92. http://www.ncbi.nlm.nih.gov/pubmed/21204594
  • Chai, F., Truong-Tran, A.Q., Ho, L.H. and Zalewski, P.D. (1999) Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: A review. Immunol Cell Biol 77:272–278.
  • Clarke, P.R. and Allan, L.A. (2009) Cell-cycle control in the face of damage - A matter of life and death. Trends Cell Biol 579:1–10.
  • Dandekar, S.P, Nadkarni, G.D, Kulkarni, V.S., Pnekar, S. (2002) Lipid peroxidation and antioxidant enzymes in male infertility. J Postgrad Med 48:186–189.
  • Dinsdale, D. and Williams, R.B. (1980) Ultrastructural changes in the sperm tail of zinc deficient rats. J Comp Pathol 90:559–566.
  • Dirami, G., Ravindranath, N., Kleinman, H.K. and Dym, M. (1995) Evidence that basement membrane prevents apoptosis of Sertoli cells in vitro in the absence of known regulators of Sertoli function. Endocrinology 135:4439–4447.
  • Dissanayake, D.M.A.B., Wijesinghe, P.S., Ratnasooriya, W.D., Wimalasena, S. (2009) Effects of zinc supplementation on sexual behavior of male rats. J Human Reprod Sci 2:57–61.
  • Duffy, J.Y., Miller, C.M., Rutschilling, G.L., Ridder, G.M., Clegg, M.S., Keen, C.L. and Daston, G.P. (2001) A decrease in intracellular zinc level precedes the detection of early indicators of apoptosis in HL-60 cells. Apoptosis 6:161–172.
  • Dym, M. and Fawcett, D.W. (1970) The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3:308–326.
  • Ebisch, I.M.W., Thomas, C.M.G., Peters, W.H.M., Bract, D.D.M. Steegers-Theunissen, R.P.M. (2007) The importance of folate, zinc and antioxidants in the pathogenesis and prevention of sub-fertility. Human Reprod Update 13:163–174.
  • Erkkilä, K., Henriksen, K., Hirvonen, V., Rannikko, S., Salo, J., Parvinen, M. and Dunkel, L. (1997) Testosterone regulates apoptosis in adult human seminiferous tubules in vitro. J Clin Endocrinol Metab 82:2314–2321.
  • Erkkilä, K., Hirvonen, V., Wuokko, E., Parvinen, M. and Dunkel, L. (1998) N-Acetyl-L-Cysteine inhibits apoptosis in human male germ cells in vitro. J Clin Endocrinol Metab 83:2523–2531.
  • Fanzo, J.C., Reaves, S.K., Cui, L., Zhu, L., Wu, J.J.Y., Wang, Y.R. and Lei, K.Y. (2001) Zinc status affects pp53, gadd45, and c-fos expression and caspase-3 activity in human bronchial epithelial cells. Am J Physiol Cell Physiol 281:C751–C757.
  • Fesharakinia, A., Zarban, A. and Sharifzadeh, G.R. (2009) Prevalence of zinc deficiency in elementary school children of South Khorasan province East Iran. Iran J Pediatr 19:249–254.
  • Fimia, G.M., De Cesau, D., Sassone-Corsi, P. (1999) CBP-independent activation of CREM and CREB by the LIM only protein ACT. Nature 398:165–169.
  • Fraker, P.J. (2005) Roles for cell death in zinc deficiency. J Nutr 135:359–362.
  • Frisch, S.M. and Francis, H. (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124:619–626.
  • Fukamachi, Y., Karaski, Y., Sugiura, T., Itoh, H., Abe, T., Yamamura, K. and Higashi, K. (1998) Zinc suppresses apoptosis of U937 cells induced by Bcl2/ Bax ratio. Biochem Biophys Res Comm 246:364–369.
  • Giannakis, C., Forbes, I.J. and Zalewski, P.D. (1991) Ca2+/Mg2+ dependent nuclease, tissue distribution, relationship to inter-nucleosomal DNA fragmentation and inhibition by Zn2+. Biochem Biophys Res Commun 181:915–920.
  • Hassan, A., El-Nashar, E.M. and Mostafa, I. (2009) Programmed cell death in varicocele-bearing testes. Andrologia 41:39–45.
  • Henkel, R., Bittner, J., Weber, R., Hüther, F., Miska, W. (1999) Relevance of zinc in human sperm flagella and its relation to motility. Fertil Steril 71:1138–1143.
  • Henriksen, K., Hakovirta, H. and Parvinen, M. (1995) In situ quantification of stage-specific apoptosis in the rat seminiferous epithelium: Effects of short-term experimental cryptorchidism. Internat J Androl 17:394–402.
  • Hesketh, J.E. (1982) Zinc stimulated microtubule assembly and evidence for zinc binding to tubulin. Internat J Biochem 14:983–990.
  • Hesketh, J.E. (1984) Microtubule assembly in rat brain extracts: Further characterization of the effects of zinc on assembly and cold stability. Internat J Biochem 16:1331–1339.
  • Hess, S.Y. and King, J.C. (2009) Effects of maternal zinc supplementation on pregnancy and lactation outcomes. Food Nutr Bull 30:S60–S78.
  • Ho, E., Ames, B.N. (2002) Low intracellular zinc induces oxidative DNA damage, disrupts pp53, NFκB and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc Natl Acad Sci USA 99:16770–16775.
  • Ho, E., Courtemanche, C. and Ames, B.N. (2003) Zinc deficiency induces oxidative DNA damage and increases pp53 expression in human lung fibroblasts. J Nutr 133:2543–2548.
  • Hunt, C.D. and Johnson, P.E. (1990) The effects of dietary zinc on human sperm morphology and seminal mineral loss. In: Trace Element Metabolism in Man and Animals-7. eds Hurley L.S., Keen, C.L., Lonnerdal, B. Rucker, R.B. Plenum Press, New York pp35–42.
  • Jankowski-Hennig, M.A., Clegg, M.S., Daston, G.P., Rogers, J.M., Keen, C.L. (2000) Zinc-deficient rat embryos have increased caspase 3–like activity and apoptosis. Biochem Biophys Res Commun 271:250–256.
  • Kaji, M. (2001) Zinc in endocrinology. Internat Pediatr 16:1–7.
  • Kerr, J.F.R., Wyllie, A.H. and Currie, A.R. (1972) Apoptosis: Basic biological phenomenon with wide range of implications in tissue kinetics. British J Canc 26:239–257.
  • Kimura, M., Itoh, N., Takagi, S., Sasao, T., Takahashi, A., Masumori, N. and Tsukamoto, T. (2003) Balance of apoptosis and proliferation of germ cells related to spermatogenesis in aged men. J Androl 24:185–191.
  • Kvist, U., Kjelberg, S., Björndahl, L., Hammar, M., Roomans, G. (1988) Zinc in sperm chromatin and chromatin stability in fertile men and men in barren unions. Scand. J Urol Nephrol 22:1–6.
  • Li, J., Xu, P. and He, Z. (1998) Effect of zinc deficiency on apoptosis of spermatogenic cell of rat testis. Zhonghua Yi Xue Za Zhi 78:91–103.
  • Linder, R.E., Strader, L.F. and McElroy, W.K. (1986) Measurement of epididymal sperm motility as a test variable in the rat. Bull Env Contamin Toxicol 36:317–324.
  • Maret, W. (2009) Molecular aspects of human cellular zinc homeostasis: Redox control of zinc potentials and zinc signals. Biometals 22:149–157.
  • Maret, W. and Sandstead, H. (2008) Possible roles of zinc nutriture in the fetal origins of disease. Exptl Gerontology 43:378–381.
  • Merker, H.J. and Günther, T. (1997) Testis damage induced by zinc deficiency in rats. pJ Trace Elem Med Biol 11:19–22.
  • Merrells, K.J., Blewett, H., Jaamieson, J.A., Taylor, C.G. and Suh, M. (2009) Relationship between abnormal sperm physiology induced by dietary zinc deficiency and lipid composition in testes of growing rats. British J Nutr 102:226–232.
  • Nair, N., Bedwal, R.S., Prasad, S., Saini,.M.R., Bedwal, R.S. (2005) Short term zinc deficiency in diet induces increased oxidative stress in testes and epididymis of rats.. Indian J Expt Biol 43:786–794.
  • Nantel, F., Monaco, L., Foulkes, N.S., Masquilier, D., LeMeur, M., Henriksen, K., (1996) Spermiogenesis deficiency and germ cell apoptosis in CREM-mutant mice. Nature 380:159–162.
  • Nodera, M., Yanagisawa, H., Wada, O. (2001) Increased apoptosis in a variety of tissues of zinc deficient rats. Life Sci 14:1639–1649.
  • Omu, A.E., Al-Azemi, M.K., Kehinde, E.O., Anim, J.T, Oriowa, M.A., Mathew, T.C. (2008) Indications of the mechanisms involved in improved sperm parameters by zinc therapy. Med Prin Prac 17:108–116.
  • Palermo, I., Litrico, L., Emmanuele, G., Giuffrida, V., Sassone-Corsi, P., De Cesare, D., (2001) Cloning and expression of activator of CREM in testis in human testicular tissue. Biochem Biophys Res Commun 283:406–411.
  • Pentikäinen, V., Erkkilä, K., Dunkel, L. (1999) Fas regulate germ cell apoptosis in the human testis in vitro. Am J Physiol 276: E310–E316.
  • Rao, L., Perez, D. and White, E. (1996) Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 135:1441–1455.
  • Russell, L.D. (1979) Spermatid Sertoli tubulobulbar complexes as devices for elimination of cytoplasm from the head region of late spermatids of the rat. Anat Rec 194:233–246.
  • Saleh, R. and Agarwal, A. (2002) Oxidative stress and male infertility: From research bench to clinical practice. J Androl 23:737–752.
  • Saraste, A., Pulkki, K. (2000) Morphological and biochemical hallmarks of apoptosis. Cardiovasc Res 45:528–537.
  • Sassone-Corsi, P. (1998) CREM: a master-switch governing male germ cell differentiation and apoptosis. Sem Dev Biol 9:475–482.
  • Saxena, R., Bedwal, R., Mathur, R.S. (1993) Histopathology of epididymis and prostate of zinc deficient Sprague Dawley rats. Trace Elem Med 10:55–59.
  • Shamsi, M.B., Kumar, R. and Dada, R. (2008) Evaluation of nuclear DNA damage in human spermatozoa in men opting for assisted reproduction. Indian J Med Res 127:115–123.
  • Sluka, P., O'Donnell, L., Bartles, J.R., Stanton and P.G. (2006) FSH regulates the formation of adherens junctions and ectoplasmic specialisations between rat Sertoli cells in vitro and in vivo. J Endocrinol 189:381–395.
  • Song, Y., Leonard, S.W., Bruno, R.S., Traber, M.G. and Ho, E. (2009) Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J Nutr 139:1626–1631.
  • Sorensen, M.B., Stoltenberg, M., Henriksen, K., Ernst, E., Dansher, G. and Parvinen, M. (1998) Histochemical tracing of zinc ions in the rat testis. Mol Human Rep 4:423–428.
  • Stennicke, H.R., Salvesen, G.S. (1997) Biochemical characteristics of caspase-3, -6, -7 and -8. J Biol Chem 272:25719–25723.
  • Takagi, S., Itoh, N., Kimura, M., Sasao, T. and Tsukamato, T. (2001) Spermatogonial proliferation and apoptosis in hypospermatogenesis associated with non-obstructive azoospermia. Fertil Steril 76:901–907.
  • Takahashi, A., Alnemri, E.S., Lazebnik, Y.A., Fernandes-Alnemri, T., Litwack, G., Moir, R.D., (1996) Cleavage of lamin A by mch 2α but not CPP32: multiple interleukin 1β-converting enzymes related proteases with distinct substrate recognition properties are active in apoptosis. Proc Natl Acad Sci USA 93:8395–8400.
  • Tramer, F., Rocco, F., Micali, F., Sandri, G. and Panfili, E. (1998) Antioxidant systems in rat epididymal spermatozoa. Biol Reprod 59:753–758
  • Tuerk, M.J. and Fazel, N. (2009) Zinc deficiency. Curr Opin Gastroenterol 25:136–143
  • Uriu-Adams, J.Y. and Keen, C.L. (2010) Zinc and reproduction: Effects of zinc deficiency on prenatal and early postnatal development. Birth Defects Res 89:313–325.
  • Ventelä, S., Toppari, J. and Parvinen, M. (2003) Intercellular organelle traffic through cytoplasmic bridges in early spermatids of the rat: Mechanisms of haploid gene product sharing. Mol Biol Cell 14:2768–2780.
  • Walingo, M.K. (2009) Indigenous food processing methods that improve zinc absorption and bioavailability of plant diets consumed by the Kenyan population. African J Food Agri Nut Dev 9:524–535.
  • Wallace, E., Calvin, H.I., Salgo, M.P., Dennis, D.E. and Ploetz, K. (1984) Normal levels of zinc and sulphydryls in morphologically abnormal populations of spermatozoa from moderately zinc deficient rats. Gamete Research 9:375–386.
  • Widlak, P., Palyvoda, O., Kumala, S. and Gerrard, W.T. (2002) Modeling apoptotic chromatin condensation in normal cell nuclei. J Biol Chem 277:21683–21690.
  • Wolf, C.M., Morana, S.J. and Eastman, A. (1997) Zinc inhibits apoptosis upstream of ICE/CED-3 protease rather than at the level of an endonuclease. Cell Death Differ. 4:125–129
  • Yan, M., Song, Y., Wong, C.P., Hardin, K. and Ho, E. (2008) Zinc deficiency alters DNA damage response genes in normal human prostate epithelial cells. J Nutr 138:667–673.
  • Zalata, A.A., Ahmed, A.H., Allamaneni, S.S., Comhaire, F.H. and Agarwal, A. (2004) Relationship between acrosin activity of human spermatozoa and oxidative stress. Asian J Androl 6:313–318.
  • Zalewski, P., Forbes, I., Giannakis, C. and Betts, W. (1991) Regulation of protein kinase C by Zn (2+)-dependent interaction with actin. Biochem Int 24:1103–1110.
  • Zhivotovsky, B., Wade, D., Gahm, A., Orrenius, S. and Nicotera, P. (1994) Formation of 50 kbp chromatin fragments in isolated liver nuclei is mediated by protease and endonuclease activation. FEBS Lett 351:150–154.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.