Testicular apoptosis after dietary zinc deficiency: Ultrastructural and TUNEL studies

Systems Biology in Reproductive Medicine

Volumn 57, Issue 5, 2011, Pages 233-243

  Kumari, Deepa ^a   Nair, Neena ^a   Bedwal, Ranveer Singh ^a  

^a UNIVERSITY OF RAJASTHAN   (India)

Author keywords

Apoptosis; Male fertility; Spermatogenesis; Testes; Zinc deficiency

Indexed keywords

ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; CELL JUNCTION; CELL LOSS; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOPLASM; DECAPITATION; EPIDIDYMIS; GERM CELL; MALE; MALE FERTILITY; MITOCHONDRION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RAT; SERTOLI CELL; SPERMATOGENESIS; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; TESTIS; ULTRASTRUCTURE; WISTAR RAT; ZINC DEFICIENCY;

APOPTOSIS; DEFICIENCY DISEASES; DIET; HUMANS; IN SITU NICK-END LABELING; MALE; MICROSCOPY, ELECTRON; TESTIS; ZINC;

EID: 80053375052     PISSN: 19396368     EISSN: 19396368     Source Type: Journal    
DOI: 10.3109/19396368.2011.584500     Document Type: Article

References (81)

1. Adamo, A.M., Oteiza and P.I. (2010) Zinc deficiency and neurodevelopment: The case of neurons. Biofactors 36:117-124.
2. Aitken, R.J., Harkiss, D. and Buckingham, D.W. (1993) Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol Reprod Dev 35:302-315. (Pubitemid 23207487)
3. 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. (Pubitemid 46409592)
4. Al-Timimi, D.J. (2009) Marginal zinc deficiency: A significant but unrecognized public health problem in Iraq. Duhok Med J 3:1-3.
5. Auld, D.S. (2009) The ins and outs of biological zinc sites. Biometals 22:141-148.
6. 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.
7. 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.
8. 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.
9. Bedwal, R.S. and Bahuguna, A. (1994) Zinc, Copper and Selenium in reproduction. Experientia 50:626-640.
10. 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.
11. Björndahl, L. and Kvist, U. (2010) Human sperm chromatin stabilization: A proposed model including zinc bridges. Mol Human Reprod 16:23-29.
12. 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
13. 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. (Pubitemid 29251581)
14. 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.
15. 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. (Pubitemid 35386075)
16. Dinsdale, D. and Williams, R.B. (1980) Ultrastructural changes in the sperm tail of zinc deficient rats. J Comp Pathol 90:559-566. (Pubitemid 11202152)
17. 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.
18. 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.
19. 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. (Pubitemid 32423725)
20. 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.
21. 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. (Pubitemid 46323193)
22. 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. (Pubitemid 27287606)
23. 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. (Pubitemid 28503057)
24. 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.
25. 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.
26. 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.
27. Fraker, P.J. (2005) Roles for cell death in zinc deficiency. J Nutr 135:359-362. (Pubitemid 40365188)
28. Frisch, S.M. and Francis, H. (1994) Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124:619-626. (Pubitemid 24064472)
29. 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.
30. 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.
31. Hassan, A., El-Nashar, E.M. and Mostafa, I. (2009) Programmed cell death in varicocele-bearing testes. Andrologia 41:39-45.
32. 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. (Pubitemid 29252510)
33. 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. (Pubitemid 26339748)
34. Hesketh, J.E. (1982) Zinc stimulated microtubule assembly and evidence for zinc binding to tubulin. Internat J Biochem 14:983-990. (Pubitemid 13210468)
35. 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. (Pubitemid 15102645)
36. Hess, S.Y. and King, J.C. (2009) Effects of maternal zinc supplementation on pregnancy and lactation outcomes. Food Nutr Bull 30: S60-S78.
37. Ho, E., Ames, B.N. (2002) Low intracellular zinc induces oxidative DNA damage, disrupts pp53, NF?B and AP1 DNA binding, and affects DNA repair in a rat glioma cell line. Proc Natl Acad Sci USA 99:16770-16775. (Pubitemid 36034048)
38. 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. (Pubitemid 36935967)
39. 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 pp. 35-42.
40. 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. (Pubitemid 30444886)
41. Kaji, M. (2001) Zinc in endocrinology. Internat Pediatr 16:1-7.
42. 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.
43. 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.
44. 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. (Pubitemid 18092625)
45. 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.
46. 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. (Pubitemid 16125768)
47. Maret,W. (2009) Molecular aspects of human cellular zinc homeostasis: Redox control of zinc potentials and zinc signals. Biometals 22:149-157.
48. Maret, W. and Sandstead, H. (2008) Possible roles of zinc nutriture in the fetal origins of disease. Exptl Gerontology 43:378-381. (Pubitemid 351522405)
49. Merker, H.J. and Günther, T. (1997) Testis damage induced by zinc deficiency in rats. pJ Trace Elem Med Biol 11:19-22. (Pubitemid 27199406)
50. 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.
51. 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. (Pubitemid 41277281)
52. Nantel, F., Monaco, L., Foulkes, N.S., Masquilier, D., LeMeur, M., Henriksen, K., et al. (1996) Spermiogenesis deficiency and germ cell apoptosis in CREM-mutant mice. Nature 380:159-162. (Pubitemid 26085881)
53. Nodera, M., Yanagisawa, H.,Wada, O. (2001) Increased apoptosis in a variety of tissues of zinc deficient rats. Life Sci 14:1639-1649. (Pubitemid 32800643)
54. 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. (Pubitemid 351301295)
55. Palermo, I., Litrico, L., Emmanuele, G., Giuffrida, V., Sassone-Corsi, P., De Cesare, D., et al. (2001) Cloning and expression of activator of CREM in testis in human testicular tissue. Biochem Biophys Res Commun 283:406-411. (Pubitemid 32924706)
56. Pentikäinen, V., Erkkilä, K., Dunkel, L. (1999) Fas regulate germ cell apoptosis in the human testis in vitro. Am J Physiol 276: E310-E316. (Pubitemid 29100587)
57. Rao, L., Perez, D. and White, E. (1996) Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 135:1441-1455. (Pubitemid 26427643)
58. 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. (Pubitemid 9172805)
59. Saleh, R. and Agarwal, A. (2002) Oxidative stress and male infertility: From research bench to clinical practice. J Androl 23:737-752. (Pubitemid 36300961)
60. Saraste, A., Pulkki, K. (2000) Morphological and biochemical hallmarks of apoptosis. Cardiovasc Res 45:528-537.
61. Sassone-Corsi, P. (1998) CREM: a master-switch governing male germ cell differentiation and apoptosis. Sem Dev Biol 9:475-482. (Pubitemid 128350675)
62. 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. (Pubitemid 23148216)
63. 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. (Pubitemid 351936161)
64. 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.
65. 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.
66. 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. (Pubitemid 28253202)
67. Stennicke, H.R., Salvesen, G.S. (1997) Biochemical characteristics of caspase-3, -6, -7 and -8. J Biol Chem 272:25719-25723.
68. Takagi, S., Itoh, N.,Kimura,M., Sasao,T. andTsukamato, T. (2001) Spermatogonial proliferation and apoptosis in hypospermatogenesis associated with non-obstructive azoospermia. Fertil Steril 76:901-907. (Pubitemid 33031313)
69. Takahashi, A., Alnemri, E.S., Lazebnik, Y.A., Fernandes-Alnemri, T., Litwack, G., Moir, R.D., et al. (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.
70. Tramer, F., Rocco, F., Micali, F., Sandri, G. and Panfili, E. (1998) Antioxidant systems in rat epididymal spermatozoa. Biol Reprod 59:753-758 (Pubitemid 28463324)
71. Tuerk, M.J. and Fazel, N. (2009) Zinc deficiency. Curr Opin Gastroenterol 25:136-143
72. 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.
73. 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. (Pubitemid 36871520)
74. 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.
75. 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. (Pubitemid 14050904)
76. 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.
77. 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 (Pubitemid 27064878)
78. 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. (Pubitemid 351469407)
79. 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. (Pubitemid 39654597)
80. 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.
81. 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. (Pubitemid 24277258)