Exacerbation of diabetes-induced testicular apoptosis by zinc deficiency is most likely associated with oxidative stress, p38 MAPK activation, and p53 activation in mice

Toxicology Letters

Volumn 200, Issue 1-2, 2011, Pages 100-106

  Zhao, Yuguang ^a,b   Tan, Yi ^b,c   Dai, Junying ^d   Li, Bing ^b,e   Guo, Luping ^c   Cui, Jiuwei ^c   Wang, Guanjun ^a   Shi, Xue ^f   Zhang, Xiang ^f   Mellen, Nicholas ^b   Li, Wei ^a   Cai, Lu ^a,b,c  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

^c WENZHOU MEDICAL UNIVERSITY   (China)

^d Liver and Gall Disease Hospital of Jilin Province   (China)

^e THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^f UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Apoptosis; Diabetes; Mitochondrial damage; Nrf 2; Oxidative stress; Testis; Zinc deficiency

Indexed keywords

ETHYLENEDIAMINE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE P38; N,N,N'N' TETRAKIS(2 PYRIDYLEMETHYL)ETHYLENEDIAMINE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHELATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE EXACERBATION; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; MALE; MOUSE; NICK END LABELING; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOZOCIN DIABETES; TESTIS DISEASE; ZINC DEFICIENCY;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; ENZYME ACTIVATION; ETHYLENEDIAMINES; MALE; MICE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; TESTIS; TUMOR SUPPRESSOR PROTEIN P53; ZINC;

MUS;

EID: 78650177805     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2010.11.001     Document Type: Article

References (42)

1. Agbaje I.M., Rogers D.A., McVicar C.M., McClure N., Atkinson A.B., Mallidis C., Lewis S.E. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum. Reprod. 2007, 22:1871-1877.
2. Amara S., Abdelmelek H., Garrel C., Guiraud P., Douki T., Ravanat J.L., Favier A., Sakly M., Ben Rhouma K. Preventive effect of zinc against cadmium-induced oxidative stress in the rat testis. J. Reprod. Dev. 2008, 54:129-134.
3. Amaral S., Mota P.C., Lacerda B., Alves M., Pereira Mde L., Oliveira P.J., Ramalho-Santos J. Testicular mitochondrial alterations in untreated streptozotocin-induced diabetic rats. Mitochondrion 2009, 9:41-50.
4. Amaral S., Oliveira P.J., Ramalho-Santos J. Diabetes and the impairment of reproductive function: possible role of mitochondria and reactive oxygen species. Curr. Diabetes Rev. 2008, 4:46-54.
5. Cai L., Chen S., Evans T., Cherian M.G., Chakrabarti S. Endothelin-1-mediated alteration of metallothionein and trace metals in the liver and kidneys of chronically diabetic rats. Int. J. Exp. Diabetes Res. 2002, 3:193-198.
6. Cai L., Chen S., Evans T., Deng D.X., Mukherjee K., Chakrabarti S. Apoptotic germ-cell death and testicular damage in experimental diabetes: prevention by endothelin antagonism. Urol. Res. 2000, 28:342-347.
7. Cai L., Li W., Wang G., Guo L., Jiang Y., Kang Y.J. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 2002, 51:1938-1948.
8. Corniola R.S., Tassabehji N.M., Hare J., Sharma G., Levenson C.W. Zinc deficiency impairs neuronal precursor cell proliferation and induces apoptosis via p53-mediated mechanisms. Brain Res. 2008, 1237:52-61.
9. Dahlquist G., Kallen B. Mortality in childhood-onset type 1 diabetes: a population-based study. Diabetes Care 2005, 28:2384-2387.
10. Erster S., Mihara M., Kim R.H., Petrenko O., Moll U.M. In vivo mitochondrial p53 translocation triggers a rapid first wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol. Cell Biol. 2004, 24:6728-6741.
11. Erster S., Moll U.M. Stress-induced p53 runs a direct mitochondrial death program: its role in physiologic and pathophysiologic stress responses in vivo. Cell Cycle 2004, 3:1492-1495.
12. Ha K.N., Chen Y., Cai J., Sternberg P. Increased glutathione synthesis through an ARE-Nrf2-dependent pathway by zinc in the RPE: implication for protection against oxidative stress. Invest. Ophthalmol. Vis. Sci. 2006, 47:2709-2715.
13. He X., Kan H., Cai L., Ma Q. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J. Mol. Cell Cardiol. 2009, 46:47-58.
14. Ho E., Courtemanche C., Ames B.N. Zinc deficiency induces oxidative DNA damage and increases p53 expression in human lung fibroblasts. J. Nutr. 2003, 133:2543-2548.
15. Kabu K., Yamasaki S., Kamimura D., Ito Y., Hasegawa A., Sato E., Kitamura H., Nishida K., Hirano T. Zinc is required for Fc epsilon RI-mediated mast cell activation. J. Immunol. 2006, 177:1296-1305.
16. Kim H.J., Vaziri N.D. Contribution of impaired Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure. Am. J. Physiol. Renal Physiol. 2010, 298:F662-671.
17. Koh P.O. Streptozotocin-induced diabetes increases the interaction of Bad/Bcl-XL and decreases the binding of pBad/14-3-3 in rat testis. Life Sci. 2007, 81:1079-1084.
18. Lee J.M., Johnson J.A. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J. Biochem. Mol. Biol. 2004, 37:139-143.
19. Lee J.S., Surh Y.J. Nrf2 as a novel molecular target for chemoprevention. Cancer Lett. 2005, 224:171-184.
20. Li G.Y., Xie P., Li H.Y., Hao L., Xiong Q., Qiu T. Involment of p53, Bax, and Bcl-2 pathway in microcystins-induced apoptosis in rat testis. Environ. Toxicol. 2009.
21. Liu G., Gong P., Bernstein L.R., Bi Y., Gong S., Cai L. Apoptotic cell death induced by low-dose radiation in male germ cells: hormesis and adaptation. Crit. Rev. Toxicol. 2007, 37:587-605.
22. Liu H., Pedram A., Kim J.K. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38{alpha}-mediated activation of p53 and by down-regulating p53 inhibition on p38{beta}. Cardiovasc. Res. 2010, September 30 [Epub ahead of print] PubMed PMID: 20724307.
23. Mayer-Davis E.J., Beyer J., Bell R.A., Dabelea D., D'Agostino R., Imperatore G., Lawrence J.M., Liese A.D., Liu L., Marcovina S., Rodriguez B. Diabetes in African American youth: prevalence, incidence, and clinical characteristics: the SEARCH for Diabetes in Youth Study. Diabetes Care 2009, 32(Suppl. (2)):S112-122.
24. Nakamura B.N., Lawson G., Chan J.Y., Banuelos J., Cortes M.M., Hoang Y.D., Ortiz L., Rau B.A., Luderer U. Knockout of the transcription factor NRF2 disrupts spermatogenesis in an age-dependent manner. Free Radic. Biol. Med. 2010, 49:1368-1379.
25. Ning J.L., Mo L.W., Lai X.N. Low- and high-dose hydrogen peroxide regulation of transcription factor NF-E2-related factor 2. Chin. Med. J. (Engl.) 2010, 123:1063-1069.
26. Oteiza P.L., Olin K.L., Fraga C.G., Keen C.L. Oxidant defense systems in testes from zinc-deficient rats. Proc. Soc. Exp. Biol. Med. 1996, 213:85-91.
27. Ozturk A., Baltaci A.K., Mogulkoc R., Oztekin E. Zinc prevention of electromagnetically induced damage to rat testicle and kidney tissues. Biol. Trace Elem. Res. 2003, 96:247-254.
28. Papoutsaki M., Moretti F., Lanza M., Marinari B., Sartorelli V., Guerrini L., Chimenti S., Levrero M., Costanzo A. A p38-dependent pathway regulates DeltaNp63 DNA binding to p53-dependent promoters in UV-induced apoptosis of keratinocytes. Oncogene 2005, 24:6970-6975.
29. Ranawat P., Bansal M.P. Apoptosis induced by modulation in selenium status involves p38 MAPK and ROS: implications in spermatogenesis. Mol. Cell Biochem. 2009, 330:83-95.
30. Rotter V., Schwartz D., Almon E., Goldfinger N., Kapon A., Meshorer A., Donehower L.A., Levine A.J. Mice with reduced levels of p53 protein exhibit the testicular giant-cell degenerative syndrome. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:9075-9079.
31. Sainio-Pollanen S., Henriksen K., Parvinen M., Simell O., Pollanen P. Stage-specific degeneration of germ cells in the seminiferous tubules of non-obese diabetic mice. Int. J. Androl. 1997, 20:243-253.
32. Sandstead H.H., Prasad A.S., Penland J.G., Beck F.W., Kaplan J., Egger N.G., Alcock N.W., Carroll R.M., Ramanujam V.M., Dayal H.H., Rocco C.D., Plotkin R.A., Zavaleta A.N. Zinc deficiency in Mexican American children: influence of zinc and other micronutrients on T cells, cytokines, and antiinflammatory plasma proteins. Am. J. Clin. Nutr. 2008, 88:1067-1073.
33. Schneider J.M., Fujii M.L., Lamp C.L., Lonnerdal B., Zidenberg-Cherr S. The prevalence of low serum zinc and copper levels and dietary habits associated with serum zinc and copper in 12- to 36-month-old children from low-income families at risk for iron deficiency. J. Am. Diet. Assoc. 2007, 107:1924-1929.
34. Song Y., Leonard S.W., Traber M.G., Ho E. Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J. Nutr. 2009, 139:1626-1631.
35. Suzuki M., Betsuyaku T., Ito Y., Nagai K., Nasuhara Y., Kaga K., Kondo S., Nishimura M. Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 2008, 39:673-682.
36. Vera Y., Erkkila K., Wang C., Nunez C., Kyttanen S., Lue Y., Dunkel L., Swerdloff R.S., Sinha Hikim A.P. Involvement of p38 mitogen-activated protein kinase and inducible nitric oxide synthase in apoptotic signaling of murine and human male germ cells after hormone deprivation. Mol. Endocrinol. 2006, 20:1597-1609.
37. 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. U.S.A. 2009, 106:10859-10864.
38. Yang S., Shih H.J., Chow Y.C., Tsai P.S., Huang C.J. Hemin induced heme oxygenase-1 over expression involves nuclear factor-E2 related factor-2, nuclear factor-kappaB and extracellular regulated kinase: an experimental study in a testicular torsion-detorsion rodent model. J. Urol. 2008, 179:2456-2463.
39. Yin Y., Stahl B.C., DeWolf W.C., Morgentaler A. p53-mediated germ cell quality control in spermatogenesis. Dev. Biol. 1998, 204:165-171.
40. Yousef M.I., El-Hendy H.A., El-Demerdash F.M., Elagamy E.I. Dietary zinc deficiency induced-changes in the activity of enzymes and the levels of free radicals, lipids and protein electrophoretic behavior in growing rats. Toxicology 2002, 175:223-234.
41. Zhang C., Tan Y., Guo W., Li C., Ji S., Li X., Cai L. Attenuation of diabetes-induced renal dysfunction by multiple exposures to low-dose radiation is associated with the suppression of systemic and renal inflammation. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E1366-1377.
42. Zhao H., Xu S., Wang Z., Li Y., Guo W., Lin C., Gong S., Li C., Wang G., Cai L. Repetitive exposures to low-dose X-rays attenuate testicular apoptotic cell death in streptozotocin-induced diabetes rats. Toxicol. Lett. 2010, 192:356-364.