Cadmium suppresses the proliferation of piglet Sertoli cells and causes their DNA damage, cell apoptosis and aberrant ultrastructure

Reproductive Biology and Endocrinology

Volumn 8, Issue , 2010, Pages

  Zhang, Ming ^a,b   He, Zuping ^c   Wen, Lixin ^a   Wu, Jing ^a   Yuan, Liyun ^a   Lu, Yin ^a   Guo, Chengzhi ^a   Zhu, Li ^a   Deng, Sijun ^a   Yuan, Hui ^a  

^a HUNAN AGRICULTURAL UNIVERSITY   (China)

^b Jiangxi Biotech Vocational College   (China)

^c GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANDROGEN BINDING PROTEIN; CADMIUM CHLORIDE; GLUTATHIONE PEROXIDASE; MALONALDEHYDE; SUPEROXIDE DISMUTASE; TRANSFERRIN; ANTIOXIDANT; CADMIUM; CYTOTOXIN; ENZYME;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL ISOLATION; CELL PROLIFERATION; CELL ULTRASTRUCTURE; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; FLOW CYTOMETRY; IMMUNOCYTOCHEMISTRY; INHIBITION KINETICS; MALE; NICK END LABELING; NONHUMAN; PIGLET; PROTEIN EXPRESSION; REPRODUCTIVE TOXICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SERTOLI CELL; TRANSMISSION ELECTRON MICROSCOPY; AGE; ANIMAL; CELL SEPARATION; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; EVALUATION; GENETICS; METABOLISM; PHYSIOLOGY; SWINE; ULTRASTRUCTURE;

MAMMALIA;

AGE FACTORS; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CADMIUM; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; CYTOTOXINS; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENZYMES; MALE; SERTOLI CELLS; SWINE;

EID: 77955537607     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-8-97     Document Type: Article

References (48)

1. Kim J, Soh J. Cadmium-induced apoptosis is mediated by the translocation of AIF to the nucleus in rat testes. Toxicol Lett 2009, 188:45-51. 10.1016/j.toxlet.2009.03.006, 19433269.
2. de Souza Predes F, Diamante MA, Dolder H. Testis response to low doses of cadmium in Wistar rats. Int J Exp Pathol 2010, 91:125-131. 10.1111/j.1365-2613.2009.00692.x, 20015210.
3. Viswanadh EK, Rao BN, Rao BS. Antigenotoxic effect of mangiferin and changes in antioxidant enzyme levels of Swiss albino mice treated with cadmium chloride. Hum Exp Toxicol 2010, 29:409-418. 10.1177/0960327110361752, 20150354.
4. Nicholson JK, Higham DP, Timbrell JA, Sadler PJ. Quantitative high resolution 1H NMR urinalysis studies on the biochemical effects of cadmium in the rat. Mol Pharmacol 1989, 36:398-404.
5. Griffin JL, Walker LA, Shore RF, Nicholson JK. Metabolic profiling of chronic cadmium exposure in the rat. Chem Res Toxicol 2001, 14:1428-1434. 10.1021/tx015521u, 11599935.
6. Belyaeva EA, Glazunov VV, Nikitina ER, Korotkov SM. Bivalent metal ions modulate Cd2+ effects on isolated rat liver mitochondria. J Bioenerg Biomembr 2001, 33:303-318. 10.1023/A:1010607307099, 11710806.
7. Kuriwaki J, Nishijo M, Honda R, Tawara K, Nakagawa H, Hori E, Nishijo H. Effects of cadmium exposure during pregnancy on trace elements in fetal rat liver and kidney. Toxicol Lett 2005, 156:369-376. 10.1016/j.toxlet.2004.12.009, 15763636.
8. Waalkes MP, Ward JM, Liu J, Diwan BA. Transplacental carcinogenicity of inorganic arsenic in the drinking water: induction of hepatic, ovarian, pulmonary, and adrenal tumors in mice. Toxicol Appl Pharmacol 2003, 186:7-17. 10.1016/S0041-008X(02)00022-4, 12583988.
9. Benoff SH, Millan C, Hurley IR, Napolitano B, Marmar JL. Bilateral increased apoptosis and bilateral accumulation of cadmium in infertile men with left varicocele. Hum Reprod 2004, 19:616-627. 10.1093/humrep/deh139, 14998961.
10. He Z, Jiang J, Hofmann MC, Dym M. Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biol Reprod 2007, 77:723-733. 10.1095/biolreprod.107.062513, 2911237, 17625109.
11. He Z, Jiang J, Kokkinaki M, Golestaneh N, Hofmann MC, Dym M. Gdnf upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 2008, 26:266-278. 10.1634/stemcells.2007-0436, 2905627, 17962702.
12. Hofmann MC. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol Cell Endocrinol 2008, 288:95-103. 10.1016/j.mce.2008.04.012, 2491722, 18485583.
13. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000, 287:1489-1493. 10.1126/science.287.5457.1489, 10688798.
14. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 2004, 101:16489-16494. 10.1073/pnas.0407063101, 534530, 15520394.
15. Kaisman-Elbaz T, Sekler I, Fishman D, Karol N, Forberg M, Kahn N, Hershfinkel M, Silverman WF. Cell death induced by zinc and cadmium is mediated by clusterin in cultured mouse seminiferous tubules. J Cell Physiol 2009, 220:222-229. 10.1002/jcp.21754, 19288494.
16. Acharya UR, Mishra M, Patro J, Panda MK. Effect of vitamins C and E on spermatogenesis in mice exposed to cadmium. Reprod Toxicol 2008, 25:84-88. 10.1016/j.reprotox.2007.10.004, 18065194.
17. Angenard G, Muczynski V, Coffigny H, Pairault C, Duquenne C, Frydman R, Habert R, Rouiller-Fabre V, Livera G. Cadmium increases human fetal germ cell apoptosis. Environ Health Perspect 118:331-337. 10.1289/ehp.0900975, 2854759, 20064782.
18. Xu DX, Shen HM, Zhu QX, Chua L, Wang QN, Chia SE, Ong CN. The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat Res 2003, 534:155-163.
19. Akinloye O, Arowojolu AO, Shittu OB, Anetor JI. Cadmium toxicity: a possible cause of male infertility in Nigeria. Reprod Biol 2006, 6:17-30.
20. Kusakabe T, Nakajima K, Nakazato K, Suzuki K, Takada H, Satoh T, Oikawa M, Arakawa K, Nagamine T. Changes of heavy metal, metallothionein and heat shock proteins in Sertoli cells induced by cadmium exposure. Toxicol In Vitro 2008, 22:1469-1475. 10.1016/j.tiv.2008.04.021, 18556172.
21. Yu X, Hong S, Faustman EM. Cadmium-induced activation of stress signaling pathways, disruption of ubiquitin-dependent protein degradation and apoptosis in primary rat Sertoli cell-gonocyte cocultures. Toxicol Sci 2008, 104:385-396. 10.1093/toxsci/kfn087, 2734295, 18463101.
22. Chung NP, Cheng CY. Is cadmium chloride-induced inter-sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis?. Endocrinology 2001, 142:1878-1888. 10.1210/en.142.5.1878, 11316753.
23. Bizarro P, Acevedo S, Nino-Cabrera G, Mussali-Galante P, Pasos F, Avila-Costa MR, Fortoul TI. Ultrastructural modifications in the mitochondrion of mouse Sertoli cells after inhalation of lead, cadmium or lead-cadmium mixture. Reprod Toxicol 2003, 17:561-566. 10.1016/S0890-6238(03)00096-0, 14555194.
24. Dym M, Jia MC, Dirami G, Price JM, Rabin SJ, Mocchetti I, Ravindranath N. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biol Reprod 1995, 52:8-19. 10.1095/biolreprod52.1.8, 7536046.
25. He Z, Kokkinaki M, Jiang J, Dobrinski I, Dym M. Isolation, characterization, and culture of human spermatogonia. Biol Reprod 2010, 82:363-372. 10.1095/biolreprod.109.078550, 19846602.
26. Dirami G, Ravindranath N, Pursel V, Dym M. Effects of stem cell factor and granulocyte macrophage-colony stimulating factor on survival of porcine type A spermatogonia cultured in KSOM. Biol Reprod 1999, 61:225-230. 10.1095/biolreprod61.1.225, 10377053.
27. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63. 10.1016/0022-1759(83)90303-4, 6606682.
28. Sun B, Zhang X, Yonz C, Cummings BS. Inhibition of calcium-independent phospholipase A2 activates p38 MAPK signaling pathways during cytostasis in prostate cancer cells. Biochem Pharmacol 2010, 79:1727-1735. 10.1016/j.bcp.2010.02.005, 20171194.
29. He ZP, Tan WQ, Tang YF, Feng MF. Differentiation of putative hepatic stem cells derived from adult rats into mature hepatocytes in the presence of epidermal growth factor and hepatocyte growth factor. Differentiation 2003, 71:281-290. 10.1046/j.1432-0436.2003.7104505.x, 12823229.
30. Heath RL, Packer L. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 1968, 125:189-198. 10.1016/0003-9861(68)90654-1, 5655425.
31. McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 1969, 244:6049-6055.
32. Flohe L, Gunzler WA. Assays of glutathione peroxidase. Methods Enzymol 1984, 105:114-121. full_text, 6727659.
33. Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988, 175:184-191. 10.1016/0014-4827(88)90265-0, 3345800.
34. Thorne D, Wilson J, Kumaravel TS, Massey ED, McEwan M. Measurement of oxidative DNA damage induced by mainstream cigarette smoke in cultured NCI-H292 human pulmonary carcinoma cells. Mutat Res 2009, 673:3-8.
35. de Oliveira EM, Suzuki MF, do Nascimento PA, da Silva MA, Okazaki K. Evaluation of the effect of 90Sr beta-radiation on human blood cells by chromosome aberration and single cell gel electrophoresis (comet assay) analysis. Mutat Res 2001, 476:109-121.
36. He Z, Feng L, Zhang X, Geng Y, Parodi DA, Suarez-Quian C, Dym M. Expression of Col1a1, Col1a2 and procollagen I in germ cells of immature and adult mouse testis. Reproduction 2005, 130:333-341. 10.1530/rep.1.00694, 16123240.
37. Wu H, Wang H, Xiong W, Chen S, Tang H, Han D. Expression patterns and functions of toll-like receptors in mouse sertoli cells. Endocrinology 2008, 149:4402-4412. 10.1210/en.2007-1776, 18499758.
38. Yao PL, Lin YC, Richburg JH. TNF alpha-mediated disruption of spermatogenesis in response to Sertoli cell injury in rodents is partially regulated by MMP2. Biol Reprod 2009, 80:581-589. 10.1095/biolreprod.108.073122, 2805399, 19038859.
39. Yefimova MG, Sow A, Fontaine I, Guilleminot V, Martinat N, Crepieux P, Canepa S, Maurel MC, Fouchecourt S, Reiter E, Benzakour O, Guillou F. Dimeric transferrin inhibits phagocytosis of residual bodies by testicular rat Sertoli cells. Biol Reprod 2008, 78:697-704. 10.1095/biolreprod.107.063107, 18094362.
40. Grover A, Sairam MR, Smith CE, Hermo L. Structural and functional modifications of sertoli cells in the testis of adult follicle-stimulating hormone receptor knockout mice. Biol Reprod 2004, 71:117-129. 10.1095/biolreprod.103.027003, 14998910.
41. Thompson J, Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 2008, 25:304-315. 10.1016/j.reprotox.2008.02.001, 18367374.
42. Shen H, Ong C. Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility. Free Radic Biol Med 2000, 28:529-536. 10.1016/S0891-5849(99)00234-8, 10719234.
43. Yuan H, Deng Y, Yuan L, Wu J, Yuan Z, Yi J, Zhang M, Guo C, Wen L, Li R, Zhu L, He Z. Gynostemma pentaphyllum protects mouse male germ cells against apoptosis caused by zearalenone via Bax and Bcl-2 regulation. Toxicol Mech Methods 2010, 20:153-158. 10.3109/15376511003660185, 20163293.
44. Alul RH, Wood M, Longo J, Marcotte AL, Campione AL, Moore MK, Lynch SM. Vitamin C protects low-density lipoprotein from homocysteine-mediated oxidation. Free Radic Biol Med 2003, 34:881-891. 10.1016/S0891-5849(03)00028-5, 12654477.
45. Korchazhkina O, Exley C, Andrew S. Measurement by reversed-phase high-performance liquid chromatography of malondialdehyde in normal human urine following derivatisation with 2,4-dinitrophenylhydrazine. J Chromatogr B Analyt Technol Biomed Life Sci 2003, 794:353-362. 10.1016/S1570-0232(03)00495-1, 12954387.
46. Ozguner F, Koyu A, Cesur G. Active smoking causes oxidative stress and decreases blood melatonin levels. Toxicol Ind Health 2005, 21:21-26. 10.1191/0748233705th211oa, 15986573.
47. Wong CH, Mruk DD, Siu MK, Cheng CY. Blood-testis barrier dynamics are regulated by {alpha}2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinology 2005, 146:1893-1908. 10.1210/en.2004-1464, 15618353.
48. Tanaka H, Iguchi N, Isotani A, Kitamura K, Toyama Y, Matsuoka Y, Onishi M, Masai K, Maekawa M, Toshimori K, Okabe M, Nishimune Y. HANP1/H1T2, a novel histone H1-like protein involved in nuclear formation and sperm fertility. Mol Cell Biol 2005, 25:7107-7119. 10.1128/MCB.25.16.7107-7119.2005, 1190238, 16055721.