Pubertal cadmium exposure impairs testicular development and spermatogenesis via disrupting testicular testosterone synthesis in adult mice

Reproductive Toxicology

Volumn 29, Issue 2, 2010, Pages 176-183

  Ji, Yan Li ^a   Wang, Hua ^a   Liu, Ping ^a   Wang, Qun ^a   Zhao, Xian Feng ^a   Meng, Xiu Hong ^a   Yu, Tao ^a   Zhang, Heng ^a   Zhang, Cheng ^a   Zhang, Ying ^a   Xu, De Xiang ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Cadmium; Endocrine disruptor; Spermatogenesis; Testes; Testosterone

Indexed keywords

CADMIUM; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450 17; MESSENGER RNA; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE; TESTOSTERONE 17BETA DEHYDROGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EPIDIDYMIS; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PUBERTY; SEMINAL VESICLE; SPERMATOGENESIS; SPERMATOZOON COUNT; TESTIS DEVELOPMENT; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE SYNTHESIS; TOXICOKINETICS;

17-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; CADMIUM CHLORIDE; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; ENVIRONMENTAL POLLUTANTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA, MALE; MALE; MICE; MICE, INBRED STRAINS; ORGAN SIZE; PHOSPHOPROTEINS; RNA, MESSENGER; SEXUAL MATURATION; SPERMATOGENESIS; STEROID 17-ALPHA-HYDROXYLASE; TESTIS; TESTOSTERONE;

MUS;

EID: 77949568371     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2009.10.014     Document Type: Article

References (51)

1. Joseph P. Mechanisms of cadmium carcinogenesis. Toxicol Appl Pharmacol; in press.
2. Waalkes M.P. Cadmium carcinogenesis in review. J Inorg Biochem 2000, 79:241-244.
3. Barr M. The teratogenicity of cadmium chloride in two stocks of Wistar rats. Teratology 1973, 7:237-242.
4. Hovland D.N., Machado A.F., Scott W.J., Collins M.D. Differential sensitivity of the SWV and C57BL/6 mouse strains to the teratogenic action of single administrations of cadmium given throughout the period of anterior neuropore closure. Teratology 1999, 60:13-21.
5. Scott W.J., Schreiner C.M., Goetz J.A., Robbins D., Bell S.M. Cadmium-induced postaxial forelimb ectrodactyly: association with altered sonic hedgehog signaling. Reprod Toxicol 2005, 19:479-485.
6. Paniagua-Castro N., Escalona-Cardoso G., Chamorro-Cevallos G. Glycine reduces cadmium-induced teratogenic damage in mice. Reprod Toxicol 2007, 23:92-97.
7. Robinson J.F., Yu X., Hong S., Griffith W.C., Beyer R., Kim E., et al. Cadmium-induced differential toxicogenomic response in resistant and sensitive mouse strains undergoing neurulation. Toxicol Sci 2009, 107:206-219.
8. Xu B., Chia S.E., Tsakok M., Ong C.N. Trace elements in blood and seminal plasma and their relationship to sperm quality. Reprod Toxicol 1993, 7:613-618.
9. Telisman S., Cvitković P., Jurasović J., Pizent A., Gavella M., Rocić B. Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 2000, 108:45-53.
10. Pant N., Upadhyay G., Pandey S., Mathur N., Saxena D.K., Srivastava S.P. Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod Toxicol 2003, 17:447-450.
11. Wu H.M., Lin-Tan D.T., Wang M.L., Huang H.Y., Wang H.S., Soong Y.K., et al. Cadmium level in seminal plasma may affect the pregnancy rate for patients undergoing infertility evaluation and treatment. Reprod Toxicol 2008, 25:481-484.
12. Xu D.X., Shen H.M., Zhu Q.X., Chua L.H., Wang Q.N., Chia S.E., et al. 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.
13. Siu ER, Mruk DD, Porto CS, Cheng CY. Cadmium-induced testicular injury. Toxicol Appl Pharmacol; in press.
14. Niewenhuis R.J., Prozialeck W.C. Calmodulin inhibitors protect against cadmium-induced testicular damage in mice. Biol Reprod 1987, 37:127-133.
15. El-Ashmawy I.M., Youssef S.A. The antagonistic effect of chlorpromazine on cadmium toxicity. Toxicol Appl Pharmacol 1999, 161:34-39.
16. El-Demerdash F.M., Yousef M.I., Kedwany F.S., Baghdadi H.H. Cadmium-induced changes in lipid peroxidation, blood hematology, biochemical parameters and semen quality of male rats: protective role of vitamin E and beta-carotene. Food Chem Toxicol 2004, 42:1563-1571.
17. Holdcraft R.W., Braun R.E. Hormonal regulation of spermatogenesis. Int J Androl 2004, 27:335-342.
18. Parizek J. The destructive effect of cadmium ion on testicular tissue and its prevention by zinc. J Endocrinol 1957, 15:56-63.
19. Parizek J., Zahor Z. Effect of cadmium salts on testicular tissue. Nature 1956, 177:1036.
20. Laskey J.W., Rehnberg G.L., Laws S.C., Hein J.F. Reproductive effects of low acute doses of cadmium chloride in adult male rats. Toxicol Appl Pharmacol 1984, 73:250-255.
21. Biswas N.M., Sen Gupta R., Chattopadhyay A., Choudhury G.R., Sarkar M. Effect of atenolol on cadmium-induced testicular toxicity in male rats. Reprod Toxicol 2001, 15:699-704.
22. Laskey J.W., Phelps P.V. Effect of cadmium and other metal cations on in vitro Leydig cell testosterone production. Toxicol Appl Pharmacol 1991, 108:296-306.
23. Yang J.M., Arnush M., Chen Q.Y., Wu X.D., Pang B., Jiang X.Z. Cadmium-induced damage to primary cultures of rat Leydig cells. Reprod Toxicol 2003, 17:553-560.
24. Latendresse J.R., Warbrittion A.R., Jonassen H., Creasy D.M. Fixation of testes and eyes using a modified Davidson's fluid: comparison with Bouin's fluid and conventional Davidson's fluid. Toxicol Pathol 2002, 30:524-533.
25. World Health Organization WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction 1999, Cambridge University Press, Cambridge, United Kingdom. 4th ed.
26. Chang C., Chen Y.T., Yeh S.D., Xu Q., Wang R.S., Guillou F., et al. Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells. Proc Natl Acad Sci USA 2004, 101:6876-6881.
27. De Gendt K., Swinnen J.V., Saunders P.T., Schoonjans L., Dewerchin M., Devos A., et al. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA 2004, 101:1327-1332.
28. Lafuente A., Márquez N., Pérez-Lorenzo M., Pazo D., Esquifino A.I. Pubertal and postpubertal cadmium exposure differentially affects the hypothalamic-pituitary-testicular axis function in the rat. Food Chem Toxicol 2000, 38:913-923.
29. Fouad A.A., Qureshi H.A., Al-Sultan A.I., Yacoubi M.T., Ali A.A. Protective effect of hemin against cadmium-induced testicular damage in rats. Toxicology 2009, 257:153-160.
30. Miller W.L. StAR Search-what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Mol Endocrinol 2007, 21:589-601.
31. Gunnarsson D., Svensson M., Selstam G., Nordberg G. Pronounced induction of testicular PGF(2 alpha) and suppression of testosterone by cadmium-prevention by zinc. Toxicology 2004, 200:49-58.
32. Payne A.H., Youngblood G.L. Regulation of expression of steroidogenic enzymes in Leydig cells. Biol Reprod 1995, 52:217-225.
33. Sen Gupta R., Kim J., Gomes C., Oh S., Park J., Im W.B., et al. Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol Cell Endocrinol 2004, 221:57-66.
34. Sen Gupta R., Sen Gupta E., Dhakal B.K., Thakur A.R., Ahnn J. Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Mol Cells 2004, 17:132-139.
35. Manna P., Sinha M., Sil P.C. Cadmium induced testicular pathophysiology: prophylactic role of taurine. Reprod Toxicol 2008, 26:282-291.
36. Lin H., Ge R.S., Chen G.R., Hu G.X., Dong L., Lian Q.Q., et al. Involvement of testicular growth factors in fetal Leydig cell aggregation after exposure to phthalate in utero. Proc Natl Acad Sci USA 2008, 105:7218-7222.
37. Mahood I.K., Hallmark N., McKinnell C., Walker M., Fisher J.S., Sharpe R.M. Abnormal Leydig Cell aggregation in the fetal testis of rats exposed to di (n-butyl) phthalate and its possible role in testicular dysgenesis. Endocrinology 2005, 146:613-623.
38. Mahood I.K., Scott H.M., Brown R., Hallmark N., Walker M., Sharpe R.M. In utero exposure to di(n-butyl) phthalate and testicular dysgenesis: comparison of fetal and adult end points and their dose sensitivity. Environ Health Perspect 2007, 115(Suppl.):55-61.
39. Ichimura T., Kawamura M., Mitani A. Co-localized expression of FasL, Fas, Caspase-3 and apoptotic DNA fragmentation in mouse testis after oral exposure to di(2-ethylhexyl)phthalate. Toxicology 2003, 194:35-42.
40. Borch J., Dalgaard M., Ladefoged O. Early testicular effects in rats perinatally exposed to DEHP in combination with DEHA-apoptosis assessment and immunohistochemical studies. Reprod Toxicol 2005, 19:517-525.
41. Sobarzo C.M., Lustig L., Ponzio R., Denduchis B. Effect of di-(2-ethylhexyl) phthalate on N-cadherin and catenin protein expression in rat testis. Reprod Toxicol 2006, 22:77-86.
42. McClusky L.M., de Jager C., Bornman M.S. Stage-related increase in the proportion of apoptotic germ cells and altered frequencies of stages in the spermatogenic cycle following gestational, lactational, and direct exposure of male rats to p-nonylphenol. Toxicol Sci 2007, 95:249-256.
43. Saradha B., Vaithinathan S., Mathur P.P. Lindane induces testicular apoptosis in adult Wistar rats through the involvement of Fas-FasL and mitochondria-dependent pathways. Toxicology 2009, 255:131-139.
44. Lambrot R., Muczynski V., Lécureuil C., Angenard G., Coffigny H., Pairault C., et al. Phthalates impair germ cell development in the human fetal testis in vitro without change in testosterone production. Environ Health Perspect 2009, 117:32-37.
45. Xu C., Johnson J.E., Singh P.K., Jones M.M., Yan H., Carter C.E. In vivo studies of cadmium-induced apoptosis in testicular tissue of the rat and its modulation by a chelating agent. Toxicology 1996, 107:1-8.
46. Zhou T., Zhou G., Song W., Eguchi N., Lu W., Lundin E., et al. Cadmium-induced apoptosis and changes in expression of p53, c-jun and MT-I genes in testes and ventral prostate of rats. Toxicology 1999, 142:1-13.
47. Ozawa N., Goda N., Makino N., Yamaguchi T., Yoshimura Y., Suematsu M. Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J Clin Invest 2002, 109:457-467.
48. Bartlett J.M., Kerr J.B., Sharpe R.M. The effect of selective destruction and regeneration of Leydig cells on the intratesticular distribution of testosterone and morphology of the seminiferous epithelium. J Androl 1986, 7:240-253.
49. Chapin R.E., Gulati D.K., Fail P.A., Hope E., Russell S.R., Heindel J.J., et al. The effects of feed restriction on reproductive function in Swiss CD-1 mice. Fundam Appl Toxicol 1993, 20:15-22.
50. Chapin R.E., Gulati D.K., Barnes L.H., Teague J.L. The effects of feed restriction on reproductive function in Sprague-Dawley rats. Fundam Appl Toxicol 1993, 20:23-29.
51. Rehm S., White T.E., Zahalka E.A., Stanislaus D.J., Boyce R.W., Wier P.J. Effects of food restriction on testis and accessory sex glands in maturing rats. Toxicol Pathol 2008, 36:687-694.