Nicotine diminishes testicular gametogenesis, steroidogenesis, and steroidogenic acute regulatory protein expression in adult albino rats: Possible influence on pituitary gonadotropins and alteration of testicular antioxidant status

Toxicological Sciences

Volumn 116, Issue 2, 2010, Pages 647-659

  Jana, Kuladip ^a,b,c   Samanta, Prabhat Kumar ^a   Kumar De, Dipak ^a  

^a WEST BENGAL UNIVERSITY OF ANIMAL AND FISHERY SCIENCES   (India)

^b SAHA INSTITUTE OF NUCLEAR PHYSICS   (India)

^c BOSE INSTITUTE   (India)

Author keywords

Androgenesis; Antioxidants; Lipid peroxidation; Nicotine; Spermatogenesis; Testosterone

Indexed keywords

ANDROGEN; ANTIOXIDANT; CHORIONIC GONADOTROPIN; CORTICOSTERONE; GLUTATHIONE; GONADOTROPIN; HYDROGEN PEROXIDE; HYDROXYL RADICAL; NICOTINE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TAURINE; TESTOSTERONE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; HYDROXYSTEROID DEHYDROGENASE; PHOSPHOPROTEIN; REACTIVE OXYGEN METABOLITE;

ANDROGEN SYNTHESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; BLOOD LEVEL; CELL DEGENERATION; CONTROLLED STUDY; ENZYME ACTIVITY; GAMETOGENESIS; GENE EXPRESSION; GERM CELL; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON COUNT; TESTIS; WESTERN BLOTTING; ANIMAL; BLOOD; DRUG EFFECTS; EATING; GENETICS; METABOLISM; ORGAN SIZE; PATHOLOGY; TOXICITY; WISTAR RAT;

17-HYDROXYSTEROID DEHYDROGENASES; 3-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; ANTIOXIDANTS; CORTICOSTERONE; EATING; GONADOTROPINS, PITUITARY; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; NICOTINE; ORGAN SIZE; PHOSPHOPROTEINS; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SPERM COUNT; SPERMATOGENESIS; TESTIS; TESTOSTERONE;

EID: 77955069710     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq149     Document Type: Article

References (51)

1. Alvarez, J. G., and Storey, B. T. (1983). Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol. Reprod. 29, 548-555.
2. Arabi, M. (2004). Nicotinic infertility: assessing DNA and plasma membrane integrity of human spermatozoa. Andrologia 36, 305-310.
3. Aruldhas, M. M., Subramanian, S., Sekar, P., Vengatesh, G., Chandrahasan, G., Govindarajulu, P., and Akbarsha, M. A. (2005). Chronic chromium exposure-induced changes in testicular histoarchitecture are associated with oxidative stress: study in a non-human primate (Macaca radiata Geoffroy. Human Reprod. 20, 2801-2813.
4. Aydos, K., Güven, M. C., Can, B., and Ergün, A. (2001). Nicotine toxicity to the ultra-structure of the testis in rats. BJU Int. 88, 622-626.
5. Bandopadhyay, G., Sinha, S., Chattopadhyay, B. D., and Chakraborty, A. (2008). Role of cucumin against nicotine induced genotoxicity on rat liver under restricted dietary protein. Eur. J. Pharmacol. 588, 151-157.
6. Beutler, E. (1983). Active transport of glutathione disulphide from erythrocytes. In Functions of Glutathione, Biochemical, Physiological, Toxicological and Clinical Aspects (A. Larsen, S. Orremium, A. Holmgren, and B. Mannervick, Eds.), p. 65. Raven Press, New York.
7. Blanco-Rodriguez, J., and Martinez-Garcia, C. (1988). Apoptosis precedes detachment of germ cells from the seminiferous epithelium after hormonal suppression by short-term oestradiol treatment of rats. Int. J. Androl. 21, 109-115.
8. Bose, M., Debnath, D., Chen, Y., and Bose, H. S. (2007). Folding, activity and import of steroidogenic acute regulatory protein into mitochondria changed by nicotine exposure. J. Mol. Endocrinol. 39, 67-79.
9. Cozzi, R., Ricordy, R., and Bartolini, F. (1995). Taurine and ellagic acid: two differently acting natural antioxidants. Environ. Mol. Mutagen 26, 248-254.
10. Crowley-Weber, C. L., Dvorakova, K., Crowley, C., Bernstein, C., Gerewal, H., and Payne, C. M. (2003). Nicotine increases oxidative stress, activates NF-kappa B and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem. Biol. Int. 145, 53-66.
11. Devasagayam, T. P., and Tarachand, U. (1987). Decreased lipid peroxidation in the rat kidney during gestation. Biochem. Biophys. Res. Commun. 145, 134-138.
12. Erat, M., Ciftci, M., Gumustekin, K., and Gul, M. (2007). Effect of nicotine and vitamin E on glutathione reductase activity in some rat tissues in vivo and in vitro. Eur. J. Pharmacol. 554, 92-97.
13. Fisher, R. A., and Yates, R. (1974). In Statistical Tables for Biological, Agricultural and Medical Research. Longman Group, London.
14. Funabasi, T., Sano, A., Matsusima, D., and Kimura, F. (2005). Nicotine inhibits pulsatile luteinizing hormone secretion in human males but not in human females, and tolerance to this nicotine effect is lost within one week of quitting smoking. J. Clin. Endocrinol. Metab. 90, 3908-3913.
15. Habig, W. H., Pabst, M. J., and Jocoby, W. B. (1974). Glutathione S-transferase: the first step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139.
16. Hales, D. B., Diemer, T., and Hales, K. H. (1999). Role of cytokines in testicular function. Endocrine 10, 201-217.
17. Hissin, P. J., and Hilf, R. (1976). A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74, 214-226.
18. Holland, M. K., and Storey, B. T. (1981). Oxygen metabolism of mammalian spermatozoa. Generation of hydrogen peroxide by rabbit epididymal spermatozoa. Biochem. J. 198, 273-280.
19. Jana, K., Jana, S., and Samanta, P. K. (2006). Effects of chronic exposure to sodium arsenite on hypothalamo-pituitary-testicular activities in adult rats: possible an estrogenic mode of action. Reprod. Biol. Endocrinol. 4, 9-22.
20. Jana, K., Yin, X., Schiffer, R. B., Chen, J. J., Pandey, A. K., Stocco, D. M., Grammas, P., and Wang, X. (2008). Chrysin, a natural flavonoid enhances steroidogenesis and steroidogenic acute regulatory protein gene expression in mouse Leydig cells. J. Endocrinol. 197, 315-323.
21. Kalikauskas, V., Blaustein, D., and Ablin, R. J. (1985). Cigarette smoking and its possible effects on sperm. Fertil. Steril. 44, 526-528.
22. Kamel, F. A., and Kubajak, C. L. (1987). Modulation of gonadotropin secretion by corticosterone interaction with gonadal steroids and mechanism of action. Endocrinol. 121, 561-565.
23. Kavitharaj, N. K., and Vijayammal, P. L. (1999). Nicotine administration induced changes in the gonadal functions in male rats. Pharmacol. 58, 2-7.
24. Kumar, V., Majumder, C., and Roy, P. (2008). Effects of endocrine disrupting chemicals from leather industry effluents on male reproductive system. J. Steroid Biochem. Mol. Biol. 111, 208-216.
25. Lobo, M. V. T., Alonso, F. J. M., and del Río, R. M. (2000). Immunohistochemical localization of taurine in the male reproductive organs of the rat. J. Histochem. Cytochem. 48, 313-320.
26. Manna, P., Sinha, M., and Sil, P. C. (2008). Cadmium induced testicular pathophysiology: prophylactic role of taurine. Reprod. Toxicol. 26, 282-291.
27. Mendelson, J. H., Scholar, M. B., Mutshler, N. H., Jaszyma-Gasior, M., Goletiami, N. V., Siegel, A. J., and Mello, N. K. (2003). Effects of intravenous cocaine and cigarette smoking on leuteinizing hormone, testosterone, and prolactin on men. J. Phamacol. Exp. Therap. 308, 339-348.
28. Miller, W. L. (2007). StAR search-what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Mol. Endo. 21, 589-601.
29. Mishra, D. P., and Shaha, C. (2005). Estrogen induced spermatogenic cell apoptosis occurs via the mitochondrial pathway. J. Biol. Chem. 280, 6181-6196.
30. Murugesan, P., Muthusamy, T., Balasubramanian, K., and Arunakaran, J. (2007). Effects of vitamins C and E on steroidogenic enzymes mRNA expression in polychlorinated biphenyl (Aroclor 1254) exposed adult rat Leydig cells. Toxicology 232, 170-182.
31. Okamoto, M., Kita, T., Okuda, H., Tanaka, T., and Nakashima, T. (1994). Effects of aging on acute toxicity of nicotine in rats. Pharmacol. Toxicol. 75, 1-6.
32. Orlowski, M., and Meister, A. (1965). Isolation of c-glutamyl transpeptidase from hog kidney. J. Biol. Chem. 240, 338-347.
33. Patterson, T. R., Stringham, J. D., and Meikle, A. W. (1990). Nicotine and cotinine inhibit steroidogenesis in mouse Leydig cells. Life Sci. 46, 265-272.
34. Puntaqulo, S., and Cederbaum, A. I. (1988). Effect of oxygen concentration on microsomal oxidation of ethanol and generation of oxygen radicals. Biochem. J. 251, 787-794.
35. Rotruck, J. T., Pope, A. L., Ganther, H. E., Swanson, A. B., Hafeman, D. G., and Hoekstra, W. G. (1973). Selenium: biochemical role as a component of glutathione peroxidase. Science 179, 588-590.
36. Sarasin, A., Schlumpf, M., Müller, M., Fleischmann, I., Lauber, M. E., and Lichtensteiger, W. (2003). Adrenal-mediated rather than direct effects of nicotine as a basis of altered sex steroid synthesis in fetal and neonatal rat. Reprod. Toxicol. 17, 153-162.
37. Seema, P., Swathy, S. S., and Indira, M. (2007). Protective effect of selenium on nicotine-induced testicular toxicity in rats. Biol. Trace Elem. Res. 120, 212-218.
38. Segarra, A. C., and Strand, F. L. (1989). Prenatal administration of nicotine alters subsequent sexual behaviour and testosterone levels of male rats. Brain Res. 480, 151-159.
39. Sener, G., Sehirli, O., Ipcxi, Y., Cetinel, S., Cikler, E., Gedik, N., and Alican, I. (2005a). Protective effects of taurine against nicotine-induced oxidative damage of rat urinary bladder and kidney. Pharmacol. 74, 37-44.
40. Sener, G., Sehirli, O., Ipcxi, Y., Cetinel, S., Cikler, E., Gedik, N., and Alican, I. (2005b). Taurine treatment protects against chronic nicotine-induced oxidative changes. Fundam. Clin. Pharmacol. 19, 155-164.
41. Sepaniak, S., Forges, T., Gerard, H., Foliguet, B., Bene, M. C., and MonnierBarbarino, P. (2006). The influence of cigarette smoking on human sperm quality and DNA fragmentation. Toxicology 223, 54-60.
42. Seyler, L., Jr, Pomerleau, O. F., Fertig, J. B., Hunt, D., and Parker, K. (1986). Pituitary hormone response to cigarette smoking. Pharmacol. Biochem. Behav. 24, 159-162.
43. Sharpe, R. M., Maddocks, S., Millar, M., Saunders, P. T. K., Kerr, J. B., and McKinnell, C. (1992). Testosterone and spermatogenesis: identification of stage dependent, androgen-regulated proteins secreted by adult rat seminiferous tubules. J. Androl. 13, 172-184.
44. Staal, G. E., Visser, J., and Veeger, C. (1969). Purification and properties of glutathione reductase of human erythrocytes. Biochem. Biophy. Acta 185, 39-48.
45. Stocco, D. M. (2001). StAR protein and the regulation of steroid hormone biosynthesis. Annual Rev. Physiol. 63, 193-213.
46. Stocco, D. M., and Clark, B. (1996). Regulation of the acute production of steroids in steroidogenic cells. Endocrine Rev. 17, 221-244.
47. Stocco, D. M., Wells, J., and Clark, B. J. (1993). The effects of hydrogen peroxide on steroidogenesis in mouse Leydig tumor cells. Endocrinol. 133, 2827-2832.
48. Sudheer, A. R., Muthukumaran, S., Devipriya, N., Devraj, H., and Menon, V. P. (2008). Influence of ferulic acid on nicotine induced lipid peroxidation, DNA damage and inflammation in experimental rats as compared to N-acetylcysteine. Toxicology 243, 317-329.
49. Vine, M. F. (1996). Smoking and male reproduction: a review. Int. J. Androl. 19, 323-337.
50. Wyrobek, A. J., and Bruce, W. R. (1975). Chemical induction of sperm abnormalities in mice. Proc. Nat. Acad. Sci. U.S.A. 72, 4425-4429.
51. Yamamoto, Y., Isoyama, E., Sofikitis, N., and Miyagawa, I. (1998). Effects of smoking on testicular function and fertilizing potential in rats. Urol. Res. 26, 45-48.