Oxidative status in testis and epididymal sperm parameters after acute and chronic stress by cold-water immersion in the adult rat

References

• Agarwal, A., Mulgund, A., Sharma, R., and Sabanegh, E. (2014) Mechanisms of oligozoospermia: An oxidative stress perspective. Syst Biol Reprod Med 60:206–16
   PubMed Web of Science ®Google Scholar
• Aitken, R.J. (1999) The Amoroso Lecture. The human spermatozoon—a cell in crisis? J Reprod Fertil 115:1–7
   PubMedGoogle Scholar
• Aitken, R.J., and Clarkson, J.S. (1987) Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil 81:459–69
   PubMedGoogle Scholar
• Al-Joudi, F.S., and Jamil, J.A. (2012) Imprisonment-associated sperm clumping and male infertility. J Int Med Res 40:393–7
   PubMed Web of Science ®Google Scholar
• Arenas-Rios, E., Leon-Galvan, M.A., Mercado, P.E., Lopez-Wilchis, R., Cervantes, D.L., and Rosado, A. (2007) Superoxide dismutase, catalase, and glutathione peroxidase in the testis of the Mexican big-eared bat (Corynorhinus mexicanus) during its annual reproductive cycle. Comp Biochem Physiol A Mol Integr Physiol 148:150–8
   PubMed Web of Science ®Google Scholar
• Arthur, J.R., and Boyne, R. (1985) Superoxide dismutase and glutathione peroxidase activities in neutrophils from selenium deficient and copper deficient cattle. Life Sci 36:1569–75
   PubMed Web of Science ®Google Scholar
• Baccetti, B., Burrini, A.G., Collodel, G., Magnano, A.R., Piomboni, P., Renieri, T., et al. (1989) Morphogenesis of the decapitated and decaudated sperm defect in two brothers. Gamete Res 23:181–8
   PubMedGoogle Scholar
• Baek, I.J., Seo, D.S., Yon, J.M., Lee, S.R., Jin, Y., Nahm, S.S., et al. (2007) Tissue expression and cellular localization of phospholipid hydroperoxide glutathione peroxidase (PHGPx) mRNA in male mice. J Mol Histol 38:237–44
   PubMed Web of Science ®Google Scholar
• Bauche, F., Fouchard, M.H., and Jegou, B. (1994) Antioxidant system in rat testicular cells. FEBS Lett 349:392–6
   PubMed Web of Science ®Google Scholar
• Bilommi, R., Nawas, B.A., Kusmayadi, D.D., Diposarosa, R., Chairul, A., and Hernowo, B.S. (2013) The effects of glutathione on malondialdehyde expression and seminiferous tubule damage in experimental testicular torsion-detorsion in Wistar rats. J Pediatr Urol 9:1059–63
   PubMedGoogle Scholar
• Bitgul, G., Tekmen, I., Keles, D., and Oktay, G. (2013) Protective Effects of Resveratrol against Chronic Immobilization Stress on Testis. ISRN Urol 2013:278720
   Google Scholar
• Caro, P., Gomez, J., Sanz, A., Portero-Otin, M., Pamplona, R., and Barja, G. (2007) Effect of graded corticosterone treatment on aging-related markers of oxidative stress in rat liver mitochondria. Biogerontology 8:1–11
   PubMed Web of Science ®Google Scholar
• Chemes, H.E., Puigdomenech, E.T., Carizza, C., Olmedo, S.B., Zanchetti, F., and Hermes, R. (1999) Acephalic spermatozoa and abnormal development of the head-neck attachment: A human syndrome of genetic origin. Hum Reprod 14:1811–18
   PubMed Web of Science ®Google Scholar
• Chidrawar, V., Chitme, H., Patel, K., Patel, N., Racharla, V., Dhoraji, N., et al. (2011) Effects of Cynodon dactylon on Stress-Induced Infertility in Male Rats. J Young Pharm 3:26–35
   PubMedGoogle Scholar
• Cohen, G., Dembiec, D., and Marcus, J. (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34:30–8
   PubMed Web of Science ®Google Scholar
• Cohen, G., and Hochstein, P. (1963) Glutathione Peroxidase: The Primary Agent for the Elimination of Hydrogen Peroxide in Erythrocytes. Biochemistry 2:1420–8
   PubMed Web of Science ®Google Scholar
• Collodel, G., Federico, M.G., Geminiani, M., Martini, S., Bonechi, C., Rossi, C., et al. (2011) Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reprod Toxicol 31:239–46
   PubMed Web of Science ®Google Scholar
• Cooper, T.G., Yeung, C.H., Wagenfeld, A., Nieschlag, E., Poutanen, M., Huhtaniemi, I., et al. (2004) Mouse models of infertility due to swollen spermatozoa. Mol Cell Endocrinol 216:55–63
   PubMed Web of Science ®Google Scholar
• Dastig, S., Nenicu, A., Otte, D.M., Zimmer, A., Seitz, J., Baumgart-Vogt, E., et al. (2011) Germ cells of male mice express genes for peroxisomal metabolic pathways implicated in the regulation of spermatogenesis and the protection against oxidative stress. Histochem Cell Biol 136:413–25
   PubMed Web of Science ®Google Scholar
• Dhanabalan, S., Jubendradass, R., Latha, P., and Mathur, P.P. (2011) Effect of restraint stress on 2,3,7,8 tetrachloro dibenzo-p-dioxin induced testicular and epididymal toxicity in rats. Hum Exp Toxicol 30:567–78
   PubMed Web of Science ®Google Scholar
• Dong, Q., Salva, A., Sottas, C.M., Niu, E., Holmes, M., and Hardy, M.P. (2004) Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J Androl 25:973–81
   PubMed Web of Science ®Google Scholar
• Doreswamy, K., and Muralidhara. (2005) Genotoxic consequences associated with oxidative damage in testis of mice subjected to iron intoxication. Toxicology 206:169–78
   PubMed Web of Science ®Google Scholar
• Dott, H.M., and Foster, G.C. (1972) A technique for studying the morphology of mammalian spermatozoa which are eosinophilic in a differential ‘life-dead’ stain. J Reprod Fertil 29:443–5
   PubMedGoogle Scholar
• Dyson, A.L., and Orgebin-Crist, M.C. (1973) Effect of hypophysectomy, castration and androgen replacement upon the fertilizing ability of rat epididymal spermatozoa. Endocrinology 93:391–402
   PubMed Web of Science ®Google Scholar
• Elsharkawy, E.E., Yahia, D., and El-Nisr, N.A. (2012) Chlorpyrifos induced testicular damage in rats: Ameliorative effect of glutathione antioxidant. Environ Toxicol 29:1011–19
   PubMed Web of Science ®Google Scholar
• Farombi, E.O., Abarikwu, S.O., Adesiyan, A.C., and Oyejola, T.O. (2013) Quercetin exacerbates the effects of subacute treatment of atrazine on reproductive tissue antioxidant defence system, lipid peroxidation and sperm quality in rats. Andrologia 45:256–65
   PubMed Web of Science ®Google Scholar
• Fernandez, C.D., Porto, E.M., Arena, A.C., and Kempinas Wde, G. (2008) Effects of altered epididymal sperm transit time on sperm quality. Int J Androl 31:427–37
   PubMedGoogle Scholar
• Forstrom, J.W., Stults, F.H., and Tappel, A.L. (1979) Rat liver cytosolic glutathione peroxidase: Reactivity with linoleic acid hydroperoxide and cumene hydroperoxide. Arch Biochem Biophys 193:51–5
   PubMed Web of Science ®Google Scholar
• Franca, L.R., Avelar, G.F., and Almeida, F.F. (2005) Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63:300–18
   PubMed Web of Science ®Google Scholar
• Ghosh, D., Das, U.B., Ghosh, S., Mallick, M., and Debnath, J. (2002) Testicular gametogenic and steroidogenic activities in cyclophosphamide treated rat: A correlative study with testicular oxidative stress. Drug Chem Toxicol 25:281–92
   PubMed Web of Science ®Google Scholar
• Goldstone, A.B., Liochev, S.I., and Fridovich, I. (2006) Inactivation of copper, zinc superoxide dismutase by H2O2: Mechanism of protection. Free Radic Biol Med 41:1860–3
   PubMed Web of Science ®Google Scholar
• Gomez-Quiroz, L.E., Factor, V.M., Kaposi-Novak, P., Coulouarn, C., Conner, E.A., and Thorgeirsson, S.S. (2008) Hepatocyte-specific c-Met deletion disrupts redox homeostasis and sensitizes to Fas-mediated apoptosis. J Biol Chem 283:14581–9
   PubMed Web of Science ®Google Scholar
• Goyal, H.O., Bartol, F.F., Wiley, A.A., Khalil, M.K., Chiu, J., and Vig, M.M. (1997) Immunolocalization of androgen receptor and estrogen receptor in the developing testis and excurrent ducts of goats. Anat Rec 249:54–62
   PubMedGoogle Scholar
• Gu, W., and Hecht, N.R. (1996) Translation of a testis-specific Cu/Zn superoxide dismutase (SOD-1) mRNA is regulated by a 65-kilodalton protein which binds to its 5′ untranslated region. Mol Cell Biol 16:4535–43
   PubMed Web of Science ®Google Scholar
• Hermo, L. (1995) Structural features and functions of principal cells of the intermediate zone of the epididymis of adult rats. Anat Rec 242:515–30
   PubMedGoogle Scholar
• Hermo, L.R., and Robaire, B. (2002) Epididymis cell types and their function. In: The Epididymis: From Molecules to Clinical Practice. Robaire, B., and Hinton, B.T., eds. New York: Kluwer Academic/Plenum, pp. 81–102
   Google Scholar
• Hodgson, E.K., and Fridovich, I. (1975) The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: Inactivation of the enzyme. Biochemistry 14:5294–9
   Web of Science ®Google Scholar
• Hou, G., Xiong, W., Wang, Chen, X., and Yuan, T.F. (2014) Chronic stress influences sexual motivation and causes damage to testicular cells in male rats. J Sex Med 11:653–63
   PubMed Web of Science ®Google Scholar
• Kaabi, M., Paz, P., Alvarez, M., Anel, E., Boixo, J.C., Rouissi, H., et al. (2003) Effect of epididymis handling conditions on the quality of ram spermatozoa recovered post-mortem. Theriogenology 60:1249–59
   PubMed Web of Science ®Google Scholar
• Kaur, P., Kaur, G., and Bansal, M.P. (2006) Tertiary-butyl hydroperoxide induced oxidative stress and male reproductive activity in mice: Role of transcription factor NF-kappaB and testicular antioxidant enzymes. Reprod Toxicol 22:479–84
   PubMed Web of Science ®Google Scholar
• Kirby, E.D., Geraghty, A.C., Ubuka, T., Bentley, G.E., and Kaufer, D. (2009) Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc Natl Acad Sci U S A 106:11324–9
   PubMed Web of Science ®Google Scholar
• Klinefelter, G.R. (2002) Actions of toxicants on the structure and function of the epididymis. In: The Epididymis: From Molecules to Clinical Practice. Robaire, B., and Hinton, B.T., eds. Kluwer Academic Plenum Publishers, pp. 353–69
   Google Scholar
• Koolhaas, J.M., Bartolomucci, A., Buwalda, B., de Boer, S.F., Flugge, G., Korte, S.M., et al. (2011) Stress revisited: A critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291–301
   PubMed Web of Science ®Google Scholar
• Kumar, T.R., and Muralidhara. (2007) Induction of oxidative stress by organic hydroperoxides in testis and epididymal sperm of rats in vivo. J Androl 28:77–85
   PubMed Web of Science ®Google Scholar
• LeBel, C.P., Ischiropoulos, H., and Bondy, S.C. (1992) Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–31
   PubMed Web of Science ®Google Scholar
• Leong, C.T., D’Souza, U.J., Iqbal, M., and Mustapha, Z.A. (2013) Lipid peroxidation and decline in antioxidant status as one of the toxicity measures of diazinon in the testis. Redox Rep 18:155–64
   PubMed Web of Science ®Google Scholar
• Long, F., Wang, Y., Qi, H.H., Zhou, X., and Jin, X.Q. (2008) Rapid non-genomic effects of glucocorticoids on oxidative stress in a guinea pig model of asthma. Respirology 13:227–32
   PubMed Web of Science ®Google Scholar
• Luers, G.H., Thiele, S., Schad, A., Volkl, A., Yokota, S., and Seitz, J. (2006) Peroxisomes are present in murine spermatogonia and disappear during the course of spermatogenesis. Histochem Cell Biol 125:693–703
   PubMed Web of Science ®Google Scholar
• MacMillan-Crow, L.A., Crow, J.P., and Thompson, J.A. (1998) Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37:1613–22
   PubMed Web of Science ®Google Scholar
• Maheshwari, A., Misro, M.M., Aggarwal, A., Sharma, R.K., and Nandan, D. (2009) Pathways involved in testicular germ cell apoptosis induced by H2O2 in vitro. FEBS J 276:870–81
   PubMed Web of Science ®Google Scholar
• McGrady, A.V. (1984) Effects of psychological stress on male reproduction: A review. Arch Androl 13:1–7
   PubMedGoogle Scholar
• Mihaljevic, B., Katusin-Razem, B., and Razem, D. (1996) The reevaluation of the ferric thiocyanate assay for lipid hydroperoxides with special considerations of the mechanistic aspects of the response. Free Radic Biol Med 21:53–63
   PubMed Web of Science ®Google Scholar
• Moore, H.D., and Bedford, J.M. (1979) Short-term effects of androgen withdrawal on the structure of different epithelial cells in the rat epididymis. Anat Rec 193:293–311
   PubMedGoogle Scholar
• Mruk, D.D., Silvestrini, B., Mo, M.Y., and Cheng, C.Y. (2002) Antioxidant superoxide dismutase – a review: Its function, regulation in the testis, and role in male fertility. Contraception 65:305–11
   PubMed Web of Science ®Google Scholar
• Mupfiga, C., Fisher, D., Kruger, T., and Henkel, R. (2013) The relationship between seminal leukocytes, oxidative status in the ejaculate, and apoptotic markers in human spermatozoa. Syst Biol Reprod Med 59:304–11
   PubMed Web of Science ®Google Scholar
• Nayanatara, A.K., Nagaraja, H.S., Anupama, B.K. (2005) The effect of repeated swimming stress on organ weights and lipid peroxidation in rats. Thai J Pharm Sci 18:3–9
   Google Scholar
• Nenicu, A., Luers, G.H., Kovacs, W., David, M., Zimmer, A., Bergmann, M., et al. (2007) Peroxisomes in human and mouse testis: Differential expression of peroxisomal proteins in germ cells and distinct somatic cell types of the testis. Biol Reprod 77:1060–72
   PubMed Web of Science ®Google Scholar
• Nirupama, M., Devaki, M., Nirupama, R., and Yajurvedi, H.N. (2013) Chronic intermittent stress-induced alterations in the spermatogenesis and antioxidant status of the testis are irreversible in albino rat. J Physiol Biochem 69:59–68
   PubMed Web of Science ®Google Scholar
• Pacak, K., Palkovits, M., Yadid, G., Kvetnansky, R., Kopin, I.J., and Goldstein, D.S. (1998) Heterogeneous neurochemical responses to different stressors: A test of Selye’s doctrine of nonspecificity. Am J Physiol 275:R1247–55
   PubMed Web of Science ®Google Scholar
• Paglia, D.E., and Valentine, W.N. (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–69
   PubMed Web of Science ®Google Scholar
• Parodi, J. (2014) Motility, viability, and calcium in the sperm cells. Syst Biol Reprod Med 60:65–71
   PubMed Web of Science ®Google Scholar
• Priya, P.H., and Reddy, P.S. (2012) Effect of restraint stress on lead-induced male reproductive toxicity in rats. J Exp Zool A Ecol Genet Physiol 317:455–65
   PubMedGoogle Scholar
• Rivier, C., and Rivest, S. (1991) Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: Peripheral and central mechanisms. Biol Reprod 45:523–32
   PubMed Web of Science ®Google Scholar
• Sahin, E., and Gumuslu, S. (2007) Immobilization stress in rat tissues: Alterations in protein oxidation, lipid peroxidation and antioxidant defense system. Comp Biochem Physiol C Toxicol Pharmacol 144:342–7
   PubMed Web of Science ®Google Scholar
• Sapolsky, R.M., Romero, L.M., and Munck, A.U. (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89
   PubMed Web of Science ®Google Scholar
• Sepaniak, S., Forges, T., Fontaine, B., Gerard, H., Foliguet, B., Guillet-May, F., et al. (2004) [Negative impact of cigarette smoking on male fertility: From spermatozoa to the offspring]. J Gynecol Obstet Biol Reprod (Paris) 33:384–90
   PubMedGoogle Scholar
• Sies, H. (1997) Oxidative stress: Oxidants and antioxidants. Exp Physiol 82:291–5
   PubMed Web of Science ®Google Scholar
• Sikka, S.C. (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–62
   PubMed Web of Science ®Google Scholar
• Srivastava, R.K., Taylor, M.F., and Mann, D.R. (1993) Effect of immobilization stress on plasma luteinizing hormone, testosterone, and corticosterone concentrations and on 3 beta-hydroxysteroid dehydrogenase activity in the testes of adult rats. Proc Soc Exp Biol Med 204:231–5
   PubMed Web of Science ®Google Scholar
• Weir, C.P., and Robaire, B. (2007) Spermatozoa have decreased antioxidant enzymatic capacity and increased reactive oxygen species production during aging in the Brown Norway rat. J Androl 28:229–40
   PubMed Web of Science ®Google Scholar
• Woodward, C.J. and Emery, P.W. (1987) Determination of plasma corticosterone using high-performance liquid chromatography. J Chromatogr 419:280–4
   PubMed Web of Science ®Google Scholar
• Yavasoglu, A., Karaaslan, M.A., Uyanikgil, Y., Sayim, F., Ates, U., and Yavasoglu, N.U. (2008) Toxic effects of anatoxin-a on testes and sperm counts of male mice. Exp Toxicol Pathol 60:391–6
   PubMed Web of Science ®Google Scholar
• Zafir, A. and Banu, N. (2009) Induction of oxidative stress by restraint stress and corticosterone treatments in rats. Indian J Biochem Biophys 46:53–8
   PubMed Web of Science ®Google Scholar
• Zhou, Q., Nie, R., Prins, G.S., Saunders, P.T., Katzenellenbogen, B.S., and Hess, R.A. (2002) Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J Androl 23:870–81
   PubMed Web of Science ®Google Scholar
• Zhu, L.J., Hardy, M.P., Inigo, I.V., Huhtaniemi, I., Bardin, C.W., and Moo-Young, A.J. (2000) Effects of androgen on androgen receptor expression in rat testicular and epididymal cells: A quantitative immunohistochemical study. Biol Reprod 63:368–76
   PubMed Web of Science ®Google Scholar
• Zini, A. and Schlegel, P.N. (2003) Effect of hormonal manipulation on mRNA expression of antioxidant enzymes in the rat testis. J Urol 169:767–71
   PubMed Web of Science ®Google Scholar