Expression of Hypoxia-Inducible Factor-1α and Association with Cu/Zn Superoxide Dismutase in the Reproductive Tract Tissues of Adult Male Roe Deer (Capreolus capreolus) During the Reproduction Season

Aitken R.J. (2002). Active oxygen in spermatozoa during epididymal transit. In: The epididymis from molecules to clinical practice, Robaire B., Hinton B.T. (eds). Springer, Boston, MA, pp. 435–447.10.1007/978-1-4615-0679-9_25Search in Google Scholar

Aitken R.J., Vernet P. (1998). Maturation of redox regulatory mechanisms in the epididymis. J. Reprod. Fertil., Suppl., 53: 109–118.Search in Google Scholar

Aitken R.J., Roman S.D. (2008). Antioxidant systems and oxidative stress in the testes. In: Molecular mechanisms in spermatogenesis, advances in experimental medicine and biology, Cheng Y.C. (ed). Landes Bioscience, Springer Science Business Media, Boston, MA, USA, 636: 154–171.Search in Google Scholar

Allen J.A., Diemer T., Janus P., Hales K.H., Hales D.B. (2004). Bacterial endotoxin lipopolysaccharide and reactive oxygen species inhibit Leydig cell steroidogenesis via perturbation of mitochondria. Endocrine, 25: 265–275.10.1385/ENDO:25:3:265Open DOISearch in Google Scholar

Bradford M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 7: 248–254.10.1016/0003-2697(76)90527-3Open DOISearch in Google Scholar

Chabory E., Damon C., Lenoir A., Henry-Berger J., Vernet P., Cadet R., Saez F., Drevet J.R. (2010). Mammalian glutathione peroxidases control acquisition and maintenance of spermatozoa integrity. J. Anim. Sci., 88: 1321–1331.10.2527/jas.2009-2583Open DOISearch in Google Scholar

Chandel N.S., Mc Clintock D.S., Feliciano C.E., Wood T.M., Melendez J.A., Rodriguez A.M., Schumacker P.T. (2000). Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1 alpha during hypoxia: a mechanism of O₂ sensing. J. Biol. Chem., 275: 25130–25138.Search in Google Scholar

Chomczynski P., Sacchi N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162: 156–159.Search in Google Scholar

de Lamirande E., Leduc B.E., Iwasaki A., Hassouna M., Gagnon C. (1995). Increased reactive oxygen species formation in semen of patients with spinal cord injury. Fertil. Steril., 63: 637–642.Search in Google Scholar

Fisher H.M., Aitken R.J. (1997). Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J. Exp. Zool., 277: 390–400.Search in Google Scholar

Georgiou M., Perkins L.M., Payne A.H. (1987). Steroid synthesis-dependent, oxygen-mediated damage of mitochondrial and microsomal cytochrome P-450 enzymes in rat Leydig cell cultures. Endocrinology, 121: 1390–1399.Search in Google Scholar

Goeritz F., Quest M., Wagener A., Fassbender M., Broich A., Hildebrandt T.B., Hofmann R.R., Blottner S. (2003). Seasonal timing of sperm production in roe deer: inter-relationship between changes in ejaculate parameters, morphology and function of testis and accessory glands. Theriogenology, 59: 1487–1502.Search in Google Scholar

Hall P.F. (1994). Testicular steroid synthesis: organization and regulation. In: The Physiology of Reproduction, Knobil E., Neill J.D. (eds). Raven Press, New York, 1: 1335–1362.Search in Google Scholar

Hanukoglu I. (2006). Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab. Rev., 38: 171–196.Search in Google Scholar

Hanukoglu I., Rapoport R., Weiner L., Sklan D. (1993). Electron leakage from the mitochondrial NADPH-adrenodoxin reductase-adrenodoxin-P450_scc (cholesterol side chain cleavage) system. Arch. Biochem. Biophys., 305: 489–498.Search in Google Scholar

Hinton B.T., Palladino M.A., Rudolph D.B., Lan Z.J., Labus J.C. (1996). The role of the epididymis in the protection of spermatozoa. Curr. Top. Dev. Biol., 33: 61–102.Search in Google Scholar

Klonisch T., Schön J., Hombach-Klonisch S., Blottner S. (2006). The roe deer as a model for studying seasonal regulation of testis function. Int. J. Androl., 29: 122–128.10.1111/j.1365-2605.2005.00603.xOpen DOISearch in Google Scholar

Kormano M. (1968). Microvasculature structure of the rat epididymis. Ann. Med. Exp. Fenn., 46: 113–118.Search in Google Scholar

Kozioł K., Koziorowski M. (2013). Steroid hormones in peripheral blood plasma and androgen receptors in testis and epididymis of roe deer male (Capreolus capreolus) during the reproduction season. Small Rumin. Res., 115: 86–93.10.1016/j.smallrumres.2013.09.008Open DOISearch in Google Scholar

Koziorowska-Gilun M., Gilun P., Fraser L., Koziorowski M., Kordan W., Stefanczyk-Krzymowska S. (2013). Antioxidant enzyme activity and mRNA expression in reproductive tract of adult male European bison (Bison bonasus, Linnaeus 1758). Reprod. Domest. Anim., 48: 7–14.10.1111/j.1439-0531.2012.02015.xOpen DOISearch in Google Scholar

Koziorowska-Gilun M., Fraser L., Gilun P., Koziorowski M., Kordan W. (2015). Activity of antioxidant enzymes and their mRNA expression in reproductive tract tissues of the male roe deer (Capreolus capreolus) during pre-rut and rut season. Small Rumin. Res., 129: 97–103.Search in Google Scholar

Lysiak J.J., Kirby J.L., Tremblay J.J., Woodson R.I., Reardon M.A., Palmer L.A., Turner T.T. (2009). Hypoxia-inducible factor-1alpha is constitutively expressed in murine Leydig cells and regulates 3beta-hydroxysteroid dehydrogenase type 1 promoter activity. J. Androl., 2: 146–156.Search in Google Scholar

Marti H.H., Katschinski D.M., Wagner K.F., Schaffer L., Stier B., Wenger RH. (2002). Isoform-specific expression of hypoxia-inducible factor-1alpha during the late stages of mouse spermiogenesis. Mol. Endocrinol., 16: 234–243.Search in Google Scholar

Martinez-Pastor F., Guerra C., Kaabi M., Garcia-Macias V., de Paz P., Alvarez M., Herraez P., Anel L. (2005). Season effect on genitalia and epididymal sperm from Iberian red deer, roe deer and Cantabrian chamois. Theriogenology, 63: 1857–1875.10.1016/j.theriogenology.2004.08.006Open DOISearch in Google Scholar

Maxwell P.H. (2005). Hypoxia-inducible factor as a physiological regulator. Exp. Physiol., 90: 791–797.10.1113/expphysiol.2005.030924Open DOISearch in Google Scholar

Michiels C., Minet E., Mottet D., Raes M. (2002). Regulation of gene expression by oxygen: NF-kappaB and HIF-1, two extremes. Free Radic. Biol. Med., 33: 1231–1242.Search in Google Scholar

Palladino M.A., Powell J.D., Korah N., Hermo L. (2004). Expression and localization of hypoxia-inducible factor-1 subunits in the adult rat epididymis. Biol. Reprod., 70: 1121–1130.Search in Google Scholar

Perry A.C., Jones R., Hall L. (1993). Isolation and characterization of a rat cDNA clone encoding a secreted superoxide dismutase reveals the epididymis to be a major site of its expression. Biochem. J., 293: 21–25.Search in Google Scholar

Powell J.D., Elshtein R., Forest D.J., Palladino M.A. (2002). Stimulation of hypoxiainducible factor-1 alpha (HIF-1alpha) protein in the adult rat testis following ischemic injury occurs without an increase in HIF-1alpha messenger RNA expression. Biol. Reprod., 67: 995–1002.Search in Google Scholar

Roelants H., Schneider F., Goritz F., Streich J., Blottner S. (2002). Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c-kit receptor, in relation to follicle-stimulating hormone, luteinizing hormone, and testosterone. Biol. Reprod., 67: 305–312.Search in Google Scholar

Schön J., Blottner S. (2009). Seasonal variations in the epididymis of the roe deer (Capreolus capreolus). Anim. Reprod. Sci., 111: 344–352.Search in Google Scholar

Schroedl C., Mc Clintock D.S., Budinger G.R., Chandel N.S. (2002). Hypoxic but not anoxic stabilization of HIF-1alpha requires mitochondrial reactive oxygen species. Am. J. Physiol. Lung. Cell Mol. Physiol., 283: 922–931.Search in Google Scholar

Semenza G.L. (1999). Regulation of mammalian O₂ homeostasis by hypoxia inducible factor 1. Annu. Rev. Cell. Dev. Biol., 15: 551–578.10.1146/annurev.cellbio.15.1.551Open DOISearch in Google Scholar

Semenza G.L. (2000). Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem. Pharmacol., 59: 47–53.Search in Google Scholar

Setchel B.P., Waites G.M., (1964). Blood flow and the uptake of glucose and oxygen in the testis and epididymis of the ram. J. Physiol., 171: 411–425.Search in Google Scholar

Setchell B.P. (2002). Innervation and vasculature of the excurrent duct system. In: The epididymis: from molecules to clinical practice, Robaire B., Hinton B.T. (eds). Kluwer Academic/Plenum Publishers, New York, USA, 1: 35–48.Search in Google Scholar

Sikka S.C. (2004). Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J. Androl., 1: 5–18.Search in Google Scholar

Vernet P., Aitken R.J., Drevet J.R. (2004). Antioxidant strategies in the epididymis. Mol. Cell. Endocrinol., 216: 31–39.Search in Google Scholar

Wang M., Kirk J.S., Venkatataraman S., Domann F.E., Zhang H.J., Schafer F.Q., Flanagan S.W., Weydert C.J., Spitz D.R., Buettner G.R., Oberley L.W. (2005). Manganese superoxide dismutase suppresses hypoxic induction of hypoxia-inducible factor-1alpha and vascular endothelial growth factor. Oncogene, 24: 8154–8166.Search in Google Scholar

Wenger R.H. (2002). Cellular adaptation to hypoxia: O₂-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O₂-regulated gene expression. Faseb. J., 16: 1151–1162.Search in Google Scholar

Zhao S., Fernald R. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol., 12: 1045–1062.10.1089/cmb.2005.12.1047271621616241897Open DOISearch in Google Scholar