Beta-carotene prevents the spermatogenic disorders induced by exogenous scrotal hyperthermia through modulations of oxidative stress, apoptosis, and androgen biosynthesis in mice |
Yon, Jung-Min
(College of Veterinary Medicine, Chungbuk National University)
Kim, Jae Seung (College of Veterinary Medicine, Chungbuk National University) Lin, Chunmei (College of Chinese Medicinal Materials, Jilin Agricultural University) Park, Seul Gi (College of Veterinary Medicine, Chungbuk National University) Gwon, Lee Wha (College of Veterinary Medicine, Chungbuk National University) Lee, Jong-Geol (College of Veterinary Medicine, Chungbuk National University) Baek, In-Jeoung (Asan Institute for Life Sciences, University of Ulsan College of Medicine) Nahm, Sang-Seop (College of Veterinary Medicine, Konkuk University) Nam, Sang-Yoon (College of Veterinary Medicine, Chungbuk National University) |
1 | Cai H, Ren Y, Li XX, Yang JL, Zhang CP, Chen M, Fan CH, Hu XQ, Hu ZY, Gao F, Liu YX. Scrotal heat stress causes a transient alteration in tight junctions and induction of TGF- expression. Int J Androl 2011;34:352-362. DOI |
2 | Choi KS, Bae MK, Jeong JW, Moon HE, Kim KW. Hypoxia-induced angiogenesis during carcinogenesis. J Biochem Mol Biol 2003;36:120-127. |
3 | Gorlach A, Bonello S. The cross-talk between NF-kappaB and HIF-1: further evidence for a significant liaison. Biochem J 2008;412:e17-e19. DOI |
4 | Turk G, Ceribasi AO, Sakin F, Sonmez M, Atessahin A. Antiperoxidative and anti-apoptotic effects of lycopene and ellagic acid on cyclophosphamide-induced testicular lipid peroxidation and apoptosis. Reprod Fertil Dev 2010;22:587-596. DOI |
5 | Rizk SM, Zaki HF, Mina MA. Propolis attenuates doxorubicininduced testicular toxicity in rats. Food Chem Toxicol 2014;67:176-186. DOI |
6 | Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 2009;80:913-919. DOI |
7 | Reyes JG, Farias JG, Henriquez-Olavarrieta S, Madrid E, Parraga M, Zepeda AB, Moreno RD. The hypoxic testicle: physiology and pathophysiology. Oxid Med Cell Longev 2012;2012:929285. |
8 | Durairajanayagam D, Agarwal A, Ong C. Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online 2015;30:14-27. DOI |
9 | Aktas C, Kanter M. A morphological study on Leydig cells of scrotal hyperthermia applied rats in short-term. J Mol Histol 2009;40:31-39. DOI |
10 | Troiano L, Fustini MF, Lovato E, Frasoldati A, Malorni W, Capri M, Grassilli E, Marrama P, Franceschi C. Apoptosis and spermatogenesis: evidence from an in vivo model of testosterone withdrawal in the adult rat. Biochem Biophys Res Commun 1994;202:1315-1321. DOI |
11 | Tapanainen JS, Tilly JL, Vihko KK, Hsueh AJ. Hormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors. Mol Endocrinol 1993;7:643-650. DOI |
12 | Krinsky NI, Johnson EJ. Carotenoid actions and their relation to health and disease. Mol Aspects Med 2005;26:459-516. DOI |
13 | Monsen ER. Dietary reference intakes for the antioxidant nutrients: vitamin C, vitamin E, selenium, and carotenoids. J Am Diet Assoc 2000;100:637-640. DOI |
14 | Suarez EC, Schramm-Sapyta NL. Race differences in the relation of vitamins A, C, E, and -carotene to metabolic and inflammatory biomarkers. Nutr Res 2014;34:1-10. DOI |
15 | Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Adv Exp Med Biol 2008;636:154-171. DOI |
16 | Park SG, Yon JM, Lin C, Gwon LW, Lee JG, Baek IJ, Lee BJ, Yun YW, Nam SY. Capsaicin attenuates spermatogenic cell death induced by scrotal hyperthermia through its antioxidative and anti-apoptotic activities. Andrologia 2017;49:e12656. DOI |
17 | Bai SK, Lee SJ, Na HJ, Ha KS, Han JA, Lee H, Kwon YG, Chung CK, Kim YM. Beta-carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redox-based NF-kappaB activation. Exp Mol Med 2005;37:323-334. DOI |
18 | El-Missiry MA, Shalaby F. Role of beta-carotene in ameliorating the cadmium-induced oxidative stress in rat brain and testis. J Biochem Mol Toxicol 2000;14:238-243. DOI |
19 | Usta C, Ozdemir S, Schiariti M, Puddu PE. The pharmacological use of ellagic acid-rich pomegranate fruit. Int J Food Sci Nutr 2013;64:907-913. DOI |
20 | Jung KY, Lin C, Yon JM, Jung AY, Park SG, Chu SB, Gwon LW, Nam SY. Postnatal expression profiles of phospholipid hydroperoxide glutathione peroxidase in spermatogenesis in mice. Turk J Vet Anim Sci 2016;40:40-46. DOI |
21 | Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408. DOI |
22 | Lin C, Yon JM, Jung AY, Lee JG, Jung KY, Kang JK, Lee BJ, Yun YW, Nam SY. Resveratrol prevents nicotine-induced teratogenesis in cultured mouse embryos. Reprod Toxicol 2012;34:340-346. DOI |
23 | Warr N, Greenfield A. The molecular and cellular basis of gonadal sex reversal in mice and humans. Wiley Interdiscip Rev Dev Biol 2012;1:559-577. DOI |
24 | Muciaccia B, Boitani C, Berloco BP, Nudo F, Spadetta G, Stefanini M, de Rooij DG, Vicini E. Novel stage classification of human spermatogenesis based on acrosome development. Biol Reprod 2013;89:60. DOI |
25 | Gu W, Hecht NB. Developmental expression of glutathione peroxidase, catalase, and manganese superoxide dismutase mRNAs during spermatogenesis in the mouse. J Androl 1996;17:256-262. |
26 | Turk G, Atessahin A, Sonmez M, Ceribasi AO, Yuce A. Improvement of cisplatin-induced injuries to sperm quality, the oxidant-antioxidant system, and the histologic structure of the rat testis by ellagic acid. Fertil Steril 2008;89 Suppl:1474-1481. DOI |
27 | Setchell BP. The Parkes Lecture. Heat and the testis. J Reprod Fertil 1998;114:179-194. DOI |
28 | Blackshaw AW, Massey PF. The effect of cryptorchidism on the quantitative histology, histochemistry and hydrolytic enzyme activity of the rat testis. Aust J Biol Sci 1978;31:53-64. DOI |
29 | Wang C, Cui YG, Wang XH, Jia Y, Sinha Hikim A, Lue YH, Tong JS, Qian LX, Sha JH, Zhou ZM, Hull L, Leung A, Swerdloff RS. transient scrotal hyperthermia and levonorgestrel enhance testosterone-induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab 2007;92:3292-3304. DOI |
30 | Ren L, Medan MS, Ozu M, Li C, Watanabe G, Taya K. Effects of experimental cryptorchidism on sperm motility and testicular endocrinology in adult male rats. J Reprod Dev 2006;52:219-228. DOI |
31 | Ikeda M, Kodama H, Fukuda J, Shimizu Y, Murata M, Kumagai J, Tanaka T. Role of radical oxygen species in rat testicular germ cell apoptosis induced by heat stress. Biol Reprod 1999;61:393-399. DOI |
32 | Jung KY, Yon JM, Lin C, Jung AY, Lee JG, Baek IJ, Lee BJ, Yun YW, Nam SY. Phospholipid hydroperoxide glutathione peroxidase is involved in the maintenance of male fertility under cryptorchidism in mice. Reprod Toxicol 2015;57:73-80. DOI |
33 | Anton E. Arrested apoptosis without nuclear fragmentation produced by efferent duct ligation in round spermatids and multinucleated giant cells of rat testis. Reproduction 2003;125:879-887. DOI |
34 | Sheynkin Y, Welliver R, Winer A, Hajimirzaee F, Ahn H, Lee K. Protection from scrotal hyperthermia in laptop computer users. Fertil Steril 2011;95:647-651. DOI |
35 | Pino JA, Osses N, Oyarzun D, Farias JG, Moreno RD, Reyes JG. Differential effects of temperature on reactive oxygen/ nitrogen species production in rat pachytene spermatocytes and round spermatids. Reproduction 2013;145:203-212. DOI |
36 | Chowdhury AK, Steinberger E. Early changes in the germinal epithelium of rat testes following exposure to heat. J Reprod Fertil 1970;22:205-212. DOI |
37 | Eisenberg ML, Lipshultz LI. Varicocele-induced infertility: newer insights into its pathophysiology. Indian J Urol 2011;27:58-64. DOI |
38 | Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, Foresta C. Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod 2013;28:877-885. DOI |
39 | Ivell R. Lifestyle impact and the biology of the human scrotum. Reprod Biol Endocrinol 2007;5:15. DOI |
40 | Shiraishi K, Takihara H, Matsuyama H. Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress-mediated apoptosis. World J Urol 2010;28:359-364. DOI |