Upregulation and nuclear translocation of testicular ghrelin protects differentiating spermatogonia from ionizing radiation injury

Cell Death and Disease

Volumn 5, Issue 5, 2014, Pages

  Li, W ^a   Zeng, Y ^b   Zhao, J ^a   Zhu, C J ^b   Hou, W G ^b   Zhang, S ^c  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Ghrelin; Ionizing radiation; Oxidative stress; p53; Spermatogonia

Indexed keywords

GHRELIN; PROTEIN P53; GHRELIN RECEPTOR; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE TRANSLOCATION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RADIATION INJURY; RADIATION PROTECTION; SIGNAL TRANSDUCTION; SPERMATOGONIUM; UPREGULATION; ACTIVE TRANSPORT; ANIMAL; APOPTOSIS; C57BL MOUSE; CELL CULTURE; CELL NUCLEUS; FEMALE; GENETICS; MALE INFERTILITY; METABOLISM; PATHOLOGY; RADIATION DOSE; RADIATION EXPOSURE; SPERMATOGENESIS; TESTIS; TIME;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; CELL NUCLEUS; CELLS, CULTURED; FEMALE; GHRELIN; INFERTILITY, MALE; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; RADIATION INJURIES; RADIATION TOLERANCE; RECEPTORS, GHRELIN; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; TESTOSTERONE; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84907958756     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.223     Document Type: Article

References (45)

1. Aly HA, Azhar AS. Methoxychlor induced biochemical alterations and disruption of spermatogenesis in adult rats. Reprod Toxicol 2013; 40: 8-15.
2. Wan HT, Mruk DD, Wong CK, Cheng CY. Targeting testis-specific proteins to inhibit spermatogenesis: lesson from endocrine disrupting chemicals. Expert Opin Ther Targets 2013; 17: 839-855.
3. Wang DH, Hu JR, Wang LY, Hu YJ, Tan FQ, Zhou H et al. The apoptotic function analysis of p53, Apaf1, Caspase3 and Caspase7 during the spermatogenesis of the Chinese fire-bellied newt Cynops orientalis. PLoS One 2012; 7: e39920.
4. Bujan L, Walschaerts M, Moinard N, Hennebicq S, Saias J, Brugnon F et al. Impact of chemotherapy and radiotherapy for testicular germ cell tumors on spermatogenesis and sperm DNA: a multicenter prospective study from the CECOS network. Fertil Steril 2013; 100: 673-680.
5. Maiorino M, Ursini F. Oxidative stress, spermatogenesis and fertility. Biol Chem 2002; 383: 591-597.
6. Turner TT, Lysiak JJ. Oxidative stress: a common factor in testicular dysfunction. J Androl 2008; 29: 488-498.
7. Rasoulpour RJ, Boekelheide K. NF-kappaB activation elicited by ionizing radiation is proapoptotic in testis. Biol Reprod 2007; 76: 279-285.
8. Xu G, Vogel KS, McMahan CA, Herbert DC, Walter CA. BAX and tumor suppressor TRP53 are important in regulating mutagenesis in spermatogenic cells in mice. Biol Reprod 2010; 83: 979-987.
9. Otala M, Suomalainen L, Pentikainen MO, Kovanen P, Tenhunen M, Erkkila K et al. Protection from radiation-induced male germ cell loss by sphingosine-1-phosphate. Biol Reprod 2004; 70: 759-767.
10. Garcia MC, Lopez M, Alvarez CV, Casanueva F, Tena-Sempere M, Dieguez C. Role of ghrelin in reproduction. Reproduction 2007; 133: 531-540.
11. Gaytan F, Barreiro ML, Caminos JE, Chopin LK, Herington AC, Morales C et al. Expression of ghrelin and its functional receptor, the type 1a growth hormone secretagogue receptor, in normal human testis and testicular tumors. J Clin Endocrinol Metab 2004; 89: 400-409.
12. Barreiro ML, Gaytan F, Caminos JE, Pinilla L, Casanueva FF, Aguilar E et al. Cellular location and hormonal regulation of ghrelin expression in rat testis. Biol Reprod 2002; 67: 1768-1776.
13. Tena-Sempere M, Barreiro ML, Gonzalez LC, Gaytan F, Zhang FP, Caminos JE et al. Novel expression and functional role of ghrelin in rat testis. Endocrinology 2002; 143: 717-725.
14. Zhu CC, Zhang H, Zhang JS, Li Z, Zhao J, Li W et al. Inhibition of ghrelin signaling improves the reproductive phenotype of male ob/ob mouse. Fertil Steril 2013; 99: 918-926.
15. Tena-Sempere M. Ghrelin and reproduction: ghrelin as novel regulator of the gonadotropic axis. Vitam Horm 2008; 77: 285-300.
16. Kheradmand A, Dezfoulian O, Alirezaei M. Ghrelin regulates Bax and PCNA but not Bcl-2 expressions following scrotal hyperthermia in the rat. Tissue Cell 2012; 44: 308-315.
17. Barreiro ML, Gaytan F, Castellano JM, Suominen JS, Roa J, Gaytan M et al. Ghrelin inhibits the proliferative activity of immature Leydig cells in vivo and regulates stem cell factor messenger ribonucleic acid expression in rat testis. Endocrinology 2004; 145: 4825-4834.
18. Filipponi D, Hobbs RM, Ottolenghi S, Rossi P, Jannini EA, Pandolfi PP et al. Repression of kit expression by Plzf in germ cells. Mol Cell Biol 2007; 27: 6770-6781.
19. Barrios F, Filipponi D, Campolo F, Gori M, Bramucci F, Pellegrini M et al. SOHLH1 and SOHLH2 control Kit expression during postnatal male germ cell development. J Cell Sci 2012; 125(Pt 6): 1455-1464.
20. Goldberg E, Eddy EM, Duan C, Odet F. LDHC: the ultimate testis-specific gene. J Androl 2010; 31: 86-94.
21. Shah FJ, Tanaka M, Nielsen JE, Iwamoto T, Kobayashi S, Skakkebaek NE et al. Gene expression profiles of mouse spermatogenesis during recovery from irradiation. Reprod Biol Endocrinol 2009; 7: 130.
22. Zhang S, Li W, Zhu C, Wang X, Li Z, Zhang J et al. Sertoli cell-specific expression of metastasis-associated protein 2 (MTA2) is required for transcriptional regulation of the follicle-stimulating hormone receptor (FSHR) gene during spermatogenesis. J Biol Chem 2012; 287: 40471-40483.
23. Li Y, Huang Y, Piao Y, Nagaoka K, Watanabe G, Taya K et al. Protective effects of nuclear factor erythroid 2-related factor 2 on whole body heat stress-induced oxidative damage in the mouse testis. Reprod Biol Endocrinol 2013; 11: 23.
24. Coureuil M, Ugolin N, Tavernier M, Chevillard S, Barroca V, Fouchet P et al. Puma and Trail/Dr5 pathways control radiation-induced apoptosis in distinct populations of testicular progenitors. PLoS One 2010; 5: e12134.
25. Wu R, Dong W, Zhou M, Zhang F, Marini CP, Ravikumar TS et al. Ghrelin attenuates sepsis-induced acute lung injury and mortality in rats. Am J Respir Crit Care Med 2007; 176: 805-813.
26. Cetin E, Kanbur M, Cetin N, Eraslan G, Atasever A. Hepatoprotective effect of ghrelin on carbon tetrachloride-induced acute liver injury in rats. Regul Pept 2011; 171: 1-5.
27. Colpi GM, Contalbi GF, Nerva F, Sagone P, Piediferro G. Testicular function following chemo-radiotherapy. Eur J Obstet Gynecol Reprod Biol 2004; 113(Suppl 1): S2-S6.
28. Rasoulpour T, DiPalma K, Kolvek B, Hixon M. Akt1 suppresses radiation-induced germ cell apoptosis in vivo. Endocrinology 2006; 147: 4213-4221.
29. Meistrich ML, Kangasniemi M. Hormone treatment after irradiation stimulates recovery of rat spermatogenesis from surviving spermatogonia. J Androl 1997; 18: 80-87.
30. Li T, Hu J, He GH, Li Y, Zhu CC, Hou WG et al. Up-regulation of NDRG2 through nuclear factor-kappa B is required for Leydig cell apoptosis in both human and murine infertile testes. Biochim Biophys Acta 2012; 1822: 301-313.
31. Zhang L, Tang J, Haines CJ, Feng HL, Lai L, Teng X et al. c-kit and its related genes in spermatogonial differentiation. Spermatogenesis 2011; 1: 186-194.
32. Hou Y, An J, Hu XR, Sun BB, Lin J, Xu D et al. Ghrelin inhibits interleukin-8 production induced by hydrogen peroxide in A549 cells via NF-kappaB pathway. Int Immunopharmacol 2009; 9: 120-126.
33. Xu Z, Lin S, Wu W, Tan H, Wang Z, Cheng C et al. Ghrelin prevents doxorubicin-induced cardiotoxicity through TNF-alpha/NF-kappaB pathways and mitochondrial protective mechanisms. Toxicology 2008; 247: 133-138.
34. Zwirska-Korczala K, Adamczyk-Sowa M, Sowa P, Pilc K, Suchanek R, Pierzchala K et al. Role of leptin, ghrelin, angiotensin II and orexins in 3T3 L1 preadipocyte cells proliferation and oxidative metabolism. J Physiol Pharmacol 2007; 58(Suppl 1): 53-64.
35. El Eter E, Al Tuwaijiri A, Hagar H, Arafa M. In vivo and in vitro antioxidant activity of ghrelin: Attenuation of gastric ischemic injury in the rat. J Gastroenterol Hepatol 2007; 22: 1791-1799.
36. Aitken RJ, Roman SD. Antioxidant systems and oxidative stress in the testes. Adv Exp Med Biol 2008; 636: 154-171.
37. Yang B, Sun H, Li W, Zhu C, Jian B, Hou W et al. Expression of Rap1 during germ cell development in the rat and its functional implications in 2-methoxyacetic acid-induced spermatocyte apoptosis. Urology 2013; 81: 696 e691-696 e698.
38. Beumer TL, Roepers-Gajadien HL, Gademan IS, van Buul PP, Gil-Gomez G, Rutgers DH et al. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 1998; 5: 669-677.
39. Porteiro B, Diaz-Ruiz A, Martinez G, Senra A, Vidal A, Serrano M et al. Ghrelin requires p53 to stimulate lipid storage in fat and liver. Endocrinology 2013; 154: 3671-3679.
40. Velasquez DA, Martinez G, Romero A, Vazquez MJ, Boit KD, Dopeso-Reyes IG et al. The central Sirtuin 1/p53 pathway is essential for the orexigenic action of ghrelin. Diabetes 2011; 60: 1177-1185.
41. Kaushal N, Bansal MP. Selenium variation induced oxidative stress regulates p53 dependent germ cell apoptosis: plausible involvement of HSP70-2. Eur J Nutr 2009; 48: 221-227.
42. 2 in vitro. FEBS J 2009; 276: 870-881.
43. Zhang S, Zeng Y, Qu J, Luo Y, Wang X, Li W. Endogenous EGF maintains Sertoli germ cell anchoring junction integrity and is required for early recovery from acute testicular ischemia/reperfusion injury. Reproduction 2013; 145: 177-189.
44. Liang Y, Dong Y, Zhao J, Li W. YES1 activation elicited by heat stress is anti-apoptotic in mouse pachytene spermatocytes. Biol Reprod 2013; 89: 131.
45. Ray SK, Schaecher KE, Shields DC, Hogan EL, Banik NL. Combined TUNEL and double immunofluorescent labeling for detection of apoptotic mononuclear phagocytes in autoimmune demyelinating disease. Brain Res Brain Res Protoc 2000; 5: 305-311.