Involvement of endoplasmic reticulum stress in apoptosis of testicular cells induced by low-dose radiation

Journal of Huazhong University of Science and Technology - Medical Science

Volumn 33, Issue 4, 2013, Pages 551-558

  Wang, Zhi Cheng ^a   Wang, Jian Feng ^a   Li, Yan Bo ^a,b   Guo, Cai Xia ^b   Liu, Yang ^a   Fang, Fang ^a   Gong, Shou Liang ^a  

^a Center for Radiological Research   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

apoptosis; endoplasmic reticulum stress; low dose radiation; signaling pathway; testicular cells

Indexed keywords

ANIMAL; APOPTOSIS; ARTICLE; ENDOPLASMIC RETICULUM STRESS; MALE; MOUSE; PHYSIOLOGY; RADIATION; RADIATION EXPOSURE; TESTIS;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; MALE; MICE; RADIATION; TESTIS;

EID: 84881289908     PISSN: 16720733     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11596-013-1157-0     Document Type: Article

References (47)

1. Feinendegen LE. Evidence for beneficial low level radiation effects and radiation hormesis. Br J Radiol, 2005,78(925):3-7
2. Cai L. Research of the adaptive response induced by low-dose radiation: where have we been and where should we go? Hum Exp Toxicol, 1999,18(7):419-425
3. Lee SJ, Choi SA, Cho CK, et al. Adaptive response is differently induced depending on the sensitivity to radiation-induced cell death in mouse epidermal cells. Cell Biol Toxicol, 2000,16(3):175-184
4. Gong SL, Liu SC, Liu JX, et al. Adaptive response of thymocyte apoptosis and cell cycle progression induced by low dose X-ray irradiation in mice. Biomed Environ Sci, 2000,13(3):180-188
5. Joksic G, Petrović S. Lack of adaptive response of human lymphocytes exposed in vivo to low doses of ionizing radiation. J Environ Pathol Toxicol Oncol, 2004, 23(3):195-206
6. Scott BR. Low-dose-radiation stimulated natural chemical and biological protection against lung cancer. Dose Response, 2008,6(3):299-318
7. Cheng GH, Wu N, Jiang DF, et al. Increased levels of p53 and PARP-1 in EL-4 cells probably related with the immune adaptive response induced by low dose ionizing radiation in vitro. Biomed Environ Sci, 2010,23(6):487-495
8. Liu G, Gong P, Zhao H, et al. Effect of low-level radiation on the death of male germ cells. Radiat Res, 2006,165(4):379-389
9. Liu G, Gong P, Bernstein LR, et al. Apoptotic cell death induced by low-dose radiation in male germ cells: hormesis and adaptation. Crit Rev Toxicol, 2007,37(7): 587-605
10. Hamer G, Gademan IS, Kal HB, et al. Role for c-Abl and p73 in the radiation response of male germ cells. Oncogene, 2001,20(32):4298-4304
11. Koji T, Hishikawa Y. Germ cell apoptosis and its molecular trigger in mouse testes. Arch Histol Cytol, 2003,66(1):1-16
12. Sinha Hikim AP, Lue Y, Diaz-Romero M, et al. Deciphering the pathways of germ cell apoptosis in the testis. J Steroid Biochem Mol Biol, 2003,85(2-5):175-182
13. Richburg JH. The relevance of spontaneous- and chemically-induced alterations in testicular germ cell apoptosis to toxicology. Toxicol Lett, 2000,112-113:79-86
14. Cisternas P, Moreno RD. Comparative analysis of apoptotic pathways in rat, mouse, and hamster spermatozoa. Mol Reprod De, 2006,73(10):1318-1325
15. Stambolsky P, Weisz L, Shats I, et al. Regulation of AIF expression by p53. Cell Death Differ, 2006,13(12): 2140-2149
16. Morales E, Ferrer C, Zuasti A, et al. Apoptosis and mo lecular pathways in the seminiferous epithelium of aged and photoinhibited Syrian hamsters (Mesocricetus auratus). J Androl, 2007,28(1):123-135
17. Bozec A, Chuzel F, Chater S, et al. The mitochondrial-dependent pathway is chronically affected in testicular germ cell death in adult rats in utero to anti-androgens. J Endocrinol, 2004,183(1):79-90
18. Harding HP, Calfon M, Urano F, et al. Transcriptional and translational control in the mammalian unfolded protein response. Annu Rev Cell Dev Biol, 2002, 18:575-599
19. Schröder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res, 2005,569(1-2):29-63
20. Li XD, Lankinen H, Putkuri N, et al. Tula hantavirus triggers pro-apoptotic signals of ER stress in Vero E6 cells. Virology, 2005,333(1):180-189
21. Schröder M. Endoplasmic reticulum stress responses. Cell Mol Life Sci, 2008, 65(6):862-894
22. Rao RV, Bredesen DE. Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Curr Opin Cell Biol, 2004,16(6):653-662
23. Wu HC, Chiu CS, Wu JL, et al. Zebrafish antiapoptotic protein zfBcl-xL can block betanodavirus protein alpha-induced mitochondria-mediated secondary necrosis cell death. Fish Shellfish Immunol, 2008,24(4):436-449
24. Austin RC. The unfolded protein response in health and disease. Antioxid Redox Signal, 2009,11(9):2279-2287
25. Rasheva VI, Domingos PM. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis, 2009,14(8):996-1007
26. Rutkowski DT, Wu J, Back SH, et al. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell, 2008,15(6):829-840
27. Wang G, Yang ZQ, Zhang K. Endoplasmic reticulum stress response in cancer: molecular mechanism and therapeutic potential. Am J Transl Res, 2010,2(1):65-74
28. Lai E, Teodoro T, Volchuk A. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda), 2007,22:193-201
29. Li Y, Guo C, Wang Z, et al. Enhanced effects of TRAIL-endostatin-based double-gene-radiotherapy on suppressing growth, promoting apoptosis and inducing cell cycle arrest in vascular endothelial cells. J Huazhong Univ Sci Technolog [Med Sci], 2012,32(2):167-172
30. Liu JF, Yang WH, Fong YC, et al. BFPP, a phloroglucinol derivative, induces cell apoptosis in human chondrosarcoma cells through endoplasmic reticulum stress. Biochem Pharmacol, 2010,79(10):1410-1417
31. van der Sanden MH, Houweling M, van Golde LM, et al. Inhibition of phosphatidylcholine synthesis induces expression of the endoplasmic reticulum stress and apoptosis-related protein CCAAT/enhancer-binding protein-homologous protein (CHOP/GADD153). Biochem J, 2003,369(Pt 3):643-650
32. Zhang Y, Liu W, Ma C, et al. Endoplasmic reticulum stress contributes to CRH-induced hippocampal neuron apoptosis. Exp Cell Res, 2012,318(6):732-740
33. Zhu H, Zhu H, Xiao S, et al. Activation and crosstalk between the endoplasmic reticulum road and JNK pathway in ischemia-reperfusion brain injury. Acta Neurochir (Wien), 2012,154(7):1197-1203
34. Lee AS. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem, 2001,26(8): 504-510
35. Lambrot R, Coffigny H, Pairault C, et al. High radiosensitivity of germ cells in human male fetus. J Clin Endocrinol Metab, 2007,92(7):2632-2639
36. Nagamori I, Yomogida K, Ikawa M, et al. The testes-specific bZip type transcription factor Tisp40 plays a role in ER stress responses and chromatin packaging during spermiogenesis. Genes Cells, 2006,11(10):1161-1171
37. Tabuchi Y, Takasaki I, Kondo T. Identification of genetic networks involved in the cell injury accompanying endoplasmic reticulum stress induced by bisphenol A in testicular Sertoli cells. Biochem Biophys Res Commun, 2006,345(3):1044-1050
38. Zhao Y, Tan Y, Dai J, et al. Exacerbation of diabetes-induced testicular apoptosis by zinc deficiency is most likely associated with oxidative stress, p38 MAPK activation, and p53 activation in mice. Toxicol Lett, 2011,200(1-2):100-106
39. Xue X, Piao JH, Nakajima A, et al. Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem, 2005,280(40):33917-33925
40. Asahi J, Kamo H, Baba R, et al. Bisphenol A induces endoplasmic reticulum stress-associated apoptosis in mouse non-parenchymal hepatocytes. Life Sci, 2010,87(13-14):431-438
41. Harding HP, Zhang Y, Zeng H, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell, 2003, 11(3):619-633
42. Bergner A, Huber RM. Regulation of the endoplasmic reticulum Ca(2+)-store in cancer. Anticancer Agents Med Chem, 2008,8(7):705-709
43. Brostrom MA, Brostrom CO. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium, 2003,34(4-5):345-363
44. Dragosits M, Stadlmann J, Graf A, et al. The response to unfolded protein is involved in osmotolerance of Pichia pastoris. BMC Genomic, 2010,11:207
45. Kadowaki H, Nishitoh H, Ichijo H. Survival and apoptosis signals in ER stress: the role of protein kinases. J Chem Neuroanatomy, 2004,28(1-2):93-100
46. Raven JF, Koromilas AE. PERK and PKR: old kinases learn new tricks. Cell Cycle, 2008, 7(9):1146-1150
47. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest, 2005,115(10):2656-2564