Up-regulation of NDRG2 through nuclear factor-kappa B is required for Leydig cell apoptosis in both human and murine infertile testes

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 2, 2012, Pages 301-313

  Li, Teng ^a   Hu, Jing ^a   He, Gong Hao ^b   Li, Yun ^a   Zhu, Chu Chao ^a   Hou, Wu Gang ^a   Zhang, Shun ^a   Li, Wei ^a   Zhang, Jin Shan ^a   Wang, Zhe ^a   Liu, Xin Ping ^a   Yao, Li Bo ^a   Zhang, Yuan Qiang ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b KUNMING GENERAL HOSPITAL   (China)

Author keywords

Apoptosis; Infertile disease; Leydig cell; N myc downstream regulated gene 2; Nuclear factor kappa B; Pyrrolidine dithiocarbamate

Indexed keywords

CASPASE 3; CYTOPLASM PROTEIN; DIMETHANESULFONIC ACID; ETHANE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN NDRG2; PYRROLIDINE DITHIOCARBAMATE; SMALL INTERFERING RNA; SULFONIC ACID DERIVATIVE; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING SITE; CELL GROWTH; CELL NUCLEUS; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; GENE AMPLIFICATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; HYPOSPERMATOGENESIS; IMMUNOHISTOCHEMISTRY; LEYDIG CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SERTOLI CELL ONLY SYNDROME; SPERMATOGENESIS; TESTIS; TESTIS DISEASE; TESTOSTERONE BLOOD LEVEL; UPREGULATION;

ANIMALS; APOPTOSIS; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASM; HUMANS; INFERTILITY, MALE; LEYDIG CELLS; MALE; MESYLATES; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SERTOLI CELL-ONLY SYNDROME; SPERMATOGENESIS; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

MURINAE; RATTUS;

EID: 83655169780     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.11.013     Document Type: Article

References (46)

1. Ozawa N., Goda N., Makino N., Yamaguchi T., Yoshimura Y., Suematsu M. Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J. Clin. Invest. 2002, 109:457-467.
2. Rulli S.B., Ahtiainen P., Mäkelä S., Toppari J., Poutanen M., Huhtaniemi I. Elevated steroidogenesis, defective reproductive organs, and infertility in transgenic male mice overexpressing human chorionic gonadotropin. Endocrinology 2003, 144:4980-4990.
3. Kim S.K., Yoon Y.D., Park Y.S., Seo J.T., Kim J.H. Involvement of the Fas-Fas ligand system and active caspase-3 in abnormal apoptosis in human testes with maturation arrest and Sertoli cell-only syndrome. Fertil. Steril. 2007, 87:547-553.
4. Boekelheide K. Mechanisms of toxic damage to spermatogenesis. J. Natl. Cancer Inst. Monogr. 2005, 2005:6-8.
5. Gao H.B., Tong M.H., Hu Y.Q., Guo Q.S., Ge R., Hardy M.P. Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 2002, 143:130-138.
6. Sivakumar R., Sivaraman P.B., Mohan-Babu N., Jainul-Abideen I.M., Kalliyappan P., Balasubramanian K. Radiation exposure impairs luteinizing hormone signal transduction and steroidogenesis in cultured human leydig cells. Toxicol. Sci. 2006, 91:550-556.
7. Turner T.T., Bang H.J., Lysiak J.J. Experimental testicular torsion: reperfusion blood flow and subsequent testicular venous plasma testosterone concentrations. Urology 2005, 65:390-394.
8. Morris A.J., Taylor M.F., Morris I.D. Leydig cell apoptosis in response to ethane dimethanesulphonate after both in vivo and in vitro treatment. J. Androl. 1997, 18:274-280.
9. Taylor M.F., Woolveridge I., Metcalfe A.D., Streuli C.H., Hickman J.A., Morris I.D. Leydig cell apoptosis in the rat testes after administration of the cytotoxin ethane dimethanesulphonate: role of the Bcl-2 family members. J. Endocrinol. 1998, 157:317-326.
10. Taylor M.F., de Boer-Brouwer M., Woolveridge I., Teerds K.J., Morris I.D. Leydig cell apoptosis after the administration of ethane dimethanesulfonate to the adult male rat is a Fas-mediated process. Endocrinology 1999, 140:3797-3804.
11. Kim J.M., Luo L., Zirkin B.R. Caspase-3 activation is required for Leydig cell apoptosis induced by ethane dimethanesulfonate. Endocrinology 2000, 141:1846-1853.
12. Hou W.G., Zhao Y., Shen L., Zhao J., Liu X.W., Li Z., Liu X.P., Yao L.B., Zhang Y.Q. Differential expression of N-Myc downstream regulated gene 2 (NDRG2) in the rat testis during postnatal development. Cell Tissue Res. 2009, 337:257-267.
13. Hu X.L., Liu X.P., Deng Y.C., Lin S.X., Wu L., Zhang J., Wang L.F., Wang X.B., Li X., Shen L., Zhang Y.Q., Yao L.B. Expression analysis of the NDRG2 gene in mouse embryonic and adult tissues. Cell Tissue Res. 2006, 325:67-76.
14. Yao L., Zhang J., Liu X. NDRG2: a Myc-repressed gene involved in cancer and cell stress. Acta Biochim. Biophys. Sin. (Shanghai) 2008, 40:625-635.
15. Ma J.J., Liao C.G., Jiang X., Zhao H.D., Yao L.B., Bao T.Y. NDRG2 suppresses the proliferation of clear cell renal cell carcinoma cell A-498. J. Exp. Clin. Cancer. Res. 2010, 29:103.
16. Deng Y., Yao L., Chau L., Ng S.S., Peng Y., Liu X., Au W.S., Wang J., Li F., Ji S., Han H., Nie X., Li Q., Kung H.F., Leung S.Y., Lin M.C. N-Myc downstream-regulated gene 2 (NDRG2) inhibits glioblastoma cell proliferation. Int. J. Cancer 2003, 106:342-347.
17. Hu X.L., Liu X.P., Lin S.X., Deng Y.C., Liu N., Li X., Yao L.B. NDRG2 expression and mutation in human liver and pancreatic cancers. World J. Gastroenterol. 2004, 10:3518-3521.
18. Liu N., Wang L., Liu X., Yang Q., Zhang J., Zhang W., Wu Y., Shen L., Zhang Y., Yang A., Han H., Zhang J., Yao L. Promoter methylation, mutation, and genomic deletion are involved in the decreased NDRG2 expression levels in several cancer cell lines. Biochem. Biophys. Res. Commun. 2007, 358:164-169.
19. Lusis E.A., Watson M.A., Chicoine M.R., Lyman M., Roerig P., Reifenberger G., Gutmann D.H., Perry A. Integrative genomic analysis identifies NDRG2 as a candidate tumor suppressor gene frequently inactivated in clinically aggressive meningioma. Cancer Res. 2005, 65:7121-7126.
20. Park Y., Shon S.K., Kim A., Kim K.I., Yang Y., Cho D.H., Lee M.S., Lim J.S. SOCS1 induced by NDRG2 expression negatively regulates STAT3 activation in breast cancer cells. Biochem. Biophys. Res. Commun. 2007, 363:361-367.
21. Wang L., Liu N., Yao L., Li F., Zhang J., Deng Y., Liu J., Ji S., Yang A., Han H., Zhang Y., Zhang J., Han W., Liu X. NDRG2 is a new HIF-1 target gene necessary for hypoxia-induced apoptosis in A549 cells. Cell. Physiol. Biochem. 2008, 21:239-250.
22. Liu N., Wang L., Li X., Yang Q., Liu X., Zhang J., Zhang J., Wu Y., Ji S., Zhang Y., Yang A., Han H., Yao L. N-Myc downstream-regulated gene 2 is involved in p53-mediated apoptosis. Nucleic Acids Res. 2008, 36:5335-5349.
23. Choi S.C., Yoon S.R., Park Y.P., Song E.Y., Kim J.W., Kim W.H., Yang Y., Lim J.S., Lee H.G. Expression of NDRG2 is related to tumor progression and survival of gastric cancer patients through Fas-mediated cell death. Exp. Mol. Med. 2007, 39:705-714.
24. Kim A., Kim M.J., Yang Y., Kim J.W., Yeom Y.I., Lim J.S. Suppression of NF-kappa B activity by NDRG2 expression attenuates the invasive potential of highly malignant tumor cells. Carcinogenesis 2009, 30:927-936.
25. Kreuz S., Siegmund D., Rumpf J.J., Samel D., Leverkus M., Janssen O., Häcker G., Dittrich-Breiholz O., Kracht M., Scheurich P., Wajant H. NF-kappa B activation by Fas is mediated through FADD, caspase-8, and RIP and is inhibited by FLIP. J. Cell Biol. 2004, 166:369-380.
26. Wang Q., Gao H.B. Involvement of nuclear factor-kappa B on corticosterone-induced rat Leydig cell apoptosis. Asian J. Androl. 2006, 8:693-702.
27. Anniballo R., Ubaldi F., Cobellis L., Sorrentino M., Rienzi L., Greco E., Tesarik J. Criteria predicting the absence of spermatozoa in the Sertoli cell-only syndrome can be used to improve success rates of sperm retrieval. Hum. Reprod. 2000, 15:2269-2277.
28. Ilbey Y.O., Ozbek E., Simsek A., Cekmen M., Otunctemur A., Somay A. Chemoprotective effect of a nuclear factor-kappa B inhibitor, pyrrolidine dithiocarbamate, against cisplatin-induced testicular damage in rats. J. Androl. 2009, 30:505-514.
29. Zhao Y., Hou W.G., Zhu H.P., Zhao J., Wang R.A., Xu R.J., Zhang Y.Q. Expression of thyrotropin-releasing hormone receptors in rat testis and their role in isolated Leydig cells. Cell Tissue Res. 2008, 334:283-294.
30. Rommerts F.F., Kuhne L., van Cappellen G.W., Stocco D.M., King S.R., Jankowska A. Specific dose-dependent effects of ethane 1,2-dimethanesulfonate in rat and mouse Leydig cells and non-steroidogenic cells on programmed cell death. J. Endocrinol. 2004, 181:169-178.
31. Zang Y., He X.H., Xin W.J., Pang R.P., Wei X.H., Zhou L.J., Li Y.Y., Liu X.G. Inhibition of NF-kappa B prevents mechanical allodynia induced by spinal ventral root transection and suppresses the re-expression of Nav1.3 in DRG neurons in vivo and in vitro. Brain Res. 2010, 1363:151-158.
32. O' Shaughnessy P.J., Willerton L., Baker P.J. Changes in Leydig cell gene expression during development in the mouse. Biol. Reprod. 2002, 66:966-975.
33. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3:R0034.
34. Mestdagh P., Van Vlierberghe P., De Weer A., Muth D., Westermann F., Speleman F., Vandesompele J. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 2009, 10:R64.
35. Chung J.Y., Kim J.Y., Kim Y.J., Jung S.J., Park J.E., Lee S.G., Kim J.T., Oh S., Lee C.J., Yoon Y.D., Yoo Y.H., Kim J.M. Cellular defense mechanisms against benzo[a]pyrene in testicular Leydig cells: implications of p53, aryl-hydrocarbon receptor, and cytochrome P450 1A1 status. Endocrinology 2007, 148:6134-6144.
36. Furuta H., Kondo Y., Nakahata S., Hamasaki M., Sakoda S., Morishita K. NDRG2 is a candidate tumor-suppressor for oral squamous-cell carcinoma. Biochem. Biophys. Res. Commun. 2010, 391:1785-1791.
37. Shi H., Li N., Li S., Chen C., Wang W., Xu C., Zhang J., Jin H., Zhang H., Zhao H., Song W., Feng Q., Feng X., Shen X., Yao L., Zhao Q. Expression of NDRG2 in esophageal squamous cell carcinoma. Cancer Sci. 2010, 101:1292-1299.
38. Shi H., Jin H., Chu D., Wang W., Zhang J., Chen C., Xu C., Fan D., Yao L. Suppression of N-myc downstream-regulated gene 2 is associated with induction of Myc in colorectal cancer and correlates closely with differentiation. Biol. Pharm. Bull. 2009, 32:968-975.
39. Shon S.K., Kim A., Kim J.Y., Kim K.I., Yang Y., Lim J.S. Bone morphogenetic protein-4 induced by NDRG2 expression inhibits MMP-9 activity in breast cancer cells. Biochem. Biophys. Res. Commun. 2009, 385:198-203.
40. Mizuno K., Hayashi Y., Kojima Y., Nakane A., Tozawa K., Kohri K. Activation of NF-kappa B associated with germ cell apoptosis in testes of experimentally induced cryptorchid rat model. Urology 2009, 73:389-393.
41. Lysiak J.J., Bang H.J., Nguyen Q.A., Turner T.T. Activation of the nuclear factor kappa B pathway following ischemia-reperfusion of the murine testis. J. Androl. 2005, 26:129-135.
42. Pentikainen V., Suomalainen L., Erkkila K., Martelin E., Parvinen M., Pentikäinen M.O., Dunkel L. Nuclear factor-kappa B activation in human testicular apoptosis. Am. J. Pathol. 2002, 160:205-218.
43. Rasoulpour R.J., Boekelheide K. NF-kappa B is activated in the rat testis following exposure to mono-(2-ethylhexyl) phthalate. Biol. Reprod. 2005, 72:479-486.
44. Rasoulpour R.J., Boekelheide K. NF-kappa B activation elicited by ionizing radiation is proapoptotic in testis. Biol. Reprod. 2007, 76:279-285.
45. Hayden M.S., Ghosh S. Signaling to NF-κB. Genes Dev. 2004, 18:2195-2224.
46. Frank D., William H.W. Stage-specific nuclear expression of NF-kB in mammalian testis. Mol. Endocrinol. 1998, 12:1696-1707.