ARHI (DIRAS3) induces autophagy in ovarian cancer cells by downregulating the epidermal growth factor receptor, inhibiting PI3K and Ras/MAP signaling and activating the FOXo3a-mediated induction of Rab7

Cell Death and Differentiation

Volumn 21, Issue 8, 2014, Pages 1275-1289

  Lu, Z ^a   Yang, H ^a   Sutton, M N ^a   Yang, M ^a   Clarke, C H ^a   Liao, W S L ^a   Bast, R C ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; RAPAMYCIN; TRANSCRIPTION FACTOR FKHRL1; DIRAS3 PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; FORKHEAD TRANSCRIPTION FACTOR; FOXO3 PROTEIN, HUMAN; RAB PROTEIN; RAB7 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ARHI GENE; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CANCER CELL; CANCER GROWTH; CANCER SURVIVAL; CELL DEATH; CELL GROWTH; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; TUMOR SUPPRESSOR GENE; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CONFOCAL MICROSCOPY; GENETIC TRANSFECTION; GENETICS; METABOLISM; OVARY TUMOR; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

AUTOPHAGY; CELL PROLIFERATION; DOWN-REGULATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICROSCOPY, CONFOCAL; OVARIAN NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; RAB GTP-BINDING PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RHO GTP-BINDING PROTEINS; TRANSFECTION;

EID: 84905053713     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.48     Document Type: Article

References (48)

1. Cecconi F, Levine B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 2008; 15: 344-357.
2. Melendez A, Levine B. Autophagy in C. elegans. WormBook 2009; 24: 1-26.
3. Rosen DG, Wang L, Jain AN, Lu KH, Luo RZ, Yu Y et al. Expression of the tumor suppressor gene ARHI in epithelial ovarian cancer is associated with increased expression of p21WAF1/CIP1 and prolonged progression-free survival. Clin Cancer Res 2004; 10: 6559-6566.
4. Yu Y, Xu F, Peng H, Fang X, Zhao S, Li Y et al. NOEY2 (ARHI), an imprinted putative tumor suppressor gene in ovarian and breast carcinomas. Proc Natl Acad Sci USA 1999; 96: 214-219.
5. Luo RZ, Fang X, Marquez R, Liu SY, Mills GB, Liao WS et al. ARHI is a Ras-related small G-protein with a novel N-terminal extension that inhibits growth of ovarian and breast cancers. Oncogene 2003; 22: 2897-2909.
6. Lu Z, Luo RZ, Lu Y, Zhang X, Yu Q, Khare S et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J Clin Invest 2008; 118: 3917-3929.
7. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem 2009; 284: 28319-28331.
8. Hofler A, Nichols T, Grant S, Lingardo L, Esposito EA, Gridley S et al. Study of the PDK1/AKT signaling pathway using selective PDK1 inhibitors, HCS, and enhanced biochemical assays. Anal Biochem 2011; 414: 179-186.
9. Rosenberger G, Meien S, Kutsche K. Oncogenic HRAS mutations cause prolonged PI3K signaling in response to epidermal growth factor in fibroblasts of patients with Costello syndrome. Hum Mutat 2009; 30: 352-362.
10. Gremer L, De Luca A, Merbitz-Zahradnik T, Dallapiccola B, Morlot S, Tartaglia M et al. Duplication of Glu37 in the switch I region of HRAS impairs effector/GAP binding and underlies Costello syndrome by promoting enhanced growth factor-dependent MAPK and AKT activation. Hum Mol Genet 2010; 19: 790-802.
11. Clague MJ. Met receptor: a moving target. Sci Signal 2011; 4: pe40.
12. Jacob C, Cottrell GS, Gehringer D, Schmidlin F, Grady EF, Bunnett NW. c-Cbl mediates ubiquitination, degradation, and down-regulation of human protease-activated receptor 2. J Biol Chem 2005; 280: 16076-16087.
13. Tanowitz M, von Zastrow M. A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J Biol Chem 2003; 278: 45978-45986.
14. Futter CE, Collinson LM, Backer JM, Hopkins CR. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 2001; 155: 1251-1264.
15. Miranda A, Mickle A, Medda B, Zhang Z, Phillips RJ, Tipnis N et al. Altered mechanosensitive properties of vagal afferent fibers innervating the stomach following gastric surgery in rats. Neuroscience 2009; 162: 1299-1306.
16. Fang L, Wang H, Zhou L, Yu D. Akt-FOXO3a signaling axis dysregulation in human oral squamous cell carcinoma and potent efficacy of FOXO3a-targeted gene therapy. Oral Oncol 2011; 47: 16-21.
17. Chen J, Gomes AR, Monteiro LJ, Wong SY, Wu LH, Ng TT et al. Constitutively nuclear FOXO3a localization predicts poor survival and promotes Akt phosphorylation in breast cancer. PLoS One 2010; 5: e12293.
18. Yang JY, Zong CS, Xia W, Yamaguchi H, Ding Q, Xie X et al. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 2008; 10: 138-148.
19. Hu MC, Lee DF, Xia W, Golfman LS, Ou-Yang F, Yang JY et al. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 2004; 117: 225-237.
20. Plas DR, Thompson CB. Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J Biol Chem 2003; 278: 12361-12366.
21. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P et al. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 2004; 117(Part 20): 4837-4848.
22. Hariharan N, Maejima Y, Nakae J, Paik J, Depinho RA, Sadoshima J. Deacetylation of FoxO by Sirt1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ Res 2010; 107: 1470-1482.
23. Gutierrez MG, Munafo DB, Beron W, Colombo MI. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 2004; 117(Part 13): 2687-2697.
24. Thi EP, Lambertz U, Reiner NE. Class IA phosphatidylinositol 3-kinase p110alpha regulates phagosome maturation. PLoS One 2012; 7: e43668.
25. Lawe DC, Patki V, Heller-Harrison R, Lambright D, Corvera S. The FYVE domain of early endosome antigen 1 is required for both phosphatidylinositol 3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization. J Biol Chem 2000; 275: 3699-3705.
26. Nazio F, Strappazzon F, Antonioli M, Bielli P, Cianfanelli V, Bordi M et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol 2013; 15: 406-416.
27. Huang S, Yang ZJ, Yu C, Sinicrope FA. Inhibition of mTOR kinase by AZD8055 can antagonize chemotherapy-induced cell death through autophagy induction and down-regulation of p62/sequestosome 1. J Biol Chem 2011; 286: 40002-40012.
28. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J et al. ULK-ATG13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20: 1992-2003.
29. Su H, Gu Y, Li F, Wang Q, Huang B, Jin X et al. The PI3K/AKT/mTOR signaling pathway is overactivated in primary aldosteronism. PLoS One 2013; 8: e62399.
30. Chen J, Crawford R, Xiao Y. Vertical inhibition of the PI3K/Akt/mTOR pathway for the treatment of osteoarthritis. J Cell Biochem 2013; 114: 245-249.
31. Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 2008; 181: 497-510.
32. Zhou WJ, Deng R, Feng GK, Zhu XF. [A G-quadruplex ligand SYUIQ-5 induces autophagy by inhibiting the Akt-FOXO3a pathway in nasopharyngeal cancer cells]. Ai Zheng 2009; 28: 1049-1053.
33. Mukherjee S, Ray D, Lekli I, Bak I, Tosaki A, Das DK. Effects of Longevinex (modified resveratrol) on cardioprotection and its mechanisms of action. Can J Physiol Pharmacol 2010; 88: 1017-1025.
34. Ganley IG, Wong PM, Gammoh N, Jiang X. Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 2011; 42: 731-743.
35. Yang JY, Hung MC. Deciphering the role of forkhead transcription factors in cancer therapy. Curr Drug Targets 2011; 12: 1284-1290.
36. Lu M, Zhao Y, Xu F, Wang Y, Xiang J, Chen D. The expression and prognosis of FOXO3a and Skp2 in human ovarian cancer. Med Oncol 2012; 29: 3409-3415.
37. Wu X, Liang L, Dong L, Yu Z, Fu X. Effect of ARHI on lung cancer cell proliferation, apoptosis and invasion in vitro. Mol Biol Rep 2012; 40: 2671-2678.
38. Field JK, Liloglou T, Warrak S, Burger M, Becker E, Berlin K et al. Methylation discriminators in NSCLC identified by a microarray based approach. Int J Oncol 2005; 27: 105-111.
39. Li Y, Shi L, Han C, Wang Y, Yang J, Cao C et al. Effects of ARHI on cell cycle progression and apoptosis levels of breast cancer cells. Tumour Biol 2012; 33: 1403-1410.
40. Chen MY, Liao WS, Lu Z, Bornmann WG, Hennessey V, Washington MN et al. Decitabine and suberoylanilide hydroxamic acid (SAHA) inhibit growth of ovarian cancer cell lines and xenografts while inducing expression of imprinted tumor suppressor genes, apoptosis, G2/M arrest, and autophagy. Cancer 2011; 117: 4424-4438.
41. Janssen EA, Ovestad IT, Skaland I, Soiland H, Gudlaugsson E, Kjellevold KH et al. LOH at 1p31 (ARHI) and proliferation in lymph node-negative breast cancer. Cell Oncol 2009; 31: 335-343.
42. Chen Y, Zaman MS, Deng G, Majid S, Saini S, Liu J et al. MicroRNAs 221/222 and genistein-mediated regulation of ARHI tumor suppressor gene in prostate cancer. Cancer Prev Res (Phila) 2011; 4: 76-86.
43. Wang Y, Yu Q, Cho AH, Rondeau G, Welsh J, Adamson E et al. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 2005; 7: 748-760.
44. Hu YQ, Si LJ, Ye ZS, Lin ZH, Zhou JP. Inhibitory effect of ARHI on pancreatic cancer cells and NF-kappaB activity. Mol Med Rep 2013; 7: 1180-1184.
45. Yang H, Lu X, Qian J, Xu F, Hu Y, Yu Y et al. Imprinted tumor suppressor gene ARHI induces apoptosis correlated with changes in DNA methylation in pancreatic cancer cells. Mol Med Rep 2010; 3: 581-587.
46. Weber F, Aldred MA, Morrison CD, Plass C, Frilling A, Broelsch CE et al. Silencing of the maternally imprinted tumor suppressor ARHI contributes to follicular thyroid carcinogen-esis. J Clin Endocrinol Metab 2005; 90: 1149-1155.
47. Badgwell DB, Lu Z, Le K, Gao F, Yang M, Suh GK et al. The tumor-suppressor gene ARHI (DIRAS3) suppresses ovarian cancer cell migration through inhibition of the Stat3 and FAK/Rho signaling pathways. Oncogene 2011; 31: 68-79.
48. Voigt W. Sulforhodamine B assay and chemosensitivity. Methods Mol Med 2005; 110: 39-48.