ARHI (DIRAS3)-mediated autophagy-associated cell death enhances chemosensitivity to cisplatin in ovarian cancer cell lines and xenografts

Cell Death and Disease

Volumn 6, Issue , 2015, Pages

  Washington, M N ^a   Suh, G ^a   Orozco, A F ^a   Sutton, M N ^a   Yang, H ^a   Wang, Y ^a   Mao, W ^a   Millward, S ^a   Ornelas, A ^a   Atkinson, N ^a   Liao, W ^a   Bast, R C ^a   Lu, Z ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CHLOROQUINE; CISPLATIN; DOXYCYCLINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; X LINKED INHIBITOR OF APOPTOSIS; AGFG1 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; BCL2 PROTEIN, HUMAN; DIRAS3 PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN; MAPK1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NUCLEOPORIN; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RIPK3 PROTEIN, HUMAN; RNA BINDING PROTEIN; XIAP PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARHI GENE; ARTICLE; AUTOPHAGY; CANCER CELL; CELL DEATH; CHEMOSENSITIVITY; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; ENZYME ACTIVATION; FEMALE; G1 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN CLEAVAGE; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OVARIAN NEOPLASMS; PATHOLOGY; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; CASPASE 3; CELL LINE, TUMOR; CHLOROQUINE; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NUCLEAR PORE COMPLEX PROTEINS; OVARIAN NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASES; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RECEPTOR, ERBB-2; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RHO GTP-BINDING PROTEINS; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84938893568     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.208     Document Type: Article

References (49)

1. Klionsky DJ. Autophagy. Curr Biol 2005; 15: R282-R283.
2. Levine B, Kroemer G. Autophagy in aging, disease and death: the true identity of a cell death impostor. Cell Death Differ 2009; 16: 1-2.
3. Fayaz SM, Suvanish Kumar VS, Rajanikant GK. Necroptosis: who knew there were so many interesting ways to die CNS Neurol Disord Drug Targets 2014; 13: 42-51.
4. Ch'en IL, Tsau JS, Molkentin JD, Komatsu M, Hedrick SM. Mechanisms of necroptosis in T cells. J Exp Med 2011; 208: 633-641.
5. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402: 672-676.
6. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 2003; 100: 15077-15082.
7. Huang S, Yang ZJ, Yu C, Sinicrope FA. Inhibition of mTOR kinase by AZD8055 can antagonize chemotherapy-induced cell death through autophagy induction and downregulation of p62/sequestosome 1. J Biol Chem 2011; 286: 40002-40012.
8. Corcelle EA, Puustinen P, Jaattela M. Apoptosis and autophagy: targeting autophagy signalling in cancer cells-'trick or treats'? FEBS J 2009; 276: 6084-6096.
9. Budillon A, Carbone C, Di Gennaro E. Tissue transglutaminase: a new target to reverse cancer drug resistance. Amino Acids 2013; 44: 63-72.
10. Aredia F, Scovassi AI. Manipulation of autophagy in cancer cells: an innovative strategy to fight drug resistance. Future Med Chem 2013; 5: 1009-1021.
11. Hisatomi H, Nagao K, Wakita K, Kohno N. ARHI/NOEY2 inactivation may be important in breast tumor pathogenesis. Oncology 2002; 62: 136-140.
12. Huang S, Chang IS, Lin W, Ye W, Luo RZ, Lu Z et al. ARHI (DIRAS3), an imprinted tumour suppressor gene, binds to importins and blocks nuclear import of cargo proteins. Biosci Rep 2010; 30(3): 159-168.
13. 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.
14. 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.
15. Lu Z, Yang H, Sutton MN, Yang M, Clarke CH, Liao WS et al. 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 Differ 2014; 21: 1275-1289.
16. 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.
17. Feng W, Marquez RT, Lu Z, Liu J, Lu KH, Issa JP et al. Imprinted tumor suppressor genes ARHI and PEG3 are the most frequently down-regulated in human ovarian cancers by loss of heterozygosity and promoter methylation. Cancer 2008; 112: 1489-1502.
18. Lu Z, Luo RZ, Peng H, Huang M, Nishmoto A, Hunt KK et al. E2F-HDAC complexes negatively regulate the tumor suppressor gene ARHI in breast cancer. Oncogene 2006; 25: 230-239.
19. 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.
20. Lu Z, Baquero MT, Yang H, Yang M, Reger AS, Kim C et al. DIRAS3 regulates the autophagosome initiation complex in dormant ovarian cancer cells. Autophagy 2014; 10: 1071-1092.
21. Bast RC Jr., Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nat Rev Cancer 2009; 9: 415-428.
22. Bast RC Jr., Skates S, Lokshin A, Moore RG. Differential diagnosis of a pelvic mass: improved algorithms and novel biomarkers. Int J Gynecol Cancer 2012; 22(Suppl 1): S5-S8.
23. Ziebarth AJ, Nowsheen S, Steg AD, Shah MM, Katre AA, Dobbin ZC et al. Endoglin (CD105) contributes to platinum resistance and is a target for tumor-specific therapy in epithelial ovarian cancer. Clin Cancer Res 2013; 19: 170-182.
24. Chen X, Wu Y, Dong H, Zhang CY, Zhang Y. Platinum-based agents for individualized cancer treatment. Curr Mol Med 2013; 13: 1603-1612.
25. Itamochi H, Nishimura M, Oumi N, Kato M, Oishi T, Shimada M et al. Checkpoint kinase inhibitor AZD7762 overcomes cisplatin resistance in clear cell carcinoma of the ovary. Int J Gynecol Cancer 2014; 24: 61-69.
26. Zhang J, Kan Y, Tian Y, Wang Z, Zhang J. Effects of poly (ADP-ribosyl) polymerase (PARP) inhibitor on cisplatin resistance & proliferation of the ovarian cancer C13 cells. Indian J Med Res 2013; 137: 527-532.
27. 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.
28. Locatelli SL, Cleris L, Stirparo GG, Tartari S, Saba E, Pierdominici M et al. BIM upregulation and ROS-dependent necroptosis mediate the antitumor effects of the HDACi Givinostat and Sorafenib in Hodgkin lymphoma cell line xenografts. Leukemia 2014; 28: 1861-1871.
29. Roca FJ, Ramakrishnan L. TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 2013; 153: 521-534.
30. Bell BD, Leverrier S, Weist BM, Newton RH, Arechiga AF, Luhrs KA et al. FADD and caspase-8 control the outcome of autophagic signaling in proliferating T cells. Proc Natl Acad Sci USA 2008; 105: 16677-16682.
31. Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C, Martin-Chouly C, Le Moigne-Muller G, Van Herreweghe F et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ 2012; 19: 2003-2014.
32. Lu Z, Luo RZ, Peng H, Rosen DG, Atkinson EN, Warneke C et al. Transcriptional and posttranscriptional down-regulation of the imprinted tumor suppressor gene ARHI (DRAS3) in ovarian cancer. Clin Cancer Res 2006; 12: 2404-2413.
33. Yuan J, Luo RZ, Fujii S, Wang L, Hu W, Andreeff M et al. Aberrant methylation and silencing of ARHI, an imprinted tumor suppressor gene in which the function is lost in breast cancers. Cancer Res 2003; 63: 4174-4180.
34. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 2000; 1: 489-495.
35. Xiao Y, Li H, Zhang J, Volk A, Zhang S,WeiWet al. TNF-Alpha/Fas-RIP-1-induced cell death signaling separates murine hematopoietic stem cells/progenitors into 2 distinct populations. Blood 2011; 118: 6057-6067.
36. Bao JJ, Le XF, Wang RY, Yuan J, Wang L, Atkinson EN et al. Reexpression of the tumor suppressor gene ARHI induces apoptosis in ovarian and breast cancer cells through a caspase-independent calpain-dependent pathway. Cancer Res 2002; 62: 7264-7272.
37. Li J, Cui G, Sun L, Wang SJ, Tian S, Guan Z et al. ARHI overexpression induces epithelial ovarian cancer cell apoptosis and excessive autophagy. Int J Gynecol Cancer 2014; 24: 437-443.
38. Yang TQ, Lu XJ, Wu TF, Ding DD, Zhao ZH, Chen GL et al. MicroRNA-16 inhibits glioma cell growth and invasion through suppression of BCL2 and the nuclear factor-kappaB1/MMP9 signaling pathway. Cancer Sci 2014; 105: 265-271.
39. Gryko M, Pryczynicz A, Zareba K, Kedra B, Kemona A, Guzinska-Ustymowicz K. The expression of Bcl-2 and BID in gastric cancer cells. J Immunol Res 2014; 2014: 953203.
40. Heinicke U, Fulda S. Chemosensitization of rhabdomyosarcoma cells by the histone deacetylase inhibitor SAHA. Cancer Lett 2014; 351: 50-58.
41. Pedersen IM, Kitada S, Schimmer A, Kim Y, Zapata JM, Charboneau L et al. The triterpenoid CDDO induces apoptosis in refractory CLL B cells. Blood 2002; 100: 2965-2972.
42. Xu W, Ngo L, Perez G, Dokmanovic M, Marks PA. Intrinsic apoptotic and thioredoxin pathways in human prostate cancer cell response to histone deacetylase inhibitor. Proc Natl Acad Sci USA 2006; 103: 15540-15545.
43. Klingauf M, Beck M, Berge U, Turgay Y, Heinzer S, Horvath P et al. The tumour suppressor DiRas3 interacts with C-RAF and downregulates MEK activity to restrict cell migration. Biol Cell 2013; 105: 91-107.
44. Ma J, Wan J, Meng J, Banerjee S, Ramakrishnan S, Roy S. Methamphetamine induces autophagy as a pro-survival response against apoptotic endothelial cell death through the Kappa opioid receptor. Cell Death Dis 2014; 5: e1099.
45. Peppard JV, Rugg C, Smicker M, Dureuil C, Ronan B, Flamand O et al. Identifying small molecules which inhibit autophagy: a phenotypic screen using image-based high-content cell analysis. Curr Chem Genom Transl Med 2014; 8: 3-15.
46. Chen Y, Zaman MS, Deng G, Majid S, Saini S, Liu J et al. MicroRNAs 221/222 and genisteinmediated regulation of ARHI tumor suppressor gene in prostate cancer. Cancer Prev Res (Phila) 2011; 4: 76-86.
47. Dalai I, Missiaglia E, Barbi S, Butturini G, Doglioni C, Falconi M et al. Low expression of ARHI is associated with shorter progression-free survival in pancreatic endocrine tumors. Neoplasia 2007; 9: 181-183.
48. 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 carcinogenesis. J Clin Endocrinol Metab 2005; 90: 1149-1155.
49. Huang J, Lin Y, Li L, Qing D, Teng XM, Zhang YL et al. ARHI, as a novel suppressor of cell growth and downregulated in human hepatocellular carcinoma, could contribute to hepatocarcinogenesis. Mol Carcinog 2009; 48: 130-140.