Oxidative metabolism drives inflammation-induced platinum resistance in human ovarian cancer

Cell Death and Differentiation

Volumn 23, Issue 9, 2016, Pages 1542-1554

  Matassa, D S ^a   Amoroso, M R ^a   Lu, H ^b   Avolio, R ^a   Arzeni, D ^a   Procaccini, C ^c   Faicchia, D ^a   Maddalena, F ^d   Simeon, V ^d   Agliarulo, I ^a   Zanini, E ^b   Mazzoccoli, C ^d   Recchi, C ^b   Stronach, E ^b   Marone, G ^a   Gabra, H ^b   Matarese, G ^a   Landriscina, M ^d,e   Esposito, F ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c CNR   (Italy)

^d REFERRAL CANCER CENTER OF BASILICATA   (Italy)

^e UNIVERSITY OF FOGGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BIOLOGICAL MARKER; CASPASE 3; CASPASE 7; CHAPERONE; CISPLATIN; INTERLEUKIN 6; INTERLEUKIN 8; METFORMIN; MULTIDRUG RESISTANCE PROTEIN 1; OLIGOMYCIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED PROTEIN 1; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN 90; IMMEDIATE EARLY PROTEIN; PROTEIN SERINE THREONINE KINASE; SERUM-GLUCOCORTICOID REGULATED KINASE; SMALL INTERFERING RNA; TRAP1 PROTEIN, HUMAN;

AEROBIC METABOLISM; APOPTOSIS; ARTICLE; BIOENERGY; CANCER GROWTH; CANCER PROGNOSIS; CANCER STAGING; CELL METABOLISM; CELL VIABILITY ASSAY; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; GENE SILENCING; GLYCOLYSIS; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INFLAMMATION; MITOCHONDRIAL RESPIRATION; OUTCOME ASSESSMENT; OVARY CANCER; OVERALL SURVIVAL; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR CELL; UPREGULATION; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DISEASE FREE SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENETICS; METABOLISM; MORTALITY; OVARY TUMOR; PATHOLOGY; RNA INTERFERENCE; TUMOR CELL LINE;

ATP-BINDING CASSETTE, SUB-FAMILY B, MEMBER 1; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GLYCOLYSIS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMEDIATE-EARLY PROTEINS; INFLAMMATION; INTERLEUKIN-6; INTERLEUKIN-8; METFORMIN; OVARIAN NEOPLASMS; OXIDATIVE PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84969730632     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2016.39     Document Type: Article

References (56)

1. Haq R, Shoag J, Reu-Perez P, Yokoyama S, Edelman H, Rowe GC et al. Oncogenic BRAF regulates oxidative metabolism via PGC1? and MITF. Cancer Cell 2013; 23: 302-315.
2. Vazquez F, Lim JH, Chim H, Bhalla K, Girnun G, Pierce K et al. PGC1? expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 2013; 23: 287-301.
3. LeBleu VS, O'Connell JT, Gonzalez Herrera KN, Wikman H, Pantel K, Haigis MC et al. PGC-1alpha mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol 2014; 16: 992-1003.
4. Tan AS, Baty JW, Dong LF, Bezawork-Geleta A, Endaya B, Goodwin J et al. Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab 2015; 21: 81-94.
5. Yang L, Moss T, Mangala LS, Marini J, Zhao H, Wahlig S et al. Metabolic shifts toward glutamine regulate tumor growth, invasion and bioenergetics in ovarian cancer. Mol Syst Biol 2014; 10: 728.
6. Pastò A, Bellio C, Pilotto G, Ciminale V, Silic-Benussi M, Guzzo G et al. Cancer stem cells from epithelial ovarian cancer patients privilege oxidative phosphorylation, resist glucose deprivation. Oncotarget 2014; 5: 4305-4319.
7. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014; 64: 364.
8. Costantino E, Maddalena F, Calise S, Piscazzi A, Tirino V, Fersini A et al. TRAP1, a novel mitochondrial chaperone responsible for multi-drug resistance and protection from apoptotis in human colorectal carcinoma cells. Cancer Lett 2009; 279: 39-46.
9. Megger DA, Bracht T, Kohl M, Ahrens M, Naboulsi W, Weber F et al. Proteomic differences between hepatocellular carcinoma and nontumorous liver tissue investigated by a combined gel-based and label-free quantitative proteomics study. Mol Cell Proteomics 2013; 12: 2006-2020.
10. Agorreta J, Hu J, Liu D, Delia D, Turley H, Ferguson DJ et al. TRAP1 regulates proliferation, mitochondrial function, has prognostic significance in NSCLC. Mol Cancer Res 2014; 12: 660-669.
11. Leav I, Plescia J, Goel HL, Li J, Jiang Z, Cohen RJ et al. Cytoprotective mitochondrial chaperone TRAP-1 as a novel molecular target in localized and metastatic prostate cancer. Am J Pathol 2010; 176: 393-401.
12. Condelli V, Piscazzi A, Sisinni L, Matassa DS, Maddalena F, Lettini G et al. TRAP1 is involved in BRAF regulation and downstream attenuation of ERK phosphorylation and cell-cycle progression: a novel target for BRAF-mutated colorectal tumors. Cancer Res 2014; 74: 6693-6704.
13. Condelli V, Maddalena F, Sisinni L, Lettini G, Matassa DS, Piscazzi A et al. Targeting TRAP1 as a downstream effector of BRAF cytoprotective pathway: a novel strategy for human BRAF-driven colorectal carcinoma. Oncotarget 2015; 6: 22298-22309.
14. Maddalena F, Sisinni L, Lettini G, Condelli V, Matassa DS, Piscazzi A et al. Resistance to paclitxel in breast carcinoma cells requires a quality control of mitochondrial antiapoptotic proteins by TRAP1. Mol Oncol 2013; 7: 895-906.
15. Sisinni L, Maddalena F, Lettini G, Condelli V, Matassa DS, Esposito F et al. TRAP1 role in endoplasmic reticulum stress protection favors resistance to anthracyclins in breast carcinoma cells. Int J Oncol 2014; 44: 573-582.
16. Caino MC, Chae YC, Vaira V, Ferrero S, Nosotti M, Martin NM et al. Metabolic stress regulates cytoskeletal dynamics and metastasis of cancer cells. J Clin Invest 2013; 123: 2907-2920.
17. Agliarulo I, Matassa DS, Amoroso MR, Maddalena F, Sisinni L, Sepe L et al. TRAP1 controls cell migration of cancer cells in metabolic stress conditions: correlations with AKT/p70S6K pathways. Biochim Biophys Acta 2015; 1853: 2570-2579.
18. Yoshida S, Tsutsumi S, Muhlebach G, Sourbier C, Lee MJ, Lee S et al. Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis. Proc Natl Acad Sci USA 2013; 110: 1604-1612.
19. Moreno-Sánchez R, Rodríguez-Enríquez S, Marín-Hernández A, Saavedra E. Energy metabolism in tumor cells. FEBS J 2007; 274: 1393-1418.
20. Rasola A, Neckers L, Picard D. Mitochondrial oxidative phosphorylation TRAP(1)ped in tumor cells. Trends Cell Biol 2014; 24: 455-463.
21. Sciacovelli M, Guzzo G, Morello V, Frezza C, Zheng L, Nannini N et al. The mitochondrial chaperone TRAP1 promotes neoplastic growth by inhibiting succinate dehydrogenase. Cell Metab 2013; 17: 988-999.
22. Aust S, Bachmayr-Heyda A, Pateisky P, Tong D, Darb-Esfahani S, Denkert C et al. Role of TRAP1 and estrogen receptor alpha in patients with ovarian cancer-a study of the OVCAD consortium. Mol Cancer 2012; 11: 69.
23. Matassa DS, Amoroso MR, Maddalena F, Landriscina M, Esposito F. New insights into TRAP1 pathway. Am J Cancer Res 2012; 2: 235-248.
24. Langdon SP, Lawrie SS, Hay FG, Hawkes MM, McDonald A, Hayward IP et al. Characterization and properties of nine human ovarian adenocarcinoma cell lines. Cancer Res 1988; 48: 6166-6172.
25. Hjerpe E, Egyhazi Brage S, Carlson J, Frostvik Stolt M, Schedvins K, Johansson H et al. Metabolic markers GAPDH, PKM2, ATP5B and BEC-index in advanced serous ovarian cancer. BMC Clin Pathol 2013; 13: 30.
26. Owen MR, Doran E, Halestrap AP. Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 2000; 348 (Pt 3): 607-614.
27. Lengyel E, Litchfield LM, Mitra AK, Nieman KM, Mukherjee A, Zhang Y et al. Metformin inhibits ovarian cancer growth and increases sensitivity to paclitaxel in mouse models. Am J Obstet Gynecol 2015; 212: 479.e10.
28. Vogel CF, Khan EM, Leung PS, Gershwin ME, Chang WL, Wu D et al. Cross-talk between aryl hydrocarbon receptor and the inflammatory response: a role for nuclear factor-?B. J Biol Chem 2014; 289: 1866-1875.
29. Coutinho AE, Chapman KE. The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol Cell Endocrinol 2011; 335: 2-13.
30. Son DS, Kabir SM, Dong YL, Lee E, Adunyah SE. Inhibitory effect of tumor suppressor p53 on proinflammatory chemokine expression in ovarian cancer cells by reducing proteasomal degradation of I?B. PLoS One 2012; 7: e51116.
31. Valencia T, Kim JY, Abu-Baker S, Moscat-Pardos J, Ahn CS, Reina-Campos M et al. Metabolic reprogramming of stromal fibroblasts through p62-mTORC1 signaling promotes inflammation and tumorigenesis. Cancer Cell 2014; 26: 121-135.
32. Stronach EA, Cunnea P, Turner C, Guney T, Aiyappa R, Senthuran Jeyapalan S et al. The role of Interleukin-8 (IL-8) and IL-8 receptors in platinum response in high grade serous ovarian carcinoma. Oncotarget 2015; 6: 31593-31603.
33. Walker G, MacLeod K, Williams AR, Cameron DA, Smyth JF, Langdon SP. Estrogenregulated gene expression predicts response to endocrine therapy in patients with ovarian cancer. Gynecol Oncol 2007; 106: 461-468.
34. O'Donnell AJ, Macleod KG, Burns DJ, Smyth JF, Langdon SP. Estrogen receptor-alpha mediates gene expression changes and growth response in ovarian cancer cells exposed to estrogen. Endocr Relat Cancer 2005; 12: 851-866.
35. Wang TH, Chan YH, Chen CW, Kung WH, Lee YS, Wang ST et al. Paclitaxel (Taxol) upregulates expression of functional interleukin-6 in human ovarian cancer cells through multiple signaling pathways. Oncogene 2006; 25: 4857-4866.
36. Stronach EA, Alfraidi A, Rama N, Datler C, Studd JB, Agarwal R et al. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Res 2011; 71: 4412-4422.
37. Patch AM, Christie EL, Etemadmoghadam D, Garsed DW, George J, Fereday S et al. Wholegenome characterization of chemoresistant ovarian cancer. Nature 2015; 521: 489-494.
38. Binkhathlan Z, Lavasanifar A. P-glycoprotein inhibition as a therapeutic approach for overcoming multidrug resistance in cancer: current status and future perspectives. Curr Cancer Drug Targets 2013; 13: 326-346.
39. Xu M, Li L, Liu Z, Jiao Z, Xu P, Kong X et al. ABCB2 (TAP1) as the downstream target of SHH signaling enhances pancreatic ductal adenocarcinoma drug resistance. Cancer Lett 2013; 333: 152-158.
40. Vaughan S, Coward JI, Bast RC Jr, Berchuck A, Berek JS, Brenton JD et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 2011; 11: 719-725.
41. Lengyel E, Burdette JE, Kenny HA, Matei D, Pilrose J, Haluska P et al. Epithelial ovarian cancer experimental models. Oncogene 2014; 33: 3619-3633.
42. Montesano Gesualdi N, Chirico G, Pirozzi G, Costantino E, Landriscina M, Esposito F. Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress 2007; 10: 342-350.
43. Landriscina M, Laudiero G, Maddalena F, Amoroso MR, Piscazzi A, Cozzolino F et al. Mitochondrial chaperone Trap1 and the calcium binding protein Sorcin interact and protect cells against apoptosis induced by antiblastic agents. Cancer Res 2010; 70: 6577-6586.
44. Amoroso MR, Matassa DS, Sisinni L, Lettini G, Landriscina M, Esposito F. TRAP1 revisited: novel localizations and functions of a 'next-generation' biomarker (review). Int J Oncol 2014; 45: 969-977.
45. Matassa DS, Amoroso MR, Agliarulo I, Maddalena F, Sisinni L, Paladino S et al. Translational control in the stress adaptive response of cancer cells: a novel role for the heat shock protein TRAP1. Cell Death Dis 2013; 4: e851.
46. Matassa DS, Agliarulo I, Amoroso MR, Maddalena F, Sepe L, Ferrari MC et al. TRAP1-dependent regulation of p70S6K is involved in the attenuation of protein synthesis and cell migration: relevance in human colorectal tumors. Mol Oncol 2014; 8: 1482-1494.
47. Amoroso MR, Matassa DS, Laudiero G, Egorova AV, Polishchuk RS, Maddalena F et al. TRAP1 and the proteasome regulatory particle TBP7/Rpt3 interact in the endoplasmic reticulum and control cellular ubiquitination of specific mitochondrial proteins. Cell Death Differ 2012; 19: 592-604.
48. Matassa DS, Arzeni D, Landriscina M, Esposito F. ER stress protection in cancer cells: the multifaceted role of the heat shock protein TRAP1. Endoplasmic Reticulum Stress Dis 2014; 1 ISSN (Online) 2300-4266.
49. Viale A, Corti D, Draetta GF. Tumors and mitochondrial respiration: a neglected connection. Cancer Res 2015; 75: 3685-3686.
50. Duan Z, Lamendola DE, Penson RT, Kronish KM, Seiden MV. Overexpression of IL-6 but not IL-8 increases paclitaxel resistance of U-2OS human osteosarcoma cells. Cytokine 2002; 17: 234-242.
51. Poth KJ, Guminski AD, Thomas GP, Leo PJ, Jabbar IA, Saunders NA. Cisplatin treatment induces a transient increase in tumorigenic potential associated with high Interleukin-6 expression in head and neck squamous cell carcinoma. Mol Cancer Ther 2010; 9: 2430-2439.
52. Cohen S, Bruchim I, Graiver D, Evron Z, Oron-Karni V, Pasmanik-Chor M et al. Platinumresistance in ovarian cancer cells is mediated by IL-6 secretion via the increased expression of its target cIAP-2. J Mol Med (Berl) 2013; 91: 357-368.
53. Browne A, Sriraksa R, Guney T, Rama N, Van Noorden S, Curry E et al. Differential expression of IL-8 and IL-8 receptors in benign, borderline and malignant ovarian epithelial tumours. Cytokine 2013; 64: 413-421.
54. Cooke SL, Ng CKY, Melnyk N, Garcia MJ, Hardcastle T, Temple J et al. Genomic analysis of genetic heterogeneity and evolution in high-grade serous ovarian carcinoma. Oncogene 2010; 29: 4905-4913.
55. Pollak MN. Investigating metformin for cancer prevention and treatment: the end of the beginning. Cancer Discov 2012; 2: 778-790.
56. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9: 671-675.