Vorinostat and hydroxychloroquine improve immunity and inhibit autophagy in metastatic colorectal cancer

Oncotarget

Volumn 7, Issue 37, 2016, Pages 59087-59097

  Patel, Sukeshi ^a   Hurez, Vincent ^a   Nawrocki, Steffan T ^a   Goros, Martin ^a   Michalek, Joel ^a   Sarantopoulos, John ^a   Curiel, Tyler ^a   Mahalingam, Devalingam ^a  

^a University of Texas Health Science Center at San Antonio   (United States)

Author keywords

Autophagy; Colorectal cancer; Hydroxychloroquine; Immunity; Vorinostat

Indexed keywords

CATHEPSIN D; CD45RO ANTIGEN; CYTOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; FLUOROURACIL; HISTONE DEACETYLASE INHIBITOR; HYDROXYCHLOROQUINE; L SELECTIN; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN P62; REGORAFENIB; TRANSCRIPTION FACTOR FOXP3; UBIQUITINATED PROTEIN; VASCULOTROPIN; VORINOSTAT; ANTINEOPLASTIC AGENT; HYDROXAMIC ACID;

ADULT; AGED; ANEMIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER PATIENT; CAUCASIAN; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CLINICAL STUDY; CONTROLLED STUDY; DRUG EFFICACY; DRUG TOLERABILITY; FATIGUE; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNITY; IMMUNOCOMPETENT CELL; MALE; METASTATIC COLORECTAL CANCER; NAUSEA; OVERALL SURVIVAL; PHARMACODYNAMICS; PRIMARY TUMOR; PROGRESSION FREE SURVIVAL; THROMBOCYTOPENIA; TUMOR CELL; VOMITING; CELLULAR IMMUNITY; COLORECTAL TUMOR; DRUG EFFECTS; IMMUNOLOGY; METASTASIS; MIDDLE AGED; MORTALITY; REGULATORY T LYMPHOCYTE; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ADULT; AGED; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AUTOPHAGY; COLORECTAL NEOPLASMS; FATIGUE; FEMALE; HUMANS; HYDROXAMIC ACIDS; HYDROXYCHLOROQUINE; IMMUNITY, CELLULAR; MALE; MIDDLE AGED; NEOPLASM METASTASIS; SURVIVAL ANALYSIS; T-LYMPHOCYTES, REGULATORY; TREATMENT OUTCOME;

EID: 84991396723     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10824     Document Type: Article

References (39)

1. Patel SR, Karnad AB, Ketchum NS, Pollock BH, Sarantopoulos J, Weitman S, Mahalingam D. Should we move beyond VEGF inhibition in metastatic colorectal cancer? Lessons from early phase clinical trials. J Gastrointest Oncol. 2014; 5:99-103
2. Grothey A, Van Cutsem E, Sobrero A, Siena S, Falcone A, Ychou M, Humblet Y, Bouche O, Mineur L, Barone C, Adenis A, Tabernero J, Yoshino T, et al. Regorafenib monotherapy for previously treated metastatic colorectal cancer (CORRECT): an international, multicentre, randomised, placebo-controlled, phase 3 trial. Lancet. 2013; 381:303-312
3. Carew JS, Nawrocki ST, Kahue CN, Zhang H, Yang C, Chung L, Houghton JA, Huang P, Giles FJ, Cleveland JL. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Ablmediated drug resistance. Blood. 2007; 110:313-322
4. Carew JS, Medina EC, Esquivel JA, 2nd, Mahalingam D, Swords R, Kelly K, Zhang H, Huang P, Mita AC, Mita MM, Giles FJ, Nawrocki ST. Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. Journal of cellular and molecular medicine. 2010; 14:2448-2459
5. Kuefer R, Hofer MD, Altug V, Zorn C, Genze F, Kunzi-Rapp K, Hautmann RE, Gschwend JE. Sodium butyrate and tributyrin induce in vivo growth inhibition and apoptosis in human prostate cancer. Br J Cancer. 2004; 90:535-541
6. Strait KA, Dabbas B, Hammond EH, Warnick CT, Iistrup SJ, Ford CD. Cell cycle blockade and differentiation of ovarian cancer cells by the histone deacetylase inhibitor trichostatin A are associated with changes in p21, Rb, and Id proteins. Mol Cancer Ther. 2002; 1:1181-1190
7. Duan H, Heckman CA, Boxer LM. Histone deacetylase inhibitors down-regulate bcl-2 expression and induce apoptosis in t(14;18) lymphomas. Mol Cell Biol. 2005; 25:1608-1619
8. Carew JS, Nawrocki ST, Cleveland JL. Modulating autophagy for therapeutic benefit. Autophagy. 2007; 3:464-467
9. Levy J, Cacheux W, Bara MA, L'Hermitte A, Lepage P, Fraudeau M, Trentesaux C, Lemarchand J, Durand A, Crain AM, Marchiol C, Renault G, Dumont F, et al. Intestinal inhibition of Atg7 prevents tumour initiation through a microbiome-influenced immune response and suppresses tumour growth. Nat Cell Biol. 2015; 17:1062-1073
10. Janji B, Viry E, Moussay E, Paggetti J, Arakelian T, Mgrditchian T, Messai Y, Noman MZ, Van Moer K, Hasmim M, Mami-Chouaib F, Berchem G, Chouaib S. The multifaceted role of autophagy in tumor evasion from immune surveillance. Oncotarget. 2016. doi: 10.18632/oncotarget.7540
11. Viry E, Paggetti J, Baginska J, Mgrditchian T, Berchem G, Moussay E, Janji B. Autophagy: an adaptive metabolic response to stress shaping the antitumor immunity. Biochem Pharmacol. 2014; 92:31-42
12. Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013; 13:722-737
13. Amaravadi RK, Lippincott-Schwartz J, Yin XM, Weiss WA, Takebe N, Timmer W, DiPaola RS, Lotze MT, White E. Principles and current strategies for targeting autophagy for cancer treatment. Clin Cancer Res. 2011; 17:654-666
14. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004; 10:942-949
15. Mahalingam D, Mita M, Sarantopoulos J, Wood L, Amaravadi R, Davis LE, Mita A, Curiel TJ, Espitia CM, Nawrocki ST, Giles FJ, Carew JS. Combined autophagy and HDAC inhibition: A phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors. Autophagy. 2014; 10
16. Leoni F, Fossati G, Lewis EC, Lee JK, Porro G, Pagani P, Modena D, Moras ML, Pozzi P, Reznikov LL, Siegmund B, Fantuzzi G, Dinarello CA, Mascagni P. The histone deacetylase inhibitor ITF2357 reduces production of proinflammatory cytokines in vitro and systemic inflammation in vivo. Mol Med. 2005; 11:1-15
17. Schmudde M, Braun A, Pende D, Sonnemann J, Klier U, Beck JF, Moretta L, Broker BM. Histone deacetylase inhibitors sensitize tumour cells for cytotoxic effects of natural killer cells. Cancer Lett. 2008; 272:110-121
18. Stephen S, Morrissey KA, Benoit BM, Kim EJ, Vittorio CC, Nasta SD, Showe LC, Wysocka M, Rook AH. Inhibition of cell-mediated immunity by the histone deacetylase inhibitor vorinostat: implications for therapy of cutaneous T-cell lymphoma. Am J Hematol. 2012; 87:226-228
19. Ogbomo H, Michaelis M, Kreuter J, Doerr HW, Cinatl J, Jr. Histone deacetylase inhibitors suppress natural killer cell cytolytic activity. FEBS Lett. 2007; 581:1317-1322
20. Oki Y, Buglio D, Zhang J, Ying Y, Zhou S, Sureda A, Ben-Yehuda D, Zinzani PL, Prince HM, Harrison SJ, Kirschbaum M, Johnston PB, Shen A, et al. Immune regulatory effects of panobinostat in patients with Hodgkin lymphoma through modulation of serum cytokine levels and T-cell PD1 expression. Blood Cancer J. 2014; 4:e236
21. Mahalingam D, Mita M, Sarantopoulos J, Wood L, Amaravadi RK, Davis LE, Mita AC, Curiel TJ, Espitia CM, Nawrocki ST, Giles FJ, Carew JS. Combined autophagy and HDAC inhibition: a phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors. Autophagy. 2014; 10:1403-1414
22. Mayer RJ, Van Cutsem E, Falcone A, Yoshino T, Garcia-Carbonero R, Mizunuma N, Yamazaki K, Shimada Y, Tabernero J, Komatsu Y, Sobrero A, Boucher E, Peeters M, et al. Randomized trial of TAS-102 for refractory metastatic colorectal cancer. N Engl J Med. 2015; 372:1909-1919
23. Livesey KM, Kang R, Zeh HJ, 3rd, Lotze MT, Tang D. Direct molecular interactions between HMGB1 and TP53 in colorectal cancer. Autophagy. 2012; 8:846-848
24. Livesey KM, Tang D, Zeh HJ, Lotze MT. Autophagy inhibition in combination cancer treatment. Curr Opin Invest Drugs. 2009; 10:1269-1279
25. Thomas A, Rajan A, Szabo E, Tomita Y, Carter CA, Scepura B, Lopez-Chavez A, Lee MJ, Redon CE, Frosch A, Peer CJ, Chen Y, Piekarz R, et al. A phase I/II trial of belinostat in combination with cisplatin, doxorubicin, and cyclophosphamide in thymic epithelial tumors: a clinical and translational study. Clin Cancer Res. 2014; 20:5392-5402
26. Curiel TJ. Immunotherapy: a useful strategy to help combat multidrug resistance. Drug Resist Updat. 2012; 15:106-113
27. Kovacs JR, Li C, Yang Q, Li G, Garcia IG, Ju S, Roodman DG, Windle JJ, Zhang X, Lu B. Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ. 2012; 19:144-152
28. Wei J, Long L, Yang K, Guy C, Shrestha S, Chen Z, Wu C, Vogel P, Neale G, Green DR, Chi H. Autophagy enforces functional integrity of regulatory T cells by coupling environmental cues and metabolic homeostasis. Nat Immunol. 2016; 17:277-285
29. Maruyama R, Yamana K, Itoi T, Hara N, Bilim V, Nishiyama T, Takahashi K, Tomita Y. Absence of Bcl-2 and Fas/CD95/APO-1 predicts the response to immunotherapy in metastatic renal cell carcinoma. Br J Cancer. 2006; 95:1244-1249
30. Moller P, Koretz K, Leithauser F, Bruderlein S, Henne C, Quentmeier A, Krammer PH. Expression of APO-1 (CD95), a member of the NGF/TNF receptor superfamily, in normal and neoplastic colon epithelium. Int J Cancer. 1994; 57:371-377
31. Yang D, Torres CM, Bardhan K, Zimmerman M, McGaha TL, Liu K. Decitabine and vorinostat cooperate to sensitize colon carcinoma cells to Fas ligand-induced apoptosis in vitro and tumor suppression in vivo. J Immunol. 2012; 188:4441-4449
32. Fritzsching B, Oberle N, Eberhardt N, Quick S, Haas J, Wildemann B, Krammer PH, Suri-Payer E. In contrast to effector T cells, CD4+CD25+FoxP3+ regulatory T cells are highly susceptible to CD95 ligand-but not to TCRmediated cell death. J Immunol. 2005; 175:32-36
33. Blank C, Gajewski TF, Mackensen A. Interaction of PDL1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: implications for tumor immunotherapy. Cancer Immunol Immunother. 2005; 54:307-314
34. Ward R, Meagher A, Tomlinson I, O'Connor T, Norrie M, Wu R, Hawkins N. Microsatellite instability and the clinicopathological features of sporadic colorectal cancer. Gut. 2001; 48:821-829
35. Popat S, Hubner R, Houlston RS. Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol. 2005; 23:609-618
36. Xiao Y, Freeman GJ. The microsatellite instable subset of colorectal cancer is a particularly good candidate for checkpoint blockade immunotherapy. Cancer Discov. 2015; 5:16-18
37. Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D, Biedrzycki B, Donehower RC, Zaheer A, et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency. The N Engl J Med. 2015; 372:2509-2520
38. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst. 2000; 92:205-216
39. Trotti A, Colevas AD, Setser A, Rusch V, Jaques D, Budach V, Langer C, Murphy B, Cumberlin R, Coleman CN, Rubin P. CTCAE v3.0: development of a comprehensive grading system for the adverse effects of cancer treatment. Semin Radiat Oncol. 2003; 13:176-181