Development of potent autophagy inhibitors that sensitize oncogenic BRAF V600E mutant melanoma tumor cells to vemurafenib

References

• Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931 - 7; http://dx.doi.org/10.1038/nrm2245; PMID: 17712358
   PubMed Web of Science ®Google Scholar
• Kohli L, Roth KA. Autophagy: cerebral home cooking. Am J Pathol 2010; 176:1065 - 71; http://dx.doi.org/10.2353/ajpath.2010.090850; PMID: 20150434
   PubMed Web of Science ®Google Scholar
• Simonsen A, Tooze SA. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 2009; 186:773 - 82; http://dx.doi.org/10.1083/jcb.200907014; PMID: 19797076
   PubMed Web of Science ®Google Scholar
• Rosenfeldt MT, Ryan KM. The role of autophagy in tumour development and cancer therapy. Expert Rev Mol Med 2009; 11:e36; http://dx.doi.org/10.1017/S1462399409001306; PMID: 19951459
   PubMed Web of Science ®Google Scholar
• White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12:401 - 10; http://dx.doi.org/10.1038/nrc3262; PMID: 22534666
   PubMed Web of Science ®Google Scholar
• Mathew R, White E. Autophagy, stress, and cancer metabolism: what doesn’t kill you makes you stronger. Cold Spring Harb Symp Quant Biol 2011; 76:389 - 96; http://dx.doi.org/10.1101/sqb.2012.76.011015; PMID: 22442109
   PubMedGoogle Scholar
• Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069 - 75; http://dx.doi.org/10.1038/nature06639; PMID: 18305538
   PubMed Web of Science ®Google Scholar
• Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol 2010; 12:814 - 22; http://dx.doi.org/10.1038/ncb0910-814; PMID: 20811353
   PubMed Web of Science ®Google Scholar
• Wu WK, Coffelt SB, Cho CH, Wang XJ, Lee CW, Chan FK, Yu J, Sung JJ. The autophagic paradox in cancer therapy. Oncogene 2012; 31:939 - 53; http://dx.doi.org/10.1038/onc.2011.295; PMID: 21765470
   PubMed Web of Science ®Google Scholar
• Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007; 7:961 - 7; http://dx.doi.org/10.1038/nrc2254; PMID: 17972889
   PubMed Web of Science ®Google Scholar
• Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5:726 - 34; http://dx.doi.org/10.1038/nrc1692; PMID: 16148885
   PubMed Web of Science ®Google Scholar
• Shingu T, Fujiwara K, Bögler O, Akiyama Y, Moritake K, Shinojima N, Tamada Y, Yokoyama T, Kondo S. Stage-specific effect of inhibition of autophagy on chemotherapy-induced cytotoxicity. Autophagy 2009; 5:537 - 9; http://dx.doi.org/10.4161/auto.5.4.8164; PMID: 19270491
   PubMed Web of Science ®Google Scholar
• Guo JY, Chen HY, Mathew R, Fan J, Strohecker AM, Karsli-Uzunbas G, Kamphorst JJ, Chen G, Lemons JM, Karantza V, et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev 2011; 25:460 - 70; http://dx.doi.org/10.1101/gad.2016311; PMID: 21317241
   PubMed Web of Science ®Google Scholar
• Guo JY, Karsli-Uzunbas G, Mathew R, Aisner SC, Kamphorst JJ, Strohecker AM, Chen G, Price S, Lu W, Teng X, et al. Autophagy suppresses progression of K-ras-induced lung tumors to oncocytomas and maintains lipid homeostasis. Genes Dev 2013; 27:1447 - 61; http://dx.doi.org/10.1101/gad.219642.113; PMID: 23824538
   PubMed Web of Science ®Google Scholar
• Yang S, Wang X, Contino G, Liesa M, Sahin E, Ying H, Bause A, Li Y, Stommel JM, Dell’antonio G, et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev 2011; 25:717 - 29; http://dx.doi.org/10.1101/gad.2016111; PMID: 21406549
   PubMed Web of Science ®Google Scholar
• Maddodi N, Huang W, Havighurst T, Kim K, Longley BJ, Setaluri V. Induction of autophagy and inhibition of melanoma growth in vitro and in vivo by hyperactivation of oncogenic BRAF. J Invest Dermatol 2010; 130:1657 - 67; http://dx.doi.org/10.1038/jid.2010.26; PMID: 20182446
   PubMed Web of Science ®Google Scholar
• Fan QW, Cheng C, Hackett C, Feldman M, Houseman BT, Nicolaides T, Haas-Kogan D, James CD, Oakes SA, Debnath J, et al. Akt and autophagy cooperate to promote survival of drug-resistant glioma. Sci Signal 2010; 3:ra81; http://dx.doi.org/10.1126/scisignal.2001017; PMID: 21062993
   PubMed Web of Science ®Google Scholar
• Boya P, González-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Métivier D, Meley D, Souquere S, Yoshimori T, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005; 25:1025 - 40; http://dx.doi.org/10.1128/MCB.25.3.1025-1040.2005; PMID: 15657430
   PubMed Web of Science ®Google Scholar
• Morselli E, Galluzzi L, Kepp O, Vicencio JM, Criollo A, Maiuri MC, Kroemer G. Anti- and pro-tumor functions of autophagy. Biochim Biophys Acta 2009; 1793:1524 - 32; http://dx.doi.org/10.1016/j.bbamcr.2009.01.006; PMID: 19371598
   PubMed Web of Science ®Google Scholar
• Liu B, Cheng Y, Liu Q, Bao JK, Yang JM. Autophagic pathways as new targets for cancer drug development. Acta Pharmacol Sin 2010; 31:1154 - 64; http://dx.doi.org/10.1038/aps.2010.118; PMID: 20694022
   PubMed Web of Science ®Google Scholar
• Apel A, Herr I, Schwarz H, Rodemann HP, Mayer A. Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 2008; 68:1485 - 94; http://dx.doi.org/10.1158/0008-5472.CAN-07-0562; PMID: 18316613
   PubMed Web of Science ®Google Scholar
• Foley M, Tilley L. Quinoline antimalarials: mechanisms of action and resistance and prospects for new agents. Pharmacol Ther 1998; 79:55 - 87; http://dx.doi.org/10.1016/S0163-7258(98)00012-6; PMID: 9719345
   PubMed Web of Science ®Google Scholar
• Loeb RF. Activity of a new antimalarial agent, chloroquine (SN7618). JAMA 1946; 130:1069 - 70; http://dx.doi.org/10.1001/jama.1946.02870160015006
   PubMed Web of Science ®Google Scholar
• Solomon VR, Lee H. Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies. Eur J Pharmacol 2009; 625:220 - 33; http://dx.doi.org/10.1016/j.ejphar.2009.06.063; PMID: 19836374
   PubMed Web of Science ®Google Scholar
• Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 2007; 117:326 - 36; http://dx.doi.org/10.1172/JCI28833; PMID: 17235397
   PubMed Web of Science ®Google Scholar
• Ma XH, Piao S, Wang D, McAfee QW, Nathanson KL, Lum JJ, Li LZ, Amaravadi RK. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin Cancer Res 2011; 17:3478 - 89; http://dx.doi.org/10.1158/1078-0432.CCR-10-2372; PMID: 21325076
   PubMed Web of Science ®Google Scholar
• Han W, Sun J, Feng L, Wang K, Li D, Pan Q, Chen Y, Jin W, Wang X, Pan H, et al. Autophagy inhibition enhances daunorubicin-induced apoptosis in K562 cells. PLoS One 2011; 6:e28491; http://dx.doi.org/10.1371/journal.pone.0028491; PMID: 22164300
   PubMed Web of Science ®Google Scholar
• Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, Smith JE, Hembruff SL, Ha K, Atadja P, et al. Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther 2012; 11:973 - 83; http://dx.doi.org/10.1158/1535-7163.MCT-11-0979; PMID: 22367781
   PubMed Web of Science ®Google Scholar
• Li DD, Sun T, Wu XQ, Chen SP, Deng R, Jiang S, Feng GK, Pan JX, Zhang XS, Zeng YX, et al. The inhibition of autophagy sensitises colon cancer cells with wild-type p53 but not mutant p53 to topotecan treatment. PLoS One 2012; 7:e45058; http://dx.doi.org/10.1371/journal.pone.0045058; PMID: 23024792
   PubMed Web of Science ®Google Scholar
• National Library of Medicine US. Clinical trials investigating the use of chloroquine in cancer: NCT01575782, NCT00969306, NCT01446016, NCT01023477, NCT01469455, NCT01438177, NCT01727531, NCT00224978. clinicaltrials.gov: Bethesda, MD, 2013
   Google Scholar
• National Library of Medicine US. Clinical trials investigating the use of hydroxychloroquine in cancer: NCT01273805, NCT00933803, NCT01006369, NCT01480154, NCT00765765, NCT00728845, NCT01266057, NCT00813423, NCT01494155, NCT01023737, NCT00786682, NCT00726596, NCT01417403, NCT00809237, NCT00909831, NCT00714181, NCT00714181, NCT01206530, NCT01026844, NCT00486603, NCT01649947, NCT00977470, NCT01506973, NCT01128296, NCT00568880, NCT01144169, NCT00962845, NCT01292408, NCT01689987, NCT01550367, NCT01396200, NCT01227135, NCT01602588, NCT01510119, NCT00031824, NCT01548768, NCT00908089, NCT01687179, NCT00405275, NCT00771056, NCT01709578. clinicaltrials.gov: Bethesda, MD, 2013
   Google Scholar
• Sotelo J, Briceño E, López-González MA. Adding chloroquine to conventional treatment for glioblastoma multiforme: a randomized, double-blind, placebo-controlled trial. Ann Intern Med 2006; 144:337 - 43; http://dx.doi.org/10.7326/0003-4819-144-5-200603070-00008; PMID: 16520474
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445 - 544; http://dx.doi.org/10.4161/auto.19496; PMID: 22966490
   PubMed Web of Science ®Google Scholar
• Martin KR, Barua D, Kauffman AL, Westrate LM, Posner RG, Hlavacek WS, Mackeigan JP. Computational model for autophagic vesicle dynamics in single cells. Autophagy 2013; 9:74 - 92; http://dx.doi.org/10.4161/auto.22532; PMID: 23196898
   PubMed Web of Science ®Google Scholar
• Qiao S, Tao S, Rojo de la Vega M, Park SL, Vonderfecht AA, Jacobs SL, Zhang DD, Wondrak GT. The antimalarial amodiaquine causes autophagic-lysosomal and proliferative blockade sensitizing human melanoma cells to starvation- and chemotherapy-induced cell death. Autophagy 2013; 9:2087 - 102; http://dx.doi.org/10.4161/auto.26506; PMID: 24113242
   PubMed Web of Science ®Google Scholar
• Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ. Autophagy regulates lipid metabolism. Nature 2009; 458:1131 - 5; http://dx.doi.org/10.1038/nature07976; PMID: 19339967
   PubMed Web of Science ®Google Scholar
• Velikkakath AK, Nishimura T, Oita E, Ishihara N, Mizushima N. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell 2012; 23:896 - 909; http://dx.doi.org/10.1091/mbc.E11-09-0785; PMID: 22219374
   PubMed Web of Science ®Google Scholar
• Chen B, Tardell C, Higgins B, Packman K, Boylan JF, Niu H. BRAFV600E negatively regulates the AKT pathway in melanoma cell lines. PLoS One 2012; 7:e42598; http://dx.doi.org/10.1371/journal.pone.0042598; PMID: 22880048
   PubMed Web of Science ®Google Scholar
• Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, et al. Mutations of the BRAF gene in human cancer. Nature 2002; 417:949 - 54; http://dx.doi.org/10.1038/nature00766; PMID: 12068308
   PubMed Web of Science ®Google Scholar
• Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O’Dwyer PJ, Lee RJ, Grippo JF, Nolop K, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010; 363:809 - 19; http://dx.doi.org/10.1056/NEJMoa1002011; PMID: 20818844
   PubMed Web of Science ®Google Scholar
• Yan H, Zhang B, Li S, Zhao Q. A formal model for analyzing drug combination effects and its application in TNF-alpha-induced NFkappaB pathway. BMC Syst Biol 2010; 4:50; http://dx.doi.org/10.1186/1752-0509-4-50; PMID: 20416113
   PubMed Web of Science ®Google Scholar
• Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 2010; 70:440 - 6; http://dx.doi.org/10.1158/0008-5472.CAN-09-1947; PMID: 20068163
   PubMed Web of Science ®Google Scholar
• Hiss DC, Gabriels GA, Folb PI. Combination of tunicamycin with anticancer drugs synergistically enhances their toxicity in multidrug-resistant human ovarian cystadenocarcinoma cells. Cancer Cell Int 2007; 7:5; http://dx.doi.org/10.1186/1475-2867-7-5; PMID: 17439664
   PubMed Web of Science ®Google Scholar
• Flaherty KT, Hodi FS, Fisher DE. From genes to drugs: targeted strategies for melanoma. Nat Rev Cancer 2012; 12:349 - 61; http://dx.doi.org/10.1038/nrc3218; PMID: 22475929
   PubMed Web of Science ®Google Scholar
• Janku F, McConkey DJ, Hong DS, Kurzrock R. Autophagy as a target for anticancer therapy. Nat Rev Clin Oncol 2011; 8:528 - 39; http://dx.doi.org/10.1038/nrclinonc.2011.71; PMID: 21587219
   PubMed Web of Science ®Google Scholar
• Corazzari MaL, Penny E. Harnessing Autophagy for Melanoma Benefit. Cell Biol 2013; 2
   Google Scholar
• Xie X, White EP, Mehnert JM. Coordinate autophagy and mTOR pathway inhibition enhances cell death in melanoma. PLoS One 2013; 8:e55096; http://dx.doi.org/10.1371/journal.pone.0055096; PMID: 23383069
   PubMed Web of Science ®Google Scholar
• Sheen JH, Zoncu R, Kim D, Sabatini DM. Defective regulation of autophagy upon leucine deprivation reveals a targetable liability of human melanoma cells in vitro and in vivo. Cancer Cell 2011; 19:613 - 28; http://dx.doi.org/10.1016/j.ccr.2011.03.012; PMID: 21575862
   PubMed Web of Science ®Google Scholar
• Sasaki K, Tsuno NH, Sunami E, Tsurita G, Kawai K, Okaji Y, Nishikawa T, Shuno Y, Hongo K, Hiyoshi M, et al. Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 2010; 10:370; http://dx.doi.org/10.1186/1471-2407-10-370; PMID: 20630104
   PubMed Web of Science ®Google Scholar
• Wu YC, Wu WK, Li Y, Yu L, Li ZJ, Wong CC, Li HT, Sung JJ, Cho CH. Inhibition of macroautophagy by bafilomycin A1 lowers proliferation and induces apoptosis in colon cancer cells. Biochem Biophys Res Commun 2009; 382:451 - 6; http://dx.doi.org/10.1016/j.bbrc.2009.03.051; PMID: 19289106
   PubMed Web of Science ®Google Scholar
• Sharma N, Thomas S, Golden EB, Hofman FM, Chen TC, Petasis NA, Schönthal AH, Louie SG. Inhibition of autophagy and induction of breast cancer cell death by mefloquine, an antimalarial agent. Cancer Lett 2012; 326:143 - 54; http://dx.doi.org/10.1016/j.canlet.2012.07.029; PMID: 22863539
   PubMed Web of Science ®Google Scholar
• Han W, Pan H, Chen Y, Sun J, Wang Y, Li J, Ge W, Feng L, Lin X, Wang X, et al. EGFR tyrosine kinase inhibitors activate autophagy as a cytoprotective response in human lung cancer cells. PLoS One 2011; 6:e18691; http://dx.doi.org/10.1371/journal.pone.0018691; PMID: 21655094
   PubMed Web of Science ®Google Scholar
• Xu Y, Yu H, Qin H, Kang J, Yu C, Zhong J, Su J, Li H, Sun L. Inhibition of autophagy enhances cisplatin cytotoxicity through endoplasmic reticulum stress in human cervical cancer cells. Cancer Lett 2012; 314:232 - 43; http://dx.doi.org/10.1016/j.canlet.2011.09.034; PMID: 22019047
   PubMed Web of Science ®Google Scholar
• Armstrong JL, Corazzari M, Martin S, Pagliarini V, Falasca L, Hill DS, Ellis N, Al Sabah S, Redfern CP, Fimia GM, et al. Oncogenic B-RAF signaling in melanoma impairs the therapeutic advantage of autophagy inhibition. Clin Cancer Res 2011; 17:2216 - 26; http://dx.doi.org/10.1158/1078-0432.CCR-10-3003; PMID: 21270111
   PubMed Web of Science ®Google Scholar
• Su F, Viros A, Milagre C, Trunzer K, Bollag G, Spleiss O, Reis-Filho JS, Kong X, Koya RC, Flaherty KT, et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med 2012; 366:207 - 15; http://dx.doi.org/10.1056/NEJMoa1105358; PMID: 22256804
   PubMed Web of Science ®Google Scholar
• De D, Krogstad FM, Byers LD, Krogstad DJ. Structure-activity relationships for antiplasmodial activity among 7-substituted 4-aminoquinolines. J Med Chem 1998; 41:4918 - 26; http://dx.doi.org/10.1021/jm980146x; PMID: 9836608
   PubMed Web of Science ®Google Scholar
• Iwaniuk DP, Whetmore ED, Rosa N, Ekoue-Kovi K, Alumasa J, de Dios AC, Roepe PD, Wolf C. Synthesis and antimalarial activity of new chloroquine analogues carrying a multifunctional linear side chain. Bioorg Med Chem 2009; 17:6560 - 6; http://dx.doi.org/10.1016/j.bmc.2009.08.003; PMID: 19703776
   PubMed Web of Science ®Google Scholar
• Anderson T, Nkhoma S, Ecker A, Fidock D. How can we identify parasite genes that underlie antimalarial drug resistance?. Pharmacogenomics 2011; 12:59 - 85; http://dx.doi.org/10.2217/pgs.10.165; PMID: 21174623
   PubMed Web of Science ®Google Scholar
• Muregi FW, Wamakima HN, Kimani FT. Novel drug targets in malaria parasite with potential to yield antimalarial drugs with long useful therapeutic lives. Curr Pharm Des 2012; 18:3505 - 21; PMID: 22607143
   PubMed Web of Science ®Google Scholar
• Solomon VR, Hu C, Lee H. Design and synthesis of chloroquine analogs with anti-breast cancer property. Eur J Med Chem 2010; 45:3916 - 23; http://dx.doi.org/10.1016/j.ejmech.2010.05.046; PMID: 20561720
   PubMed Web of Science ®Google Scholar
• Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3:452 - 60; PMID: 17534139
   PubMed Web of Science ®Google Scholar