DIRAS3 induces autophagy and enhances sensitivity to anti-autophagic therapy in KRAS-driven pancreatic and ovarian carcinomas

References

• Downward J. Ras signalling and apoptosis. Curr Opin Genet Dev. 1998;8(1):49–54. doi: 10.1016/S0959-437X(98)80061-0
   PubMed Web of Science ®Google Scholar
• Marshall C. How do small GTPase signal transduction pathways regulate cell cycle entry? Curr Opin Cell Biol. 1999;11(6):732–736. doi: 10.1016/S0955-0674(99)00044-7
   PubMed Web of Science ®Google Scholar
• Malumbres M, Barbacid M. RAS oncogenes: the first 30 years. Nat Rev Cancer. 2003;3(6):459–465. doi: 10.1038/nrc1097
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay S, Vander Heiden MG, McCormick F. The metabolic landscape of RAS-Driven cancers from biology to therapy. Nat Cancer. 2021;2(3):271–283. doi: 10.1038/s43018-021-00184-x
   PubMedGoogle Scholar
• Diaz-Padilla I, Malpica AL, Minig L, et al. Ovarian low-grade serous carcinoma: a comprehensive update. Gynecol Oncol. 2012;126(2):279–285. doi: 10.1016/j.ygyno.2012.04.029
   PubMed Web of Science ®Google Scholar
• Kimmelman AC. Metabolic dependencies in RAS-Driven cancers. Clin Cancer Res. 2015;21(8):1828–1834. doi: 10.1158/1078-0432.CCR-14-2425
   PubMed Web of Science ®Google Scholar
• Pupo E, Avanzato D, Middonti E, et al. KRAS-Driven metabolic rewiring reveals novel actionable targets in cancer. Front Oncol. 2019;9:848. doi: 10.3389/fonc.2019.00848
   PubMed Web of Science ®Google Scholar
• Kinsey CG, Camolotto SA, Boespflug AM, et al. Protective autophagy elicited by RAF→MEK→ERK inhibition suggests a treatment strategy for RAS-driven cancers. Nat Med. 2019;25(4):620–627. doi: 10.1038/s41591-019-0367-9
   PubMed Web of Science ®Google Scholar
• Bryant KL, Stalnecker CA, Zeitouni D, et al. Combination of ERK and autophagy inhibition as a treatment approach for pancreatic cancer. Nat Med. 2019;25(4):628–640. doi: 10.1038/s41591-019-0368-8
   PubMed Web of Science ®Google Scholar
• Sutton MN, Lu Z, Li YC, et al. DIRAS3 (ARHI) blocks RAS/MAPK signaling by binding directly to RAS and disrupting RAS clusters. Cell Rep. 2019;29:3448–3459 e6. doi: 10.1016/j.celrep.2019.11.045
   PubMed Web of Science ®Google Scholar
• Nakamura H, Takada K. Reactive oxygen species in cancer: Current findings and future directions. Cancer Sci. 2021;112:3945–3952. doi: 10.1111/cas.15068
   PubMed Web of Science ®Google Scholar
• Wu WL, Papagiannakopoulos T. The pleiotropic role of the KEAP1/NRF2 pathway in cancer. Annu Rev Cancer Biol. 2020;4:413–435. doi: 10.1146/annurev-cancerbio-030518-055627
   Google Scholar
• Nowosad A, Jeannot P, Callot C, et al. p27 controls Ragulator and mTOR activity in amino acid-deprived cells to regulate the autophagy–lysosomal pathway and coordinate cell cycle and cell growth. Nat Cell Biol. 2020;22(9):1076–1090. doi: 10.1038/s41556-020-0554-4
   PubMed Web of Science ®Google Scholar
• Liang J, Shao SH, Xu Z-X, et al. The energy sensing LKB1–AMPK pathway regulates p27kip1 phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol. 2007;9(2):218–224. doi: 10.1038/ncb1537
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Polito VA, et al. TFEB Links Autophagy to Lysosomal Biogenesis. Science. 2011;332(6036):1429–1433. doi: 10.1126/science.1204592
   PubMed Web of Science ®Google Scholar
• Napolitano G, Ballabio A. TFEB at a glance. J Cell Sci. 2016;129:2475–2481. doi: 10.1242/jcs.146365
   PubMed Web of Science ®Google Scholar
• Hennig P, Fenini G, Di Filippo M, et al. The pathways underlying the multiple roles of p62 in inflammation and cancer. Biomedicines. 2021;9(7):707. doi: 10.3390/biomedicines9070707
   PubMed Web of Science ®Google Scholar
• Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12(3):213–223. doi: 10.1038/ncb2021
   PubMed Web of Science ®Google Scholar
• Prior IA, Muncke C, Parton RG, et al. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Bio. 2003;160(2):165–170. doi: 10.1083/jcb.200209091
   PubMed Web of Science ®Google Scholar
• Zhou Y, Gorfe AA, Hancock JF. RAS nanoclusters selectively sort distinct lipid headgroups and acyl chains. Front Mol Biosci. 2021;8:686338. doi: 10.3389/fmolb.2021.686338
   PubMed Web of Science ®Google Scholar
• Jeon S-M, Hay N. The dark face of AMPK as an essential tumor promoter. Cell Logist. 2012;2:197–202. doi: 10.4161/cl.22651
   PubMedGoogle Scholar
• Kimmelman AC, White E. Autophagy and tumor metabolism. Cell Metab. 2017;25(5):1037–1043. doi: 10.1016/j.cmet.2017.04.004
   PubMed Web of Science ®Google Scholar
• Guo JY, Teng X, Laddha SV, et al. Autophagy provides metabolic substrates to maintain energy charge and nucleotide pools in Ras-driven lung cancer cells. Genes Dev. 2016;30(15):1704–1717. doi: 10.1101/gad.283416.116
   PubMed Web of Science ®Google Scholar
• Filomeni G, De Zio D, Cecconi F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 2015;22(3):377–388. doi: 10.1038/cdd.2014.150
   PubMed Web of Science ®Google Scholar
• Reczek CR, Chandel NS. The two faces of reactive oxygen species in cancer. Annu Rev Cancer Biol. 2017;1(1):79–98. doi: 10.1146/annurev-cancerbio-041916-065808
   Google Scholar
• Mauthe M, Orhon I, Rocchi C, et al. Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion. Autophagy. 2018;14(8):1435–1455. doi: 10.1080/15548627.2018.1474314
   PubMed Web of Science ®Google Scholar
• Rebecca VW, Nicastri MC, Fennelly C, et al. PPT1 promotes tumor growth and is the molecular target of chloroquine derivatives in cancer. Cancer Discov. 2019;9(2):220–229. doi: 10.1158/2159-8290.CD-18-0706
   PubMed Web of Science ®Google Scholar
• Gray JP, Bildik GE, Sutton MN, et al. Abstract 3599: helical stapled peptides derived from DIRAS3 block KRAS dimerization and downstream MEK/ERK signaling in pancreatic and ovarian carcinomas. Cancer Res. 2022;82(12_Supplement):3599–3599. doi: 10.1158/1538-7445.AM2022-3599
   Web of Science ®Google Scholar
• Bildik G, Liang X, Sutton MN, et al. DIRAS3: an imprinted tumor suppressor gene that regulates RAS and PI3K-driven cancer growth, motility, autophagy, and tumor dormancy. Mol Cancer Ther. 2022;21(1):25–37. doi: 10.1158/1535-7163.MCT-21-0331
   PubMed Web of Science ®Google Scholar
• Wu X, Liang L, Dong L, et al. Effect of ARHI on lung cancer cell proliferation, apoptosis and invasion in vitro. Mol Biol Rep. 2013;40(3):2671–2678. doi: 10.1007/s11033-012-2353-x
   PubMed Web of Science ®Google Scholar
• Yuan J, Luo RZ, Fujii S, 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.
   PubMed Web of Science ®Google Scholar
• Ouyang J, Pan X, Hu Z. The role of aplysia ras homolog I in colon cancer cell invasion and adhesion. Exp Ther Med. 2017;14:5193–5199. doi: 10.3892/etm.2017.5122
   PubMed Web of Science ®Google Scholar
• Fernandez ML, DiMattia GE, Dawson A, et al. Differences in MEK inhibitor efficacy in molecularly characterized low-grade serous ovarian cancer cell lines. Am J Cancer Res. 2016;6:2235–2251.
   PubMed Web of Science ®Google Scholar
• De Thaye E, Van de Vijver K, Van der Meulen J, et al. Establishment and characterization of a cell line and patient-derived xenograft (PDX) from peritoneal metastasis of low-grade serous ovarian carcinoma. Sci Rep. 2020;10:6688. doi: 10.1038/s41598-020-63738-6
   PubMed Web of Science ®Google Scholar
• Gump JM, Thorburn A. Sorting cells for basal and induced autophagic flux by quantitative ratiometric flow cytometry. Autophagy. 2014;10(7):1327–1334. doi: 10.4161/auto.29394
   PubMed Web of Science ®Google Scholar