Dual inhibition of REV-ERBβ and autophagy as a novel pharmacological approach to induce cytotoxicity in cancer cells

Oncogene

Volumn 34, Issue 20, 2015, Pages 2597-2608

  De Mei, C ^a   Ercolani, L ^a   Parodi, C ^a   Veronesi, M ^a   Vecchio, C Lo ^a   Bottegoni, G ^a   Torrente, E ^a   Scarpelli, R ^a   Marotta, R ^a   Ruffili, R ^a   Mattioli, M ^a   Reggiani, A ^a   Wade, M ^a   Grimaldi, B ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CELL RECEPTOR; CYTOTOXIN; NR1D1 PROTEIN, HUMAN; NR1D2 PROTEIN, HUMAN; NUCLEAR RECEPTOR NR1D1; REPRESSOR PROTEIN;

ANTAGONISTS AND INHIBITORS; AUTOPHAGY; DRUG EFFECTS; DRUG SCREENING; GENETICS; HEK293 CELL LINE; HEPG2 CELL LINE; HUMAN; METABOLISM; NEOPLASMS;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; CYTOTOXINS; DRUG SCREENING ASSAYS, ANTITUMOR; HEK293 CELLS; HEP G2 CELLS; HUMANS; NEOPLASMS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRESSOR PROTEINS;

EID: 84938063155     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.203     Document Type: Article

References (44)

1. Harding HP, Lazar MA. The orphan receptor Rev-ErbA alpha activates transcription via a novel response element. Mol Cell Biol 1993; 13: 3113-3121.
2. Duez H, Staels B. Rev-erb-alpha: An integrator of circadian rhythms and metabolism. J Appl Physiol 2009; 107: 1972-1980.
3. Raghuram S, Stayrook KR, Huang P, Rogers PM, Nosie AK, McClure DB et al. Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat Struct Mol Biol 2007; 14: 1207-1213.
4. Teboul M, Grechez-Cassiau A, Guillaumond F, Delaunay F. How nuclear receptors tell time. J Appl Physiol 2009; 107: 1965-1971.
5. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT et al. Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 2012; 485: 123-127.
6. Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, Wang F et al. Rev-erbalpha and Rev-erbbeta coordinately protect the circadian clock and normal metabolic function. Genes Dev 2012; 26: 657-667.
7. Hastings MH, Reddy AB, Maywood ES. A clockwork web: Circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 2003; 4: 649-661.
8. Rossetti S, Esposito J, Corlazzoli F, Gregorski A, Sacchi N. Entrainment of breast (cancer) epithelial cells detects distinct circadian oscillation patterns for clock and hormone receptor genes. Cell Cycle 2012; 11: 350-360.
9. Sahar S, Sassone-Corsi P. Metabolism and cancer: The circadian clock connection. Nat Rev Cancer 2009; 9: 886-896.
10. Engelen E, Janssens RC, Yagita K, Smits VA, van der Horst GT, Tamanini F. Mammalian TIMELESS is involved in period determination and DNA damage-dependent phase advancing of the circadian clock. PLoS ONE 2013; 8: E56623.
11. Fu L, Lee CC. The circadian clock: Pacemaker and tumour suppressor. Nat Rev Cancer 2003; 3: 350-361.
12. Kelleher FC, Rao A, Maguire A. Circadian molecular clocks and cancer. Cancer Lett 2013; 342: 9-18.
13. Savvidis C, Koutsilieris M. Circadian rhythm disruption in cancer biology. Mol Med 2012; 18: 1249-1260.
14. Kourtidis A, Jain R, Carkner RD, Eifert C, Brosnan MJ, Conklin DS. An RNA interference screen identifies metabolic regulators NR1D1 and PBP as novel survival factors for breast cancer cells with the ERBB2 signature. Cancer Res 2010; 70: 1783-1792.
15. Solt LA, Wang Y, Banerjee S, Hughes T, Kojetin DJ, Lundasen T et al. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 2012; 485: 62-68.
16. Trump RP, Bresciani S, Cooper AW, Tellam JP, Wojno J, Blaikley J et al. Optimized chemical probes for REV-ERBalpha. J Med Chem 2013; 56: 4729-4737.
17. Kumar N, Solt LA, Wang Y, Rogers PM, Bhattacharyya G, Kamenecka TM et al. Regulation of adipogenesis by natural and synthetic REV-ERB ligands. Endocrinology 2010; 151: 3015-3025.
18. Kojetin D, Wang Y, Kamenecka TM, Burris TP. Identification of SR8278, a synthetic antagonist of the nuclear heme receptor REV-ERB. ACS Chem Biol 2011; 6: 131-134.
19. Bertucci F, Borie N, Ginestier C, Groulet A, Charafe-Jauffret E, Adelaide J et al. Identification and validation of an ERBB2 gene expression signature in breast cancers. Oncogene 2004; 23: 2564-2575.
20. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM et al. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 2000; 289: 2344-2347.
21. Holliday DL, Speirs V. Choosing the right cell line for breast cancer research. Breast Cancer Res 2011; 13: 215.
22. Konigshoff M, Wilhelm J, Bohle RM, Pingoud A, Hahn M. HER-2/neu gene copy number quantified by real-time PCR: Comparison of gene amplification, heterozygosity, and immunohistochemical status in breast cancer tissue. Clin Chem 2003; 49: 219-229.
23. Grimaldi B, Nakahata Y, Kaluzova M, Masubuchi S, Sassone-Corsi P. Chromatin remodeling, metabolism and circadian clocks: The interplay of CLOCK and SIRT1. Int J Biochem Cell Biol 2009; 41: 81-86.
24. Ozturk N, Lee JH, Gaddameedhi S, Sancar A. Loss of cryptochrome reduces cancer risk in p53 mutant mice. Proc Natl Acad Sci USA 2009; 106: 2841-2846.
25. Hastak K, Alli E, Ford JM. Synergistic chemosensitivity of triple-negative breast cancer cell lines to poly(ADP-Ribose) polymerase inhibition, gemcitabine, and cisplatin. Cancer Res 2010; 70: 7970-7980.
26. Carew JS, Espitia CM, Esquivel JA 2nd, Mahalingam D, Kelly KR, Reddy G et al. Lucanthone is a novel inhibitor of autophagy that induces cathepsin D-mediated apoptosis. J Biol Chem 2011; 286: 6602-6613.
27. Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007; 7: 961-967.
28. Woldt E, Sebti Y, Solt LA, Duhem C, Lancel S, Eeckhoute J et al. Rev-erb-alpha modulates skeletal muscle oxidative capacity by regulating mitochondrial biogenesis and autophagy. Nat Med 2013; 19: 1039-1046.
29. Nazio F, Strappazzon F, Antonioli M, Bielli P, Cianfanelli V, Bordi M et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol 2013; 15: 406-416.
30. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
31. Carew JS, Kelly KR, Nawrocki ST. Autophagy as a target for cancer therapy: New developments. Cancer Manag Res 2012; 4: 357-365.
32. Tormo D, Checinska A, Alonso-Curbelo D, Perez-Guijarro E, Canon E, Riveiro-Falkenbach E et al. Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell 2009; 16: 103-114.
33. Nadanaciva S, Lu S, Gebhard DF, Jessen BA, Pennie WD, Will Y. A high content screening assay for identifying lysosomotropic compounds. Toxicol In Vitro 2011; 25: 715-723.
34. Totrov M. Atomic property fields: Generalized 3D pharmacophoric potential for automated ligand superposition, pharmacophore elucidation and 3D QSAR. Chem Biol Drug Des 2008; 71: 15-27.
35. Vulpetti A, Dalvit C. Fluorine local environment: From screening to drug design. Drug Discov Today 2012; 17: 890-897.
36. Zhou C, Zhong W, Zhou J, Sheng F, Fang Z, Wei Y et al. Monitoring autophagic flux by an improved tandem fluorescent-tagged LC3 (mTagRFP-mWasabi-LC3) reveals that high-dose rapamycin impairs autophagic flux in cancer cells. Autophagy 2012; 8: 1215-1226.
37. Hu C, Solomon VR, Ulibarri G, Lee H. The efficacy and selectivity of tumor cell killing by Akt inhibitors are substantially increased by chloroquine. Bioorg Med Chem 2008; 16: 7888-7893.
38. Checinska A, Soengas MS. The gluttonous side of malignant melanoma: Basic and clinical implications of macroautophagy. Pigment Cell Melanoma Res 2011; 24: 1116-1132.
39. White E. Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer 2012; 12: 401-410.
40. Nishimura M, Naito S, Yokoi T. Tissue-specific mRNA expression profiles of human nuclear receptor subfamilies. Drug Metab Pharmacokinet 2004; 19: 135-149.
41. Tagad HD, Hamada Y, Nguyen JT, Hidaka K, Hamada T, Sohma Y et al. Structureguided design and synthesis of P1' position 1-phenylcycloalkylamine-derived pentapeptidic BACE1 inhibitors. Bioorg Med Chem 2011; 19: 5238-5246.
42. Dalvit C, Flocco M, Veronesi M, Stockman BJ. Fluorine-NMR competition binding experiments for high-throughput screening of large compound mixtures. Comb Chem High Throughput Screen 2002; 5: 605-611.
43. Grimaldi B, Bellet MM, Katada S, Astarita G, Hirayama J, Amin RH et al. PER2 controls lipid metabolism by direct regulation of PPARgamma. Cell Metab 2010; 12: 509-520.
44. Marotta R, Falqui A, Curcio A, Quarta A, Pellegrino T. Immunocytochemistry, electron tomography, and energy dispersive X-ray spectroscopy (EDXS) on cryosections of human cancer cells doped with stimuli responsive polymeric nanogels loaded with iron oxide nanoparticles. Methods Mol Biol 2013; 1025: 179-198.