Oncogenic BRAF Regulates Oxidative Metabolism via PGC1α and MITF

Cancer Cell - Tập 23 - Trang 302-315 - 2013
Rizwan Haq1,2, Jonathan Shoag3, Pedro Andreu-Perez2, Satoru Yokoyama2,4, Hannah Edelman2, Glenn C. Rowe3, Dennie T. Frederick5, Aeron D. Hurley6, Abhinav Nellore7, Andrew L. Kung8, Jennifer A. Wargo5, Jun S. Song7, David E. Fisher1,2, Zolt Arany3, Hans R. Widlund6
1Massachusetts General Hospital Cancer Center, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA
2Department of Dermatology, Cutaneous Biology Research Center, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA
3Cardiovascular Institute, Beth Israel Deaconess Medical Center, Boston, MA 02116, USA
4Division of Pathogenic Biochemistry, Institute of Natural Medicine, University of Toyama, 2630 Sugitani, Toyama 930-0194, Japan
5Department of Surgery, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA
6Department of Dermatology, Brigham and Women’s Hospital, Boston, MA 02115, USA
7Department of Epidemiology and Biostatistics, Institute for Human Genetics, University of California, San Francisco, San Francisco, CA 94143-0794, USA
8Department of Pediatrics, Columbia University Medical Center, New York, NY 10032, USA

Tài liệu tham khảo

Arany, 2008, HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha, Nature, 451, 1008, 10.1038/nature06613 Bensaad, 2006, TIGAR, a p53-inducible regulator of glycolysis and apoptosis, Cell, 126, 107, 10.1016/j.cell.2006.05.036 Bertolotto, 2011, A SUMOylation-defective MITF germline mutation predisposes to melanoma and renal carcinoma, Nature, 480, 94, 10.1038/nature10539 Bhalla, 2011, PGC1α promotes tumor growth by inducing gene expression programs supporting lipogenesis, Cancer Res., 71, 6888, 10.1158/0008-5472.CAN-11-1011 Board, 2009, Detection of BRAF mutations in the tumour and serum of patients enrolled in the AZD6244 (ARRY-142886) advanced melanoma phase II study, Br. J. Cancer, 101, 1724, 10.1038/sj.bjc.6605371 Bogunovic, 2009, Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival, Proc. Natl. Acad. Sci. USA, 106, 20429, 10.1073/pnas.0905139106 Bollag, 2010, Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma, Nature, 467, 596, 10.1038/nature09454 Boni, 2010, Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function, Cancer Res., 70, 5213, 10.1158/0008-5472.CAN-10-0118 Bonnet, 2007, A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth, Cancer Cell, 11, 37, 10.1016/j.ccr.2006.10.020 Carreira, 2006, Mitf regulation of Dia1 controls melanoma proliferation and invasiveness, Genes Dev., 20, 3426, 10.1101/gad.406406 Chapman, 2011, Improved survival with vemurafenib in melanoma with BRAF V600E mutation, N. Engl. J. Med., 364, 2507, 10.1056/NEJMoa1103782 Chinsomboon, 2009, The transcriptional coactivator PGC-1alpha mediates exercise-induced angiogenesis in skeletal muscle, Proc. Natl. Acad. Sci. USA, 106, 21401, 10.1073/pnas.0909131106 Colombi, 2011, Genome-wide shRNA screen reveals increased mitochondrial dependence upon mTORC2 addiction, Oncogene, 30, 1551, 10.1038/onc.2010.539 Cui, 2007, Central role of p53 in the suntan response and pathologic hyperpigmentation, Cell, 128, 853, 10.1016/j.cell.2006.12.045 Curtin, 2005, Distinct sets of genetic alterations in melanoma, N. Engl. J. Med., 353, 2135, 10.1056/NEJMoa050092 Cutting, 1933, Metabolic actions of dinitrophenol with the use of balanced and unbalanced diets, J. Am. Med. Assoc., 101 Dang, 2012, Links between metabolism and cancer, Genes Dev., 26, 877, 10.1101/gad.189365.112 Dankort, 2009, Braf(V600E) cooperates with Pten loss to induce metastatic melanoma, Nat. Genet., 41, 544, 10.1038/ng.356 Davies, 2002, Mutations of the BRAF gene in human cancer, Nature, 417, 949, 10.1038/nature00766 Dhomen, 2009, Oncogenic Braf induces melanocyte senescence and melanoma in mice, Cancer Cell, 15, 294, 10.1016/j.ccr.2009.02.022 D’Orazio, 2006, Topical drug rescue strategy and skin protection based on the role of Mc1r in UV-induced tanning, Nature, 443, 340, 10.1038/nature05098 Eichner, 2010, miR-378(∗) mediates metabolic shift in breast cancer cells via the PGC-1β/ERRγ transcriptional pathway, Cell Metab., 12, 352, 10.1016/j.cmet.2010.09.002 Fantin, 2006, Mitochondriotoxic compounds for cancer therapy, Oncogene, 25, 4787, 10.1038/sj.onc.1209599 Fantin, 2006, Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance, Cancer Cell, 9, 425, 10.1016/j.ccr.2006.04.023 Finck, 2006, PGC-1 coactivators: inducible regulators of energy metabolism in health and disease, J. Clin. Invest., 116, 615, 10.1172/JCI27794 Flaherty, 2010, Inhibition of mutated, activated BRAF in metastatic melanoma, N. Engl. J. Med., 363, 809, 10.1056/NEJMoa1002011 Garraway, 2005, Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma, Nature, 436, 117, 10.1038/nature03664 Girnun, 2012, The diverse role of the PPARγ coactivator 1 family of transcriptional coactivators in cancer, Semin. Cell Dev. Biol., 23, 381, 10.1016/j.semcdb.2012.01.007 Goding, 2011, Commentary. A picture of Mitf in melanoma immortality, Oncogene, 30, 2304, 10.1038/onc.2010.641 Gray-Schopfer, 2007, Melanoma biology and new targeted therapy, Nature, 445, 851, 10.1038/nature05661 Greger, 2012, Combinations of BRAF, MEK, and PI3K/mTOR inhibitors overcome acquired resistance to the BRAF inhibitor GSK2118436 dabrafenib, mediated by NRAS or MEK mutations, Mol. Cancer Ther., 11, 909, 10.1158/1535-7163.MCT-11-0989 Handschin, 2009, The biology of PGC-1α and its therapeutic potential, Trends Pharmacol. Sci., 30, 322, 10.1016/j.tips.2009.03.006 Handschin, 2003, An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle, Proc. Natl. Acad. Sci. USA, 100, 7111, 10.1073/pnas.1232352100 Haq, 2011, Biology and clinical relevance of the micropthalmia family of transcription factors in human cancer, J. Clin. Oncol., 29, 3474, 10.1200/JCO.2010.32.6223 Hemesath, 1998, MAP kinase links the transcription factor Microphthalmia to c-Kit signalling in melanocytes, Nature, 391, 298, 10.1038/34681 Herzig, 2001, CREB regulates hepatic gluconeogenesis through the coactivator PGC-1, Nature, 413, 179, 10.1038/35093131 Hingorani, 2003, Suppression of BRAF(V599E) in human melanoma abrogates transformation, Cancer Res., 63, 5198 Hoeflich, 2006, Oncogenic BRAF is required for tumor growth and maintenance in melanoma models, Cancer Res., 66, 999, 10.1158/0008-5472.CAN-05-2720 Hoek, 2006, Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature, Pigment Cell Res., 19, 290, 10.1111/j.1600-0749.2006.00322.x Joseph, 2010, The RAF inhibitor PLX4032 inhibits ERK signaling and tumor cell proliferation in a V600E BRAF-selective manner, Proc. Natl. Acad. Sci. USA, 107, 14903, 10.1073/pnas.1008990107 Karasarides, 2004, B-RAF is a therapeutic target in melanoma, Oncogene, 23, 6292, 10.1038/sj.onc.1207785 Kelly, 2004, Transcriptional regulatory circuits controlling mitochondrial biogenesis and function, Genes Dev., 18, 357, 10.1101/gad.1177604 Klimcakova, 2012, PGC-1α promotes the growth of ErbB2/Neu-induced mammary tumors by regulating nutrient supply, Cancer Res., 72, 1538, 10.1158/0008-5472.CAN-11-2967 Lehman, 2000, Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis, J. Clin. Invest., 106, 847, 10.1172/JCI10268 Leone, 2011, Transcriptional control of cardiac fuel metabolism and mitochondrial function, Cold Spring Harb. Symp. Quant. Biol., 76, 175, 10.1101/sqb.2011.76.011965 Li, 2012, YY1 regulates melanocyte development and function by cooperating with MITF, PLoS Genet., 8, e1002688, 10.1371/journal.pgen.1002688 Lin, 2002, Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres, Nature, 418, 797, 10.1038/nature00904 Lin, 2005, Metabolic control through the PGC-1 family of transcription coactivators, Cell Metab., 1, 361, 10.1016/j.cmet.2005.05.004 Lin, 2005, Hyperlipidemic effects of dietary saturated fats mediated through PGC-1β coactivation of SREBP, Cell, 120, 261, 10.1016/j.cell.2004.11.043 Lin, 2008, Modeling genomic diversity and tumor dependency in malignant melanoma, Cancer Res., 68, 664, 10.1158/0008-5472.CAN-07-2615 Matoba, 2006, p53 regulates mitochondrial respiration, Science, 312, 1650, 10.1126/science.1126863 Miura, 2008, Isoform-specific increases in murine skeletal muscle peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1alpha) mRNA in response to beta2-adrenergic receptor activation and exercise, Endocrinology, 149, 4527, 10.1210/en.2008-0466 Mootha, 2003, PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes, Nat. Genet., 34, 267, 10.1038/ng1180 Poulikakos, 2011, Mutant BRAF melanomas—dependence and resistance, Cancer Cell, 19, 11, 10.1016/j.ccr.2011.01.008 Pratilas, 2009, (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway, Proc. Natl. Acad. Sci. USA, 106, 4519, 10.1073/pnas.0900780106 Prickett, 2009, Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4, Nat. Genet., 41, 1127, 10.1038/ng.438 Sahin, 2011, Telomere dysfunction induces metabolic and mitochondrial compromise, Nature, 470, 359, 10.1038/nature09787 Sosman, 2012, Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib, N. Engl. J. Med., 366, 707, 10.1056/NEJMoa1112302 Stark, 2012, Frequent somatic mutations in MAP3K5 and MAP3K9 in metastatic melanoma identified by exome sequencing, Nat. Genet., 44, 165, 10.1038/ng.1041 Straussman, 2012, Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion, Nature, 487, 500, 10.1038/nature11183 Tainter, 1934, Use of dinitrophenol in nutritional disorders : a critical survey of clinical results, Am. J. Public Health Nations Health, 24, 1045, 10.2105/AJPH.24.10.1045 Tsai, 2008, Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity, Proc. Natl. Acad. Sci. USA, 105, 3041, 10.1073/pnas.0711741105 Uldry, 2006, Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation, Cell Metab., 3, 333, 10.1016/j.cmet.2006.04.002 Vachtenheim, 2010, “Transcription physiology” of pigment formation in melanocytes: central role of MITF, Exp. Dermatol., 19, 617, 10.1111/j.1600-0625.2009.01053.x Vander Heiden, 2009, Understanding the Warburg effect: the metabolic requirements of cell proliferation, Science, 324, 1029, 10.1126/science.1160809 Wan, 2004, Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF, Cell, 116, 855, 10.1016/S0092-8674(04)00215-6 Wang, 2011, Increases in mitochondrial biogenesis impair carcinogenesis at multiple levels, Mol. Oncol., 5, 399, 10.1016/j.molonc.2011.07.008 Warburg, 1956, On the origin of cancer cells, Science, 123, 309, 10.1126/science.123.3191.309 Weinberg, 2010, Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity, Proc. Natl. Acad. Sci. USA, 107, 8788, 10.1073/pnas.1003428107 Wellbrock, 2005, Elevated expression of MITF counteracts B-RAF-stimulated melanocyte and melanoma cell proliferation, J. Cell Biol., 170, 703, 10.1083/jcb.200505059 Wellbrock, 2008, Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF, PLoS One, 3, e2734, 10.1371/journal.pone.0002734 Wise, 2010, Glutamine addiction: a new therapeutic target in cancer, Trends Biochem. Sci., 35, 427, 10.1016/j.tibs.2010.05.003 Wolfrum, 2006, Coactivation of Foxa2 through Pgc-1beta promotes liver fatty acid oxidation and triglyceride/VLDL secretion, Cell Metab., 3, 99, 10.1016/j.cmet.2006.01.001 Wu, 1999, Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1, Cell, 98, 115, 10.1016/S0092-8674(00)80611-X Wu, 2000, c-Kit triggers dual phosphorylations, which couple activation and degradation of the essential melanocyte factor Mi, Genes Dev., 14, 301, 10.1101/gad.14.3.301 Yokoyama, 2011, A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma, Nature, 480, 99, 10.1038/nature10630 Yoon, 2001, Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1, Nature, 413, 131, 10.1038/35093050 Yun, 2009, Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells, Science, 325, 1555, 10.1126/science.1174229