Elucidating distinct roles for NF1 in melanomagenesis

Cancer Discovery

Volumn 3, Issue 3, 2013, Pages 339-349

  Maertens, Ophélia ^a,b   Johnson, Bryan ^a,b   Hollstein, Pablo ^a,b   Frederick, Dennie T ^c   Cooper, Zachary A ^c   Messiaen, Ludwine ^e   Bronson, Roderick T ^b   McMahon, Martin ^f,g   Granter, Scott ^a,b   Flaherty, Keith ^c   Wargo, Jennifer A ^c   Marais, Richard ^h   Cichowski, Karen ^a,b,d  

^a Brigham and Women's Hospital   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; DABRAFENIB; HYDROXYTAMOXIFEN; MAMMALIAN TARGET OF RAPAMYCIN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; N (2, 3 DIHYDROXYPROPOXY) 3, 4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO) BENZAMIDE; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; N [3 (5 CHLORO 1H PYRROLO [2, 3 B] PYRIDINE 3 CARBONYL) 2, 4 DIFLUOROPHENYL] PROPANESULFONAMIDE; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; NEUROFIBROMIN; PHOSPHATIDYLINOSITOL 3 KINASE; PICTILISIB; PROTEIN HYDROLYSATE; RAPAMYCIN; SHORT HAIRPIN RNA; T 5648; TAMOXIFEN; TRAMETINIB; UNCLASSIFIED DRUG; VEMURAFENIB; BRAF PROTEIN, HUMAN; INDOLE DERIVATIVE; SULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; GENE MUTATION; GENOTYPE; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MELANOGENESIS; MELANOMA; METASTASIS; METASTATIC MELANOMA; MOUSE; MULTIPLEX LIGATION DEPENDENT PROBE AMPLIFICATION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE ANALYSIS; TUMOR BIOPSY; TUMOR REGRESSION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOGENESIS; CELL GROWTH; DEFICIENCY; DISEASE MODEL; DRUG RESISTANCE; DRUG SCREENING; GENETICS; MELANOCYTE; METABOLISM; MUTATION; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CARCINOGENESIS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; GENES, NEUROFIBROMATOSIS 1; GENOTYPE; HUMANS; INDOLES; MELANOCYTES; MELANOMA; MICE; MICE, NUDE; MUTATION; NEUROFIBROMIN 1; PROTO-ONCOGENE PROTEINS B-RAF; SIGNAL TRANSDUCTION; SULFONAMIDES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84876037369     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-12-0313     Document Type: Article

References (57)

1. Courtois-Cox S, Jones SL, Cichowski K. Many roads lead to oncogeneinduced senescence. Oncogene 2008; 27: 2801-9.
2. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes Dev 2010; 24: 2463-79.
3. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444: 633-7.
4. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444: 638-42.
5. Mallette FA, Gaumont-Leclerc MF, Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev 2007; 21: 43-8.
6. Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003; 113: 703-16.
7. Courtois-Cox S, Genther Williams SM, Reczek EE, Johnson BW, McGillicuddy LT, Johannessen CM, et al. A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell 2006; 10: 459-72.
8. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 2008; 132: 363-74.
9. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, et al. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 2008; 133: 1006-18.
10. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, et al. Oncogene-induced senescence relayed by an interleukin-dependent infl ammatory network. Cell 2008; 133: 1019-31.
11. Gray-Schopfer VC, Cheong SC, Chong H, Chow J, Moss T, Abdel-Malek ZA, et al. Cellular senescence in naevi and immortalisation in melanoma: a role for p16? Br J Cancer 2006; 95: 496-505.
12. Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM, et al. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005; 436: 720-4.
13. Garnett MJ, Marais R. Guilty as charged: B-RAF is a human oncogene. Cancer Cell 2004; 6: 313-9.
14. Dankort D, Curley DP, Cartlidge RA, Nelson B, Karnezis AN, Damsky WE, et al. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 2009; 41: 544-52.
15. Dhomen N, Reis-Filho JS, da Rocha Dias S, Hayward R, Savage K, Delmas V, et al. Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 2009; 15: 294-303.
16. Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, Robbins CM, et al. High frequency of BRAF mutations in nevi. Nat Genet 2003; 33: 19-20.
17. Vredeveld LC, Possik PA, Smit MA, Meissl K, Michaloglou C, Horlings HM, et al. Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Genes Dev 2012; 26: 1055-69.
18. Bernards A, Settleman J. GAPs in growth factor signalling. Growth Factors 2005; 23: 143-9.
19. Dasgupta B, Yi Y, Chen DY, Weber JD, Gutmann DH. Proteomic analysis reveals hyperactivation of the mammalian target of rapamycin pathway in neurofi bromatosis 1-associated human and mouse brain tumors. Cancer Res 2005; 65: 2755-
20. Johannessen CM, Reczek EE, James MF, Brems H, Legius E, Cichowski K. The NF1 tumor suppressor critically regulates TSC2 and mTOR. Proc Natl Acad Sci U S A 2005; 102: 8573-8.
21. Cancer Genome Atlas Research Network. Comprehensive genomic characterization defi nes human glioblastoma genes and core pathways. Nature 2008; 455: 1061-8.
22. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008; 455: 1069-75.
23. McGillicuddy LT, Fromm JA, Hollstein PE, Kubek S, Beroukhim R, De Raedt T, et al. Proteasomal and genetic inactivation of the NF1 tumor suppressor in gliomagenesis. Cancer Cell 2009; 16: 44-54.
24. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008; 321: 1807-12.
25. Holzel M, Huang S, Koster J, Ora I, Lakeman A, Caron H, et al. NF1 is a tumor suppressor in neuroblastoma that determines retinoic acid response and disease outcome. Cell 2010; 142: 218-29.
26. Bosch E, Cherwinski H, Peterson D, McMahon M. Mutations of critical amino acids affect the biological and biochemical properties of oncogenic A-Raf and Raf-1. Oncogene 1997; 15: 1021-33.
27. Zhu J, Woods D, McMahon M, Bishop JM. Senescence of human fi broblasts induced by oncogenic Raf. Genes Dev 1998; 12: 2997-3007.
28. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, McMahon M. Rafinduced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 1997; 17: 5598-611.
29. De Schepper S, Boucneau J, Lambert J, Messiaen L, Naeyaert JM. Pigment cell-related manifestations in neurofi bromatosis type 1: an overview. Pigment Cell Res 2005; 18: 13-24.
30. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, et al. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 2001; 15: 859-76.
31. Dankort D, Filenova E, Collado M, Serrano M, Jones K, McMahon M. A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors. Genes Dev 2007; 21: 379-84.
32. Bosenberg M, Muthusamy V, Curley DP, Wang Z, Hobbs C, Nelson B, et al. Characterization of melanocyte-specifi c inducible Cre recombinase transgenic mice. Genesis 2006; 44: 262-7.
33. Ramjaun AR, Downward J. Ras and phosphoinositide 3-kinase: partners in development and tumorigenesis. Cell Cycle 2007; 6: 2902-5.
34. Johannessen CM, Johnson BW, Williams SM, Chan AW, Reczek EE, Lynch RC, et al. TORC1 is essential for NF1-associated malignancies. Curr Biol 2008; 18: 56-62.
35. Ji Z, Flaherty KT, Tsao H. Targeting the RAS pathway in melanoma. Trends Mol Med 2012; 18: 27-35.
36. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, et al. Clinical effi cacy of a RAF inhibitor needs broad target blockade in BRAFmutant melanoma. Nature 2010; 467: 596-9.
37. De Raedt T, Walton Z, Yecies JL, Li D, Chen Y, Malone CF, et al. Exploiting cancer cell vulnerabilities to develop a combination therapy for ras-driven tumors. Cancer Cell 2011; 20: 400-13.
38. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010; 140: 209-21.
39. Lin WM, Baker AC, Beroukhim R, Winckler W, Feng W, Marmion JM, et al. Modeling genomic diversity and tumor dependency in malignant melanoma. Cancer Res 2008; 68: 664-73.
40. Smalley KS, Xiao M, Villanueva J, Nguyen TK, Flaherty KT, Letrero R, et al. CRAF inhibition induces apoptosis in melanoma cells with non-V600E BRAF mutations. Oncogene 2009; 28: 85-94.
41. Guldberg P, thor Straten P, Birck A, Ahrenkiel V, Kirkin AF, Zeuthen J. Disruption of the MMAC1/PTEN gene by deletion or mutation is a frequent event in malignant melanoma. Cancer Res 1997; 57: 3660-3.
42. J ohannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010; 468: 968-72.
43. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010; 468: 973-7.
44. Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, Moriceau G, et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 2011; 480: 387-90.
45. Shi H, Moriceau G, Kong X, Lee MK, Lee H, Koya RC, et al. Melanoma whole-exome sequencing identifi es (V600E)B-RAF amplifi cationmediated acquired B-RAF inhibitor resistance. Nat Commun 2012; 3: 724.
46. Villanueva J, Vultur A, Lee JT, Somasundaram R, Fukunaga-Kalabis M, Cipolla AK, et al. Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell 2010; 18: 683-95.
47. P araiso K H, X iang Y, R ebecca V W, A bel E V, Chen Y A, Munko A C, et al. PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res 2011; 71: 2750-60.
48. Shao Y, Aplin AE. Akt3-mediated resistance to apoptosis in B-RAFtargeted melanoma cells. Cancer Res 2010; 70: 6670-81.
49. Cichowski K, Santiago S, Jardim M, Johnson BW, Jacks T. Dynamic regulation of the Ras pathway via proteolysis of the NF1 tumor suppressor. Genes Dev 2003; 17: 449-54.
50. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al. A biomarker that identifi es senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995; 92: 9363-7.
51. Messiaen LM, Callens T, Mortier G, Beysen D, Vandenbroucke I, Van Roy N, et al. Exhaustive mutation analysis of the NF1 gene allows identifi cation of 95% of mutations and reveals a high frequency of unusual splicing defects. Hum Mutat 2000; 15: 541-55.
52. W immer K, Yao S, Claes K, Kehrer-Sawatzki H, Tinschert S, De Raedt T, et al. Spectrum of single-and multiexon NF1 copy number changes in a cohort of 1,100 unselected NF1 patients. Genes Chromosomes Cancer 2006; 45: 265-76.
53. B arretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483: 603-7.
54. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011; 39: D945-50.
55. Berger MF, Hodis E, Heffernan TP, Deribe YL, Lawrence MS, Protopopov A, et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 2012; 485: 502-6.
56. H odis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, et al. A landscape of driver mutations in melanoma. Cell 2012; 150: 251-63.
57. Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, et al. Exome sequencing identifi es recurrent somatic RAC1 mutations in melanoma. Nat Genet 2012; 44: 1006-14