Home LiteratureArticle Details
PMID: 23288408 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

A genome-scale RNA interference screen implicates NF1 loss in resistance to RAF inhibition.

Cancer discovery ·Vol. 3 ·No. 3 ·2013-03-00 ·Pages 350-62

Whittaker SR, Theurillat JP, Van Allen E, Wagle N, Hsiao J, Cowley GS, Schadendorf D, Root DE, Garraway LA

Abstract

RAF inhibitors such as vemurafenib and dabrafenib block BRAF-mediated cell proliferation and achieve meaningful clinical benefit in the vast majority of patients with BRAF(V600E)-mutant melanoma. However, some patients do not respond to this regimen, and nearly all progress to therapeutic resistance. We used a pooled RNA interference screen targeting more than 16,500 genes to discover loss-of-function events that could drive resistance to RAF inhibition. The highest ranking gene was NF1, which encodes neurofibromin, a tumor suppressor that inhibits RAS activity. NF1 loss mediates resistance to RAF and mitogen-activated protein kinase (MAPK) kinase kinase (MEK) inhibitors through sustained MAPK pathway activation. However, cells lacking NF1 retained sensitivity to the irreversible RAF inhibitor AZ628 and an ERK inhibitor. NF1 mutations were observed in BRAF-mutant tumor cells that are intrinsically resistant to RAF inhibition and in melanoma tumors obtained from patients exhibiting resistance to vemurafenib, thus showing the clinical potential for NF1-driven resistance to RAF/MEK-targeted therapies.

MeSH Terms
Cell Line, Tumor Cell Proliferation Drug Resistance, Neoplasm Humans MAP Kinase Signaling System Melanoma/drug therapy,genetics,metabolism Mutation Neurofibromin 1/deficiency,genetics Protein Kinase Inhibitors/pharmacology Proto-Oncogene Proteins B-raf/antagonists & inhibitors,genetics,metabolism RNA Interference
Chemicals
Neurofibromin 1 Protein Kinase Inhibitors BRAF protein, human Proto-Oncogene Proteins B-raf
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Whittaker Steven R
Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, Massachusetts 02215, USA.
Theurillat Jean-Philippe
Van Allen Eliezer
Wagle Nikhil
Hsiao Jessica
Cowley Glenn S
Schadendorf Dirk
Root David E
Garraway Levi A
References (44)
44 references, click to expand
  1. Elevated CRAF as a potential mechanism of acquired resistance to BRAF inhibition in melanoma.
    Cancer Res. 2008 Jun 15;68(12):4853-61 PMID: 18559533
  2. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion.
    Nature. 2012 Jul 26;487(7408):500-4 PMID: 22763439
  3. Acquired resistance to tyrosine kinase inhibitors during cancer therapy.
    Curr Opin Genet Dev. 2008 Feb;18(1):73-9 PMID: 18325754
  4. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia.
    Cancer Cell. 2002 Aug;2(2):117-25 PMID: 12204532
  5. The RAF inhibitor PLX4032 inhibits ERK signaling and tumor cell proliferation in a V600E BRAF-selective manner.
    Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14903-8 PMID: 20668238
  6. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E).
    Nature. 2011 Nov 23;480(7377):387-90 PMID: 22113612
  7. Improved survival with vemurafenib in melanoma with BRAF V600E mutation.
    N Engl J Med. 2011 Jun 30;364(26):2507-16 PMID: 21639808
  8. A public genome-scale lentiviral expression library of human ORFs.
    Nat Methods. 2011 Jun 26;8(8):659-61 PMID: 21706014
  9. Gatekeeper mutations mediate resistance to BRAF-targeted therapies.
    Sci Transl Med. 2010 Jun 9;2(35):35ra41 PMID: 20538618
  10. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing.
    Nat Biotechnol. 2009 Feb;27(2):182-9 PMID: 19182786
  11. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF.
    Cell. 2010 Jan 22;140(2):209-21 PMID: 20141835
  12. 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 Dec 14;18(6):683-95 PMID: 21156289
  13. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial.
    Lancet. 2012 Jul 28;380(9839):358-65 PMID: 22735384
  14. Highly parallel identification of essential genes in cancer cells.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20380-5 PMID: 19091943
  15. Nature and mRNA effect of 282 different NF1 point mutations: focus on splicing alterations.
    Hum Mutat. 2008 Sep;29(9):E173-93 PMID: 18546366
  16. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP.
    Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2070-5 PMID: 18227510
  17. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity.
    Nature. 2012 Mar 28;483(7391):603-7 PMID: 22460905
  18. Improved survival with MEK inhibition in BRAF-mutated melanoma.
    N Engl J Med. 2012 Jul 12;367(2):107-14 PMID: 22663011
  19. In melanoma, RAS mutations are accompanied by switching signaling from BRAF to CRAF and disrupted cyclic AMP signaling.
    Cancer Res. 2006 Oct 1;66(19):9483-91 PMID: 17018604
  20. Gene sets identified with oncogene cooperativity analysis regulate in vivo growth and survival of leukemia stem cells.
    Cell Stem Cell. 2012 Sep 7;11(3):359-72 PMID: 22863534
  21. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation.
    Nature. 2010 Dec 16;468(7326):973-7 PMID: 21107323
  22. Raf-1 promotes cell survival by antagonizing apoptosis signal-regulating kinase 1 through a MEK-ERK independent mechanism.
    Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7783-8 PMID: 11427728
  23. ContEst: estimating cross-contamination of human samples in next-generation sequencing data.
    Bioinformatics. 2011 Sep 15;27(18):2601-2 PMID: 21803805
  24. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF.
    Nature. 2010 Mar 18;464(7287):427-30 PMID: 20179705
  25. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation.
    Nature. 2010 Dec 16;468(7326):968-72 PMID: 21107320
  26. Proteins regulating Ras and its relatives.
    Nature. 1993 Dec 16;366(6456):643-54 PMID: 8259209
  27. A MEK-independent role for CRAF in mitosis and tumor progression.
    Nat Med. 2011 Nov 13;17(12):1641-5 PMID: 22081024
  28. The catalytic domain of the neurofibromatosis type 1 gene product stimulates ras GTPase and complements ira mutants of S. cerevisiae.
    Cell. 1990 Nov 16;63(4):835-41 PMID: 2121369
  29. A landscape of driver mutations in melanoma.
    Cell. 2012 Jul 20;150(2):251-63 PMID: 22817889
  30. Predicting the functional impact of protein mutations: application to cancer genomics.
    Nucleic Acids Res. 2011 Sep 1;39(17):e118 PMID: 21727090
  31. MEK1 mutations confer resistance to MEK and B-RAF inhibition.
    Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20411-6 PMID: 19915144
  32. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth.
    Nature. 2010 Mar 18;464(7287):431-5 PMID: 20130576
  33. Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1.
    Science. 2004 Dec 24;306(5705):2267-70 PMID: 15618521
  34. Resistance to selective BRAF inhibition can be mediated by modest upstream pathway activation.
    Cancer Res. 2012 Feb 15;72(4):969-78 PMID: 22205714
  35. Integrative genomics viewer.
    Nat Biotechnol. 2011 Jan;29(1):24-6 PMID: 21221095
  36. A new mutation in the KIT ATP pocket causes acquired resistance to imatinib in a gastrointestinal stromal tumor patient.
    Gastroenterology. 2004 Jul;127(1):294-9 PMID: 15236194
  37. Human Splicing Finder: an online bioinformatics tool to predict splicing signals.
    Nucleic Acids Res. 2009 May;37(9):e67 PMID: 19339519
  38. Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma.
    Nat Genet. 2012 Sep;44(9):1006-14 PMID: 22842228
  39. RIP2 is a Raf1-activated mitogen-activated protein kinase kinase.
    J Biol Chem. 1999 Nov 19;274(47):33684-90 PMID: 10559258
  40. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma.
    Nature. 2005 Jul 7;436(7047):117-22 PMID: 16001072
  41. EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib.
    Cancer Discov. 2012 Mar;2(3):227-35 PMID: 22448344
  42. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors.
    Nature. 2012 Jul 26;487(7408):505-9 PMID: 22763448
  43. Structure-guided design of potent and selective pyrimidylpyrrole inhibitors of extracellular signal-regulated kinase (ERK) using conformational control.
    J Med Chem. 2009 Oct 22;52(20):6362-8 PMID: 19827834
  44. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations.
    N Engl J Med. 2012 Nov;367(18):1694-703 PMID: 23020132
Article Info
Journal
Cancer discovery
Abbr.
Cancer Discov
ISSN
2159-8290
Published
2013-03-00
Epub
2013-00-03
Pages
350-62
Language
English
Region
United States
NLM ID
101561693
PMCID
PMC3606893
Subset
IM
Grants
NCI NIH HHS · 5P50CA127003-05 · United States
NCI NIH HHS · T32 CA009172 · United States
NCI NIH HHS · R33 CA155554 · United States
NCI NIH HHS · P50 CA127003 · United States
NCI NIH HHS · P01 CA163222 · United States
NCI NIH HHS · P50 CA093683 · United States
NIH HHS · DP2OD002750 · United States
NIH HHS · DP2 OD002750 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com