Home LiteratureArticle Details
PMID: 24251082 Published · ppublish English Journal Article

BRAF inhibition is associated with increased clonality in tumor-infiltrating lymphocytes.

Oncoimmunology ·Vol. 2 ·No. 10 ·2013-10-01 ·Pages e26615

Cooper ZA, Frederick DT, Juneja VR, Sullivan RJ, Lawrence DP, Piris A, Sharpe AH, Fisher DE, Flaherty KT, Wargo JA

Abstract

There have been significant advances with regard to BRAF-targeted therapies against metastatic melanoma. However, the majority of patients receiving BRAF inhibitors (BRAFi) manifest disease progression within a year. We have recently shown that melanoma patients treated with BRAFi exhibit an increase in melanoma-associated antigens and in CD8+ tumor-infiltrating lymphocytes in response to therapy. To characterize such a T-cell infiltrate, we analyzed the complementarity-determining region 3 (CDR3) of rearranged T-cell receptor (TCR) β chain-coding genes in tumor biopsies obtained before the initiation of BRAFi and 10-14 d later. We observed an increase in the clonality of tumor-infiltrating lymphocytes in 7 of 8 patients receiving BRAFi, with a statistically significant 21% aggregate increase in clonality. Over 80% of individual T-cell clones detected after initiation of BRAFi treatment were new clones. Interestingly, the comparison of tumor infiltrates with clinical responses revealed that patients who had a high proportion of pre-existing dominant clones after the administration of BRAFi responded better to therapy than patients who had a low proportion of such pre-existing dominant clones following BRAFi. These data suggest that although the inhibition of BRAF in melanoma patients results in tumor infiltration by new lymphocytes, the response to treatment appears to be related to the presence of a pre-existing population of tumor-infiltrating T-cell clones.

Keywords
BRAF T cells TILs melanoma vemurafenib
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Cooper Zachary A
Department of Surgical Oncology; University of Texas MD Anderson Cancer Center; Houston, TX USA ; Department of Genomic Medicine; University of Texas MD Anderson Cancer Center; Houston, TX USA.
Frederick Dennie T
Juneja Vikram R
Sullivan Ryan J
Lawrence Donald P
Piris Adriano
Sharpe Arlene H
Fisher David E
Flaherty Keith T
Wargo Jennifer A
References (32)
32 references, click to expand
  1. Resistance to BRAF inhibition in melanomas.
    N Engl J Med. 2011 Feb 24;364(8):772-4 PMID: 21345109
  2. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer.
    N Engl J Med. 2012 Jun 28;366(26):2455-65 PMID: 22658128
  3. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion.
    Nature. 2012 Jul 26;487(7408):500-4 PMID: 22763439
  4. MEK inhibitors selectively suppress alloreactivity and graft-versus-host disease in a memory stage-dependent manner.
    Blood. 2013 Jun 6;121(23):4617-26 PMID: 23575444
  5. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E).
    Nature. 2011 Nov 23;480(7377):387-90 PMID: 22113612
  6. Oncogenic BRAF(V600E) promotes stromal cell-mediated immunosuppression via induction of interleukin-1 in melanoma.
    Clin Cancer Res. 2012 Oct 1;18(19):5329-40 PMID: 22850568
  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. Paradoxical activation and RAF inhibitor resistance of BRAF protein kinase fusions characterizing pediatric astrocytomas.
    Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):5957-62 PMID: 23533272
  9. Mutations of the BRAF gene in human cancer.
    Nature. 2002 Jun 27;417(6892):949-54 PMID: 12068308
  10. Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function.
    Cancer Res. 2010 Jul 1;70(13):5213-9 PMID: 20551059
  11. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation.
    Nature. 2010 Dec 16;468(7326):968-72 PMID: 21107320
  12. BRAF inhibition increases tumor infiltration by T cells and enhances the antitumor activity of adoptive immunotherapy in mice.
    Clin Cancer Res. 2013 Jan 15;19(2):393-403 PMID: 23204132
  13. 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
  14. Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance.
    Nature. 2013 Feb 14;494(7436):251-5 PMID: 23302800
  15. Mutation-driven drug development in melanoma.
    Curr Opin Oncol. 2010 May;22(3):178-83 PMID: 20401974
  16. 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
  17. Heterogeneity of T-cell clones infiltrating primary malignant melanomas.
    J Invest Dermatol. 2006 Feb;126(2):393-8 PMID: 16374454
  18. Point mutations in the beta chain CDR3 can alter the T cell receptor recognition pattern on an MHC class I/peptide complex over a broad interface area.
    Mol Immunol. 1998 Jul;35(10):593-607 PMID: 9823758
  19. 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
  20. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1).
    Eur J Cancer. 2009 Jan;45(2):228-47 PMID: 19097774
  21. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib.
    N Engl J Med. 2012 Feb 23;366(8):707-14 PMID: 22356324
  22. Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma.
    Clin Cancer Res. 2012 Mar 1;18(5):1386-94 PMID: 22156613
  23. Improved survival with ipilimumab in patients with metastatic melanoma.
    N Engl J Med. 2010 Aug 19;363(8):711-23 PMID: 20525992
  24. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation.
    Nature. 2010 Dec 16;468(7326):973-7 PMID: 21107323
  25. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer.
    N Engl J Med. 2012 Jun 28;366(26):2443-54 PMID: 22658127
  26. Disparate individual fates compose robust CD8+ T cell immunity.
    Science. 2013 May 3;340(6132):630-5 PMID: 23493420
  27. Predicted complementarity determining regions of the T cell antigen receptor determine antigen specificity.
    EMBO J. 1995 Mar 1;14(5):927-38 PMID: 7534228
  28. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations.
    N Engl J Med. 2012 Nov;367(18):1694-703 PMID: 23020132
  29. A genome-scale RNA interference screen implicates NF1 loss in resistance to RAF inhibition.
    Cancer Discov. 2013 Mar;3(3):350-62 PMID: 23288408
  30. Overlap and effective size of the human CD8+ T cell receptor repertoire.
    Sci Transl Med. 2010 Sep 1;2(47):47ra64 PMID: 20811043
  31. Elucidating distinct roles for NF1 in melanomagenesis.
    Cancer Discov. 2013 Mar;3(3):338-49 PMID: 23171796
  32. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma.
    Clin Cancer Res. 2013 Mar 1;19(5):1225-31 PMID: 23307859
Article Info
Journal
Oncoimmunology
Abbr.
Oncoimmunology
ISSN
2162-4011
Published
2013-10-01
Epub
2013-00-15
Pages
e26615
Language
English
Region
United States
NLM ID
101570526
PMCID
PMC3827093
Grants
NCI NIH HHS · P01 CA163222 · United States
NIAMS NIH HHS · R01 AR043369 · United States
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