Blocking oncogenic RAS enhances tumour cell surface MHC class I expression but does not alter susceptibility to cytotoxic lymphocytes

Molecular Immunology

Volumn 58, Issue 2, 2013, Pages 160-168

  El Jawhari, Jehan J ^a,c   El Sherbiny, Yasser M ^a,c   Scott, Gina B ^a   Morgan, Ruth S M ^a   Prestwich, Robin ^a   Bowles, Paul A ^a,b   Blair, G Eric ^b   Tanaka, Tomoyuki ^a   Rabbitts, Terence H ^a,d   Meade, Josephine L ^a,b   Cook, Graham P ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c MANSOURA UNIVERSITY   (Egypt)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Antigen presentation; MHC class I; Natural killer cells; RAS oncogene; Tumour immune evasion; Tumour immunology

Indexed keywords

ACTIN; BETA 2 MICROGLOBULIN; CALNEXIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GAMMA INTERFERON; HLA A2 ANTIGEN; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MELAN A; MESSENGER RNA; RAS PROTEIN; TAPASIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; CANCER CELL CULTURE; CANCER SUSCEPTIBILITY; CD8+ T LYMPHOCYTE; CELL STRAIN HCT116; CELL SURFACE; CODON; COLORECTAL CANCER; CYTOTOXIC LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DEGRANULATION; FIBROSARCOMA; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; NATURAL KILLER CELL; ONCOGENE RAS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; TUMOR CELL LINE; WILD TYPE;

ANTIGEN PRESENTATION; MHC CLASS I; NATURAL KILLER CELLS; RAS ONCOGENE; TUMOUR IMMUNE EVASION; TUMOUR IMMUNOLOGY;

ANTIBODIES; ANTIGENS, SURFACE; CELL LINE, TUMOR; GENE DELETION; HCT116 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; NEOPLASMS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84890851726     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.11.020     Document Type: Article

References (64)

1. Almeida C.R., Davis D.M. Segregation of HLA-C from ICAM-1 at NK cell immune synapses is controlled by its cell surface density. J. Immunol. 2006, 177:6904-6910.
2. Almeida C.R., Ashkenazi A., Shahaf G., Kaplan D., Davis D.M., Mehr R. Human NK cells differ more in their KIR2DL1-dependent thresholds for HLA-Cw6-mediated inhibition than in their maximal killing capacity. PLoS ONE 2011, 6:e24927.
3. Atkins D., Breuckmann A., Schmahl G.E., Binner P., Ferrone S., Krummenauer F., Storkel S., Seliger B. MHC class I antigen processing pathway defects, ras mutations and disease stage in colorectal carcinoma. Int. J. Cancer 2004, 109:265-273.
4. Bernards R., Schrier P.I., Houweling A., Bos J.L., van der Eb A.J., Zijlstra M., Melief C.J. Tumorigenicity of cells transformed by adenovirus type 12 by evasion of T-cell immunity. Nature 1983, 305:776-779.
5. Bernards R., Dessain S.K., Weinberg R.A. N-myc amplification causes down-modulation of MHC class I antigen expression in neuroblastoma. Cell 1986, 47:667-674.
6. Betts M.R., Brenchley J.M., Price D.A., De Rosa S.C., Douek D.C., Roederer M., Koup R.A. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 2003, 281:65-78.
7. Bicknell D.C., Rowan A., Bodmer W.F. Beta 2-microglobulin gene mutations: a study of established colorectal cell lines and fresh tumors. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:4751-4755.
8. Campoli M., Ferrone S. HLA antigen changes in malignant cells: epigenetic mechanisms and biologic significance. Oncogene 2008, 27:5869-5885.
9. Chowdhury D., Lieberman J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 2008, 26:389-420.
10. Cohen G.B., Gandhi R.T., Davis D.M., Mandelboim O., Chen B.K., Strominger J.L., Baltimore D. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 1999, 10:661-671.
11. Delp K., Momburg F., Hilmes C., Huber C., Seliger B. Functional deficiencies of components of the MHC class I antigen pathway in human tumors of epithelial origin. Bone Marrow Transpl. 2000, 25(Suppl. 2):S88-S95.
12. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
13. Eagle R.A., Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 2007, 7:737-744.
14. Forbes S.A., Tang G., Bindal N., Bamford S., Dawson E., Cole C., Kok C.Y., Jia M., Ewing R., Menzies A., Teague J.W., Stratton M.R., Futreal P.A. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res. 2010, 38:D652-D657.
15. Forbes S.A., Bindal N., Bamford S., Cole C., Kok C.Y., Beare D., Jia M., Shepherd R., Leung K., Menzies A., Teague J.W., Campbell P.J., Stratton M.R., Futreal P.A. COSMIC: mining complete cancer genomes in the catalogue of somatic mutations in cancer. Nucleic Acids Res. 2011, 39:D945-D950.
16. Gasser S., Orsulic S., Brown E.J., Raulet D.H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005, 436:1186-1190.
17. Gogusev J., Teutsch B., Morin M.T., Mongiat F., Haguenau F., Suskind G., Rabotti G.F. Inhibition of HLA class I antigen and mRNA expression induced by Rous sarcoma virus in transformed human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:203-207.
18. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
19. Henderson R.A., Michel H., Sakaguchi K., Shabanowitz J., Appella E., Hunt D.F., Engelhard V.H. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 1992, 255:1264-1266.
20. Hirota T., Irie K., Okamoto R., Ikeda W., Takai Y. Transcriptional activation of the mouse Necl-5/Tage4/PVR/CD155 gene by fibroblast growth factor or oncogenic Ras through the Raf-MEK-ERK-AP-1 pathway. Oncogene 2005, 24:2229-2235.
21. Holmes T.D., El-Sherbiny Y.M., Davison A., Clough S.L., Blair G.E., Cook G.P. A human NK cell activation/inhibition threshold allows small changes in the target cell surface phenotype to dramatically alter susceptibility to NK cells. J. Immunol. 2011, 186:1538-1545.
22. Howcroft T.K., Richardson J.C., Singer D.S. MHC class I gene expression is negatively regulated by the proto-oncogene, c-jun. EMBO J. 1993, 12:3163-3169.
23. Karnoub A.E., Weinberg R.A. Ras oncogenes: split personalities. Nat. Rev. Mol. Cell Biol. 2008, 9:517-531.
24. Klampfer L., Huang J., Corner G., Mariadason J., Arango D., Sasazuki T., Shirasawa S., Augenlicht L. Oncogenic Ki-ras inhibits the expression of interferon-responsive genes through inhibition of STAT1 and STAT2 expression. J. Biol. Chem. 2003, 278:46278-46287.
25. Krzewski K., Coligan J.E. Human NK cell lytic granules and regulation of their exocytosis. Front. Immunol. 2012, 3:335.
26. Kulkarni S., Martin M.P., Carrington M. The Yin and Yang of HLA and KIR in human disease. Semin. Immunol. 2008, 20:343-352.
27. Lam R.A., Chwee J.Y., Le Bert N., Sauer M., Pogge von Strandmann E., Gasser S. Regulation of self-ligands for activating natural killer cell receptors. Ann. Med. 2013, 45:384-394.
28. Lanier L.L. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 2008, 9:495-502.
29. Liu X.V., Ho S.S., Tan J.J., Kamran N., Gasser S. Ras activation induces expression of Raet1 family NK receptor ligands. J. Immunol. 2012, 189:1826-1834.
30. Ljunggren H.G., Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 1990, 11:237-244.
31. McDougall C.J., Ngoi S.S., Goldman I.S., Godwin T., Felix J., DeCosse J.J., Rigas B. Reduced expression of HLA class I and II antigens in colon cancer. Cancer Res. 1990, 50:8023-8027.
32. Meade J.L., Wilson E.B., Holmes T.D., de Wynter E.A., Brett P., Straszynski L., Ballard P.A., Trapani J.A., McDermott M.F., Cook G.P. Proteolytic activation of the cytotoxic phenotype during human NK cell development. J. Immunol. 2009, 183:803-813.
33. Montagut C., Settleman J. Targeting the RAF-MEK-ERK pathway in cancer therapy. Cancer Lett. 2009, 283:125-134.
34. Oliva M.R., Cabrera T., Esquivias J., Perez-Ayala M., Redondo M., Ruiz-Cabello F., Garrido F. K-ras mutations (codon 12) are not involved in down-regulation of MHC class-I genes in colon carcinomas. Int. J. Cancer 1990, 46:426-431.
35. Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 2005, 5:201-214.
36. Peaper D.R., Cresswell P. Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 2008, 24:343-368.
37. Perez-Martinez D., Tanaka T., Rabbitts T.H. Intracellular antibodies and cancer: new technologies offer therapeutic opportunities. Bioessays 2010, 32:589-598.
38. Pylayeva-Gupta Y., Grabocka E., Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer 2011, 11:761-774.
39. Raulet D.H., Gasser S., Gowen B.G., Deng W., Jung H. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 2013, 31:413-441.
40. Restifo N.P., Esquivel F., Kawakami Y., Yewdell J.W., Mule J.J., Rosenberg S.A., Bennink J.R. Identification of human cancers deficient in antigen processing. J. Exp. Med. 1993, 177:265-272.
41. Schoenborn J.R., Wilson C.B. Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 2007, 96:41-101.
42. Schrier P.I., Bernards R., Vaessen R.T., Houweling A., van der Eb A.J. Expression of class I major histocompatibility antigens switched off by highly oncogenic adenovirus 12 in transformed rat cells. Nature 1983, 305:771-775.
43. Schroder K., Hertzog P.J., Ravasi T., Hume D.A. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leuk. Biol. 2004, 75:163-189.
44. Scott G.B., Bowles P.A., Wilson E.B., Meade J.L., Low B.C., Davison A., Blair G.E., Cook G.P. Identification of the BCL2/adenovirus E1B-19K protein-interacting protein 2 (BNIP-2) as a granzyme B target during human natural killer cell-mediated killing. Biochem. J. 2010, 431:423-431.
45. Seliger B., Harders C., Wollscheid U., Staege M.S., Reske-Kunz A.B., Huber C. Suppression of MHC class I antigens in oncogenic transformants: association with decreased recognition by cytotoxic T lymphocytes. Exp. Hematol. 1996, 24:1275-1279.
46. Seliger B., Harders C., Lohmann S., Momburg F., Urlinger S., Tampe R., Huber C. Down-regulation of the MHC class I antigen-processing machinery after oncogenic transformation of murine fibroblasts. Eur. J. Immunol. 1998, 28:122-133.
47. Sers C., Kuner R., Falk C.S., Lund P., Sueltmann H., Braun M., Buness A., Ruschhaupt M., Conrad J., Mang-Fatehi S., Stelniec I., Krapfenbauer U., Poustka A., Schafer R. Down-regulation of HLA Class I and NKG2D ligands through a concerted action of MAPK and DNA methyltransferases in colorectal cancer cells. Int. J. Cancer 2009, 125:1626-1639.
48. Shirasawa S., Furuse M., Yokoyama N., Sasazuki T. Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 1993, 260:85-88.
49. Simpson J.A., Al-Attar A., Watson N.F., Scholefield J.H., Ilyas M., Durrant L.G. Intratumoral T cell infiltration, MHC class I and STAT1 as biomarkers of good prognosis in colorectal cancer. Gut 2010, 59:926-933.
50. Tanaka T., Rabbitts T.H. Intrabodies based on intracellular capture frameworks that bind the RAS protein with high affinity and impair oncogenic transformation. EMBO J. 2003, 22:1025-1035.
51. Tanaka T., Rabbitts T.H. Interfering with RAS-effector protein interactions prevent RAS-dependent tumour initiation and causes stop-start control of cancer growth. Oncogene 2010, 29:6064-6070.
52. Tanaka T., Williams R.L., Rabbitts T.H. Tumour prevention by a single antibody domain targeting the interaction of signal transduction proteins with RAS. EMBO J. 2007, 26:3250-3259.
53. Textor S., Fiegler N., Arnold A., Porgador A., Hofmann T.G., Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res. 2011, 71:5998-6009.
54. Tokuyama M., Lorin C., Delebecque F., Jung H., Raulet D.H., Coscoy L. Expression of the RAE-1 family of stimulatory NK-cell ligands requires activation of the PI3K pathway during viral infection and transformation. PLoS Pathog. 2011, 7:e1002265.
55. Versteeg R., Noordermeer I.A., Kruse-Wolters M., Ruiter D.J. Schrier PI. c-myc down-regulates class I HLA expression in human melanomas. EMBO J. 1988, 7:1023-1029.
56. Vesely M.D., Kershaw M.H., Schreiber R.D., Smyth M.J. Natural innate and adaptive immunity to cancer. Annu. Rev. Immunol. 2011, 29:235-271.
57. Vivier E., Raulet D.H., Moretta A., Caligiuri M.A., Zitvogel L., Lanier L.L., Yokoyama W.M., Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331:44-49.
58. Wang Y., Ngo V.N., Marani M., Yang Y., Wright G., Staudt L.M., Downward J. Critical role for transcriptional repressor Snail2 in transformation by oncogenic RAS in colorectal carcinoma cells. Oncogene 2010, 29:4658-4670.
59. Watson N.F., Ramage J.M., Madjd Z., Spendlove I., Ellis I.O., Scholefield J.H., Durrant L.G. Immunosurveillance is active in colorectal cancer as downregulation but not complete loss of MHC class I expression correlates with a poor prognosis. Int. J. Cancer 2006, 118:6-10.
60. Wei M.L., Cresswell P. HLA-A2 molecules in an antigen-processing mutant cell contain signal sequence-derived peptides. Nature 1992, 356:443-446.
61. Weinstein I.B., Joe A. Oncogene addiction. Cancer Res. 2008, 68:3077-3080. (discussion 80).
62. West E., Morgan R., Scott K., Merrick A., Lubenko A., Pawson D., Selby P., Hatfield P., Prestwich R., Fraser S., Eves D., Anthoney A., Twelves C., Beirne D., Patel P., O'Donnell D., Watt S., Waller M., Dietz A., Robinson P., Melcher A. Clinical grade OK432-activated dendritic cells: in vitro characterization and tracking during intralymphatic delivery. J. Immunother. 2009, 32:66-78.
63. Wilson E.B., El-Jawhari J.J., Neilson A.L., Hall G.D., Melcher A.A., Meade J.L., Cook G.P. Human tumour immune evasion via TGF-beta blocks NK cell activation but not survival allowing therapeutic restoration of anti-tumour activity. PLoS ONE 2011, 6:e22842.
64. Yamshchikov G.V., Mullins D.W., Chang C.C., Ogino T., Thompson L., Presley J., Galavotti H., Aquila W., Deacon D., Ross W., Patterson J.W., Engelhard V.H., Ferrone S., Slingluff C.L. Sequential immune escape and shifting of T cell responses in a long-term survivor of melanoma. J. Immunol. 2005, 174:6863-6871.