An immune-active tumor microenvironment favors clinical response to ipilimumab

Cancer Immunology, Immunotherapy

Volumn 61, Issue 7, 2012, Pages 1019-1031

  Ji, Rui Ru ^a   Chasalow, Scott D ^a   Wang, Lisu ^a   Hamid, Omid ^b   Schmidt, Henrik ^c   Cogswell, John ^a   Alaparthy, Suresh ^a   Berman, David ^a   Jure Kunkel, Maria ^a   Siemers, Nathan O ^a   Jackson, Jeffrey R ^a   Shahabi, Vafa ^a  

^a BRISTOL MYERS SQUIBB   (United States)

^b Angeles Clinic and Research Institute   (United States)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Cytotoxic T lymphocyte antigen 4; Gene expression profiling; Immunotherapy; Ipilimumab; Metastatic melanoma

Indexed keywords

BIOLOGICAL MARKER; IPILIMUMAB; MELANOMA ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ADVANCED CANCER; ANTIGEN FUNCTION; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER STAGING; CELL METABOLISM; CELL PROLIFERATION; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; FOLLOW UP; GENE EXPRESSION PROFILING; GENE FUNCTION; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; LYMPHOCYTIC INFILTRATION; MAINTENANCE DRUG DOSE; MAJOR CLINICAL STUDY; METASTATIC MELANOMA; MULTICENTER STUDY; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE CHARACTERIZATION; TREATMENT RESPONSE; TUMOR BIOPSY; TUMOR LOCALIZATION; TUMOR MICROENVIRONMENT;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BIOPSY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; NEOPLASM METASTASIS; NEOPLASM STAGING; SKIN NEOPLASMS; SURVIVAL ANALYSIS; TUMOR MICROENVIRONMENT;

EID: 84862769116     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1172-6     Document Type: Article

References (51)

1. American Cancer Society (2009) Cancer facts and figures 2009. http://www.cancer.org/acs/groups/content/@nho/documents/document/500809webpdf. pdf
2. Howlader N, Noone AM, Krapcho M, Neyman N, Aminou R, Waldron W, Altekruse SF, Kosary CL, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Eisner MP, Lewis DR, Chen HS, Feuer EJ, Cronin KA, Edwards BK (eds). SEER Cancer Statistics Review, 1975-2008, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/ 1975-2008/, based on November 2010 SEER data submission, posted to the SEER web site, 2011
3. MB Atkins MT Lotze JP Dutcher RI Fisher G Weiss K Margolin J Abrams M Sznol D Parkinson M Hawkins C Paradise, et al. 1999 High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985, 1993 J Clin Oncol 17 7 2105 2116 10561265 1:CAS:528:DyaK1MXkvVSmur4%3D
4. PB Chapman A Hauschild C Robert JB Haanen P Ascierto J Larkin R Dummer C Garbe A Testori M Maio D Hogg, et al. 2011 Improved survival with vemurafenib in melanoma with braf v600e mutation N Engl J Med 364 26 2507 2516 21639808 10.1056/NEJMoa1103782 1:CAS:528:DC%2BC3MXosVeitbs%3D
5. FS Hodi SJ O'Day DF McDermott RW Weber JA Sosman JB Haanen R Gonzalez C Robert D Schadendorf JC Hassel W Akerley, et al. 2010 Improved survival with ipilimumab in patients with metastatic melanoma N Engl J Med 363 8 711 723 20525992 10.1056/NEJMoa1003466 1:CAS:528:DC%2BC3cXhtVCrtrbN
6. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ, Davidson N, Richards J, Maio M, Hauschild A, Miller WH, Gascon P, Lotem M, Harmankaya K, Ibrahim R, Francis S, Chen TT, Humphrey R, Hoos A, Wolchok J (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26):2517-2526
7. HJ Steer RA Lake AK Nowak BW Robinson 2010 Harnessing the immune response to treat cancer Oncogene 29 48 6301 6313 20856204 10.1038/onc.2010.437 1:CAS:528:DC%2BC3cXhtFOht7vL
8. CA Chambers MS Kuhns JG Egen JP Allison 2001 Ctla-4-mediated inhibition in regulation of t cell responses: mechanisms and manipulation in tumor immunotherapy Annu Rev Immunol 19 565 594 11244047 10.1146/annurev.immunol.19.1. 565 1:CAS:528:DC%2BD3MXivFKgurc%3D
9. O Murillo A Arina S Hervas-Stubbs A Gupta B McCluskey J Dubrot A Palazon A Azpilikueta MC Ochoa C Alfaro S Solano, et al. 2008 Therapeutic antitumor efficacy of anti-cd137 agonistic monoclonal antibody in mouse models of myeloma Clin Cancer Res 14 21 6895 6906 18980984 10.1158/1078-0432.CCR-08-0285 1:CAS:528:DC%2BD1cXhtlens7nJ
10. Chen H, Liakou CI, Kamat A, Pettaway C, Ward JF, Tang DN, Sun J, Jungbluth AA, Troncoso P, Logothetis C, Sharma P (2009) Anti-ctla-4 therapy results in higher cd4+ ICOShi t cell frequency and IFN-gamma levels in both nonmalignant and malignant prostate tissues. Proceedings of the National Academy of Sciences of the United States of America 106(8):2729-2734
11. CA Chambers MF Krummel B Boitel A Hurwitz TJ Sullivan S Fournier D Cassell M Brunner JP Allison 1996 The role of ctla-4 in the regulation and initiation of t-cell responses Immunol Rev 153 27 46 9010718 10.1111/j.1600-065X.1996.tb00919.x 1:CAS:528:DyaK2sXktVyrsw%3D%3D
12. Tarhini AA, Iqbal F (2010) CTLA-4 blockade: Therapeutic potential in cancer treatments. OncoTarg Ther 3:15-25
13. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W et al (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711-723
14. H Harlin TV Kuna AC Peterson Y Meng TF Gajewski 2006 Tumor progression despite massive influx of activated cd8(+) t cells in a patient with malignant melanoma ascites Cancer Immunol Immunother 55 10 1185 1197 16468035 10.1007/s00262-005-0118-2 1:CAS:528:DC%2BD28Xmtl2qurc%3D
15. M Kunz A Toksoy M Goebeler E Engelhardt E Brocker R Gillitzer 1999 Strong expression of the lymphoattractant c-x-c chemokine mig is associated with heavy infiltration of t cells in human malignant melanoma J Pathol 189 4 552 558 10629557 10.1002/(SICI)1096-9896(199912)189:4<552::AID-PATH469>3.0.CO;2-I 1:CAS:528:DC%2BD3cXltlSrtA%3D%3D
16. Hamid O, Schmidt H, Nissan A, Ridolfi L, Aamdal S, Hansson J, Guida M, Hyams DM, Gomez H, Bastholt L, Chasalow SD, Berman D (2011) A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Trans Med 9:204
17. Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457-481
18. Hodi FS, Butler M, Oble DA, Seiden MV, Haluska FG, Kruse A, Macrae S, Nelson M, Canning C, Lowy I, Korman A et al (2008) Immunologic and clinical effects of antibody blockade of cytotoxic t lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proceedings of the National Academy of Sciences of the United States of America 105(8):3005-3010
19. KE Cole CA Strick TJ Paradis KT Ogborne M Loetscher RP Gladue W Lin JG Boyd B Moser DE Wood BG Sahagan, et al. 1998 Interferon-inducible t cell alpha chemoattractant (i-tac): A novel non-elr cxc chemokine with potent activity on activated t cells through selective high affinity binding to cxcr3 J Exp Med 187 12 2009 2021 9625760 10.1084/jem.187.12.2009 1:CAS:528:DyaK1cXktVeitr8%3D
20. F Liao G Alkhatib KW Peden G Sharma EA Berger JM Farber 1997 Strl33, a novel chemokine receptor-like protein, functions as a fusion cofactor for both macrophage-tropic and t cell line-tropic HIV-1 J Exp Med 185 11 2015 2023 9166430 10.1084/jem.185.11.2015 1:CAS:528:DyaK2sXjsF2gtrg%3D
21. X Du A Poltorak Y Wei B Beutler 2000 Three novel mammalian toll-like receptors: gene structure, expression, and evolution Eur Cytokine Netw 11 3 362 371 11022119 1:CAS:528:DC%2BD3cXotFKqsLc%3D
22. MM Gorska SJ Stafford O Cen S Sur R Alam 2004 Unc119, a novel activator of lck/fyn, is essential for t cell activation J Exp Med 199 3 369 379 14757743 10.1084/jem. 20030589 1:CAS:528:DC%2BD2cXhtVCitLk%3D
23. E Mavoungou MC Georges-Courbot V Poaty-Mavoungou HT Nguyen P Yaba A Delicat AJ Georges F Russo-Marie 1997 HIV and SIV envelope glycoproteins induce phospholipase A2 activation in human and macaque lymphocytes J Acquir Immune Defic Syndr Hum Retrovirol 16 1 1 9 9377118 10.1097/00042560-199709010-00001 1:CAS:528:DyaK2sXnsVentr0%3D
24. Y Laabi MP Gras F Carbonnel JC Brouet R Berger CJ Larsen A Tsapis 1992 A new gene, bcm, on chromosome 16 is fused to the interleukin 2 gene by a t(4;16)(q26;p13) translocation in a malignant t cell lymphoma EMBO J 11 11 3897 3904 1396583 1:CAS:528:DyaK3sXks1Cgur4%3D
25. IM Tomlinson GP Cook G Walter NP Carter H Riethman L Buluwela TH Rabbitts G Winter 1995 A complete map of the human immunoglobulin vh locus Ann NY Acad Sci 764 43 46 7486559 10.1111/j.1749-6632.1995.tb55804.x 1:CAS:528: DyaK28XkvFelsA%3D%3D
26. ED Crouser DA Culver KS Knox MW Julian G Shao S Abraham S Liyanarachchi JE Macre MD Wewers MA Gavrilin P Ross, et al. 2009 Gene expression profiling identifies mmp-12 and adamdec1 as potential pathogenic mediators of pulmonary sarcoidosis Am J Respir Crit Care Med 179 10 929 938 19218196 10.1164/rccm.200803-490OC 1:CAS:528:DC%2BD1MXmt1KisrY%3D
27. Bakos RM, Maier T, Besch R, Mestel DS, Ruzicka T, Sturm RA, Berking C Nestin and sox9 and sox10 transcription factors are coexpressed in melanoma. Exp Dermatol 19(8):e89-e94
28. K Yasumoto K Yokoyama K Shibata Y Tomita S Shibahara 1994 Microphthalmia-associated transcription factor as a regulator for melanocyte-specific transcription of the human tyrosinase gene Mol Cell Biol 14 12 8058 8070 7969144 1:CAS:528:DyaK2MXisVWgt7g%3D
29. VJ Hearing 1973 Mammalian melanogenesis: tyrosinase versus peroxidase involvement, and activation mechanisms Arch Biochem Biophys 158 2 720 725 4131388 10.1016/0003-9861(73)90566-3 1:CAS:528:DyaE2cXhslak
30. MS Cheah CD Wallace RM Hoffman 1984 Hypomethylation of DNA in human cancer cells: a site-specific change in the c-myc oncogene J Natl Cancer Inst 73 5 1057 1065 6092764 1:CAS:528:DyaL2MXktVylsA%3D%3D
31. UN Rao A Bakker PA Swalsky SD Finkelstein 1999 Max interacting protein 1: loss of heterozygosity is frequent in desmoplastic melanoma Mod Pathol 12 4 344 350 10229497 1:STN:280:DyaK1M3ksVGjsQ%3D%3D
32. RW Furlanetto SE Harwell RB Baggs 1993 Effects of insulin-like growth factor receptor inhibition on human melanomas in culture and in athymic mice Cancer Res 53 11 2522 2526 8495414 1:CAS:528:DyaK3sXkvFamu7Y%3D
33. M Rieber MS Rieber 1994 Cyclin-dependent kinase 2 and cyclin a interaction with e2f are targets for tyrosine induction of b16 melanoma terminal differentiation Cell Growth Differ 5 12 1339 1346 7696182 1:CAS:528: DyaK2MXisFCit74%3D
34. GF Draetta 1994 Mammalian g1 cyclins Curr Opin Cell Biol 6 6 842 846 7880531 10.1016/0955-0674(94)90054-X 1:CAS:528:DyaK2MXisVSqsrc%3D
35. Schmollinger JC, Vonderheide RH, Hoar KM, Maecker B, Schultze JL, Hodi FS, Soiffer RJ, Jung K, Kuroda MJ, Letvin NL, Greenfield EA et al (2003) Melanoma inhibitor of apoptosis protein (ml-iap) is a target for immune-mediated tumor destruction. Proceedings of the National Academy of Sciences of the United States of America 100(6):3398-3403
36. TS Griffith WA Chin GC Jackson DH Lynch MZ Kubin 1998 Intracellular regulation of trail-induced apoptosis in human melanoma cells J Immunol 161 6 2833 2840 9743343 1:CAS:528:DyaK1cXmtVKgs74%3D
37. Chen YT, Gure AO, Tsang S, Stockert E, Jager E, Knuth A, Old LJ (1998) Identification of multiple cancer/testis antigens by allogeneic antibody screening of a melanoma cell line library. Proceedings of the National Academy of Sciences of the United States of America 95(12):6919-6923
38. G Parmiani 2001 Melanoma antigens and their recognition by t cells Keio J Med 50 2 86 90 11450597 10.2302/kjm.50.86 1:CAS:528:DC%2BD3MXmsV2ks78%3D
39. JR Schoenborn CB Wilson 2007 Regulation of interferon-gamma during innate and adaptive immune responses Adv Immunol 96 41 101 17981204 10.1016/S0065-2776(07)96002-2 1:CAS:528:DC%2BD1cXhs1ajtbw%3D
40. W Zeng A Miyazato G Chen S Kajigaya NS Young JP Maciejewski 2006 Interferon-gamma-induced gene expression in cd34 cells: Identification of pathologic cytokine-specific signature profiles Blood 107 1 167 175 16131564 10.1182/blood-2005-05-1884 1:CAS:528:DC%2BD28XhsVGntQ%3D%3D
41. A Bosco KL McKenna CJ Devitt MJ Firth PD Sly PG Holt 2006 Identification of novel th2-associated genes in t memory responses to allergens J Immunol 176 8 4766 4777 16585570 1:CAS:528:DC%2BD28XjtV2gsLY%3D
42. S Narayanan R Silva G Peruzzi Y Alvarez VR Simhadri K Debell JE Coligan F Borrego 2010 Human th1 cells that express cd300a are polyfunctional and after stimulation up-regulate the t-box transcription factor eomesodermin PLoS One 5 5 e10636 20498708 10.1371/journal.pone.0010636
43. M Tosolini A Kirilovsky B Mlecnik T Fredriksen S Mauger G Bindea A Berger P Bruneval WH Fridman F Pages J Galon 2011 Clinical impact of different classes of infiltrating t cytotoxic and helper cells (th1, th2, treg, th17) in patients with colorectal cancer Cancer Res 71 4 1263 1271 21303976 10.1158/0008-5472. CAN-10-2907 1:CAS:528:DC%2BC3MXhvFSjsLw%3D
44. H Harlin Y Meng AC Peterson Y Zha M Tretiakova C Slingluff M McKee TF Gajewski 2009 Chemokine expression in melanoma metastases associated with cd8+ t-cell recruitment Cancer Res 69 7 3077 3085 19293190 10.1158/0008-5472.CAN-08- 2281 1:CAS:528:DC%2BD1MXjvVWitr8%3D
45. P Kalinski RB Mailliard A Giermasz HJ Zeh P Basse DL Bartlett JM Kirkwood MT Lotze RB Herberman 2005 Natural killer-dendritic cell cross-talk in cancer immunotherapy Expert Opin Biol Ther 5 10 1303 1315 16197336 10.1517/14712598.5. 10.1303 1:CAS:528:DC%2BD2MXhtVGjsLrN
46. Yuan J, Gnjatic S, Li H, Powel S, Gallardo HF, Ritter E, Ku GY, Jungbluth AA, Segal NH, Rasalan TS, Manukian G et al (2008) Ctla-4 blockade enhances polyfunctional ny-eso-1 specific t cell responses in metastatic melanoma patients with clinical benefit. Proceedings of the National Academy of Sciences of the United States of America 105(51):20410-20415
47. A Ebrahimnejad T Streichert P Nollau AK Horst C Wagener AM Bamberger J Brummer 2004 Ceacam1 enhances invasion and migration of melanocytic and melanoma cells Am J Pathol 165 5 1781 1787 15509546 10.1016/S0002-9440(10)63433-5 1:CAS:528:DC%2BD2cXhtVCgsbrO
48. V Winnepenninckx V Lazar S Michiels P Dessen M Stas SR Alonso MF Avril PL Ortiz Romero T Robert O Balacescu AM Eggermont, et al. 2006 Gene expression profiling of primary cutaneous melanoma and clinical outcome J Natl Cancer Inst 98 7 472 482 16595783 10.1093/jnci/djj103 1:CAS:528:DC%2BD28Xjtlamt7c%3D
49. Bogunovic D, O'Neill DW, Belitskaya-Levy I, Vacic V, Yu YL, Adams S, Darvishian F, Berman R, Shapiro R, Pavlick AC, Lonardi S et al (2009) Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proceedings of the National Academy of Sciences of the United States of America 106(48):20429-20434
50. Ascierto ML, Kmieciak M, Idowu MO, Manjili R, Zhao Y, Grimes M, Dumur C, Wang E, Ramakrishnan V, Wang XY, Bear HD et al (2011) A signature of immune function genes associated with recurrence-free survival in breast cancer patients. Breast Cancer Res Treat
51. J Galon A Costes F Sanchez-Cabo A Kirilovsky B Mlecnik C Lagorce-Pages M Tosolini M Camus A Berger P Wind F Zinzindohoue, et al. 2006 Type, density, and location of immune cells within human colorectal tumors predict clinical outcome Science 313 5795 1960 1964 17008531 10.1126/science.1129139 1:CAS:528:DC%2BD28XhtVSnsrnK