The Continuum of Cancer Immunosurveillance: Prognostic, Predictive, and Mechanistic Signatures

Immunity

Volumn 39, Issue 1, 2013, Pages 11-26

  Galon, Jérôme ^a,b   Angell, HelenK ^a,b   Bedognetti, Davide ^c   Marincola, FrancescoM ^c,d  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE;

ADAPTIVE IMMUNITY; BREAST CANCER; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER THERAPY; COLORECTAL CANCER; CYTOTOXICITY; ENVIRONMENTAL STRESS; GENE DELETION; HUMAN; IMMUNE CONTEXTURE; IMMUNOGENICITY; IMMUNOLOGIC CONSTANT OF REJECTION; IMMUNOLOGICAL PARAMETERS; IMMUNOSCORE; IMMUNOSURVEILLANCE; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; MEMORY T LYMPHOCYTE; MOLECULAR BIOLOGY; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; REVIEW; TH1 CELL;

CYTOKINES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNE SYSTEM; MODELS, IMMUNOLOGICAL; MONITORING, IMMUNOLOGIC; NEOPLASMS; PROGNOSIS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84880704621     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.07.008     Document Type: Review

References (145)

1. Abbas A.R., Wolslegel K., Seshasayee D., Modrusan Z., Clark H.F. Deconvolution of blood microarray data identifies cellular activation patterns in systemic lupus erythematosus. PLoS ONE 2009, 4:e6098.
2. Ajuebor M.N., Carey J.A., Swain M.G. CCR5 in Tcell-mediated liver diseases: what's going on?. J.Immunol. 2006, 177:2039-2045.
3. Angell H.K., Galon J. From the immune contexture to the Immunoscore: the role of prognostic and predictive immune markers in cancer. Curr. Opin. Immunol. 2013, 25:261-267.
4. Ascierto P.A., Marincola F.M. Combination therapy: the next opportunity and challenge of medicine. J.Transl. Med. 2011, 9:115.
5. Ascierto M.L., De Giorgi V., Liu Q., Bedognetti D., Spivey T.L., Murtas D., Uccellini L., Ayotte B.D., Stroncek D.F., Chouchane L., et al. Animmunologic portrait of cancer. J.Transl. Med. 2011, 9:146.
6. Ascierto M.L., Kmieciak M., Idowu M.O., Manjili R., Zhao Y., Grimes M., Dumur C., Wang E., Ramakrishnan V., Wang X.Y., et al. A signature of immune function genes associated with recurrence-free survival in breast cancer patients. Breast Cancer Res. Treat. 2012, 131:871-880.
7. Ascierto M.L., Idowu M.O., Zhao Y., Khalak H., Payne K.K., Wang X.Y., Dumur C.I., Bedognetti D., Tomei S., Ascierto P.A., et al. Molecular signatures mostly associated with NK cells are predictive of relapse free survival in breast cancer patients. J.Transl. Med. 2013, 11:145.
8. Balkwill F.R. The chemokine system and cancer. J.Pathol. 2012, 226:148-157.
9. Bedognetti D., Wang E., Sertoli M.R., Marincola F.M. Gene-expression profiling in vaccine therapy and immunotherapy for cancer. Expert Rev. Vaccines 2010, 9:555-565.
10. Bindea G., Mlecnik B., Fridman W.H., Pagès F., Galon J. Natural immunity to cancer in humans. Curr. Opin. Immunol. 2010, 22:215-222.
11. Brahmer J.R., Tykodi S.S., Chow L.Q., Hwu W.J., Topalian S.L., Hwu P., Drake C.G., Camacho L.H., Kauh J., Odunsi K., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N.Engl. J. Med. 2012, 366:2455-2465.
12. Broussard E.K., Disis M.L. TNM staging in colorectal cancer: T is for Tcell and M is for memory. J.Clin. Oncol. 2011, 29:601-603.
13. Burnet F.M. The concept of immunological surveillance. Prog. Exp. Tumor Res. 1970, 13:1-27.
14. Callahan M.J., Nagymanyoki Z., Bonome T., Johnson M.E., Litkouhi B., Sullivan E.H., Hirsch M.S., Matulonis U.A., Liu J., Birrer M.J., et al. Increased HLA-DMB expression in the tumor epithelium is associated with increased CTL infiltration and improved prognosis in advanced-stage serous ovarian cancer. Clin. Cancer Res. 2008, 14:7667-7673.
15. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068. Cancer Genome Atlas Research Network.
16. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615. Cancer Genome Atlas Research Network.
17. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012, 489:519-525. Cancer Genome Atlas Research Network.
18. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012, 487:330-337. Cancer Genome Atlas Network.
19. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. Cancer Genome Atlas Network.
20. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N.Engl. J. Med. 2013, 368:2059-2074. Cancer Genome Atlas Research Network.
21. Carretero R., Wang E., Rodriguez A.I., Reinboth J., Ascierto M.L., Engle A.M., Liu H., Camacho F.M., Marincola F.M., Garrido F., Cabrera T. Regression of melanoma metastases after immunotherapy is associated with activation of antigen presentation and interferon-mediated rejection genes. Int. J. Cancer 2012, 131:387-395.
22. Carswell E.A., Old L.J., Kassel R.L., Green S., Fiore N., Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc. Natl. Acad. Sci. USA 1975, 72:3666-3670.
23. Castiello L., Sabatino M., Jin P., Clayberger C., Marincola F.M., Krensky A.M., Stroncek D.F. Monocyte-derived DC maturation strategies and related pathways: a transcriptional view. Cancer Immunol. Immunother. 2011, 60:457-466.
24. Chen D.S., Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013, 39:1-10. this issue.
25. Chew V., Chen J., Lee D., Loh E., Lee J., Lim K.H., Weber A., Slankamenac K., Poon R.T., Yang H., et al. Chemokine-driven lymphocyte infiltration: an early intratumoural event determining long-term survival in resectable hepatocellular carcinoma. Gut 2012, 61:427-438.
26. Coley W.B. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. Am. J. Med. Sci. 1893, 105:487-511.
27. Corless C.L., Barnett C.M., Heinrich M.C. Gastrointestinal stromal tumours: origin and molecular oncology. Nat. Rev. Cancer 2011, 11:865-878.
28. Costa C., Rufino R., Traves S.L., Lapa E Silva J.R., Barnes P.J., Donnelly L.E. CXCR3 and CCR5 chemokines in induced sputum from patients with COPD. Chest 2008, 133:26-33.
29. Curtis C., Shah S.P., Chin S.F., Turashvili G., Rueda O.M., Dunning M.J., Speed D., Lynch A.G., Samarajiwa S., Yuan Y., et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352. METABRIC Group.
30. Denkert C., Loibl S., Noske A., Roller M., Müller B.M., Komor M., Budczies J., Darb-Esfahani S., Kronenwett R., Hanusch C., et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J.Clin. Oncol. 2010, 28:105-113.
31. Desmedt C., Haibe-Kains B., Wirapati P., Buyse M., Larsimont D., Bontempi G., Delorenzi M., Piccart M., Sotiriou C. Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin. Cancer Res. 2008, 14:5158-5165.
32. Dunn G.P., Old L.J., Schreiber R.D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004, 21:137-148.
33. Feld J.J., Nanda S., Huang Y., Chen W., Cam M., Pusek S.N., Schweigler L.M., Theodore D., Zacks S.L., Liang T.J., Fried M.W. Hepatic gene expression during treatment with peginterferon and ribavirin: Identifying molecular pathways for treatment response. Hepatology 2007, 46:1548-1563.
34. Finak G., Bertos N., Pepin F., Sadekova S., Souleimanova M., Zhao H., Chen H., Omeroglu G., Meterissian S., Omeroglu A., et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 2008, 14:518-527.
35. Florholmen J., Kristiansen M.G., Steigen S.E., Sørbye S.W., Paulssen E.J., Kvamme J.M., Konopski Z., Gutteberg T., Goll R. A rapid chemokine response of macrophage inflammatory protein (MIP)-1α, MIP-1β and the regulated on activation, normal T expressed and secreted chemokine is associated with a sustained virological response in the treatment of chronic hepatitis C. Clin. Microbiol. Infect. 2011, 17:204-209.
36. Formenti S.C., Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J.Natl. Cancer Inst. 2013, 105:256-265.
37. Franciszkiewicz K., Boissonnas A., Boutet M., Combadière C., Mami-Chouaib F. Role of chemokines and chemokine receptors in shaping the effector phase of the antitumor immune response. Cancer Res. 2012, 72:6325-6332.
38. Frederick D.T., Piris A., Cogdill A.P., Cooper Z.A., Lezcano C., Ferrone C.R., Mitra D., Boni A., Newton L.P., Liu C., et al. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res. 2013, 19:1225-1231.
39. Fridman W.H., Pagès F., Sautès-Fridman C., Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 2012, 12:298-306.
40. Gajewski T.F., Louahed J., Brichard V.G. Gene signature in melanoma associated with clinical activity: a potential clue to unlock cancer immunotherapy. Cancer J. 2010, 16:399-403.
41. Galluzzi L., Senovilla L., Vacchelli E., Eggermont A., Fridman W.H., Galon J., Sautès-Fridman C., Tartour E., Zitvogel L., Kroemer G. Trial watch: Dendritic cell-based interventions for cancer therapy. OncoImmunology 2012, 1:1111-1134.
42. Galluzzi L., Vacchelli E., Eggermont A., Fridman W.H., Galon J., Sautès-Fridman C., Tartour E., Zitvogel L., Kroemer G. Trial Watch: Adoptive cell transfer immunotherapy. OncoImmunology 2012, 1:306-315.
43. Galluzzi L., Vacchelli E., Fridman W.H., Galon J., Sautès-Fridman C., Tartour E., Zucman-Rossi J., Zitvogel L., Kroemer G. Trial Watch: Monoclonal antibodies in cancer therapy. OncoImmunology 2012, 1:28-37.
44. Galon J., Costes A., Sanchez-Cabo F., Kirilovsky A., Mlecnik B., Lagorce-Pagès C., Tosolini M., Camus M., Berger A., Wind P., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006, 313:1960-1964.
45. Galon J., Fridman W.H., Pagès F. The adaptive immunologic microenvironment in colorectal cancer: a novel perspective. Cancer Res. 2007, 67:1883-1886.
46. Galon J., Pagès F., Marincola F.M., Angell H.K., Thurin M., Lugli A., Zlobec I., Berger A., Bifulco C., Botti G., et al. Cancer classification using the Immunoscore: a worldwide task force. J.Transl. Med. 2012, 10:205.
47. Godessart N., Kunkel S.L. Chemokines in autoimmune disease. Curr. Opin. Immunol. 2001, 13:670-675.
48. Gorer P.A. The role of antibodies in immunity to transplanted leukemia in mice. J.Pathol. Bacteriol. 1942, 54:51-65.
49. Grivennikov S.I., Wang K., Mucida D., Stewart C.A., Schnabl B., Jauch D., Taniguchi K., Yu G.Y., Osterreicher C.H., Hung K.E., et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012, 491:254-258.
50. Guidoboni M., Gafà R., Viel A., Doglioni C., Russo A., Santini A., Del Tin L., Macrì E., Lanza G., Boiocchi M., Dolcetti R. Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favorable prognosis. Am. J. Pathol. 2001, 159:297-304.
51. Halama N., Michel S., Kloor M., Zoernig I., Benner A., Spille A., Pommerencke T., von Knebel D.M., Folprecht G., Luber B., et al. Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res. 2011, 71:5670-5677.
52. Hamid O., Schmidt H., Nissan A., Ridolfi L., Aamdal S., Hansson J., Guida M., Hyams D.M., Gómez H., Bastholt L., et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J.Transl. Med. 2011, 9:204.
53. Harlin H., Meng Y., Peterson A.C., Zha Y., Tretiakova M., Slingluff C., McKee M., Gajewski T.F. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009, 69:3077-3085.
54. Hodi F.S., O'Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., Gonzalez R., Robert C., Schadendorf D., Hassel J.C., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N.Engl. J. Med. 2010, 363:711-723.
55. Ignatiadis M., Singhal S.K., Desmedt C., Haibe-Kains B., Criscitiello C., Andre F., Loi S., Piccart M., Michiels S., Sotiriou C. Gene modules and response to neoadjuvant chemotherapy in breast cancer subtypes: apooled analysis. J.Clin. Oncol. 2012, 30:1996-2004.
56. Imanguli M.M., Swaim W.D., League S.C., Gress R.E., Pavletic S.Z., Hakim F.T. Increased T-bet+ cytotoxic effectors and type I interferon-mediated processes in chronic graft-versus-host disease of the oral mucosa. Blood 2009, 113:3620-3630.
57. Ji R.R., Chasalow S.D., Wang L., Hamid O., Schmidt H., Cogswell J., Alaparthy S., Berman D., Jure-Kunkel M., Siemers N.O., et al. Animmune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol. Immunother. 2012, 61:1019-1031.
58. Jiang Z., Xu Y., Cai S. CXCL10 expression and prognostic significance in stage II and III colorectal cancer. Mol. Biol. Rep. 2010, 37:3029-3036.
59. Jochems C., Schlom J. Tumor-infiltrating immune cells and prognosis: the potential link between conventional cancer therapy and immunity. Exp. Biol. Med. (Maywood) 2011, 236:567-579.
60. Kalos M., June C.H. Adoptive Tcell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 2013, 39:49-60. this issue.
61. Kandoth C., Schultz N., Cherniack A.D., Akbani R., Liu Y., Shen H., Robertson A.G., Pashtan I., Shen R., Benz C.C., et al. Integrated genomic characterization of endometrial carcinoma. Nature 2013, 497:67-73. Cancer Genome Atlas Research Network.
62. Kantoff P.W., Higano C.S., Shore N.D., Berger E.R., Small E.J., Penson D.F., Redfern C.H., Ferrari A.C., Dreicer R., Sims R.B., et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N.Engl. J. Med. 2010, 363:411-422. IMPACT Study Investigators.
63. Kim M.J., Romero R., Kim C.J., Tarca A.L., Chhauy S., LaJeunesse C., Lee D.C., Draghici S., Gotsch F., Kusanovic J.P., et al. Villitis of unknown etiology is associated with a distinct pattern of chemokine up-regulation in thefeto-maternal and placental compartments: implications for conjoint maternal allograft rejection and maternal anti-fetal graft-versus-host disease. J.Immunol. 2009, 182:3919-3927.
64. Kim H.S., Minna J.D., White M.A. GWAS meets TCGA to illuminate mechanisms of cancer predisposition. Cell 2013, 152:387-389.
65. Koebel C.M., Vermi W., Swann J.B., Zerafa N., Rodig S.J., Old L.J., Smyth M.J., Schreiber R.D. Adaptive immunity maintains occult cancer inan equilibrium state. Nature 2007, 450:903-907.
66. Lake R.A., van der Most R.G. A better way for a cancer cell to die. N.Engl. J. Med. 2006, 354:2503-2504.
67. Leffers N., Fehrmann R.S., Gooden M.J., Schulze U.R., Ten Hoor K.A., Hollema H., Boezen H.M., Daemen T., de Jong S., Nijman H.W., van der Zee A.G. Identification of genes and pathways associated with cytotoxic T lymphocyte infiltration of serous ovarian cancer. Br. J. Cancer 2010, 103:685-692.
68. Lesinski G.B., Trefry J., Brasdovich M., Kondadasula S.V., Sackey K., Zimmerer J.M., Chaudhury A.R., Yu L., Zhang X., Crespin T.R., et al. Melanoma cells exhibit variable signal transducer and activator of transcription 1 phosphorylation and a reduced response to IFN-alpha compared with immune effector cells. Clin. Cancer Res. 2007, 13:5010-5019.
69. Li Q., Seo J.H., Stranger B., McKenna A., Pe'er I., Laframboise T., Brown M., Tyekucheva S., Freedman M.L. Integrative eQTL-based analyses reveal the biology of breast cancer risk loci. Cell 2013, 152:633-641.
70. Loi S., Sirtaine N., Piette F., Salgado R., Viale G., Van Eenoo F., Rouas G., Francis P., Crown J.P., Hitre E., et al. Prognostic and predictive valueof tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. J.Clin. Oncol. 2013, 31:860-867.
71. Ma Y., Adjemian S., Mattarollo S.R., Yamazaki T., Aymeric L., Yang H., Portela Catani J.P., Hannani D., Duret H., Steegh K., et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013, 38:729-741.
72. Mann G.J., Pupo G.M., Campain A.E., Carter C.D., Schramm S.J., Pianova S., Gerega S.K., De Silva C., Lai K., Wilmott J.S., et al. BRAF mutation, NRAS mutation, and the absence of an immune-related expressed gene profile predict poor outcome in patients with stage III melanoma. J.Invest. Dermatol. 2013, 133:509-517.
73. Mantovani A., Romero P., Palucka A.K., Marincola F.M. Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 2008, 371:771-783.
74. Marincola F.M. The trouble with translational medicine. J.Intern. Med. 2011, 270:123-127.
75. Medawar P.B. The behaviour and fate of skin autografts and skin homografts in rabbits: A report to the War Wounds Committee of the Medical Research Council. J.Anat. 1944, 78:176-199.
76. Melero I., Grimaldi A.M., Perez-Gracia J.L., Ascierto P.A. Clinical development of immunostimulatory monoclonal antibodies and opportunities for combination. Clin. Cancer Res. 2013, 19:997-1008.
77. Messina J.L., Fenstermacher D.A., Eschrich S., Qu X., Berglund A.E., Lloyd M.C., Schell M.J., Sondak V.K., Weber J.S., Mule J.J. 12-Chemokine gene signature identifies lymph node-like structures in melanoma: potential for patient selection for immunotherapy?. Sci. Rep. 2012, 2:765.
78. Mlecnik B., Tosolini M., Charoentong P., Kirilovsky A., Bindea G., Berger A., Camus M., Gillard M., Bruneval P., Fridman W.H., et al. Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 2010, 138:1429-1440.
79. Mlecnik B., Bindea G., Pagès F., Galon J. Tumor immunosurveillance in human cancers. Cancer Metastasis Rev. 2011, 30:5-12.
80. Mlecnik B., Tosolini M., Kirilovsky A., Berger A., Bindea G., Meatchi T., Bruneval P., Trajanoski Z., Fridman W.H., Pagès F., Galon J. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J.Clin. Oncol. 2011, 29:610-618.
81. Monsurrò V., Beghelli S., Wang R., Barbi S., Coin S., Di Pasquale G., Bersani S., Castellucci M., Sorio C., Eleuteri S., et al. Anti-viral state segregates two molecular phenotypes of pancreatic adenocarcinoma: potential relevance for adenoviral gene therapy. J.Transl. Med. 2010, 8:10.
82. Moran C.J., Arenberg D.A., Huang C.C., Giordano T.J., Thomas D.G., Misek D.E., Chen G., Iannettoni M.D., Orringer M.B., Hanash S., Beer D.G. RANTES expression is a predictor of survival in stage I lung adenocarcinoma. Clin. Cancer Res. 2002, 8:3803-3812.
83. Morris M., Platell C., Iacopetta B. Tumor-infiltrating lymphocytes and perforation in colon cancer predict positive response to 5-fluorouracil chemotherapy. Clin. Cancer Res. 2008, 14:1413-1417.
84. Motz G.T., Coukos G. The impossible task of tumor-reactive Tcells and how to enable them: deciphering tumor immune suppression. Immunity 2013, 39:61-73. this issue.
85. Mueller T.F., Einecke G., Reeve J., Sis B., Mengel M., Jhangri G.S., Bunnag S., Cruz J., Wishart D., Meng C., et al. Microarray analysis of rejection in human kidney transplants using pathogenesis-based transcript sets. Am. J. Transplant. 2007, 7:2712-2722.
86. Murtas D., Maric D., De Giorgi V., Reinboth J., Worschech A., Fetsch P., Filie A., Ascierto M.L., Bedognetti D., Liu Q., et al. IRF-1 responsiveness to IFN-γ predicts different cancer immune phenotypes. Br. J. Cancer 2013, 109:76-82. Published online June 27, 2013. 10.1038/bjc.2013.33.
87. Muthuswamy R., Berk E., Junecko B.F., Zeh H.J., Zureikat A.H., Normolle D., Luong T.M., Reinhart T.A., Bartlett D.L., Kalinski P. NF-κB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells. Cancer Res. 2012, 72:3735-3743.
88. Nagtegaal I.D., Quirke P., Schmoll H.J. Has the new TNM classification for colorectal cancer improved care?. Nat Rev Clin Oncol 2012, 9:119-123.
89. Nosho K., Baba Y., Tanaka N., Shima K., Hayashi M., Meyerhardt J.A., Giovannucci E., Dranoff G., Fuchs C.S., Ogino S. Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J.Pathol. 2010, 222:350-366.
90. Ogino S., Galon J., Fuchs C.S., Dranoff G. Cancer immunology-analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol 2011, 8:711-719.
91. Okamoto Y., Folco E.J., Minami M., Wara A.K., Feinberg M.W., Sukhova G.K., Colvin R.A., Kihara S., Funahashi T., Luster A.D., Libby P. Adiponectin inhibits the production of CXC receptor 3 chemokine ligands in macrophages and reduces T-lymphocyte recruitment in atherogenesis. Circ. Res. 2008, 102:218-225.
92. Pagès F., Berger A., Camus M., Sanchez-Cabo F., Costes A., Molidor R., Mlecnik B., Kirilovsky A., Nilsson M., Damotte D., et al. Effector memory Tcells, early metastasis, and survival in colorectal cancer. N.Engl. J. Med. 2005, 353:2654-2666.
93. Pagès F., Kirilovsky A., Mlecnik B., Asslaber M., Tosolini M., Bindea G., Lagorce C., Wind P., Marliot F., Bruneval P., et al. In situ cytotoxic and memory Tcells predict outcome in patients with early-stage colorectal cancer. J.Clin. Oncol. 2009, 27:5944-5951.
94. Pagès F., Galon J., Dieu-Nosjean M.C., Tartour E., Sautès-Fridman C., Fridman W.H. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 2010, 29:1093-1102.
95. Palucka K., Banchereau J. Dendritic cell-based cancer therapeutic vaccines. Immunity 2013, 39:38-48. this issue.
96. Panelli M.C., Wang E., Phan G., Puhlmann M., Miller L., Ohnmacht G.A., Klein H.G., Marincola F.M. Gene-expression profiling of the response of peripheral blood mononuclear cells and melanoma metastases to systemic IL-2 administration. Genome Biol. 2002, 3. RESEARCH0035.
97. Panelli M.C., Stashower M.E., Slade H.B., Smith K., Norwood C., Abati A., Fetsch P., Filie A., Walters S.A., Astry C., et al. Sequential gene profiling of basal cell carcinomas treated with imiquimod in a placebo-controlled study defines the requirements for tissue rejection. Genome Biol. 2007, 8:R8.
98. Prehn R.T., Main J.M. Immunity to methylcholanthrene-induced sarcomas. J.Natl. Cancer Inst. 1957, 18:769-778.
99. Prieto P.A., Yang J.C., Sherry R.M., Hughes M.S., Kammula U.S., White D.E., Levy C.L., Rosenberg S.A., Phan G.Q. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin. Cancer Res. 2012, 18:2039-2047.
100. Restifo N.P., Dudley M.E., Rosenberg S.A. Adoptive immunotherapy for cancer: harnessing the Tcell response. Nat. Rev. Immunol. 2012, 12:269-281.
101. Ribas A., Wolchok J.D. Combining cancer immunotherapy and targeted therapy. Curr. Opin. Immunol. 2013, 25:291-296.
102. Robert C., Thomas L., Bondarenko I., O'Day S., M D J.W., Garbe C., Lebbe C., Baurain J.F., Testori A., Grob J.J., et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N.Engl. J. Med. 2011, 364:2517-2526.
103. Rotondi M., Chiovato L. The chemokine system as a therapeutic target in autoimmune thyroid diseases: a focus on the interferon-γ inducible chemokines and their receptor. Curr. Pharm. Des. 2011, 17:3202-3216.
104. Saint-Mezard P., Berthier C.C., Zhang H., Hertig A., Kaiser S., Schumacher M., Wieczorek G., Bigaud M., Kehren J., Rondeau E., et al. Analysis of independent microarray datasets of renal biopsies identifies a robust transcript signature of acute allograft rejection. Transpl. Int. 2009, 22:293-302.
105. Salk J. Immunological paradoxes: theoretical considerations in the rejection or retention of grafts, tumors, and normal tissue. Ann. N Y Acad. Sci. 1969, 164:365-380.
106. Sarasin-Filipowicz M., Oakeley E.J., Duong F.H., Christen V., Terracciano L., Filipowicz W., Heim M.H. Interferon signaling and treatment outcome in chronic hepatitis C. Proc. Natl. Acad. Sci. USA 2008, 105:7034-7039.
107. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565-1570.
108. Schwartzentruber D.J., Lawson D.H., Richards J.M., Conry R.M., Miller D.M., Treisman J., Gailani F., Riley L., Conlon K., Pockaj B., et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N.Engl. J. Med. 2011, 364:2119-2127.
109. Senovilla L., Vacchelli E., Galon J., Adjemian S., Eggermont A., Fridman W.H., Sautès-Fridman C., Ma Y., Tartour E., Zitvogel L., et al. Trial watch: Prognostic and predictive value of the immune infiltrate in cancer. OncoImmunology 2012, 1:1323-1343.
110. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., Schreiber R.D. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001, 410:1107-1111.
111. Sharma A., Shah S.R., Illum H., Dowell J. Vemurafenib: targeted inhibition of mutated BRAF for treatment of advanced melanoma and its potential in other malignancies. Drugs 2012, 72:2207-2222.
112. Shen-Orr S.S., Tibshirani R., Khatri P., Bodian D.L., Staedtler F., Perry N.M., Hastie T., Sarwal M.M., Davis M.M., Butte A.J. Cell type-specific gene expression differences in complex tissues. Nat. Methods 2010, 7:287-289.
113. Spivey T.L., Uccellini L., Ascierto M.L., Zoppoli G., De Giorgi V., Delogu L.G., Engle A.M., Thomas J.M., Wang E., Marincola F.M., Bedognetti D. Gene expression profiling in acute allograft rejection: challenging the immunologic constant of rejection hypothesis. J.Transl. Med. 2011, 9:174.
114. Spivey T.L., De Giorgi V., Zhao Y.D., Bedognetti D., Pos Z., Liu Q.Z., Tomei S., Ascierto M.L., Uccellini L., Reinboth J., et al. The stable traits ofmelanoma genetics: an alternate approach to target discovery. BMC Genomics 2012, 13:156.
115. Stutman O. Tumor development after 3-methylcholanthrene in immunologically deficient athymic-nude mice. Science 1974, 183:534-536.
116. Stutman O. Immunodepression and malignancy. Adv. Cancer Res. 1975, 22:261-422.
117. Terme M., Pernot S., Marcheteau E., Sandoval F., Benhamouda N., Colussi O., Dubreuil O., Carpentier A.F., Tartour E., Taieb J. VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res. 2013, 73:539-549.
118. Teschendorff A.E., Miremadi A., Pinder S.E., Ellis I.O., Caldas C. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol. 2007, 8:R157.
119. Thomas L. On immunosurveillance in human cancer. Yale J. Biol. Med. 1982, 55:329-333.
120. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N.Engl. J. Med. 2012, 366:2443-2454.
121. Tosolini M., Kirilovsky A., Mlecnik B., Fredriksen T., Mauger S., Bindea G., Berger A., Bruneval P., Fridman W.H., Pagès F., Galon J. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res. 2011, 71:1263-1271.
122. Trinchieri G. Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu. Rev. Immunol. 2012, 30:677-706.
123. Uccellini L., De Giorgi V., Zhao Y., Tumaini B., Erdenebileg N., Dudley M.E., Tomei S., Bedognetti D., Ascierto M.L., Liu Q., et al. IRF5 gene polymorphisms in melanoma. J.Transl. Med. 2012, 10:170.
124. Ulloa-Montoya F., Louahed J., Dizier B., Gruselle O., Spiessens B., Lehmann F.F., Suciu S., Kruit W.H., Eggermont A.M., Vansteenkiste J., Brichard V.G. Predictive gene signature in MAGE-A3 antigen-specific cancer immunotherapy. J.Clin. Oncol. 2013, 31:2388-2395.
125. Vacchelli E., Galluzzi L., Eggermont A., Fridman W.H., Galon J., Sautès-Fridman C., Tartour E., Zitvogel L., Kroemer G. Trial watch: FDA-approved Toll-like receptor agonists for cancer therapy. OncoImmunology 2012, 1:894-907.
126. Vacchelli E., Galluzzi L., Fridman W.H., Galon J., Sautès-Fridman C., Tartour E., Kroemer G. Trial watch: Chemotherapy with immunogenic cell death inducers. OncoImmunology 2012, 1:179-188.
127. Vacchelli E., Martins I., Eggermont A., Fridman W.H., Galon J., Sautès-Fridman C., Tartour E., Zitvogel L., Kroemer G., Galluzzi L. Trial watch: Peptide vaccines in cancer therapy. OncoImmunology 2012, 1:1557-1576.
128. van den Boorn J.G., Hartmann G. Turning tumors into vaccines: co-opting the innate immune system. Immunity 2013, 39:27-37. this issue.
129. van der Bruggen P., Traversari C., Chomez P., Lurquin C., De Plaen E., Van den Eynde B., Knuth A., Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991, 254:1643-1647.
130. Van Pel A., Vessière F., Boon T. Protection against two spontaneous mouse leukemias conferred by immunogenic variants obtained by mutagenesis. J.Exp. Med. 1983, 157:1992-2001.
131. Verhaak R.G., Tamayo P., Yang J.Y., Hubbard D., Zhang H., Creighton C.J., Fereday S., Lawrence M., Carter S.L., Mermel C.H., et al. Prognostically relevant gene signatures of high-grade serous ovarian carcinoma. J.Clin. Invest. 2013, 123:517-525. Cancer Genome Atlas Research Network.
132. Wang E., Miller L.D., Ohnmacht G.A., Mocellin S., Perez-Diez A., Petersen D., Zhao Y., Simon R., Powell J.I., Asaki E., et al. Prospective molecular profiling of melanoma metastases suggests classifiers of immune responsiveness. Cancer Res. 2002, 62:3581-3586.
133. Wang E., Worschech A., Marincola F.M. The immunologic constant of rejection. Trends Immunol. 2008, 29:256-262.
134. Wang E., Zhao Y., Monaco A., Uccellini L., Kirkwood J.M., Spyropoulou-Vlachou M., Panelli M.C., Marincola F.M., Gogas H. Amulti-factorial genetic model for prognostic assessment of high risk melanoma patients receiving adjuvant interferon. PLoS ONE 2012, 7:e40805.
135. Wang E., Bedognetti D., Marincola F.M. Prediction of response to anticancer immunotherapy using gene signatures. J.Clin. Oncol. 2013, 31:2369-2371.
136. Wang E., Bedognetti D., Tomei S., Marincola F.M. Common pathways to tumor rejection. Ann. N Y Acad. Sci. 2013, 1284:75-79.
137. Weiss G.R., Grosh W.W., Chianese-Bullock K.A., Zhao Y., Liu H., Slingluff C.L., Marincola F.M., Wang E. Molecular insights on the peripheral and intratumoral effects of systemic high-dose rIL-2 (aldesleukin) administration for the treatment of metastatic melanoma. Clin. Cancer Res. 2011, 17:7440-7450.
138. Wittekind C., Compton C.C., Greene F.L., Sobin L.H. TNM residual tumor classification revisited. Cancer 2002, 94:2511-2516.
139. Yoshida S., Arakawa F., Higuchi F., Ishibashi Y., Goto M., Sugita Y., Nomura Y., Niino D., Shimizu K., Aoki R., et al. Gene expression analysis of rheumatoid arthritis synovial lining regions by cDNA microarray combined with laser microdissection: up-regulation of inflammation-associated STAT1, IRF1, CXCL9, CXCL10, and CCL5. Scand. J. Rheumatol. 2012, 41:170-179.
140. Zeimet A.G., Reimer D., Wolf D., Fiegl H., Concin N., Wiedemair A., Wolf A.M., Rumpold H., Muller-Holzner E., Marth C. Intratumoral interferon regulatory factor (IRF)-1 but not IRF-2 is of relevance in predicting patient outcome in ovarian cancer. Int. J. Cancer 2009, 124:2353-2360.
141. Zeremski M., Petrovic L.M., Chiriboga L., Brown Q.B., Yee H.T., Kinkhabwala M., Jacobson I.M., Dimova R., Markatou M., Talal A.H. Intrahepatic levels of CXCR3-associated chemokines correlate with liver inflammation and fibrosis in chronic hepatitis C. Hepatology 2008, 48:1440-1450.
142. Zhang L., Conejo-Garcia J.R., Katsaros D., Gimotty P.A., Massobrio M., Regnani G., Makrigiannakis A., Gray H., Schlienger K., Liebman M.N., et al. Intratumoral Tcells, recurrence, and survival in epithelial ovarian cancer. N.Engl. J. Med. 2003, 348:203-213.
143. Zhao Y., Simon R. Gene expression deconvolution in clinical samples. Genome Med. 2010, 2:93.
144. Zitvogel L., Kepp O., Galluzzi L., Kroemer G. Inflammasomes in carcinogenesis and anticancer immune responses. Nat. Immunol. 2012, 13:343-351.
145. Zitvogel L., Galluzzi L., Smyth M.J., Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 2013, 39:74-88. this issue.