The immune microenvironment of human tumors: General significance and clinical impact

Cancer Microenvironment

Volumn 6, Issue 2, 2013, Pages 117-122

  Fridman, Wolf Herman ^a,b,c,d   Dieu Nosjean, Marie Caroline ^a,b,c   Pagès, Franck ^a,b,c,d   Cremer, Isabelle ^a,b,c   Damotte, Diane ^a,b,c,e   Sautès Fridman, Catherine ^a,b,c   Galon, Jérôme ^a,b,c  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^e HÔTEL DIEU   (France)

Author keywords

Immune contexture; Immune control in human cancers; Immunoscore

Indexed keywords

CXCL13 CHEMOKINE; CXCL9 CHEMOKINE; FRACTALKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 6; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; CANCER CELL; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CELL DENSITY; CELL FUNCTION; CELL INFILTRATION; COLORECTAL CANCER; CYTOKINE PRODUCTION; DENDRITIC CELL; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LUNG CANCER; MACROPHAGE; MAST CELL; MEMORY T LYMPHOCYTE; NATURAL KILLER T CELL; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; REVIEW; SECONDARY IMMUNE RESPONSE; T LYMPHOCYTE; TH1 CELL; TUMOR IMMUNITY; TUMOR INVASION; TUMOR MICROENVIRONMENT;

EID: 84880924265     PISSN: 18752292     EISSN: 18752284     Source Type: Journal    
DOI: 10.1007/s12307-012-0124-9     Document Type: Review

References (63)

1. Coussens LM and Werb 2 (2002) Inflammation and Cancer. Nature 420:860-867 (Pubitemid 36019639)
2. Hannahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646-674
3. Noman MZ, Messai Y, Carré T, Akalay I, Méron M, Janji B, Hasmim M, Chouaib S (2011) Microenvironmental hypoxia orchestrating the cell stroma cross talk, tumor progression and antitumor response. Crit Rev Immunol 31(5):357-377
4. Qin Z, Blankenstein T (2004) A cancer immunosurveillance controversy. Nat Immunol 5:3-4 (Pubitemid 38081458)
5. Birkeland SA, Storm HH, Lamm LU, Barlow L, Blohmé I, Forsberg B, Eklund B, Fjeldborg O, Friedberg M, Frödin L et al (1995) Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int J Cancer 60(2):183-189
6. Long HM, Taylor GS, Rickinson AB (2011) Immune defence against EBV and EBV-associated disease. Curr Opin Immunol 23:258-264
7. Fridman WH, Mlecnik B, Bindea G, Pagès F, Galon J (2011) Immunosurveillance in human non-viral cancers. Curr Opin Immunol 23:272-278
8. Burnet FM (1964) Immunological factors in the process of carcinogenesis. Br Med Bull 202:154-158
9. Thomas L (1982) On immunosurveillance in human cancer. Yale J Biol 55:329-333 (Pubitemid 13119667)
10. Dunn GP, Old LJ, Screiber RD (2004) The three Es of cancer immunoediting. Annu Rev Immunol 22:329-360 (Pubitemid 38680426)
11. Koebel CM et al (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450:903-907 (Pubitemid 350231320)
12. Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331:1565-1570
13. Mackie RM, Reid R, Junor B (2003) Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N Engl J Med 348:567-568 (Pubitemid 36159900)
14. Fridman WH, Pagès F, Sautès-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298-306
15. Pagès F, Galon J, Dieu-Nosjean MC, Tartour E, Sautès- Fridman C, Fridman WH (2010) Immune infiltration in human tumors, a prognostic factor that should not be ignored. Oncogene 29(8):1093-1102
16. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Berger A, Camus M, Mlecnik B, Bruneval P, Molidor R, Cugnenc PH, Trajanoski Z, Fridman WH, Pagès F (2006) Type, density, and location of immune cells within human colorectal tumors predicts clinical outcome. Science 313:1960-1964 (Pubitemid 44498003)
17. Pagès F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, Lagorce C, Wind P, Bruneval P, Zatloukal K, Trajanoski Z, Berger A, Fridman WH, Galon J (2009) In situ cytotoxic and memory T cells predict outcome in early-stage colorectal cancer patients. J Clin Oncol 27(35):5944-5951
18. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, Bruneval P, Trajanoski Z, Fridman WH, Pages F, Galon J et al (2011) Histopathological-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 29(6):610-618
19. Katz SC, Pillarisetty V, Bamboat ZM et al (2009) T cell infiltrate predicts long-term survival following resection of colorectal cancer liver metastases. Ann Surg Oncol 16:2524-2530
20. Leffers N, Gooden MJ, de Jong RA et al (2009) Prognostic significance of tumor-infiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother 58:449-459
21. Halama N, Michel S, Kloor M et al (2011) Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res 71:5670-5677
22. Hodi FS et al (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363:711-723
23. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M (2012) Safety, activity and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366:2443-2454
24. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM (2012) Safety and activity of anti-PD-1 antibody in patients with advanced cancer. N Engl J Med 366:2455-2465
25. Pardoll DM (2012) The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12:252-264
26. Mantovani A, Allavena P, Sica A, Balckwill F (2008) Cancer-related inflammation. Nature 454:436-444
27. Sautès-Fridman C, Cherfils-Vicini J, Damotte D, Fisson S, Fridman WH, Cremer I, Dieu-Nosjean MC (2011) Tumor microenvironment is multifaceted. Cancer Metastasis Rev 30:13-25
28. Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, André P, Dieu-Nosjean MC, Alifano M, Régnard JF, Fridman WH, Sautès-Fridman C, Cremer I (2011) Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res 71:5412-5422
29. Donskov F, von der Maase H (2006) Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol 24:1997-2005 (Pubitemid 46622107)
30. Galon J, Fridman WH, Pagès F (2007) The adaptive immunologic microenvironment in colorectal cancer: a novel perspective. Cancer Res 67:1883-1886 (Pubitemid 46424201)
31. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L, Lebecque S, Fridman WH, Cadranel J (2008) Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 26:4410-4417
32. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Galon J (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353:2654-2666 (Pubitemid 41817714)
33. de Chaisemartin L, Goc J, Damotte D, Validire P, Magdeleinat P, Alifano M, Cremer I, Fridman WH, Sautès-Fridman C, Dieu-Nosjean MC (2011) Characterization of chemokines and adhesion moleucles associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res 71:6391-6399
34. Martinet L, Garrido I, Filleron T, Le Guellec S, Bellard E, Fournie JJ, Rochaix P, Girard JP (2011) Human solid tumors contain high endothelial venules: association with T-and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res 71:5678-5687
35. Galon J, Pagès F, Marincola FM, Thurin M, Trinchieri G, Fox BA, Gajewski TF, Ascierto PA (2012) The immune score as a new possible approach for the classification of cancer. J Transl Med 10:1
36. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, Berger A, Camus M, Gillard M, Bruneval P, Fridman WH, Pagès F, Trajanoski Z, Galon J (2010) Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 138:1429-1440
37. Mellman I, Coukos G, Dranoff G (2011) Cancer immunotherapy comes of age. Nature 480:480-489
38. Carragher DM, Rangel-Moreno J, Randall TD (2008) Ectopic lymphoid tissues and local immunity. Semin Immunol 20(1):26-42
39. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K, Hartson L, Sprague F, Goodrich S, Woodland DL, Lund FE, Randall TD (2004) Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat Med 10(9):927-934 (Pubitemid 39273733)
40. Moyron-Quiroz JE, Rangel-Moreno J, Hartson L, Kusser K, Tighe MP, Klonowski KD, Lefrançois L, Cauley LS, Harmsen AG, Lund FE, Randall TD (2006) Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity 25(4):643-654 (Pubitemid 44529043)
41. Fridman WH, Teillaud JL, Sautès-Fridman C, Pagès F, Galon J, Zucman-Rossi J, Tartour E, Zitvogel L, Kroemer G (2011) The ultimate goal of curative anti-cancer therapies: inducing an adaptive anti-tumor immune response. Front Immunol 2:66
42. Nakano O, Sato M, Naito Y, Suzuki K, Orikasa S, Aizawa M, Suzuki Y, Shintaku I, Nagura H, Ohtani H (2001) Proliferative activity of intratumoral CD8(+) T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res 61:5132-5136 (Pubitemid 32681545)
43. Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS, Xu Y, Li YW, Tang ZY (2007) Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 25:2586-2593 (Pubitemid 47041232)
44. de Visser KE, Korets LV, Coussens LM (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7:411-423 (Pubitemid 40719125)
45. Andreu P, Johansson M, Affara NI, Pucci F, Tan T, Junankar S, Korets L, Lam J, Tawfik D, DeNardo DG, Naldini L, de Visser KE, De Palma M, Coussens LM (2010) FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 17:121-134
46. Qin Z, Richter G, Schüler T, Ibe S, Cao X, Blankenstein T (1998) B cells inhibit induction of T cell-dependent tumor immunity. Nat Med 4(5):627-630 (Pubitemid 28237366)
47. Kim S, Fridlender ZG, Dunn R, Kehry MR, Kapoor V, Blouin A, Kaiser LR, Albelda SM (2008) B-cell depletion using an anti-CD20 antibody augments antitumor immune responses and immunotherapy in nonhematopoetic murine tumor models. J Immunother 31(5):446-457
48. Menegaz RA, Michelin MA, Etchebehere RM, Fernandes PC, Murta EF (2008) Peri and intratumoral T and B lymphocytic infiltration in breast cancer. Eur J Gynaecol Oncol 29:321-326
49. Simsa P, Teillaud JL, Stott DI, Tóth J, Kotlan B (2005) Tumor-infiltrating B cell immunoglobulin variable region gene usage in invasive ductal breast carcinoma. Pathol Oncol Res 11(2):92-97 (Pubitemid 41039445)
50. Kotlan B, Simsa P, Teillaud JL, Fridman WH, Toth J, McKnight M, Glassy MC (2005) Novel ganglioside antigen identified by B cells in human medullary breast carcinomas: the proof of principle concerning the tumor-infiltrating B lymphocytes. J Immunol 175(4):2278-2285 (Pubitemid 41113835)
51. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, Gonçalves A, André P, Romagné F, Thibault G, Viens P, Birnbaum D, Bertucci F, Moretta A, Olive D (2011) Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest 121:3609-3622
52. Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pagès F, Galon J (2011) Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res 71:1263-1271
53. Zitvogel L, Kepp O, Kroemer G (2011) Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 8:151-160
54. Nardin A, Wong WC, Tow C, Molina TJ, Tissier F, Audebourg A, Garcette M, Caignard A, Avril MF, Abastado JP, Prévost-Blondel A (2011) Dacarbazine promotes stromal remodeling and lymphocyte infiltration in cutaneous melanoma lesions. J Invest Dermatol 131:1896-1905
55. Wilmott JS, Long GV, Howle JR, Haydu LE, Sharma RN, Thompson JF, Kefford RF, Hersey P, Scolyer RA (2011) Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma. Clin Cancer Res 18:1386-1394
56. Adotevi O, Pere H, Ravel P, Haicheur N, Badoual C, Merillon N, Medioni J, Peyrard S, Roncelin S, Verkarre V, Mejean A, Fridman WH, Oudard S, Tartour E (2010) A decrease of regulatory T cells correlates with overall survival after sunitinib-based antiangiogenic therapy in metastatic renal cancer patients. J Immunother 33:991-998
57. Yang JC, Haworth L, Sherry RM, Hwu P, Schwartzentruber DJ, Topalian SL, Steinberg SM, Chen HX, Rosenberg SA (2003) A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349:427-434 (Pubitemid 36910021)
58. Rosenblatt J, Glotzbecker B, Mills H, Vasir B, Tzachanis D, Levine JD, Joyce RM, Wellenstein K, Keefe W, Schickler M, Rotem-Yehudar R, Kufe D, Avigan D (2011) PD-1 blockade by CT-011, anti-PD-1 antibody, enhances ex vivo T-cell responses to autologous dendritic cell/myeloma fusion vaccine. J Immunother 34:409-418
59. Nomi T, Sho M, Akahori T, Hamada K, Kubo A, Kanehiro H, Nakamura S, Enomoto K, Yagita H, Azuma M, Nakajima Y (2007) Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res 13:2151-2157 (Pubitemid 46649885)
60. Jass JR (1986) Lymphocytic infiltration and survival in rectal cancer. J Clin Pathol 39:585-589 (Pubitemid 16069660)
61. Tartour E, Fossiez F, Joyeux I, Galinha A, Gey A, Claret E, Sastre-Garau X, Couturier J, Mosseri V, Vives V, Banchereau J, Fridman WH, Wijdenes J, Lebecque S, Sautès-Fridman C (1999) Interleukin 17, a T-cell-derived cytokine, promotes tumorigenicity of human cervical tumors in nude mice. Cancer Res 59:3698-3704 (Pubitemid 29381875)
62. Tartour E, Gey A, Sastre-Garau X, Lombard Surin I, Mosseri V, Fridman WH (1998) Prognostic value of intratumoral interferon gamma messenger RNA expression in invasive cervical carcinomas. J Natl Cancer Inst 90:287-294 (Pubitemid 28182384)
63. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, Rubin SC, Coukos G (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348:203-213 (Pubitemid 36077915) Médicale Cancéropole Cancéropole Cancéropole