The immune contexture of primary and metastatic human tumours

Current Opinion in Immunology

Volumn 27, Issue 1, 2014, Pages 8-15

  Giraldo, Nicolas A ^a,b,c   Becht, Etienne ^a,b,c   Remark, Romain ^a,b,c   Damotte, Diane ^a,b,c,d   Sautès Fridman, Catherine ^a,b,c   Fridman, Wolf H ^a,b,c  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d Hôpital Cochin ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; VASCULOTROPIN;

BONE MARROW CELL; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER SURVIVAL; CARDIOVASCULAR SYSTEM; COLORECTAL CANCER; CORRELATION ANALYSIS; CYTOTOXIC T LYMPHOCYTE; HUMAN; INFLAMMATION; KIDNEY CARCINOMA; LYMPHATIC SYSTEM; LYMPHOCYTIC INFILTRATION; LYMPHOID CELL; MACROPHAGE; METASTASIS; NONHUMAN; PRIMARY TUMOR; PROTEIN SYNTHESIS; REVIEW; STROMA CELL; TH1 CELL; TUMOR GROWTH; TUMOR IMMUNOLOGY; TUMOR MICROENVIRONMENT;

HUMANS; INFLAMMATION; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASM METASTASIS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84893425203     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2014.01.001     Document Type: Review

References (63)

1. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
2. 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.
3. Vogelstein B., Papadopoulos N., Velculescu V.E., Zhou S., Diaz L.A., Kinzler K.W. Cancer genome landscapes. Science 2013, 339:1546-1558.
4. Friedl P., Alexander S. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011, 14:992-1009.
5. 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.
6. 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.
7. Tosolini M., Kirilovsky A., Mlecnik B., Fredriksen T., Mauger S., Bindea G., Berger A., Bruneval P., Fridman W.H., Pagès F., et al. 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.
8. Mlecnik B., Tosolini M., Kirilovsky A., Berger A., Bindea G., Meatchi T., Bruneval P., Trajanoski Z., Fridman W.H., Pagès F., et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 2011, 29:610-618.
9. Bindea G., Mlecnik B., Tosoloni M., Kirilovsky A., Waldner M., Obenauf A., Angell H., Fredriksen T., Lafontaine L., Berger A., et al. Spatio-temporal dynamics of intratumoral cells reveal the immune landscape in human cancer. Immunity 2013, 39:782-795. (in press).
10. Fridman W.H., Mlecnik B., Bindea G., Pagès F., Galon J. Immunosurveillance in human non-viral cancers. Curr Opin Immunol 2011, 23:272-278.
11. Marisa L., de Reyniès A., Duval A., Selves J., Gaub M.P., Vescovo L., Etienne-Grimaldi M.C., Schiappa R., Guenot D., Ayadi M., et al. Gene expression classification of colon cancer into molecular subtypes: characterization, validation, and prognostic value. PLoS Med 2013, 10:e1001453.
12. Nagalla S., Chou J.W., Willingham M.C., Ruiz J., Vaughn J.P., Dubey P., Lash T.L., Hamilton-Dutoit S.J., Bergh J., Sotiriou C., et al. Interactions between immunity, proliferation and molecular subtype in breast cancer prognosis. Genome Biol 2013, 14:R34.
13. Galon J., Angell H.K., Bedognetti D., Marincola F.M. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013, 39:11-26.
14. Gabrilovich D., Ostrand-Rosenberg S., Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012, 12:253-268.
15. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
16. 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 T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009, 27:5944-5951.
17. 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.
18. Fu T., He Q., Sharma P. The ICOS/ICOSL pathway is required for optimal antitumor responses mediated by anti-CTLA-4 therapy. Cancer Res 2011, 71:5445-5454.
19. Wang W., Yu D., Sarnaik A.A., Yu B., Hall M., Morelli D., Zhang Y., Zhao X., Weber J.S. Biomarkers on melanoma patient T cells associated with ipilimumab treatment. J Transl Med 2012, 10. 10.1186/1479-5876-10-146.
20. 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.
21. 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.
22. Remark R., Alifano M., Cremer I., Lupo A., Dieu-Nosjean M.C., Riquet M., Crozet L., Ouakrim H., Goc J., Cazes A., et al. Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin. Clin Cancer Res 2013, 19:4079-4091.
23. Castle P.E., Hillier S.L., Rabe L.K., Hildesheim A., Herrero R., Bratti M.C., Sherman M.E., Burk R.D., Rodriguez A.C., Alfaro M., et al. An association of cervical inflammation with high-grade cervical neoplasia in women infected with oncogenic human papillomavirus (HPV). Cancer Epidemiol Biomarkers Prev 2001, 10:1021-1027.
24. Rothenberg S.M., Ellisen L.W. The molecular pathogenesis of head and neck squamous cell carcinoma. J Clin Invest 2012, 122:1951-1957.
25. Arzumanyan A., Reis H.M., Feitelson M.A. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nat Rev Cancer 2013, 13:123-135.
26. Salama N.R., Hartung M.L., Müller A. Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat Rev Microbiol 2013, 11:385-399.
27. Parsonnet J., Hansen S., Rodriguez L., Gelb A.B., Warnke R.A., Jellum E., Orentreich N., Vogelman J.H., Friedman G.D. Helicobacter pylori infection and gastric lymphoma. N Engl J Med 1994, 330:1267-1271.
28. 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.
29. Houghton A.M. Mechanistic links between COPD and lung cancer. Nat Rev Cancer 2013, 13:233-245.
30. Motz G.T., Coukos G. The parallel lives of angiogenesis and immunosuppression: cancer and other tale. Nat Rev Immunol 2011, 11:702-711.
31. Chia W.K., Ali R., Toh H.C. Aspirin as adjuvant therapy for colorectal cancer - reinterpreting paradigms. Nat Rev Clin Oncol 2012, 9:561-570.
32. Malfertheiner P., Fry L., Mönkemüller K. Can gastric cancer be prevented by Helicobacter pylori eradication?. Best Pract Res Clin Gastroenterol 2006, 7:709-719.
33. Jemal A., Simard E.P., Dorell C., Noone A.M., Markowitz L.E., Kohler B., Eheman C., Saraiya M., Bandi P., Saslow D., et al. Annual Report to the Nation on the Status of Cancer, 1975-2009, featuring the burden and trends in human papillomavirus(HPV)-associated cancers and HPV vaccination coverage level. J Natl Cancer Inst 2013, 105:175-201.
34. Cabibbo G., Maida M., Genco C., Antonucci M., Cammà C. Causes of and prevention strategies for hepatocellular carcinoma. Semin Oncol 2012, 39:374-383.
35. Beck A.H., Espinosa I., Edris B., Li R., Montgomery K., Zhu S., Varma S., Marinelli R.J., van de Rijn M., West R.B. The macrophage colony-stimulating factor 1 response signature in breast carcinoma. Clin Cancer Res 2009, 15:778-787.
36. Dai F., Liu L., Che G., Yu N., Pu Q., Zhang S., Ma J., Ma L., You Z. The number and microlocalization of tumor-associated immune cells are associated with patient's survival time in non-small cell lung cancer. BMC Cancer 2010, 10. 10.1186/1471-2407-10-220.
37. Qing W., Fang W.Y., Ye L., Shen L.Y., Zhang X.F., Fei X.C., Chen X., Wang W.Q., Li X.Y., Xiao J.C., et al. Density of tumor-associated macrophages correlates with lymph node metastasis in papillary thyroid carcinoma. Thyroid 2012, 22:905-910.
38. Kong L.Q., Zhu X.D., Xu H.X., Zhang J.B., Lu L., Wang W.Q., Zhang Q.B., Wu W.Z., Wang L., Fan J., et al. The clinical significance of the CD163+ and CD68+ macrophages in patients with hepatocellular carcinoma. PLoS ONE 2013, 8:e59771.
39. Robinson B.D., Sica G.L., Liu Y.F., Rohan T.E., Gertler F.B., Condeelis J.S., Jones J.G. Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination. Clin Cancer Res 2009, 15:2433-2441.
40. Gandhi N.M., Morales A., Lamm D.L. Bacillus Calmette-Guérin immunotherapy for genitourinary cancer. BJU Int 2013, 112:288-297.
41. Bower M., Palmieri C., Dhillon T. AIDS-related malignancies: changing epidemiology and the impact of highly active antiretroviral therapy. Curr Opin Infect Dis 2006, 19:14-19.
42. Birkeland S.A., Storm H.H., Lamm L.U., Barlow L., Blohmé I., Forsberg B., Eklund B., Fjeldborg O., Friedberg M., Frödin L., et al. Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int J Cancer 1995, 60:183-189.
43. Bais A.G., Beckmann I., Lindemans J., Ewing P.C., Meijer C.J., Snijders P.J., Helmerhorst T.J. A shift to a peripheral Th2-type cytokine pattern during the carcinogenesis of cervical cancer becomes manifest in CIN III lesions. J Clin Pathol 2005, 58:1096-1100.
44. Zheng L., Xue J., Jaffee E.M., Habtezion A. Role of immune cells and immune-based therapies in pancreatitis and pancreatic ductal adenocarcinoma. Gastroenterology 2013, 144:1230-1240.
45. Camus M., Tosolini M., Mlecnik B., Pagès F., Kirilovsky A., Berger A., Costes A., Bindea G., Charoentong P., Bruneval P., et al. Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res 2009, 69:2685-2693.
46. Dieu-Nosjean M.C., Antoine M., Danel C., Heudes D., Wislez M., Poulot V., Rabbe N., Laurans L., Tartour E., de Chaisemartin L., et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008, 26:4410-4417.
47. Martinet L., Garrido I., Filleron T., Le Guellec S., Bellard E., Fournie J.J., Rochaix P., Girard J.P. Human solid tumors contain high endothelial venules: association with T- and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res 2011, 71:5678-5687.
48. Cipponi A., Mercier M., Seremet T., Baurain J.F., Théate I., van den Oord J., Stas M., Boon T., Coulie P.G., van Baren N. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res 2012, 72:3997-4007.
49. de Chaisemartin L., Goc J., Damotte D., Validire P., Magdeleinat P., Alifano M., Cremer I., Fridman W.H., Sautès-Fridman C., Dieu-Nosjean M.C. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res 2011, 71:6391-6399.
50. Goc J., Germain C., Vo-Bourgais T.K.D., Lupo A., Klein C., Knockaert S., de Chaisemartin L., Ouakrim H., Becht E., Alifano M., et al. Tertiary lymphoid structure dendritic cells signal a Th1 and cytotoxic immune contexture, and are required for good prognostic value of CD8+ T cells in lung cancer patients. Cancer Res 2013, 74:1-11. (in press).
51. 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.
52. Matsushita H., Vesely M.D., Koboldt D.C., Rickert C.G., Uppaluri R., Magrini V.J., Arthur C.D., White J.M., Chen Y.S., Shea L.K., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012, 482:400-404.
53. Stoecklein N.H., Klein C.A. Genetic disparity between primary tumours, disseminated tumour cells, and manifest metastasis. Int J Cancer 2010, 126:589-598.
54. Nakano O., Sato M., Naito Y., Suzuki K., Orikasa S., Aizawa M., Suzuki Y., Shintaku I., Nagura H., Ohtani H. Proliferative activity of intratumoral CD8(+) T-lymphocytes as a prognostic factor in human renal cell carcinoma: clinicopathologic demonstration of antitumor immunity. Cancer Res 2001, 61:5132-5136.
55. Creighton C.J., Morgan M., Gunaratne P.H., Wheeler D.A., Gibbs R.A., Robertson A., Chu A., Beroukhim R., Cibulskis K., Signoretti S., et al. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013, 499:43-49.
56. Scott D.W., Chan F.C., Hong F., Rogic S., Tan K.L., Meissner B., Ben-Neriah S., Boyle M., Kridel R., Telenius A., et al. Gene expression-based model using formalin-fixed paraffin-embedded biopsies predicts overall survival in advanced-stage classical Hodgkin lymphoma. J Clin Oncol 2013, 31:692-700.
57. Smith J.J., Deane N.G., Wu F., Merchant N.B., Zhang B., Jiang A., Lu P., Johnson J.C., Schmidt C., Bailey C.E., et al. Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 2010, 138:958-968.
58. Pardoll D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012, 12:252-264.
59. Adotevi O., Pere H., Ravel P., Haicheur N., Badoual C., Merillon N., Medioni J., Peyrard S., Roncelin S., Verkarre V., et al. A decrease of regulatory T cells correlates with overall survival after sunitinib-based antiangiogenic therapy in metastatic renal cancer patients. J Immunother 2010, 33:991-998.
60. Löb S., Königsrainer A., Rammensee H.G., Opelz G., Terness P. Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees?. Nat Rev Cancer 2009, 9:445-452.
61. Bargou R., Leo E., Zugmaier G., Klinger M., Goebeler M., Knop S., Noppeney R., Viardot A., Hess G., Schuler M., et al. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008, 321:974-977.
62. Wolchok J.D., Kluger H., Callahan M.K., Postow M.A., Rizvi N.A., Lesokhin A.M., Segal N.H., Ariyan C.E., Gordon R.A., Reed K., et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013, 369:122-133.
63. 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. 10.1186/1479-5876-10-205.