The essential role of the in situ immune reaction in human colorectal cancer

Journal of Leukocyte Biology

Volumn 84, Issue 4, 2008, Pages 981-987

  Pagès, Franck ^a,b,c,d   Galon, Jérôme ^a,b,c   Fridman, Wolf H ^a,b,c,d  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

^d HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

Memory T cells; Prognostic factors; Tumor immunology

Indexed keywords

ADAPTIVE IMMUNITY; CANCER CHEMOTHERAPY; CANCER SURGERY; CELL DENSITY; CELL FUNCTION; CELL POPULATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; COLORECTAL CANCER; CONFERENCE PAPER; CORRELATION ANALYSIS; GENE MUTATION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL PARAMETERS; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC INFILTRATION; MEMORY T LYMPHOCYTE; METASTASIS; MICROARRAY ANALYSIS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROGNOSIS; TH1 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR RECURRENCE;

COLORECTAL NEOPLASMS; HUMANS; IMMUNOLOGIC MEMORY; LYMPHATIC METASTASIS; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASM STAGING; PROGNOSIS; RECURRENCE; T-LYMPHOCYTES;

EID: 54249127469     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1107773     Document Type: Conference Paper

References (44)

1. Mueller, M. M., Fusenig, N. E. (2004) Friends or foes - bipolar effects of the tumor stroma in cancer. Nat. Rev. Cancer 4, 839-849.
2. Balkwill, F., Charles, K. A., Mantovani, A. (2005) Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 7, 211-217.
3. Coussens, L. M., Werb, Z. (2002) Inflammation and cancer. Nature 420, 860-867.
4. Pollard, J. W. (2004) Tumor-educated macrophages promote tumor progression and metastasis. Nat. Rev. Cancer 4, 71-78.
5. Sylvester, R. J., van der Meijden, A. P., Lamm, D. L. (2002) Intravesical bacillus Calmette-Guerin reduces the risk of progression in patients with superficial bladder cancer: a meta-analysis of the published results of randomized clinical trials. J. Urol. 168, 1964-1970.
6. Krieg, A. M. (2006) Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 5, 471-484.
7. Burnet, F. M. (1970) The concept of immunological surveillance. Prog. Exp. Tumor Res. 13, 1-27.
8. Birkeland, S. A., Storm, H. H., Lamm, L. U., Barlow, L., Blohme, 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, 183-189.
9. Myron Kauffman, H., McBride, M. A., Cherikh, W. S., Spain, P. C., Marks, W. H., Roza, A. M. (2002) Transplant tumor registry: donor related malignancies. Transplantation 74, 358-362.
10. Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., Schreiber, R. D. (2001) IFNγ and lymphocytes prevent primary tumor development and shape tumor immunogenicity. Nature 410, 1107-1111.
11. Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., Schreiber, R. D. (2002) Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3, 991-998.
12. Koebel, C. M., Vermi, W., Swann, J. B., Zerafa, N., Rodig, S. J., Old, L. J., Smyth, M. J., Schreiber, R. D. (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450, 903-907.
13. Clark Jr., W. H., Elder, D. E., Guerry IV, D., Braitman, L. E., Trock, B. J., Schultz, D., Synnestvedt, M., Halpern, A. C. (1989) Model predicting survival in stage I melanoma based on tumor progression. J. Natl. Cancer Inst. 81, 1893-1904.
14. Clemente, C. G., Mihm Jr., M. C., Bufalino, R., Zurrida, S., Collini, P., Cascinelli, N. (1996) Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer 77, 1303-1310.
15. Gajewski, T. F., Meng, Y., Blank, C., Brown, I., Kacha, A., Kline, J., Harlin, H. (2006) Immune resistance orchestrated by the tumor microenvironment. Immunol. Rev. 213, 131-145.
16. Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pages, C., Tosolini, M., Camus, M., Berger, A., Wind, P., Zinzindohoue, F., Bruneval, P., Cugnenc, P. H., Trajanoski, Z., Fridman, W. H., Pages, F. (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960-1964.
17. 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, P. H., Trajanoski, Z., Fridman, W. H., Galon, J. (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353, 2654-2666.
18. Tsavellas, G., Patel, H., Allen-Mersh, T. G. (2001) Detection and clinical significance of occult tumor cells in colorectal cancer. Br. J. Surg. 88, 1307-1320.
19. Curiel, T. J., Coukos, G., Zou, L., Alvarez, X., Cheng, P., Mottram, P., Evdemon-Hogan, M., Conejo-Garcia, J. R., Zhang, L., Burow, M., Zhu, Y., Wei, S., Kryczek, I., Daniel, B., Gordon, A., Myers, L., Lackner, A., Disis, M. L., Knutson, K. L., Chen, L., Zou, W. (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10, 942-949.
20. Wolf, D., Wolf, A. M., Rumpold, H., Fiegl, H., Zeimet, A. G., Muller-Holzner, E., Deibl, M., Gastl, G., Gunsilius, E., Marth, C. (2005) The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin. Cancer Res. 11, 8326-8331.
21. Wolf, D., Marth, C., Wolf, A. M. (2006) Immune cells in colorectal cancer. N. Engl. J. Med. 354, 1531-1532.
22. Bronte, V., Zanovello, P. (2005) Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5, 641-654.
23. Kusmartsev, S. A., Li, Y., Chen, S. H. (2000) Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J. Immunol. 165, 779-785.
24. Valenti, R., Huber, V., Filipazzi, P., Pilla, L., Sovena, G., Villa, A., Corbelli, A., Fais, S., Parmiani, G., Rivoltini, L. (2006) Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-β-mediated suppressive activity on T lymphocytes. Cancer Res. 66, 9290-9298.
25. Arango, D., Laiho, P., Kokko, A., Alhopuro, P., Sammalkorpi, H., Salovaara, R., Nicorici, D., Hautaniemi, S., Alazzouzi, H., Mecklin, J. P., Jarvinen, H., Hemminki, A., Astola, J., Schwartz Jr., S., Aaltonen, L. A. (2005) Gene-expression profiling predicts recurrence in Dukes' C colorectal cancer. Gastroenterology 129, 874-884.
26. Eschrich, S., Yang, I., Bloom, G., Kwong, K. Y., Boulware, D., Cantor, A., Coppola, D., Kruhoffer, M., Aaltonen, L., Orntoft, T. F., Quackenbush, J., Yeatman, T. J. (2005) Molecular staging for survival prediction of colorectal cancer patients. J. Clin. Oncol. 23, 3526-3535.
27. Wang, Y., Jatkoe, T., Zhang, Y., Mutch, M. G., Talantov, D., Jiang, J., McLeod, H. L., Atkins, D. (2004) Gene expression profiles and molecular markers to predict recurrence of Dukes' B colon cancer. J. Clin. Oncol. 22, 1564-1571.
28. Bremers, A. J., Andreola, S., Leo, E., Gallino, F., Rini, F., Lombardo, C., Belli, F., Kuppen, P. J., Parmiani, G., Castelli, C. (2000) T cell responses in colorectal cancer patients: evidence for class II HLA-restricted recognition of shared tumor-associated antigens. Int. J. Cancer 88, 956-961.
29. Guidoboni, M., Gafa, R., Viel, A., Doglioni, C., Russo, A., Santini, A., Del Tin, L., Macri, E., Lanza, G., Boiocchi, M., Dolcetti, R. (2001) Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favorable prognosis. Am. J. Pathol. 159, 297-304.
30. Naito, Y., Saito, K., Shiiba, K., Ohuchi, A., Saigenji, K., Nagura, H., Ohtani, H. (1998) CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res. 58, 3491-3494.
31. Ropponen, K. M., Eskelinen, M. J., Lipponen, P. K., Alhava, E., Kosma, V. M. (1997) Prognostic value of tumor-infiltrating lymphocytes (TILs) in colorectal cancer. J. Pathol. 182, 318-324.
32. Svennevig, J. L., Lunde, O. C., Holter, J., Bjorgsvik, D. (1984) Lymphoid infiltration and prognosis in colorectal carcinoma. Br. J. Cancer 49, 375-377.
33. Nanni, O., Volpi, A., Frassineti, G. L., De Paola, F., Granato, A. M., Dubini, A., Zoli, W., Scarpi, E., Turci, D., Oliverio, G., Gambi, A., Amadori, D. (2002) Role of biological markers in the clinical outcome of colon cancer. Br. J. Cancer 87, 868-875.
34. Faraggi, D., Simon, R. (1996) A simulation study of cross-validation for selecting an optimal cutpoint in univariate survival analysis. Stat. Med. 15, 2203-2213.
35. Popat, S., Hubner, R., Houlston, R. S. (2005) Systematic review of microsatellite instability and colorectal cancer prognosis. J. Clin. Oncol. 23, 609-618.
36. Sankila, R., Aaltonen, L. A., Jarvinen, H. J., Mecklin, J. P. (1996) Better survival rates in patients with MLH1-associated hereditary colorectal cancer. Gastroenterology 110, 682-687.
37. Elsaleh, H., Joseph, D., Grieu, F., Zeps, N., Spry, N., Iacopetta, B. (2000) Association of tumor site and sex with survival benefit from adjuvant chemotherapy in colorectal cancer. Lancet 355, 1745-1750.
38. Dalerba, P., Maccalli, C., Casati, C., Castelli, C., Parmiani, G. (2003) Immunology and immunotherapy of colorectal cancer. Crit. Rev. Oncol. Hematol. 46, 33-57.
39. Lu, H., Goodell, V., Disis, M. L. (2007) Targeting serum antibody for cancer diagnosis: a focus on colorectal cancer. Expert Opin. Ther. Targets 11, 235-244.
40. Sallusto, F., Geginat, J., Lanzavecchia, A. (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763.
41. Xiang, R., Lode, H. N., Gillies, S. D., Reisfeld, R. A. (1999) T cell memory against colon carcinoma is long-lived in the absence of antigen. J. Immunol. 163, 3676-3683.
42. American Joint Committee on Cancer (1988) Manual for Staging of Cancer: Colon and Rectum, 3rd ed. (O. Beahrs, D. Henson, R. Hutter, M. Myers, eds.), Philadelphia, PA, USA, J. B. Lippincott, 75.
43. Locker, G. Y., Hamilton, S., Harris, J., Jessup, J. M., Kemeny, N., Macdonald, J. S., Somerfield, M. R., Hayes, D. F., Bast Jr., R. C. (2006) ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J. Clin. Oncol. 24, 5313-5327.
44. Galon, J., Fridman, W. H., Pages, F. (2007) The adaptive immunologic microenvironment in colorectal cancer: a novel perspective. Cancer Res. 67, 1883-1886.