Cancer immunoediting and "spontaneous" tumor regression

Pathology Research and Practice

Volumn 206, Issue 1, 2010, Pages 1-8

  Sengupta, Neel ^a   MacFie, Tammie S ^a   MacDonald, Thomas T ^b   Pennington, Daniel ^b   Silver, Andrew R ^a  

^a Institute of Cell and Molecular Science   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Immunoediting; Immunogenicity; Immunotherapy; Innate and adaptive immunity

Indexed keywords

ANTINEOPLASTIC AGENT; BCG VACCINE; CANCER VACCINE; CHEMOKINE; CYTOKINE; HLA ANTIGEN; IMMUNOSUPPRESSIVE AGENT; TOXIN;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; AUTOIMMUNITY; BLADDER TUMOR; CANCER CELL; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER REGRESSION; CANCER RISK; CANCER SURVIVAL; CELL THERAPY; CELLULAR IMMUNITY; CHEMICAL CARCINOGENESIS; DISEASE ACTIVITY; DRUG EFFICACY; GRAFT RECIPIENT; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MICROSATELLITE INSTABILITY; NONHUMAN; OVERALL SURVIVAL; PROGNOSIS; REVIEW; T LYMPHOCYTE; TUMOR; TUMOR IMMUNITY;

ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; HUMANS; IMMUNOTHERAPY; NEOPLASM REGRESSION, SPONTANEOUS; NEOPLASMS;

EID: 73849109183     PISSN: 03440338     EISSN: 16180631     Source Type: Journal    
DOI: 10.1016/j.prp.2009.10.001     Document Type: Review

References (73)

1. Alexandroff A.B., Jackson A.M., O'Donnell M.A., and James K. BCG immunotherapy of bladder cancer: 20 years on. Lancet 353 (1999) 1689-1694
2. Anastassiou G., Rebmann V., Wagner S., Bornfeld N., and Grosse-Wilde H. Expression of classic and nonclassic HLA class I antigens in uveal melanoma. Invest. Ophthalmol.Vis. Sci. 44 (2003) 2016-2019
3. Barbe S., Van M.L., and Anne J. The use of clostridial spores for cancer treatment. J. Appl. Microbiol. 101 (2006) 571-578
4. Birkeland S.A., Storm H.H., Lamm L.U., Barlow L., Blohme I., Forsberg B., Eklund B., Fjeldborg O., Friedberg M., and Frodin L. Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int. J. Cancer 60 (1995) 183-189
5. Boshoff C., and Weiss R. AIDS-related malignancies. Nat. Rev. Cancer 2 (2002) 373-382
6. Braun S.E., Chen K., Foster R.G., Kim C.H., Hromas R., Kaplan M.H., Broxmeyer H.E., and Cornetta K. The CC chemokine CK beta-11/MIP-3 beta/ELC/Exodus 3 mediates tumor rejection of murine breast cancer cells through NK cells. J. Immunol. 164 (2000) 4025-4031
7. Bubenik J. MHC class I down regulation, tumour escape from immune surveillance and design of therapeutic strategies. Folia Biol. (Praha) 51 (2005) 1-2
8. Bui J.D., and Schreiber R.D. Cancer immunosurveillance immunoediting and inflammation: independent or interdependent processes?. Curr. Opin. Immunol. 19 (2007) 203-208
9. Cabrera T., Lara E., Romero J.M., Maleno I., Real L.M., Ruiz-Cabello F., Valero P., Camacho F.M., and Garrido F. HLA class I expression in metastatic melanoma correlates with tumor development during autologous vaccination. Cancer Immunol. Immunother. 56 (2007) 709-717
10. Cabrera T., Lopez-Nevot M.A., Gaforio J.J., Ruiz-Cabello F., and Garrido F. Analysis of HLA expression in human tumor tissues. Cancer Immunol. Immunother. 52 (2003) 1-9
11. Cairns C.M., Gordon J.R., Li F., Baca-Estrada M.E., Moyana T., and Xiang J. Lymphotactin expression by engineered myeloma cells drives tumor regression: mediation by CD4+ and CD8+ T cells and neutrophils expressing XCR1 receptor. J. Immunol. 167 (2001) 57-65
12. Coley W.B. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin. Orthop. Relat. Res. (1991) 3-11
13. Dannull J., Su Z., Rizzieri D., Yang B.K., Coleman D., Yancey D., Zhang A., Dahm P., Chao N., Gilboa E., and Vieweg J. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J. Clin. Invest. 115 (2005) 3623-3633
14. Delp K., Momburg F., Hilmes C., Huber C., and Seliger B. Functional deficiencies of components of the MHC class I antigen pathway in human tumors of epithelial origin. Bone Marrow Transplant. 25 Suppl. 2 (2000) S88-S95
15. Dilloo D., Bacon K., Holden W., Zhong W., Burdach S., Zlotnik A., and Brenner M. Combined chemokine and cytokine gene transfer enhances antitumor immunity. Nat. Med. 2 (1996) 1090-1095
16. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., and Schreiber R.D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3 (2002) 991-998
17. Dunn G.P., Old L.J., and Schreiber R.D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21 (2004) 137-148
18. Dunn G.P., Old L.J., and Schreiber R.D. The three Es of cancer immunoediting. Annu. Rev. Immunol. 22 (2004) 329-360
19. Facoetti A., Nano R., Zelini P., Morbini P., Benericetti E., Ceroni M., Campoli M., and Ferrone S. Human leukocyte antigen and antigen processing machinery component defects in astrocytic tumors. Clin. Cancer Res. 11 (2005) 8304-8311
20. Fushimi T., Kojima A., Moore M.A., and Crystal R.G. Macrophage inflammatory protein 3alpha transgene attracts dendritic cells to established murine tumors and suppresses tumor growth. J. Clin. Invest. 105 (2000) 1383-1393
21. 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., and Pages F. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313 (2006) 1960-1964
22. Garnett C.T., Greiner J.W., Tsang K.Y., Kudo-Saito C., Grosenbach D.W., Chakraborty M., Gulley J.L., Arlen P.M., Schlom J., and Hodge J.W. TRICOM vector based cancer vaccines. Curr. Pharm. Des. 12 (2006) 351-361
23. Gascon J. Epidemiology, etiology and pathophysiology of traveler's diarrhea. Digestion 73 Suppl. 1 (2006) 102-108
24. Giovarelli M., Cappello P., Forni G., Salcedo T., Moore P.A., LeFleur D.W., Nardelli B., Carlo E.D., Lollini P.L., Ruben S., Ullrich S., Garotta G., and Musiani P. Tumor rejection and immune memory elicited by locally released LEC chemokine are associated with an impressive recruitment of APCs, lymphocytes, and granulocytes. J. Immunol. 164 (2000) 3200-3206
25. Girardi M., Oppenheim D.E., Steele C.R., Lewis J.M., Glusac E., Filler R., Hobby P., Sutton B., Tigelaar R.E., and Hayday A.C. Regulation of cutaneous malignancy by gammadelta T cells. Science 294 (2001) 605-609
26. Gramham F.O., and Coleman P.N. Infection of a secondary carcinoma by salmonella montevideo. BMJ 1 (1952) 1116 (Ref Type: Generic)
27. Griffioen M., Steegenga W.T., Ouwerkerk I.J., Peltenburg L.T., Jochemsen A.G., and Schrier P.I. Repression of the minimal HLA-B promoter by c-myc and p53 occurs through independent mechanisms. Mol. Immunol. 35 (1998) 829-835
28. Groh V., Rhinehart R., Secrist H., Bauer S., Grabstein K.H., and Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96 (1999) 6879-6884
29. Guidoboni M., Gafa R., Viel A., Doglioni C., Russo A., Santini A., Del T.L., Macri E., Lanza G., Boiocchi M., and Dolcetti R. Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favorable prognosis. Am. J. Pathol. 159 (2001) 297-304
30. Hirose K., Hakozaki M., Nyunoya Y., Kobayashi Y., Matsushita K., Takenouchi T., Mikata A., Mukaida N., and Matsushima K. Chemokine gene transfection into tumour cells reduced tumorigenicity in nude mice in association with neutrophilic infiltration. Br. J. Cancer 72 (1995) 708-714
31. Hodi F.S. Cytotoxic T-lymphocyte-associated antigen-4. Clin. Cancer Res. 13 (2007) 5238-5242
32. Hodi F.S., Butler M., Oble D.A., Seiden M.V., Haluska F.G., Kruse A., Macrae S., Nelson M., Canning C., Lowy I., Korman A., Lautz D., Russell S., Jaklitsch M.T., Ramaiya N., Chen T.C., Neuberg D., Allison J.P., Mihm M.C., and Dranoff G. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc. Natl. Acad. Sci. USA 105 (2008) 3005-3010
33. Janeway Jr. C.A., Fischer-Lindahl K., and Hammerling U. The Mls locus: new clues to a lingering mystery. Immunol. Today 9 (1988) 125-126
34. Kauffman H.M. Malignancies in organ transplant recipients. J. Surg. Oncol. 94 (2006) 431-433
35. Kimura N.T., Taniguchi S., Aoki K., and Baba T. Selective localization and growth of Bifidobacterium bifidum in mouse tumors following intravenous administration. Cancer Res. 40 (1980) 2061-2068
36. Kirk C.J., Hartigan-O'Connor D., Nickoloff B.J., Chamberlain J.S., Giedlin M., Aukerman L., and Mule J.J. T cell-dependent antitumor immunity mediated by secondary lymphoid tissue chemokine: augmentation of dendritic cell-based immunotherapy. Cancer Res. 61 (2001) 2062-2070
37. Koebel C.M., Vermi W., Swann J.B., Zerafa N., Rodig S.J., Old L.J., Smyth M.J., and Schreiber R.D. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450 (2007) 903-907
38. Laning J., Kawasaki H., Tanaka E., Luo Y., and Dorf M.E. Inhibition of in vivo tumor growth by the beta chemokine, TCA3. J. Immunol. 153 (1994) 4625-4635
39. Laust A.K., Sur B.W., Wang K., Hubby B., Smith J.F., and Nelson E.L. VRP immunotherapy targeting neu: treatment efficacy and evidence for immunoediting in a stringent rat mammary tumor model. Breast Cancer Res. Treat. 106 (2007) 371-382
40. Le H.N., Lee N.C., Tsung K., and Norton J.A. Pre-existing tumor-sensitized T cells are essential for eradication of established tumors by IL-12 and cyclophosphamide plus IL-12. J. Immunol. 167 (2001) 6765-6772
41. Loeb L.A., Loeb K.R., and Anderson J.P. Multiple mutations and cancer. Proc. Natl. Acad. Sci. USA 100 (2003) 776-781
42. Luster A.D., and Leder P. IP-10, a -C-X-C- chemokine, elicits a potent thymus-dependent antitumor response in vivo. J. Exp. Med. 178 (1993) 1057-1065
43. MacKie R.M., Reid R., and Junor B. Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N. Engl. J. Med. 348 (2003) 567-568
44. Maleno I., Romero J.M., Cabrera T., Paco L., Aptsiauri N., Cozar J.M., Tallada M., Lopez-Nevot M.A., and Garrido F. LOH at 6p21.3 region and HLA class I altered phenotypes in bladder carcinomas. Immunogenetics 58 (2006) 503-510
45. Minton N.P. Clostridia in cancer therapy. Nat. Rev. Microbiol. 1 (2003) 237-242
46. Morgan R.A., Dudley M.E., Wunderlich J.R., Hughes M.S., Yang J.C., Sherry R.M., Royal R.E., Topalian S.L., Kammula U.S., Restifo N.P., Zheng Z., Nahvi A., de Vries C.R., Rogers-Freezer L.J., Mavroukakis S.A., and Rosenberg S.A. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314 (2006) 126-129
47. Mule J.J., Custer M., Averbook B., Yang J.C., Weber J.S., Goeddel D.V., Rosenberg S.A., and Schall T.J. RANTES secretion by gene-modified tumor cells results in loss of tumorigenicity in vivo: role of immune cell subpopulations. Hum. Gene Ther. 7 (1996) 1545-1553
48. Murdoch C., Muthana M., and Lewis C.E. Hypoxia regulates macrophage functions in inflammation. J. Immunol. 175 (2005) 6257-6263
49. Nakashima E., Oya A., Kubota Y., Kanada N., Matsushita R., Takeda K., Ichimura F., Kuno K., Mukaida N., Hirose K., Nakanishi I., Ujiie T., and Matsushima K. A candidate for cancer gene therapy: MIP-1 alpha gene transfer to an adenocarcinoma cell line reduced tumorigenicity and induced protective immunity in immunocompetent mice. Pharm. Res. 13 (1996) 1896-1901
50. Nemunaitis J., Cunningham C., Senzer N., Kuhn J., Cramm J., Litz C., Cavagnolo R., Cahill A., Clairmont C., and Sznol M. Pilot trial of genetically modified, attenuated Salmonella expressing the E. coli cytosine deaminase gene in refractory cancer patients. Cancer Gene Ther. 10 (2003) 737-744
51. Norell H., Carlsten M., Ohlum T., Malmberg K.J., Masucci G., Schedvins K., Altermann W., Handke D., Atkins D., Seliger B., and Kiessling R. Frequent loss of HLA-A2 expression in metastasizing ovarian carcinomas associated with genomic haplotype loss and HLA-A2-restricted HER-2/neu-specific immunity. Cancer Res. 66 (2006) 6387-6394
52. Oppenheim D.E., Roberts S.J., Clarke S.L., Filler R., Lewis J.M., Tigelaar R.E., Girardi M., and Hayday A.C. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat. Immunol. 6 (2005) 928-937
53. Pages 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., and Galon J. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353 (2005) 2654-2666
54. Pawinski A., Sylvester R., Kurth K.H., Bouffioux C., van der M.A., Parmar M.K., and Bijnens L. A combined analysis of European Organization for Research and Treatment of Cancer, and Medical Research Council randomized clinical trials for the prophylactic treatment of stage TaT1 bladder cancer, European Organization for Research and Treatment of Cancer Genitourinary Tract Cancer Cooperative Group and the Medical Research Council Working Party on Superficial Bladder Cancer. J. Urol. 156 (1996) 1934-1940 (discussion)
55. Peng G., Wang H.Y., Peng W., Kiniwa Y., Seo K.H., and Wang R.F. Tumor-infiltrating gammadelta T cells suppress T and dendritic cell function via mechanisms controlled by a unique toll-like receptor signaling pathway. Immunity 27 (2007) 334-348
56. Raffaghello L., Nozza P., Morandi F., Camoriano M., Wang X., Garre M.L., Cama A., Basso G., Ferrone S., Gambini C., and Pistoia V. Expression and functional analysis of human leukocyte antigen class I antigen-processing machinery in medulloblastoma. Cancer Res. 67 (2007) 5471-5478
57. Rosenberg S.A. Progress in human tumour immunology and immunotherapy. Nature 411 (2001) 380-384
58. Rubinstein N., Alvarez M., Zwirner N.W., Toscano M.A., Ilarregui J.M., Bravo A., Mordoh J., Fainboim L., Podhajcer O.L., and Rabinovich G.A. Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection; a potential mechanism of tumor-immune privilege. Cancer Cell 5 (2004) 241-251
59. Sharma S., Stolina M., Luo J., Strieter R.M., Burdick M., Zhu L.X., Batra R.K., and Dubinett S.M. Secondary lymphoid tissue chemokine mediates T cell-dependent antitumor responses in vivo. J. Immunol. 164 (2000) 4558-4563
60. Singal D.P., Ye M., and Qiu X. Molecular basis for lack of expression of HLA class I antigens in human small-cell lung carcinoma cell lines. Int. J. Cancer 68 (1996) 629-636
61. Sluimer J.C., Gasc J.M., van Wanroij J.L., Kisters N., Groeneweg M., Sollewijn G., Cleutjens J.P., van den Akker L.H., Corvol P., Wouters B.G., Daemen M.J., and Bijnens A.P. Hypoxia, hypoxia-inducible transcription factor and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J. Am. Coll. Cardiol. 51 (2008) 1258-1265
62. Smyth M.J., Crowe N.Y., Hayakawa Y., Takeda K., Yagita H., and Godfrey D.I. NKT cells - conductors of tumor immunity?. Curr. Opin. Immunol. 14 (2002) 165-171
63. Smyth M.J., Dunn G.P., and Schreiber R.D. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv. Immunol. 90 (2006) 1-50
64. Starnes C.O. Coley's toxins in perspective. Nature 357 (1992) 11-12
65. Steinman R.M., and Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 311 (2006) 17-58
66. Toso J.F., Gill V.J., Hwu P., Marincola F.M., Restifo N.P., Schwartzentruber D.J., Sherry R.M., Topalian S.L., Yang J.C., Stock F., Freezer L.J., Morton K.E., Seipp C., Haworth L., Mavroukakis S., White D., MacDonald S., Mao J., Sznol M., and Rosenberg S.A. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J. Clin. Oncol. 20 (2002) 142-152
67. Tsung K., and Norton J.A. Lessons from Coley's toxin. Surg. Oncol. 15 (2006) 25-28
68. van der B.P., Traversari C., Chomez P., Lurquin C., De P.E., Van den E.B., Knuth A., and Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254 (1991) 1643-1647
69. Vicari A.P., it-Yahia S., Chemin K., Mueller A., Zlotnik A., and Caux C. Antitumor effects of the mouse chemokine 6Ckine/SLC through angiostatic and immunological mechanisms. J. Immunol. 165 (2000) 1992-2000
70. Watson N.F., Spendlove I., Madjd Z., McGilvray R., Green A.R., Ellis I.O., Scholefield J.H., and Durrant L.G. Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients. Int. J. Cancer 118 (2006) 1445-1452
71. Wei M.Q., Ellem K.A., Dunn P., West M.J., Bai C.X., and Vogelstein B. Facultative or obligate anaerobic bacteria have the potential for multimodality therapy of solid tumours. Eur. J. Cancer 43 (2007) 490-496
72. Wei M.Q., Mengesha A., Good D., and Anne J. Bacterial targeted tumour therapy - dawn of a new era. Cancer Lett. 259 (2008) 16-27
73. Zitvogel L., Tesniere A., and Kroemer G. Cancer despite immunosurveillance: immunoselection and immunosubversion. Nat. Rev. Immunol. 6 (2006) 715-727