The three Es of cancer immunoediting

Annual Review of Immunology

Volumn 22, Issue , 2004, Pages 329-360

  Dunn, Gavin P ^a   Old, Lloyd J ^b   Schreiber, Robert D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Immunosurveillance; Interferon; Lymphocytes; Tumor; Tumor sculpting

Indexed keywords

GAMMA INTERFERON; PERFORIN;

CANCER; CANCER SURVIVAL; CANCER TRANSPLANTATION; CELLULAR IMMUNITY; CORRELATION ANALYSIS; DISEASE COURSE; HOST CELL; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOSURVEILLANCE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR ESCAPE; TUMOR IMMUNITY;

ANIMALS; HUMANS; IMMUNOLOGIC SURVEILLANCE; NEOPLASMS;

EID: 2542430341     PISSN: 07320582     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.immunol.22.012703.104803     Document Type: Review

References (170)

1. Ehrlich P. 1909. Ueber den jetzigen Stand der Karzinomforschung. Ned. Tijdschr. Geneeskd. 5(Part 1):273-90
2. Thomas L. 1959. Discussion. In Cellular and Humoral Aspects of the Hypersensitive States, ed. HS Lawrence, pp. 529-32. New York: Hoeber-Harper
3. Burnet FM. 1970. The concept of immunological surveillance. Prog. Exp. Tumor Res. 13:1-27
4. Stutman O. 1974. Tumor development after 3-methylcholanthrene in immunologically deficient athymic-nude mice. Science 183:534-36
5. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, et al. 2001. IFNγ lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:1107-11
6. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. 2002. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3:991-98
7. Burnet FM. 1971. Immunological surveillance in neoplasia. Transplant Rev. 7:3-25
8. Burnet FM. 1957. Cancer - a biological approach. Br. Med. J. 1:841-47
9. Burnet FM. 1964. Immunological factors in the process of carcinogenesis. Br. Med. Bull. 20:154-58
10. Medawar P. 1944. The behavior and fate of skin autografts and skin homografts in rabbits. J. Anat. 78:176-99
11. Medawar P. 1945. A second study of the behaviour and fate of skin homografts in rabbits. J. Anat. 79:157-76
12. Foley EJ. 1953. Antigenic properties of methylcholanthrene-induced tumors in mice of the strain of origin. Cancer Res. 13:835-37
13. Prehn RT, Main JM. 1957. Immunity to methylcholanthrene-induced sarcomas. J. Natl Cancer Inst. 18:769-78
14. Old LJ, Boyse EA. 1966. Specific antigens of tumors and leukemias of experimental animals. Med. Clin. North Am. 50:901-12
15. Klein G. 1966. Tumor antigens. Annu. Rev. Microbiol. 20:223-52
16. Flanagan SP. 1966. 'Nude', a new hairless gene with pleiotropic effects in the mouse. Genet. Res. 8:295-309
17. Pantelouris EM. 1968. Absence of thymus in a mouse mutant. Nature 217:370-71
18. Stutman O. 1979. Chemical carcinogenesis in nude mice: comparison between nude mice from homozygous and heterzygous matings and effect of age and carcinogen dose. J. Natl. Cancer Inst. 2:353-58
19. Stutman O. 1978. Spontaneous, viral, and chemically induced tumors in the nude mouse. In The Nude Mouse in Experimental and Clinical Research., ed. J Fogh, BC Giovanella, pp. 411-35. New York: Academic
20. Stutman O. 1973. Tumor development in immunologically deficient nude mice after exposure to chemical carcinogens. Proc. Int. Workshop Nude Mice. Scanticon, Aarhus, Denmark, Oct. 11-13, 1973. 1:257-64
21. Rygaard J, Povlsen CO. 974. Is immunological surveillance not a cell-mediated immune function? Transplantation 17: 135-36
22. Rygaard J, Povlsen CO. 1974. The mouse mutant nude does not develop spontaneous tumours. An argument against immunological surveillance. Acta Pathol. Microbiol. Scand. Sect. B 82:99-106
23. Maleckar JR, Sherman LA. 1987. The composition of the T cell receptor repertoire in nude mice. J. Immunol. 138:3873-76
24. Ikehara S, Pahwa RN, Fernandes G, Hansen CT, Good RA. 1984. Functional T cells in athymic nude mice. Proc. Natl. Acad. Sci. USA 81:886-88
25. Hunig T. 1983. T-cell function and specificity in athymic mice. Immunol. Today 4:84-87
26. Herberman RB, Holden HT. 1978. Natural cell-mediated immunity. Adv. Cancer Res. 27:305-77
27. Janeway CA, Jr. 1989. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harbor Symp. Quant. Biol. 54(Part 1):1-13
28. Heidelberger C. 1975. Chemical carcinogenesis. Annu. Rev. Biochem. 44:79-121
29. Kouri RE, Nebert DW. 1977. Genetic regulation of susceptibility to polycyclic-hydrocarbon-induced tumors in the mouse. In Origins of Human Cancer, ed. HH Hiatt, JD Watson, JA Winsten, pp. 811-35. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
30. Dighe AS, Richards E, Old LJ, Schreiber RD. 1994. Enhanced in vivo growth resistance to rejection of tumor cells expressing dominant negative IFNγ receptors. Immunity 1:447-56
31. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, et al. 1998. Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. USA 95:7556-61
32. Street SE, Cretney E, Smyth MJ. 2001. Perform and interferon-γ activities independently control tumor initiation, growth, and metastasis. Blood 97:192-97
33. Street SE, Trapani JA, MacGregor D, Smyth MJ. 2002. Suppression of lymphoma and epithelial malignancies effected by interferon γ. J. Exp. Med. 196: 129-34
34. Bach EA, Aguet M, Schreiber RD. 1997. The IFNγ receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15:563-91
35. van den Broek MF, Kagi D, Ossendorp F, Toes R, Vamvakas S, et al. 1996. Decreased tumor surveillance in perforin-deficient mice. J. Exp. Med. 184:1781-90
36. Smyth MJ, Thia KY, Street SE, Cretney E, Trapani JA, et al. 2000. Differential tumor surveillance by natural killer (NK) and NKT cells. J. Exp. Med. 191:661-68
37. Smyth MJ, Thia KY, Street SE, MacGregor D, Godfrey DI, Trapani JA. 2000. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J. Exp. Med. 192:755-60
38. Russell JH, Ley TJ. 2002. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20:323-70
39. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855-67
40. Smyth MJ, Crowe NY, Godfrey DI. 2001. NK cells and NKT cells collaborate in host protection from methylcholantnrene-induced fibrosarcoma. Int. Immunol. 13: 459-63
41. Dighe AS, Farrar MA, Schreiber RD. 1993. Inhibition of cellular responsiveness to interferon-γ (IFNγ) induced by overexpression of inactive forms of the IFNγ receptor. J. Biol. Chem. 268:10645-53
42. Chin YE, Kitagawa M, Su WS, You Z, Iwamoto Y, Fu X. 1996. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 mediated by Stat1. Science 272:719-22
43. Bromberg JF, Horvath CM, Wen Z, Schreiber RD, Darnell JE Jr. 1996. Transcriptionally active Stat1 is required for the antiproliferative effects of both interferonα and interferonγ. Proc. Natl. Acad. Sci. USA 93:7673-78
44. Chin YE, Kitagawa M, Kuida K, Flavell RA, Fu XY. 1997. Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol. 17:5328-37
45. Detjen KM, Farwig K, Welzel M, Wiedenmann B, Rosewicz S. 2001. Interferon-γ inhibits growth of human pancreatic carcinoma cells via caspase-1 dependent induction of apoptosis. Gut 49:251-62
46. Xu X, Fu XY, Plate J, Chong AS. 1998. IFNγ induces cell growth inhibition by Fas-medialed apoplosis: requirement of STAT1 prolein for up-regulation of Fas and FasL expression. Cancer Res. 58:2832-37
47. Luster AD, Leder P. 1993. IP-10, a -C-X-C-chemokine, elicits a potent thymus-dependent antitumor response in vivo. J. Exp. Med. 178:1057-65
48. Voest EE, Kenyon BM, O'Reilly MS, Truitt G, D'Amalo RJ, Folkman J. 1995. Inhibition of angiogenesis in vivo by interleukin 12. J. Natl. Cancer Inst. 87:581-86
49. Strieter RM, Kunkel SL, Arenberg DA, Burdick MD, Polverini PJ. 1995. Interferon γ-inducible prolein 10 (IP-10), a member of the C-X-C chemokine family, is an inhibitor of angiogenesis. Biochem. Biophys. Res. Commun. 210:51-57
50. Sgadari C, Angiolillo AL, Cherney BW, Pike SE, Farber JM, et al. 1996. Interferon-inducible protein-10 identified as a mediator of tumor necrosis in vivo. Proc. Natl. Acad. Sci. USA 93:13791-96
51. Sgadari C, Farber JM, Angiolillo AL, Liao F, Teruya-Feldslein J, et al. 1997. Mig, the monokine induced by interferon-γ, promotes tumor necrosis in vivo. Blood 89:2635-43
52. Coughlin CM, Salhany KE, Gee MS, LaTemple DC, Kotenko S, et al. 1998. Tumor cell responses to IFNγ affect tumorigenicity and response to IL-12 therapy and antiangiogenesis. Immunity 9:25-34
53. Fallarino F, Gajewski TF. 1999. Cutting edge: differentiation of antitumor CTL in vivo requires host expression of Stat1. J. Immunol. 163:4109-13
54. Kacha AK, Fallarino F, Markiewicz MA, Gajewski TF. 2000. Cutting edge: spontaneous rejection of poorly immunogenic P1.HTR tumors by Stat6-deficient mice. J. Immunol. 165:6024-28
55. Enzler T, Gillessen S, Manis JP, Ferguson D, Fleming J, et al. 2003. Deficiencies of GM-CSF and interferonγ link inflammation and cancer. J. Exp. Med. 197:1213-19
56. + T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFNγ receptor expression by non-hematopoietic cells. Immunity 12:677-86
57. Ibe S, Qin Z, Schuler T, Preiss S, Blankenstein T. 2001. Tumor rejection by disturbing tumor stroma cell interactions. J. Exp. Med. 194:1549-59
58. Girardi M, Oppenheim DE, Steele CR, Lewis JM, Glusac E, et al. 2001. Regulation of cutaneous malignancy by γδ T cells. Science 294:605-9
59. Smyth MJ, Takeda K, Hayakawa Y, Peschon JJ, van den Brink MR, Yagita H. 2003. Nature's TRAIL - on a path to cancer immunotherapy. Immunity 18:1-6
60. Takeda K, Smyth MJ, Cretney E, Hayakawa Y, Kayagaki N, et al. 2002. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J. Exp. Med. 195:161-69
61. Cretney E, Takeda K, Yagita H, Glaccum M, Peschon JJ, Smyth MJ. 2002. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J. Immunol. 168:1356-61
62. Noguchi Y, Jungbluth A, Richards E, Old LJ. 1996. Effect of interleukin 12 on tumor induction by 3-methylcholanthrene. Proc. Natl. Acad. Sci. USA 93:11798-801
63. Hayakawa Y, Rovero S, Forni G, Smyth MJ. 2003. α-Galactosylceramide (KRN7000) suppression of chemical-and oncogene-dependent carcinogenesis. Proc. Natl. Acad. Sci. USA http:// www.pnas.org/cgi/doi/10.1073/pnas.1630 663100
64. Penn I. 1970. Malignant Tumors in Organ Transplant Recipients. New York: Springer-Verlag. 51 pp.
65. Gatti RA, Good RA. 1971. Occurrence of malignancy in immunodeficiency diseases. A literature review. Cancer 28:89-98
66. Boshoff C, Weiss R. 2002. AIDS-related malignancies. Nat. Rev. Cancer 2:373-82
67. Birkeland SA, Storm HH, Lamm LU, Barlow L, Blohme I, et al. 1995. Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int. J. Cancer 60:183-89
68. Sheil AGR. 2001. Cancer in dialysis and transplant patients. In Kidney Transplantation, ed. PJ Morris, pp. 558-70. Philadelphia: W.B. Saunders
69. Pham SM, Kormos RL, Landreneau RJ, Kawai A, Gonzalez-Cancel I, et al. 1995. Solid tumors after heart transplantation: lethality of lung cancer. Ann. Thorac. Surg. 60:1623-26
70. Penn I. 1996. Malignant melanoma in organ allograft recipients. Transplantation 61:274-78
71. Hoover RN. 1977. Effects of drugs-immunosuppression. See Ref. 29, pp. 369-79
72. Sheil AG. 1986. Cancer after transplantation. World J. Surg. 10:389-96
73. Penn I. 1995. Sarcomas in organ allograft recipients. Transplantation 60:1485-91
74. Old LJ. 1981. Cancer immunology: the search for specificity - G.H.A. Clowes memorial lecture. Cancer Res. 41:361-75
75. Carey TE, Takahashi T, Resnick LA, Oettgen HF, Old LJ. 1976. Cell surface antigens of human malignant melanoma: mixed hemadsorption assays for humoral immunity to cultured autologous melanoma cells. Proc. Natl. Acad. Sci. USA 73:3278-82
76. Ueda R, Shiku H, Pfreundschuh M, Takahashi T, Li LT, et al. 1979. Cell surface antigens of human renal cancer defined by autologous typing. J. Exp. Med. 150:564-79
77. Knuth A, Danowski B, Oettgen HF, Old LJ. 1984. T-cell-mediated cytotoxicity against autologous malignant melanoma: analysis with interleukin 2-dependent T-cell cultures. Proc. Natl. Acad. Sci. USA 81:3511-15
78. Traversari C, van der Bruggen P, Van den Eynde B, Hainaut P, Lemoine C, et al. 1992. Transfection expression of a gene coding for a human melanoma antigen recognized by autologous cytolytic T lymphocytes. Immunogenetics 35:145-52
79. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, et al. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254:1643-47
80. Sahin U, Tureci O, Schmitt H, Cochlovius B, Johannes T, et al. 1995. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc. Natl. Acad. Sci. USA 92:11810-13
81. Wang RF, Rosenberg SA. 1999. Human tumor antigens for cancer vaccine development. Immunol. Rev. 170:85-100
82. Boon T, van der Bruggen P. 1996. Human tumor antigens recognized by T lymphocytes. J. Exp. Med. 183:725-29
83. Old LJ, Chen YT. 1998. New paths in human cancer serology. J. Exp. Med. 187:1163-67
84. Rosenberg SA. 1999. A new era for cancer immunotherapy based on the genes that encode cancer antigens. Immunity 10:281-87
85. Scanlan MJ, Gure AO, Jungbluth AA, Old LJ, Chen YT. 2002. Cancer/testis antigens: an expanding family of targets for cancer immunotherapy. Immunol. Rev. 188:22-32
86. Chen YT, Scanlan MJ, Sahin U, Tureci O, Gure AO, et al. 1997. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl. Acad. Sci. USA 94:1914-18
87. Jungbluth AA, Chen YT,. Stockert E, Busam KJ, Kolb D, et al. 2001. Immunohistochemical analysis of NY-ESO-1 antigen expression in normal malignant human tissues. Int. J. Cancer 92:856-60
88. Stockert E, Jager E, Chen YT, Scanlan MJ, Gout I, et al. 1998. A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J. Exp. Med. 187:1349-54
89. Jager E, Stockert E, Zidianakis Z, Chen YT, Karbach J, et al. 1999. Humoral immune responses of cancer patients against "Cancer-Testis" antigen NY-ESO-1: correlation with clinical events. Int. J. Cancer 84:506-10
90. Jager E, Nagata Y, Gnjatic S, Wada H, Stockert E, et al. 2000. Monitoring CD8 T cell responses to NY-ESO-1: correlation of humoral cellular immune responses. Proc. Natl. Acad. Sci. USA 97:4760-65
91. + T cell epitopes from NY-ESO-1 presented by HLA-DR molecules. J. Immunol. 165:1153-59
92. + T cell responses against NY-ESO-1 in cancer patients: correlation with antibody responses. Proc. Natl. Acad. Sci. USA 100:8862-67
93. Posner JB, Furneaux HM. 1990. Paraneoplastic syndromes. In Immunologic Mechanisms in Neurologic and Psychiatric Disease, ed. BH Waksman, pp. 187-219. New York: Raven
94. Darnell RB. 1996. Onconeural antigens and the paraneoplastic neurologic disorders: at the intersection of cancer, immunity, and the brain. Proc. Natl. Acad. Sci. USA 93:4529-36
95. Musunuru K, Darnell RB. 2001. Paraneoplastic neurologic disease antigens: RNA-binding proteins and signaling proteins in neuronal degeneration. Annu. Rev. Neurosci. 24:239-62
96. Albert ML, Darnell JC, Bender A, Francisco LM, Bhardwaj N, Darnell RB. 1998. Tumor-specific killer cells in paraneoplastic cerebellar degeneration. Nat. Med. 4:1321-24
97. Albert ML, Austin LM, Darnell RB. 2000. Detection and treatment of activated T cells in the cerebrospinal fluid of patients with paraneoplastic cerebellar degeneration. Ann. Neurol. 47:9-17
98. Dalmau J, Furneaux HM, Gralla RJ, Kris MG, Posner JB. 1990. Detection of the anti-Hu antibody in the serum of patients with small cell lung cancer - a quantitative western blot analysis. Ann. Neurol. 27:544-52
99. Darnell RB, DeAngelis LM. 1993. Regression of small-cell lung carcinoma in patients with paraneoplastic neuronal antibodies. Lancet 341:21-22
100. Graus F, Dalmou J, Rene R, Tora M, Malats N, et al. 1997. Anti-Hu antibodies in patients with small-cell lung cancer: association with complete response to therapy and improved survival. J. Clin. Oncol. 15:2866-72
101. Groh V, Bahrain S, Bauer S, Herman A, Beauchamp M, Spies T. 1996. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc. Natl. Acad. Sci. USA 93:12445-50
102. Bahrain S. 2000. MIC genes: from genetics to biology. Adv. Immunol. 76:1-60
103. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. 2001. Costimulation of CD8αβ T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2:255-60
104. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. 1999. Broad tumor-associated expression and recognition by tumor-derived γδT cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96:6879-84
105. Vetter CS, Groh V, Thor Strafen P, Spies T, Brocker EB, Becker JC. 2002. Expression of stress-induced MHC class I related chain molecules on human melanoma. J. Invest. Dermatol. 118:600-5
106. Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, et al. 2003. Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int. J. Cancer 104:354-61
107. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, et al. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727-29
108. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. 2002. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat. Immunol. 3:1150-55
109. Pende D, Rivera P, Marcenaro S, Chang CC, Biassoni R, et al. 2002. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res. 62:6178-86
110. Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, et al. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123-33
111. Groh V, Steinle A, Bauer S, Spies T. 1998. Recognition of stress-induced MHC molecules by intestinal epithelial γδT cells. Science 279:1737-40
112. Wu J, Groh V, Spies T. 2002. T cell antigen receptor engagement and specificity in the recognition of stress-inducible MHC class I-related chains by human epithelial γδT cells. J. Immunol. 169:1236-40
113. Groh V, Wu J, Yee C, Spies T. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419:734-38
114. Salih HR, Rammensee HG, Steinle A. 2002. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J. Immunol. 169:4098-102
115. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. 2000. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1:119-26
116. Cerwenka A, Bakker AB, McClanahan T, Wagner J, Wu J, et al. 2000. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12:721-27
117. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. 2001. Rael and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413:165-71
118. Clark WH Jr, Elder DE, Guerry D, Braitman LE, Trock BJ, et al. 1989. Model predicting survival in stage I melanoma based on tumor progression. J. Natl. Cancer Inst. 81:1893-904
119. Mihm MC Jr, Clemente CG, Cascinelli N. 1996. Tumor infiltrating lymphocytes in lymph node melanoma metastases: a histopathologic prognostic indicator and an expression of local immune response. Lab. Invest. 74:43-47
120. Clemente CG, Mihm MC Jr, 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 77:1303-10
121. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, et al. 2003. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348:203-13
122. + T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res. 58:3491-94
123. + T cell infiltrations within esophageal carcinomas. Cancer Res. 61:3932-36
124. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Che X, et al. 2000. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 88:577-83
125. Villegas FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, et al. 2002. Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 35:23-28
126. Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, et al. 1997. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 79:2320-28
127. Balch CM, Riley LB, Bae YJ, Salmeron MA, Platsoucas CD, et al. 1990. Patterns of human tumor-infiltrating lymphocytes in 120 human cancers. Arch. Surg. 125:200-5
128. Svane IM, Engel AM, Nielsen MB, Ljunggren HG, Rygaard J, Werdelin O. 1996. Chemically induced sarcomas from nude mice are more immunogenic than similar sarcomas from congenic normal mice. Em. J. Immunol. 26:1844-50
129. Engel AM, Svane IM, Rygaard J, Werdelin O. 1997. MCA sarcomas induced in scid mice are more immunogenic than MCA sarcomas induced in congenic, immunocompetent mice. Scand. J. Immunol. 45:463-70
130. Macleod K. 2000. Tumor suppressor genes. Curr. Opin. Genet. Dev. 10:81-93
131. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100:57-70
132. Hanahan D, Folkman J. 1996. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353-64
133. Carmeliet P, Jain RK. 2000. Angiogenesis in cancer and other diseases. Nature 407:249-57
134. Sternlicht MD, Werb Z. 2001. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell. Dev. Biol. 17:463-516
135. Vicari AP, Caux C. 2002. Chemokines in cancer. Cytokine Growth Factor Rev. 13:143-54
136. Matzinger P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12:991-1045
137. Wrenshall LE, Stevens RB, Cerra FB, Platt JL. 1999. Modulation of macrophage B and cell function by glycosaminoglycans. J. Leukoc. Biol. 66:391-400
138. Benlagha K, Bendelac A. 2000. CD1d-restricted mouse Vα14 and human Vα24 T cells: lymphocytes of innate immunity. Semin. Immunol. 12:537-42
139. Hodge-Dufour J, Noble PW, Horton MR, Bao C, Wysoka M, et al. 1997. Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages. J. Immunol. 159:2492-500
140. Bancroft GJ, Schreiber RD, Unanue ER. 1991. Natural immunity: a T-cell-independent pathway of macrophage activation, defined in the scid mouse. Immunol. Rev. 124:5-24
141. Kumar A, Commane M, Flickinger TW, Horvath CM, Stark GR. 1997. Defective TNF-α-induced apoptosis in STAT1-null cells due to low constitutive levels of caspases. Science 278:1630-32
142. Schreiber RD, Pace JL, Russell SW, Altman A, Katz D. 1983. Macrophage activating factor produced by a T cell hybridoma: physicochemical and biosynthetic resemblance to gamma-interferon. J. Immunol. 131:826-32
143. Nathan CF, Murray HW, Wiebe ME, Rubin BY. 1983. Identification of interferon-γ as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158:670-89
144. MacMicking J, Xie QW, Nathan C. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15:323-50
145. Takeda K, Hayakawa Y, Smyth MJ, Kayagaki N, Yamaguchi N, et al. 2001. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat. Med. 7:94-100
146. Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM, et al. 2001. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon γ-dependent natural killer cell protection from tumor metastasis. J. Exp. Med. 193:661-70
147. Hayakawa Y, Kelly JM, Westwood JA, Darcy PK, Diefenbach A, et al. 2002. Cutting edge: tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J. Immunol. 169:5377-81
148. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med. 195:327-33
149. Srivastava P. 2002. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20:395-425
150. Li Z, Menoret A, Srivastava P. 2002. Roles of heat-shock proteins in antigen presentation and cross-presentation. Curr. Opin. Immunol. 14:45-51
151. Sallusto F, Mackay CR, Lanzavecchia A. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18:593-620
152. Huang AY, Golumbek P, Ahmadzadeh M, Jaffee E, Pardoll D, Levitsky H. 1994. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 264:961-65
153. Albert ML, Sauter B, Bhardwaj N. 1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392:86-89
154. Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480-83
155. + T cells. J. Exp. Med. 197:985-95
156. Loeb LA, Loeb KR, Anderson JP. 2003. Multiple mutations and cancer. Proc. Natl. Acad. Sci. USA 100:776-81
157. Loeb LA. 1991. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 51:3075-19
158. Lengauer C, Kinzler KW, Vogelstein B. 1998. Genetic instabilities in human cancers. Nature 396:643-49
159. MacKie RM, Reid R, Junor B. 2003. Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N. Engl. J. Med. 348:567-68
160. Elder GJ, Hersey P, Branley P. 1997. Remission of transplanted melanoma-clinical course and tumour cell characterisation. Clin. Transplant. 11:565-68
161. Suranyi MG, Hogan PG, Falk MC, Axelsen RA, Rigby R, et al. 1998. Advanced donor-origin melanoma in a renal transplant recipient: immunotherapy, cure, and retransplantation. Transplantation 66:655-61
162. Penn I. 1991. Donor transmitted disease: cancer. Transplant Proc. 23:2629-31
163. + regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol. Rev. 182:18-32
164. Khong HT, Restifo NP. 2002. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 3:999-1005
165. Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. 2000. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv. Immunol. 74:181-273
166. Catlett-Falcone R, Landowski TH, Oshiro MM, Turkson J, Levitzki A, et al. 1999. Constitutive activation of stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10:105-15
167. Algarra I, Cabrera T, Garrido F. 2000. The HLA crossroad in tumor immunology. Hum. Immunol. 61:65-73
168. Seliger B, Maeurer MJ, Ferrone S. 2000. Antigen-processing machinery breakdown and tumor growth. Immunol. Today 21:455-64
169. Hayashi T, Faustman DL. Development of spontaneous uterine tumors in low molecular mass polypeptide-2 knockout mice. Cancer Res. 62:24-27
170. Folkman J, Hahnfeldt P, Hlatky L. 2000. Cancer: looking outside the genome. Nat. Rev. Mol. Cell Biol. 1:76-79