The immunobiology of cancer immunosurveillance and immunoediting

Immunity

Volumn 21, Issue 2, 2004, Pages 137-148

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

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; ALPHA INTERFERON; ANTIBIOTIC AGENT; BETA INTERFERON; GAMMA INTERFERON; GLYCOPROTEIN GP 100; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 2; MELAN A; MONOCLONAL ANTIBODY; MONOPHENOL MONOOXYGENASE; RECOMBINANT GAMMA INTERFERON; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTINEOPLASTIC ACTIVITY; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CORRELATION ANALYSIS; CYTOTOXICITY; HUMAN; IMMUNE SYSTEM; IMMUNOBIOLOGY; IMMUNOCOMPETENT CELL; IMMUNOSURVEILLANCE; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR CELL; TUMOR MODEL;

ANIMALS; HUMANS; IMMUNITY, NATURAL; IMMUNOLOGIC SURVEILLANCE; INTERFERON TYPE II; NEOPLASMS; TUMOR ESCAPE;

EID: 4143141823     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2004.07.017     Document Type: Review

References (118)

1. Algarra I., Cabrera T., Garrido F. The HLA crossroad in tumor immunology. Hum. Immunol. 61:2000;65-73
2. Asea A., Rehli M., Kabingu E., Boch J.A., Bare O., Auron P.E., Stevenson M.A., Calderwood S.K. Novel signal transduction pathway utilized by extracellular HSP70. role of toll-like receptor (TLR) 2 and TLR4 J. Biol. Chem. 277:2002;15028-15034
3. Bach E.A., Aguet M., Schreiber R.D. The IFNγ receptor. a paradigm for cytokine receptor signaling Annu. Rev. Immunol. 15:1997;563-591
4. Bahram S. MIC genes. from genetics to biology Adv. Immunol. 76:2000;1-60
5. Balkwill, F., and Mantovani, A. (2001). Inflammation and cancer: back to Virchow? Lancet 357 539-545.
6. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 285:1999;727-729
7. Belardelli F., Ferrantini M., Proietti E., Kirkwood J.M. Interferon-alpha in tumor immunity and immunotherapy. Cytokine Growth Factor Rev. 13:2002;119-134
8. Boon T., van der Bruggen P. Human tumor antigens recognized by T lymphocytes. J. Exp. Med. 183:1996;725-729
9. Burnet F.M. Cancer - a Biological Approach. BMJ. 1:1957;841-847
10. Burnet F.M. Immunological factors in the process of carcinogenesis. Br. Med. Bull. 20:1964;154-158
11. Burnet F.M. The concept of immunological surveillance. Prog. Exp. Tumor Res. 13:1970;1-27
12. Burnet F.M. Immunological surveillance in neoplasia. Transplant. Rev. 7:1971;3-25
13. Carayannopoulos L.N., Naidenko O.V., Fremont D.H., Yokoyama W.M. Cutting edge. murine UL16-binding protein-like transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D J. Immunol. 169:2002;4079-4083
14. Cerwenka A., Baron J.L., Lanier L.L. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc. Natl. Acad. Sci. USA. 98:2001;11521-11526
15. Chalupny J.N., Sutherland C.L., Lawrence W.A., Rein-Weston A., Cosman D. ULBP4 is a novel ligand for human NKG2D. Biochem. Biophys. Res. Commun. 305:2003;129-135
16. Conejo-Garcia J.R., Benencia F., Courreges M.C., Khang E., Zhang L., Mohamed-Hadley A., Vinocur J.M., Buckanovich R.J., Thompson C.B., Levine B., Coukos G. Letal, A tumor-associated NKG2D immunoreceptor ligand, induces activation and expansion of effector immune cells. Cancer Biol. Ther. 2:2003;446-451
17. Cosman D., Mullberg J., Sutherland C.L., Chin W., Armitage R., Fanslow W., Kubin M., Chalupny N.J. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 14:2001;123-133
18. Coussens L.M., Werb Z. Inflammation and cancer. Nature. 420:2002;860-867
19. Cretney E., Takeda K., Yagita H., Glaccum M., Peschon J.J., Smyth M.J. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J. Immunol. 168:2002;1356-1361
20. Cui Z., Willingham M.C., Hicks A.M., Alexander-Miller M.A., Howard T.D., Hawkins G.A., Miller M.S., Weir H.M., Du W., DeLong C.J. Spontaneous regression of advanced cancer. identification of a unique genetically determined, age-dependent trait in mice Proc. Natl. Acad. Sci. USA. 100:2003;6682-6687
21. Das H., Groh V., Kuijl C., Sugita M., Morita C.T., Spies T., Bukowski J.F. MICA engagement by human Vγ2Vδ2 T cells enhances their antigen-dependent effector function. Immunity. 15:2001;83-93
22. Diefenbach A., Jamieson A.M., Liu S.D., Shastri N., Raulet D.H. Ligands for the murine NKG2D receptor. expression by tumor cells and activation of NK cells and macrophages Nat. Immunol. 1:2000;119-126
23. Diefenbach A., Jensen E.R., Jamieson A.M., Raulet D.H. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature. 413:2001;165-171
24. Diefenbach A., Hsia J.K., Hsiung M.Y., Raulet D.H. A novel ligand for the NKG2D receptor activates NK cells and macrophages and induces tumor immunity. Eur. J. Immunol. 33:2003;381-391
25. Dighe A.S., Richards E., Old L.J., Schreiber R.D. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFNγ receptors. Immunity. 1:1994;447-456
26. Dunn G.P., Old L.J., Schreiber R.D. The Three Es of Cancer Immunoediting. Annu. Rev. Immunol. 22:2004;329-360
27. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., Schreiber R.D. Cancer immunoediting. from immunosurveillance to tumor escape Nat. Immunol. 3:2002;991-998
28. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat. Rev. Cancer. 4:2004;11-22
29. Ehrlich P. Ueber den jetzigen Stand der Karzinomforschung. Ned. Tijdschr. Geneeskd. 5:1909;273-290
30. Elder G.J., Hersey P., Branley P. Remission of transplanted melanoma-clinical course and tumour cell characterisation. Clin. Transplant. 11:1997;565-568
31. Engel A.M., Svane I.M., Mouritsen S., Rygaard J., Clausen J., Werdelin O. Methylcholanthrene-induced sarcomas in nude mice have short induction times and relatively low levels of surface MHC class I expression. APMIS. 104:1996;629-639
32. Fallarino F., Gajewski T.F. Cutting edge. differentiation of antitumor CTL in vivo requires host expression of Stat1 J. Immunol. 163:1999;4109-4113
33. Gao Y., Yang W., Pan M., Scully E., Girardi M., Augenlicht L.H., Craft J., Yin Z. γδ T cells provide an early source of interferon γ in tumor immunity. J. Exp. Med. 198:2003;433-442
34. Gilfillan S., Ho E.L., Cella M., Yokoyama W.M., Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat. Immunol. 3:2002;1150-1155
35. + T cells to different stages of chemically induced skin cancer. J. Exp. Med. 198:2003;747-755
36. Girardi M., Oppenheim D.E., Steele C.R., Lewis J.M., Glusac E., Filler R., Hobby P., Sutton B., Tigelaar R.E., Hayday A.C. Regulation of cutaneous malignancy by γδ T cells. Science. 294:2001;605-609
37. Gresser I., Belardelli F. Endogenous type I interferons as a defense against tumors. Cytokine Growth Factor Rev. 13:2002;111-118
38. Groh V., Bahram S., Bauer S., Herman A., Beauchamp M., Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc. Natl. Acad. Sci. USA. 93:1996;12445-12450
39. Groh V., Rhinehart R., Secrist H., Bauer S., Grabstein K.H., Spies T. Broad tumor-associated expression and recognition by tumor-derived γδ T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA. 96:1999;6879-6884
40. Groh V., Rhinehart R., Randolph-Habecker J., Topp M.S., Riddell S.R., Spies T. Costimulation of CD8αβ T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2:2001;255-260
41. Groh V., Wu J., Yee C., Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 419:2002;734-738
42. Hahn W.C., Weinberg R.A. Modelling the molecular circuitry of cancer. Nat. Rev. Cancer. 2:2002;331-341. a
43. Hahn W.C., Weinberg R.A. Rules for making human tumor cells. N. Engl. J. Med. 347:2002;1593-1603. b
44. Hayakawa Y., Rovero S., Forni G., Smyth M.J. α-Galactosylceramide (KRN7000) suppression of chemical- and oncogene-dependent carcinogenesis. Proc. Natl. Acad. Sci. USA. 100:2003;9464-9469
45. Jager E., Ringhoffer M., Altmannsberger M., Arand M., Karbach J., Jager D., Oesch F., Knuth A. Immunoselection in vivo. independent loss of MHC class I and melanocyte differentiation antigen expression in metastatic melanoma Int. J. Cancer. 71:1997;142-147
46. Janeway C.A. Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb. Symp. Quant. Biol. 54:1989;1-13
47. Jinushi M., Takehara T., Kanto T., Tatsumi T., Groh V., Spies T., Miyagi T., Suzuki T., Sasaki Y., Hayashi N. Critical role of MHC class I-related chain A and B expression on IFN-α-stimulated dendritic cells in NK cell activation. impairment in chronic hepatitis C virus infection J. Immunol. 170:2003;1249-1256. a
48. Jinushi M., Takehara T., Tatsumi T., Kanto T., Groh V., Spies T., Kimura R., Miyagi T., Mochizuki K., Sasaki Y., Hayashi N. Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int. J. Cancer. 104:2003;354-361. b
49. Johnson G.B., Brunn G.J., Kodaira Y., Platt J.L. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J. Immunol. 168:2002;5233-5239
50. Kaplan D.H., Shankaran V., Dighe A.S., Stockert E., Aguet M., Old L.J., Schreiber R.D. Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. USA. 95:1998;7556-7561
51. Khong H.T., Restifo N.P. Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 3:2002;999-1005
52. Khong H.T., Wang Q.J., Rosenberg S.A. Identification of multiple antigens recognized by tumor-infiltrating lymphocytes from a single patient. tumor escape by antigen loss and loss of MHC expression J. Immunother. 27:2004;184-190
53. Lengauer C., Kinzler K.W., Vogelstein B. Genetic instabilities in human cancers. Nature. 396:1998;643-649
54. Liyanage U.K., Moore T.T., Joo H.G., Tanaka Y., Herrmann V., Doherty G., Drebin J.A., Strasberg S.M., Eberlein T.J., Goedegebuure P.S., Linehan D.C. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol. 169:2002;2756-2761
55. Loeb L.A. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 51:1991;3075-3079
56. Loeb L.A., Loeb K.R., Anderson J.P. Multiple mutations and cancer. Proc. Natl. Acad. Sci. USA. 100:2003;776-781
57. MacKie R.M., Reid R., Junor B. Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. N. Engl. J. Med. 348:2003;567-568
58. Marincola F.M., Jaffee E.M., Hicklin D.J., Ferrone S. Escape of human solid tumors from T-cell recognition. molecular mechanisms and functional significance Adv. Immunol. 74:2000;181-273
59. Matzinger P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12:1994;991-1045
60. + T cells responding to serologically defined autoantigens suppress antitumor immune responses. Proc. Natl. Acad. Sci. USA. 100:2003;10902-10906
61. Nomura M., Takihara Y., Shimada K. Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells. one of the early inducible clones encodes a novel protein sharing several highly homologous regions with a Drosophila polyhomeotic protein Differentiation. 57:1994;39-50
62. Ohashi K., Burkart V., Flohe S., Kolb H. Cutting edge. heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex J. Immunol. 164:2000;558-561
63. Old L.J. Cancer vaccines 2003. opening address Cancer Immun. 3(Suppl 2):2003;1
64. Old L.J., Boyse E.A. Immunology of Experimental Tumors. Annu. Rev. Med. 15:1964;167-186
65. Onizuka S., Tawara I., Shimizu J., Sakaguchi S., Fujita T., Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor α) monoclonal antibody. Cancer Res. 59:1999;3128-3133
66. Pardoll D. Does the immune system see tumors as foreign or self? Annu. Rev. Immunol. 21:2003;807-839
67. Pende D., Rivera P., Marcenaro S., Chang C.C., Biassoni R., Conte R., Kubin M., Cosman D., Ferrone S., Moretta L., Moretta A. 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. 62:2002;6178-6186
68. Penn I. Donor transmitted disease. cancer Transplant. Proc. 23:1991;2629-2631
69. Penn I. Malignant melanoma in organ allograft recipients. Transplantation. 61:1996;274-278
70. Radosavljevic M., Cuillerier B., Wilson M.J., Clement O., Wicker S., Gilfillan S., Beck S., Trowsdale J., Bahram S. A cluster of ten novel MHC class I related genes on human chromosome 6q24.2-q25.3. Genomics. 79:2002;114-123
71. Raulet D.H. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3:2003;781-790
72. + T cells. a population of T cells with immune regulatory activities in vitro Eur. J. Immunol. 28:1998;3435-3447
73. Rosenberg S.A. A new era for cancer immunotherapy based on the genes that encode cancer antigens. Immunity. 10:1999;281-287
74. Rubinstein N., Alvarez M., Zwirner N.W., Toscano M.A., Ilarregui J.M., Bravo A., Mordoh J., Fainboim L., Podhajcer O.L., 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
75. Sahin U., Tureci O., Schmitt H., Cochlovius B., Johannes T., Schmits R., Stenner F., Luo G., Schobert I., Pfreundschuh M. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc. Natl. Acad. Sci. USA. 92:1995;11810-11813
76. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155:1995;1151-1164
77. Schreiber R.D., Old L.J., Hayday A.C., Smyth M.J. Response to 'A cancer immunosurveillance controversy'. Nat. Immunol. 5:2004;4-5
78. Seliger B., Maeurer M.J., Ferrone S. Antigen-processing machinery breakdown and tumor growth. Immunol. Today. 21:2000;455-464
79. Seong S.Y., Matzinger P. Hydrophobicity. an ancient damage-associated molecular pattern that initiates innate immune responses Nat. Rev. Immunol. 4:2004;469-478
80. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., Schreiber R.D. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 410:2001;1107-1111
81. Shi Y., Evans J.E., Rock K.L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature. 425:2003;516-521
82. + T cells. a common basis between tumor immunity and autoimmunity J. Immunol. 163:1999;5211-5218
83. Shinkai Y., Rathbun G., Lam K.P., Oltz E.M., Stewart V., Mendelsohn M., Charron J., Datta M., Young F., Stall A.M., Alt F.W. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 68:1992;855-867
84. Smyth M.J., Crowe N.Y., Godfrey D.I. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int. Immunol. 13:2001;459-463. a
85. Smyth M.J., Godfrey D.I., Trapani J.A. A fresh look at tumor immunosurveillance and immunotherapy. Nat. Immunol. 2:2001;293-299. b
86. Smyth M.J., Takeda K., Hayakawa Y., Peschon J.J., van den Brink M.R., Yagita H. Nature's TRAIL-on a path to cancer immunotherapy. Immunity. 18:2003;1-6
87. Smyth M.J., Thia K.Y., Street S.E., Cretney E., Trapani J.A., Taniguchi M., Kawano T., Pelikan S.B., Crowe N.Y., Godfrey D.I. Differential tumor surveillance by natural killer (NK) and NKT cells. J. Exp. Med. 191:2000;661-668. a
88. Smyth M.J., Thia K.Y., Street S.E., MacGregor D., Godfrey D.I., Trapani J.A. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J. Exp. Med. 192:2000;755-760. b
89. Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells. chaperoning of the innate and adaptive immune responses Annu. Rev. Immunol. 20:2002;395-425
90. Street S.E., Cretney E., Smyth M.J. Perforin and interferon-γ activities independently control tumor initiation, growth, and metastasis. Blood. 97:2001;192-197
91. Street S.E., Trapani J.A., MacGregor D., Smyth M.J. Suppression of lymphoma and epithelial malignancies effected by interferon γ J. Exp. Med. 196:2002;129-134
92. Street S.E., Hayakawa Y., Zhan Y., Lew A.M., MacGregor D., Jamieson A.M., Diefenbach A., Yagita H., Godfrey D.I., Smyth M.J. Innate immune surveillance of spontaneous B cell lymphomas by natural killer cells and γδ T cells. J. Exp. Med. 199:2004;879-884
93. Stutman O. Tumor development after 3-methylcholanthrene in immunologically deficient athymic-nude mice. Science. 183:1974;534-536
94. Stutman O. 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. 2:1979;353-358
95. Suranyi M.G., Hogan P.G., Falk M.C., Axelsen R.A., Rigby R., Hawley C., Petrie J. Advanced donor-origin melanoma in a renal transplant recipient. immunotherapy, cure, and retransplantation Transplantation. 66:1998;655-661
96. Svane I.M., Engel A.M., Nielsen M.B., Ljunggren H.G., Rygaard J., Werdelin O. Chemically induced sarcomas from nude mice are more immunogenic than similar sarcomas from congenic normal mice. Eur. J. Immunol. 26:1996;1844-1850
97. Takaoka A., Hayakawa S., Yanai H., Stoiber D., Negishi H., Kikuchi H., Sasaki S., Imai K., Shibue T., Honda K., Taniguchi T. Integration of interferon-α/β signaling to p53 responses in tumour suppression and antiviral defence. Nature. 424:2003;516-523
98. Takeda K., Smyth M.J., Cretney E., Hayakawa Y., Kayagaki N., Yagita H., Okumura K. Critical role for tumor necrosis factor-related apoptosis-inducing ligand in immune surveillance against tumor development. J. Exp. Med. 195:2002;161-169
99. Terabe M., Berzofsky J.A. Immunoregulatory T cells in tumor immunity. Curr. Opin. Immunol. 16:2004;157-162
100. Terabe M., Matsui S., Noben-Trauth N., Chen H., Watson C., Donaldson D.D., Carbone D.P., Paul W.E., Berzofsky J.A. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway. Nat. Immunol. 1:2000;515-520
101. Termeer C., Benedix F., Sleeman J., Fieber C., Voith U., Ahrens T., Miyake K., Freudenberg M., Galanos C., Simon J.C. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J. Exp. Med. 195:2002;99-111
102. Thomas L. Discussion. Lawrence H.S. Cellular and Humoral Aspects of the Hypersensitive States. 1959;529-532 Hoeber-Harper, New York
103. Thomas L. On immunosurveillance in human cancer. Yale J. Biol. Med. 55:1982;329-333
104. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:1998;287-296
105. Tieng V., Le Bouguenec C., du Merle L., Bertheau P., Desreumaux P., Janin A., Charron D., Toubert A. Binding of Escherichia coli adhesin AfaE to CD55 triggers cell-surface expression of the MHC class I-related molecule MICA. Proc. Natl. Acad. Sci. USA. 99:2002;2977-2982
106. Uhr J.W., Tucker T., May R.D., Siu H., Vitetta E.S. Cancer dormancy. studies of the murine BCL1 lymphoma Cancer Res. 51:1991;5045s-5053s
107. Uyttenhove C., Pilotte L., Theate I., Stroobant V., Colau D., Parmentier N., Boon T., Van den Eynde B.J. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 9:2003;1269-1274
108. van den Broek M.F., Kagi D., Ossendorp F., Toes R., Vamvakas S., Lutza W.K., Melief C.J.M., Zinkernagel R.M., Hengartner H. Decreased tumor surveillance in perforin-deficient mice. J. Exp. Med. 184:1996;1781-1790
109. van der Bruggen P., Traversari C., Chomez P., Lurquin C., De Plaen E., Van den Eynde B., Knuth A., Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 254:1991;1643-1647
110. Vetter C.S., Groh V., thor Straten P., Spies T., Brocker E.B., Becker J.C. Expression of stress-induced MHC class I related chain molecules on human melanoma. J. Invest. Dermatol. 118:2002;600-605
111. + regulatory T cells and their ligands. implications for immunotherapy Immunity. 20:2004;107-118
112. Wang T., Niu G., Kortylewski M., Burdelya L., Shain K., Zhang S., Bhattacharya R., Gabrilovich D., Heller R., Coppola D., et al. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat. Med. 10:2003;48-54
113. Wheelock E.F., Weinhold K.J., Levich J. The tumor dormant state. Adv. Cancer Res. 34:1981;107-140
114. Wong L.H., Krauer K.G., Hatzinisiriou I., Estcourt M.J., Hersey P., Tam N.D., Edmondson S., Devenish R.J., Ralph S.J. Interferon-resistant human melanoma cells are deficient in ISGF3 components, STAT1, STAT2, and p48-ISGF3γ J. Biol. Chem. 272:1997;28779-28785
115. + T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 61:2001;4766-4772
116. Wu G.S., Burns T.F., McDonald E.R. 3rd, Jiang W., Meng R., Krantz I.D., Kao G., Gan D.D., Zhou J.Y., Muschel R., et al. KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat. Genet. 17:1997;141-143
117. Wu G.S., Burns T.F., Zhan Y., Alnemri E.S., El-Deiry W.S. Molecular cloning and functional analysis of the mouse homologue of the KILLER/DR5 tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor. Cancer Res. 59:1999;2770-2775
118. + T cell clones for the treatment of patients with metastatic melanoma. in vivo persistence, migration, and antitumor effect of transferred T cells Proc. Natl. Acad. Sci. USA. 99:2002;16168-16173