Inflammation and breast cancer. Balancing immune response: Crosstalk between adaptive and innate immune cells during breast cancer progression

Breast Cancer Research

Volumn 9, Issue 4, 2007, Pages

  DeNardo, David G ^a   Coussens, Lisa M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST TUMOR; CELLULAR IMMUNITY; DISEASE COURSE; HUMAN; IMMUNE SYSTEM; IMMUNOLOGY; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE; PHYSIOLOGY; REVIEW;

BREAST NEOPLASMS; DISEASE PROGRESSION; HUMANS; IMMUNE SYSTEM; IMMUNITY, CELLULAR; IMMUNITY, NATURAL; INFLAMMATION; LYMPHOCYTES;

EID: 40349094954     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr1746     Document Type: Review

References (113)

1. American Cancer Society Cancer Facts & Figures 2007 2007, Alanta, GA: American Cancer Society, American Cancer Society.
2. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 2001, 357:539-545. 10.1016/S0140-6736(00)04046-0, 11229684.
3. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002, 420:860-867. 10.1038/nature01322, 12490959.
4. Meylan E, Tschopp J, Karin M. Intracellular pattern recognition receptors in the host response. Nature 2006, 442:39-44. 10.1038/nature04946, 16823444.
5. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006, 441:431-436. 10.1038/nature04870, 16724054.
6. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005, 5:749-759. 10.1038/nri1703, 16175180.
7. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006, 6:24-37. 10.1038/nrc1782, 16397525.
8. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005, 7:211-217. 10.1016/j.ccr.2005.02.013, 15766659.
9. de Visser KE, Coussens LM. The inflammatory tumor microenvironment and its impact on cancer development. Contrib Microbiol 2006, 13:118-137.
10. Coussens LM, Werb Z. Inflammatory cells and cancer: think different!. J Exp Med 2001, 193:F23-F26. 10.1084/jem.193.6.F23, 11257144.
11. Osada T, Clay TM, Woo CY, Morse MA, Lyerly HK. Dendritic cell-based immunotherapy. Int Rev Immunol 2006, 25:377-413. 10.1080/08830180600992456, 17169781.
12. Ghiringhelli F, Apetoh L, Housseau F, Kroemer G, Zitvogel L. Links between innate and cognate tumor immunity. Curr Opin Immunol 2007, 19:224-231. 10.1016/j.coi.2007.02.003, 17303400.
13. David H. Rudolf Virchow and modern aspects of tumor pathology. Pathol Res Pract 1988, 183:356-364.
14. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004, 21:137-148. 10.1016/j.immuni.2004.07.017, 15308095.
15. Boshoff C, Weiss R. AIDS-related malignancies. Nat Rev Cancer 2002, 2:373-382. 10.1038/nrc797, 12044013.
16. Penn I. Posttransplant malignancies. Transplant Proc 1999, 31:1260-1262. 10.1016/S0041-1345(98)01987-3, 10083562.
17. Euvrard S, Kanitakis J, Claudy A. Skin cancers after organ transplantation. N Engl J Med 2003, 348:1681-1691. 10.1056/NEJMra022137, 12711744.
18. Birkeland SA, Storm HH, Lamm LU, Barlow L, Blohme I, Forsberg B, Eklund B, Fjeldborg O, Friedberg M, Frodin L, et al. Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int J Cancer 1995, 60:183-189.
19. Fung JJ, Jain A, Kwak EJ, Kusne S, Dvorchik I, Eghtesad B. De novo malignancies after liver transplantation: a major cause of late death. Liver Transpl 2001, 7(11 Suppl 1):S109-S118. 10.1053/jlts.2001.28645, 11689783.
20. Pham SM, Kormos RL, Landreneau RJ, Kawai A, Gonzalez-Cancel I, Hardesty RL, Hattler BG, Griffith BP. Solid tumors after heart transplantation: lethality of lung cancer. Ann Thorac Surg 1995, 60:1623-1626. 10.1016/0003-4975(95)00120-4, 8787454.
21. Stewart T, Tsai SC, Grayson H, Henderson R, Opelz G. Incidence of de-novo breast cancer in women chronically immunosuppressed after organ transplantation. Lancet 1995, 346:796-798. 10.1016/S0140-6736(95)91618-0, 7674744.
22. Gallagher B, Wang Z, Schymura MJ, Kahn A, Fordyce EJ. Cancer incidence in New York State acquired immunodeficiency syndrome patients. Am J Epidemiol 2001, 154:544-556. 10.1093/aje/154.6.544, 11549560.
23. Oluwole SF, Ali AO, Shafaee Z, DePaz HA. Breast cancer in women with HIV/AIDS: report of five cases with a review of the literature. J Surg Oncol 2005, 89:23-27. 10.1002/jso.20171, 15612013.
24. McHeyzer-Williams MG. B cells as effectors. Curr Opin Immunol 2003, 15:354-361. 10.1016/S0952-7915(03)00046-3, 12787764.
25. Youinou P, Jamin C, Saraux A. B-cell: a logical target for treatment of rheumatoid arthritis. Clin Exp Rheumatol 2007, 25:318-328.
26. Whitford PGW, Cambell AM. Flow cytometric analysis of tumour infiltrating lymphocyte activation and tumour cell MHC class I and II expression in breast cancer patients. Cancer Lett 1992, 61:157-164. 10.1016/0304-3835(92)90174-T, 1730139.
27. Morton BA, Ramey WG, Paderon H, Miller RE. Monoclonal antibody-defined phenotypes of regional lymph node and peripheral blood lymphocyte subpopulations in early breast cancer. Cancer Res 1986, 46(4 Pt 2):2121-2126.
28. Wernicke M. Quantitative morphologic assessment of immunoreactivity in regional lymph nodes of patients with carcinoma of the breast. Surg Gynecol Obstet 1975, 140:919-924.
29. Urdiales-Viedma M, Nogales-Fernandez F, Martos-Padilla S, Sanchez-Cantalejo E. Correlation of histologic grade and lymph node status with some histopathologic discriminants in breast cancer. Tumori 1986, 72:43-51.
30. Shimokawara I, Imamura M, Yamanaka N, Ishii Y, Kikuchi K. Identification of lymphocyte subpopulations in human breast cancer tissue and its significance: an immunoperoxidase study with anti-human T- and B-cell sera. Cancer 1982, 49:1456-1464. 10.1002/1097-0142(19820401)49:7<1456::AID-CNCR2820490724>3.0.CO;2-#, 6277465.
31. Lee AH, Happerfield LC, Bobrow LG, Millis RR. Angiogenesis and inflammation in ductal carcinoma in situ of the breast. J Pathol 1997, 181:200-206. 10.1002/(SICI)1096-9896(199702)181:2<200::AID-PATH726>3.0.CO;2-K, 9120726.
32. Coronella JA, Telleman P, Kingsbury GA, Truong TD, Hays S, Junghans RP. Evidence for an antigen-driven humoral immune response in medullary ductal breast cancer. Cancer Res 2001, 61:7889-7899.
33. Punt CJ, Barbuto JA, Zhang H, Grimes WJ, Hatch KD, Hersh EM. Anti-tumor antibody produced by human tumor-infiltrating and peripheral blood B lymphocytes. Cancer Immunol Immunother 1994, 38:225-232.
34. Coronella-Wood JA, Hersh EM. Naturally occurring B-cell responses to breast cancer. Cancer Immunol Immunother 2003, 52:715-738. 10.1007/s00262-003-0409-4, 12920480.
35. Wang BL, Springer GF, Kaufman MW. Concurrent immunohistochemical staining of tumor-infiltrating lymphocytes and carcinoma-associated T (Thomsen-Friedenreich)/Tn antigens in human breast carcinoma. J Histochem Cytochem 1996, 44:187-191.
36. Jaume JC, Portolano S, Prummel MF, McLachlan SM, Rapoport B. Molecular cloning and characterization of genes for antibodies generated by orbital tissue-infiltrating B-cells in Graves' ophthalmopathy. J Clin Endocrinol Metab 1994, 78:348-352. 10.1210/jc.78.2.348, 8106623.
37. Stott DI, Hiepe F, Hummel M, Steinhauser G, Berek C. Antigen-driven clonal proliferation of B cells within the target tissue of an autoimmune disease. The salivary glands of patients with Sjogren's syndrome. J Clin Invest 1998, 102:938-946. 508959, 9727062.
38. Colombo M, Dono M, Gazzola P, Roncella S, Valetto A, Chiorazzi N, Mancardi GL, Ferrarini M. Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of multiple sclerosis patients. J Immunol 2000, 164:2782-2789.
39. Kim HJ, Krenn V, Steinhauser G, Berek C. Plasma cell development in synovial germinal centers in patients with rheumatoid and reactive arthritis. J Immunol 1999, 162:3053-3062.
40. Tomer Y, Sherer Y, Shoenfeld Y. Autoantibodies, autoimmunity and cancer [review]. Oncol Rep 1998, 5:753-761.
41. Tan EM, Shi FD. Relative paradigms between autoantibodies in lupus and autoantibodies in cancer. Clin Exp Immunol 2003, 134:169-177. 1808856, 14616773, 10.1046/j.1365-2249.2003.02259.x.
42. Disis ML, Pupa SM, Gralow JR, Dittadi R, Menard S, Cheever MA. High-titer HER-2/neu protein-specific antibody can be detected in patients with early-stage breast cancer. J Clin Oncol 1997, 15:3363-3367.
43. Fernandez Madrid F. Autoantibodies in breast cancer sera: candidate biomarkers and reporters of tumorigenesis. Cancer Lett 2005, 230:187-198. 10.1016/j.canlet.2004.12.017, 16297705.
44. Sheikh KM, Quismorio FP, Friou GJ, Lee YT. Ductular carcinoma of the breast: serum antibodies to tumor-associated antigens. Cancer 1979, 44:2083-2089. 10.1002/1097-0142(197912)44:6<2083::AID-CNCR2820440619>3.0.CO;2-E, 92359.
45. Lee YT, Sheikh KM, Quismorio FP, Friou GJ. Circulating anti-tumor and autoantibodies in breast carcinoma: relationship to stage and prognosis. Breast Cancer Res Treat 1985, 6:57-65. 10.1007/BF01806011, 3902126.
46. Wong PY, Staren ED, Tereshkova N, Braun DP. Functional analysis of tumor-infiltrating leukocytes in breast cancer patients. J Surg Res 1998, 76:95-103. 10.1006/jsre.1998.5301, 9695747.
47. Chin Y, Janseens J, Vandepitte J, Vandenbrande J, Opdebeek L, Raus J. Phenotypic analysis of tumor-infiltrating lymphocytes from human breast cancer. Anticancer Res 1992, 12:1463-1466.
48. Aaltomaa S, Lipponen P, Eskelinen M, Kosma VM, Marin S, Alhava E, Syrjanen K. Lymphocyte infiltrates as a prognostic variable in female breast cancer. Eur J Cancer 1992, 28A:859-864. 10.1016/0959-8049(92)90134-N, 1524909.
49. Veronesi U, Paganelli G, Viale G, Luini A, Zurrida S, Galimberti V, Intra M, Veronesi P, Robertson C, Maisonneuve P, et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 2003, 349:546-553. 10.1056/NEJMoa012782, 12904519.
50. Page DL, Jensen RA, Simpson JF. Routinely available indicators of prognosis in breast cancer. Breast Cancer Res Treat 1998, 51:195-208. 10.1023/A:1006122716137, 10068079.
51. Badwe RA, Thorat MA, Parmar VV. Sentinel-node biopsy in breast cancer. N Engl J Med 2003, 349:1968-1971. author reply 1968-1971, 10.1056/NEJM200311133492017, 14614174.
52. Kohrt HE, Nouri N, Nowels K, Johnson D, Holmes S, Lee PP. Profile of immune cells in axillary lymph nodes predicts disease-free survival in breast cancer. PLoS Med 2005, 2:e284. 1198041, 16124834, 10.1371/journal.pmed.0020284.
53. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages 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. 10.1126/science.1129139, 17008531.
54. Naito Y, Saito K, Shiiba K, Ohuchi A, Saigenji K, Nagura H, Ohtani H. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res 1998, 58:3491-3494.
55. Moss RB, Moll T, El-Kalay M, Kohne C, Soo Hoo W, Encinas J, Carlo DJ. Th1/Th2 cells in inflammatory disease states: therapeutic implications. Expert Opin Biol Ther 2004, 4:1887-1896. 10.1517/14712598.4.12.1887, 15571451.
56. Munk ME, Emoto M. Functions of T-cell subsets and cytokines in mycobacterial infections. Eur Respir J Suppl 1995, 20:668s-675s.
57. Romagnani S. The Th1/Th2 paradigm. Immunol Today 1997, 18:263-266. 10.1016/S0167-5699(97)80019-9, 9190109.
58. Stout RD, Bottomly K. Antigen-specific activation of effector macrophages by IFN-gamma producing (TH1) T cell clones. Failure of IL-4-producing (TH2) T cell clones to activate effector function in macrophages. J Immunol 1989, 142:760-765.
59. Parker DC. T cell-dependent B cell activation. Annu Rev Immunol 1993, 11:331-360.
60. Kacha AK, Fallarino F, Markiewicz MA, Gajewski TF. Cutting edge: spontaneous rejection of poorly immunogenic P1.HTR tumors by Stat6-deficient mice. J Immunol 2000, 165:6024-6028.
61. Fallarino F, Gajewski TF. Cutting edge: differentiation of antitumor CTL in vivo requires host expression of Stat1. J Immunol 1999, 163:4109-4113.
62. Lowes MA, Bishop GA, Crotty K, Barnetson RS, Halliday GM. T helper 1 cytokine mRNA is increased in spontaneously regressing primary melanomas. J Invest Dermatol 1997, 108:914-919. 10.1111/1523-1747.ep12292705, 9182821.
63. Tsung K, Meko JB, Peplinski GR, Tsung YL, Norton JA. IL-12 induces T helper 1-directed antitumor response. J Immunol 1997, 158:3359-3365.
64. Hu HM, Urba WJ, Fox BA. Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from a type 2 to a type 1 cytokine profile. J Immunol 1998, 161:3033-3041.
65. Pellegrini P, Berghella AM, Del Beato T, Cicia S, Adorno D, Casciani CU. Disregulation in TH1 and TH2 subsets of CD4+ T cells in peripheral blood of colorectal cancer patients and involvement in cancer establishment and progression. Cancer Immunol Immunother 1996, 42:1-8. 10.1007/s002620050244, 8625361.
66. Ostrand-Rosenberg S, Grusby MJ, Clements VK. Cutting edge: STAT6-deficient mice have enhanced tumor immunity to primary and metastatic mammary carcinoma. J Immunol 2000, 165:6015-6019.
67. Kobayashi M, Kobayashi H, Pollard RB, Suzuki F. A pathogenic role of Th2 cells and their cytokine products on the pulmonary metastasis of murine B16 melanoma. J Immunol 1998, 160:5869-5873.
68. Tan TT, Coussens LM. Humoral immunity, inflammation and cancer. Curr Opin Immunol 2007, 19:209-216. 10.1016/j.coi.2007.01.001, 17276050.
69. Johansson M, Tan T, de Visser KE, Coussens LM. Immune cells as anti-cancer therapeutic targets and tools. J Cell Biochem 2007, 101:918-926. 10.1002/jcb.21230, 17265430.
70. Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, Harris AL, Banham AH. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 2006, 24:5373-5380. 10.1200/JCO.2006.05.9584, 17135638.
71. Azuma T, Takahashi T, Kunisato A, Kitamura T, Hirai H. Human CD4+ CD25+ regulatory T cells suppress NKT cell functions. Cancer Res 2003, 63:4516-4520.
72. Lim HW, Hillsamer P, Banham AH, Kim CH. Cutting edge: direct suppression of B cells by CD4+ CD25+ regulatory T cells. J Immunol 2005, 175:4180-4183.
73. Trzonkowski P, Szmit E, Mysliwska J, Dobyszuk A, Mysliwski A. CD4+CD25+ T regulatory cells inhibit cytotoxic activity of T CD8+ and NK lymphocytes in the direct cell-to-cell interaction. Clin Immunol 2004, 112:258-267. 10.1016/j.clim.2004.04.003, 15308119.
74. Romagnani C, Della Chiesa M, Kohler S, Moewes B, Radbruch A, Moretta L, Moretta A, Thiel A. Activation of human NK cells by plasmacytoid dendritic cells and its modulation by CD4+ T helper cells and CD4+ CD25hi T regulatory cells. Eur J Immunol 2005, 35:2452-2458. 10.1002/eji.200526069, 15997468.
75. Chen W. Dendritic cells and (CD4+)CD25+ T regulatory cells: crosstalk between two professionals in immunity versus tolerance. Front Biosci 2006, 11:1360-1370. 10.2741/1889, 16368522.
76. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004, 10:942-949. 10.1038/nm1093, 15322536.
77. Ellner JJ. Suppressor cells of man. Clin Immunol Rev 1981, 1:119-214.
78. Columba-Cabezas S, Serafini B, Ambrosini E, Sanchez M, Penna G, Adorini L, Aloisi F. Induction of macrophage-derived chemokine/CCL22 expression in experimental autoimmune encephalomyelitis and cultured microglia: implications for disease regulation. J Neuroimmunol 2002, 130:10-21. 10.1016/S0165-5728(02)00170-4, 12225884.
79. Goodwin JS, Ceuppens J. Regulation of the immune response by prostaglandins. J Clin Immunol 1983, 3:295-315. 10.1007/BF00915791, 6140268.
80. Ribatti D, Ennas MG, Vacca A, Ferreli F, Nico B, Orru S, Sirigu P. Tumor vascularity and tryptase-positive mast cells correlate with a poor prognosis in melanoma. Eur J Clin Invest 2003, 33:420-425. 10.1046/j.1365-2362.2003.01152.x, 12760367.
81. Esposito I, Menicagli M, Funel N, Bergmann F, Boggi U, Mosca F, Bevilacqua G, Campani D. Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma. J Clin Pathol 2004, 57:630-636. 1770337, 15166270, 10.1136/jcp.2003.014498.
82. Yano H, Kinuta M, Tateishi H, Nakano Y, Matsui S, Monden T, Okamura J, Sakai M, Okamoto S. Mast cell infiltration around gastric cancer cells correlates with tumor angiogenesis and metastasis. Gastric Cancer 1999, 2:26-32. 10.1007/s101200050017, 11957067.
83. Sparmann A, Bar-Sagi D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 2004, 6:447-458. 10.1016/j.ccr.2004.09.028, 15542429.
84. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, Werb Z, Caughey GH, Hanahan D. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 1999, 13:1382-1397. 316772, 10364156.
85. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005, 7:411-423. 10.1016/j.ccr.2005.04.014, 15894262.
86. Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 2001, 193:727-740. 10.1084/jem.193.6.727, 11257139.
87. Lin EY, Pollard JW. Macrophages: modulators of breast cancer progression. Novartis Found Symp 2004, 256:158-168. discussion 168-172, 259-269.
88. Imada A, Shijubo N, Kojima H, Abe S. Mast cells correlate with angiogenesis and poor outcome in stage I lung adenocarcinoma. Eur Respir J 2000, 15:1087-1093. 10.1034/j.1399-3003.2000.01517.x, 10885428.
89. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 2002, 196:254-265. 10.1002/path.1027, 11857487.
90. Benitez-Bribiesca L, Wong A, Utrera D, Castellanos E. The role of mast cell tryptase in neoangiogenesis of premalignant and malignant lesions of the uterine cervix. J Histochem Cytochem 2001, 49:1061-1062.
91. Snell GD. Incompatibility reactions to tumor homotransplants with particular reference to the role of the tumor; a review. Cancer Res 1957, 17:2-10.
92. Kaliss N. Immunological enhancement of tumor homografts in mice: a review. Cancer Res 1958, 18:992-1003.
93. Agassy-Cahalon L, Yaakubowicz M, Witz IP, Smorodinsky NI. The immune system during the precancer period: naturally-occurring tumor reactive monoclonal antibodies and urethane carcinogenesis. Immunol Lett 1988, 18:181-189. 10.1016/0165-2478(88)90017-X, 3169848.
94. Siegel CT, Schreiber K, Meredith SC, Beck-Engeser GB, Lancki DW, Lazarski CA, Fu YX, Rowley DA, Schreiber H. Enhanced growth of primary tumors in cancer-prone mice after immunization against the mutant region of an inherited oncoprotein. J Exp Med 2000, 191:1945-1956. 10.1084/jem.191.11.1945, 10839809.
95. Schreiber H, Wu TH, Nachman J, Rowley DA. Immunological enhancement of primary tumor development and its prevention. Semin Cancer Biol 2000, 10:351-357. 10.1006/scbi.2000.0331, 11100883.
96. Barbera-Guillem E, Nyhus JK, Wolford CC, Friece CR, Sampsel JW. Vascular endothelial growth factor secretion by tumor-infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune complexes potentiate the process. Cancer Res 2002, 62:7042-7049.
97. Barbera-Guillem E, May KF, Nyhus JK, Nelson MB. Promotion of tumor invasion by cooperation of granulocytes and macrophages activated by anti-tumor antibodies. Neoplasia 1999, 1:453-460. 1508114, 10933061, 10.1038/sj.neo.7900054.
98. Hogarth PM. Fc receptors are major mediators of antibody based inflammation in autoimmunity. Curr Opin Immunol 2002, 14:798-802. 10.1016/S0952-7915(02)00409-0, 12413532.
99. Ravetch JV, Bolland S. IgG Fc receptors. Annu Rev Immunol 2001, 19:275-290. 10.1146/annurev.immunol.19.1.275, 11244038.
100. Maglione JE, Moghanaki D, Young LJ, Manner CK, Ellies LG, Joseph SO, Nicholson B, Cardiff RD, MacLeod CL. Transgenic Polyoma middle-T mice model premalignant mammary disease. Cancer Res 2001, 61:8298-8305.
101. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, Qian H, Xue XN, Pollard JW. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006, 66:11238-11246. 10.1158/0008-5472.CAN-06-1278, 17114237.
102. Society AC. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004, 4:71-78. 10.1038/nrc1256, 14708027.
103. Hayakawa Y, Takeda K, Yagita H, Smyth MJ, Van Kaer L, Okumura K, Saiki I. IFN-gamma-mediated inhibition of tumor angiogenesis by natural killer T-cell ligand, alpha-galactosylceramide. Blood 2002, 100:1728-1733.
104. Smyth MJ, Crowe NY, Godfrey DI. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 2001, 13:459-463. 10.1093/intimm/13.4.459, 11282985.
105. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005, 5:263-274. 10.1038/nrc1586, 15776005.
106. Finke J, Ferrone S, Frey A, Mufson A, Ochoa A. Where have all the T cells gone? Mechanisms of immune evasion by tumors. Immunol Today 1999, 20:158-160. 10.1016/S0167-5699(98)01435-2, 10203710.
107. Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 2001, 166:678-689.
108. Serafini P, De Santo C, Marigo I, Cingarlini S, Dolcetti L, Gallina G, Zanovello P, Bronte V. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol Immunother 2004, 53:64-72. 10.1007/s00262-003-0443-2, 14593498.
109. Gabrilovich DI, Velders MP, Sotomayor EM, Kast WM. Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J Immunol 2001, 166:5398-5406.
110. Yang L, Debusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004, 6:409-421. 10.1016/j.ccr.2004.08.031, 15488763.
111. Pistoia V, Corcione A. Relationships between B cell cytokine production in secondary lymphoid follicles and apoptosis of germinal center B lymphocytes. Stem Cells 1995, 13:487-500.
112. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002, 23:549-555. 10.1016/S1471-4906(02)02302-5, 12401408.
113. Mantovani A, Allavena P, Sica A. Tumour-associated macrophages as a prototypic type II polarised phagocyte population: role in tumour progression. Eur J Cancer 2004, 40:1660-1667. 10.1016/j.ejca.2004.03.016, 15251154.