Immune consequences of protracted host-tumor interactions in a transgenic mouse model of mammary carcinoma

Cancer Investigation

Volumn 26, Issue 3, 2008, Pages 237-249

  Stewart, Trina J ^a   Lutsiak, M E Christine ^a   Abrams, Scott I ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Host tumor interactions; Immune suppression; Immunobiology; Inflammatory mediators; Mammary carcinoma tumor model; MMTV PyMT; Transgenic

Indexed keywords

MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BREAST CARCINOMA; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNE SYSTEM; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; TUMOR GROWTH;

ANIMALS; CELL PROLIFERATION; CYTOKINES; DISEASE PROGRESSION; FEMALE; FLOW CYTOMETRY; LYMPH NODES; LYMPHOCYTES, TUMOR-INFILTRATING; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, TRANSGENIC; SPLEEN; T-LYMPHOCYTES;

EID: 40149092963     PISSN: 07357907     EISSN: 15324192     Source Type: Journal    
DOI: 10.1080/07357900701708419     Document Type: Article

References (71)

1. Ben-Baruch, A. Host microenvironment in breast cancer development: inflammatory cells, cytokines and chemokines in breast cancer progression: reciprocal tumor-microenvironment interactions. Breast Cancer Res. 2003, 5, 31-36.
2. Shekhar, M.P.; Pauley, R.; Heppner, G. Host microenvironment in breast cancer development: extracellular matrix-stromal cell contribution to neoplastic phenotype of epithelial cells in the breast. Breast Cancer Res. 2003, 5, 130-135.
3. Ostrand-Rosenberg, S. Animal models of tumor immunity, immunotherapy and cancer vaccines. Curr. Opin. Immunol. 2004, 16(2), 143-150.
4. Gendler, S.J.; Mukherjee, P. Spontaneous adenocarcinoma mouse models for immunotherapy. Trends Mol. Med. 2001, 7(10), 471-475.
5. Guy, C.T.; Cardiff, R.D.; Muller, W.J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell Biol. 1992, 12(3), 954-961.
6. Lin, E.Y.; Jones, J.G.; Li, P.; Zhu, L.; Whitney, K.D.; Muller, W.J.; Pollard, J.W. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 2003, 163(5), 2113-2126.
7. Basu, G.D.; Pathangey, L.B.; Tinder, T.L.; Lagioia, M.; Gendler, S.J.; Mukherjee, P. Cyclooxygenase-2 inhibitor induces apoptosis in breast cancer cells in an in vivo model of spontaneous metastatic breast cancer. Mol. Cancer Res. 2004, 2(11), 632-642.
8. Mukherjee, P.; Madsen, C.S.; Ginardi, A.R.; Tinder, T.L.; Jacobs, F.; Parker, J.; Agrawal B.; Longenecker, B.M.; Gendler, S.J. Mucin 1-specific immunotherapy in a mouse model of spontaneous breast cancer. J. Immunother. 2003, 26(1), 47-62.
9. Knutson, K.L.; Dang, Y.; Lu, H.; Lukas, J.; Almand, B.; Gad, E.; Azeke, E.; Disis, M.L. IL-2 immunotoxin therapy modulates tumor-associated regulatory T cells and leads to lasting immune-mediated rejection of breast cancers in neu-transgenic mice. J. Immunol. 2006, 177(1), 84-91.
10. Pannellini, T.; Forni, G.; Musiani, P. Immunobiology of her-2/neu transgenic mice. Breast Dis. 2004, 20, 33-42.
11. Reilly, R.T.; Machiels, J.P.; Emens, L.A.; Ercolini, A.M.; Okoye, F.I.; Lei, R.Y.; Weintraub, D.; Jaffee, E.M. The collaboration of both humoral and cellular HER-2/neu-targeted immune responses is required for the complete eradication of HER-2/neu-expressing tumors. Cancer Res. 2001, 61(3), 880-883.
12. Sakai, Y.; Morrison, B.J.; Burke, J.D.; Park, J.M.; Terabe, M.; Janik, J.E.; Forni, G.; Berzofsky, J.A.; Morris, J.C. Vaccination by genetically modified dendritic cells expressing a truncated neu oncogene prevents development of breast cancer in transgenic mice. Cancer Res. 2004, 64(21), 8022-8028.
13. Astolfi, A.; Rolla, S.; Nanni, P.; Quaglino, E.; De Giovanni C.; Iezzi, M.; Musiani, P.; Forni, G.; Lollini, P.L.; Cavallo, F.; Calogero, R.A. Immune prevention of mammary carcinogenesis in HER-2/neu transgenic mice: a microarray scenario. Cancer Immunol. Immunother. 2005, 54(6), 599-610.
14. Ellies, L.G.; Fishman, M.; Hardison, J.; Kleeman, J.; Maglione, J.E.; Manner, C.K.; Cardiff, R.D.; MacLeod, C.L. Mammary tumor latency is increased in mice lacking the inducible nitric oxide synthase. Int. J. Cancer. 2003, 106(1), 1-7.
15. Knutson, K.L.; Lu, H.; Stone, B.; Reiman, J.M.; Behrens, M.D.; Prosperi, C.M.; Gad, E.A.; Smorlesi, A.; Disis, M.L. Immunoediting of cancers may lead to epithelial to mesenchymal transition. J. Immunol. 2006, 177(3), 1526-1533.
16. Niemeyer, C.C.; Spencer-Dene, B.; Wu, J.X.; Adamson, E.D. Preneoplastic mammary tumor markers: Cripto and Amphiregulin are overexpressed in hyperplastic stages of tumor progression in transgenic mice. Int. J. Cancer 1999, 81(4), 588-591.
17. Qiu, T.H.; Chandramouli, G.V.; Hunter, K.W.; Alkharouf, N.W.; Green, J.E.; Liu, E.T. Global expression profiling identifies signatures of tumor virulence in MMTV-PyMT-transgenic mice: correlation to human disease. Cancer Res. 2004, 64(17), 5973-5981.
18. Degl'Innocenti, E.; Grioni, M.; Boni, A.; Camporeale, A.; Bertilaccio, M.T.; Freschi, M.; Monno, A.; Arcelloni, C.; Greenberg, N.M.; Bellone, M. Peripheral T cell tolerance occurs early during spontaneous prostate cancer development and can be rescued by dendritic cell immunization. Eur. J. Immunol. 2005, 35(1), 66-75.
19. Otahal, P.; Schell, T.D.; Hutchinson, S.C.; Knowles, B.B.; Tevethia, S.S. Early immunization induces persistent tumor-infiltrating CD8+ T cells against an immunodominant epitope and promotes lifelong control of pancreatic tumor progression in SV40 tumor antigen transgenic mice. J. Immunol. 2006, 177(5), 3089-3099.
20. Park, J.M.; Terabe, M.; Sakai, Y.; Munasinghe, J.; Forni, G.; Morris, J.C.; Berzofsky, J.A. Early role of CD4+ Th1 cells and antibodies in HER-2 adenovirus vaccine protection against autochthonous mammary carcinomas. J. Immunol. 2005, 174(7), 4228-4236.
21. Rowse, G.J.; Tempero, R.M.; M.L. VanLith; Hollingsworth, M.A.; Gendler, S.J. Tolerance and immunity to MUC1 in a human MUC1 transgenic murine model. Cancer Res. 1998, 58(2), 315-321.
22. Leek, R.D.; Harris, A.L. Tumor-associated macrophages in breast cancer. J. Mammary Gland Biol. Neoplasia. 2002, 7(2), 177-189.
23. Luo, Y.; Zhou, H.; Krueger, J.; Kaplan, C.; Lee, S.H.; Dolman, C.; Markowitz, D.; Wu, W.; Liu, C.; Reisfeld, R.A.; Xiang, R. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J. Clin. Invest. 2006, 116(8), 2132-2141.
24. Melani, C.; Chiodoni, C.; Forni, G.; Colombo, M.P. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood. 2003, 102(6), 2138-2145.
25. Sinha, P.; Clements, V.K.; Miller, S.; Ostrand-Rosenberg, S. Tumor immunity: a balancing act between T cell activation, macrophage activation and tumor-induced immune suppression. Cancer Immunol. Immunother. 2005, 54(11), 1137-1142.
26. Molling, J.W.; Kolgen, W.; van der Vliet, H.J.; Boomsma, M.F.; Kruizenga, H.; Smorenburg, C.H.; Molenkamp, B.G.; Langendijk, J.A.; Leemans, C.R.; von Blomberg, B.M.; Scheper, R.J.; van den Eertwegh, A.J. Peripheral blood IFN-gamma-secreting Valpha24+Vbeta11+ NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int. J. Cancer. 2005, 116(1), 87-93.
27. Terabe, M.; Swann, J.; Ambrosino, E.; Sinha, P.; Takaku, S.; Hayakawa, Y.; Godfrey, D.I.; Ostrand-Rosenberg, S.; Smyth, M.J.; Berzofsky, J.A. A nonclassical non-Valpha14Jalpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J. Exp. Med. 2005, 202(12), 1627-1633.
28. Hueman, M.T.; Stojadinovic, A.; Storrer, C.E.; Foley, R.J.; Gurney, J.M.; Shriver, C.D.; Ponniah, S.; Peoples, G.E. Levels of circulating regulatory CD4(+)CD25 (+) T cells are decreased in breast cancer patients after vaccination with a HER2/neu peptide (E75) and GM-CSF vaccine(bigstar). Breast Cancer Res Treat. 2006, 98(1), 17-29.
29. 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. 2002, 169(5), 2756-2761.
30. Okita, R.; Saeki, T.; Takashima, S.; Yamaguchi, Y.; Toge, T. CD4+CD25+ regulatory T cells in the peripheral blood of patients with breast cancer and non-small cell lung cancer. Oncol. Rep. 2005, 14(5), 1269-1273.
31. Jackson, J.R.; Seed, M.P.; Kircher, C.H.; Willoughby, D.A.; Winkler, J.D. The codependence of angiogenesis and chronic inflammation. Faseb. J. 1997, 11(6), 457-465.
32. Speiser, D.E.; Miranda, R.; Zakarian, A.; Bachmann, M.F.; McKall-Faienza, K.; Odermatt, B.; Hanahan, D.; Zinkernagel, R.M.; Ohashi, P.S. Self antigens expressed by solid tumors Do not efficiently stimulate naive or activated T cells: implications for immunotherapy. J. Exp. Med. 1997, 186(5), 645-653.
33. Stewart, T.J.; Greeneltch, K.M.; Lutsiak, M.E.; Abrams, S.I. Immunological responses can have both pro- and antitumour effects: implications for immunotherapy. Expert Rev. Mol. Med. 2007, 9(4), 1-20.
34. Ueno, T.; Toi, M.; Saji, H.; Muta, M.; Bando, H.; Kuroi, K.; Koike, M.; Inadera, H.; Matsushima, K. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin. Cancer Res. 2000, 6(8), 3282-3289.
35. Lebrecht, A.; Grimm, C.; Lantzsch, T.; Ludwig, E.; Hefler, L.; Ulbrich, E.; Koelbl, H. Monocyte chemoattractant protein-1 serum levels in patients with breast cancer. Tumour Biol. 2004, 25(1-2), 14-17.
36. Fuentes, M.E.; Durham, S.K.; Swerdel, M.R.; Lewin, A.C.; Barton, D.S.; Megill, J.R.; Bravo, R.; Lira, S.A. Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J. Immunol. 1995, 155(12), 5769-5776.
37. Lu, B.; Rutledge, B.J.; Gu, L.; Fiorillo, J.; Lukacs, N.W.; Kunkel, S.L.; North, R.; Gerard, C.; Rollins, B.J. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J. Exp. Med. 1998, 187(4), 601-608.
38. Zhang, L.; Khayat, A.; Cheng, H.; Graves, D.T. The pattern of monocyte recruitment in tumors is modulated by MCP-1 expression and influences the rate of tumor growth. Lab. Invest. 1997, 76(4), 579-590.
39. Burke, F.; Relf, M.; Negus, R.; Balkwill, F. A cytokine profile of normal and malignant ovary. Cytokine. 1996, 8(7), 578-585.
40. Naylor, M.S.; Stamp, G.W.; Foulkes, W.D.; Eccles, D.; Balkwill, F.R. Tumor necrosis factor and its receptors in human ovarian cancer. Potential role in disease progression. J. Clin. Invest. 1993, 91(5), 2194-2206.
41. Leek, R.D.; Landers, R.; Fox, S.B.; Ng, F.; Harris, A.L.; Lewis, C.E. Association of tumour necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma. Br. J. Cancer. 1998, 77(12), 2246-2251.
42. Malik, S.T.; Griffin, D.B.; Fiers, W.; Balkwill, F.R. Paradoxical effects of tumour necrosis factor in experimental ovarian cancer. Int. J. Cancer. 1989, 44(5), 918-925.
43. Malik, S.T.; Naylor, M.S.; East, N.; Oliff, A.; Balkwill, F.R. Cells secreting tumour necrosis factor show enhanced metastasis in nude mice. Eur. J. Cancer. 1990, 26(10), 1031-1034.
44. Moore, R.J.; Owens, D.M.; Stamp, G.; Arnott, C.; Burke, F.; East, N.; Holdsworth, H.; Turner, L.; Rollins, B.; Pasparakis, M.; Kollias, G.; Balkwill, F. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat. Med. 1999, 5(7), 828-831.
45. Negus, R.P.; Stamp, G.W.; Hadley, J.; Balkwill, F.R. Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C-C chemokines. Am. J. Pathol. 1997, 150(5), 1723-1734.
46. Warzocha, K.; Salles, G.; Bienvenu, J.; Bastion, Y.; Dumontet, C.; Renard, N.; Neidhardt-Berard, E.M.; Coiffier, B. Tumor necrosis factor ligand-receptor system can predict treatment outcome in lymphoma patients. J. Clin. Oncol. 1997, 15(2), 499-508.
47. Chen, D.; Xia, J.; Tanaka, Y.; Chen, H.; Koido, S.; Wernet, O.; Mukherjee, P.; Gendler, S.J.; Kufe, D.; Gong, J. Immunotherapy of spontaneous mammary carcinoma with fusions of dendritic cells and mucin 1-positive carcinoma cells. Immunology. 2003, 109(2), 300-307.
48. Lin, E.Y.; Pollard, J.W. Macrophages: modulators of breast cancer progression. Novartis Found Symp. 2004, 256, 158-168; discussion 168-172, 259-169.
49. Heys, S.D.; Eremin, O. The relevance of tumor draining lymph nodes in cancer. Surg. Gynecol. Obstet. 1992, 174(6), 533-540.
50. Lores, B.; Garcia-Estevez, J.M.; Arias, C. Lymph nodes and human tumors (review). Int. J. Mol. Med. 1998, 1(4), 729-733.
51. Bronte, V.; Serafini, P.; Apolloni, E.; Zanovello, P. Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J. Immunother. 2001, 24(6), 431-446.
52. Sinha, P.; Clements, V.K.; Ostrand-Rosenberg, S. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J. Immunol. 2005, 174(2), 636-645.
53. Kay, N.E.; Leong, T.L.; Bone, N.; Vesole, D.H.; Greipp, P.R.; Van Ness, B.; Oken, M.M.; Kyle, R.A. Blood levels of immune cells predict survival in myeloma patients: results of an Eastern Cooperative Oncology Group phase 3 trial for newly diagnosed multiple myeloma patients. Blood. 2001, 98(1), 23-28.
54. Kuss, I.; Hathaway, B.; Ferris, R.L.; Gooding, W.; Whiteside, T.L. Decreased absolute counts of T lymphocyte subsets and their relation to disease in squamous cell carcinoma of the head and neck. Clin. Cancer Res. 2004, 10(11), 3755-3762.
55. Stewart, T.J.; Abrams, S.I. Altered immune function during long-term Host-Tumor interactions can be modulated to retard autochthonous neoplastic growth. J. Immunol. 2007, 179(5), 2851-2859.
56. Baecher-Allan, C.; Anderson, D.E. Immune regulation in tumor-bearing hosts. Curr. Opin. Immunol. 2006, 18(2), 214-219.
57. Leong, P.P.; Mohammad, R.; Ibrahim, N.; Ithnin, H.; Abdullah, M.; Davis, W.C.; Seow, H.F. Phenotyping of lymphocytes expressing regulatory and effector markers in infiltrating ductal carcinoma of the breast. Immunol. Lett. 2006, 102(2), 229-236.
58. Ambrosino, E.; Spadaro, M.; Iezzi, M.; Curcio, C.; Forni, G.; Musiani, P.; Wei, W.Z.; Cavallo, F. Immunosurveillance of Erbb2 carcinogenesis in transgenic mice is concealed by a dominant regulatory T-cell self-tolerance. Cancer Res. 2006, 66(15), 7734-7740.
59. Yang, L.; DeBusk, L.M.; Fukuda, K.; Fingleton, B.; Green-Jarvis, B.; Shyr, Y.; Matrisian, L.M.; Carbone, D.P.; Lin, P.C. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 2004, 6(4), 409-421.
60. 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(2), 64-72.
61. Serafini, P.; Borrello, I.; Bronte, V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin. Cancer Biol. 2006, 16(1), 53-65.
62. Balkwill, F.; Mantovani, A. Inflammation and cancer: back to Virchow? Lancet. 2001, 357(9255), 539-545.
63. Neumark, E.; Sagi-Assif, O.; Shalmon, B.; Ben-Baruch, A.; Witz, I.P. Progression of mouse mammary tumors: MCP-1-TNFalpha cross-regulatory pathway and clonal expression of promalignancy and antimalignancy factors. Int. J. Cancer. 2003, 106(6), 879-886.
64. Bachelot, T.; Ray-Coquard, I.; Menetrier-Caux, C.; Rastkha, M.; Duc, A.; Blay, J.Y. Prognostic value of serum levels of interleukin 6 and of serum and plasma levels of vascular endothelial growth factor in hormone-refractory metastatic breast cancer patients. Br. J. Cancer. 2003, 88(11), 1721-1726.
65. Dehqanzada, Z.A.; Storrer, C.E.; Hueman, M.T.; Foley, R.J.; Harris, K.A.; Jama, Y.H.; Kao, T.C.; Shriver, C.D.; Ponniah, S.; Peoples, G.E. Correlations between serum monocyte chemotactic protein-1 levels, clinical prognostic factors, and HER-2/neu vaccine-related immunity in breast cancer patients. Clin. Cancer Res. 2006, 12(2), 478-486.
66. Sheen-Chen, S.M.; Chen, W.J.; Eng, H.L.; Chou, F.F. Serum concentration of tumor necrosis factor in patients with breast cancer. Breast Cancer Res. Treat. 1997, 43(3), 211-215.
67. Saji, H.; Koike, M.; Yamori, T.; Saji, S.; Seiki, M.; Matsushima, K.; Toi, M. Significant correlation of monocyte chemoattractant protein-1 expression with neovascularization and progression of breast carcinoma. Cancer. 2001, 92(5), 1085-1091.
68. Peng, L.; Shu, S.; Krauss, J.C. Monocyte chemoattractant protein inhibits the generation of tumor-reactive T cells. Cancer Res. 1997, 57(21), 4849-4854.
69. Gu, L.; Tseng, S.; Horner, R.M.; Tam, C.; Loda, M.; Rollins, B.J. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature. 2000, 404(6776), 407-411.
70. Rutledge, B.J.; Rayburn, H.; Rosenberg, R.; North, R.J.; Gladue, R.P.; Corless, C.L.; Rollins, B.J. High level monocyte chemoattractant protein-1 expression in transgenic mice increases their susceptibility to intracellular pathogens. J. Immunol. 1995, 155(10), 4838-4843.
71. Amann, B.; Perabo, F.G.; Wirger, A.; Hugenschmidt, H.; Schultze-Seemann, W. Urinary levels of monocyte chemo-attractant protein-1 correlate with tumour stage and grade in patients with bladder cancer. Br. J. Urol. 1998, 82(1), 118-121.