The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance

Immunological Reviews

Volumn 222, Issue 1, 2008, Pages 155-161

  Allavena, Paola ^a   Sica, Antonio ^a   Garlanda, Cecilia ^a   Mantovani, Alberto ^a,b  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Cancer; Inflammation; Macrophages; Surveillance; Tumor promotion

Indexed keywords

SEX HORMONE;

ADAPTIVE IMMUNITY; ANGIOGENESIS; CARCINOGENESIS; HUMAN; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; MACROPHAGE; METASTASIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; DISEASE PROGRESSION; FEMALE; GONADAL STEROID HORMONES; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC SURVEILLANCE; INFLAMMATION; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MATRIX METALLOPROTEINASES; MICE; MYELOID CELLS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PHAGOCYTOSIS; RATS; SIGNAL TRANSDUCTION; TUMOR ESCAPE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 41149164902     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2008.00607.x     Document Type: Review

References (60)

1. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005 7 : 211 217.
2. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001 357 : 539 545.
3. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002 420 : 860 867.
4. Mantovani A, Balkwill F. RalB signaling: a bridge between inflammation and cancer. Cell 2006 127 : 42 44.
5. 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.
6. Paik S, et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004 351 : 2817 2826.
7. Bunt SK, Yang L, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res 2007 67 : 10019 10026.
8. Nagaraj S, Gabrilovich DI. Myeloid-derived suppressor cells. Adv Exp Med Biol 2007 601 : 213 223.
9. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007 117 : 1155 1166.
10. Crowther M, Brown NJ, Bishop ET, Lewis CE. Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J Leukoc Biol 2001 70 : 478 490.
11. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996 86 : 353 364.
12. Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med 2007 13 : 1211 1218.
13. Salcedo R, et al. Vascular endothelial growth factor and basic fibroblast growth factor induce expression of CXCR4 on human endothelial cells: in vivo neovascularization induced by stromal-derived factor-1alpha. Am J Pathol 1999 154 : 1125 1135.
14. Cursiefen C, et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 2004 113 : 1040 1050.
15. Schioppa T, et al. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 2003 198 : 1391 1402.
16. Schoppmann SF, et al. Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 2002 161 : 947 956.
17. Hotchkiss KA, Ashton AW, Klein RS, Lenzi ML, Zhu GH, Schwartz EL. Mechanisms by which tumor cells and monocytes expressing the angiogenic factor thymidine phosphorylase mediate human endothelial cell migration. Cancer Res 2003 63 : 527 533.
18. Azenshtein E, et al. The CC chemokine RANTES in breast carcinoma progression: regulation of expression and potential mechanisms of promalignant activity. Cancer Res 2002 62 : 1093 1102.
19. Ueno T, et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res 2000 6 : 3282 3289.
20. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004 25 : 280 288.
21. Grohmann U, Fallarino F, Puccetti P. Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol 2003 24 : 242 248.
22. Bronte V, Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 2005 5 : 641 654.
23. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med 2005 11 : 312 319.
24. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003 3 : 23 35.
25. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004 25 : 677 686.
26. Mantovani A. Cancer: inflammation by remote control. Nature 2005 435 : 752 753.
27. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol 2002 2 : 725 734.
28. Moore RJ, et al. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med 1999 5 : 828 831.
29. Hagemann T, Robinson SC, Schulz M, Trumper L, Balkwill FR, Binder C. Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-alpha dependent up-regulation of matrix metalloproteases. Carcinogenesis 2004 25 : 1543 1549.
30. Pollard JW. Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 2004 4 : 71 78.
31. Giavazzi R, et al. Interleukin 1-induced augmentation of experimental metastases from a human melanoma in nude mice. Cancer Res 1990 50 : 4771 4775.
32. 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.
33. Hiratsuka S, et al. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002 2 : 289 300.
34. Lin EY, et al. 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 : 2113 2126.
35. Browatzki M, Pfeiffer CA, Schmidt J, Kranzhofer R. Endothelin-1 induces CD40 but not IL-6 in human monocytes via the proinflammatory transcription factor NF-kappaB. Eur J Med Res 2005 10 : 197 201.
36. Spinella F, Rosano L, Di Castro V, Natali PG, Bagnato A. Endothelin-1 induces vascular endothelial growth factor by increasing hypoxia-inducible factor-1alpha in ovarian carcinoma cells. J Biol Chem 2002 277 : 27850 27855.
37. Leek RD, Harris AL. Tumor-associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia 2002 7 : 177 189.
38. O'Sullivan C, Lewis CE. Tumour-associated leucocytes: friends or foes in breast carcinoma. J Pathol 1994 172 : 229 235.
39. Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW. The macrophage growth factor CSF-1 in mammary gland development and tumor progression. J Mammary Gland Biol Neoplasia 2002 7 : 147 162.
40. Ishikawa S, et al. Identification of genes related to invasion and metastasis in pancreatic cancer by cDNA representational difference analysis. J Exp Clin Cancer Res 2003 22 : 299 306.
41. Eubank TD, Galloway M, Montague CM, Waldman WJ, Marsh CB. M-CSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J Immunol 2003 171 : 2637 2643.
42. Hildenbrand R, Dilger I, Horlin A, Stutte HJ. Urokinase and macrophages in tumour angiogenesis. Br J Cancer 1995 72 : 818 823.
43. Ahmed F, et al. GFP expression in the mammary gland for imaging of mammary tumor cells in transgenic mice. Cancer Res 2002 62 : 7166 7169.
44. Goswami S, et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res 2005 65 : 5278 5283.
45. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005 7 : 411 423.
46. Mantovani A. Cancer: an infernal triangle. Nature 2007 448 : 547 548.
47. Zhu P, et al. Macrophage/cancer cell interactions mediate hormone resistance by a nuclear receptor derepression pathway. Cell 2006 124 : 615 629.
48. Naugler WE, et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent-IL-6 production. Science 2007 317 : 121 124.
49. Mantovani A, Bottazzi B, Colotta F, Sozzani S, Ruco L. The origin and function of tumor-associated macrophages. Immunol Today 1992 13 : 265 270.
50. Mantovani A, Caprioli V, Gritti P, Spreafico F. Human mature macrophages mediate antibody-dependent cellular cytotoxicity on tumour cells. Transplantation 1977 24 : 291 293.
51. Mantovani A. Tumor-associated macrophages in neoplastic progression: a paradigm for the in vivo function of chemokines. Lab Invest 1994 71 : 5 16.
52. Taskinen M, Karjalainen-Lindsberg ML, Nyman H, Eerola LM, Leppa S. A high tumor-associated macrophage content predicts favorable outcome in follicular lymphoma patients treated with rituximab and cyclophosphamide-Doxorubicin- vincristine- prednisone. Clin Cancer Res 2007 13 : 5784 5789.
53. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 2004 21 : 137 148.
54. Smyth MJ, Dunn GP, Schreiber RD. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 2006 90 : 1 50.
55. Galon J, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006 313 : 1960 1964.
56. Pages F, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005 353 : 2654 2666.
57. Garlanda C, et al. Increased susceptibility to colitis-associated cancer of mice lacking TIR8, an inhibitory member of the IL-1 receptor family. Cancer Res 2007 67 : 6017 6021.
58. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006 6 : 24 37.
59. Apetoh L, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007 13 : 1050 1059.
60. Colombo MP, Mantovani A. Targeting myelomonocytic cells to revert inflammation-dependent cancer promotion. Cancer Res 2005 65 : 9113 9116.