Immune cells as mediators of solid tumor metastasis

Cancer and Metastasis Reviews

Volumn 27, Issue 1, 2008, Pages 11-18

  DeNardo, David G ^a   Johansson, Magnus ^a   Coussens, Lisa M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Breast cancer; Inflammation; Metastasis

Indexed keywords

ANGIOGENESIS; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER INVASION; CANCER MORTALITY; CANCER SURVIVAL; CARCINOGENESIS; CELL INTERACTION; CELL PROLIFERATION; CYTOKINE PRODUCTION; ENZYME ACTIVATION; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFLAMMATION; LEUKOCYTE ACTIVATION; MACROPHAGE; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOLID TUMOR; STROMA CELL; TUMOR LOCALIZATION;

ANIMALS; HUMANS; IMMUNE SYSTEM; IMMUNITY, CELLULAR; IMMUNITY, NATURAL; INFLAMMATION; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS;

EID: 38549146376     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10555-007-9100-0     Document Type: Review

References (87)

1. Jemal, A., Siegel, R., Ward, E., Murray, T., Xu, J., & Thun, M. J. (2007). Cancer statistics. CA A Cancer Journal for Clinicians, 57, 43-66 2007.
2. Paget, S. (1889). The distribution of secondary growths in cancer of the breast. Lancet, 1, 571-573.
3. Karin, M., & Greten, F. R. (2005). NF-kappaB: Linking inflammation and immunity to cancer development and progression. Nature Reviews. Immunology, 5, 749-759.
4. Coussens, L. M., & Werb, Z. (2001). Inflammatory cells and cancer: Think different!. Journal of Experimental Medicine, 193, F23-F26.
5. Coussens, L. M., & Werb, Z. (2002). Inflammation and cancer. Nature, 420, 860-867.
6. Balkwill, F., & Coussens, L. M. (2004). Cancer: An inflammatory link. Nature, 431, 405-406.
7. Balkwill, F., & Mantovani, A. (2001). Inflammation and cancer: Back to Virchow? Lancet, 357, 539-545.
8. Balkwill, F., Charles, K. A., & Mantovani, A. (2005). Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell, 7, 211-217.
9. de Visser, K. E., Eichten, A., & Coussens, L. M. (2006). Paradoxical roles of the immune system during cancer development. Nature Reviews Cancer, 6, 24-37.
10. Fidler, I. J. (2003). The pathogenesis of cancer metastasis: The 'seed and soil' hypothesis revisited. Nature Reviews. Cancer, 3, 453-458.
11. Chambers, A. F., Naumov, G. N., Varghese, H. J., Nadkarni, K. V., MacDonald, I. C., & Groom, A. C. (2001). Critical steps in hematogenous metastasis: An overview. Surgical Oncology Clinics of North America, 10, 243-255 vii.
12. Folkman, J. (1992). The role of angiogenesis in tumor growth. Seminars in Cancer Biology, 3, 65-71.
13. Woodhouse, E. C., Chuaqui, R. F., & Liotta, L. A. (1997). General mechanisms of metastasis. Cancer, 80, 1529-1537.
14. Hanahan, D., & Weinberg, R. A. (2000). The hallmarks of cancer. Cell, 100, 57-70.
15. Muller, A., Homey, B., Soto, H., Ge, N., Catron, D., Buchanan, M. E., et al. (2001). Involvement of chemokine receptors in breast cancer metastasis. Nature, 410, 50-56.
16. Wilson, J., & Balkwill, F. (2002). The role of cytokines in the epithelial cancer microenvironment. Seminars in Cancer Biology, 12, 113-120.
17. Borsig, L., Wong, R., Hynes, R. O., Varki, N. M., & Varki, A. (2002). Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proceedings of the National Academy of Sciences of the United States of America, 99, 2193-2198.
18. Laakkonen, P., Porkka, K., Hoffman, J. A., & Ruoslahti, E. (2002). A tumor-homing peptide with a targeting specificity related to lymphatic vessels. Nature Medicine, 8, 751-755.
19. Karin, M., Lawrence, T., & Nizet, V. (2006). Innate immunity gone awry: Linking microbial infections to chronic inflammation and cancer. Cell, 124, 823-835.
20. Wu, J., & Lanier, L. L. (2003). Natural killer cells and cancer. Advances in Cancer Research, 90, 127-156.
21. Theoharides, T. C., & Conti, P. (2004). Mast cells: The Jekyll and Hyde of tumor growth. Trends in Immunology, 25, 235-241.
22. Condeelis, J., & Pollard, J. W. (2006). Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell, 124, 263-266.
23. Mantovani, A., Allavena, P., & Sica, A. (2004). Tumour-associated macrophages as a prototypic type II polarised phagocyte population: Role in tumour progression. European Journal of Cancer, 40, 1660-1667.
24. Goswami, S., Sahai, E., Wyckoff, J. B., Cammer, M., Cox, D., Pixley, F. J., et al. (2005). Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Research, 65, 5278-5283.
25. Wyckoff, J., Wang, W., Lin, E. Y., Wang, Y., Pixley, F., Stanley, E. R., et al. (2004). A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Research, 64, 7022-7029.
26. Bergers, G., & Benjamin, L. E. (2003). Angiogenesis: Tumorigenesis and the angiogenic switch. Nature Reviews. Cancer, 3, 401-410.
27. Wyckoff, J. B., Wang, Y., Lin, E. Y., Li, J. F., Goswami, S., Stanley, E. R., et al. (2007). Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Research, 67, 2649-2656.
28. Lee, T. H., Seng, S., Sekine, M., Hinton, C., Fu, Y., Avraham, H. K., et al. (2007). Vascular endothelial growth factor mediates intracrine survival in human breast carcinoma cells through internally expressed VEGFR1/FLT1. PLoS Medicine, 4, e186.
29. Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., et al. (2000). Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nature Cell Biology, 2, 737-744.
30. Coussens, L. M., Raymond, W. W., Bergers, G., Laig-Webster, M., Behrendtsen, O., Werb, Z., et al. (1999). Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes & Development, 13, 1382-1397.
31. Lin, E. Y., & Pollard, J. W. (2007). Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Research, 67, 5064-5066.
32. Robinson-Smith, T. M., Isaacsohn, I., Mercer, C. A., Zhou, M., Van Rooijen, N., Husseinzadeh, N., et al. (2007). Macrophages mediate inflammation-enhanced metastasis of ovarian tumors in mice. Cancer Research, 67, 5708-5716.
33. Guy, C. T., Cardiff, R. D., & Muller, W. J. (1992). Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Molecular and Cellular Biology, 12, 954-961.
34. Lin, E. Y., Gouon-Evans, V., Nguyen, A. V., & Pollard, J. W. (2002). The macrophage growth factor CSF-1 in mammary gland development and tumor progression. Journal of Mammary Gland Biology and Neoplasia, 7, 147-162.
35. Lin, E. Y., Li, J. F., Gnatovskiy, L., Deng, Y., Zhu, L., Grzesik, D. A., et al. (2006). Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Research, 66, 11238-11246.
36. O'Sullivan, C., & Lewis, C. E. (1994). Tumour-associated leucocytes: Friends or foes in breast carcinoma. Journal of Pathology, 172, 229-235.
37. Leek, R. D., & Harris, A. L. (2002). Tumor-associated macrophages in breast cancer. Journal of Mammary Gland Biology and Neoplasia, 7, 177-189.
38. Bolat, F., Kayaselcuk, F., Nursal, T. Z., Yagmurdur, M. C., Bal, N., & Demirhan, B. (2006). Microvessel density, VEGF expression, and tumor-associated macrophages in breast tumors: Correlations with prognostic parameters. Journal of Experimental & Clinical Cancer Research, 25, 365-372.
39. Tsutsui, S., Yasuda, K., Suzuki, K., Tahara, K., Higashi, H., & Era, S. (2005). Macrophage infiltration and its prognostic implications in breast cancer: The relationship with VEGF expression and microvessel density. Oncology Reports, 14, 425-431.
40. Ohno, S., Ohno, Y., Suzuki, N., Kamei, T., Koike, K., Inagawa, H., et al. (2004). Correlation of histological localization of tumor-associated macrophages with clinicopathological features in endometrial cancer. Anticancer Research, 24, 3335-3342.
41. Oosterling, S. J., van der Bij, G. J., Meijer, G. A., Tuk, C. W., van Garderen, E., van Rooijen, N., et al. (2005). Macrophages direct tumour histology and clinical outcome in a colon cancer model. Journal of Pathology, 207, 147-155.
42. Coussens, L. M., Tinkle, C. L., Hanahan, D., & Werb, Z. (2000). MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell, 103, 481-490.
43. Ribatti, D., Crivellato, E., Roccaro, A. M., Ria, R., & Vacca, A. (2004). Mast cell contribution to angiogenesis related to tumour progression. Clinical & Experimental Allergy, 34, 1660-1664.
44. Ribatti, D., Vacca, A., Nico, B., Crivellato, E., Roncali, L., & Dammacco, F. (2001). The role of mast cells in tumour angiogenesis. British Journal of Haematology, 115, 514-521.
45. Benelli, R., Albini, A., & Noonan, D. (2003). Neutrophils and angiogenesis: Potential initiators of the angiogenic cascade. Chemical Immunology and Allergy, 83, 167-181.
46. Sinha, P., Clements, V. K., Fulton, A. M., & Ostrand-Rosenberg, S. (2007). Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Research, 67, 4507-4513.
47. De Palma, M., Venneri, M. A., Galli, R., Sergi Sergi, L., Politi, L. S., Sampaolesi, M., et al. (2005). Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell, 8, 211-226.
48. Bunt, S. K., Sinha, P., Clements, V. K., Leips, J., & Ostrand-Rosenberg, S. (2006). Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. Journal of Immunology, 176, 284-290.
49. Egeblad, M., & Werb, Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nature Reviews. Cancer, 2, 161-174.
50. Mueller, M. M., & Fusenig, N. E. (2004). Friends or foes-Bipolar effects of the tumour stroma in cancer. Nature Reviews. Cancer, 4, 839-849.
51. Joyce, J. A., & Hanahan, D. (2004). Multiple roles for cysteine cathepsins in cancer. Cell Cycle, 3, 1516-1619.
52. Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W. G., & Quaranta, V. (1997). Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science, 277, 225-228.
53. Pirila, E., Ramamurthy, N. S., Sorsa, T., Salo, T., Hietanen, J., & Maisi, P. (2003). Gelatinase A (MMP-2), collagenase-2 (MMP-8), and laminin-5 gamma2-chain expression in murine inflammatory bowel disease (ulcerative colitis). Digestive Diseases and Sciences, 48, 93-98.
54. Kalluri, R. (2003). Basement membranes: Structure, assembly and role in tumour angiogenesis. Nature Reviews. Cancer, 3, 422-433.
55. van Kempen, L. C., de Visser, K. E., & Coussens, L. M. (2006). Inflammation, proteases and cancer. European Journal of Cancer, 42, 728-734.
56. Cheng, K., Xie, G., & Raufman, J. P. (2007). Matrix metalloproteinase-7-catalyzed release of HB-EGF mediates deoxycholyltaurine- induced proliferation of a human colon cancer cell line. Biochemical Pharmacology, 73, 1001-1012.
57. Wang, F., Sloss, C., Zhang, X., Lee, S. W., & Cusack, J. C. (2007). Membrane-bound heparin-binding epidermal growth factor like growth factor regulates E-cadherin expression in pancreatic carcinoma cells. Cancer Research, 67, 8486-8493.
58. Gocheva, V., Zeng, W., Ke, D., Klimstra, D., Reinheckel, T., Peters, C., et al. (2006). Distinct roles for cysteine cathepsin genes in multistage tumorigenesis. Genes & Development, 20, 543-556.
59. Vasiljeva, O., Papazoglou, A., Kruger, A., Brodoefel, H., Korovin, M., Deussing, J., et al. (2006). Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Research, 66, 5242-5250.
60. Lin, E. Y., Jones, J. G., Li, P., Zhu, L., Whitney, K. D., Muller, W. J., et al. (2003). Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. American Journal of Pathology, 163, 2113-2126.
61. Hagemann, T., Wilson, J., Kulbe, H., Li, N. F., Leinster, D. A., Charles, K., et al. (2005). Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK. Journal of Immunology, 175, 1197-1205.
62. Scott, K. A., Arnott, C. H., Robinson, S. C., Moore, R. J., Thompson, R. G., Marshall, J. F., et al. (2004). TNF-alpha regulates epithelial expression of MMP-9 and integrin alphavbeta6 during tumour promotion. A role for TNF-alpha in keratinocyte migration? Oncogene, 23, 6954-6966.
63. Szlosarek, P. W., Grimshaw, M. J., Kulbe, H., Wilson, J. L., Wilbanks, G. D., Burke, F., et al. (2006). Expression and regulation of tumor necrosis factor alpha in normal and malignant ovarian epithelium. Molecular Cancer Therapeutics, 5, 382-390.
64. Szlosarek, P., Charles, K. A., & Balkwill, F. R. (2006). Tumour necrosis factor-alpha as a tumour promoter. European Journal of Cancer, 42, 745-750.
65. Luo, J. L., Tan, W., Ricono, J. M., Korchynskyi, O., Zhang, M., Gonias, S. L., et al. (2007). Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature, 446, 690-694.
66. Abraham, S., Zhang, W., Greenberg, N., & Zhang, M. (2003). Maspin functions as tumor suppressor by increasing cell adhesion to extracellular matrix in prostate tumor cells. Journal of Urology, 169, 1157-1161.
67. Sager, R., Sheng, S., Pemberton, P., & Hendrix, M. J. (1997). Maspin. A tumor suppressing serpin. Advances in Experimental Medicine and Biology, 425, 77-88.
68. Chen, E. I., & Yates, J. R. (2006). Maspin and tumor metastasis. IUMB Life, 58, 25-29.
69. Jones, D. H., Nakashima, T., Sanchez, O. H., Kozieradzki, I., Komarova, S. V., Sarosi, I., et al. (2006). Regulation of cancer cell migration and bone metastasis by RANKL. Nature, 440, 692-696.
70. Shi, H. Y., Zhang, W., Liang, R., Kittrell, F., Templeton, N. S., Medina, D., et al. (2003). Modeling human breast cancer metastasis in mice: Maspin as a paradigm. Histology and Histopathology, 18, 201-206.
71. Lockett, J., Yin, S., Li, X., Meng, Y., & Sheng, S. (2006). Tumor suppressive maspin and epithelial homeostasis. Journal of Cellular Biochemistry, 97, 651-660.
72. Gorden, D. L., Fingleton, B., Crawford, H. C., Jansen, D. E., Lepage, M., & Matrisian, L. M. (2007). Resident stromal cell-derived MMP-9 promotes the growth of colorectal metastases in the liver microenvironment. International Journal of Cancer, 121, 495-500.
73. Lynch, C. C., Hikosaka, A., Acuff, H. B., Martin, M. D., Kawai, N., Singh, R. K., et al. (2005). MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell, 7, 485-496.
74. Lewis, C. E., & Pollard, J. W. (2006). Distinct role of macrophages in different tumor microenvironments. Cancer Research, 66, 605-612.
75. Leek, R. D., Hunt, N. C., Landers, R. J., Lewis, C. E., Royds, J. A., & Harris, A. L. (2000). Macrophage infiltration is associated with VEGF and EGFR expression in breast cancer. Journal of Pathology, 190, 430-436.
76. Wyckoff, J. B., Segall, J. E., & Condeelis, J. S. (2000). The collection of the motile population of cells from a living tumor. Cancer Research, 60, 5401-5404.
77. Wang, W., Wyckoff, J. B., Goswami, S., Wang, Y., Sidani, M., Segall, J. E., et al. (2007). Coordinated regulation of pathways for enhanced cell motility and chemotaxis is conserved in rat and mouse mammary tumors. Cancer Research, 67, 3505-3511.
78. Condeelis, J., & Segall, J. E. (2003). Intravital imaging of cell movement in tumours. Nature Reviews. Cancer, 3, 921-930.
79. Luzzi, K. J., MacDonald, I. C., Schmidt, E. E., Kerkvliet, N., Morris, V. L., Chambers, A. F., et al. (1998). Multistep nature of metastatic inefficiency: Dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. American Journal of Pathology, 153, 865-873.
80. Hiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., et al. (2002). MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell, 2, 289-300.
81. Acuff, H. B., Carter, K. J., Fingleton, B., Gorden, D. L., & Matrisian, L. M. (2006). Matrix metalloproteinase-9 from bone marrow-derived cells contributes to survival but not growth of tumor cells in the lung microenvironment. Cancer Research, 66, 259-266.
82. Hiratsuka, S., Watanabe, A., Aburatani, H., & Maru, Y. (2006). Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nature Cell Biology, 8, 1369-1375.
83. Lin, E. Y., & Pollard, J. W. (2004). Macrophages: Modulators of breast cancer progression. Novartis Foundation Symposium, 256, 158-168 discussion 68-72, 259-69.
84. Kaplan, R. N., Psaila, B., & Lyden, D. (2006). Bone marrow cells in the 'pre-metastatic niche': Within bone and beyond. Cancer and Metastasis Reviews, 25, 521-529.
85. Kaplan, R. N., Riba, R. D., Zacharoulis, S., Bramley, A. H., Vincent, L., Costa, C., et al. (2005). VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature, 438, 820-827.
86. Coussens, L. M., Fingleton, B., & Matrisian, L. M. (2002). Matrix metalloproteinase inhibitors and cancer: Trials and tribulations. Science, 295, 2387-2392.
87. Psaty, B. M., & Furberg, C. D. (2005). COX-2 inhibitors-Lessons in drug safety. New England Journal of Medicine, 352, 1133-1135.