Monocyte/macrophage infiltration in tumors: Modulators of angiogenesis

Journal of Leukocyte Biology

Volumn 80, Issue 6, 2006, Pages 1183-1196

  Dirkx, Anita E M ^a   Oude Egbrink, Mirjam G A ^b   Wagstaff, John ^c   Griffioen, Arjan W ^a,d  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c SINGLETON HOSPITAL   (United Kingdom)

^d MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Immunotherapy; Leukocyte

Indexed keywords

CELL ADHESION MOLECULE; CHEMOKINE; CYTOKINE; FIBROBLAST GROWTH FACTOR 2; GELATINASE B; INTERLEUKIN 1; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 8; MACROPHAGE ELASTASE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANGIOGENESIS; CANCER GROWTH; CANCER PATIENT; CANCER SURVIVAL; CELL FUNCTION; CELL INFILTRATION; CYTOTOXICITY; GENE THERAPY; HUMAN; IMMUNOTHERAPY; METASTASIS; MONOCYTE; PRIORITY JOURNAL; PROGNOSIS; REVIEW; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL;

ANGIOGENESIS INHIBITORS; ANIMALS; CELL PROLIFERATION; COMBINED MODALITY THERAPY; HUMANS; IMMUNITY, CELLULAR; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MACROPHAGES; NEOPLASM METASTASIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR ESCAPE;

EID: 33845466231     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0905495     Document Type: Review

References (171)

1. Folkman, J. (1971) Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285, 1182-1186.
2. Holmgren, L., O'Reilly, M. S., Folkman, J. (1995) Dormancy of micrometastases - balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med. 1, 149-153.
3. Hanahan, D., Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364.
4. Folkman, J. (2002) Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29, 15-18.
5. Carmeliet, P., Jain, R. K. (2000) Angiogenesis in cancer and other diseases. Nature 407, 249-257.
6. Virchow, R. (1863) Die Krankenhaften Geschwülste, August Hirschwald, Berlin.
7. Brigati, C., Noonan, D. M., Albini, A., Benelli, R. (2002) Tumors and inflammatory infiltrates: friends or foes? Clin. Exp. Metastasis 19, 247-258.
8. Scanlan, M. J., Gout, I., Gordon, C. M., Williamson, B., Stockert, E., Gure, A. O., Jager, D., Chen, Y. T., Mackay, A., O'Hare, M. J., Old, L. J. (2001) Humoral immunity to human breast cancer: antigen definition and quantitative analysis of mRNA expression. Cancer Immun. 1, 4.
9. Vaughan, H. A., St Clair, F., Scanlan, M. J., Chen, Y. T., Maraskovsky, E., Sizeland, A., Old, L. J., Cebon, J. (2004) The humoral immune response to head and neck cancer antigens as defined by the serological analysis of tumor antigens by recombinant cDNA expression cloning. Cancer Immun. 4, 5.
10. Nathan, C. (2002) Points of control in inflammation. Nature 420, 846-852.
11. Lin, E. Y., Pollard, J. W. (2004) Role of infiltrated leucocytes in tumor growth and spread. Br. J. Cancer 90, 2053-2058.
12. Dvorak, H. F. (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650-1659.
13. Schreurs, M. W., Eggert, A. A., de Boer, A. J., Vissers, J. L., van Hall, T., Offringa, R., Figdor, C. G., Adema, G. J. (2000) Dendritic cells break tolerance and induce protective immunity against a melanocyte differentiation antigen in an autologous melanoma model. Cancer Res. 60, 6995-7001.
14. Borgstrom, P., Hughes, G. K., Hansell, P., Wolitsky, B. A., Sriramarao, P. (1997) Leukocyte adhesion in angiogenic blood vessels. Role of Eselectin, P-selectin, and β2 integrin in lymphotoxin-mediated leukocyte recruitment in tumor microvessels. J. Clin. Invest. 99, 2246-2253.
15. Fukumura, D., Salehi, H. A., Witwer, B., Tuma, R. F., Melder, R. J., Jain, R. K. (1995) Tumor necrosis factor α-induced leukocyte adhesion in normal and tumor vessels: effect of tumor type, transplantation site, and host strain. Cancer Res. 55, 4824-4829.
16. Wu, N. Z., Klitzman, B., Dodge, R., Dewhirst, M. W. (1992) Diminished leukocyte-endothelium interaction in tumor microvessels. Cancer Res. 52, 4265-4268.
17. Jain, R. K., Koenig, G. C., Dellian, M., Fukumura, D., Munn, L. L., Melder, R. J. (1996) Leukocyte-endothelial adhesion and angiogenesis in tumors. Cancer Metastasis Rev. 15, 195-204.
18. Dirkx, A. E. M., Oude Egbrink, M. G., Kuijpers, M. J., van der Niet, S. T., Heijnen, V. V., Bouma-ter Steege, J. C., Wagstaff, J., Griffioen, A. W. (2003) Tumor angiogenesis modulates leukocyte-vessel wall interactions in vivo by reducing endothelial adhesion molecule expression. Cancer Res. 63, 2322-2329.
19. Chen, Q., Wang, W. C., Evans, S. S. (2003) Tumor microvasculature as a barrier to antitumor immunity. Cancer Immunol. Immunother. 52, 670-679.
20. Carlos, T. M. (2001) Leukocyte recruitment at sites of tumor: dissonant orchestration. J. Leukoc. Biol. 70, 171-184.
21. Melder, R. J., Koenig, G. C., Witwer, B. P., Safabakhsh, N., Munn, L. L., Jain, R. K. (1996) During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat. Med. 2, 992-997.
22. Griffioen, A. W., Molema, G. (2000) Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases and chronic inflammation. Pharmacol. Rev. 52, 237-268.
23. Inoshima, N., Nakanishi, Y., Minami, T., Izumi, M., Takayama, K., Yoshino, I., Hara, N. (2002) The influence of dendritic cell infiltration and vascular endothelial growth factor expression on the prognosis of non-small cell lung cancer. Clin. Cancer Res. 8, 3480-3486.
24. Malmberg, K. J. (2004) Effective immunotherapy against cancer: a question of overcoming immune suppression and immune escape? Cancer Immunol. Immunother. 53, 879-892.
25. Zhang, H., Issekutz, A. C. (2001) Growth factor regulation of neutrophil-endothelial cell interactions. J. Leukoc. Biol. 70, 225-232.
26. Bodey, B., Bodey Jr., B., Siegel, S. E., Kaiser, H. E. (2000) Controversies on the prognostic significance of tumor infiltrating leukocytes in solid human tumors. Anticancer Res. 20, 1759-1768.
27. Scapini, P., Nesi, L., Morini, M., Tanghetti, E., Belleri, M., Noonan, D., Presta, M., Albini, A., Cassatella, M. A. (2002) Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils. J. Immunol. 168, 5798-5804.
28. Bellocq, A., Antoine, M., Flahault, A., Philippe, C., Crestani, B., Bernaudin, J. F., Mayaud, C., Milleron, B., Baud, L., Cadranel, J. (1998) Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome. Am. J. Pathol. 152, 83-92.
29. Caruso, R. A., Bellocco, R., Pagano, M., Bertoli, G., Rigoli, L., Inferrera, C. (2002) Prognostic value of intratumoral neutrophils in advanced gastric carcinoma in a high-risk area in northern Italy. Mod. Pathol. 15, 831-837.
30. Repp, R., van Ojik, H. H., Valerius, T., Groenewegen, G., Wieland, G., Oetzel, C., Stockmeyer, B., Becker, W., Eisenhut, M., Steininger, H., Deo Y. M., Blijham, G. H., Kalden, J. R., van de Winkel, J. G., Gramatzki, M. (2003) Phase I clinical trial of the bispecific antibody MDX-H210 (anti-FcγRI x anti-HER-2/neu) in combination with Filgrastim (G-CSF) for treatment of advanced breast cancer. Br. J. Cancer 89, 2234-2243.
31. Benelli, R., Morini, M., Carrozzino, F., Ferrari, N., Minghelli, S., Santi, L., Cassatella, M., Noonan, D. M., Albini, A. (2002) Neutrophils as a key cellular target for angiostatin: implications for regulation of angiogenesis and inflammation. FASEB J. 16, 267-269.
32. Imai, K., Matsuyama, S., Miyake, S., Suga, K., Nakachi, K. (2000) Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356, 1795-1799.
33. Kataki, A., Scheid, P., Piet, M., Marie, B., Martinet, N., Martinet, Y., Vignaud, J. M. (2002) Tumor infiltrating lymphocytes and macrophages have a potential dual role in lung cancer by supporting both host-defense and tumor progression. J. Lab. Clin. Med. 140, 320-328.
34. Tazi, A., Bouchonnet, F., Grandsaigne, M., Boumsell, L., Hance, A. J., Soler, P. (1993) Evidence that granulocyte macrophage-colony-stimulating factor regulates the distribution and differentiated state of dendritic cells/Langerhans cells in human lung and lung cancers. J. Clin. Invest. 91, 566-576.
35. Yao, L., Sgadari, C., Furuke, K., Bloom, E. T., Teruya, F. J., Tosato, G. (1999) Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood 93, 1612-1621.
36. Hayakawa, Y., Takeda, K., Yagita, H., Smyth, M. J., Van Kaer, L., Okumura, K., Saiki, I. (2002) IFN-γ-mediated inhibition of tumor angiogenesis by natural killer T-cell ligand, α-galactosylceramide. Blood 100, 1728-1733.
37. Allavena, P., Paganin, C., Martin-Padura, I., Peri, G., Gaboli, M., Dejana, E., Marchisio, P. C., Mantovani, A. (1991) Molecules and structures involved in the adhesion of natural killer cells to vascular endothelium. J. Exp. Med. 173, 439-448.
38. Damle, N. K., Doyle, L. V. (1989) IL-2-activated human killer lymphocytes but not their secreted products mediate increase in albumin flux across cultured endothelial monolayers. Implications for vascular leak syndrome. J. Immunol. 142, 2660-2669.
39. Freeman, M. R., Schneck, F. X., Gagnon, M. L., Corless, C., Soker, S., Niknejad, K., Peoples, G. E., Klagsbrun, M. (1995) Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res. 55, 4140-4145.
40. Nielsen, H. J., Hansen, U., Christensen, I. J., Reimert, C. M., Brunner, N., Moesgaard, F. (1999) Independent prognostic value of eosinophil and mast cell infiltration in colorectal cancer tissue. J. Pathol. 189, 487-495.
41. Zhang, L., Conejo-Garcia, J. R., Katsaros, D., Gimotty, P. A., Massobrio, M., Regnani, G., Makrigiannakis, A., Gray, H., Schlienger, K., Liebman, M. N., Rubin, S. C., Coukos, G. (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348, 203-213.
42. Kondratiev, S., Sabo, E., Yakirevich, E., Lavie, O., Resnick, M. B. (2004) Intratumoral CD8+ T lymphocytes as a prognostic factor of survival in endometrial carcinoma. Clin. Cancer Res. 10, 4450-4456.
43. Beatty, G., Paterson, Y. (2001) IFN-γ-dependent inhibition of tumor angiogenesis by tumor-infiltrating CD4+ T cells requires tumor responsiveness to IFN-γ. J. Immunol. 166, 2276-2282.
44. Lee, I. Y., Kim, J., Ko, E. M., Jeoung, E. J., Kwon, Y. G., Choe, J. (2002) Interleukin-4 inhibits the vascular endothelial growth factor- and basic fibroblast growth factor-induced angiogenesis in vitro. Mol. Cells 14, 115-121.
45. Mizoguchi, H., O'Shea, J. J., Longo, D. L., Loeffler, C. M., McVicar, D. W., Ochoa, A. C. (1992) Alterations in signal transduction molecules in T lymphocytes from tumor-bearing mice. Science 258, 1795-1798.
46. Luscher, U., Filgueira, L., Juretic, A., Zuber, M., Luscher, N. J., Heberer, M., Spagnoli, G. C. (1994) The pattern of cytokine gene expression in freshly excised human metastatic melanoma suggests a state of reversible anergy of tumor-infiltrating lymphocytes. Int. J. Cancer 57, 612-619.
47. Javia, L. R., Rosenberg, S. A. (2003) CD4+CD25+ suppressor lymphocytes in the circulation of patients immunized against melanoma antigens. J. Immunother. 26, 85-93.
48. Antony, P. A., Piccirillo, C. A., Akpinarli, A., Finkelstein, S. E., Speiss, P. J., Surman, D. R., Palmer, D. C., Chan, C. C., Klebanoff, C. A., Overwijk, W. W., Rosenberg, S. A., Restifo, N. P. (2005) CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174, 2591-2601.
49. Peoples, G. E., Blotnick, S., Takahashi, K., Freeman, M. R., Klagsbrun, M., Eberlein, T. J. (1995) T lymphocytes that infiltrate tumors and atherosclerotic plaques produce heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor: a potential pathologic role. Proc. Natl. Acad. Sci. USA 92, 6547-6551.
50. Mor, F., Quintana, F. J., Cohen, I. R. (2004) Angiogenesis-inflammation cross-talk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J. Immunol. 172, 4618-4623.
51. De Visser, K. E., Korets, L. V., Coussens, L. M. (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7, 411-423.
52. De Visser, K. E., Coussens, L. M. (2005) The interplay between innate and adaptive immunity regulates cancer development. Cancer Immunol. Immunother. 54, 1143-1152.
53. Figdor, C. G., de Vries, I. J., Lesterhuis, W. J., Melief, C. J. (2004) Dendritic cell immunotherapy: mapping the way. Nat. Med. 10, 475-480.
54. Menetrier-Caux, C., Thomachot, M. C., Alberti, L., Montmain, G., Blay, J. Y. (2001) IL-4 prevents the blockade of dendritic cell differentiation induced by tumor cells. Cancer Res. 61, 3096-3104.
55. Steinman, R. M., Nussenzweig, M. C. (2002) Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99, 351-358.
56. Dadabayev, A. R., Sandel, M. H., Menon, A. G., Morreau, H., Melief, C. J., Offringa, R., Van Der Burg, S. H., Rhijn, C. J., Ensink, N. G., Tollenaar, R. A., Van De Velde, C. J., Kuppen, P. J. (2004) Dendritic cells in colorectal cancer correlate with other tumor-infiltrating immune cells. Cancer Immunol. Immunother. 53, 978-986.
57. Nestle, F. O., Banchereau, J., Hart, D. (2001) Dendritic cells: on the move from bench to bedside. Nat. Med. 7, 761-765.
58. De Vries, I. J., Lesterhuis, W. J., Scharenborg, N. M., Engelen, L. P., Ruiter, D. J., Gerritsen, M. J., Croockewit, S., Britten, C. M., Torensma, R., Adema, G. J., Figdor, C. G., Punt, C. J. (2003) Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin. Cancer Res. 9, 5091-5100.
59. Gilboa, E., Nair, S. K., Lyerly, H. K. (1998) Immunotherapy of cancer with dendritic-cell-based vaccines. Cancer Immunol. Immunother. 46, 82-87.
60. Hiromatsu, Y., Toda, S. (2003) Mast cells and angiogenesis. Microsc. Res. Tech. 60, 64-69.
61. Coussens, L. M., Raymond, W. W., Bergers, G., Laig-Webster, M., Behrendtsen, O., Werb, Z., Caughey, G. H., Hanahan, D. (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 13, 1382-1397.
62. Ribatti, D., Vacca, A., Nico, B., Crivellato, E., Roncali, L., Dammacco, F. (2001) The role of mast cells in tumor angiogenesis. Br. J. Haematol. 115, 514-521.
63. Zhang, W., Stoica, G., Tasca, S. I., Kelly, K. A., Meininger, C. J. (2000) Modulation of tumor angiogenesis by stem cell factor. Cancer Res. 60, 6757-6762.
64. Bingle, L., Brown, N. J., Lewis, C. E. (2002) The role of tumor-associated macrophages in tumor progression: implications for new anticancer therapies. J. Pathol. 196, 254-265.
65. Leek, R. D., Lewis, C. E., Whitehouse, R., Greenall, M., Clarke, J., Harris, A. L. (1996) Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 56, 4625-4629.
66. Polverini, P. J. (1996) How the extracellular matrix and macrophages contribute to angiogenesis-dependent diseases. Eur. J. Cancer 32A, 2430-2437.
67. Leek, R. D., Harris, A. L. (2002) Tumor-associated macrophages in breast cancer. J. Mammary Gland Biol. Neoplasia 7, 177-189.
68. Torisu, H., Ono, M., Kiryu, H., Furue, M., Ohmoto, Y., Nakayama, J., Nishioka, Y., Sone, S., Kuwano, M. (2000) Macrophage infiltration correlates with tumor stage and angiogenesis in human malignant melanoma: possible involvement of TNFα and IL-1α. Int. J. Cancer 85, 182-188.
69. Fujimoto, J., Sakaguchi, H., Aoki, I., Tamaya, T. (2000) Clinical implications of expression of interleukin 8 related to angiogenesis in uterine cervical cancers. Cancer Res. 60, 2632-2635.
70. Salvesen, H. B., Akslen, L. A. (1999) Significance of tumor-associated macrophages, vascular endothelial growth factor and thrombospondin-1 expression for tumor angiogenesis and prognosis in endometrial carcinomas. Int. J. Cancer 84, 538-543.
71. Lee, A. H., Happerfield, L. C., Bobrow, L. G., Millis, R. R. (1997) Angiogenesis and inflammation in invasive carcinoma of the breast. J. Clin. Pathol. 50, 669-673.
72. De Palma, M., Venneri, M. A., Galli, R., Sergi, S. L., Politi, L. S., Sampaolesi, M., Naldini, L. (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.
73. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686.
74. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., Sica, A. (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555.
75. Shimura, S., Yang, G., Ebara, S., Wheeler, T. M., Frolov, A., Thompson, T. C. (2000) Reduced infiltration of tumor-associated macrophages in human prostate cancer: association with cancer progression. Cancer Res. 60, 5857-5861.
76. Migita, T., Sato, E., Saito, K., Mizoi, T., Shiiba, K., Matsuno, S., Nagura, H., Ohtani, H. (1999) Differing expression of MMPs-1 and -9 and urokinase receptor between diffuse- and intestinal-type gastric carcinoma. Int. J. Cancer 84, 74-79.
77. Nesbit, M., Schaider, H., Miller, T. H., Herlyn, M. (2001) Low-level monocyte chemoattractant protein-1 stimulation of monocytes leads to tumor formation in nontumorigenic melanoma cells. J. Immunol. 166, 6483-6490.
78. Strieter, R. M., Belperio, J. A., Phillips, R. J., Keane, M. P. (2004) CXC chemokines in angiogenesis of cancer. Semin. Cancer Biol. 14, 195-200.
79. Murdoch, C., Giannoudis, A., Lewis, C. E. (2004) Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 104, 2224-2234.
80. Zhang, H., Issekutz, A. C. (2002) Down-modulation of monocyte transendothelial migration and endothelial adhesion molecule expression by fibroblast growth factor: reversal by the anti-angiogenic agent SU6668. Am. J. Pathol. 160, 2219-2230.
81. Varney, M. L., Olsen, K. J., Mosley, R. L., Bucana, C. D., Talmadge, J. E., Singh, R. K. (2002) Monocyte/macrophage recruitment, activation and differentiation modulate interleukin-8 production: a paracrine role of tumor-associated macrophages in tumor angiogenesis. In Vivo 16, 471-477.
82. Liss, C., Fekete, M. J., Hasina, R., Lam, C. D., Lingen, M. W. (2001) Paracrine angiogenic loop between head-and-neck squamous-cell carcinomas and macrophages. Int. J. Cancer 93, 781-785.
83. Locati, M., Deuschle, U., Massardi, M. L., Martinez, F. O., Sironi, M., Sozzani, S., Bartfai, T., Mantovani, A. (2002) Analysis of the gene expression profile activated by the CC chemokine ligand 5/RANTES and by lipopolysaccharide in human monocytes. J. Immunol. 168, 3557-3562.
84. Azenshtein, E., Luboshits, G., Shina, S., Neumark, E., Shahbazian, D., Weil, M., Wigler, N., Keydar, I., Ben Baruch, A. (2002) The CC chemokine RANTES in breast carcinoma progression: regulation of expression and potential mechanisms of promalignant activity. Cancer Res. 62, 1093-1102.
85. Gerszten, R. E., Garcia-Zepeda, E. A., Lim, Y. C., Yoshida, M., Ding, H. A., Gimbrone Jr., M. A., Luster, A. D., Luscinskas, F. W., Rosenzweig, A. (1999) MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 398, 718-723.
86. Clauss, M., Gerlach, M., Gerlach, H., Brett, J., Wang, F., Familletti, P. C., Pan, Y. C., Olander, J. V., Connolly, D. T., Stern, D. (1990) Vascular permeability factor: a tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration. J. Exp. Med. 172, 1535-1545.
87. Sawano, A., Iwai, S., Sakurai, Y., Ito, M., Shitara, K., Nakahata, T., Shibuya, M. (2001) Flt-1, vascular endothelial growth factor receptor 1, is a novel cell surface marker for the lineage of monocyte-macrophages in humans. Blood 97, 785-791.
88. 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. J. Pathol. 190, 430-436.
89. Crowther, M., Brown, N. J., Bishop, E. T., Lewis, C. E. (2001) Microenvironmental influence on macrophage regulation of angiogenesis in wounds and malignant tumors. J. Leukoc. Biol. 70, 478-490.
90. Kacinski, B. M. (1995) CSF-1 and its receptor in ovarian, endometrial and breast cancer. Ann. Med. 27, 79-85.
91. Lin, E. Y., Nguyen, A. V., Russell, R. G., Pollard, J. W. (2001) Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193, 727-740.
92. Tang, R., Beuvon, F., Ojeda, M., Mosseri, V., Pouillart, P., Scholl, S. (1992) M-CSF (monocyte colony stimulating factor) and M-CSF receptor expression by breast tumour cells: M-CSF mediated recruitment of tumor infiltrating monocytes? J. Cell. Biochem. 50, 350-356.
93. Scholl, S. M., Pallud, C., Beuvon, F., Hacene, K., Stanley, E. R., Rohrschneider, L., Tang, R., Pouillart, P., Lidereau, R. (1994) Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J. Natl. Cancer Inst. 86, 120-126.
94. Chambers, S. K., Kacinski, B. M., Ivins, C. M., Carcangiu, M. L. (1997) Overexpression of epithelial macrophage colony-stimulating factor (CSF-1) and CSF-1 receptor: a poor prognostic factor in epithelial ovarian cancer, contrasted with a protective effect of stromal CSF-1. Clin. Cancer Res. 3, 999-1007.
95. Toy, E. P., Chambers, J. T., Kacinski, B. M., Flick, M. B., Chambers, S. K. (2001) The activated macrophage colony-stimulating factor (CSF-1) receptor as a predictor of poor outcome in advanced epithelial ovarian carcinoma. Gynecol. Oncol. 80, 194-200.
96. Eubank, T. D., Galloway, M., Montague, C. M., Waldman, W. J., Marsh, C. B. (2003) M-CSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J. Immunol. 171, 2637-2643.
97. Etzioni, A., Doerschuk, C. M., Harlan, J. M. (1999) Of man and mouse: leukocyte and endothelial adhesion molecule deficiencies. Blood 94, 3281-3288.
98. Springer, T. A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration - the multistep paradigm. Cell 76, 301-314.
99. Vestweber, D., Blanks, J. E. (1999) Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79, 181-213.
100. Butcher, E. C. (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67, 1033-1036.
101. Muller, W. A. (2002) Leukocyte-endothelial cell interactions in the inflammatory response. Lab. Invest. 82, 521-533.
102. Muller, W. A. (2003) Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24, 327-334.
103. Tromp, S. C., oude Egbrink, M. G., Dings, R. P. M., Van Velzen, S., Slaaf, D. W., Hillen, H. F. P., Tangelder, G. J., Reneman, R. S., Griffioen, A. W. (2000) Tumor angiogenesis factors reduce leukocyte adhesion in vivo. Int. Immunol. 12, 671-676.
104. Griffioen, A. W., Damen, C. A., Blijham, G. H., Groenewegen, G. (1996) Tumor angiogenesis is accompanied by a decreased inflammatory response of tumor associated endothelium. Blood 88, 667-673.
105. Belardelli, F., Ferrantini, M. (2002) Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol. 23, 201-208.
106. Voest, E. E., Kenyon, B. M., O'Reilly, M. S., Truitt, G., D'Amato, R. J., Folkman, J. (1995) Inhibition of angiogenesis in vivo by interleukin 12. J. Natl. Cancer Inst. 87, 581-586.
107. Coughlin, C. M., Salhany, K. E., Wysocka, M., Aruga, E., Kurzawa, H., Chang, A. E., Hunter, C. A., Fox, J. C., Trinchieri, G., Lee, W. M. F. (1998) Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J. Clin. Invest. 101, 1441-1452.
108. Mitola, S., Strasly, M., Prato, M., Ghia, P., Bussolino, F. (2003) IL-12 regulates an endothelial cell-lymphocyte network: effect on metalloproteinase-9 production. J. Immunol. 171, 3725-3733.
109. Strasly, M., Cavallo, F., Geuna, M., Mitola, S., Colombo, M. P., Forni, G., Bussolino, F. (2001) IL-12 inhibition of endothelial cell functions and angiogenesis depends on lymphocyte-endothelial cell cross-talk. J. Immunol. 166, 3890-3899.
110. Sgadari, C., Angiolillo, A. L., Tosato, G. (1996) Inhibition of angiogenesis by interleukin-12 is mediated by the interferon-inducible protein 10. Blood 87, 3877-3882.
111. Strieter, R. M., Polverini, P. J., Kunkel, S. L., Arenberg, D. A., Burdick, M. D., Kasper, J., Dzuiba, J., Van Damme, J., Walz, A., Marriott, D. (1995) The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem. 270, 27348-27357.
112. Wahl, L. M., Kleinman, H. K. (1998) Tumor-associated macrophages as targets for cancer therapy. J. Natl. Cancer Inst. 90, 1583-1584.
113. Okamura, H., Tsutsi, H., Komatsu, T., Yutsudo, M., Hakura, A., Tanimoto, T., Torigoe, K., Okura, T., Nukada, Y., Hattori, K. (1995) Cloning of a new cytokine that induces IFN-γ production by T cells. Nature 378, 88-91.
114. Nakanishi, K., Yoshimoto, T., Tsutsui, H., Okamura, H. (2001) Interleukin-18 is a unique cytokine that stimulates both Th1 and Th2 responses depending on its cytokine milieu. Cytokine Growth Factor Rev. 12, 53-72.
115. Cao, R., Farnebo, J., Kurimoto, M., Cao, Y. (1999) Interleukin-18 acts as an angiogenesis and tumor suppressor. FASEB J. 13, 2195-2202.
116. Tatsumi, T., Huang, J., Gooding, W. E., Gambotto, A., Robbins, P. D., Vujanovic, N. L., Alber, S. M., Watkins, S. C., Okada, H., Storkus, W. J. (2003) Intratumoral delivery of dendritic cells engineered to secrete both interleukin (IL)-12 and IL-18 effectively treats local and distant disease in association with broadly reactive Tc1-type immunity. Cancer Res. 63, 6378-6386.
117. Kerkela, E., Ala-aho, R., Klemi, P., Grenman, S., Shapiro, S. D., Kahari, V. M., Saarialho-Kere, U. (2002) Metalloelastase (MMP-12) expression by tumor cells in squamous cell carcinoma of the vulva correlates with invasiveness, while that by macrophages predicts better outcome. J. Pathol. 198, 258-269.
118. Cornelius, L. A., Nehring, L. C., Harding, E., Bolanowski, M., Welgus, H. G., Kobayashi, D. K., Pierce, R. A., Shapiro, S. D. (1998) Matrix metalloproteinases generate angiostatin: effects on neovascularization. J. Immunol. 161, 6845-6852.
119. Gorrin-Rivas, M. J., Arii, S., Mori, A., Takeda, Y., Mizumoto, M., Furutani, M., Imamura, M. (2000) Implications of human macrophage metalloelastase and vascular endothelial growth factor gene expression in angiogenesis of hepatocellular carcinoma. Ann. Surg. 231, 67-73.
120. Dong, Z., Kumar, R., Yang, X., Fidler, I. J. (1997) Macrophage-derived metalloelastase is responsible for the generation of angiostatin in Lewis lung carcinoma. Cell 88, 801-810.
121. Tsung, K., Dolan, J. P., Tsung, Y. L., Norton, J. A. (2002) Macrophages as effector cells in interleukin 12-induced T cell-dependent tumor rejection. Cancer Res. 62, 5069-5075.
122. Inoue, Y., Nakayama, Y., Minagawa, N., Katsuki, T., Nagashima, N., Matsumoto, K., Shibao, K., Tsurudome, Y., Hirata, K., Nagata, N., Itoh, H. (2005) Relationship between interleukin-12-expressing cells and antigen-presenting cells in patients with colorectal cancer. Anticancer Res. 25, 3541-3546.
123. Dias, S., Boyd, R., Balkwill, F. (1998) IL-12 regulates VEGF and MMPs in a murine breast cancer model. Int. J. Cancer 78, 361-365.
124. Van Herpen, C. M., Looman, M., Zonneveld, M., Scharenborg, N., de Wilde, P. C., van de Locht, L., Merkx, M. A., Adema, G. J., de Mulder, P. H. (2004) Intratumoral administration of recombinant human interleukin 12 in head and neck squamous cell carcinoma patients elicits a T-helper 1 profile in the locoregional lymph nodes. Clin. Cancer Res. 10, 2626-2635.
125. Wadler, S., Levy, D., Frederickson, H. L., Falkson, C. I., Wang, Y., Weller, E., Burk, R., Ho, G., Kadish, A. S. (2004) A phase II trial of interleukin-12 in patients with advanced cervical cancer: clinical and immunologic correlates. Eastern Cooperative Oncology Group study E1E96. Gynecol. Oncol. 92, 957-964.
126. Gollob, J. A., Veenstra, K. G., Parker, R. A., Mier, J. W., McDermott, D. F., Clancy, D., Tutin, L., Koon, H., Atkins, M. B. (2003) Phase I trial of concurrent twice-weekly recombinant human interleukin-12 plus low-dose IL-2 in patients with melanoma or renal cell carcinoma. J. Clin. Oncol. 21, 2564-2573.
127. Kerkela, E., Ala-aho, R., Jeskanen, L., Rechardt, O., Grenman, R., Shapiro, S. D., Kahari, V. M., Saarialho-Kere, U. (2000) Expression of human macrophage metalloelastase (MMP-12) by tumor cells in skin cancer. J. Invest. Dermatol. 114, 1113-1119.
128. O'Reilly, M. S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R. A., Moses, M., Lane, W. S., Cao, Y., Sage, E. H., Folkman, J. (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79, 315-328.
129. Voronov, E., Shouval, D. S., Krelin, Y., Cagnano, E., Benharroch, D., Iwakura, Y., Dinarello, C. A., Apte, R. N. (2003) IL-1 is required for tumor invasiveness and angiogenesis. Proc. Natl. Acad. Sci. USA 100, 2645-2650.
130. Song, X., Voronov, E., Dvorkin, T., Fima, E., Cagnano, E., Benharroch, D., Shendler, Y., Bjorkdahl, O., Segal, S., Dinarello, C. A., Apte, R. N. (2003) Differential effects of IL-1 α and IL-1 β on tumorigenicity patterns and invasiveness. J. Immunol. 171, 6448-6456.
131. Saijo, Y., Tanaka, M., Miki, M., Usui, K., Suzuki, T., Maemondo, M., Hong, X., Tazawa, R., Kikuchi, T., Matsushima, K., Nukiwa, T. (2002) Proinflammatory cytokine IL-1 β promotes tumor growth of Lewis lung carcinoma by induction of angiogenic factors: in vivo analysis of tumor-stromal interaction. J. Immunol. 169, 469-475.
132. Etoh, T., Shibuta, K., Barnard, G. F., Kitano, S., Mori, M. (2000) Angiogenin expression in human colorectal cancer: the role of focal macrophage infiltration. Clin. Cancer Res. 6, 3545-3551.
133. Bar, D., Apte, R. N., Voronov, E., Dinarello, C. A., Cohen, S. (2004) A continuous delivery system of IL-1 receptor antagonist reduces angiogenesis and inhibits tumor development. FASEB J. 18, 161-163.
134. Coussens, L. M., Werb, Z. (2002) Inflammation and cancer. Nature 420, 860-867.
135. Ferrara, N., Hillan, K. J., Gerber, H. P., Novotny, W. (2004) Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 3, 391-400.
136. Hiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., Shipley, J. M., Senior, R. M., Shibuya, M. (2002) MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2, 289-300.
137. Burke, B., Tang, N., Corke, K. P., Tazzyman, D., Ameri, K., Wells, M., Lewis, C. E. (2002) Expression of HIF-1α by human macrophages: implications for the use of macrophages in hypoxia-regulated cancer gene therapy. J. Pathol. 196, 204-212.
138. Lewis, J. S., Lee, J. A., Underwood, J. C., Harris, A. L., Lewis, C. E. (1999) Macrophage responses to hypoxia: relevance to disease mechanisms. J. Leukoc. Biol. 66, 889-900.
139. Mole, D. R., Maxwell, P. H., Pugh, C. W., Ratcliffe, P. J. (2001) Regulation of HIF by the von Hippel-Lindau tumor suppressor: implications for cellular oxygen sensing. IUBMB Life 52, 43-47.
140. Leek, R. D., Talks, K. L., Pezzella, F., Turley, H., Campo, L., Brown, N. S., Bicknell, R., Taylor, M., Gatter, K. C., Harris, A. L. (2002) Relation of hypoxia-inducible factor-2 α (HIF-2 α) expression in tumor-infiltrative macrophages to tumor angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res. 62, 1326-1329.
141. Chen, J. J., Yao, P. L., Yuan, A., Hong, T. M., Shun, C. T., Kuo, M. L., Lee, Y. C., Yang, P. C. (2003) Up-regulation of tumor interleukin-8 expression by infiltrating macrophages: its correlation with tumor angiogenesis and patient survival in non-small cell lung cancer. Clin. Cancer Res. 9, 729-737.
142. Sparmann, A., Bar-Sagi, D. (2004) Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 6, 447-458.
143. Fujimoto, J., Aoki, I., Khatun, S., Toyoki, H., Tamaya, T. (2002) Clinical implications of expression of interleukin-8 related to myometrial invasion with angiogenesis in uterine endometrial cancers. Ann. Oncol. 13, 430-434.
144. Fujioka, S., Yoshida, K., Yanagisawa, S., Kawakami, M., Aoki, T., Yamazaki, Y. (2001) Angiogenesis in pancreatic carcinoma: thymidine phosphorylase expression in stromal cells and intratumoral microvessel density as independent predictors of overall and relapse-free survival. Cancer 92, 1788-1797.
145. Lewis, C. E., Leek, R., Harris, A., McGee, J. O. (1995) Cytokine regulation of angiogenesis in breast cancer: the role of tumor-associated macrophages. J. Leukoc. Biol. 57, 747-751.
146. Esposito, I., Menicagli, M., Funel, N., Bergmann, F., Boggi, U., Mosca, F., Bevilacqua, G., Campani, D. (2004) Inflammatory cells contribute to the generation of an angiogenic phenotype in pancreatic ductal adenocarcinoma. J. Clin. Pathol. 57, 630-636.
147. Vestweber, D., Blanks, J. E. (1999) Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev. 79, 181-213.
148. Muller, W. A. (2002) Leukocyte-endothelial cell interactions in the inflammatory response. Lab. Invest. 82, 521-533.
149. Ono, M., Torisu, H., Fukushi, J., Nishie, A., Kuwano, M. (1999) Biological implications of macrophage infiltration in human tumor angiogenesis. Cancer Chemother. Pharmacol. 43 (Suppl.), S69-S71.
150. Leek, R. D., Landers, R., Fox, S. B., Ng, F., Harris, A. L., Lewis, C. E. (1998) Association of tumor necrosis factor α and its receptors with thymidine phosphorylase expression in invasive breast carcinoma. Br. J. Cancer 77, 2246-2251.
151. Huang, S., Van Arsdall, M., Tedjarati, S., McCarty, M., Wu, W., Langley, R., Fidler, I. J. (2002) Contributions of stromal metalloproteinase-9 to
152. Chantrain, C. F., Shimada, H., Jodele, S., Groshen, S., Ye, W., Shalinsky, D. R., Werb, Z., Coussens, L. M., DeClerck, Y. A. (2004) Stromal matrix metalloproteinase-9 regulates the vascular architecture in neuroblastoma by promoting pericyte recruitment. Cancer Res. 64, 1675-1686.
153. Valleala, H., Hanemaaijer, R., Mandelin, J., Salminen, A., Teronen, O., Monkkonen, J., Konttinen, Y. T. (2003) Regulation of MMP-9 (gelatinase B) in activated human monocyte/macrophages by two different types of bisphosphonates. Life Sci. 73, 2413-2420.
154. Hiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., Shipley, J. M., Senior, R. M., Shibuya, M. (2002) MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2, 289-300.
155. Coussens, L. M., Fingleton, B., Matrisian, L. M. (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295, 2387-2392.
156. Hildenbrand, R., Wolf, G., Bohme, B., Bleyl, U., Steinborn, A. (1999) Urokinase plasminogen activator receptor (CD87) expression of tumor-associated macrophages in ductal carcinoma in situ, breast cancer, and resident macrophages of normal breast tissue. J. Leukoc. Biol. 66, 40-49.
157. White, E. S., Flaherty, K. R., Carskadon, S., Brant, A., Iannettoni, M. D., Yee, J., Orringer, M. B., Arenberg, D. A. (2003) Macrophage migration inhibitory factor and CXC chemokine expression in non-small cell lung cancer: role in angiogenesis and prognosis. Clin. Cancer Res. 9, 853-860.
158. Nishihira, J., Ishibashi, T., Fukushima, T., Sun, B., Sato, Y., Todo, S. (2003) Macrophage migration inhibitory factor (MIF): its potential role in tumor growth and tumor-associated angiogenesis. Ann. N. Y. Acad. Sci. 995, 171-182.
159. Seo, K. H., Ko, H. M., Choi, J. H., Jung, H. H., Chun, Y. H., Choi, I. W., Lee, H. K., Im, S. Y. (2004) Essential role for platelet-activating factor-induced NF-κB activation in macrophage-derived angiogenesis. Eur. J. Immunol. 34, 2129-2137.
160. Ongusaha, P. P., Kwak, J. C., Zwible, A. J., Macip, S., Higashiyama, S., Taniguchi, N., Fang, L., Lee, S. W. (2004) HB-EGF is a potent inducer of tumor growth and angiogenesis. Cancer Res. 64, 5283-5290.
161. Uutela, M., Wirzenius, M., Paavonen, K., Rajantie, I., He, Y., Karpanen, T., Lohela, M., Wiig, H., Salven, P., Pajusola, K., Eriksson, U., Alitalo, K. (2004) PDGF-D induces macrophage recruitment, increased interstitial pressure and blood vessel maturation during angiogenesis. Blood 104, 3198-3204.
162. Koch, A. E., Polverini, P. J., Kunkel, S. L., Harlow, L. A., DiPietro, L. A., Elner, V. M., Elner, S. G., Strieter, R. M. (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258, 1798-1801.
163. Eubank, T. D., Galloway, M., Montague, C. M., Waldman, W. J., Marsh, C. B. (2003) M-CSF induces vascular endothelial growth factor production and angiogenic activity from human monocytes. J. Immunol. 171, 2637-2643.
164. Fidler, I. J. (1974) Inhibition of pulmonary metastasis by intravenous injection of specifically activated macrophages. Cancer Res. 34, 1074-1078.
165. Andreesen, R., Hennemann, B., Krause, S. W. (1998) Adoptive immunotherapy of cancer using monocyte-derived macrophages: rationale, current status, and perspectives. J. Leukoc. Biol. 64, 419-426.
166. Lei, H., Ju, D. W., Yu, Y., Tao, Q., Chen, G., Gu, S., Hamada, H., Cao, X. (2000) Induction of potent antitumor response by vaccination with tumor lysate-pulsed macrophages engineered to secrete macrophage colony-stimulating factor and interferon-γ. Gene Ther. 7, 707-713.
167. Griffiths, L., Binley, K., Iqball, S., Kan, O., Maxwell, P., Ratcliffe, P., Lewis, C., Harris, A., Kingsman, S., Naylor, S. (2000) The macrophage - a novel system to deliver gene therapy to pathological hypoxia. Gene Ther. 7, 255-262.
168. Burke, B., Sumner, S., Maitland, N., Lewis, C. E. (2002) Macrophages in gene therapy: cellular delivery vehicles and in vivo targets. J. Leukoc. Biol. 72, 417-428.
169. Paul, S., Snary, D., Hoebeke, J., Allen, D., Balloul, J. M., Bizouarne, N., Dott, K., Geist, M., Hilgers, J., Kieny, M. P., Burchell, J., Taylor-Papadimitriou, J., Acres, R. B. (2000) Targeted macrophage cytotoxicity using a nonreplicative live vector expressing a tumor-specific single-chain variable region fragment. Hum. Gene Ther. 11, 1417-1428.
170. Rosenberg, S. A., Yang, J. C., Restifo, N. P. (2004) Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10, 909-915.
171. Dirkx, A. E., oude Egbrink, M. G., Castermans, K., van der Schaft, D. W., Thijssen, V. L., Dings, R. P., Kwee, L., Mayo, K. H., Wagstaff, J., Bouma-ter Steege, J. C., Griffioen, A. W. (2006) Anti-angiogenesis therapy can overcome endothelial cell anergy and promote leukocyte-endothelium interactions and infiltration in tumors. FASEB J. 20, 621-630.