Skip to main content

Advertisement

Log in

Inflammation, inflammatory cells and angiogenesis: decisions and indecisions

  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Abstract

Endothelial-immune cell cross-talk goes well beyond leukocyte and lymphocyte trafficking, since immune cells are able to intimately regulate vessel formation and function. Here we review the evidence that most immune cells are capable of polarization towards a dichotomous activity either inducing or inhibiting angiogenesis. In addition to the well-known roles of tumor associated macrophages, we find that neutrophils, myeloid-derived suppressor and dendritic cells clearly have the potential for influencing tumor angiogenesis. Further, the physiological functions of NK cells suggest that these cells may also show a potentially important role in pro- or anti-angiogenesis regulation within the tumor microenvironment. At the same time many angiogenic factors influence the activity and function of immune cells that generally favor tumor survival and tolerance. Thus the immune system itself represents a major pharmaceutical target and links angiogenesis inhibition to immunotherapy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Kerbel, R., & Folkman, J. (2002). Clinical translation of angiogenesis inhibitors. Nature Reviews. Cancer, 2, 727–739.

    PubMed  CAS  Google Scholar 

  2. Viloria-Petit, A., Crombet, T., Jothy, S., Hicklin, D., Bohlen, P., Schlaeppi, J. M., et al. (2001). Acquired resistance to the antitumor effect of epidermal growth factor receptor-blocking antibodies in vivo: A role for altered tumor angiogenesis. Cancer Research, 61, 5090–5101.

    PubMed  CAS  Google Scholar 

  3. Casanovas, O., Hicklin, D. J., Bergers, G., & Hanahan, D. (2005). Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell, 8, 299–309.

    PubMed  CAS  Google Scholar 

  4. Dorrell, M. I., Aguilar, E., Scheppke, L., Barnett, F. H., & Friedlander, M. (2007). Combination angiostatic therapy completely inhibits ocular and tumor angiogenesis. Proceedings of the National Academy of Sciences of the United States of America, 104, 967–972.

    PubMed  CAS  Google Scholar 

  5. Folkman, J. (2007). Angiogenesis: An organizing principle for drug discovery? Nature Reviews Drug Discovery, 6, 273–286.

    PubMed  CAS  Google Scholar 

  6. Folkman, J. (2006). Angiogenesis. Annual Review of Medicine, 57, 1–18.

    PubMed  CAS  Google Scholar 

  7. 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.

    PubMed  CAS  Google Scholar 

  8. Balkwill, F., & Mantovani, A. (2001). Inflammation and cancer: Back to Virchow? Lancet, 357, 539–545.

    PubMed  CAS  Google Scholar 

  9. Pollard, J. W. (2004). Tumour-educated macrophages promote tumour progression and metastasis. Nature Reviews. Cancer, 4, 71–78.

    PubMed  CAS  Google Scholar 

  10. Orimo, A., & Weinberg, R. A. (2006). Stromal fibroblasts in cancer: A novel tumor-promoting cell type. Cell Cycle, 5, 1597–1601.

    PubMed  CAS  Google Scholar 

  11. Brigati, C., Noonan, D. M., Albini, A., & Benelli, R. (2002). Tumors and inflammatory infiltrates: Friends or foes? Clinical & Experimental Metastasis, 19, 247–258.

    CAS  Google Scholar 

  12. Coussens, L. M., & Werb, Z. (2002). Inflammation and cancer. Nature, 420, 860–867.

    PubMed  CAS  Google Scholar 

  13. 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.

    PubMed  Google Scholar 

  14. Lin, E. Y., & Pollard, J. W. (2004). Macrophages: Modulators of breast cancer progression. Novartis Foundation Symposium, 256, 158–168 discussion 168–172, 259–169.

    PubMed  CAS  Google Scholar 

  15. Biswas, S. K., Gangi, L., Paul, S., Schioppa, T., Saccani, A., Sironi, M., et al. (2006). A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation). Blood, 107, 2112–2122.

    PubMed  CAS  Google Scholar 

  16. Murdoch, C., Muthana, M., & Lewis, C. E. (2005). Hypoxia regulates macrophage functions in inflammation. Journal of Immunology, 175, 6257–6263.

    CAS  Google Scholar 

  17. Egeblad, M., & Werb, Z. (2002). New functions for the matrix metalloproteinases in cancer progression. Nature Reviews. Cancer, 2, 161–174.

    PubMed  CAS  Google Scholar 

  18. Balkwill, F. (2006). TNF-alpha in promotion and progression of cancer. Cancer and Metastasis Reviews, 25, 409–416.

    PubMed  CAS  Google Scholar 

  19. Bronte, V., & Zanovello, P. (2005). Regulation of immune responses by l-arginine metabolism. Nature Reviews. Immunology, 5, 641–654.

    PubMed  CAS  Google Scholar 

  20. Sawano, A., Iwai, S., Sakurai, Y., Ito, M., Shitara, K., Nakahata, T., et al. (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.

    PubMed  CAS  Google Scholar 

  21. Barleon, B., Sozzani, S., Zhou, D., Weich, H. A., Mantovani, A., & Marme, D. (1996). Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood, 87, 3336–3343.

    PubMed  CAS  Google Scholar 

  22. Clauss, M., Weich, H., Breier, G., Knies, U., Rockl, W., Waltenberger, J., et al. (1996). The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. Journal of Biological Chemistry, 271, 17629–17634.

    PubMed  CAS  Google Scholar 

  23. Aplin, A. C., Gelati, M., Fogel, E., Carnevale, E., & Nicosia, R. F. (2006). Angiopoietin-1 and vascular endothelial growth factor induce expression of inflammatory cytokines before angiogenesis. Physiological Genomics, 27, 20–28.

    PubMed  CAS  Google Scholar 

  24. Di Carlo, E., Forni, G., Lollini, P., Colombo, M. P., Modesti, A., & Musiani, P. (2001). The intriguing role of polymorphonuclear neutrophils in antitumor reactions. Blood, 97, 339–345.

    PubMed  Google Scholar 

  25. Heryanto, B., Girling, J. E., & Rogers, P. A. (2004). Intravascular neutrophils partially mediate the endometrial endothelial cell proliferative response to oestrogen in ovariectomised mice. Reproduction, 127, 613–620.

    PubMed  CAS  Google Scholar 

  26. Gargett, C. E., Lederman, F., Heryanto, B., Gambino, L. S., & Rogers, P. A. (2001). Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neutrophils. Human Reproduction, 16, 1065–1075.

    PubMed  CAS  Google Scholar 

  27. Na, Y. J., Yang, S. H., Baek, D. W., Lee, D. H., Kim, K. H., Choi, Y. M., et al. (2006). Effects of peritoneal fluid from endometriosis patients on the release of vascular endothelial growth factor by neutrophils and monocytes. Human Reproduction, 21, 1846–1855.

    PubMed  CAS  Google Scholar 

  28. Lin, Y. J., Lai, M. D., Lei, H. Y., & Wing, L. Y. (2006). Neutrophils and macrophages promote angiogenesis in the early stage of endometriosis in a mouse model. Endocrinology, 147, 1278–1286.

    PubMed  CAS  Google Scholar 

  29. Schruefer, R., Sulyok, S., Schymeinsky, J., Peters, T., Scharffetter-Kochanek, K., & Walzog, B. (2006). The proangiogenic capacity of polymorphonuclear neutrophils delineated by microarray technique and by measurement of neovascularization in wounded skin of CD18-deficient mice. Journal of Vascular Research, 43, 1–11.

    PubMed  CAS  Google Scholar 

  30. Benelli, R., Barbero, A., Ferrini, S., Scapini, P., Cassatella, M., Bussolino, F., et al. (2000). Human Immunodeficiency Virus Transactivator Protein (Tat) stimulates chemotaxis, calcium mobilization, and activation of human polymorphonuclear leukocytes: Implications for Tat-mediated pathogenesis. Journal of Infectious Diseases, 182, 1643–1651.

    PubMed  CAS  Google Scholar 

  31. Kibbey, M. C., Corcoran, M. L., Wahl, L. M., & Kleinman, H. K. (1994). Laminin SIKVAV peptide induced angiogenesis in vivo is potentiated by neutrophils. Journal of Cellular Physiology, 160, 185–193.

    PubMed  CAS  Google Scholar 

  32. Benelli, R., Morini, M., Carrozzino, F., Ferrari, N., Minghelli, S., Santi, L., et al. (2002). Neutrophils as a key cellular target for angiostatin: Implications for regulation of angiogenesis and inflammation. FASEB Journal, 16, 267–269.

    PubMed  CAS  Google Scholar 

  33. Scapini, P., Morini, M., Tecchio, C., Minghelli, S., Di Carlo, E., Tanghetti, E., et al. (2004). CXCL1/macrophage inflammatory protein-2-induced angiogenesis in vivo is mediated by neutrophil-derived vascular endothelial growth factor-A. Journal of Immunology, 172, 5034–5040.

    CAS  Google Scholar 

  34. Ohki, Y., Heissig, B., Sato, Y., Akiyama, H., Zhu, Z., Hicklin, D. J., et al. (2005). Granulocyte colony-stimulating factor promotes neovascularization by releasing vascular endothelial growth factor from neutrophils. FASEB Journal, 19, 2005–2007.

    PubMed  CAS  Google Scholar 

  35. Coussens, L. M., & Werb, Z. (2001). Inflammatory cells and cancer: Think different!. Journal of Experimental Medicine, 193, F23–F26.

    PubMed  CAS  Google Scholar 

  36. 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.

    PubMed  CAS  Google Scholar 

  37. Nozawa, H., Chiu, C., & Hanahan, D. (2006). Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proceedings of the National Academy of Sciences of the United States of America, 103, 12493–12498.

    PubMed  CAS  Google Scholar 

  38. Karin, M. (2005). Inflammation and cancer: The long reach of Ras. Nature Medicine, 11, 20–21.

    PubMed  CAS  Google Scholar 

  39. 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.

    PubMed  CAS  Google Scholar 

  40. Cassatella, M. A. (2006). On the production of TNF-related apoptosis-inducing ligand (TRAIL/Apo-2L) by human neutrophils. Journal of Leukocyte Biology, 79, 1140–1149.

    PubMed  CAS  Google Scholar 

  41. Tsuda, Y., Takahashi, H., Kobayashi, M., Hanafusa, T., Herndon, D. N., & Suzuki, F. (2004). Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity, 21, 215–226.

    PubMed  CAS  Google Scholar 

  42. Benelli, R., Albini, A., & Noonan, D. (2003). Neutrophils and angiogenesis: Potential initiators of the angiogenic cascade. In M. Cassatella (Ed.) The neutrophil (vol. vol. 83, (pp. 167–181)). Basel: Karger.

    Google Scholar 

  43. Scapini, P., Nesi, L., Morini, M., Tanghetti, E., Belleri, M., Noonan, D., et al. (2002). Generation of biologically active angiostatin kringle 1–3 by activated human neutrophils. Journal of Immunology, 168, 5798–5804.

    CAS  Google Scholar 

  44. Kaipainen, A., Kieran, M. W., Huang, S., Butterfield, C., Bielenberg, D., Mostoslavsky, G., et al. (2007). PPARalpha deficiency in inflammatory cells suppresses tumor growth. PLoS ONE, 2, e260.

    PubMed  Google Scholar 

  45. Cui, Z., Willingham, M. C., Hicks, A. M., Alexander-Miller, M. A., Howard, T. D., Hawkins, G. A., et al. (2003). Spontaneous regression of advanced cancer: Identification of a unique genetically determined, age-dependent trait in mice. Proceedings of the National Academy of Sciences of the United States of America, 100, 6682–6687.

    PubMed  CAS  Google Scholar 

  46. Hicks, A. M., Riedlinger, G., Willingham, M. C., Alexander-Miller, M. A., Von Kap-Herr, C., Pettenati, M. J., et al. (2006). Transferable anticancer innate immunity in spontaneous regression/complete resistance mice. Proceedings of the National Academy of Sciences of the United States of America, 103, 7753–7758.

    PubMed  CAS  Google Scholar 

  47. Hicks, A. M., Willingham, M. C., Du, W., Pang, C. S., Old, L. J., & Cui, Z. (2006). Effector mechanisms of the anti-cancer immune responses of macrophages in SR/CR mice. Cancer Immunity, 6, 11.

    PubMed  Google Scholar 

  48. Donà, M., Dell’Aica, I., Calabrese, F., Benelli, R., Morini, M., Albini, A., et al. (2003). Neutrophil restraint by green tea: Inhibition of inflammation, associated angiogenesis, and pulmonary fibrosis. Journal of Immunology, 170, 4335–4341.

    Google Scholar 

  49. Dell’Aica, I., Niero, R., Piazza, F., Cabrelle, A., Sartor, L., Colalto, C., et al. (2007). Hyperforin blocks neutrophil activation of matrix metalloproteinase-9, motility and recruitment, and restrains inflammation-triggered angiogenesis and lung fibrosis. Journal of Pharmacology and Experimental Therapeutics, 321, 492–500.

    PubMed  CAS  Google Scholar 

  50. Dell’Aica, I., Sartor, L., Galletti, P., Giacomini, D., Quintavalla, A., Calabrese, F., et al. (2006). Inhibition of leukocyte elastase, polymorphonuclear chemoinvasion, and inflammation-triggered pulmonary fibrosis by a 4-alkyliden-beta-lactam with a galloyl moiety. Journal of Pharmacology and Experimental Therapeutics, 316, 539–546.

    PubMed  CAS  Google Scholar 

  51. O’Reilly, M. S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R. A., Moses, M., et al. (1994). Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell, 79, 315–328.

    PubMed  CAS  Google Scholar 

  52. Benelli, R., Morini, M., Brigati, C., Noonan, D. M., & Albini, A. (2003). Angiostatin inhibits extracellular HIV-Tat-induced inflammatory angiogenesis. International Journal of Oncology, 22, 87–91.

    PubMed  CAS  Google Scholar 

  53. Chavakis, T., Athanasopoulos, A., Rhee, J. S., Orlova, V., Schmidt-Woll, T., Bierhaus, A., et al. (2005). Angiostatin is a novel anti-inflammatory factor by inhibiting leukocyte recruitment. Blood, 105, 1036–1043.

    PubMed  CAS  Google Scholar 

  54. Perri, S. R., Annabi, B., & Galipeau, J. (2007). Angiostatin inhibits monocyte/macrophage migration via disruption of actin cytoskeleton. FASEB Journal (in press).

  55. Perri, S. R., Nalbantoglu, J., Annabi, B., Koty, Z., Lejeune, L., Francois, M., et al. (2005). Plasminogen kringle 5-engineered glioma cells block migration of tumor-associated macrophages and suppress tumor vascularization and progression. Cancer Research, 65, 8359–8365.

    PubMed  CAS  Google Scholar 

  56. Albini, A., Noonan, D. M., & Ferrari, N. (2007). Molecular pathways for cancer angioprevention. Clinical Cancer Research, 13, 4320–4325.

    PubMed  CAS  Google Scholar 

  57. Albini, A., & Sporn, M. B. (2007). The tumour microenvironment as a target for chemoprevention. Nature Reviews. Cancer, 7, 139–147.

    PubMed  CAS  Google Scholar 

  58. Noonan, D. M., Benelli, R., & Albini, A. (2007). Angiogenesis and cancer prevention: A vision. Recent Results in Cancer Research, 174, 219–224.

    PubMed  CAS  Google Scholar 

  59. Albini, A., Tosetti, F., Benelli, R., & Noonan, D. M. (2005). Tumor inflammatory angiogenesis and its chemoprevention. Cancer Research, 65, 10637–10641.

    PubMed  CAS  Google Scholar 

  60. Karin, M. (2006). Nuclear factor-kappaB in cancer development and progression. Nature, 441, 431–436.

    PubMed  CAS  Google Scholar 

  61. Goebel, S., Huang, M., Davis, W. C., Jennings, M., Siahaan, T. J., Alexander, J. S., et al. (2006). VEGF-A stimulation of leukocyte adhesion to colonic microvascular endothelium: Implications for inflammatory bowel disease. American Journal of Physiology: Gastrointestinal and Liver Physiology, 290, G648–G654.

    PubMed  CAS  Google Scholar 

  62. Melder, R. J., Koenig, G. C., Munn, L. L., & Jain, R. K. (1996). Adhesion of activated natural killer cells to tumor necrosis factor-alpha-treated endothelium under physiological flow conditions. Natural Immunity, 15, 154–163.

    PubMed  Google Scholar 

  63. Ferrara, N. (1996). Natural killer cells, adhesion and tumor angiogenesis. Nature Medicine, 2, 971–972.

    PubMed  CAS  Google Scholar 

  64. 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.

    PubMed  CAS  Google Scholar 

  65. Yao, L., Sgadari, C., Furuke, K., Bloom, E. T., Teruya-Feldstein, J., & Tosato, G. (1999). Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood, 93, 1612–1621.

    PubMed  CAS  Google Scholar 

  66. Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron, S., et al. (2006). Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nature Medicine, 12, 1065–1074.

    PubMed  CAS  Google Scholar 

  67. Chaouat, G., Ledee-Bataille, N., Chea, K. B., & Dubanchet, S. (2005). Cytokines and implantation. Chemical Immunology and Allergy, 88, 34–63.

    Article  PubMed  CAS  Google Scholar 

  68. Chaouat, G., Ledee-Bataille, N., & Dubanchet, S. (2007). Immune cells in uteroplacental tissues throughout pregnancy: A brief review. Reproductive Biomedicine Online, 14, 256–266.

    Article  PubMed  CAS  Google Scholar 

  69. Coudert, J. D., Zimmer, J., Tomasello, E., Cebecauer, M., Colonna, M., Vivier, E., et al. (2005). Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood, 106, 1711–1717.

    PubMed  CAS  Google Scholar 

  70. Loza, M. J., Peters, S. P., Zangrilli, J. G., & Perussia, B. (2002). Distinction between IL-13+ and IFN-gamma+ natural killer cells and regulation of their pool size by IL-4. European Journal of Immunology, 32, 413–423.

    PubMed  CAS  Google Scholar 

  71. Marcenaro, E., Della Chiesa, M., Bellora, F., Parolini, S., Millo, R., Moretta, L., et al. (2005). IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. Journal of Immunology, 174, 3992–3998.

    CAS  Google Scholar 

  72. Keskin, D. B., Allan, D. S., Rybalov, B., Andzelm, M. M., Stern, J. N., Kopcow, H. D., et al. (2007). TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proceedings of the National Academy of Sciences of the United States of America, 104, 3378–3383.

    PubMed  CAS  Google Scholar 

  73. Carrega, P., Morandi, B., Costa, R., Frumento, G., Forte, G., Altavilla, G., et al. (2007). Natural killer cells infiltrating human non-small cell lung cancer are enriched in CD56brightCD16-cells and display an impaired capability to kill tumor cells. Cancer (in press).

  74. Morini, M., Albini, A., Lorusso, G., Moelling, K., Lu, B., Cilli, M., et al. (2004). Prevention of angiogenesis by naked DNA IL-12 gene transfer: Angioprevention by immunogene therapy. Gene Therapy, 11, 284–291.

    PubMed  CAS  Google Scholar 

  75. Shi, X., Cao, S., Mitsuhashi, M., Xiang, Z., & Ma, X. (2004). Genome-wide analysis of molecular changes in IL-12-induced control of mammary carcinoma via IFN-gamma-independent mechanisms. Journal of Immunology, 172, 4111–4122.

    CAS  Google Scholar 

  76. Faggioli, F., Soldati, S., Scanziani, E., Cato, E. M., Adorni, F., Vezzoni, P., et al. (2007). Effects of IL-12 gene therapy on spontaneous transgenic and transplanted breast tumors. Breast Cancer Research and Treatment (in press).

  77. Serafini, P., Borrello, I., & Bronte, V. (2006). Myeloid suppressor cells in cancer: Recruitment, phenotype, properties, and mechanisms of immune suppression. Seminars in Cancer Biology, 16, 53–65.

    PubMed  CAS  Google Scholar 

  78. Gallina, G., Dolcetti, L., Serafini, P., De Santo, C., Marigo, I., Colombo, M. P., et al. (2006). Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. Journal of Clinical Investigation, 116, 2777–2790.

    PubMed  CAS  Google Scholar 

  79. Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., et al. (2004). Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell, 6, 409–421.

    PubMed  CAS  Google Scholar 

  80. Bronte, V., Apolloni, E., Cabrelle, A., Ronca, R., Serafini, P., Zamboni, P., et al. (2000). Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood, 96, 3838–3846.

    PubMed  CAS  Google Scholar 

  81. Song, X., Krelin, Y., Dvorkin, T., Bjorkdahl, O., Segal, S., Dinarello, C. A., et al. (2005). CD11b+/Gr-1+ immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1beta-secreting cells. Journal of Immunology, 175, 8200–8208.

    CAS  Google Scholar 

  82. 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.

    CAS  Google Scholar 

  83. Valenti, R., Huber, V., Filipazzi, P., Pilla, L., Sovena, G., Villa, A., et al. (2006). Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Research, 66, 9290–9298.

    PubMed  CAS  Google Scholar 

  84. O’Garra, A., & Vieira, P. (2004). Regulatory T cells and mechanisms of immune system control. Nature Medicine, 10, 801–805.

    PubMed  CAS  Google Scholar 

  85. Marie, J. C., Letterio, J. J., Gavin, M., & Rudensky, A. Y. (2005). TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. Journal of Experimental Medicine, 201, 1061–1067.

    PubMed  CAS  Google Scholar 

  86. Huang, B., Pan, P. Y., Li, Q., Sato, A. I., Levy, D. E., Bromberg, J., et al. (2006). Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Research, 66, 1123–1131.

    PubMed  CAS  Google Scholar 

  87. Qin, Z., & Blankenstein, T. (2000). CD4+ T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity, 12, 677–686.

    PubMed  CAS  Google Scholar 

  88. Qin, Z., Schwartzkopff, J., Pradera, F., Kammertoens, T., Seliger, B., Pircher, H., et al. (2003). A critical requirement of interferon gamma-mediated angiostasis for tumor rejection by CD8+ T cells. Cancer Research, 63, 4095–4100.

    PubMed  CAS  Google Scholar 

  89. Gupta, S., Joshi, K., Wig, J. D., & Arora, S. K. (2007). Intratumoral FOXP3 expression in infiltrating breast carcinoma: Its association with clinicopathologic parameters and angiogenesis. Acta Oncológica, 46, 792–797.

    PubMed  CAS  Google Scholar 

  90. Degli-Esposti, M. A., & Smyth, M. J. (2005). Close encounters of different kinds: Dendritic cells and NK cells take centre stage. Nature Reviews. Immunology, 5, 112–124.

    PubMed  CAS  Google Scholar 

  91. Ludwig, I. S., Geijtenbeek, T. B., & van Kooyk, Y. (2006). Two way communication between neutrophils and dendritic cells. Current Opinion in Pharmacology, 6, 408–413.

    PubMed  CAS  Google Scholar 

  92. Tettamanti, G., Malagoli, D., Benelli, R., Albini, A., Grimaldi, A., Perletti, G., et al. (2006). Growth factors and chemokines: A comparative functional approach between invertebrates and vertebrates. Current Medicinal Chemistry, 13, 2737–2750.

    PubMed  CAS  Google Scholar 

  93. Sozzani, S., Rusnati, M., Riboldi, E., Mitola, S., & Presta, M. (2007). Dendritic cell-endothelial cell cross-talk in angiogenesis. Trends in Immunology, 28, 385–392.

    Google Scholar 

  94. Gabrilovich, D. I., Chen, H. L., Girgis, K. R., Cunningham, H. T., Meny, G. M., Nadaf, S., et al. (1996). Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nature Medicine, 2, 1096–1103.

    PubMed  CAS  Google Scholar 

  95. Almand, B., Resser, J. R., Lindman, B., Nadaf, S., Clark, J. I., Kwon, E. D., et al. (2000). Clinical significance of defective dendritic cell differentiation in cancer. Clinical Cancer Research, 6, 1755–1766.

    PubMed  CAS  Google Scholar 

  96. Dikov, M. M., Ohm, J. E., Ray, N., Tchekneva, E. E., Burlison, J., Moghanaki, D., et al. (2005). Differential roles of vascular endothelial growth factor receptors 1 and 2 in dendritic cell differentiation. Journal of Immunology, 174, 215–222.

    CAS  Google Scholar 

  97. Laxmanan, S., Robertson, S. W., Wang, E., Lau, J. S., Briscoe, D. M., & Mukhopadhyay, D. (2005). Vascular endothelial growth factor impairs the functional ability of dendritic cells through Id pathways. Biochemical and Biophysical Research Communications, 334, 193–198.

    PubMed  CAS  Google Scholar 

  98. Okunishi, K., Dohi, M., Nakagome, K., Tanaka, R., Mizuno, S., Matsumoto, K., et al. (2005). A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function. Journal of Immunology, 175, 4745–4753.

    CAS  Google Scholar 

  99. Marteau, F., Gonzalez, N. S., Communi, D., Goldman, M., Boeynaems, J. M., & Communi, D. (2005). Thrombospondin-1 and indoleamine 2,3-dioxygenase are major targets of extracellular ATP in human dendritic cells. Blood, 106, 3860–3866.

    PubMed  CAS  Google Scholar 

  100. Xia, C. Q., & Kao, K. J. (2003). Effect of CXC chemokine platelet factor 4 on differentiation and function of monocyte-derived dendritic cells. International Immunology, 15, 1007–1015.

    PubMed  CAS  Google Scholar 

  101. Shellenberger, T. D., Wang, M., Gujrati, M., Jayakumar, A., Strieter, R. M., Burdick, M. D., et al. (2004). BRAK/CXCL14 is a potent inhibitor of angiogenesis and a chemotactic factor for immature dendritic cells. Cancer Research, 64, 8262–8270.

    PubMed  CAS  Google Scholar 

  102. Renkl, A. C., Wussler, J., Ahrens, T., Thoma, K., Kon, S., Uede, T., et al. (2005). Osteopontin functionally activates dendritic cells and induces their differentiation toward a Th1-polarizing phenotype. Blood, 106, 946–955.

    PubMed  CAS  Google Scholar 

  103. Shinohara, M. L., Lu, L., Bu, J., Werneck, M. B., Kobayashi, K. S., Glimcher, L. H., et al. (2006). Osteopontin expression is essential for interferon-alpha production by plasmacytoid dendritic cells. Nature Immunology, 7, 498–506.

    PubMed  CAS  Google Scholar 

  104. Weiss, J. M., Renkl, A. C., Maier, C. S., Kimmig, M., Liaw, L., Ahrens, T., et al. (2001). Osteopontin is involved in the initiation of cutaneous contact hypersensitivity by inducing Langerhans and dendritic cell migration to lymph nodes. Journal of Experimental Medicine, 194, 1219–1229.

    PubMed  CAS  Google Scholar 

  105. Riboldi, E., Musso, T., Moroni, E., Urbinati, C., Bernasconi, S., Rusnati, M., et al. (2005). Cutting edge: Proangiogenic properties of alternatively activated dendritic cells. Journal of Immunology, 175, 2788–2792.

    CAS  Google Scholar 

  106. Geissmann, F., Revy, P., Brousse, N., Lepelletier, Y., Folli, C., Durandy, A., et al. (2003). Retinoids regulate survival and antigen presentation by immature dendritic cells. Journal of Experimental Medicine, 198, 623–634.

    PubMed  CAS  Google Scholar 

  107. Curiel, T. J., Cheng, P., Mottram, P., Alvarez, X., Moons, L., Evdemon-Hogan, M., et al. (2004). Dendritic cell subsets differentially regulate angiogenesis in human ovarian cancer. Cancer Research, 64, 5535–5538.

    PubMed  CAS  Google Scholar 

  108. Bourbie-Vaudaine, S., Blanchard, N., Hivroz, C., & Romeo, P. H. (2006). Dendritic cells can turn CD4+ T lymphocytes into vascular endothelial growth factor-carrying cells by intercellular neuropilin-1 transfer. Journal of Immunology, 177, 1460–1469.

    CAS  Google Scholar 

  109. Coukos, G., Benencia, F., Buckanovich, R. J., & Conejo-Garcia, J. R. (2005). The role of dendritic cell precursors in tumour vasculogenesis. British Journal of Cancer, 92, 1182–1187.

    PubMed  CAS  Google Scholar 

  110. De Palma, M., & Naldini, L. (2006). Role of haematopoietic cells and endothelial progenitors in tumour angiogenesis. Biochimica et Biophysica Acta, 1766, 159–166.

    PubMed  Google Scholar 

  111. Morelli, A. E., & Thomson, A. W. (2007). Tolerogenic dendritic cells and the quest for transplant tolerance. Nature Reviews. Immunology, 7, 610–621.

    PubMed  CAS  Google Scholar 

  112. Macpherson, A. J., & Harris, N. L. (2004). Interactions between commensal intestinal bacteria and the immune system. Nature Reviews. Immunology, 4, 478–485.

    PubMed  CAS  Google Scholar 

  113. Hooper, L. V., Stappenbeck, T. S., Hong, C. V., & Gordon, J. I. (2003). Angiogenins: A new class of microbicidal proteins involved in innate immunity. Nature Immunology, 4, 269–273.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors were supported by grants from the AIRC, MUIR Cofin, Compagnia San Paolo, Funds of the University of Insubria. Nicola Vannini is in the Immunopathology and Degenerative disease PhD program at the faculty of Medicine, University of Insubria, Varese.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Douglas M. Noonan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Noonan, D.M., De Lerma Barbaro, A., Vannini, N. et al. Inflammation, inflammatory cells and angiogenesis: decisions and indecisions. Cancer Metastasis Rev 27, 31–40 (2008). https://doi.org/10.1007/s10555-007-9108-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-007-9108-5

Keywords

Navigation