Top

Published in:

01-03-2008

Inflammation, inflammatory cells and angiogenesis: decisions and indecisions

Authors: Douglas M. Noonan, Andrea De Lerma Barbaro, Nicola Vannini, Lorenzo Mortara, Adriana Albini

Published in: Cancer and Metastasis Reviews | Issue 1/2008

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.

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

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

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

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

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

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

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

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

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

10.

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

11.

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

12.

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

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

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

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

16.

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

17.

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

18.

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

19.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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.

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

35.

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

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

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

38.

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

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

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

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

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.

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.

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

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

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

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

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.

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

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

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

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

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

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

56.

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

57.

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

58.

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

59.

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

60.

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

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

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

63.

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

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

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

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

67.

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

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.PubMedCrossRef

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

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

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.

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

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

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.

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

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

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

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

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.

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.

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

84.

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

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

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

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

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

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

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

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

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

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.

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

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

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.

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

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.

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

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

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

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

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

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

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.

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

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

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.

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

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

111.

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

112.

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

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

Title: Inflammation, inflammatory cells and angiogenesis: decisions and indecisions
Authors: Douglas M. Noonan
Andrea De Lerma Barbaro
Nicola Vannini
Lorenzo Mortara
Adriana Albini
Publication date: 01-03-2008
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 1/2008
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-007-9108-5

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2008

A “class action” against the microenvironment: do cancer cells cooperate in metastasis?

The bone microenvironment in metastasis; what is special about bone?

Chemotherapy and the tumor microenvironment: the contribution of circulating endothelial cells

Tumor microenvironment, a dangerous society leading to cancer metastasis. From mechanisms to therapy and prevention

Osteopontin: regulation in tumor metastasis

Bio

Keynote webinar | Spotlight on antibody–drug conjugates in cancer