Simultaneous blockade of VEGFR-1 and VEGFR-2 activation is necessary to efficiently inhibit experimental melanoma growth and metastasis formation

International Journal of Cancer

Volumn 120, Issue 9, 2007, Pages 1899-1908

  Gille, Jens ^a,b,g   Heidenreich, Regina ^b,c   Pinter, Andreas ^a   Schmitz, Judith ^b   Boehme, Beatrice ^a   Hicklin, Daniel J ^d   Henschler, Reinhard ^e   Breier, Georg ^b,f  

^a GOETHE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d ELI LILLY AND COMPANY   (United States)

^e Red Cross Blood Donor Service   (Germany)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^g UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Experimental melanoma; Neoplasm metastasis; Pathologic neovascularization; Vascular endothelial growth factor receptors

Indexed keywords

CD45 ANTIGEN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER MODEL; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATORY INFILTRATE; LUNG METASTASIS; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; TUMOR VASCULARIZATION;

ANIMALS; ANTIGENS, CD45; HEMATOPOIETIC STEM CELL MOBILIZATION; HUMANS; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; RETROVIRIDAE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 33947191124     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22531     Document Type: Article

References (57)

1. Chudnovsky Y, Khavari PA, Adams AE. Melanoma genetics and the development of rational therapeutics. J Clin Invest 2005;115:813-24.
2. Fidler IJ. The organ microenvironment and cancer metastasis. Differentiation 2002;70:498-505.
3. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature 2001;411:375-9.
4. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420: 860-7.
5. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 2000;103:481-90.
6. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M. MMP9 induction by vascular endothelial growth factor receptor-1 is involved in lung-specific metastasis. Cancer Cell 2002;2:289-300.
7. Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001;7:1194-201.
8. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med 2003;9:789-95.
9. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, Moore MA, Rafii S. Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 2001;193:1005-14.
10. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002;109: 625-37.
11. Jabbour HN, Boddy SC, Lincoln GA. Pattern and localisation of expression of vascular endothelial growth factor and its receptor flt-1 in the ovine pituitary gland: expression is independent of hypothalamic control. Mol Cell Endocrinol 1997;134:91-100.
12. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76.
13. Kerbel R, Folkman J. Clinical translation of angiogenesis inhibitors. Nat Rev Cancer 2002;2:727-39.
14. Millauer B, Shawver LK, Plate KH, Risau W, Ullrich A. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 1994;367:576-9.
15. Millauer B, Longhi MP, Plate KH, Shawver LK, Risau W, Ullrich A, Strawn LM. Dominant-negative inhibition of Flk-1 suppresses the growth of many tumor types in vivo. Cancer Res 1996;56:1615-20.
16. Prewett M, Huber J, Li Y, Santiago A, O'Connor W, King K, Overholser J, Hooper A, Pytowski B, Witte L, Bohlen P, Hicklin DJ. Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer Res 1999;59:5209-18.
17. Izumi Y, di Tomaso E, Hooper A, Huang P, Huber J, Hicklin DJ, Fukumura D, Jain RK, Suit HD. Responses to antiangiogenesis treatment of spontaneous autochthonous tumors and their isografts. Cancer Res 2003;63:747-51.
18. Heidenreich R, Machein M, Nicolaus A, Hilbig A, Wild C, Clauss M, Plate KH, Breier G. Inhibition of solid tumor growth by gene transfer of VEGF receptor-1 mutants. Int J Cancer 2004;111:348-57.
19. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, et al. Revascularization of ischemic tissues by PIGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 2002;8:831-40.
20. Markowitz DGS, Bank A. A safe packaging line for gene transfer: separating viral genes on two different plasmids. J Virol 1988;62:1120-4.
21. Vecchi A, Garlanda C, Lampugnani MG, Resnati M, Matteucci C, Stoppacciaro A, Schnurch H, Risau W, Ruco L, Mantovani A, Dejana E. Monoclonal antibodies specific for endothelial cells of mouse blood vessels. Their application in the identification of adult and embryonic endothelium. Eur J Cell Biol 1994;63:247-54.
22. Kataoka H, Takakura N, Nishikawa S, Tsuchida K, Kodama H, Kunisada T, Risau W, Kita T, Nishikawa SI. Expressions of PDGF receptor α, c-Kit and Flk1 genes clustering in mouse chromosome 5 define distinct subsets of nascent mesodermal cells. Dev Growth Differ 1997;39:729-40.
23. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, Mildner-Rihm C, Martin H, Zeiher AM, Dimmeler S. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood 2003;102:1340-6.
24. Vasa M, Fichtlscherer S, Adler K, Aicher A, Martin H, Zeiher AM, Dimmeler S. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 2001;103:2885-90.
25. Heidenreich R, Kappel A, Breier G. Tumor endothelium-specific transgene expression directed by vascular endothelial growth factor receptor-2 (Flk-1) promoter/enhancer sequences. Cancer Res 2000;60: 6142-7.
26. Ludwig RJ, Boehme B, Podda M, Henschler R, Jager E, Tandi C, Boehncke WH, Zollner TM, Kaufmann R, Gille J. Endothelial P-selectin as a target of heparin action in experimental melanoma lung metastasis. Cancer Res 2004;64:2743-50.
27. Lacal PM, Failla CM, Pagani E, Odorisio T, Schietroma C, Falcinelli S, Zambruno G, D'Atri S. Human melanoma cells secrete and respond to placenta growth factor and vascular endothelial growth factor. J Invest Dermatol 2000;115:1000-7.
28. Liu B, Earl HM, Baban D, Shoaibi M, Fabra A, Kerr DJ, Seymour LW. Melanoma cell lines express VEGF receptor KDR and respond to exogenously added VEGF. Biochem Biophys Res Commun 1995; 217:721-7.
29. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer, in press.
30. Rockmann H, Schadendorf D. Drug resistance in human melanoma: mechanisms and therapeutic opportunities. Onkologie 2003;26:581-7.
31. Sulaimon SS, Kitchell BE. The basic biology of malignant melanoma: molecular mechanisms of disease progression and comparative aspects. J Vet Intern Med 2003;17:760-72.
32. Srivastava A, Laidler P, Davies RP, Horgan K, Hughes LE. The prognostic significance of tumor vascularity in intermediate-thickness (0.76-4.0 mm thick) skin melanoma. A quantitative histologic study. Am J Pathol 1988;133:419-23.
33. Straume O, Salvesen HB, Akslen LA. Angiogenesis is prognostically important in vertical growth phase melanomas. Int J Oncol 1999;15:595-9.
34. Vlaykova T, Laurila P, Muhonen T, Hahka-Kemppinen M, Jekunen A, Alitalo K, Pyrhonen S. Prognostic value of tumour vascularity in metastatic melanoma and association of blood vessel density with vascular endothelial growth factor expression. Melanoma Res 1999;9:59-68.
35. Carnochan P, Briggs JC, Westbury G, Davies AJ. The vascularity of cutaneous melanoma: a quantitative histological study of lesions 0.85-1.25 mm in thickness. Br J Cancer 1991;64:102-7.
36. Busam KJ, Berwick M, Blessing K, Fandrey K, Kang S, Karaoli T, Fine J, Cochran AJ, White WL, Rivers J, Elder DE; Duan-Ren PW, et al. Tumor vascularity is not a prognostic factor for malignant melanoma of the skin. Am J Pathol 1995;147:1049-56.
37. Rak J, Yu JL, Kerbel RS, Coomber BL. What do oncogenic mutations have to do with angiogenesis/vascular dependence of tumors? Cancer Res 2002;62:1931-4.
38. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Pe'er J, Trent JM, Meltzer PS, Hendrix MJ. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999;155:739-52.
39. Folberg R, Hendrix MJ, Maniotis AJ. Vasculogenic mimicry and tumor angiogenesis. Am J Pathol 2000;156:361-81.
40. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-7.
41. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85: 221-8.
42. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003;9:702-12.
43. De Palma M, Naldini L. Role of haematopoietic cells and endothelial progenitors in tumour angiogenesis. Biochim Biophys Acta 2006;1766: 159-66.
44. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002;297:2256-9.
45. Machein MR, Renninger S, de Lima-Hahn E, Plate KH. Minor contribution of bone marrow-derived endothelial progenitors to the vascularization of murine gliomas. Brain Pathol 2003;13:582-97.
46. Ziegelhoeffer T, Fernandez B, Kostin S, Heil M, Voswinckel R, Helisch A, Schaper W. Bone marrow-derived cells do not incorporate into the adult growing vasculature. Circ Res 2004;94:230-8.
47. Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, Fuks Z, Kolesnick R. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003;300:1155-9.
48. Schatteman GC, Dunnwald M, Jiao C. Biology of bone marrow-derived endothelial cell precursors. Am J Physiol Heart Circ Physiol, in press.
49. Barber CL, Iruela-Arispe ML. The ever-elusive endothelial progenitor cell: identities, functions and clinical implications. Pediatr Res 2006; 59:26R-32R.
50. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Yung S, Chimenti S, Landsman L, Abramovitch R, Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006;124:175-89.
51. Hattori K, Heissig B, Tashiro K, Honjo T, Tateno M, Shieh JH, Hackett NR, Quitoriano MS, Crystal RG, Rafii S, Moore MA. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 2001; 97:3354-60.
52. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005;7:211-17.
53. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001;357:539-45.
54. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002;23:549-55.
55. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996;56:4625-9.
56. Torisu H, Ono M, Kiryu H, Furue M, Ohmoto Y, Nakayama J, Nishioka Y, Sone S, Kuwano M. Macrophage infiltration correlates with tumor stage and angiogenesis in human malignant melanoma: possible involvement of TNFα and IL-1a. Int J Cancer 2000;85:182-8.
57. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004; 4:540-50.