Following up tumour angiogenesis: From the basic laboratory to the clinic

Clinical and Translational Oncology

Volumn 10, Issue 8, 2008, Pages 468-477

  Orgaz, José L ^a   Martínez Poveda, Beatriz ^a   Fernández García, Nuria I ^a   Jiménez, Benilde ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Angiogenesis; Angiogenesis assays; Anti angiogenic therapy; Cancer

Indexed keywords

ANGIOGENESIS INHIBITOR; TUMOR MARKER;

BLOOD; DIAGNOSTIC IMAGING; HUMAN; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; REVIEW; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; DIAGNOSTIC IMAGING; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MARKERS, BIOLOGICAL;

EID: 54549094797     PISSN: 1699048X     EISSN: 16993055     Source Type: Journal    
DOI: 10.1007/s12094-008-0235-4     Document Type: Article

References (98)

1. Nguyen DX, Massague J (2007) Genetic determinants of cancer metastasis. Nat Rev Genet 8:341-352 (Pubitemid 46625811)
2. Bergers G, Benjamin LE (2003) Tumorigenesis and the angiogenic switch. Nat Rev Cancer 3: 401-410 (Pubitemid 37328844)
3. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182-1186
4. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9:653-660 (Pubitemid 36749213)
5. Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9:685-693 (Pubitemid 36749217)
6. Jimenez B, Volpert OV (2001) Mechanistic insights on the inhibition of tumor angiogenesis. J Mol Med 78:663-672
7. Gao D, Nolan DJ, Mellick AS et al (2008) Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 319: 195-198
8. Bertolini F, Mancuso P, Shaked Y et al (2007) Molecular and cellular biomarkers for angiogenesis in clinical oncology. Drug Discov Today 12: 806-812 (Pubitemid 47539970)
9. Weissleder R, Pittet MJ (2008) Imaging in the era of molecular oncology. Nature 452:580-589 (Pubitemid 351483372)
10. Jackson CJ, Nguyen M (1997) Human microvascular endothelial cells differ from macrovascular endothelial cells in their expression of matrix metalloproteinases. Int J Biochem Cell Biol 29:1167-1177 (Pubitemid 27522556)
11. Auerbach R, Auerbach W (2001) Assays to study angiogenesis. In: Voest EE, D'Amore PA (eds) Tumor angiogenesis and microcirculation. Marcel Dekker, New York, pp 91-102
12. Denizot F, Lang R (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89:271-277 (Pubitemid 16080782)
13. Staton CA, Stribbling SM, Tazzyman S et al (2004) Current methods for assaying angiogenesis in vitro and in vivo. Int J Exp Pathol 85:233-248 (Pubitemid 39319155)
14. Alessandri G, Raju K, Gullino PM (1983) Mobilization of capillary endothelium in vitro induced by effectors of angiogenesis in vivo. Cancer Res 43:1790-1797 (Pubitemid 13122586)
15. Falk W, Goodwin RH Jr, Leonard EJ (1980) A 48-well micro chemotaxis assembly for rapid and accurate measurement of leukocyte migration. J Immunol Methods 33:239-247
16. Zetter BR (1987) Assay of capillary endothelial cell migration. Methods Enzymol 147:135-144
17. Pepper MS, Belin D, Montesano R et al (1990) Transforming growth factor-beta 1 modulates basic fibroblast growth factor-induced proteolytic and angiogenic properties of endothelial cells in vitro. J Cell Biol 111:743-755
18. Taraboletti G, Giavazzi R (2004) Modelling approaches for angiogenesis. Eur J Cancer 40:881-889 (Pubitemid 38519766)
19. Lawley TJ, Kubota Y (1989) Induction of morphologic differentiation of endothelial cells in culture. J Invest Dermatol 93:59S-61S
20. Gagnon E, Cattaruzzi P, Griffith M et al (2002) Human vascular endothelial cells with extended life spans: in vitro cell response, protein expression, and angiogenesis. Angiogenesis 5:21-33 (Pubitemid 36076920)
21. Montesano R, Pepper MS, Orci L (1993) Paracrine induction of angiogenesis in vitro by Swiss 3T3 fibroblasts. J Cell Sci 105:1013-1024 (Pubitemid 23258664)
22. Nehls V, Drenckhahn D (1995) A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc Res 50:311-322
23. Nakatsu MN, Sainson RC, Aoto JN et al (2003) Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and angiopoietin-1. Microvasc Res 66:102-112 (Pubitemid 36962872)
24. Auerbach R, Lewis R, Shinners B et al (2003) Angiogenesis assays: a critical overview. Clin Chem 49:32-40 (Pubitemid 36078551)
25. Auerbach R, Akhtar N, Lewis RL et al (2000) Angiogenesis assays: problems and pitfalls. Cancer Metastasis Rev 19:167-172 (Pubitemid 32004706)
26. Nicosia RF, Villaschi S (1995) Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab Invest 73:658-666
27. Muthukkaruppan VR, Shinneers BL, Lewis R et al (2000) The chick embryo aortic arch assay: a new, rapid, quantifiable in vitro method for testing the efficacy of angiogenic and anti-angiogenic factors in a three-dimensional, serum-free organ culture system. Proc Am Assoc Cancer 41:65
28. Jain RK, Schlenger K, Hockel M et al (1997) Quan titative angiogenesis assays: progress and pro blems. Nat Med 3:1203-1208
29. McDonald DM, Choyke PL (2003) Imaging of angiogenesis: from microscope to clinic. Nat Med 9:713-725 (Pubitemid 36749220)
30. Norrby K (2006) In vivo models of angiogenesis. J Cell Mol Med 10:588-612 (Pubitemid 44874273)
31. Auerbach R, Kubai L, Knighton D et al (1974) A simple procedure for the long-term cultivation of chicken embryos. Dev Biol 41:391-394
32. Ausprunk DH, Knighton DR, Folkman J (1974) Differentiation of vascular endothelium in the chick chorioallantois: a structural and autoradiographic study. Dev Biol 38:237-248
33. Ribatti D, Vacca A, Roncali L et al (2000) The chick embryo chorioallantoic membrane as a model for in vivo research on anti-angiogenesis. Curr Pharm Biotechnol 1:73-82
34. Ribatti D (2008) The chick embryo chorioallantoic membrane in the study of tumor angiogenesis. Rom J Morphol Embryol 49:131-135
35. Seidlitz E, Korbie D, Marien L et al (2004) Quantification of anti-angiogenesis using the capillaries of the chick chorioallantoic membrane demonstrates that the effect of human angiostatin is agedependent. Microvasc Res 67:105-116 (Pubitemid 38326996)
36. Narita K, Staub J, Chien J et al (2006) HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res 66:6025-6032
37. Nishikawa T, Akiyama N, Kunimasa K et al (2006) Inhibition of in vivo angiogenesis by Nbeta-alanyl-5-S-glutathionyl-3,4-dihydroxyphenylalanine. Eur J Pharmacol 539:151-157
38. Berndt S, Perrier d'Hauterive S, Blacher S et al (2006) Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium. Faseb J 20:2630-2632
39. Martinez-Poveda B, Munoz-Chapuli R, Rodriguez-Nieto S et al (2007) IB05204, a dichloropyridodithienotriazine, inhibits angiogenesis in vitro and in vivo. Mol Cancer Ther 6:2675-2685 (Pubitemid 350058148)
40. Park K, Kim YS, Lee GY et al (2007) Antiangiogenic effect of bile acid acylated heparin derivative. Pharm Res 24:176-185 (Pubitemid 44902582)
41. Guedez L, Rivera AM, Salloum R et al (2003) Quantitative assessment of angiogenic responses by the directed in vivo angiogenesis assay. Am J Pathol 162:1431-1439 (Pubitemid 36512825)
42. Chu J, Lloyd FL, Trifan OC et al (2003) Potential involvement of the cyclooxygenase-2 pathway in the regulation of tumor-associated angiogenesis and growth in pancreatic cancer. Mol Cancer Ther 2:1-7
43. Gimbrone MA Jr, Cotran RS, Leapman SB, Folkman J et al (1974) Tumor growth and neovascularization: an experimental model using the rabbit cornea. J Natl Cancer Inst 52:413-427
44. Rogers MS, Birsner AE, D'Amato RJ (2007) The mouse cornea micropocket angiogenesis assay. Nat Protoc 2:2545-2550
45. Shen J, Vil MD, Zhang H et al (2007) An antibody directed against PDGF receptor beta enhances the antitumor and the anti-angiogenic activities of an anti-VEGF receptor 2 antibody. Biochem Biophys Res Commun 357:1142-1147 (Pubitemid 46693690)
46. Ma J, Waxman DJ (2008) Modulation of the antitumor activity of metronomic cyclophosphamide by the angiogenesis inhibitor axitinib. Mol Cancer Ther 7:79-89
47. Salvador C, Li B, Hansen R et al (2008) Yeast-derived beta-glucan augments the therapeutic efficacy mediated by anti-vascular endothelial growth factor monoclonal antibody in human carcinoma xenograft models. Clin Cancer Res 14:1239-1247 (Pubitemid 351302573)
48. Shaner NC, Campbell RE, Steinbach PA et al (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572 (Pubitemid 40039460)
49. Shcherbo D, Merzlyak EM, Chepurnykh TV et al (2007) Bright far-red fluorescent protein for whole-body imaging. Nat Methods 4:741-746 (Pubitemid 47338169)
50. Veikkola T, Alitalo K (1999) VEGFs, receptors and angiogenesis. Semin Cancer Biol 9:211-220 (Pubitemid 29273837)
51. Ferrara N (2005) VEGF as a therapeutic target in cancer. Oncology 69 Suppl 3:11-16 (Pubitemid 41680948)
52. Fukumura D, Xavier R, Sugiura T et al (1998) Tumor induction of VEGF promoter activity in stromal cells. Cell 94:715-725 (Pubitemid 28436004)
53. Motoike T, Loughna S, Perens E et al (2000) Universal GFP reporter for the study of vascular development. Genesis 28:75-81
54. Hillen F, Kaijzel EL, Castermans K et al (2008) A transgenic Tie2-GFP athymic mouse model; a tool for vascular biology in xenograft tumors. Biochem Biophys Res Commun 368:364-367
55. Wang Y, Iyer M, Annala A et al (2006) Noninvasive indirect imaging of vascular endothelial growth factor gene expression using bioluminescence imaging in living transgenic mice. Physiol Genomics 24:173-180
56. Zhang N, Fang Z, Contag PR et al (2004) Tracking angiogenesis induced by skin wounding and contact hypersensitivity using a Vegfr2-luciferase transgenic mouse. Blood 103:617-626 (Pubitemid 38140096)
57. Hoffman RM (2004) Imaging tumor angiogenesis with fluorescent proteins. APMIS 112:441-449 (Pubitemid 39626052)
58. Amoh Y, Yang M, Li L et al (2005) Nestin-linked green fluorescent protein transgenic nude mouse for imaging human tumor angiogenesis. Cancer Res 65:5352-5357 (Pubitemid 40827348)
59. Faley SL, Takahashi K, Crooke CE et al (2007) Bioluminescence imaging of vascular endothelial growth factor promoter activity in murine mammary tumorigenesis. Mol Imaging 6:331-339 (Pubitemid 350013539)
60. Jimenez B, Volpert OV, Crawford SE et al (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41-48 (Pubitemid 30048524)
61. Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307:58-62 (Pubitemid 40093472)
62. Jain RK (2008) Lessons from multidisciplinary translational trials on anti-angiogenic therapy of cancer. Nat Rev Cancer 8:309-316 (Pubitemid 351430862)
63. Duda DG, Batchelor TT, Willett CG et al (2007) VEGF-targeted cancer therapy strategies: current progress, hurdles and future prospects. Trends Mol Med 13:223-230 (Pubitemid 46836870)
64. Larkin JM, Chowdhury S, Gore ME (2007) Drug insight: advances in renal cell carcinoma and the role of targeted therapies. Nat Clin Pract Oncol 4:470-479 (Pubitemid 47393803)
65. Demetri GD, van Oosterom AT, Garrett CR et al (2006) Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 368:1329-1338 (Pubitemid 44528723)
66. Willett CG, Boucher Y, di Tomaso E et al (2004) Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 10:145-147 (Pubitemid 38524883)
67. Batchelor TT, Sorensen AG, di Tomaso E et al (2007) AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11:83-95 (Pubitemid 46075199)
68. Weidner N (2004) The importance of tumor angiogenesis: the evidence continues to grow. Am J Clin Pathol 122:675-677 (Pubitemid 39434747)
69. Bamberger ES, Perrett CW (2002) Angiogenesis in epithelian ovarian cancer. Mol Pathol 55:348-359 (Pubitemid 35454510)
70. Leek RD (2001) The prognostic role of angiogenesis in breast cancer. Anticancer Res 21:4325-4331 (Pubitemid 34240962)
71. Hlatky L, Hahnfeldt P, Folkman J (2002) Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst 94:883-893 (Pubitemid 34778087)
72. Willett CG, Boucher Y, Duda DG et al (2005) Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J Clin Oncol 23:8136-8139 (Pubitemid 46657433)
73. Lyden D, Hattori K, Dias S et al (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7:1194-1201 (Pubitemid 33063774)
74. Rafii S, Lyden D, Benezra R et al (2002) Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat Rev Cancer 2:826-835 (Pubitemid 37328901)
75. Carmeliet P (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med 6:389-395 (Pubitemid 30208155)
76. Guba M, Seeliger H, Kleespies A et al (2004) Vascular endothelial growth factor in colorectal cancer. Int J Colorectal Dis 19:510-517 (Pubitemid 39445405)
77. Gasparini G (2001) Clinical significance of determination of surrogate markers of angiogenesis in breast cancer. Crit Rev Oncol Hematol 37:97-114 (Pubitemid 32106909)
78. Kammula US, Kuntz EJ, Francone TD et al (2007) Molecular co-expression of the c-Met oncogene and hepatocyte growth factor in primary colon cancer predicts tumor stage and clinical outcome. Cancer Lett 248:219-228 (Pubitemid 46330555)
79. Iwasaki A, Kuwahara M, Yoshinaga Y et al (2004) Basic fibroblast growth factor (bFGF) and vascular endothelial growth factor (VEGF) levels, as prognostic indicators in NSCLC. Eur J Cardiothorac Surg 25:443-448 (Pubitemid 38340585)
80. Masuya D, Huang C, Liu D et al (2004) The tumour-stromal interaction between intratumoral c-Met and stromal hepatocyte growth factor associated with tumour growth and prognosis in non-small-cell lung cancer patients. Br J Cancer 90:1555-1562 (Pubitemid 38648238)
81. Jakob C, Sterz J, Zavrski I et al (2006) Angiogenesis in multiple myeloma. Eur J Cancer 42:1581-1590 (Pubitemid 44118769)
82. Kumar H, Heer K, Greenman J et al (2002) Soluble FLT-1 is detectable in the sera of colorectal and breast cancer patients. Anticancer Res 22: 1877-1880 (Pubitemid 34839213)
83. Byrne GJ, Ghellal A, Iddon J et al (2000) Serum soluble vascular cell adhesion molecule-1: role as a surrogate marker of angiogenesis. J Natl Cancer Inst 92:1329-1336 (Pubitemid 30660593)
84. Qin LX, Tang ZY (2002) The prognostic molecular markers in hepatocellular carcinoma. World J Gastroenterol 8:385-392
85. Opala T, Drews K, Rzymski P et al (2003) Evaluation of soluble intracellular adhesion molecule-1 (sICAM-1) in benign and malignant ovarian masses. Eur J Gynaecol Oncol 24:255-257 (Pubitemid 36644611)
86. Li H, Gerald WL, Benezra R (2004) Utilization of bone marrow-derived endothelial cell precursors in spontaneous prostate tumors varies with tumor grade. Cancer Res 64:6137-6143 (Pubitemid 39129414)
87. Mancuso P, Calleri A, Cassi C et al (2003) Circulating endothelial cells as a novel marker of angiogenesis. Adv Exp Med Biol 522:83-97 (Pubitemid 36570529)
88. Furstenberger G, von Moos R, Lucas R et al (2006) Circulating endothelial cells and angiogenic serum factors during neoadjuvant chemotherapy of primary breast cancer. Br J Cancer 94: 524-531 (Pubitemid 43289756)
89. Norden-Zfoni A, Desai J, Manola J et al (2007) Blood-based biomarkers of SU11248 activity and clinical outcome in patients with metastatic imatinib-resistant gastrointestinal stromal tumor. Clin Cancer Res 13:2643-2650 (Pubitemid 46788031)
90. Blann AD, Woywodt A, Bertolini F et al (2005) Circulating endothelial cells. Biomarker of vascular disease. Thromb Haemost 93:228-235 (Pubitemid 40253726)
91. Naik RP, Jin D, Chuang E et al (2008) Circulating endothelial progenitor cells correlate to stage in patients with invasive breast cancer. Breast Cancer Res Treat 107:133-138 (Pubitemid 350179580)
92. Lin EH, Hassan M, Li Y et al (2007) Elevated circulating endothelial progenitor marker CD133 messenger RNA levels predict colon cancer recurrence. Cancer 110:534-542 (Pubitemid 47106141)
93. Zheng PP, Hop WC, Luider TM et al (2007) Increased levels of circulating endothelial progenitor cells and circulating endothelial nitric oxide synthase in patients with gliomas. Ann Neurol 62:40-48 (Pubitemid 47235279)
94. Igreja C, Courinha M, Cachaco AS et al (2007) Characterization and clinical relevance of circulating and biopsy-derived endothelial progenitor cells in lymphoma patients. Haematologica 92: 469-477 (Pubitemid 350144292)
95. Capillo M, Mancuso P, Gobbi A et al (2003) Continuous infusion of endostatin inhibits differentiation, mobilization, and clonogenic potential of endothelial cell progenitors. Clin Cancer Res 9:377-382 (Pubitemid 36109755)
96. Duda DG, Cohen KS, Scadden DT et al (2007) A protocol for phenotypic detection and enumeration of circulating endothelial cells and circulating progenitor cells in human blood. Nat Protoc 2:805-810 (Pubitemid 46745577)
97. Miller JC, Pien HH, Sahani D et al (2005) Imaging angiogenesis: applications and potential for drug development. J Natl Cancer Institute 97: 172-187 (Pubitemid 40277367)
98. Perini R, Choe R, Yodh AG et al (2008) Non-invasive assessment of tumor neovasculature: techniques and clinical applications. Cancer Metastasis Rev [Epub ahead of print]