Tumours can adapt to anti-angiogenic therapy depending on the stromal context: Lessons from endothelial cell biology

European Journal of Cell Biology

Volumn 85, Issue 2, 2006, Pages 61-68

  van Kempen, Léon C L ^a   Leenders, William P J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DIMETHYL 5 (2 OXO 1H INDOL 3 YLMETHYLENE) 3 PYRROLEPROPIONIC ACID; ANGIOGENESIS INHIBITOR; CANCER ANTIBODY; MONOCLONAL ANTIBODY LM 609; SEMAXANIB; VANDETANIB; VASCULAR CELL ADHESION MOLECULE 1; VASCULAR TARGETING AGENT; VASCULOTROPIN;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BLOOD BRAIN BARRIER; BLOOD VESSEL; CANCER PREVENTION; CARCINOGENESIS; CLINICAL TRIAL; DRUG TARGETING; ENDOTHELIUM CELL; HUMAN; IN VIVO STUDY; METASTASIS POTENTIAL; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE TUMOR; TUMOR GROWTH; TUMOR MODEL; TUMOR REGRESSION; TUMOR VASCULARIZATION;

EID: 31344474864     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2005.10.003     Document Type: Review

References (63)

1. A. Abramsson P. Lindblom C. Betsholtz Endothelial and nonendothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors J. Clin. Invest. 112 2003 1142-1151
2. W. Arap W. Haedicke M. Bernasconi R. Kain D. Rajotte S. Krajewski H.M. Ellerby D.E. Bredesen R. Pasqualini E. Ruoslahti Targeting the prostate for destruction through a vascular address Proc. Natl. Acad. Sci. USA 99 2002 1527-1531
3. P. Auguste S. Lemiere F. Larrieu-Lahargue A. Bikfalvi Molecular mechanisms of tumor vascularization Crit. Rev. Oncol. Hematol. 54 2005 53-61
4. D.O. Bates T.G. Cui J.M. Doughty M. Winkler M. Sugiono J.D. Shields D. Peat D. Gillatt S.J. Harper VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma Cancer Res. 62 2002 4123-4131
5. F.M. Belgore A.D. Blann G.Y. Lip sFlt-1, a potential antagonist for exogenous VEGF Circulation 102 2000 E108-E109
6. G. Bergers R. Brekken G. McMahon T.H. Vu T. Itoh K. Tamaki K. Tanzawa P. Thorpe S. Itohara Z. Werb D. Hanahan Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis Nat. Cell Biol. 2 2000 737-744
7. G. Bergers S. Song N. Meyer-Morse E. Bergsland D. Hanahan Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors J. Clin. Invest. 111 2003 1287-1295
8. C. Blancher J.W. Moore N. Robertson A.L. Harris Effects of ras and von Hippel-Lindau (VHL) gene mutations on hypoxia-inducible factor (HIF)-1alpha, HIF-2alpha, and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3′-kinase/Akt signaling pathway Cancer Res. 61 2001 7349-7355
9. P. Castellani L. Borsi B. Carnemolla A. Biro A. Dorcaratto G.L. Viale D. Neri L. Zardi Differentiation between high- and low-grade astrocytoma using a human recombinant antibody to the extra domain-B of fibronectin Am. J. Pathol. 161 2002 1695-1700
10. A. Dienst A. Grunow M. Unruh B. Rabausch J.E. Nor J.W. Fries C. Gottstein Specific occlusion of murine and human tumor vasculature by VCAM-1-targeted recombinant fusion proteins J. Natl. Cancer Inst. 97 2005 733-747
11. H.F. Dvorak L.F. Brown M. Detmar A.M. Dvorak Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis Am. J. Pathol. 146 1995 1029-1039
12. J. Folkman Tumor angiogenesis: Therapeutic implications N. Engl. J. Med. 285 1971 1182-1186
13. G.H. Fong J. Rossant M. Gertsenstein M.L. Breitman Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium Nature 376 1995 66-70
14. T.A. Fong L.K. Shawver L. Sun C. Tang H. App T.J. Powell Y.H. Kim R. Schreck X. Wang W. Risau A. Ullrich K.P. Hirth G. McMahon SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types Cancer Res. 59 1999 99-106
15. D. Hanahan Signaling vascular morphogenesis and maintenance Science 277 1997 48-50
16. D. Hanahan J. Folkman Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis Cell 86 1996 353-364
17. D. Hanahan G. Christofori P. Naik J. Arbeit Transgenic mouse models of tumour angiogenesis: The angiogenic switch, its molecular controls, and prospects for preclinical therapeutic models Eur. J. Cancer 32A 1996 2386-2393
18. A.L. Harris von Hippel-Lindau syndrome: Target for anti-vascular endothelial growth factor (VEGF) receptor therapy Oncologist 5 2000 32-36
19. A.L. Harris Hypoxia - a key regulatory factor in tumour growth Nat. Rev. Cancer 2 2002 38-47
20. H. Hashizume P. Baluk S. Morikawa J.W. McLean G. Thurston S. Roberge R.K. Jain D.M. McDonald Openings between defective endothelial cells explain tumor vessel leakiness Am. J. Pathol. 156 2000 1363-1380
21. J.A. Hoffman E. Giraudo M. Singh L. Zhang M. Inoue K. Porkka D. Hanahan E. Ruoslahti Progressive vascular changes in a transgenic mouse model of squamous cell carcinoma Cancer Cell 4 2003 383-391
22. J. Holash P.C. Maisonpierre D. Compton P. Boland C.R. Alexander D. Zagzag G.D. Yancopoulos S.J. Wiegand Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF Science 284 1999 1994-1998
23. J. Holash S.J. Wiegand G.D. Yancopoulos New model of tumor angiogenesis: dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF Oncogene 18 1999 5356-5362
24. J. Holash S. Davis N. Papadopoulos S.D. Croll L. Ho M. Russell P. Boland R. Leidich D. Hylton E. Burova E. Ioffe T. Huang C. Radziejewski K. Bailey J.P. Fandl T. Daly S.J. Wiegand G.D. Yancopoulos J.S. Rudge VEGF-Trap: A VEGF blocker with potent antitumor effects Proc. Natl. Acad. Sci. USA 99 2002 11393-11398
25. K.A. Houck D.W. Leung A.M. Rowland J. Winer N. Ferrara Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms J. Biol. Chem. 267 1992 26031-26037
26. H. Hurwitz L. Fehrenbacher W. Novotny T. Cartwright J. Hainsworth W. Heim J. Berlin A. Baron S. Griffing E. Holmgren N. Ferrara G. Fyfe B. Rogers R. Ross F. Kabbinavar Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer N. Engl. J. Med. 350 2004 2335-2342
27. R.V. Iozzo J.D. San Antonio Heparan sulfate proteoglycans: Heavy hitters in the angiogenesis arena J. Clin. Invest. 108 2001 349-355
28. M.L. Janssen W.J. Oyen I. Dijkgraaf L.F. Massuger C. Frielink D.S. Edwards M. Rajopadhye H. Boonstra F.H. Corstens O.C. Boerman Tumor targeting with radiolabeled alpha(v)beta(3) integrin binding peptides in a nude mouse model Cancer Res. 62 2002 6146-6151
29. J.A. Joyce P. Laakkonen M. Bernasconi G. Bergers E. Ruoslahti D. Hanahan Stage-specific vascular markers revealed by phage display in a mouse model of pancreatic islet tumorigenesis Cancer Cell 4 2003 393-403
30. B.A. Keyt L.T. Berleau H.V. Nguyen H. Chen H. Heinsohn R. Vandlen N. Ferrara The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency J. Biol. Chem. 271 1996 7788-7795
31. B.A. Keyt H.V. Nguyen L.T. Berleau C.M. Duarte J. Park H. Chen N. Ferrara Identification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors. Generation of receptor-selective VEGF variants by site-directed mutagenesis J. Biol. Chem. 271 1996 5638-5646
32. B. Kusters J.R. Westphal D. Smits D.J. Ruiter P. Wesseling U. Keilholz R.M. de Waal The pattern of metastasis of human melanoma to the central nervous system is not influenced by integrin alpha(v)beta(3) expression Int. J. Cancer 92 2001 176-180
33. B. Kusters W.P. Leenders P. Wesseling D. Smits K. Verrijp D.J. Ruiter J.P. Peters A.J. van Der Kogel R.M. de Waal Vascular endothelial growth factor-A(165) induces progression of melanoma brain metastases without induction of sprouting angiogenesis Cancer Res. 62 2002 341-345
34. B. Kusters R.M. de Waal P. Wesseling K. Verrijp C. Maass A. Heerschap J.O. Barentsz F. Sweep D.J. Ruiter W.P. Leenders Differential effects of vascular endothelial growth factor A isoforms in a mouse brain metastasis model of human melanoma Cancer Res. 63 2003 5408-5413
35. P. Lee K. Goishi A.J. Davidson R. Mannix L. Zon M. Klagsbrun Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish Proc. Natl. Acad. Sci. USA 99 2002 10470-10475
36. S. Lee S.M. Jilani G.V. Nikolova D. Carpizo M.L. Iruela-Arispe Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors J. Cell Biol. 169 2005 681-691
37. W. Leenders B. Kusters R. De Waal Vessel co-option: How tumors obtain blood supply in the absence of sprouting angiogenesis Endothelium 9 2002 83-87
38. W. Leenders N. Lubsen M. van Altena M. Clauss M. Deckers C. Lowik G. Breier D. Ruiter R. de Waal Design of a variant of vascular endothelial growth factor-A (VEGF-A) antagonizing KDR/Flk-1 and Flt-1 Lab. Invest. 82 2002 473-481
39. W. Leenders B. Küsters J. Pikkemaat P. Wesseling D. Ruiter A. Heerschap J. Barentsz R.M.W. de Waal Vascular endothelial growth factor-A determines detectability of experimental melanoma brain metastasis in Gd-DTPA-enhanced MRI Int. J. Cancer 105 2003 437-443
40. P. Lindblom H. Gerhardt S. Liebner A. Abramsson M. Enge M. Hellstrom G. Backstrom S. Fredriksson U. Landegren H.C. Nystrom G. Bergstrom E. Dejana A. Ostman P. Lindahl C. Betsholtz Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall Genes Dev. 17 2003 1835-1840
41. P.C. Maisonpierre C. Suri P.F. Jones S. Bartunkova S.J. Wiegand C. Radziejewski D. Compton J. McClain T.H. Aldrich N. Papadopoulos T.J. Daly S. Davis T.N. Sato G.D. Yancopoulos Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis Science 277 1997 55-60
42. R. Mamluk Z. Gechtman M.E. Kutcher N. Gasiunas J. Gallagher M. Klagsbrun Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2 and heparin via its b1b2 domain J. Biol. Chem. 277 2002 24818-24825
43. J. Marx Cancer. Encouraging results for second-generation antiangiogenesis drugs Science 308 2005 1248-1249
44. H.Q. Miao M. Klagsbrun Neuropilin is a mediator of angiogenesis Cancer Metastasis Rev. 19 2000 29-37
45. B. Millauer M.P. Longhi K.H. Plate L.K. Shawver W. Risau A. Ullrich L.M. Strawn Dominant-negative inhibition of Flk-1 suppresses the growth of many tumor types in vivo Cancer Res. 56 1996 1615-1620
46. S. Morikawa P. Baluk T. Kaidoh A. Haskell R.K. Jain D.M. McDonald Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors Am. J. Pathol. 160 2002 985-1000
47. D. Mukhopadhyay K. Datta Multiple regulatory pathways of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) expression in tumors Semin. Cancer Biol. 14 2004 123-130
48. D. Mukhopadhyay J.A. Nagy E.J. Manseau H.F. Dvorak Vascular permeability factor/vascular endothelial growth factor-mediated signaling in mouse mesentery vascular endothelium Cancer Res. 58 1998 1278-1284
49. D. Neri R. Bicknell Tumour vascular targeting Nat. Rev. Cancer 5 2005 436-446
50. G. Neufeld T. Cohen S. Gengrinovitch Z. Poltorak Vascular endothelial growth factor (VEGF) and its receptors FASEB J. 13 1999 9-22
51. G. Neufeld O. Kessler Y. Herzog The interaction of neuropilin-1 and neuropilin-2 with tyrosine-kinase receptors for VEGF Adv. Exp. Med. Biol. 515 2002 81-90
52. T. Nishishita P.C. Lin Angiopoietin 1, PDGF-B, and TGF-beta gene regulation in endothelial cell and smooth muscle cell interaction J. Cell. Biochem. 91 2004 584-593
53. T.P. Padera B.R. Stoll J.B. Tooredman D. Capen E. di Tomaso R.K. Jain Pathology: Cancer cells compress intratumour vessels Nature 427 2004 695
54. J. Plouet F. Moro S. Bertagnolli N. Coldeboeuf H. Mazarguil S. Clamens F. Bayard Extracellular cleavage of the vascular endothelial growth factor 189-amino acid form by urokinase is required for its mitogenic effect J. Biol. Chem. 272 1997 13390-13396
55. J.A. Posey M.B. Khazaeli A. DelGrosso M.N. Saleh C.Y. Lin W. Huse A.F. LoBuglio A pilot trial of vitaxin, a humanized anti-vitronectin receptor (anti alpha v beta 3) antibody in patients with metastatic cancer Cancer Biother. Radiopharm. 16 2001 125-132
56. L.G. Presta H. Chen S.J. O'Connor V. Chisholm Y.G. Meng L. Krummen M. Winkler N. Ferrara Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders Cancer Res. 57 1997 4593-4599
57. C.J. Robinson S.E. Stringer The splice variants of vascular endothelial growth factor (VEGF) and their receptors J. Cell Sci. 114 2001 853-865
58. M. Santimaria G. Moscatelli G.L. Viale L. Giovannoni G. Neri F. Viti A. Leprini L. Borsi P. Castellani L. Zardi D. Neri P. Riva Immunoscintigraphic detection of the ED-B domain of fibronectin, a marker of angiogenesis, in patients with cancer Clin. Cancer Res. 9 2003 571-579
59. P. Sweeney T. Karashima S.J. Kim D. Kedar B. Mian S. Huang C. Baker Z. Fan D.J. Hicklin C.A. Pettaway C.P. Dinney Anti-vascular endothelial growth factor receptor 2 antibody reduces tumorigenicity and metastasis in orthotopic prostate cancer xenografts via induction of endothelial cell apoptosis and reduction of endothelial cell matrix metalloproteinase type 9 production Clin. Cancer Res. 8 2002 2714-2724
60. T. Takahashi H. Ueno M. Shibuya VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells Oncogene 18 1999 2221-2230
61. P.B. Vermeulen C. Colpaert R. Salgado R. Royers H. Hellemans E. Van Den Heuvel G. Goovaerts L.Y. Dirix E. Van Marck Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasia J. Pathol. 195 2001 336-342
62. S.R. Wedge D.J. Ogilvie M. Dukes J. Kendrew R. Chester J.A. Jackson S.J. Boffey P.J. Valentine J.O. Curwen H.L. Musgrove G.A. Graham G.D. Hughes A.P. Thomas E.S. Stokes B. Curry G.H. Richmond P.F. Wadsworth A.L. Bigley L.F. Hennequin ZD6474 inhibits vascular endothelial growth factor signaling, angiogenesis, and tumor growth following oral administration Cancer Res. 62 2002 4645-4655
63. F. Winkler S.V. Kozin R.T. Tong S.S. Chae M.F. Booth I. Garkavtsev L. Xu D.J. Hicklin D. Fukumura E. di Tomaso L.L. Munn R.K. Jain Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: Role of oxygenation, angiopoietin-1, and matrix metalloproteinases Cancer Cell 6 2004 553-563