Cellular source and amount of vascular endothelial growth factor and platelet-derived growth factor in tumors determine response to angiogenesis inhibitors

Cancer Research

Volumn 69, Issue 10, 2009, Pages 4527-4536

  Sennino, Barbara ^a   Kuhnert, Frank ^b   Tabruyn, Sebastien P ^a   Mancuso, Michael R ^a,b   Hu Lowe, Dana D ^c   Kuo, Calvin J ^b   McDonald, Donald M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXITINIB; IMATINIB; PLATELET DERIVED GROWTH FACTOR; VASCULOTROPIN; VIRUS VECTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BLOOD VESSEL; CELL DENSITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; IMMUNOREACTIVITY; LEWIS CARCINOMA; MOUSE; NONHUMAN; PERICYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR REGRESSION; TUMOR VASCULARIZATION; TUMOR VOLUME;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; IMIDAZOLES; IMMUNOGLOBULIN FC FRAGMENTS; INDAZOLES; LUNG NEOPLASMS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PIPERAZINES; PLATELET-DERIVED GROWTH FACTOR; PYRIMIDINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 66249101249     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-3779     Document Type: Article

References (48)

1. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
2. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86:353-364 (Pubitemid 26272076)
3. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature 2005;438:967-974 (Pubitemid 43093963)
4. Homsi J, Daud AI. Spectrum of activity and mechanism of action of VEGF/PDGF inhibitors. Cancer Control 2007;14:285-294 (Pubitemid 47057799)
5. Crawford Y, Ferrara N. VEGF inhibition: insights from preclinical and clinical studies. Cell Tissue Res 2009;335:261-269
6. Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008;8:579-591
7. Hashizume H, Baluk P, Morikawa S, et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 2000;156:1363-1380 (Pubitemid 30660013)
8. Hirschi KK, D'Amore PA. Pericytes in the microvasculature. Cardiovasc Res 1996;32:687-698 (Pubitemid 26332308)
9. Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGFB-deficient mice. Science 1997;277:242-245 (Pubitemid 27446080)
10. von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res 2006;312:623-629
11. Abramsson A, Berlin O, Papayan H, Paulin D, Shani M, Betsholtz C. Analysis of mural cell recruitment to tumor vessels. Circulation 2002;105:112-117 (Pubitemid 34049151)
12. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, McDonald DM. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 2002;160:985-1000. (Pubitemid 34224587)
13. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res 2005;97:512-523 (Pubitemid 41361741)
14. Ferrara N. The role of VEGF in the regulation of physiological and pathological angiogenesis. EXS 2005;94:209-231
15. Erber R, Thurnher A, Katsen AD, et al. Combined inhibition of VEGF and PDGF signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms. FASEB J 2004;18:338-340
16. Reinmuth N, Liu W, Jung YD, et al. Induction of VEGF in perivascular cells defines a potential paracrine mechanism for endothelial cell survival. FASEB J 2001;15:1239-1241
17. Darland DC, Massingham LJ, Smith SR, Piek E, Saint-Geniez M, D'Amore PA. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 2003;264:275-288 (Pubitemid 37393463)
18. Enge M, Bjarnegard M, Gerhardt H, et al. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 2002;21:4307-4316
19. Hellstrom M, Kal n M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999;126:3047-3055
20. Bjarnegard M, Enge M, Norlin J, et al. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 2004;131:1847-1857 (Pubitemid 38559851)
21. Betsholtz C. Biology of platelet-derived growth factors in development. Birth Defects Res C Embryo Today 2003;69:272-285 (Pubitemid 38076452)
22. Hellstrom M, Gerhardt H, Kalen M, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 2001;153:543-553 (Pubitemid 34280141)
23. Sennino B, Falcon BL, McCauley D, et al. Sequential loss of tumor vessel pericytes and endothelial cells after inhibition of platelet-derived growth factor B by selective aptamer AX102. Cancer Res 2007;67:7358-7367 (Pubitemid 47206566)
24. Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest 2003;111:1287-1295 (Pubitemid 36554699)
25. + perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 2005;7:870-879
26. Miller KD, Sweeney CJ, Sledge GW, Jr. Redefining the target: chemotherapeutics as antiangiogenics. J Clin Oncol 2001;19:1195-1206 (Pubitemid 32176298)
27. Fudge K, Wang CY, Stearns ME. Immunohistochemistry analysis of platelet-derived growth factor A and B chains and platelet-derived growth factor α and β receptor expression in benign prostatic hyperplasias and Gleason-graded human prostate adenocarcinomas. Mod Pathol 1994;7:549-554
28. Henriksen R, Funa K, Wilander E, Backstrom T, Ridderheim M, Oberg K. Expression and prognostic significance of platelet-derived growth factor and its receptors in epithelial ovarian neoplasms. Cancer Res 1993;53:4550-4554 (Pubitemid 23304378)
29. Potapova O, Laird AD, Nannini MA, et al. Contribution of individual targets to the antitumor efficacy of the multitargeted receptor tyrosine kinase inhibitor SU11248. Mol Cancer Ther 2006;5:1280-1289 (Pubitemid 43881321)
30. Laird AD, Vajkoczy P, Shawver LK, et al. SU6668 is a potent antiangiogenic and antitumor agent that induces regression of established tumors. Cancer Res 2000;60:4152-4160 (Pubitemid 30636598)
31. Druker BJ. STI571 (Gleevec) as a paradigm for cancer therapy. Trends Mol Med 2002;8:S14-8.
32. Kuo CJ, Farnebo F, Yu EY, et al. Comparative evaluation of the antitumor activity of antiangiogenic proteins delivered by gene transfer. Proc Natl Acad Sci U S A 2001;98:4605-4610 (Pubitemid 32295023)
33. Kuhnert F, Tam BY, Sennino B, et al. Soluble receptor-mediated selective inhibition of VEGFR and PDGFRβ signaling during physiologic and tumor angiogenesis. Proc Natl Acad Sci U S A 2008;105:10185-10190
34. Hanahan D. Heritable formation of pancreatic β-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature 1985;315:115-122 (Pubitemid 15064530)
35. Hu-Lowe D, Hallin M, Feeley R, et al. Characterization of potency and activity of the VEGF/PDGF receptor tyrosine kinase inhibitor AG013736. Proc Am Assoc Cancer Res 2002;43:A5357.
36. Inai T, Mancuso M, Hashizume H, et al. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004;165:35-52. (Pubitemid 38821812)
37. Manley PW, Cowan-Jacob SW, Buchdunger E, et al. Imatinib: a selective tyrosine kinase inhibitor. Eur J Cancer 2002;38 Suppl 5:S19-27.
38. Chartier C, Degryse E, Gantzer M, Dieterle A, Pavirani A, Mehtali M. Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J Virol 1996;70:4805-4810 (Pubitemid 26187479)
39. Hu-Lowe DD, Zou HY, Grazzini ML, et al. Nonclinical antiangiogenesis and antitumor activities of axitinib (AG-013736), an oral, potent, and selective inhibitor of vascular endothelial growth factor receptor tyrosine kinases 1, 2, 3. Clin Cancer Res 2008;14:7272-7283
40. Ono M. Molecular links between tumor angiogenesis and inflammation: inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci 2008;99:1501-1506
41. Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008;22:1276-1312
42. Baluk P, Hashizume H, McDonald DM. Cellular abnormalities of blood vessels as targets in cancer. Curr Opin Genet Dev 2005;15:102-111 (Pubitemid 40127638)
43. Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro-oncol 2005;7:452-464 (Pubitemid 41555617)
44. Sims DE. Diversity within pericytes. Clin Exp Pharmacol Physiol 2000;27:842-846
45. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-744
46. Inoue M, Hager JH, Ferrara N, Gerber HP, Hanahan D. VEGF-A has a critical, nonredundant role in angiogenic switching and pancreatic β cell carcinogenesis. Cancer Cell 2002;1:193-202. (Pubitemid 41039165)
47. Mancuso MR, Davis R, Norberg SM, et al. Rapid vascular regrowth in tumors after reversal of VEGF inhibition. J Clin Invest 2006;116:2610-2621 (Pubitemid 44511625)
48. Redmer DA, Doraiswamy V, Bortnem BJ, et al. Evidence for a role of capillary pericytes in vascular growth of the developing ovine corpus luteum. Biol Reprod 2001;65:879-889 (Pubitemid 32777376)