Caveolin-1 - Deficient mice have increased tumor microvascular permeability, angiogenesis, and growth

Cancer Research

Volumn 67, Issue 6, 2007, Pages 2849-2856

  Lin, Michelle I ^a   Yu, Jun ^a   Murata, Takahisa ^a,b   Sessa, William C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CAVTRATIN; EVANS BLUE; FIBRINOGEN; PEPTIDE DERIVATIVE; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CANCER TRANSPLANTATION; CELL DEATH; CELL ISOLATION; CONTROLLED STUDY; ENDOTHELIUM CELL; KNOCKOUT MOUSE; LEWIS CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR GROWTH; TUMOR VASCULARIZATION; WILD TYPE;

ADHERENS JUNCTIONS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CAPILLARY PERMEABILITY; CARCINOMA, LEWIS LUNG; CAVEOLIN 1; CELL GROWTH PROCESSES; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 34047251876     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-4082     Document Type: Article

References (39)

1. Dvorak HF, Nagy JA, Dvorak JT, Dvorak AM. Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules. Am J Pathol 1988;133:95-109.
2. Hashizume H, Baluk P, Morikawa S, et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 2000;156:1363-80.
3. Daldrup H, Shames DM, Wendland M, et al. Correlation of dynamic contrast-enhanced MR imaging with histologic tumor grade: comparison of macromolecular and small-molecular contrast media. AJR Am J Roentgenol 1998;171:941-9.
4. Dvorak HF, Dvorak AM, Manseau EJ, Wiberg L, Churchill WH. Fibrin gel investment associated with line 1 and line 10 solid tumor growth, angiogenesis, and fibroplasia in guinea pigs. Role of cellular immunity, myofibroblasts, microvascular damage, and infarction in line 1 tumor regression. J Natl Cancer Inst 1979;62: 1459-72.
5. Thurston G, Suri C, Smith K, et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999;286:2511-4.
6. Thurston G, Rudge JS, Ioffe E, et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000;6:460-3.
7. Stoeltzing O, Ahmad SA, Liu W, et al. Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res 2003;63: 3370-7.
8. Gratton JP, Lin MI, Yu J, et al. Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell 2003;4:31-9.
9. Sima J, Zhang SX, Shao C, Fant J, Ma JX. The effect of angiostatin on vascular leakage and VEGF expression in rat retina. FEBS Lett 2004;564:19-23.
10. Satchi-Fainaro R, Mamluk R, Wang L, et al. Inhibition of vessel permeability by TNP-470 and its polymer conjugate, caplostatin. Cancer Cell 2005;7:251-61.
11. Goligorsky MS, Li H, Brodsky S, Chen J. Relationships between caveolae and eNOS: everything in proximity and the proximity of everything. Am J Physiol Renal Physiol 2002;283:F1-10.
12. Schubert W, Frank PG, Woodman SE, et al. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem 2002; 277:40091-8.
13. Drab M, Verkade P, Elger M, et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001;293:2449-52.
14. Ackah E, Yu J, Zoellner S, et al. Akt1/protein kinase Bα is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest 2005;115:2119-27.
15. Dvorak HN, Senger DR, Dvorak AM, Harvey VS, McDonagh J. Regulation of extravascular coagulation by microvascular permeability. Science 1985;227:1059-61.
16. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol 1999;237:97-132.
17. Gratton JP, Yu J, Griffith JW, et al. Cell-permeable peptides improve cellular uptake and therapeutic gene delivery of replication-deficient viruses in cells and in vivo. Nat Med 2003;9:357-62.
18. Razani B, Engelman JA, Wang XB, et al. Caveolin-1 null mice are viable but show evidence of hyper-proliferative and vascular abnormalities. J Biol Chem 2001;276:38121-38.
19. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Beliveau R. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Mol Biol Cell 2003;14: 334-47.
20. Lampugnani MG, Zanetti A, Corada M, et al. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, β-catenin, and the phosphatase DEP-1/CD148. J Cell Biol 2003;161:793-804.
21. Tanimoto T, Jin ZG, Berk BC. Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J Biol Chem 2002;277:42997-3001.
22. Zanetti A, Lampugnani MG, Balconi G, et al. Vascular endothelial growth factor induces SHC association with vascular endothelial cadherin: a potential feedback mechanism to control vascular endothelial growth factor receptor-2 signaling. Arterioscler Thromb Vasc Biol 2002;22:617-22.
23. Carmeliet P, Lampugnani MG, Moons L, et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999;98:147-57.
24. Zhao YY, Liu Y, Stan RV, et al. Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc Natl Acad Sci U S A 2002;99:11375-80.
25. Garcia-Cardena G, Martasek P, Masters BS, et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the NOS caveolin binding domain in vivo. J Biol Chem 1997;272: 25437-40.
26. Fukumura D, Gohongi T, Kadambi A, et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci U S A 2001;98:2604-9.
27. Murohara T, Asahara T, Silver M, et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 1998;101:2567-78.
28. Kashiwagi S, Izumi Y, Gohongi T, et al. NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels. J Clin Invest 2005;115:1816-27.
29. Liu J, Wang XB, Park DS, Lisanti MP. Caveolin-1 expression enhances endothelial capillary tubule formation. J Biol Chem 2002;277:10661-8.
30. Woodman SE, Ashton AW, Schubert W, et al. Caveolin-1 knockout mice show an impaired angiogenic response to exogenous stimuli. Am J Pathol 2003;162:2059-68.
31. Brouet A, DeWever J, Martinive P, et al. Antitumor effects of in vivo caveolin gene delivery are associated with the inhibition of the proangiogenic and vasodilatory effects of nitric oxide. FASEB J 2005;19:602-4.
32. O'Reilly MS, Boehm T, Shing Y, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997;88:277-85.
33. O'Reilly MS, Holmgren L, Chen C, Folkman J. Angiostatin induces and sustains dormancy of human primary tumors in mice. Nat Med 1996;2:689-92.
34. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995;1:149-53.
35. Garcia-Barros M, Paris F, Cordon-Cardo C, et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003;300:1155-9.
36. Ju H, Zou R, Venema VJ, Venema RC. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 1997; 272:18522-5.
37. Bucci M, Gratton JP, Rudic RD, et al. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med 2000;6: 1362-7.
38. Yoshiji H, Harris SR, Thorgeirsson UP. Vascular endothelial growth factor is essential for initial but not continued in vivo growth of human breast carcinoma cells. Cancer Res 1997;57:3924-8.
39. Shay-Salit A, Shushy M, Wolfovitz E, et al. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc Natl Acad Sci U S A 2002;99:9462-7.