Molecular regulation of vessel maturation

Nature Medicine

Volumn 9, Issue 6, 2003, Pages 685-693

  Jain, Rakesh K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; CICLOPIROXOLAMINE; DNA; FIBROBLAST GROWTH FACTOR; HYBRID PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIGAND; PEPTIDE; PLATELET DERIVED GROWTH FACTOR; PR 39; PROTEIN VP16; RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN; VIRUS PROTEIN;

ANGIOGENESIS; BLOOD VESSEL FUNCTION; BLOOD VESSEL WALL; CELL TYPE; CONCENTRATION (PARAMETERS); DRUG DELIVERY SYSTEM; EXTRACELLULAR MATRIX; FORCE; GENE EXPRESSION; HUMAN; ISCHEMIA; MATURATION; MURAL CELL; NONHUMAN; PARENCHYMA; PATHOLOGY; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING; TUMOR;

ANIMALS; BLOOD VESSELS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION;

EID: 0038376002     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm0603-685     Document Type: Review

References (100)

1. Folkman, J. Angiogenesis. in Harrison's Principles of International Medicine (eds. Braunwald, E. et al.) 517-530 (McGraw-Hill, New York, 2001).
2. Jain, R.K. & Carmeliet, P.F. Vessels of death or life. Sci. Am. 285, 38-45 (2001).
3. Carmeliet, P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6, 389-395 (2000).
4. Yancopoulos, G.D. et al. Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248 (2000).
5. Carmeliet, P. & Jain, R.K. Angiogenesis in cancer and other diseases. Nature 407, 249-257 (2000).
6. Nguyen, L.L. & D'Amore, P.A. Cellular interactions in vascular growth and differentiation. Int. Rev. Cytol. 204, 1-48 (2001).
7. Rossant, J. & Howard, L. Signaling pathways in vascular development. Annu. Rev. Cell Dev. Biol. 18, 541-573 (2002).
8. Ferrara, N. VEGF and the quest for tumour angiogenesis factors. Nat. Rev. Cancer 2, 795-803 (2002).
9. Nagy, J.A. et al. VEGF-A induces angiogenesis, arteriogenesis, lymphangiogenesis, and vascular malformations. Cold Spring Harbor Symposium on Quantitative Biology 67, 227-237 (2002).
10. Hellstrom, M. et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153, 543-553 (2001).
11. Kluk, M.J. & Hla, T. Signaling of sphingosine-1-phosphate via the S1P/EDG-family of G-protein-coupled receptors. Biochim. Biophys. Acta 1582, 72-80 (2002).
12. Kluk, M.J., Colmont, C., Wu, M.T. & Hla, T. Platelet-derived growth factor (PDGF)-induced chemotaxis does not require the G protein-coupled receptor S1P1 in murine embryonic fibroblasts and vascular smooth muscle cells. FEBS Lett. 533, 25-28 (2003).
13. Cho, H., Kozasa, T., Bondjers, C., Betsholtz, C. & Kehrl, J.H. Pericyte-specific expression of Rgs5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J. 13, 440-442 (2003).
14. Loughna, S. & Sato, T.N. Angiopoietin and Tie signaling pathways in vascular development. Matrix Biol. 20, 319-325 (2001).
15. Uemura, A. et al. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J. Clin. Invest. 110, 1619-1628 (2002).
16. Pepper, M.S. Transforming growth factor-β: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 8, 21-43 (1997).
17. Chambers, R.C., Leoni, P., Kaminski, N., Laurent, G.J. & Heller, R.A. Global expression profiling of fibroblast responses to transforming growth factor-β(1) reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am. J. Pathol. 162, 533-546 (2003).
18. Gohongi, T. et al. Tumor-host interactions in the gallbladder suppress distal angiogenesis and tumor growth: involvement of transforming growth factor β1. Nat. Med. 5, 1203-1208 (1999).
19. Weinstein, M., Yang, X. & Deng, C. Functions of mammalian Smad genes as revealed by targeted gene disruption in mice. Cytokine Growth Factor Rev. 11, 49-58 (2000).
20. Goumans, M.J. et al. Balancing the activation state of the endothelium via two distinct TGF-β type I receptors. EMBO J. 21, 1743-1753 (2002).
21. Mukouyama, Y.S., Shin, D., Britsch, S., Taniguchi, M. & Anderson, D.J. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109, 693-705 (2002).
22. Neufeld, G. et al. The neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis. Trends Cardiovasc. Med. 12, 13-19 (2002).
23. Kalluri, R. Basement membranes: structural features, assembly, cellular interactions and role in cancer angiogenesis. Nat. Rev. Cancer (in the press).
24. Lawler, J. The functions of thrombospondin-1 and -2. Curr. Opin. Cell Biol. 12, 634-640 (2000).
25. Hynes, R.O. A reevaluation of integrins as regulators of angiogenesis. Nat. Med. 8, 918-921 (2002).
26. Stupack, D.G. & Cheresh, D.A. Get a ligand, get a life: integrins, signaling and cell survival. J. Cell Sci. 115, 3729-3738 (2002).
27. Fukai, N. et al. Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J. 21, 1535-1544 (2002).
28. 3 prevents maturation of blood vessels during embryonic neovascularization. J. Cell Sci. 108, 2655-2661 (1995).
29. Ruoslahti, E. Specialization of tumour vasculature. Nat. Rev. Cancer 2, 83-90 (2002).
30. Alitalo, K. & Carmeliet, P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 1, 219-227 (2002).
31. Wilting, J., Tomarev, S. & Christ, B. Lymphangioblasts in embryonic lymphangiogenesis. Lymphatic Res. Biol. 1, 33-44 (2003).
32. + lymphatic/vascular endothelial precursor cells. Blood 101, 168-172 (2003).
33. Jain, R.K. & Padera, T.P. Development. Lymphatics make the break. Science 299, 209-210 (2003).
34. Boardman, K.C. & Swartz, M.A. Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 92, 801-808 (2003).
35. Topper, J.N. & Gimbrone, M.A., Jr. Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol. Med. Today 5, 40-46 (1999).
36. Semenza, G.L. HIF-1 and mechanisms of hypoxia sensing. Curr. Opin. Cell Biol. 13, 167-171 (2001).
37. Xu, L., Fukumura, D. & Jain, R.K. Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF. J. Biol. Chem. 277, 11368-11374 (2002).
38. Helisch, A. & Schaper, W. Arteriogenesis - the development and growth of collateral arteries. Microcirculation 10, 83-97 (2003).
39. Coussens, L.M. & Werb, Z. Inflammation and cancer. Nature 420, 860-867 (2002).
40. Tomasek, J.J., Gabbiani, G., Hinz, B., Chaponnier, C. & Brown, R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349-363 (2002).
41. Zawicki, D.F., Jain, R.K., Schmid-Schoenbein, G.W. & Chien, S. Dynamics of neovascularization in normal tissue. Microvasc. Res. 21, 27-47 (1981).
42. Bloch, W. et al. The angiogenesis inhibitor endostatin impairs blood vessel maturation during wound healing. FASEB J. 14, 2373-2376 (2000).
43. Altavilla, D. et al. Inhibition of lipid peroxidation restores impaired vascular endothelial growth factor expression and stimulates wound healing and angiogenesis in the genetically diabetic mouse. Diabetes 50, 667-674 (2001).
44. Carmeliet, P. Angiogenesis in health and disease. Nat. Med. 9, 653-660 (2003).
45. Jain, R.K. Angiogenesis and lymphangiogenesis in tumors: insights from intravital microscopy. Cold Spring Harbor Symposium on Quantitative Biology 67, 239-248 (2002).
46. Jain, R.K., Munn, L.L. & Fukumura, D. Dissecting tumour pathophysiology using intravital microscopy. Nat. Rev. Cancer 2, 266-276 (2002).
47. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat. Med. 3, 177-182 (1997).
48. Baish, J.W. & Jain, R.K. Fractals and cancer. Cancer Res. 60, 3683-3688 (2000).
49. Helmlinger, G., Netti, P.A., Lichtenbeld, H.C., Melder, R.J. & Jain, R.K. Solid stress inhibits the growth of multicellular tumor spheroids. Nat. Biotechnol. 15, 778-783 (1997).
50. Chang, Y.S. et al. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. USA 97, 14608-14613 (2000).
51. Melder, R.J. et al. During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nat. Med. 2, 992-997 (1996).
52. Morikawa, S. et al. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 160, 985-1000 (2002).
53. Brown, E.B. et al. In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat. Med. 7, 864-868 (2001).
54. Fukumura, D. et al. Tumor induction of VEGF promoter activity in stromal cells. Cell 94, 715-725 (1998).
55. Hobbs, S.K. et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl. Acad. Sci. USA 95, 4607-4612 (1998).
56. Hashizume, H. et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am. J. Pathol. 156, 1363-1380 (2000).
57. Jain, R.K. & Munn, L.L. Leaky vessels? Call Angl! Nat. Med. 6, 131-132 (2000).
58. Ramanujan, S., Koenig, G.C., Padera, T.P., Stoll, B.R. & Jain, R.K. Local imbalance of proangiogenic and antiangiogenic factors: a potential mechanism of focal necrosis and dormancy in tumors. Cancer Res. 60, 1442-1448 (2000).
59. Jain, R.K. & Fenton, B.T. Intratumoral lymphatic vessels: a case of mistaken identity or malfunction? J. Natl. Cancer Inst. 94, 417-421 (2002).
60. Padera, T.P. et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296, 1883-1886 (2002).
61. Jain, R.K. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med. 7, 987-989 (2001).
62. Jain, R.K. et al. Endothelial cell death, angiogenesis, and microvascular function after castration in an androgen-dependent tumor: role of vascular endothelial growth factor. Proc. Natl. Acad. Sci. USA 95, 10820-10825 (1998).
63. Izumi, Y., Xu, L., di Tomaso, E., Fukumura, D. & Jain, R.K. Tumour biology: herceptin acts as an anti-angiogenic cocktail. Nature 416, 279-280 (2002).
64. Kadambi, A. et al. Vascular endothelial growth factor (VEGF)-C differentially affects tumor vascular function and leukocyte recruitment: role of VEGF-receptor 2 and host VEGF-A. Cancer Res. 61, 2404-2408 (2001).
65. Benjamin, L.E., Golijanin, D., Itin, A., Pode, D. & Keshet, E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J. Clin. Invest. 103, 159-165 (1999).
66. Bergers, G., Song, S., Meyer-Morse, N., Bergstand, E. & Hanahan, D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J. Clin. Invest. 111, 1287-1295 (2003).
67. Isner, J.M. Myocardial gene therapy. Nature 415, 234-239 (2002).
68. Langer, R. Where a pill won't reach. Sci. Am. 288, 50-57 (2003).
69. Baumgartner, I. et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 97, 1114-1123 (1998).
70. Dellian, M., Witwer, B.P., Salehi, H.A., Yuan, F. & Jain, R.K. Quantitation and physiological characterization of angiogenic vessels in mice: effect of basic fibroblast growth factor, vascular endothelial growth factor/vascular permeability factor, and host microenvironment. Am. J. Pathol. 149, 59-71 (1996).
71. Richardson, T.P., Peters, M.C., Ennett, A.B. & Mooney, D.J. Polymeric system for dual growth factor delivery. Nat. Biotechnol. 19, 1029-1034 (2001).
72. Thurston, G. et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med. 6, 460-463 (2000).
73. Li, J. et al. PR39, a peptide regulator of angiogenesis. Nat. Med. 6, 49-55 (2000).
74. Linden, T. et al. The antimycotic ciclopirox olamine induces HIF-1α stability, VEGF expression, and angiogenesis. FASEB J. 17, 761-763 (2003).
75. Vincent, K.A. et al. Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding an HIF-1α/VP16 hybrid transcription factor. Circulation 102, 2255-2261 (2000).
76. Shyu, K.G. et al. Intramyocardial injection of naked DNA encoding HIF-1α/VP16 hybrid to enhance angiogenesis in an acute myocardial infarction model in the rat. Cardiovasc. Res. 54, 576-583 (2002).
77. Elson, D.A. et al. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1α. Genes Dev. 15, 2520-2532 (2001).
78. Schechner, J.S. et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc. Natl. Acad. Sci. USA 97, 9191-9196 (2000).
79. Yang, J. et al. Telomerized human microvasculature is functional in vivo. Nat. Biotechnol. 19, 219-224 (2001).
80. Hirschi, K.K., Rohovsky, S.A., Beck, L.H., Smith, S.R. & D'Amore, P.A. Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ. Res. 84, 298-305 (1999).
81. Darland, D.C. & D'Amore, P.A. TGF β is required for the formation of capillary-like structures in three-dimensional cocultures of 10T1/2 and endothelial cells. Angiogenesis 4, 11-20 (2001).
82. Niklason, L.E. et al. Functional arteries grown in vitro. Science 284, 489-493 (1999).
83. Levenberg, S., Golub, J.S., Amit, M., Itskovitz-Eldor, J. & Langer, R. Endothelial cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 99, 4391-4396 (2002).
84. Yamashita, J. et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408, 92-96 (2000).
85. Yurugi-Kobayashi, T. et al. Effective contribution of transplanted vascular progenitor cells derived from embryonic stem cells to adult neovascularization in proper differentiation stage. Blood 101, 2675-2678 (2003).
86. Jiang, Y. et al. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp. Hematol. 30, 896-904 (2002).
87. Kocher, A.A. et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7, 430-436 (2001).
88. Simper, D., Stalboerger, P.G., Panetta, C.J., Wang, S. & Caplice, N.M. Smooth muscle progenitor cells in human blood. Circulation 106, 1199-1204 (2002).
89. Majka, S.M. et al. Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J. Clin. Invest. 111, 71-79 (2003).
90. Luttun, A. et al. Revascularization of ischemic tissues by PIGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat. Med. 8, 831-840 (2002).
91. Rafii, S. et al. Contribution of marrow-derived progenitors to vascular and cardiac regeneration. Semin. Cell Dev. Biol. 13, 61-67 (2002).
92. Stoll, B.R., Migliorini, C., Kadambi, A., Munn, L.L. & Jain, R.K. A mathematical model of the contribution of endothelial progenitor cells to angiogenesis in solid tumors: implications for anti-angiogenic therapy. Blood (in the press).
93. Schmid-Schoenbein, G. The second valve system in lymphatics. Lymphatic Res. Biol. 1, 25-29 (2003).
94. Reyes, M. et al. Origin of endothelial progenitors in human postnatal bone marrow. J. Clin. Invest. 109, 337-346 (2002).
95. Hungerford, J.E. & Little, C.D. Developmental biology of the vascular smooth muscle cell: building a multilayered vessel wall. J. Vasc. Res. 36, 2-27 (1999).
96. Sartore, S. et al. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ. Res. 89, 1111-1121 (2001).
97. Elenbaas, B. & Weinberg, R.A. Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp. Cell Res. 264, 169-184 (2001).
98. Powell, D.W. et al. Myofibroblasts. I. Paracrine cells important in health and disease. Am. J. Physiol. 277, C1-C9 (1999).
99. McDonald, D.M. & Choyke, P.L. Imaging of angiogenesis: from microscope to clinic. Nat. Med. 9, 713-725 (2003).
100. Gazit, Y. et al. Fractal characteristics of tumor vascular architecture during tumor growth and regression. Microcirculation 4, 395-402 (1997).