NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels

Journal of Clinical Investigation

Volumn 115, Issue 7, 2005, Pages 1816-1827

  Kashiwagi, Satoshi ^a   Izumi, Yotaro ^a   Gohongi, Takeshi ^a   Demou, Zoe N ^a   Xu, Lei ^a   Huang, Paul L ^a   Buerk, Donald G ^b   Munn, Lance L ^a   Jain, Rakesh K ^a   Fukumura, Dai ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; FLUORESCENT DYE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; PROTEOGLYCAN 4; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BLOOD VESSEL WALL; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; HISTOLOGY; IMMUNOFLUORESCENCE; IN VIVO STUDY; MELANOMA; MORPHOGENESIS; MOUSE; MURAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TISSUE ENGINEERING;

ANIMALS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME INHIBITORS; GENE EXPRESSION; HUMANS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OMEGA-N-METHYLARGININE; TISSUE ENGINEERING;

EID: 22144456034     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI24015     Document Type: Article

References (63)

1. Moncada, S. 1997. Nitric oxide in the vasculature: physiology and pathophysiology. Ann. N. Y. Acad. Sci. 811:60-67.
2. Nathan, C., and Xie, Q.-W. 1994. Nitric oxide synthases: roles, tolls, and controls. Cell. 78:915-918.
3. Ignarro, L.J., Cirino, G., Casini, A., and Napoli, C. 1999. Nitric oxide as a signaling molecule in the vascular system: an overview. J. Cardiovasc. Pharmacol. 34:879-886.
4. Fukumura, D., and Jain, R.K. 1998. Role of nitric oxide in angiogenesis and microcirculation in tumors. Cancer Metastasis Rev. 17:77-89.
5. Duda, D.G., Fukumura, D., and Jain, R.K. 2004. Role of eNOS in neovascularization: NO for endothelial progenitor cells [review]. Trends Mol. Med. 10:143-145.
6. van der Zee, R., et al. 1997. Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation. 95:1030-1037.
7. Babaei, S., et al. 2003. Angiogenic actions of angiopoietin-1 require endothelium-derived nitric oxide. Am. J. Pathol. 162:1927-1936.
8. Igarashi, J., Bernier, S.G., and Michel, T. 2001. Sphingosine 1-phosphate and activation of endothelial nitric-oxide synthase, differential regulation of Akt and MAP kinase pathways by EDG and bradykinin receptors in vascular endothelial cells. J. Biol. Chem. 276:12420-12426.
9. Dimmeler, S., et al. 1999. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 399:601-605.
10. Dulak, J., et al. 2000. Nitric oxide induces the synthesis of vascular endothelial growth factor by rat vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 20:659-666.
11. Ziche, M., et al. 1997. Nitric oxide promotes proliferation and plasminogen activator production by cornoary venular endothliuim through endogenous bFGF. Circ. Res. 80:845-852.
12. Gratton, J.P., et al. 2003. Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell. 4:31-39.
13. Gallo, O., et al. 1998. Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. J. Natl. Cancer Inst. 90:584-596.
14. Lorraine, J.C., and Lala, P.K. 1999. Nitric oxide synthase inhibition by NG-nitro-L-arginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am. J. Pathol. 155:1381-1390.
15. Lee, P.C., et al. 1999. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol. 277:H1600-H1608.
16. Murohara, T., et al. 1998. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 101:2567-2578.
17. Fukumura, D., et al. 2001. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. U. S. A. 98:2604-2609.
18. Ando, A., et al. 2002. Nitric oxide is proangiogenic in the retina and choroid. J. Cell. Physiol. 191:116-124.
19. Wang, B., et al. 2001. Genetic disruption of host nitric oxide synthase II gene impairs melanoma-induced angiogenesis and suppresses pleural effusion. Int. J. Cancer. 91:607-611.
20. Konopka, T.E., et al. 2001. Nitric oxide synthase II gene disruption: implication for tumor growth and vascular endothelial growth factor production. Cancer Res. 61:3182-3187.
21. Hirschi, K.K., and D'Amore, P.A. 1996. Pericytes in the microvasculature. Cardiovasc. Res. 32:687-698.
22. Jain, R.K. 2003. Molecular regulation of vessel maturation. Nat. Med. 9:685-693.
23. Gerhardt, H., and Betsholtz, C. 2003. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 314:15-23.
24. Perlis, C., and Herlyn, M. 2004. Recent advances in melanoma biology. Oncologist. 9:182-187.
25. Hsu, M.-Y., Meier, F., and Herlyn, M. 2002. Melanoma development and progression: a conspiracy between tumor and host. Differentiation. 70:522-536.
26. Jain, R.K., Brown, E.B., Munn, L.L., and Fukumura, D. 2004. Intravital microscopy of normal and diseased tissues in mice. In Live cell imaging: a laboratory manual. R. Goldman and D. Spector, editors. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York, USA. 435-466.
27. Jain, R.K., Munn, L.L., and Fukumura, D. 2002. Dissecting tumour pathophysiology using intravital microscopy. Nat. Rev. Cancer. 2:266-276.
28. Hirschi, K.K., Rohovsky, S.A., and D'Amore, P.A. 1998. PDGF. TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J. Cell Biol 141:805-814.
29. Koike, N., et al. 2004. Tissue engineering: creation of long-lasting blood vessels. Nature. 428:138-139.
30. Folkman, J., and Kalluri, R. 2004. Cancer without disease. Nature. 427:787.
31. Carmeliet, P., and Jain, R.K. 2000. Angiogenesis in cancer and other diseases: from genes to function to therapy. Nature. 407:249-257.
32. Fidler, I.J., and Ellis, L.M. 1994. The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 79:185-188.
33. Ziche, M., et al. 1994. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 94:2036-2044.
34. Buerk, D.G., Riva, C.E., and Cranstoun, S.D. 1996. Nitric oxide has a vasodilatory role in rat optic nerve head during flicker stimuli. Microvasc. Res. 52:13-26.
35. Fulton, D., Gratton, J.P., and Sessa, W.C. 2001. Post-translational control of endothelial nitric oxide synthase: Why isn't calcium/calmodulin enough? J. Pharmacol. Exp. Ther. 299:818-824.
36. Aktan, F. 2004. iNOS-mediated nitric oxide production and its regulation. Life Sci. 75:639-653.
37. Kojima, H., et al. 1998. Development of a fluorescent indicator for nitric oxide based on the fluorescein chromophore. Chem. Pharm. Bull. 46:373-375.
38. Kojima, H., et al. 1998. Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA. Neuroreport. 9:3345-3348.
39. Blute, T.A., Lee, M.R., and Eldred, W.D. 2000. Direct imaging of NMDA-stimulated nitric oxide production in the retina. Vis. Neurosci. 17:557-566.
40. Darland, D.C., and D'Amore, P.A. 2001. Cell-cell interactions in vascular development. Curr. Top. Dev. Biol. 52:107-149.
41. Kashiwagi, S., Kaijimura, M., Yoshimura, Y., and Suematsu, M. 2002. Nonendothelial source of nitric oxide in arterioles but not in venules. Circ. Res. 91:e55-e64.
42. Jain, R.K. 1988. Determinants of tumor blood flow: a review. Cancer Res. 48:2641-2658.
43. Ambs, S., et al. 1998. p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat. Med. 4:1371-1376.
44. Papapetropoulos, A., Garcia-Cardena, G., Madri, J.A., and Sessa, W.C. 1997. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100:3131-3139.
45. Morikawa, S., et al. 2002. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 160:985-1000.
46. Hirschi, K.K., Rohovsky, S.A., Beck, L.H., Smith, S.R., and D'Amore, P.A. 1999. Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ. Res. 84:298-305.
47. Schlingemann, R.O., et al. 1991. Differential expression of markers for endothelial cells, pericytes, and basal lamina in the microvasculature of tumors and granulation tissue. Am. J. Pathol. 138:1335-1347.
48. Liu, Y., et al. 2000. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Invest. 106:951-961.
49. Suri, C., et al. 1996. Requisite role of angiopoietin-I, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 87:1171-1180.
50. Lindahl, P., Johansson, B.R., Leveen, P., and Betsholtz, C. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 277:242-245.
51. Sreejayan, N., Lin, Y., and Hassid, A. 2002. NO attenuates insulin signaling and motility in aortic smooth muscle cells via protein tyrosine phosphatase 1B-mediated mechanism. Arterioscler. Thromb. Vasc. Biol. 22:1086-1092.
52. Brown, C., Pan, X., and Hassid, A. 1999. Nitric oxide and C-type atrial natriuretic peptide stimulate primary aortic smooth muscle cell migration via a cGMP-dependent mechanism: relationship to microfilament dissociation and altered cell morphology. Circ. Res. 84:655-667.
53. Cunningham, L.D., Brecher, P., and Cohen, R.A. 1992. Platelet-derived growth factor receptors on macrovascular endothelial cells mediate relaxation via nitric oxide in rat aorta. J. Clin. Invest. 89:878-882.
54. Inoue, N., et al. 1995. Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1. Arterioscler. Thromb. Vasc. Biol. 15:1255-1261.
55. Jain, R.K. 2005. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy [review]. Science. 307:58-62.
56. Abramsson, A., et al. 2002. Analysis of mural cell recruitment to tumor vessels. Circulation. 105:112-117.
57. Moncada, S. 1992. The L-arginine: nitric oxide pathway. Acta Physiol. Scand. 145:201-227.
58. Joyce, N.C., DeCamilli, P., and Boyles J. 1984. Pericytes, like vascular smooth muscle cells, are immunocytochemically positive for cyclic GMP-dependent protein kinase. Microvasc. Res. 28:206-219.
59. Yamahara, K., et al. 2003. Significance and therapeutic potential of the natriuretic peptides/cGMP/cGMP-dependent protein kinase pathway in vascular regeneration. Proc. Natl. Acad. Sci. U. S. A. 100:3404-3409.
60. Gow, A.J., Farkouh, C.R., Munson, D.A., Posencheg, M.A., and Ischiropoulos, H. 2004. Biological significance of nitric oxide-mediated protein modifications. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L262-L268.
61. Fidler, I. 1973. Selection of successive tumour lines for metastasis. Nat. New Biol. 242:148-149.
62. Fukumura, D., et al. 2003. Patacrine regulation of angiogenesis and adipocyte differentiation during in vivo adipogenesis. Circ. Res. 93:e88-e97.
63. Demou, Z.N., and McIntire, L.V. 2002. Fully automated three-dimensional tracking of cancer cells in collagen gels: determination of motility phenotypes at the cellular level. Cancer Res. 62:5301-5307.