The vasostatin-I fragment of chromogranin A inhibits VEGF-induced endothelial cell proliferation and migration

FASEB Journal

Volumn 21, Issue 12, 2007, Pages 3052-3062

  Belloni, Daniela ^a   Scabini, Silvia ^a   Foglieni, Chiara ^a   Veschini, Lorenzo ^a   Giazzon, Alessio ^a   Colombo, Barbara ^a   Fulgenzi, Alessandro ^c   Helle, Karen B ^b   Ferrero, Maria Elena ^c   Corti, Angelo ^a   Ferrero, Elisabetta ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF BERGEN   (Norway)

^c CNR   (Italy)

Author keywords

Capillary like structure; ERK MAPK

Indexed keywords

CD31 ANTIGEN; CHROMOGRANIN A; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; UNCLASSIFIED DRUG; VASCULOTROPIN; VASOSTATIN I; VON WILLEBRAND FACTOR; COLLAGEN; LAMININ; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDE FRAGMENT; PROTEOGLYCAN; RECOMBINANT PROTEIN; VASCULOTROPIN A;

AMINO TERMINAL SEQUENCE; ANGIOGENESIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; COLLAGEN METABOLISM; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; IN VITRO STUDY; NEUROENDOCRINE TUMOR; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CELL MOTION; CELL SHAPE; CULTURE TECHNIQUE; CYTOLOGY; DRUG COMBINATION; FISCHER 344 RAT; GENETICS; HOMEOSTASIS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

RATTUS;

ANIMALS; ANTIGENS, CD31; CELL CULTURE TECHNIQUES; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CHROMOGRANIN A; COLLAGEN; DRUG COMBINATIONS; ENDOTHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HOMEOSTASIS; HUMANS; LAMININ; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEOGLYCANS; RATS; RATS, INBRED F344; RECOMBINANT PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VON WILLEBRAND FACTOR;

EID: 35248847560     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-6829com     Document Type: Article

References (49)

1. Michiels, C. (2003) Endothelial cell functions. J. Cell. Physiol. 196, 430-443
2. Patan, S. (2000) Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J. Neuro-Oncol. 50, 1-15
3. Meadows, K. N., Bryant, P., Vincent, P. A., and Pumiglia, K. M. (2004) Activated ras induces a proangiogenic phenotype in primary endothelial cells. Oncogene 23, 192-200
4. Carmeliet, P. (2005) VEGF as a key mediator of angiogenesis in cancer. Oncology 69 Suppl. 3, 4-10
5. Roux, P. P., and Blenis, J. (2004) ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev.: MMBR. 68, 320-344
6. Ferrero, E., Scabini, S., Magni, E., Foglieni, C., Belloni, D., Colombo, B., Curnis, F., Villa, A., Ferrero, M. E., and Corti, A. (2004) Chromogranin A protects vessels against tumor necrosis factor alpha-induced vascular leakage. FASEB J. 18, 554-556
7. Helle, K. B. (2004) The granin family of uniquely acidic proteins of the diffuse neuroendocrine system: Comparative and functional aspects. Biol. Rev. Cambridge Philos. Soc. 79, 769-794
8. Blois, A., Srebo, B., Mandalà, M., Corti, A., Helle, K. B., and Serck-Hanssen, G. (2006) The chromogranin A peptide vasostatin-I inhibits gap formation and signal transduction mediated by inflammatory agents in cultured bovine pulmonary and coronary arterial endothelial cells. Reg. Peptides 135, 554-556
9. Huttner, W. B., Gerdes, H. H., and Rosa, P. (1991) The granin (chromogranin/secretogranin) family. Trends Biochem. Sci. 16, 27-30
10. Winkler, H., and Fischer-Colbrie, R. (1992) The chromogranins A and B: The first 25 years and future perspectives. Neuroscience 49, 497-528
11. Deftos, L. J. (1991) Chromogranin A: Its role in endocrine function and as an endocrine and neuroendocrine tumor marker. Endocr. Rev. 12, 181-187
12. Helle, K. B., and Angeletti, R. H. (1994) Chromogranin A: A multipurpose prohormone? Acta. Physiol. Scand. 152, 1-10
13. Iacangelo, A. L., and Eiden, L. E. (1995) Chromogranin A: Current status as a precursor for bioactive peptides and a granulogenic/sorting factor in the regulated secretory pathway. Reg. Peptides 58, 65-88
14. O'Connor, D. T., and Bernstein, K. N. (1984) Radioimmunoassay of chromogranin A in plasma as a measure of exocytotic sympathoadrenal activity in normal subjects and patients with pheochromocytoma. New Engl. J. Med. 311, 764-770
15. Bernini, G. P., Moretti, A., Ferdeghini, M., Ricci, S., Letizia, C., D'Erasmo, E., Argenio, G. F., and Salvetti, A. (2001) A new human chromogranin 'A' immunoradiometric assay for the diagnosis of neuroendocrine tumours. Br. J. Cancer 84, 636-642
16. Ziegler, M. G., Kennedy, B., Morrissey, E., and O'Connor, D. T. (1990) Norepinephrine clearance, chromogranin A and dopamine beta hydroxylase in renal failure. Kidney Int. 37, 1357-1362
17. Corti, A., Ferrari, R., and Ceconi, C. (2000) Chromogranin A and tumor necrosis factor-alpha (TNF) in chronic heart failure. Adv. Exper. Med. Biol. 482, 351-359
18. Ceconi, C., Ferrari, R., Bachetti, T., Opasich, C., Volterrani, M., Colombo, B., Parrinello, G., and Corti, A. (2002) Chromogranin A in heart failure; a novel neurohumoral factor and a predictor for mortality. Eur. Heart J. 23, 967-974
19. Corti, A., Sanchez, L. P., Gasparri, A., Curnis, F., Longhi, R., Brandazza, A., Siccardi, A. G., and Sidoli, A. (1997) Production and structure characterisation of recombinant chromogranin A N-terminal fragments (vasostatins) - evidence of dimer-monomer equilibria. Eur. J. Biochem. 248, 692-699
20. Ferrero, E., Ferrero, M. E., Pardi, R., and Zocchi, M. R. (1995) The platelet endothelial cell adhesion molecule-1 (PECAM1) contributes to endothelial barrier function. FEBS Lett. 374, 323-326
21. Meadows, K. N., Bryant, P., and Pumiglia, K. (2001) Vascular endothelial growth factor induction of the angiogenic phenotype requires ras activation. J. Biol. Chem. 276, 49289-49298
22. Chow, S., Patel, H., and Hedley, D. W. (2001) Measurement of MAP kinase activation by flow cytometry using phospho-specific antibodies to MEK and ERK: Potential for pharmacodynamic monitoring of signal transduction inhibitors. Cytometry 46, 72-78
23. Orr, A. W., Elzie, C. A., Kucik, D. F., and Murphy-Ullrich, J. E. (2003) Thrombospondin signaling through the calreticulin/ LDL receptor-related protein co-complex stimulates random and directed cell migration. J. Cell Sci. 116, 2917-2927
24. Strasly, M., Doronzo, G., Capello, P., Valdembri, D., Arese, M., Mitola, S., Moore, P., Alessandri, G., Giovarelli, M., and Bussolino, F. (2004) CCL16 activates an angiogenic program in vascular endothelial cells. Blood 103, 40-49
25. Prewett, M., Huber, J., Li, Y., Santiago, A., O'Connor, W., King, K., Overholser, J., Hooper, A., Pytowski, B., Witte, L., Bohlen, P., and Hicklin, D. J. (1999) Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer Res. 59, 5209-5218
26. Kaneko, Y., Kitazato, K., and Basaki, Y. (2004) Integrin-linked kinase regulates vascular morphogenesis induced by vascular endothelial growth factor. J. Cell Sci. 117, 407-415
27. Aardal, S., and Helle, K. B. (1992) The vasoinhibitory activity of bovine chromogranin A fragment (vasostatin) and its independence of extracellular calcium in isolated segments of human blood vessels. Reg. Peptides 41, 9-18
28. Metz-Boutigue, M. H., Helle, K. B., and Aunis, D. (2001) The innate immunity: Roles for new antifungal and antibacterial peptidessecreted by chromaffin granules in the adrenal medulla. Curr. Med. Chem. - Immunol., Endocr. Metabol. Agents 1, 119-140
29. Blois, A., Holmsen, H., Martino, G., Corti, A., Metz-Boutigue, M. H., and Helle, K. B. (2006) Interactions of chromogranin A-derived vasostatins and monolayers of phosphatidylserine, phosphatidylcholine and phosphatidylethanolamine. Reg. Peptides 134, 30-37
30. Kang, Y. K., and Yoo, S. H. (1997) Identification of the secretory vesicle membrane binding region of chromogranin A. FEBS Lett. 404, 87-90
31. Griffioen, A. W., and Molema, G. (2000) Angiogenesis: Potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol. Rev. 52, 237-268
32. Pike, S. E., Yao, L., Jones, K. D., Cherney, B., Appella, E., Sakaguchi, K., Nakhasi, H., Teruya-Feldstein, J., Wirth, P., Gupta, G., and Tosato, G. (1998) Vasostatin, a calreticulin fragment, inhibits angiogenesis and suppresses tumor growth. J. Exper. Med. 188, 2349-2356
33. Hoefen, R. J., and Berk, B. C. (2002) The role of MAP kinases in endothelial activation. Vasc. Pharmacol. 38, 271-273
34. Waltenberger, J., Claesson-Welsh, L., Siegbahn, A., Shibuya, M., and Heldin, C. H. (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem. 269, 26988-26995
35. Cai, J., Jiang, W. G., Ahmed, A., and Boulton, M. (2006) Vascular endothelial growth factor-induced endothelial cell proliferation is regulated by interaction between VEGFR-2, SH-PTP1 and eNOS. Microvasc. Res. 71, 20-31
36. Gupta, K., Kshirsagar, S., Li, W., Gui, L., Ramakrishnan, S., Gupta, P., Law, P. Y., and Hebbel, R. P. (1999) VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exper. Cell Res. 247, 495-504
37. Zachary, I. (2003) VEGF signalling: integration and multitasking in endothelial cell biology. Biochem. Soc. Trans. 31, 1171-1177
38. Wong, C., and Jin, Z.-G. (2005) Protein kinase C- dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by vascular endothelial growth factor. J. Biol. Chem. 280, 33263-33269
39. Bullard, L. E., Qi, X., and Penn, J. S. (2003) Role of extracellular signal-responsive kinase-1 and -2 in retinal angiogenesis. Invest. Ophthalmol. Vis. Sci. 44, 1722-1731
40. Yu, Y., and Sato, J. D. (1999) MAP kinases, phosphatidylinositol 3-kinase, and p70 S6 kinase mediate the mitogenic response of human endothelial cells to vasculare endothelial growth factor. J. Cell. Physiol. 178, 235-246
41. White, C. R., Stevens, H. Y., Haidekker, M., and Frangos, J. A. (2005) Temporal gradients in shear but not spatial gradients, stimulate ERK1/2 activation in human endothelial cells. Am. J. Physiol. - Heart Circ. Physiol. 289, 2350-2355
42. Colombo, B., Curnis, F., Foglieni, C., Monno, A., Arrigoni, G., and Corti, A. (2002) Chromogranin A expression in neoplastic cells affects tumor growth and morphogenesis in mouse models. Cancer Res. 62, 941-946
43. Corti, A., and Ferrero, E. (2004) Chromogranin A in tumors: More than a marker for diagnosis and prognosis. Cur. Med. Chem. - Immunol. Endocr. Metabol. Agents 4, 161-167
44. Hsiao, R. J., Neumann, H. P., Parmer, R. J., Barbosa, J. A., and O'Connor, D. T. (1990) Chromogranin A in familial pheochromocytoma: diagnostic screening value, prediction of tumor mass, and post-resection kinetics indicating two-compartment distribution. Am. J. Med. 88, 607-613
45. Pepper, M. S. (2001) Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler. Thromb. Vasc. Biol. 21, 1104-1117
46. Heissig, B., Hattori, K., Friedrich, M., Rafii, S., and Werb, Z. (2003) Angiogenesis: Vascular remodeling of the extracellular matrix involves metalloproteinases. Cur. Opin. Hematol. 10, 136-141
47. Colombo, B., Longhi, R., Marinzi, C., Magni, F., Cattaneo, A., Yoo, S. H., Curnis, F., and Corti, A. (2002) Cleavage of chromogranin A N-terminal domain by plasmin provides a new mechanism for regulating cell adhesion. J. Biol. Chem. 277, 45911-45919
48. Andreasen, P. A., Egelund, R., and Petersen, H. H. (2000) The plasminogen activation system in tumor growth, invasion, and metastasis. Cell. Mol. Life Sci. 57, 25-40
49. Ratti, S., Curnis, F., Longhi, R., Colombo, B., Gasparri, A., Magni, F., Manera, E., Metz-Boutigue, M. H., and Corti, A. (2000) Structure-activity relationships of chromogranin A in cell adhesion. identification of an adhesion site for fibroblasts and smooth muscle cells. J. Biol. Chem. 275, 29257-29263