Endothelial-derived FGF2 contributes to the progression of pulmonary hypertension in humans and rodents

Journal of Clinical Investigation

Volumn 119, Issue 3, 2009, Pages 512-523

  Izikki, Mohamed ^a   Guignabert, Christophe ^a   Fadel, Elie ^b   Humbert, Marc ^c   Tu, Ly ^a   Zadigue, Patricia ^a   Dartevelle, Philippe ^b   Simonneau, Gerald ^c   Adnot, Serge ^a   Maitre, Bernard ^a   Raffestin, Bernadette ^a   Eddahibi, Saadia ^a  

^a FACULTÉ DE MÉDECINE   (France)

^b CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

3 [4 METHYL 2 (2 OXO 3 INDOLINYLMETHYLIDENYL) 3 PYRROLYL]PROPIONIC ACID; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 2 SMALL INTERFERINF RNA; FIBROBLAST GROWTH FACTOR RECEPTOR 1; MESSENGER RNA; MONOCROTALINE; PLATELET DERIVED GROWTH FACTOR BB; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; FIBROBLAST GROWTH FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CLINICAL ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; GROWTH STIMULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN SITU HYBRIDIZATION; LUNG; MALE; NONHUMAN; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; VASCULAR ENDOTHELIUM; ANIMAL; CELL CULTURE; CELL DIVISION; DISEASE COURSE; DISEASE MODEL; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL DIVISION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; HUMANS; HYPERTENSION, PULMONARY; IN SITU HYBRIDIZATION; LUNG; MUSCLE, SMOOTH, VASCULAR; PULMONARY ARTERY; RATS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 65649128937     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI35070     Document Type: Article

References (48)

1. Rubin, L.J. 1997. Primary pulmonary hypertension. N. Engl. J. Med. 336:111-117.
2. Humbert, M., et al. 2004. Cellular and molecular pathobiology of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 43:13S-24S.
3. Eddahibi, S., et al. 2006. Cross talk between endothelial and smooth muscle cells in pulmonary hypertension: critical role for serotonininduced smooth muscle hyperplasia. Circulation. 113:1857-1864.
4. Armulik, A., Abramsson, A., and Betsholtz, C. 2005. Endothelial/pericyte interactions. Circ. Res. 97:512-523.
5. Dewachter, L., et al. 2006. Angiopoietin/Tie2 pathway influences smooth muscle hyperplasia in idiopathic pulmonary hypertension. Am. J. Respir. Crit. Care Med. 174:1025-1033.
6. Powers, C.J., McLeskey, S.W., and Wellstein, A. 2000. Fibroblast growth factors, their receptors and signaling. Endocr. Relat. Cancer. 7:165-197.
7. Presta, M., et al. 2005. Fibroblast growth factor/ fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 16:159-178.
8. Arcot, S.S., Fagerland, J.A., Lipke, D.W., Gillespie, M.N., and Olson, J.W. 1995. Basic fibroblast growth factor alterations during development of monocrotaline-induced pulmonary hypertension in rats. Growth Factors. 12:121-130.
9. Potgens, A.J., Westphal, H.R., de Waal, R.M., and Ruiter, D.J. 1995. The role of vascular permeability factor and basic fibroblast growth factor in tumor angiogenesis. Biol. Chem. Hoppe-Seyler. 376:57-70.
10. Smith, K., et al. 1999. Upregulation of basic fibroblast growth factor in breast carcinoma and its relationship to vascular density, oestrogen receptor, epidermal growth factor receptor and survival. Ann. Oncol. 10:707-713.
11. Benezra, M., Vlodavsky, I., Ishai-Michaeli, R., Neufeld, G., and Bar-Shavit, R. 1993. Thrombininduced release of active basic fibroblast growth factor-heparan sulfate complexes from subendothelial extracellular matrix. Blood. 81:3324-3331.
12. Buczek-Thomas, J.A., and Nugent, M.A. 1999. Elastase-mediated release of heparan sulfate proteoglycans from pulmonary fibroblast cultures. A mechanism for basic fibroblast growth factor (bFGF) release and attenuation of bfgf binding following elastase-induced injury. J. Biol. Chem. 274:25167-25172.
13. George, S.J., Johnson, J.L., Smith, M.A., and Jackson, C.L. 2001. Plasmin-mediated fibroblast growth factor-2 mobilisation supports smooth muscle cell proliferation in human saphenous vein. J. Vasc. Res. 38:492-501.
14. Thompson, K., and Rabinovitch, M. 1996. Exogenous leukocyte and endogenous elastases can mediate mitogenic activity in pulmonary artery smooth muscle cells by release of extracellularmatrix bound basic fibroblast growth factor. J. Cell. Physiol. 166:495-505.
15. Dionne, C.A., Jaye, M., and Schlessinger, J. 1991. Structural diversity and binding of FGF receptors. Ann. N. Y. Acad. Sci. 638:161-166.
16. Inoue, Y., et al. 2002. Basic fibroblast growth factor and its receptors in idiopathic pulmonary fibrosis and lymphangioleiomyomatosis. Am. J. Respir. Crit. Care Med. 166:765-773.
17. Powell, P.P., et al. 1998. Differential expression of fibroblast growth factor receptors 1 to 4 and ligand genes in late fetal and early postnatal rat lung. Am. J. Respir. Cell Mol. Biol. 19:563-572.
18. Sher, I., et al. 2000. Identification of residues important both for primary receptor binding and specificity in fibroblast growth factor-7. J. Biol. Chem. 275:34881-34886.
19. Benisty, J.I., et al. 2004. Elevated basic fibroblast growth factor levels in patients with pulmonary arterial hypertension. Chest. 126:1255-1261.
20. Wedgwood, S., et al. 2007. Fibroblast growth factor-2 expression is altered in lambs with increased pulmonary blood flow and pulmonary hypertension. Pediatr. Res. 61:32-36.
21. Molteni, A., Ward, W.F., Ts'ao, C.H., and Hinz, J.M. 1989. Monocrotaline-induced cardiopulmonary injury in rats. Modification by the neutrophil elastase inhibitor SC39026. Biochem. Pharmacol. 38:2411-2419.
22. Molteni, A., Ward, W.F., Ts'ao, C.H., and Solliday, N.H. 1986. Monocrotaline-induced cardiopulmonary damage in rats: amelioration by the angiotensin-converting enzyme inhibitor CL242817. Proc. Soc. Exp. Biol. Med. 182:483-493.
23. Molteni, A., Ward, W.F., Ts'ao, C.H., and Solliday, N.H. 1989. Monocrotaline pneumotoxicity in mice. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 57:149-155.
24. Pan, L.C., Wilson, D.W., Lame, M.W., Jones, A.D., and Segall, H.J. 1993. COR pulmonale is caused by monocrotaline and dehydromonocrotaline, but not by glutathione or cysteine conjugates of dihydropyrrolizine. Toxicol. Appl. Pharmacol. 118:87-97.
25. Baird, A., and Ling, N. 1987. Fibroblast growth factors are present in the extracellular matrix produced by endothelial cells in vitro: implications for a role of heparinase-like enzymes in the neovascular response. Biochem. Biophys. Res. Commun. 142:428-435.
26. Vlodavsky, I., et al. 1987. Endothelial cell-derived basic fibroblast growth factor: synthesis and deposition into subendothelial extracellular matrix. Proc. Natl. Acad. Sci. U. S. A. 84:2292-2296.
27. Cucina, A., et al. 2002. Autocrine production of basic fibroblast growth factor translated from novel synthesized mRNA mediates thrombininduced mitogenesis in smooth muscle cells. Cell Biochem. Funct. 20:39-46.
28. Lee, T.H., et al. 2006. Heterogeneity of capillary endothelial cells for basic fibroblast growth factor-induced paracrine signaling. Endothelium. 13:191-203.
29. Billottet, C., Elkhatib, N., Thiery, J.P., and Jouanneau, J. 2004. Targets of fibroblast growth factor 1 (FGF-1) and FGF-2 signaling involved in the invasive and tumorigenic behavior of carcinoma cells. Mol. Biol. Cell. 15:4725-4734.
30. Gabrilove, J.L. 2001. Angiogenic growth factors: autocrine and paracrine regulation of survival in hematologic malignancies. Oncologist. 6(Suppl. 5):4-7.
31. Giavazzi, R., et al. 2003. Distinct role of fibroblast growth factor-2 and vascular endothelial growth factor on tumor growth and angiogenesis. Am. J. Pathol. 162:1913-1926.
32. Nguyen, M., et al. 1994. Elevated levels of an angiogenic peptide, basic fibroblast growth factor, in the urine of patients with a wide spectrum of cancers. J. Natl. Cancer Inst. 86:356-361.
33. Guignabert, C., et al. 2005. Serotonin transporter inhibition prevents and reverses monocrotalineinduced pulmonary hypertension in rats. Circulation. 111:2812-2819.
34. van Suylen, R.J., Smits, J.F., and Daemen, M.J. 1998. Pulmonary artery remodeling differs in hypoxia- and monocrotaline-induced pulmonary hypertension. Am. J. Respir. Crit. Care Med. 157:1423-1428.
35. Pardo, O.E., et al. 2006. FGF-2 protects small cell lung cancer cells from apoptosis through a complex involving PKCepsilon, B-Raf and S6K2. EMBO J. 25:3078-3088.
36. Xiao, D., et al. 2008. Inhibition of fibroblast growth factor 2-induced apoptosis involves survivin expression, protein kinase C alpha activation and subcellular translocation of Smac in human small cell lung cancer cells. Acta Biochim. Biophys. Sin. (Shanghai). 40:297-303.
37. Kennedy, S.H., et al. 1997. Basic FGF regulates interstitial collagenase gene expression in human smooth muscle cells. J. Cell. Biochem. 65:32-41.
38. Holnthoner, W., Kerenyi, M., Groger, M., Kratochvill, F., and Petzelbauer, P. 2006. Regulation of matrilysin expression in endothelium by fibroblast growth factor-2. Biochem. Biophys. Res. Commun. 342:725-733.
39. Pintucci, G., et al. 2003. Induction of stromelysin-1 (MMP-3) by fibroblast growth factor-2 (FGF-2) in FGF-2-/- microvascular endothelial cells requires prolonged activation of extracellular signal-regulated kinases-1 and -2 (ERK-1/2). J. Cell. Biochem. 90:1015-1025.
40. Besser, D., Presta, M., and Nagamine, Y. 1995. Elucidation of a signaling pathway induced by FGF-2 leading to uPA gene expression in NIH 3T3 fibroblasts. Cell Growth Differ. 6:1009-1017.
41. Ribatti, D., et al. 1999. In vivo angiogenic activity of urokinase: role of endogenous fibroblast growth factor-2. J. Cell Sci. 112:4213-4221.
42. Naik, M.U., Vuppalanchi, D., and Naik, U.P. 2003. Essential role of junctional adhesion molecule-1 in basic fibroblast growth factor-induced endothelial cell migration. Arterioscler. Thromb. Vasc. Biol. 23:2165-2171.
43. Merklinger, S.L., Jones, P.L., Martinez, E.C., and Rabinovitch, M. 2005. Epidermal growth factor receptor blockade mediates smooth muscle cell apoptosis and improves survival in rats with pulmonary hypertension. Circulation. 112:423-431.
44. Schermuly, R.T., et al. 2005. Reversal of experimental pulmonary hypertension by PDGF inhibition. J. Clin. Invest. 115:2811-2821.
45. Eddahibi, S., et al. 2001. Serotonin transporter overexpression is responsible for pulmonary artery smooth muscle hyperplasia in primary pulmonary hypertension. J. Clin. Invest. 108:1141-1150.
46. Schalling, M., Dagerlind, A., Stieg, P., Lindquist, C., and Hokfelt, T. 1991. Colocalization of neurotransmitters analyzed by in situ hybridization. Eur. Neuropsychopharmacol. 1:173-176.
47. Raj, T., et al. 2006. Inhibition of fibroblast growth factor receptor signaling attenuates atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 26:1845-1851.
48. Carson, F.L. 1997. Histotechnology: a self-instructional text. American Society for Clinical Pathologists Press. Chicago, Illinois, USA. 304 pp.