Loss of glypican-3 function causes growth factor-dependent defects in cardiac and coronary vascular development

Developmental Biology

Volumn 335, Issue 1, 2009, Pages 208-215

  Ng, Ann ^a,b   Wong, Michelle ^a   Viviano, Beth ^a   Erlich, Jonathan M ^a   Alba, George ^a,b   Pflederer, Camila ^a   Jay, Patrick Y ^a,b   Saunders, Scott ^a,b  

^a ST LOUIS CHILDREN S HOSPITAL   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Coronary; FGF; Heart; Heparan sulfate; Proteoglycans; SHH; Vasculature

Indexed keywords

FIBROBLAST GROWTH FACTOR 9; GLYPICAN 3; GROWTH FACTOR; MESSENGER RNA; SONIC HEDGEHOG PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONGENITAL HEART DISEASE; CONTROLLED STUDY; CORONARY ARTERY FISTULA; EMBRYO; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART VENTRICLE SEPTUM DEFECT; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOUSE; MUTANT; NEWBORN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALIA; ERINACEIDAE; MUS; VERTEBRATA;

EID: 70349786507     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.08.029     Document Type: Article

References (58)

1. Aikawa T., Whipple C.A., Lopez M.E., Gunn J., Young A., Lander A.D., and Korc M. Glypican-1 modulates the angiogenic and metastatic potential of human and mouse cancer cells. J. Clin. Invest. 118 (2008) 89-99
2. Andelfinger G. Genetic factors in congenital heart malformation. Clin. Genet. 73 (2008) 516-527
3. Bashkin P., Neufeld G., Gitay-Goren H., and Vlodavsky I. Release of cell surface-associated basic fibroblast growth factor by glycosylphosphatidylinositol-specific phospholipase C. J. Cell. Physiol. 151 (1992) 126-137
4. Beckett K., Franch-Marro X., and Vincent J.P. Glypican-mediated endocytosis of Hedgehog has opposite effects in flies and mice. Trends Cell. Biol. 18 (2008) 360-363
5. Black B.L. A single mutation causes a spectrum of cardiovascular defects: the potential role of genetic modifiers, epigenetic influences, and stochastic events in phenotypic variability. J. Mol. Cell. Cardiol. 40 (2006) 201-204
6. Bonneh-Barkay D., Shlissel M., Berman B., Shaoul E., Admon A., Vlodavsky I., Carey D.J., Asundi V.K., Reich-Slotky R., and Ron D. Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors. J. Biol. Chem. 272 (1997) 12415-12421
7. Brunner G., Gabrilove J., Rifkin D.B., and Wilson E.L. Phospholipase C release of basic fibroblast growth factor from human bone marrow cultures as a biologically active complex with a phosphatidylinositol-anchored heparan sulfate proteoglycan. J. Cell. Biol. 114 (1991) 1275-1283
8. Cano-Gauci D.F., Song H.H., Yang H., McKerlie C., Choo B., Shi W., Pullano R., Piscione T.D., Grisaru S., Soon S., Sedlackova L., Tanswell A.K., Mak T.W., Yeger H., Lockwood G.A., Rosenblum N.D., and Filmus J. Glypican-3-deficient mice exhibit developmental overgrowth and some of the abnormalities typical of Simpson-Golabi-Behmel syndrome. J. Cell. Biol. 146 (1999) 255-264
9. Capurro M.I., Xu P., Shi W., Li F., Jia A., and Filmus J. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev. Cell. 14 (2008) 700-711
10. Chiao E., Fisher P., Crisponi L., Deiana M., Dragatsis I., Schlessinger D., Pilia G., and Efstratiadis A. Overgrowth of a mouse model of the Simpson-Golabi-Behmel syndrome is independent of IGF signaling. Dev. Biol. 243 (2002) 185-206
11. Colvin J.S., White A.C., Pratt S.J., and Ornitz D.M. Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development 128 (2001) 2095-2106
12. David G., Lories V., Decock B., Marynen P., Cassiman J.J., and Van den Berghe H. Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J. Cell. Biol. 111 (1990) 3165-3176
13. De Cat B., Muyldermans S.Y., Coomans C., Degeest G., Vanderschueren B., Creemers J., Biemar F., Peers B., and David G. Processing by proprotein convertases is required for glypican-3 modulation of cell survival, Wnt signaling, and gastrulation movements. J. Cell. Biol. 163 (2003) 625-635
14. Filmus J., Capurro M., and Rast J. Glypicans. Genome Biol. 9 (2008) 224
15. Flamme I., Frolich T., and Risau W. Molecular mechanisms of vasculogenesis and embryonic angiogenesis. J. Cell. Physiol. 173 (1997) 206-210
16. Gallet A., Staccini-Lavenant L., and Therond P.P. Cellular trafficking of the glypican Dally-like is required for full-strength Hedgehog signaling and wingless transcytosis. Dev. Cell. 14 (2008) 712-725
17. Goddeeris M.M., Schwartz R., Klingensmith J., and Meyers E.N. Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development 134 (2007) 1593-1604
18. Goddeeris M.M., Rho S., Petiet A., Davenport C.L., Johnson G.A., Meyers E.N., and Klingensmith J. Intracardiac septation requires hedgehog-dependent cellular contributions from outside the heart. Development 135 (2008) 1887-1895
19. Goodger S.J., Robinson C.J., Murphy K.J., Gasiunas N., Harmer N.J., Blundell T.L., Pye D.A., and Gallagher J.T. Evidence that heparin saccharides promote FGF2 mitogenesis through two distinct mechanisms. J. Biol. Chem. 283 (2008) 13001-13008
20. Grisaru S., Cano-Gauci D., Tee J., Filmus J., and Rosenblum N.D. Glypican-3 modulates BMP- and FGF-mediated effects during renal branching morphogenesis. Dev. Biol. 231 (2001) 31-46
21. Henry G.D., Byrne R., Hunyh T.T., Abraham V., Annex B.H., Hagen P.O., and Donatucci C.F. Intracavernosal injections of vascular endothelial growth factor protects endothelial dependent corpora cavernosal smooth muscle relaxation in the hypercholesterolemic rabbit: a preliminary study. Int. J. Impot. Res. 12 (2000) 334-339
22. Herr A.B., Ornitz D.M., Sasisekharan R., Venkataraman G., and Waksman G. Heparin-induced self-association of fibroblast growth factor-2. Evidence for two oligomerization processes. J. Biol. Chem. 272 (1997) 16382-16389
23. Hutson M.R., Zhang P., Stadt H.A., Sato A.K., Li Y.X., Burch J., Creazzo T.L., and Kirby M.L. Cardiac arterial pole alignment is sensitive to FGF8 signaling in the pharynx. Dev. Biol. 295 (2006) 486-497
24. Kan M., Wang F., Xu J., Crabb J.W., Hou J., and McKeehan W.L. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 259 (1993) 1918-1921
25. Kusano K.F., Pola R., Murayama T., Curry C., Kawamoto A., Iwakura A., Shintani S., Ii M., Asai J., Tkebuchava T., Thorne T., Takenaka H., Aikawa R., Goukassian D., von Samson P., Hamada H., Yoon Y.S., Silver M., Eaton E., Ma H., Heyd L., Kearney M., Munger W., Porter J.A., Kishore R., and Losordo D.W. Sonic hedgehog myocardial gene therapy: tissue repair through transient reconstitution of embryonic signaling. Nat. Med. 11 (2005) 1197-1204
26. Lai J.P., Sandhu D.S., Yu C., Han T., Moser C.D., Jackson K.K., Guerrero R.B., Aderca I., Isomoto H., Garrity-Park M.M., Zou H., Shire A.M., Nagorney D.M., Sanderson S.O., Adjei A.A., Lee J.S., Thorgeirsson S.S., and Roberts L.R. Sulfatase 2 up-regulates glypican 3, promotes fibroblast growth factor signaling, and decreases survival in hepatocellular carcinoma. Hepatology 47 (2008) 1211-1222
27. Lavine K.J., White A.C., Park C., Smith C.S., Choi K., Long F., Hui C.C., and Ornitz D.M. Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev. 20 (2006) 1651-1666
28. Lavine K.J., Kovacs A., and Ornitz D.M. Hedgehog signaling is critical for maintenance of the adult coronary vasculature in mice. J. Clin. Invest. 118 (2008) 2404-2414
29. Lavine K.J., Long F., Choi K., Smith C., and Ornitz D.M. Hedgehog signaling to distinct cell types differentially regulates coronary artery and vein development. Development 135 (2008) 3161-3171
30. Li W.E., Waldo K., Linask K.L., Chen T., Wessels A., Parmacek M.S., Kirby M.L., and Lo C.W. An essential role for connexin43 gap junctions in mouse coronary artery development. Development 129 (2002) 2031-2042
31. Lin A.E., Neri G., Hughes-Benzie R., and Weksberg R. Cardiac anomalies in the Simpson-Golabi-Behmel syndrome. Am. J. Med. Genet. 83 (1999) 378-381
32. Losordo D.W., Vale P.R., Hendel R.C., Milliken C.E., Fortuin F.D., Cummings N., Schatz R.A., Asahara T., Isner J.M., and Kuntz R.E. Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia. Circulation 105 (2002) 2012-2018
33. Morabito C.J., Kattan J., and Bristow J. Mechanisms of embryonic coronary artery development. Curr. Opin. Cardiol. 17 (2002) 235-241
34. Nugent M.A., and Edelman E.R. Kinetics of basic fibroblast growth factor binding to its receptor and heparan sulfate proteoglycan: A mechanism for cooperativity. Biochemistry 31 (1992) 8876-8883
35. Ornitz D.M., Herr A.B., Nilsson M., Westman J., Svahn C.M., and Waksman G. FGF binding and FGF receptor activation by synthetic heparan-derived di- and trisaccharides. Science 268 (1995) 432-436
36. Paine-Saunders S., Viviano B.L., and Saunders S. GPC6, a novel member of the glypican gene family, encodes a product structurally related to GPC4 and is colocalized with GPC5 on human chromosome 13. Genomics 57 (1999) 455-458
37. Paine-Saunders S., Viviano B.L., Zupicich J., Skarnes W.C., and Saunders S. Glypican-3 controls cellular responses to Bmp4 in limb patterning and skeletal development. Dev. Biol. 225 (2000) 179-187
38. Pantoliano M.W., Horlick R.A., Springer B.A., Dyk D.E.V., Tobery T., Wetmore D.R., Lear J.D., Nahapetian A.T., Bradley J.D., and Sisk W.P. Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization. Biochemistry 33 (1994) 10229-10248
39. Park E.J., Watanabe Y., Smyth G., Miyagawa-Tomita S., Meyers E., Klingensmith J., Camenisch T., Buckingham M., and Moon A.M. An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development 135 (2008) 3599-3610
40. Penisson-Besnier I., Lebouvier T., Moizard M.P., Ferre M., Barth M., Marc G., Raynaud M., and Bonneau D. Carotid artery dissection in an adult with the Simpson-Golabi-Behmel syndrome. Am. J. Med. Genet. A. 146A (2008) 464-467
41. Perrimon N., and Bernfield M. Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404 (2000) 725-728
42. Rapraeger A., Krufka A., and Olwin B.B. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252 (1991) 1705-1708
43. Ratajska A., Ciszek B., and Sowinska A. Embryonic development of coronary vasculature in rats: corrosion casting studies. Anat. Rec. A. Discov. Mol. Cell. Evol. Biol. 270 (2003) 109-116
44. Ratajska A., Zlotorowicz R., Blazejczyk M., and Wasiutynski A. Coronary artery embryogenesis in cardiac defects induced by retinoic acid in mice. Birth. Defects Res. A. Clin. Mol. Teratol. 73 (2005) 966-979
45. Reese D.E., Mikawa T., and Bader D.M. Development of the coronary vessel system. Circ. Res. 91 (2002) 761-768
46. Risau W. Mechanisms of angiogenesis. Nature 386 (1997) 671-674
47. Roghani M., Mansukhani A., Dell'Era P., Bellosta P., Basilico C., Rifkin D.B., and Moscatelli D. Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J. Biol. Chem. 269 (1994) 3976-3984
48. Saunders S., Jalkanen M., O'Farrell S., and Bernfield M. Molecular cloning of syndecan, an integral membrane proteoglycan. J. Cell. Biol. 108 (1989) 1547-1556
49. Simons M., Annex B.H., Laham R.J., Kleiman N., Henry T., Dauerman H., Udelson J.E., Gervino E.V., Pike M., Whitehouse M.J., Moon T., and Chronos N.A. Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial. Circulation 105 (2002) 788-793
50. Song H.H., Shi W., Xiang Y.Y., and Filmus J. The loss of glypican-3 induces alterations in Wnt signaling. J. Biol. Chem. 280 (2005) 2116-2125
51. Springer B.A., Pantoliano M.W., Barbera F.A., Gunyuzlu P.L., Thompson L.D., Herblin W.F., Rosenfeld S.A., and Book G.W. Identification and concerted function of two receptor binding surfaces on basic fibroblast growth factor required for mitogenesis. J. Biol. Chem. 269 (1994) 26879-26884
52. Steinfeld R., Van Den Berghe H., and David G. Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypicans. J. Cell. Biol. 133 (1996) 405-416
53. Venkataraman G., Sasisekharan V., Herr A.B., Ornitz D.M., Waksman G., Cooney C.L., Langer R., and Sasisekharan R. Preferential self-association of basic fibroblast growth factor is stabilized by heparin during receptor dimerization and activation. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 845-850
54. Veugelers M., De Cat B., Ceulemans H., Bruystens A.M., Coomans C., Durr J., Vermeesch J., Marynen P., and David G. Glypican-6, a new member of the glypican family of cell surface heparan sulfate proteoglycans. J. Biol. Chem. 274 (1999) 26968-26977
55. Wada A.M., Willet S.G., and Bader D. Coronary vessel development: a unique form of vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 2138-2145
56. White A.C., Lavine K.J., and Ornitz D.M. FGF9 and SHH regulate mesenchymal Vegfa expression and development of the pulmonary capillary network. Development 134 (2007) 3743-3752
57. Yan D., and Lin X. Drosophila glypican Dally-like acts in FGF-receiving cells to modulate FGF signaling during tracheal morphogenesis. Dev. Biol. 312 (2007) 203-216
58. Yayon A., Klagsbrun M., Esko J.D., Leder P., and Ornitz D.M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64 (1991) 841-848