Essential role of glycosaminoglycans in Fgf signaling during mouse gastrulation

Cell

Volumn 114, Issue 6, 2003, Pages 727-737

  García García, María J ^a   Anderson, Kathryn V ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; GLYCOSAMINOGLYCAN; MOLECULAR MARKER; PROTEOGLYCAN; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE;

ARTICLE; CONTROLLED STUDY; EMBRYO; ENDODERM; FIBROBLAST; GASTRULATION; GENE MUTATION; GENETIC CODE; IN VITRO STUDY; MAMMAL; MESODERM; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 10744221616     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)00715-3     Document Type: Article

References (69)

1. Arman E., Haffner-Krausz R., Chen Y., Heath J.K., Lonai P. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl. Acad. Sci. USA. 95:1998;5082-5087.
2. Baeg G.H., Perrimon N. Functional binding of secreted molecules to heparan sulfate proteoglycans in Drosophila. Curr. Opin. Cell Biol. 12:2000;575-580.
3. Baeg G.H., Lin X., Khare N., Baumgartner S., Perrimon N. Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development. 128:2001;87-94.
4. Bellaiche Y., The I., Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature. 394:1998;85-88.
5. Bellosta P., Iwahori A., Plotnikov A.N., Eliseenkova A.V., Basilico C., Mohammadi M. Identification of receptor and heparin binding sites in fibroblast growth factor 4 by structure-based mutagenesis. Mol. Cell. Biol. 21:2001;5946-5957.
6. Belo J.A., Bouwmeester T., Leyns L., Kertesz N., Gallo M., Follettie M., De Robertis E.M. Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68:1997;45-57.
7. Bernfield M., Sanderson R.D. Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors. Philos. Trans. R. Soc. Lond. B Biol. Sci. 327:1990;171-186.
8. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:1999;729-777.
9. Binari R.C., Staveley B.E., Johnson W.A., Godavarti R., Sasisekharan R., Manoukian A.S. Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling. Development. 124:1997;2623-2632.
10. Brennan J., Lu C.C., Norris D.P., Rodriguez T.A., Beddington R.S., Robertson E.J. Nodal signalling in the epiblast patterns the early mouse embryo. Nature. 411:2001;965-969.
11. Burdsal C.A., Damsky C.H., Pedersen R.A. The role of E-cadherin and integrins in mesoderm differentiation and migration at the mammalian primitive streak. Development. 118:1993;829-844.
12. Campbell R.E., Mosimann S.C., van De Rijn I., Tanner M.E., Strynadka N.C. The first structure of UDP-glucose dehydrogenase reveals the catalytic residues necessary for the two-fold oxidation. Biochemistry. 39:2000;7012-7023.
13. Chapman D.L., Papaioannou V.E. Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature. 391:1998;695-697.
14. Chapman D.L., Garvey N., Hancock S., Alexiou M., Agulnik S.I., Gibson-Brown J.J., Cebra-Thomas J., Bollag R.J., Silver L.M., Papaioannou V.E. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev. Dyn. 206:1996;379-390.
15. Chiao E., Fisher P., Crisponi L., Deiana M., Dragatsis I., Schlessinger D., Pilia G., Efstratiadis A. Overgrowth of a mouse model of the Simpson-Golabi-Behmel syndrome is independent of IGF signaling. Dev. Biol. 243:2002;185-206.
16. Ciruna B., Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell. 1:2001;37-49.
17. Conlon F.L., Lyons K.M., Takaesu N., Barth K.S., Kispert A., Herrmann B., Robertson E.J. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development. 120:1994;1919-1928.
18. Costell M., Carmona R., Gustafsson E., Gonzalez-Iriarte M., Fassler R., Munoz-Chapuli R. Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecan-null mice. Circ. Res. 91:2002;158-164.
19. Crossley P.H., Martin G.R. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development. 121:1995;439-451.
20. Damjanov I., Damjanov A., Damsky C.H. Developmentally regulated expression of the cell-cell adhesion glycoprotein cell-CAM 120/80 in peri-implantation mouse embryos and extraembryonic membranes. Dev. Biol. 116:1986;194-202.
21. DasGupta R., Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 126:1999;4557-4568.
22. De Cat B., David G. Developmental roles of the glypicans. Semin. Cell Dev. Biol. 12:2001;117-125.
23. Deng C.X., Wynshaw-Boris A., Shen M.M., Daugherty C., Ornitz D.M., Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8:1994;3045-3057.
24. Furukawa K., Okajima T. Galactosyltransferase I is a gene responsible for progeroid variant of Ehlers-Danlos syndrome. molecular cloning and identification of mutations Biochim. Biophys. Acta. 1573:2002;377-381.
25. Hacker U., Lin X., Perrimon N. The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development. 124:1997;3565-3573.
26. Haerry T.E., Heslip T.R., Marsh J.L., O'Connor M.B. Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development. 124:1997;3055-3064.
27. Hastbacka J., de la Chapelle A., Mahtani M.M., Clines G., Reeve-Daly M.P., Daly M., Hamilton B.A., Kusumi K., Trivedi B., Weaver A.et al. The diastrophic dysplasia gene encodes a novel sulfate transporter. positional cloning by fine-structure linkage disequilibrium mapping Cell. 78:1994;1073-1087.
28. Hempel J., Perozich J., Romovacek H., Hinich A., Kuo I., Feingold D.S. UDP-glucose dehydrogenase from bovine liver. primary structure and relationship to other dehydrogenases Protein Sci. 3:1994;1074-1080.
29. Hogan, B.L., Blessing, M., Winnier, G.E., Suzuki, N., and Jones, C.M. (1994). Growth factors in development: the role of TGF-beta related polypeptide signalling molecules in embryogenesis. Dev. Suppl, 53-60.
30. Hynes R.O. Integrins. bidirectional, allosteric signaling machines Cell. 110:2002;673-687.
31. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:1999;195-202.
32. Kasarskis A., Manova K., Anderson K.V. A phenotype-based screen for embryonic lethal mutations in the mouse. Proc. Natl. Acad. Sci. USA. 95:1998;7485-7490.
33. Kelly R.G., Brown N.A., Buckingham M.E. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell. 1:2001;435-440.
34. Li Y., Olsen B.R. Murine models of human genetic skeletal disorders. Matrix Biol. 16:1997;49-52.
35. Lin X., Buff E.M., Perrimon N., Michelson A.M. Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development. 126:1999;3715-3723.
36. Liu P., Wakamiya M., Shea M.J., Albrecht U., Behringer R.R., Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22:1999;361-365.
37. Luo J., Sladek R., Bader J.A., Matthyssen A., Rossant J., Giguere V. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature. 388:1997;778-782.
38. Makover A., Soprano D.R., Wyatt M.L., Goodman D.S. An in situ-hybridization study of the localization of retinol-binding protein and transthyretin messenger RNAs during fetal development in the rat. Differentiation. 40:1989;17-25.
39. Martin G.R. The roles of FGFs in the early development of vertebrate limbs. Genes Dev. 12:1998;1571-1586.
40. -/- mutant mouse. J. Biol. Chem. 276:2001;35429-35434.
41. Meyers E.N., Lewandoski M., Martin G.R. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18:1998;136-141.
42. Minowada G., Jarvis L.A., Chi C.L., Neubuser A., Sun X., Hacohen N., Krasnow M.A., Martin G.R. Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development. 126:1999;4465-4475.
43. Mjaatvedt C.H., Yamamura H., Capehart A.A., Turner D., Markwald R.R. The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation. Dev. Biol. 202:1998;56-66.
44. Ornitz, D.M., and Itoh, N. (2001). Fibroblast growth factors. Genome Biol 2, reviews3005.1-30005.12.
45. Orr-Urtreger A., Givol D., Yayon A., Yarden Y., Lonai P. Developmental expression of two murine fibroblast growth factor receptors, flg and bek. Development. 113:1991;1419-1434.
46. Perrimon N., Bernfield M. Specificities of heparan sulphate proteoglycans in developmental processes. Nature. 404:2000;725-728.
47. Pilia G., Hughes-Benzie R.M., MacKenzie A., Baybayan P., Chen E.Y., Huber R., Neri G., Cao A., Forabosco A., Schlessinger D. Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat. Genet. 12:1996;241-247.
48. Rousseau F., el Ghouzzi V., Delezoide A.L., Legeai-Mallet L., Le Merrer M., Munnich A., Bonaventure J. Missense FGFR3 mutations create cysteine residues in thanatophoric dwarfism type I (TD1). Hum. Mol. Genet. 5:1996;509-512.
49. Saga Y., Miyagawa-Tomita S., Takagi A., Kitajima S., Miyazaki J., Inoue T. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development. 126:1999;3437-3447.
50. Schlessinger J., Plotnikov A.N., Ibrahimi O.A., Eliseenkova A.V., Yeh B.K., Yayon A., Linhardt R.J., Mohammadi M. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell. 6:2000;743-750.
51. Selleck S.B. Proteoglycans and pattern formation. sugar biochemistry meets developmental genetics Trends Genet. 16:2000;206-212.
52. Spicer A.P., Kaback L.A., Smith T.J., Seldin M.F. Molecular cloning and characterization of the human and mouse UDP-glucose dehydrogenase genes. J. Biol. Chem. 273:1998;25117-25124.
53. Stepp M.A., Gibson H.E., Gala P.H., Iglesia D.D., Pajoohesh-Ganji A., Pal-Ghosh S., Brown M., Aquino C., Schwartz A.M., Goldberger O.et al. Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J. Cell Sci. 115:2002;4517-4531.
54. Stickens D., Clines G., Burbee D., Ramos P., Thomas S., Hogue D., Hecht J.T., Lovett M., Evans G.A. The EXT2 multiple exostoses gene defines a family of putative tumour suppressor genes. Nat. Genet. 14:1996;25-32.
55. Sun X., Meyers E.N., Lewandoski M., Martin G.R. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 13:1999;1834-1846.
56. Sutherland A.E., Sanderson R.D., Mayes M., Seibert M., Calarco P.G., Bernfield M., Damsky C.H. Expression of syndecan, a putative low affinity fibroblast growth factor receptor, in the early mouse embryo. Development. 113:1991;339-351.
57. Tam P.P., Behringer R.R. Mouse gastrulation. the formation of a mammalian body plan Mech. Dev. 68:1997;3-25.
58. Tanaka S., Kunath T., Hadjantonakis A.K., Nagy A., Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science. 282:1998;2072-2075.
59. The I., Bellaiche Y., Perrimon N. Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol. Cell. 4:1999;633-639.
60. Thomas P., Beddington R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6:1996;1487-1496.
61. Thomas P.Q., Brown A., Beddington R.S. Hex. a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors Development. 125:1998;85-94.
62. Tsuda M., Kamimura K., Nakato H., Archer M., Staatz W., Fox B., Humphrey M., Olson S., Futch T., Kaluza V.et al. The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature. 400:1999;276-280.
63. Walsh E.C., Stainier D.Y. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science. 293:2001;1670-1673.
64. Wang Y., Saigoh K., Osaka H., Yamanishi T., Suh J., Kiyosawa H., Sakai Y., Wakana S., Wada K. YAC/BAC-based physical and transcript mapping around the gracile axonal dystrophy (gad) locus identifies Uchl1, Pmx2b, Atp3a2, and Hip2 genes. Genomics. 66:2000;333-336.
65. Wilkinson D.G., Peters G., Dickson C., McMahon A.P. Expression of the FGF-related proto-oncogene int-2 during gastrulation and neurulation in the mouse. EMBO J. 7:1988;691-695.
66. Winnier G., Blessing M., Labosky P.A., Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9:1995;2105-2116.
67. Yamada T., Pfaff S.L., Edlund T., Jessell T.M. Control of cell pattern in the neural tube. motor neuron induction by diffusible factors from notochord and floor plate Cell. 73:1993;673-686.
68. Yamaguchi T.P., Dumont D.J., Conlon R.A., Breitman M.L., Rossant J. flk-1, an flt-related receptor tyrosine kinase is an early marker for endothelial cell precursors. Development. 118:1993;489-498.
69. Yamaguchi T.P., Harpal K., Henkemeyer M., Rossant J. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 8:1994;3032-3044.