Fibrillin-1 Mutations Causing Weill-Marchesani Syndrome and Acromicric and Geleophysic Dysplasias Disrupt Heparan Sulfate Interactions

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Cain, Stuart A ^a   McGovern, Amanda ^a   Baldwin, Andrew K ^a   Baldock, Clair ^a   Kielty, Cay M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLIN 1; FIBRILLIN 2; HEPARAN SULFATE; HEPARIN; ISOPROTEIN; OLIGOSACCHARIDE;

ACROMICRIC DYSPLASIA; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL ADHESION; CELL SPREADING; CONTROLLED STUDY; DYSPLASIA; GELEOPHYSIC DYSPLASIA; HUMAN; HUMAN CELL; MUTAGENESIS; MUTATIONAL ANALYSIS; PATHOPHYSIOLOGY; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN FUNCTION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; WEILL MARCHESANI SYNDROME;

BINDING SITES; BONE DISEASES, DEVELOPMENTAL; CELL LINE; FIBROBLASTS; GENE DELETION; HEK293 CELLS; HEPARITIN SULFATE; HUMANS; LIMB DEFORMITIES, CONGENITAL; MICROFILAMENT PROTEINS; MUTAGENESIS; MUTATION; OLIGOSACCHARIDES; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; WEILL-MARCHESANI SYNDROME;

EID: 84868306933     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048634     Document Type: Article

References (39)

1. Pereira L, D'Alessio M, Ramirez F, Lynch JR, Sykes B, et al. (1993) Genomic organization of the sequence coding for fibrillin, the defective gene product in Marfan syndrome. Hum Mol Genet 2: 961-968.
2. Kielty CM, (2006) Elastic fibres in health and disease. Expert Rev Mol Med 8: 1-23.
3. Hubmacher D, El-Hallous EI, Nelea V, Kaartinen MT, Lee ER, et al. (2008) Biogenesis of extracellular microfibrils: Multimerization of the fibrillin-1 C terminus into bead-like structures enables self-assembly. Proc Natl Acad Sci U S A 105: 6548-6553.
4. Ritty TM, Broekelmann TJ, Werneck CC, Mecham RP, (2003) Fibrillin-1 and-2 contain heparin-binding sites important for matrix deposition and that support cell attachment. Biochem J 375: 425-432.
5. Tiedemann K, Batge B, Muller PK, Reinhardt DP, (2001) Interactions of fibrillin-1 with heparin/heparan sulfate, implications for microfibrillar assembly. J Biol Chem 276: 36035-36042.
6. Cain SA, Baldock C, Gallagher J, Morgan A, Bax DV, et al. (2005) Fibrillin-1 interactions with heparin. Implications for microfibril and elastic fiber assembly. J Biol Chem 280: 30526-30537.
7. Cain SA, Baldwin AK, Mahalingam Y, Raynal B, Jowitt TA, et al. (2008) Heparan sulfate regulates fibrillin-1 N- and C-terminal interactions. J Biol Chem 283: 27017-27027.
8. Bax DV, Bernard SE, Lomas A, Morgan A, Humphries J, et al. (2003) Cell adhesion to fibrillin-1 molecules and microfibrils is mediated by alpha 5 beta 1 and alpha v beta 3 integrins. J Biol Chem 278: 34605-34616.
9. Bax DV, Mahalingam Y, Cain S, Mellody K, Freeman L, et al. (2007) Cell adhesion to fibrillin-1: identification of an Arg-Gly-Asp-dependent synergy region and a heparin-binding site that regulates focal adhesion formation. J Cell Sci 120: 1383-1392.
10. Jovanovic J, Takagi J, Choulier L, Abrescia NG, Stuart DI, et al. (2007) alphaVbeta6 is a novel receptor for human fibrillin-1. Comparative studies of molecular determinants underlying integrin-rgd affinity and specificity. J Biol Chem 282: 6743-6751.
11. Pfaff M, Reinhardt DP, Sakai LY, Timpl R, (1996) Cell adhesion and integrin binding to recombinant human fibrillin-1. FEBS Lett 384: 247-250.
12. Sakamoto H, Broekelmann T, Cheresh DA, Ramirez F, Rosenbloom J, et al. (1996) Cell-type specific recognition of RGD- and non-RGD-containing cell binding domains in fibrillin-1. J Biol Chem 271: 4916-4922.
13. Robinson PN, Arteaga-Solis E, Baldock C, Collod-Beroud G, Booms P, et al. (2006) The molecular genetics of Marfan syndrome and related disorders. J Med Genet 43: 769-787.
14. Faivre L, Gorlin RJ, Wirtz MK, Godfrey M, Dagoneau N, et al. (2003) In frame fibrillin-1 gene deletion in autosomal dominant Weill-Marchesani syndrome. J Med Genet 40: 34-36.
15. Sengle G, Tsutsui K, Keene DR, Tufa SF, Carlson EJ, et al. (2012) Microenvironmental regulation by fibrillin-1. PLoS Genet 8: e1002425.
16. Le Goff C, Mahaut C, Wang LW, Allali S, Abhyankar A, et al. (2011) Mutations in the TGFbeta binding-protein-like domain 5 of FBN1 are responsible for acromicric and geleophysic dysplasias. Am J Hum Genet 89: 7-14.
17. Rock MJ, Cain SA, Freeman LJ, Morgan A, Mellody K, et al. (2004) Molecular basis of elastic fiber formation. Critical interactions and a tropoelastin-fibrillin-1 cross-link. J Biol Chem 279: 23748-23758.
18. Roessle MW, Klaering R, Ristau U, Robrahn B, Jahn D, et al. (2007) Upgrade of the small-angle X-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg. J Appl Crystallogr 40: S190-S194.
19. Berry A, Helsby WI, Parker BT, Hall CJ, Buksh PA, et al. (2003) The Rapid2 X-ray detection system. Nuclear Instruments & Methods in Physics Research Section a-Accelerators Spectrometers Detectors and Associated Equipment 513: 260-263.
20. Lewis RA, Helsby WI, Jones AO, Hall CJ, Parker B, et al. (1997) The "RAPID" high rate large area X-ray detector system. Nuclear Instruments & Methods in Physics Research Section a-Accelerators Spectrometers Detectors and Associated Equipment 392: 32-41.
21. Petoukhov MV, Svergun DI, (2005) Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys J 89: 1237-1250.
22. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
23. Smallridge RS, Whiteman P, Werner JM, Campbell ID, Handford PA, et al. (2003) Solution structure and dynamics of a calcium binding epidermal growth factor-like domain pair from the neonatal region of human fibrillin-1. J Biol Chem 278: 12199-12206.
24. Lee SS, Knott V, Jovanovic J, Harlos K, Grimes JM, et al. (2004) Structure of the integrin binding fragment from fibrillin-1 gives new insights into microfibril organization. Structure (Camb) 12: 717-729.
25. Volkov VV, Svergun DI, (2003) Uniqueness of ab initio shape determination in small-angle scattering. Journal of Applied Crystallography 36: 860-864.
26. Svergun D, Barberato C, Koch MHJ, (1995) CRYSOL- A program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. Journal of Applied Crystallography 28: 768-773.
27. de la Torre JG, Huertas ML, Carrasco B, (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophysical Journal 78: 719-730.
28. Rai N, Nollmann M, Spotorno B, Tassara G, Byron O, et al. (2005) SOMO (SOlution MOdeler) differences between X-Ray- and NMR-derived bead models suggest a role for side chain flexibility in protein hydrodynamics. Structure 13: 723-734.
29. Rhys NH, Wang MC, Jowitt TA, Helliwell JR, Grossmann JG, et al. (2011) Deriving the ultrastructure of alpha-crustacyanin using lower-resolution structural and biophysical methods. J Synchrotron Radiat 18: 79-83.
30. Schuck P, (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
31. Laue TM, Shah BD, Ridgeway TM, Pelletier SL (1992) Computer-aided interpretation of analytical sedimentation data for proteins. In: Harding SE, Rowe AJ, Horton JC, editors. Analytical ultracentrifugation in biochemistry and polymer science. Cambridge, United Kingdom: Royal Society of Chemistry. 90-125.
32. Couchman JR, (2010) Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 26: 89-114.
33. Mahalingam Y, Gallagher JT, Couchman JR, (2007) Cellular adhesion responses to the heparin-binding (HepII) domain of fibronectin require heparan sulfate with specific properties. J Biol Chem 282: 3221-3230.
34. Baldock C, Siegler V, Bax DV, Cain SA, Mellody KT, et al. (2006) Nanostructure of fibrillin-1 reveals compact conformation of EGF arrays and mechanism for extensibility. Proc Natl Acad Sci U S A 103: 11922-11927.
35. Loeys BL, Gerber EE, Riegert-Johnson D, Iqbal S, Whiteman P, et al. (2010) Mutations in fibrillin-1 cause congenital scleroderma: stiff skin syndrome. Sci Transl Med 2: 23ra20.
36. Dagoneau N, Benoist-Lasselin C, Huber C, Faivre L, Megarbane A, et al. (2004) ADAMTS10 mutations in autosomal recessive Weill-Marchesani syndrome. Am J Hum Genet 75: 801-806.
37. Morales J, Al-Sharif L, Khalil DS, Shinwari JM, Bavi P, et al. (2009) Homozygous mutations in ADAMTS10 and ADAMTS17 cause lenticular myopia, ectopia lentis, glaucoma, spherophakia, and short stature. Am J Hum Genet 85: 558-568.
38. Kutz WE, Wang LW, Bader HL, Majors AK, Iwata K, et al. (2011) ADAMTS10 protein interacts with fibrillin-1 and promotes its deposition in extracellular matrix of cultured fibroblasts. J Biol Chem 286: 17156-17167.
39. Manon-Jensen T, Itoh Y, Couchman JR, (2010) Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J 277: 3876-3889.