Structure of the fibrillin-1 N-terminal domains suggests that heparan sulfate regulates the early stages of microfibril assembly

Structure

Volumn 21, Issue 10, 2013, Pages 1743-1756

  Yadin, David A ^a   Robertson, Ian B ^a   McNaught Davis, Joanne ^a   Evans, Paul ^a   Stoddart, David ^a   Handford, Penny A ^a   Jensen, Sacha A ^a   Redfield, Christina ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBRILLIN 1; HEPARAN SULFATE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; FIBER; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; HEPARITIN SULFATE; HUMANS; HYDROGEN BONDING; MICROFIBRILS; MICROFILAMENT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84885421427     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.08.004     Document Type: Article

References (58)

1. C. Baldock, V. Siegler, D.V. Bax, S.A. Cain, K.T. Mellody, A. Marson, J.L. Haston, R. Berry, M.C. Wang, and J.G. Grossmann Nanostructure of fibrillin-1 reveals compact conformation of EGF arrays and mechanism for extensibility Proc. Natl. Acad. Sci. USA 103 2006 11922 11927
2. B. Bishop, A.R. Aricescu, K. Harlos, C.A. O'Callaghan, E.Y. Jones, and C. Siebold Structural insights into hedgehog ligand sequestration by the human hedgehog-interacting protein HHIP Nat. Struct. Mol. Biol. 16 2009 698 703
3. P. Bork, A.K. Downing, B. Kieffer, and I.D. Campbell Structure and distribution of modules in extracellular proteins Q. Rev. Biophys. 29 1996 119 167
4. G. Bruylants, and C. Redfield (15)N NMR relaxation data reveal significant chemical exchange broadening in the alpha-domain of human alpha-lactalbumin Biochemistry 48 2009 4031 4039
5. S.A. Cain, C. Baldock, J. Gallagher, A. Morgan, D.V. Bax, A.S. Weiss, C.A. Shuttleworth, and C.M. Kielty Fibrillin-1 interactions with heparin. Implications for microfibril and elastic fiber assembly J. Biol. Chem. 280 2005 30526 30537
6. B.H. Chung, S.T. Lam, T.M. Tong, S.Y. Li, K.S. Lun, D.H. Chan, S.F. Fok, J.S. Or, D.K. Smith, W. Yang, and Y.L. Lau Identification of novel FBN1 and TGFBR2 mutations in 65 probands with Marfan syndrome or Marfan-like phenotypes Am. J. Med. Genet. A. 149A 2009 1452 1459
7. J. Cordle, S. Johnson, J.Z. Tay, P. Roversi, M.B. Wilkin, B.H. de Madrid, H. Shimizu, S. Jensen, P. Whiteman, and B. Jin A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cis-inhibition Nat. Struct. Mol. Biol. 15 2008 849 857
8. J. Cordle, C. Redfield, M. Stacey, P.A. van der Merwe, A.C. Willis, B.R. Champion, S. Hambleton, and P.A. Handford Localization of the delta-like-1-binding site in human Notch-1 and its modulation by calcium affinity J. Biol. Chem. 283 2008 11785 11793
9. A.K. Downing, V. Knott, J.M. Werner, C.M. Cardy, I.D. Campbell, and P.A. Handford Solution structure of a pair of calcium-binding epidermal growth factor-like domains: implications for the Marfan syndrome and other genetic disorders Cell 85 1996 597 605
10. E. El-Hallous, T. Sasaki, D. Hubmacher, M. Getie, K. Tiedemann, J. Brinckmann, B. Bätge, E.C. Davis, and D.P. Reinhardt Fibrillin-1 interactions with fibulins depend on the first hybrid domain and provide an adaptor function to tropoelastin J. Biol. Chem. 282 2007 8935 8946
11. L. Faivre, R.J. Gorlin, M.K. Wirtz, M. Godfrey, N. Dagoneau, J.R. Samples, M. Le Merrer, G. Collod-Beroud, C. Boileau, A. Munnich, and V. Cormier-Daire In frame fibrillin-1 gene deletion in autosomal dominant Weill-Marchesani syndrome J. Med. Genet. 40 2003 34 36
12. A. Grishaev, and A. Bax An empirical backbone-backbone hydrogen-bonding potential in proteins and its applications to NMR structure refinement and validation J. Am. Chem. Soc. 126 2004 7281 7292
13. L. Holm, and P. Rosenström Dali server: conservation mapping in 3D Nucleic Acids Res. 38 Web Server issue 2010 W545 W549
14. D. Hubmacher, E.I. El-Hallous, V. Nelea, M.T. Kaartinen, E.R. Lee, and D.P. Reinhardt Biogenesis of extracellular microfibrils: Multimerization of the fibrillin-1 C terminus into bead-like structures enables self-assembly Proc. Natl. Acad. Sci. USA 105 2008 6548 6553
15. S.A. Jensen, A.R. Corbett, V. Knott, C. Redfield, and P.A. Handford Ca2+-dependent interface formation in fibrillin-1 J. Biol. Chem. 280 2005 14076 14084
16. S.A. Jensen, S. Iqbal, E.D. Lowe, C. Redfield, and P.A. Handford Structure and interdomain interactions of a hybrid domain: a disulphide-rich module of the fibrillin/LTBP superfamily of matrix proteins Structure 17 2009 759 768
17. L.E. Kay, D.A. Torchia, and A. Bax Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease Biochemistry 28 1989 8972 8979
18. L. Kay, B. Brooks, S. Sparks, D. Torchia, and A. Bax Measurement of NH-C-alpha-H coupling-constants in staphylococcal nuclease by two-dimensional NMR and comparison with X-ray crystallographic result J. Am. Chem. Soc. 111 1989 5488 5490
19. D.R. Keene, B.K. Maddox, H.J. Kuo, L.Y. Sakai, and R.W. Glanville Extraction of extendable beaded structures and their identification as fibrillin-containing extracellular matrix microfibrils J. Histochem. Cytochem. 39 1991 441 449
20. S. Kettle, C.M. Card, S. Hutchinson, B. Sykes, and P.A. Handford Characterisation of fibrillin-1 cDNA clones in a human fibroblast cell line that assembles microfibrils Int. J. Biochem. Cell Biol. 32 2000 201 214
21. C.M. Kielty, C. Cummings, S.P. Whittaker, C.A. Shuttleworth, and M.E. Grant Isolation and ultrastructural analysis of microfibrillar structures from foetal bovine elastic tissues. Relative abundance and supramolecular architecture of type VI collagen assemblies and fibrillin J. Cell Sci. 99 1991 797 807
22. V. Knott, A.K. Downing, C.M. Cardy, and P. Handford Calcium binding properties of an epidermal growth factor-like domain pair from human fibrillin-1 J. Mol. Biol. 255 1996 22 27
23. C.L. Kuo, Z. Isogai, D.R. Keene, N. Hazeki, R.N. Ono, G. Sengle, H.P. Bächinger, and L.Y. Sakai Effects of fibrillin-1 degradation on microfibril ultrastructure J. Biol. Chem. 282 2007 4007 4020
24. J. Kuszewski, A.M. Gronenborn, and G.M. Clore Improving the quality of NMR and crystallographic protein structures by means of a conformational database potential derived from structure databases Protein Sci. 5 1996 1067 1080
25. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486
26. C. Le Goff, C. Mahaut, L.W. Wang, S. Allali, A. Abhyankar, S. Jensen, L. Zylberberg, G. Collod-Beroud, D. Bonnet, and Y. Alanay Mutations in the TGFβ binding-protein-like domain 5 of FBN1 are responsible for acromicric and geleophysic dysplasias Am. J. Hum. Genet. 89 2011 7 14
27. B. Lee, M. Godfrey, E. Vitale, H. Hori, M.G. Mattei, M. Sarfarazi, P. Tsipouras, F. Ramirez, and D.W. Hollister Linkage of Marfan syndrome and a phenotypically related disorder to two different fibrillin genes Nature 352 1991 330 334
28. S.S. Lee, V. Knott, J. Jovanović, K. Harlos, J.M. Grimes, L. Choulier, H.J. Mardon, D.I. Stuart, and P.A. Handford Structure of the integrin binding fragment from fibrillin-1 gives new insights into microfibril organization Structure 12 2004 717 729
29. Z. Lian, J. Liu, L. Li, X. Li, M. Clayton, M.C. Wu, H.Y. Wang, P. Arbuthnot, M. Kew, D. Fan, and M.A. Feitelson Enhanced cell survival of Hep3B cells by the hepatitis B x antigen effector, URG11, is associated with upregulation of beta-catenin Hepatology 43 2006 415 424
30. G. Lin, K. Tiedemann, T. Vollbrandt, H. Peters, B. Batge, J. Brinckmann, and D.P. Reinhardt Homo- and heterotypic fibrillin-1 and -2 interactions constitute the basis for the assembly of microfibrils J. Biol. Chem. 277 2002 50795 50804
31. B.L. Loeys, E.E. Gerber, D. Riegert-Johnson, S. Iqbal, P. Whiteman, V. McConnell, C.R. Chillakuri, D. Macaya, P.J. Coucke, and A. De Paepe Mutations in fibrillin-1 cause congenital scleroderma: stiff skin syndrome Sci. Transl. Med. 2 2010 23ra20
32. L. Lönnqvist, D. Reinhardt, L. Sakai, and L. Peltonen Evidence for furin-type activity-mediated C-terminal processing of profibrillin-1 and interference in the processing by certain mutations Hum. Mol. Genet. 7 1998 2039 2044
33. R. Maiti, G.H. Van Domselaar, H. Zhang, and D.S. Wishart SuperPose: a simple server for sophisticated structural superposition Nucleic Acids Res. 32 Web Server issue 2004 W590 W594
34. T. Malinauskas, A.R. Aricescu, W. Lu, C. Siebold, and E.Y. Jones Modular mechanism of Wnt signaling inhibition by Wnt inhibitory factor 1 Nat. Struct. Mol. Biol. 18 2011 886 893
35. A. Marson, M.J. Rock, S.A. Cain, L.J. Freeman, A. Morgan, K. Mellody, C.A. Shuttleworth, C. Baldock, and C.M. Kielty Homotypic fibrillin-1 interactions in microfibril assembly J. Biol. Chem. 280 2005 5013 5021
36. R.N. Ono, G. Sengle, N.L. Charbonneau, V. Carlberg, H.P. Bächinger, T. Sasaki, S. Lee-Arteaga, L. Zilberberg, D.B. Rifkin, and F. Ramirez Latent transforming growth factor beta-binding proteins and fibulins compete for fibrillin-1 and exhibit exquisite specificities in binding sites J. Biol. Chem. 284 2009 16872 16881
37. L. Pereira, M. D'Alessio, F. Ramirez, J.R. Lynch, B. Sykes, T. Pangilinan, and J. Bonadio Genomic organization of the sequence coding for fibrillin, the defective gene product in Marfan syndrome Hum. Mol. Genet. 2 1993 961 968
38. M. Pfaff, D.P. Reinhardt, L.Y. Sakai, and R. Timpl Cell adhesion and integrin binding to recombinant human fibrillin-1 FEBS Lett. 384 1996 247 250
39. A. Piha-Gossack, W. Sossin, and D.P. Reinhardt The evolution of extracellular fibrillins and their functional domains PLoS ONE 7 2012 e33560
40. S. Reber-Müller, T. Spissinger, P. Schuchert, J. Spring, and V. Schmid An extracellular matrix protein of jellyfish homologous to mammalian fibrillins forms different fibrils depending on the life stage of the animal Dev. Biol. 169 1995 662 672
41. D.P. Reinhardt, D.R. Keene, G.M. Corson, E. Pöschl, H.P. Bächinger, J.E. Gambee, and L.Y. Sakai Fibrillin-1: organization in microfibrils and structural properties J. Mol. Biol. 258 1996 104 116
42. D.P. Reinhardt, J.E. Gambee, R.N. Ono, H.P. Bächinger, and L.Y. Sakai Initial steps in assembly of microfibrils. Formation of disulfide-cross-linked multimers containing fibrillin-1 J. Biol. Chem. 275 2000 2205 2210
43. I. Robertson, S. Jensen, and P. Handford TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs Biochem. J. 433 2011 263 276
44. I.B. Robertson, I. Osuch, D.A. Yadin, P.A. Handford, S.A. Jensen, and C. Redfield (1)H, (13)C and (15)N resonance assignments for the fibrillin-1 EGF2-EGF3-hybrid1-cbEGF1 four-domain fragment Biomol. NMR Assign. 2013 10.1007/s12104-013-9481-7 Published online May 7, 2013
45. L.Y. Sakai, D.R. Keene, and E. Engvall Fibrillin, a new 350-kD glycoprotein, is a component of extracellular microfibrils J. Cell Biol. 103 1986 2499 2509
46. L.Y. Sakai, D.R. Keene, R.W. Glanville, and H.P. Bächinger Purification and partial characterization of fibrillin, a cysteine-rich structural component of connective tissue microfibrils J. Biol. Chem. 266 1991 14763 14770
47. H. Sakai, R. Visser, S. Ikegawa, E. Ito, H. Numabe, Y. Watanabe, H. Mikami, T. Kondoh, H. Kitoh, and R. Sugiyama Comprehensive genetic analysis of relevant four genes in 49 patients with Marfan syndrome or Marfan-related phenotypes Am. J. Med. Genet. A. 140 2006 1719 1725
48. C. Schwieters, J. Kuszewski, and G. Clore Using Xplor-NIH for NMR molecular structure determination Prog. Nucl. Magn. Reson. Spectrosc. 48 2006 47 62
49. G. Sengle, N.L. Charbonneau, R.N. Ono, T. Sasaki, J. Alvarez, D.R. Keene, H.P. Bächinger, and L.Y. Sakai Targeting of bone morphogenetic protein growth factor complexes to fibrillin J. Biol. Chem. 283 2008 13874 13888
50. G. Sengle, R.N. Ono, T. Sasaki, and L.Y. Sakai Prodomains of transforming growth factor beta (TGFbeta) superfamily members specify different functions: extracellular matrix interactions and growth factor bioavailability J. Biol. Chem. 286 2011 5087 5099
51. Y. Shen, F. Delaglio, G. Cornilescu, and A. Bax TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44 2009 213 223
52. C. Stheneur, G. Collod-Béroud, L. Faivre, J.F. Buyck, L. Gouya, J.M. Le Parc, B. Moura, C. Muti, B. Grandchamp, and G. Sultan Identification of the minimal combination of clinical features in probands for efficient mutation detection in the FBN1 gene Eur. J. Hum. Genet. 17 2009 1121 1128
53. K. Tiedemann, B. Bätge, P.K. Müller, and D.P. Reinhardt Interactions of fibrillin-1 with heparin/heparan sulfate, implications for microfibrillar assembly J. Biol. Chem. 276 2001 36035 36042
54. P. Whiteman, A.C. Willis, A. Warner, J. Brown, C. Redfield, and P.A. Handford Cellular and molecular studies of Marfan syndrome mutations identify co-operative protein folding in the cbEGF12-13 region of fibrillin-1 Hum. Mol. Genet. 16 2007 907 918
55. D.A. Yadin, I.B. Robertson, S.A. Jensen, P.A. Handford, and C. Redfield (1)H, (13)C and (15)N assignments of the four N-terminal domains of human fibrillin-1 Biomol. NMR Assign. 2012 10.1007/s12104-012-9456-0 Published online December 23, 2012
56. H. Yanagisawa, and E.C. Davis Unraveling the mechanism of elastic fiber assembly: The roles of short fibulins Int. J. Biochem. Cell Biol. 42 2010 1084 1093
57. X. Yuan, A.K. Downing, V. Knott, and P.A. Handford Solution structure of the transforming growth factor beta-binding protein-like module, a domain associated with matrix fibrils EMBO J. 16 1997 6659 6666
58. X. Yuan, J.M. Werner, J. Lack, V. Knott, P.A. Handford, I.D. Campbell, and A.K. Downing Effects of the N2144S mutation on backbone dynamics of a TB-cbEGF domain pair from human fibrillin-1 J. Mol. Biol. 316 2002 113 125