Prediction of heparin binding sites in bone morphogenetic proteins (BMPs)

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 12, 2012, Pages 1374-1381

  Gandhi, Neha S ^a,b   Mancera, Ricardo L ^a,b  

^a CURTIN UNIVERSITY   (Australia)

^b CURTIN UNIVERSITY   (Australia)

Author keywords

Bone morphogenetic protein (BMP); Docking; Growth and differentiation factor (GDF); Heparin; Transforming growth factor (TGF )

Indexed keywords

ARGININE; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 14; BONE MORPHOGENETIC PROTEIN 2; DIMER; GLYCOSAMINOGLYCAN; GROWTH DIFFERENTIATION FACTOR; HEPARIN; HISTIDINE DERIVATIVE; LYSINE; OSTEOGENIC PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ACIDITY; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; BONE DEVELOPMENT; MOLECULAR DOCKING; NUCLEOTIDE SEQUENCE; PKA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; SIMULATION;

AMINO ACID SEQUENCE; BINDING SITES; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 7; BONE MORPHOGENETIC PROTEINS; GROWTH DIFFERENTIATION FACTOR 5; HEPARIN; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY;

EID: 84867677301     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.07.002     Document Type: Article

References (70)

1. A. Herpin, C. Lelong, and P. Favrel Transforming growth factor-β-related proteins: an ancestral and widespread superfamily of cytokines in metazoans Dev. Comp. Immunol. 28 2004 461 485 (Pubitemid 38177448)
2. J.M. Wozney Overview of bone morphogenetic proteins Spine (Phila Pa 1976) 27 2002 S2 S8
3. D. Chen, M. Zhao, and G.R. Mundy Bone morphogenetic proteins Growth Factors 22 2004 233 241 (Pubitemid 40136452)
4. P. Ducy, and G. Karsenty The family of bone morphogenetic proteins Kidney Int. 57 2000 2207 2214 (Pubitemid 30340719)
5. S.C. Chang, B. Hoang, J.T. Thomas, S. Vukicevic, F.P. Luyten, N.J. Ryba, C.A. Kozak, A.H. Reddi, and M. Moos Jr. Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development J. Biol. Chem. 269 1994 28227 28234
6. A. Mac Sweeney, S. Gil-Parrado, D. Vinzenz, A. Bernardi, A. Hein, U. Bodendorf, P. Erbel, C. Logel, and B. Gerhartz Structural basis for the substrate specificity of bone morphogenetic protein 1/Tolloid-like metalloproteases J. Mol. Biol. 384 2008 228 239
7. C.C. Rider, and B. Mulloy Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists Biochem. J. 429 2010 1 12
8. S.J. Lin, T.F. Lerch, R.W. Cook, T.S. Jardetzky, and T.K. Woodruff The structural basis of TGF-beta, bone morphogenetic protein, and activin ligand binding Reproduction 132 2006 179 190 (Pubitemid 44269702)
9. T. Takada, T. Katagiri, M. Ifuku, N. Morimura, M. Kobayashi, K. Hasegawa, A. Ogamo, and R. Kamijo Sulfated polysaccharides enhance the biological activities of bone morphogenetic proteins J. Biol. Chem. 278 2003 43229 43235 (Pubitemid 37345942)
10. M. Hazama, A. Aono, N. Ueno, and Y. Fujisawa Efficient expression of a heterodimer of bone morphogenetic protein subunits using a baculovirus expression system Biochem. Biophys. Res. Commun. 209 1995 859 866
11. D.I. Israel, J. Nove, K.M. Kerns, R.J. Kaufman, V. Rosen, K.A. Cox, and J.M. Wozney Heterodimeric bone morphogenetic proteins show enhanced activity in vitro and in vivo Growth Factors 13 1996 291 300 (Pubitemid 26378947)
12. W.-J. Kuo, M.A. Digman, and A.D. Lander Heparan sulfate acts as a bone morphogenetic protein coreceptor by facilitating ligand-induced receptor hetero-oligomerization Mol. Biol. Cell 21 2010 4028 4041
13. N.S. Gandhi, and R.L. Mancera The structure of glycosaminoglycans and their interactions with proteins Chem. Biol. Drug Des. 72 2008 455 482
14. J.M. Wozney, V. Rosen, A.J. Celeste, L.M. Mitsock, M.J. Whitters, R.W. Kriz, R.M. Hewick, and E.A. Wang Novel regulators of bone formation: molecular clones and activities Science 242 1988 1528 1534 (Pubitemid 19023695)
15. E.A. Wang, V. Rosen, J.S. D'Alessandro, M. Bauduy, P. Cordes, T. Harada, D.I. Israel, R.M. Hewick, K.M. Kerns, and P. LaPan Recombinant human bone morphogenetic protein induces bone formation Proc. Natl. Acad. Sci. U. S. A. 87 1990 2220 2224
16. S.E. Kim, S.-H. Song, Y.P. Yun, B.-J. Choi, I.K. Kwon, M.S. Bae, H.-J. Moon, and Y.-D. Kwon The effect of immobilization of heparin and bone morphogenic protein-2 (BMP-2) to titanium surfaces on inflammation and osteoblast function Biomaterials 32 2011 366 373
17. G.P. Allendorph, W.W. Vale, and S. Choe Structure of the ternary signaling complex of a TGF-beta superfamily member Proc. Natl. Acad. Sci. U. S. A. 103 2006 7643 7648
18. S. Keller, J. Nickel, J.L. Zhang, W. Sebald, and T.D. Mueller Molecular recognition of BMP-2 and BMP receptor IA Nat. Struct. Mol. Biol. 11 2004 481 488 (Pubitemid 38568954)
19. T. Kirsch, W. Sebald, and M.K. Dreyer Crystal structure of the BMP-2-BRIA ectodomain complex Nat. Struct. Biol. 7 2000 492 496 (Pubitemid 30414472)
20. J. Nickel, M.K. Dreyer, T. Kirsch, and W. Sebald The crystal structure of the BMP-2:BMPR-IA complex and the generation of BMP-2 antagonists J. Bone Joint Surg. Am. 83-A Suppl. 1 2001 S7 S14
21. R. Ruppert, E. Hoffmann, and W. Sebald Human bone morphogenetic protein 2 contains a heparin-binding site which modifies its biological activity Eur. J. Biochem. 237 1996 295 302 (Pubitemid 26110301)
22. A.J. Celeste, J.A. Iannazzi, R.C. Taylor, R.M. Hewick, V. Rosen, E.A. Wang, and J.M. Wozney Identification of transforming growth factor beta family members present in bone-inductive protein purified from bovine bone Proc. Natl. Acad. Sci. U. S. A. 87 1990 9843 9847 (Pubitemid 120016540)
23. W.K. Jones, E.A. Richmond, K. White, H. Sasak, W. Kusmik, J. Smart, H. Oppermann, D.C. Rueger, and R.F. Tucker Osteogenic protein-1 (OP-1) expression and processing in Chinese hamster ovary cells: isolation of a soluble complex containing the mature and pro-domains of OP-1 Growth Factors 11 1994 215 225
24. K.E. Gregory, R.N. Ono, N.L. Charbonneau, C.-L. Kuo, D.R. Keene, H.P. Bächinger, and L.Y. Sakai The prodomain of BMP-7 targets the BMP-7 complex to the extracellular matrix J. Biol. Chem. 280 2005 27970 27980 (Pubitemid 41076914)
25. A.P. White, A.R. Vaccaro, J.A. Hall, P.G. Whang, B.C. Friel, and M.D. McKee Clinical applications of BMP-7/OP-1 in fractures, nonunions and spinal fusion Int. Orthop. 31 2007 735 741 (Pubitemid 350160312)
26. K.A. Hruska, G. Guo, M. Wozniak, D. Martin, S. Miller, H. Liapis, K. Loveday, S. Klahr, T.K. Sampath, and J. Morrissey Osteogenic protein-1 prevents renal fibrogenesis associated with ureteral obstruction Am. J. Physiol. Renal Physiol. 279 2000 F130 F143
27. G. Luo, C. Hofmann, A.L. Bronckers, M. Sohocki, A. Bradley, and G. Karsenty BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning Genes Dev. 9 1995 2808 2820
28. D.L. Griffith, P.C. Keck, T.K. Sampath, D.C. Rueger, and W.D. Carlson Three-dimensional structure of recombinant human osteogenic protein 1: structural paradigm for the transforming growth factor beta superfamily Proc. Natl. Acad. Sci. U. S. A. 93 1996 878 883 (Pubitemid 26041187)
29. J. Greenwald, J. Groppe, P. Gray, E. Wiater, W. Kwiatkowski, W. Vale, and S. Choe The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly Mol. Cell 11 2003 605 617 (Pubitemid 36385117)
30. J. Groppe, J. Greenwald, E. Wiater, J. Rodriguez-Leon, A.N. Economides, W. Kwiatkowski, M. Affolter, W.W. Vale, J.C. Belmonte, and S. Choe Structural basis of BMP signalling inhibition by the cystine knot protein Noggin Nature 420 2002 636 642 (Pubitemid 36764490)
31. A. Irie, H. Habuchi, K. Kimata, and Y. Sanai Heparan sulfate is required for bone morphogenetic protein-7 signaling Biochem. Biophys. Res. Commun. 308 2003 858 865 (Pubitemid 36976539)
32. D. McClarence, An investigation into the location of the heparan sulphate/heparin-binding site of human bone morphogenetic protein-7, in: School of Biological Sciences, vol. Ph.D., University of London, Royal Holloway, 2011, pp. 209.
33. G. Hotten, H. Neidhardt, B. Jacobowsky, and J. Pohl Cloning and expression of recombinant human growth/differentiation factor 5 Biochem. Biophys. Res. Commun. 204 1994 646 652
34. L. Frank P Cartilage-derived morphogenetic protein-1 Int. J. Biochem. Cell Biol. 29 1997 1241 1244
35. P. Buxton, C. Edwards, C.W. Archer, and P. Francis-West Growth/differentiation factor-5 (GDF-5) and skeletal development J. Bone Surg. Am. 83-A Suppl. 1 2001 S23 S30
36. P.H. Francis-West, A. Abdelfattah, P. Chen, C. Allen, J. Parish, R. Ladher, S. Allen, S. MacPherson, F.P. Luyten, and C.W. Archer Mechanisms of GDF-5 action during skeletal development Development 126 1999 1305 1315 (Pubitemid 29182125)
37. P.H. Francis-West, J. Parish, K. Lee, and C.W. Archer BMP/GDF-signalling interactions during synovial joint development Cell Tissue Res. 296 1999 111 119 (Pubitemid 29179378)
38. A.M. Sullivan, and G.W. O'Keeffe The role of growth/differentiation factor 5 (GDF5) in the induction and survival of midbrain dopaminergic neurones: relevance to Parkinson's disease treatment J. Anat. 207 2005 219 226 (Pubitemid 41300997)
39. H. Schreuder, A. Liesum, J. Pohl, M. Kruse, and M. Koyama Crystal structure of recombinant human growth and differentiation factor 5: evidence for interaction of the type I and type II receptor-binding sites Biochem. Biophys. Res. Commun. 329 2005 1076 1086 (Pubitemid 40341385)
40. J. Nickel, A. Kotzsch, W. Sebald, and T.D. Mueller A single residue of GDF-5 defines binding specificity to BMP receptor IB J. Mol. Biol. 349 2005 933 947 (Pubitemid 40779617)
41. A. Kotzsch, J. Nickel, A. Seher, W. Sebald, and T.D. Muller Crystal structure analysis reveals a spring-loaded latch as molecular mechanism for GDF-5-type I receptor specificity EMBO J. 28 2009 937 947
42. B. Zhao, T. Katagiri, H. Toyoda, T. Takada, T. Yanai, T. Fukuda, U.-i. Chung, T. Koike, K. Takaoka, and R. Kamijo Heparin potentiates the in vivo ectopic bone formation induced by bone morphogenetic protein-2 J. Biol. Chem. 281 2006 23246 23253
43. N.S. Gandhi, and R.L. Mancera Heparin/heparan sulphate-based drugs Drug Discov. Today 15 2010 1058 1069
44. C. Berezin, F. Glaser, J. Rosenberg, I. Paz, T. Pupko, P. Fariselli, R. Casadio, and N. Ben-Tal ConSeq: the identification of functionally and structurally important residues in protein sequences Bioinformatics 20 2004 1322 1324 (Pubitemid 38807587)
45. J. Pei, B.-H. Kim, and N.V. Grishin PROMALS3D: a tool for multiple protein sequence and structure alignments Nucleic Acids Res. 36 2008 2295 2300 (Pubitemid 351567002)
46. C. Combet, C. Blanchet, C. Geourjon, and G. Deléage NPS@: network protein sequence analysis Trends Biochem. Sci. 25 2000 147 150 (Pubitemid 30122428)
47. J. Soding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 2005 W244 W248
48. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815 (Pubitemid 24007801)
49. W. Rocchia, E. Alexov, and B. Honig Extending the applicability of the nonlinear Poisson-Boltzmann equation: multiple dielectric constants and multivalent ions J. Phys. Chem. B 105 2001 6507 6514 (Pubitemid 35339019)
50. A. Roy, and Y. Zhang Recognizing Protein-Ligand Binding Sites by Global Structural Alignment and Local Geometry Refinement 2011 University of Michigan Ann Arbor, MI
51. D. Schneidman-Duhovny, Y. Inbar, V. Polak, M. Shatsky, I. Halperin, H. Benyamini, A. Barzilai, O. Dror, N. Haspel, R. Nussinov, and H.J. Wolfson Taking geometry to its edge: fast unbound rigid (and hinge-bent) docking Proteins 52 2003 107 112 (Pubitemid 36648858)
52. D. Schneidman-Duhovny, Y. Inbar, R. Nussinov, and H.J. Wolfson PatchDock and SymmDock: servers for rigid and symmetric docking Nucleic Acids Res. 33 2005 W363 W367
53. G.M. Morris, R. Huey, W. Lindstrom, M.F. Sanner, R.K. Belew, D.S. Goodsell, and A.J. Olson AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility J. Comput. Chem. 30 2009 2785 2791
54. B. Ohkawara, S.-i. Iemura, P. ten Dijke, and N. Ueno Action range of BMP is defined by its N-terminal basic amino acid core Curr. Biol. 12 2002 205 209 (Pubitemid 34122375)
55. N.S. Gandhi, and R.L. Mancera Molecular dynamics simulations of CXCL-8 and its interactions with a receptor peptide, heparin fragments, and sulfated linked cyclitols J. Chem. Inf. Model. 51 2011 335 358
56. N.S. Gandhi, C. Freeman, C.R. Parish, and R.L. Mancera Computational analyses of the catalytic and heparin-binding sites and their interactions with glycosaminoglycans in glycoside hydrolase family 79 endo-β-d-glucuronidase (heparanase) Glycobiology 22 2012 35 55
57. N.S. Gandhi, D.R. Coombe, and R.L. Mancera Platelet endothelial cell adhesion molecule 1 (PECAM-1) and its interactions with glycosaminoglycans: 1. Molecular modeling studies Biochemistry 47 2008 4851 4862 (Pubitemid 351574992)
58. B. Swencki-Underwood, J.K. Mills, J. Vennarini, K. Boakye, J. Luo, S. Pomerantz, M.R. Cunningham, F.X. Farrell, M.F. Naso, and B. Amegadzie Expression and characterization of a human BMP-7 variant with improved biochemical properties Protein Expr. Purif. 57 2008 312 319 (Pubitemid 350296967)
59. J.N. Cash, C.A. Rejon, A.C. McPherron, D.J. Bernard, and T.B. Thompson The structure of myostatin:follistatin 288: insights into receptor utilization and heparin binding EMBO J. 28 2009 2662 2676
60. D.S. Bramono, S. Murali, B. Rai, L. Ling, W.T. Poh, Z.X. Lim, G.S. Stein, V. Nurcombe, A.J. van Wijnen, and S.M. Cool Bone marrow-derived heparan sulfate potentiates the osteogenic activity of bone morphogenetic protein-2 (BMP-2) Bone 50 2012 954 964
61. J. Ratanavaraporn, and Y. Tabata Enhanced osteogenic activity of bone morphogenetic protein-2 by 2-O-desulfated heparin Acta Biomater. 8 2012 173 182
62. X. Jiao, P.C. Billings, M.P. O'Connell, F.S. Kaplan, E.M. Shore, and D.L. Glaser Heparan sulfate proteoglycans (HSPGs) modulate BMP2 osteogenic bioactivity in C2C12 cells J. Biol. Chem. 282 2007 1080 1086 (Pubitemid 47076568)
63. J.C. Gordon, J.B. Myers, T. Folta, V. Shoja, L.S. Heath, and A. Onufriev H++: a server for estimating pKas and adding missing hydrogens to macromolecules Nucleic Acids Res. 33 2005 W368 W371
64. M.H.M. Olsson, C.R. Sondergaard, M. Rostkowski, and J.H. Jensen PROPKA3: consistent treatment of internal and surface residues in empirical pKa predictions J Chem Theory Comput 7 2011 525 537
65. C. Mücksch, and H.M. Urbassek Adsorption of BMP-2 on a hydrophobic graphite surface: a molecular dynamics study Chem. Phys. Lett. 510 2011 252 256
66. X. Dong, Q. Wang, T. Wu, and H. Pan Understanding adsorption-desorption dynamics of BMP-2 on hydroxyapatite (001) surface Biophys. J. 93 2007 750 759 (Pubitemid 47219770)
67. A.F. Oliveira, S. Gemming, and G. Seifert Molecular dynamics simulations of BMP-2 adsorption on a hydrophobic surface. Molekulardynamische Simulation des BMP-2-adsorption auf einer hydrophoben Oberfläche Materialwiss Werkst 41 2010 1048 1053
68. H. Zhou, T. Wu, X. Dong, Q. Wang, and J. Shen Adsorption mechanism of BMP-7 on hydroxyapatite (001) surfaces Biochem. Biophys. Res. Commun. 361 2007 91 96 (Pubitemid 47102272)
69. T. Utesch, G. Daminelli, and M.A. Mroginski Molecular dynamics simulations of the adsorption of bone morphogenetic protein-2 on surfaces with medical relevance Langmuir 27 2011 13144 13153
70. A.F. Oliveira, S. Gemming, and G. Seifert Conformational analysis of aqueous BMP-2 using atomistic molecular dynamics simulations J. Phys. Chem. B 115 2010 1122 1130