Control of growth factor networks by heparan sulfate proteoglycans

Annals of Biomedical Engineering

Volumn 36, Issue 12, 2008, Pages 2134-2148

  Forsten Williams, Kimberly ^a   Chu, Chia Lin ^b   Fannon, Michael ^c   Buczek Thomas, Jo Ann ^b   Nugent, Matthew A ^b,d  

^a State University   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d Boston University   (United States)

Author keywords

Binding; Epidermal growth factor; Fibroblast growth factor 2; Growth factor; Heparin; Heparin binding EGF like growth factor; Network; Receptors

Indexed keywords

BINDING ENERGY; BIOACTIVITY; BIOCHEMISTRY; CELL CULTURE; CELL GROWTH; COMPUTATIONAL METHODS; FIBROBLASTS; GLYCOPROTEINS; GROWTH KINETICS; HYSTERESIS MOTORS; PEPTIDES; POLYSACCHARIDES;

BINDING; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR-2; GROWTH FACTOR; HEPARIN; HEPARIN-BINDING-EGF-LIKE GROWTH FACTOR; NETWORK; RECEPTORS;

BINDING SITES;

ACID PHOSPHATASE; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR 2; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; HEPARIN-BINDING EGF-LIKE GROWTH FACTOR; PROTEOHEPARAN SULFATE; RADIOACTIVE IODINE; RECOMBINANT PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL; AORTA; ARTICLE; BIOLOGICAL MODEL; CATTLE; CELL COUNT; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; SMOOTH MUSCLE FIBER;

ACID PHOSPHATASE; ANIMALS; AORTA; CATTLE; CELL COUNT; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; IODINE RADIOISOTOPES; MODELS, BIOLOGICAL; MYOCYTES, SMOOTH MUSCLE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT PROTEINS;

EID: 56449095100     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-008-9575-z     Document Type: Article

References (41)

1. D. H. Atha J. C. Lormeau M. Petitou R. D. Rosenberg J. Choay 1987 Contribution of 3-O- and 6-O-sulfated glucosamine residues in the heparin-induced conformational change in antithrombin III Biochemistry 26 6454 6461 10.1021/bi00394a024
2. D. H. Atha A. W. Stephens R. D. Rosenberg 1984 Evaluation of critical groups required for the binding of heparin to antithrombin Proc. Natl. Acad. Sci. U.S.A. 81 1030 1034 10.1073/pnas.81.4.1030
3. E. M. Bublil Y. Yarden 2007 The EGF receptor family: spearheading a merger of signaling and therapeutics Curr. Opin. Cell Biol. 19 124 134 10.1016/j.ceb.2007.02.008
4. I. Capila R. J. Linhardt 2002 Heparin-protein interactions Angew Chem. Int. Ed. Engl. 41 391 412 10.1002/1521-3773(20020201)41:3<390::AID- ANIE390>3.0.CO;2-B
5. C. L. Chu J. A. Buczek-Thomas M. A. Nugent 2004 Heparan sulphate proteoglycans modulate fibroblast growth factor-2 binding through a lipid raft-mediated mechanism Biochem. J. 379 331 341 10.1042/BJ20031082
6. C. L. Chu A. L. Goerges M. A. Nugent 2005 Identification of common and specific growth factor binding sites in heparan sulfate proteoglycans Biochemistry 44 12203 12213 10.1021/bi050241p
7. C. C. Chua N. Rahimi K. Forsten-Williams M. A. Nugent 2004 Heparan sulfate proteoglycans function as receptors for fibroblast growth factor-2 activation of extracellular signal-regulated kinases 1 and 2 Circ. Res. 94 316 323 10.1161/01.RES.0000112965.70691.AC
8. D. T. Connolly M. B. Knight N. K. Harakas A. J. Wittwer J. Feder 1986 Determination of the number of endothelial cells in culture using an acid phosphatase assay Anal. Biochem. 152 136 140 10.1016/0003-2697(86)90131-4
9. Conrad H. E. 1998 Heparin-binding proteins. San Diego: Academic Press
10. J. D. Esko S. B. Selleck 2002 Order out of chaos: assembly of ligand binding sites in heparan sulfate Annu. Rev. Biochem. 71 435 471 10.1146/annurev.biochem.71.110601.135458
11. V. P. Eswarakumar I. Lax J. Schlessinger 2005 Cellular signaling by fibroblast growth factor receptors Cytokine Growth Factor Rev. 16 139 149 10.1016/j.cytogfr.2005.01.001
12. M. Fannon K. E. Forsten M. A. Nugent 2000 Potentiation and inhibition of bFGF binding by heparin: a model for regulation of cellular response Biochemistry 39 1434 1445 10.1021/bi991895z
13. W. J. Fantl D. E. Johnson L. T. Williams 1993 Signalling by receptor tyrosine kinases Annu. Rev. Biochem. 62 453 481
14. K. Forsten-Williams C. C. Chua M. A. Nugent 2005 The kinetics of FGF-2 binding to heparan sulfate proteoglycans and MAP kinase signaling J. Theor. Biol. 233 483 499 10.1016/j.jtbi.2004.10.020
15. J. T. Gallagher 2001 Heparan sulfate: growth control with a restricted sequence menu J. Clin. Invest. 108 357 361
16. M. Gavutis E. Jaks P. Lamken J. Piehler 2006 Determination of the two-dimensional interaction rate constants of a cytokine receptor complex Biophys. J. 90 3345 3355 10.1529/biophysj.105.072546
17. H. Gitay-Goren S. Soker I. Vlodavsky G. Neufeld 1992 The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules J. Biol. Chem. 267 6093 6098
18. A. L. Goerges M. A. Nugent 2003 Regulation of vascular endothelial growth factor binding and activity by extracellular pH J. Biol. Chem. 278 19518 19525 10.1074/jbc.M211208200
19. A. L. Goerges M. A. Nugent 2004 pH regulates vascular endothelial growth factor binding to fibronectin: a mechanism for control of extracellular matrix storage and release J. Biol. Chem. 279 2307 2315 10.1074/jbc.M308482200
20. M. Gopalakrishnan K. Forsten-Williams U. C. Tauber 2004 Ligand-induced coupling versus receptor pre-association: cellular automaton simulations of FGF-2 binding J. Theo. Biol. 227 239 251 10.1016/j.jtbi.2003.11.004
21. J. M. Haugh A. C. Huang H. S. Wiley A. Wells D. A. Lauffenburger 1999 Internalized epidermal growth factor receptors participate in the activation of p21(ras) in fibroblasts J. Biol. Chem. 274 34350 34360 10.1074/jbc.274.48.34350
22. B. S. Hendriks L. K. Opresko H. S. Wiley D. Lauffenburger 2003 Quantitative analysis of HER2-mediated effects on HER2 and epidermal growth factor receptor endocytosis: distribution of homo- and heterodimers depends on relative HER2 levels J. Biol. Chem. 278 23343 23351 10.1074/jbc.M300477200
23. S. Higashiyama J. A. Abraham M. Klagsbrun 1993 Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulfate J. Cell Biol. 122 933 940 10.1083/jcb.122.4.933
24. J. T. Jones R. W. Akita M. X. Sliwkowski 1999 Binding specificities and affinities of egf domains for ErbB receptors FEBS Let. 447 227 231 10.1016/S0014-5793(99)00283-5
25. J. Kreuger D. Spillmann J. P. Li U. Lindahl 2006 Interactions between heparan sulfate and proteins: the concept of specificity J. Cell Biol. 174 323 327 10.1083/jcb.200604035
26. M. A. Lemmon J. Schlessinger 1998 Transmembrane signaling by receptor oligomerization Methods Mol. Biol. 84 49 71
27. U. Lindahl G. Backstrom L. Thunberg I. G. Leder 1980 Evidence for a 3-O-sulfated d-glucosamine residue in the antithrombin-binding sequence of heparin Proc. Natl. Acad. Sci. U.S.A. 77 6551 6555 10.1073/pnas.77.11.6551
28. F. Mac Grabhann A. S. Popel 2007 Dimerization of VEGF receptors and implications for signal transduction: a computational study Biophys. Chem. 128 125 139
29. D. Moscatelli 1987 High and low affinity binding sites for basic fibroblast growth factor on cultured cells: absence of a role for low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells J. Cell. Physiol. 131 123 130 10.1002/jcp.1041310118
30. M. A. Nugent 2000 Heparin sequencing brings structure to the function of complex oligosaccharides Proc. Natl. Acad. Sci. U.S.A. 97 10301 10303 10.1073/pnas.97.19.10301
31. M. A. Nugent E. R. Edelman 1992 Kinetics of basic fibroblast growth factor binding to its receptor and heparan sulfate proteoglycan: a mechanism for cooperativity Biochemistry 31 8876 8883 10.1021/bi00152a026
32. Nugent, M.A., K. Forsten-Williams, M.J. Karnovsky, and E.R. Edelman. Mechanisms of cell growth regulation by heparin and heparan sulfate. In: Chemistry and Biology of Heparin and Heparan Sulfate, edited by H. G. Garg. Elsevier Ltd., 2005, pp. 533-570
33. R. Perona 2006 Cell signalling: growth factors and tyrosine kinase receptors Clin. Transl. Oncol. 8 77 82 10.1007/s12094-006-0162-1
34. G. Raab M. Klagsbrun 1997 Heparin-binding EGF-like growth factor Biochim. Biophys. Acta. 1333 F179 199
35. N. Shraga-Heled O. Kessler C. Prahst J. Kroll H. Augustin G. Neufeld 2007 Neuropilin-1 and neuropilin-2 enhance VEGF121 stimulated signal transduction by the VEGFR-2 receptor FASEB J. 211 915 926 10.1096/fj.06-6277com
36. G. V. Sperinde M. A. Nugent 1998 Heparan sulfate proteoglycans control bFGF processing in vascular smooth muscle cells Biochemistry 37 13153 13164 10.1021/bi980600z
37. G. V. Sperinde M. A. Nugent 2000 Mechanisms of FGF-2 intracellular processing: A kinetic analysis of the role of heparan sulfate proteoglycans Biochemistry 39 3788 3796 10.1021/bi992243d
38. E. Tkachenko J. M. Rhodes M. Simons 2005 Syndecans: new kids on the signaling block Circ. Rec. 96 488 500 10.1161/01.RES.0000159708.71142.c8
39. J. Turnbull A. Powell S. Guimond 2001 Heparan sulfate: decoding a dynamic multifunctional cell regulator Trends Cell Biol. 11 75 82 10.1016/S0962- 8924(00)01897-3
40. P. Wouters-Ballman I. Donnay N. Devleeschouwer J. Verstegen 1995 Iodination of mouse EGF with chloramine T at 4 degrees C: characterization of the iodinated peptide and comparison with other labelling methods J. Recept. Signal. Transduct. Res. 15 737 746 10.3109/10799899509079903
41. Y. Zhang J. Li C. Partovian F. W. Sellke M. Simons 2003 Syndecan-4 modulates basic fibroblast growth factor 2 signaling in vivo Am. J. Physiol. Heart Circ. Physiol. 284 H2078 H2082