Interactions of signaling proteins, growth factors and other proteins with heparan sulfate: Mechanisms and mysteries

Connective Tissue Research

Volumn 56, Issue 4, 2015, Pages 272-280

  Billings, Paul C ^a   Pacifici, Maurizio ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Extracellular matrix; heparan sulfate proteoglycans; heparan sulfate heparin binding domains; signaling and growth factor proteins

Indexed keywords

AMPHIREGULIN; ARGININE; FIBROBLAST GROWTH FACTOR; GROWTH FACTOR; HEPARAN SULFATE; HEPARANASE; LYSINE; PROTEOGLYCAN; SCLEROSTIN; SONIC HEDGEHOG PROTEIN; SIGNAL PEPTIDE;

EXTRACELLULAR MATRIX; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; REVIEW; ANIMAL; EXOSTOSES, MULTIPLE HEREDITARY; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PROCEDURES; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; TRANSLATIONAL RESEARCH;

ERINACEIDAE;

AMINO ACID MOTIFS; ANIMALS; EXOSTOSES, MULTIPLE HEREDITARY; HEPARITIN SULFATE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84937107228     PISSN: 03008207     EISSN: 16078438     Source Type: Journal    
DOI: 10.3109/03008207.2015.1045066     Document Type: Review

References (93)

1. Bishop JR, Schuksz M, Esko JD. Heparan sulphate proteoglycans fine-Tune mammalian physiology. Nature 2007;446:1030-7.
2. Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 2011;3:1-33.
3. Couchman JR, Pataki CA. An introduction to proteoglycans and their localization. J Histochem Cytochem 2012;60:885-97.
4. Huegel J, Sgariglia F, Enomoto-Iwamoto M, Koyama E, Dormans JP, Pacifici M. Heparan sulfate in skeletal development, growth, and pathology: the case of hereditary multiple exostoses. Dev Dyn 2013;242:1021-32.
5. Hammond E, Khurana A, Shridhar V, Dredge K. The role of heparanase and sulfatases in the modification of heparan sulfate proteoglycans within the tumor microenvironment and opportunities for novel cancer therapeutics. Front Oncol 2014;4:195.
6. Vlodavsky I, Iozzo RV, Sanderson RD. Heparanase: multiple functions in inflammation, diabetes and atherosclerosis. Matrix Biol 2013;32:220-2.
7. Uechi G, Sun Z, Schreiber EM, Halfter W, Balasubramani M. Proteomic view of basement membranes from human retinal blood vessels, inner limiting membranes, and lens capsules. J Proteome Res 2014;13:3693-705.
8. Bilandzic M, Stenvers KL. Betaglycan: a multifunctional accessory. Mol Cell Endocrinol 2011;339:180-9.
9. Couchman JR, Gopal S, Lim HC, Norgaard S, Multhaupt HAB. Syndecans: from peripheral coreceptors to mainstream regulators of cell behaviour. Int J Exp Pathol 2015;96:1-10.
10. Fears CY, Woods A. The role of syndecans in disease and wound healing. Matrix Biol 2006;25:443-56.
11. Choi Y, Chung H, Jung H, Couchman JR, Oh E-S. Syndecans as cell surface receptors: unique structure equates with functional diversity. Matrix Biol 2011;30:93-9.
12. Nasarre P, Gemmill RM, Drabkin HA. The emerging role of class-3 semaphorins and their neuropilin receptors in oncology. Onco Targets Ther 2014;7:1663-87.
13. Fransson L. Glypicans. Int J Biochem Cell Biol 2003;35:125-9.
14. Kolset SO, Pejler G. Serglycin: a structural and functional chameleon with wide impact on immune cells. J Immunol 2011; 187:4927-33.
15. Marneros AG, Olsen BR. Physiological role of collagen XVIII and endostatin. FASEB J 2005;19:716-28.
16. Farach-Carson MC, Warren CR, Harrington DA, Carson DD. Border patrol: insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol 2014; 34:64-79.
17. Edgell C-JS, BaSalamah MA, Marr HS. Testican-1: a differentially expressed proteoglycan with protease inhibiting activities. Int Rev Cytol 2004;236:101-22.
18. Ronnberg E, Pejler G. Serglycin: the master of the mast cell. Methods Mol Biol 2012;836:201-17.
19. Wernersson S, Pejler G. Mast cell secretory granules: armed for battle. Nat Rev Immunol 2014;14:478-94.
20. Couchman JR. Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 2010;26:89-114.
21. Ryan KE, Chiang C. Hedgehog secretion and signal transduction in vertebrates. J Biol Chem 2012;287:17905-13.
22. Cardin AD, Weintraub HJ. Molecular modeling of proteinglycosaminoglycan interactions. Arterioscler Thromb Vasc Biol 1989;9:21-32.
23. Hileman RE, Fromm JR, Weiler JM, Linhardt RJ. Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 1998;20: 156-67.
24. Beckner ME, Krutzsch HC, Stracke ML, Williams ST, Gallardo JA, Liotta LA. Identification of a new immunoglobulin superfamily protein expressed in blood vessels with a heparin-binding consensus sequence. Cancer Res 1995;55:2140-9.
25. Johnson GR, Wong L. Heparan sulfate is essential to amphiregulininduced mitogenic signaling by the epidermal growth factor receptor. J Biol Chem 1994;269:27149-54.
26. Fromm JR, Hileman RE, Caldwell EE, Weiler JM, Linhardt RJ. Pattern and spacing of basic amino acids in heparin binding sites. Arch Biochem Biophys 1997;343:92-100.
27. Tyler-Cross R, Sobel M, Marques D, Harris RB. Heparin binding domain peptides of antithrombin III: analysis by isothermal titration calorimetry and circular dichroism spectroscopy. Protein Sci 1994; 3:620-7.
28. Villanueva GB. Predictions of the secondary structure of antithrombin III and the location of the heparin-binding site. J Biol Chem 1984;259:2531-6.
29. Weisgraber KH, Rall SC. Human apolipoprotein B-100 heparinbinding sites. J Biol Chem 1987;262:11097-103.
30. Cardin AD, Hirose N, Blankenship DT, Jackson RL, Harmony JA, Sparrow DA, Sparrow JT. Binding of a high reactive heparin to human apolipoprotein E: identification of two heparin-binding domains. Biochem Biophys Res Commun 1986;134:783-9.
31. Wong P, Hampton B, Szylobryt E, Gallagher AM, Jaye M, Burgess WH. Analysis of putative heparin-binding domains of fibroblast growth factor-1. Using site-directed mutagenesis and peptide analogues. J Biol Chem 1995;270:25805-11.
32. Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K. Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem 2004;279:12346-54.
33. Ye S, Luo Y, Lu W, Jones RB, Linhardt RJ, Capila I, Toida T, Kan M, Pelletier H, McKeehan WL. Structural basis for interaction of FGF-1, FGF-2, and FGF-7 with different heparan sulfate motifs. Biochemistry 2001;40:14429-39.
34. Bellosta P, Iwahori A, Plotnikov AN, Eliseenkova AV, Basilico C, Mohammadi M. Identification of receptor and heparin binding sites in fibroblast growth factor 4 by structure-based mutagenesis. Mol Cell Biol 2001;21:5946-57.
35. Barkalow FJ, Schwarzbauer JE. Localization of the major heparinbinding site in fibronectin. J Biol Chem 1991;266:7812-18.
36. McCarthy JB, Skubitz AP, Qi Z, Yi XY, Mickelson DJ, Klein DJ, Furcht LT. RGD-independent cell adhesion to the carboxy-Terminal heparin-binding fragment of fibronectin involves heparin-dependent and-independent activities. J Cell Biol 1990;110:777-87.
37. Haugen PK, McCarthy JB, Skubitz AP, Furcht LT, Letourneau PC. Recognition of the A chain carboxy-Terminal heparin binding region of fibronectin involves multiple sites: two contiguous sequences act independently to promote neural cell adhesion. J Cell Biol 1990;111:2733-45.
38. Zhou H, Mazzulla MJ, Kaufman JD, Stahl SJ, Wingfield PT, Rubin JS, Bottaro DP, Byrd RA. The solution structure of the N-Terminal domain of hepatocyte growth factor reveals a potential heparin-binding site. Structure 1998;6:109-16.
39. Thompson SA, Higashiyama S, Wood K, Pollitt NS, Damm D, McEnroe G, Garrick B, Ashton N, Lau K, Hancock N, Klagsbrun M, Abraham JA. Characterization of sequences within heparin-binding EGF-like growth factor that mediate interaction with heparin. J Biol Chem 1994;269:2541-9.
40. Levy-Adam F, Abboud-Jarrous G, Guerrini M, Beccati D, Vlodavsky I, Ilan N. Identification and characterization of heparin/heparan sulfate binding domains of the endoglycosidase heparanase. J Biol Chem 2005;280:20457-66.
41. Saesen E, Sarrazin S, Laguri C, Sadir R, Maurin D, Thomas A, Imberty A, Lortat-Jacob H. Insights into the mechanism by which interferon-g basic amino acid clusters mediate protein binding to heparan sulfate. J Am Chem Soc 2013;135:9384-90.
42. Fowlkes JL, Thrailkill KM, George-Nascimento C, Rosenberg CK, Serra DM. Heparin-binding, highly basic regions within the thyroglobulin type-1 repeat of insulin-like growth factor (IGF)-binding proteins (IGFBPs)-3,-5, and-6 inhibit IGFBP-4 degradation. Endocrinology 1997;138:2280-5.
43. Arai T, Parker A, Busby W, Clemmons DR. Heparin, heparan sulfate, and dermatan sulfate regulate formation of the insulin-like growth factor-I and insulin-like growth factor-binding protein complexes. J Biol Chem 1994;269:20388-93.
44. Salek-Ardakani S, Arrand JR, Shaw D, Mackett M. Heparin and heparan sulfate bind interleukin-10 and modulate its activity. Blood 2000;96:1879-88.
45. Charonis AS, Skubitz AP, Koliakos GG, Reger LA, Dege J, Vogel AM, Wohlhueter R, Furcht LT. A novel synthetic peptide from the B1 chain of laminin with heparin-binding and cell adhesionpromoting activities. J Cell Biol 1988;107:1253-60.
46. Kouzi-Koliakos K, Koliakos GG, Tsilibary EC, Furcht LT, Charonis AS. Mapping of three major heparin-binding sites on laminin and identification of a novel heparin-binding site on the B1 chain. J Biol Chem 1989;264:17971-8.
47. Hata A, Ridinger DN, Sutherland S, Emi M, Shuhua Z, Myers RL, Ren K, Cheng T, Inoue I, Wilson DE, Iveriusli PH, Lalouel JM. Binding of lipoprotein lipase to heparin. Identification of five critical residues in two distinct segments of the amino-Terminal domain. J Biol Chem 1993;268:8447-57.
48. Kallapur SG, Akeson RA. The neural cell adhesion molecule (NCAM) heparin binding domain binds to cell surface heparan sulfate proteoglycans. J Neurosci Res 1992;33:538-48.
49. Khachigian LM, Owensby DA, Chesterman CN. A tyrosinated peptide representing the alternatively spliced exon of the plateletderived growth factor A-chain binds specifically to cultured cells and interferes with binding of several growth factors. J Biol Chem 1992;267:1660-6.
50. Jin C, Ekwall AK, Bylund J, Bjorkman L, Estrella RP, Whitelock JM, Eisler T, Bokarewa M, Karlsson NG. Human synovial lubricin expresses sialyl Lewis-determinant and has L-selectin ligand activity. J Biol Chem 2012;287: 35922-33.
51. Shirk RA, Elisen MG, Meijers JC, Church FC. Role of the H helix in heparin binding to protein C inhibitor. J Biol Chem 1994;269: 28690-5.
52. Veverka V, Henry AJ, Slocombe PM, Ventom A, Mulloy B, Muskett FW, Muzylak M, Greenslade K, Moore A, Zhang L, Gong J, Qian X, Paszty C, Taylor RJ, Robinson MK, Carr MD. Characterization of the structural features and interactions of sclerostin: molecular insight into a key regulator of Wnt-mediated bone formation. J Biol Chem 2009;284:10890-900.
53. Verrecchio A, Germann MW, Schick BP, Kung B, Twardowski T, San Antonio JD. Design of peptides with high affinities for heparin and endothelial cell proteoglycans. J Biol Chem 2000;275: 7701-7.
54. Chang S-C, Mulloy B, Magee AI, Couchman JR. Two distinct sites in sonic Hedgehog combine for heparan sulfate interactions and cell signaling functions. J Biol Chem 2011;286:44391-402.
55. Whalen DM, Malinauskas T, Gilbert RJC, Siebold C. Structural insights into proteoglycan-shaped Hedgehog signaling. Proc Natl Acad Sci USA 2013;110:16420-5.
56. Sandstrom J, Carlsson L, Marklund SL, Edlund T. The heparinbinding domain of extracellular superoxide dismutase C and formation of variants with reduced heparin affinity. J Biol Chem 1992;267:18205-9.
57. Frese M-A, Milz F, Dick M, Lamanna WC, Dierks T. Characterization of the human sulfatase Sulf1 and its high affinity heparin/heparan sulfate interaction domain. J Biol Chem 2009;284: 28033-44.
58. Enjyoji K, Miyata T, Kamikubo Y, Kato H. Effect of heparin on the inhibition of factor Xa by tissue factor pathway inhibitor: a segment, Gly212-Phe243, of the third Kunitz domain is a heparinbinding site. Biochemistry 1995;34:5725-35.
59. McCaffrey TA, Falcone DJ, Du B. Transforming growth factor-beta 1 is a heparin-binding protein: identification of putative heparinbinding regions and isolation of heparins with varying affinity for TGF-beta 1. J Cell Physiol 1992;152:430-40.
60. Murphy-Ullrich JE, Gurusiddappa S, Frazier WA, Hook M. Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity. J Biol Chem 1993;268: 26784-9.
61. Fairbrother WJ, Champe MA, Christinger HW, Keyt BA, Starovasnik MA. Solution structure of the heparin-binding domain of vascular endothelial growth factor. Structure 1998;6: 637-48.
62. De Boer HC, Preissner KT, Bouma BN, de Groot PG. Binding of vitronectin-Thrombin-Antithrombin III complex to human endothelial cells is mediated by the heparin binding site of vitronectin. J Biol Chem 1992;267:2264-8.
63. Sobel M, Solern DF, Kerrnodes C, Harrisn B. Localization and characterization of a heparin binding domain peptide of human von Willebrand factor. J Biol Chem 1992;267:8857-62.
64. Fukushima T, Adachi T, Hirano K. The heparinbinding site of human xanthine oxidase. Biol Pharm Bull 1995; 18:156-8.
65. Beenken A, Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov 2009;8:235-53.
66. Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 2010;10:116-29.
67. Sterner E, Masuko S, Li G, Li L, Green DE, Otto NJ, Xu Y, DeAngelis PL, Liu J, Dordick JS, Linhardt RJ. Fibroblast growth factor-based signaling through synthetic heparan sulfate blocks copolymers studied using high cell density three-dimensional cell printing. J Biol Chem 2014;289:9754-65.
68. Luo Y, Lu W, Mohamedali KA, Jang JH, Jones RB, Gabriel JL, Kan M, McKeehan WL. The glycine box: a determinant of specificity for fibroblast growth factor. Biochemistry 1998;37: 16506-15.
69. Chiodelli P, Mitola S, Ravelli C, Oreste P, Rusnati M, Presta M. Heparan sulfate proteoglycans mediate the angiogenic activity of the vascular endothelial growth factor receptor-2 agonist gremlin. Arterioscler Thromb Vasc Biol 2011;31:e116-27.
70. Seidel C, Sundan A, Hjorth M, Turesson I, Dahl IM, Abildgaard N, Waage A, Borset M. Serum syndecan-1: a new independent prognostic marker in multiple myeloma. Blood 2000;95:388-92.
71. Khotskaya YB, Dai Y, Ritchie JP, MacLeod V, Yang Y, Zinn K, Sanderson RD. Syndecan-1 is required for robust growth, vascularization, and metastasis of myeloma tumors in vivo. J Biol Chem 2009;284:26085-95.
72. Larkin J, Ahmed CM, Wilson TD, Johnson HM. Regulation of interferon gamma signaling by suppressors of cytokine signaling and regulatory T cells. Front Immunol 2013;4:469.1-469.8.
73. Burglin TR. The Hedgehog protein family. Genome Biol 2008;9: 241.1-241.9.
74. Chan JA, Balasubramanian S, Witt RM, Nazemi KJ, Choi Y, Pazyra-Murphy MF, Walsh CO, Thompson M, Segal RA. Proteoglycan interactions with Sonic Hedgehog specify mitogenic responses. Nat Neurosci 2009;12:409-17.
75. Pathi S, Pagan-Westphal S, Baker DP, Garber EA, Rayhorn P, Bumcrot D, Tabin CJ, Blake Pepinsky R, Williams KP. Comparative biological responses to human Sonic, Indian, and Desert hedgehog. Mech Dev 2001;106:107-17.
76. Beachy PA, Hymowitz SG, Lazarus RA, Leahy DJ, Siebold C. Interactions between Hedgehog proteins and their binding partners come into view. Genes Dev 2010;24:2001-12.
77. Jochmann K, Bachvarova V, Vortkamp A. Heparan sulfate as a regulator of endochondral ossification and osteochondroma development. Matrix Biol 2014;34:55-63.
78. Koyama E, Young B, Nagayama M, Shibukawa Y, Enomoto-Iwamoto M, Iwamoto M, Maeda Y, Lanske B, Song B, Serra R, Pacifici M. Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 2007;134:2159-69.
79. Koziel L, Kunath M, Kelly OG, Vortkamp A. Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev Cell 2004;6:801-13.
80. Okoniewska M, Tanaka T, Yada RY. The pepsin residue glycine-76 contributes to active-site loop flexibility and participates in catalysis. Biochem J 2000;349:169-77.
81. Morgan AA, Rubenstein E. Proline: the distribution, frequency, positioning, and common functional roles of proline and polyproline sequences in the human proteome. PLoS One 2013;8:e53785.
82. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 2008;9:40.
83. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 2010;5:725-38.
84. Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y. The I-TASSER Suite: protein structure and function prediction. Nat Methods 2014; 12:7-8.
85. Hayano S, Kurosaka H, Yanagita T, Kalus I, Milz F, Ishihara Y, Islam MN, Kawanabe N, Saito M, Kamioka H, Adachi T, Dierks T, Yamashiro T. Roles of heparan sulfate sulfation in dentinogenesis. J Biol Chem 2012;287:12217-29.
86. Milz F, Harder A, Neuhaus P, Breitkreuz-Korff O, Walhorn V, Lubke T, Anselmetti D, Dierks T. Cooperation of binding sites at the hydrophilic domain of cell-surface sulfatase Sulf1 allows for dynamic interaction of the enzyme with its substrate heparan sulfate. Biochim Biophys Acta 2013;1830:5287-98.
87. Ng A, Wong M, Viviano B, Erlich JM, Alba G, Pflederer C, Jay PY, Saunders S. Loss of glypican-3 function causes growth factordependent defects in cardiac and coronary vascular development. Dev Biol 2009;335:208-15.
88. Tenorio J, Arias P, Martýnez-Glez V, Santos F, Garcýa-Minaur S, Nevado J, Lapunzina P. Simpson-Golabi-Behmel syndrome types I and II. Orphanet J Rare Dis 2014;9:138.1-138.8.
89. Iozzo RV, Sanderson RD. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J Cell Mol Med 2011;15: 1013-31.
90. Jones KB, Pacifici M, Hilton MJ. Multiple hereditary exostoses (MHE): elucidating the pathogenesis of a rare skeletal disorder through interdisciplinary research. Connect Tissue Res 2014;55: 80-8.
91. Anower-E-Khuda MF, Matsumoto K, Habuchi H, Morita H, Yokochi T, Shimizu K, Kimata K. Glycosaminoglycans in the blood of hereditary multiple exostoses patients: half reduction of heparan sulfate to chondroitin sulfate ratio and the possible diagnostic application. Glycobiology 2013;23:865-76.
92. Sgariglia F, Candela ME, Huegel J, Jacenko O, Koyama E, Yamaguchi Y, Pacifici M, Enomoto-Iwamoto M. Epiphyseal abnormalities, trabecular bone loss and articular chondrocyte hypertrophy develop in the long bones of postnatal Ext1-deficient mice. Bone 2013;57:220-31.
93. Zak BM, Schuksz M, Koyama E, Mundy C, Wells DE, YamaguchiY, Pacifici M, Esko JD. Compound heterozygous loss of Ext1 and Ext2 is sufficient for formation of multiple exostoses in mouse ribs and long bones. Bone 2011;48:979-87.