Heparan sulfate proteoglycans mediate the angiogenic activity of the vascular endothelial growth factor receptor-2 agonist gremlin

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 12, 2011, Pages

  Chiodelli, Paola ^a   Mitola, Stefania ^a   Ravelli, Cosetta ^a   Oreste, Pasqua ^b   Rusnati, Marco ^a   Presta, Marco ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b Glycores 2000   (Italy)

Author keywords

angiogenesis; endothelium; gremlin; heparan sufate proteoglycans

Indexed keywords

GREMLIN; HEPARIN; HEPARIN LYASE; MITOGEN ACTIVATED PROTEIN KINASE; POLYSACCHARIDE; PROTEOHEPARAN SULFATE; SODIUM CHLORATE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN INHIBITOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; AUTOPHOSPHORYLATION; CELL MOTILITY; CHICK EMBRYO; DRUG BINDING; EMBRYO; ENDOTHELIUM CELL; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; UMBILICAL ARTERY; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BACTERIAL CAPSULES; CATTLE; CELL LINE; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROPILIN-1; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 81755180517     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.235184     Document Type: Article

References (58)

1. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249-257.
2. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242-248.
3. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999;13:9-22. (Pubitemid 29038270)
4. Grunewald FS, Prota AE, Giese A, Ballmer-Hofer K. Structure-function analysis of VEGF receptor activation and the role of coreceptors in angiogenic signaling. Biochim Biophys Acta. 2010;1804:567-580.
5. Krilleke D, DeErkenez A, Schubert W, Giri I, Robinson GS, Ng YS, Shima DT. Molecular mapping and functional characterization of the VEGF164 heparin-binding domain. J Biol Chem. 2007;282: 28045-28056. (Pubitemid 47533565)
6. Lindahl U. Heparan sulfate-protein interactions: a concept for drug design? Thromb Haemost. 2007;98:109-115. (Pubitemid 47074185)
7. Iozzo RV, San Antonio JD. Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J Clin Invest. 2001;108:349-355. (Pubitemid 32730778)
8. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem. 1992;267:26031-26037. (Pubitemid 23014012)
9. Kawamura H, Li X, Goishi K, Van Meeteren LA, Jakobsson L, Cebe-Suarez S, Shimizu A, Edholm D, Ballmer-Hofer K, Kjellen L, Klagsbrun M, Claesson-Welsh L. Neuropilin-1 in regulation of VEGF-induced activation of p38MAPK and endothelial cell organization. Blood. 2008;112: 3638-3649.
10. Robinson CJ, Mulloy B, Gallagher JT, Stringer SE. VEGF165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by K5 lyase. J Biol Chem. 2006;281:1731-1740.
11. Maccarana M, Casu B, Lindahl U. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J Biol Chem. 1994;269:3903-3903.
12. Guimond S, Maccarana M, Olwin BB, Lindahl U, Rapraeger AC. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J Biol Chem. 1993;268: 23906-23914. (Pubitemid 23335365)
13. Rusnati M, Urbinati C. Polysulfated/sulfonated compounds for the development of drugs at the crossroad of viral infection and oncogenesis. Curr Pharm Des. 2009;15:2946-2957.
14. Presta M, Leali D, Stabile H, Ronca R, Camozzi M, Coco L, Moroni E, Liekens S, Rusnati M. Heparin derivatives as angiogenesis inhibitors. Curr Pharm Des. 2003;9:553-566. (Pubitemid 36221723)
15. Presta M, Oreste P, Zoppetti G, Belleri M, Tanghetti E, Leali D, Urbinati C, Bugatti A, Ronca R, Nicoli S, Moroni E, Stabile H, Camozzi M, Hernandez GA, Mitola S, Dell'Era P, Rusnati M, Ribatti D. Antiangiogenic activity of semisynthetic biotechnological heparins: lowmolecular-weight-sulfated Escherichia coli K5 polysaccharide derivatives as fibroblast growth factor antagonists. Arterioscler Thromb Vasc Biol. 2005;25:71-76. (Pubitemid 40054256)
16. Rusnati M, Oreste P, Zoppetti G, Presta M. Biotechnological engineering of heparin/heparan sulphate: a novel area of multi-target drug discovery. Curr Pharm Des. 2005;11:2489-2499. (Pubitemid 40872693)
17. Pearce JJ, Penny G, Rossant J. A mouse cerberus/Dan-related gene family. Dev Biol. 1999;209:98-110. (Pubitemid 29194316)
18. Vitt UA, Hsu SY, Hsueh AJ. Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol Endocrinol. 2001;15:681-694. (Pubitemid 32411309)
19. Balemans W, Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol. 2002;250:231-250. (Pubitemid 35216412)
20. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM. Gremlin is the bmp antagonist required for maintenance of SHH and FGF signals during limb patterning. Nat Genet. 2003;34:303-307. (Pubitemid 36792863)
21. Lu MM, Yang H, Zhang L, Shu W, Blair DG, Morrisey EE. The bone morphogenic protein antagonist gremlin regulates proximal-distal patterning of the lung. Dev Dyn. 2001;222:667-680. (Pubitemid 33136337)
22. Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A. Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development. 2004;131:3401-3410. (Pubitemid 39139886)
23. Costello CM, Cahill E, Martin F, Gaine S, McLoughlin P. Role of gremlin in the lung: development and disease. Am J Respir Cell Mol Biol;42: 517-523.
24. Lappin DW, McMahon R, Murphy M, Brady HR. Gremlin: an example of the re-emergence of developmental programmes in diabetic nephropathy. Nephrol Dial Transplant. 2002;17(suppl 9):65-67.
25. Namkoong H, Shin SM, Kim HK, Ha SA, Cho GW, Hur SY, Kim TE, Kim JW. The bone morphogenetic protein antagonist gremlin 1 is overexpressed in human cancers and interacts with YWHAH protein. BMC Cancer. 2006;6:74.
26. Sneddon JB, Zhen HH, Montgomery K, Van de Rijn M, Tward AD, West R, Gladstone H, Chang HY, Morganroth GS, Oro AE, Brown PO. Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation. Proc Natl Acad Sci USA. 2006;103:14842-14847. (Pubitemid 44527816)
27. Stabile H, Mitola S, Moroni E, Belleri M, Nicoli S, Coltrini D, Peri F, Pessi A, Orsatti L, Talamo F, Castronovo V, Waltregny D, Cotelli F, Ribatti D, Presta M. Bone morphogenic protein antagonist Drm/gremlin is a novel proangiogenic factor. Blood. 2007;109:1834-1840. (Pubitemid 46348177)
28. Mitola S, Moroni E, Ravelli C, Andres G, Belleri M, Presta M. Angiopoietin-1 mediates the pro-angiogenic activity of the bone morphogenic protein antagonist Drm. Blood. 2008;112:1154-1157.
29. Mitola S, Ravelli C, Moroni E, Salvi V, Leali D, Ballmer-Hofer K, Zammataro L, Presta M. Gremlin is a novel agonist of the major proangiogenic receptor VEGFR2. Blood. 2010;116:3677-3680.
30. Topol LZ, Bardot B, Zhang Q, Resau J, Huillard E, Marx M, Calothy G, Blair DG. Biosynthesis, post-translation modification, and functional characterization of Drm/gremlin. J Biol Chem. 2000;275:8785-8793. (Pubitemid 30180233)
31. 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: 10890-10900.
32. Rider CC, Mulloy B. Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists. Biochem J. 2010;429:1-12.
33. Leali D, Belleri M, Urbinati C, Coltrini D, Oreste P, Zoppetti G, Ribatti D, Rusnati M, Presta M. Fibroblast growth factor-2 antagonist activity and angiostatic capacity of sulfated Escherichia coli K5 polysaccharide derivatives. J Biol Chem. 2001;276:37900-37908.
34. Rusnati M, Coltrini D, Oreste P, Zoppetti G, Albini A, Noonan D, d'Adda di Fagagna F, Giacca M, Presta M. Interaction of HIV-1 Tat protein with heparin: role of the backbone structure, sulfation, and size. J Biol Chem. 1997;272:11313-11320. (Pubitemid 27184133)
35. Zhang Z, Coomans C, David G. Membrane heparan sulfate proteoglycansupported FGF2-FGFR1 signaling: evidence in support of the "cooperative end structures" model. J Biol Chem. 2001;276:41921-41929.
36. Rusnati M, Urbinati C, Caputo A, Possati L, Lortat-Jacob H, Giacca M, Ribatti D, Presta M. Pentosan polysulfate as an inhibitor of extracellular HIV-1 Tat. J Biol Chem. 2001;276:22420-22425.
37. Grinspan JB, Mueller SN, Levine EM. Bovine endothelial cells transformed in vitro by benzo(a)pyrene. J Cell Physiol. 1983;114:328-338. (Pubitemid 13161554)
38. Esko JD. Genetic analysis of proteoglycan structure, function and metabolism. Curr Opin Cell Biol. 1991;3:805-816. (Pubitemid 121006137)
39. Safaiyan F, Kolset SO, Prydz K, Gottfridsson E, Lindahl U, Salmivirta M. Selective effects of sodium chlorate treatment on the sulfation of heparan sulfate. J Biol Chem. 1999;274:36267-36273.
40. De Palma M, Naldini L. Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol. 2002;346: 514-529. (Pubitemid 41103156)
41. Rusnati M, Urbinati C, Presta M. Internalization of basic fibroblast growth factor (bFGF) in cultured endothelial cells: role of the low affinity heparin-like bFGF receptors. J Cell Physiol. 1993;154:152-161. (Pubitemid 23024006)
42. Margosio B, Marchetti D, Vergani V, Giavazzi R, Rusnati M, Presta M, Taraboletti G. Thrombospondin 1 as a scavenger for matrix-associated fibroblast growth factor 2. Blood. 2003;102:4399-4406. (Pubitemid 37494101)
43. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J. 2008;50:346-363.
44. Mousa SA, Petersen LJ. Anti-cancer properties of low-molecular-weight heparin: preclinical evidence. Thromb Haemost. 2009;102:258-267.
45. Rostand KS, Esko JD. Microbial adherence to and invasion through proteoglycans. Infect Immun. 1997;65:1-8. (Pubitemid 27008896)
46. Gitay-Goren H, Soker S, Vlodavsky I, Neufeld G. The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J Biol Chem. 1992;267: 6093-6098.
47. Cohen T, Gitay-Goren H, Sharon R, Shibuya M, Halaban R, Levi BZ, Neufeld G. VEGF121, a vascular endothelial growth factor (VEGF) isoform lacking heparin binding ability, requires cell-surface heparan sulfates for efficient binding to the VEGF receptors of human melanoma cells. J Biol Chem. 1995;270:11322-11326.
48. Casu B, Grazioli G, Razi N, Guerrini M, Naggi A, Torri G, Oreste P, Tursi F, Zoppetti G, Lindahl U. Heparin-like compounds prepared by chemical modification of capsular polysaccharide from E. coli K5. Carbohydr Res. 1994;263:271-284. (Pubitemid 24320402)
49. Esko JD, Lindahl U. Molecular diversity of heparan sulfate. J Clin Invest. 2001;108:169-173. (Pubitemid 32656238)
50. Ono K, Hattori H, Takeshita S, Kurita A, Ishihara M. Structural features in heparin that interact with VEGF165 and modulate its biological activity. Glycobiology. 1999;9:705-711. (Pubitemid 29329014)
51. Pellet-Many C, Frankel P, Jia H, Zachary I. Neuropilins: structure, function and role in disease. Biochem J. 2008;411:211-226. (Pubitemid 351580173)
52. Shintani Y, Takashima S, Asano Y, Kato H, Liao Y, Yamazaki S, Tsukamoto O, Seguchi O, Yamamoto H, Fukushima T, Sugahara K, Kitakaze M, Hori M. Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling. EMBO J. 2006;25:3045-3055. (Pubitemid 44106757)
53. Geretti E, Klagsbrun M. Neuropilins: novel targets for anti-angiogenesis therapies. Cell Adh Migr. 2007;1:56-61.
54. Lee TH, Seng S, Li H, Kennel SJ, Avraham HK, Avraham S. Integrin regulation by vascular endothelial growth factor in human brain microvascular endothelial cells: role oF2641 integrin in angiogenesis. J Biol Chem. 2006;281:40450-40460. (Pubitemid 46041848)
55. Rusnati M, Vicenzi E, Donalisio M, Oreste P, Landolfo S, Lembo D. Sulfated K5 Escherichia coli polysaccharide derivatives: a novel class of candidate antiviral microbicides. Pharmacol Ther. 2009;123:310-322.
56. Goodwin AM, D'Amore PA. Wnt signaling in the vasculature. Angiogenesis. 2002;5:1-9. (Pubitemid 36076918)
57. Poggi A, Rossi C, Casella N, Bruno C, Sturiale L, Dossi C, Naggi A. Inhibition of b16-bl6 melanoma lung colonies by semisynthetic sulfaminoheparosan sulfates from E. coli K5 polysaccharide. Semin Thromb Hemost. 2002;28:383-392.
58. Boers W, Aarrass S, Linthorst C, Pinzani M, Elferink RO, Bosma P. Transcriptional profiling reveals novel markers of liver fibrogenesis: gremlin and insulin-like growth factor-binding proteins. J Biol Chem. 2006;281:16289-16295.