Long pentraxin 3/tumor necrosis factor-stimulated gene-6 interaction a biological rheostat for fibroblast growth factor 2-mediated angiogenesis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 3, 2012, Pages 696-703

  Leali, Daria ^a   Inforzato, Antonio ^c,e   Ronca, Roberto ^a   Bianchi, Roberta ^a   Belleri, Mirella ^a   Coltrini, Daniela ^b   Di Salle, Emanuela ^a   Sironi, Marina ^c   Norata, Giuseppe Danilo ^d   Bottazzi, Barbara ^c   Garlanda, Cecilia ^c   Day, Anthony J ^e   Presta, Marco ^a  

^a Unit of General Pathology and Immunology   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico)   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

angiogenesis; endothelium; FGF2; pentraxin; TSG 6

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; MATRIGEL; PENTRAXIN 3; PROTEOHEPARAN SULFATE;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING ASSAY; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SOLID PHASE BINDING ASSAY; SURFACE PLASMON RESONANCE; VASCULARIZATION;

ANIMALS; BINDING, COMPETITIVE; C-REACTIVE PROTEIN; CATTLE; CELL ADHESION MOLECULES; CHICK EMBRYO; CHO CELLS; CRICETINAE; CRICETULUS; FEMALE; FIBROBLAST GROWTH FACTOR 2; HEK293 CELLS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RECOMBINANT PROTEINS; SERUM AMYLOID P-COMPONENT; SURFACE PLASMON RESONANCE; TRANSFECTION;

EID: 84857658490     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.243998     Document Type: Article

References (56)

1. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249-257.
2. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86:353-364. (Pubitemid 26272076)
3. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1:27-31.
4. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005;16:159-178. (Pubitemid 40616114)
5. Klint P, Claesson-Welsh L. Signal transduction by fibroblast growth factor receptors. Front Biosci. 1999;4:D165-D177.
6. Schlessinger J, Lax I, Lemmon M. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell. 1995;83:357-360.
7. Rusnati M, Presta M. Interaction of angiogenic basic fibroblast growth factor with endothelial cell heparan sulfate proteoglycans: biological implications in neovascularization. Int J Clin Lab Res. 1996;26:15-23.
8. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell. 2000;6:743-750.
9. Rusnati M, Presta M. Extracellular angiogenic growth factor interactions: an angiogenesis interactome survey. Endothelium. 2006;13:93-111. (Pubitemid 44173111)
10. Breviario F, d'Aniello EM, Golay J, Peri G, Bottazzi B, Bairoch A, Saccone S, Marzella R, Predazzi V, Rocchi M, et al. Interleukin-1-inducible genes in endothelial cells. Cloning of a new gene related to C-reactive protein and serum amyloid P component. J Biol Chem. 1992; 267:22190-22197.
11. Mantovani A, Garlanda C, Bottazzi B. Pentraxin 3, a non-redundant soluble pattern recognition receptor involved in innate immunity. Vaccine. 2003;21(suppl 2):S43-S47. (Pubitemid 36588649)
12. Inforzato A, Rivieccio V, Morreale AP, Bastone A, Salustri A, Scarchilli L, Verdoliva A, Vincenti S, Gallo G, Chiapparino C, Pacello L, Nucera E, Serlupi-Crescenzi O, Day AJ, Bottazzi B, Mantovani A, De Santis R, Salvatori G. Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. J Biol Chem. 2008;283:10147-10161.
13. Inforzato A, Baldock C, Jowitt TA, Holmes DF, Lindstedt R, Marcellini M, Rivieccio V, Briggs DC, Kadler KE, Verdoliva A, Bottazzi B, Mantovani A, Salvatori G, Day AJ. The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. J Biol Chem. 2010;285:17681-17692.
14. Lee GW, Lee TH, Vilcek J. TSG-14, a tumor necrosis factor-and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J Immunol. 1993;150:1804-1812. (Pubitemid 23129656)
15. Vouret-Craviari V, Matteucci C, Peri G, Poli G, Introna M, Mantovani A. Expression of a long pentraxin, PTX3, by monocytes exposed to the mycobacterial cell wall component lipoarabinomannan. Infect Immun. 1997;65:1345-1350. (Pubitemid 27146623)
16. Deban L, Russo RC, Sironi M, Moalli F, Scanziani M, Zambelli V, Cuccovillo I, Bastone A, Gobbi M, Valentino S, Doni A, Garlanda C, Danese S, Salvatori G, Sassano M, Evangelista V, Rossi B, Zenaro E, Constantin G, Laudanna C, Bottazzi B, Mantovani A. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol. 2010; 11:328-334.
17. Garlanda C, Bottazzi B, Bastone A, Mantovani A. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu Rev Immunol. 2005;23:337-366. (Pubitemid 40563173)
18. Presta M, Camozzi M, Salvatori G, Rusnati M. Role of the soluble pattern recognition receptor PTX3 in vascular biology. J Cell Mol Med. 2007; 11:723-738. (Pubitemid 47313297)
19. Rusnati M, Camozzi M, Moroni E, Bottazzi B, Peri G, Indraccolo S, Amadori A, Mantovani A, Presta M. Selective recognition of fibroblast growth factor-2 by the long pentraxin PTX3 inhibits angiogenesis. Blood. 2004;104:92-99. (Pubitemid 38879843)
20. Camozzi M, Rusnati M, Bugatti A, Bottazzi B, Mantovani A, Bastone A, Inforzato A, Vincenti S, Bracci L, Mastroianni D, Presta M. Identification of an antiangiogenic FGF2-binding site in the N terminus of the soluble pattern recognition receptor PTX3. J Biol Chem. 2006;281:22605-22613.
21. Nicoli S, Presta M. The zebrafish/tumor xenograft angiogenesis assay. Nat Protoc. 2007;2:2918-2923.
22. Nicoli S, De Sena G, Presta M. Fibroblast Growth Factor 2-induced angiogenesis in zebrafish: the zebrafish yolk membrane (ZFYM) angiogenesis assay. J Cell Mol Med. 2009;13:2061-2068.
23. Camozzi M, Zacchigna S, Rusnati M, Coltrini D, Ramirez-Correa G, Bottazzi B, Mantovani A, Giacca M, Presta M. Pentraxin 3 inhibits fibroblast growth factor 2-dependent activation of smooth muscle cells in vitro and neointima formation in vivo. Arterioscler Thromb Vasc Biol. 2005;25:1837-1842. (Pubitemid 41243451)
24. Kohda D, Morton CJ, Parkar AA, Hatanaka H, Inagaki FM, Campbell ID, Day AJ. Solution structure of the link module: a hyaluronan-binding domain involved in extracellular matrix stability and cell migration. Cell. 1996;86:767-775. (Pubitemid 26303445)
25. Kuznetsova SA, Mahoney DJ, Martin-Manso G, Ali T, Nentwich HA, Sipes JM, Zeng B, Vogel T, Day AJ, Roberts DD. TSG-6 binds via its CUB-C domain to the cell-binding domain of fibronectin and increases fibronectin matrix assembly. Matrix Biol. 2008;27:201-210.
26. Maina V, Cotena A, Doni A, Nebuloni M, Pasqualini F, Milner CM, Day AJ, Mantovani A, Garlanda C. Coregulation in human leukocytes of the long pentraxin PTX3 and TSG-6. J Leukoc Biol. 2009;86:123-132.
27. Wisniewski HG, Maier R, Lotz M, Lee S, Klampfer L, Lee TH, Vilcek J. TSG-6: a TNF-, IL-1-, and LPS-inducible secreted glycoprotein associated with arthritis. J Immunol. 1993;151:6593-6601. (Pubitemid 23340406)
28. Wisniewski HG, Vilcek J. TSG-6: an IL-1/TNF-inducible protein with anti-inflammatory activity. Cytokine Growth Factor Rev. 1997;8: 143-156. (Pubitemid 27299142)
29. Milner CM, Day AJ. TSG-6: a multifunctional protein associated with inflammation. J Cell Sci. 2003;116:1863-1873. (Pubitemid 36622285)
30. Milner CM, Higman VA, Day AJ. TSG-6: a pluripotent inflammatory mediator? Biochem Soc Trans. 2006;34:446-450. (Pubitemid 43954008)
31. Lee RT, Yamamoto C, Feng Y, Potter-Perigo S, Briggs WH, Landschulz KT, Turi TG, Thompson JF, Libby P, Wight TN. Mechanical strain induces specific changes in the synthesis and organization of proteoglycans by vascular smooth muscle cells. J Biol Chem. 2001;276: 13847-13851.
32. Ye L, Mora R, Akhayani N, Haudenschild CC, Liau G. Growth factor and cytokine-regulated hyaluronan-binding protein TSG-6 is localized to the injury-induced rat neointima and confers enhanced growth in vascular smooth muscle cells. Circ Res. 1997;81:289-296. (Pubitemid 27362514)
33. Bayliss MT, Howat SL, Dudhia J, Murphy JM, Barry FP, Edwards JC, Day AJ. Up-regulation and differential expression of the hyaluronanbinding protein TSG-6 in cartilage and synovium in rheumatoid arthritis and osteoarthritis. Osteoarthritis Cartilage. 2001;9:42-48. (Pubitemid 32154916)
34. Baranova NS, Nileback E, Haller FM, Briggs DC, Svedhem S, Day AJ, Richter RP. The inflammation-associated protein TSG-6 cross-links hyaluronan via hyaluronan-induced TSG-6 oligomers J Biol Chem. 2011; 286:25675-25686.
35. Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, Day AJ, Salustri A, Hascall VC, Glant TT, Mikecz K. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development. 2003;130:2253-2261. (Pubitemid 36656719)
36. Rugg MS, Willis AC, Mukhopadhyay D, Hascall VC, Fries E, Fulop C, Milner CM, Day AJ. Characterization of complexes formed between TSG-6 and inter-β-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J Biol Chem. 2005;280: 25674-25686. (Pubitemid 40962277)
37. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P, Salvatori G, Mahoney DJ, Day AJ, Siracusa G, Romani L, Mantovani A. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development. 2004;131:1577-1586. (Pubitemid 38559284)
38. Scarchilli L, Camaioni A, Bottazzi B, Negri V, Doni A, Deban L, Bastone A, Salvatori G, Mantovani A, Siracusa G, Salustri A. PTX3 interacts with inter-β-trypsin inhibitor: implications for hyaluronan organization and cumulus oophorus expansion. J Biol Chem. 2007;282:30161-30170. (Pubitemid 350035268)
39. 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.
40. Mitola S, Moroni E, Ravelli C, Andres G, Belleri M, Presta M. Angiopoietin-1 mediates the proangiogenic activity of the bone morphogenic protein antagonist Drm. Blood. 2008;112:1154-1157.
41. Garlanda C, Hirsch E, Bozza S, Salustri A, De Acetis M, Nota R, Maccagno A, Riva F, Bottazzi B, Peri G, Doni A, Vago L, Botto M, De Santis R, Carminati P, Siracusa G, Altruda F, Vecchi A, Romani L, Mantovani A. Non-redundant role of the long pentraxin PTX3 in antifungal innate immune response. Nature. 2002;420:182-186. (Pubitemid 35340122)
42. Selbi W, Day AJ, Rugg MS, Fulop C, de la Motte CA, Bowen T, Hascall VC, Phillips AO. Overexpression of hyaluronan synthase 2 alters hyaluronan distribution and function in proximal tubular epithelial cells. J Am Soc Nephrol. 2006;17:1553-1567. (Pubitemid 43794658)
43. Leali D, Bianchi R, Bugatti A, Nicoli S, Mitola S, Ragona L, Tomaselli S, Gallo G, Catello S, Rivieccio V, Zetta L, Presta M. Fibroblast growth factor 2-antagonist activity of a long-pentraxin 3-derived antiangiogenic pentapeptide. J Cell Mol Med. 2010;14:2109-2121.
44. Leali D, Alessi P, Coltrini D, Rusnati M, Zetta L, Presta M. Fibroblast growth factor-2 antagonist and antiangiogenic activity of long-pentraxin 3-derived synthetic peptides. Curr Pharm Des. 2009;15:3577-3589.
45. Ribatti D, Nico B, Vacca A, Presta M. The gelatin sponge-chorioallantoic membrane assay. Nat Protoc. 2006;1:85-91.
46. Akhtar N, Dickerson EB, Auerbach R. The sponge/Matrigel angiogenesis assay. Angiogenesis. 2002;5:75-80. (Pubitemid 36076925)
47. Andres G, Leali D, Mitola S, Coltrini D, Camozzi M, Corsini M, Belleri M, Hirsch E, Schwendener RA, Christofori G, Alcami A, Presta M. A pro-inflammatory signature mediates FGF2-induced angiogenesis. J Cell Mol Med. 2009;13:2083-2108.
48. Leali D, Alessi P, Coltrini D, Ronca R, Corsini M, Nardo G, Indraccolo S, Presta M. Long pentraxin-3 inhibits FGF8b-dependent angiogenesis and growth of steroid hormone-regulated tumors. Mol Cancer Ther. 2011;10:1600-1610.
49. Alessi P, Leali D, Camozzi M, Cantelmo A, Albini A, Presta M. Anti-FGF2 approaches as a strategy to compensate resistance to anti-VEGF therapy: long-pentraxin 3 as a novel antiangiogenic FGF2-antagonist. Eur Cytokine Netw. 2009;20:225-234.
50. Day AJ, de la Motte CA. Hyaluronan cross-linking: a protective mechanism in inflammation? Trends Immunol. 2005;26:637-643. (Pubitemid 41628196)
51. Miguita L, Martinez EF, de Araujo NS, de Araujo VC. FGF-2, TGfβ-1, PDGF-A and respective receptors expression in pleomorphic adenoma myoepithelial cells: an in vivo and in vitro study. J Appl Oral Sci. 2010;18:83-91.
52. Zhang W, Chu YQ, Ye ZY, Zhao ZS, Tao HQ. Expression of hepatocyte growth factor and basic fibroblast growth factor as prognostic indicators in gastric cancer. Anat Rec (Hoboken). 2009;292:1114-1121.
53. Oh JY, Roddy GW, Choi H, Lee RH, Ylostalo JH, Rosa RH Jr, Prockop DJ. Anti-inflammatory protein TSG-6 reduces inflammatory damage to the cornea following chemical and mechanical injury. Proc Natl Acad Sci USA. 2010;107:16875-16880.
54. Ribatti D, Presta M, Vacca A, Ria R, Giuliani R, Dell'Era P, Nico B, Roncali L, Dammacco F. Human erythropoietin induces a pro-angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. Blood. 1999;93:2627-2636. (Pubitemid 29181195)
55. Hatanaka H, Abe Y, Naruke M, Tokunaga T, Oshika Y, Kawakami T, Osada H, Nagata J, Kamochi J, Tsuchida T, Kijima H, Yamazaki H, Inoue H, Ueyama Y, Nakamura M. Significant correlation between interleukin 10 expression and vascularization through angiopoietin/TIE2 networks in non-small cell lung cancer. Clin Cancer Res. 2001;7:1287-1292. (Pubitemid 32708682)
56. Heba G, Krzeminski T, Porc M, Grzyb J, Ratajska A, Dembinska-Kiec A. The time course of tumor necrosis factor-κ, inducible nitric oxide synthase and vascular endothelial growth factor expression in an experimental model of chronic myocardial infarction in rats. J Vasc Res. 2001;38:288-300. (Pubitemid 32588841)