Identification of fibronectin type I domains as amyloid-binding modules on tissue-type plasminogen activator and three homologs

Amyloid

Volumn 15, Issue 3, 2008, Pages 166-180

  Maas, Coen ^a   Schiks, Bettina ^a,b   Strangi, Remo D ^c   Hackeng, Tilman M ^c   Bouma, Bonno N ^d   Gebbink, Martijn F B G ^a,b,e   Bouma, Barend ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b Crossbeta Biosciences BV   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e NONE   (Netherlands)

Author keywords

Amyloid; Fibrinolysis; Fibronectin type I domain; tPA

Indexed keywords

AMYLOID; BLOOD CLOTTING FACTOR 12; FIBRONECTIN; FIBRONECTIN TYPE 1; PLASMIN; SCATTER FACTOR; SCLEROPROTEIN; TISSUE PLASMINOGEN ACTIVATOR; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING ASSAY; BINDING SITE; ENZYME ACTIVITY; ENZYME ISOLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE MICROSCOPY; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; THROMBOCYTE AGGREGATION;

AMYLOID; AMYLOID BETA-PROTEIN; BINDING SITES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FACTOR XII; FIBRONECTINS; HUMANS; MICROSCOPY, FLUORESCENCE; PEPTIDE FRAGMENTS; PLASMIN; PLATELET AGGREGATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; TISSUE PLASMINOGEN ACTIVATOR;

EID: 54249150387     PISSN: 13506129     EISSN: 17442818     Source Type: Journal    
DOI: 10.1080/13506120802193498     Document Type: Article

References (69)

1. Syrovets T, Tippler B, Rieks M, Simmet T. Plasmin is a potent and specific chemoattractant for human peripheral monocytes acting via a cyclic guanosine monophosphate-dependent pathway. Blood 1997;89:4574-4583.
2. Syrovets T, Jendrach M, Rohwedder A, Schule A, Simmet T. Plasmin-induced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKKbeta-mediated NF-kappaB activation. Blood 2001;97:3941-3950.
3. Baricos WH, Cortez SL, el-Dahr SS, Schnaper HW. ECM degradation by cultured human mesangial cells is mediated by a PA/plasmin/MMP-2 cascade. Kidney Int 1995;47:1039-1047.
4. Ling C, Zou T, Hsiao Y, Tao X, Chen ZL, Strickland S, Song H. Disruption of tissue plasminogen activator gene reduces macrophage migration. Biochem Biophys Res Commun 2006;349:906-912.
5. Brodsky S, Chen J, Lee A, Akassoglou K, Norman J, Goligorsky MS. Plasmin-dependent and -independent effects of plasminogen activators and inhibitor-1 on ex vivo angiogenesis. Am J Physiol Heart Circ Physiol 2001;281:H1784-H1792.
6. Syrovets T, Simmet T. Novel aspects and new roles for the serine protease plasmin. Cell Mol Life Sci 2004;61:873-885.
7. Galantai R, Modos K, Fidy J, Kolev K, Machovich R. Structural basis of the cofactor function of denatured albumin in plasminogen activation by tissue-type plasminogen activator. Biochem Biophys Res Commun 2006;341:736-741.
8. Bobbink IW, Tekelenburg WL, Sixma JJ, de Boer HC, Banga JD, de Groot PG. Glycated proteins modulate tissue-plasminogen activator-catalyzed plasminogen activation. Biochem Biophys Res Commun 1997;240:595-601.
9. Machovich R, Owen WG. Denatured proteins as cofactors for plasminogen activation. Arch Biochem Biophys 1997;344:343-349.
10. Haddeland U, Bennick A, Brosstad F. Stimulating effect on tissue-type plasminogen activator - a new and sensitive indicator of denatured fibrinogen. Thromb Res 1995;77:329-336.
11. Haddeland U, Sletten K, Bennick A, Nieuwenhuizen W, Brosstad F. Aggregated, conformationally changed fibrinogen exposes the stimulating sites for t-PA-catalysed plasminogen activation. Thromb Haemost 1996;75:326-331.
12. Reijerkerk A, Mosnier LO, Kranenburg O, Bouma BN, Carmeliet P, Drixler T, Meijers JC, Voest EE, Gebbink MF. Amyloid endostatin induces endothelial cell detachment by stimulation of the plasminogen activation system. Mol Cancer Res 2003;1:561-568.
13. Kranenburg O, Bouma B, Kroon-Batenburg LM, Reijerkerk A, Wu YP, Voest EE, Gebbink MF. Tissue-type plasminogen activator is a multiligand cross-beta structure receptor. Curr Biol 2002;12:1833-1839.
14. Maas C, Hermeling S, Bouma B, Jiskoot W, Gebbink MF. A role for protein misfolding in immunogenicity of biopharmaceuticals. J Biol Chem 2007;282:2229-2236.
15. Herczenik E, Bouma B, Korporaal SJ, Strangi R, Zeng Q, Gros P, Van EM, Van Berkel TJ, Gebbink MF, Akkerman JW. Activation of human platelets by misfolded proteins. Arterioscler Thromb Vasc Biol 2007;27:1657-1665.
16. Ursini F, Davies KJ, Maiorino M, Parasassi T, Sevanian A. Atherosclerosis: another protein misfolding disease? Trends Mol Med 2002;8:370-374.
17. Lee JY, Kweon HS, Cho E, Lee JY, Byun HR, Kim DH, Kim YH, Han PL, Koh JY. Upregulation of tPA/plasminogen proteolytic system in the periphery of amyloid deposits in the Tg2576 mouse model of Alzheimer's disease. Neurosci Lett 2007;423:82-87.
18. Melchor JP, Pawlak R, Strickland S. The tissue plasminogen activator-plasminogen proteolytic cascade accelerates amyloid-beta (Abeta) degradation and inhibits Abeta-induced neurodegeneration. J Neurosci 2003;23:8867-8871.
19. Periz G, Fortini ME. Proteolysis in Alzheimer's disease. Can plasmin tip the balance? EMBO Rep 2000;1:477-478.
20. Siao CJ, Tsirka SE. Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J Neurosci 2002;22:3352-3358.
21. Tucker HM, Kihiko-Ehmann M, Wright S, Rydel RE, Estus S. Tissue plasminogen activator requires plasminogen to modulate amyloid-beta neurotoxicity and deposition. J Neurochem 2000;75:2172-2177.
22. Tucker HM, Kihiko M, Caldwell JN, Wright S, Kawarabayashi T, Price D, Walker D, Scheff S, McGillis JP, Rydel RE, Estus S. The plasmin system is induced by and degrades amyloid-beta aggregates. J Neurosci 2000;20:3937-3946.
23. Xanthopoulos K, Paspaltsis I, Apostolidou V, Petrakis S, Siao CJ, Kalpatsanidis A, Grigoriadis N, Tsaftaris A, Tsirka SE, Sklaviadis T. Tissue plasminogen activator in brain tissues infected with transmissible spongiform encephalopathies. Neurobiol Dis 2005;20:519-527.
24. Jaroniec CP, MacPhee CE, Astrof NS, Dobson CM, Griffin RG. Molecular conformation of a peptide fragment of transthyretin in an amyloid fibril. Proc Natl Acad Sci U S A 2002;99:16748-16753.
25. Yamada M, Kadoya Y, Kasai S, Kato K, Mochizuki M, Nishi N, Watanabe N, Kleinman HK, Yamada Y, Nomizu M. Ile-Lys-Val-Ala-Val (IKVAV)-containing laminin alpha1 chain peptides form amyloid-like fibrils. FEBS Lett 2002;530:48-52.
26. Schielen JG, Adams HP, Voskuilen M, Tesser GJ, Nieuwenhuizen W. Structural requirements of position A alpha-157 in fibrinogen for the fibrin-induced rate enhancement of the activation of plasminogen by tissue-type plasminogen activator. Biochem J 1991;276:655-659.
27. Johannessen M, Diness V, Pingel K, Petersen LC, Rao D, Lioubin P, O'Hara P, Mulvihill E. Fibrin affinity and clearance of t-PA deletion and substitution analogues. Thromb Haemost 1990;63:54-59.
28. Gebbink MF, Zondag GC, Koningstein GM, Feiken E, Wubbolts RW, Moolenaar WH. Cell surface expression of receptor protein tyrosine phosphatase RPTP mu is regulated by cell-cell contact. J Cell Biol 1995;131:251-260.
29. van Zonneveld AJ, Veerman H, Pannekoek H. On the interaction of the finger and the kringle-2 domain of tissue-type plasminogen activator with fibrin. Inhibition of kringle-2 binding to fibrin by epsilon-amino caproic acid. J Biol Chem 1986;261:14214-14218.
30. Rostagno A, Williams MJ, Baron M, Campbell ID, Gold LI. Further characterization of the NH2-terminal fibrin-binding site on fibronectin. J Biol Chem 1994;269:31938-31945.
31. Rostagno AA, Schwarzbauer JE, Gold LI. Comparison of the fibrin-binding activities in the N- and C-termini of fibronectin. Biochem J 1999;338:375-386.
32. Schnolzer M, Alewood P, Jones A, Alewood D, Kent SB. In situ neutralization in Boc-chemistry solid phase peptide synthesis. Rapid, high yield assembly of difficult sequences. Int J Pept Protein Res 1992;40:180-193.
33. Dawson PE, Muir TW, Clark-Lewis I, Kent SB. Synthesis of proteins by native chemical ligation. Science 1994;266:776-779.
34. Hackeng TM, Griffin JH, Dawson PE. Protein synthesis by native chemical ligation: expanded scope by using straightforward methodology. Proc Natl Acad Sci USA 1999;96:10068-10073.
35. Bobbink IW, de Boer HC, Tekelenburg WL, Banga JD, de Groot PG. Effect of extracellular matrix glycation on endothelial cell adhesion and spreading: involvement of vitronectin. Diabetes 1997;46:87-93.
36. Renne T, Pozgajova M, Gruner S, Schuh K, Pauer HU, Burfeind P, Gailani D, Nieswandt B. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med 2005;202:271-281.
37. Renne T, Nieswandt B, Gailani D. The intrinsic pathway of coagulation is essential for thrombus stability in mice. Blood Cells Mol Dis 2006;36:148-151.
38. Miyazawa K, Shimomura T, Kitamura N. Activation of hepatocyte growth factor in the injured tissues is mediated by hepatocyte growth factor activator. J Biol Chem 1996;271:3615-3618.
39. Itoh H, Naganuma S, Takeda N, Miyata S, Uchinokura S, Fukushima T, Uchiyama S, Tanaka H, Nagaike K, Shimomura T, Miyazawa K, Yamada G, Kitamura N, Koono M, Kataoka H. Regeneration of injured intestinal mucosa is impaired in hepatocyte growth factor activator-deficient mice. Gastroenterology 2004;127:1423-1435.
40. Matsubara Y, Ichinose M, Yahagi N, Tsukada S, Oka M, Miki K, Kimura S, Omata M, Shiokawa K, Kitamura N, Kaneko Y, Fukamachi H. Hepatocyte growth factor activator: a possible regulator of morphogenesis during fetal development of the rat gastrointestinal tract. Biochem Biophys Res Commun 1998;253:477-484.
41. Maas C, Govers-Riemslag JWP, Bouma B, Schiks B, Hazenberg BPC, Lokhorst HM, Hammarstrõm P, ten Cate H, de Groot PG, Bouma BN, Gebbink MFBG. Factor XII is activated by misfolded proteins, which leads to kallikrein formation without initiating coagulation. J Clin Invest 2008; in press.
42. Shibayama Y, Joseph K, Nakazawa Y, Ghebreihiwet B, Peerschke EI, Kaplan AP. Zinc-dependent activation of the plasma kinin-forming cascade by aggregated beta amyloid protein. Clin Immunol 1999;90:89-99.
43. Bouma B, Kroon-Batenburg LM, Wu YP, Brunjes B, Posthuma G, Kranenburg O, de Groot PG, Voest EE, Gebbink MF. Glycation induces formation of amyloid cross-beta structure in albumin. J Biol Chem 2003;278:41810-41819.
44. Mao Y, Ootaka T, Saito T, Sato H, Sato T, Ito S. The involvement of advanced glycation endproducts (AGEs) in renal injury of diabetic glomerulosclerosis: association with phenotypic change in renal cells and infiltration of immune cells. Clin Exp Nephrol 2003;7:201-209.
45. Hudry-Clergeon G, Freyssinet JM, Torbet J, Marx J. Orientation of fibrin in strong magnetic fields. Ann N Y Acad Sci 1983;408:380-387.
46. Downing AK, Driscoll PC, Harvey TS, Dudgeon TJ, Smith BO, Baron M, Campbell ID. Solution structure of the fibrin binding finger domain of tissue-type plasminogen activator determined by 1H nuclear magnetic resonance. J Mol Biol 1992;225:821-833.
47. Ledesma MD, Da Silva JS, Crassaerts K, Delacourte A, De SB, Dotti CG. Brain plasmin enhances APP alpha-cleavage and Abeta degradation and is reduced in Alzheimer's disease brains. EMBO Rep 2000;1:530-535.
48. Paul J, Strickland S, Melchor JP. Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease. J Exp Med 2007;204:1999-2008.
49. Van Nostrand WE, Melchor J, Wagner M, Davis J. Cerebrovascular smooth muscle cell surface fibrillar A beta. Alteration of the proteolytic environment in the cerebral vessel wall. Ann N Y Acad Sci 2000;903:89-96.
50. Medina MG, Ledesma MD, Dominguez JE, Medina M, Zafra D, Alameda F, Dotti CG, Navarro P. Tissue plasminogen activator mediates amyloid-induced neurotoxicity via Erk1/2 activation. EMBO J 2005;24:1706-1716.
51. Yasuhara O, Walker DG, McGeer PL. Hageman factor and its binding sites are present in senile plaques of Alzheimer's disease. Brain Res 1994;654:234-240.
52. Bergamaschini L, Parnetti L, Pareyson D, Canziani S, Cugno M, Agostoni A. Activation of the contact system in cerebrospinal fluid of patients with Alzheimer disease. Alzheimer Disease & Associated Disorders 1998;12:102-108.
53. Bergamaschini L, Donarini C, Gobbo G, Parnetti L, Gallai V. Activation of complement and contact system in Alzheimer's disease. Mech Ageing Develop 2001;122:1971-1983.
54. Miklossy J, Taddei K, Martins R, Escher G, Kraftsik R, Pillevuit O, Lepori D, Campiche M. Alzheimer disease: curly fibers and tangles in organs other than brain. J Neuropathol Exp Neurol 1999;58:803-814.
55. van Duinen SG, Maat-Schieman ML, Bruijn JA, Haan J, Roos RA. Cortical tissue of patients with hereditary cerebral hemorrhage with amyloidosis (Dutch) contains various extracellular matrix deposits. Lab Invest 1995;73:183-189.
56. Yamada T, Tsujioka Y, Taguchi J, Takahashi M, Tsuboi Y, Shimomura T. White matter astrocytes produce hepatocyte growth factor activator inhibitor in human brain tissues. Exp Neurol 1998;153:60-64.
57. Shikano M, Kushimoto H, Hasegawa H, Tomita M, Hasegawa M, Murakami K, Kawashima S. Usefulness of serum hepatocyte growth factor for the diagnosis of amyloidosis. Intern Med 2000;39:715-719.
58. Williams MJ, Phan I, Baron M, Driscoll PC, Campbell ID. Secondary structure of a pair of fibronectin type 1 modules by two-dimensional nuclear magnetic resonance. Biochemistry 1993;32:7388-7395.
59. Limper AH, Quade BJ, LaChance RM, Birkenmeier TM, Rangwala TS, McDonald JA. Cell surface molecules that bind fibronectin's matrix assembly domain. J Biol Chem 1991;266:9697-9702.
60. Hocking DC, Sottile J, Keown-Longo PJ. Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin. J Biol Chem 1994;269:19183-19187.
61. Ohashi T, Erickson HP. Domain unfolding plays a role in superfibronectin formation. J Biol Chem 2005;280:39143-39151.
62. Ingham KC, Brew SA, Huff S, Litvinovich SV. Cryptic self-association sites in type III modules of fibronectin. J Biol Chem 1997;272:1718-1724.
63. Litvinovich SV, Brew SA, Aota S, Akiyama SK, Haudenschild C, Ingham KC. Formation of amyloid-like fibrils by self-association of a partially unfolded fibronectin type III module. J Mol Biol 1998;280:245-258.
64. Schlunegger MP, Bennett MJ, Eisenberg D. Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. Adv Protein Chem 1997;50:61-122.
65. Bennett MJ, Schlunegger MP, Eisenberg D. 3D domain swapping: a mechanism for oligomer assembly. Protein Sci 1995;4:2455-2468.
66. Schwarz-Linek U, Pilka ES, Pickford AR, Kim JH, Hook M, Campbell ID, Potts JR. High affinity streptococcal binding to human fibronectin requires specific recognition of sequential F1 modules. J Biol Chem 2004;279:39017-39025.
67. Sagare A, Deane R, Bell RD, Johnson B, Hamm K, Pendu R, Marky A, Lenting PJ, Wu Z, Zarcone T, Goate A, Mayo K, Perlmutter D, Coma M, Zhong Z, Zlokovic BV. Clearance of amyloid-beta by circulating lipoprotein receptors. Nat Med 2007;13:1029-1031.
68. Bu G, Cam J, Zerbinatti C. LRP in amyloid-beta production and metabolism. Ann N Y Acad Sci 2006;1086:35-53.
69. Donahue JE, Flaherty SL, Johanson CE, Duncan JA, III, Silverberg GD, Miller MC, Tavares R, Yang W, Wu Q, Sabo E, Hovanesian V, Stopa EG. RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol (Berl) 2006;112:405-415.