Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-β after vascular damage

Journal of Neuroscience

Volumn 30, Issue 17, 2010, Pages 5843-5854

  Schachtrup, Christian ^a   Ryu, Jae K ^a   Helmrick, Matthew J ^a   Vagena, Eirini ^a   Galanakis, Dennis K ^b   Degen, Jay L ^c   Margolis, Richard U ^d   Akassoglou, Katerina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN; NEUROCAN; PROTEOGLYCAN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; BLOOD VESSEL PERMEABILITY; BLOOD VESSEL RUPTURE; BRAIN CORTEX; BRAIN INJURY; CELL ACTIVATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GENETICS; GLIA; GLIA CELL; IN VITRO STUDY; IN VIVO STUDY; INJECTION; MALE; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; SCAR FORMATION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CEREBRAL CORTEX; CICATRIX; FIBRINOGEN; GLIOSIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURITES; PHOSPHORYLATION; PROTEOGLYCANS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 77951664911     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0137-10.2010     Document Type: Article

References (79)

1. Abbott NJ, Rönnbäck L, Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41-53.
2. Adams RA, Passino M, Sachs BD, Nuriel T, Akassoglou K (2004) Fibrin mechanisms and functions in nervous system pathology. Mol Interv 4:163-176. (Pubitemid 38960845)
3. Adams RA, Schachtrup C, Davalos D, Tsigelny I, Akassoglou K (2007a) Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis. Curr Med Chem 14:2925-2936. (Pubitemid 350201659)
4. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, Degen JL, Akassoglou K (2007b) The fibrin-derived gamma377-395 peptide inhibits microglia activation and suppresses relapsing paralysis in central nervous system autoimmune disease. J Exp Med 204:571-582. (Pubitemid 46457080)
5. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, Vorhees CV, Wills-Karp M, Degen JL, Davis RJ, Mizushima N, Rakic P, Dardzinski BJ, Holland SK, Sharp FR, KuanCY (2006) Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy.Am J Pathol 169:566-583.
6. Akassoglou K, Strickland S (2002) Nervous system pathologies: the fibrin perspective. Biol Chem 383:37-45. (Pubitemid 34224026)
7. Akassoglou K, Yu WM, Akpinar P, Strickland S (2002) Fibrin inhibits peripheral nerve remyelination by regulating Schwann cell differentiation. Neuron 33:861-875. (Pubitemid 34246353)
8. Akassoglou K, Adams RA, Bauer J, Mercado P, Tseveleki V, Lassmann H, Probert L, Strickland S (2004) Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumor necrosis factor transgenic mouse model for multiple sclerosis. Proc Natl Acad Sci U S A 101:6698-6703. (Pubitemid 38586037)
9. Annes JP, Munger JS, Rifkin DB (2003) Making sense of latent TGFbeta activation. J Cell Sci 116:217-224.
10. Annes JP, Chen Y, Munger JS, Rifkin DB (2004) Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J Cell Biol 165:723-734.
11. Araya J, Cambier S, Morris A, Finkbeiner W, Nishimura SL (2006) Integrin-mediated transforming growth factor-beta activation regulates homeostasis of the pulmonary epithelial-mesenchymal trophic unit. Am J Pathol 169:405-415. (Pubitemid 44156303)
12. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438. (Pubitemid 30220330)
13. Attisano L, Wrana JL, López-Casillas F, Massagué J (1994) TGF-beta receptors and actions. Biochim Biophys Acta 1222:71-80.
14. Belkin AM, Tsurupa G, Zemskov E, Veklich Y, Weisel JW, Medved L (2005) Transglutaminase-mediated oligomerization of the fibrin(ogen) alphaC domains promotes integrin-dependent cell adhesion and signaling. Blood 105:3561-3568. (Pubitemid 40628201)
15. Blobe GC, Schiemann WP, Lodish HF (2000) Role of transforming growth factor beta in human disease. N Engl J Med 342:1350-1358.
16. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640. (Pubitemid 34406764)
17. Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn AP, Mori T, Götz M (2008) Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 105:3581-3586. (Pubitemid 351723595)
18. Burton RA, Tsurupa G, Medved L, Tjandra N (2006) Identification of an ordered compact structure within the recombinant bovine fibrinogen alphaC-domain fragment by NMR. Biochemistry 45:2257-2266. (Pubitemid 43271325)
19. Busch SA, Horn KP, Silver DJ, Silver J (2009) Overcoming macrophage-mediated axonal dieback following CNS injury. J Neurosci 29:9967-9976.
20. Cambier S, Gline S, Mu D, Collins R, Araya J, Dolganov G, Einheber S, Boudreau N, Nishimura SL (2005) Integrin alpha(v)beta8-mediated activation of transforming growth factor-beta by perivascular astrocytes: an angiogenic control switch. Am J Pathol 166:1883-1894.
21. Chernousov MA, Carey DJ (2003) alphaVbeta8 integrin is a Schwann cell receptor for fibrin. Exp Cell Res 291:514-524.
22. de Maat MP, Verschuur M (2005) Fibrinogen heterogeneity: inherited and noninherited. Curr Opin Hematol 12:377-383.
23. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143-2155.
24. Fawcett JW, Asher RA (1999) The glial scar and central nervous system repair. Brain Res Bull 49:377-391.
25. Fitch MT, Doller C, Combs CK, Landreth GE, Silver J (1999) Cellular and molecular mechanisms of glial scarring and progressive cavitation: in vivo and in vitro analysis of inflammation-induced secondary injury after CNS trauma. J Neurosci 19:8182-8198.
26. Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669-680.
27. Galanakis DK, Neerman-Arbez M, Scheiner T, Henschen A, Hubbs D, Nagaswami C, Weisel JW (2007) Homophenotypic Aalpha R16H fibrinogen (Kingsport): uniquely altered polymerization associated with slower fibrinopeptide A than fibrinopeptide B release. Blood Coagul Fibrinolysis 18:731-737.
28. Gay D, EsiriM (1991) Blood-brain barrier damage in acute multiple sclerosis plaques. An immunocytological study. Brain 114:557-572.
29. Gentry LE, Nash BW (1990) The pro domain of pre-pro-transforming growth factor beta 1 when independently expressed is a functional binding protein for the mature growth factor. Biochemistry 29:6851-6857.
30. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285:1028-1032.
31. Grainger DJ, Wakefield L, Bethell HW, Farndale RW, Metcalfe JC (1995) Release and activation of platelet latent TGF-beta in blood clots during dissolution with plasmin. Nat Med 1:932-937.
32. Grainger DJ, Mosedale DE, Metcalfe JC (2000) TGF-beta in blood: a complex problem. Cytokine Growth Factor Rev 11:133-145.
33. Huang XZ, Wu JF, Cass D, Erle DJ, Corry D, Young SG, Farese RV Jr, Sheppard D (1996) Inactivation of the integrin beta 6 subunit gene reveals a role of epithelial integrins in regulating inflammation in the lung and skin. J Cell Biol 133:921-928.
34. Jones LL, Margolis RU, Tuszynski MH (2003) The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 182:399-411.
35. Kim AH, Yano H, Cho H, Meyer D, Monks B, Margolis B, Birnbaum MJ, Chao MV (2002) Akt1 regulates a JNK scaffold during excitotoxic apoptosis. Neuron 35:697-709.
36. Lagord C, Berry M, Logan A (2002) Expression of TGFbeta2 but not TGF-beta 1 correlates with the deposition of scar tissue in the lesioned spinal cord. Mol Cell Neurosci 20:69-92.
37. Li MO, Flavell RA (2008) TGF-beta: a master of all T cell trades. Cell 134:392-404.
38. Li MO, Wan YY, Flavell RA (2007) T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 26:579-591.
39. Lin AH, Luo J, Mondshein LH, ten Dijke P, Vivien D, Contag CH, Wyss-Coray T (2005) Global analysis of Smad2/3-dependent TGF-beta signaling in living mice reveals prominent tissue-specific responses to injury. J Immunol 175:547-554.
40. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
41. Lord ST (2007) Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr Opin Hematol 14:236-241.
42. Marik C, Felts PA, Bauer J, Lassmann H, Smith KJ (2007) Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity? Brain 130:2800-2815.
43. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
44. McKeon RJ, Jurynec MJ, Buck CR (1999) The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci 19:10778-10788.
45. Medved L, Nieuwenhuizen W (2003) Molecular mechanisms of initiation of fibrinolysis by fibrin. Thromb Haemost 89:409-419.
46. Milev P, Maurel P, Häring M, Margolis RK, Margolis RU (1996) TAG-1/ axonin-1 is a high-affinity ligand of neurocan, phosphacan/protein-tyrosine phosphatase-zeta/beta, and N-CAM. J Biol Chem 271:15716-15723.
47. Milner R, Relvas JB, Fawcett J, ffrench-Constant C (2001) Developmental regulation of alphav integrins produces functional changes in astrocyte behavior. Mol Cell Neurosci 18:108-118.
48. Miyazono K, Hellman U, Wernstedt C, Heldin CH (1988) Latent high molecular weight complex of transforming growth factor beta 1. Purification from human platelets and structural characterization. J Biol Chem 263:6407-6415.
49. Moro L, Dolce L, Cabodi S, Bergatto E, Boeri Erba E, Smeriglio M, Turco E, Retta SF, GiuffridaMG,Venturino M, Godovac-Zimmermann J, Conti A, Schaefer E, Beguinot L, Tacchetti C, Gaggini P, Silengo L, Tarone G, Defilippi P (2002) Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J Biol Chem 277:9405-9414.
50. Mosesson MW, Sherry S (1966) The preparation and properties of human fibrinogen of relatively high solubility. Biochemistry 5:2829-2835.
51. Mosesson MW, Finlayson JS, Umfleet RA, Galanakis D (1972) Human fibrinogen heterogeneities. I. Structural and related studies of plasma fibrinogens which are high solubility catabolic intermediates. J Biol Chem 247:5210-5219.
52. Mosesson MW, Siebenlist KR, Meh DA (2001) The structure and biological features of fibrinogen and fibrin. Ann N Y Acad Sci 936:11-30.
53. Mu D, Cambier S, Fjellbirkeland L, Baron JL, Munger JS, Kawakatsu H, Sheppard D, Broaddus VC, Nishimura SL (2002) The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J Cell Biol 157:493-507.
54. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, Rifkin DB, Sheppard D (1999) The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96:319-328.
55. Niederöst BP, Zimmermann DR, Schwab ME, Bandtlow CE (1999) Bovine CNS myelin contains neurite growth-inhibitory activity associated with chondroitin sulfate proteoglycans. J Neurosci 19:8979-8989.
56. Passino MA, Adams RA, Sikorski SL, Akassoglou K (2007) Regulation of hepatic stellate cell differentiation by the neurotrophin receptor p75NTR. Science 315:1853-1856.
57. Paul J, Strickland S, Melchor JP (2007) Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of Alzheimer's disease. J Exp Med 204:1999-2008.
58. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118:2190-2199.
59. Preston E, Webster J, Small D (2001) Characteristics of sustained bloodbrain barrier opening and tissue injury in a model for focal trauma in the rat. J Neurotrauma 18:83-92.
60. Ryu JK, McLarnon JG (2008) A leaky blood-brain barrier, fibrinogen infiltration and microglial reactivity in inflamed Alzheimer's disease brain. J Cell Mol Med 13:2911-2925.
61. Saharinen J, Hyytiäinen M, Taipale J, Keski-Oja J (1999) Latent transforming growth factor-beta binding proteins (LTBPs)-structural extracellular matrix proteins for targeting TGF-beta action. Cytokine Growth Factor Rev 10:99-117.
62. Sahni A, Francis CW (2000) Vascular endothelial growth factor binds to fibrinogen and fibrin and stimulates endothelial cell proliferation. Blood 96:3772-3778.
63. Sahni A, Altland OD, Francis CW (2003) FGF-2 but not FGF-1 binds fibrin and supports prolonged endothelial cell growth. J Thromb Haemost 1:1304-1310.
64. Sahni A, Guo M, Sahni SK, Francis CW (2004) Interleukin-1beta but not IL-1alpha binds to fibrinogen and fibrin and has enhanced activity in the bound form. Blood 104:409-414.
65. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T (1997) TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124:2659-2670.
66. Schachtrup C, Lu P, Jones LL, Lee JK, Lu J, Sachs BD, Zheng B, Akassoglou K (2007) Fibrinogen inhibits neurite outgrowth via beta3 integrin-mediated phosphorylation of the EGF receptor. Proc Natl Acad Sci U S A 104:11814-11819.
67. Schnell L, Fearn S, Klassen H, Schwab ME, Perry VH (1999) Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci 11:3648-3658.
68. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D (1992) Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359:693-699.
69. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
70. Smith GM, Strunz C (2005) Growth factor and cytokine regulation of chondroitin sulfate proteoglycans by astrocytes. Glia 52:209-218.
71. Sofroniew MV (2005) Reactive astrocytes in neural repair and protection. Neuroscientist 11:400-407.
72. Spraggon G, Applegate D, Everse SJ, Zhang JZ, Veerapandian L, Redman C, Doolittle RF, Grieninger G (1998) Crystal structure of a recombinant alphaEC domain from human fibrinogen-420. Proc Natl Acad Sci U S A 95:9099-9104.
73. Suh TT, Holmbäck K, Jensen NJ, Daugherty CC, Small K, Simon DI, Potter S, Degen JL (1995) Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev 9:2020-2033.
74. Tesseur I, Zou K, Esposito L, Bard F, Berber E, Can JV, Lin AH, Crews L, Tremblay P, Mathews P, Mucke L, Masliah E, Wyss-Coray T (2006) Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J Clin Invest 116:3060-3069.
75. Unsold C, Hyytiäinen M, Bruckner-Tuderman L, Keski-Oja J (2001) Latent TGF-beta binding protein LTBP-1 contains three potential extracellular matrix interacting domains. J Cell Sci 114:187-197.
76. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z (2002) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417:941-944.
77. Wipff PJ, Hinz B (2008) Integrins and the activation of latent transforming growth factor beta1 - an intimate relationship. Eur J Cell Biol 87:601-615.
78. Wipff PJ, Rifkin DB, Meister JJ, Hinz B (2007) Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 179:1311-1323.
79. Yang Z, Mu Z, Dabovic B, Jurukovski V, Yu D, Sung J, Xiong X, Munger JS (2007) Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice. J Cell Biol 176:787-793.