Vascular damage in the central nervous system: A multifaceted role for vascular-derived TGF-β

Cell and Tissue Research

Volumn 347, Issue 1, 2012, Pages 187-201

  Beck, Kristina ^a   Schachtrup, Christian ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Astrocyte; Blood brain barrier; Fibrinogen; Neurovascular unit; Regeneration

Indexed keywords

AMYLOID BETA PROTEIN; FIBRINOGEN; TRANSFORMING GROWTH FACTOR BETA;

ALZHEIMER DISEASE; ANGIOGENESIS; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD VESSEL INJURY; BLOOD VESSEL PERMEABILITY; BRAIN INJURY; BRAIN LEVEL; CAPILLARY LEAK SYNDROME; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; HUMAN; INTRACELLULAR SIGNALING; NERVE CELL NETWORK; NERVE FIBER REGENERATION; NEUROMODULATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW;

ANIMALS; BLOOD VESSELS; BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEM; HUMANS; MODELS, ANIMAL; NEURONS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84859438562     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-011-1228-0     Document Type: Review

References (182)

1. Abbott NJ, Ronnback L, Hansson E (2006) Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 7:41-53 (Pubitemid 41828930)
2. Acharya M, Mukhopadhyay S, Paidassi H, Jamil T, Chow C, Kissler S, Stuart LM, Hynes RO, Lacy-Hulbert A (2010) alphav Integrin expression by DCs is required for Th17 cell differentiation and development of experimental autoimmune encephalomyelitis in mice. J Clin Invest 120:4445-4452
3. Adams RA, Bauer J, Flick MJ, Sikorski SL, Nuriel T, Lassmann H, Degen JL, Akassoglou K (2007a) 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)
4. Adams RA, Schachtrup C, Davalos D, Tsigelny I, Akassoglou K (2007b) Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis. Curr Med Chem 14:2925-2936 (Pubitemid 350201659)
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, Kuan CY (2006) Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 169:566-583 (Pubitemid 44156315)
6. 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)
7. 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 USA 101:6698-6703 (Pubitemid 38586037)
8. Annes JP, Munger JS, Rifkin DB (2003) Making sense of latent TGFbeta activation. J Cell Sci 116:217-224 (Pubitemid 36163863)
9. 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 (Pubitemid 38765773)
10. 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)
11. Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C (2010) Pericytes regulate the blood-brain barrier. Nature 468:557-561
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. Behzadian MA, Wang XL, Jiang B, Caldwell RB (1995) Angiostatic role of astrocytes: suppression of vascular endothelial cell growth by TGF-beta and other inhibitory factor(s). Glia 15:480-490
14. Behzadian MA, Wang XL, Windsor LJ, Ghaly N, Caldwell RB (2001) TGF-beta increases retinal endothelial cell permeability by increasing MMP-9: possible role of glial cells in endothelial barrier function. Invest Ophthalmol Vis Sci 42:853-859 (Pubitemid 32206931)
15. Bell RD, Zlokovic BV (2009) Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol 118:103-113
16. Bengtsson L (2007) What MAN1 does to the Smads. TGFbeta/BMP signaling and the nuclear envelope. FEBS J 274:1374-1382
17. Binder DK, Steinhauser C (2006) Functional changes in astroglial cells in epilepsy. Glia 54:358-368 (Pubitemid 44422938)
18. Bottner M, Krieglstein K, Unsicker K (2000) The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J Neurochem 75:2227-2240
19. Brionne TC, Tesseur I, Masliah E, Wyss-Coray T (2003) Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 40:1133-1145 (Pubitemid 38032790)
20. Buckwalter MS, Yamane M, Coleman BS, Ormerod BK, Chin JT, Palmer T, Wyss-Coray T (2006) Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol 169:154-164
21. Buisson A, Nicole O, Docagne F, Sartelet H, Mackenzie ET, Vivien D (1998) Up-regulation of a serine protease inhibitor in astrocytes mediates the neuroprotective activity of transforming growth factor beta1. FASEB J 12:1683-1691 (Pubitemid 28553663)
22. Buisson A, Lesne S, Docagne F, Ali C, Nicole O, MacKenzie ET, Vivien D (2003) Transforming growth factor-beta and ischemic brain injury. Cell Mol Neurobiol 23:539-550 (Pubitemid 37071483)
23. Burton T, Liang B, Dibrov A, Amara F (2002) Transcriptional activation and increase in expression of Alzheimer's beta-amyloid precursor protein gene is mediated by TGF-beta in normal human astrocytes. Biochem Biophys Res Commun 295:702-712 (Pubitemid 34756907)
24. Cacheaux LP, Ivens S, David Y, Lakhter AJ, Bar-Klein G, Shapira M, Heinemann U, Friedman A, Kaufer D (2009) Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J Neurosci 29:8927-8935
25. Calvo CF, Fontaine RH, Soueid J, Tammela T, Makinen T, Alfaro-Cervello C, Bonnaud F, Miguez A, Benhaim L, Xu Y, Barallobre MJ, Moutkine I, Lyytikka J, Tatlisumak T, Pytowski B, Zalc B, Richardson W, Kessaris N, Garcia-Verdugo JM, Alitalo K, Eichmann A, Thomas JL (2011) Vascular endothelial growth factor receptor 3 directly regulates murine neurogenesis. Genes Dev 25:831-844
26. 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 (Pubitemid 40734410)
27. Carmeliet P, Tessier-Lavigne M (2005) Common mechanisms of nerve and blood vessel wiring. Nature 436:193-200 (Pubitemid 41021263)
28. Cheifetz S, Bellon T, Cales C, Vera S, Bernabeu C, Massague J, Letarte M (1992) Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 267:19027-19030
29. Choi DW (1992) Excitotoxic cell death. J Neurobiol 23:1261-1276
30. Choi ME, Ballermann BJ (1995) Inhibition of capillary morphogenesis and associated apoptosis by dominant negative mutant transforming growth factor-beta receptors. J Biol Chem 270:21144-21150
31. Clifford PM, Zarrabi S, Siu G, Kinsler KJ, Kosciuk MC, Venkataraman V, D'Andrea MR, Dinsmore S, Nagele RG (2007) Abeta peptides can enter the brain through a defective blood-brain barrier and bind selectively to neurons. Brain Res 1142:223-236 (Pubitemid 46413194)
32. Cortes-Canteli M, Paul J, Norris EH, Bronstein R, Ahn HJ, Zamolodchikov D, Bhuvanendran S, Fenz KM, Strickland S (2010) Fibrinogen and beta-amyloid association alters thrombosis and fibrinolysis: a possible contributing factor to Alzheimer's disease. Neuron 66:695-709
33. Cross AH, Waubant E (2011) MS and the B cell controversy. Biochim Biophys Acta 1812:231-238
34. Croxford AL, Kurschus FC, Waisman A (2011) Mouse models for multiple sclerosis: historical facts and future implications. Biochim Biophys Acta 1812:177-183
35. Csuka E, Morganti-Kossmann MC, Lenzlinger PM, Joller H, Trentz O, Kossmann T (1999) IL-10 levels in cerebrospinal fluid and serum of patients with severe traumatic brain injury: relationship to IL-6, TNF-alpha, TGF-beta1 and blood-brain barrier function. J Neuroimmunol 101:211-221 (Pubitemid 29516464)
36. Daneman R, Zhou L, Kebede AA, Barres BA (2010) Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 468:562-566
37. De Simone R, Niturad CE, De Nuccio C, Ajmone-Cat MA, Visentin S, Minghetti L (2010) TGF-beta and LPS modulate ADP-induced migration of microglial cells through P2Y1 and P2Y12 receptor expression. J Neurochem 115:450-459
38. Dhandapani KM, Hadman M, De Sevilla L, Wade MF, Mahesh VB, Brann DW (2003) Astrocyte protection of neurons: role of transforming growth factor-beta signaling via a c-Jun-AP-1 protective pathway. J Biol Chem 278:43329-43339 (Pubitemid 37345954)
39. Diamond B, Huerta PT, Mina-Osorio P, Kowal C, Volpe BT (2009) Losing your nerves? Maybe it's the antibodies. Nat Rev Immunol 9:449-456
40. Dohgu S, Takata F, Yamauchi A, Nakagawa S, Egawa T, Naito M, Tsuruo T, Sawada Y, Niwa M, Kataoka Y (2005) Brain pericytes contribute to the induction and up-regulation of blood-brain barrier functions through transforming growth factor-beta production. Brain Res 1038:208-215 (Pubitemid 40332685)
41. Doyle KP, Cekanaviciute E, Mamer LE, Buckwalter MS (2010) TGFbeta signaling in the brain increases with aging and signals to astrocytes and innate immune cells in the weeks after stroke. J Neuroinflammation 7:62
42. Faber-Elman A, Solomon A, Abraham JA, Marikovsky M, Schwartz M (1996) Involvement of wound-associated factors in rat brain astrocyte migratory response to axonal injury: in vitro simulation. J Clin Invest 97:162-171 (Pubitemid 26021707)
43. Ferrari G, Cook BD, Terushkin V, Pintucci G, Mignatti P (2009) Transforming growth factor-beta 1 (TGF-beta1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J Cell Physiol 219:449-458
44. Finch CE, Laping NJ, Morgan TE, Nichols NR, Pasinetti GM (1993) TGF-beta 1 is an organizer of responses to neurodegeneration. J Cell Biochem 53:314-322
45. Flanders KC, Lippa CF, Smith TW, Pollen DA, Sporn MB (1995) Altered expression of transforming growth factor-beta in Alzheimer's disease. Neurology 45:1561-1569
46. Flanders KC, Ren RF, Lippa CF (1998) Transforming growth factor-betas in neurodegenerative disease. Prog Neurobiol 54:71-85 (Pubitemid 28049820)
47. Frautschy SA, Yang F, Calderon L, Cole GM (1996) Rodent models of Alzheimer's disease: rat A beta infusion approaches to amyloid deposits. Neurobiol Aging 17:311-321 (Pubitemid 26167642)
48. Frautschy SA, Horn DL, Sigel JJ, Harris-White ME, Mendoza JJ, Yang F, Saido TC, Cole GM (1998) Protease inhibitor coinfusion with amyloid beta-protein results in enhanced deposition and toxicity in rat brain. J Neurosci 18:8311-8321 (Pubitemid 28465007)
49. Friedman A, Kaufer D, Heinemann U (2009) Blood-brain barrier breakdown-inducing astrocytic transformation: novel targets for the prevention of epilepsy. Epilepsy Res 85:142-149
50. Garcia CM, Darland DC, Massingham LJ, D'Amore PA (2004) Endothelial cell-astrocyte interactions and TGF beta are required for induction of blood-neural barrier properties. Brain Res Dev Brain Res 152:25-38 (Pubitemid 38993285)
51. Glebova NO, Ginty DD (2005) Growth and survival signals controlling sympathetic nervous system development. Annu Rev Neurosci 28:191-222 (Pubitemid 41098904)
52. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P (2002) Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J 21:1743-1753 (Pubitemid 34614630)
53. 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
54. Grainger DJ, Mosedale DE, Metcalfe JC (2000) TGF-beta in blood: a complex problem. Cytokine Growth Factor Rev 11:133-145
55. Gross CE, Bednar MM, Howard DB, Sporn MB (1993) Transforming growth factor-beta 1 reduces infarct size after experimental cerebral ischemia in a rabbit model. Stroke 24:558-562 (Pubitemid 23100743)
56. Gutcher I, Donkor MK, Ma Q, Rudensky AY, Flavell RA, Li MO (2011) Autocrine transforming growth factor-beta1 promotes in vivo Th17 cell differentiation. Immunity 34:396-408
57. Hardy J, Cullen K (2006) Amyloid at the blood vessel wall. Nat Med 12:756-757 (Pubitemid 44050057)
58. Harris-White ME, Chu T, Balverde Z, Sigel JJ, Flanders KC, Frautschy SA (1998) Effects of transforming growth factor-beta (isoforms 1-3) on amyloid-beta deposition, inflammation, and cell targeting in organotypic hippocampal slice cultures. J Neurosci 18:10366-10374 (Pubitemid 29016556)
59. Hawkins BT, Davis TP (2005) The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173-185 (Pubitemid 41043883)
60. Heinemann U, Gabriel S, Jauch R, Schulze K, Kivi A, Eilers A, Kovacs R, Lehmann TN (2000) Alterations of glial cell function in temporal lobe epilepsy. Epilepsia 41(Suppl 6):S185-S189
61. Heldin CH, Miyazono K, ten Dijke P (1997) TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465-471 (Pubitemid 28013118)
62. Henrich-Noack P, Prehn JH, Krieglstein J (1996) TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neuroprotective mechanisms. Stroke 27:1609-1614, discussion 1615
63. Honma Y, Araki T, Gianino S, Bruce A, Heuckeroth R, Johnson E, Milbrandt J (2002) Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35:267-282 (Pubitemid 34876730)
64. Hori S, Ohtsuki S, Hosoya K, Nakashima E, Terasaki T (2004) A pericyte-derived angiopoietin-1 multimeric complex induces occludin gene expression in brain capillary endothelial cells through Tie-2 activation in vitro. J Neurochem 89:503-513 (Pubitemid 38495998)
65. Hsieh HL, Wang HH, Wu WB, Chu PJ, Yang CM (2010) Transforming growth factor-beta1 induces matrix metalloproteinase-9 and cell migration in astrocytes: roles of ROS-dependent ERK-and JNK-NF-kappaB pathways. J Neuroinflammation 7:88
66. 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 (Pubitemid 26160991)
67. Iadecola C, Nedergaard M (2007) Glial regulation of the cerebral microvasculature. Nat Neurosci 10:1369-1376 (Pubitemid 350014688)
68. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, Seiffert E, Heinemann U, Friedman A (2007) TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 130:535-547 (Pubitemid 46181106)
69. Jager A, Dardalhon V, Sobel RA, Bettelli E, Kuchroo VK (2009) Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J Immunol 183:7169-7177
70. Janzer RC, Raff MC (1987) Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325:253-257 (Pubitemid 17049884)
71. Kim ES, Kim RS, Ren RF, Hawver DB, Flanders KC (1998) Transforming growth factor-beta inhibits apoptosis induced by beta-amyloid peptide fragment 25-35 in cultured neuronal cells. Brain Res Mol Brain Res 62:122-130 (Pubitemid 29010379)
72. Kirk J, Plumb J, Mirakhur M, McQuaid S (2003) Tight junctional abnormality in multiple sclerosis white matter affects all calibres of vessel and is associated with blood-brain barrier leakage and active demyelination. J Pathol 201:319-327 (Pubitemid 37258943)
73. Kohta M, Kohmura E, Yamashita T (2009) Inhibition of TGF-beta1 promotes functional recovery after spinal cord injury. Neurosci Res 65:393-401
74. Kojima T, Hirota Y, Ema M, Takahashi S, Miyoshi I, Okano H, Sawamoto K (2010) Subventricular zone-derived neural progenitor cells migrate along a blood vessel scaffold toward the poststroke striatum. Stem Cells 28:545-554
75. Kokovay E, Goderie S, Wang Y, Lotz S, Lin G, Sun Y, Roysam B, Shen Q, Temple S (2010) Adult SVZ lineage cells home to and leave the vascular niche via differential responses to SDF1/CXCR4 signaling. Cell Stem Cell 7:163-173
76. Konde E, Bourgeois B, Tellier-Lebegue C, Wu W, Perez J, Caputo S, Attanda W, Gasparini S, Charbonnier JB, Gilquin B, Worman HJ, Zinn-Justin S (2010) Structural analysis of the Smad2-MAN1 interaction that regulates transforming growth factor-beta signaling at the inner nuclear membrane. Biochemistry 49:8020-8032
77. Konig HG, Kogel D, Rami A, Prehn JH (2005) TGF-{beta}1 activates two distinct type I receptors in neurons: implications for neuronal NF-{kappa}B signaling. J Cell Biol 168:1077-1086
78. Kose N, Asashima T, Muta M, Iizasa H, Sai Y, Terasaki T, Nakashima E (2007) Altered expression of basement membrane-related molecules in rat brain pericyte, endothelial, and astrocyte cell lines after transforming growth factor-beta1 treatment. Drug Metab Pharmacokinet 22:255-266
79. Krieglstein K, Suter-Crazzolara C, Unsicker K (1995) Development of mesencephalic dopaminergic neurons and the transforming growth factor-beta superfamily. J Neural Transm Suppl 46:209-216 (Pubitemid 26046561)
80. Krupinski J, Kumar P, Kumar S, Kaluza J (1996) Increased expression of TGF-beta 1 in brain tissue after ischemic stroke in humans. Stroke 27:852-857 (Pubitemid 26142515)
81. Kuruvilla R, Zweifel LS, Glebova NO, Lonze BE, Valdez G, Ye H, Ginty DD (2004) A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118:243-255 (Pubitemid 38962579)
82. Lagord C, Berry M, Logan A (2002) Expression of TGFbeta2 but not TGFbeta1 correlates with the deposition of scar tissue in the lesioned spinal cord. Mol Cell Neurosci 20:69-92 (Pubitemid 34634329)
83. Laouar Y, Town T, Jeng D, Tran E, Wan Y, Kuchroo VK, Flavell RA (2008) TGF-beta signaling in dendritic cells is a prerequisite for the control of autoimmune encephalomyelitis. Proc Natl Acad Sci USA 105:10865-10870
84. Lehrmann E, Kiefer R, Christensen T, Toyka KV, Zimmer J, Diemer NH, Hartung HP, Finsen B (1998) Microglia and macrophages are major sources of locally produced transforming growth factor-beta1 after transient middle cerebral artery occlusion in rats. Glia 24:437-448 (Pubitemid 28494763)
85. Lenzlinger PM, Morganti-Kossmann MC, Laurer HL, McIntosh TK (2001) The duality of the inflammatory response to traumatic brain injury. Mol Neurobiol 24:169-181 (Pubitemid 34066684)
86. Lesne S, Docagne F, Gabriel C, Liot G, Lahiri DK, Buee L, Plawinski L, Delacourte A, MacKenzie ET, Buisson A, Vivien D (2003) Transforming growth factor-beta 1 potentiates amyloid-beta generation in astrocytes and in transgenic mice. J Biol Chem 278:18408-18418
87. Li MO, Flavell RA (2008) TGF-beta: a master of all T cell trades. Cell 134:392-404
88. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA (2006) Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol 24:99-146
89. Lindholm D, Castren E, Kiefer R, Zafra F, Thoenen H (1992) Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J Cell Biol 117:395-400
90. Lippa CF, Smith TW, Flanders KC (1995) Transforming growth factor-beta: neuronal and glial expression in CNS degenerative diseases. Neurodegeneration 4:425-432 (Pubitemid 26016588)
91. Louissaint A Jr, Rao S, Leventhal C, Goldman SA (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34:945-960 (Pubitemid 34722284)
92. Luo J, Ho PP, Buckwalter MS, Hsu T, Lee LY, Zhang H, Kim DK, Kim SJ, Gambhir SS, Steinman L, Wyss-Coray T (2007) Gliadependent TGF-beta signaling, acting independently of the TH17 pathway, is critical for initiation of murine autoimmune encephalomyelitis. J Clin Invest 117:3306-3315 (Pubitemid 350096987)
93. Madri JA, Pratt BM, Tucker AM (1988) Phenotypic modulation of endothelial cells by transforming growth factor-beta depends upon the composition and organization of the extracellular matrix. J Cell Biol 106:1375-1384
94. Mahesh VB, Dhandapani KM, Brann DW (2006) Role of astrocytes in reproduction and neuroprotection. Mol Cell Endocrinol 246:1-9 (Pubitemid 43238391)
95. Makita T, Sucov HM, Gariepy CE, Yanagisawa M, Ginty DD (2008) Endothelins are vascular-derived axonal guidance cues for developing sympathetic neurons. Nature 452:759-763 (Pubitemid 351521084)
96. Marchi N, Angelov L, Masaryk T, Fazio V, Granata T, Hernandez N, Hallene K, Diglaw T, Franic L, Najm I, Janigro D (2007) Seizure-promoting effect of blood-brain barrier disruption. Epilepsia 48:732-742 (Pubitemid 46587627)
97. 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 (Pubitemid 350033973)
98. Massague J (1998) TGF-beta signal transduction. Annu Rev Biochem 67:753-791
99. Massague J (2000) How cells read TGF-beta signals. Nat Rev Mol Cell Biol 1:169-178
100. Massague J (2008) TGFbeta in cancer. Cell 134:215-230
101. Massague J, Seoane J, Wotton D (2005) Smad transcription factors. Genes Dev 19:2783-2810 (Pubitemid 41739965)
102. Mehler MF, Mabie PC, Zhang D, Kessler JA (1997) Bone morphogenetic proteins in the nervous system. Trends Neurosci 20:309-317 (Pubitemid 27348741)
103. 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 (Pubitemid 32695196)
104. Mishra L, Marshall B (2006) Adaptor proteins and ubiquinators in TGF-beta signaling. Cytokine Growth Factor Rev 17:75-87 (Pubitemid 43117517)
105. 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
106. Moon LD, Fawcett JW (2001) Reduction in CNS scar formation without concomitant increase in axon regeneration following treatment of adult rat brain with a combination of antibodies to TGFbeta1 and beta2. Eur J Neurosci 14:1667-1677 (Pubitemid 35478035)
107. Morgan L, Shah B, Rivers LE, Barden L, Groom AJ, Chung R, Higazi D, Desmond H, Smith T, Staddon JM (2007) Inflammation and dephosphorylation of the tight junction protein occludin in an experimental model of multiple sclerosis. Neuroscience 147:664-673 (Pubitemid 46990645)
108. Morganti-Kossmann MC, Hans VH, Lenzlinger PM, Dubs R, Ludwig E, Trentz O, Kossmann T (1999) TGF-beta is elevated in the CSF of patients with severe traumatic brain injuries and parallels blood-brain barrier function. J Neurotrauma 16:617-628 (Pubitemid 29350520)
109. Mousseau DD, Chapelsky S, De Crescenzo G, Kirkitadze MD, Magoon J, Inoue S, Teplow DB, O'Connor-McCourt MD (2003) A direct interaction between transforming growth factor (TGF)-betas and amyloid-beta protein affects fibrillogenesis in a TGF-beta receptor-independent manner. J Biol Chem 278:38715-38722 (Pubitemid 37221769)
110. Mu Y, Gudey SK, Landstrom M (2011) Non-Smad signaling pathways. Cell Tissue Res (in press)
111. Mukasa R, Balasubramani A, Lee YK, Whitley SK, Weaver BT, Shibata Y, Crawford GE, Hatton RD, Weaver CT (2010) Epigenetic instability of cytokine and transcription factor gene loci underlies plasticity of the T helper 17 cell lineage. Immunity 32:616-627
112. Murphy KM, Stockinger B (2010) Effector T cell plasticity: flexibility in the face of changing circumstances. Nat Immunol 11:674-680
113. Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523-530 (Pubitemid 37176906)
114. Nishimura SL, Boylen KP, Einheber S, Milner TA, Ramos DM, Pytela R (1998) Synaptic and glial localization of the integrin alphavbeta8 in mouse and rat brain. Brain Res 791:271-282 (Pubitemid 28238335)
115. Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26:13007-13016 (Pubitemid 44954619)
116. Padua D, Massague J (2009) Roles of TGFbeta in metastasis. Cell Res 19:89-102
117. Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479-494
118. Pardali E, Goumans MJ, ten Dijke P (2010) Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol 20:556-567
119. 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 (Pubitemid 47236333)
120. Peress NS, Perillo E (1995) Differential expression of TGF-beta 1, 2 and 3 isotypes in Alzheimer's disease: a comparative immunohistochemical study with cerebral infarction, aged human and mouse control brains. J Neuropathol Exp Neurol 54:802-811
121. Petermann F, Korn T (2011) Cytokines and effector T cell subsets causing autoimmune CNS disease. FEBS Lett (in press)
122. Pollman MJ, Naumovski L, Gibbons GH (1999a) Vascular cell apoptosis: cell type-specific modulation by transforming growth factor-beta1 in endothelial cells versus smooth muscle cells. Circulation 99:2019-2026 (Pubitemid 29183900)
123. Pollman MJ, Naumovski L, Gibbons GH (1999b) Endothelial cell apoptosis in capillary network remodeling. J Cell Physiol 178:359-370 (Pubitemid 29070344)
124. Popovich PG, Horner PJ, Mullin BB, Stokes BT (1996) A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury. Exp Neurol 142:258-275 (Pubitemid 26414059)
125. Prehn JH, Backhauss C, Krieglstein J (1993) Transforming growth factor-beta 1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse neocortex from ischemic injury in vivo. J Cereb Blood Flow Metab 13:521-525 (Pubitemid 23129406)
126. Rifkin DB (2005) Latent transforming growth factor-beta (TGF-beta) binding proteins: orchestrators of TGF-beta availability. J Biol Chem 280:7409-7412
127. Rivest S (2009) Regulation of innate immune responses in the brain. Nat Rev Immunol 9:429-439
128. Robel S, Berninger B, Gotz M (2011) The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 12:88-104
129. Roberts AB, Sporn MB, Assoian RK, Smith JM, Roche NS, Wakefield LM, Heine UI, Liotta LA, Falanga V, Kehrl JH et al (1986) Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc Natl Acad Sci USA 83:4167-4171 (Pubitemid 16057012)
130. Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M (2006) Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J Cereb Blood Flow Metab 26:125-134 (Pubitemid 41818076)
131. Ruocco A, Nicole O, Docagne F, Ali C, Chazalviel L, Komesli S, Yablonsky F, Roussel S, MacKenzie ET, Vivien D, Buisson A (1999) A transforming growth factor-beta antagonist unmasks the neuroprotective role of this endogenous cytokine in excitotoxic and ischemic brain injury. J Cereb Blood Flow Metab 19:1345-1353 (Pubitemid 30013626)
132. Sato Y, Tsuboi R, Lyons R,Moses H, Rifkin DB (1990) Characterization of the activation of latent TGF-beta by co-cultures of endothelial cells and pericytes or smooth muscle cells: a self-regulating system. J Cell Biol 111:757-763
133. Schachtrup C, Lu P, Jones LL, Lee JK, Lu J, Sachs BD, Zheng B, Akassoglou K (2007) Fibrinogen inhibits neurite outgrowth via beta 3 integrin-mediated phosphorylation of the EGF receptor. Proc Natl Acad Sci USA 104:11814-11819 (Pubitemid 47175095)
134. Schachtrup C, Ryu JK, Helmrick MJ, Vagena E, Galanakis DK, Degen JL, Margolis RU, Akassoglou K (2010) Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J Neurosci 30:5843-5854
135. Schachtrup C, Le Moan N, Passino MA, Akassoglou K (2011) Hepatic stellate cells and astrocytes: stars of scar formation and tissue repair. Cell Cycle 10:1764-1771
136. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, Friedman A (2004) Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 24:7829-7836 (Pubitemid 39215686)
137. Shi Y, Massague J (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685-700 (Pubitemid 36724933)
138. Shi M, Zhu J, Wang R, Chen X, Mi L, Walz T, Springer TA (2011) Latent TGF-beta structure and activation. Nature 474:343-349
139. Shih SC, Ju M, Liu N, Mo JR, Ney JJ, Smith LE (2003) Transforming growth factor beta1 induction of vascular endothelial growth factor receptor 1: mechanism of pericyte-induced vascular survival in vivo. Proc Natl Acad Sci USA 100:15859-15864 (Pubitemid 38021080)
140. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156 (Pubitemid 38160289)
141. Stipursky J, Gomes FC (2007) TGF-beta1/SMAD signaling induces astrocyte fate commitment in vitro: implications for radial glia development. Glia 55:1023-1033 (Pubitemid 47066742)
142. Tabata T, Kawakatsu H, Maidji E, Sakai T, Sakai K, Fang-Hoover J, Aiba M, Sheppard D, Pereira L (2008) Induction of an epithelial integrin alphavbeta6 in human cytomegalovirus-infected endothelial cells leads to activation of transforming growth factorbeta1 and increased collagen production. Am J Pathol 172:1127-1140 (Pubitemid 351520008)
143. Tate CC, Garcia AJ, LaPlaca MC (2007) Plasma fibronectin is neuroprotective following traumatic brain injury. Exp Neurol 207:13-22 (Pubitemid 47332478)
144. Tatti O, Vehvilainen P, Lehti K, Keski-Oja J (2008) MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp Cell Res 314:2501-2514
145. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279-288
146. 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 (Pubitemid 44684491)
147. Thored P, Wood J, Arvidsson A, Cammenga J, Kokaia Z, Lindvall O (2007) Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke. Stroke 38:3032-3039 (Pubitemid 350035699)
148. Town T, Laouar Y, Pittenger C, Mori T, Szekely CA, Tan J, Duman RS, Flavell RA (2008) Blocking TGF-beta-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat Med 14:681-687 (Pubitemid 351809551)
149. Tran ND, Schreiber SS, Fisher M (1998) Astrocyte regulation of endothelial tissue plasminogen activator in a blood-brain barrier model. J Cereb Blood Flow Metab 18:1316-1324 (Pubitemid 28559679)
150. Tran ND, Correale J, Schreiber SS, Fisher M (1999) Transforming growth
151. Unsicker K, Strelau J (2000) Functions of transforming growth factor-beta isoforms in the nervous system. Cues based on localization and experimental in vitro and in vivo evidence. Eur J Biochem 267:6972-6975 (Pubitemid 32009437)
152. Unsicker K, Krieglstein K (2002) TGF-betas and their roles in the regulation of neuron survival. Adv Exp Med Biol 513:353-374 (Pubitemid 36332414)
153. Unsold C, Hyytiainen 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 (Pubitemid 32118068)
154. Unterberg AW, Stroop R, Thomale UW, Kiening KL, Pauser S, Vollmann W (1997) Characterisation of brain edema following "controlled cortical impact injury" in rats. Acta Neurochir Suppl 70:106-108 (Pubitemid 127502066)
155. van der Wal EA, Gomez-Pinilla F, Cotman CW (1993) Transforming growth factor-beta 1 is in plaques in Alzheimer and Down pathologies. Neuroreport 4:69-72 (Pubitemid 23066393)
156. Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB, Roberts AB (1988) Transforming growth factor beta 1 positively regulates its own expression in normal and transformed cells. J Biol Chem 263:7741-7746
157. van Vliet EA, da Costa AS, Redeker S, van Schaik R, Aronica E, Gorter JA (2007) Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 130:521-534
158. Veldhoen M, Hocking RJ, Flavell RA, Stockinger B (2006) Signals mediated by transforming growth factor-beta initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat Immunol 7:1151-1156 (Pubitemid 44594310)
159. Veldhoen M, Uyttenhove C, van Snick J, Helmby H, Westendorf A, Buer J, Martin B, Wilhelm C, Stockinger B (2008) Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol 9:1341-1346
160. Vergeli M, Mazzanti B, Ballerini C, Gran B, Amaducci L, Massacesi L (1995) Transforming growth factor-beta 1 inhibits the proliferation of rat astrocytes induced by serum and growth factors. J Neurosci Res 40:127-133
161. Vos CM, Geurts JJ, Montagne L, van Haastert ES, Bo L, van der Valk P, Barkhof F, de Vries HE (2005) Blood-brain barrier alterations in both focal and diffuse abnormalities on postmortem MRI in multiple sclerosis. Neurobiol Dis 20:953-960 (Pubitemid 41619370)
162. Wang Y, Symes AJ (2010) Smad3 deficiency reduces neurogenesis in adult mice. J Mol Neurosci 41:383-396
163. Wang Y, Moges H, Bharucha Y, Symes A (2007) Smad3 null mice display more rapid wound closure and reduced scar formation after a stab wound to the cerebral cortex. Exp Neurol 203:168-184 (Pubitemid 44821175)
164. 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
165. Worthington JJ, Klementowicz JE, Travis MA (2011) TGFbeta: a sleeping giant awoken by integrins. Trends Biochem Sci 36:47-54
166. Wyss-Coray T, Feng L, Masliah E, Ruppe MD, Lee HS, Toggas SM, Rockenstein EM, Mucke L (1995) Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol 147:53-67
167. Wyss-Coray T, Borrow P, Brooker MJ, Mucke L (1997a) Astroglial overproduction of TGF-beta 1 enhances inflammatory central nervous system disease in transgenic mice. J Neuroimmunol 77:45-50 (Pubitemid 27286375)
168. Wyss-Coray T, Masliah E, Mallory M, McConlogue L, Johnson-Wood K, Lin C, Mucke L (1997b) Amyloidogenic role of cytokine TGF-beta1 in transgenic mice and in Alzheimer's disease. Nature 389:603-606 (Pubitemid 27446177)
169. Wyss-Coray T, Lin C, Sanan DA, Mucke L, Masliah E (2000) Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am J Pathol 156:139-150 (Pubitemid 30644446)
170. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, Masliah E, Mucke L (2001) TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 7:612-618 (Pubitemid 32448330)
171. Xiao BG, Zhang GX, Ma CG, Link H (1996) Transforming growth factor-beta 1 (TGF-beta1)-mediated inhibition of glial cell proliferation and down-regulation of intercellular adhesion molecule-1 (ICAM-1) are interrupted by interferon-gamma (IFN-gamma). Clin Exp Immunol 103:475-481
172. Yamashita T, Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K (2006) Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26:6627-6636 (Pubitemid 44318344)
173. Yang EY, Moses HL (1990) Transforming growth factor beta 1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane. J Cell Biol 111:731-741
174. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp M (2004) Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24:441-448 (Pubitemid 38452235)
175. Zhang RL, Chopp M, Gregg SR, Toh Y, Roberts C, Letourneau Y, Buller B, Jia L, Davarani SPN, Zhang ZG (2009) Patterns and dynamics of subventricular zone neuroblast migration in the ischemic striatum of the adult mouse. J Cereb Blood Flow Metab 29:1240-1250
176. Zhong Z, Deane R, Ali Z, Parisi M, Shapovalov Y, O'Banion MK, Stojanovic K, Sagare A, Boillee S, Cleveland DW, Zlokovic BV (2008) ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci 11:420-422 (Pubitemid 351441888)
177. Zhu J, Paul WE (2008) CD4 T cells: fates, functions, and faults. Blood 112:1557-1569
178. Zhu J, Motejlek K, Wang D, Zang K, Schmidt A, Reichardt LF (2002a) beta8 integrins are required for vascular morphogenesis in mouse embryos. Development 129:2891-2903 (Pubitemid 34874268)
179. Zhu Y, Yang GY, Ahlemeyer B, Pang L, Che XM, Culmsee C, Klumpp S, Krieglstein J (2002b) Transforming growth factor-beta 1 increases bad phosphorylation and protects neurons against damage. J Neurosci 22:3898-3909 (Pubitemid 37465698)
180. Zhu Y, Culmsee C, Klumpp S, Krieglstein J (2004) Neuroprotection by transforming growth factor-beta1 involves activation of nuclear factor-kappaB through phosphatidylinositol-3-OH kinase/Akt and mitogen-activated protein kinase-extracellular-signal regulated kinase1,2 signaling pathways. Neuroscience 123:897-906 (Pubitemid 38130100)
181. Zlokovic BV (2005) Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci 28:202-208
182. Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57:178-201