Potential neuroprotective role of transforming growth factor β1 (TGFβ1) in the brain

References

• Lindholm D, Castren E, Kiefer R, Transforming growth factor-beta 1 in the rat brain: increase after injury and inhibition of astrocyte proliferation. J Cell Biol 1992;117:395–400.
   PubMed Web of Science ®Google Scholar
• Chin J, Angers A, Cleary LJ, TGF-beta1 in Aplysia: role in long-term changes in the excitability of sensory neurons and distribution of TbetaR-II-like immunoreactivity. Learn Mem 1999;6:317–30.
   PubMed Web of Science ®Google Scholar
• Herpin A, Lelong C, Favrel P. Transforming growth factor-beta-related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev Comp Immunol 2004;28:461–85.
   PubMed Web of Science ®Google Scholar
• Burt DW, Law AS. Evolution of the transforming growth factor-beta superfamily. Prog Growth Factor Res 1994;5:99–118.
   PubMedGoogle Scholar
• Lefebvre PP, Martin D, Staecker H, TGF beta 1 expression is initiated in adult auditory neurons by sectioning of the auditory nerve. Neuroreport 1992;3:295–8.
   PubMed Web of Science ®Google Scholar
• da Cunha A, Vitkovic L. Transforming growth factor-beta 1 (TGF-beta 1) expression and regulation in rat cortical astrocytes. J Neuroimmunol 1992;36:157–69.
   PubMed Web of Science ®Google Scholar
• Lin AH, Luo J, Mondshein LH, Global analysis of Smad2/3-dependent TGF-beta signaling in living mice reveals prominent tissue-specific responses to injury. J Immunol 2005;175:547–54.
   PubMed Web of Science ®Google Scholar
• Bae JJ, Xiang YY, Martinez-Canabal A, Increased transforming growth factor-beta1 modulates glutamate receptor expression in the hippocampus. Int J Physiol Pathophysiol Pharmacol 2011;3:9–20.
   PubMedGoogle Scholar
• Martinez-Canabal A, Wheeler AL, Sarkis D, Chronic over-expression of TGFbeta1 alters hippocampal structure and causes learning deficits. Hippocampus 2013;23:1198–211.
   PubMed Web of Science ®Google Scholar
• Battaglia G, Cannella M, Riozzi B, Early defect of transforming growth factor beta1 formation in Huntington's disease. J Cell Mol Med 2011;15:555–71.
   PubMed Web of Science ®Google Scholar
• Di Pardo A, Alberti S, Maglione V, Changes of peripheral TGF-beta1 depend on monocytes-derived macrophages in Huntington disease. Mol Brain 2013;6:55.
   PubMed Web of Science ®Google Scholar
• Wilcox JN, Derynck R. Localization of cells synthesizing transforming growth factor-alpha mRNA in the mouse brain. J Neurosci 1988;8:1901–4.
   PubMed Web of Science ®Google Scholar
• Maharaj AS, Walshe TE, Saint-Geniez M, VEGF and TGF-beta are required for the maintenance of the choroid plexus and ependyma. J Exp Med 2008;205:491–501.
   PubMed Web of Science ®Google Scholar
• Vincze C, Pal G, Wappler EA, Distribution of mRNAs encoding transforming growth factors-beta1, -2, and -3 in the intact rat brain and after experimentally induced focal ischemia. J Comp Neurol 2010;518:3752–70.
   PubMed Web of Science ®Google Scholar
• Nichols NR, Finch CE. Transforming growth factor-beta1 mRNA decreases in brain in response to glucocorticoid treatment of adrenalectomized rats. Mol Cell Neurosci 1991;2:221–7.
   PubMedGoogle Scholar
• Dheen ST, Kaur C, Ling EA. Microglial activation and its implications in the brain diseases. Curr Med Chem 2007;14:1189–97.
   PubMed Web of Science ®Google Scholar
• von Zahn J, Moller T, Kettenmann H, Nolte C. Microglial phagocytosis is modulated by pro- and anti-inflammatory cytokines. Neuroreport 1997;8:3851–6.
   PubMed Web of Science ®Google Scholar
• O'Keefe GM, Nguyen VT, Benveniste EN. Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGF-beta, IL-4, IL-13 and IL-10. Eur J Immunol 1999;29:1275–85.
   PubMed Web of Science ®Google Scholar
• Hailer NP, Heppner FL, Haas D, Nitsch R. Astrocytic factors deactivate antigen presenting cells that invade the central nervous system. Brain Pathol 1998;8:459–74.
   PubMed Web of Science ®Google Scholar
• Milner R, Campbell IL. The extracellular matrix and cytokines regulate microglial integrin expression and activation. J Immunol 2003;170:3850–8.
   PubMed Web of Science ®Google Scholar
• Basu A, Krady JK, Enterline JR, Levison SW. Transforming growth factor beta1 prevents IL-1beta-induced microglial activation, whereas TNFalpha- and IL-6-stimulated activation are not antagonized. Glia 2002;40:109–20.
   PubMed Web of Science ®Google Scholar
• Herrera-Molina R, von Bernhardi R. Transforming growth factor-beta 1 produced by hippocampal cells modulates microglial reactivity in culture. Neurobiol Dis 2005;19:229–36.
   PubMed Web of Science ®Google Scholar
• Jung B, Kim MO, Yun SJ, Lee EH. Down-regulation of the expression of rat inhibitor-of-apoptosis protein-1 and -3 during transforming growth factor-beta1-mediated apoptosis in rat brain microglia. Neuroreport 2003;14:857–60.
   PubMed Web of Science ®Google Scholar
• Xiao BG, Bai XF, Zhang GX, Link H. Transforming growth factor-beta1 induces apoptosis of rat microglia without relation to bcl-2 oncoprotein expression. Neurosci Lett 1997;226:71–4.
   PubMed Web of Science ®Google Scholar
• Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 2009;32:638–47.
   PubMed Web of Science ®Google Scholar
• Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol 2010;119:7–35.
   PubMed Web of Science ®Google Scholar
• Reilly JF, Maher PA, Kumari VG. Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2. Glia 1998;22:202–10.
   PubMed Web of Science ®Google Scholar
• de Sampaio e Spohr TC, Martinez R, da Silva EF, Neuro-glia interaction effects on GFAP gene: a novel role for transforming growth factor-beta1. Eur J Neurosci 2002;16:2059–69.
   PubMed Web of Science ®Google Scholar
• Sousa Vde O, Romao L, Neto VM, Gomes FC. Glial fibrillary acidic protein gene promoter is differently modulated by transforming growth factor-beta 1 in astrocytes from distinct brain regions. Eur J Neurosci 2004;19:1721–30.
   PubMed Web of Science ®Google Scholar
• Docagne F, Nicole O, Marti HH, Transforming growth factor-beta1 as a regulator of the serpins/t-PA axis in cerebral ischemia. Faseb J 1999;13:1315–24.
   PubMed Web of Science ®Google Scholar
• Jeon H, Kim JH, Kim JH, Plasminogen activator inhibitor type 1 regulates microglial motility and phagocytic activity. J Neuroinflammation 2012;9:149.
   PubMed Web of Science ®Google Scholar
• Wang YF, Tsirka SE, Strickland S, Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 1998;4:228–31.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Mohsenzadegan M. TGF-beta as a promising option in the treatment of multiple sclerosis. Neuropharmacology 2009;56:929–36.
   PubMed Web of Science ®Google Scholar
• Diemel LT, Jackson SJ, Cuzner ML. Role for TGF-beta1, FGF-2 and PDGF-AA in a myelination of CNS aggregate cultures enriched with macrophages. J Neurosci Res 2003;74: 858–67.
   PubMed Web of Science ®Google Scholar
• Racke MK, Dhib-Jalbut S, Cannella B, Prevention and treatment of chronic relapsing experimental allergic encephalomyelitis by transforming growth factor-beta 1. J Immunol 1991;146:3012–17.
   PubMed Web of Science ®Google Scholar
• Johns LD, Flanders KC, Ranges GE, Sriram S. Successful treatment of experimental allergic encephalomyelitis with transforming growth factor-beta 1. J Immunol 1991;147:1792–6.
   PubMed Web of Science ®Google Scholar
• Luo J, Ho PP, Buckwalter MS, Glia-dependent TGF-beta signaling, acting independently of the TH17 pathway, is critical for initiation of murine autoimmune encephalomyelitis. J Clin Invest 2007;117:3306–15.
   PubMed Web of Science ®Google Scholar
• Xiao BG, Zhu WH, Lu CZ. The presence of GM-CSF and IL-4 interferes with effect of TGF-beta1 on antigen presenting cells in patients with multiple sclerosis and in rats with experimental autoimmune encephalomyelitis. Cell Immunol 2007;249: 30–6.
   PubMed Web of Science ®Google Scholar
• Houi K, Kobayashi T, Kato S, Increased plasma TGF-beta1 in patients with amyotrophic lateral sclerosis. Acta Neurol Scand 2002;106:299–301.
   PubMed Web of Science ®Google Scholar
• Katsuno M, Adachi H, Banno H, Transforming growth factor-beta signaling in motor neuron diseases. Curr Mol Med 2011;11:48–56.
   PubMedGoogle Scholar
• Ilzecka J, Stelmasiak Z, Dobosz B. Transforming growth factor-beta 1 (TGF-Beta 1) in patients with amyotrophic lateral sclerosis. Cytokine 2002;20:239–43.
   PubMed Web of Science ®Google Scholar
• Hensley K, Fedynyshyn J, Ferrell S, Message and protein-level elevation of tumor necrosis factor alpha (TNF alpha) and TNF alpha-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 2003;14:74–80.
   PubMed Web of Science ®Google Scholar
• Mogi M, Harada M, Kondo T, Transforming growth factor-beta 1 levels are elevated in the striatum and in ventricular cerebrospinal fluid in Parkinson's disease. Neurosci Lett 1995;193:129–32.
   PubMed Web of Science ®Google Scholar
• Mogi M, Harada M, Kondo T, Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 1994;180:147–50.
   PubMed Web of Science ®Google Scholar
• Sanchez-Capelo A, Colin P, Guibert B, Transforming growth factor beta1 overexpression in the nigrostriatal system increases the dopaminergic deficit of MPTP mice. Mol Cell Neurosci 2003;23:614–25.
   PubMed Web of Science ®Google Scholar
• Lin LF, Doherty DH, Lile JD, GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993;260:1130–2.
   PubMed Web of Science ®Google Scholar
• Tomac A, Lindqvist E, Lin LF, Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 1995;373:335–9.
   PubMed Web of Science ®Google Scholar
• Wyss-Coray T, Masliah E, Mallory M, Amyloidogenic role of cytokine TGF-beta1 in transgenic mice and in Alzheimer's disease. Nature 1997;389:603–6.
   PubMed Web of Science ®Google Scholar
• Zetterberg H, Andreasen N, Blennow K. Increased cerebrospinal fluid levels of transforming growth factor-beta1 in Alzheimer's disease. Neurosci Lett 2004;367:194–6.
   PubMed Web of Science ®Google Scholar
• Apelt J, Schliebs R. Beta-amyloid-induced glial expression of both pro- and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain Res 2001;894:21–30.
   PubMed Web of Science ®Google Scholar
• Hamaguchi T, Okino S, Sodeyama N, Association of a polymorphism of the transforming growth factor-beta1 gene with cerebral amyloid angiopathy. J Neurol Neurosurg Psychiatry 2005;76:696–9.
   PubMed Web of Science ®Google Scholar
• Araria-Goumidi L, Lambert JC, Mann DM, Association study of three polymorphisms of TGF-beta1 gene with Alzheimer's disease. J Neurol Neurosurg Psychiatry 2002;73:62–4.
   PubMed Web of Science ®Google Scholar
• Luedecking EK, DeKosky ST, Mehdi H, Analysis of genetic polymorphisms in the transforming growth factor-beta1 gene and the risk of Alzheimer's disease. Hum Genet 2000;106:565–9.
   PubMed Web of Science ®Google Scholar
• Stoeck K, Bodemer M, Zerr I. Pro- and anti-inflammatory cytokines in the CSF of patients with Creutzfeldt-Jakob disease. J Neuroimmunol 2006;172:175–81.
   PubMed Web of Science ®Google Scholar
• Baker CA, Lu ZY, Zaitsev I, Manuelidis L. Microglial activation varies in different models of Creutzfeldt-Jakob disease. J Virol 1999;73:5089–97.
   PubMed Web of Science ®Google Scholar
• Battaglia G, Cannella M, Riozzi B, Early defect of transforming growth factor beta-1 formation in Huntington's disease. J Cell Mol Med 2011;15:555–71.
   PubMed Web of Science ®Google Scholar
• Buisson A, Lesne S, Docagne F, Transforming growth factor-beta and ischemic brain injury. Cell Mol Neurobiol 2003;23:539–50.
   PubMed Web of Science ®Google Scholar
• Henrich-Noack P, Prehn JH, Krieglstein J. TGF-beta 1 protects hippocampal neurons against degeneration caused by transient global ischemia. Dose-response relationship and potential neuroprotective mechanisms. Stroke 1996;27:1609–14; discussion 1615.
   PubMed Web of Science ®Google Scholar
• Kim Y, Lee C. The gene encoding transforming growth factor beta 1 confers risk of ischemic stroke and vascular dementia. Stroke 2006;37:2843–5.
   PubMed Web of Science ®Google Scholar
• Lehrmann E, Kiefer R, Finsen B, Cytokines in cerebral ischemia: expression of transforming growth factor beta-1 (TGF-beta 1) mRNA in the postischemic adult rat hippocampus. Exp Neurol 1995;131:114–23.
   PubMed Web of Science ®Google Scholar
• Lehrmann E, Kiefer R, Christensen T, Microglia and macrophages are major sources of locally produced transforming growth factor-beta1 after transient middle cerebral artery occlusion in rats. Glia 1998;24:437–48.
   PubMed Web of Science ®Google Scholar
• Ruocco A, Nicole O, Docagne F, 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 1999;19:1345–53.
   PubMed Web of Science ®Google Scholar
• Westerhausen DR, Jr., Hopkins WE, Billadello JJ. Multiple transforming growth factor-beta-inducible elements regulate expression of the plasminogen activator inhibitor type-1 gene in Hep G2 cells. J Biol Chem 1991;266:1092–1100.
   PubMed Web of Science ®Google Scholar
• Buisson A, Nicole O, Docagne F, Up-regulation of a serine protease inhibitor in astrocytes mediates the neuroprotective activity of transforming growth factor beta1. Faseb J 1998;12:1683–91.
   PubMed Web of Science ®Google Scholar
• Nicole O, Docagne F, Ali C, The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med 2001;7:59–64.
   PubMed Web of Science ®Google Scholar
• Lin CH, Cheng FC, Lu YZ, Protection of ischemic brain cells is dependent on astrocyte-derived growth factors and their receptors. Exp Neurol 2006;201:225–33.
   PubMed Web of Science ®Google Scholar
• Shull MM, Ormsby I, Kier AB, Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992;359:693–9.
   PubMed Web of Science ®Google Scholar
• Kulkarni AB, Huh CG, Becker D, Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 1993;90:770–4.
   PubMed Web of Science ®Google Scholar
• Brionne TC, Tesseur I, Masliah E, Wyss-Coray T. Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron 2003;40:1133–45.
   PubMed Web of Science ®Google Scholar
• Jhappan C, Geiser AG, Kordon EC, Targeting expression of a transforming growth factor beta 1 transgene to the pregnant mammary gland inhibits alveolar development and lactation. Embo J 1993;12:1835–45.
   PubMedGoogle Scholar
• Pierce DF, Jr., Johnson MD, Matsui Y, Inhibition of mammary duct development but not alveolar outgrowth during pregnancy in transgenic mice expressing active TGF-beta 1. Genes Dev 1993;7:2308–17.
   PubMed Web of Science ®Google Scholar
• Wyss-Coray T, Feng L, Masliah E, 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 1995;147:53–67.
   PubMed Web of Science ®Google Scholar
• Kanaji M, Tada T, Kobayashi S. A murine model of communicating hydrocephalus: role of TGF-beta1. J Clin Neurosci 1997;4:51–6.
   PubMed Web of Science ®Google Scholar
• Tada T, Kanaji M, Kobayashi S. Induction of communicating hydrocephalus in mice by intrathecal injection of human recombinant transforming growth factor-beta 1. J Neuroimmunol 1994;50:153–8.
   PubMed Web of Science ®Google Scholar
• Wyss-Coray T, Lin C, Sanan DA, Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am J Pathol 2000;156:139–50.
   PubMed Web of Science ®Google Scholar
• Wyss-Coray T, Lin C, Yan F, TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 2001;7:612–18.
   PubMed Web of Science ®Google Scholar
• Gaertner RF, Wyss-Coray T, Von Euw D, Reduced brain tissue perfusion in TGF-beta 1 transgenic mice showing Alzheimer's disease-like cerebrovascular abnormalities. Neurobiol Dis 2005;19:38–46.
   PubMed Web of Science ®Google Scholar
• Nicolakakis N, Aboulkassim T, Aliaga A, Intact memory in TGF-beta1 transgenic mice featuring chronic cerebrovascular deficit: recovery with pioglitazone. J Cereb Blood Flow Metab: Official Journal of the International Society of Cerebral Blood Flow and Metabolism. 2011;31:200–211.
   PubMed Web of Science ®Google Scholar
• Buckwalter MS, Yamane M, Coleman BS, Chronically increased transforming growth factor-beta1 strongly inhibits hippocampal neurogenesis in aged mice. Am J Pathol 2006;169:154–64.
   PubMed Web of Science ®Google Scholar
• Dupret D, Fabre A, Dobrossy MD, Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 2007;5:e214.
   Web of Science ®Google Scholar
• Kantor S, Szabo L, Varga J, Progressive sleep and electroencephalogram changes in mice carrying the Huntington's disease mutation. Brain 2013;136:2147–58.
   PubMed Web of Science ®Google Scholar
• Deniselle MC, Lavista-Llanos S, Ferrini MG, In vitro differences between astrocytes of control and wobbler mice spinal cord. Neurochem Res 1999;24:1535–41.
   PubMed Web of Science ®Google Scholar