Brain injury: prolonged induction of transcription factors

• Autorzy: Pennypacker K R , Kassed C.A. , Eidizadeh S. , O'Callaghan J.P.
• Języki publikacji: EN

Abstrakty

EN

A specific temporal order of events at the cellular and molecular level occurs in response to injury to the brain. Injury-compromised neurons degenerate while surviving neurons undergo neuritogenesis and synaptogenesis to establish neuronal connectivity destroyed in the injury. Several genes, such as those coding cytoskeletal proteins and growth factors, have been shown to be regulated by AP-1 and NF-kB transcription factors, two of the most studied DNA binding regulatory proteins. Our laboratory has discovered that Fos-related antigen-2 from AP-1 transcription factor family and NF-kB p65 and p50 subunits are induced long-term (days to months) in the brain after neurotoxic, excitotoxic or ischemic insult. Fos-related antigen-2 is induced in neurons in several models of injury and its elevated expression lasts days to months, corresponding to the severity. The time-course of FRA-2 induction is abbreviated with less severe insult (terminal damage) relative to the cell death, but the induction occurs during the period of regeneration and repair in both models. NF-kB p65 is basally expressed in hippocampal and cortical neurons, but is elevated in reactive astrocytes in hippocampus and entorhinal cortex starting at two days and lasting at least two weeks after kainate treatment. Neurons of the hippocampus surviving ischemic or neurotoxic injury increase expression of NF-kB p50 for at least a week after injury, suggesting a function for p50 in neuronal survival and/or repair. The extended expression of these transcription factors implies a role in the activation of genes related to repair and regeneration, such as growth factors and synaptic proteins, after injury to the CNS.

Słowa kluczowe

EN

brain injury; astrocyte; gene expression; in vivo; exicitotoxicity; cortical neuron; microglia; transcription factor; phosphorylation; entorhinal cortex; lymphocyte; immunohistochemical analysis; cytoskeletal protein; ischaemia; neurotoxicity; DNA; apoptosis; hippocampus; growth factor; blood brain barrier; induction

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2000
• Tom: 60
• Numer: 4
• Opis fizyczny: p.515-530,fig

Twórcy

autor

Pennypacker K R

• University of South Florida, College of Medicine, 12901 Bruce B.Downs Boulevard MDC 9, Tampa, FL 33612, USA

autor

Kassed C.A.

autor

Eidizadeh S.

autor

O'Callaghan J.P.

Bibliografia

• Altar C., Baudry M. (1990) Systemic injection of kainic acid: gliosis in olfactory and limbic brain regions quantified with [3H]PK 11195 binding autoradiography. Exp. Neurol. 109: 333-341.
• Baeuerle P., Baltimore D. (1989) A specific inhibitor of the NFkB. Science 242: 540-546. Baeuerle P., Baltimore D. (1991) The physiology of the NFkB transcription factor. In: Molecular aspects of cellular regu­lation (Eds. P. Cohen and J. Foulkes). Elsvier, Amsterdam, p. 409-432.
• Barger S.W., Horster D., Furukawa K., Goodman Y., Krieglstein J., Mattson M.P. (1995) Tumor necrosis factors alpha and beta protect neurons against amyloid beta-pep- tide toxicity: evidence for involvement of a kappa B-binding factor and attenuation of peroxide and Ca2+ accu­mulation. Proc. Natl. Acad. Sci. USA 92: 9328-9332.
• Barger SW., Mattson M.P. (1996) Induction of neuroprotec­tive kappa B-dependent transcription by secreted forms of the Alzheimer's beta-amyloid precursor. Mol. Brain Res. 40: 116-126.
• Barger S.W., Mattson M.P. (1996) Participation of gene ex­pression in the protection against amyloid beta-peptide tox­icity by the beta-amyloid precursor protein. Ann. NY Acad. Sci. 777: 303-309.
• Beg F., Baltimore D. (1996) Essential role for NF-kB in pre­venting TNFalpha induced cell death. Science 274: 782-784.
• Brock T., O'Callaghan J. (1987) Quanitative changes in the synaptic vesicle proteins synapsin 1 and the astrocyte-specific protein glial fibrillary acidic protein are assocaiated with chemical-induced injury to the rat central nervous sys­tem. J. Neurosci. 7: 931-942.
• Bronstein D., Ye H., Pennypacker K., Hudson P., Hong J. (1994) Role of a 35 kDa fos-related antigen (FRA) in the long-term induction of striatal dynorphin expression in the 6-hydroxydopamine lesioned rat. Mol. Brain Res. 23: 191-203.
• Bruce A., Boling W., Kindy M., Peschon J., Kraemer P., Car­penter M., Holtsberg F., Mattson M. (1996) Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Na­ture Med. 2: 788-794.
• Brunjes P. (1994) Unilateral naris closure and olfactory sys­tem development. Brain Res. Rev 19: 146-160.
• Chauvet N., Apert C., Dumoulin A., Epelbaum J., Alonso G. (1997) Mab22C11 antibody to amyloid precursor protein recognizes a protein associated with specific astroglial cells of the rat central nervous system characterized by their ca­pacity to support axonal outgrowth. J. Comp. Neurol. 377: 550-564.
• de Moissac D., Mustapha S., Greenberg A., Kirshenbaum L. (1998) Bcl-2 activates the transcription factor NFkB through degradation of the cytoplasmic inhibitor IkBo,. J. Biol. Chem. 273: 23946-23951.
• Dragunow M., Preston K. (1995) The role of inducible tran­scription factors in apoptotic nerve cell death. Brain Res. Rev. 21: 1-28.
• Dragunow M., Robertson G., Faull R., Robertson H., Jansen K. (1990) D2 dopamine receptor antagonists induced fos and related proteins in striatal neurons. Neuroscience 37: 287-294.
• Eddleston M., Mucke L. (1993) Molecular profile of reactive astrocytes: Implications for their role in neurologic disease. Neuroscience 54: 15-36.
• Estus S., Zaks W.J., Freeman R.S., GrudaM., Bravo R., John­son E.M. (1994) Altered gene expression in neurons during programmed cell death: Identification of c-jun as necessary for neuronal apoptosis. J. Cell. Biol. 127: 1717-1727.
• Friedman W., Thakur S., Seidman L., Rabson A. (1996) Reg­ulation of nerve growth factor mRNA by interleukin-1 in rat hippocampal astrocytes is mediated by NFkB. J. Biol. Chem. 271:31115-31120.
• Galter D., Mihm S., Droge W. (1994) Distinct effects of glutathione disulfide on the nuclear transcription factors kappaB and the activator protein-1. Eur. J. Biochem. 221: 639-648.
• Gass P., Herdegen T. (1995) Neuronal expression of AP-1 proteins in excitoxic-neurodegenerative disorders and fol­lowing nerve fiber lesions. Prog. Neurobiol. 47: 257-290.
• Ghosh S., Baltimore D. (1990) Activation in vitro of NFkB by phosphorylation of its inhibitor IkP. Nature 344:678-682.
• Giulian D., Vaca K., Corpuz M. (1993) Brain glia release fac­tors with opposing actions on neuronal survival. J. Neurosci. 13: 29-37.
• Goss J., O'Malley M., Zou L., Styren S., Kochanek P., DeKoskey S. (1998) Astrocytes are the major source of nerve growth factor upregulation following traumatic brain injury in the rat. Exp. Neurol. 149: 301-309.
• Gruda M., Kovary K., Metz R., Bravo R. (1994) Regulation of Fra-1 and Fra-2 phosphorylation differs during the cell cy­cle of fibroblasts and phosphorylation in vitro by MAP kinase affects DNA binding activity. Oncogene 9: 2537-2547.
• Hai T., Curran T. (1991) Cross-family dimerization of tran­scription factors Fos/Jun and ATF/CREB alters DNA bind­ing specificity. Proc. Natl. Acad. Sci. USA 88:3720-3724.
• Hall E., Oostveen J., Dunn E., Carter D. (1995) Increased am­yloid protein precursor and apolipoprotein E immunore- activity in the selectively vulnerable hippocampus follow­ing transient forebrain ischemia in gerbils. Exp. Neurol. 135: 17-27.
• Henkel T., Machleidt T., Alkalay I., Kronke M., Ben-Neriah Y., Baeuerle P. (1993) Rapid proteolysis of IkP is necessary for activation of transcription factor NFkB. Nature 365: 182-185.
• Herdegen T., Skene P., Bahr M. (1997) The c-Jun transcrip­tion factor-bipotential mediator of neuronal death, survival and regeneration. TINS 20: 227-231.
• Huhtala P., Tuuttila A., Chow L., Lohi J., Keski-Oja J., Tryggvason K. (1991) Complete structure of the human gene for 92-kDa type IV collagenase. Divergent regulation of expression for the 92- and 72-kilodalton enzyme genes in HT-108 cells. J. Biol. Chem. 266: 16485-16490.
• Jacobson R., Virag I., Skene J. (1986) A protein associated with axon growth, GAP-43, is widely distributed and de- velopmentally regulated in rat CNS. J. Neurosci. 6: 1843-1855.
• KaczmarekL. (1993) Molecular biology of learning: is c-fos a new beginning? J. Neurosci. Res. 34: 377-381.
• Kaltschmidt B., Uherek M., Volk B., Baeuerle P.A., Kaltschmidt C. (1997) Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc. Natl. Acad. Sci. USA 94:2642-7.
• Kaltschmidt C., Kaltschmidt B., Baeuerle P.A. (1995) Stimu­lation of ionotropic glutamate receptors activates transcrip­tion factor NF-kappa B in primary neurons. Proc. Natl. Acad. Sci. USA 92: 9618-22.
• Kaltschmidt C., Kaltschmidt B., Neumann H., Wekerle H., Baeuerle P.A. (1994) Constitutive NF-kappa B activity in neurons. Mol. Cell. Biol. 14: 3981-92.
• Kamińska B., Filipkowski R., Zurkowska G., Lason W., Przewłocki R., Kaczmarek L. (1994) Dynamic changes in the composition of the AP-1 transcription factor DNA-binding activity in rat brain following kainate-in- duced seizures and cell death. Eur. J. Neurosci. 6: 1558-1566.
• Kasof G., Mandelzys A., Maika S., Hammer R., Curran T.,.Morgan J. (1995) Kainic acid-induced neuronal death is associated with DNA damage and a unique immedi­ate-early gene response in c-fos-lacZ transgenic rats. J. Neurosci. 15: 4238-4249.
• Kita T., Liu L., Tanaka N., Kinoshita Y. (1997) The expres­sion of tumor necrosis factor-alpha in the rat brain after fluid percussive head injury. Internat. J. Legal. Med. 110: 305-311.
• Lafortune L., Nalbantoglu J., Antel J.P. (1996) Expression of tumor necrosis factor alpha (TNF alpha) and interleukin 6 (IL-6) mRNA in adult human astrocytes: comparison with adult microglia and fetal astrocytes. J. Neuropathol. Exp. Neurol. 55: 515-21.
• Lahiri D., Nall C. (1995) Promoter activity of the gene encod­ing the beta-amyloid precursor protein is up-regulated by growth factors, phorbol ester, retinoic acid and interleukin-1. Mol. Brain Res. 32: 233-240.
• Lee T., Kato H., Kogure K., Itoyama Y. (1996) Temporal pro­file of nerve growth factor-like immunoreactivity after transient focal ischemia in rats. Brain Res. 713: 199-210.
• Link E., Kerr L., Shreck R., Zabel U., Verma I., Baeuerle P. (1992) Purified I kappa-beta is inactivated upon dephosphorylation. J. Biol. Chem. 267: 239-246.
• Lipton S. (1997) Janus faces of NF-kB: neurodestruction ver­sus neuroprotection. Nature Med. 3: 20-22.
• Little A., O'Callaghan J. (1999) TNF-alpha, IL-1alpha, and IL-1beta gene expression is not altered in response to trimethyltin-induced neuronal damage in the adult rat hip­pocampus. Soc. Neurosci. Abstr. 25: 1535.
• Liu J., Marino M., Wong G., Grail D., Dunn A., Bettadapura J., Slavin A., Old L., Bernard C. (1998) TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nature Med. 4: 78-83.
• Lowenstein D., Seren M., Longo F. (1993) Prolonged in­creases in neurotropic activity associated with kainate-in- duced hippocampal synaptic reorganization. Neuroscience 56: 597-604.
• Masliah E., Westland C., Rockenstein E., Abraham C., Mallory M., Veinberg I., Sheldon E., Mucke L. (1997) Am­yloid precursor proteins protect neurons of transgenic mice against acute and chronic excitotoxic injuries in vivo. Neu­roscience 78: 135-146.
• Meyer M., Schreck R., Baeurle P. (1993) H2O2 and antioxi­dants have opposite effects on activation of NF-kB and
• AP-1 in intact cells: AP-1 as secondary antioxi- dant-responsive factor. EMBO J. 12: 2005-2015.
• Miller., O'Callaghan J. (1994) Environment-, drug- and stress-induced alterations in body temperature affect the neurotoxicity of substituted amphetamines in the C57BL/6J mouse. J. Pharm. Exp. Ther. 270: 752-760.
• Morgan J., Cohen D., Hempstead J., Curran T. (1987) Map­ping patterns of c-fos expression in the central nervous sys­tem after seizure. Science 237: 192-197.
• Murakami M., Sonobe M., Ui M., Kabuyama Y., Watanabe H., Wada T., HandaH., IbaH. (1997) Phosphorylation and high level expression of Fra-2 in v-src transformed cells: a pathway of activation of endogenous AP-1. Oncogene 14: 2435-2444.
• Nedivi E., Basi G., Akey I., Skene J. (1992) A neural-specific GAP-43 core promoter located between unusual DNA ele­ments that interact to regulate its activity. J. Neurosci. 12: 691-704.
• Nishina H., Sato H., Suzuki T., Sato M., Iba H. (1990) Isola­tion and characterization of fra-2, an additional member of the fos gene family. Proc. Natl. Acad. Sci. USA 87: 3619-3623.
• O'Callaghan J., Miller D. (1994) Neurotoxicity profiles of substituted amphetamines in the C57BL/6J mouse. J. Pharm. Exp. Ther. 270: 741-751.
• O'Neill L., Kaltschmidt C (1997) NFkB: a crucial transcrip­tion factor for glial and neuronal cell function. TINS 20: 252-258.
• Oderfeld-Nowak B., Zaremba M.. (1998) GM1 ganglioside potentiates trimethyltin-induced expression of interleukin- -1beta and nerve growth factor in reactive astrocytes in the rat hippocampus: an immunocytochemical study. Neurochem. Res. 23: 443-453.
• Pennypacker K., Hernandez H., Benkovic S., Morgan D., Willing A., Sanberg P. (1999) Induction of presenilins in the rat brain after middle cerebral arterial occlusion. Brain Res. Bull. 48: 539-543.
• Pennypacker K., Hong J., Douglass J.,McMillian M. (1992) Constitutive expression of AP-1 transcription factors in the rat adrenal. J. Biol. Chem. 267: 20148-20152.
• Pennypacker K., Hong J., McMillian M. (1995) Implications of prolonged expression of Fos-related antigens. TIPS 16: 317-321.
• Pennypacker K., Hong J., Mullis S., Hudson P., McMillian M. (1996) Transcription factors in primary glial cultures: changes with neuronal interactions. Mol. Brain Res. 37: 224-230.
• Pennypacker K., Hudson P., Hong J., McMillian M. (1995) DNA binding activity of CREB transcription factor during ontogeny of the central nervous system. Dev. Brain Res. 86: 242-249.
• Pennypacker K., Lennard D., Hudson P., Hong J., McMillian M. (1995) Basal expression of 35 kDafos-related antigen in olfactory bulb. Mol. Brain Res. 34: 161-165.
• Pennypacker K., Thai L., Hong J., McMillian M. (1994) Pro­longed expression of AP-1 transcription factors in the rat hippocampus after systemic kainate treatment. J. Neurosci. 14: 3998-4006.
• Pennypacker K., Walczak D., Thai L., Fannin R., Mason E., Douglass J., Hong J. (1993) Kainate-induced changes in opioid peptide genes and AP-1 protein expression in rat hippocampus. J. Neurochem. 60: 204-211.
• Pennypacker K., Zhang W., Ye H., Hong J. (1992) Apomor- phine induction of AP-1 DNA binding in the rat striatum af­ter dopamine depletion. Mol. Brain Res. 15: 151-155.
• Perez-Otano I., McMillian M., Chen J, Bing G., Hong J., Pennypacker K. (1996) Induction of NFkB-like transcrip­tion factors in brain areas susceptible to kainate toxicity. Glia 16: 306-315.
• Poirier J. (1994) Apolipoprotein E in animal model of CNS in­jury and in Alzheimer's disease. TINS 17: 525-530.
• Pollard H., Khrestchatisky M., Moreau J., Ben-Ari Y., Represa A. (1994) Correlation between reactive sprouting and microtubule protein expression in epileptic hippocam­pus. Neuroscience 61: 773-787.
• Quan N., Whiteside M., Kim L., Herkenham M. (1997) Induc­tion of inhibitory factor kB alpha mRNA in the central ner­vous system after periphral lipopolysaccharide admini­stration: an in situ hybridization histochemistry study in the rat. Proc. Natl Acad. Sci. USA 94: 10985-10990.
• Quitsche W., Goldgaber D. (1992) The amyloid beta-protein precursor promoter. J. Biol. Chem. 267: 17362-17368.
• Robertson G., HerreraD., Dragunow M., Robertson H. (1991) L-DOPA activates c-fos in the striatum ipsilateral to a 6-hydroxydopamine lesion of the substantia nigra. Eur. J. Pharmacol. 150: 99-100.
• Robinson G. (1996) Changes in expression of transcription factors ATF-2 and Fra-2 after axotomy and during regener­ation in rat retinal ganglion cells. Mol. Brain Res. 41: 57-64.
• Rosen J., Chuang E., Iadarola M. (1994) Differential induc­tion of Fos protein and a Fos-related antigen following acute and repeated cocaine administration. Mol. Brain Res. 25: 168-172.
• Schaninger M., Neher M., Viegas E., Schneider A., Spranger M. (1997) Stimulation of interleukin-6 secretion and gene transcription in primary astrocytes by adenosine. J. Neurochem. 69: 1145-1150.
• Schenk H., Klein M., Erdbrugger W., Droge W., Schulze- -Osthoff K. (1993) Distinct effects of thioredoxin and anti­oxidants on the activation of NF-kappaB and AP-1. Proc. Natl. Acad. Sci. USA 91: 1672-1676.
• Schneider A., Martin-Villaba A., Weih F., Vogel J., Wirth T., Schwaninger M. (1999) NF-kappaB is activated and pro­motes cell death in focal cerebral ischemia. Nature Med. 5: 554-559.
• Shirakawa F., Mizel S. (1989) In vitro activation and nuclear translocation of NFkB catalyzed by cAMP-dependent pro­tein kinase and protein kinase C. Mol. Cell. Biol. 9: 2424-2430.
• Smeyne R.J., Vendrell M., Hayward M, Baker S., Miao G., Schilling K., Robertson L., Curran T., Morgan J. (1993) Continuous c-fos expression precedes programmed cell death in vivo. Nature 363: 166-169.
• Smith-Swintosky V., Pettigrew L., Craddock S., Culwell A. Rydel R., Mattson M. (1994) Secreted forms of beta-amy­loid precursor protein protect against ischemic brain injury. J. Neurochem. 63: 781-784.
• Sonnenberg J., Macgregor-Leon P., Curran T., Morgan J. (1989) Dynamic alterations occur in the levels and compo­sition of transcription factor AP-1 complexes after seizure. Neuron 3: 359-365.
• Sparacio S., Zhang Y., Vilcek J., Benveniste E. (1992) Cytokine regulation of interleukin-6 gene expression in astrocytes involves activation of an NFkB-like nuclear pro­tein. J. Neuroimmunol 39: 231-242.
• Stancovski I., Baltimore D. (1997) NF-kB activation: The IkB kinase revealed. Cell 91: 299-302.
• Strauss S., Otten U., Joggerst B., Pluss K., Volk B. (1994) In­creased levels of nerve growth factor (NGF) protein and mRNA and reactive gliosis following kainic acid injection in the rat striatum. Neurosci. Lett. 168: 193-196.
• Takami K., Iwane M., Kiyota Y., Miyamoto M., Tsukuda R., Shiosaka S. (1992) Increase in basic fibroblast growth factor immunoreactivity and its mRNA level in rat brain follow­ing transient forebrain ischemia. Exp. Brain Res. 90:1-10.
• Uno H., Matsuyama T., Akita H., Nishimura H., Sugita M. (1997) Induction of tumor necrosis factor-alpha. J. Cereb. Blood Flow Metab. 17: 491-499.
• Van-Den-Berg K., Gramsbergen J. (1993) Long-term changes in glial fibrillary acidic protein and calcium levels in rat hip­pocampus after a single systemic dose of kainic acid. Ann. NY Acad. Sci. 679: 394-401.
• Voraberger G., Schafer R., Stratowa C. (1991) Cloning of the human gene for intercellular adhesion molecule 1 and analy­sis of its 5'-regulatory region. J. Immunol. 147:2777-2786.
• Wang C-Y., Mayo M., Korneluk R., Goeddel D., Baldwin A.J. (1998) NF-kB Antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 acti­vation. Science 281: 1680-1683.
• White L. (1994) Two activator protein-1 elements in the ma­trix metalloproteinase-1 promoter have differential effects on transcription and bind JunD, c-Fos and Fra-2. Matrix Biol. 14: 715-725.
• Wissnik S., Stolpe A., Caldenhoven E., Koenderman L., Van Der Saag P. (1997) NF kappaB/Rel family members regu­lating the ICAM-1 promoter in monocytic THP-1 cells. Immunobiology 198: 50-64.
• Wu M., Ao Z., Prasad K., Wu R Schlossman S. (1998) IEX-1L, an apoptosis inhibitor involved in NF-kB-medi- ated cell survival. Science 281: 998-1000.
• Xiao Y., Harry G., Pennypacker K. (1999) Expression of AP-1 transcription factors in rat hippocampus and cerebel­lum after trimethyltin neurotoxicity. Neurotoxol. 20: 761-766.
• Yan S.D., Chen X., Fu J., Chen M., Zhu H., Roher A., Slattery T., Zhao L., Nagashima M., Morser J., Migheli A., Nawroth P., Stern D., Schmidt AM (1996) RAGE and amy­loid-beta peptide neurotoxicity in Alzheimer's disease. Na­ture 382: 685-91.
• Yan S.D., Yan S.F., Chen X., Fu J., Chen M., Kuppusamy P., Smith M.A., Perry G., Godman G.C., Nawroth P. (1995) Non-enzymatically glycated tau in Alzheimer's disease in­duces neuronal oxidant stress resulting in cytokine gene ex­pression and release of amyloid beta-peptide. Nature Med. 1: 693-9.
• Zhang Y., Lin., Vilcek J. (1990) Interleukin-6 induction by tu­mor necrosis factor and interleukin-1 in human fibroblasts involves activation of a nuclear factor binding to a kB se­quence. Mol. Cell. Biol. 10: 3818-3823.
• Zhang, J.W., Deb S., Gottschall, P.E. (1998) Regional and dif­ferential expression of gelatinases in rat brain after sys­temic kainic or biculine administration. Eur. J. Biol.10: 3358-3368.