TGFβ1 treatment reduces hippocampal damage, spontaneous recurrent seizures, and learning memory deficits in pilocarpine-treated rats

Journal of Molecular Neuroscience

Volumn 50, Issue 1, 2013, Pages 109-123

  Li, Liang Yong ^a,b   Li, Jia Lin ^a,c   Zhang, Hui Min ^a,d   Yang, Wen Ming ^b   Wang, Kai ^a   Fang, Yuan ^e   Wang, Yu ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b ANHUI UNIVERSITY OF CHINESE MEDICINE   (China)

^c Tongling Vocational and Technical College ^*  (China)

^d Shaoxing Second Hospital   (China)

^e HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Apoptosis; Cognitive function; Neuronal degeneration; Spontaneous recurrent seizures; Transforming growth factor beta 1

Indexed keywords

CASPASE 3; PILOCARPINE; PROTEIN BAX; PROTEIN BCL 2; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DAMAGE; COGNITIVE DEFECT; CONTROLLED STUDY; EPILEPTIC STATE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING DISORDER; MAZE TEST; MEMORY DISORDER; NERVE CELL DEGENERATION; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PROTEIN EXPRESSION; RAT; RECURRENT DISEASE; SEIZURE;

ADMINISTRATION, INTRANASAL; ANIMALS; APOPTOSIS; HIPPOCAMPUS; LITHIUM; MALE; MAZE LEARNING; MEMORY DISORDERS; PILOCARPINE; RATS; RATS, SPRAGUE-DAWLEY; STATUS EPILEPTICUS; TRANSFORMING GROWTH FACTOR BETA1;

RATTUS;

EID: 84876053599     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-012-9879-1     Document Type: Article

References (58)

1. Acharya MM, Hattiangady B, Shetty AK (2008) Progress in neuroprotective strategies for preventing epilepsy. Prog Neurobiol 84:363-404
2. Bahar AS, Shirvalkar PR, Shapiro ML (2011) Memory-guided learning: CA1 and CA3 neuronal ensembles differentially encode the commonalities and differences between situations. J Neurosci 31:12270-12281
3. Battaglia G, Cannella M, Riozzi B, Orobello S, Maat-Schieman ML, Aronica E, Busceti CL, Ciarmiello A, Alberti S, Amico E, Sassone J, Sipione S, Bruno V, Frati L, Nicoletti F, Squitieri F (2011) Early defect of transforming growth factor beta1 formation in Huntington's disease. J Cell Mol Med 15:555-571
4. Bernasconi A, Tasch E, Cendes F, Li LM, Arnold DL (2002) Proton magnetic resonance spectroscopic imaging suggests progressive neuronal damage in human temporal lobe epilepsy. Prog Brain Res 135:297-304 (Pubitemid 35461026)
5. Biagini G, Baldelli E, Longo D, Contri MB, Guerrini U, Sironi L, Gelosa P, Zini I, Ragsdale DS, Avoli M (2008) Proepileptic influence of a focal vascular lesion affecting entorhinal cortex-CA3 connections after status epilepticus. J Neuropathol Exp Neurol 67:687-701
6. Boche D, Cunningham C, Gauldie J, Perry VH (2003) Transforming growth factor-beta 1-mediated neuroprotection against excitotoxic injury in vivo. J Cereb Blood Flow Metab 23:1174-1182 (Pubitemid 37229521)
7. 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)
8. Bumanglag AV, Sloviter RS (2008) Minimal latency to hippocampal epileptogenesis and clinical epilepsy after perforant pathway stimulation-induced status epilepticus in awake rats. J Comp Neurol 510:561-580
9. 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
10. Caraci F, Battaglia G, Bruno V, Bosco P, Carbonaro V, Giuffrida ML, Drago F, Sortino MA, Nicoletti F, Copani A (2011) TGF-beta1 pathway as a new target for neuroprotection in Alzheimer's disease. CNS Neurosci Ther 17:237-249
11. Chauviere L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C (2009) Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci 29:5402-5410
12. Chin J, Angers A, Cleary LJ, Eskin A, Byrne JH (1999) TGF-beta1 in aplysia: role in long-term changes in the excitability of sensory neurons and distribution of TbetaR-II-like immunoreactivity. Learn Mem 6:317-330 (Pubitemid 29422834)
13. de Lanerolle NC, Kim JH, Williamson A, Spencer SS, Zaveri HP, Eid T, Spencer DD (2003) A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44:677-687 (Pubitemid 36554636)
14. 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)
15. Docagne F, Nicole O, Gabriel C, Fernandez-Monreal M, Lesne S, Ali C, Plawinski L, Carmeliet P, MacKenzie ET, Buisson A, Vivien D (2002) Smad3-dependent induction of plasminogen activator inhibitor-1 in astrocytes mediates neuroprotective activity of transforming growth factor-beta 1 against NMDA-induced necrosis. Mol Cell Neurosci 21:634-644 (Pubitemid 36062720)
16. Engel T, Tanaka K, Jimenez-Mateos EM, Caballero-Caballero A, Prehn JH, Henshall DC (2010a) Loss of p53 results in protracted electrographic seizures and development of an aggravated epileptic phenotype following status epilepticus. Cell Death Dis 1:e79
17. Engel T, Murphy BM, Hatazaki S, Jimenez-Mateos EM, Concannon CG, Woods I, Prehn JH, Henshall DC (2010b) Reduced hippocampal damage and epileptic seizures after status epilepticus in mice lacking proapoptotic Puma. FASEB J 24:853-861
18. Fannjiang Y, Kim CH, Huganir RL, Zou S, Lindsten T, Thompson CB, Mito T, Traystman RJ, Larsen T, Griffin DE, Mandir AS, Dawson TM, Dike S, Sappington AL, Kerr DA, Jonas EA, Kaczmarek LK, Hardwick JM (2003) BAK alters neuronal excitability and can switch from anti- to pro-death function during postnatal development. Dev Cell 4:575-585 (Pubitemid 36437563)
19. Fujikawa DG (1996) The temporal evolution of neuronal damage from pilocarpine-induced status epilepticus. Brain Res 725:11-22 (Pubitemid 26231668)
20. Gonzalez-Aparicio R, Flores JA, Fernandez-Espejo E (2010) Antiparkinsonian trophic action of glial cell line-derived neurotrophic factor and transforming growth factor beta1 is enhanced after co-infusion in rats. Exp Neurol 226:136-147
21. Gorter JA, Goncalves Pereira PM, van Vliet EA, Aronica E, Lopes da Silva FH, Lucassen PJ (2003) Neuronal cell death in a rat model for mesial temporal lobe epilepsy is induced by the initial status epilepticus and not by later repeated spontaneous seizures. Epilepsia 44:647-658 (Pubitemid 36554632)
22. Graciarena M, Depino AM, Pitossi FJ (2010) Prenatal inflammation impairs adult neurogenesis and memory related behavior through persistent hippocampal TGFbeta1 downregulation. Brain Behav Immun 24:1301-1309
23. Hanson LR, Frey WH (2008) Intranasal delivery bypasses the blood-brain barrier to target therapeutic agents to the central nervous system and treat neurodegenerative disease. BMC Neurosci 9(Suppl 3):S5
24. 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)
25. Jiao S, Li Z (2011) Nonapoptotic function of BAD and BAX in long-term depression of synaptic transmission. Neuron 70:758-772
26. Jimenez-Mateos EM, Hatazaki S, Johnson MB, Bellver-Estelles C, Mouri G, Bonner C, Prehn JH, Meller R, Simon RP, Henshall DC (2008) Hippocampal transcriptome after status epilepticus in mice rendered seizure damage-tolerant by epileptic preconditioning features suppressed calcium and neuronal excitability pathways. Neurobiol Dis 32:442-453
27. Kang TC, Kim DS, Kwak SE, Kim JE, Won MH, Kim DW, Choi SY, Kwon OS (2006) Epileptogenic roles of astroglial death and regeneration in the dentate gyrus of experimental temporal lobe epilepsy. Glia 54:258-271 (Pubitemid 44316231)
28. Kastin AJ, Akerstrom V, Pan W (2003) Circulating TGF-beta1 does not cross the intact blood-brain barrier. J Mol Neurosci 21:43-48 (Pubitemid 37204871)
29. Kim DS, Kim JE, Kwak SE, Choi KC, Kim DW, Kwon OS, Choi SY, Kang TC (2008) Spatiotemporal characteristics of astroglial death in the rat hippocampo-entorhinal complex following pilocarpine-induced status epilepticus. J Comp Neurol 511:581-598
30. 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
31. Krieglstein K, Zheng F, Unsicker K, Alzheimer C (2011) More than being protective: functional roles for TGF-beta/activin signaling pathways at central synapses. Trends Neurosci 34:421-429
32. Kubova H, Druga R, Haugvicova R, Suchomelova L, Pitkanen A (2002) Dynamic changes of status epilepticus-induced neuronal degeneration in the mediodorsal nucleus of the thalamus during postnatal development of the rat. Epilepsia 43(Suppl 5):54-60 (Pubitemid 34864208)
33. Kudryashova IV, Onufriev MV, Kudryashov IE, Gulyaeva NV (2009) Caspase-3 activity in hippocampal slices reflects changes in synaptic plasticity. Neurosci Behav Physiol 39:13-20
34. Kundrotiene J, Wagner A, Liljequist S (2004) Fluoro-Jade and TUNEL staining as useful tools to identify ischemic brain damage following moderate extradural compression of sensorimotor cortex. Acta Neurobiol Exp (Wars) 64:153-162 (Pubitemid 38649376)
35. Li T, Ren G, Lusardi T, Wilz A, Lan JQ, Iwasato T, Itohara S, Simon RP, Boison D (2008) Adenosine kinase is a target for the prediction and prevention of epileptogenesis in mice. J Clin Invest 118:571-582 (Pubitemid 351206547)
36. Lochhead JJ, Thorne RG (2012) Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 64:614-628
37. Ma YP, Ma MM, Ge S, Guo RB, Zhang HJ, Frey WH 2nd, Xu GL, Liu XF (2007) Intranasally delivered TGF-beta1 enters brain and regulates gene expressions of its receptors in rats. Brain Res Bull 74:271-277 (Pubitemid 47285524)
38. Ma M, Ma Y, Yi X, Guo R, Zhu W, Fan X, Xu G, Frey WH 2nd, Liu X (2008) Intranasal delivery of transforming growth factor-beta1 in mice after stroke reduces infarct volume and increases neurogenesis in the subventricular zone. BMC Neurosci 9:117
39. Muller CJ, Bankstahl M, Groticke I, Loscher W (2009) Pilocarpine vs. lithium-pilocarpine for induction of status epilepticus in mice: development of spontaneous seizures, behavioral alterations and neuronal damage. Eur J Pharmacol 619:15-24
40. Narkilahti S, Pirttila TJ, Lukasiuk K, Tuunanen J, Pitkanen A (2003) Expression and activation of caspase 3 following status epilepticus in the rat. Eur J Neurosci 18:1486-1496 (Pubitemid 37215102)
41. Pauli E, Hildebrandt M, Romstock J, Stefan H, Blumcke I (2006) Deficient memory acquisition in temporal lobe epilepsy is predicted by hippocampal granule cell loss. Neurology 67:1383-1389 (Pubitemid 44632061)
42. Pitkanen A, Lukasiuk K (2011) Mechanisms of epileptogenesis and potential treatment targets. Lancet Neurol 10:173-186
43. Qian L, Wei SJ, Zhang D, Hu X, Xu Z, Wilson B, El-Benna J, Hong JS, Flood PM (2008) Potent anti-inflammatory and neuroprotective effects of TGF-beta1 are mediated through the inhibition of ERK and p47phox-Ser345 phosphorylation and translocation in microglia. J Immunol 181:660-668
44. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294
45. Sander JW (2003) The epidemiology of epilepsy revisited. Curr Opin Neurol 16:165-170 (Pubitemid 36521202)
46. Schmued LC, Hopkins KJ (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 874:123-130
47. Simonato M, Tongiorgi E, Kokaia M (2006) Angels and demons: neurotrophic factors and epilepsy. Trends Pharmacol Sci 27:631-638 (Pubitemid 44738088)
48. Stienen MN, Haghikia A, Dambach H, Thone J, Wiemann M, Gold R, Chan A, Dermietzel R, Faustmann PM, Hinkerohe D, Prochnow N (2011) Anti-inflammatory effects of the anticonvulsant drug levetiracetam on electrophysiological properties of astroglia are mediated via TGFbeta1 regulation. Br J Pharmacol 162:491-507
49. Sun M, Gewirtz JC, Bofenkamp L, Wickham RJ, Ge H, O'Connor MB (2010) Canonical TGF-beta signaling is required for the balance of excitatory/ inhibitory transmission within the hippocampus and prepulse inhibition of acoustic startle. J Neurosci 30:6025-6035
50. Tasch E, Cendes F, Li LM, Dubeau F, Andermann F, Arnold DL (1999) Neuroimaging evidence of progressive neuronal loss and dysfunction in temporal lobe epilepsy. Ann Neurol 45:568-576 (Pubitemid 29217584)
51. Thom M, Eriksson S, Martinian L, Caboclo LO, McEvoy AW, Duncan JS, Sisodiya SM (2009) Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: neuropathological features. J Neuropathol Exp Neurol 68:928-938
52. Vezzani A, Aronica E, Mazarati A, Pittman QJ (2012) Epilepsy and brain inflammation. Exp Neurol (in press)
53. Wang Y, Symes AJ (2010) Smad3 deficiency reduces neurogenesis in adult mice. J Mol Neurosci 41:383-396
54. Wang Y, Liu PP, Li LY, Zhang HM, Li T (2011) Hypothermia reduces brain edema, spontaneous recurrent seizure attack, and learning memory deficits in the kainic acid treated rats. CNS Neurosci Ther 17:271-280
55. Wu CL, Huang LT, Liou CW, Wang TJ, Tung YR, Hsu HY, Lai MC (2001) Lithium-pilocarpine-induced status epilepticus in immature rats result in long-term deficits in spatial learning and hippocampal cell loss. Neurosci Lett 312:113-117 (Pubitemid 32938241)
56. Zhu Y, Roth-Eichhorn S, Braun N, Culmsee C, Rami A, Krieglstein J (2000) The expression of transforming growth factor-beta1 (TGF-beta1) in hippocampal neurons: a temporary upregulated protein level after transient forebrain ischemia in the rat. Brain Res 866:286-298 (Pubitemid 30313033)
57. Zhu Y, Yang GY, Ahlemeyer B, Pang L, Che XM, Culmsee C, Klumpp S, Krieglstein J (2002) Transforming growth factor-beta 1 increases bad phosphorylation and protects neurons against damage. J Neurosci 22:3898-3909 (Pubitemid 37465698)
58. 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)