Neuregulin 1 protects against ischemic brain injury via ErbB4 receptors by increasing GABAergic transmission

Neuroscience

Volumn 307, Issue , 2015, Pages 151-159

  Guan, Y F ^a   Wu, C Y ^a,b   Fang, Y Y ^a   Zeng, Y N ^a   Luo, Z Y ^a   Li, S J ^a   Li, X W ^a   Zhu, X H ^a   Mei, L ^c   Gao, T M ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Apoptosis; ErbB4; GABA; NRG1; OGD; Stroke

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; PARVALBUMIN; 4 AMINOBUTYRIC ACID; ERBB4 PROTEIN, MOUSE; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN PROTECTION; CONTROLLED STUDY; GABAERGIC TRANSMISSION; INTERNEURON; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BLOCKING; ANIMAL; APOPTOSIS; BRAIN INJURIES; CELL CULTURE; CELL HYPOXIA; CEREBRAL ARTERY DISEASE; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; BRAIN INJURIES; CELL HYPOXIA; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GABA AGONISTS; GAMMA-AMINOBUTYRIC ACID; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MICE; MICE, TRANSGENIC; NEUREGULIN-1; NEURONS; NEUROPROTECTIVE AGENTS; PARVALBUMINS; RATS; RECEPTOR, ERBB-4; SYNAPTIC TRANSMISSION;

EID: 84941029164     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.08.047     Document Type: Article

References (41)

1. Aika Y., Ren J.Q., Kosaka K., Kosaka T. Quantitative analysis of GABA-like-immunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the dissector. Exp Brain Res 1994, 99:267-276.
2. Bublil E.M., Yarden Y. The EGF receptor family: spearheading a merger of signaling and therapeutics. Curr Opin Cell Biol 2007, 19:124-134.
3. Buonanno A. The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits. Brain Res Bull 2010, 83:122-131.
4. Chen Q., Pan H.L. Regulation of synaptic input to hypothalamic presympathetic neurons by GABA(B) receptors. Neuroscience 2006, 142:595-606.
5. Chen Y.J., Zhang M., Yin D.M., Wen L., Ting A., Wang P., Lu Y.S., Zhu X.H., Li S.J., Wu C.Y., Wang X.M., Lai C., Xiong W.C., Mei L., Gao T.M. ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. PNAS 2010, 107:21818-21823.
6. Costa C., Leone G., Saulle E., Pisani F., Bernardi G., Calabresi P. Coactivation of GABA(A) and GABA(B) receptor results in neuroprotection during in vitro ischemia. Stroke 2004, 35:596-600.
7. Croslan D.R., Schoell M.C., Ford G.D., Pulliam J.V., Gates A., Clement C.M., Harris A.E., Ford B.D. Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia. Brain Res 2008, 1210:39-47.
8. DeFazio R.A., Raval A.P., Lin H.W., Dave K.R., Della-Morte D., Perez-Pinzon M.A. GABA synapses mediate neuroprotection after ischemic and epsilonPKC preconditioning in rat hippocampal slice cultures. J Cereb Blood Flow Metab 2009, 29:375-384.
9. Falls D.L. Neuregulins: functions, forms, and signaling strategies. Exp Cell Res 2003, 284:14-30.
10. Fazzari P., Paternain A.V., Valiente M., Pla R., Lujan R., Lloyd K., Lerma J., Marín O., Rico B. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010, 464:1376-1380.
11. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
12. Fukazawa R., Miller T.A., Kuramochi Y., Frantz S., Kim Y.D., Marchionni M.A., Kelly R.A., Sawyer D.B. Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J Mol Cell Cardiol 2003, 35:1473-1479.
13. Guo W.P., Wang J., Li R.X., Peng Y.W. Neuroprotective effects of neuregulin-1 in rat models of focal cerebral ischemia. Brain Res 2006, 1087:180-185.
14. Halasy K., Somogyi P. Distribution of GABAergic synapses and their targets in the dentate gyrus of rat: a quantitative immunoelectron microscopic analysis. J Hirnforsch 1993, 34:299-308.
15. Harrison P.J., Law A.J. Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry 2006, 60:132-140.
16. Jeon S.J., Rhee S.Y., Seo J.E., Bak H.R., Lee S.H., Ryu J.H., Cheong J.H., Shin C.Y., Kim G.H., Lee Y.S., Ko K.H. Oroxylin A increases BDNF production by activation of MAPK-CREB pathway in rat primary cortical neuronal culture. Neurosci Res 2011, 69:214-222.
17. Lai C., Lemke G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 1991, 6:691-704.
18. Li Y.G., Xu Z.F., Ford G.D., Croslan D.R., Cairobe T., Li Z.Z., Ford B.D. Neuroprotection by neuregulin-1 in a rat model of permanent focal cerebral ischemia. Brain Res 2007, 1184:277-283.
19. McBain C.J., Fisahn A. Interneurons unbound. Nat Rev Neurosci 2001, 2:11-23.
20. Mei L., Nave K.A. Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron 2014, 83:27-49.
21. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008, 9:437-452.
22. Moskowitz M.A., Lo E.H., Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010, 67:181-198.
23. Mozaffarian D., Benjamin E.J., Go A.S., Arnett D.K., Blaha M.J., Cushman M., de Ferranti S., Despres J., Fullerton H.J., Howard V.J., Huffman M.D., Judd S.E., Kissela B.M., Lackland D.T., Lichtman J.H., Lisabeth L.D., Liu S., Mackey R.H., Matchar D.B., McGuire D.K., Mohler E.R., Moy C.S., Muntner P., Mussolino M.E., Nasir K., Neumar R.W., Nichol G., Palaniappan L., Pandey D.K., Reeves M.J., Rodriguez C.J., Sorlie P.D., Stein J., Towfighi A., Turan T.N., Virani S.S., Willey J.Z., Woo D., Yeh R.W., Turner M.B. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation 2014, 131:e1-e294.
24. Schwartz-Bloom R.D., McDonough K.J., Chase P.J., Chadwick L.E., Inglefield J.R., Levin E.D. Long-term neuroprotection by benzodiazepine: full versus partial agonists after transient cerebral ischemia in the gerbil. J Cereb Blood Flow Metab 1998, 18:548-558.
25. Schwartz-Bloom R.D., Sah R. Γ-Aminobutyric acidA neurotransmission and cerebral ischemia. J Neurochem 2001, 77:353-371.
26. Schwartz R.D., Yu X., Katzman M.R., Hayden-Hixson D.M., Perry J.M. Diazepam, given postischemia, protects selectively vulnerable neurons in the rat hippocampus and striatum. J Neurosci 1995, 15:529-539.
27. Shyu W.C., Lin S.Z., Chiang M.F., Yang H.I., Thajeb P., Li H. Neuregulin-1 reduces ischemia-induced brain damage in rats. Neurobiol Aging 2004, 25:935-944.
28. Soghomonian J.J., Martin D.L. Two isoforms of glutamate decarboxylase: why?. Trends Pharmacol Sci 1998, 19:500-505.
29. Steinthorsdottir V., Stefansson H., Ghosh S., Birgisdottir B., Bjornsdottir S., Fasquel A.C., Olafsson O., Stefansson K., Gulcher J.R. Multiple novel transcription initiation sites for NRG1. Gene 2004, 342:97-105.
30. Tan W., Wang Y., Gold B., Chen J., Dean M., Harrison P.J., Weinberger D.R., Law A.J. Molecular cloning of a brain-specific, developmentally regulated neuregulin 1 (NRG1) isoform and identification of a functional promoter variant associated with schizophrenia. J Biol Chem 2007, 282:24343-24351.
31. Uchida M., Palmateer J.M., Herson P.S., DeVries A.C., Cheng J., Hurn P.D. Dose-dependent effects of androgens on outcome after focal cerebral ischemia in adult male mice. J Cereb Blood Flow Metab 2009, 29:1454-1462.
32. Vullhorst D., Neddens J., Karavanova I., Tricoire L., Petralia R.S., McBain C.J., Buonanno A. Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 2009, 29:12255-12264.
33. Wahlgren N.G., Lyden P. Neuroprotectants in the treatment of stroke-an overview. J Stroke Cerebrovasc Dis 2000, 9:32-35.
34. Wang Q., Gong Q., Wu Q., Shi J. Neuroprotective effects of Dendrobium alkaloids on rat cortical neurons injured by oxygen-glucose deprivation and reperfusion. Phytomedicine 2010, 17:108-115.
35. Woo R.S., Li X.M., Tao Y.M., Ezekiel C.H., Huang Y.Z., Weber J., Neiswender H., Dong X.P., Wu J., Gassmann M., Lai C., Xiong W.C., Gao T.M., Mei L. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 2007, 54:599-610.
36. Xu Z., Croslan D.R., Harris A.E., Ford G.D., Ford B.D. Extended therapeutic window and functional recovery after intraarterial administration of neuregulin-1 after focal ischemic stroke. J Cereb Blood Flow Metab 2006, 26:527-535.
37. Xu Z., Ford B.D. Upregulation of erbB receptors in rat brain after middle cerebral arterial occlusion. Neurosci Lett 2005, 375:181-186.
38. Xu Z., Ford G.D., Croslan D.R., Jiang J., Gates A., Allen R., Ford B.D. Neuroprotection by neuregulin-1 following focal stroke is associated with the attenuation of ischemia-induced pro-inflammatory and stress gene expression. Neurobiol Dis 2005, 19:461-470.
39. Xu Z., Jiang J., Ford G.D., Ford B.D. Neuregulin-1 is neuroprotective and attenuates inflammatory responses induced by ischemic stroke. Biochem Biophys Res Commun 2004, 322:440-446.
40. Zhou C., Li C., Yu H.M., Zhang F., Han D., Zhang G.Y. Neuroprotection of gamma-aminobutyric acid receptor agonists via enhancing neuronal nitric oxide synthase (Ser847) phosphorylation through increased neuronal nitric oxide synthase and PSD95 interaction and inhibited protein phosphatase activity in cerebral ischemia. J Neurosci Res 2008, 86:2973-2983.
41. Zhu X.H., Yan H.C., Zhang J., Qu H.D., Qiu X.S., Chen L., Li S.J., Cao X., Bean J.C., Chen L.H., Qin X.H., Liu J.H., Bai X.C., Mei L., Gao T.M. Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J Neurosci 2010, 30:12653-12663.