Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia

Brain Research

Volumn 1210, Issue , 2008, Pages 39-47

  Croslan, DaJoie R ^a   Schoell, Matthew C ^a   Ford, Gregory D ^a   Pulliam, John V ^a   Gates, Alicia ^a   Clement, Ceilessia M ^a   Harris, Adalynn E ^a   Ford, Byron D ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine receptor reducing activity; Apoptosis; Glial growth factor; Glutamate excitotoxicity; Heregulin; Ischemia; Neu differentiation factor; Neuregulin; Neuronal cell culture; Oxygen glucose deprivation

Indexed keywords

GLUCOSE; GLUTAMIC ACID; LIPOCORTIN 5; NEU DIFFERENTIATION FACTOR; OXYGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; CELL LINE; CELL SURVIVAL; CONTROLLED STUDY; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEURITE; NEUROBLASTOMA CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

RATTUS;

EID: 42749089288     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.02.059     Document Type: Article

References (46)

1. Bermingham-McDonogh O. McCabe K. Reh T. Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina Dev. Suppl. 122 1996 1427 1438
2. Bruno V.M. Goldberg M.P. Dugan L.L. Giffard R.G. Choi D.W. Neuroprotective effect of hypothermia in cortical cultures exposed to oxygen–glucose deprivation or excitatory amino acids J. Neurochem. 63 1994 1398 1406
3. Buonanno A. Fischbach G.D. Neuregulin and ErbB receptor signaling pathways in the nervous system Curr. Opin. Neurobiol. 11 2001 287 296
4. Burden S. Yarden Y. Neuregulins and their receptors: a versatile signaling module in organogenesis and oncogenesis Neuron 18 1997 847 855
5. Chan P.H. Mitochondria and neuronal death/survival signaling pathways in cerebral ischemia Neurochem. Res. 29 2004 1943 1949
6. del Zoppo G. Ginis I. Hallenbeck J.M. Iadecola C. Wang X. Feuerstein G.Z. Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia Brain Pathol. 10 2000 95 112
7. Di Segni A. Shaharabani E. Stein R. Pinkas-Kramarski R. Neuregulins rescue PC12-ErbB-4 cells from cell death induced by beta-amyloid peptide: involvement of PI3K and PKC J. Mol. Neurosci. 26 2005 57 69
8. Di Segni A. Farin K. Pinkas-Kramarski R. ErbB4 activation inhibits MPP+-induced cell death in PC12-ErbB4 cells: involvement of PI3K and Erk signaling J. Mol. Neurosci. 29 2006 257 268
9. Dirnagl U. Iadecola C. Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view Trends Neurosci. 22 1999 391 397
10. Downward J. PI 3-kinase, Akt and cell survival Semin. Cell Dev. Biol. 15 2004 177 182
11. Erlich S. Goldshmit Y. Lupowitz Z. Pinkas-Kramarski R. ErbB-4 activation inhibits apoptosis in PC12 cells Neuroscience 107 2001 353 362
12. Falls D.L. Neuregulins: functions, forms, and signaling strategies Exp. Cell Res. 284 2003 14 30
13. Falls D.L. Rosen K.M. Corfas G. Lane W.S. Fischbach G.D. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family Cell 72 1993 801 815
14. Goldberg M.P. Choi D.W. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury J. Neurosci. 13 1993 3510 3524
15. Goldshmit Y. Erlich S. Pinkas-Kramarski R. Neuregulin rescues PC12-ErbB4 cells from cell death induced by H(2)O(2). Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase J. Biol. Chem. 276 2001 46379 46385
16. 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. 1087 2006 180 185
17. Gwag B.J. Lobner D. Koh J.Y. Wie M.B. Choi D.W. Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen–glucose deprivation in vitro Neuroscience 68 1995 615 619
18. Hillion J.A. Li Y. Maric D. Takanohashi A. Klimanis D. Barker J.L. Hallenbeck J.M. Involvement of Akt in preconditioning-induced tolerance to ischemia in PC12 cells J. Cereb. Blood Flow Metab. 26 2006 1323 1331
19. Ho Armanini M.P. Nuijens A. Phillips H.S. Osheroff P.L. Sensory and motor neuron-derived factor. A novel heregulin variant highly expressed in sensory and motor neurons J. Biol. Chem. 270 1995 26722
20. Holmes W.E. Sliwkowski M.X. Akita R.W. Henzel W.J. Lee J. Park J.W. Yansura D. Abadi N. Raab H. Lewis G.D. Identification of heregulin, a specific activator of p185erbB2 Science 256 1992 1205 1210
21. Horn A.P. Gerhardt D. Geyer A.B. Valentim L. Cimarosti H. Tavares A. Horn F. Lenz G. Salbego C. Cellular death in hippocampus in response to PI3K pathway inhibition and oxygen and glucose deprivation Neurochem. Res. 30 2005 355 361
22. Iadecola C. Alexander M. Cerebral ischemia and inflammation Curr. Opin. Neurol. 14 2001 89 94
23. Lawlor M.A. Alessi D.R. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114 2001 2903 2910
24. Lee J.M. Grabb M.C. Zipfel G.J. Choi D.W. Brain tissue responses to ischemia J. Clin. Invest. 106 2000 723 731
25. Lo E.H. Moskowitz M.A. Jacobs T.P. Exciting, radical, suicidal: how brain cells die after stroke Stroke 36 2005 189 192
26. Malhotra S. Savitz S.I. Ocava L. Rosenbaum D.M. Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack J. Neurosci. Res. 83 2006 19 27
27. Marchionni M.A. Goodearl A.D. Chen M.S. Bermingham-McDonogh O. Kirk C. Hendricks M. Danehy F. Misumi D. Sudhalter J. Kobayashi K. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system Nature 362 1993 312 318
28. Mitsiades C.S. Mitsiades N. Koutsilieris M. The Akt pathway: molecular targets for anti-cancer drug development Curr. Cancer Drug Targets 4 2004 235 256
29. Noraberg J. Poulsen F.R. Blaabjerg M. Kristensen B.W. Bonde C. Montero M. Meyer M. Gramsbergen J.B. Zimmer J. Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair Curr. Drug Targets CNS. Neurol. Disord. 4 2005 435 452
30. Otey C.A. Boukhelifa M. Maness P. B35 neuroblastoma cells: an easily transfected, cultured cell model of central nervous system neurons Methods Cell Biol. 71 2003 287 304
31. Ouyang Y.B. Giffard R.G. Cellular neuroprotective mechanisms in cerebral ischemia: Bcl-2 family proteins and protection of mitochondrial function Cell Calcium 36 2004 303 311
32. Schubert D. Heinemann S. Carlisle W. Tarikas H. Kimes B. Patrick J. Steinbach J.H. Culp W. Brandt B.L. Clonal cell lines from the rat central nervous system Nature 249 1974 224 227
33. 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 25 2004 935 944
34. Stadelmann C. Lassmann H. Detection of apoptosis in tissue sections Cell Tissue Res. 301 2000 19 31
35. Sundaresan S. Penuel E. Sliwkowski M.X. The biology of human epidermal growth factor receptor 2 Curr. Oncol. Rep. 1 1999 16 22
36. Tymianski M. Charlton M.P. Carlen P.L. Tator C.H. Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons J. Neurosci. 13 1993 2085 2104
37. van den Eijnde S.M. Luijsterburg A.J. Boshart L. De Zeeuw C.I. van Dierendonck J.H. Reutelingsperger C.P. Vermeij-Keers C. In situ detection of apoptosis during embryogenesis with annexin V: from whole mount to ultrastructure. Cytometry 29 1997 313 320
38. Vaskovsky A. Lupowitz Z. Erlich S. Pinkas-Kramarski R. ErbB-4 activation promotes neurite outgrowth in PC12 cells J. Neurochem. 74 2000 979 987
39. Verdi J.M. Groves A.K. Farinas I. Jones K. Marchionni M.A. Reichardt L.F. Anderson D.J. A reciprocal cell–cell interaction mediated by NT-3 and neuregulins controls the early survival and development of sympathetic neuroblasts Neuron 16 1996 515 527
40. Vincent A.M. Maiese K. Direct temporal analysis of apoptosis induction in living adherent neurons J. Histochem. Cytochem. 47 1999 661 672
41. Vinores S.A. Marangos P.J. Bonnin J.M. Rubinstein L.J. Immunoradiometric and immunohistochemical demonstration of neuron-specific enolase in experimental rat gliomas Cancer Res. 44 1984 2595 2599
42. Wen D. Peles E. Cupples R. Suggs S.V. Bacus S.S. Luo Y. Trail G. Hu S. Silbiger S.M. Levy R.B. Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit Cell 69 1992 559 572
43. Xu Z. Jiang J. Ford G. Ford B.D. Neuregulin-1 is neuroprotective and attenuates inflammatory responses induced by ischemic stroke Biochem. Biophys. Res. Commun. 322 2004 440 446
44. 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. 19 2005 461 470
45. 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. 26 2006 527 535
46. Zhao H. Shimohata T. Wang J.Q. Sun G. Schaal D.W. Sapolsky R.M. Steinberg G.K. Akt contributes to neuroprotection by hypothermia against cerebral ischemia in rats J. Neurosci. 25 2005 9794 9806