Chronic CXCL10 alters the level of activated ERK1/2 and transcriptional factors CREB and NF-κB in hippocampal neuronal cell culture

Journal of Neuroimmunology

Volumn 195, Issue 1-2, 2008, Pages 36-46

  Bajova, Hilda ^a   Nelson, Thomas E ^a   Gruol, Donna L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Chemokines; CNS; Neuroinflammation; Neuroprotection

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL 2;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GLIA CELL; HIPPOCAMPUS; INFLAMMATION; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ACTINS; ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; CHEMOKINE CXCL10; CREB-BINDING PROTEIN; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MAP KINASE SIGNALING SYSTEM; NEURONS; NF-KAPPA B; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 41949116388     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2008.01.003     Document Type: Article

References (75)

1. Alessandrini A., Namura S., Moskowitz M.A., and Bonventre J.V. MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 12866-12869
2. Asensio V.C., and Campbell I.L. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci. 22 (1999) 504-512
3. Bahr B.A., Bendiske J., Brown Q.B., Munirathinam S., Caba E., Rudin M., Urwyler S., Sauter A., and Rogers G. Survival signaling and selective neuroprotection through glutamatergic transmission. Exp. Neurol. 174 (2002) 37-47
4. Bailey C.H., Kaang B.K., Chen M., Martin K.C., Lim C.S., Casadio A., and Kandel E.R. Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron 18 (1997) 913-924
5. Biber K., Sauter A., Brouwer N., Copray S.C., and Boddeke H.W. Ischemia-induced neuronal expression of the microglia attracting chemokine Secondary Lymphoid-tissue Chemokine (SLC). Glia 34 (2001) 121-133
6. Bito H., Deisseroth K., and Tsien R.W. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87 (1996) 1203-1214
7. Bonacchi A., Romagnani P., Romanelli R.G., Efsen E., Annunziato F., Lasagni L., Francalanci M., Serio M., Laffi G., Pinzani M., Gentilini P., and Marra F. Signal transduction by the chemokine receptor CXCR3: activation of Ras/ERK, Src, and phosphatidylinositol 3-kinase/Akt controls cell migration and proliferation in human vascular pericytes. J. Biol. Chem. 276 (2001) 9945-9954
8. Bonni A., Brunet A., West A.E., Datta S.R., Takasu M.A., and Greenberg M.E. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286 (1999) 1358-1362
9. Carter S.L., Muller M., Manders P.M., and Campbell I.L. Induction of the genes for Cxcl9 and Cxcl10 is dependent on IFN-gamma but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia 55 (2007) 1728-1739
10. Cartier L., Hartley O., Dubois-Dauphin M., and Krause K.H. Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res. Brain Res. Rev. 48 (2005) 16-42
11. Cinque P., Bestetti A., Marenzi R., Sala S., Gisslen M., Hagberg L., and Price R.W. Cerebrospinal fluid interferon-gamma-inducible protein 10 (IP-10, CXCL10) in HIV-1 infection. J. Neuroimmunol. 168 (2005) 154-163
12. Coughlan C.M., McManus C.M., Sharron M., Gao Z., Murphy D., Jaffer S., Choe W., Chen W., Hesselgesser J., Gaylord H., Kalyuzhny A., Lee V.M., Wolf B., Doms R.W., and Kolson D.L. Expression of multiple functional chemokine receptors and monocyte chemoattractant protein-1 in human neurons. Neuroscience 97 (2000) 591-600
13. Drewes G., Lichtenberg-Kraag B., Doring F., Mandelkow E.M., Biernat J., Goris J., Doree M., and Mandelkow E. Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J. 11 (1992) 2131-2138
14. Epstein L.G., and Gelbard H.A. HIV-1-induced neuronal injury in the developing brain. J. Leukoc. Biol. 65 (1999) 453-457
15. Farina C., Aloisi F., and Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol. 28 (2007) 138-145
16. Franciotta D., Martino G., Zardini E., Furlan R., Bergamaschi R., Andreoni L., and Cosi V. Serum and CSF levels of MCP-1 and IP-10 in multiple sclerosis patients with acute and stable disease and undergoing immunomodulatory therapies. J. Neuroimmunol. 115 (2001) 192-198
17. Freudenthal R., Romano A., and Routtenberg A. Transcription factor NF-kappaB activation after in vivo perforant path LTP in mouse hippocampus. Hippocampus 14 (2004) 677-683
18. Fukunaga K., and Miyamoto E. Role of MAP kinase in neurons. Mol. Neurobiol. 16 (1998) 79-95
19. Galimberti D., Schoonenboom N., Scheltens P., Fenoglio C., Bouwman F., Venturelli E., Guidi I., Blankenstein M.A., Bresolin N., and Scarpini E. Intrathecal chemokine synthesis in mild cognitive impairment and Alzheimer disease. Arch. Neurol. 63 (2006) 538-543
20. Gutkind J.S. The pathways connecting G protein-coupled receptors to the nucleus through divergent mitogen-activated protein kinase cascades. J. Biol. Chem. 273 (1998) 1839-1842
21. Hetman M., and Gozdz A. Role of extracellular signal regulated kinases 1 and 2 in neuronal survival. Eur. J. Biochem. 271 (2004) 2050-2055
22. Hinerfeld D., Traini M.D., Weinberger R.P., Cochran B., Doctrow S.R., Harry J., and Melov S. Endogenous mitochondrial oxidative stress: neurodegeneration, proteomic analysis, specific respiratory chain defects, and efficacious antioxidant therapy in superoxide dismutase 2 null mice. J. Neurochem. 88 (2004) 657-667
23. Hu S.C., Chrivia J., and Ghosh A. Regulation of CBP-mediated transcription by neuronal calcium signaling. Neuron 22 (1999) 799-808
24. Kanterewicz B.I., Urban N.N., McMahon D.B., Norman E.D., Giffen L.J., Favata M.F., Scherle P.A., Trzskos J.M., Barrionuevo G., and Klann E. The extracellular signal-regulated kinase cascade is required for NMDA receptor-independent LTP in area CA1 but not area CA3 of the hippocampus. J. Neurosci. 20 (2000) 3057-3066
25. Kieseier B.C., Tani M., Mahad D., Oka N., Ho T., Woodroofe N., Griffin J.W., Toyka K.V., Ransohoff R.M., and Hartung H.P. Chemokines and chemokine receptors in inflammatory demyelinating neuropathies: a central role for IP-10. Brain 125 (2002) 823-834
26. Knowles R.B., Chin J., Ruff C.T., and Hyman B.T. Demonstration by fluorescence resonance energy transfer of a close association between activated MAP kinase and neurofibrillary tangles: implications for MAP kinase activation in Alzheimer disease. J. Neuropathol. Exp. Neurol. 58 (1999) 1090-1098
27. Kolb S.A., Sporer B., Lahrtz F., Koedel U., Pfister H.W., and Fontana A. Identification of a T cell chemotactic factor in the cerebrospinal fluid of HIV-1-infected individuals as interferon-gamma inducible protein 10. J. Neuroimmunol. 93 (1999) 172-181
28. Kornhauser J.M., and Greenberg M.E. A kinase to remember: dual roles for MAP kinase in long-term memory. Neuron 18 (1997) 839-842
29. Kutsch O., Oh J., Nath A., and Benveniste E.N. Induction of the chemokines interleukin-8 and IP-10 by human immunodeficiency virus type 1 tat in astrocytes. J. Virol. 74 (2000) 9214-9221
30. Lee J.I., and Burckart G.J. Nuclear factor kappa B: important transcription factor and therapeutic target. J. Clin. Pharmacol. 38 (1998) 981-993
31. Letendre S.L., Lanier E.R., and McCutchan J.A. Cerebrospinal fluid beta chemokine concentrations in neurocognitively impaired individuals infected with human immunodeficiency virus type 1. J. Infect. Dis. 180 (1999) 310-319
32. Liberto C.M., Albrecht P.J., Herx L.M., Yong V.W., and Levison S.W. Pro-regenerative properties of cytokine-activated astrocytes. J. Neurochem. 89 (2004) 1092-1100
33. Liu Z., Geng L., Li R., He X., Zheng J.Q., and Xie Z. Frequency modulation of synchronized Ca2+ spikes in cultured hippocampal networks through G-protein-coupled receptors. J. Neurosci. 23 (2003) 4156-4163
34. Martinou J.C., Dubois-Dauphin M., Staple J.K., Rodriguez I., Frankowski H., Missotten M., Albertini P., Talabot D., Catsicas S., Pietra C., et al. Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13 (1994) 1017-1030
35. Mattson M.P. NF-kappaB in the survival and plasticity of neurons. Neurochem. Res. 30 (2005) 883-893
36. Mattson M.P., and Meffert M.K. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ. 13 (2006) 852-860
37. Mattson M.P., Goodman Y., Luo H., Fu W., and Furukawa K. Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res 49 (1997) 681-697
38. Mayr B., and Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev., Mol, Cell Biol, 2 (2001) 599-609
39. Meffert M.K., and Baltimore D. Physiological functions for brain NF-kappaB. Trends Neurosci. 28 (2005) 37-43
40. Memet S. NF-kappaB functions in the nervous system: from development to disease. Biochem. Pharmacol. 72 (2006) 1180-1195
41. Mennicken F., Maki R., de Souza E.B., and Quirion R. Chemokines and chemokine receptors in the CNS: a possible role in neuroinflammation and patterning. Trends Pharmacol. Sci. 20 (1999) 73-78
42. Meucci O., Fatatis A., Simen A.A., Bushell T.J., Gray P.W., and Miller R.J. Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 14500-14505
43. Moser B., and Loetscher P. Lymphocyte traffic control by chemokines. Nat. Immunol. 2 (2001) 123-128
44. Murphy A.N. Ca(2+)-mediated mitochondrial dysfunction and the protective effects of Bcl-2. Ann. N. Y. Acad. Sci. 893 (1999) 19-32
45. Murray B., Alessandrini A., Cole A.J., Yee A.G., and Furshpan E.J. Inhibition of the p44/42 MAP kinase pathway protects hippocampal neurons in a cell-culture model of seizure activity. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 11975-11980
46. Nelson T.E., and Bajova H. The chemokine CXCL10 inhibits NMDA-induced ERK activation in hippocampal neurons. 2007 Neuroscience Meeting Planner (2007)
47. Nelson T.E., and Gruol D.L. The chemokine CXCL10 modulates excitatory activity and intracellular calcium signaling in cultured hippocampal neurons. J. Neuroimmunol. 156 (2004) 74-87
48. Neumann M., and Naumann M. Beyond IkappaBs: alternative regulation of NF-kappaB activity. FASEB J. 21 (2007) 2642-2654
49. O'Neill L.A., and Kaltschmidt C. NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci. 20 (1997) 252-258
50. Oh S.B., Endoh T., Simen A.A., Ren D., and Miller R.J. Regulation of calcium currents by chemokines and their receptors. J. Neuroimmunol. 123 (2002) 66-75
51. Perry G., Roder H., Nunomura A., Takeda A., Friedlich A.L., Zhu X., Raina A.K., Holbrook N., Siedlak S.L., Harris P.L., and Smith M.A. Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport 10 (1999) 2411-2415
52. Ransohoff R.M., Hamilton T.A., Tani M., Stoler M.H., Shick H.E., Major J.A., Estes M.L., Thomas D.M., and Tuohy V.K. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J. 7 (1993) 592-600
53. Riccio A., Ahn S., Davenport C.M., Blendy J.A., and Ginty D.D. Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286 (1999) 2358-2361
54. Ridet J.L., Malhotra S.K., Privat A., and Gage F.H. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci. 20 (1997) 570-577
55. Rossi D., and Zlotnik A. The biology of chemokines and their receptors. Annu. Rev. Immunol. 18 (2000) 217-242
56. Runden E., Seglen P.O., Haug F.M., Ottersen O.P., Wieloch T., Shamloo M., and Laake J.H. Regional selective neuronal degeneration after protein phosphatase inhibition in hippocampal slice cultures: evidence for a MAP kinase-dependent mechanism. J. Neurosci. 18 (1998) 7296-7305
57. Schwartz J.P., Sheng J.G., Mitsuo K., Shirabe S., and Nishiyama N. Trophic factor production by reactive astrocytes in injured brain. Ann. N. Y. Acad. Sci. 679 (1993) 226-234
58. Shen Q., Zhang R., and Bhat N.R. MAP kinase regulation of IP10/CXCL10 chemokine gene expression in microglial cells. Brain Res. 1086 (2006) 9-16
59. Simpson J., Rezaie P., Newcombe J., Cuzner M.L., Male D., and Woodroofe M.N. Expression of the beta-chemokine receptors CCR2, CCR3 and CCR5 in multiple sclerosis central nervous system tissue. J. Neuroimmunol. 108 (2000) 192-200
60. Sorensen T.L., Tani M., Jensen J., Pierce V., Lucchinetti C., Folcik V.A., Qin S., Rottman J., Sellebjerg F., Strieter R.M., Frederiksen J.L., and Ransohoff R.M. Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. J. Clin. Invest. 103 (1999) 807-815
61. Sui Y., Potula R., Dhillon N., Pinson D., Li S., Nath A., Anderson C., Turchan J., Kolson D., Narayan O., and Buch S. Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am. J. Pathol. 164 (2004) 1557-1566
62. Sui Y., Stehno-Bittel L., Li S., Loganathan R., Dhillon N.K., Pinson D., Nath A., Kolson D., Narayan O., and Buch S. CXCL10-induced cell death in neurons: role of calcium dysregulation. Eur J. Neurosci. 23 (2006) 957-964
63. Takeuchi Y., and Fukunaga K. Differential regulation of NF-kappaB, SRE and CRE by dopamine D1 and D2 receptors in transfected NG108-15 cells. J. Neurochem. 85 (2003) 729-739
64. Takeuchi Y., and Fukunaga K. Dopamine D2 receptor activates extracellular signal-regulated kinase through the specific region in the third cytoplasmic loop. J. Neurochem. 89 (2004) 1498-1507
65. Treisman R. Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8 (1996) 205-215
66. Trojanowski J.Q., Mawal-Dewan M., Schmidt M.L., Martin J., and Lee V.M. Localization of the mitogen activated protein kinase ERK2 in Alzheimer's disease neurofibrillary tangles and senile plaque neurites. Brain Res. 618 (1993) 333-337
67. van Marle G., Henry S., Todoruk T., Sullivan A., Silva C., Rourke S.B., Holden J., McArthur J.C., Gill M.J., and Power C. Human immunodeficiency virus type 1 Nef protein mediates neural cell death: a neurotoxic role for IP-10. Virology 329 (2004) 302-318
68. Vaudry D., Stork P.J., Lazarovici P., and Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296 (2002) 1648-1649
69. Veeranna, Amin N.D., Ahn N.G., Jaffe H., Winters C.A., Grant P., and Pant H.C. Mitogen-activated protein kinases (Erk1,2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18 (1998) 4008-4021
70. Vlkolinsky R., Siggins G.R., Campbell I.L., and Krucker T. Acute exposure to CXC chemokine ligand 10, but not its chronic astroglial production, alters synaptic plasticity in mouse hippocampal slices. J. Neuroimmunol. 150 (2004) 37-47
71. Waetzig V., and Herdegen T. The concerted signaling of ERK1/2 and JNKs is essential for PC12 cell neuritogenesis and converges at the level of target proteins. Mol. Cell Neurosci. 24 (2003) 238-249
72. Walker W.H., Fucci L., and Habener J.F. Expression of the gene encoding transcription factor cyclic adenosine 3′,5′-monophosphate (cAMP) response element-binding protein (CREB): regulation by follicle-stimulating hormone-induced cAMP signaling in primary rat Sertoli cells. Endocrinology 136 (1995) 3534-3545
73. Walton M., Woodgate A.M., Muravlev A., Xu R., During M.J., and Dragunow M. CREB phosphorylation promotes nerve cell survival. J. Neurochem. 73 (1999) 1836-1842
74. Wang X., Ellison J.A., Siren A.L., Lysko P.G., Yue T.L., Barone F.C., Shatzman A., and Feuerstein G.Z. Prolonged expression of interferon-inducible protein-10 in ischemic cortex after permanent occlusion of the middle cerebral artery in rat. J. Neurochem. 71 (1998) 1194-1204
75. Xia M.Q., Bacskai B.J., Knowles R.B., Qin S.X., and Hyman B.T. Expression of the chemokine receptor CXCR3 on neurons and the elevated expression of its ligand IP-10 in reactive astrocytes: in vitro ERK1/2 activation and role in Alzheimer's disease. J. Neuroimmunol. 108 (2000) 227-235