Mechanisms of regulation of oligodendrocyte development by p38 mitogen-activated protein kinase

Journal of Neuroscience

Volumn 30, Issue 33, 2010, Pages 11011-11027

  Chew, Li Jin ^a   Coley, William ^a   Cheng, Ying ^a   Gallo, Vittorio ^a  

^a CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELIN; MYELIN BASIC PROTEIN; PLATELET DERIVED GROWTH FACTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR SOX10;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE REPRESSION; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; WHITE MATTER;

ANIMALS; BRAIN; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; DNA; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NERVE FIBERS, MYELINATED; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; SOXE TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 77955875358     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2546-10.2010     Document Type: Article

References (88)

1. Agresti C, D'Urso D, Levi G (1996) Reversible inhibitory effects of interferon-gamma and tumor necrosis factor-alpha on oligodendroglial lineage cell proliferation and differentiation in vitro. Eur J Neurosci 8:1106-1116. (Pubitemid 26174637)
2. Aguirre-Ghiso JA, Estrada Y, Liu D, Ossowski L (2003) ERK-MAPK activity as a determinant of tumor growth and dormancy; regulation by p38-SAPK. Cancer Res 63:1684-1695. (Pubitemid 36373662)
3. Aguirre-Ghiso JA, Ossowski L, Rosenbaum SK (2004) Green fluorescent protein tagging of extracellular signal-regulated kinase and p38 pathways reveals novel dynamics of pathway activation during primary and metastatic growth. Cancer Res 64:7336-7345. (Pubitemid 39372072)
4. Arkell RS, Dickinson RJ, Squires M, Hayat S, Keyse SM, Cook SJ (2008) DUSP6/MKP3 inactivates ERK1/2 but fails to bind and inactivate ERK5. Cell Signal 20:836-843.
5. Armstrong RC, Le TQ, Frost EE, Borke RC, Vana AC (2002) Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J Neurosci 22:8574-8585.
6. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408:297-315.
7. Barnett SC, Rosario M, Doyle A, Kilbey A, Lovatt A, Gillespie DA (1995) Differential regulation of AP-1 and novel TRE-specific DNA-binding complexes during differentiation of oligodendrocyte-type-2-astrocyte (O-2A) progenitor cells. Development 121:3969-3977. (Pubitemid 26007348)
8. Baron W, Metz B, Bansal R, Hoekstra D, de Vries H (2000) PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Cell Neurosci 15:314-329.
9. Bermudez O, Marchetti S, Pagès G, Gimond C (2008) Post-translational regulation of the ERK phosphatase DUSP6/MKP3 by the mTOR pathway. Oncogene 27:3685-3691. (Pubitemid 351912973)
10. Bhat NR, Zhang P, Mohanty SB (2007) p38 MAP kinase regulation of oligodendrocyte differentiation with CREB as a potential target. Neurochem Res 32:293-302.
11. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, Wegner M (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15:66-78.
12. Browaeys-Poly E, Fafeur V, Vilain JP, Cailliau K (2005) ERK2 is required for FGF1-induced JNK1 phosphorylation in Xenopus oocyte expressing FGF receptor 1. Biochim Biophys Acta 1743:1-4.
13. Bulavin DV, Demidov ON, Saito S, Kauraniemi P, Phillips C, Amundson SA, Ambrosino C, Sauter G, Nebreda AR, Anderson CW, Kallioniemi A, Fornace AJ Jr, Appella E (2002) Amplification of PPM1D in human tumors abrogates p53 tumor suppressor activity. Nat Genet 31:210-215.
14. Bulavin DV, Phillips C, Nannenga B, Timofeev O, Donehower LA, Anderson CW, Appella E, Fornace AJ Jr (2004) Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat Genet 36:343-350.
15. Chang F, Steelman LS, Lee JT, Shelton JG, Navolanic PM, Blalock WL, Franklin RA, McCubrey JA (2003) Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia 17:1263-1293.
16. Chao JI, Yang JL (2001) Opposite roles of ERK and p38 mitogen-activated protein kinases in cadmium-induced genotoxicity and mitotic arrest. Chem Res Toxicol 14:1193-1202.
17. Chen G, Hitomi M, Han J, Stacey DW (2000) The p38 pathway provides negative feedback for Ras proliferative signaling. J Biol Chem 275:38973-38980. (Pubitemid 32058908)
18. Cheng B, Song J, Zou Y, Wang Q, Lei Y, Zhu C, Hu C (2009) Responses of vascular smooth muscle cells to estrogen are dependent on balance between ERK and p38 MAPK pathway activities. Int J Cardiol 134:356-365.
19. Chew LJ, King WC, Kennedy A, Gallo V (2005) Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia 52:127-143.
20. Chico LK, Van Eldik LJ, Watterson DM (2009) Targeting protein kinases in central nervous system disorders. Nat Rev Drug Discov 8:892-909.
21. Clark GJ, Westwick JK, Der CJ (1997) p120 GAP modulates Ras activation of Jun kinases and transformation. J Biol Chem 272:1677-1681.
22. Colucci-D'Amato L, Perrone-Capano C, di Porzio U (2003) Chronic activation of ERK and neurodegenerative diseases. Bioessays 25:1085-1095. (Pubitemid 37411768)
23. Curtis R, Cohen J, Fok-Seang J, Hanley MR, Gregson NA, Reynolds R, Wilkin GP (1988) Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J Neurocytol 17:43-54.
24. Dell'Albani P, Kahn MA, Cole R, Condorelli DF, Giuffrida-Stella AM, de Vellis J (1998) Oligodendroglial survival factors, PDGF-AA and CNTF, activate similar JAK/STAT signaling pathways. J Neurosci Res 54:191-205.
25. Deryckere F, Gannon F (1994) A one-hour minipreparation technique for extraction of DNA-binding proteins from animal tissues. Biotechniques 16:405. (Pubitemid 24079501)
26. Fei H, Zhao B, Zhao S, Wang Q (2008) Requirement of calcium fluxes and ERK kinase activation for glucose-and interleukin-1 beta-induced betacell apoptosis. Mol Cell Biochem 315:75-84.
27. Finzsch M, Stolt CC, Lommes P, Wegner M (2008) Sox9 and Sox10 influence survival and migration of oligodendrocyte precursors in the spinal cord by regulating PDGF receptor alpha expression. Development 135:637-646.
28. Fragoso G, Robertson J, Athlan E, Tam E, Almazan G, Mushynski WE (2003) Inhibition of p38 mitogen-activated protein kinase interferes with cell shape changes and gene expression associated with Schwann cell myelination. Exp Neurol 183:34-46.
29. Fragoso G, Haines JD, Roberston J, Pedraza L, Mushynski WE, Almazan G (2007) p38 mitogen-activated protein kinase is required for central nervous system myelination. Glia 55:1531-1541.
30. Freshney NW, Rawlinson L, Guesdon F, Jones E, Cowley S, Hsuan J, Saklatvala J (1994) Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell 78:1039-1049. (Pubitemid 24292331)
31. Gallo V, Armstrong RC (1995) Developmental and growth factor induced regulation of nestin in oligodendrocyte lineage cells. J Neurosci 15:394-406.
32. Gallo V, Zhou JM, McBain CJ, Wright P, Knutson PL, Armstrong RC (1996) Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J Neurosci 16:2659-2670. (Pubitemid 26124352)
33. Gravel M, Di Polo A, Valera PB, Braun PE (1998) Four kilobase sequence of the mouse CNP gene directs spatial and temporal expression of lacZ in transgenic mice. J Neurosci Res 53:393-404.
34. Haines JD, Fragoso G, Hossain S, Mushynski WE, Almazan G (2008) p38 mitogen-activated protein kinase regulates myelination. J Mol Neurosci 35:23-33.
35. Hamanoue M, Sato K, Takamatsu K (2007) Inhibition of p38 mitogen-activated protein kinase-induced apoptosis in cultured mature oligodendrocytes using SB202190 and SB203580. Neurochem Int 51:16-24. (Pubitemid 47002043)
36. Harrisingh MC, Perez-Nadales E, Parkinson DB, Malcolm DS, Mudge AW, Lloyd AC (2004) The Ras/Raf/ERK signaling pathway drives Schwann cell dedifferentiation. EMBO J 23:3061-3071.
37. Hayashi H, Tsuchiya Y, Nakayama K, Satoh T, Nishida E (2008) Down-regulation of the PI3-kinase/Akt pathway by ERK MAP kinase in growth factor signaling. Genes Cells 13:941-947.
38. Horiuchi M, Itoh A, Pleasure D, Itoh T (2006) MEK-ERK signaling is involved in interferon-gamma-induced death of oligodendroglial progenitor cells. J Biol Chem 281:20095-20106.
39. Hui L, Bakiri L, Mairhorfer A, Schweifer N, Haslinger C, Kenner L, Komnenovic V, Scheuch H, Beug H, Wagner EF (2007) p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway. Nat Genet 39:741-749.
40. Jessen KR, Mirsky R (2008) Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 56:1552-1565.
41. Juretic N, Santibáñez JF, Hurtado C, Martínez J (2001) ERK1,2 and p38 pathways are involved in the proliferative stimuli mediated by urokinase in osteoblastic SaOS-2 cell line. J Cell Biochem 83:92-98.
42. Kanai Y, Kanai-Azuma M, Noce T, Saido TC, Shiroishi T, Hayashi Y, Yazaki K (1996) Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis. J Cell Biol 133:667-681. (Pubitemid 26160974)
43. Kawasaki H, Morooka T, Shimohama S, Kimura J, Hirano T, Gotoh Y, Nishida E (1997) Activation and involvement of p38 mitogen-activated protein kinase in glutamate-induced apoptosis in rat cerebellar granule cells. J Biol Chem 272:18518-18521.
44. Kim M, Cha GH, Kim S, Lee JH, Park J, Koh H, Choi KY, Chung J (2004) MKP-3 has essential roles as a negative regulator of the Ras/mitogen-activated protein kinase pathway during Drosophila development. Mol Cell Biol 24:573-583.
45. Kim SM, Park JG, Baek WK, Suh MH, Lee H, Yoo SK, Jung KH, Suh SI, Jang BC (2008) Cadmium specifically induces MKP-1 expression via the glutathione depletion-mediated p38 MAPK activation in C6 glioma cells. Neurosci Lett 440:289-293.
46. Lahti A, Sareila O, Kankaanranta H, Moilanen E (2006) Inhibition of p38 mitogen-activated protein kinase enhances c-Jun N-terminal kinase activity: implication in inducible nitric oxide synthase expression. BMC Pharmacol 6:5. (Pubitemid 44102721)
47. Lavoie JN, L'Allemain G, Brunet A, Müller R, Pouysségur J (1996) Cyclin D1 expression is regulated positively by the p42/44MAPK and negatively by the p38/HOGMAPK pathway. J Biol Chem 271:20608-20616. (Pubitemid 26281839)
48. Levi G, Gallo V, Ciotti MT (1986) Bipotential precursors of putative fibrous astrocytes and oligodendrocytes in rat cerebellar cultures express distinct surface features and "neuron-like" GABA transport. Proc Natl Acad Sci U S A 83:1504-1508.
49. Lin W, Kemper A, McCarthy KD, Pytel P, Wang JP, Campbell IL, Utset MF, Popko B (2004) Interferon-gamma induced medulloblastoma in the developing cerebellum. J Neurosci 24:10074-10083.
50. Maillet M, Purcell NH, Sargent MA, York AJ, Bueno OF, Molkentin JD (2008) DUSP6 (MKP3) null mice show enhanced ERK1/2 phosphorylation at baseline and increased myocyte proliferation in the heart affecting disease susceptiblity. J Biol Chem 283:31246-31255.
51. Maruyama M, Sudo T, Kasuya Y, Shiga T, Hu B, Osada H (2000) Immunolocalization of p38 MAP kinase in mouse brain. Brain Res 887:350-358. (Pubitemid 32008058)
52. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
53. Miskimins R, Miskimins WK (2001) A role for an AP-1-like site in the expression of the myelin basic protein gene during differentiation. Int J Dev Neurosci 19:85-91. (Pubitemid 32156976)
54. Muda M, Theodosiou A, Rodrigues N, Boschert U, Camps M, Gillieron C, Davies K, Ashworth A, Arkinstall S (1996) The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinase. J Biol Chem 271:27205-27208.
55. Muniyappa H, Das KC (2008) Activation of c-Jun N-terminal kinase (JNK) by widely used specific p38 MAPK inhibitors SB202190 and SB203580: a MLK-3-MKK7-dependent mechanism. Cell Signal 20:675-683.
56. Murtie JC, Zhou YX, Le TQ, Vana AC, Armstrong RC (2005) PDGF and FGF2 pathways regulate distinct oligodendrocyte lineage responses in experimental demyelination with spontaneous remyelination. Neurobiol Dis 19:171-182.
57. Ness JK, Scaduto RC Jr, Wood TL (2004) IGF-1 prevents glutamate-mediated bax translocation and cytochrome c release in O4+ oligodendrocyte progenitors. Glia 46:183-194.
58. Ogata T, Iijima S, Hoshikawa S, Miura T, Yamamoto S, Oda H, Nakamura K, Tanaka S (2004) Opposing extracellular signal-regulated kinase and Akt pathways control Schwann cell myelination. J Neurosci 24:6724-6732.
59. 2-terminal kinase/c-Jun to control Schwann cell proliferation and death. J Cell Biol 164:385-394.
60. Parkinson DB, Bhaskaran A, Arthur-Farraj P, Noon LA, Woodhoo A, Lloyd AC, Feltri ML, Wrabetz L, Behrens A, Mirsky R, Jessen KR (2008) c-Jun is a negative regulator of myelination. J Cell Biol 181:625-637.
61. Pende M, Fisher TL, Simpson PB, Russell JT, Blenis J, Gallo V (1997) Neurotransmitter- and growth factor-induced cAMP response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ribosomal S6 kinase pathway. J Neurosci 17:1291-1301. (Pubitemid 27073731)
62. Potzner MR, Griffel C, Lütjen-Drecoll E, Bösl MR, Wegner M, Sock E (2007) Prolonged Sox4 expression in oligodendrocytes interferes with normal myelination in the central nervous system. Mol Cell Biol 27:5316-5326.
63. Qi X, Tang J, Pramanik R, Schultz RM, Shirasawa S, Sasazuki T, Han J, Chen G (2004) p38 MAPK activation selectively induces cell death in K-rasmutated human colon cancer cells through regulation of vitamin D receptor. J Biol Chem 279:22138-22144.
64. Raingeaud J, Whitmarsh AJ, Barrett T, Dérijard B, Davis RJ (1996) MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol Cell Biol 16:1247-1255. (Pubitemid 26061695)
65. Rosenberger SF, Gupta A, Bowden GT (1999) Inhibition of p38MAP kinase increases okadaic acid mediated AP-1 expression and DNA binding but has no effect on TRE dependent transcription. Oncogene 18:3626-3632.
66. Sobota RM, Müller PJ, Heinrich PC, Schaper F (2008) Prostaglandin E1 inhibits IL-6 induced MCP-1 expression by interfering specifically in IL-6-dependent ERK1/2, but not STAT3, activation. Biochem J 412:65-72.
67. Sohn J, Natale J, Chew LJ, Belachew S, Cheng Y, Aguirre A, Lytle J, Nait-Oumesmar B, Kerninon C, Kanai-Azuma M, Kanai Y, Gallo V (2006) Identification of Sox17 as a transcription factor that regulates oligodendrocyte development. J Neurosci 26:9722-9735.
68. Sriraman V, Modi SR, Bodenburg Y, Denner LA, Urban RJ (2008) Identification of ERK and JNK as signaling mediators on protein kinase C activation in cultured granulosa cells. Mol Cell Endocrinol 294:52-60.
69. Stariha RL, Kim SU (2001a) Protein kinaseCand mitogen-activated protein kinase signalling in oligodendrocytes. Microsc Res Tech 52:680-688. (Pubitemid 32222195)
70. Stariha RL, Kim SU (2001b) Mitogen-activated protein kinase signalling in oligodendrocytes: a comparison of primary cultures and CG4 cells. Int J Dev Neurosci 19:427-437.
71. Stariha RL, Kikuchi S, Siow YL, Pelech SL, Kim M, Kim SU (1997) Role of extracellular signal-regulated protein kinases 1 and 2 in oligodendroglial process extension. J Neurochem 68:945-953.
72. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, Bartsch U, Wegner M (2002) Terminal differentiation of myelinforming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 16:165-170.
73. Stolt CC, Lommes P, Friedrich RP, Wegner M (2004) Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy. Development 131:2349-2358.
74. Treinies I, Paterson HF, Hooper S, Wilson R, Marshall CJ (1999) Activated MEK stimulates expression of AP-1 components independently of phosphatidylinositol 3-kinase (PI3-kinase) but requires a PI3-kinase signal to stimulate DNA synthesis. Mol Cell Biol 19:321-329. (Pubitemid 29018434)
75. Tyler WA, Gangoli N, Gokina P, Kim HA, Covey M, Levison SW, Wood TL (2009) Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J Neurosci 29:6367-6378.
76. Ventura JJ, Tenbaum S, Perdiguero E, Huth M, Guerra C, Barbacid M, Pasparakis M, Nebreda AR (2007) p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat Genet 39:750-758.
77. Waetzig V, Herdegen T (2005) MEKK1 controls neurite regrowth after experimental injury by balancing ERK1/2 and JNK2 signaling. Mol Cell Neurosci 30:67-78.
78. Wei Q, Miskimins WK, Miskimins R (2004) Sox10 acts as a tissue-specific transcription factor enhancing activation of the myelin basic protein gene promoter by p27Kip1 and Sp1. J Neurosci Res 78:796-802. (Pubitemid 39657567)
79. Westermarck J, Li SP, Kallunki T, Han J, Kähäri VM (2001) p38 mitogen-activated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase 1 (MMP-1) gene expression. Mol Cell Biol 21:2373-2383.
80. Westwick JK, Cox AD, Der CJ, Cobb MH, Hibi M, Karin M, Brenner DA (1994) Oncogenic Ras activates c-Jun via a separate pathway from the activation of extracellular signal-regulated kinases. Proc Natl Acad Sci U S A 91:6030-6034.
81. Wissmüller S, Kosian T, Wolf M, Finzsch M, Wegner M (2006) The high-mobility-group domain of Sox proteins interacts with DNA-binding domains of many transcription factors. Nucleic Acids Res 34:1735-1744.
82. Xia Y, Makris C, Su B, Li E, Yang J, Nemerow GR, Karin M (2000) MEK kinase 1 is critically required for c-Jun N-terminal kinase activation by proinflammatory stimuli and growth factor-induced cell migration. Proc Natl Acad Sci U S A 97:5243-5248.
83. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
84. Yuan X, Eisen AM, McBain CJ, Gallo V (1998) A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125:2901-2914. (Pubitemid 28410214)
85. Yuan X, Chittajallu R, Belachew S, Anderson S, McBain CJ, Gallo V (2002) Expression of the green fluorescent protein in the oligodendrocyte lineage: a transgenic mouse for developmental and physiological studies. J Neurosci Res 70:529-545.
86. Zentrich E, Han SY, Pessoa-Brandao L, Butterfield L, Heasley LE (2002) Collaboration of JNKs and ERKs in nerve growth factor regulation of the neurofilament light chain promoter in PC12 cells. J Biol Chem 277:4110-4118.
87. Zetser A, Gredinger E, Bengal E (1999) p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J Biol Chem 274:5193-5200. (Pubitemid 129501542)
88. Zhang R, Murakami S, Coustry F, Wang Y, de Crombrugghe B (2006) Constitutive activation of MKK6 in chondrocytes of transgenic mice inhibits proliferation and delays endochondral bone formation. Proc Natl Acad Sci U S A 103:365-370.