Constitutively active Akt induces enhanced myelination in the CNS

Journal of Neuroscience

Volumn 28, Issue 28, 2008, Pages 7174-7183

  Flores, Ana I ^a,c   Narayanan, S Priyadarshini ^a   Morse, Emily N ^a   Shick, H Elizabeth ^a   Yin, Xinghua ^a   Kidd, Grahame ^a   Avila, Robin L ^b   Kirschner, Daniel A ^b   Macklin, Wendy B ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b BOSTON COLLEGE   (United States)

^c HOSPITAL UNIVERSITARIO 12 DE OCTUBRE   (Spain)

Author keywords

Akt; Myelin; Oligodendrocyte; Phosphatidylinositol 3 OH kinase; Schwann cell; Transgenic

Indexed keywords

BETA ACTIN; GLYCOGEN SYNTHASE KINASE; MYELIN; NEU DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; BROXURIDINE; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; ONCOPROTEIN; PLP1 PROTEIN, MOUSE; PROTEOLIPID PROTEIN; SERINE; THREONINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL DENSITY; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; IN VIVO STUDY; MOUSE; MYELINATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION; SCHWANN CELL; SIGNAL TRANSDUCTION; WHITE MATTER; WILD TYPE; AGE; ANIMAL; BIOSYNTHESIS; CELL DEATH; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; MYELIN SHEATH; PHYSIOLOGY; SCIATIC NERVE; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AGE FACTORS; ANIMALS; BROMODEOXYURIDINE; CELL DEATH; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; OLIGODENDROGLIA; ONCOGENE PROTEIN V-AKT; OPTIC NERVE; SCIATIC NERVE; SERINE; THREONINE;

EID: 49049095578     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0150-08.2008     Document Type: Article

References (55)

1. Avila RL, Inouye H, Baek RC, Yin X, Trapp BD, Feltri ML, Wrabetz L, Kirschner DA (2005) Structure and stability of internodal myelin in mouse models of hereditary neuropathy. J Neuropathol Exp Neurol 64:976-990.
2. Azari MF, Profyris C, Karnezis T, Bernard CC, Small DH, Cheema SS, Ozturk E, Hatzinisiriou I, Petratos S (2006) Leukemia inhibitory factor arrests oligodendrocyte death and demyelination in spinal cord injury. J Neuropathol Exp Neurol 65:914-929.
3. Baron W, Decker L, Colognato H, ffrench-Constant C (2003) Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr Biol 13:151-155.
4. Bellacosa A, Testa JR, Staal SP, Tsichlis PN (1991) A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 254:274-277.
5. Bernal-Mizrachi E, Wen W, Stahlhut S, Welling CM, Permutt MA (2001) Islet beta cell expression of constitutively active Akt1/PKB alpha induces striking hypertrophy, hyperplasia, and hyperinsulinemia. J Clin Invest 108:1631-1638.
6. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014-1019.
7. Canoll PD, Kraemer R, Teng KK, Marchionni MA, Salzer JL (1999) GGF/neuregulin induces a phenotypic reversion of oligodendrocytes. Mol Cell Neurosci 13:79-94.
8. Carson MJ, Behringer RR, Brinster RL, McMorris FA (1993) Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 10:729-740.
9. Casaccia-Bonnefil P, Tikoo R, Kiyokawa H, Friedrich V Jr, Chao MV, Koff A (1997) Oligodendrocyte precursor differentiation is perturbed in the absence of the cyclin-dependent kinase inhibitor p27Kip1. Genes Dev 11:2335-2346.
10. Chen S, Velardez MO, Warot X, Yu ZX, Miller SJ, Cros D, Corfas G (2006) Neuregulin 1-erbB signaling is necessary for normal myelination and sensory function. J Neurosci 26:3079-3086.
11. Coggeshall RE (1992) A consideration of neural counting methods. Trends Neurosci 15:9-13.
12. Cui QL, Almazan G (2007) IGF-I-induced oligodendrocyte progenitor proliferation requires PI3K/Akt, MEK/ERK, and Src-like tyrosine kinases. J Neurochem 100:1480-1493.
13. Cui QL, Zheng WH, Quirion R, Almazan G (2005) Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival. J Biol Chem 280:8918-8928.
14. Cui QL, Fogle E, Almazan G (2006) Muscarinic acetylcholine receptors mediate oligodendrocyte progenitor survival through Src-like tyrosine kinases and PI3K/Akt pathways. Neurochem Int 48:383-393.
15. Diehl JA, Cheng M, Roussel MF, Sherr CJ (1998) Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12:3499-3511.
16. Du Y, Lercher LD, Zhou R, Dreyfus CF (2006) Mitogen-activated protein kinase pathway mediates effects of brain-derived neurotrophic factor on differentiation of basal forebrain oligodendrocytes. J Neurosci Res 84:1692-1702.
17. Ebner S, Dunbar M, McKinnon RD (2000) Distinct roles for PI3K in proliferation and survival of oligodendrocyte progenitor cells. J Neurosci Res 62:336-345.
18. Flores AI, Mallon BS, Matsui T, Ogawa W, Rosenzweig A, Okamoto T, Macklin WB (2000) Akt-mediated survival of oligodendrocytes induced by neuregulins. J Neurosci 20:7622-7630.
19. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736.
20. Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates, Ed 3. New York: Academic.
21. Frederick TJ, Min J, Altieri SC, Mitchell NE, Wood TL (2007) Synergistic induction of cyclin D1 in oligodendrocyte progenitor cells by IGF-1 and FGF-2 requires differential stimulation of multiple signaling pathways. Glia 55:1011-1022.
22. Frohman EM, Racke MK, Raine CS (2006) Multiple sclerosis - the plaque and its pathogenesis. N Engl J Med 354:942-955.
23. Fuss B, Mallon B, Phan T, Ohlemeyer C, Kirchhoff F, Nishiyama A, Macklin WB (2000) Purification and analysis of in vivo-differentiated oligodendrocytes expressing the green fluorescent protein. Dev Biol 218:259-274.
24. Hedley-Whyte ET, Kirschner DA (1976) Morphological evidence of alteration in myelin structure with maturation. Brain Res 113:487-497.
25. Hu X, Jin L, Feng L (2004) Erk1/2 but not PI3K pathway is required for neurotrophin 3-induced oligodendrocyte differentiation of post-natal neural stem cells. J Neurochem 90:1339-1347.
26. Hu X, Hicks CW, He W, Wong P, Macklin WB, Trapp BD, Yan R (2006) Bace1 modulates myelination in the central and peripheral nervous system. Nat Neurosci 9:1520-1525.
27. Huang Z, Tang XM, Cambi F (2002) Down-regulation of the retinoblastoma protein (rb) is associated with rat oligodendrocyte differentiation. Mol Cell Neurosci 19:250-262.
28. Hutchinson J, Jin J, Cardiff RD, Woodgett JR, Muller WJ (2001) Activation of Akt (protein kinase B) in mammary epithelium provides a critical cell survival signal required for tumor progression. Mol Cell Biol 21:2203-2212.
29. Inouye H, Karthigasan J, Kirschner DA (1989) Membrane structure in isolated and intact myelins. Biophys J 56:129-137.
30. Jaillard C, Harrison S, Stankoff B, Aigrot MS, Calver AR, Duddy G, Walsh FS, Pangalos MN, Arimura N, Kaibuchi K, Zalc B, Lubetzki C (2005) Edg8/S1P5: an oligodendroglial receptor with dual function on process retraction and cell survival. J Neurosci 25:1459-1469.
31. Jiang H, Duchala CS, Awatramani R, Shumas S, Carlock L, Kamholz J, Garbern J, Scherer SS, Shy ME, Macklin WB (2000) Proteolipid protein mRNA stability is regulated by axonal contact in the rodent peripheral nervous system. J Neurobiol 44:7-19.
32. Jiang H, Guo W, Liang X, Rao Y (2005) Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120:123-135.
33. Kirschner DA, Sidman RL (1976) X-ray diffraction study of myelin structure in immature and mutant mice. Biochim Biophys Acta 448:73-87.
34. Liang G, Cline GW, Macica CM (2007) IGF-1 stimulates de novo fatty acid biosynthesis by Schwann cells during myelination. Glia 55:632-641.
35. Mallon BS, Shick HE, Kidd GJ, Macklin WB (2002) Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22:876-885.
36. Markus A, Zhong J, Snider WD (2002) Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35:65-76.
37. Matsui T, Li L, Wu JC, Cook SA, Nagoshi T, Picard MH, Liao R, Rosenzweig A (2002) Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J Biol Chem 277:22896-22901.
38. Maurel P, Salzer JL (2000) Axonal regulation of Schwann cell proliferation and survival and the initial events of myelination requires PI 3-kinase activity. J Neurosci 20:4635-4645.
39. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700-703.
40. Ness JK, Wood TL (2002) Insulin-like growth factor I, but not neurotrophin-3, sustains Akt activation and provides long-term protection of immature oligodendrocytes from glutamate-mediated apoptosis. Mol Cell Neurosci 20:476-488.
41. Ness JK, Mitchell NE, Wood TL (2002) IGF-I and NT-3 signaling pathways in developing oligodendrocytes: differential regulation and activation of receptors and the downstream effector Akt. Dev Neurosci 24:437-445.
42. 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.
43. Palacios N, Sánchez-Franco F, Fernández M, Sánchez I, Cacicedo L (2005) Intracellular events mediating insulin-like growth factor I-induced oligodendrocyte development: modulation by cyclic AMP. J Neurochem 5:1091-1107.
44. Pang Y, Zheng B, Fan LW, Rhodes PG, Cai Z (2007) IGF-1 protects oligodendrocyte progenitors against TNFalpha-induced damage by activation of PI3K/Akt and interruption of the mitochondrial apoptotic pathway. Glia 55:1099-1107.
45. Peters A, Sethares C, Killiany RJ (2001) Effects of age on the thickness of myelin sheaths in monkey primary visual cortex. J Comp Neurol 435:241-248.
46. Puckett C, Hudson L, Ono K, Friedrich V, Benecke J, Dubois-Dalcq M, Lazzarini RA (1987) Myelin-specific proteolipid protein is expressed in myelinating Schwann cells but is not incorporated into myelin sheaths. J Neurosci Res 18:511-518.
47. Shioi T, McMullen JR, Kang PM, Douglas PS, Obata T, Franke TF, Cantley LC, Izumo S (2002) Akt/protein kinase B promotes organ growth in transgenic mice. Mol Cell Biol 22:2799-2809.
48. Tang DG, Tokumoto YM, Apperly JA, Lloyd AC, Raff MC (2001) Lack of replicative senescence in cultured rat oligodendrocyte precursor cells. Science 291:868-871.
49. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681-694.
50. Trapp BD, Nishiyama A, Cheng D, Macklin W (1997) Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137:459-468.
51. Wight PA, Duchala CS, Readhead C, Macklin WB (1993) A myelin proteolipid protein-LacZ fusion protein is developmentally regulated and targeted to the myelin membrane in transgenic mice. J Cell Biol 123:443-454.
52. Wight PA, Duchala CS, Shick HE, Gudz TI, Macklin WB (2007) Expression of a myelin proteolipid protein (Plp)-lacZ transgene is reduced in both the CNS and PNS of Plp (jp) mice. Neurochem Res 32:343-351.
53. Yates MA, Juraska JM (2007) Increases in size and myelination of the rat corpus callosum during adulthood are maintained into old age. Brain Res 1142:13-18.
54. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K (2005) GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120:137-149.
55. Zaka M, Rafi MA, Rao HZ, Luzi P, Wenger DA (2005) Insulin-like growth factor-1 provides protection against psychosine-induced apoptosis in cultured mouse oligodendrocyte progenitor cells using primarily the PI3K/Akt pathway. Mol Cell Neurosci 30:398-407.