Cyclin-dependent kinase 5 mediates adult OPC maturation and myelin repair through modulation of Akt and GsK-3β signaling

Journal of Neuroscience

Volumn 34, Issue 31, 2014, Pages 10415-10429

  Luo, FuCheng ^a   Burke, Kathryn ^a   Kantor, Christopher ^a   Miller, Robert H ^a   Yang, Yan ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cyclin dependent kinase 5; Demyelination; Myelination; Oligodendrocyte; Remyelinatio

Indexed keywords

CYCLIN-DEPENDENT KINASE 5; DEMYELINATION; MYELINATION; OLIGODENDROCYTE; REMYELINATION;

2',3'-CYCLIC NUCLEOTIDE 3'-PHOSPHODIESTERASE; ANALYSIS OF VARIANCE; ANIMALS; CEREBELLUM; CYCLIN-DEPENDENT KINASE 5; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; GLYCOGEN SYNTHASE KINASE 3; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MYELIN SHEATH; OLIGODENDROGLIA; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 84905055328     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0710-14.2014     Document Type: Article

References (55)

1. Aparicio E, Mathieu P, Pereira Luppi M, Almeira Gubiani MF, Adamo AM (2013) The notch signaling pathway: its role in focal CNS demyelination and apotransferrin-induced remyelination. J Neurochem 127: 819-836. CrossRef Medline.
2. Azim K, Butt AM (2011) GSK3beta negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 59: 540-553. CrossRef Medline.
3. Bankston AN, Li W, Zhang H, Ku L, Liu G, Papa F, Zhao L, Bibb JA, Cambi F, Tiwari-Woodruff SK, Feng Y (2013) p39, the primary activator for cyclin-dependent kinase 5 (Cdk5) in oligodendroglia, is essential for oligodendroglia differentiation and myelin repair. J Biol Chem 288: 18047-18057. CrossRef Medline.
4. Bibollet-Bahena O, Almazan G (2009) IGF-1-stimulated protein synthesis in oligodendrocyte progenitors requires PI3K/mTOR/Akt and MEK/ERK pathways. J Neurochem 109: 1440-1451. CrossRef Medline.
5. Birgbauer E, Rao TS, WebbM (2004) Lysolecithin induces demyelination in vitro in a cerebellar slice culture system. J Neurosci Res 78: 157-166. CrossRef Medline.
6. Caillava C, Vandenbosch R, Jablonska B, Deboux C, Spigoni G, Gallo V, Malgrange B, Baron-Van Evercooren A (2011) Cdk2 loss accelerates precursor differentiation and remyelination in the adult central nervous system. J Cell Biol 193: 397-407. CrossRef Medline.
7. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp BD (2000) NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20: 6404-6412. Medline.
8. Fancy SP, Chan JR, Baranzini SE, Franklin RJ, Rowitch DH (2011) Myelin regeneration: a recapitulation of development? Annu Rev Neurosci 34: 21-43. CrossRef Medline.
9. Fang WQ, Ip JP, Li R, Ng YP, Lin SC, Chen Y, Fu AK, Ip NY (2011) Cdk5-mediated phosphorylation of Axin directs axon formation during cerebral cortex development. J Neurosci 31: 13613-13624. CrossRef Medline.
10. Flores AI, Narayanan SP, Morse EN, Shick HE, Yin X, Kidd G, Avila RL, Kirschner DA, Macklin WB (2008) Constitutively active Akt induces enhanced myelination in the CNS. J Neurosci 28: 7174-7183. CrossRef Medline.
11. Foote AK, BlakemoreWF (2005) Inflammation stimulates remyelination in areas of chronic demyelination. Brain 128: 528-539. CrossRef Medline.
12. Franklin RJ (2002) Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 3: 705-714. CrossRef Medline.
13. Franklin RJ, Ffrench-Constant C (2008) Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9: 839-855. CrossRef Medline.
14. Fu AK, Ip FC, Fu WY, Cheung J, Wang JH, Yung WH, Ip NY (2005) Aberrant motor axon projection, acetylcholine receptor clustering, and neurotransmission in cyclin-dependent kinase 5 null mice. Proc Natl Acad Sci U S A 102: 15224-15229. CrossRef Medline.
15. Fyffe-Maricich SL, Schott A, Karl M, Krasno J, Miller RH (2013) Signaling through ERK1/2 controls myelin thickness during myelin repair in the adult central nervous system. J Neurosci 33: 18402-18408. CrossRef Medline.
16. Galimberti D, Macmurray J, Scalabrini D, Fenoglio C, De Riz M, Comi C, Comings D, Cortini F, Villa C, Serpente M, Cantoni C, Ridolfi E, Fardipoor MH, Leone M, Monaco F, Bresolin N, Scarpini E (2011) GSK3beta genetic variability in patients with Multiple Sclerosis. Neurosci Lett 497: 46-48. CrossRef Medline.
17. Gao L, Macklin W, Gerson J, Miller RH (2006) Intrinsic and extrinsic inhibition of oligodendrocyte development by rat retina. Dev Biol 290: 277-286. CrossRef Medline.
18. Gauthier MK, Kosciuczyk K, Tapley L, Karimi-Abdolrezaee S (2013) Dysregulation of the neuregulin-1-ErbB network modulates endogenous oligodendrocyte differentiation and preservation after spinal cord injury. Eur J Neurosci 38: 2693-2715. CrossRef Medline.
19. Ghasemlou N, Jeong SY, Lacroix S, David S (2007) T cells contribute to lysophosphatidylcholine-induced macrophage activation and demyelination in the CNS. Glia 55: 294-302. CrossRef Medline.
20. Gilmore EC, Ohshima T, Goffinet AM, Kulkarni AB, Herrup K (1998) Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J Neurosci 18: 6370-6377. Medline.
21. Guardiola-Diaz HM, Ishii A, Bansal R (2012) Erk1/2 MAPK and mTOR signaling sequentially regulates progression through distinct stages of oligodendrocyte differentiation. Glia 60: 476-486. CrossRef Medline.
22. Gupta A, Tsai LH (2003) Cyclin-dependent kinase 5 and neuronal migration in the neocortex. Neurosignals 12: 173-179. CrossRef Medline.
23. Gupta A, Sanada K, Miyamoto DT, Rovelstad S, Nadarajah B, Pearlman AL, Brunstrom J, Tsai LH (2003) Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat Neurosci 6: 1284-1291. CrossRef Medline.
24. Han MH, Hwang SI, Roy DB, Lundgren DH, Price JV, Ousman SS, Fernald GH, Gerlitz B, RobinsonWH, Baranzini SE, Grinnell BW, Raine CS, Sobel RA, Han DK, Steinman L (2008) Proteomic analysis of active multiple sclerosis lesions reveals therapeutic targets. Nature 451: 1076-1081. CrossRef Medline.
25. Hu X, Schlanger R, He W, Macklin WB, Yan R (2013) Reversing hypomy-elination in BACE1-null mice with Akt-DD overexpression. FASEB J 27: 1868-1873. Medline.
26. Huang JK, Franklin RJ (2011) Regenerative medicine in multiple sclerosis: identifying pharmacological targets of adult neural stem cell differentiation. Neurochem Int 59: 329-332. CrossRef Medline.
27. Huang JK, Jarjour AA, Nait Oumesmar B, Kerninon C, Williams A, Krezel W, Kagechika H, Bauer J, Zhao C, Baron-Van Evercooren A, Chambon P, Ffrench-Constant C, Franklin RJ (2011) Retinoid X receptor gamma signaling accelerates CNS remyelination. Nat Neurosci 14: 45-53. CrossRef Medline.
28. Jeffery ND, Blakemore WF (1997) Locomotor deficits induced by experimental spinal cord demyelination are abolished by spontaneous remyelination. Brain 120: 27-37. CrossRef Medline.
29. Knapp PE, Skoff RP, Sprinkle TJ (1988) Differential expression of galactocerebroside, myelin basic protein, and 2, 3-cyclic nucleotide 3-phosphohydrolase during development of oligodendrocytes in vitro. J Neurosci Res 21: 249-259. CrossRef Medline.
30. Kumar S, Patel R, Moore S, Crawford DK, Suwanna N, Mangiardi M, Tiwari-Woodruff SK (2013) Estrogen receptor beta ligand therapy activates PI3K/Akt/mTOR signaling in oligodendrocytes and promotes remyelination in a mouse model of multiple sclerosis. Neurobiol Dis 56: 131-144. CrossRef Medline.
31. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33: 366-374. CrossRef Medline.
32. Lebrun-Julien F, Bachmann L, Norrmen C, Trotzmuller M, Kofeler H, Ruegg MA, Hall MN, Suter U (2014) Balanced mTORC1 activity in oligodendrocytes is required for accurate CNS myelination. J Neurosci 34: 8432-8448. CrossRef Medline.
33. Lew J, Huang QQ, Qi Z, Winkfein RJ, Aebersold R, Hunt T, Wang JH (1994) A brain-specific activator of cyclin-dependent kinase 5. Nature 371: 423-426. CrossRef Medline.
34. Li BS, Ma W, Jaffe H, Zheng Y, Takahashi S, Zhang L, Kulkarni AB, Pant HC (2003) Cyclin-dependent kinase-5 is involved in neuregulin-dependent activation of phosphatidylinositol 3-kinase and Akt activity mediating neuronal survival. J Biol Chem 278: 35702-35709. CrossRef Medline.
35. Liebetanz D, Merkler D (2006) Effects of commissural de-and remyelination on motor skill behaviour in the cuprizone mouse model of multiple sclerosis. Exp Neurol 202: 217-224. CrossRef Medline.
36. Lyman M, Lloyd DG, Ji X, Vizcaychipi MP, Ma D (2014) Neuroinflammation: the role and consequences. Neurosci Res 79: 1-12. CrossRef Medline.
37. Mi S, Sandrock A, MillerRH (2008) LINGO-1 and its role in CNS repair. Int J Biochem Cell Biol 40: 1971-1978. CrossRef Medline.
38. Miyamoto Y, Yamauchi J, Chan JR, Okada A, Tomooka Y, Hisanaga S, Tanoue A (2007) Cdk5 regulates differentiation of oligodendrocyte precursor cells through the direct phosphorylation of paxillin. J Cell Sci 120: 4355-4366. CrossRef Medline.
39. Miyamoto Y, Yamauchi J, Tanoue A (2008) Cdk5 phosphorylation of WAVE2regulates oligodendrocyte precursor cell migration through nonreceptor tyrosine kinase Fyn. J Neurosci 28: 8326-8337. CrossRef Medline.
40. Narayanan SP, Flores AI, Wang F, Macklin WB (2009) Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci 29: 6860-6870. CrossRef Medline.
41. Ohshima T, Ward JM, Huh CG, Longenecker G, Veeranna, Pant HC, Brady RO, Martin LJ, Kulkarni AB (1996) Targeted disruption of the cyclindependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc Natl Acad SciU S A 93: 11173-11178. CrossRef Medline.
42. Pareek TK, Lam E, Zheng X, Askew D, Kulkarni AB, Chance MR, Huang AY, Cooke KR, Letterio JJ (2010) Cyclin-dependent kinase 5 activity is required for T cell activation and induction of experimental autoimmune encephalomyelitis. J Exp Med 207: 2507-2519. CrossRef Medline.
43. Patrick GN, Zhou P, Kwon YT, Howley PM, Tsai LH (1998) p35, the neuronal-specific activator of cyclin-dependent kinase 5 (Cdk5) is degraded by the ubiquitin-proteasome pathway. J Biol Chem 273: 24057-24064. CrossRef Medline.
44. Patrikios P, Stadelmann C, Kutzelnigg A, Rauschka H, Schmidbauer M, Laursen H, Sorensen PS, Brück W, Lucchinetti C, Lassmann H (2006) Remyelination is extensive in a subset of multiple sclerosis patients. Brain 129: 3165-3172. CrossRef Medline.
45. Setzu A, Lathia JD, Zhao C, Wells K, Rao MS, Ffrench-Constant C, Franklin RJ (2006) Inflammation stimulates myelination by transplanted oligodendrocyte precursor cells. Glia 54: 297-303. CrossRef Medline.
46. Skripuletz T, Hackstette D, Bauer K, Gudi V, Pul R, Voss E, Berger K, Kipp M, Baumgärtner W, StangelM (2013) Astrocytes regulate myelin clearance through recruitment of microglia during cuprizone-induced demyelination. Brain 136: 147-167. CrossRef Medline.
47. Sundaram JR, Chan ES, Poore CP, Pareek TK, Cheong WF, Shui G, Tang N, Low CM, Wenk MR, Kesavapany S (2012) Cdk5/p25-induced cytosolic PLA2-mediated lysophosphatidylcholine production regulates neuroinflammation and triggers neurodegeneration. J Neurosci 32: 1020-1034. CrossRef Medline.
48. Sussman CR, Vartanian T, MillerRH (2005) The ErbB4 neuregulin receptor mediates suppression of oligodendrocyte maturation. J Neurosci 25: 5757-5762. CrossRef Medline.
49. Tsai LH, Takahashi T, Caviness VS Jr, Harlow E (1993) Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119: 1029-1040. Medline.
50. Tsai LH, Delalle I, Caviness VS Jr, Chae T, Harlow E (1994) p35 is a neuralspecific regulatory subunit of cyclin-dependent kinase 5. Nature 371: 419-423. CrossRef Medline.
51. Wang CX, Song JH, Song DK, Yong VW, Shuaib A, Hao C (2006) Cyclindependent kinase-5 prevents neuronal apoptosis through ERK-mediated upregulation of Bcl-2. Cell Death Differ 13: 1203-1212. CrossRef Medline.
52. Wahl SE, McLane LE, Bercury KK, Macklin WB, Wood TL (2014) Mammalian target of rapamycin promotes oligodendrocyte differentiation, initiation and extent of CNS myelination. J Neurosci 34: 4453-4465. CrossRef Medline.
53. Yang Y, Wang H, Zhang J, Luo F, Herrup K, Bibb JA, Lu R, Miller RH (2013) Cyclin-dependent kinase 5 is required for the normal development of oligodendrocytes and myelin formation. Dev Biol 378: 94-106. CrossRef Medline.
54. Yu WP, Collarini EJ, Pringle NP, Richardson WD (1994) Embryonic expression of myelin genes: evidence for a focal source of oligodendrocyte precursors in the ventricular zone of the neural tube. Neuron 12: 1353-1362. CrossRef Medline.
55. Zhang H, Jarjour AA, Boyd A, Williams A (2011) Central nervous system remyelination in culture: a tool for multiple sclerosis research. Exp Neurol 230: 138-148. CrossRef Medline.