Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase-c-jun N-terminal kinase pathway

Journal of Neuroscience

Volumn 31, Issue 17, 2011, Pages 6468-6480

  Hirai, Syu Ichi ^a   Banba, Yumi ^a   Satake, Tomoko ^a   Ohno, Shigeo ^a  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL LEUCINE ZIPPER KINASE; PHOSPHOTRANSFERASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; ENZYME ACTIVITY; FEMALE; GROWTH DISORDER; IN VITRO STUDY; MALE; MICROTUBULE; MOUSE; NEOCORTEX; NERVE CELL; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE;

ANIMALS; ANTIBODIES, MONOCLONAL; AXONS; CELL POLARITY; CELLS, CULTURED; DRUG INTERACTIONS; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; MALE; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULES; MITOGEN-ACTIVATED PROTEIN KINASE 8; MODELS, BIOLOGICAL; MUTATION; NEOCORTEX; NERVE TISSUE PROTEINS; NEURITES; NEUROFILAMENT PROTEINS; NEURONS; PACLITAXEL; PHYSICAL STIMULATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFECTION; TUBULIN MODULATORS;

EID: 79955751903     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5038-10.2011     Document Type: Article

References (50)

1. Antonsson B, Kassel DB, Di Paolo G, Lutjens R, Riederer BM, Grenningloh G (1998) Identification of in vitro phosphorylation sites in the growth cone protein SCG10. J Biol Chem 273:8439-8446.
2. Baas PW, Black MM (1990) Individual microtubules in the axon consist of domains that differ in both composition and stability. J Cell Biol 111:495-509.
3. Barnat M, Enslen H, Propst F, Davis RJ, Soares S, Nothias F (2010) Distinct roles of c-Jun N-terminal kinase isoforms in neurite initiation and elongation during axonal regeneration. J Neurosci 30:7804-7816.
4. Barnes AP, Lilley BN, Pan YA, Plummer LJ, Powell AW, Raines AN, Sanes JR, Polleux F (2007) LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129:549-563.
5. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, Leisten JC, Motiwala A, Pierce S, Satoh Y, Bhagwat SS, Manning AM, Anderson DW (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal ki-nase. Proc Natl Acad Sci USA 98:13681-13686.
6. Bloom AJ, Miller BR, Sanes JR, DiAntonio A (2007) The requirement for Phr1 in CNS axon tract formation reveals the corticostriatal boundary as a choice point for cortical axons. Genes Dev 21:2593-2606.
7. Brady ST, Black MM (1986) Axonal transport of microtubule proteins: cy-totypic variation of tubulin and MAPs in neurons. Ann N Y Acad Sci 466:199-217.
8. Canty AJ, Murphy M (2008) Molecular mechanismsof axon guidanceinthe developing corticospinal tract. Prog Neurobiol 85:214-235.
9. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M (2003) JNK1 is required for maintenance of neuronal microtubules and controls phos-phorylation of microtubule-associated proteins. Dev Cell 4:521-533.
10. Collins CA, Wairkar YP, Johnson SL, DiAntonio A (2006) Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51:57-69.
11. de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704-708.
12. Dehmelt L, Smart FM, Ozer RS, Halpain S (2003) The role of microtubule-associated protein 2c in the reorganization of microtubules and lamelli-podia during neurite initiation. J Neurosci 23:9479-9490.
13. Deuel TA, Liu JS, Corbo JC, Yoo SY, Rorke-Adams LB, Walsh CA (2006) Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 49:41-53.
14. Dong C, Yang DD, Tournier C, Whitmarsh AJ, Xu J, Davis RJ, Flavell RA (2000) JNK is required for effector T-cell function but not for T-cell activation. Nature 405:91-94.
15. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
16. Ducret C, Maira SM, Dierich A, Wasylyk B (1999) The net repressor is regulated by nuclear export in response to anisomycin, UV, and heat shock. Mol Cell Biol 19:7076-7087.
17. Gallo KA, Johnson GL (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat Rev Mol Cell Biol 3:663-672.
18. Gdalyahu A, Ghosh I, Levy T, Sapir T, Sapoznik S, Fishler Y, Azoulai D, Reiner O (2004) DCX, a new mediator of the JNK pathway. EMBO J 23:823-832.
19. Grenningloh G, Soehrman S, Bondallaz P, Ruchti E, Cadas H (2004) Role of the microtubule destabilizing proteins SCG10 and stathmin in neuronal growth. J Neurobiol 58:60-69.
20. Hammarlund M, Nix P, Hauth L, Jorgensen EM, Bastiani M (2009) Axon regeneration requires a conserved MAP kinase pathway. Science 323:802-806.
21. Hatanaka Y, Murakami F (2002) In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells. J Comp Neurol 454:1-14.
22. Hirai S, Kawaguchi A, Suenaga J, Ono M, Cui DF, Ohno S (2005) Expression of MUK/DLK/ZPK, an activator of the JNK pathway, in the nervous system of the developing mouse embryo. Gene Expr Patterns 5:517-523.
23. Hirai S, Cui DF, Miyata T, Ogawa M, Kiyonari H, Suda Y, Aizawa S, Banba Y, Ohno S (2006) The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J Neurosci 26:11992-12002.
24. Horesh D, Sapir T, Francis F, Wolf SG, Caspi M, Elbaum M, Chelly J, Reiner O (1999) Doublecortin, a stabilizer of microtubules. Hum Mol Genet 8:1599-1610.
25. Jacobson C, Schnapp B, Banker GA (2006) A change in the selective translocation report of the kinesin-1 motor domain marks the initial specification of the axon. Neuron 49:797-804.
26. 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-3β and its upstream regulators. Cell 120:123-135.
27. Jones L, Lopez-Bendito G, Gruss P, Stoykova A, Molnar Z (2002) Pax6 is required for the normal development of the forebrain axonal connections. Development 129:5041-5052.
28. Koizumi H, Tanaka T, Gleeson JG (2006) Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 49:55-66.
29. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apo-ptosis during early brain development. Neuron 22:667-676.
30. Miller BR, Press C, Daniels RW, Sasaki Y, Milbrandt J, DiAntonio A (2009) A dual leucine kinase-dependent axon self-destruction program promotes Wallerian degeneration. Nat Neurosci 12:387-389.
31. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761-772.
32. Morii H, Shiraishi-Yamaguchi Y, Mori N (2006) SCG10, a microtubule destabilizing factor, stimulates the neurite outgrowth by modulating microtubule dynamics in rat hippocampal primary cultured neurons. J Neurobiol 66:1101-1114.
33. Nakata K, Abrams B, Grill B, Goncharov A, Huang X, Chisholm AD, Jin Y (2005) Regulation of a DLK-1 andp38MAP kinase pathway by the ubiq-uitin ligase RPM-1 is required for presynaptic development. Cell 120:407-420.
34. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136-144.
35. Oliva AA Jr, Atkins CM, Copenagle L, Banker GA (2006) Activated c-Jun N-terminal kinase is required for axon formation. J Neurosci 26:9462-9470.
36. Otto IM, Raabe T, Rennefahrt UE, Bork P, Rapp UR, Kerkhoff E (2000) The p150-Spir protein provides a link between c-Jun N-terminal kinase function and actin reorganization. Curr Biol 10:345-348.
37. Raivich G, Bohatschek M, Da Costa C, Iwata O, Galiano M, Hristova M, Nateri AS, Makwana M, Riera-Sans L, Wolfer DP, Lipp HP, Aguzzi A, Wagner EF, Behrens A (2004) The AP1 transcription factor c-Jun is required for efficient axonal regeneration. Neuron 43:57-67.
38. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM (2007) LKB1/ STRAD promotes axon initiation during neuronal polarization. Cell 129:565-577.
39. Swenson-Fields KI, Sandquist JC, Rossol-Allison J, Blat IC, Wennerberg K, Burridge K, Means AR (2008) MLK3 limits activated Gaq signaling to Rho by binding to p63RhoGEF. Mol Cell 32:43-56.
40. Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996-10001.
41. Tararuk T, Ostman N, Li W, Bjorkblom B, Padzik A, Zdrojewska J, Hongisto V, Herdegen T, Konopka W, Courtney MJ, Coffey ET (2006) JNK1 phosphorylation of SCG10 determines microtubule dynamics and axodendritic length. J Cell Biol 173:265-277.
42. Teng J, Takei Y, Harada A, Nakata T, Chen J, Hirokawa N (2001) Synergistic effects of MAP2 and MAP1B knockout in neuronal migration, dendritic outgrowth, and microtubule organization. J Cell Biol 155:65-76.
43. Tissir F, Bar I, Jossin Y, De Backer O, Goffinet AM (2005) Protocadherin Celsr3 is crucial in axonal tract development. Nat Neurosci 8:451-457.
44. Wang Y, Thekdi N, Smallwood PM, Macke JP, Nathans J (2002) Frizzled-3 is required for the development of major fiber tracts in the rostral CNS. J Neurosci 22:8563-8573.
45. Witte H, Neukirchen D, Bradke F (2008) Microtubule stabilization specifies initial neuronal polarization. J Cell Biol 180:619-632.
46. Yan D, Wu Z, Chisholm AD, Jin Y (2009) The DLK-1 kinase promotes mRNA stability and local translation in C. elegans synapses and axon regeneration. Cell 138:1005-1018.
47. Yi JJ, Barnes AP, Hand R, Polleux F, Ehlers MD (2010) TGF-β signaling specifies axons during brain development. Cell 142:144-157.
48. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K (2005) GSK-3β regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120:137-149.
49. Yuan XB, Jin M, Xu X, Song YQ, Wu CP, Poo MM, Duan S (2003) Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 5:38-45.
50. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD (2004) NGF-induced axon growth is mediated by localized inactivation of GSK-3β and functions of the microtubule plus end binding protein APC. Neuron 42:897-912.