The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex

Journal of Neuroscience

Volumn 26, Issue 46, 2006, Pages 11992-12002

  Hirai, Syu Ichi ^a   De, Feng Cui ^a   Miyata, Takaki ^b   Ogawa, Masaharu ^c   Kiyonari, Hiroshi ^d   Suda, Yoko ^d   Aizawa, Shinichi ^d   Banba, Yumi ^a   Ohno, Shigeo ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d RIKEN   (Japan)

Author keywords

Axon; c Jun; Cerebral cortex; Microtubules; Migration; Pyramidal cell

Indexed keywords

DOUBLECORTIN; DUAL LEUCINE ZIPPER KINASE; ENZYME; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE DISRUPTION; GENE TARGETING; MALE; MORPHOGENESIS; MOUSE; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CEREBRAL CORTEX; CHIMERA; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; GROWTH CONES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, INBRED ICR; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL PATHWAYS; NEUROPEPTIDES; ORGAN CULTURE TECHNIQUES; PROTO-ONCOGENE PROTEINS C-JUN; PYRAMIDAL CELLS;

EID: 33751082080     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2272-06.2006     Document Type: Article

References (54)

1. Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S, Quattrocchi CC, Antalffy BA, Sheldon M, Armstrong DD, Wynshaw-Boris A, Herz J, D'Arcangelo G, Clark GD (2003) Interaction of reelin signaling and Lis1 in brain development. Nat Genet 35:270-276.
2. 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 kinase. Proc Natl Acad Sci USA 98:13681-13686.
3. Björkblom B, Östman N, Hongisto V, Komarovski V, Filén J-J, Nyman TA, Kallunki T, Courtney MJ, Coffey ET (2005) Constitutively active cytoplasmic c-Jun N-terminal kinase 1 is a dominant regulator of dendritic architecture: role of microtubule-associated protein 2 as an effector. J Neurosci 25:6350-6351.
4. Caspi M, Atlas R, Kantor A, Sapir T, Reiner O (2000) Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum Mol Genet 9:2205-2213.
5. Chang L, Jones Y, Ellisman MH, Goldstein LSB, Karin M (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4:521-533.
6. Chi H, Sarkisian MR, Rakic P, Flavell RA (2005) Loss of mitogen-activated protein kinase kinase kinase 4 (MEKK4) results in enhanced apoptosis and defective neural tube development. Proc Natl Acad Sci USA 102:3846-3851.
7. Deuel TAS, Liu JS, Corbo JC, Yoo S-Y, Rorke-Adams LB, Walsh CA (2006) Genetic interactions between Doublecortin and Doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 49:41-53.
8. Drewes G, Ebneth A, Preuss U, Mandelkow E-M, Mandelkow E (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297-308.
9. Gallo KA, Johnson GL (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat Rev Mol Cell Biol 3:663-672.
10. 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.
11. Gleeson JG, Walsh CA (2000) Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci 23:352-359.
12. Godfraind C, Schachner M, Goffinet AM (1988) Immunohistological localization of cell adhesion molecules L1, J1, N-CAM and their common carbohydrate L2 in the embryonic cortex of normal and reeler mice. Brain Res 470:99-111.
13. 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.
14. Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
15. Hibi M, Lin A, Smeal T, Minden A, Karin M (1993) Identification of an oncoprotein- and UV-responsive protein kinae that binds and potentiates the c-Jun activation domain. Genes Dev 7:2135-2148.
16. Hirai S, Kawaguchi A, Hirasawa R, Baba M, Ohnishi T, Ohno S (2002) MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo. Development 129:4483-4495.
17. 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.
18. 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.
19. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M (2003) The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J 22:4190-4201.
20. Kelkar N, Delmotte M-H, Weston CR, Barrett T, Sheppard BJ, Flabell RA, Davis RJ (2003) Morphogenesis of the telencephalic commissure requires scaffold protein JNK-interacting protein 3 (JIP3). Proc Natl Acad Sci USA 100:9843-9848.
21. Kerjan G, Dolan J, Haumaitre C, Schneider-Maunoury S, Fujisawa H, Mitchell K, Chédotal A (2005) The transmembrane semaphoring Sema6A controls cerebellar granule cell migration. Nat Neurosci 8:1516-1524.
22. Kholmanskikh SS, Koeller HB, Wynshaw-Boris A, Gomez T, Letourneau PC, Ross ME (2006) Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat Neurosci 9:50-57.
23. Koizumi H, Tanaka T, Gleeson J (2006) Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 49:55-66.
24. 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 apoptosis during early brain development. Neuron 22:667-676.
25. López-Bendito G, Cautinat A, Sánchez JA, Bielle F, Flames N, Garratt AN, Talmage DA, Role LW, Charnay P, Marín O, Garel S (2006) Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125:127-142.
26. Magdaleno SM, Curran T (2001) Brain development: integrins and the Reelin pathway. Curr Biol 11:R1032-R1035.
27. Martín-Blanco E (1997) Regulation of cell differentiation by the Drosophila Jun kinase cascade. Curr Opin Genet Dev 7:666-671.
28. Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727-741.
29. Nadarajah B, Brunstrom JE, Grutzendler J, Wong ROL, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143-150.
30. Nakata K, Abrams B, Grill B, Goncharov A, Huang X, Chisholm AD, Jin Y (2005) Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120:407-420.
31. Niethammer M, Smith DS, Ayala R, Peng J, Ko J, Lee M-S, Morabito M, Tsai L-H (2000) NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697-711.
32. Noctor S, Martínes-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.
33. Ohshima T, Ogawa M, Veeranna, Hirasawa M, Longenecker G, Ishiguro K, Pant HC, Brady RO, Kulkarni AB, Mikoshiba K (2001) Synergistic contributions of cyclin-dependent kinase 5/p35 and Reelin/Dab1 to the positioning of cortical neurons in the developing mouse brain. Proc Natl Acad Sci USA 98:2764-2769.
34. Parnavelas JG (2000) The origin and migration of cortical neurons: new vistas. Trends Neurosci 23:126-131.
35. Rakic P (1990) Principles of neural cell migration. Experientia 46:882-891.
36. Rege TA, Hagood JS (2006) Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J 20:1045-1054.
37. Richards LJ, Koester SE, Tuttle R, O'Leary DM (1997) Directed growth of early cortical axons is influenced by a chemoattractant released from an intermediate target. J Neurosci 17:2445-2458.
38. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC (2004) Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 8:34-42.
39. Sakai K, Miyazaki J (1997) A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the cre transgene transmission. Biochem Biophys Res Commun 237:318-324.
40. Schaar BT, Kinoshita K, McConnell SK (2004) Doublecortin microtubule affinity is a regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 41:203-213.
41. Schmid RS, Shelton S, Stanco A, Yokota Y, Kreidberg JA, Anton ES (2004) α3β1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development. Development 131:6023-6031.
42. Stensaas LJ, Stensaas SS (1968) An electron microscope study of cells in the matrix and intermediate laminae of the cerebral hemisphere of the 45mm rabbit embryo. Z Zellforsch Mikrosk Anat 91:341-365.
43. Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996-10001.
44. Tamagnone L, Comoglio PM (2004) To move or not to move? EMBO Rep 5:356-361.
45. Tanaka T, Serneo FF, Tseng H-C, Kulkarni AB, Tsai L-H, Gleeson JG (2004) Cdk5 phosphorylation of Doublecortin Ser297 regulates its effect on neuronal migration. Neuron 41:215-227.
46. Tararuk T, Östman N, Li W, Björkblom 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.
47. 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.
48. Tissir F, Bar I, Jossin Y, DeBacker O, Goffinet AM (2005) Protocadherin Celsr3 is crucial in axonal tract development. Nat Neurosci 9:451-457.
49. Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689-701.
50. Tsai J-W, Chen Y, Kriegstein AR, Vallee RB (2005) Lis1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J Cell Biol 170:935-945.
51. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180.
52. Xia Y, Karin M (2004) The control of cell motility and epithelial morphogenesis by Jun kinas. Trends Cell Biol 14:94-101.
53. Yoshida H, Hastie CJ, McLauchlan H, Cohen P, Goedert M (2004) Phosphorylation of microtubule-associated protein tau by isoforms of c-Jun N-terminal kinase (JNK). J Neurochem 90:352-358.
54. 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.