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

Journal of Neuroscience

Volumn 25, Issue 27, 2005, Pages 6350-6361

  Björkblom, Benny ^a   Östman, Nina ^a   Hongisto, Vesa ^a   Komarovski, Vladislav ^b   Filén, Jan Jonas ^a   Nyman, Tuula A ^a   Kallunki, Tuula ^c   Courtney, Michael J ^b   Coffey, Eleanor T ^a  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

Dendrite; JNK; MAP2; Morphology; Neuron; Phosphorylation

Indexed keywords

COMPLEMENTARY DNA; MICROTUBULE ASSOCIATED PROTEIN 2; STRESS ACTIVATED PROTEIN KINASE 1;

ANIMAL CELL; ARTICLE; CEREBELLUM; CONTROLLED STUDY; CYTOPLASM; DENDRITE; ENZYME ASSAY; GRANULE CELL; IMMUNOCYTOCHEMISTRY; MICROTUBULE; MOUSE; NERVOUS SYSTEM; NEWBORN; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TWO DIMENSIONAL ELECTROPHORESIS;

ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CEREBELLAR CORTEX; COS CELLS; CYTOSOL; DENDRITES; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE 8; MOTOR CORTEX; NEURONS; PHOSPHORYLATION; PROSENCEPHALON; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

EID: 21844475890     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1517-05.2005     Document Type: Article

References (65)

1. Barrett JN, Crill WE (1974) Influence of dendritic location and membrane properties on the effectiveness of synapses on cat motoneurones. J Physiol (Lond) 239:325-345.
2. Berling B, Wille H, Roll B, Mandelkow EM, Garner C, Maridelkow E (1994) Phosphorylation of microtubule-associated proteins MAP2a,b and MAP2c at Ser136 by proline-directed kinases in vivo and in vitro. Eur J Cell Biol 64:120-130.
3. Bienvenu T, des Portes V, McDonell N, Carrie A, Zemni R, Couvert P, Ropers HH, Moraine C, van Bokhoven H, Fryns JP, Allen K, Walsh CA, Boue I, Kahn A, Chelly I, Beldjord C (2000) Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am J Med Genet 93:294-298.
4. Boucher M, Belanger D, Beaulieu C, Leclerc N (1999) Tau-mediated process outgrowth is differentially altered by the expression of MAP2b and MAP2c in Sf9 cells. Cell Motil Cytoskeleton 42:257-273.
5. Boulton TG, Gregory JS, Cobb MH (1991) Purification and properties of extracellular signal-regulated kinase 1, an insulin-stimulated microtubule-associated protein 2 kinase. Biochemistry 30:278-286.
6. Bozyczko-Coyne D, Saporito MS, Hudkins RL (2002) Targeting the INK pathway for therapeutic benefit in CNS disease. Curr Drug Targets CNS Neurol Disord 1:31-49.
7. Broadbelt K, Byne W, Jones LB (2002) Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex. Schizophr Res 58:75-81.
8. Brown JL, Stowers L, Baer M, Trejo I, Coughlin S, Chant I (1996) Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase pathway. Curr Biol 6:598-605.
9. Brugg B, Matus A (1991) Phosphorylation determines the binding of microtubule-associated protein 2 (MAP2) to microtubules in living cells. J Cell Biol 114:735-743.
10. Burgoyne RD, Cambray-Deakin MA (1988) The cellular neurobiology of neuronal development: the cerebellar granule cell. Brain Res 472:77-101.
11. Byrd DT, Kawasaki M, Walcoff M, Hisamoto N, Matsumoto K, Jin Y (2001) UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 32:787-800.
12. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4:521-533.
13. Coffey ET, Hongisto V, Dickens M, Davis RJ, Courtney MJ (2000) Dual roles for c-Jun N-terminal kinase in developmental and stress responses in cerebellar granule neurons. J Neurosci 20:7602-7613.
14. Coffey ET, Smiciene G, Hongisto V, Cao J, Brecht S, Herdegen T, Courtney MJ (2002) c-Jun N-terminal protein kinase (JNK) 2/3 is specifically activated by stress, mediating c-Jun activation, in the presence of constitutive JNK1 activity in cerebellar neurons. J Neurosci 22:4335-4345.
15. Desai A, Mitchison TJ (1997) Microtubule polymerization dynamics. Annu Rev Cell Dev Biol 13:83-117.
16. Dickens M, Rogers JS, Cavanagh J, Raitano A, Xia Z, Halpern JR, Greenberg ME, Sawyers CL, Davis RJ (1997) A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277:693-696.
17. Fiala JC, Spacek J, Harris KM (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Brain Res Rev 39:29-54.
18. Gdalyahu A, Ghosh I, Levy T, Sapir T, Sapoznik S, Fishier Y, Azoulai D, Reiner O (2004) DCX, a new mediator of the JNK pathway. EMBO J 23:823-832.
19. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N (2002) MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158:541-549.
20. Hausser M, Spruston N, Stuart GJ (2000) Diversity and dynamics of dendritic signaling. Science 290:739-744.
21. Hazzalin CA, Mahadevan LC (2002) MAPK-regulated transcription: a continuously variable gene switch? Nat Rev Mol Cell Biol 3:30-40.
22. Hetman M, Kanning K, Cavanaugh JE, Xia Z (1999) Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase. J Biol Chem 274:22569-22580.
23. Hongisto V, Smeds N, Brecht S, Herdegen T, Courtney MJ, Coffey ET (2003) Lithium blocks the c-Jun stress response and protects neurons via its action on glycogen synthase kinase 3. Mol Cell Biol 23:6027-6036.
24. Huang C, Rajfur Z, Borchers C, Schaller MD, Jacobson K (2003) JNK phosphorylates paxillin and regulates cell migration. Nature 424:219-223.
25. Inomata H, Nakamura Y, Hayakawa A, Takata H, Suzuki T, Miyazawa K, Kitamura N (2003) A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1. J Biol Chem 278:22946-22955.
26. Kallunki T, Su B, Tsigelny I, Sluss HK, Derijard B, Moore G, Davis R, Karin M (1994) JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev 8:2996-3007.
27. Kolb B, Pedersen B, Ballermann M, Gibb R, Whishaw IQ (1999) Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. J Neurosci 19:2337-2346.
28. Kuan CY, Whitmarsh AJ, Yang DD, Liao G, Schloemer AJ, Dong C, Bao J, Banasiak KJ, Haddad GG, Flavell RA, Davis RJ, Rakic P (2003) A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci USA 100:15184-15189.
29. Kyriakis JM, Avruch J (1990) pp54 microtubule-associated protein 2 kinase. A novel serine/threonine protein kinase regulated by phosphorylation and stimulated by poly-L-lysine. J Biol Chem 265:17355-17363.
30. Lamprecht R, LeDoux J (2004) Structural plasticity and memory. Nat Rev Neurosci 5:45-54.
31. Libersat F, Duch C (2004) Mechanisms of dendritic maturation. Mol Neurobiol 29:303-320.
32. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363-366.
33. Malus A (1994) Stiff microtubules and neuronal morphology. Trends Neurosci 17:19-22.
34. McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295-318.
35. McDonald PH, Chow CW, Miller WE, Laporte SA, Field ME, Lin FT, Davis RJ, Lefkowitz RJ (2000) Beta-arrestin 2: a receptor-regulated MAPK scaffold for the activation of JNK3. Science 290:1574-1577.
36. Miller FD, Kaplan DR (2003) Signaling mechanisms underlying dendrite formation. Curr Opin Neurobiol 13:391-398.
37. Mukaetova-Ladinska EB, Arnold H, Jaros E, Perry R, Perry E (2004) Depletion of MAP2 expression and laminar cytoarchitectonic changes in dorsolateral prefrontal cortex in adult autistic individuals. Neuropathol Appl Neurobiol 30:615-623.
38. Nakamura S, Akiguchi I, Kameyama M, Mizuno N (1985) Age-related changes of pyramidal cell basal dendrites in layers III and V of human motor cortex: a quantitative Golgi study. Acta Neuropathol (Berl) 65:281-284.
39. Niu S, Renfro A, Quattrocchi CC, Sheldon M, D'Arcangelo G (2004) Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dabl pathway. Neuron 41:71-84.
40. O'Connell KL, Stults JT (1997) Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis 18:349-359.
41. O'Ferrall EK, Robertson J, Mushynski WE (2000) Inhibition of aberrant and constitutive phosphorylation of the high-molecular-mass neurofilament subunit by CEP-1347 (KT7515), an inhibitor of the stress-activated protein kinase signaling pathway. J Neurochem 75:2358-2367.
42. Park KS, Lee RD, Kang SK, Han SY, Park KL, Yang KH, Song YS, Park HJ, Lee YM, Yun YP, Oh KW, Kim DJ, Yun YW, Hwang SJ, Lee SE, Hong JT (2004) Neuronal differentiation of embryonic midbrain cells by upregulation of peroxisome proliferator-activated receptor-gamma via the JNK-dependent pathway. Exp Cell Res 297:424-433.
43. Peters A, Palay SL, Webster HD (1991) The fine structure of the nervous system. Neurons and their supporting cells. New York: Oxford UP.
44. Quinlan EM, Halpain S (1996) Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron 16:357-368.
45. Riederer BM, Draberova E, Viklkky V, Draber P (1995) Changes of MAP2 phosphorylation during brain development. J Histochem Cytochem 43:1269-1284.
46. Rosoklija G, Toomayan G, Ellis SP, Keilp J, Mann JJ, Latov N, Hays AP, Dwork AJ (2000) Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 57:349-356.
47. Sailer M, Fischl B, Salat D, Tempelmann C, Schonfeld MA, Busa E, Bodammer N, Heinze HJ, Dale A (2003) Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126:1734-1744.
48. Sanchez C, Tompa P, Szucs K, Friedrich P, Avila J (1996) Phosphorylation and dephosphorylation in the proline-rich C-terminal domain of microtubule-associated protein 2. Eur J Biochem 241:765-771.
49. Sanchez C, Diaz-Nido J, Avila J (2000) Phosphorylation of microtubule-associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog Neurobiol 61:133-168.
50. Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131-E136.
51. Shepherd GM (1999) Electronic properties of axons and dendrites. In: Fundamental neuroscience (Zigmond MJ, Bloom FE, Landis SC, Roberts JL, Squire LR, eds), pp 107-127. Toronto: Academic.
52. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamid gels. Anal Chem 68:850-858.
53. Shoichet S (2004) Identification and characterisation of genes involved in cognitive function. Dissertation doi http://www.diss.fu-berlin.de/2004/218/ indexe.html.
54. Silliman CC, Sturgill TW (1989) Phosphorylation of microtubule-associated protein 2 by MAP kinase primarily involves the projection domain. Biochem Biophys Res Commun 160:993-998.
55. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051-1063.
56. Tsuyama S, Terayama Y, Matsuyama S (1987) Numerous phosphates of microtubule-associated protein 2 in living rat brain. J Biol Chem 262:10886-10892.
57. Vaillant AR, Zanassi P, Walsh GS, Aumont A, Alonso A, Miller FD (2002) Signaling mechanisms underlying reversible, activity-dependent dendrite formation. Neuron 34:985-998.
58. Waetzig V, Herdegen T (2003) The concerted signaling of ERK1/2 and JNKs is essential for PC12 cell neuritogenesis and converges at the level of target proteins. Mol Cell Neurosci 24:238-249.
59. Weston CR, Wong A, Hall JP, Goad ME, Flavell RA, Davis RJ (2003) JNK initiates a cytokine cascade that causes Pax2 expression and closure of the optic fissure. Genes Dev 17:1271-1280.
60. Whitford KL, Dijkhuizen P, Polleux F, Ghosh A (2002) Molecular control of cortical dendrite development. Annu Rev Neurosci 25:127-149.
61. Wu GY, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4:151-158.
62. Xia Y, Karin M (2004) The control of cell motility and epithelial morphogenesis by Jun kinases. Trends Cell Biol 14:94-101.
63. Xu X, Raber J, Yang D, Su B, Mucke L (1997) Dynamic regulation of c-Jun N-terminal kinase activity in mouse brain by environmental stimuli. Proc Natl Acad Sci USA 94:12655-12660.
64. 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.
65. Zoghbi HY (2003) Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302:826-830.