ERK2-mediated phosphorylation of par3 regulates neuronal polarization

Journal of Neuroscience

Volumn 33, Issue 33, 2013, Pages 13270-13285

  Funahashi, Yasuhiro ^a,b   Namba, Takashi ^a,b   Fujisue, Shin ^a   Itoh, Norimichi ^a   Nakamuta, Shinichi ^a   Kato, Katsuhiro ^a   Shimada, Akiko ^a   Xu, Chundi ^a   Shan, Wei ^a   Nishioka, Tomoki ^a   Kaibuchi, Kozo ^a,b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GUANINE NUCLEOTIDE EXCHANGE FACTOR; KINESIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEINASE ACTIVATED RECEPTOR 3; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; CONTROLLED STUDY; ELECTROPORATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE MUTATION; GENETIC TRANSFECTION; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MOUSE; NERVE FIBER; NONHUMAN; POLARIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RAT; RNA INTERFERENCE;

ANIMALS; CARRIER PROTEINS; CELL POLARITY; CERCOPITHECUS AETHIOPS; COS CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KINESIN; MICE; MICE, INBRED ICR; MITOGEN-ACTIVATED PROTEIN KINASE 1; NEURONS; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RNA, SMALL INTERFERING; TRANSFECTION; XENOPUS;

EID: 84881528589     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4210-12.2013     Document Type: Article

References (88)

1. Amano M, Mukai H, Ono Y, Chihara K, Matsui T, Hamajima Y, Okawa K, Iwamatsu A, Kaibuchi K (1996) Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science 271:648-650.
2. Arimura N, Kaibuchi K (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8:194-205.
3. Arimura N, Hattori A, Kimura T, Nakamuta S, Funahashi Y, Hirotsune S, Furuta K, Urano T, Toyoshima YY, Kaibuchi K (2009a) CRMP-2 directly binds to cytoplasmic dynein and interferes with its activity. J Neu-rochem 111:380-390.
4. Arimura N, Kimura T, Nakamuta S, Taya S, Funahashi Y, Hattori A, Shimada A, Ménager C, Kawabata S, Fujii K, Iwamatsu A, Segal RA, Fukuda M, Kaibuchi K (2009b) Anterograde transportof TrkB inaxonsismediated by direct interaction with Slp1 and Rab27. Dev Cell 16:675-686.
5. Barnes AP, Polleux F (2009) Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 32:347-381.
6. Bengs F, Scholz A, Kuhn D, Wiese M (2005) LmxMPK9, a mitogen-activated protein kinase homologue affects flagellar length in Leishmania mexicana. Mol Microbiol 55:1606-1615.
7. Berman SA, Wilson NF, Haas NA, Lefebvre PA (2003) A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr Biol 13:1145-1149.
8. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, Gindhart JG, Goldstein LS (2000) Kinesin-dependent axonal transportismediated by the sunday driver (SYD) protein. Cell 103:583-594.
9. Bradke F, Dotti CG (2000) Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr Opin Neurobiol 10:574-581.
10. Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH (2009) Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189-202.
11. Burghoorn J, Dekkers MP, Rademakers S, de Jong T, Willemsen R, Jansen G (2007) Mutation of the MAP kinase DYF-5 affects docking and undock-ing of kinesin-2 motors and reduces their speed in the cilia of Caenorhab-ditis elegans. Proc Natl Acad Sci U S A 104:7157-7162.
12. 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.
13. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, et al. (2005) The transcriptional landscape of the mammalian genome. Science 309:1559-1563.
14. Chen X, Macara IG (2005) Par-3 controls tight junction assembly through the Rac exchange factor Tiam1. Nat Cell Biol 7:262-269.
15. Cheng PL, Song AH, Wong YH, Wang S, Zhang X, Poo MM (2011) Self-amplifying autocrine actions of BDNF in axon development. Proc Natl Acad Sci U S A 108:18430-18435.
16. Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267-310.
17. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
18. Dow LE, Humbert PO (2007) Polarity regulators and the control of epithelial architecture, cell migration, and tumorigenesis. Int Rev Cytol 262: 253-302.
19. Drees F, Gertler FB (2008) Ena/VASP: proteins at the tip of the nervous system. Curr Opin Neurobiol 18:53-59.
20. Errede B, Cade RM, Yashar BM, Kamada Y, Levin DE, Irie K, Matsumoto K (1995) Dynamics and organization of MAP kinase signal pathways. Mol Reprod Dev 42:477-485.
21. Galbraith JA, Reese TS, Schlief ML, Gallant PE (1999) Slow transport of unpolymerized tubulin and polymerized neurofilament inthe squid giant axon. Proc Natl Acad Sci U S A 96:11589-11594.
22. Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13:609-622.
23. Goslin K, Banker G (1989) Experimental observations on the development of polarity by hippocampal neuronsinculture. J Cell Biol 108:1507-1516.
24. Guillaud L, Wong R, Hirokawa N (2008) Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat Cell Biol 10:19-29.
25. Hatanaka Y, Yamauchi K (2013) Excitatory cortical neurons with multipo-lar shape establish neuronal polarity by forming a tangentially oriented axon in the intermediate zone. Cereb Cortex 23:105-113.
26. Hatanaka Y, Hisanaga S, Heizmann CW, Murakami F (2004) Distinct migratory behavior ofearly- and late-born neurons derived from the cortical ventricular zone. J Comp Neurol 479:1-14.
27. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10:682-696.
28. Horiuchi D, Collins CA, Bhat P, Barkus RV, Diantonio A, Saxton WM (2007) Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr Biol 17:1313-1317.
29. Hurd TW, Fan S, Liu CJ, Kweon HK, Hakansson K, Margolis B (2003) Phosphorylation-dependent binding of 14-3-3 to the polarity protein Par3 regulates cell polarity in mammalian epithelia. Curr Biol 13:2082-2090.
30. Iida N, Namikawa K, Kiyama H, Ueno H, Nakamura S, Hattori S (2001) Requirementof Ras for the activation ofmitogen-activated protein kinase by calcium influx, cAMP, and neurotrophin in hippocampal neurons. J Neurosci 21:6459-6466.
31. Inagaki N, Chihara K, Arimura N, Ménager C, Kawano Y, Matsuo N, Nishimura T, Amano M, Kaibuchi K (2001) CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 4:781-782.
32. Insolera R, Chen S, Shi SH (2011) Par proteins and neuronal polarity. Dev Neurobiol 71:483-494.
33. Itoh N, Nakayama M, Nishimura T, Fujisue S, Nishioka T, Watanabe T, Kaibuchi K (2010) Identification of focal adhesion kinase (FAK) and phosphatidylinositol 3-kinase (PI3-kinase) as Par3 partnersby proteomic analysis. Cytoskeleton (Hoboken) 67:297-308.
34. Izumi Y, Hirose T, Tamai Y, Hirai S, Nagashima Y, Fujimoto T, Tabuse Y, Kemphues KJ, Ohno S (1998) An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian ho-mologue of Caenorhabditis elegans polarity protein PAR-3. J Cell Biol 143:95-106.
35. Joberty G, Petersen C, Gao L, Macara IG (2000) The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531-539.
36. Johansson A, Driessens M, Aspenstrom P (2000) The mammalian homo-logue of the Caenorhabditis elegans polarity protein PAR-6 is a binding partner for the Rho GTPases Cdc42 and Rac1. J Cell Sci 113:3267-3275.
37. Kawano Y, Yoshimura T, Tsuboi D, Kawabata S, Kaneko-Kawano T, Shi-rataki H, Takenawa T, Kaibuchi K (2005) CRMP-2 is involved in kinesin-1-dependent transport of the Sra-1/WAVE1 complex and axon formation. Mol Cell Biol 25:9920-9935.
38. 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.
39. Kemphues KJ, Priess JR, Morton DG, Cheng NS (1988) Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52:311-320.
40. Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K (2005) Tubulin and CRMP-2 complex is transported via kinesin-1. J Neurochem 93:1371-1382.
41. Knoblich JA (2001) Asymmetric cell division during animal development. Nat Rev Mol Cell Biol 2:11-20.
42. Kolch W (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat Rev Mol Cell Biol 6:827-837.
43. Kriegstein AR, Noctor SC (2004) Patterns of neuronal migration in the embryonic cortex. Trends Neurosci 27:392-399.
44. Labelle C, Leclerc N (2000) Exogenous BDNF, NT-3 and NT-4 differentially regulate neurite outgrowth in cultured hippocampal neurons. Brain Res Dev Brain Res 123:1-11.
45. Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T (2000) A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2:540-547.
46. LoTurco JJ, Bai J (2006) The multipolar stage and disruptions in neuronal migration. Trends Neurosci 29:407-413.
47. MacKenzie SJ, Baillie GS, McPhee I, Bolger GB, Houslay MD (2000) ERK2 mitogen-activated protein kinase binding, phosphorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases. J Biol Chem 275: 16609-16617.
48. Manabe N, Hirai S, Imai F, Nakanishi H, Takai Y, Ohno S (2002) Association of ASIP/mPAR-3 with adherens junctions of mouse neuroepithelial cells. DevDyn 225:61-69.
49. Markus A, Patel TD, Snider WD (2002) Neurotrophic factors and axonal growth. Curr Opin Neurobiol 12:523-531.
50. McCaffrey LM, Montalbano J, Mihai C, Macara IG (2012) Loss of the Par3 polarity protein promotes breast tumorigenesis and metastasis. Cancer Cell 22:601-614.
51. Mertens AE, Rygiel TP, Olivo C, van der Kammen R, Collard JG (2005) The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex. J Cell Biol 170:1029-1037.
52. Morfini G, DiTella MC, Feiguin F, Carri N, Caceres A (1994) Neurotrophin-3 enhances neurite outgrowth in cultured hippocampal pyramidal neurons. J Neurosci Res 39:219-232.
53. Morrison DK, Davis RJ (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19:91-118.
54. Nagai-Tamai Y, Mizuno K, Hirose T, Suzuki A, Ohno S (2002) Regulated protein-protein interaction between aPKC and PAR-3 plays an essential role in the polarization of epithelial cells. Genes Cells 7:1161-1171.
55. 2+/calmodulin-dependent protein kinases. Sci Signal 4:ra76.
56. Nakayama M, Goto TM, Sugimoto M, Nishimura T, Shinagawa T, Ohno S, Amano M, Kaibuchi K (2008) Rho-kinase phosphorylates PAR-3 and disrupts PAR complex formation. Dev Cell 14:205-215.
57. Namba T, Nakamuta S, Funahashi Y, Kaibuchi K (2011) The role of selective transport in neuronal polarization. Dev Neurobiol 71:445-457.
58. Nishimura T, Kato K, Yamaguchi T, Fukata Y, Ohno S, Kaibuchi K (2004) Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat Cell Biol 6:328-334.
59. Nishimura T, Yamaguchi T, Kato K, Yoshizawa M, Nabeshima Y, Ohno S, Hoshino M, Kaibuchi K (2005) PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1. Nat Cell Biol 7:270-277.
60. Pertz OC, Wang Y, Yang F, Wang W, Gay LJ, Gristenko MA, Clauss TR, Anderson DJ, Liu T, Auberry KJ, Camp DG, Smith RD, Klemke RL (2008) Spatial mapping of the neurite and soma proteomes reveals a functional Cdc42/Rac regulatory network. Proc Natl Acad Sci U S A 105: 1931-1936.
61. Pinto L, Götz M (2007) Radial glial cell heterogeneity: the source of diverse progeny in the CNS. Prog Neurobiol 83:2-23.
62. Qiu RG, Abo A, Steven Martin G (2000) A human homolog of the C. elegans polarity determinant Par-6 links Rac and Cdc42 to PKC zeta signaling and cell transformation. Curr Biol 10:697-707.
63. Reiner O, Sapir T (2009) Polarity regulation in migrating neurons in the cortex. Mol Neurobiol 40:1-14.
64. Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237-246.
65. Sakakibara A, Sato T, Ando R, Noguchi N, Masaoka M, Miyata T (2013) Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cereb Cortex Advance online publication. Retrieved Jan. 10, 2013. doi: 10.1093/cercor/bhs411.
66. Schlager MA, Hoogenraad CC (2009) Basic mechanisms for recognition and transport of synaptic cargos. Mol Brain 2:25.
67. Schwamborn JC, Püschel AW (2004) The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7:923-929.
68. Schwamborn JC, Khazaei MR, Püschel AW (2007) The interaction of mPar3 with the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. J Biol Chem 282:35259-35268.
69. Schwartz ML, Rakic P, Goldman-Rakic PS (1991) Early phenotype expression of cortical neurons: evidence that a subclass of migrating neurons have callosal axons. Proc Natl Acad Sci U S A 88:1354-1358.
70. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM (2007) LKB1/ STRAD promotes axon initiation during neuronal polarization. Cell 129: 565-577.
71. Shi SH, Jan LY, Jan YN (2003) Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112:63-75.
72. Shinoda T, Taya S, Tsuboi D, Hikita T, Matsuzawa R, Kuroda S, Iwamatsu A, Kaibuchi K (2007) DISC1 regulates neurotrophin-induced axon elongation via interaction with Grb2. J Neurosci 27:4-14.
73. Suzuki A, Ohno S (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119:979-987.
74. Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865-872.
75. Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996-10001.
76. Tahirovic S, Bradke F (2009) Neuronal polarity. Cold Spring Harbor Per-spect Biol 1:a001644.
77. Taya S, Shinoda T, Tsuboi D, Asaki J, Nagai K, Hikita T, Kuroda S, Kuroda K, Shimizu M, Hirotsune S, Iwamatsu A, Kaibuchi K (2007) DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J Neurosci 27:15-26.
78. Toda H, Mochizuki H, Flores R 3rd, Josowitz R, Krasieva TB, Lamorte VJ, Suzuki E, Gindhart JG, Furukubo-Tokunaga K, Tomoda T (2008) UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly. Genes Dev 22:3292-3307.
79. Vagnoni A, Rodriguez L, Manser C, De Vos KJ, Miller CC (2011) Phosphor-ylation of kinesin light chain 1 at serine 460 modulates binding and trafficking of calsyntenin-1. J Cell Sci 124:1032-1042.
80. Ventura A, Meissner A, Dillon CP, McManus M, Sharp PA, Van Parijs L, Jaenisch R, Jacks T (2004) Cre-lox-regulated conditional RNA interference from transgenes. Proc Natl Acad Sci U S A 101:10380-10385.
81. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, Rapoport TA, Margolis B (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152:959-970.
82. Wang Y, Du D, Fang L, Yang G, Zhang C, Zeng R, Ullrich A, Lottspeich F, Chen Z (2006) Tyrosine phosphorylated Par3 regulates epithelial tight junction assembly promoted by EGFR signaling. EMBO J 25:5058-5070.
83. Watabe-Uchida M, Govek EE, Van Aelst L (2006) Regulators of Rho GT-Pases in neuronal development. J Neurosci 26:10633-10635.
84. Wiznerowicz M, Szulc J, Trono D (2006) Tuning silence: conditional systems for RNA interference. Nat Methods 3:682-688.
85. 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.
86. Yoshimura T, Arimura N, Kawano Y, Kawabata S, Wang S, Kaibuchi K (2006) Ras regulates neuronal polarity via the PI3-kinase/Akt/GSK- 3beta/CRMP-2 pathway. Biochem Biophys Res Commun 340:62-68.
87. Yoshimura Y, Terabayashi T, Miki H (2010) Par1b/MARK2 phosphorylates kinesin-like motor protein GAKIN/KIF13B to regulate axon formation. Mol Cell Biol 30:2206-2219.
88. Zhou FQ, Snider WD (2006) Intracellular control of developmental and regenerative axon growth. Philos Trans R S Lond B Biol Sci 361:1575-1592.