NYAP: A phosphoprotein family that links PI3K to WAVE1 signalling in neurons

EMBO Journal

Volumn 30, Issue 23, 2011, Pages 4739-4754

  Yokoyama, Kazumasa ^a   Tezuka, Tohru ^a   Kotani, Masaharu ^b   Nakazawa, Takanobu ^a   Hoshina, Naosuke ^a,c   Shimoda, Yasushi ^d   Kakuta, Shigeru ^a   Sudo, Katsuko ^a,f   Watanabe, Kazutada ^d   Iwakura, Yoichiro ^a,e   Yamamoto, Tadashi ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b OHU UNIVERSITY   (Japan)

^c OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^d NAGAOKA UNIVERSITY OF TECHNOLOGY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f TOKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Neuron; NYAP; PI3K; Tyrosine phosphorylation; WAVE

Indexed keywords

CONTACTIN; NEURONAL TYROSINE PHOSPHORYLATED ADAPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN; PROTEIN KINASE B; PROTEIN KINASE FYN; PROTEIN P85; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN SIZE; CELL ELONGATION; CELL MIGRATION; CYTOSKELETON; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BRAIN; CYTOSKELETON; HELA CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEOCORTEX; NEURITES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-FYN; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TYROSINE; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

MUS;

EID: 82455208709     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.348     Document Type: Article

References (80)

1. Acosta-Martínez M, Luo J, Elias C, Wolfe A, Levine JE (2009) Malebiased effects of gonadotropin-releasing hormone neuron-specific deletion of the phosphoinositide 3-kinase regulatory subunit p85alpha on the reproductive axis. Endocrinology 150: 4203-4212
2. Ardern H, Sandilands E, Machesky LM, Timpson P, Frame MC, Brunton VG (2006) Src-dependent phosphorylation of Scar1 promotes its association with the Arp2/3 complex. Cell Motil Cytoskeleton 63: 6-13
3. Backman SA, Stambolic V, Suzuki A, Haight J, Elia A, Pretorius J, Tsao MS, Shannon P, Bolon B, Ivy GO, Mak TW (2001) Deletion of Pten in mouse brain causes seizures, ataxia and defects in soma size resembling Lhermitte-Duclos disease. Nat Genet 29: 396-403
4. Bourgeron T (2009) A synaptic trek to autism. Curr Opin Neurobiol 19: 231-234
5. Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11: 297-305
6. Butler MG, Dasouki MJ, Zhou XP, Talebizadeh Z, Brown M, Takahashi TN, Miles JH, Wang CH, Stratton R, Pilarski R, Eng C (2005) Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumor suppressor gene mutations. J Med Genet 42: 318-321
7. Cameron RS, Liu C, Mixon AS, Pihkala JP, Rahn RJ, Cameron PL (2007) Myosin16b: the COOH-tail region directs localization to the nucleus and overexpression delays S-phase progression. Cell Motil Cytoskeleton 64: 19-48
8. Cantrell DA (2001) Phosphoinositide 3-kinase signalling pathways. J Cell Sci 114: 1439-1445
9. Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z, Ismail AM, Umetani J, Billadeau DD, Otwinowski Z, Rosen MK (2010) Structure and control of the actin regulatory WAVE complex. Nature 468: 533-538
10. Dubielecka PM, Machida K, Xiong X, Hossain S, Ogiue-Ikeda M, Carrera AC, Mayer BJ, Kotula L (2010) Abi1/Hssh3bp1 pY213 links Abl kinase signaling to p85 regulatory subunit of PI-3 kinase in regulation of macropinocytosis in LNCaP cells. FEBS Lett 584: 3279-3286
11. Easton RM, Cho H, Roovers K, Shineman DW, Mizrahi M, Forman MS, Lee VM, Szabolcs M, de Jong R, Oltersdorf T, Ludwig T, Efstratiadis A, Birnbaum MJ (2005) Role for Akt3/protein kinase Bg in attainment of normal brain size. Mol Cell Biol 25: 1869-1878
12. Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418: 790-793
13. Eickholt BJ, Ahmed AI, Davies M, Papakonstanti EA, Pearce W, Starkey ML, Bilancio A, Need AC, Smith AJ, Hall SM, Hamers FP, Giese KP, Bradbury EJ, Vanhaesebroeck B (2007) Control of axonal growth and regeneration of sensory neurons by the p110delta PI 3-kinase. PLoS One 2: e869
14. Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137: 191-196
15. Furley AJ, Morton SB, Manalo D, Karagogeos D, Dodd J, Jessell TM (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61: 157-170
16. Goto J, Tezuka T, Nakazawa T, Sagara H, Yamamoto T (2008) Loss of Fyn tyrosine kinase on the C57BL/6 genetic background causes hydrocephalus with defects in oligodendrocyte development. Mol Cell Neurosci 38: 203-212
17. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER (1992) Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258: 1903-1910
18. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279: 509-514
19. Hawkins PT, Eguinoa A, Qiu RG, Stokoe D, Cooke FT, Walters R, Wennström S, Claesson-Welsh L, Evans T, Symons M, Stephens L (1995) PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Curr Biol 5: 393-403
20. Innocenti M, Frittoli E, Ponzanelli I, Falck JR, Brachmann SM, Di Fiore PP, Scita G (2003) Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1. J Cell Biol 160: 17-23
21. International Molecular Genetic Study of Autism Consortium (2001a) A genomewide screen for autism: strong evidence for linkage to chromosomes 2q, 7q, and 16p. Am J Hum Genet 69: 570-581
22. International Molecular Genetic Study of Autism Consortium (2001b) Further characterization of the autism susceptibility locus AUTS1 on chromosome 7q. Hum Mol Genet 10: 973-982
23. Jaworski J, Spangler S, Seeburg DP, Hoogenraad CC, Sheng M (2005) Control of dendritic arborization by the phosphoinositide- 3-kinase-Akt-mammalian target of Rapamycin pathway. J Neurosci 25: 11300-11312
24. Kasahara K, Watanabe K, Kozutsumi Y, Oohira A, Yamamoto T, Sanai Y (2002) Association of GPI-anchored protein TAG-1 with src-family kinase Lyn in lipid rafts of cerebellar granule cells. Neurochem Res 27: 823-829
25. Kassai H, Terashima T, Fukaya M, Nakao K, Sakahara M, Watanabe M, Aiba A (2008) Rac1 in cortical projection neurons is selectively required for midline crossing of commissural axonal formation. Eur J Neurosci 28: 257-267
26. Kim Y, Sung JY, Ceglia I, Lee KW, Ahn JH, Halford JM, Kim AM, Kwak SP, Park JB, Ho Ryu S, Schenck A, Bardoni B, Scott JD, Nairn AC, Greengard P (2006) Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442: 814-817
27. Klippel A, Reinhard C, Kavanaugh WM, Apell G, Escobedo MA, Williams LT (1996) Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol Cell Biol 16: 4117-4127
28. Kobayashi K, Kuroda S, Fukata M, Nakamura T, Nagase T, Nomura N, Matsuura Y, Yoshida-Kubomura N, Iwamatsu A, Kaibuchi K (1998) p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J Biol Chem 273: 291-295
29. Kotani T, Morone N, Yuasa S, Nada S, Okada M (2007) Constitutive activation of neuronal Src causes aberrant dendritic morphogenesis in mouse cerebellar Purkinje cells. Neurosci Res 57: 210-219
30. Kumar V, Zhang M, Swank MW, Kunz J, Wu G (2005) Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J Neurosci 25: 11288-11299
31. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, Baker SJ, Parada LF (2006) Pten regulates neuronal arborization and social interaction in mice. Neuron 50: 377-388
32. Kwon CH, Zhu X, Zhang J, Knoop LL, Tharp R, Smeyne RJ, Eberhart CG, Burger PC, Baker SJ (2001) Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat Genet 29: 404-411
33. Laurino L, Wang XX, de la Houssaye BA, Sosa L, Dupraz S, Cáceres A, Pfenninger KH, Quiroga S (2005) PI3K activation by IGF-1 is essential for the regulation of membrane expansion at the nerve growth cone. J Cell Sci 118: 3653-3662
34. Lebensohn AM, Kirschner MW (2009) Activation of the WAVE complex by coincident signals controls actin assembly. Mol Cell 36: 512-524
35. Leng Y, Zhang J, Badour K, Arpaia E, Freeman S, Cheung P, Siu M, Siminovitch K (2005) Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc Natl Acad Sci USA 102: 1098-1103
36. Morita A, Yamashita N, Sasaki Y, Uchida Y, Nakajima O, Nakamura F, Yagi T, Taniguchi M, Usui H, Katoh-Semba R, Takei K, Goshima Y (2006) Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J Neurosci 26: 2971-2980
37. Nakazawa T, Kuriu T, Tezuka T, Umemori H, Okabe S, Yamamoto T (2008) Regulation of dendritic spine morphology by an NMDA receptor-associated Rho GTPase-activating protein, p250GAP. J Neurochem 105: 1384-1393
38. Napoli I, Mercaldo V, Boyl PP, Eleuteri B, Zalfa F, De Rubeis S, Di Marino D, Mohr E, Massimi M, Falconi M, Witke W, Costa- Mattioli M, Sonenberg N, Achsel T, Bagni C (2008) The fragile ×syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134: 1042-1054
39. Ogawa J, Lee S, Itoh K, Nagata S, Machida T, Takeda Y, Watanabe K (2001) Neural recognition molecule NB-2 of the contactin/F3 subgroup in rat: Specificity in neurite outgrowth-promoting activity and restricted expression in the brain regions. J Neurosci Res 65: 100-110
40. Ohta Y, Hartwig JH, Stossel TP (2006) FilGAP, a Rho- and ROCKregulated GAP for Rac binds filamin A to control actin remodelling. Nat Cell Biol 8: 803-814
41. Oikawa T, Yamaguchi H, Itoh T, Kato M, Ijuin T, Yamazaki D, Suetsugu S, Takenawa T (2004) PtdIns(3,4,5)P3 binding is necessary for WAVE2-induced formation of lamellipodia. Nat Cell Biol 6: 420-426
42. Patel KG, Liu C, Cameron PL, Cameron RS (2001) Myr 8, a novel unconventional myosin expressed during brain development associates with the protein phosphatase catalytic subunits 1a and 1g1. J Neurosci 21: 7954-7968
43. Petrone A, Battaglia F, Wang C, Dusa A, Su J, Zagzag D, Bianchi R, Casaccia-Bonnefil P, Arancio O, Sap J (2003) Receptor protein tyrosine phosphatase alpha is essential for hippocampal neuronal migration and long-term potentiation. EMBO J 22: 4121-4131
44. Ponniah S, Wang DZ, Lim KL, Pallen CJ (1999) Targeted disruption of the tyrosine phosphatase PTPa leads to constitutive downregulation of the kinases Src and Fyn. Curr Biol 9: 535-538
45. Poupon V, Bègue B, Gagnon J, Dautry-Varsat A, Cerf-Bensussan N, Benmerah A (1999) Molecular cloning and characterization of MT-ACT48, a novel mitochondrial acyl-CoA thioesterase. J Biol Chem 274: 19188-19194
46. Qurashi A, Sahin HB, Carrera P, Gautreau A, Schenck A, Giangrande A (2007) HSPC300 and its role in neuronal connectivity. Neural Dev 2: 18
47. Rodgers EE, Theibert AB (2002) Functions of PI 3-kinase in development of the nervous system. Int J Dev Neurosci 20: 187-197
48. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22: 3359-3365
49. Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, Sahai E, Marshall CJ (2008) Rac activation and inactivation control plasticity of tumor cell movement. Cell 135: 510-523
50. Sasaki Y, Cheng C, Uchida Y, Nakajima O, Ohshima T, Yagi T, Taniguchi M, Nakayama T, Kishida R, Kudo Y, Ohno S, Nakamura F, Goshima Y (2002) Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35: 907-920
51. Schenck A, Bardoni B, Langmann C, Harden N, Mandel JL, Giangrande A (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile × protein. Neuron 38: 887-898
52. Schenck A, Bardoni B, Moro A, Bagni C, Mandel JL (2001) A highly conserved protein family interacting with the fragile×mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc Natl Acad Sci USA 98: 8844-8849
53. 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
54. Shimoda Y, Watanabe K (2009) Contactins: emerging key roles in the development and function of the nervous system. Cell Adh Migr 3: 64-70
55. Shinohara M, Terada Y, Iwamatsu A, Shinohara A, Mochizuki N, Higuchi M, Gotoh Y, Ihara S, Nagata S, Itoh H, Fukui Y, Jessberger R (2002) SWAP-70 is a guanine-nucleotide-exchange factor that mediates signalling of membrane ruffling. Nature 416: 759-763
56. Soderling SH, Guire ES, Kaech S, White J, Zhang F, Schutz K, Langeberg LK, Banker G, Raber J, Scott JD (2007) AWAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J Neurosci 27: 355-365
57. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser G, King F, Roberts T, Ratnofsky S, Lechleider RJ, Neel BG, Birge RB, Fajardo JE, Chou MM, Hanafusa H, Schaffhausen B, Cantley LC (1993) SH2 domains recognize specific phosphopeptide sequences. Cell 72: 767-778
58. Sossey-Alaoui K, Li X, Cowell JK (2007) c-Abl-mediated phosphorylation of WAVE3 is required for lamellipodia formation and cell migration. J Biol Chem 282: 26257-26265
59. Sossey-Alaoui K, Li X, Ranalli TA, Cowell JK (2005) WAVE3- mediated cell migration and lamellipodia formation are regulated downstream of phosphatidylinositol 3-kinase. J Biol Chem 280: 21748-21755
60. Steffen A, Rottner K, Ehinger J, Innocenti M, Scita G, Wehland J, Stradal TE (2004) Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J 23: 749-759
61. Stradal TE, Scita G (2006) Protein complexes regulating Arp2/3- mediated actin assembly. Curr Opin Cell Biol 18: 4-10
62. Stuart JR, Gonzalez FH, Kawai H, Yuan ZM (2006) c-Abl interacts with the WAVE2 signaling complex to induce membrane ruffling and cell spreading. J Biol Chem 281: 31290-31297
63. Su J, Muranjan M, Sap J (1999) Receptor protein tyrosine phosphatase a activates Src-family kinases and controls integrin-mediated responses in fibroblasts. Curr Biol 9: 505-511
64. Suetsugu S, Miki H, Takenawa T (1999) Identification of two human WAVE/SCAR homologues as general actin regulatory molecules which associate with the Arp2/3 complex. Biochem Biophys Res Commun 260: 296-302
65. Suetsugu S, Takenawa T (2003) Regulation of cortical actin networks in cell migration. Int Rev Cytol 229: 245-286
66. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T (2003) Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 5: 595-609
67. Taylor JM, Macklem MM, Parsons JT (1999) Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho. J Cell Sci 112: 231-242
68. Tohda C, Nakanishi R, Kadowaki M (2006) Learning deficits and agenesis of synapses and myelinated axons in phosphoinositide-3 kinase-deficient mice. Neurosignals 15: 293-306
69. Tohda C, Nakanishi R, Kadowaki M (2009) Hyperactivity, memory deficit and anxiety-related behaviors in mice lacking the p85alpha subunit of phosphoinositide-3 kinase. Brain Dev 31: 69-74
70. Tolias KF, Cantley LC, Carpenter CL (1995) Rho family GTPases bind to phosphoinositide kinases. J Biol Chem 270: 17656-17659
71. Toyoshima M, Sakurai K, Shimazaki K, Takeda Y, Nakamoto M, Serizawa S, Shimoda Y, Watanabe K (2009) Preferential localization of neural cell recognition molecule NB-2 in developing glutamatergic neurons in the rat auditory brainstem. J Comp Neurol 513: 349-362
72. Tschopp O, Yang ZZ, Brodbeck D, Dummler BA, Hemmings- Mieszczak M, Watanabe T, Michaelis T, Frahm J, Hemmings BA (2005) Essential role of protein kinase Bg (PKBg/Akt3) in postnatal brain development but not in glucose homeostasis. Development 132: 2943-2954
73. Umemori H, Wanaka A, Kato H, Takeuchi M, Tohyama M, Yamamoto T (1992) Specific expressions of Fyn and Lyn, lymphocyte antigen receptor-associated tyrosine kinases, in the central nervous system. Brain Res Mol Brain Res 16: 303-310
74. Viard P, Butcher AJ, Halet G, Davies A, Nürnberg B, Heblich F, Dolphin AC (2004) PI3K promotes voltage-dependent calcium channel trafficking to the plasma membrane. Nat Neurosci 7: 939-946
75. Wang K, Zhang H, Ma D, Bucan M, Glessner JT et al (2009) Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459: 528-533
76. Weiner OD, Rentel MC, Ott A, Brown GE, Jedrychowski M, Yaffe MB, Gygi SP, Cantley LC, Bourne HR, Kirschner MW (2006) Hem- 1 complexes are essential for Rac activation, actin polymerization, and myosin regulation during neutrophil chemotaxis. PLoS Biol 4: e38
77. Ye H, Tan YL, Ponniah S, Takeda Y, Wang SQ, Schachner M, Watanabe K, Pallen CJ, Xiao ZC (2008) Neural recognition molecules CHL1 and NB-3 regulate apical dendrite orientation in the neocortex via PTPa. EMBO J 27: 188-200
78. Yokota Y, Ring C, Cheung R, Pevny L, Anton ES (2007) Nap1- regulated neuronal cytoskeletal dynamics is essential for the final differentiation of neurons in cerebral cortex. Neuron 54: 429-445
79. Yokoyama K, Su I-h, Tezuka T, Yasuda T, Mikoshiba K, Tarakhovsky A, Yamamoto T (2002) BANK regulates BCR-induced calcium mobilization by promoting tyrosine phosphorylation of IP3 receptor. EMBO J 21: 83-92
80. Yokoyama K, Tezuka T, Hoshina N, Nakazawa T, Yamamoto T (2006) Phosphorylation at Tyr-694 of Nogo-A by Src-family kinases. Biochem Biophys Res Commun 349: 1401-1405