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PMID: 17290217 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Role of activation of PIP5Kgamma661 by AP-2 complex in synaptic vesicle endocytosis.

The EMBO journal ·Vol. 26 ·No. 4 ·2007-02-21 ·Pages 1105-16

Nakano-Kobayashi A, Yamazaki M, Unoki T, Hongu T, Murata C, Taguchi R, Katada T, Frohman MA, Yokozeki T, Kanaho Y

Abstract

Synaptic vesicles (SVs) are retrieved by clathrin-mediated endocytosis at the nerve terminals. Phosphatidylinositol 4,5-bisphosphate [PI(4,5)P2] drives this event by recruiting the components of the endocytic machinery. However, the molecular mechanisms that result in local generation of PI(4,5)P2 remain unclear. We demonstrate here that AP-2 complex directly interacts with phosphatidylinositol 4-phosphate 5-kinase gamma661 (PIP5Kgamma661), the major PI(4,5)P2-producing enzyme in the brain. The beta2 subunit of AP-2 was found to bind to the C-terminal tail of PIP5Kgamma661 and cause PIP5Kgamma661 activation. The interaction is regulated by PIP5Kgamma661 dephosphorylation, which is triggered by depolarization in mouse hippocampal neurons. Finally, overexpression of the PIP5Kgamma661 C-terminal region in hippocampal neurons suppresses depolarization-dependent SV endocytosis. These findings provide evidence for the molecular mechanism through which PIP5Kgamma661 locally generates PI(4,5)P2 in hippocampal neurons and suggest a model in which the interaction trigger SV endocytosis.

MeSH Terms
Adaptor Protein Complex 2/metabolism Animals Endocytosis/physiology Enzyme Activation/physiology Hippocampus/metabolism Immunohistochemistry Mice Models, Biological Neurons/metabolism Phosphatidylinositol 4,5-Diphosphate/metabolism Phosphotransferases (Alcohol Group Acceptor)/metabolism Synaptic Vesicles/metabolism,physiology
Chemicals
Adaptor Protein Complex 2 Phosphatidylinositol 4,5-Diphosphate Phosphotransferases (Alcohol Group Acceptor) 1-phosphatidylinositol-4-phosphate 5-kinase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Nakano-Kobayashi Akiko
Department of Physiological Chemistry, Graduate School of Comprehensive Human Sciences and Institute of Basic Medical Sciences, University of Tsukuba, Tsukuba, Japan.
Yamazaki Masakazu
Unoki Takamitsu
Hongu Tsunaki
Murata Chie
Taguchi Ryo
Katada Toshiaki
Frohman Michael A
Yokozeki Takeaki
Kanaho Yasunori
References (47)
47 references, click to expand
  1. Stabilization of clathrin coats by the core of the clathrin-associated protein complex AP-2.
    Biochemistry. 1990 Dec 4;29(48):10791-8 PMID: 2125494
  2. Stimulation of phosphatidylinositol kinase type I-mediated phosphatidylinositol (4,5)-bisphosphate synthesis by AP-2mu-cargo complexes.
    Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):11934-9 PMID: 16880396
  3. A clathrin-binding site in the hinge of the beta 2 chain of mammalian AP-2 complexes.
    J Biol Chem. 1995 Dec 29;270(52):31083-90 PMID: 8537368
  4. Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase.
    J Biol Chem. 1996 Sep 27;271(39):23611-4 PMID: 8798574
  5. The phosphatidylinositol 4-phosphate 5-kinase family.
    Adv Enzyme Regul. 1996;36:115-40 PMID: 8869744
  6. Beta3A-adaptin, a subunit of the adaptor-like complex AP-3.
    J Biol Chem. 1997 Jun 13;272(24):15078-84 PMID: 9182526
  7. Type I phosphatidylinositol-4-phosphate 5-kinases. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family.
    J Biol Chem. 1998 Apr 10;273(15):8741-8 PMID: 9535851
  8. Cloning of the gene encoding the murine clathrin-associated adaptor medium chain mu 2: gene organization, alternative splicing and chromosomal assignment.
    Gene. 1998 Apr 14;210(2):187-93 PMID: 9573360
  9. Role of phosphorylation in regulation of the assembly of endocytic coat complexes.
    Science. 1998 Aug 7;281(5378):821-4 PMID: 9694653
  10. Identification and characterization of novel clathrin adaptor-related proteins.
    J Biol Chem. 1998 Sep 18;273(38):24693-700 PMID: 9733768
  11. Structure of type IIbeta phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation.
    Cell. 1998 Sep 18;94(6):829-39 PMID: 9753329
  12. Real-time visualization of PH domain-dependent translocation of phospholipase C-delta1 in renal epithelial cells (MDCK): response to hypo-osmotic stress.
    Biochem Biophys Res Commun. 1999 Jan 19;254(2):284-91 PMID: 9918830
  13. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits.
    J Cell Biol. 1999 Aug 23;146(4):755-64 PMID: 10459011
  14. Evolving nature of the AP2 alpha-appendage hub during clathrin-coated vesicle endocytosis.
    EMBO J. 2004 Nov 10;23(22):4371-83 PMID: 15496985
  15. Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation.
    Cell. 1999 Nov 24;99(5):521-32 PMID: 10589680
  16. Protein phosphorylation is required for endocytosis in nerve terminals: potential role for the dephosphins dynamin I and synaptojanin, but not AP180 or amphiphysin.
    J Neurochem. 2001 Jan;76(1):105-16 PMID: 11145983
  17. Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis.
    Science. 2001 Feb 9;291(5506):1047-51 PMID: 11161217
  18. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes.
    Science. 2001 Feb 9;291(5506):1051-5 PMID: 11161218
  19. Similar subunit interactions contribute to assembly of clathrin adaptor complexes and COPI complex: analysis using yeast three-hybrid system.
    Biochem Biophys Res Commun. 2001 Jun 22;284(4):1083-9 PMID: 11409905
  20. PIP kinase Igamma is the major PI(4,5)P(2) synthesizing enzyme at the synapse.
    Neuron. 2001 Oct 11;32(1):79-88 PMID: 11604140
  21. The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis.
    Trends Neurosci. 2001 Nov;24(11):659-65 PMID: 11672811
  22. Molecular architecture and functional model of the endocytic AP2 complex.
    Cell. 2002 May 17;109(4):523-35 PMID: 12086608
  23. A phosphatidylinositol (4,5)-bisphosphate binding site within mu2-adaptin regulates clathrin-mediated endocytosis.
    J Cell Biol. 2002 Jul 22;158(2):209-14 PMID: 12119359
  24. Calcium-regulated exocytosis of dense-core vesicles requires the activation of ADP-ribosylation factor (ARF)6 by ARF nucleotide binding site opener at the plasma membrane.
    J Cell Biol. 2002 Oct 14;159(1):79-89 PMID: 12379803
  25. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin.
    Nature. 2002 Nov 7;420(6911):85-9 PMID: 12422219
  26. Type I gamma phosphatidylinositol phosphate kinase targets and regulates focal adhesions.
    Nature. 2002 Nov 7;420(6911):89-93 PMID: 12422220
  27. Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/Thr205 of human tau.
    J Biol Chem. 2002 Nov 15;277(46):44525-30 PMID: 12226093
  28. Single synaptic vesicles fusing transiently and successively without loss of identity.
    Nature. 2003 Jun 5;423(6940):643-7 PMID: 12789339
  29. ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma.
    J Cell Biol. 2003 Jul 7;162(1):113-24 PMID: 12847086
  30. Cdk5 is essential for synaptic vesicle endocytosis.
    Nat Cell Biol. 2003 Aug;5(8):701-10 PMID: 12855954
  31. Cell biology of the presynaptic terminal.
    Annu Rev Neurosci. 2003;26:701-28 PMID: 14527272
  32. Formation of an endophilin-Ca2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis.
    Cell. 2003 Oct 3;115(1):37-48 PMID: 14532001
  33. Cophosphorylation of amphiphysin I and dynamin I by Cdk5 regulates clathrin-mediated endocytosis of synaptic vesicles.
    J Cell Biol. 2003 Nov 24;163(4):813-24 PMID: 14623869
  34. Localization of mRNAs for phosphatidylinositol phosphate kinases in the mouse brain during development.
    Brain Res Gene Expr Patterns. 2002 Jan;1(2):123-33 PMID: 15018809
  35. A novel neuronal-specific splice variant of Type I phosphatidylinositol 4-phosphate 5-kinase isoform gamma.
    Biochem J. 2004 Apr 15;379(Pt 2):489-96 PMID: 14741049
  36. The synaptic vesicle cycle.
    Annu Rev Neurosci. 2004;27:509-47 PMID: 15217342
  37. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking.
    Nature. 2004 Sep 23;431(7007):415-22 PMID: 15386003
  38. A role for talin in presynaptic function.
    J Cell Biol. 2004 Oct 11;167(1):43-50 PMID: 15479735
  39. Limited proteolytic digestion of coated vesicle assembly polypeptides abolishes reassembly activity.
    J Cell Biochem. 1985;28(1):47-58 PMID: 2863276
  40. Clathrin-coated vesicle assembly polypeptides: physical properties and reconstitution studies with brain membranes.
    J Cell Biol. 1988 Jan;106(1):39-50 PMID: 2892842
  41. Deep-etch visualization of proteins involved in clathrin assembly.
    J Cell Biol. 1988 Sep;107(3):877-86 PMID: 3417785
  42. Production and characterization of monoclonal antibodies that bind to phosphatidylinositol 4,5-bisphosphate.
    Mol Immunol. 1988 Oct;25(10):1025-31 PMID: 2851103
  43. Structural and functional division into two domains of the large (100- to 115-kDa) chains of the clathrin-associated protein complex AP-2.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2612-6 PMID: 2495531
  44. Regulation of the interaction between PIPKI gamma and talin by proline-directed protein kinases.
    J Cell Biol. 2005 Feb 28;168(5):789-99 PMID: 15738269
  45. Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis.
    J Biol Chem. 2005 Nov 11;280(45):37901-7 PMID: 16162509
  46. Type Igamma661 phosphatidylinositol phosphate kinase directly interacts with AP2 and regulates endocytosis.
    J Biol Chem. 2006 Jul 21;281(29):20632-42 PMID: 16707488
  47. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons.
    Neuron. 1993 Oct;11(4):713-24 PMID: 8398156
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2007-02-21
Epub
2007-00-08
Pages
1105-16
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1852847
Subset
IM
Grants
NIGMS NIH HHS · R01 GM071520 · United States
NIGMS NIH HHS · R01 GM71520 · United States
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