Phosphorylation of syndapin I F-BAR domain at two helix-capping motifs regulates membrane tubulation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 10, 2012, Pages 3760-3765

  Quan, Annie ^a   Xue, Jing ^a   Wielens, Jerome ^b   Smillie, Karen J ^c   Anggono, Victor ^d   Parker, Michael W ^b,e   Cousin, Michael A ^c   Graham, Mark E ^a   Robinson, Phillip J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; MEMBRANE PROTEIN; SYNDAPIN I; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; ENDOCYTOSIS; IN VITRO STUDY; MUTATION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PHOSPHORYLATION; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; ANIMALS; BRAIN; CARRIER PROTEINS; CELL MEMBRANE; ENDOCYTOSIS; HUMANS; LIPID BILAYERS; LIPIDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RATS; SYNAPTOSOMES;

EID: 84857979517     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1108294109     Document Type: Article

References (37)

1. Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: Membranemolding macromolecules. Cell 137:191-196.
2. Peter BJ, et al. (2004) BAR domains as sensors of membrane curvature: The amphiphysin BAR structure. Science 303:495-499. (Pubitemid 38120842)
3. Frost A, et al. (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132:807-817. (Pubitemid 351320580)
4. Plomann M, et al. (1998) PACSIN, a brain protein that is upregulated upon differentiation into neuronal cells. Eur J Biochem 256:201-211. (Pubitemid 28399114)
5. Qualmann B, Roos J, DiGregorio PJ, Kelly RB (1999) Syndapin I a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell 10:501-513. (Pubitemid 29156487)
6. Modregger J, Ritter B, Witter B, Paulsson M, Plomann M (2000) All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci 113:4511-4521. (Pubitemid 32117911)
7. Braun A, et al. (2005) EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 16:3642-3658. (Pubitemid 41078817)
8. Itoh T, et al. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9:791-804. (Pubitemid 41724107)
9. Wang Q, et al. (2009) Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc Natl Acad Sci USA 106: 12700-12705.
10. Rao Y, et al. (2010) Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc Natl Acad Sci USA 107:8213-8218.
11. Anggono V, et al. (2006) Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 9:752-760.
12. Koch D, et al. (2011) Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J, 10.1038/emboj.2011.339.
13. Clayton EL, et al. (2009) The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J Neurosci 29:7706-7717.
14. Dharmalingam E, et al. (2009) F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuromorphogenesis. J Neurosci 29:13315-13327.
15. Schwintzer L, et al. (2011) The functions of the actin nucleator Cobl in cellular morphogenesis critically depend on syndapin I. EMBO J 30:3147-3159.
16. Hilton JM, et al. (2001) Phosphorylation of a synaptic vesicle-associated protein by an inositol hexakisphosphate-regulated protein kinase. J Biol Chem 276:16341-16347.
17. Cousin MA, Robinson PJ (2001) The dephosphins: Dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci 24:659-665. (Pubitemid 33152773)
18. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785. (Pubitemid 23066304)
19. Shimada A, et al. (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129:761-772. (Pubitemid 46813111)
20. Henne WM, et al. (2007) Structure and analysis of FCHo2 F-BAR domain: A dimerizing and membrane recruitment module that effects membrane curvature. Structure 15:839-852. (Pubitemid 47042426)
21. Aurora R, Rose GD (1998) Helix capping. Protein Sci 7:21-38. (Pubitemid 28133743)
22. Wan WY, Milner-White EJ (1999) A recurring two-hydrogen-bond motif incorporating a serine or threonine residue is found both at alpha-helical N termini and in other situations. J Mol Biol 286:1651-1662.
23. Halbach A, et al. (2007) PACSIN 1 forms tetramers via its N-terminal F-BAR domain. FEBS J 274:773-782. (Pubitemid 46144037)
24. Zhou Z, et al. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52:255-269. (Pubitemid 44548348)
25. Gant-Branum RL, Broussard JA, Mahsut A,Webb DJ, McLean JA (2010) Identification of phosphorylation sites within the signaling adaptor APPL1 by mass spectrometry. J Proteome Res 9:1541-1548.
26. Roberts-Galbraith RH, et al. (2010) Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Mol Cell 39:86-99.
27. Tweedie-Cullen RY, Reck JM, Mansuy IM (2009) Comprehensive mapping of posttranslational modifications on synaptic, nuclear, and histone proteins in the adult mouse brain. J Proteome Res 8:4966-4982.
28. Seale JW, Srinivasan R, Rose GD (1994) Sequence determinants of the capping box, a stabilizing motif at the N-termini of alpha-helices. Protein Sci 3:1741-1745. (Pubitemid 24356598)
29. Richardson JS, Richardson DC (1988) Amino acid preferences for specific locations at the ends of alpha helices. Science 240:1648-1652.
30. Hurley JH, Dean AM, Thorsness PE, Koshland DE, Jr, Stroud RM (1990) Regulation of isocitrate dehydrogenase by phosphorylation involves no long-range conformational change in the free enzyme. J Biol Chem 265:3599-3602.
31. Pullen K, et al. (1995) Phosphorylation of serine-46 in HPr, a key regulatory protein in bacteria, results in stabilization of its solution structure. Protein Sci 4:2478-2486.
32. Szilak L, Moitra J, Krylov D, Vinson C (1997) Phosphorylation destabilizes alpha-helices. Nat Struct Biol 4:112-114.
33. Andrew CD, Warwicker J, Jones GR, Doig AJ (2002) Effect of phosphorylation on alphahelix stability as a function of position. Biochemistry 41:1897-1905. (Pubitemid 34132265)
34. Edeling MA, et al. (2009) Structural requirements for PACSIN/Syndapin operation during zebrafish embryonic notochord development. PLoS ONE 4(12):e8150.
35. Kumar V, et al. (2009) Syndapin promotes formation of a postsynaptic membrane system in Drosophila. Mol Biol Cell 20:2254-2264.
36. Guerrier S, et al. (2009) The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138:990-1004.
37. Tsujita K, et al. (2006) Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J Cell Biol 172:269-279. (Pubitemid 43112973)