Identification of neuronal substrates implicates Pak5 in synaptic vesicle trafficking

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

Volumn 109, Issue 11, 2012, Pages 4116-4121

  Strochlic, Todd I ^a   Concilio, Susanna ^a   Viaud, Julien ^b   Eberwine, Ryan A ^a   Wong, Lisa Epstein ^c   Minden, Audrey ^c   Turk, Benjamin E ^d   Plomann, Markus ^e   Peterson, Jeffrey R ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b INSERM   (France)

^c RUTGERS UNIVERSITY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Autoinhibition; F BAR; Kinase substrate; Syndapin1

Indexed keywords

BRAIN EXTRACT; BRAIN PROTEIN; MUTANT PROTEIN; P21 ACTIVATED KINASE 5; PACSIN 1; PROTEIN P55; PROTEIN SERINE THREONINE KINASE; SYNAPTOJANIN 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL MIGRATION; COGNITIVE DEFECT; ENDOCYTOSIS; ENZYME SUBSTRATE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; ION EXCHANGE CHROMATOGRAPHY; ISOTOPE LABELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; MICE; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDES; P21-ACTIVATED KINASES; PHOSPHOPROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN BINDING; SUBSTRATE SPECIFICITY; SYNAPTIC VESICLES;

MURINAE; MUS;

EID: 84858248556     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1116560109     Document Type: Article

References (43)

1. Boda B, Dubos A, Muller D (2010) Signaling mechanisms regulating synapse formation and function in mental retardation. Curr Opin Neurobiol 20:519-527.
2. Nadif Kasri N, Van Aelst L (2008) Rho-linked genes and neurological disorders. Pflugers Arch 455:787-797. (Pubitemid 50003204)
3. Kreis P, Barnier JV (2009) PAK signalling in neuronal physiology. Cell Signal 21:384-393.
4. Nadif Kasri N, Nakano-Kobayashi A, Malinow R, Li B, Van Aelst L (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev 23:1289-1302.
5. Rex CS, et al. (2009) Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation. J Cell Biol 186:85-97.
6. Boda B, et al. (2004) The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J Neurosci 24:10816-10825. (Pubitemid 39602393)
7. Meng J, Meng Y, Hanna A, Janus C, Jia Z (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J Neurosci 25:6641-6650. (Pubitemid 40995296)
8. Kreis P, et al. (2007) The p21-activated kinase 3 implicated in mental retardation regulates spine morphogenesis through a Cdc42-dependent pathway. J Biol Chem 282:21497-21506. (Pubitemid 47099969)
9. Huang W, et al. (2011) p21-Activated kinases 1 and 3 control brain size through coordinating neuronal complexity and synaptic properties. Mol Cell Biol 31:388-403.
10. Li X, Minden A (2003) Targeted disruption of the gene for the PAK5 kinase inmice. Mol Cell Biol 23:7134-7142. (Pubitemid 37210996)
11. Wells CM, Jones GE (2010) The emerging importance of group II PAKs. Biochem J 425:465-473.
12. Arias-Romero LE, Chernoff J (2008) A tale of two Paks. Biol Cell 100:97-108. (Pubitemid 351266767)
13. Qu J, et al. (2003) PAK4 kinase is essential for embryonic viability and for proper neuronal development. Mol Cell Biol 23:7122-7133. (Pubitemid 37210995)
14. Pandey A, et al. (2002) Cloning and characterization of PAK5, a novel member of mammalian p21-activated kinase-II subfamily that is predominantly expressed in brain. Oncogene 21:3939-3948. (Pubitemid 34620863)
15. Lee SR, et al. (2002) AR and ER interaction with a p21-activated kinase (PAK6). Mol Endocrinol 16:85-99. (Pubitemid 34044500)
16. Nekrasova T, Jobes ML, Ting JH, Wagner GC, Minden A (2008) Targeted disruption of the Pak5 and Pak6 genes in mice leads to deficits in learning and locomotion. Dev Biol 322:95-108.
17. Elphick LM, Lee SE, Gouverneur V, Mann DJ (2007) Using chemical genetics and ATP analogues to dissect protein kinase function. ACS Chem Biol 2:299-314. (Pubitemid 350001578)
18. Deacon SW, et al. (2008) An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase. Chem Biol 15:322-331. (Pubitemid 351508427)
19. McPherson PS, et al. (1996) A presynaptic inositol-5-phosphatase. Nature 379:353-357. (Pubitemid 26033932)
20. Cremona O, et al. (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99:179-188. (Pubitemid 29491784)
21. Hutti JE, et al. (2004) A rapid method for determining protein kinase phosphorylation specificity. Nat Methods 1:27-29.
22. Rennefahrt UE, et al. (2007) Specificity profiling of Pak kinases allows identification of novel phosphorylation sites. J Biol Chem 282:15667-15678. (Pubitemid 47093302)
23. 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)
24. Kessels MM, Qualmann B (2004) The syndapin protein family: Linking membrane trafficking with the cytoskeleton. J Cell Sci 117:3077-3086. (Pubitemid 39144341)
25. 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)
26. 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.
27. 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)
28. Huttlin EL, et al. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143:1174-1189.
29. Cotteret S, Chernoff J (2006) Nucleocytoplasmic shuttling of Pak5 regulates its anti-apoptotic properties. Mol Cell Biol 26:3215-3230.
30. Cotteret S, Jaffer ZM, Beeser A, Chernoff J (2003) p21-Activated kinase 5 (Pak5) localizes to mitochondria and inhibits apoptosis by phosphorylating BAD. Mol Cell Biol 23:5526-5539. (Pubitemid 36951321)
31. Dan C, Nath N, Liberto M, Minden A (2002) PAK5, a new brain-specific kinase, promotes neurite outgrowth in N1E-115 cells. Mol Cell Biol 22:567-577. (Pubitemid 34027501)
32. Wong LE, Reynolds AB, Dissanayaka NT, Minden A (2010) p120-catenin is a binding partner and substrate for group B Pak kinases. J Cell Biochem 110:1244-1254.
33. Wu X, Carr HS, Dan I, Ruvolo PP, Frost JA (2008) p21 activated kinase 5 activates Raf-1 and targets it to mitochondria. J Cell Biochem 105:167-175.
34. Matenia D, et al. (2005) PAK5 kinase is an inhibitor of MARK/Par-1, which leads to stable microtubules and dynamic actin. Mol Biol Cell 16:4410-4422. (Pubitemid 41262907)
35. 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.
36. Kim WT, et al. (2002) Delayed reentry of recycling vesicles into the fusion-competent synaptic vesicle pool in synaptojanin 1 knockout mice. Proc Natl Acad Sci USA 99:17143-17148. (Pubitemid 36034112)
37. 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.
38. Roberts-Galbraith RH, Gould KL (2010) Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9:4091-4097.
39. Perez-Otano I, et al. (2006) Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat Neurosci 9:611-621. (Pubitemid 44012258)
40. Mani M, et al. (2007) The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56:1004-1018. (Pubitemid 350251112)
41. Gong LW, De Camilli P (2008) Regulation of postsynaptic AMPA responses by synaptojanin 1. Proc Natl Acad Sci USA 105:17561-17566.
42. Lee HK, Kirkwood A (2011) AMPA receptor regulation during synaptic plasticity in hippocampus and neocortex. Semin Cell Dev Biol 5:514-520.
43. Zalc B, Goujet D, Colman D (2008) The origin of the myelination program in vertebrates. Curr Biol 18:R511-512. (Pubitemid 351842651)