Activity-dependent facilitation of Synaptojanin and synaptic vesicle recycling by the Minibrain kinase

Nature Communications

Volumn 5, Issue , 2014, Pages

  Chen, Chun Kan ^a   Bregere, Catherine ^a   Paluch, Jeremy ^b   Lu, Jason F ^a   Dickman, Dion K ^b   Chang, Karen T ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MINIBRAIN KINASE; PROTEIN SERINE THREONINE KINASE; SYNAPTOJANIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; MINIBRAIN PROTEIN, DROSOPHILA; NERVE PROTEIN; PHOSPHATASE;

CALIBRATION; ENZYME ACTIVITY; NERVOUS SYSTEM; NEUROLOGY; SIGNALING;

ARTICLE; AUTISM; CONTROLLED STUDY; DOWN SYNDROME; ENDOCYTOSIS; ENZYME ACTIVITY; FACILITATION; IN VIVO STUDY; NERVE CELL; NERVE CELL GROWTH; NERVE CELL STIMULATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNAPTOSOME; UPREGULATION; ANIMAL; DROSOPHILA; ENZYMOLOGY; GENETICS; METABOLISM; NEUROMUSCULAR JUNCTION; PHOSPHORYLATION; PHYSIOLOGY; SYNAPSE;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; ENDOCYTOSIS; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SYNAPSES; SYNAPTIC VESICLES;

EID: 84903624810     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5246     Document Type: Article

References (70)

1. Cousin, M. A., Tan, T. C. & Robinson, P. J. 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. 76, 105-116 (2001). (Pubitemid 32044373)
2. Slepnev, V. I., Ochoa, G. C., Butler, M. H., Grabs, D. & De Camilli, P. Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281, 821-824 (1998). (Pubitemid 28376042)
3. Greengard, P., Valtorta, F., Czernik, A. J. & Benfenati, F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259, 780-785 (1993). (Pubitemid 23066304)
4. Clayton, E. L. et al. Dynamin I phosphorylation by GSK3 controls activitydependent bulk endocytosis of synaptic vesicles. Nat. Neurosci. 13, 845-851 (2010).
5. Matta, S. et al. LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis. Neuron 75, 1008-1021 (2012).
6. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002). (Pubitemid 35425239)
7. Guimera, J., Casas, C., Estivill, X. & Pritchard, M. Human minibrain homologue (MNBH/DYRK1): characterization, alternative splicing, differential tissue expression, and overexpression in Down syndrome. Genomics 57, 407-418 (1999). (Pubitemid 29239228)
8. O'Roak, B. J. et al. Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 338, 1619-1622 (2012).
9. Iossifov, I. et al. De novo gene disruptions in children on the autistic spectrum. Neuron 74, 285-299 (2012).
10. Park, J., Oh, Y. & Chung, K. C. Two key genes closely implicated with the neuropathological characteristics in Down syndrome: DYRK1A and RCAN1. BMB Rep. 42, 6-15 (2009).
11. Dierssen, M. Down syndrome: the brain in trisomic mode. Nat. Rev. Neurosci. 13, 844-858 (2012).
12. Himpel, S. et al. Specificity determinants of substrate recognition by the protein kinase DYRK1A. J. Biol. Chem. 275, 2431-2438 (2000). (Pubitemid 30082003)
13. Campbell, L. E. & Proud, C. G. Differing substrate specificities of members of the DYRK family of arginine-directed protein kinases. FEBS Lett. 510, 31-36 (2002). (Pubitemid 34084879)
14. Tejedor, F. et al. minibrain: a new protein kinase family involved in postembryonic neurogenesis in Drosophila. Neuron 14, 287-301 (1995).
15. Fotaki, V. et al. Dyrk1A haploinsufficiency affects viability and causes developmental delay and abnormal brain morphology in mice. Mol. Cell Biol. 22, 6636-6647 (2002).
16. Arque, G. et al. Impaired spatial learning strategies and novel object recognition in mice haploinsufficient for the dual specificity tyrosine-regulated kinase-1A (Dyrk1A). PLoS ONE 3, e2575 (2008).
17. Ahn, K. J. et al. DYRK1A BAC transgenic mice show altered synaptic plasticity with learning and memory defects. Neurobiol. Dis. 22, 463-472 (2006).
18. Altafaj, X. et al. Neurodevelopmental delay, motor abnormalities and cognitive deficits in transgenic mice overexpressing Dyrk1A (minibrain), a murine model of Down's syndrome. Hum. Mol. Genet. 10, 1915-1923 (2001). (Pubitemid 32910536)
19. Tejedor, F. J. & Hammerle, B. MNB/DYRK1A as a multiple regulator of neuronal development. FEBS J. 278, 223-235 (2011).
20. Hammerle, B. et al. Mnb/Dyrk1A is transiently expressed and asymmetrically segregated in neural progenitor cells at the transition to neurogenic divisions. Dev. Biol. 246, 259-273 (2002). (Pubitemid 34775346)
21. Yabut, O., Domogauer, J. & D'Arcangelo, G. Dyrk1A overexpression inhibits proliferation and induces premature neuronal differentiation of neural progenitor cells. J. Neurosci. 30, 4004-4014 (2010).
22. Arque, G., de Lagran, M. M., Arbones, M. L. & Dierssen, M. Age-associated motor and visuo-spatial learning phenotype in Dyrk1A heterozygous mutant mice. Neurobiol. Dis. 36, 312-319 (2009).
23. Wegiel, J. et al. Cell type- and brain structure-specific patterns of distribution of minibrain kinase in human brain. Brain Res. 1010, 69-80 (2004). (Pubitemid 38569854)
24. Arque, G., Casanovas, A. & Dierssen, M. Dyrk1A is dynamically expressed on subsets of motor neurons and in the neuromuscular junction: possible role in Down syndrome. PLoS ONE 8, e54285 (2013).
25. Adayev, T., Chen-Hwang, M. C., Murakami, N., Wang, R. & Hwang, Y. W. MNB/DYRK1A phosphorylation regulates the interactions of synaptojanin 1 with endocytic accessory proteins. Biochem. Biophys. Res. Commun. 351, 1060-1065 (2006). (Pubitemid 44715892)
26. Huang, Y. et al. Mnb/Dyrk1A phosphorylation regulates the interaction of dynamin 1 with SH3 domain-containing proteins. Biochemistry 43, 10173-10185 (2004). (Pubitemid 39030908)
27. Murakami, N., Bolton, D. C., Kida, E., Xie, W. & Hwang, Y. W. Phosphorylation by Dyrk1A of clathrin coated vesicle-associated proteins: identification of the substrate proteins and the effects of phosphorylation. PLoS ONE 7, e34845 (2012).
28. Ringstad, N., Nemoto, Y. & De Camilli, P. The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc. Natl Acad. Sci. USA 94, 8569-8574 (1997). (Pubitemid 27335079)
29. Roos, J. & Kelly, R. B. Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem. 273, 19108-19119 (1998). (Pubitemid 28366307)
30. Verstreken, P. et al. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40, 733-748 (2003). (Pubitemid 37431034)
31. Harris, T. W., Hartwieg, E., Horvitz, H. R. & Jorgensen, E. M. Mutations in synaptojanin disrupt synaptic vesicle recycling. J. Cell Biol. 150, 589-600 (2000).
32. Schuske, K. R. et al. Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40, 749-762 (2003). (Pubitemid 37431035)
33. Koh, T. W., Verstreken, P. & Bellen, H. J. Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron 43, 193-205 (2004). (Pubitemid 38942960)
34. Marie, B. et al. Dap160/intersectin scaffolds the periactive zone to achieve highfidelity endocytosis and normal synaptic growth. Neuron 43, 207-219 (2004). (Pubitemid 38942961)
35. Cremona, O. et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188 (1999). (Pubitemid 29491784)
36. Dickman, D. K., Horne, J. A., Meinertzhagen, I. A. & Schwarz, T. L. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123, 521-533 (2005). (Pubitemid 41546680)
37. Lee, S. Y., Wenk, M. R., Kim, Y., Nairn, A. C. & De Camilli, P. Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc. Natl Acad. Sci. USA 101, 546-551 (2004). (Pubitemid 38084673)
38. Irie, F., Okuno, M., Pasquale, E. B. & Yamaguchi, Y. EphrinB-EphB signalling regulates clathrin-mediated endocytosis through tyrosine phosphorylation of synaptojanin 1. Nat. Cell Biol. 7, 501-509 (2005). (Pubitemid 40637410)
39. Schwarz, T. L. Transmitter release at the neuromuscular junction. Int. Rev. Neurobiol. 75, 105-144 (2006). (Pubitemid 44809140)
40. Verstreken, P. et al. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101-112 (2002). (Pubitemid 34327520)
41. Collins, C. A., Wairkar, Y. P., Johnson, S. L. & DiAntonio, A. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51, 57-69 (2006). (Pubitemid 43963338)
42. Lee, S., Liu, H. P., Lin, W. Y., Guo, H. & Lu, B. LRRK2 kinase regulates synaptic morphology through distinct substrates at the presynaptic and postsynaptic compartments of the Drosophila neuromuscular junction. J. Neurosci. 30, 16959-16969 (2010).
43. Hong, S. H. et al. Minibrain/Dyrk1a regulates food intake through the Sir2- FOXO-sNPF/NPY pathway in Drosophila and mammals. PLoS Genet. 8, e1002857 (2012).
44. Zhang, B. et al. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21, 1465-1475 (1998). (Pubitemid 29022547)
45. Makrantoni, V., Antrobus, R., Botting, C. H. & Coote, P. J. Rapid enrichment and analysis of yeast phosphoproteins using affinity chromatography, 2DPAGE and peptide mass fingerprinting. Yeast 22, 401-414 (2005). (Pubitemid 40561555)
46. Shupliakov, O. et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263 (1997). (Pubitemid 27172685)
47. Voronov, S. V. et al. Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down's syndrome. Proc. Natl Acad. Sci. USA 105, 9415-9420 (2008).
48. Di Paolo, G. et al. Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431, 415-422 (2004). (Pubitemid 39329574)
49. Mani, M. et al. The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56, 1004-1018 (2007). (Pubitemid 350251112)
50. Khuong, T. M., Habets, R. L., Slabbaert, J. R. & Verstreken, P. WASP is activated by phosphatidylinositol-4,5-bisphosphate to restrict synapse growth in a pathway parallel to bone morphogenetic protein signaling. Proc. Natl Acad. Sci. USA 107, 17379-17384 (2010).
51. Verstreken, P. et al. Tweek, an evolutionarily conserved protein, is required for synaptic vesicle recycling. Neuron 63, 203-215 (2009).
52. Ogawa, Y. et al. Development of a novel selective inhibitor of the Down syndrome-related kinase Dyrk1A. Nat. Commun. 1, 86 (2010).
53. Raucher, D. et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228 (2000). (Pubitemid 30064910)
54. Chang, K. T. & Min, K. T. Upregulation of three Drosophila homologs of human chromosome 21 genes alters synaptic function: implications for Down syndrome. Proc. Natl Acad. Sci. USA 106, 17117-17122 (2009).
55. Saheki, Y. & De Camilli, P. Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 4, a005645 (2012).
56. Broadie, K. Synapse scaffolding: intersection of endocytosis and growth. Curr. Biol. 14, R853-R855 (2004). (Pubitemid 39301157)
57. Sundborger, A. et al. An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J. Cell. Sci. 124, 133-143 (2011).
58. Milosevic, I. et al. Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72, 587-601 (2011).
59. Coyle, I. P. et al. Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila. Neuron 41, 521-534 (2004). (Pubitemid 38253065)
60. Collins, C. A. & DiAntonio, A. Coordinating synaptic growth without being a nervous wreck. Neuron 41, 489-491 (2004). (Pubitemid 38253060)
61. Sechi, A. S. & Wehland, J. The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane. J. Cell Sci. 113(Pt 21): 3685-3695 (2000).
62. Rodal, A. A., Motola-Barnes, R. N. & Littleton, J. T. Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J. Neurosci. 28, 8316-8325 (2008).
63. Dickman, D. K., Lu, Z., Meinertzhagen, I. A. & Schwarz, T. L. Altered synaptic development and active zone spacing in endocytosis mutants. Curr. Biol. 16, 591-598 (2006).
64. Krebs, C. E. et al. The Sac1 domain of SYNJ1 identified mutated in a family with early-onset progressive Parkinsonism with generalized seizures. Hum. Mutat. 34, 1200-1207 (2013).
65. Dowjat, W. K. et al. Trisomy-driven overexpression of DYRK1A kinase in the brain of subjects with Down syndrome. Neurosci. Lett. 413, 77-81 (2007). (Pubitemid 46149186)
66. Arai, Y., Ijuin, T., Takenawa, T., Becker, L. E. & Takashima, S. Excessive expression of synaptojanin in brains with Down syndrome. Brain Dev. 24, 67-72 (2002). (Pubitemid 34224905)
67. Cossec, J. C. et al. Trisomy for synaptojanin1 in Down syndrome is functionally linked to the enlargement of early endosomes. Hum. Mol. Genet. 21, 3156-3172 (2012).
68. Pauli, A. et al. Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev. Cell. 14, 239-251 (2008). (Pubitemid 351189182)
69. Littleton, J. T., Bellen, H. J. & Perin, M. S. Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles to the synapse. Development 118, 1077-1088 (1993). (Pubitemid 23252398)
70. Zhou, Y. et al. Rapid and enhanced proteolytic digestion using electric-fieldoriented enzyme reactor. J. Proteomics 74, 1030-1035 (2011).