Age-dependent targeting of protein phosphatase 1 to Ca 2+/calmodulin-dependent protein kinase II by spinophilin in mouse striatum

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Baucum II, Anthony J ^a   Strack, Stefan ^a,b   Colbran, Roger J ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERNEXIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; F ACTIN; MYOSIN VA; PHOSPHOPROTEIN PHOSPHATASE 1; SPINOPHILIN; THREONINE; ACTIN BINDING PROTEIN; NERVE PROTEIN; NEURABIN;

AGING; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORPUS STRIATUM; CYTOSKELETON; DENDRITIC SPINE; ENZYME ACTIVITY; ENZYME LOCALIZATION; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MORPHOLOGY; MOUSE; NERVE CELL; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; AGE; ANIMAL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

MUS;

AGE FACTORS; AGING; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CORPUS STRIATUM; DENDRITIC SPINES; MICE; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PHOSPHATASE 1;

EID: 84856911771     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031554     Document Type: Article

References (72)

1. Zhou Q, Homma KJ, Poo MM, (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44: 749-757.
2. Levine MS, Adinolfi AM, Fisher RS, Hull CD, Buchwald NA, et al. (1986) Quantitative morphology of medium-sized caudate spiny neurons in aged cats. Neurobiol Aging 7: 277-286.
3. Levine MS, Fisher RS, Hull CD, Buchwald NA, (1986) Postnatal development of identified medium-sized caudate spiny neurons in the cat. Brain Res 389: 47-62.
4. Tada T, Sheng M, (2006) Molecular mechanisms of dendritic spine morphogenesis. Curr Opin Neurobiol 16: 95-101.
5. Holtmaat A, Svoboda K, (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10: 647-658.
6. Sheng M, Hoogenraad CC, (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76: 823-847.
7. Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, et al. (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics 5: 1158-1170.
8. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR, (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276: 2042-2045.
9. Fukunaga K, Stoppini L, Miyamoto E, Muller D, (1993) Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 268: 7863-7867.
10. Bingol B, Wang CF, Arnott D, Cheng D, Peng J, et al. (2010) Autophosphorylated CaMKIIalpha acts as a scaffold to recruit proteasomes to dendritic spines. Cell 140: 567-578.
11. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ, (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279: 870-873.
12. Hudmon A, Schulman H, (2002) Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu Rev Biochem 71: 473-510.
13. Strack S, Choi S, Lovinger DM, Colbran RJ, (1997) Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density. J Biol Chem 272: 13467-13470.
14. Gustin RM, Shonesy BC, Robinson SL, Rentz TJ, Baucum AJ 2nd, et al. (2011) Loss of Thr286 phosphorylation disrupts synaptic CaMKIIalpha targeting, NMDAR activity and behavior in pre-adolescent mice. Mol Cell Neurosci 47: 286-292.
15. Zhang GR, Cheng XR, Zhou WX, Zhang YX, (2009) Age-related expression of calcium/calmodulin-dependent protein kinase II A in the hippocampus and cerebral cortex of senescence accelerated mouse prone/8 mice is modulated by anti-Alzheimer's disease drugs. Neuroscience 159: 308-315.
16. Brocke L, Srinivasan M, Schulman H, (1995) Developmental and regional expression of multifunctional Ca2+/calmodulin-dependent protein kinase isoforms in rat brain. J Neurosci 15: 6797-6808.
17. Bodhinathan K, Kumar A, Foster TC, (2010) Intracellular redox state alters NMDA receptor response during aging through Ca2+/calmodulin-dependent protein kinase II. J Neurosci 30: 1914-1924.
18. Ouimet CC, da Cruz e Silva EF, Greengard P, (1995) The alpha and gamma 1 isoforms of protein phosphatase 1 are highly and specifically concentrated in dendritic spines. Proc Natl Acad Sci U S A 92: 3396-3400.
19. Strack S, Kini S, Ebner FF, Wadzinski BE, Colbran RJ, (1999) Differential cellular and subcellular localization of protein phosphatase 1 isoforms in brain. J Comp Neurol 413: 373-384.
20. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, et al. (1998) Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 280: 1940-1942.
21. Norris CM, Halpain S, Foster TC, (1998) Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol 80: 1567-1570.
22. Brown AM, Baucum AJ, Bass MA, Colbran RJ, (2008) Association of protein phosphatase 1 gamma 1 with spinophilin suppresses phosphatase activity in a Parkinson disease model. J Biol Chem 283: 14286-14294.
23. Picconi B, Gardoni F, Centonze D, Mauceri D, Cenci MA, et al. (2004) Abnormal Ca2+-calmodulin-dependent protein kinase II function mediates synaptic and motor deficits in experimental parkinsonism. J Neurosci 24: 5283-5291.
24. Colbran RJ, (2004) Targeting of calcium/calmodulin-dependent protein kinase II. Biochem J 378: 1-16.
25. Bollen M, Peti W, Ragusa MJ, Beullens M, (2010) The extended PP1 toolkit: designed to create specificity. Trends Biochem Sci 35: 450-458.
26. Terry-Lorenzo RT, Elliot E, Weiser DC, Prickett TD, Brautigan DL, et al. (2002) Neurabins recruit protein phosphatase-1 and inhibitor-2 to the actin cytoskeleton. J Biol Chem 277: 46535-46543.
27. Buchsbaum RJ, Connolly BA, Feig LA, (2003) Regulation of p70 S6 kinase by complex formation between the Rac guanine nucleotide exchange factor (Rac-GEF) Tiam1 and the scaffold spinophilin. J Biol Chem 278: 18833-18841.
28. Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu GY, et al. (2005) The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47: 85-100.
29. Tolias KF, Bikoff JB, Kane CG, Tolias CS, Hu L, et al. (2007) The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proc Natl Acad Sci U S A 104: 7265-7270.
30. Penzes P, Johnson RC, Sattler R, Zhang X, Huganir RL, et al. (2001) The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29: 229-242.
31. Baucum AJ 2nd, Jalan-Sakrikar N, Jiao Y, Gustin RM, Carmody LC, et al. (2010) Identification and validation of novel spinophilin-associated proteins in rodent striatum using an enhanced ex vivo shotgun proteomics approach. Mol Cell Proteomics 9: 1243-1259.
32. Satoh A, Nakanishi H, Obaishi H, Wada M, Takahashi K, et al. (1998) Neurabin-II/spinophilin. An actin filament-binding protein with one pdz domain localized at cadherin-based cell-cell adhesion sites. J Biol Chem 273: 3470-3475.
33. Barnes AP, Smith FD 3rd, VanDongen HM, VanDongen AM, Milgram SL, (2004) The identification of a second actin-binding region in spinophilin/neurabin II. Brain Res Mol Brain Res 124: 105-113.
34. Allen PB, Ouimet CC, Greengard P, (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci U S A 94: 9956-9961.
35. Cheng HY, Schiavone AP, Smithgall TE, (2001) A point mutation in the N-terminal coiled-coil domain releases c-Fes tyrosine kinase activity and survival signaling in myeloid leukemia cells. Mol Cell Biol 21: 6170-6180.
36. Wolf E, Kim PS, Berger B, (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci 6: 1179-1189.
37. Carmody LC, Baucum AJ 2nd, Bass MA, Colbran RJ, (2008) Selective targeting of the gamma1 isoform of protein phosphatase 1 to F-actin in intact cells requires multiple domains in spinophilin and neurabin. Faseb J 22: 1660-1671.
38. Fink CC, Bayer KU, Myers JW, Ferrell JE Jr, Schulman H, et al. (2003) Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 39: 283-297.
39. Lin YC, Redmond L, (2008) CaMKIIbeta binding to stable F-actin in vivo regulates F-actin filament stability. Proc Natl Acad Sci U S A 105: 15791-15796.
40. Okamoto K, Narayanan R, Lee SH, Murata K, Hayashi Y, (2007) The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure. Proc Natl Acad Sci U S A 104: 6418-6423.
41. Brown AM, Deutch AY, Colbran RJ, (2005) Dopamine depletion alters phosphorylation of striatal proteins in a model of Parkinsonism. Eur J Neurosci 22: 247-256.
42. Feng J, Yan Z, Ferreira A, Tomizawa K, Liauw JA, et al. (2000) Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad Sci U S A 97: 9287-9292.
43. Yoshimura Y, Yamauchi T, (1997) Phosphorylation-dependent reversible association of Ca2+/calmodulin-dependent protein kinase II with the postsynaptic densities. J Biol Chem 272: 26354-26359.
44. Rao MV, Mohan PS, Kumar A, Yuan A, Montagna L, et al. (2011) The myosin Va head domain binds to the neurofilament-L rod and modulates endoplasmic reticulum (ER) content and distribution within axons. PLoS One 6: e17087.
45. Costa MC, Mani F, Santoro W Jr, Espreafico EM, Larson RE, (1999) Brain myosin-V, a calmodulin-carrying myosin, binds to calmodulin-dependent protein kinase II and activates its kinase activity. J Biol Chem 274: 15811-15819.
46. MacMillan LB, Bass MA, Cheng N, Howard EF, Tamura M, et al. (1999) Brain actin-associated protein phosphatase 1 holoenzymes containing spinophilin, neurabin, and selected catalytic subunit isoforms. J Biol Chem 274: 35845-35854.
47. Jiao Y, Jalan-Sakrikar N, Robison AJ, Baucum AJ 2nd, Bass MA, et al. (2011) Characterization of a central Ca2+/calmodulin-dependent protein kinase IIalpha/beta binding domain in densin that selectively modulates glutamate receptor subunit phosphorylation. J Biol Chem 286: 24806-24818.
48. Nikandrova YA, Jiao Y, Baucum AJ, Tavalin SJ, Colbran RJ, (2010) Ca2+/calmodulin-dependent protein kinase II binds to and phosphorylates a specific SAP97 splice variant to disrupt association with AKAP79/150 and modulate alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-type glutamate receptor (AMPAR) activity. J Biol Chem 285: 923-934.
49. Robison AJ, Bass MA, Jiao Y, MacMillan LB, Carmody LC, et al. (2005) Multivalent interactions of calcium/calmodulin-dependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and alpha-actinin-2. J Biol Chem 280: 35329-35336.
50. O'Leary H, Lasda E, Bayer KU, (2006) CaMKIIbeta association with the actin cytoskeleton is regulated by alternative splicing. Mol Biol Cell 17: 4656-4665.
51. Sanabria H, Swulius MT, Kolodziej SJ, Liu J, Waxham MN, (2009) {beta}CaMKII regulates actin assembly and structure. J Biol Chem 284: 9770-9780.
52. Woodgett JR, Davison MT, Cohen P, (1983) The calmodulin-dependent glycogen synthase kinase from rabbit skeletal muscle. Purification, subunit structure and substrate specificity. Eur J Biochem 136: 481-487.
53. Erondu NE, Kennedy MB, (1985) Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. J Neurosci 5: 3270-3277.
54. Benson DL, Gall CM, Isackson PJ, (1992) Dendritic localization of type II calcium calmodulin-dependent protein kinase mRNA in normal and reinnervated rat hippocampus. Neuroscience 46: 851-857.
55. Sarrouilhe D, di Tommaso A, Metaye T, Ladeveze V, (2006) Spinophilin: from partners to functions. Biochimie 88: 1099-1113.
56. Yoshimura Y, Aoi C, Yamauchi T, (2000) Investigation of protein substrates of Ca(2+)/calmodulin-dependent protein kinase II translocated to the postsynaptic density. Brain Res Mol Brain Res 81: 118-128.
57. Lisman JE, Zhabotinsky AM, (2001) A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron 31: 191-201.
58. Logue JS, Scott JD, (2010) Organizing signal transduction through A-kinase anchoring proteins (AKAPs). FEBS J 277: 4370-4375.
59. Dosemeci A, Reese TS, (1993) Inhibition of endogenous phosphatase in a postsynaptic density fraction allows extensive phosphorylation of the major postsynaptic density protein. J Neurochem 61: 550-555.
60. Hsieh-Wilson LC, Allen PB, Watanabe T, Nairn AC, Greengard P, (1999) Characterization of the neuronal targeting protein spinophilin and its interactions with protein phosphatase-1. Biochemistry 38: 4365-4373.
61. Ragusa MJ, Dancheck B, Critton DA, Nairn AC, Page R, et al. (2010) Spinophilin directs protein phosphatase 1 specificity by blocking substrate binding sites. Nat Struct Mol Biol 17: 459-464.
62. Mullasseril P, Dosemeci A, Lisman JE, Griffith LC, (2007) A structural mechanism for maintaining the 'on-state' of the CaMKII memory switch in the post-synaptic density. J Neurochem 103: 357-364.
63. Hsieh-Wilson LC, Benfenati F, Snyder GL, Allen PB, Nairn AC, et al. (2003) Phosphorylation of spinophilin modulates its interaction with actin filaments. J Biol Chem 278: 1186-1194.
64. Grossman SD, Futter M, Snyder GL, Allen PB, Nairn AC, et al. (2004) Spinophilin is phosphorylated by Ca2+/calmodulin-dependent protein kinase II resulting in regulation of its binding to F-actin. J Neurochem 90: 317-324.
65. Fleming IN, Elliott CM, Buchanan FG, Downes CP, Exton JH, (1999) Ca2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation. J Biol Chem 274: 12753-12758.
66. Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, et al. (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56: 640-656.
67. Shioda N, Beppu H, Fukuda T, Li E, Kitajima I, et al. (2011) Aberrant Calcium/Calmodulin-Dependent Protein Kinase II (CaMKII) Activity Is Associated with Abnormal Dendritic Spine Morphology in the ATRX Mutant Mouse Brain. J Neurosci 31: 346-358.
68. McNeill RB, Colbran RJ, (1995) Interaction of autophosphorylated Ca2+/calmodulin-dependent protein kinase II with neuronal cytoskeletal proteins. Characterization of binding to a 190-kDa postsynaptic density protein. J Biol Chem 270: 10043-10049.
69. Carmody LC, Bauman PA, Bass MA, Mavila N, DePaoli-Roach AA, et al. (2004) A protein phosphatase-1gamma1 isoform selectivity determinant in dendritic spine-associated neurabin. J Biol Chem 279: 21714-21723.
70. Jiao Y, Robison AJ, Bass MA, Colbran RJ, (2008) Developmentally regulated alternative splicing of densin modulates protein-protein interaction and subcellular localization. J Neurochem 105: 1746-1760.
71. Brickey DA, Colbran RJ, Fong YL, Soderling TR, (1990) Expression and characterization of the alpha-subunit of Ca2+/calmodulin-dependent protein kinase II using the baculovirus expression system. Biochem Biophys Res Commun 173: 578-584.
72. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, et al. (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24: 4070-4081.