Spinophilin-targeted protein phosphatase-1 alleviated inflammatory pain by negative control of MEK/ERK signaling in spinal cord dorsal horn of rats

Journal of Neuroscience

Volumn 35, Issue 41, 2015, Pages 13989-14001

  Hu, Xiao Dong ^a   Liu, Yan Ni ^a   Zhang, Zi Yang ^a   Ma, Zheng An ^a   Suo, Zhan Wei ^a   Yang, Xian ^a  

^a LANZHOU UNIVERSITY   (China)

Author keywords

Extracellular signal regulated kinase; NMDA receptor; Pain; Protein phosphatase 1; Spinophilin

Indexed keywords

GLUTAMATE RECEPTOR; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 1; SPINOPHILIN; ACTIN BINDING PROTEIN; AMINO ACID RECEPTOR BLOCKING AGENT; CENTRAL STIMULANT AGENT; FREUND ADJUVANT; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; NERVE PROTEIN; NEURABIN; PICROTOXIN;

ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSFECTION; GLUTAMATERGIC SYNAPSE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INFLAMMATORY PAIN; INTRACELLULAR SIGNALING; MALE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; POLYMERASE CHAIN REACTION; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; RAT; SPATIOTEMPORAL ANALYSIS; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; ANIMAL; CHEMICALLY INDUCED; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; HEK293 CELL LINE; HUMAN; IN VITRO STUDY; INFLAMMATION; METABOLISM; PAIN; PAIN MEASUREMENT; PATCH CLAMP TECHNIQUE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; CENTRAL NERVOUS SYSTEM STIMULANTS; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FREUND'S ADJUVANT; HEK293 CELLS; HUMANS; IN VITRO TECHNIQUES; INFLAMMATION; MALE; MAP KINASE KINASE KINASES; MAP KINASE SIGNALING SYSTEM; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; PAIN; PAIN MEASUREMENT; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PROTEIN PHOSPHATASE 1; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD DORSAL HORN;

EID: 84944564619     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2293-15.2015     Document Type: Article

References (53)

1. 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. CrossRef Medline
2. Allen PB, Zachariou V, Svenningsson P, Lepore AC, Centonze D, Costa C, Rossi S, Bender G, Chen G, Feng J, Snyder GL, Bernardi G, Nestler EJ, Yan Z, Calabresi P, Greengard P (2006) Distinct roles for spinophilin and neurabin in dopamine-mediated plasticity. Neuroscience 140:897-911. CrossRef Medline
3. Alter BJ, Zhao C, Karim F, Landreth GE, Gereau RW (2010) Genetic targeting of ERK1 suggests a predominant role for ERK2 in murine pain models. J Neurosci 30:11537-11547. CrossRef Medline
4. Amparan D, Avram D, Thomas CG, Lindahl MG, Yang J, Bajaj G, Ishmael JE (2005) Direct interaction of myosin regulatory light chain with the NMDA receptor. J Neurochem 92:349-361. CrossRef Medline
5. Baucum AJ 2nd, Jalan-Sakrikar N, Jiao Y, Gustin RM, Carmody LC, Tabb DL, Ham AJ, Colbran RJ (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. CrossRef Medline
6. Cohen PT (2002) Protein phosphatase 1—targeted in many directions. J Cell Sci 115:241-256. Medline
7. Dard N, Peter M (2006) Scaffold proteins in MAP kinase signaling: more than simple passive activating platforms. Bioessays 28:146-156. CrossRef Medline
8. Fan QQ, Li L, Wang WT, Yang X, Suo ZW, Hu XD (2014) Activation of alpha2 adrenoceptors inhibited NMDA receptor-mediated nociceptive transmission in spinal dorsal horn of mice with inflammatory pain. Neuropharmacology 77:185-192. CrossRef Medline
9. Feng J, Yan Z, Ferreira A, Tomizawa K, Liauw JA, Zhuo M, Allen PB, Ouimet CC, Greengard P (2000) Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad SciU S A97:9287-9292. CrossRef Medline
10. Hédou GF, Koshibu K, Farinelli M, Kilic E, Gee CE, Kilic U, Baumgärtel K, Hermann DM, Mansuy IM (2008) Protein phosphatase 1-dependent bidirectional synaptic plasticity controls ischemic recovery in the adult brain. J Neurosci 28:154-162. CrossRef Medline
11. 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. CrossRef Medline
12. Hu HJ, Carrasquillo Y, Karim F, Jung WE, Nerbonne JM, Schwarz TL, Gereau RW (2006) The kv4.2 potassium channel subunit is required for pain plasticity. Neuron 50:89-100. CrossRef Medline
13. Hu XD, Huang Q, Yang X, Xia H (2007) Differential regulation of AMPA receptor trafficking by neurabin-targeted synaptic protein phosphatase-1 in synaptic transmission and long-term depression in hippocampus. J Neurosci 27:4674-4686. CrossRef Medline
14. Ikeda H, Stark J, Fischer H, Wagner M, Drdla R, Jager T, Sandkühler J (2006) Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312:1659-1662. CrossRef Medline
15. Jaworski J, Kapitein LC, Gouveia SM, Dortland BR, Wulf PS, Grigoriev I, Camera P, Spangler SA, Di Stefano P, Demmers J, Krugers H, Defilippi P, Akhmanova A, Hoogenraad CC (2009) Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61:85-100. CrossRef Medline
16. Ji RR, Baba H, Brenner GJ, Woolf CJ (1999) Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2:1114-1119. CrossRef Medline
17. Ji RR, Befort K, Brenner GJ, Woolf CJ (2002) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 22:478-485. Medline
18. Ji RR, Gereau RW, Malcangio M, Strichartz GR (2009) MAP kinase and pain. Brain Res Rev 60:135-148. CrossRef Medline
19. Jurado S, Goswami D, Zhang Y, Molina AJ, Südhof TC, Malenka RC (2013) LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77:542-558. CrossRef Medline
20. Karim F, Wang CC, Gereau RW 4th (2001) Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 21:3771-3779. Medline
21. Karim F, Hu HJ, Adwanikar H, Kaplan D, Gereau RW 4th (2006) Impaired inflammatory pain and thermal hyperalgesia in mice expressing neuronspecific dominant negative mitogen activated protein kinase kinase (MEK). Mol Pain 2:2. CrossRef Medline
22. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA (1997) Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137:481-492. CrossRef Medline
23. KolchW (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat Rev Mol Cell Biol 6:827-837. CrossRef Medline
24. Lei S, Czerwinska E, Czerwinski W, Walsh MP, MacDonald JF (2001) Regulation of NMDA receptor activity by F-actin and myosin light chain kinase. J Neurosci 21:8464-8472. Medline
25. Li L, Shi L, Xu YM, Yang X, Suo ZW, Hu XD (2015) GABAergic inhibition regulated pain sensitization through STEP61 signaling in spinal dorsal horn of mice. Anesthesiology 122:686-697. CrossRef Medline
26. Luo C, Gangadharan V, Bali KK, Xie RG, Agarwal N, Kurejova M, Tappe-Theodor A, Tegeder I, Feil S, Lewin G, Polgar E, Todd AJ, Schlossmann J, Hofmann F, Liu DL, Hu SJ, Feil R, Kuner T, Kuner R (2012) Presynaptically localized cyclic GMP-dependent protein kinase 1 is a key determinant of spinal synaptic potentiation and pain hypersensitivity. PLoS Biol 10:e1001283. CrossRef Medline
27. MacMillan LB, Bass MA, Cheng N, Howard EF, Tamura M, Strack S, Wadzinski BE, Colbran RJ (1999) Brain actin-associated protein phosphatase 1 holoenzymes containing spinophilin, neurabin, and selected catalytic subunit isoforms. J Biol Chem 274:35845-35854. CrossRef Medline
28. Mannes AJ, Caudle RM, O’Connell BC, Iadarola MJ (1998) Adenoviral gene transfer to spinal-cord neurons: intrathecal vs. intraparenchymal administration. Brain Res 793:1-6. CrossRef Medline
29. Matallanas D, Birtwistle M, Romano D, Zebisch A, Rauch J, von Kriegsheim A, Kolch W (2011) Raf family kinases: old dogs have learned new tricks. Genes Cancer 2:232-260. CrossRef Medline
30. McAvoy T, Allen PB, Obaishi H, Nakanishi H, Takai Y, Greengard P, Nairn AC, Hemmings HC Jr (1999) Regulation of neurabin I interaction with protein phosphatase 1 by phosphorylation. Biochemistry 38:12943-12949. CrossRef Medline
31. Mitsuhashi S, Shima H, Tanuma N, Matsuura N, Takekawa M, Urano T, Kataoka T, Ubukata M, Kikuchi K (2003) Usage of tautomycetin, a novel inhibitor of protein phosphatase 1 (PP1), reveals that PP1 is a positive regulator of Raf-1 in vivo. J Biol Chem 278:82-88. Medline
32. Morishita W, Connor JH, Xia H, Quinlan EM, Shenolikar S, Malenka RC (2001) Regulation of synaptic strength by protein phosphatase 1. Neuron 32:1133-1148. CrossRef Medline
33. Morrison DK, Davis RJ (2003) Regulation ofMAPkinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19:91-118. CrossRef Medline
34. Oliver CJ, Terry-Lorenzo RT, Elliott E, Bloomer WA, Li S, Brautigan DL, Colbran RJ, Shenolikar S (2002) Targeting protein phosphatase 1 (PP1) to the actin cytoskeleton: the neurabin I/PP1 complex regulates cell morphology. Mol Cell Biol 22:4690-4701. CrossRef Medline
35. Ory S, Zhou M, Conrads TP, Veenstra TD, Morrison DK (2003) Protein phosphatase 2A positively regulates Ras signaling by dephosphorylating KSR1 and Raf-1 on critical 14-3-3 binding sites. Curr Biol 13:1356-1364. CrossRef Medline
36. Patterson KI, Brummer T, O’Brien PM, Daly RJ (2009) Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem J 418:475-489. CrossRef Medline
37. Paul S, Nairn AC, Wang P, Lombroso PJ (2003) NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nat Neurosci 6:34-42. Medline
38. Roskoski R Jr (2012a) MEK1/2 dual-specificity protein kinases: structure and regulation. Biochem Biophys Res Commun 417:5-10. CrossRef Medline
39. Roskoski R Jr (2012b) ERK1/2 MAP kinases: structure, function, and regulation. Pharmacol Res 66:105-143. CrossRef Medline
40. Sanz-Clemente A, Matta JA, Isaac JT, Roche KW (2010) Casein kinase 2 regulates the NR2 subunit composition of synaptic NMDA receptors. Neuron 67:984-996. CrossRef Medline
41. Sarrouilhe D, di Tommaso A, Métayé T, Ladeveze V (2006) Spinophilin: from partners to functions. Biochimie 88:1099-1113. CrossRef Medline
42. Satoh A, Nakanishi H, Obaishi H, Wada M, Takahashi K, Satoh K, Hirao K, Nishioka H, Hata Y, Mizoguchi A, Takai Y (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. CrossRef Medline
43. Satoh Y, Endo S, Ikeda T, Yamada K, Ito M, Kuroki M, Hiramoto T, Imamura O, Kobayashi Y, Watanabe Y, Itohara S, Takishima K (2007) Extracellular signal-regulated kinase 2 (ERK2) knockdown mice show deficits in long-term memory; ERK2 has a specific function in learning and memory. J Neurosci 27:10765-10776. CrossRef Medline
44. Smith KE, Gibson ES, Dell’Acqua ML (2006) cAMP-dependent protein kinase postsynaptic localization regulated by NMDA receptor activation through translocation of an A-kinase anchoring protein scaffold protein. J Neurosci 26:2391-2402. CrossRef Medline
45. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183. CrossRef Medline
46. Westermarck J, Li SP, Kallunki T, Han J, Kähäri VM (2001) p38 mitogenactivated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase 1 (MMP-1) gene expression. Mol Cell Biol 21:2373-2383. CrossRef Medline
47. Weyerbacher AR, Xu Q, Tamasdan C, Shin SJ, Inturrisi CE (2010) N-Methyl-D-aspartate receptor (NMDAR) independent maintenance of inflammatory pain. Pain 148:237-246. CrossRef Medline
48. Wu JQ, Guo JY, Tang W, Yang CS, Freel CD, Chen C, Nairn AC, Kornbluth S (2009) PP1-mediated dephosphorylation of phosphoproteins at mitotic exit is controlled by inhibitor-1 and PP1 phosphorylation. Nat Cell Biol 11:644-651. CrossRef Medline
49. Xin WJ, Gong QJ, Xu JT, Yang HW, Zang Y, Zhang T, Li YY, Liu XG (2006) Role of phosphorylation of ERK in induction and maintenance of LTP of the C-fiber evoked field potentials in spinal dorsal horn. J Neurosci Res 84:934-943. CrossRef Medline
50. Xu Q, Garraway SM, Weyerbacher AR, Shin SJ, Inturrisi CE (2008) Activation of the neuronal extracellular signal-regulated kinase 2 in the spinal cord dorsal horn is required for complete Freund’s adjuvantinduced pain hypersensitivity. J Neurosci 28:14087-14096. CrossRef Medline
51. Yan Z, Hsieh-Wilson L, Feng J, Tomizawa K, Allen PB, Fienberg AA, Nairn AC, Greengard P (1999) Protein phosphatase 1 modulation of neostriatal AMPA channels: regulation by DARPP-32 and spinophilin. Nat Neurosci 2:13-17. CrossRef Medline
52. Zhou B, Wang ZX, Zhao Y, Brautigan DL, Zhang ZY (2002) The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases. J Biol Chem 277:31818-31825. CrossRef Medline
53. Zhou HY, Chen SR, Chen H, Pan HL (2010) Opioid-induced long-term potentiation in the spinal cord is a presynaptic event. J Neurosci 30:4460-4466. CrossRef Medline