Raf kinase inhibitory protein is required for cerebellar long-term synaptic depression by mediating PKC-dependent MAPK activation

Journal of Neuroscience

Volumn 32, Issue 41, 2012, Pages 14254-14264

  Yamamoto, Yukio ^a   Lee, Dongwon ^a   Kim, Yoonhee ^a   Lee, Bokyoung ^a   Seo, Changwoo ^a   Kawasaki, Hiroshi ^b   Kuroda, Shinya ^c   Tanaka Yamamoto, Keiko ^a,c,d  

^a Korea Institute of Science and Technology   (South Korea)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PROTEIN KINASE C;

ANIMAL TISSUE; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; EPISTASIS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LONG TERM DEPRESSION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL;

ANIMALS; CEREBELLUM; ENZYME ACTIVATION; FEMALE; GENETIC VECTORS; HEK293 CELLS; HUMANS; LONG-TERM SYNAPTIC DEPRESSION; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED ICR; MITOGEN-ACTIVATED PROTEIN KINASES; NIH 3T3 CELLS; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PROTEIN KINASE C; VIRAL ENVELOPE PROTEINS;

EID: 84867238409     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2812-12.2012     Document Type: Article

References (54)

1. Antoun G, Cannon PB, Cheng HY (2012) Regulation of MAPK/ERK signaling and photic entrainment of the suprachiasmatic nucleus circadian clock by Raf kinase inhibitor protein. J Neurosci 32:4867-4877.
2. Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283:381-387.
3. Carman CV, Benovic JL (1998) G-protein-coupled receptors: turn-ons and turn-offs. Curr Opin Neurobiol 8:335-344.
4. Chung HJ, Steinberg JP, Huganir RL, Linden DJ (2003) Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 300:1751-1755.
5. Cobb MH, Goldsmith EJ (1995) How MAP kinases are regulated. J Biol Chem 270:14843-14846.
6. Corbit KC, Trakul N, Eves EM, Diaz B, Marshall M, Rosner MR (2003) Activation of Raf-1 signaling by protein kinase C through a mechanism involving Raf kinase inhibitory protein. J Biol Chem 278:13061-13068.
7. De Zeeuw CI, Hansel C, Bian F, Koekkoek SK, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495-508.
8. Dhami GK, Babwah AV, Sterne-Marr R, Ferguson SS (2005) Phosphorylation-independent regulation of metabotropic glutamate receptor 1 signaling requires G protein-coupled receptor kinase 2 binding to the second intracellular loop. J Biol Chem 280:24420-24427.
9. Endo S, Launey T (2003) ERKs regulate PKC-dependent synaptic depression and declustering of glutamate receptors in cerebellar Purkinje cells. Neuropharmacology 45:863-872.
10. Finch EA, Tanaka K, Augustine GJ (2012) Calcium as a trigger for cerebellar long-term synaptic depression. Cerebellum 11:706-717.
11. Frayne J, Ingram C, Love S, Hall L (1999) Localisation of phosphatidylethanolamine-binding protein in the brain and other tissues of the rat. Cell Tissue Res 298:415-423.
12. Granovsky AE, Rosner MR (2008) Raf kinase inhibitory protein: a signal transduction modulator and metastasis suppressor. Cell Res 18:452-457.
13. Hanawa H, Kelly PF, Nathwani AC, Persons DA, Vandergriff JA, Hargrove P, Vanin EF, Nienhuis AW (2002) Comparison of various envelope proteins for their ability to pseudotype lentiviral vectors and transduce primitive hematopoietic cells from human blood. Mol Ther 5:242-251.
14. Hartell NA (1994) CGMP acts within cerebellar Purkinje cells to produce long term depression via mechanisms involving PKC and PKG. Neuroreport 5:833-836.
15. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143-1195.
16. Ito-Ishida A, Kakegawa W, Yuzaki M (2006) ERK1/2 but not p38 MAP kinase is essential for the long-term depression in mouse cerebellar slices. Eur J Neurosci 24:1617-1622.
17. Jaarsma D, Ruigrok TJ, Caffé R, Cozzari C, Levey AI, Mugnaini E, Voogd J (1997) Cholinergic innervation and receptors in the cerebellum. Prog Brain Res 114:67-96.
18. Kano M, Hashimoto K, Tabata T (2008) Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination. Philos Trans R Soc Lond B Biol Sci 363:2173-2186.
19. Kawasaki H, Fujii H, Gotoh Y, Morooka T, Shimohama S, Nishida E, Hirano T (1999) Requirement for mitogen-activated protein kinase in cerebellar long term depression. J Biol Chem 274:13498-13502.
20. Keller ET, Fu Z, Brennan M (2005) The biology of a prostate cancer metastasis suppressor protein: Raf kinase inhibitor protein. J Cell Biochem 94:273-278.
21. Klysik J, Theroux SJ, Sedivy JM, Moffit JS, Boekelheide K (2008) Signaling crossroads: the function of Raf kinase inhibitory protein in cancer, thecentral nervous system and reproduction. Cell Signal 20:1-9.
22. Kolch W, Heidecker G, Kochs G, Hummel R, Vahidi H, Mischak H, Finkenzeller G, Marmé D, Rapp UR (1993) Protein kinase Cα activates RAF-1 by direct phosphorylation. Nature 364:249-252.
23. Kondo T, Kakegawa W, Yuzaki M (2005) Induction of long-term depression and phosphorylation of the α2 glutamate receptor by protein kinase C in cerebellar slices. Eur J Neurosci 22:1817-1820.
24. Kuroda S, Schweighofer N, Kawato M (2001) Exploration of signal transduction pathways in cerebellar long-term depression by kinetic simulation. J Neurosci 21:5693-5702.
25. Le TD, Shirai Y, Okamoto T, Tatsukawa T, Nagao S, Shimizu T, Ito M (2010) Lipid signaling in cytosolic phospholipase A2α-cyclooxygenase-2 cascade mediates cerebellar long-term depression and motor learning. Proc Natl Acad Sci U S A 107:3198-3203.
26. Leitges M, Kovac J, Plomann M, Linden DJ (2004) A unique PDZ ligand in PKCα confers induction of cerebellar long-term synaptic depression. Neuron 44:585-594.
27. 2+ in the induction of cerebellar long-term depression. Neuron 18:1025-1038.
28. Linden DJ (1994) Long-term synaptic depression in the mammalian brain. Neuron 12:457-472.
29. Linden DJ (1995) Phospholipase A2 controls the induction of short-term versus long-term depression in the cerebellar Purkinje neuron in culture. Neuron 15:1393-1401.
30. Linden DJ, Connor JA (1991) Participation of postsynaptic PKC in cerebellar long-term depression in culture. Science 254:1656-1659.
31. Lorenz K, Lohse MJ, Quitterer U (2003) Protein kinase C switches the Raf kinase inhibitor from Raf-1 to GRK-2. Nature 426:574-579.
32. Marais R, Light Y, Mason C, Paterson H, Olson MF, Marshall CJ (1998) Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 280:109-112.
33. Miyata M, Finch EA, Khiroug L, Hashimoto K, Hayasaka S, Oda SI, Inouye M, Takagishi Y, Augustine GJ, Kano M (2000) Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28:233-244.
34. Morice C, Nothias F, König S, Vernier P, Baccarini M, Vincent JD, Barnier JV (1999) Raf-1 and B-Raf proteins have similar regional distributions but differential subcellular localization in adult rat brain. Eur J Neurosci 11:1995-2006.
35. Ohtsuki G, Piochon C, Hansel C (2009) Climbing fiber signaling and cerebellar gain control. Front Cell Neurosci 3:4.
36. Ojika K, Mitake S, Tohdoh N, Appel SH, Otsuka Y, Katada E, Matsukawa N (2000) Hippocampal cholinergic neurostimulating peptides (HCNP). Prog Neurobiol 60:37-83.
37. Reynolds T, Hartell NA (2001) Roles for nitric oxide and arachidonic acid in the induction of heterosynaptic cerebellar LTD. Neuroreport 12:133-136.
38. Schönwasser DC, Marais RM, Marshall CJ, Parker PJ (1998) Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel, and atypical protein kinase C isotypes. Mol Cell Biol 18:790-798.
39. Steinberg JP, Takamiya K, Shen Y, Xia J, Rubio ME, Yu S, Jin W, Thomas GM, Linden DJ, Huganir RL (2006) Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron 49:845-860.
40. Takács J, Gombos G, Görcs T, Becker T, de Barry J, Hámori J (1997) Distribution of metabotropic glutamate receptor type 1a in Purkinje cell dendritic spines is independent of the presence of presynaptic parallel fibers. J Neurosci Res 50:433-442.
41. Tanaka K, Augustine GJ (2008) Apositive feedback signal transduction loop determines timing of cerebellar long-term depression. Neuron 59: 608-620.
42. Tanaka K, Khiroug L, Santamaria F, Doi T, Ogasawara H, Ellis-Davies GC, Kawato M, Augustine GJ (2007) Ca2+ requirements for cerebellar long-term synaptic depression: role for a postsynaptic leaky integrator. Neuron 54:787-800.
43. Torashima T, Okoyama S, Nishizaki T, Hirai H (2006) In vivo transductionof murine cerebellar Purkinje cells by HIV-derived lentiviral vectors. Brain Res 1082:11-22.
44. Verin AD, Liu F, Bogatcheva N, Borbiev T, Hershenson MB, Wang P, Garcia JG (2000) Role of Ras-dependent ERK activation in phorbol esterinduced endothelial cell barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 279:L360-L370.
45. Wang SS, Augustine GJ (1995) Confocal imaging and local photolysis of caged compounds: dual probes of synaptic function. Neuron 15:755-760.
46. Wang SS, Khiroug L, Augustine GJ (2000) Quantification of spread of cerebellar long-term depression with chemical two-photon uncaging of glutamate. Proc Natl Acad Sci U S A 97:8635-8640.
47. Wang X, Wang S, Tang X, Zhang A, Grabinski T, Guo Z, Hudson E, Berghuis B, Webb C, Zhao P, Cao B (2010) Development and evaluation of monoclonal antibodies against phosphatidylethanolamine binding protein 1 in pancreatic cancer patients. J Immunol Methods 362:151-160.
48. Wen-Sheng W (2006) Protein kinase Cα trigger Ras and Raf-independent MEK/ERK activation for TPA-induced growth inhibition of human hepatoma cell HepG2. Cancer Lett 239:27-35.
49. Wiegert JS, Bengtson CP, Bading H (2007) Diffusion and not active transport underlies and limits ERK1/2 synapse-to-nucleus signaling in hippocampal neurons. J Biol Chem 282:29621-29633.
50. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, Fee F, Katsanakis KD, Rose DW, Mischak H, Sedivy JM, Kolch W (1999) Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 401:173-177.
51. Yeung K, Janosch P, McFerran B, Rose DW, Mischak H, Sedivy JM, Kolch W (2000) Mechanism of suppression of the Raf/MEK/extracellular signalregulated kinase pathway by the raf kinase inhibitor protein. Mol Cell Biol 20:3079-3085.
52. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, Chatterjee D, McFerran B, Wyche J, Kolch W, Sedivy JM (2001) Raf kinase inhibitor protein interacts with NF-κB-inducing kinase and TAK1 and inhibits NF- κB activation. Mol Cell Biol 21:7207-7217.
53. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M (2006) Localization of diacylglycerol lipase- 128 around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26:4740-4751.
54. Zheng Y, Liu H, Coughlin J, Zheng J, Li L, Stone JC (2005) Phosphorylation of RasGRP3 on threonine 133 provides a mechanistic link between PKC and Ras signaling systems in B cells. Blood 105:3648-3654.