Stress-evoked tyrosine phosphorylation of signal regulatory protein α regulates behavioral immobility in the forced swim test

Journal of Neuroscience

Volumn 30, Issue 31, 2010, Pages 10472-10483

  Ohnishi, Hiroshi ^a   Murata, Takaaki ^a,b   Kusakari, Shinya ^a   Hayashi, Yuriko ^a   Takao, Keizo ^c,d   Maruyama, Toshi ^a   Ago, Yukio ^e   Koda, Ken ^e   Jin, Feng Jie ^a   Okawa, Katsuya ^f   Oldenborg, Per Arne ^g   Okazawa, Hideki ^a   Murata, Yoji ^a   Furuya, Nobuhiko ^b   Matsuda, Toshio ^e   Miyakawa, Tsuyoshi ^c,d   Matozaki, Takashi ^a,h  

^a GUNMA UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d FUJITA HEALTH UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f KYOWA HAKKO KOGYO CO LTD   (Japan)

^g UMEÅ UNIVERSITY   (Sweden)

^h KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD47 ANTIGEN; DESIPRAMINE; FLUOXETINE; IMIPRAMINE; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; POTASSIUM CHANNEL; POTASSIUM CHANNEL SUBUNIT KV BETA 2; PRAZOSIN; PROPRANOLOL; PROTEIN TYROSINE KINASE; REBOXETINE; SIGNAL REGULATORY PROTEIN ALPHA; UNCLASSIFIED DRUG; YOHIMBINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DEPRESSION; FORCED SWIMMING TEST; IMMOBILIZATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; STRESS; WILD TYPE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CELL LINE; CEREBRAL CORTEX; HIPPOCAMPUS; HUMANS; IMMOBILITY RESPONSE, TONIC; MICE; MICRODIALYSIS; PHOSPHORYLATION; RECEPTORS, IMMUNOLOGIC; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 77955370664     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0257-10.2010     Document Type: Article

References (53)

1. Ago Y, Nakamura S, Uda M, Kajii Y, Abe M, Baba A, Matsuda T (2006) Attenuation by the 5-HT1A receptor agonist osemozotan of the behavioral effects of single and repeated methamphetamine in mice. Neuropharmacology 51:914-922. (Pubitemid 44376402)
2. Ballif BA, Carey GR, Sunyaev SR, Gygi SP (2008) Large-scale identification and evolution indexing of tyrosine phosphorylation sites from murine brain. J Proteome Res 7:311-318.
3. Barclay AN (2009) Signal regulatory protein α (SIRPα)/CD47 interaction and function. Curr Opin Immunol 21:47-52.
4. Brown EJ, Frazier WA (2001) Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11:130-135.
5. Cryan JF, Markou A, Lucki I (2002) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23:238-245. (Pubitemid 34465544)
6. Cryan JF, Mombereau C, Vassout A (2005) The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 29:571-625. (Pubitemid 40755457)
7. De Pablo JM, Parra A, Segovia S, Guillamon A (1989) Learned immobility explains the behavior of rats in the forced swimming test. Physiol Behav 46:229-237. (Pubitemid 19244084)
8. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116-1127. (Pubitemid 43912554)
9. Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates. San Diego: Academic.
10. Fujino K, Yoshitake T, Inoue O, Ibii N, Kehr J, Ishida J, Nohta H, Yamaguchi M (2002) Increased serotonin release in mice frontal cortex and hippocampus induced by acute physiological stressors. Neurosci Lett 320:91-95.
11. Galeotti N, Ghelardini C, Caldari B, Bartolini A (1999) Effect of potassium channel modulators in mouse forced swimming test. Br J Pharmacol 126:1653-1659. (Pubitemid 29182351)
12. Grunwald IC, Klein R (2002) Axon guidance: receptor complexes and signaling mechanisms. Curr Opin Neurobiol 12:250-259.
13. Heckman KL, Pease LR (2007) Gene splicing and mutagenesis by PCRdriven overlap extension. Nat Protoc 2:924-932.
14. Heurteaux C, Lucas G, Guy N, El Yacoubi M, Thummler S, Peng XD, Noble F, Blondeau N, Widmann C, Borsotto M, Gobbi G, Vaugeois JM, Debonnel G, Lazdunski M (2006) Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat Neurosci 9:1134-1141. (Pubitemid 44306306)
15. Inagaki K, Yamao T, Noguchi T, Matozaki T, Fukunaga K, Takada T, Hosooka T, Akira S, Kasuga M (2000) SHPS-1 regulates integrinmediated cytoskeletal reorganization and cell motility. EMBO J 19:6721-6731. (Pubitemid 32011665)
16. Iwasaki Y, Ishikawa M, Okada N, Koizumi S (1997) Induction of a distinct morphology and signal transduction in TrkB/PC12 cells by nerve growth factor and brain-derived neurotrophic factor. J Neurochem 68:927-934. (Pubitemid 27086196)
17. Jiang P, Lagenaur CF, Narayanan V (1999) Integrin-associated protein is a ligand for the P84 neural adhesion molecule. J Biol Chem 274:559-562. (Pubitemid 129535207)
18. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453-462.
19. Lai HC, Jan LY (2006) The distribution and targeting of neuronal voltagegated ion channels. Nat Rev Neurosci 7:548-562. (Pubitemid 43989774)
20. Lindquist JM, Fredriksson JM, Rehnmark S, Cannon B, Nedergaard J (2000) β3-and α1-Adrenergic Erk1/2 activation is Src-but not Gi-mediated in Brown adipocytes. J Biol Chem 275:22670-22677.
21. Maness PF, Schachner M (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
22. Martinowich K, Manji H, Lu B (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10:1089-1093. (Pubitemid 47339961)
23. Matozaki T, Murata Y, Okazawa H, Ohnishi H (2009) Functions and molecular mechanisms of the CD47-SIRPα signalling pathway. Trends Cell Biol 19:72-80.
24. + channel β1 gene and functional expression of the β2 gene product. FEBS Lett 370:32-36.
25. Mi ZP, Jiang P, Weng WL, Lindberg FP, Narayanan V, Lagenaur CF (2000) Expression of a synapse-associated membrane protein, P84/SHPS-1, and its ligand, IAP/CD47, in mouse retina. J Comp Neurol 416:335-344. (Pubitemid 30027131)
26. Minichiello L, Korte M, Wolfer D, Kuhn R, Unsicker K, Cestari V, Rossi-Arnaud C, Lipp HP, Bonhoeffer T, Klein R (1999) Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24:401-414.
27. Miyakawa T, Yamada M, Duttaroy A, Wess J (2001) Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J Neurosci 21:5239-5250. (Pubitemid 32622949)
28. Miyakawa T, Leiter LM, Gerber DJ, Gainetdinov RR, Sotnikova TD, Zeng H, Caron MG, Tonegawa S (2003) Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Proc Natl Acad Sci U S A 100:8987-8992. (Pubitemid 36899210)
29. Morishima Y, Miyakawa T, Furuyashiki T, Tanaka Y, Mizuma H, Nakanishi S (2005) Enhanced cocaine responsiveness and impaired motor coordination in metabotropic glutamate receptor subtype 2 knockout mice. Proc Natl Acad Sci U S A 102:4170-4175. (Pubitemid 40388574)
30. Murata T, Ohnishi H, Okazawa H, Murata Y, Kusakari S, Hayashi Y, Miyashita M, Itoh H, Oldenborg PA, Furuya N, Matozaki T (2006) CD47 promotes neuronal development through Src- and FRG/ Vav2-mediated activation of Rac and Cdc42. J Neurosci 26:12397-12407. (Pubitemid 44864504)
31. Nakagawa S, Watanabe M, Isobe T, Kondo H, InoueY (1998) Cytological compartmentalization in the staggerer cerebellum, as revealed by calbindin immunohistochemistry for Purkinje cells. J Comp Neurol 395:112-120.
32. Nakazawa T, Komai S, Watabe AM, Kiyama Y, Fukaya M, Arima-Yoshida F, Horai R, Sudo K, Ebine K, Delawary M, Goto J, Umemori H, Tezuka T, Iwakura Y, Watanabe M, Yamamoto T, Manabe T (2006) NR2B tyrosine phosphorylation modulates fear learning as well as amygdaloid synaptic plasticity. EMBO J 25:2867-2877. (Pubitemid 43980393)
33. Neel BG, Gu H, Pao L (2003) The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 28:284-293. (Pubitemid 36776291)
34. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34:13-25.
35. Obata K, Kojima N, Nishiye H, Inoue H, Shirao T, Fujita SC, Uchizono K (1987) Four synaptic vesicle-specific proteins: identification by monoclonal antibodies and distribution in the nervous tissue and the adrenal medulla. Brain Res 404:169-179. (Pubitemid 17021893)
36. Ohe Y, Ohnishi H, Okazawa H, Tomizawa K, Kobayashi H, Okawa K, Matozaki T (2003) Characterization of nucleotide pyrophosphatase-5 as an oligomannosidic glycoprotein in rat brain. Biochem Biophys Res Commun 308:719-725. (Pubitemid 36976522)
37. Ohnishi H, Kaneko Y, Okazawa H, Miyashita M, Sato R, Hayashi A, Tada K, Nagata S, Takahashi M, Matozaki T (2005) Differential localization of Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 and CD47 and its molecular mechanisms in cultured hippocampal neurons. J Neurosci 25:2702-2711.
38. Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP (2000) Role of CD47 as a marker of self on red blood cells. Science 288:2051-2054. (Pubitemid 30397687)
39. Padovan CM, Guimaraes FS (2004) Antidepressant-like effects of NMDA-receptor antagonist injected into the dorsal hippocampus of rats. Pharmacol Biochem Behav 77:15-19. (Pubitemid 38076976)
40. Page ME, Brown K, Lucki I (2003) Simultaneous analyses of the neurochemical and behavioral effects of the norepinephrine reuptake inhibitor reboxetine in a rat model of antidepressant action. Psychopharmacology (Berl) 165:194-201. (Pubitemid 36056997)
41. Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730-732. (Pubitemid 8073804)
42. Salter MW, Kalia LV (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5:317-328. (Pubitemid 38478658)
43. Sandi C (2004) Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci 5:917-930. (Pubitemid 39593355)
44. Sato R, Ohnishi H, Kobayashi H, Kiuchi D, Hayashi A, Kaneko Y, Honma N, Okazawa H, Hirata Y, Matozaki T (2003) Regulation of multiple functions of SHPS-1, a transmembrane glycoprotein, by its cytoplasmic region. Biochem Biophys Res Commun 309:584-590.
45. Seligman ME, Maier SF (1967) Failure to escape traumatic shock. J Exp Psychol 71:1-9.
46. Shibata M, Yamasaki N, Miyakawa T, Kalaria RN, Fujita Y, Ohtani R, Ihara M, Takahashi R, Tomimoto H (2007) Selective impairment of working memory in a mouse model of chronic cerebral hypoperfusion. Stroke 38:2826-2832. (Pubitemid 47494024)
47. Takenaka K, Prasolava TK, Wang JC, Mortin-Toth SM, Khalouei S, Gan OI, Dick JE, Danska JS (2007) Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat Immunol 8:1313-1323. (Pubitemid 350138972)
48. Urani A, Chourbaji S, Gass P (2005) Mutant mouse models of depression: candidate genes and current mouse lines. Neurosci Biobehav Rev 29:805-828. (Pubitemid 40755466)
49. Wong EH, Sonders MS, Amara SG, Tinholt PM, Piercey MF, Hoffmann WP, Hyslop DK, Franklin S, Porsolt RD, Bonsignori A, Carfagna N, McArthur RA (2000) Reboxetine: a pharmacologically potent, selective, and specific norepinephrine reuptake inhibitor. Biol Psychiatry 47:818-829.
50. Xu W, Doshi A, Lei M, Eck MJ, Harrison SC (1999) Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol Cell 3:629-638. (Pubitemid 29268446)
51. Yagi T, Aizawa S, Tokunaga T, Shigetani Y, Takeda N, Ikawa Y (1993) A role for Fyn tyrosine kinase in the suckling behaviour of neonatal mice. Nature 366:742-745. (Pubitemid 24038514)
52. Yamagata M, Sanes JR, Weiner JA (2003) Synaptic adhesion molecules. Curr Opin Cell Biol 15:621-632.
53. Yasunaga M, Yagi T, Hanzawa N, Yasuda M, Yamanashi Y, Yamamoto T, Aizawa S, Miyauchi Y, Nishikawa S (1996) Involvement of Fyn tyrosine kinase in progression of cytokinesis of B lymphocyte progenitor. J Cell Biol 132:91-99. (Pubitemid 26035077)