Noradrenergic antidepressant responses to desipramine in vivo are reciprocally regulated by arrestin3 and spinophilin

Neuropharmacology

Volumn 62, Issue 7, 2012, Pages 2354-2362

  Cottingham, Christopher ^a   Li, Xiaohua ^b,c   Wang, Qin ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c St Vincent's Health System   (United States)

Author keywords

Arrestin; Depression; Desipramine; Forced swim test; Spinophilin

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; ARRESTIN 3; CLONIDINE; DESIPRAMINE; FLUOXETINE; MEMBRANE PROTEIN; REBOXETINE; SPINOPHILIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; ADRENERGIC RECEPTOR AFFECTING AGENT; ALPHA 2 ADRENERGIC RECEPTOR; ANTIDEPRESSANT AGENT; ARRESTIN3; NERVE PROTEIN; NEURABIN; RETINA S ANTIGEN;

ADRENERGIC TRANSMISSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG PROTEIN BINDING; DRUG RECEPTOR BINDING; DRUG RESPONSE; FORCED SWIMMING TEST; IMMOBILIZATION; IN VIVO STUDY; MALE; MAZE TEST; MOUSE; NONHUMAN; NORADRENERGIC SYSTEM; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RECEPTOR UPREGULATION; REGULATORY MECHANISM; REVIEW; SINGLE DRUG DOSE; WILD TYPE; ADRENERGIC NERVE CELL; ANIMAL; ARTICLE; C57BL MOUSE; COMPARATIVE STUDY; DRUG EFFECT; MOUSE MUTANT; PHYSIOLOGY; SWIMMING; TRANSGENIC MOUSE;

ADRENERGIC NEURONS; ADRENERGIC UPTAKE INHIBITORS; ANIMALS; ANTIDEPRESSIVE AGENTS; ARRESTINS; DESIPRAMINE; IMMOBILIZATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; NERVE TISSUE PROTEINS; RECEPTORS, ADRENERGIC, ALPHA-2; SWIMMING;

EID: 84871904171     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.02.011     Document Type: Article

References (46)

1. P.B. Allen, C.C. Ouimet, and P. Greengard Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines Proc. Natl. Acad. Sci. U.S.A. 94 1997 9956 9961 (Pubitemid 27408172)
2. J.D. Altman, A.U. Trendelenburg, L. MacMillan, D. Bernstein, L. Limbird, K. Starke, B.K. Kobilka, and L. Hein Abnormal regulation of the sympathetic nervous system in alpha2A-adrenergic receptor knockout mice Mol. Pharmacol. 56 1999 154 161 (Pubitemid 29309824)
3. R.J. Baldessarini Drug therapy of depression and anxiety disorders L.L. Brunton, J.S. Lazo, K.L. Parker, Goodman & Gilman's The Pharmacological Basis of Therapeutics 11th ed 2006 McGraw-Hill, Inc. New York 429 460
4. L.M. Bohn, R.J. Lefkowitz, R.R. Gainetdinov, K. Peppel, M.G. Caron, and F.T. Lin Enhanced morphine analgesia in mice lacking beta-arrestin 2 Science 286 1999 2495 2498
5. L. Cervo, and R. Samanin Clonidine causes antidepressant-like effects in rats by activating alpha 2-adrenoceptors outside the locus coeruleus Eur. J. Pharmacol. 193 1991 309 313
6. L. Cervo, G. Grignaschi, and R. Samanin Alpha 2-adrenoceptor blockade prevents the effect of desipramine in the forced swimming test Eur. J. Pharmacol. 175 1990 301 307 (Pubitemid 20035536)
7. L. Chen, W. Zhou, P.C. Chen, I. Gaisina, S. Yang, and X. Li Glycogen synthase kinase-3beta is a functional modulator of serotonin-1B receptors Mol. Pharmacol. 79 2011 974 986
8. C. Cottingham, Y. Chen, K. Jiao, and Q. Wang The antidepressant desipramine is an arrestin-biased ligand at the alpha2A adrenergic receptor driving receptor downregulation in vitro and in vivo J. Biol. Chem. 286 2011 36063 36075
9. J.J. Crowley, M.D. Jones, O.F. O'Leary, and I. Lucki Automated tests for measuring the effects of antidepressants in mice Pharmacol. Biochem. Behav. 78 2004 269 274 (Pubitemid 38829362)
10. J.F. Cryan, A. Dalvi, S.H. Jin, B.R. Hirsch, I. Lucki, and S.A. Thomas Use of dopamine-beta-hydroxylase-deficient mice to determine the role of norepinephrine in the mechanism of action of antidepressant drugs J. Pharmacol. Exp. Ther. 298 2001 651 657 (Pubitemid 32673416)
11. J.F. Cryan, O.F. O'Leary, S.H. Jin, J.C. Friedland, M. Ouyang, B.R. Hirsch, M.E. Page, A. Dalvi, S.A. Thomas, and I. Lucki Norepinephrine-deficient mice lack responses to antidepressant drugs, including selective serotonin reuptake inhibitors Proc. Natl. Acad. Sci. U.S.A. 101 2004 8186 8191 (Pubitemid 38698075)
12. V.H. De, G. Vauquelin, K.J. De, J.P. De Backer, and L.I. Van Regional distribution of alpha 2A- and alpha 2B-adrenoceptor subtypes in postmortem human brain J. Neurochem. 58 1992 1555 1560
13. C.H. Duman, L. Schlesinger, M. Kodama, D.S. Russell, and R.S. Duman A role for MAP kinase signaling in behavioral models of depression and antidepressant treatment Biol. Psychiatry 61 2007 661 670 (Pubitemid 46328865)
14. J. Feng, Z. Yan, A. Ferreira, K. Tomizawa, J.A. Liauw, M. Zhuo, P.B. Allen, C.C. Ouimet, and P. Greengard Spinophilin regulates the formation and function of dendritic spines Proc. Natl. Acad. Sci. U.S.A. 97 2000 9287 9292 (Pubitemid 30626711)
15. N. Galeotti, and C. Ghelardini Selective modulation of the PKCvarepsilon/p38MAP kinase signalling pathway for the antidepressant-like activity of amitriptyline Neuropharmacology 2011
16. R. Gilsbach, C. Roser, N. Beetz, M. Brede, K. Hadamek, M. Haubold, J. Leemhuis, M. Philipp, J. Schneider, M. Urbanski, B. Szabo, D. Weinshenker, and L. Hein Genetic dissection of alpha2-adrenoceptor functions in adrenergic versus nonadrenergic cells Mol. Pharmacol. 75 2009 1160 1170
17. L. Hein, J.D. Altman, and B.K. Kobilka Two functionally distinct alpha2-adrenergic receptors regulate sympathetic neurotransmission Nature 402 1999 181 184
18. L.H. Jacobson, and J.F. Cryan Feeling strained? Influence of genetic background on depression-related behavior in mice: a review Behav. Genet. 37 2007 171 213 (Pubitemid 46150858)
19. A.E. Knaus, V. Muthig, S. Schickinger, E. Moura, N. Beetz, R. Gilsbach, and L. Hein Alpha2-adrenoceptor subtypes-unexpected functions for receptors and ligands derived from gene-targeted mouse models Neurochem. Int. 51 2007 277 281 (Pubitemid 47374320)
20. M. Kurtuncu, L.J. Luka, N. Dimitrijevic, T. Uz, and H. Manev Reliability assessment of an automated forced swim test device using two mouse strains J. Neurosci. Methods 149 2005 26 30 (Pubitemid 41606014)
21. X. Li, and R.S. Jope Is glycogen synthase kinase-3 a central modulator in mood regulation? Neuropsychopharmacology 35 2010 2143 2154
22. R. Lu, Y. Chen, C. Cottingham, N. Peng, K. Jiao, L.E. Limbird, J.M. Wyss, and Q. Wang Enhanced hypotensive, bradycardic, and hypnotic responses to alpha2-adrenergic agonists in spinophilin-null mice are accompanied by increased G protein coupling to the alpha2A-adrenergic receptor Mol. Pharmacol. 78 2010 279 286
23. M.J. Millan, A. Gobert, F. Lejeune, A. Newman-Tancredi, J.M. Rivet, A. Auclair, and J.L. Peglion S33005, a novel ligand at both serotonin and norepinephrine transporters: I. Receptor binding, electrophysiological, and neurochemical profile in comparison with venlafaxine, reboxetine, citalopram, and clomipramine J. Pharmacol. Exp. Ther. 298 2001 565 580 (Pubitemid 32673407)
24. E.J. Nestler, and S.E. Hyman Animal models of neuropsychiatric disorders Nat. Neurosci. 13 2010 1161 1169
25. E.J. Nestler, E. Gould, H. Manji, M. Buncan, R.S. Duman, H.K. Greshenfeld, R. Hen, S. Koester, I. Lederhendler, M. Meaney, T. Robbins, L. Winsky, and S. Zalcman Preclinical models: status of basic research in depression Biol. Psychiatry 52 2002 503 528 (Pubitemid 35284020)
26. M.F. O'Neill, D.J. Osborne, S.M. Woodhouse, and M.W. Conway Selective imidazoline I2 ligands do not show antidepressant-like activity in the forced swim test in mice J. Psychopharmacol. 15 2001 18 22 (Pubitemid 32242099)
27. B. Petit-Demouliere, F. Chenu, and M. Bourin Forced swimming test in mice: a review of antidepressant activity Psychopharmacology (Berl) 177 2005 245 255 (Pubitemid 40137284)
28. A. Polter, S. Yang, A.A. Zmijewska, G.T. van, J.H. Paik, R.A. Depinho, S.L. Peng, R.S. Jope, and X. Li Forkhead box, class O transcription factors in brain: regulation and behavioral manifestation Biol. Psychiatry 65 2009 150 159
29. R.D. Porsolt, A. Bertin, and M. Jalfre Behavioral despair in mice: a primary screening test for antidepressants Arch. Int. Pharmacodyn. Ther. 229 1977 327 336 (Pubitemid 8225714)
30. R.D. Porsolt, P.M. Le, and M. Jalfre Depression: a new animal model sensitive to antidepressant treatments Nature 266 1977 730 732 (Pubitemid 8073804)
31. S. Rajagopal, K. Rajagopal, and R.J. Lefkowitz Teaching old receptors new tricks: biasing seven-transmembrane receptors Nat. Rev. Drug Discov. 9 2010 373 386
32. J.P. Reneric, M. Bouvard, and L. Stinus Idazoxan and 8-OH-DPAT modify the behavioral effects induced by either NA, or 5-HT, or dual NA/5-HT reuptake inhibition in the rat forced swimming test Neuropsychopharmacology 24 2001 379 390 (Pubitemid 32157554)
33. M. Sastre, and J.A. Garcia-Sevilla Alpha 2-adrenoceptor subtypes identified by [3H]RX821002 binding in the human brain: the agonist guanoxabenz does not discriminate different forms of the predominant alpha 2A subtype J. Neurochem. 63 1994 1077 1085
34. A. Satoh, H. Nakanishi, H. Obaishi, M. Wada, K. Takahashi, K. Satoh, K. Hirao, H. Nishioka, Y. Hata, A. Mizoguchi, and Y. Takai Neurabin-II/spinophilin. An actin filament-binding protein with one pdz domain localized at cadherin-based cell-cell adhesion sites J. Biol. Chem. 273 1998 3470 3475 (Pubitemid 28109767)
35. C.L. Schmid, and L.M. Bohn Physiological and pharmacological implications of beta-arrestin regulation Pharmacol. Ther. 121 2009 285 293
36. C.L. Schmid, and L.M. Bohn Serotonin, but not N-methyltryptamines, activates the serotonin 2A receptor via a ss-arrestin2/Src/Akt signaling complex in vivo J. Neurosci. 30 2010 13513 13524
37. N.L. Schramm, M.P. McDonald, and L.E. Limbird The alpha(2a)-adrenergic receptor plays a protective role in mouse behavioral models of depression and anxiety J. Neurosci. 21 2001 4875 4882 (Pubitemid 32565645)
38. S.K. Shenoy, and R.J. Lefkowitz Multifaceted roles of beta-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling Biochem. J. 375 2003 503 515 (Pubitemid 37433499)
39. A.D. Shields, Q. Wang, and D.G. Winder alpha2A-adrenergic receptors heterosynaptically regulate glutamatergic transmission in the bed nucleus of the stria terminalis Neuroscience 163 2009 339 351
40. J.D. Sweatt Mechanisms of Memory second ed. 2010 Academic Press London
41. J.D. Violin, and R.J. Lefkowitz Beta-arrestin-biased ligands at seven-transmembrane receptors Trends Pharmacol. Sci. 28 2007 416 422
42. Q. Wang, and L.E. Limbird Regulation of alpha2AR trafficking and signaling by interacting proteins Biochem. Pharmacol. 73 2007 1135 1145 (Pubitemid 46413176)
43. R. Wang, L.B. Macmillan, R.T. Fremeau Jr., M.A. Magnuson, J. Lindner, and L.E. Limbird Expression of alpha 2-adrenergic receptor subtypes in the mouse brain: evaluation of spatial and temporal information imparted by 3 kb of 5′ regulatory sequence for the alpha 2A AR-receptor gene in transgenic animals Neuroscience 74 1996 199 218
44. Q. Wang, J. Zhao, A.E. Brady, J. Feng, P.B. Allen, R.J. Lefkowitz, P. Greengard, and L.E. Limbird Spinophilin blocks arrestin actions in vitro and in vivo at G protein-coupled receptors Science 304 2004 1940 1944 (Pubitemid 38822181)
45. S.U. Yanpallewar, K. Fernandes, S.V. Marathe, K.C. Vadodaria, D. Jhaveri, K. Rommelfanger, U. Ladiwala, S. Jha, V. Muthig, L. Hein, P. Bartlett, D. Weinshenker, and V.A. Vaidya Alpha2-adrenoceptor blockade accelerates the neurogenic, neurotrophic, and behavioral effects of chronic antidepressant treatment J. Neurosci. 30 2010 1096 1109
46. H.T. Zhang, L.R. Whisler, Y. Huang, Y. Xiang, and J.M. O'Donnell Postsynaptic alpha-2 adrenergic receptors are critical for the antidepressant-like effects of desipramine on behavior Neuropsychopharmacology 34 2009 1067 1077