Alteration by p11 of mGluR5 localization regulates depression-like behaviors

Molecular Psychiatry

Volumn 20, Issue 12, 2015, Pages 1546-1556

  Lee, K W ^a   Westin, L ^b   Kim, J ^c   Chang, J C ^a   Oh, Y S ^a   Amreen, B ^a   Gresack, J ^a   Flajolet, M ^a   Kim, D ^c   Aperia, A ^b   Kim, Y ^a   Greengard, P ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; METABOTROPIC RECEPTOR 5; PARVALBUMIN; PROTEIN S100A10; SEROTONIN RECEPTOR; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID; GRM5 PROTEIN, MOUSE; LIPOCORTIN 2; PROTEIN S 100; S100 CALCIUM BINDING PROTEIN A10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; BEHAVIOR; CELL CULTURE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DEPRESSION; DRUG MECHANISM; ELECTROPHYSIOLOGY; GENE OVEREXPRESSION; GLUTAMATERGIC NEURON; INTERNEURON; INVESTIGATIVE PROCEDURES; MALE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; HEK293 CELL LINE; HUMAN; METABOLISM; NERVE CELL INHIBITION; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; ANNEXIN A2; DEPRESSION; GABAERGIC NEURONS; GLUTAMIC ACID; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONS; PARVALBUMINS; RECEPTOR, METABOTROPIC GLUTAMATE 5; S100 PROTEINS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84947615912     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.132     Document Type: Article

References (68)

1. Belmaker RH, Agam G. Major depressive disorder. N Engl J Med 2008; 358: 55-68.
2. Svenningsson P, Kim Y, Warner-Schmidt J, Oh YS, Greengard P. p11 and its role in depression and therapeutic responses to antidepressants. Nat Rev Neurosci 2013; 14: 673-680.
3. Svenningsson P, Chergui K, Rachleff I, Flajolet M, Zhang X, El Yacoubi M et al. Alterations in 5-HT1B receptor function by p11 in depression-like states. Science 2006; 311: 77-80.
4. Warner-Schmidt JL, Flajolet M, Maller A, Chen EY, Qi H, Svenningsson P et al. Role of p11 in cellular and behavioral effects of 5-HT4 receptor stimulation. J Neurosci 2009; 29: 1937-1946.
5. Alexander B, Warner-Schmidt J, Eriksson T, Tamminga C, Arango-Lievano M, Ghose S et al. Reversal of depressed behaviors in mice by p11 gene therapy in the nucleus accumbens. Sci Transl Med 2010; 2: 54ra76.
6. Oh YS, Gao P, Lee KW, Ceglia I, Seo JS, Zhang X et al. SMARCA3, a chromatinremodeling factor, is required for p11-dependent antidepressant action. Cell 2013; 152: 831-843.
7. Schmidt EF, Warner-Schmidt JL, Otopalik BG, Pickett SB, Greengard P, Heintz N. Identification of the cortical neurons that mediate antidepressant responses. Cell 2012; 149: 1152-1163.
8. Egeland M, Warner-Schmidt J, Greengard P, Svenningsson P. Neurogenic effects of fluoxetine are attenuated in p11 (S100A10) knockout mice. Biol Psychiatry 2010; 67: 1048-1056.
9. Conn PJ, Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 1997; 37: 205-237.
10. Chaki S, Ago Y, Palucha-Paniewiera A, Matrisciano F, A Pilc. mGlu2/3 and mGlu5 receptors: potential targets for novel antidepressants. Neuropharmacology 2013; 66: 40-52.
11. Goeldner C, Ballard TM, Knoflach F, Wichmann J, Gatti S, Umbricht D. Cognitive impairment in major depression and the mGlu2 receptor as a therapeutic target. Neuropharmacology 2013; 64: 337-346.
12. Palucha-Poniewiera A, Wieronska JM, Branski P, Burnat G, Chruscicka B, Pilc A. Is the mGlu5 receptor a possible target for new antidepressant drugs? Pharmacol Rep 2013; 65: 1506-1511.
13. Warner-Schmidt JL, Vanover KE, Chen EY, Marshall JJ, Greengard P. Antidepressant effects of selective serotonin reuptake inhibitors (SSRIs) are attenuated by antiinflammatory drugs in mice and humans. Proc Natl Acad Sci USA 2011; 108: 9262-9267.
14. Xu J, Zhu Y, Contractor A, Heinemann SF. mGluR5 has a critical role in inhibitory learning. J Neurosci 2009; 29: 3676-3684.
15. Tatarczynska E, Klodzinska A, Chojnacka-Wojcik E, Palucha A, Gasparini F, Kuhn R et al. Potential anxiolytic-and antidepressant-like effects of MPEP, a potent, selective and systemically active mGlu5 receptor antagonist. Br J Pharmacol 2001; 132: 1423-1430.
16. Li X, Need AB, Baez M, Witkin JM. Metabotropic glutamate 5 receptor antagonism is associated with antidepressant-like effects in mice. J Pharmacol Exp Ther 2006; 319: 254-259.
17. Iijima M, Fukumoto K, Chaki S. Acute and sustained effects of a metabotropic glutamate 5 receptor antagonist in the novelty-suppressed feeding test. Behav Brain Res 2012; 235: 287-292.
18. Wang H, Westin L, Nong Y, Birnbaum S, Bendor J, Brismar H et al. Norbin is an endogenous regulator of metabotropic glutamate receptor 5 signaling. Science 2009; 326: 1554-1557.
19. Joseph G, Pick E. "Peptide walking" is a novel method for mapping functional domains in proteins. Its application to the Rac1-dependent activation of NADPH oxidase. J Biol Chem 1995; 270: 29079-29082.
20. Li N, Lee B, Liu RJ, Banasr M, Dwyer JM, Iwata M et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 2010; 329: 959-964.
21. Chang JC, Tomlinson ID, Warnement MR, Ustione A, Carneiro AM, Piston DW et al. Single molecule analysis of serotonin transporter regulation using antagonistconjugated quantum dots reveals restricted, p38 MAPK-dependent mobilization underlying uptake activation. J Neurosci 2012; 32: 8919-8929.
22. Izumi J, Washizuka M, Hayashi-Kuwabara Y, Yoshinaga K, Tanaka Y, Ikeda Y et al. Evidence for a depressive-like state induced by repeated saline injections in Fischer 344 rats. Pharmacol Biochem Behav 1997; 57: 883-888.
23. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P. Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 2004; 29: 2007-2017.
24. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC et al. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 2012; 15: 769-775.
25. Anikeeva P, Andalman AS, Witten I, Warden M, Goshen I, Grosenick L et al. Optetrode: A multichannel readout for optogenetic control in freely moving mice. Nat Neurosci 2012; 15: 163-170.
26. Wilson FA, O'Scalaidhe SP, Goldman-Rakic PS. Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci USA 1994; 91: 4009-4013.
27. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 1990; 13: 99-104.
28. Homayoun H, Moghaddam B. NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 2007; 27: 11496-11500.
29. Girard C, Tinel N, Terrenoire C, Romey G, Lazdunski M, Borsotto M. p11, an annexin II subunit, an auxiliary protein associated with the background K+ channel, TASK-1. EMBO J 2002; 21: 4439-4448.
30. van de Graaf SF, Hoenderop JG, Gkika D, Lamers D, Prenen J, Rescher U et al. Functional expression of the epithelial Ca(2+) channels (TRPV5 and TRPV6) requires association of the S100A10-annexin 2 complex. EMBO J 2003; 22: 1478-1487.
31. Rezvanpour A, Phillips JM, Shaw GS. Design of high-affinity S100-target hybrid proteins. Protein Sci 2009; 18: 2528-2536.
32. Okuse K, Malik-Hall M, Baker MD, Poon WY, Kong H, Chao MV et al. Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature 2002; 417: 653-656.
33. Donier E, Rugiero F, Okuse K, Wood JN. Annexin II light chain p11 promotes functional expression of acid-sensing ion channel ASIC1a. J Biol Chem 2005; 280: 38666-38672.
34. Lopez-Bendito G, Shigemoto R, Fairen A, Lujan R. Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb Cortex 2002; 12: 625-638.
35. van Hooft JA, Giuffrida R, Blatow M, Monyer H. Differential expression of group I metabotropic glutamate receptors in functionally distinct hippocampal interneurons. J Neurosci 2000; 20: 3544-3551.
36. Sun QQ, Zhang Z, Jiao Y, Zhang C, Szabo G, Erdelyi F. Differential metabotropic glutamate receptor expression and modulation in two neocortical inhibitory networks. J Neurophysiol 2009; 101: 2679-2692.
37. Egeland M, Warner-Schmidt J, Greengard P, Svenningsson P. Co-expression of serotonin 5-HT(1B) and 5-HT(4) receptors in p11 containing cells in cerebral cortex, hippocampus, caudate-putamen and cerebellum. Neuropharmacology 2011; 61: 442-450.
38. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011; 477: 171-178.
39. Lapidus KA, Soleimani L, Murrough JW. Novel glutamatergic drugs for the treatment of mood disorders. Neuropsychiatr Dis Treat 2013; 9: 1101-1112.
40. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-809.
41. Dulawa SC, Hen R. Recent advances in animal models of chronic antidepressant effects: The novelty-induced hypophagia test. Neurosci Biobehav Rev 2005; 29: 771-783.
42. Koike H, Fukumoto K, Iijima M, Chaki S. Role of BDNF/TrkB signaling in antidepressant-like effects of a group II metabotropic glutamate receptor antagonist in animal models of depression. Behav Brain Res 2013; 238: 48-52.
43. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 2011; 71: 45-61.
44. Chu Z, Hablitz JJ. Activation of group I mGluRs increases spontaneous IPSC frequency in rat frontal cortex. J Neurophysiol 1998; 80: 621-627.
45. Govindaiah G, Cox CL. Metabotropic glutamate receptors differentially regulate GABAergic inhibition in thalamus. J Neurosci 2006; 26: 13443-13453.
46. Campanac E, Gasselin C, Baude A, Rama S, Ankri N, Debanne D. Enhanced intrinsic excitability in basket cells maintains excitatory-inhibitory balance in hippocampal circuits. Neuron 2013; 77: 712-722.
47. Elliott R, Baker SC, Rogers RD, O'Leary DA, Paykel ES, Frith CD et al. Prefrontal dysfunction in depressed patients performing a complex planning task: A study using positron emission tomography. Psychol Med 1997; 27: 931-942.
48. Disner SG, Beevers CG, Haigh EA, Beck AT. Neural mechanisms of the cognitive model of depression. Nat Rev Neurosci 2011; 12: 467-477.
49. Covington HE 3rd, Lobo MK, Maze I, Vialou V, Hyman JM, Zaman S et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci 2010; 30: 16082-16090.
50. Hamani C, Diwan M, Macedo CE, Brandao ML, Shumake J, Gonzalez-Lima F et al. Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol Psychiatry 2010; 67: 117-124.
51. Romano C, Sesma MA, McDonald CT, O'Malley K, Van den Pol AN, Olney JW. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J Comp Neurol 1995; 355: 455-469.
52. Warner-Schmidt JL, Schmidt EF, Marshall JJ, Rubin AJ, Arango-Lievano M, Kaplitt MG et al. Cholinergic interneurons in the nucleus accumbens regulate depression-like behavior. Proc Natl Acad Sci USA 2012; 109: 11360-11365.
53. Svenningsson P, Greengard P. p11 (S100A10)-an inducible adaptor protein that modulates neuronal functions. Curr Opin Pharmacol 2007; 7: 27-32.
54. Compan V, Zhou M, Grailhe R, Gazzara RA, Martin R, Gingrich J et al. Attenuated response to stress and novelty and hypersensitivity to seizures in 5-HT4 receptor knock-out mice. J Neurosci 2004; 24: 412-419.
55. Coryell MW, Wunsch AM, Haenfler JM, Allen JE, Schnizler M, Ziemann AE et al. Acid-sensing ion channel-1a in the amygdala, a novel therapeutic target in depression-related behavior. J Neurosci 2009; 29: 5381-5388.
56. Warner-Schmidt JL, Chen EY, Zhang X, Marshall JJ, Morozov A, Svenningsson P et al. A role for p11 in the antidepressant action of brain-derived neurotrophic factor. Biol Psychiatry 2010; 68: 528-535.
57. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL et al. Homer: A protein that selectively binds metabotropic glutamate receptors. Nature 1997; 386: 284-288.
58. Choi KY, Chung S, Roche KW. Differential binding of calmodulin to group I metabotropic glutamate receptors regulates receptor trafficking and signaling. J Neurosci 2011; 31: 5921-5930.
59. Kitano J, Yamazaki Y, Kimura K, Masukado T, Nakajima Y, Nakanishi S. Tamalin is a scaffold protein that interacts with multiple neuronal proteins in distinct modes of protein-protein association. J Biol Chem 2003; 278: 14762-14768.
60. Rietschel M, Mattheisen M, Frank J, Treutlein J, Degenhardt F, Breuer R et al. Genome-wide association-, replication-, and neuroimaging study implicates HOMER1 in the etiology of major depression. Biol Psychiatry 2010; 68: 578-585.
61. Carroll FI. Antagonists at metabotropic glutamate receptor subtype 5: structure activity relationships and therapeutic potential for addiction. Ann NY Acad Sci 2008; 1141: 221-232.
62. Gregory KJ, Dong EN, Meiler J, Conn PJ. Allosteric modulation of metabotropic glutamate receptors: structural insights and therapeutic potential. Neuropharmacology 2011; 60: 66-81.
63. Yin S, Niswender CM. Progress toward advanced understanding of metabotropic glutamate receptors: structure, signaling and therapeutic indications. Cell Signal 2014; 26: 2284-2297.
64. Piers TM, Kim DH, Kim BC, Regan P, Whitcomb DJ, Cho K. Translational Concepts of mGluR5 in Synaptic Diseases of the Brain. Front Pharmacol 2012; 3: 199.
65. Krueger DD, Bear MF. Toward fulfilling the promise of molecular medicine in fragile X syndrome. Annu Rev Med 2011; 62: 411-429.
66. Bezard E, Pioli EY, Li Q, Girard F, Mutel V, Keywood C et al. The mGluR5 negative allosteric modulator dipraglurant reduces dyskinesia in the MPTP macaque model. Mov Disord 2014; 29: 1074-1079.
67. Awad H, Hubert GW, Smith Y, Levey AI, Conn PJ. Activation of metabotropic glutamate receptor 5 has direct excitatory effects and potentiates NMDA receptor currents in neurons of the subthalamic nucleus. J Neurosci 2000; 20: 7871-7879.
68. Rosenbrock H, Kramer G, Hobson S, Koros E, Grundl M, Grauert M et al. Functional interaction of metabotropic glutamate receptor 5 and NMDA-receptor by a metabotropic glutamate receptor 5 positive allosteric modulator. Eur J Pharmacol 2010; 639: 40-46.