Adult siRNA-induced knockdown of mGlu7 receptors reduces anxiety in the mouse

Neuropharmacology

Volumn 72, Issue , 2013, Pages 66-73

  O'Connor, Richard M ^a   Thakker, Deepak R ^b,e   Schmutz, Markus ^b   Van Der Putten, Herman ^b   Hoyer, Daniel ^b,f   Flor, Peter J ^c   Cryan, John F ^a,d  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITY OF REGENSBURG   (Germany)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e MEDTRONIC INC   (United States)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Anxiety; Glutamate; SiRNA

Indexed keywords

MESSENGER RNA; METABOTROPIC RECEPTOR 7; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; DEPRESSION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; FEAR; FORCED SWIMMING TEST; GENE FUNCTION; GENE SILENCING; HEAT STRESS; HYPERTHERMIA; LOCOMOTION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC MINIPUMP; PATHOPHYSIOLOGY; PRIORITY JOURNAL; STARTLE REFLEX;

EID: 84884877004     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.03.028     Document Type: Article

References (51)

1. Andlin-Sobocki, P., Jonsson, B., Wittchen, H.U., Olesen, J., 2005. Cost of disorders of the brain in Europe. Eur. J. Neurol. 12 (Suppl. 1), 1-27.
2. Baldwin, D.S., Anderson, I.M., Nutt, D.J., Bandelow, B., Bond, A., Davidson, J.R., den Boer, J.A., Fineberg, N.A., Knapp, M., Scott, J., Wittchen, H.U., 2005. Evidencebased guidelines for the pharmacological treatment of anxiety disorders: recommendations from the British Association for Psychopharmacology. J. Psychopharmacol. 19, 567-596. (Pubitemid 41578819)
3. Belzung, C., Griebel, G., 2001. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav. Brain Res. 125, 141-149. (Pubitemid 33000452)
4. Bischoff, S., Barhanin, J., Bettler, B., Mulle, C., Heinemann, S., 1997. Spatial distribution of kainate receptor subunit mRNA in the mouse basal ganglia and ventral mesencephalon. J. Comp. Neurol. 379, 541-562. (Pubitemid 27111154)
5. Bourin, M., Hascoet, M., 2003. The mouse light/dark box test. Eur. J. Pharmacol. 463, 55-65. (Pubitemid 36205072)
6. Bradley, S.R., Uslaner, J.M., Flick, R.B., Lee, A., Groover, K.M., Hutson, P.H., 2012. The mGluR7 allosteric agonist AMN082 produces antidepressant-like effects by modulating glutamatergic signaling. Pharmacol. Biochem. Behav. 101, 35-40.
7. Callaerts-Vegh, Z., Beckers, T., Ball, S.M., Baeyens, F., Callaerts, P.F., Cryan, J.F., Molnar, E., D'Hooge, R., 2006. Concomitant deficits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-deficient mice. J. Neurosci. 26, 6573-6582. (Pubitemid 44318338)
8. Crawley, J.N., 1999. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 835, 18-26. (Pubitemid 29336546)
9. Cryan, J.F., Sweeney, F.F., 2011. The age of anxiety: role of animal models of anxiolytic action in drug discovery. Br. J. Pharmacol. 164, 1129-1161.
10. Cryan, J.F., Hoyer, D., Markou, A., 2003a. Withdrawal from chronic amphetamine induces depressive-like behavioral effects in rodents. Biol. Psychiatry 54, 49-58. (Pubitemid 36776723)
11. Cryan, J.F., Kelly, P.H., Neijt, H.C., Sansig, G., Flor, P.J., van Der Putten, H., 2003b. Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur. J. Neurosci. 17, 2409-2417. (Pubitemid 36793749)
12. Cryan, J.F., Kelly, P.H., Chaperon, F., Gentsch, C., Mombereau, C., Lingenhoehl, K., Froestl, W., Bettler, B., Kaupmann, K., Spooren, W.P., 2004. Behavioral characterization of the novel GABAB receptor-positive modulator GS39783 (N, N'- dicyclopentyl-2-methylsulfanyl-5-nitro-pyrimidine-4,6-diamine): anxiolyticlike activity without side effects associated with baclofen or benzodiazepines. J. Pharmacol. Exp. Ther. 310, 952-963. (Pubitemid 39108915)
13. Falls, W.A., Carlson, S., Turner, J.G., Willott, J.F., 1997. Fear-potentiated startle in two strains of inbred mice. Behav. Neurosci. 111, 855-861. (Pubitemid 27335398)
14. Fendt, M., Schmid, S., Thakker, D.R., Jacobson, L.H., Yamamoto, R., Mitsukawa, K., Maier, R., Natt, F., Husken, D., Kelly, P.H., McAllister, K.H., Hoyer, D., van der Putten, H., Cryan, J.F., Flor, P.J., 2008. mGluR7 facilitates extinction of aversive memories and controls amygdala plasticity. Mol. Psychiatry 13, 970-979.
15. Fendt, M., Burki, H., Imobersteg, S., Lingenhohl, K., McAllister, K.H., Orain, D., Uzunov, D.P., Chaperon, F., 2009. Fear-reducing effects of intra-amygdala neuropeptide Y infusion in animal models of conditioned fear: an NPY Y1 receptor independent effect. Psychopharmacology (Berl) 206, 291-301.
16. Fendt, M., Burki, H., Imobersteg, S., van der Putten, H., McAllister, K., Leslie, J.C., Shaw, D., Holscher, C., 2010. The effect of mGlu8 deficiency in animal models of psychiatric diseases. Genes Brain Behav. 9, 33-44.
17. Ferraguti, F., Shigemoto, R., 2006. Metabotropic glutamate receptors. Cell. Tissue Res. 326, 483-504. (Pubitemid 44435821)
18. Finger, B.C., Dinan, T.G., Cryan, J.F., 2010. Leptin-deficient mice retain normal appetitive spatial learning yet exhibit marked increases in anxiety-related behaviours. Psychopharmacology (Berl) 210, 559-568.
19. Flor, P.J., Van Der Putten, H., Ruegg, D., Lukic, S., Leonhardt, T., Bence, M., Sansig, G., Knopfel, T., Kuhn, R., 1997. A novel splice variant of a metabotropic glutamate receptor, human mGluR7b. Neuropharmacology 36, 153-159. (Pubitemid 27149503)
20. Gerlai, R., 2002. Afraid of complications in gene targeting? Anxiety plays a role! Trends Neurosci. 25, 136. (Pubitemid 34164336)
21. Gu, Z., Liu, W.,Wei, J., Yan, Z., 2012. Regulation of N-methyl-D-aspartic acid (NMDA) receptors by metabotropic glutamate receptor 7. J. Biol. Chem. 287, 10265-10275.
22. Huesken, D., Lange, J., Mickanin, C., Weiler, J., Asselbergs, F., Warner, J., Meloon, B., Engel, S., Rosenberg, A., Cohen, D., Labow, M., Reinhardt, M., Natt, F., Hall, J., 2005. Design of a genome-wide siRNA library using an artificial neural network. Nat. Biotechnol. 23, 995-1001. (Pubitemid 41114034)
23. Jacobson, L.H., Cryan, J.F., 2007. Feeling strained? Influence of genetic background on depression-related behavior in mice: a review. Behav. Genet. 37, 171-213. (Pubitemid 46150858)
24. Kalinichev, M., Rouillier, M., Girard, F., Royer-Urios, I., Bournique, B., Finn, T., Charvin, D., Campo, B., Le Poul, E., Mutel, V., Poli, S., Neale, S.A., Salt, T.E., Lutjens, R., 2013. ADX71743, a potent and selective negative allosteric modulator of metabotropic glutamate receptor 7: in vitro and in vivo characterization. J. Pharmacol. Exp. Ther. 344, 624-636.
25. Klimesch, W., 2012. Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn. Sci. 16, 606-617.
26. Masugi, M., Yokoi, M., Shigemoto, R., Muguruma, K., Watanabe, Y., Sansig, G., van der Putten, H., Nakanishi, S., 1999. Metabotropic glutamate receptor subtype 7ablation causes deficit in fear response and conditioned taste aversion. J. Neurosci. 19, 955-963. (Pubitemid 29066158)
27. Mitsukawa, K., Mombereau, C., Lotscher, E., Uzunov, D.P., van der Putten, H., Flor, P.J., Cryan, J.F., 2006. Metabotropic glutamate receptor subtype 7 ablation causes dysregulation of the HPA axis and increases hippocampal BDNF protein levels: implications for stress-related psychiatric disorders. Neuropsychopharmacology 31, 1112-1122. (Pubitemid 43971829)
28. Mombereau, C., Kaupmann, K., Froestl, W., Sansig, G., van der Putten, H., Cryan, J.F., 2004. Genetic and pharmacological evidence of a role for GABA(B) receptors in the modulation of anxiety- and antidepressant-like behavior. Neuropsychopharmacology 29, 1050-1062. (Pubitemid 38670043)
29. Musazzi, L., Treccani, G., Mallei, A., Popoli, M., 2012. The action of antidepressants on the glutamate system: regulation of glutamate release and glutamate receptors. Biol. Psychiatry.
30. Nutt, D.J., 2005. Overview of diagnosis and drug treatments of anxiety disorders. CNS Spectr. 10, 49-56. (Pubitemid 40139743)
31. O'Connor, R.M., Cryan, J.F., 2010. Role of metabotropic glutamate receptors in CNS disorders. In: Siehler, S., Milligan, G. (Eds.), G Protein-coupled Receptors: Structure, Signaling, and Physiology. Cambridge University Press, pp. 321-379.
32. O'Connor, R.M., Cryan, J.F., 2013. The effects of mGlu7 receptor modulation in behavioural models sensitive to antidepressant action in two mouse strains. Behav. Pharmacol. 24, 105-113.
33. O'Connor, R.M., Finger, B.C., Flor, P.J., Cryan, J.F., 2010. Metabotropic glutamate receptor 7: at the interface of cognition and emotion. Eur. J. Pharmacol. 639, 123-131.
34. O'Connor, R.M., Pusceddu, M.M., O'Leary, O.F., Savignac, H.M., Bravo, J.A., El Yacoubi, M., Vaugeois, J.M., Dinan, T.G., Cryan, J.F., 2013. Hippocampal group III mGlu receptor mRNA levels are not altered in specific mouse models of stress, depression and antidepressant action. Pharmacol. Biochem. Behav. 103, 561-567.
35. O'Mahony, C.M., Bravo, J.A., Dinan, T.G., Cryan, J.F., 2010. Comparison of hippocampal metabotropic glutamate receptor 7 (mGlu7) mRNA levels in two animal models of depression. Neurosci. Lett. 482, 137-141.
36. Palucha, A., Klak, K., Branski, P., van der Putten, H., Flor, P.J., Pilc, A., 2007. Activation of the mGlu7 receptor elicits antidepressant-like effects in mice. Psychopharmacology (Berl) 194, 555-562. (Pubitemid 47492987)
37. Palucha-Poniewiera, A., Pilc, A., 2013. A selective mGlu7 receptor antagonist MMPIP reversed antidepressant-like effects of AMN082 in rats. Behav. Brain Res. 238, 109-112.
38. Palucha-Poniewiera, A., Branski, P., Lenda, T., Pilc, A., 2010. The antidepressant-like action of metabotropic glutamate 7 receptor agonist N, N'-bis(diphenylmethyl)- 1,2-ethanediamine (AMN082) is serotonin-dependent. J. Pharmacol. Exp. Ther. 334, 1066-1074.
39. Paxinos, G., Franklin, K.B.J., 2001. The Mouse Brain in Stereotaxic Coordinates. Academic Press.
40. Pelkey, K.A., Yuan, X., Lavezzari, G., Roche, K.W., McBain, C.J., 2007. mGluR7 undergoes rapid internalization in response to activation by the allosteric agonist AMN082. Neuropharmacology 52, 108-117. (Pubitemid 46026829)
41. Prosser, H.M., Gill, C.H., Hirst, W.D., Grau, E., Robbins, M., Calver, A., Soffin, E.M., Farmer, C.E., Lanneau, C., Gray, J., Schenck, E., Warmerdam, B.S., Clapham, C., Reavill, C., Rogers, D.C., Stean, T., Upton, N., Humphreys, K., Randall, A., Geppert, M., Davies, C.H., Pangalos, M.N., 2001. Epileptogenesis and enhanced prepulse inhibition in GABA(B1)-deficient mice. Mol. Cell. Neurosci. 17, 1059-1070. (Pubitemid 32641874)
42. Risbrough, V.B., Geyer, M.A., 2005. Anxiogenic treatments do not increase fearpotentiated startle in mice. Biol. Psychiatry 57, 33-43. (Pubitemid 39647589)
43. Sansig, G., Bushell, T.J., Clarke, V.R., Rozov, A., Burnashev, N., Portet, C., Gasparini, F., Schmutz, M., Klebs, K., Shigemoto, R., Flor, P.J., Kuhn, R., Knoepfel, T., Schroeder, M., Hampson, D.R., Collett, V.J., Zhang, C., Duvoisin, R.M., Collingridge, G.L., van Der Putten, H., 2001. Increased seizure susceptibility in mice lacking metabotropic glutamate receptor 7. J. Neurosci. 21, 8734-8745. (Pubitemid 33054837)
44. Schuler, V., Luscher, C., Blanchet, C., Klix, N., Sansig, G., Klebs, K., Schmutz, M., Heid, J., Gentry, C., Urban, L., Fox, A., Spooren, W., Jaton, A.L., Vigouret, J., Pozza, M., Kelly, P.H., Mosbacher, J., Froestl, W., Kaslin, E., Korn, R., Bischoff, S., Kaupmann, K., van der Putten, H., Bettler, B., 2001. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 31, 47-58. (Pubitemid 32757088)
45. Senechal, Y., Prut, L., Kelly, P.H., Staufenbiel, M., Natt, F., Hoyer, D., Wiessner, C., Dev, K.K., 2008. Increased exploratory activity of APP23 mice in a novel environment is reversed by siRNA. Brain Res. 1243, 124-133.
46. Stachowicz, K., Branski, P., Klak, K., van der Putten, H., Cryan, J.F., Flor, P.J., Andrzej, P., 2008. Selective activation of metabotropic G-protein-coupled glutamate 7 receptor elicits anxiolytic-like effects in mice by modulating GABAergic neurotransmission. Behav. Pharmacol. 19, 597-603.
47. Sukoff Rizzo, S.J., Leonard, S.K., Gilbert, A., Dollings, P., Smith, D.L., Zhang, M.Y., Di, L., Platt, B.J., Neal, S., Dwyer, J.M., Bender, C.N., Zhang, J., Lock, T., Kowal, D., Kramer, A., Randall, A., Huselton, C., Vishwanathan, K., Tse, S.Y., Butera, J., Ring, R.H., Rosenzweig-Lipson, S., Hughes, Z.A., Dunlop, J., 2011. The metabotropic glutamate receptor 7 allosteric modulator AMN082: a monoaminergic agent in disguise? J. Pharmacol. Exp. Ther. 338, 345-352.
48. Swanson, C.J., Bures, M., Johnson, M.P., Linden, A.M., Monn, J.A., Schoepp, D.D., 2005. Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nat. Rev. Drug Discov. 4, 131-144. (Pubitemid 40277494)
49. Thakker, D.R., Natt, F., Husken, D., Maier, R., Muller, M., van der Putten, H., Hoyer, D., Cryan, J.F., 2004. Neurochemical and behavioral consequences of widespread gene knockdown in the adult mouse brain by using nonviral RNA interference. Proc. Natl. Acad. Sci. U. S. A. 101, 17270-17275. (Pubitemid 39627809)
50. Thakker, D.R., Natt, F., Husken, D., van der Putten, H., Maier, R., Hoyer, D., Cryan, J.F., 2005. siRNA-mediated knockdown of the serotonin transporter in the adult mouse brain. Mol. Psychiatry 10, 782-789, 714. (Pubitemid 41129051)
51. Whittle, N., Schmuckermair, C., Gunduz Cinar, O., Hauschild, M., Ferraguti, F., Holmes, A., Singewald, N., 2013. Deep brain stimulation, histone deacetylase inhibitors and glutamatergic drugs rescue resistance to fear extinction in a genetic mouse model. Neuropharmacology 64, 414-423.