Negative allosteric modulation of the mGlu7 receptor reduces visceral hypersensitivity in a stress-sensitive rat strain

Neurobiology of Stress

Volumn 2, Issue , 2015, Pages 28-33

  Moloney, Rachel D ^a,b   Golubeva, Anna V ^a   O'Connor, Richard M ^b   Kalinichev, Mikhail ^c   Dinan, Timothy G ^a,b   Cryan, John F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c Addex Therapeutics Plan les Ouates Switzerland   (Switzerland)

Author keywords

Anxiety; Glutamate; Visceral pain; Wistar Kyoto

Indexed keywords

ADX71743; BETA CYCLODEXTRIN; CORTICOSTERONE; ISOFLURANE; METABOTROPIC RECEPTOR 7; UNCLASSIFIED DRUG;

ALLOSTERISM; ANIMAL MODEL; ANXIETY; ARTICLE; BLOOD ANALYSIS; COLON DILATATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HYPERSENSITIVITY; MALE; NONHUMAN; OPEN FIELD BEHAVIOR; PAIN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STIMULUS; STRESS;

EID: 84927539538     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2015.04.001     Document Type: Article

References (67)

1. Aguilera M., Vergara P., Martinez V. Stress and antibiotics alter luminal and wall-adhered microbiota and enhance the local expression of visceral sensory-related systems in mice. Neurogastroenterol. Motil. 2013, 25:e515-e529.
2. Blackshaw L.A., Page A.J., Young R.L. Metabotropic glutamate receptors as novel therapeutic targets on visceral sensory pathways. Front. Neurosci. 2011, 5:40.
3. Callaerts-Vegh Z., Beckers T., Ball S.M., Baeyens F., Callaerts P.F., Cryan J.F., Molnar E., D'Hooge R. Concomitant deficits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-deficient mice. J.Neurosci. 2006, 26:6573-6582.
4. Cao D.Y., Bai G., Ji Y., Traub R.J. Epigenetic upregulation of metabotropic glutamate receptor 2 in the spinal cord attenuates oestrogen-induced visceral hypersensitivity. Gut 2014 Nov 6, pii: gutjnl-2014-307748. 10.1136/gutjnl-2014-307748.
5. Carroll S.Y., O'Mahony S.M., Grenham S., Cryan J.F., Hyland N.P. Disodium cromoglycate reverses colonic visceral hypersensitivity and influences colonic ion transport in a stress-sensitive rat strain. PLoS One 2013, 8:e84718.
6. Cartmell J., Schoepp D.D. Regulation of neurotransmitter release by metabotropic glutamate receptors. J.Neurochem. 2000, 75:889-907.
7. Cervero F. Visceral pain: mechanisms of peripheral and central sensitization. Ann. Med. 1995, 27:235-239.
8. Cervero F. Visceral pain-central sensitisation. Gut 2000, 47(Suppl.4):iv56-iv57. (discussion iv58).
9. Cervero F. Visceral versus somatic pain: similarities and differences. Dig. Dis. 2009, 27(Suppl.1):3-10.
10. Chaloner A., Greenwood-Van Meerveld B. Sexually dimorphic effects of unpredictable early life adversity on visceral pain behavior in a rodent model. J.Pain 2013, 14:270-280.
11. Crock L.W., Kolber B.J., Morgan C.D., Sadler K.E., Vogt S.K., Bruchas M.R., Gereau R.W.T. Central amygdala metabotropic glutamate receptor 5 in the modulation of visceral pain. J.Neurosci. 2012, 32:14217-14226.
12. Crock L.W., Stemler K.M., Song D.G., Abbosh P., Vogt S.K., Qiu C.S., Lai H.H., Mysorekar I.U., Gereau R.W.T. Metabotropic glutamate receptor 5 (mGluR5) regulates bladder nociception. Mol. Pain 2012, 8:20.
13. Cryan J.F., Kelly P.H., Neijt H.C., Sansig G., Flor P.J., van der Putten H. Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur. J. Neurosci. 2003, 17:2409-2417.
14. Dolan S., Gunn M.D., Biddlestone L., Nolan A.M. The selective metabotropic glutamate receptor 7 allosteric agonist AMN082 inhibits inflammatory pain-induced and incision-induced hypersensitivity in rat. Behav. Pharmacol. 2009, 20:596-604.
15. Dolan S., Gunn M.D., Crossan C., Nolan A.M. Activation of metabotropic glutamate receptor 7 in spinal cord inhibits pain and hyperalgesia in a novel formalin model in sheep. Behav. Pharmacol. 2011, 22:582-588.
16. Felice V.D., Gibney S.M., Gosselin R.D., Dinan T.G., O'Mahony S.M., Cryan J.F. Differential activation of the prefrontal cortex and amygdala following psychological stress and colorectal distension in the maternally separated rat. Neuroscience 2014, 267:252-262.
17. Fendt M., Imobersteg S., Peterlik D., Chaperon F., Mattes C., Wittmann C., Olpe H.R., Mosbacher J., Vranesic I., van der Putten H., McAllister K.H., Flor P.J., Gee C.E. Differential roles of mGlu(7) and mGlu(8) in amygdala-dependent behavior and physiology. Neuropharmacology 2013, 72:215-223.
18. 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. mGluR7 facilitates extinction of aversive memories and controls amygdala plasticity. Mol. Psychiatry 2008, 13:970-979.
19. Flor P.J., van der Putten H., Ruegg D., Lukic S., Leonhardt T., Bence M., Sansig G., Knopfel T., Kuhn R. Anovel splice variant of a metabotropic glutamate receptor, human mGluR7b. Neuropharmacology 1997, 36:153-159.
20. Fukudo S. Stress and visceral pain: focusing on irritable bowel syndrome. Pain 2013, 154(Suppl.1):S63-S70.
21. Fundytus M.E. Glutamate receptors and nociception: implications for the drug treatment of pain. CNS Drugs 2001, 15:29-58.
22. G S., Suvarna P., Hadigal S., Kamath P., Prabhu N., Shenoy K.A., Lc P. Can metabotropic glutamate receptor 7 (mGluR 7) be a novel target for analgesia?. J.Clin. Diagn. Res. 2014, 8:HC16-HC18.
23. Golubeva A.V., Moloney R.D., O'Connor R.M., Dinan T.G., Cryan J.F. Metabotropic glutamate receptors in central nervous system diseases. Curr. Drug Targets 2015, Epub ahead of print.
24. Gunter W.D., Shepard J.D., Foreman R.D., Myers D.A., Greenwood-Van Meerveld B. Evidence for visceral hypersensitivity in high-anxiety rats. Physiol. Behav. 2000, 69:379-382.
25. Hong S., Zheng G., Wiley J.W. Epigenetic regulation of genes that modulate chronic stress-induced visceral pain in the peripheral nervous system. Gastroenterology 2015, 148:148-157e7.
26. Hyland N.P., O'Mahony S.M., O'Malley D., O'Mahony C.M., Dinan T.G., Cryan J.F. Early-life stress selectively affects gastrointestinal but not behavioral responses in a genetic model of brain-gut axis dysfunction. Neurogastroenterol. Motil. 2015, 27:105-113.
27. Jennings E.M., Okine B.N., Roche M., Finn D.P. Stress-induced hyperalgesia. Prog. Neurobiol. 2014, 121:1-18.
28. Johnson A.C., Greenwood-Van Meerveld B. Stress-induced pain: a target for the development of novel therapeutics. J.Pharmacol. Exp. Ther. 2014, 351:327-335.
29. Johnson M.P., Kelly G., Chamberlain M. Changes in rat serum corticosterone after treatment with metabotropic glutamate receptor agonists or antagonists. J.Neuroendocrinol. 2001, 13:670-677.
30. Julio-Pieper M., Flor P.J., Dinan T.G., Cryan J.F. Exciting times beyond the brain: metabotropic glutamate receptors in peripheral and non-neural tissues. Pharmacol. Rev. 2011, 63:35-58.
31. 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. ADX71743, a potent and selective negative allosteric modulator of metabotropic glutamate receptor 7: invitro and invivo characterization. J.Pharmacol. Exp. Ther. 2013, 344:624-636.
32. Kinoshita A., Shigemoto R., Ohishi H., van der Putten H., Mizuno N. Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J.Comp. Neurol. 1998, 393:332-352.
33. Larauche M., Mulak A., Tache Y. Stress and visceral pain: from animal models to clinical therapies. Exp. Neurol. 2012, 233:49-67.
34. Lee U.J., Ackerman A.L., Wu A., Zhang R., Leung J., Bradesi S., Mayer E.A., Rodriguez L.V. Chronic psychological stress in high-anxiety rats induces sustained bladder hyperalgesia. Physiol. Behav. 2015, 139:541-548.
35. Lindstrom E., Brusberg M., Hughes P.A., Martin C.M., Brierley S.M., Phillis B.D., Martinsson R., Abrahamsson C., Larsson H., Martinez V., Blackshaw L.A. Involvement of metabotropic glutamate 5 receptor in visceral pain. Pain 2008, 137:295-305.
36. Liu X.H., Han M., Zhu J.X., Sun N., Tang J.S., Huo F.Q., Li J., Xu F.Y., Du J.Q. Metabotropic glutamate subtype 7 and 8 receptors oppositely modulate cardiac nociception in the rat nucleus tractus solitarius. Neuroscience 2012, 220:322-329.
37. Masugi M., Yokoi M., Shigemoto R., Muguruma K., Watanabe Y., Sansig G., van der Putten H., Nakanishi S. Metabotropic glutamate receptor subtype 7 ablation causes deficit in fear response and conditioned taste aversion. J.Neurosci. 1999, 19:955-963.
38. Mayer E.A. The neurobiology of stress and gastrointestinal disease. Gut 2000, 47:861-869.
39. Mayer E.A., Craske M., Naliboff B.D. Depression, anxiety, and the gastrointestinal system. J.Clin. Psychiatry 2001, 62(Suppl.8):28-36. (discussion 37).
40. Mayer E.A., Naliboff B.D., Chang L., Coutinho S.V. V.Stress and irritable bowel syndrome. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280:G519-G524.
41. McEwen B.S. Protective and damaging effects of stress mediators. N.Engl. J. Med. 1998, 338:171-179.
42. Mitsukawa K., Mombereau C., Lotscher E., Uzunov D.P., van der Putten H., Flor P.J., Cryan J.F. 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 2006, 31:1112-1122.
43. Mitsukawa K., Yamamoto R., Ofner S., Nozulak J., Pescott O., Lukic S., Stoehr N., Mombereau C., Kuhn R., McAllister K.H., van der Putten H., Cryan J.F., Flor P.J. Aselective metabotropic glutamate receptor 7 agonist: activation of receptor signaling via an allosteric site modulates stress parameters invivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18712-18717.
44. Moghaddam B., Adams B.W. Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 1998, 281:1349-1352.
45. Moloney R.D., O'Mahony S.M., Dinan T.G., Cryan J.F. Stress-induced visceral pain: towards animal models of irritable-bowel syndrome and associated co-morbidities. Front. Psychiatry 2015, 6.
46. Neugebauer V., Carlton S.M. Peripheral metabotropic glutamate receptors as drug targets for pain relief. Expert Opin. Ther. Targets 2002, 6:349-361.
47. Newcomer J.W., Farber N.B., Olney J.W. NMDA receptor function, memory, and brain aging. Dialogues Clin. Neurosci. 2000, 2:219-232.
48. O'Mahony S.M., Clarke G., Mckernan D.P., Bravo J.A., Dinan T.G., Cryan J.F. Differential visceral nociceptive, behavioural and neurochemical responses to an immune challenge in the stress-sensitive Wistar Kyoto rat strain. Behav. Brain Res. 2013, 253:310-317.
49. O'Connor R.M., Cryan J.F. The effects of mGlu(7) receptor modulation in behavioural models sensitive to antidepressant action in two mouse strains. Behav. Pharmacol. 2013, 24:105-113.
50. O'Connor R.M., Finger B.C., Flor P.J., Cryan J.F. Metabotropic glutamate receptor 7: at the interface of cognition and emotion. Eur. J. Pharmacol. 2010, 639:123-131.
51. O'Connor R.M., Thakker D.R., Schmutz M., van der Putten H., Hoyer D., Flor P.J., Cryan J.F. Adult siRNA-induced knockdown of mGlu7 receptors reduces anxiety in the mouse. Neuropharmacology 2013, 72:66-73.
52. O'Mahony C.M., Bravo J.A., Dinan T.G., Cryan J.F. Comparison of hippocampal metabotropic glutamate receptor 7 (mGlu7) mRNA levels in two animal models of depression. Neurosci. Lett. 2010, 482:137-141.
53. O'Mahony S.M., Bulmer D.C., Coelho A.M., Fitzgerald P., Bongiovanni C., Lee K., Winchester W., Dinan T.G., Cryan J.F. 5-HT(2B) receptors modulate visceral hypersensitivity in a stress-sensitive animal model of brain-gut axis dysfunction. Neurogastroenterol. Motil. 2010, 22:573-578. e124.
54. O'Mahony S.M., Tramullas M., Fitzgerald P., Cryan J.F. Rodent models of colorectal distension. Curr. Protoc. Neurosci. 2012, 40. (Chapter 9), Unit 9.
55. Olango W.M., Finn D.P. Neurobiology of stress-induced hyperalgesia. Curr. Top. Behav. Neurosci. 2014, 20:251-280.
56. Palazzo E., Marabese I., Luongo L., Boccella S., Bellini G., Giordano M.E., Rossi F., Scafuro M., Novellis V., Maione S. Effects of a metabotropic glutamate receptor subtype 7 negative allosteric modulator in the periaqueductal grey on pain responses and rostral ventromedial medulla cell activity in rat. Mol. Pain 2013, 9:44.
57. Prusator D.K., Greenwood-Van Meerveld B. Gender specific effects of neonatal limited nesting on viscerosomatic sensitivity and anxiety-like behavior in adult rats. Neurogastroenterol. Motil. 2015, 27:72-81.
58. Sanacora G., Treccani G., Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012, 62:63-77.
59. Slawinska A., WIeronska J.M., Stachowicz K., Palucha-Poniewiera A., Uberti M.A., Bacolod M.A., Doller D., Pilc A. Anxiolytic- but not antidepressant-like activity of Lu AF21934, a novel, selective positive allosteric modulator of the mGlu(4) receptor. Neuropharmacology 2013, 66:225-235.
60. Stachowicz K., Branski P., Klak K., van der Putten H., Cryan J.F., Flor P.J., Andrzej P. Selective activation of metabotropic G-protein-coupled glutamate 7 receptor elicits anxiolytic-like effects in mice by modulating GABAergic neurotransmission. Behav. Pharmacol. 2008, 19:597-603.
61. Stachowicz K., Chojnacka-Wojcik E., Klak K., Pilc A. Anxiolytic-like effect of group III mGlu receptor antagonist is serotonin-dependent. Neuropharmacology 2007, 52:306-312.
62. 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. The metabotropic glutamate receptor 7 allosteric modulator AMN082: a monoaminergic agent in disguise?. J.Pharmacol. Exp. Ther. 2011, 338:345-352.
63. Theodorou V. Susceptibility to stress-induced visceral sensitivity: a bad legacy for next generations. Neurogastroenterol. Motil. 2013, 25:927-930.
64. Varty G.B., Grilli M., Forlani A., Fredduzzi S., Grzelak M.E., Guthrie D.H., Hodgson R.A., Lu S.X., Nicolussi E., Pond A.J., Parker E.M., Hunter J.C., Higgins G.A., Reggiani A., Bertorelli R. The antinociceptive and anxiolytic-like effects of the metabotropic glutamate receptor 5 (mGluR5) antagonists, MPEP and MTEP, and the mGluR1 antagonist, LY456236, in rodents: a comparison of efficacy and side-effect profiles. Psychopharmacol. Berl. 2005, 179:207-217.
65. Walker D.L., Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol. Biochem. Behav. 2002, 71:379-392.
66. Wieronska J.M., Stachowicz K., Palucha-Poniewiera A., Acher F., Branski P., Pilc A. Metabotropic glutamate receptor 4 novel agonist LSP1-2111 with anxiolytic, but not antidepressant-like activity, mediated by serotonergic and GABAergic systems. Neuropharmacology 2010, 59:627-634.
67. Zhou L., Huang J., Gao J., Zhang G., Jiang J. NMDA and AMPA receptors in the anterior cingulate cortex mediates visceral pain in visceral hypersensitivity rats. Cell. Immunol. 2014, 287:86-90.