Group II metabotropic glutamate receptor type 2 allosteric potentiators prevent sodium lactate-induced panic-like response in panic-vulnerable rats

Journal of Psychopharmacology

Volumn 27, Issue 2, 2013, Pages 152-161

  Johnson, Philip L ^a   Fitz, Stephanie D ^a   Engleman, Eric A ^a   Svensson, Kjell A ^b   Schkeryantz, Jeffrey M ^b   Shekhar, Anantha ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ELI LILLY AND COMPANY   (United States)

Author keywords

alprazolam; anti panic drugs; anxiety; CBiPES; GABA; glutamate receptor; hypertension; hypothalamus; panic; pre clinical study; social interaction; sodium lactate; stress; tachycardia; THIIC

Indexed keywords

ALPRAZOLAM; BENZODIAZEPINE; ETHANESULFONAMIDE HYDROCHLORIDE; LACTATE SODIUM; METABOTROPIC RECEPTOR 2; N [4 [[3 HYDROXY 4 (2 METHYLPROPANOYL) 2 (TRIFLUOROMETHYL)PHENOXY]METHYL]]BENZYL 1 METHYL 1H IMIDAZOLE 4 CARBOXAMIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; FLIGHT; HYPERTENSION; LOCOMOTION; MALE; NONHUMAN; PANIC; PRIORITY JOURNAL; RAT; SOCIAL INTERACTION; TACHYCARDIA; TRANQUILIZING ACTIVITY;

ALPRAZOLAM; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; CARDIOVASCULAR SYSTEM; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; PANIC; PANIC DISORDER; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SODIUM LACTATE;

EID: 84872837494     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881112454230     Document Type: Article

References (69)

1. Abshire VM, Hankins KD, Roehr KE, et al. Injection of L-allylglycine into the posterior hypothalamus in rats causes decreases in local GABA which correlate with increases in heart rate. Neuropharmacol. 1988 ; 27: 1171-1177
2. Baldwin DS, Anderson IM, Nutt DJ, et al. Evidence-based guidelines for the pharmacological treatment of anxiety disorders: Recommendations from the British Association for Psychopharmacology. J Psychopharmacol. 2005 ; 19: 567-596
3. Bandelow B, Zohar J, Hollander E, et al. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for the pharmacological treatment of anxiety, obsessive-compulsive and post-traumatic stress disorders - first revision. World J Biol Psychiatry. 2008 ; 9: 248-312
4. Bard P, Mountcastle VB. Some forebrain mechanisms involved in the expression of rage with special reference to suppression of angry behavior. Res Publ Assoc Res Nerv Ment Dis. 1948 ; 27: 362-404
5. Bernardis LL, Bellinger LL. Proc Soc Exp Biol Med. 1998 1998 ; 218: 284-306
6. Boshuisen ML, Ter Horst GJ, Paans AM, et al. rCBF differences between panic disorder patients and control subjects during anticipatory anxiety and rest. Biol Psy. 2002 ; 52: 126-135
7. Bourdelais A, Kalivas PW. High sensitivity HPLC assay for GABA in brain dialysis studies. J Neurosci Meth. 1991 ; 39: 115-121
8. Chamberlin NL, Saper CB. Topographic organization of respiratory responses to glutamate microstimulation of the parabrachial nucleus in the rat. J Neurosci. 1994 ; 14: 6500-6510
9. Chen T, Hui R, Dong YX, et al. Endomorphin 1- and endomorphin 2-like immunoreactive neurons in the hypothalamus send axons to the parabrachial nucleus in the rat. Neurosci Lett. 2004 ; 357: 139-142
10. Chou TC, Scammell TE, Gooley JJ, et al. Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. J Neurosci. 2003 ; 23: 10691-10702
11. Cloos JM, Ferreira V. Current use of benzodiazepines in anxiety disorders. Curr Opin Psych. 2009 ; 22: 90-95
12. DiMicco JA, Samuels BC, Zaretskaia MV, et al. The dorsomedial hypothalamus and the response to stress: Part renaissance, part revolution. Pharmacol Biochem Behav. 2002 ; 71: 469-480
13. Donzanti BA, Yamamoto BK. An improved and rapid HPLC-EC method for the isocratic separation of amino acid neurotransmitters from brain tissue and microdialysis perfusates. Life Sci. 1988 ; 43: 913-922
14. Feldblum S, Erlander MG, Tobin AJ. Different distributions of GAD65 and GAD67 mRNAs suggest that the two glutamate decarboxylases play distinctive functional roles. J Neurosci Res. 1993 ; 34: 689-706
15. File SE. The use of social interaction as a method for detecting anxiolytic activity of chlordiazepoxide-like drugs. J Neurosci Meth. 1980 ; 2: 219-238
16. Fontes MA, Tagawa T, Polson JW, et al. Descending pathways mediating cardiovascular response from dorsomedial hypothalamic nucleus. Am J Physiol Heart Circ Physiol. 2001 ; 280: H2891 - H2901
17. Goddard AW, Mason GF, Almai A, et al. Reductions in occipital cortex GABA levels in panic disorder detected with 1h-magnetic resonance spectroscopy. Arch Gen Psych. 2001 ; 58: 556-561
18. Gorman JM. New molecular targets for antianxiety interventions. J Clin Psych. 2003 ; 64: 28-35
19. Gorman JM, Kent JM, Sullivan GM, et al. Neuroanatomical hypothesis of panic disorder, revised. Am J Psych. 2000 ; 157: 493-505
20. Gorman JM, Papp LA, Coplan JD, et al. Anxiogenic effects of CO2 and hyperventilation in patients with panic disorder. Am J Psych. 1994 ; 151: 547-553
21. Grillon C, Cordova J, Levine LR, et al. Anxiolytic effects of a novel group II metabotropic glutamate receptor agonis (LY354740) in the fear-potentiated startle paradigm in humans. Psychopharmacology (Berl). 2003 ; 168: 446-54
22. Grob M, Trottier JF, Drolet G, et al. Characterization of the neurochemical content of neuronal populations of the lamina terminalis activated by acute hydromineral challenge. Neurosci. 2003 ; 122: 247-257
23. Gu G, Lorrain DS, Wei H, et al. Distribution of metabotropic glutamate 2 and 3 receptors in the rat forebrain: Implication in emotional responses and central disinhibition. Brain Res. 2008 ; 1197: 47-62
24. Helton DR, Tizzano JP, Monn JA, et al. Anxiolytic and side-effect profile of LY354740: A potent, highly selective, orally active agonist for group II metabotropic glutamate receptors. J Pharmacol Exp Ther. 1998 ; 284: 651-660
25. Hirschfeld RMA. Panic disorder: Diagnosis, epidemiology, and clinical course. J Clin Psych. 1996 ; 57: 3-8
26. Jardim MC, Guimaraes FS. Role of glutamate ionotropic receptors in the dorsomedial hypothalamic nucleus on anxiety and locomotor behavior. Pharmacol Biochem Behav. 2004 ; 79: 541-546
27. Johnson MP, Barda D, Britton TC, et al. Metabotropic glutamate 2 receptor potentiators: Receptor modulation, frequency-dependent synaptic activity, and efficacy in preclinical anxiety and psychosis model(s). Psychopharmacol. 2005 ; 179: 271-283
28. Johnson PL, Shekhar A. Panic-prone state induced in rats with GABA dysfunction in the dorsomedial hypothalamus is mediated by NMDA receptors. J Neurosci. 2006 ; 26: 7093-7104
29. Johnson PL, Truitt WA, Fitz SD, et al. Neural pathways underlying lactate-induced panic. Neuropsychopharmacol. 2008 ; 33: 2093-2107
30. Johnson PL, Truitt W, Fitz SD, et al. A key role for orexin in panic anxiety. Nat Med. 2010 ; 16: 111-115
31. Katon WJ, Roy-Byrne P, Russo J, et al. Cost-effectiveness and cost offset of a collaborative care intervention for primary care patients with panic disorder. Arch Gen Psych. 2002 ; 59: 1098-1104
32. Kessler RC, McGonagle KA, Zhao S, et al. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Arch Gen Psych. 1994 ; 51: 8-19
33. Klein DF. False suffocation alarms, spontaneous panics, and related conditions. Arch Gen Psych. 1993 ; 50: 306-317
34. Liebowitz MR, Gorman J, Fyer A, et al. Biological accompaniments of lactate-induced panic. Psychopharmacol Bull. 1984 ; 20: 43-44
35. Molosh AI, Johnson PL, Fitz SD, et al. Changes in central sodium and not osmolarity or lactate induce panic-like responses in a model of panic disorder. Neuropsychopharmacol. 2010 ; 35: 1333-1347
36. Monn JA, Valli MJ, Massey SM, et al. Design, synthesis, and pharmacological characterization of (+)-2-aminobicyclo[3.1.0]hexane-2,6- dicarboxylic acid (LY354740): A potent, selective, and orally active group 2 metabotropic glutamate receptor agonist possessing anticonvulsant and anxiolytic properties. J Med Chem. 1997 ; 40: 528-537
37. Neki A, Ohishi H, Kaneko T, et al. Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: An immunohistochemical study with a monoclonal antibody. Neurosci Lett. 1996 ; 202: 197-200
38. Nicoletti F, Bockaert J, Collingridge GL, et al. Metabotropic glutamate receptors: From the workbench to the bedside. Neuropharmacology. 2010 ; 60: 1017-1041
39. Nutt DJ, Ballenger JC, Sheehan D, et al. Generalized anxiety disorder: Comorbidity, comparative biology and treatment. Int J Neuropsychopharmacol. 2002 ; 5: 315-325
40. Ohishi H, Shigemoto R, Nakanishi S, et al. Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neurosci. 1993a ; 53: 1009-1018
41. Ohishi H, Shigemoto R, Nakanishi S, et al J Comp Neurol. in the rat brain: An in situ hybridization study ; 1993b: 252-266.
42. Parsons CG, Danysz W, Quack G Neuropharmacol. receptor antagonist: A review of preclinical data ; 1999: 735-767.
43. Petralia RS, Wang YX, Niedzielski AS, et al. The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neurosci. 1996 ; 71: 949-976
44. Pin JP, Duvoisin R. The metabotropic glutamate receptors: Structure and functions. Neuropharmacol. 1995 ; 34: 1-26
45. Plaznik A, Palejko W, Nazar M, et al. Effects of antagonists at the NMDA receptor complex in two models of anxiety. Eur Neuropsychopharmacol. 1994 ; 4: 503-512
46. Pohl R, Balon R, Bechou R, et al. Lactate-induced anxiety after imapramine and diazepam treatment. Anxiety. 1994 ; 1: 54-63
47. Price LH, Goddard AW, Barr LC, et al Psychopharmacology: The fourth generation of progression. Bloom FE Kupfer DJ, ed. New York: Raven ; 1995: 1311-1323.
48. Richard D, Bourque CW. Synaptic activation of rat supraoptic neurons by osmotic stimulation of the organum vasculosum lamina terminalis. Neuroendocrinol. 1992 ; 55: 609-611
49. Risold PY, Swanson LW. Connections of the rat lateral septal complex. Brain Res Rev. 1997 ; 24: 115-195
50. Sajdyk TJ, Shekhar A. Sodium lactate elicits anxiety in rats after repeated GABA receptor blockade in the basolateral amygdala. Eur J Pharmacol. 2000 ; 394: 265-273
51. Samuels BC, Zaretsky DV, DiMicco JA. Dorsomedial hypothalamic sites where disinhibition evokes tachycardia correlate with location of raphe-projecting neurons. Am J Physiol Regul Integr Comp Physiol. 2004 ; 287: R472 - R478
52. Sanders SK, Shekhar A. Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav. 1995 ; 52: 701-706
53. Schenberg LC, Bittencourt AS, Sudre EC, et al. Modeling panic attacks. Neurosci Biobehav Rev. 2001 ; 25: 647-659
54. Schimitel FG, De Almeida GM, Pitol DN, et al. Evidence of a suffocation alarm system within the periaqueductal gray matter of the rat. Neurosci. 2012 ; 200: 59-73
55. Schoepp DD, Wright RA, Levine LR, et al. LY354740, an mGlu2/3 receptor agonist as a novel approach to treat anxiety/stress. Stress. 2003 ; 6: 189-197
56. Shekhar A, Johnson PL, Sajdyk TJ, et al. Angiotensin-II is a putative neurotransmitter in lactate-induced panic-like responses in rats with disruption of GABAergic inhibition in the dorsomedial hypothalamus. J Neurosci. 2006 ; 26: 9205-9215
57. Shekhar A, Katner JS. Dorsomedial hypothalamic GABA regulates anxiety in the social interaction test. Pharmacol Biochem Behav. 1995 ; 50: 253-258
58. Shekhar A, Keim SR. The circumventricular organs form a potential neural pathway for lactate sensitivity: Implications for panic disorder. J Neurosci. 1997 ; 17: 9726-9735
59. Shekhar A, Keim SR. LY354740, a potent group II metabotropic glutamate receptor agonist prevents lactate-induced panic-like response in panic-prone rats. Neuropharmacol. 2000 ; 39: 1139-1146
60. Shekhar A, Keim SR, Simon JR, et al. Dorsomedial hypothalamic GABA dysfunction produces physiological arousal following sodium lactate infusions. Pharmacol Biochem Behav. 1996 ; 55: 249-256
61. Shekhar A, Sajdyk TJ, Gehlert DR, et al. The amygdala, panic disorder, and cardiovascular responses. Ann NY Acad Sci. 2003 ; 985: 308-325
62. Shigemoto R, Kinoshita A, Wada E, et al. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci. 1997 ; 17: 7503-7522
63. Swanson CJ, Bures M, Johnson MP, et al. Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nature Rev. 2005 ; 4: 131-144
64. Swanson CJ, Schoepp DD. The group II metabotropic glutamate receptor agonist (-)-2-oxa-4-aminobicyclo[3.1.0.]hexane-4,6-dicarboxylate (LY379268) and clozapine reverse phencyclidine-induced behaviors in monoamine-depleted rats. J Pharmacol Exp Ther. 2002 ; 303: 919-927
65. Thompson RH, Canteras NS, Swanson LW. Organization of projections from the dorsomedial nucleus of the hypothalamus: A PHA-L study in the rat. J Comp Neurol. 1996 ; 376: 143-173
66. Thompson RH, Swanson LW. Organization of inputs to the dorsomedial nucleus of the hypothalamus: A reexamination with Fluorogold and PHAL in the rat. Brain Res Rev. 1998 ; 27: 89-118
67. Walker DL, Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol Biochem Behav. 2002 ; 71: 379-392
68. Weissman MM, Merikangas KR. The epidemiology of anxiety and panic disorders: An update. J Clin Psych. 1986 ; 47: 11-17
69. Xie Z, Commissaris RL. Anxiolytic-like effects of the noncompetitive NMDA antagonist MK 801. Pharmacol Biochem Behav. 1992 ; 43: 471-477