Prodynorphin gene deletion increased anxiety-like behaviours, impaired the anxiolytic effect of bromazepam and altered GABAA receptor subunits gene expression in the amygdala

Journal of Psychopharmacology

Volumn 25, Issue 1, 2011, Pages 87-95

  Femenía, Teresa ^a   Pérez Rial, Sandra ^a,b   Urigüen, Leyre ^a,c   Manzanares, Jorge ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^c Hospital UniversitarioFundación Jiménez Díaz   (Spain)

Author keywords

Anxiety; benzodiazepine; GABAA receptor; prodynorphin gene

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; BROMAZEPAM; CORTICOTROPIN RELEASING FACTOR; PRODYNORPHIN; PROOPIOMELANOCORTIN;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARCUATE NUCLEUS; ARTICLE; DRUG EFFICACY; EMOTION; GENE DELETION; GENE EXPRESSION; GENOTYPE; HYPOTHALAMUS; MALE; MOTOR ACTIVITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SOCIAL INTERACTION; TRANQUILIZING ACTIVITY;

AMYGDALA; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; ANXIETY DISORDERS; BROMAZEPAM; ENKEPHALINS; EXPLORATORY BEHAVIOR; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; PROTEIN PRECURSORS; RECEPTORS, GABA-A; STRESS, PHYSIOLOGICAL;

EID: 78650602366     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881110367724     Document Type: Article

References (76)

1. Akil H., Owens C., Gutstein H., Taylor L., Curran E. and Watson S. (1998) Endogenous opioids: overview and current issues. Drug Alcohol Depend 51: 127-140.
2. Akil H., Watson SJ, Young E., Lewis ME, Khachaturian H. and Walker JM (1984) Endogenous opioids: biology and function. Ann Rev Neurosci 7: 223-255.
3. Bailey SJ and Toth M. (2004) Variability in the benzodiazepine response of serotonin 5-HT1A receptor null mice displaying anxiety-like phenotype: evidence for genetic modifiers in the 5-HT-mediated regulation of GABA(A) receptors. J Neurosci 24: 6343-6351.
4. Baubet V., Fevre-Montange M., Gay N., Debilly G., Bobillier P. and Cespuglio R. (1994) Effects of an acute immobilization stress upon proopiomelanocortin (POMC) mRNA levels in the mediobasal hypothalamus: a quantitative in situ hybridization study. Brain Res Mol Brain Res 26: 163-168.
5. Bilkei-Gorzo A., Racz I., Michel K., et al. (2008) Control of hormonal stress reactivity by the endogenous opioid system. Psychoneuroendocrinology 33: 425-436.
6. Bourin M. and Hascoet M. (2003) The mouse light/dark box test. Eur J Pharmacol 463: 55-65.
7. Bremner JD, Innis RB, Southwick SM, Staib L., Zoghbi S. and Charney DS (2000) Decreased benzodiazepine receptor binding in prefrontal cortex in combat-related posttraumatic stress disorder. Am J Psychiatry 157: 1120-1126.
8. Calogero AE (1995) Neurotransmitter regulation of the hypothalamic corticotropin-releasing hormone neuron. Ann N Y Acad Sci 771: 31-40.
9. Commissaris RL, Harrington GM and Altman HJ (1990) Benzodiazepine anti-conflict effects in Maudsley reactive (MR/ Har) and non-reactive (MNRA/Har) rats. Psychopharmacology 100: 287-292.
10. Corchero J., Romero J., Berrendero F., et al. (1999) Time-dependent differences of repeated administration with Delta9-tetrahydrocannabinol in proenkephalin and cannabinoid receptor gene expression and G-protein activation by mu-opioid and CB1-cannabinoid receptors in the caudate-putamen. Brain Res Mol Brain Res 67: 148-157.
11. Cowley DS, Ha EH and Roy-Byrne PP (1997) Determinants of pharmacologic treatment failure in panic disorder. J Clin Psychiatry 58: 555-561 ; quiz 562-553.
12. Crawley J. and Goodwin FK (1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13: 167-170.
13. Crawley JN (1996) Unusual behavioral phenotypes of inbred mouse strains. Trends Neurosci 19: 181-182 ; discussion 188-189.
14. Crawley JN, Belknap JK, Collins A., et al. (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132: 107-124.
15. Crestani F., Lorez M., Baer K., et al. (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2: 833-839.
16. Da Settimo F., Taliani S., Trincavelli ML, Montali M. and Martini C. (2007) GABA A/Bz receptor subtypes as targets for selective drugs. Curr Med Chem 14: 2680-2701.
17. Dickenson AH (1991) Mechanisms of the analgesic actions of opiates and opioids. Br Med Bull 47: 690-702.
18. Domino EF, French J., Pohorecki R., Galus CF and Pandit SK (1989) Further observations on the effects of subhypnotic doses of midazolam in normal volunteers. Psychopharmacol Bull 25: 460-465.
19. Eipper BA and Mains RE (1980) Structure and biosynthesis of proadrenocorticotropin/endorphin and related peptides. Endocr Rev 1: 1-27.
20. Emeson RB and Eipper BA (1986) Characterization of pro-ACTH/ endorphin-derived peptides in rat hypothalamus. J Neurosci 6: 837-849.
21. File SE and Hyde JR (1978) Can social interaction be used to measure anxiety ? Br J Pharmacol 62: 19-24.
22. Gerlai R. (1996) Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype ? Trends Neurosci 19: 177-181.
23. Gonzalez LE and File SE (1997) A five minute experience in the elevated plus-maze alters the state of the benzodiazepine receptor in the dorsal raphe nucleus. J Neurosci 17: 1505-1511.
24. Gramsch C., Kleber G., Hollt V., Pasi A., Mehraein P. and Herz A. (1980) Pro-opiocortin fragments in human and rat brain: beta-endorphin and alpha-MSH are the predominant peptides. Brain Res 192: 109-119.
25. Gunther U., Benson J., Benke D., et al. (1995) Benzodiazepine-insensitive mice generated by targeted disruption of the gamma 2 subunit gene of gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 92: 7749-7753.
26. Gupta A., Lind S., Eklund A. and Lennmarken C. (1997) The effects of midazolam and flumazenil on psychomotor function. J Clin Anesth 9: 21-25.
27. Guy AP and Gardner CR (1985) Pharmacological characterisation of a modified social interaction model of anxiety in the rat. Neuropsychobiology 13: 194-200.
28. Hamon A., Morel A., Hue B., Verleye M. and Gillardin JM (2003) The modulatory effects of the anxiolytic etifoxine on GABA(A) receptors are mediated by the beta subunit. Neuropharmacology 45: 293-303.
29. Handley SL and Mithani S. (1984) Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of 'fear'-motivated behaviour. Naunyn Schmiedebergs Arch Pharmacol 327: 1-5.
30. Hascoet M. and Bourin M. (1998) A new approach to the light/dark test procedure in mice. Pharmacol Biochem Behav 60: 645-653.
31. Hollt V., Haarmann I., Bovermann K., Jerlicz M. and Herz A. (1980) Dynorphin-related immunoreactive peptides in rat brain and pituitary. Neurosci Lett 18: 149-153.
32. Hollt V., Przewlocki R., Haarmann I., et al. (1986) Stress-induced alterations in the levels of messenger RNA coding for proopiomelanocortin and prolactin in rat pituitary. Neuroendocrinology 43: 277-282.
33. Jhamandas KH (1984) Opioid-neurotransmitter interactions: significance in analgesia, tolerance and dependence. Prog Neuropsychopharmacol Biol Psychiatry 8: 565-570.
34. Kaschka W., Feistel H. and Ebert D. (1995) Reduced benzodiazepine receptor binding in panic disorders measured by iomazenil SPECT. J Psychiatr Res 29: 427-434.
35. Knoll AT, Meloni EG, Thomas JB, Carroll FI and Carlezon WA Jr (2007) Anxiolytic-like effects of kappa-opioid receptor antagonists in models of unlearned and learned fear in rats. J Pharmacol Exp Ther 323: 838-845.
36. Kudryavtseva NN, Gerrits MA, Avgustinovich DF, Tenditnik MV and Van Ree JM (2004) Modulation of anxiety-related behaviors by mu- and kappa-opioid receptor agonists depends on the social status of mice. Peptides 25: 1355-1363.
37. Kuzmin A., Madjid N., Terenius L., Ogren SO and Bakalkin G. (2006) Big dynorphin, a prodynorphin-derived peptide produces NMDA receptor-mediated effects on memory, anxiolytic-like and locomotor behavior in mice. Neuropsychopharmacology 31: 1928-1937.
38. Land BB, Bruchas MR, Lemos JC, Xu M., Melief J. and Chavkin C. (2008) The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 28: 407-414.
39. Larsen PJ and Mau SE (1994) Effect of acute stress on the expression of hypothalamic messenger ribonucleic acids encoding the endogenous opioid precursors preproenkephalin A and proopiomelanocortin. Peptides 15: 783-790.
40. Lin S., Boey D., Lee N., Schwarzer C., Sainsbury A. and Herzog H. (2006) Distribution of prodynorphin mRNA and its interaction with the NPY system in the mouse brain. Neuropeptides 40: 115-123.
41. Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 92: 180-185.
42. Loacker S., Sayyah M., Wittmann W., Herzog H. and Schwarzer C. (2007) Endogenous dynorphin in epileptogenesis and epilepsy: anticonvulsant net effect via kappa opioid receptors. Brain 130: 1017-1028.
43. Low K., Crestani F., Keist R., et al. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290: 131-134.
44. Mains RE and Eipper BA (1980) Biosynthetic studies on ACTH, beta-endorphin, and alpha-melanotropin in the rat. Ann N Y Acad Sci 343: 94-110.
45. Malizia AL, Cunningham VJ, Bell CJ, Liddle PF, Jones T. and Nutt DJ (1998) Decreased brain GABA(A)-benzodiazepine receptor binding in panic disorder: preliminary results from a quantitative PET study. Arch Gen Psychiatry 55: 715-720.
46. Mansour A., Khachaturian H., Lewis ME, Akil H. and Watson SJ (1988) Anatomy of CNS opioid receptors. Trends Neurosci 11: 308-314.
47. Marchant NJ, Densmore VS and Osborne PB (2007) Coexpression of prodynorphin and corticotrophin-releasing hormone in the rat central amygdala: evidence of two distinct endogenous opioid systems in the lateral division. J Comp Neurol 504: 702-715.
48. McKernan M., Rosahl TW, Reynolds DS, et al. (2000) Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABA(A) receptor alpha1 subtype. Nat Neurosci 3: 587-592.
49. McLaughlin JP, Land BB, Li S., Pintar JE and Chavkin C. (2006 a) Prior activation of kappa opioid receptors by U50,488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology 31: 787-794.
50. McLaughlin JP, Li S., Valdez J., Chavkin TA and Chavkin C. (2006 b) Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology 31: 1241-1248.
51. McLaughlin JP, Marton-Popovici M. and Chavkin C. (2003) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23: 5674-5683.
52. Nabeshima T., Katoh A., Wada M. and Kameyama T. (1992) Stress-induced changes in brain Met-enkephalin, Leu-enkephalin and dynorphin concentrations. Life Sci 51: 211-217.
53. Nutt DJ and Glue P. (1989) Clinical pharmacology of anxiolytics and antidepressants: a psychopharmacological perspective. Pharmacol Ther 44: 309-334.
54. Palkovits M. (1983) Punch sampling biopsy technique. Methods Enzymol 103: 368-376.
55. Paxinos G. and Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. New York: Academic Press. Harcourt Science and Technology Company.
56. Pellow S., Chopin P., File SE and Briley M. (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14: 149-167.
57. Pritchett DB, Sontheimer H., Shivers BD, et al. (1989) Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338: 582-585.
58. Rainnie DG, Asprodini EK and Shinnick-Gallagher P. (1992) Kindling-induced long-lasting changes in synaptic transmission in the basolateral amygdala. J Neurophysiol 67: 443-454.
59. Roth KA, Weber E., Barchas JD, Chang D. and Chang JK (1983) Immunoreactive dynorphin-(1-8) and corticotropin-releasing factor in subpopulation of hypothalamic neurons. Science 219: 189-191.
60. Rudolph U., Crestani F., Benke D., et al. (1999) Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 401: 796-800.
61. Russell IJ (1998) Advances in fibromyalgia: possible role for central neurochemicals. Am J Med Sci 315: 377-384.
62. Schlegel S., Steinert H., Bockisch A., Hahn K., Schloesser R. and Benkert O. (1994) Decreased benzodiazepine receptor binding in panic disorder measured by IOMAZENIL-SPECT. A preliminary report. Eur Arch Psychiatry Clin Neurosci 244: 49-51.
63. Sharifi N., Diehl N., Yaswen L., Brennan MB and Hochgeschwender U. (2001) Generation of dynorphin knockout mice. Brain Res Mol Brain Res 86: 70-75.
64. Sibille E., Pavlides C., Benke D. and Toth M. (2000) Genetic inactivation of the Serotonin(1A) receptor in mice results in downregulation of major GABA(A) receptor alpha subunits, reduction of GABA(A) receptor binding, and benzodiazepine-resistant anxiety. J Neurosci 20: 2758-2765.
65. Sigel E., Baur R., Trube G., Mohler H. and Malherbe P. (1990) The effect of subunit composition of rat brain GABAA receptors on channel function. Neuron 5: 703-711.
66. Simonato M. and Romualdi P. (1996) Dynorphin and epilepsy. Prog Neurobiol 50: 557-583.
67. Tiihonen J., Kuikka J., Rasanen P., et al. (1997) Cerebral benzodiazepine receptor binding and distribution in generalized anxiety disorder: a fractal analysis. Mol Psychiatry 2: 463-471.
68. Tsagarakis S., Rees LH, Besser GM and Grossman A. (1990) Gamma-aminobutyric acid modulation of corticotrophin-releasing factor-41 secretion from the rat hypothalamus in vitro. J Neuroendocrinol 2: 221-224. (Pubitemid 20282755)
69. Tsuda M., Suzuki T., Misawa M. and Nagase H. (1996) Involvement of the opioid system in the anxiolytic effect of diazepam in mice. Eur J Pharmacol 307: 7-14.
70. Urigüen L., Pérez-Rial S., Ledent C., Palomo T. and Manzanares J. (2004) Impaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors. Neuropharmacology 46: 966-973.
71. Vaccarino AL, Olson GA, Olson RD and Kastin AJ (1999) Endogenous opiates: 1998. Peptides 20: 1527-1574.
72. Wall PM and Messier C. (2002) Infralimbic kappa opioid and muscarinic M1 receptor interactions in the concurrent modulation of anxiety and memory. Psychopharmacology (Berl) 160: 233-244.
73. Warnault V., Houchi H., Barbier E., et al. (2007) The lack of CB1 receptors prevents neuroadapatations of both NMDA and GABA(A) receptors after chronic ethanol exposure. J Neurochem 102: 741-752.
74. Wittmann W., Schunk E., Rosskothen I., et al. (2009) Prodynorphin-derived peptides are critical modulators of anxiety and regulate neurochemistry and corticosterone. Neuropsychopharmacology 34: 775-785.
75. Young WS III, Bonner TI and Brann MR (1986) Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain. Proc Natl Acad Sci U S A 83: 9827-9831.
76. Zimmer A., Valjent E., Konig M., et al. (2001) Absence of delta -9-tetrahydrocannabinol dysphoric effects in dynorphin-deficient mice. J Neurosci 21: 9499-9505.