Prodynorphin-derived peptides are critical modulators of anxiety and regulate neurochemistry and corticosterone

Neuropsychopharmacology

Volumn 34, Issue 3, 2009, Pages 775-785

  Wittmann, Walter ^a,c   Schunk, Eduard ^a   Rosskothen, Iris ^a   Gaburro, Stefano ^a   Singewald, Nicolas ^a   Herzog, Herbert ^b   Schwarzer, Christoph ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

opioid receptor; Amygdala; Hypothalamic pituitary adrenal axis; Paraventricular; Prodynorphin knockout; Stress

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE METHANESULFONATE; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; KAPPA OPIATE RECEPTOR; MESSENGER RNA; NORBINALTORPHIMINE; PEPTIDE DERIVATIVE; PRODYNORPHIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; COPING BEHAVIOR; CORTICOSTERONE BLOOD LEVEL; EXPLORATORY BEHAVIOR; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MAZE TEST; MOUSE; NEUROCHEMISTRY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; STRESS; THALAMUS MIDLINE NUCLEUS;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; AMYGDALA; ANIMALS; ANXIETY; BRAIN STEM; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DYNORPHINS; ENKEPHALINS; EXPLORATORY BEHAVIOR; FEMALE; HYPOTHALAMUS; MALE; MAZE LEARNING; MESENCEPHALON; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NALTREXONE; NEUROPEPTIDE Y; NEUROPEPTIDES; PROTEIN PRECURSORS; RAPHE NUCLEI; RECEPTORS, OPIOID, KAPPA; STRESS, PSYCHOLOGICAL;

EID: 58149470808     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2008.142     Document Type: Article

References (50)

1. Aguiar MS, Brandao ML (1996). Effects of microinjections of the neuropeptide substance P in the dorsal periaqueductal gray on the behaviour of rats in the plus-maze test. Physiol Behav 60: 1183-1186.
2. Bachli H, Steiner MA, Habersetzer U, Wotjak CT (2008). Increased water temperature renders single-housed C57BL/6J mice susceptible to antidepressant treatment in the forced swim test. Behav Brain Res 187: 67-71.
3. Bale TL, Contarino A, Smith GW, Chan R, Gold LH, Sawchenko PE et al (2000). Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat Genet 24: 410-414.
4. Bilkei-Gorzo A, Racz I, Michel K, Mauer D, Zimmer A, Klingmuller D et al (2008). Control of hormonal stress reactivity by the endogenous opioid system. Psychoneuroendocrinology 33: 425-436.
5. Brunello N, Blier P, Judd LL, Mendlewicz J, Nelson CJ, Souery D et al (2003). Noradrenaline in mood and anxiety disorders: basic and clinical studies. Int Clin Psychopharmacol 18: 191-202.
6. Coste SC, Kesterson RA, Heldwein KA, Stevens SL, Heard AD, Hollis JH et al (2000). Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat Genet 24: 403-409.
7. Crawley JN (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.
8. Ebner K, Rupniak NM, Saria A, Singewald N (2004). Substance P in the medial amygdala: emotional stress-sensitive release and modulation of anxiety-related behavior in rats. Proc Natl Acad Sci USA 101: 4280-4285.
9. Ebner K, Singewald N (2006). The role of substance P in stress and anxiety responses. Amino Acids 31: 251-272.
10. Engelhardt G, Homma D, Schlegel K, Schnitzler C, Utzmann R (1996). General pharmacology of meloxicam - Part I: effects on CNS, gastric emptying, intestinal transport, water, electrolyte and creatinine excretion. Gen Pharmacol 27: 673-677.
11. Gavioli EC, Canteras NS, De Lima TC (1999). Anxiogenic-like effect induced by substance P injected into the lateral septal nucleus. Neuroreport 10: 3399-3403.
12. Graeff FG (2002). On serotonin and experimental anxiety. Psychopharmacology (Berl) 163: 467-476.
13. Hamke M, Herpfer I, Lieb K, Wandelt C, Fiebich BL (2006). Substance P induces expression of the corticotropin-releasing factor receptor 1 by activation of the neurokinin-1 receptor. Brain Res 1102: 135-144.
14. Heilig M, Koob GF, Ekman R, Britton KT (1994). Corticotropin-releasing factor and neuropeptide Y: role in emotional integration. Trends Neurosci 17: 80-85.
15. Holm S (1979). A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70.
16. Jewett DC, Grace MK, Jones RM, Billington CJ, Portoghese PS, Levine AS (2001). The kappa-opioid antagonist GNTI reduces U50,488-, DAMGO-, and deprivation-induced feeding, but not butorphanol- and neuropeptide Y-induced feeding in rats. Brain Res 909: 75-80.
17. Jones RM, Portoghese PS (2000). 5′-Guanidinonaltrindole, a highly selective and potent kappa-opioid receptor antagonist. Eur J Pharmacol 396: 49-52.
18. Karl T, Pabst R, von Horsten S (2003). Behavioral phenotyping of mice in pharmacological and toxicological research. Exp Toxicol Pathol 55: 69-83.
19. Karlsson RM, Choe JS, Cameron HA, Thorsell A, Crawley JN, Holmes A et al (2008). The neuropeptide Y Y1 receptor subtype is necessary for the anxiolytic-like effects of neuropeptide Y, but not the antidepressant-like effects of fluoxetine, in mice. Psychopharmacology (Berl) 195: 547-557.
20. Kask A, Harro J, von Horsten S, Redrobe JP, Dumont Y, Quirion R (2002). The neurocircuitry and receptor subtypes mediating anxiolytic-like effects of neuropeptide Y. Neurosci Biobehav Rev 26: 259-283.
21. Kask A, Schioth HB, Mutulis F, Wikberg JE, Rago L (2000). Anorexigenic cocaine- and amphetamine-regulated transcript peptide intensifies fear reactions in rats. Brain Res 857: 283-285.
22. Kishimoto T, Radulovic J, Radulovic M, Lin CR, Schrick C, Hooshmand F et al (2000). Deletion of crhr2 reveals an anxiolytic role for corticotropin-releasing hormone receptor-2. Nat Genet 24: 415-419.
23. Knoll AT, Meloni EG, Thomas JB, Carroll FI, Carlezon WA (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.
24. Kudryavtseva NN, Gerrits MA, Avgustinovich DF, Tenditnik MV, 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.
25. Kuzmin A, Madjid N, Terenius L, Ogren SO, 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.
26. Land BB, Bruchas MR, Lemos JC, Xu M, Melief EJ, Chavkin C (2008). The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 28: 407-414.
27. Lin S, Boey D, Lee N, Schwarzer C, Sainsbury A, Herzog H (2006). Distribution of prodynorphin mRNA and its interaction with the NPY system in the mouse brain. Neuropeptides 40: 115-123.
28. Loacker S, Sayyah M, Wittmann W, Herzog H, Schwarzer C (2007). Endogenous dynorphin in epileptogenesis and epilepsy: anticonvulsant net effect via kappa opioid receptors. Brain 130: 1017-1028.
29. Marchant NJ, Densmore VS, 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.
30. McLaughlin JP, Marton-Popovici M, Chavkin C (2003). Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23: 5674-5683.
31. Narita M, Kaneko C, Miyoshi K, Nagumo Y, Kuzumaki N, Nakajima M et al (2006). Chronic pain induces anxiety with concomitant changes in opioidergic function in the amygdala. Neuropsychopharmacology 31: 739-750.
32. Olivier B, Zethof T, Pattij T, van Boogaert M, van Oorschot R, Leahy C et al (2003). Stress-induced hyperthermia and anxiety: pharmacological validation. Eur J Pharmacol 463: 117-132.
33. Sainsbury A, Schwarzer C, Couzens M, Herzog H (2002). Y2 receptor deletion attenuates the type 2 diabetic syndrome of ob/ob mice. Diabetes 51: 3420-3427.
34. Sajdyk TJ, Shekhar A, Gehlert DR (2004). Interactions between NPY and CRF in the amygdala to regulate emotionality. Neuropeptides 38: 225-234.
35. Schoffelmeer AN, Hogenboom F, Mulder AH (1997). Kappa1- and kappa2-opioid receptors mediating presynaptic inhibition of dopamine and acetylcholine release in rat neostriatum. Br J Pharmacol 122: 520-524.
36. Schwarzer C, Kofler N, Sperk G (1998). Up-regulation of neuropeptide Y-Y2 receptors in an animal model of temporal lobe epilepsy. Mol Pharmacol 53: 6-13.
37. Sharifi N, Diehl N, Yaswen L, Brennan MB, Hochgeschwender U (2001). Generation of dynorphin knockout mice. Brain Res Mol Brain Res 86: 70-75.
38. Shepard JD, Barron KW, Myers DA (2000). Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Res 861: 288-295.
39. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH et al (1998). Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20: 1093-1102.
40. Solbrig MV, Adrian R, Baratta J, Lauterborn JC, Koob GF (2006). Kappa opioid control of seizures produced by a virus in an animal model. Brain 129: 642-654.
41. Stanek LM (2006). Cocaine- and amphetamine related transcript (CART) and anxiety. Peptides 27: 2005-2011.
42. Stenzel-Poore MP, Duncan JE, Rittenberg MB, Bakke AC, Heinrichs SC (1996). CRH overproduction in transgenic mice: behavioral and immune system modulation. Ann NY Acad Sci 780: 36-48.
43. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK et al (1998). Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 19: 162-166.
44. Tsuda M, Suzuki T, Misawa M, Nagase H (1996). Involvement of the opioid system in the anxiolytic effect of diazepam in mice. Eur J Pharmacol 307: 7-14.
45. Vlachakis ND, De Guia D, Mendlowitz M, Antram S, Wolf RL (1974). Hypertension and anxiety. A trial with epinephrine and norepinephrine infusion. Mt Sinai J Med 41: 615-625.
46. Wahlestedt C, Pich EM, Koob GF, Yee F, Heilig M (1993). Modulation of anxiety and neuropeptide Y-Y1 receptors by antisense oligodeoxynucleotides. Science 259: 528-531.
47. Wang Z, Gardell LR, Ossipov MH, Vanderah TW, Brennan MB, Hochgeschwender U et al (2001). Pronociceptive actions of dynorphin maintain chronic neuropathic pain. J Neurosci 21: 1779-1786.
48. Westenberg HG, den Boer JA, Kahn RS (1987). Psychopharmacology of anxiety disorders: on the role of serotonin in the treatment of anxiety states and phobic disorders. Psychopharmacol Bull 23: 145-149.
49. Wise CD, Berger BD, Stein L (1970). Serotonin: a possible mediator of behavioral suppression induced by anxiety. Dis Nerv Syst 31(Suppl): 34-37.
50. Wollemann M, Benyhe S (2004). Non-opioid actions of opioid peptides. Life Sci 75: 257-270.