A hypomorphic vasopressin allele prevents anxiety-related behavior

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Bunck, Mirjam ^a   Czibere, Ludwig ^a   Horvath, Charlotte ^a   Graf, Cornelia ^a   Frank, Elisabeth ^a,e   Keßler, Melanie S ^a   Murgatroyd, Chris ^a   Müller Myhsok, Bertram ^a   Gonik, Mariya ^a   Weber, Peter ^a   Pütz, Benno ^a   Muigg, Patrik ^b   Panhuysen, Markus ^c   Singewald, Nicolas ^b   Bettecken, Thomas ^a   Deussing, Jan M ^a,d   Holsboer, Florian ^a   Spengler, Dietmar ^a   Landgraf, Rainer ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c Affectis Pharmaceutical AG   (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; VASOPRESSIN; ARGIPRESSIN; OXYTOCIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BREEDING; CONTROLLED STUDY; DEPRESSION; FEMALE; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENOTYPE PHENOTYPE CORRELATION; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICROARRAY ANALYSIS; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; POLYMORPHIC LOCUS; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SUPRAOPTIC NUCLEUS; ALLELE; ANIMAL; ANTERIOR HYPOTHALAMUS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALIA; MUS;

ALLELES; ANIMALS; ANXIETY; ARGININE VASOPRESSIN; BEHAVIOR, ANIMAL; DEPRESSION; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MICE; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYTOCIN; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; SUPRAOPTIC NUCLEUS;

EID: 65249104881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005129     Document Type: Article

References (60)

1. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, et al. (2002) Neurobiology of depression. Neuron 34(1): 13-25.
2. Ustun TB, Ayuso-Mateos JL, Chatterji S, Mathers C, Murray CJ (2004) Global burden of depressive disorders in the year 2000. Br J Psychiatry 184: 386-92.
3. Kessler RC, McGonagle KA, Zhao S, Nelson CB, Hughes M, et al. (1994) Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry 51(1): 8-19.
4. Fava M, Kendler KS (2000) Major depressive disorder. Neuron 28(2): 335-41.
5. Sanders AR, Detera-Wadleigh SD, Gershon ES (1999) Molecular genetics of mood disorders. In: Charney DS, Nestler EJ, Bunney BS, eds. Neurobiology of mental illness. 1st ed. New York: Oxford University Press. pp 299-316.
6. Ressler KJ, Nemeroff CB (2000) Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12 Suppl 1: 2-19.
7. Landgraf R (2001) Neuropeptides and anxiety-related behavior. Endocr J 48(5): 517-33.
8. Gillespie NA, Kirk KM, Evans DM, Heath AC, Hickie IB, et al. (2004) Do the genetic or environmental determinants of anxiety and depression change with age? A longitudinal study of Australian twins. Twin Res 7(1): 39-53.
9. Kas MJ, Fernandes C, Schalkwyk LC, Collier DA (2007) Genetics of behavioural domains across the neuropsychiatric spectrum; of mice and men. Mol Psychiatry 12(4): 324-30.
10. Ring RH (2005) The central vasopressinergic system: examining the opportunities for psychiatric drug development. Curr Pharm Des 11(2): 205-25.
11. Landgraf R (2006) The involvement of the vasopressin system in stress-related disorders. CNS Neurol Disord Drug Targets 5(2): 167-79.
12. Frank E, Landgraf R (2008) The vasopressin system - from antidiuresis to psychopathology. Eur J Pharmacol 583(2-3): 226-42.
13. Birkett SD, Pickering BT (1993) The aberrant vasopressin precursor in rats with central diabetes insipidus (Brattleboro rats). Response to stimuli. Ann N Y Acad Sci 689: 83-90.
14. Bohus B, de Wied D (1998) The vasopressin deficient Brattleboro rats: a natural knockout model used in the search for CNS effects of vasopressin. Prog Brain Res 119: 555-73.
15. Bruins J, Kovacs GL, Abbes AP, Burbach JP, van den Akker EL, et al. (2006) Minor disturbances in central nervous system function in familial neurohypophysial diabetes insipidus. Psychoneuroendocrinology 31(1): 80-91.
16. Verbalis JG (2003) Diabetes insipidus. Rev Endocr Metab Disord 4(2): 177-85.
17. Landgraf R, Kessler MS, Bunck M, Murgatroyd C, Spengler D, et al. (2007) Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glyoxalase-I. Neurosci Biobehav Rev 31(1): 89-102.
18. Murgatroyd C, Wigger A, Frank E, Singewald N, Bunck M, et al. (2004) Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J Neurosci 24(35): 7762-70.
19. Keck ME, Welt T, Muller MB, Uhr M, Ohl F, et al. (2003) Reduction of hypothalamic vasopressinergic hyperdrive contributes to clinically relevant behavioral and neuroendocrine effects of chronic paroxetine treatment in a psychopathological rat model. Neuropsychopharmacology 28(2): 235-43.
20. Wigger A, Sanchez MM, Mathys KC, Ebner K, Frank E, et al. (2004) Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29(1): 1-14.
21. Landgraf R, Gerstberger R, Montkowski A, Probst JC, Wotjak CT, et al. (1995) V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J Neurosci 15(6): 4250-8.
22. Young LJ (2001) Oxytocin and vasopressin as candidate genes for psychiatric disorders: lessons from animal models. Am J Med Genet 105(1): 53-4.
23. Scott LV, Dinan TG (2002) Vasopressin as a target for antidepressant development: an assessment of the available evidence. J Affect Disord 72(2): 113-24.
24. Kromer SA, Kessler MS, Milfay D, Birg IN, Bunck M, et al. (2005) Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety. J Neurosci 25(17): 4375-84.
25. Kessler MS, Murgatroyd C, Bunck M, Czibere L, Frank E, et al. (2007) Diabetes insipidus and, partially, low anxiety-related behaviour are linked to a SNP-associated vasopressin deficit in LAB mice. Eur J Neurosci 26(10): 2857-64.
26. Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl) 92(2): 180-5.
27. Steru L, Chermat R, Thierry B, Simon P (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 85(3): 367-70.
28. Porsolt RD, Bertin A, Jalfre M (1978) "Behavioural despair" in rats and mice: strain differences and the effects of imipramine. Eur J Pharmacol 51(3): 291-4.
29. Palkovits M (1973) Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59: 449-50.
30. Paxinos G, Franklin K (2001) The mouse brain in stereotaxic coordinates. 2nd Edition ed. San Diego, San Francisco, New York, Boston, London, Sydney, Tokyo: Academic Press.
31. Deussing JM, Kuhne C, Putz B, Panhuysen M, Breu J, et al. (2007) Expression profiling identifies the CRH/CRH-R1 system as a modulator of neurovascular gene activity. J Cereb Blood Flow Metab 27(8): 1476-95.
32. Tsolakidou A, Trumbach D, Panhuysen M, Putz B, Deussing J, et al. (2008) Acute stress regulation of neuroplasticity genes in mouse hippocampus CA3 area - Possible novel signalling pathways. Mol Cell Neurosci 38(3): 444-52.
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(2Delta Delta C(T)) Method. Methods 25(4): 402-8.
34. Muller MB, Keck ME, Binder EB, Kresse AE, Hagemeyer TP, et al. (2003) ABCB1 (MDR1)-type P-glycoproteins at the blood-brain barrier modulate the activity of the hypothalamic-pituitary-adrenocortical system: implications for affective disorder. Neuropsychopharmacology 28(11): 1991-9.
35. Ivell R, Richter D (1984) Structure and comparison of the oxytocin and vasopressin genes from rat. Proc Natl Acad Sci U S A 81(7): 2006-10.
36. Villar MJ, Ceccatelli S, Ronnqvist M, Hokfelt T (1994) Nitric oxide synthase increases in hypothalamic magnocellular neurons after salt loading in the rat. An immunohistochemical and in situ hybridization study. Brain Res 644(2): 273-81.
37. Hetzenauer A, Sinnegger-Brauns MJ, Striessnig J, Singewald N (2006) Brain activation pattern induced by stimulation of L-type Ca2+-channels: contribution of Ca(V)1.3 and Ca(V)1.2 isoforms. Neuroscience 139(3): 1005-15.
38. Bielsky IF, Hu SB, Ren X, Terwilliger EF, Young LJ (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47(4): 503-13.
39. Bielsky IF, Hu SB, Szegda KL, Westphal H, Young LJ (2004) Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29(3): 483-93.
40. Egashira N, Tanoue A, Matsuda T, Koushi E, Harada S, et al. (2007) Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav Brain Res 178(1): 123-7.
41. Griebel G, Simiand J, Serradeil-Le Gal C, Wagnon J, Pascal M, et al. (2002) Anxiolytic- and antidepressant-like effects of the non-peptide vasopressin V1b receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders. Proc Natl Acad Sci U S A 99(9): 6370-5.
42. Engin E, Treit D (2008) Dissociation of the anxiolytic-like effects of Avpr1a and Avpr1b receptor antagonists in the dorsal and ventral hippocampus. Neuropeptides 42(4): 411-21.
43. Fields RL, House SB, Gainer H (2003) Regulatory domains in the intergenic region of the oxytocin and vasopressin genes that control their hypothalamus-specific expression in vitro. J Neurosci 23(21): 7801-9.
44. Veenema AH, Neumann ID (2008) Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res 170: 261-76.
45. Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc Natl Acad Sci U S A 104(42): 16681-4.
46. Ji C, Chen Y, Centrella M, McCarthy TL (1999) Activation of the insulin-like growth factor-binding protein-5 promoter in osteoblasts by cooperative E box, CCAAT enhancer-binding protein, and nuclear factor-1 deoxyribonucleic acid-binding sequences. Endocrinology 140(10): 4564-72.
47. Alikhani-Koupaei R, Fouladkou F, Fustier P, Cenni B, Sharma AM, et al. (2007) Identification of polymorphisms in the human 11beta-hydroxysteroid dehydrogenase type 2 gene promoter: functional characterization and relevance for salt sensitivity. Faseb J 21(13): 3618-28.
48. Chakrabarty A, Roberts MR (2007) Ets-2 and C/EBP-beta are important mediators of ovine trophoblast Kunitz domain protein-1 gene expression in trophoblast. BMC Mol Biol 8: 14.
49. Kraus RJ, Shadley L, Mertz JE (2001) Nuclear factor 1 family members mediate repression of the BK virus late promoter. Virology 287(1): 89-104.
50. Shabalina SA, Ogurtsov AY, Spiridonov NA (2006) A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res 34(8): 2428-37.
51. Cervino AC, Li G, Edwards S, Zhu J, Laurie C, et al. (2005) Integrating QTL and high-density SNP analyses in mice to identify Insig2 as a susceptibility gene for plasma cholesterol levels. Genomics 86(5): 505-17.
52. Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29(3): 386-97.
53. Turri MG, DeFries JC, Henderson ND, Flint J (2004) Multivariate analysis of quantitative trait loci influencing variation in anxiety-related behavior in laboratory mice. Mamm Genome 15(2): 69-76.
54. Willis-Owen SA, Flint J (2006) The genetic basis of emotional behaviour in mice. Eur J Hum Genet 14(6): 721-8.
55. Delaval K, Feil R (2004) Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 14(2): 188-95.
56. Wilkins JF, Haig D (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4(5): 359-68.
57. Jacobi F, Wittchen HU, Holting C, Hofler M, Pfister H, et al. (2004) Prevalence, co-morbidity and correlates of mental disorders in the general population: results from the German Health Interview and Examination Survey (GHS). Psychol Med 34(4): 597-611.
58. Mlynarik M, Zelena D, Bagdy G, Makara GB, Jezova D (2007) Signs of attenuated depression-like behavior in vasopressin deficient Brattleboro rats. Horm Behav 51(3): 395-405.
59. Touma C, Bunck M, Glasl L, Nussbaumer M, Palme R, et al. (2008) Mice selected for high versus low stress reactivity: A new animal model for affective disorders. Psychoneuroendocrinology 33(6): 839-62.
60. Neumann ID, Landgraf R (2008) Advances in vasopressin and oxytocin - from genes to behaviour to disease. Prog. Brain Res. 170, 1st ed. Oxford, Amsterdam: Elsevier.