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Stress
The International Journal on the Biology of Stress
Volume 19, 2016 - Issue 4: Smolenice Symposium
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Original Article

Vasopressinergic control of stress-related behavior: studies in Brattleboro rats

, , , , , , , & show all
Pages 349-361 | Received 12 Nov 2015, Accepted 23 Apr 2016, Published online: 17 May 2016

References

  • Aguilera G. (1994). Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15:321–50.
  • Albers HE. (2015). Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network. Front Neuroendocrinol 36:49–71.
  • Altemus M, Cizza G, Gold PW. (1992). Chronic fluoxetine treatment reduces hypothalamic vasopressin secretion in vitro. Brain Res 593:311–13.
  • Appenrodt E, Schnabel R, Schwarzberg H. (1998). Vasopressin administration modulates anxiety-related behavior in rats. Physiol Behav 64:543–7.
  • Bagdy G, Graf M, Anheuer ZE, Modos EA, Kantor S. (2001). Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. Int J Neuropsychopharmacol 4:399–408.
  • Balazsfi D, Pinter O, Klausz B, Kovacs KB, Fodor A, Torok B, Engelmann M, Zelena D. (2015). Restoration of peripheral V2 receptor vasopressin signaling fails to correct behavioral changes in Brattleboro rats. Psychoneuroendocrinology 51:11–23.
  • 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 47:503–13.
  • 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 29:483–93.
  • Bitew T. (2014). Prevalence and risk factors of depression in Ethiopia: a review. Ethiop J Health Sci 24:161–9.
  • 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.
  • Bosch OJ, Neumann ID. (2012). Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm Behav 61:293–303.
  • Breuer ME, van Gaalen MM, Wernet W, Claessens SE, Oosting RS, Behl B, Korte SM, et al. (2009). SSR149415, a non-peptide vasopressin V1b receptor antagonist, has long-lasting antidepressant effects in the olfactory bulbectomy-induced hyperactivity depression model. Naunyn Schmiedebergs Arch Pharmacol 379:101–6.
  • Burnard DM, Pittman QJ, Veale WL. (1985). Brattleboro rats display increased sensitivity to arginine vasopressin-induced motor disturbances. Brain Res 342:316–22.
  • Caffe AR, van Leeuwen FW, Luiten PG. (1987). Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus. J Comp Neurol 261:237–52.
  • Carroll BJ. (1982). Clinical applications of the dexamethasone suppression test for endogenous depression. Pharmacopsychiatria 15:19–25.
  • Compaan JC, Buijs RM, Pool CW, De Ruiter AJ, Koolhaas JM. (1993). Differential lateral septal vasopressin innervation in aggressive and nonaggressive male mice. Brain Res Bull 30:1–6.
  • Cryan JF, Slattery DA. (2007). Animal models of mood disorders: recent developments. Curr Opin Psychiatry 20:1–7.
  • Dallman MF. (1993). Stress update adaptation of the hypothalamic–pituitary–adrenal axis to chronic stress. Trends Endocrinol Metab 4:62–9.
  • De Bellis MD, Gold PW, Geracioti TD, Jr., Listwak SJ, Kling MA. (1993). Association of fluoxetine treatment with reductions in CSF concentrations of corticotropin-releasing hormone and arginine vasopressin in patients with major depression. Am J Psychiatry 150:656–7.
  • de Wied D. (1978). Vasopressin in affective illness. Lancet 2:273.
  • Dinan TG, Scott LV. (2005). Anatomy of melancholia: focus on hypothalamic-pituitary-adrenal axis overactivity and the role of vasopressin. J Anat 207:259–64.
  • Douglas AJ, Johnstone LE, Neumann I, Leng G, Russell JA. (1994). Oxytocin neurones in the supraoptic nucleus (SON) are inhibited by endogenous opioids in late pregnant rats. Gene Ther 1:S84.
  • Ebner K, Wotjak CT, Holsboer F, Landgraf R, Engelmann M. (1999). Vasopressin released within the septal brain area during swim stress modulates the behavioural stress response in rats. Eur J Neurosci 11:997–1002.
  • Ebner K, Wotjak CT, Landgraf R, Engelmann M. (2002). Forced swimming triggers vasopressin release within the amygdala to modulate stress-coping strategies in rats. Eur J Neurosci 15:384–8.
  • Egashira N, Tanoue A, Matsuda T, Koushi E, Harada S, Takano Y, Tsujimoto G, et al. (2007). Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav Brain Res 178:123–7.
  • Engelmann M, Ebner K, Landgraf R, Holsboer F, Wotjak CT. (1999). Emotional stress triggers intrahypothalamic but not peripheral release of oxytocin in male rats. J Neuroendocrinol 11:867–72.
  • Engelmann M, Landgraf R, Wotjak CT. (2004). The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited. Front Neuroendocrinol 25:132–49.
  • Engelmann M, Ludwig M, Landgraf R. (1992). Microdialysis administration of vasopressin and vasopressin antagonists into the septum during pole-jumping behavior in rats. Behav Neural Biol 58:51–7.
  • Engelmann M, Thrivikraman KV, Su Y, Nemeroff CB, Montkowski A, Landgraf R, Holsboer F, Plotsky PM. (1996). Endocrine and behavioral effects of airpuff-startle in rats. Psychoneuroendocrinology 21:391–400.
  • Engelmann M, Wotjak CT, Ebner K, Landgraf R. (2000). Behavioural impact of intraseptally released vasopressin and oxytocin in rats. Exp Physiol 85:125S–30S.
  • Feifel D, Melendez G, Priebe K, Shilling PD. (2007). The effects of chronic administration of established and putative antipsychotics on natural prepulse inhibition deficits in Brattleboro rats. Behav Brain Res 181:278–86.
  • Fodor A, Klausz B, Pinter O, Daviu N, Rabasa C, Rotllant D, Balazsfi D, et al. (2012). Maternal neglect with reduced depressive-like behavior and blunted c-fos activation in Brattleboro mothers, the role of central vasopressin. Horm Behav 62:539–51.
  • Fodor A, Kovacs KB, Balazsfi D, Klausz B, Pinter O, Demeter K, Daviu N, et al. (2016). Depressive- and anxiety-like behaviors and stress-related neuronal activation in vasopressin-deficient female Brattleboro rats. Physiol Behav 158:100–11.
  • Fodor A, Pinter O, Domokos A, Langnaese K, Barna I, Engelmann M, Zelena D. (2013). Blunted HPA axis response in lactating, vasopressin-deficient Brattleboro rats. J Endocrinol 219:89–100.
  • Friedmann AS, Memoli VA, Yu XM, North WG. (1993). Biosynthesis of vasopressin by gastrointestinal cells of Brattleboro and Long-Evans rats. Peptides 14:607–12.
  • Garcia FD, Coquerel Q, Kiive E, Dechelotte P, Harro J, Fetissov SO. (2011). Autoantibodies reacting with vasopressin and oxytocin in relation to cortisol secretion in mild and moderate depression. Prog Neuropsychopharmacol Biol Psychiatry 35:118–25.
  • Gillespie CF, Nemeroff CB. (2005). Hypercortisolemia and depression. Psychosom Med 67:S26–S8.
  • Goekoop J, de Winter R, Wolterbeek R, Wiegant V. (2011). Support for two increased vasopressinergic activities in depression at large and the differential effect of antidepressant treatment. J Psychopharmacol (Oxford) 25:1304–12.
  • Goekoop JG, de Winter RF, Wolterbeek R, Spinhoven P, Zitman FG, Wiegant VM. (2009). Reduced cooperativeness and reward-dependence in depression with above-normal plasma vasopressin concentration. J Psychopharmacol (Oxford) 23:891–7.
  • Gold PW, Goodwin FK, Reus VI. (1978). Vasopressin in affective illness. Lancet 1:1233–6.
  • Griebel G, Beeske S, Stahl SM. (2012). The vasopressin V(1b) receptor antagonist SSR149415 in the treatment of major depressive and generalized anxiety disorders: results from 4 randomized, double-blind, placebo-controlled studies. J Clin Psychiatry 73:1403–11.
  • Griebel G, Simiand J, Serradeil-Le Gal C, Wagnon J, Pascal M, Scatton B, Maffrand JP, Soubrie P. (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 USA 99:6370–5.
  • Griebel G, Simiand J, Stemmelin J, Gal CS, Steinberg R. (2003). The vasopressin V1b receptor as a therapeutic target in stress-related disorders. Curr Drug Targets CNS Neurol Disord 2:191–200.
  • Hodgson RA, Mullins D, Lu SX, Guzzi M, Zhang X, Bleickardt CJ, Scott JD, et al. (2014). Characterization of a novel vasopressin V1b receptor antagonist, V1B-30N, in animal models of anxiety-like and depression-like behavior. Eur J Pharmacol 730:157–63.
  • Ideno J, Mizukami H, Honda K, Okada T, Hanazono Y, Kume A, Saito T, et al. (2003). Persistent phenotypic correction of central diabetes insipidus using adeno-associated virus vector expressing arginine-vasopressin in Brattleboro rats. Mol Ther 8:895–902.
  • Inder WJ, Donald RA, Prickett TC, Frampton CM, Sullivan PF, Mulder RT, Joyce PR. (1997). Arginine vasopressin is associated with hypercortisolemia and suicide attempts in depression. Biol Psychiatry 42:744–7.
  • Ivell R, Schmale H, Krisch B, Nahke P, Richter D. (1986). Expression of a mutant vasopressin gene: differential polyadenylation and read-through of the mRNA 3′ end in a frame-shift mutant. EMBO J 5:971–7.
  • Keck ME, Welt T, Muller MB, Uhr M, Ohl F, Wigger A, Toschi N, 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 28:235–43.
  • Kokras N, Sotiropoulos I, Pitychoutis PM, Almeida OF, Papadopoulou-Daifoti Z. (2011). Citalopram-mediated anxiolysis and differing neurobiological responses in both sexes of a genetic model of depression. Neuroscience 194:62–71.
  • Krahn DD, Meller WH, Shafer RB, Morley JE. (1985). Cortisol response to vasopressin in depression. Biol Psychiatry 20:918–21.
  • Landgraf R. (2006). The involvement of the vasopressin system in stress-related disorders. CNS Neurol Disord Drug Targets 5:167–79.
  • Landgraf R, Gerstberger R, Montkowski A, Probst JC, Wotjak CT, Holsboer F, Engelmann M. (1995). V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J Neurosci 15:4250–8.
  • Landgraf R, Kessler MS, Bunck M, Murgatroyd C, Spengler D, Zimbelmann M, Nussbaumer M, et al. (2007). Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glyoxalase-I. Neurosci Biobehav Rev 31:89–102.
  • Landgraf R, Ludwig M. (1991). Vasopressin release within the supraoptic and paraventricular nuclei of the rat brain: osmotic stimulation via microdialysis. Brain Res 558:191–6.
  • Landgraf R, Neumann ID. (2004). Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol 25:150–76.
  • Liebsch G, Wotjak CT, Landgraf R, Engelmann M. (1996). Septal vasopressin modulates anxiety-related behaviour in rats. Neurosci Lett 217:101–4.
  • Ludwig M, Bull PM, Tobin VA, Sabatier N, Landgraf R, Dayanithi G, Leng G. (2005). Regulation of activity-dependent dendritic vasopressin release from rat supraoptic neurones. J Physiol (Lond) 564:515–22.
  • Ludwig M, Leng G. (1998). Intrahypothalamic vasopressin release. An inhibitor of systemic vasopressin secretion? Adv Exp Med Biol 449:163–73.
  • Ludwig M, Stern J. (2015). Multiple signalling modalities mediated by dendritic exocytosis of oxytocin and vasopressin. Philos Trans R Soc Lond B Biol Sci 370. doi: 10.1098/rstb.2014.0182.
  • Meller WH, Kathol RC, Jaeckle RS, Lopez JF. (1987). Stimulation of the pituitary-adrenal axis with arginine vasopressin in patients with depression. J Psychiatr Res 21:269–77.
  • Merali Z, Kent P, Du L, Hrdina P, Palkovits M, Faludi G, Poulter MO, et al. (2006). Corticotropin-releasing hormone, arginine vasopressin, gastrin-releasing peptide, and neuromedin B alterations in stress-relevant brain regions of suicides and control subjects. Biol Psychiatry 59:594–602.
  • Mlynarik M, Zelena D, Bagdy G, Makara GB, Jezova D. (2007). Signs of attenuated depression-like behavior in vasopressin deficient Brattleboro rats. Horm Behav 51:395–405.
  • Muller MB, Landgraf R, Keck ME. (2000). Vasopressin, major depression, and hypothalamic-pituitary-adrenocortical desensitization. Biol Psychiatry 48:330–3.
  • Murgatroyd C, Spengler D. (2011). Epigenetic programming of the HPA axis: early life decides. Stress 14:581–9.
  • Murgatroyd C, Wu Y, Bockmuhl Y, Spengler D. (2010). Genes learn from stress: how infantile trauma programs us for depression. Epigenetics 5:194–9.
  • Nussey SS, Ang VT, Jenkins JS, Chowdrey HS, Bisset GW. (1984). Brattleboro rat adrenal contains vasopressin. Nature 310:64–6.
  • Poirier GL, Cordero MI, Sandi C. (2013). Female vulnerability to the development of depression-like behavior in a rat model of intimate partner violence is related to anxious temperament, coping responses, and amygdala vasopressin receptor 1a expression. Front Behav Neurosci 7:35.
  • Purba JS, Hoogendijk WJ, Hofman MA, Swaab DF. (1996). Increased number of vasopressin- and oxytocin-expressing neurons in the paraventricular nucleus of the hypothalamus in depression. Arch Gen Psychiatry 53:137–43.
  • Rotzinger S, Lovejoy DA, Tan LA. (2010). Behavioral effects of neuropeptides in rodent models of depression and anxiety. Peptides 31:736–56.
  • Rush AJ, Giles DE, Schlesser MA, Orsulak PJ, Parker CR, Jr., Weissenburger JE, Crowley GT, et al. (1996). The dexamethasone suppression test in patients with mood disorders. J Clin Psychiatry 57:470–84.
  • Salome N, Stemmelin J, Cohen C, Griebel G. (2006). Differential roles of amygdaloid nuclei in the anxiolytic- and antidepressant-like effects of the V1b receptor antagonist, SSR149415, in rats. Psychopharmacology (Berl) 187:237–44.
  • Sawyer WH, Valtin H, Sokol HW. (1964). Neurohypophysial principles in rats with familial hypothalamic diabetes insipidus (Brattleboro strain). Endocrinology 74:153–5.
  • Schmale H, Richter D. (1984). Single base deletion in the vasopressin gene is the cause of diabetes insipidus in Brattleboro rats. Nature 308:705–9.
  • Scott LV, Dinan TG. (1998). Vasopressin and the regulation of hypothalamic-pituitary-adrenal axis function: implications for the pathophysiology of depression. Life Sci 62:1985.
  • Silva MT, Galvao TF, Martins SS, Pereira MG. (2014). Prevalence of depression morbidity among Brazilian adults: a systematic review and meta-analysis. Rev Bras Psiquiatr 36:262–70.
  • Smock T, Cach R, Topple A. (1987). Action of vasopressin on neurons and microvessels in the rat hippocampal slice. Exp Brain Res 66:401–8.
  • Sokol W, Valtin H. (1982). The Brattleboro rat. Ann NY Acad Sci 394:1–802.
  • Somova L, Ivanova E, Zaharieva S, Machuganska A. (1986). Changes of adrenal vasopressin during hemorrhagic shock in rats with hereditary diabetes insipidus (Brattleboro strain). Acta Physiol Pharmacol Bulg 12:70–5.
  • Stemmelin J, Lukovic L, Salome N, Griebel G. (2005). Evidence that the lateral septum is involved in the antidepressant-like effects of the vasopressin V1b receptor antagonist, SSR149415. Neuropsychopharmacology 30:35–42.
  • Sterrenburg L, Borch A, Peeters BW, Pinter O, Zelena D, Roubos EW, Kozicz T. (2011). Acute ether stress differentially affects corticotropin-releasing factor and urocortin 1 in the Brattleboro rat. Brain Res 1398:21–9.
  • Stewart LQ, Roper JA, Scott Young W, 3rd, O'Carroll AM, Lolait SJ. (2008). The role of the arginine vasopressin Avp1b receptor in the acute neuroendocrine action of antidepressants. Psychoneuroendocrinology 33:405–15.
  • Takahashi LK, Kalin NH, Vanden Burgt JA, Sherman JE (1989). Corticotropin-releasing factor modulates defensive-withdrawal and exploratory behavior in rats. Behav Neurosci 103:648–54.
  • Valtin H, Schroeder HA. (1964). Familial hypothalamic diabetes insipidus in rats (Brattleboro strain). Am J Physiol 206:425–30.
  • van Londen L, Goekoop JG, Kerkhof GA, Zwinderman KH, Wiegant VM, De Wied D. (2001). Weak 24-h periodicity of body temperature and increased plasma vasopressin in melancholic depression. Eur Neuropsychopharmacol 11:7–14.
  • van Londen L, Kerkhof GA, van den Berg F, Goekoop JG, Zwinderman KH, Frankhuijzen-Sierevogel AC, Wiegant VM, de Wied D. (1998). Plasma arginine vasopressin and motor activity in major depression. Biol Psychiatry 43:196–204.
  • van West D, Del-Favero J, Aulchenko Y, Oswald P, Souery D, Forsgren T, Sluijs S, et al. (2004). A major SNP haplotype of the arginine vasopressin 1B receptor protects against recurrent major depression. Mol Psychiatry 9:287–92.
  • Veenema AH. (2009). Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front Neuroendocrinol 30:497–518.
  • Wersinger SR, Ginns EI, O'Carroll AM, Lolait SJ, Young WS. 3rd. (2002). Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol Psychiatry 7:975–84.
  • Wigger A, Sanchez MM, Mathys KC, Ebner K, Frank E, Liu D, Kresse A, et al. (2004). Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29:1–14.
  • Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M. (1998). Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons. Neuroscience 85:1209–22.
  • Wotjak CT, Landgraf R, Engelmann M. (2008). Listening to neuropeptides by microdialysis: echoes and new sounds? Pharmacol Biochem Behav 90:125–34.
  • Zelena D. (2012). Vasopressin in health and disease with a focus on affective disorders. Cent Nerv Syst Agents Med Chem 12:286–303.
  • Zelena D, Langnaese K, Domokos A, Pinter O, Landgraf R, Makara GB, Engelmann M. (2009). Vasopressin administration into the paraventricular nucleus normalizes plasma oxytocin and corticosterone levels in Brattleboro rats. Endocrinology 150:2791–8.
  • Zelena D, Mergl Z, Makara GB. (2006). The role of vasopressin in diabetes mellitus-induced hypothalamo-pituitary-adrenal axis activation: studies in Brattleboro rats. Brain Res Bull 69:48–56.
  • Zelena D, Pinter O, Langnaese K, Richter K, Landgraf R, Makara GB, Engelmann M. (2013). Oxytocin in Brattleboro rats: increased synthesis is contrasted by blunted intrahypothalamic release from supraoptic nucleus neurones. J Neuroendocrinol 25:711–18.
  • Zink CF, Stein JL, Kempf L, Hakimi S, Meyer-Lindenberg A. (2010). Vasopressin modulates medial prefrontal cortex-amygdala circuitry during emotion processing in humans. J Neurosci 30:7017–22.

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