The hypothalamic-pituitary-adrenal axis response to stress in mice lacking functional vasopressin V1b receptors

Endocrinology

Volumn 148, Issue 2, 2007, Pages 849-856

  Lolait, Stephen J ^a   Stewart, Lesley Q ^a   Jessop, David S ^a   Young III, W Scott ^b   O'Carroll, Anne Marie ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; INSULIN; VASOPRESSIN V1B RECEPTOR;

ANIMAL EXPERIMENT; ANTERIOR HYPOTHALAMUS; ARTICLE; CONTROLLED STUDY; FEMALE; GENOTYPE; HORMONE BLOOD LEVEL; HYPOGLYCEMIA; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRESS;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; CORTICOSTERONE; HORMONES; HYPOGLYCEMIA; HYPOGLYCEMIC AGENTS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INSULIN; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; PITUITARY-ADRENAL SYSTEM; RECEPTORS, VASOPRESSIN; RESTRAINT, PHYSICAL; STRESS; TIME FACTORS;

EID: 33846529087     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2006-1309     Document Type: Article

References (71)

1. Knepper MA 1997 Molecular physiology of urinary concentrating mechanism: regulation of aquaporin water channels by vasopressin. Am J Physiol Renal Physiol 272:F3-F12
2. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR 1999 Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400:766-768
3. Storm EE, Tecott LH 2005 Social circuits: Peptidergic regulation of mammalian social behaviour. Neuron 47:483-486
4. Koshimizu T, Nasa Y, Tanoue A, Oikawa R, Kawahara Y, Kiyono Y, Adachi T, Tanaka T, Kuwaki T, Mori T, Takeo S, Okamura H, Tsujimoto G 2006 V1a vasopressin receptors maintain normal blood pressure by regulating circulating blood volume and baroreflex sensitivity. Proc Natl Acad Sci USA 103:7807-7812
5. Wersinger SR, Ginns EI, O'Carroll AM, Lolait SJ, Young 3rd WS 2002 Vasopressin V1b receptor knockout reduces aggressive behaviour in male mice. Mol Psychiatry 7:975-984
6. Antoni F 1993 Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front Neuroendocrinol 14:76-122
7. Volpi S, Rabadan-Diehl C, Aguilera G 2004 Vasopressinergic regulation of the hypothalamic pituitary adrenal axis and stress adaptation. Stress 7:75-83
8. Lolait SJ, O'Carroll A-M, Mahan LC, Felder CC, Button DC, Young 3rd WS, Mezey E, Brownstein MJ 1995 Extrapituitary expression of the rat V1b vasopressin receptor gene. Proc Natl Acad Sci USA 92:6783-6787
9. Cunningham Jr ET, Sawchenko PE 1991 Reflex control of magnocellular vasopressin and oxytocin secretion. Trends Neurosci 14:406-411
10. Whitnall MH 1993 Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog Neurobiol 40:573-629
11. Pacak K, Palkovits M 2001 Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22:502-548
12. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE 2003 Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151-180
13. Wotjak C, Naruo T, Muraoka S, Simchen R, Landgraf R, Engelmann M 2001 Forced swimming stimulates the expression of vasopressin and oxytocin in magnocellular neurons of the rat hypothalamic paraventricular nucleus. Eur J Neurosci 13:2273-2281
14. Wotjak T, Ludwig M, Ebner K, Russell JA, Singewald S, Landgraf R, Engelmann M 2002 Vasopressin from hypothalamic magnocellular neurons has opposite effects at the adenohypophysis and in the supraoptic nucleus on ACTH secretion. Eur J Neurosci 16:477-485
15. Muglia L, Jacobson L, Dikkes P, Majzoub JA 1995 Corticotropin-releasing hormone deficiency reveals major fetal but not adult glucocorticoid need. Nature 373:427-432
16. Timpl P, Spanagel R, Sillaber T, Kresse A, Reul JMHM, Stalla GK, Blanquet V, Steckler T, Holsboer F, Wurst W 1998 Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 19:162-166
17. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian M, Gold LH, Chen R, Marchuk Y, Hauser C, Bentley CA, Sawchenko PE, Koob GF, Vale W, Lee KF 1998 Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20:1093-1102
18. Muller MB, Landgraf R, Preil J, Sillaber I, Kresse AE, Keck ME, Zimmerman S, Holsboer, F, Wurst W 2000 Selective activation of the hypothalamic vasopressinergic system in mice deficient for the corticotropin-releasing hormone receptor 1 is dependent on glucocorticoids. Endocrinology 141:4262-4269
19. Makara GB, Mergl Z, Zelena D 2004 The role of vasopressin in hypothalamopituitary-adrenal axis activation during stress: an assessment of the evidence. Ann NY Acad Sci 1018:151-161
20. Kjaer A, Knigge U, Bach FW, Warberg J 1992 Histamine- and stress-induced secretion of ACTH and β-endorphin: involvement of corticotropin-releasing hormone and vasopressin. Neuroendocrinology 56:419-428
21. Suda T, Nakano Y, Tozawa F, Sumitomo T, Sata Y, Yamada M, Demura H 1992 The role of corticotropin-releasing factor and vasopressin in hypoglycemia-induced proopiomelanocortin gene expression in the rat anterior pituitary gland. Brain Res 579:303-308
22. Turnbull AV, Lee S, Rivier, C 1998 Mechanisms of hypothalamic-pituitary-adrenal axis stimulation by immune signals in the adult rat. Ann NY Acad Sci 840:434-443
23. Plotsky PM, Bruhn TO, Vale W 1985 Hypophysiotropic regulation of adrenocorticotropin secretion in response to insulin-induced hypoglycemia. Endocrinology 117:323-329
24. Paulmyer-Lacroix O, Anglade G, Grino M 1994 Insulin-induced hypoglycaemia increases colocalization of corticotrophin-releasing factor and arginine vasopressin mRNAs in the rat hypothalamic paraventricular nucleus. J Mol Endocrinol 13:313-320
25. Baylis PH, Heath DA 1977 Plasma-arginine-vasopressin response to insulin-induced hypoglycaemia. Lancet 2:428-430
26. Fisher BM, Baylis PH, Frier BM 1987 Plasma oxytocin, arginine vasopressin and atrial natriuretic peptide responses to insulin-induced hypoglycaemia in man. Clin Endocrinol 26:179-185
27. Ellis MJ, Schmidli RS, Donald RA, Livesey JH, Espiner EA 1990 Plasma corticotrophin-releasing factor and vasopressin responses to hypoglycaemia in normal man. Clin Endocrinol 32:93-100
28. Engler D, Pham T, Fullerton MJ, Ooi G, Funder JW, Clarke IJ 1989 Studies of the secretion of corticotropin-releasing factor and arginine vasopressin into the hypophysial-portal circulation of the conscious sheep. I. Effect of an audiovisual stimulus and insulin-induced hypoglycemia. Neuroendocrinology 49:367-381
29. Guillaume V, Conte-Devolx B, Magnan E, Boudouresque F, Grino M, Cataldi M, Muret L, Priou A, Figarili JC, Oliver C 1992 Effect of chronic active immunization with antiarginine vasopressin on pituitary-adrenal function in sheep. Endocrinology 130:3007-3014
30. Berkenbosch F, De Goeij DCE, Tilders FJH 1989 Hypoglycemia enhances turnover of corticotropin-releasing factor and of vasopressin in the zona externa of the rat median eminence. Endocrinology 125:28-34
31. Alexander SL, Roud HK, Irvine CHG 1997 Effect of insulin-induced hypoglycaemia on secretion patterns and rates of corticotropin-releasing hormone, arginine vasopressin and adrenocorticotrophin in horses. J Endocrinol 153:401-409
32. Caraty A, Grino M, Locatelli A, Guillaume V, Boudouresque F, Conte-Devoix B, Oliver C 1990 Insulin-induced hypoglycenia stimulates corticotropin-releasing factor and arginine vasopressin secretion into hypophysial portal blood of conscious, unrestrained rams. J Clin Invest 85:1716-1721
33. Harbuz MS, Lightman SL 1992 Stress and the hypothalamo-pituitary- adrenal axis: acute, chronic and immunological activation. J Endocrinol 134:327-339
34. Aguilera G 1994 Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15:321-350
35. De Goeij DCE, Jezova D, Tilders FJ 1992 Repeated stress enhances vasopressin synthesis in corticotropin releasing factor neurons in the paraventricular nucleus. Brain Res 577:165-168
36. Rabadan-Diehl C, Lolait SJ, Aguilera G 1995 Regulation of pituitary vasopressin V1b receptor mRNA during stress in the rat. J Neuroendocrinol 7:903-910
37. Hashimoto K, Suemaru S, Takao T, Sugarwara M, Makino S, Ota S 1988 Corticotropin-releasing hormone and pituitary-adrenocortical responses to chronically stressed rats. Regul Pept 23:117-126
38. Ma XM, Levy A, Lightman SL 1997 Emergence of an isolated arginine vasopressin (AVP) response to stress after repeated restraint: a study of both AVP and corticotropin-releasing hormone messenger ribonucleic acid (RNA) and heteronuclear RNA. Endocrinology 138:4351-4357
39. Tanoue A, Ito S, Honda K, Oshikawa S, Kitagawa Y, Koshimizu T, Mori T, Tsujimoto G 2004 The vasopressin V1b receptor critically regulates hypothalamic-pituitary-adrenal axis activity under both stress and resting conditions. J Clin Invest 113:302-309
40. Keeney A, Jessop DS, Harbuz MS, Marsden CA, Hogg S, Blackburn-Munro RE 2006 Differential effects of acute and chronic social defeat stress on HPA axis function and hippocampal serotonin release in mice. J Neuroendocrinol 18:330-338
41. Harbuz MS, Rees RG, Eckland DJA, Jessop DS, Brewerton D, Lightman SL 1992 Paradoxical responses of hypothalamic CRF mRNA and CRF-41 peptide and adenohypophyseal POMC mRNA during chronic inflammatory stress. Endocrinology 130:1394-1400
42. Jessop DS, Eckland DJA, Todd K, Lightman SL 1989 Osmotic regulation of hypothalamo-neurointermediate lobe corticotrophin-releasing factor-41 in the rat. J Endocrinol 120:119-124
43. Young 3rd WS, Mezey E, Siegel RE 1986 Vasopressin and oxytocin mRNAs in adrenalectomized and Brattleboro rats: analysis by quantitative in situ hybridisation histochemistry. Brain Res 387:231-241
44. Young 3rd WS, Mezey E, Siegel RE 1986 Quantitative in situ hybridization histochemistry reveals increased levels of corticotropin-releasing factor-mRNA after adrenalectomy in rats. Neurosci Lett 70:198-203
45. O'Carroll AM, Raynor K, Lolait SJ, Reisine T 1994 Characterization of cloned human somatostatin receptor SSTR5. Mol Pharmacol 46:291-298
46. Slominski A, Ermak G, Hwang J, Mazurkiewicz J, Corliss D, Eastman A 1996 The expression of proopiomelanocortin (POMC) and of corticotropin releasing hormone receptor (CRH-R) genes in mouse skin. Biochim Biophys Acta 1289:247-251
47. Young 3rd WS, Bonner TJ, Brann MR 1986 Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain. Proc Natl Acad Sci USA 83:9827-9831
48. Kitay JI 1961 Sex differences in adrenal cortical secretion in the rat. Endocrinology 68:818-824
49. Wersinger SR, Kelliher KR, Zufall F, Lolait SJ, O'Carroll A-M, Young 3rd SW 2004 Social motivation is reduced in vasopressin 1b receptor null mice despite normal performance in an olfactory discrimination task. Hormones Behav 46:638-645
50. Bhatnagar S, Sun LM, Raber J, Manes S, Julius DMF, Dallman MF 2004 Changes in anxiety-related behaviour and hypothalamic pituitary adrenal activity in mice lacking the 5-HT-3A receptor. Physiol Behav 81:545-555
51. Ehrhart-Bornstein M, Hinson JP, Bornstein SF, Scherbaum WA, Vinson GP 1998 Intraadrenal interactions in the regulation of adrenocortical steroidogenesis. Endocr Rev 19:101-143
52. Bornstein SR, Chrousos GP 1999 Adrenocorticotropin (ACTH)- and non-ACTH-mediated regulation of the adrenal cortex: neural and immune inputs. J Clin Endocrinol Metab 84:1729-1736
53. Zhou D, Kusnecov AW, Shurin MR, DePaoli M, Rabin BS 1993 Exposure to physical and psychological stressors elevates plasma interleukin 6: relationship to the activation of hypothalamic-pituitary-adrenal axis. Endocrinology 133:2523-2530
54. Bethin KE, Vogt SK, Muglia LJ 2000 Interleukin-6 is an essential, corticotropin-releasing hormone-independent stimulator of the adrenal axis during immune system activation. Proc Natl Acad Sci USA 97:9317-9322
55. Jasper MS, Engeland WC 1997 Spanchnicotomy increases adrenal sensitivity to ACTH in nonstressed rats. Am J Physiol Endocrinol Metab 273:E363-E368
56. Carrasco GA, Van de Kar LD 2003 Neuroendocrine pharmacology of stress. Eur J Pharmacol 463:235-272
57. Giordano R, Picu A, Broglio F, Bonelli L, Baldi M, Berardelli R, Ghigo E, Arvat E 2004 Ghrelin, hypothalamus-pituitary-adrenal (HPA) axis and Cushing's syndrome. Pituitary 7:243-248
58. Spinazzi R, Andreis PG, Rossi GP, Nussdorfer GG 2006 Orexins in the regulation of the hypothalamic-pituitary-adrenal axis. Pharmacol Rev 58:46-57
59. Medvedev A, Igosheva N, Crumeyrolle-Arias M, Glover V 2005 Isatin: role in stress and anxiety. Stress 8:175-183
60. Link H, Dayanithi G, Fohr KJ, Gratzl M 1992 Oxytocin at physiological concentrations evokes adrenocorticotropin (ACTH) release from corticotrophs by increasing intracellular free calcium mobilized mainly from intracellular stores. Oxytocin displays synergistic or additive effects on ACTH-releasing factor or arginine vasopressin-induced ACTH secretion, respectively. Endocrinology 130:2183-2191
61. Schlosser SF, Almeida OFX, Patchev VK, Yassouridis A, Elands J 1994 Oxytocin-stimulated release of adrenocorticotropin from the rat pituitary is mediated by arginine vasopressin receptors of the V1b type. Endocrinology 135:2058-2063
62. Serradeil-Le Gal C, Wagnon J, Simiand J, Griebel G, Lacour C, Guillon G, Barberis C, Brossard G, Soubrie P, Nisato D, Pascal M, Pruss R, Scatton B, Maffrand JP, Le Fur G 2002 Characterization of (2S,4R)-1-[5-chloro- 1[(2,4-dimethoxyphenyl)sulfonyl]-3-(2-methoxy-phenyl)-2-oxo-2. 3-dihydro-1H-indol-3-yl]-4-hydroxy-N,N-dimethyl-2-pyrrolidine carboxamide (SSR149415), a selective and orally active vasopressin V1b receptor antagonist. J Pharmacol Exp Ther 300:1122-1130
63. 4]AVP and SSR149415 at human vasopressin and oxytocin receptors: evidence that SSR149415 is a mixed V1b/oxytocin receptor antagonist. Br J Pharmacol 146:744-751
64. Zelena D, Foldes A, Mergl Z, Barna I, Kovacs KJ, Makara GB 2004 Effects of repeated restraint stress on hypothalamo-pituitary-adrenocortical function in vasopressin-deficient Brattleboro rats. Brain Res Bull 15:521-530
65. Dallman MF, Viau VG, Bhatnagar S, Gomez F, Laugero K, Bell ME 2002 Corticotropin-releasing factor, corticosteroids, stress, and sugar: energy balance, the brain, and behaviour. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, brain and behaviour. New York: Academic Press; 571-631
66. deGoeij DEC, Kvetnansky R, Whitnall MH, Jesova D, Berkenbosch F, Tilders FJH 1991 Repeated stress-induced activation of corticotropin- releasing factor neurons enhances vasopressin stores and colocalization with corticotropin releasing factor neurons in the median eminence of rats. Neuroendocrinology 53:150-159
67. Marti O, Armario A 1998 Anterior pituitary response to stress: time-related changes and adaptation. Int J Neurosci 16:241-260
68. Dhabhar FS, McEwen BS, Spencer RL 1997 Adaptation to prolonged or repeated stress: comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology 65:360-368
69. Baylis PH, Robertson GL 1980 Rat vasopressin response to insulin-induced hypoglycemia. Endocrinology 107:1975-1979
70. Schmidt ED, Binnekade R, Jansze, AAJW, Tilders FJH 1996 Short stressor induced long-lasting increases of vasopressin stores in hypothalamic corticotropin-releasing hormone (CRH) neurons in adult rats. J Neuroendocrinol 8:703-712
71. Ma XM, Lightman SL, Aguilera G 1999 Vasopressin and corticotropin-releasing hormone gene responses to novel stress in rats adapted to repeated restraint. Endocrinology 140:3623-3632