Control of neurohypophysial hormone secretion, blood osmolalityand volume in pregnancy

Journal of Physiology and Pharmacology

Volumn 59, Issue SUPPL. 8, 2008, Pages 27-45

  Brunton, P J ^a   Arunachalam, S ^a   Russell, J A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cholecystokinin; Interleukin 1 ; Leptin; Oxytocin; Post prandial natriuresis; Vasopressin

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; 4 AMINOBUTYRIC ACID; CHOLECYSTOKININ; ENDOCANNABINOID; ESTROGEN; NATRIURETIC FACTOR; NEUROHYPOPHYSIS HORMONE; NEUROPEPTIDE Y; NITRIC OXIDE; OPIATE; OXYTOCIN; PROGESTERONE; RELAXIN; VASOPRESSIN; VASOPRESSIN DERIVATIVE;

BLOOD VOLUME; BRAIN NERVE CELL; BRAIN STEM; CONFERENCE PAPER; CORPUS LUTEUM; ESTROGEN BLOOD LEVEL; HORMONE RELEASE; HYPEROSMOTIC STRESS; HYPERVOLEMIA; HYPONATREMIA; NONHUMAN; OXYTOCIN RELEASE; PLASMA OSMOLALITY; PREGNANCY; PROGESTERONE BLOOD LEVEL; SATIETY; SODIUM RETENTION; SUPRAOPTIC NUCLEUS; THIRD TRIMESTER PREGNANCY; UPREGULATION; VASOPRESSIN RELEASE; WATER RETENTION; ANIMAL; BREEDING; FEMALE; HUMAN; METABOLISM; OSMOLARITY; RAT; REVIEW; SECRETION;

ANIMALS; ESTROGENS; FEMALE; HUMANS; HYPONATREMIA; OSMOLAR CONCENTRATION; OXYTOCIN; PREGNANCY; PREGNANCY, ANIMAL; PROGESTERONE; RATS; RELAXIN; VASOPRESSINS;

EID: 63649095226     PISSN: 08675910     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Conference Paper

References (92)

1. Brunton PJ, Russell JA. The expectant brain: adapting for motherhood. Nat Rev Neurosci 2008; 9: 11-25.
2. Atherton JC, Dark JM, Garland HO, Morgan MR, Pidgeon J, Soni S. Changes in water and electrolyte balance, plasma volume and composition during pregnancy in the rat. J Physiol 1982; 330: 81-93.
3. Barron WM, Stamoutsos BA, Lindheimer MD. Role of volume in the regulation of vasopressin secretion during pregnancy in the rat. J Clin Invest 1984; 73: 923-932.
4. Antunes-Rodrigues J, de Castro M, Elias LL, Valenca MM, McCann SM. Neuroendocrine control of body fluid metabolism. Physiol Rev 2004; 84: 169-208.
5. Brooks FP, Pickford M. The effect of posterior pituitary hormones on the excretion of electrolytes, in dogs. J Physiol 1958; 142: 468-493.
6. Verbalis JG, Mangione MP, Stricker EM. Oxytocin produces natriuresis in rats at physiological plasma concentrations. Endocrinology 1991; 128: 1317-1322.
7. Haanwinckel MA Elias LK, Favaretto AL, Gutkowska J, McCann SM, Antunes-Rodrigues J. Oxytocin mediates atrial natriuretic peptide release and natriuresis after volume expansion in the rat. Proc Natl Acad Sci USA 1995; 92: 7902-7906.
8. Villarreal D, Reams G, Freeman R, Spear R, Tchoukina I, Samar H. Leptin blockade attenuates sodium excretion in saline-loaded normotensive rats. Mol Cell Biochem 2006; 283(1-2): 153-157.
9. Leng G, Brown CH, Russell JA. Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 1999; 57: 625-655.
10. Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 2008; 9: 519-531.
11. Manning M, Stoev S, Chini B, Durroux T, Mouillac B, Guillon G. Peptide and non-peptide agonists and antagonists for the vasopressin and oxytocin V1a, V1b, V2 and OT receptors: research tools and potential therapeutic agents. Prog Brain Res 2008; 170: 473-512.
12. Renaud LP. CNS pathways mediating cardiovascular regulation of vasopressin. Clin Exp Pharmacol Physiol 1996; 23: 157-160.
13. Durr JA, Stamoutsos B, Lindheimer MD. Osmoregulation during pregnancy in the rat. Evidence for resetting of the threshold for vasopressin secretion during gestation. J Clin Invest 1981; 68: 337-346.
14. Burbach PJ, Young L, Russell JA. Oxytocin: Synthesis, secretion, and reproductive function. In: Knobil and Neill's Physiology of Reproduction, J D Neill (ed). Third Edition, San Diego, Elsevier, 2006, pp. 3055-3128.
15. Srisawat R, Ludwig M, Bull PM, Douglas AJ, Russell JA, Leng G. Nitric oxide and the oxytocin system in pregnancy. J Neurosci 2000; 20: 6721-6727.
16. Leng G, Brown CH, Bull PM, et al. Responses of magnocellular neurons to osmotic stimulation involves coactivation of excitatory and inhibitory input: an experimental and theoretical analysis. J Neurosci 2001; 21: 6967-6977.
17. Bourque CW, Ciura S, Trudel E, Stachniak TJ, Sharif-Naeini R. Neurophysiological characterization of mammalian osmosensitive neurones. Exp Physiol 2007; 92: 499-505.
18. Mukaddam-Daher S, Jankowski M, Wang D, Menaouar A, Gutkowska J. Regulation of cardiac oxytocin system and natriuretic peptide during rat gestation and postpartum. J Endocrinol 2002; 175: 211-216.
19. McCann SM, Gutkowska J, Antunes-Rodrigues J. Neuroendocrine control of body fluid homeostasis. Braz J Med Biol Res 2003; 36: 165-181.
20. Jansakul C, King RG, Boura AL, Brennecke SP, Handberg GM. Plasma levels of atrial natriuretic peptides during pregnancy and post partum in the rat. J Endocrinol 1989; 120: 113-117.
21. Nadel AS, Ballermann BJ, Anderson S, Brenner BM. Interrelationships among atrial peptides, renin, and blood volume in pregnant rats. Am J Physiol 1988; 254: R793-R800.
22. Masilamani S, Castro L, Baylis C. Pregnant rats are refractory to the natriuretic actions of atrial natriuretic peptide. Am J Physiol 1994; 267: R1611-R1616.
23. Knight S, Snellen H, Humphreys M, Baylis C. Increased renal phosphodiesterase-5 activity mediates the blunted natriuretic response to ANP in the pregnant rat. Am J Physiol Renal Physiol 2007; 292: F655-F659.
24. Randolph RR, Li Q, Curtis KS, Sullivan MJ, Cunningham JT. Fos expression following isotonic volume expansion of the unanesthetized male rat. Am J Physiol 1998; 274: R1345-R1352.
25. Godino A, Giusti-Paiva A, Antunes-Rodrigues J, Vivas L. Neurochemical brain groups activated after an isotonic blood volume expansion in rats. Neuroscience 2005; 133: 493-505.
26. Ludwig M, Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci 2006; 7: 126-136.
27. Geerling JC, Loewy AD. Central regulation of sodium appetite. Exp Physiol 2008; 93: 177-209.
28. Stricker EM, Verbalis JG. Central inhibition of salt appetite by oxytocin in rats. Regul Pept 1996; 66: 83-85.
29. Puryear R, Rigatto KV, Amico JA, Morris M. Enhanced salt intake in oxytocin deficient mice. Exp Neurol 2001; 171: 323-328.
30. Douglas AJ, Johnstone LE, Leng G. Neuroendocrine mechanisms of change in food intake during pregnancy: a potential role for brain oxytocin. Physiol Behav 2007; 91: 352-365.
31. Verbalis JG, Dohanics J. Vasopressin and oxytocin secretion in chronically hyposmolar rats. Am J Physiol 1991; 261: R1028-R1038.
32. Brimble MJ, Dyball RE. Characterization of the responses of oxytocin- and vasopressin-secreting neurones in the supraoptic nucleus to osmotic stimulation. J Physiol 1977; 271: 253-271.
33. Johnson AK, Buggy J. Periventricular preoptic-hypothalamus is vital for thirst and normal water economy. Am J Physiol 1978; 234: R122-R129.
34. Gruber KA, Wilkin LD, Johnson AK. Neurohypophyseal hormone release and biosynthesis in rats with lesions of the anteroventral third ventricle (AV3V) region. Brain Res 1986; 378: 115-119.
35. Leng G, Blackburn RE, Dyball REJ, Russell JA. Role of anterior peri-third ventricular structures in the regulation of supraoptic neuronal activity and neurohypophysial hormone secretion in the rat. J Neuroendocrinol 1989; 1: 35-46.
36. McKinley MJ, Mathai ML, McAllen RM, et al. Vasopressin secretion: osmotic and hormonal regulation by the lamina terminalis. J Neuroendocrinol 2004; 16: 340-347.
37. Geddes BJ, Parry LJ, Summerlee AJ. Brain angiotensin-II partially mediates the effects of relaxin on vasopressin and oxytocin release in anesthetized rats. Endocrinology 1994; 134: 1188-1192.
38. Chriguer RS, Antunes-Rodrigues J, Franci CR. Atrial natriuretic peptide mediates oxytocin secretion induced by osmotic stimulus. Brain Res Bull 2003; 59: 505-511.
39. Fitzsimons JT. Angiotensin, thirst, and sodium appetite. Physiol Rev 1998; 78: 583-686.
40. Sunn N, Egli M, Burazin TC, et al. Circulating relaxin acts on subfornical organ neurons to stimulate water drinking in the rat. Proc Natl Acad Sci USA 2002; 99: 1701-1706.
41. Egan G, Silk T, Zamarripa F, et al. Neural correlates of the emergence of consciousness of thirst. Proc Natl Acad Sci USA 2003; 100: 15241-15246.
42. Antunes-Rodrigues J, Ramalho MJ, Reis LC, et al. Lesions of the hypothalamus and pituitary inhibit volume-expansion-induced release of atrial natriuretic peptide. Proc Natl Acad Sci USA 1991; 88: 2956-2960.
43. Jankowski M, Marcinkiewicz M, Bouanga JC, Gutkowska J. Changes of atrial natriuretic peptide in rat supraoptic neurones during pregnancy. J Neuroendocrinol 2004; 16: 441-449.
44. Cunningham JT, Bruno SB, Grindstaff RR, et al. Cardiovascular regulation of supraoptic vasopressin neurons. Prog Brain Res 2002; 139: 257-273.
45. McCann MJ, Verbalis JG, Stricker EM. LiCl and CCK inhibit gastric emptying and feeding and stimulate OT secretion in rats. Am J Physiol 1989; 256: R463-R468.
46. Buller KM, Day TA. Involvement of medullary catecholamine cells in neuroendocrine responses to systemic cholecystokinin. J Neuroendocrinol 1996; 8: 819-824.
47. Brunton PJ, Meddle SL, Ma S, Ochedalski T, Douglas AJ, Russell JA. Endogenous opioids and attenuated hypothalamic-pituitary-adrenal axis responses to immune challenge in pregnant rats. J Neurosci 2005; 25: 5117-5126.
48. Bull PM, Douglas AJ, Russell JA. Opioids and coupling of the anterior peri-third ventricular input to oxytocin neurones in anaesthetized pregnant rats. J Neuroendocrinol 1994; 6: 267-274.
49. Koehler EM, McLemore GL, Martel JK, Summy-Long JY. Response of the magnocellular system in rats to hypovolemia and cholecystokinin during pregnancy and lactation. Am J Physiol 1994; 266: R1327-R1337.
50. Douglas AJ, Dye S, Leng G, Russell JA, Bicknell RJ. Endogenous opioid regulation of oxytocin secretion through pregnancy in the rat. J Neuroendocrinol 1993; 5: 307-314.
51. Russell JA, Douglas AJ, Bull PM, Pumford KM, Bicknell RJ, Leng G. Pregnancy and opioid interactions with the anterior perithird ventricular input to magnocellular oxytocin neurones. Prog Brain Res 1992; 91: 41-53.
52. Douglas AJ, Neumann I, Meeren HK, et al. Central endogenous opioid inhibition of supraoptic oxytocin neurons in pregnant rats. J Neurosci 1995; 15: 5049-5057.
53. Brunton PJ, Sabatier N, Leng G, Russell JA. Suppressed oxytocin neuron responses to immune challenge in late pregnant rats: a role for endogenous opioids. Eur J Neurosci 2006; 23: 1241-1247.
54. Brunton PJ, Russell JA. Keeping oxytocin neurons under control during stress in pregnancy. Prog Brain Res 2008; 170: 365-377.
55. Russell JA, Leng G, Douglas AJ. The magnocellular oxytocin system, the fount of maternity: adaptations in pregnancy. Front Neuroendocrinol 2003; 24: 27-61.
56. Di S, Malcher-Lopes R, Marcheselli VL, Bazan NG, Tasker JG. Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology 2005; 146: 4292-4301.
57. Sabatier N, Leng G. Presynaptic actions of endocannabinoids mediate alpha-MSH-induced inhibition of oxytocin cells. Am J Physiol Regul Integr Comp Physiol 2006; 290: R577-R584.
58. Koksma JJ, van Kesteren RE, Rosahl TW, et al. Oxytocin regulates neurosteroid modulation of GABA(A) receptors in supraoptic nucleus around parturition. J Neurosci 2003; 23: 788-797.
59. Concas A, Mostallino MC, Porcu P, et al. Role of brain allopregnanolone in the plasticity of gamma-aminobutyric acid type Areceptor in rat brain during pregnancy and after delivery. Proc Natl Acad Sci USA 1998; 95: 13284-13289.
60. Voisin DL, Simonian SX, Herbison AE. Identification of estrogen receptor-containing neurons projecting to the rat supraoptic nucleus. Neuroscience 1997; 78: 215-228.
61. Somponpun SJ, Holmes MC, Seckl JR, Russell JA. Modulation of oestrogen receptor-beta mRNA expression in rat paraventricular and supraoptic nucleus neurones following adrenal steroid manipulation and hyperosmotic stimulation. J Neuroendocrinol 2004; 16: 472-482.
62. Sladek CD, Somponpun SJ. Estrogen receptors: their roles in regulation of vasopressin release for maintenance of fluid and electrolyte homeostasis. Front Neuroendocrinol 2008; 29: 114-127.
63. Somponpun SJ, Johnson AK, Beltz T, Sladek CD. Estrogen receptor-alpha expression in osmosensitive elements of the lamina terminalis: regulation by hypertonicity. Am J Physiol Regul Integr Comp Physiol 2004b; 287: R661-R669.
64. Brailoiu E, Dun SL, Brailoiu GC, et al. Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 2007; 193: 311-321.
65. Brown CH, Brunton PJ, Russell JA. Rapid estradiol-17beta modulation of opioid actions on the electrical and secretory activity of rat oxytocin neurons in vivo. Neurochem Res 2008; 33: 614-623.
66. Francis K Meddle SL, Bishop VR, Russell JA. Progesterone receptor expression in the pregnant and parturient rat hypothalamus and brainstem. Brain Res 2002; 927: 18-26.
67. Bull PM, Brown LA, Russell JA. Ovarian hormones and reduced osmoresponsiveness of oxytocin neurones in urethane-anaesthetized pregnant rats. J Physiol 1996; 495.P: P113-P114.
68. Douglas AJ, Johnstone H, Brunton P, Russell JA. Sex-steroid induction of endogenous opioid inhibition on oxytocin secretory responses to stress. J Neuroendocrinol 2000; 12: 343-350.
69. Barron WM, Schreiber J, Lindheimer MD. Effect of ovarian sex steroids on osmoregulation and vasopressin secretion in the rat. Am J Physiol 1986; 250: E352-E361.
70. Bathgate RA, Ivell R, Sherwood OD, Summers RJ. International Union of Pharmacology LVII: Recommendations for the Nomenclature of Receptors for Relaxin Family Peptides. Pharmacol Rev 2006; 58: 7-31.
71. Sherwood OD, Crnekovic VE, Gordon WL, Rutherford JE. Radioimmunoassay of relaxin throughout pregnancy and during parturition in the rat. Endocrinology 1980; 107: 691-698.
72. Zhao L, Roche PJ, Gunnersen JM, et al. Mice without a functional relaxin gene are unable to deliver milk to their pups. Endocrinology 1999; 140: 445-453.
73. Zhao S, Malmgren CH, Shanks RD, Sherwood OD. Monoclonal antibodies specific for rat relaxin. VIII. Passive immunization with monoclonal antibodies throughout the second half of pregnancy reduces water consumption in rats. Endocrinology 1995; 136: 1892-1897.
74. Hornsby DJ, Wilson BC, Summerlee AJ. Relaxin and drinking in pregnant rats. Prog Brain Res 2001; 133: 229-240.
75. Sinnayah P, Burns P, Wade JD, Weisinger RS, McKinley MJ. Water drinking in rats resulting from intravenous relaxin and its modification by other dipsogenic factors. Endocrinology 1999; 140: 5082-5086.
76. Thornton SN, Fitzsimons JT. The effects of centrally administered porcine relaxin on drinking behaviour in male and female rats. J Neuroendocrinol 1995; 7: 165-169.
77. Way SA, Leng G. Relaxin increases the firing rate of supraoptic neurones and increases oxytocin secretion in the rat. J Endocrinol 1992; 132: 149-158.
78. Parry LJ, Poterski RS, Summerlee AJ. Effects of relaxin on blood pressure and the release of vasopressin and oxytocin in anesthetized rats during pregnancy and lactation. Biol Reprod 1994; 50: 622-628.
79. Summerlee AJ, Hornsby DJ, Ramsey DG. The dipsogenic effects of rat relaxin: The effect of photoperiod and the potential role of relaxin on drinking in pregnancy. Endocrinology 1998; 139: 2322-2328.
80. Silvertown JD, Fraser R, Poterski RS, Geddes B, Summerlee AJ. Central effects of long-term relaxin expression in the rat. Ann N Y Acad Sci 2005; 1041: 216-222.
81. Weisinger RS, Burns P, Eddie LW, Wintour EM. Relaxin alters the plasma osmolality-arginine vasopressin relationship in the rat. J Endocrinol 1993; 137: 505-510.
82. Osheroff PL, Phillips HS. Autoradiographic localization of relaxin binding sites in rat brain. Proc Natl Acad Sci USA 1991; 88: 6413-6417.
83. 33P]-relaxin binding sites in rat brain: restricted somatic co-expression a clue to relaxin action? Neuroscience 2006; 141: 329-344.
84. Neumann I, Landgraf R, Takahashi Y, Pittman QJ, Russell JA. Stimulation of oxytocin release within the supraoptic nucleus and into blood by CCK-8. Am J Physiol 1994; 267: R1626-R1631.
85. Brunton PJ, Bales J, Russell JA. Neuroendocrine stress but not feeding responses to centrally administered neuropeptide Yare suppressed in pregnant rats. Endocrinology 2006; 147: 3737-3745.
86. Leng G, Dye S, Bicknell RJ. Kappa-opioid restraint of oxytocin secretion: plasticity through pregnancy. Neuroendocrinology 1997; 66: 378-383.
87. Wolak ML, DeJoseph MR, Cator AD, Mokashi AS, Brownfield MS, Urban JH. Comparative distribution of neuropeptide Y Y1 and Y5 receptors in the rat brain by using immunohistochemistry. J Comp Neurol 2003; 464: 285-311.
88. Ellacott KL, Halatchev IG, Cone RD. Characterization of leptin-responsive neurons in the caudal brainstem. Endocrinology 2006; 147: 3190-3195.
89. Hakansson ML, Brown H, Ghilardi N, Skoda RC, Meister B. Leptin receptor immunoreactivity in chemically defined target neurons of the hypothalamus. J Neurosci 1998; 18: 559-572.
90. Kawai M, Yamaguchi M, Murakami T, Shima K, Murata Y, Kishi K. The placenta is not the main source of leptin production in pregnant rat: gestational profile of leptin in plasma and adipose tissues. Biochem Biophys Res Commun 1997; 240: 798-802.
91. Grattan DR, Ladyman SR, Augustine RA. Hormonal induction of leptin resistance during pregnancy. Physiol Behav 2007; 91: 366-374.
92. Ladyman SR, Grattan DR. Region-specific reduction in leptin-induced phosphorylation of signal transducer and activator of transcription-3 (STAT3) in the rat hypothalamus is associated with leptin resistance during pregnancy. Endocrinology 2004; 145: 3704-3711.