Stanniocalcin-1 in the subfornical organ inhibits the dipsogenic response to angiotensin II

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 303, Issue 9, 2012, Pages

  Moreau, Jason M ^a   Iqbal, Waseem ^a   Turner, Jeffrey K ^a   Wagner, Graham F ^a   Ciriello, John ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

Body fluid homeostasis; Calciumregulating glycoprotein; Circumventricular organs; Thirst

Indexed keywords

ANGIOTENSIN II; GLYCOPROTEIN; MESSENGER RNA; STANNIOCALCIN 1; UNCLASSIFIED DRUG; HYPOCALCIN;

ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; CONTROLLED STUDY; FLUID INTAKE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ASSAY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUBFORNICAL ORGAN; THIRST; WESTERN BLOTTING; ANIMAL; ANIMAL MODEL; CYTOLOGY; DRINKING; DRUG EFFECT; ELECTROLYTE BALANCE; HOMEOSTASIS; MICROINJECTION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; ANIMAL CELL; BODY FLUID; CEREBELLUM CORTEX; INHIBITION KINETICS; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS;

ANGIOTENSIN II; ANIMALS; DRINKING; GLYCOPROTEINS; HOMEOSTASIS; MALE; MICROINJECTIONS; MODELS, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; SUBFORNICAL ORGAN; WATER-ELECTROLYTE BALANCE;

EID: 84868346030     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00057.2012     Document Type: Article

References (70)

1. Anderson JW, Washburn DL, Ferguson AV. Intrinsic osmosensitivity of subfornical organ neurons. Neuroscience 100: 539-547, 2000.
2. Anthes N, Schmid HA, Hashimoto M, Riediger T, Simon E. Heterogeneous actions of vasopressin on ANG II-sensitive neurons in the subfornical organ of rats. Am J Physiol Regul Integr Comp Physiol 273: R2105-R2111, 1997.
3. Antunes-Rodrigues J, de Castro M, Elias LL, Valença MM, McCann SM. Neuroendocrine control of body fluid metabolism. Physiol Rev 84: 169-208, 2004.
4. Araujo M, Carreira BP, Pereira T, Santos PF, Soulet D, Inacio A, Bahr BA, Carvalho AP, Ambrosio AF, Carvalho CM. Changes in calcium dynamics following the reversal of the sodium-calcium exchanger have a key role in AMPA receptor-mediated neurodegeneration via calpain activation in hippocampal neurons. Cell Death Diff 14: 1635-1646, 2007.
5. Bai D, Renaud LP. ANG II AT1 receptors induce depolarization and inward current in rat median preoptic neurons in vitro. Am J Physiol Regul Integr Comp Physiol 275: R632-R639, 1998.
6. Ciriello J, Oiamo TH, Moreau JM, Turner JK, Wagner GF. Effects of the calcium-regulating glycoprotein hormone stanniocalcin-1 within the nucleus of the solitary tract on arterial pressure and the baroreceptor reflex. Neuroscience 207: 88-102, 2012.
7. Cottrell GT, Ferguson AV. Sensory circumventricular organs: central roles in integrated autonomic regulation. Regul Pept 117: 11-23, 2004.
8. De Niu P, Radman DP, Jaworski EM, Deol H, Gentz R, Su J, Olsen HS, Wagner GF. Development of a human stanniocalcin radioimmunoassay: serum and tissue hormone levels and pharmacokinetics in the rat. Mol Cell Endocrinol 162: 131-144, 2000.
9. Deol H, Stasko SE, De Niu P, James KA, Wagner GF. Post-natal ontogeny of stanniocalcin gene expression in rodent kidney and regulation by dietary calcium and phosphate. Kidney Int 60: 2142-2152, 2001.
10. Ellard JP, McCudden CR, Tanega C, James KA, Ratkovic S, Staples JF, Wagner GF. The respiratory effects of stanniocalcin-1 (STC-1) on intact mitochondria and cells: STC-1 uncouples oxidative phosphorylation and its actions are modulated by nucleotide triphosphates. Mol Cell Endocrinol 264: 90-101, 2007.
11. Fenwick JC. The corpuscles of stannous and calcium regulation in the North American eel (Anguilla rostrata LeSueur). Gen Comp Endocrinol 23: 127-135, 1974.
12. Ferguson AV, Wall KM. Central actions of angiotensin in cardiovascular control: multiple roles for a single peptide. Can J Physiol Pharmacol 70: 779-785, 1992.
13. Fitzsimons JT. Angiotensin, thirst, and sodium appetite. Physiol Rev 78: 583-686, 1998.
14. Fontaine M. Stannius' corpuscles and ionic [Ca, K, Na] of the interior environment of the eel (Anguilla Anguilla L.). C R Hebd Seances Acad Sci 259: 875-879, 1964.
15. Fry M, Ferguson AV. The sensory circumventricular organs: brain targets for circulating signals controlling ingestive behavior. Physiol Behav 91: 413-423, 2007.
16. 2+ channels. Antioxid Redox Signal 10: 31-42, 2008.
17. Gebke E, Muller AR, Jurzak M, Gerstberger R. Angiotensin II-induced calcium signalling in neurons and astrocytes of rat circumventricular organs. Neuroscience 85: 509-520, 1998.
18. Gerritsen ME, Wagner GF. Stanniocalcin: no longer just a fish tale. Vitam Horm 70: 105-135, 2005.
19. Gross PM, Weindl A. Peering through the windows of the brain. J Cereb Blood Flow Metab 7: 663-672, 1987.
20. Gutman MB, Ciriello J, Mogenson GJ. Effects of plasma angiotensin II and hypernatremia on subfornical organ neurons. Am J Physiol Regul Integr Comp Physiol 254: R746-R754, 1988.
21. Haddad M, Roder S, Olsen HS, Wagner GF. Immunocytochemical localization of stanniocalcin cells in the rat kidney. Endocrinology 137: 2113-2117, 1996.
22. Healy DP, Printz MP. Autoradiographic localization of angiotensin II binding sites I the brain, pituitary, kidney and adrenal gland of the rat. J Hypertens Suppl 2: S57-S61, 1984.
23. Heck N, Golbs A, Riedemann T, Sun JJ, Lessmann V, Luhmann HJ. Activity-dependent regulation of neuronal apoptosis in neonatal mouse cerebral cortex. Cereb Cortex 18: 1335-1349, 2008.
24. Ishibashi K, Imai M. Prospect of a stanniocalcin endocrine/paracrine system in mammals. Am J Physiol Renal Physiol 282: F367-F375, 2002.
25. Johnson AK. The periventricular anteroventral third ventricle (AV3V): its relationship with the subfornical organ and neural systems involved in maintaining body fluid homeostasis. Brain Res Bull 15: 595-601, 1985.
26. 2+ in subfornical organ cells projecting to the supraoptic nucleus. Am J Physiol Regul Integr Comp Physiol 280: R1592-R1599, 2001.
27. 2+ transients in cells cultured from rat circumventricular organs. Brain Res 673: 349-355, 1995.
28. Jurzak M, Müller AR, Schmid HA, Gerstberger R. Primary culture of circumventricular organs from the rat brain lamina terminalis. Brain Res 662: 198-208, 1994.
29. Kaneko T, Hasegawa S, Hirano T. Embryonic origin and development of the corpuscles of Stannius in chum salmon (Onchorhynchus keta). Cell Tissue Res 268: 65-70, 1992.
30. 2+ overload and cell hypercontracture in cardiomyocytes. Circ J 71: 796-801, 2007.
31. Krause EG, Melhorn SJ, Davis JF, Scott KA, Ma LY, de Kloet AD, Benoit SC, Woods SC, Sakai RR. Angiotensin type 1 receptors in the subfornical organ mediate the drinking and hypothalamic-pituitary-adrenal response to systemic isoproterenol. Endocrinology 149: 6416-6424, 2008.
32. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
33. Leng G. Rat supraoptic neurones: the effects of locally applied hypertonic saline. J Physiol 304: 405-414, 1980.
34. Luo CW, Kawamura K, Klein C, Hsueh AJ. Paracrine regulation of ovarian granulosa cell differentiation by stanniocalcin (STC) 1: mediation through specific STC-1 receptors. Mol Endocrinol 18: 2085-2096, 2004.
35. McCudden CR, James KA, Hasilo C, Wagner GF. Characterization of mammalian stanniocalcin receptors. Mitochondrial targeting of ligand and receptor for regulation of cellular metabolism. J Biol Chem 277: 45249-45258, 2002.
36. McKinley MJ, Allen AM, Burns P, Colvill LM, Oldfield BJ. Interaction of circulating hormones with the brain: the roles of the subfornical organ and the organum vasculosum of the lamina terminalis. Clin Exp Pharmacol Physiol Suppl 25: S61-S67, 1998.
37. McKinley MJ, Allen AM, May CN, McAllen RM, Oldfield BJ, Sly D, Mendelsohn FA. Neural pathways from the lamina terminalis influencing cardiovascular and body fluid homeostasis. Clin Exp Pharmacol Physiol 28: 990-992, 2001.
38. Mendelsohn FA, Quirion R, Saavedra JM, Aguilera G, Catt KJ. Autoradiographic localization of angiotensin II receptors in rat brain. Proc Natl Acad Sci USA 81: 1575-1579, 1984.
39. Morris CE, Sigurdson WJ. Stretch-inactivated ion channels coexist with stretch-activated ion channels. Science 243: 807-809, 1989.
40. Oliet SH, Bourque CW. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 364: 341-343, 1993.
41. Olsen HS, Cepeda MA, Zhang QQ, Rosen CA, Vozzolo BL, Wagner GF. Human stanniocalcin: a possible hormonal regulator of mineral metabolism. Proc Natl Acad Sci USA 93: 1792-1796, 1996.
42. Paciga M, McCudden CR, Londos C, DiMattia GE, Wagner GF. Targeting of big stanniocalcin and its receptor to lipid storage droplets of ovarian steroidogenic cells. J Biol Chem 278: 49549-49554, 2003.
43. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd ed. New York: Academic Press, 1986.
44. Phillips MI, Shen L, Richards EM, Raizada MK. Immunohistochemical mapping of angiotensin AT1 receptors in the brain. Regul Pept 44: 95-107, 1993.
45. Ratkovic S, Wagner GF, Ciriello J. Distribution of stanniocalcin binding sites in the lamina terminalis of the rat. Brain Res 1218: 141-150, 2008.
46. Robertson A, Kucharczyk J, Mogenson GJ. Drinking behaviour following electrical stimulation of the subfornical organ in the rat. Brain Res 274: 197-200, 1983.
47. Rowe BP, Saylor DL, Speth RC. Analysis of angiotensin II receptor subtypes in individual rat brain nuclei. Neuroendocrinology 55: 563-573, 1992.
48. Saad WA, Camargo LA, Guarda IF, Santos TA. Subfornical organ mediates pressor effect of angiotensin: Influence of nitric oxide synthase inhibitors, AT(1) and AT(2) angiotensin antagonist's receptors. J Am Soc Hypertens 2: 326-331, 2008.
49. Sazonova O, James KA, McCudden CR, Segal D, Talebian A, Wagner GF. Stanniocalcin-1 secretion and receptor regulation in kidney cells. Am J Physiol Renal Physiol 294: F788-F794, 2008.
50. Serlachiusa M, Zhang MK, Andersson LC. Stanniocalcin in terminally differentiated mammalian cells. Peptides 25 1657-1662, 2004.
51. Sheikh-Hamad D, Bick R, Wu GY, Christensen BM, Razeghi P, Poindexter B, Taegtmeyer H, Wamsley A, Padda R, Entman M, Nielsen S, Youker K. Stanniocalcin-1 is a naturally occurring L-channel inhibitor in cardiomyocytes: relevance to human heart failure. Am J Physiol Heart Circ Physiol 285: H442-H448, 2003.
52. Sheikh-Hamad D, Rouse D, Yang Y. Regulation of stanniocalcin in MDCK cells by hypertonicity and extracellular calcium. Am J Physiol Renal Physiol 278: F417-F424, 2000.
53. Simpson JB, Epstein AN, Camardo JS. Localization of receptors for the dipsogenic action of angiotensin II in the subfornical organ of the rat. J Comp Physiol Psychol 92: 561-608, 1978.
54. Simpson JB, Routtenberg A. Subfornical organ: site of drinking elicitation by angiotensin II. Science 181: 1172-1175, 1973.
55. Smith PM, Rozanski G, Ferguson AV. Acute electrical stimulation of the subfornical organ induces feeding in satiated rats. Physiol Behav 99: 534-537, 2010.
56. Song K, Allen AM, Paxinos G, Mendelsohn FA. Angiotensin II receptor subtypes in rat brain. Clin Exp Pharmacol Physiol 18: 93-96, 1991.
57. Turner J, Sazonova O, Wang H, Pozzi A, Wagner GF. Induction of the renal stanniocalcin-1 gene in rodents by water deprivation. Mol Cell Endocrinol 328: 8-15, 2010.
58. Turner J, Xiang FL, Feng Q, Wagner GF. The renal stanniocalcin-1 gene is differentially regulated by hypertonicity and hypovolemia in the rat. Mol Cell Endocrinol 331: 150-157, 2011.
59. Varghese R, Wong CK, Deol H, Wagner GF, DiMattia GE. Comparative analysis of mammalian stanniocalcin genes. Endocrinology 139: 4714-4725, 1998.
60. Verney EB. The antidiuretic hormone and factors which determine its release. Proc R Soc Lond B Biol Sci 135: 25-106, 1947.
61. von Boguslawsky K. Immunohistochemical detection of progesterone receptors in paraffin sections. A novel method using microwave oven pretreatment. APMIS 102: 641-646, 1994.
62. Wagner GF. The molecular biology of the corpuscles of stannius and regulation of stanniocalcin gene expression. Mol Endocrinol Fish 13: 273-306, 1994.
63. Wagner GF, Dimattia GE. The stanniocalcin family of proteins. J Exp Zool A Comp Exp Biol 305: 769-780, 2006.
64. Wagner GF, Guiraudon CC, Milliken C, Copp DH. Immunological and biological evidence for stanniocalcin-like hormone in human kidney. Proc Natl Acad Sci USA 92: 1871-1875, 1995.
65. Wagner GF, Hampong M, Park CM, Copp DH. Purification, characterization, and bioassay of teleocalcin, a glycoprotein from salmon corpuscles of Stannius. Gen Comp Endocrinol 63: 481-491, 1986.
66. Washburn DL, Ferguson AV. Selective potentiation of N-type calcium channels by angiotensin II in rat subfornical organ neurones. J Physiol 536: 667-675, 2001.
67. Wong CK, Ho MA, Wagner GF. The co-localization of stanniocalcin protein, mRNA and kidney cell markers in the rat kidney. J Endocrinol 158: 183-189, 1998.
68. Wong CK, Yeung HY, Mak NK, DiMattia GE, Chan DK, Wagner GF. Effects of dibutyryl cAMP on stanniocalcin and stanniocalcin-related protein mRNA expression in neuroblastoma cells. J Endocrinol 173: 199-209, 2002.
69. Zhang KZ, Westberg JA, Paetau A, von Boguslawsky K, Lindsberg P, Erlander M, Guo H, Su J, Olsen HS, Andersson LC. High expression of stanniocalcin in differentiated brain neurons. Am J Pathol 153: 439-445, 1998.
70. Zhang KZ, Lindsberg PJ, Tatlisumak T, Kaste M, Olsen HS, Andersson LC. Stanniocalcin: A molecular guard of neurons during cerebral ischemia. Proc Natl Acad Sci USA 97: 3637-3642, 2000.