A comparison of physiological and transcriptome responses to water deprivation and salt loading in the rat supraoptic nucleus

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 308, Issue 7, 2015, Pages R559-R568

  Greenwood, Michael P ^a   Mecawi, Andre S ^b,c   Hoe, See Ziau ^b   Mustafa, Mohd Rais ^b   Johnson, Kory R ^d   Al Mahmoud, Ghada A ^e   Elias, Lucila L K ^f   Paton, Julian F R ^a   Antunes Rodrigues, Jose ^f   Gainer, Harold ^d   Murphy, David ^a,b   Hindmarch, Charles C T ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF MALAYA   (Malaysia)

^c FEDERAL RURAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^e Qatar University ^*  (Qatar)

^f UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Neuroendocrine; Salt load; Supraoptic nucleus; Transcriptome; Water restriction

Indexed keywords

ARGIPRESSIN; OXYTOCIN; TRANSCRIPTOME; MESSENGER RNA; SALT INTAKE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VOLUME; BODY WEIGHT; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; DRINKING BEHAVIOR; FEEDING BEHAVIOR; FLUID INTAKE; GENE EXPRESSION; GENETIC DIFFERENCE; HORMONE RESPONSE; HYPOPHYSIS; HYPOTHALAMUS; MALE; MICROARRAY ANALYSIS; NERVE CELL PLASTICITY; NONHUMAN; PHYSIOLOGICAL PROCESS; PLASMA OSMOLALITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; SALT LOADING; SUPRAOPTIC NUCLEUS; URINE OSMOLALITY; VALIDATION PROCESS; WATER DEPRIVATION; WEIGHT REDUCTION; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; DNA MICROARRAY; DRINKING; EATING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; OSMOLARITY; OSMOREGULATION; PHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALT INTAKE; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; ARGININE VASOPRESSIN; BLOOD VOLUME; BODY WEIGHT; DRINKING; EATING; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSMOLAR CONCENTRATION; OSMOREGULATION; OXYTOCIN; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM CHLORIDE, DIETARY; SUPRAOPTIC NUCLEUS; TIME FACTORS; TRANSCRIPTOME; WATER DEPRIVATION;

EID: 84926330844     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00444.2014     Document Type: Article

References (62)

1. Abramow-Newerly M, Roy AA, Nunn C, Chidiac P. RGS proteins have a signalling complex: interactions between RGS proteins and GPCRs, effectors, and auxiliary proteins. Cell Signal 18: 579-591, 2006.
2. Adem A, Al Haj M, Benedict S, Yasin J, Nagelkerke N, Nyberg F, Yandle TG, Frampton CM, Lewis LK, Nicholls MG, Kazzam E. ANP and BNP responses to dehydration in the one-humped camel and effects of blocking the renin-angiotensin system. PLos One 8: e57806, 2013.
3. Amabebe E, Idu F, Obika LF. Relationship between thirst perception and plasma arginine vasopressin concentration in man. Niger J Physiol Sci 27: 3-10, 2012.
4. Antunes-Rodrigues J, de Castro M, Elias LL, Valenca MM, McCann SM. Neuroendocrine control of body fluid metabolism. Physiol Rev 84: 169-208, 2004.
5. Antunes-Rodrigues J, Ruginsk SG, Mecawi AS, Margatho LO, Reis WL, Ventura RR, da Silva AL, Vilhena-Franco T, Elias LLK. Frontiers in neuroscience neuroendocrinology of hydromineral homeostasis. In: Neurobiology of Body Fluid Homeostasis: Transduction and Integration, edited by De Luca LA, Menani JV, and Johnson AK. Boca Raton, FL: CRC, 2014.
6. Balment RJ, Brimble MJ, Forsling ML. Release of oxytocin induced by salt loading and its influence on renal excretion in the male rat. J Physiol 308: 439-449, 1980.
7. Barth SW, Gerstberger R. Differential regulation of angiotensinogen and AT1A receptor mRNA within the rat subfornical organ during dehydration. Brain Res Mol Brain Res 64: 151-164, 1999.
8. Boyle CN, Lorenzen SM, Compton D, Watts AG. Dehydration-anorexia derives from a reduction in meal size, but not meal number. Physiol Behav 105: 305-314, 2012.
9. Caquineau C, Douglas AJ, Leng G. Effects of cholecystokinin in the supraoptic nucleus and paraventricular nucleus are negatively modulated by leptin in 24-h fasted lean male rats. J Neuroendocrinol 22: 446-452, 2010.
10. Carter DA, Murphy D. Cyclic nucleotide dynamics in the rat hypothalamus during osmotic stimulation: in vivo and in vitro studies. Brain Res 487: 350-356, 1989.
11. Chen Y, Morris M. Differentiation of brain angiotensin type 1a and 1b receptor mRNAs: a specific effect of dehydration. Hypertension 37: 692-697, 2001.
12. da Silveira LT, Junta CM, Monesi N, de Oliveira-Pelegrin GR, Passos GA, Rocha MJ. Time course of c-fos, vasopressin and oxytocin mRNA expression in the hypothalamus following long-term dehydration. Cell Mol Neurobiol 27: 575-584, 2007.
13. De Bold AJ, Borenstein HB, Veress AT, Sonnenberg H. A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sci 28: 89-94, 1981.
14. De Luca LA Jr, Pereira-Derderian DT, Vendramini RC, David RB, Menani JV. Water deprivation-induced sodium appetite. Physiol Behav 100: 535-544, 2010.
15. Fitzsimons JT. Angiotensin, thirst, and sodium appetite. Physiol Rev 78: 583-686, 1998.
16. Furuya S. An essential role for de novo biosynthesis of L-serine in CNS development. Asia Pac J Clin Nutri 17, Suppl 1: 312-315, 2008.
17. Greenwood M, Bordieri L, Greenwood MP, Rosso Melo M, Colombari DS, Colombari E, Paton JF, Murphy D. Transcription factor CREB3L1 regulates vasopressin gene expression in the rat hypothalamus. J Neurosci 34: 3810-3820, 2014.
18. Hakansson ML, Meister B. Transcription factor STAT3 in leptin target neurons of the rat hypothalamus. Neuroendocrinology 68: 420-427, 1998.
19. Hammer M, Ladefoged J, Olgaard K. Relationship between plasma osmolality and plasma vasopressin in human subjects. Am J Physiol Endocrinol Metab 238: E313-E317, 1980.
20. Hatton GI. Function-related plasticity in hypothalamus. Annual Rev Neurosci 20: 375-397, 1997.
21. Heilig CW, Stromski ME, Blumenfeld JD, Lee JP, Gullans SR. Characterization of the major brain osmolytes that accumulate in saltloaded rats. Am J Physiol Renal Fluid Electrolyte Physiol 257: F1108-F1116, 1989.
22. Hindmarch C, Fry M, Yao ST, Smith PM, Murphy D, Ferguson AV. Microarray analysis of the transcriptome of the subfornical organ in the rat: regulation by fluid and food deprivation. Am J Physiol Regul Integr Comp Physiol 295: R1914-R1920, 2008.
23. Hindmarch C, Yao S, Beighton G, Paton J, Murphy D. A comprehensive description of the transcriptome of the hypothalamoneurohypophyseal system in euhydrated and dehydrated rats. Proc Natl Acad Sci USA 103: 1609-1614, 2006.
24. Hindmarch CC, Franses P, Goodwin B, Murphy D. Whole transcriptome organisation in the dehydrated supraoptic nucleus. Braz J Med Biol Res 46: 1000-1006, 2013.
25. Hindmarch CC, Fry M, Smith PM, Yao ST, Hazell GG, Lolait SJ, Paton JF, Ferguson AV, Murphy D. The transcriptome of the medullary area postrema: the thirsty rat, the hungry rat and the hypertensive rat. Exp Physiol 96: 495-504, 2011.
26. Hindmarch CC, Murphy D. The transcriptome and the hypothalamoneurohypophyseal system. Endocr Develop 17: 1-10, 2010.
27. Kamoi K, Sato F, Arai O, Ishibashi M, Yamaji T. Effects of plasma volume and osmolality on secretion of atrial natriuretic peptide and vasopressin in man. Acta Endocr 118: 51-58, 1988.
28. Kanzaki M, Nagasawa M, Kojima I, Sato C, Naruse K, Sokabe M, Iida H. Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285: 882-886, 1999.
29. Kawasaki M, Yamaguchi K, Saito J, Ozaki Y, Mera T, Hashimoto H, Fujihara H, Okimoto N, Ohnishi H, Nakamura T, Ueta Y. Expression of immediate early genes and vasopressin heteronuclear RNA in the paraventricular and supraoptic nuclei of rats after acute osmotic stimulus. J Neuroendocrinol 17: 227-237, 2005.
30. Kim G, Lee Y, Jeong EY, Jung S, Son H, Lee DH, Roh GS, Kang SS, Cho GJ, Choi WS, Kim HJ. Acute stress responsive RGS proteins in the mouse brain. Mol cells 30: 161-165, 2010.
31. Kurtz A. Control of renin synthesis and secretion. Am J Hypertens 25: 839-847, 2012.
32. Lightman SL, Young WS 3rd. Vasopressin, oxytocin, dynorphin, enkephalin and corticotrophin-releasing factor mRNA stimulation in the rat. J Physiol 394: 23-39, 1987.
33. Lubelski D, Ponzio TA, Gainer H. Effects of A-CREB, a dominant negative inhibitor of CREB, on the expression of c-fos and other immediate early genes in the rat SON during hyperosmotic stimulation in vivo. Brain Res 1429: 18-28, 2012.
34. Maejima Y, Sedbazar U, Suyama S, Kohno D, Onaka T, Takano E, Yoshida N, Koike M, Uchiyama Y, Fujiwara K, Yashiro T, Horvath TL, Dietrich MO, Tanaka S, Dezaki K, Oh IS, Hashimoto K, Shimizu H, Nakata M, Mori M, Yada T. Nesfatin-1-regulated oxytocinergic signaling in the paraventricular nucleus causes anorexia through a leptinindependent melanocortin pathway. Cell Metab 10: 355-365, 2009.
35. McKinley MJ, Johnson AK. The physiological regulation of thirst and fluid intake. News Physiol Sci 19: 1-6, 2004.
36. Mecawi AS, Vilhena-Franco T, Araujo IG, Reis LC, Elias LL, Antunes-Rodrigues J. Estradiol potentiates hypothalamic vasopressin and oxytocin neuron activation and hormonal secretion induced by hypovolemic shock. Am J Physiol Regul Integr Comp Physiol 301: R905-R915, 2011.
37. Mecawi AS, Vilhena-Franco T, Fonseca FV, Reis LC, Elias LL, Antunes-Rodrigues J. The role of angiotensin II on sodium appetite after a low-sodium diet. J Neuroendocrinol 25: 281-291, 2013.
38. Mohan Rao LV, Esmon CT, Pendurthi UR. Endothelial cell protein C receptor: a multiliganded and multifunctional receptor. Blood 124: 1553-1562, 2014.
39. Mutsuga N, Shahar T, Verbalis JG, Brownstein MJ, Xiang CC, Bonner RF, Gainer H. Selective gene expression in magnocellular neurons in rat supraoptic nucleus. J Neurosci 24: 7174-7185, 2004.
40. Mutsuga N, Shahar T, Verbalis JG, Xiang CC, Brownstein MJ, Gainer H. Regulation of gene expression in magnocellular neurons in rat supraoptic nucleus during sustained hypoosmolality. Endocrinology 146: 1254-1267, 2005.
41. Nedungadi TP, Dutta M, Bathina CS, Caterina MJ, Cunningham JT. Expression and distribution of TRPV2 in rat brain. Exp Neurol 237: 223-237, 2012.
42. Obika LO, Amabebe E, Ozoene JO, Inneh CA. Thirst perception, plasma osmolality and estimated plasma arginine vasopressin concentration in dehydrated and oral saline loaded subjects. Niger J Physiol Sci 28: 83-89, 2013.
43. Perello M, Raingo J. Leptin activates oxytocin neurons of the hypothalamic paraventricular nucleus in both control and diet-induced obese rodents. PLos One 8: e59625, 2013.
44. Pollock DM, Banks RO. Effect of atrial extract on renal function in the rat. Clin Sci 65: 47-55, 1983.
45. Qiu J, Hindmarch CC, Yao ST, Tasker JG, Murphy D. Transcriptomic analysis of the osmotic and reproductive remodeling of the female rat supraoptic nucleus. Endocrinology 152: 3483-3491, 2011.
46. Qiu J, Yao S, Hindmarch C, Antunes V, Paton J, Murphy D. Transcription factor expression in the hypothalamo-neurohypophyseal system of the dehydrated rat: upregulation of gonadotrophin inducible transcription factor 1 mRNA is mediated by cAMP-dependent protein kinase A. J Neurosci 27: 2196-2203, 2007.
47. Rinaman L, Vollmer RR, Karam J, Phillips D, Li X, Amico JA. Dehydration anorexia is attenuated in oxytocin-deficient mice. Am J Physiol Regul Integr Comp Physiol 288: R1791-R1799, 2005.
48. Russo MW, Sevetson BR, Milbrandt J. Identification of NAB1, a repressor of NGFI-A-and Krox20-mediated transcription. Proc Natl Acad Sci USA 92: 6873-6877, 1995.
49. Scalera G, Tarozzi G. Sapid solutions and food intake in repeated dehydration and rehydration periods in rats. Exp Physiol 86: 489-498, 2001.
50. Sharman G, Ghorbel M, Leroux M, Beaucourt S, Wong LF, Murphy D. Deciphering the mechanisms of homeostatic plasticity in the hypothalamo-neurohypophyseal system-genomic and gene transfer strategies. Prog Biophysics Molec Biol 84: 151-182, 2004.
51. Snyder SE, Salton SR. Expression of VGF mRNA in the adult rat central nervous system. J Comp Neurol 394: 91-105, 1998.
52. Song Z, Levin BE, Stevens W, Sladek CD. Supraoptic oxytocin and vasopressin neurons function as glucose and metabolic sensors. Am J Physiol Regul Integr Comp Physiol 306: R447-R456, 2014.
53. Stewart L, Hindmarch CC, Qiu J, Tung YC, Yeo GS, Murphy D. Hypothalamic transcriptome plasticity in two rodent species reveals divergent differential gene expression but conserved pathways. J Neuroendocrinol 23: 177-185, 2011.
54. Theodosis DT, El Majdoubi M, Pierre K, Poulain DA. Factors governing activity-dependent structural plasticity of the hypothalamoneurohypophysial system. Cell Mol Neurobiol 18: 285-298, 1998.
55. Torres-Peraza JF, Engel T, Martin-Ibanez R, Sanz-Rodriguez A, Fernandez-Fernandez MR, Esgleas M, Canals JM, Henshall DC, Lucas JJ. Protective neuronal induction of ATF5 in endoplasmic reticulum stress induced by status epilepticus. Brain 136: 1161-1176, 2013.
56. Toshinai K, Saito T, Yamaguchi H, Sasaki K, Tsuchimochi W, Minamino N, Ueta Y, Nakazato M. Neuroendocrine regulatory peptide-1 and-2 (NERPs) inhibit the excitability of magnocellular neurosecretory cells in the hypothalamus. Brain Res 1563: 52-60, 2014.
57. van Beek J, van Meurs M, t Hart BA, Brok HP, Neal JW, Chatagner A, Harris CL, Omidvar N, Morgan BP, Laman JD, Gasque P. Decay-accelerating factor (CD55) is expressed by neurons in response to chronic but not acute autoimmune central nervous system inflammation associated with complement activation. J Immunol 174: 2353-2365, 2005.
58. Vassiliou AG, Kotanidou A, Mastora Z, Maniatis NA, Albani P, Jahaj E, Koutsoukou A, Armaganidis A, Orfanos SE. Elevated soluble endothelial protein C receptor levels at ICU admission are associated with sepsis development. Minerva Anestesiol 81: 125-134, 2015.
59. Verbalis JG, Mangione MP, Stricker EM. Oxytocin produces natriuresis in rats at physiological plasma concentrations. Endocrinology 128: 1317-1322, 1991.
60. Wang Y, Li Y, Dalle Lucca SL, Simovic M, Tsokos GC, Dalle Lucca JJ. Decay accelerating factor (CD55) protects neuronal cells from chemical hypoxia-induced injury. J Neuroinflammation 7: 24, 2010.
61. Weiss ML, Hatton GI. Collateral input to the paraventricular and supraoptic nuclei in rat. I. Afferents from the subfornical organ and the anteroventral third ventricle region. Brain Res Bull 24: 231-238, 1990.
62. Yue C, Mutsuga N, Verbalis J, Gainer H. Microarray analysis of gene expression in the supraoptic nucleus of normoosmotic and hypoosmotic rats. Cell Mol Neurobiol 26: 959-978, 2006.