Macrophage migration inhibitory factor in the paraventricular nucleus plays a major role in the sympathoexcitatory response to salt

Hypertension

Volumn 56, Issue 5, 2010, Pages 956-963

  Colombari, Eduardo ^a,e   Colombari, Debora ^b,d   Li, Hongwei ^c   Shi, Peng ^c   Dong, Ying ^c   Jiang, Nan ^c   Raizada, Mohan K ^c   Sumners, Colin ^c   Murphy, David ^b   Paton, Julian F R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF FLORIDA   (United States)

^d SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^e FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

angiotensin type 1 receptors; gene transfer; hypothalamus; macrophage migration inhibitory factor; sympathetic nerve activity

Indexed keywords

GREEN FLUORESCENT PROTEIN; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; OXIDOREDUCTASE; SODIUM CHLORIDE; THIOL PROTEINASE; ARGIPRESSIN;

ADENO ASSOCIATED VIRUS; ADRENERGIC STIMULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXCITATION AND STIMULATION; MALE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYMPATHETIC NERVE; THALAMUS MIDLINE NUCLEUS; ADRENERGIC SYSTEM; ANIMAL; ANTERIOR HYPOTHALAMUS; DRUG EFFECT; GENE TRANSFER; IMMUNOHISTOCHEMISTRY; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WISTAR RAT;

ANIMALS; ARGININE VASOPRESSIN; GENE TRANSFER TECHNIQUES; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAVENTRICULAR; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RNA, MESSENGER; SALINE SOLUTION, HYPERTONIC; SYMPATHETIC NERVOUS SYSTEM;

EID: 78149268125     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.110.155101     Document Type: Article

References (35)

1. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci. 2006;7:335-346.
2. Toney GM, Chen QH, Cato MJ, Stocker SD. Central osmotic regulation of sympathetic nerve activity. Acta Physiol Scand. 2003;177:43-55.
3. Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci. 2008;9:519-531.
4. Johnson AK, Gross PM. Sensory circumventricular organs and brain homeostatic pathways. FASEB J. 1993;7:678-686.
5. 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. 2001;28:990-992.
6. McKinley MJ, Johnson AK. The physiological regulation of thirst and fluid intake. News Physiol Sci. 2004;19:1-6.
7. Stocker SD, Osborn JL, Carmichael SP. Forebrain osmotic regulation of the sympathetic nervous system. Clin Exp Pharmacol Physiol. 2008;35:695-700.
8. Ciura S, Bourque CW. Transient receptor potential vanilloid 1 is required for intrinsic osmoreception in organum vasculosum lamina terminalis neurons and for normal thirst responses to systemic hyperosmolality. J Neurosci. 2006;26:9069-9075.
9. Shi P, Stocker SD, Toney GM. Organum vasculosum laminae terminalis contributes to increased sympathetic nerve activity induced by central hyperosmolality. Am J Physiol Regul Integr Comp Physiol. 2007;293:R2279-R2289.
10. Shi P, Martinez MA, Calderon AS, Chen Q, Cunningham JT, Toney GM. Intra-carotid hyperosmotic stimulation increases fos staining in forebrain organum vasculosum laminae terminalis neurones that project to the hypothalamic paraventricular nucleus. J Physiol. 2008;586:5231-5245.
11. Thrasher TN, Keil LC, Ramsay DJ. Lesions of the organum vasculosum of the lamina terminalis (OVLT) attenuate osmotically-induced drinking and vasopressin secretion in the dog. Endocrinology. 1982;110:1837-1839.
12. Ho JM, Zierath DK, Savos AV, Femiano DJ, Bassett JE, McKinley MJ, Fitts DA. Differential effects of intravenous hyperosmotic solutes on drinking latency and c-fos expression in the circumventricular organs and hypothalamus of the rat. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1690-R1698.
13. McKinley MJ, Denton DA, Leksell LG, Mouw DR, Scoggins BA, Smith MH, Weisinger RS, Wright RD. Osmoregulatory thirst in sheep is disrupted by ablation of the anterior wall of the optic recess. Brain Res. 1982;236:210-215.
14. Morris M, Rocha MJ, Sim LJ, Johnson AK, Callahan MF. Dissociation between vasopressin and oxytocin mRNA and peptide secretion after AV3V lesions. Am J Physiol. 1994;267:R1640-R1645.
15. Saper CB, Levisohn D. Afferent connections of the median preoptic nucleus in the rat: anatomical evidence for a cardiovascular integrative mechanism in the anteroventral third ventricular (AV3V) region. Brain Res. 1983;288:21-31.
16. Camacho A, Phillips MI. Horseradish peroxidase study in rat of the neural connections of the organum vasculosum of the lamina terminalis. Neurosci Lett. 1981;25:201-204.
17. Stocker SD, Toney GM. Vagal afferent input alters the discharge of osmotic and ANG II-responsive median preoptic neurons projecting to the hypothalamic paraventricular nucleus. Brain Res. 2007;1131:118-128.
18. Stocker SD, Hunwick KJ, Toney GM. Hypothalamic paraventricular nucleus differentially supports lumbar and renal sympathetic outflow in water-deprived rats. J Physiol. 2005;563:249-263.
19. Antunes VR, Yao ST, Pickering AE, Murphy D, Paton JF. A spinal vasopressinergic mechanism mediates hyperosmolality-induced sympathoexcitation. J Physiol. 2006;576:569-583.
20. Chen QH, Toney GM. AT (1)-receptor blockade in the hypothalamic PVN reduces central hyperosmolality-induced renal sympathoexcitation. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1844-R1853.
21. Freeman KL, Brooks VL. AT (1) and glutamatergic receptors in paraventricular nucleus support blood pressure during water deprivation. Am J Physiol Regul Integr Comp Physiol. 2007;292:R1675-R1682.
22. Coote JH, Yang Z, Pyner S, Deering J. Control of sympathetic outflows by the hypothalamic paraventricular nucleus. Clin Exp Pharmacol Physiol. 1998;25:461-463.
23. Badoer E. Hypothalamic paraventricular nucleus and cardiovascular regulation. Clin Exp Pharmacol Physiol. 2001;28:95-99.
24. Saper CB, Loewy AD, Swanson LW, Cowan WM. Direct hypothalamoautonomic connections. Brain Res. 1976;117:305-312.
25. Yang Z, Bertram D, Coote JH. The role of glutamate and vasopressin in the excitation of RVL neurones by paraventricular neurones. Brain Res. 2001;908:99-103.
26. Stocker SD, Simmons JR, Stornetta RL, Toney GM, Guyenet PG. Water deprivation activates a glutamatergic projection from the hypothalamic paraventricular nucleus to the rostral ventrolateral medulla. J Comp Neurol. 2006;494:673-685.
27. Sun C, Li H, Leng L, Raizada MK, Bucala R, Sumners C. Macrophage migration inhibitory factor: an intracellular inhibitor of angiotensin II-induced increases in neuronal activity. J Neurosci. 2004;24:9944-9952.
28. Li H, Gao Y, Freire CD, Raizada MK, Toney GM, Sumners C. Macrophage migration inhibitory factor in the PVN attenuates the central pressor and dipsogenic actions of angiotensin II. FASEB J. 2006;20:1748-1750.
29. Li H, Gao Y, Qi Y, Katovich MJ, Jiang N, Braseth LN, Scheuer DA, Shi P, Sumners C. Macrophage migration inhibitory factor in hypothalamic paraventricular nucleus neurons decreases blood pressure in spontaneously hypertensive rats. FASEB J. 2008;22:3175-3185.
30. Paton JF. A working heart-brainstem preparation of the mouse. J Neurosci Methods. 1996;65:63-68.
31. Jiang N, Shi P, Li H, Lu S, Braseth L, Cuadra AE, Raizada MK, Sumners C. Phosphate-activated glutaminase-containing neurons in the rat paraventricular nucleus express angiotensin type 1 receptors. Hypertension. 2009;54:845-851.
32. Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Juttner S, Brunner H, Bernhagen J. Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol. 1998;280:85-102.
33. Li DP, Chen SR, Pan HL. Angiotensin II stimulates spinally projecting paraventricular neurons through presynaptic disinhibition. J Neurosci. 2003;23:5041-5049.
34. Cato MJ, Toney GM. Angiotensin II excites paraventricular nucleus neurons that innervate the rostral ventrolateral medulla: an in vitro patch-clamp study in brain slices. J Neurophysiol. 2005;93:403-413.
35. Qadri F, Edling O, Wolf A, Gohlke P, Culman J, Unger T. Release of angiotensin in the paraventricular nucleus in response to hyperosmotic stimulation in conscious rats: a microdialysis study. Brain Res. 1994;637:45-49.