Proinflammatory cytokines upregulate sympathoexcitatory mechanisms in the subfornical organ of the rat

Hypertension

Volumn 65, Issue 5, 2015, Pages 1126-1133

  Wei, Shun Guang ^a   Yu, Yang ^a   Zhang, Zhi Hua ^a   Felder, Robert B ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

cyclooxygenase 2; cytokine receptors; paraventricular nucleus; sympathetic nervous system

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; CAPTOPRIL; CYCLOOXYGENASE 2; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; LOSARTAN; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PROSTAGLANDIN E2; PROTEIN P55; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; URETHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; EXCITATION; HEART RATE; HYPOTHALAMUS; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MALE; MEAN ARTERIAL PRESSURE; MICROINJECTION; NEUROTRANSMISSION; NONHUMAN; PARASYMPATHETIC FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; SUBFORNICAL ORGAN; SYMPATHETIC NERVE; SYMPATHOEXCITATORY MECHANISM; UPREGULATION; ADRENERGIC SYSTEM; ANIMAL; DISEASE MODEL; DRUG EFFECTS; FOLLOW UP; HEMODYNAMICS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; INFLAMMATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSCRIPTION INITIATION;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; FOLLOW-UP STUDIES; HEMODYNAMICS; INFLAMMATION; MALE; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; SUBFORNICAL ORGAN; SYMPATHETIC NERVOUS SYSTEM; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84937500876     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.114.05112     Document Type: Article

References (38)

1. Aukrust P, Ueland T, Müller F, Andreassen AK, Nordøy I, Aas H, Kjekshus J, Simonsen S, Frøland SS, Gullestad L. Elevated circulating levels of C-C chemokines in patients with congestive heart failure. Circulation. 1998; 97: 1136-1143
2. Skultetyova D, Filipova S, Desser L, Liska B, Riecansky I. Cytokine levels in patients with hypertension. J Hypertens. 2002; 20: S266-S266
3. Lisman KA, Stetson SJ, Koerner MM, Farmer JA, Torre-Amione G. The role of inflammation in the pathogenesis of heart failure. Curr Cardiol Rep. 2002; 4: 200-205
4. Guggilam A, Cardinale JP, Mariappan N, Sriramula S, Haque M, Francis J. Central TNF inhibition results in attenuated neurohumoral excitation in heart failure: a role for superoxide and nitric oxide. Basic Res Cardiol. 2011; 106: 273-286. doi: 10.1007/s00395-010-0146-8
5. Shi P, Diez-Freire C, Jun JY, Qi Y, Katovich MJ, Li Q, Sriramula S, Francis J, Sumners C, Raizada MK. Brain microglial cytokines in neurogenic hypertension. Hypertension. 2010; 56: 297-303. doi: 10.1161/HYPERTENSIONAHA.110.150409
6. Wei SG, Zhang ZH, Beltz TG, Yu Y, Johnson AK, Felder RB. Subfornical organ mediates sympathetic and hemodynamic responses to bloodborne proinflammatory cytokines. Hypertension. 2013; 62: 118-125. doi: 10.1161/HYPERTENSIONAHA.113.01404
7. Lippoldt A, Bunnemann B, Iwai N, Metzger R, Inagami T, Fuxe K, Ganten D. Cellular localization of angiotensin type 1 receptor and angiotensinogen mRNAs in the subfornical organ of the rat brain. Neurosci Lett. 1993; 150: 153-158
8. Saavedra JM, Chevillard C. Angiotensin-converting enzyme is present in the subfornical organ and other circumventricular organs of the rat. Neurosci Lett. 1982; 29: 123-127
9. Ferguson AV, Bains JS. Actions of angiotensin in the subfornical organ and area postrema: implications for long term control of autonomic output. Clin Exp Pharmacol Physiol. 1997; 24: 96-101
10. Ferguson AV, Renaud LP. Systemic angiotensin acts at subfornical organ to facilitate activity of neurohypophysial neurons. Am J Physiol Regul Integr Comp Physiol. 1986; 251: R712-R717
11. Llewellyn TL, Sharma NM, Zheng H, Patel KP. Effects of exercise training on SFO-mediated sympathoexcitation during chronic heart failure. Am J Physiol Heart Circ Physiol. 2014; 306: H121-H131. doi: 10.1152/ajpheart.00534.2013
12. Osborn JW, Hendel MD, Collister JP, Ariza-Guzman PA, Fink GD. The role of the subfornical organ in angiotensin II-salt hypertension in the rat. Exp Physiol. 2012; 97: 80-88. doi: 10.1113/expphysiol.2011.060491
13. Sriramula S, Cardinale JP, Francis J. Inhibition of TNF in the brain reverses alterations in RAS components and attenuates angiotensin II-induced hypertension. PLoS One. 2013; 8: e63847. doi: 10.1371/journal. pone.0063847
14. Kang YM, Zhang ZH, Xue B, Weiss RM, Felder RB. Inhibition of brain proinflammatory cytokine synthesis reduces hypothalamic excitation in rats with ischemia-induced heart failure. Am J Physiol Heart Circ Physiol. 2008; 295: H227-H236. doi: 10.1152/ajpheart.01157.2007
15. Simmons DL, Botting RM, Hla T. Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev. 2004; 56: 387-437. doi: 10.1124/pr.56.3.3
16. Summy-Long JY, Hu S. Peripheral osmotic stimulation inhibits the brain's innate immune response to microdialysis of acidic perfusion fluid adjacent to supraoptic nucleus. Am J Physiol Regul Integr Comp Physiol. 2009; 297: R1532-R1545. doi: 10.1152/ajpregu.00340.2009
17. Tabarean IV, Behrens MM, Bartfai T, Korn H. Prostaglandin E2-increased thermosensitivity of anterior hypothalamic neurons is associated with depressed inhibition. Proc Natl Acad Sci U S A. 2004; 101: 2590-2595
18. Cao X, Peterson JR, Wang G, Anrather J, Young CN, Guruju MR, Burmeister MA, Iadecola C, Davisson RL. Angiotensin II-dependent hypertension requires cyclooxygenase 1-derived prostaglandin E2 and EP1 receptor signaling in the subfornical organ of the brain. Hypertension. 2012; 59: 869-876. doi: 10.1161/HYPERTENSIONAHA.111.182071
19. Yu Y, Zhang ZH, Wei SG, Serrats J, Weiss RM, Felder RB. Brain perivascular macrophages and the sympathetic response to inflammation in rats after myocardial infarction. Hypertension. 2010; 55: 652-659. doi: 10.1161/HYPERTENSIONAHA.109.142836
20. Li Z, Ferguson AV. Subfornical organ efferents to paraventricular nucleus utilize angiotensin as a neurotransmitter. Am J Physiol Regul Integr Comp Physiol. 1993; 265: R302-R309
21. Dampney RA, Horiuchi J, Killinger S, Sheriff MJ, Tan PS, McDowall LM. Long-Term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions. Clin Exp Pharmacol Physiol. 2005; 32: 419-425. doi: 10.1111/j.1440-1681.2005.04205.x.
22. Patel KP. Role of paraventricular nucleus in mediating sympathetic outflow in heart failure. Heart Fail Rev. 2000; 5: 73-86. doi: 10.1023/A: 1009850224802
23. Zhang ZH, Wei SG, Francis J, Felder RB. Cardiovascular and renal sympathetic activation by blood-borne TNF-Alpha in rat: the role of central prostaglandins. Am J Physiol Regul Integr Comp Physiol. 2003; 284: R916-R927. doi: 10.1152/ajpregu.00406.2002
24. Kang YM, Ma Y, Elks C, Zheng JP, Yang ZM, Francis J. Cross-Talk between cytokines and renin-Angiotensin in hypothalamic paraventricular nucleus in heart failure: role of nuclear factor-kappaB. Cardiovasc Res. 2008; 79: 671-678. doi: 10.1093/cvr/cvn119
25. Zhang W, Huang BS, Leenen FH. Brain renin-Angiotensin system and sympathetic hyperactivity in rats after myocardial infarction. Am J Physiol Heart Circ Physiol. 1999; 276: H1608-H1615
26. Osborn JW, Fink GD, Sved AF, Toney GM, Raizada MK. Circulating angiotensin II and dietary salt: converging signals for neurogenic hypertension. Curr Hypertens Rep. 2007; 9: 228-235
27. Cheung WJ, Kent MA, El-Shahat E, Wang H, Tan J, White R, Leenen FH. Central and peripheral renin-Angiotensin systems in ouabain-induced hypertension. Am J Physiol Heart Circ Physiol. 2006; 291: H624-H630. doi: 10.1152/ajpheart.01148.2005
28. Wei SG, Yu Y, Zhang ZH, Felder RB. Angiotensin II upregulates hypothalamic AT1 receptor expression in rats via the mitogen-Activated protein kinase pathway. Am J Physiol Heart Circ Physiol. 2009; 296: H1425-H1433. doi: 10.1152/ajpheart.00942.2008
29. Blank T, Nijholt I, Grammatopoulos DK, Randeva HS, Hillhouse EW, Spiess J. Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: role in neuronal excitability and associative learning. J Neurosci. 2003; 23: 700-707
30. Gomes P, Soares-da-Silva P. Role of cAMP-PKA-PLC signaling cascade on dopamine-induced PKC-mediated inhibition of renal Na(+)-K(+)- ATPase activity. Am J Physiol Renal Physiol. 2002; 282: F1084-F1096. doi: 10.1152/ajprenal.00318.2001
31. Hsiao HY, Mak OT, Yang CS, Liu YP, Fang KM, Tzeng SF. TNFalpha/IFN-gamma-induced iNOS expression increased by prostaglandin E2 in rat primary astrocytes via EP2-evoked cAMP/PKA and intracellular calcium signaling. Glia. 2007; 55: 214-223. doi: 10.1002/glia.20453
32. Wei SG, Yu Y, Zhang ZH, Weiss RM, Felder RB. Angiotensin II-Triggered p44/42 mitogen-Activated protein kinase mediates sympathetic excitation in heart failure rats. Hypertension. 2008; 52: 342-350. doi: 10.1161/HYPERTENSIONAHA.108.110445
33. Adams JP, Anderson AE, Varga AW, Dineley KT, Cook RG, Pfaffinger PJ, Sweatt JD. The A-Type potassium channel Kv4.2 is a substrate for the mitogen- activated protein kinase ERK. J Neurochem. 2000; 75: 2277-2287
34. Sonner PM, Stern JE. Functional role of A-Type potassium currents in rat presympathetic PVN neurones. J Physiol. 2007; 582(Pt 3): 1219-1238. doi: 10.1113/jphysiol.2007.134379
35. Han P, Whelan PJ. Tumor necrosis factor alpha enhances glutamatergic transmission onto spinal motoneurons. J Neurotrauma. 2010; 27: 287-292. doi: 10.1089/neu.2009.1016
36. Olmos G, Lladó J. Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity. Mediators Inflamm. 2014; 2014: 861231. doi: 10.1155/2014/861231
37. Denis RG, Arruda AP, Romanatto T, Milanski M, Coope A, Solon C, Razolli DS, Velloso LA. TNF-A transiently induces endoplasmic reticulum stress and an incomplete unfolded protein response in the hypothalamus. Neuroscience. 2010; 170: 1035-1044. doi: 10.1016/j.neuroscience.2010.08.013
38. Young CN, Cao X, Guruju MR, Pierce JP, Morgan DA, Wang G, Iadecola C, Mark AL, Davisson RL. ER stress in the brain subfornical organ mediates angiotensin-dependent hypertension. J Clin Invest. 2012; 122: 3960-3964. doi: 10.1172/JCI64583