Abstract
Background: This study tested the hypothesis that genetically ablation of transient receptor potential vanilloid type 1 (TRPV1) exacerbates impairment of baroreflex in mice fed a western diet (WD) and leads to distinct diurnal and nocturnal blood pressure patterns.
Methods: TRPV1 gene knockout (TRPV1-/-) and wild-type (WT) mice were given a WD or normal diet (CON) for 4 months.
Results: Capsaicin, a selective TRPV1 agonist, increased ipsilateral afferent renal nerve activity in WT but not TRPV1-/- mice. The sensitivity of renal sympathetic nerve activity and heart rate responses to baroreflex were reduced in TRPV1-/--CON and WT-WD and further decreased in TRPV1-/--WD compared to the WT-CON group. Urinary norepinephrine and serum insulin and leptin at day and night were increased in WT-WD and TRPV1-/--WD, with further elevation at night in TRPV1-/--WD. WD intake increased leptin, IL-6, and TNF-α in adipose tissue, and TNF-α antagonist III, R-7050, decreased leptin in TRPV1-/--WD. The urinary albumin level was higher in TRPV1-/--WD than WT-WD. Blood pressure was not different during daytime among all groups, but increased at night in the TRPV1-/--WD group compared with other groups.
Conclusions: TRPV1 ablation leads to elevated nocturnal but not diurnal blood pressure, which is probably attributed to further enhancement of sympathetic drives at night.
Keywords: TRPV1, western diet, afferent renal nerve activity, sympathetic nerve activity, blood pressure, TNF-α.
Graphical Abstract
[1]
Hall JE, Crook ED, Jones DW, et al. Mechanisms of obesity-associated cardiovascular and renal disease. Am J Med Sci 2002; 324: 127-37.
[2]
Alvarez GE, Beske SD, Ballard TP, et al. Sympathetic neural activation in visceral obesity. Circulation 2002; 106: 2533-6.
[3]
Tentolouris N, Liatis S, Katsilambros N. Sympathetic system activity in obesity and metabolic syndrome. Ann N Y Acad Sci 2006; 1083: 129-52.
[4]
Boustany CM, Bharadwaj K, Daugherty A, et al. Activation of the systemic and adipose renin-angiotensin system in rats with diet-induced obesity and hypertension. Am J Physiol Regul Integr Comp Physiol 2004; 287: R943-9.
[5]
Kassab S, Kato T, Wilkins FC, et al. Renal denervation attenuates the sodium retention and hypertension associated with obesity. Hypertension 1995; 25: 893-7.
[6]
Gao L, Zhu Z, Zucker IH, et al. Cardiac sympathetic afferent stimulation impairs baroreflex control of renal sympathetic nerve activity in rats. Am J Physiol Heart Circ Physiol 2004; 286: H1706-11.
[7]
Skrapari I, Tentolouris N, Perrea D, et al. Baroreflex sensitivity in obesity: relationship with cardiac autonomic nervous system activity. Obesity (Silver Spring) 2007; 15: 1685-93.
[8]
Grassi G, Seravalle G, Colombo M, et al. Body weight reduction, sympathetic nerve traffic, and arterial baroreflex in obese normotensive humans. Circulation 1998; 97: 2037-42.
[9]
Fardin NM, Oyama LM, Campos RR. Changes in baroreflex control of renal sympathetic nerve activity in high-fat-fed rats as a predictor of hypertension. Obesity (Silver Spring) 2012; 20(8): 1591-7.
[10]
Lohmeier TE, Iliescu R, Liu B, et al. Systemic and renal-specific sympathoinhibition in obesity hypertension. Hypertension 2012; 59: 331-8.
[11]
La Rovere MT, Bigger JT Jr, Marcus FI, et al. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction). Investigators Lancet 1998; 351: 478-84.
[12]
Haddock RE, Hill CE. Sympathetic overdrive in obesity involves purinergic hyperactivity in the resistance vasculature. J Physiol 2011; 589: 3289-307.
[13]
Gunthorpe MJ, Benham CD, Randall A, et al. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol Sci 2002; 23: 183-91.
[14]
Caterina MJ, Leffler A, Malmberg AB, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000; 288: 306-13.
[15]
Davis JB, Gray J, Gunthorpe MJ, et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 2000; 405: 183-7.
[16]
Sun H, Li DP, Chen SR, et al. Sensing of blood pressure increase by transient receptor potential vanilloid 1 receptors on baroreceptors. J Pharmacol Exp Ther 2009; 331: 851-9.
[17]
Wang Y, Babankova D, Huang J, et al. Deletion of transient receptor potential vanilloid type 1 receptors exaggerates renal damage in deoxycorticosterone acetate-salt hypertension. Hypertension 2008; 52: 264-70.
[18]
Xie C, Wang DH. Ablation of transient receptor potential vanilloid 1 abolishes endothelin-induced increases in afferent renal nerve activity: Mechanisms and functional significance. Hypertension 2009; 54: 1298-305.
[19]
Okamoto H, Hoka S, Kawasaki T, et al. Effects of CGRP on baroreflex control of heart rate and renal sympathetic nerve activity in rabbits. Am J Physiol 1992; 263: R874-9.
[20]
Oh-hashi Y, Shindo T, Kurihara Y, et al. Elevated sympathetic nervous activity in mice deficient in alphaCGRP. Circ Res 2001; 89: 983-90.
[21]
Brattstrom A, Seidenbecher T. Central substance P increased blood pressure, heart rate and splanchnic nerve activity in anaesthetized rats without impairment of the baroreflex regulation. Neuropeptides 1992; 23: 81-6.
[22]
Zhu Y, Wang Y, Wang DH. Diuresis and natriuresis caused by activation of VR1-positive sensory nerves in renal pelvis of rats. Hypertension 2005; 46: 992-7.
[23]
Xie C, Sachs JR, Wang DH. Interdependent regulation of afferent renal nerve activity and renal function: Role of transient receptor potential vanilloid type 1, neurokinin 1, and calcitonin gene-related peptide receptors. J Pharmacol Exp Ther 2008; 325: 751-7.
[24]
Kopp UC, Jones SY, DiBona GF. Afferent renal denervation impairs baroreflex control of efferent renal sympathetic nerve activity. Am J Physiol Regul Integr Comp Physiol 2008; 295: R1882-90.
[25]
Ditting T, Freisinger W, Siegel K, et al. Tonic postganglionic sympathetic inhibition induced by afferent renal nerves? Hypertension 2012; 59: 467-76.
[26]
Zhu Y, Xie C, Wang DH. TRPV1-mediated diuresis and natriuresis induced by hypertonic saline perfusion of the renal pelvis. Am J Nephrol 2007; 27: 530-7.
[27]
Dunn SR, Qi Z, Bottinger EP, et al. Utility of endogenous creatinine clearance as a measure of renal function in mice. Kidney Int 2004; 65: 1959-67.
[28]
Michael GJ, Priestley JV. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 1999; 19: 1844-54.
[29]
Patterson LM, Zheng H, Ward SM, et al. Vanilloid receptor (VR1) expression in vagal afferent neurons innervating the gastrointestinal tract. Cell Tissue Res 2003; 311: 277-87.
[30]
Birder LA, Nakamura Y, Kiss S, et al. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 2002; 5: 856-60.
[31]
Zahner MR, Li DP, Chen SR, et al. Cardiac vanilloid receptor 1-expressing afferent nerves and their role in the cardiogenic sympathetic reflex in rats. J Physiol 2003; 551: 515-23.
[32]
Rong W, Hillsley K, Davis JB, et al. Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. J Physiol 2004; 560: 867-81.
[33]
Tank J, Jordan J, Diedrich A, et al. Clonidine improves spontaneous baroreflex sensitivity in conscious mice through parasympathetic activation. Hypertension 2004; 43: 1042-7.
[34]
Marfella R, Nappo F, Marfella MA, et al. Acute hyperglycemia and autonomic function. Diabetes Care 2001; 24: 2016-7.
[35]
de Lima DC, Silveira SA, Haibara AS, et al. The enhanced hyperglycemic response to hemorrhage hypotension in obese rats is related to an impaired baroreflex. Metab Brain Dis 2008; 23: 361-73.
[36]
Arnold AC, Shaltout HA, Gallagher PE, et al. Leptin impairs cardiovagal baroreflex function at the level of the solitary tract nucleus. Hypertension 2009; 54: 1001-8.
[37]
McKernan AM, Calaresu FR. Insulin microinjection into the nucleus tractus solitarii of the rat attenuates the baroreceptor reflex. J Auton Nerv Syst 1996; 61: 128-38.
[38]
Zhang LL, Yan Liu D, Ma LQ, et al. Activation of transient receptor potential vanilloid type-1 channel prevents adipogenesis and obesity. Circ Res 2007; 100: 1063-70.
[39]
Lacolley P, Bezie Y, Girerd X, et al. Aortic distensibility and structural changes in sinoaortic-denervated rats. Hypertension 1995; 26: 337-40.
[40]
Steinback CD, O’Leary DD, Bakker J, et al. Carotid distensibility, baroreflex sensitivity, and orthostatic stress. J Appl Physiol 2005; 99: 64-70.
[41]
Goldstein DS. Arterial baroreflex sensitivity, plasma catecholamines, and pressor responsiveness in essential hypertension. Circulation 1983; 68: 234-40.
[42]
Singhal A, Farooqi IS, Cole TJ, et al. Influence of leptin on arterial distensibility: A novel link between obesity and cardiovascular disease? Circulation 2002; 106: 1919-24.
[43]
Rider OJ, Holloway CJ, Emmanuel Y, et al. Increasing plasma free fatty acids in healthy subjects induces aortic distensibility changes seen in obesity. Circ Cardiovasc Imaging 2012; 5: 367-75.
[44]
Arroyo-Espliguero R, Mollichelli N, Avanzas P, et al. Chronic inflammation and increased arterial stiffness in patients with cardiac syndrome X. Eur Heart J 2003; 24: 2006-11.
[45]
Howe PR, Rogers PF, Minson JB. Influence of dietary sodium on blood pressure in baroreceptor-denervated rats. J Hypertens 1985; 3: 457-60.
[46]
Osborn JW, Hornfeldt BJ. Arterial baroreceptor denervation impairs long-term regulation of arterial pressure during dietary salt loading. Am J Physiol 1998; 275: H1558-66.
[47]
Wang DH, Wu W, Lookingland KJ. Degeneration of capsaicin-sensitive sensory nerves leads to increased salt sensitivity through enhancement of sympathoexcitatory response. Hypertension 2001; 37: 440-3.
[48]
Lohmeier TE, Dwyer TM, Irwin ED, et al. Prolonged activation of the baroreflex abolishes obesity-induced hypertension. Hypertension 2007; 49: 1307-14.
[49]
Lohmeier TE, Iliescu R, Dwyer TM, et al. Sustained suppression of sympathetic activity and arterial pressure during chronic activation of the carotid baroreflex. Am J Physiol Heart Circ Physiol 2010; 299: H402-9.
[50]
Lohmeier TE, Irwin ED, Rossing MA, et al. Prolonged activation of the baroreflex produces sustained hypotension. Hypertension 2004; 43: 306-11.
[51]
Sanya EO, Brown CM, Dutsch M, et al. Impaired cardiovagal and vasomotor responses to baroreceptor stimulation in type II diabetes mellitus. Eur J Clin Invest 2003; 33: 582-8.
[52]
Ruiz J, Monbaron D, Parati G, et al. Diabetic neuropathy is a more important determinant of baroreflex sensitivity than carotid elasticity in type 2 diabetes. Hypertension 2005; 46: 162-7.
[53]
Hajduczok G, Chapleau MW, Johnson SL, et al. Increase in sympathetic activity with age. I. Role of impairment of arterial baroreflexes. Am J Physiol 1991; 260: H1113-20.
[54]
Kopp UC, Cicha MZ, Yorek MA. Impaired responsiveness of renal sensory nerves in streptozotocin-treated rats and obese Zucker diabetic fatty rats: Role of angiotensin. Am J Physiol Regul Integr Comp Physiol 2008; 294: R858-66.
[55]
DiBona GF. Sympathetic neural control of the kidney in hypertension. Hypertension 1992; 19: I28-35.
[56]
Esler M, Straznicky N, Eikelis N, et al. Mechanisms of sympathetic activation in obesity-related hypertension. Hypertension 2006; 48: 787-96.
[57]
Schlaich MP, Sobotka PA, Krum H, et al. Renal denervation as a therapeutic approach for hypertension: novel implications for an old concept. Hypertension 2009; 54: 1195-201.
[58]
Esler MD, Krum H, Sobotka PA, et al. Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): A randomised controlled trial. Lancet 2010; 376: 1903-9.
[59]
Krum H, Schlaich M, Whitbourn R, et al. Catheter-based renal sympathetic denervation for resistant hypertension: a multicentre safety and proof-of-principle cohort study. Lancet 2009; 373: 1275-81.
[60]
De Schepper HU, De Winter BY, Van Nassauw L, et al. TRPV1 receptors on unmyelinated C-fibres mediate colitis-induced sensitization of pelvic afferent nerve fibres in rats. J Physiol 2008; 586: 5247-58.
[61]
Xie C, Wang DH. Inhibition of renin release by arachidonic acid metabolites, 12(s)-HPETE and 12-HETE: Role of TRPV1 channels. Endocrinology 2011; 152: 3811-9.
[62]
Coleridge HM, Coleridge JC, Schultz HD. Afferent pathways involved in reflex regulation of airway smooth muscle. Pharmacol Ther 1989; 42: 1-63.
[64]
Kopp UC, Smith LA. Inhibitory renorenal reflexes: A role for substance P or other capsaicin-sensitive neurons. Am J Physiol 1991; 260: R232-9.
[65]
Feng NH, Lee HH, Shiang JC, et al. Transient receptor potential vanilloid type 1 channels act as mechanoreceptors and cause substance P release and sensory activation in rat kidneys. Am J Physiol Renal Physiol 2008; 294: F316-25.
[66]
Guo A, Vulchanova L, Wang J, et al. Immunocytochemical localization of the vanilloid receptor 1 (VR1): Relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 1999; 11: 946-58.
[67]
Stiefel P, Vallejo-Vaz AJ, Garcia Morillo S, et al. Role of the Renin-Angiotensin system and aldosterone on cardiometabolic syndrome. Int J Hypertens 2011; 2011: 685238.
[68]
Kalil GZ, Haynes WG. Sympathetic nervous system in obesity-related hypertension: Mechanisms and clinical implications. Hypertens Res 2012; 35: 4-16.
[69]
Prior LJ, Eikelis N, Armitage JA, et al. Exposure to a high-fat diet alters leptin sensitivity and elevates renal sympathetic nerve activity and arterial pressure in rabbits. Hypertension 2010; 55: 862-8.
[70]
Mark AL, Agassandian K, Morgan DA, et al. Leptin signaling in the nucleus tractus solitarii increases sympathetic nerve activity to the kidney. Hypertension 2009; 53: 375-80.
[71]
Malmstrom R, Taskinen MR, Karonen SL, et al. Insulin increases plasma leptin concentrations in normal subjects and patients with NIDDM. Diabetologia 1996; 39: 993-6.
[72]
Lee MJ, Yang RZ, Gong DW, et al. Feeding and insulin increase leptin translation. Importance of the leptin mRNA untranslated regions. J Biol Chem 2007; 282: 72-80.
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