Effects of a High-Salt Diet on TRPV-1-Dependent Renal Nerve Activity in Dahl Salt-Sensitive Rats

Xie, Chaoqin; Wang, Donna H.

doi:10.1159/000316528

Cited by 14 publications

(12 citation statements)

References 78 publications

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“…21 Rats develop salt-sensitive hypertension after TRPV1 sensory degeneration by capsaicin treatment. 22 Induction of hypertension by deoxycorticosterone acetate treatment in TRPV1 -/-mice aggravated kidney damage. 23 Mutants of TRPV1 not only detected NaCl in the presence of amiloride but also preferred NaCl over water at concentrations avoided by the WT mice.…”

Section: Discussionmentioning

confidence: 99%

Transient Receptor Potential Vanilloid 1 Activation by Dietary Capsaicin Promotes Urinary Sodium Excretion by Inhibiting Epithelial Sodium Channel α Subunit–Mediated Sodium Reabsorption

Wang

Xing

et al. 2014

Hypertension

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T he pathogenesis of hypertension is caused by both genetic susceptibility and environmental risk factors.1 One of major environmental factors for hypertension is high-sodium or lowpotassium dietary intake.2 Maintenance of a constant intravascular fluid volume and blood pressure depends on the kidneys' ability to regulate the urinary sodium excretion (U Na V).3 Several renal sodium transporters, such as the thiazide-sensitive NaCl cotransporter (NCC) and the amiloride-sensitive epithelial sodium channel (ENaC), play crucial roles in regulating renal sodium reabsorption and blood pressure. 4 Multigene kinases, including Ste20-related proline-alanine-rich kinase (SPAK), with-no-lysine kinase (WNK) 4 and 1, oxidative stress response kinase 1 (OSR1), and serum-and glucocorticoid-inducible protein kinase 1 (SGK1), regulate renal electrolyte transport. Abnormal signaling pathways attributable to aberrations of these kinases can result in renal sodium retention and hypertension. 5 Currently, strategies to prevent the development of hypertension include avoidance of a high-salt (HS) diet and increased vegetables intake in general population. In addition, thiazide diuretics are commonly used to treat patients with hypertension through inhibiting renal sodium reabsorption in the distal convoluted tubule, thereby increasing the U Na V and reducing extracellular fluid volume. 6 However, nondrug interventionmediated U Na V is scarcely studied.The transient receptor potential vanilloid 1 (TRPV1) cation channel is a polymodal nonselective cation channel that can Abstract-High salt (HS) intake contributes to the development of hypertension. Epithelial sodium channels play crucial roles in regulating renal sodium reabsorption and blood pressure. The renal transient receptor potential vanilloid 1 (TRPV1) cation channel can be activated by its agonist capsaicin. However, it is unknown whether dietary factors can act on urinary sodium excretion and renal epithelial sodium channel (ENaC) function. Here, we report that TRPV1 activation by dietary capsaicin increased urinary sodium excretion through reducing sodium reabsorption in wild-type (WT) mice on a HS diet but not in TRPV1 -/-mice. The effect of capsaicin on urinary sodium excretion was involved in inhibiting αENaC and its related with-no-lysine kinase 1/serum-and glucocorticoid-inducible protein kinase 1 pathway in renal cortical collecting ducts of WT mice. Dietary capsaicin further reduced the increased αENaC activity in WT mice attributed to the HS diet. In contrast, this capsaicin effect was absent in TRPV1 -/-mice. Immunoprecipitation study indicated αENaC specifically coexpressed and functionally interact with TRPV1 in renal cortical collecting ducts of WT mice. Additionally, ENaC activity and expression were suppressed by capsaicin-mediated TRPV1 activation in cultured M1-cortical collecting duct cells. Long-term dietary capsaicin prevented the development of high blood pressure in WT mice on a HS diet. It concludes that TRPV1 activation in the cortical collecting du...

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Section: Discussionmentioning

confidence: 99%

Transient Receptor Potential Vanilloid 1 Activation by Dietary Capsaicin Promotes Urinary Sodium Excretion by Inhibiting Epithelial Sodium Channel α Subunit–Mediated Sodium Reabsorption

Wang

Xing

et al. 2014

Hypertension

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“…In contrast, renal afferent nerves were described to act protectively against salt-sensitive hypertension and the structural renal damage of high blood pressure (24,44). A more recent study using a more selective method of renal afferent denervation suggests that this might not be the case, but it could be shown that selective renal afferent denervation was able to blunt the development of deoxycorticosterone acetate-salt hypertension (12).…”

mentioning

confidence: 99%

Impaired excitability of renal afferent innervation after exposure to the inflammatory chemokine CXCL1

Ditting

Freisinger

Rodionova

et al. 2016

American Journal of Physiology-Renal Physiology

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Recently, we showed that renal afferent neurons exhibit a unique firing pattern, i.e., predominantly sustained firing, upon stimulation. Pathological conditions such as renal inflammation likely alter excitability of renal afferent neurons. Here, we tested whether the proinflammatory chemokine CXCL1 alters the firing pattern of renal afferent neurons. Rat dorsal root ganglion neurons (Th11-L2), retrogradely labeled with dicarbocyanine dye, were incubated with CXCL1 (20 h) or vehicle before patchclamp recording. The firing pattern of neurons was characterized as tonic, i.e., sustained action potential (AP) firing, or phasic, i.e., Ͻ5 APs following current injection. Of the labeled renal afferents treated with vehicle, 58.9% exhibited a tonic firing pattern vs. 7.8%, in unlabeled, nonrenal neurons (P Ͻ 0.05). However, after exposure to CXCL1, significantly more phasic neurons were found among labeled renal neurons; hence the occurrence of tonic neurons with sustained firing upon electrical stimulation decreased (35.6 vs. 58.9%, P Ͻ 0.05). The firing frequency among tonic neurons was not statistically different between control and CXCL1-treated neurons. However, the lower firing frequency of phasic neurons was even further decreased with CXCL1 exposure [control: 1 AP/600 ms (1-2) vs. CXCL1: 1 AP/600 ms (1-1); P Ͻ 0.05; median (25th-75th percentile)]. Hence, CXCL1 shifted the firing pattern of renal afferents from a predominantly tonic to a more phasic firing pattern, suggesting that CXCL1 reduced the sensitivity of renal afferent units upon stimulation. chemokine; CXCL1; renal afferent nerve; voltage-gated sodium channel; tonic; phasic; firing pattern OBSERVATIONS IN PATIENTS with renal failure and/or hypertension who were nephrectomized (7, 17) strongly suggest that renal sensory afferent innervation increases sympathetic-mediated vasoconstriction. Moreover, sympathetic nerve activity in patients after renal transplantation was only normalized with concomitant bilateral nephrectomy (17). Additional work in experimental models indicated (21, 23) that efferent neurogenic influences on cardiac pathology in renal insufficiency are mediated by renal afferent nerve activity (1).In experimental animals, afferent innervation of the kidney was reported to contribute to the sustained blood pressure increases when renal structural damage was present (3, 46). In contrast, renal afferent nerves were described to act protectively against salt-sensitive hypertension and the structural renal damage of high blood pressure (24,44). A more recent study using a more selective method of renal afferent denervation suggests that this might not be the case, but it could be shown that selective renal afferent denervation was able to blunt the development of deoxycorticosterone acetate-salt hypertension (12).Therefore, the benefit of afferent renal nerve ablation for the treatment of refractory hypertension remains controversial (31). In any case, the modulatory influence of afferent renal nerves on sympathetic tone is not well understood....

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“…Clinical reports on patients after thermal ablation point to an independent role of afferent renal innervation on blood pressure (33). Experimental data suggest that renal afferent denervation may be protective against the development of high blood pressure (26,42) as well as the progression of renal structural damage in renal disease (6,43). Hence, nonselective thermal ablation of afferent renal nerves in resistant human hypertension may not be always beneficial since the exact pathophysiological situation is normally not well defined (27).…”

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confidence: 99%

Sensory renal innervation: a kidney-specific firing activity due to a unique expression pattern of voltage-gated sodium channels?

Freisinger

Schatz

Ditting

et al. 2013

American Journal of Physiology-Renal Physiology

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Freisinger W, Schatz J, Ditting T, Lampert A, Heinlein S, Lale N, Schmieder R, Veelken R. Sensory renal innervation: a kidney-specific firing activity due to a unique expression pattern of voltage-gated sodium channels? Am J Physiol Renal Physiol 304: F491-F497, 2013. First published January 2, 2013; doi:10.1152/ajprenal.00011.2012.-Sensory neurons with afferent axons from the kidney are extraordinary in their response to electrical stimulation. More than 50% exhibit a tonic firing pattern, i.e., sustained action potential firing throughout depolarizing, pointing to an increased excitability, whereas nonrenal neurons show mainly a phasic response, i.e., less than five action potentials. Here we investigated whether these peculiar firing characteristics of renal afferent neurons are due to differences in the expression of voltage-gated sodium channels (Na vs). Dorsal root ganglion (DRG) neurons from rats were recorded by the current-clamp technique and distinguished as "tonic" or "phasic. .67]; P Ͻ 0.05). These findings point to an increased presence of the TTX-resistant Na vs 1.8 and 1.9. Furthermore, tonic neurons exhibited a relatively higher portion of TTX-resistant sodium currents. Interestingly, mRNA expression of TTX-resistant sodium channels was significantly increased in renal, predominantly tonic, DRG neurons. Hence, under physiological conditions, renal sensory neurons exhibit predominantly a firing pattern associated with higher excitability. Our findings support that this is due to an increased expression and activation of TTX-resistant Na vs.

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Effects of a High-Salt Diet on TRPV-1-Dependent Renal Nerve Activity in Dahl Salt-Sensitive Rats

Cited by 14 publications

References 78 publications

Transient Receptor Potential Vanilloid 1 Activation by Dietary Capsaicin Promotes Urinary Sodium Excretion by Inhibiting Epithelial Sodium Channel α Subunit–Mediated Sodium Reabsorption

Transient Receptor Potential Vanilloid 1 Activation by Dietary Capsaicin Promotes Urinary Sodium Excretion by Inhibiting Epithelial Sodium Channel α Subunit–Mediated Sodium Reabsorption

Impaired excitability of renal afferent innervation after exposure to the inflammatory chemokine CXCL1

Sensory renal innervation: a kidney-specific firing activity due to a unique expression pattern of voltage-gated sodium channels?

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