Acute stimulatory effect of tumor necrosis factor on the basolateral 50 pS K channels in the thick ascending limb of the rat kidney

Zhang,Guoyan; Gui,Shiliang; Wang,Weiqun; Meng,Dexin; Meng,Qingmin; Luan,Haiyan; Zhao,Rixin; Zhang,Jiatian; Sui,Hongyu

doi:10.3892/mmr.2018.9475

Acute stimulatory effect of tumor necrosis factor on the basolateral 50 pS K channels in the thick ascending limb of the rat kidney

Authors:
- Guoyan Zhang
- Shiliang Gui
- Weiqun Wang
- Dexin Meng
- Qingmin Meng
- Haiyan Luan
- Rixin Zhao
- Jiatian Zhang
- Hongyu Sui
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Affiliations: Department of Urology, First Affiliated Hospital, Jiamusi University, Jiamusi, Heilongjiang 154007, P.R. China, Department of Physiology, Basic Medical College, Jiamusi University, Jiamusi, Heilongjiang 154007, P.R. China
Published online on: September 10, 2018 https://doi.org/10.3892/mmr.2018.9475
Pages: 4733-4738

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Abstract

The aim of the present study was to investigate the acute effect and mechanism of tumor necrosis factor (TNF) on basolateral 50 pS K channels in the thick ascending limb (TAL) of the rat kidney. The TAL tubules were isolated from the rat kidney, and the activity of the 50 pS K channels was recorded using the patch‑clamp technique. The results indicated that the application of TNF (10 nM) significantly activated the 50 pS K channels and the TNF effect was concentration‑dependent. Inhibition of protein kinase A, phospholipase A2 and protein tyrosine kinase using pathway inhibitors (H89, AACOCF3 and Herbimycin A, respectively) did not abolish the stimulatory effect of TNF, indicating that none of these pathways mediated the TNF effect. By contrast, the phenylarsine oxide inhibitor against protein tyrosine phosphatase (PTP) decreased the activity of the 50 pS K channels and blocked the stimulatory effect of TNF on these channels. Furthermore, western blot analysis demonstrated that the application of TNF (10 nM) in the TAL increased the phosphorylation of PTP, an indication of PTP activity stimulation. Thus, it was concluded that the acute application of TNF may stimulate the basolateral 50 pS K channel in the TAL and the stimulatory effect of TNF may be mediated by the PTP‑dependent pathway.

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1	Greger R: Ion transport mechanisms in thick ascending limb of Henle's loop of mammalian nephron. Physiol Rev. 65:760–797. 1985. View Article : Google Scholar : PubMed/NCBI
2	Hebert SC: Roles of Na-K-2Cl and Na-Cl cotransporters and ROMK potassium channels in urinary concentrating mechanism. Am J Physiol. 275:F325–F327. 1998.PubMed/NCBI
3	Vitzthum H, Castrop H, Meier-Meitinger M, Riegger GA, Kurtz A, Krämer BK and Wolf K: Nephron specific regulation of chloride channel CLC-K2 mRNA in the rat. Kidney Int. 61:547–554. 2002. View Article : Google Scholar : PubMed/NCBI
4	Simon DB, Karet FE, Rodriguez-Soriano J, Hamdan JH, DiPietro A, Trachtman H, Sanjad SA and Lifton RP: Genetic heterogeneity of Bartter's syndrome revealed by mutations in the K+ channel, ROMK. Nat Genet. 14:152–156. 1996. View Article : Google Scholar : PubMed/NCBI
5	Hebert SC, Desir G, Giebisch G and Wang W: Molecular diversity and regulation of renal potassium channels. Physiol Rev. 85:319–371. 2005. View Article : Google Scholar : PubMed/NCBI
6	Gu R, Wang J, Zhang Y, Li W, Xu Y, Shan H, Wang WH and Yang B: Adenosine stimulates the basolateral 50 pS K channels in the thick ascending limb of the rat kidney. Am J Physiol Renal Physiol. 293:F299–F305. 2007. View Article : Google Scholar : PubMed/NCBI
7	Paulais M, Lourdel S and Teulon J: Properties of an inwardly rectifying K(+) channel in the basolateral membrane of mouse TAL. Am J Physiol Renal Physiol. 282:F866–F876. 2002. View Article : Google Scholar : PubMed/NCBI
8	Foster D, Parrish-Novak J, Fox B and Xu W: Cytokinereceptor pairing: Accelerating discovery of cytokine function. Nat Rev Drug Discov. 3:160–170. 2004. View Article : Google Scholar : PubMed/NCBI
9	Hehlgans T and Pfeffer K: The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: Players, rules and the games. Immunology. 115:1–20. 2005. View Article : Google Scholar : PubMed/NCBI
10	Tansey MG and Szymkowski DE: The TNF superfamily in 2009: New pathways, new indications, and new drugs. Drug Discovery Today. 14:1082–1088. 2009. View Article : Google Scholar : PubMed/NCBI
11	Wei Y, Babilonia E, Pedraza PL, Ferreri NR and Wang WH: Acute application of TNF stimulates apical 70-pS K+ channels in the thick ascending limb of rat kidney. Am J Physiol Renal Physiol. 285:F491–F497. 2003. View Article : Google Scholar : PubMed/NCBI
12	Wang M, Sui H, Li W, Wang J, Liu Y, Gu L, Wang WH and Gu R: Stimulation of A(2a) adenosine receptor abolishes the inhibitory effect of arachidonic acid on the basolateral 50-pS K channel in the thick ascending limb. Am J Physiol Renal Physiol. 300:F906–F913. 2011. View Article : Google Scholar : PubMed/NCBI
13	Kong S, Zhang C, Li W, Wang L, Luan H, Wang W and Gu R: Stimulation of Ca2+-sensing receptor inhibits the basolateral 50-pS K channels in the thick ascending limb of rat kidney. Biochim Biophys Acta. 1823:273–281. 2012. View Article : Google Scholar : PubMed/NCBI
14	Sasaki CY and Patek PQ: Transformation is associated with an increase in sensitivity to TNF-mediated lysis as a result of an increase in TNF-induced protein tyrosine phosphatase activity. Int J Cancer. 81:141–147. 1999. View Article : Google Scholar : PubMed/NCBI
15	Gu RM, Wei Y, Falck JR, Krishna UM and Wang WH: Effects of protein tyrosine kinase and protein tyrosine phosphatase on apical K(+) channels in the TAL. Am J Physiol Cell Physiol. 281:C1188–C1195. 2001. View Article : Google Scholar : PubMed/NCBI
16	MacEwan DJ: TNF receptor subtype signaling: Differences and cellular consequences. Cell Signal. 14:477–492. 2002. View Article : Google Scholar : PubMed/NCBI
17	Klahr S and Morrissey JJ: The role of vasoactive compounds, growth factors and cytokines in the progression of renal disease. Kidney Int Suppl. 75:S7–S14. 2000. View Article : Google Scholar : PubMed/NCBI
18	Cunningham PN, Dyanov HM, Park P, Wang J, Newell KA and Quigg RJ: Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J Immunol. 168:5817–5823. 2002. View Article : Google Scholar : PubMed/NCBI
19	Xu C, Chang A, Hack BK, Eadon MT, Seth LA and Cunningham PN: TNF-mediated damage to glomerular endothelium is an important determinant of acute kidney injury in sepsis. Kidney Int. 85:72–81. 2014. View Article : Google Scholar : PubMed/NCBI
20	Wang D, Pedraza PL, Abdullah HI, McGiff JC and Ferreri NR: Calcium-sensing receptor-mediated TNF production in medullary thick ascending limb cells. Am J Physiol Renal Physiol. 283:F963–F970. 2002. View Article : Google Scholar : PubMed/NCBI
21	Abdullah HI, Pedraza PL, Hao S, Rodland KD, McGiff JC and Ferreri NR: NFAT regulates calcium-sensing receptor-mediated TNF production. Am J Physiol Renal Physiol. 290:F1110–F1117. 2006. View Article : Google Scholar : PubMed/NCBI
22	Abdullah HI, Pedraza PL, McGiff JC and Ferreri NR: CaR activation increases TNF production by mTAL cells via a Gi-dependent mechanism. Am J Physiol Renal Physiol. 294:F345–F354. 2008. View Article : Google Scholar : PubMed/NCBI
23	Hao S, Bellner L and Ferreri NR: NKCC2A and NFAT5 regulate renal TNF production induced by hypertonic NaCl intake. Am J Physiol Renal Physiol. 304:F533–F542. 2013. View Article : Google Scholar : PubMed/NCBI
24	Liu HJ, Wei Y, Ferreri NR, Nasjletti A and Wang WH: Vasopressin and PGE(2) regulate the apical 70 pS K(+) channel in the thick ascending limb of rat kidney. Am J Physiol Cell Physiol. 278:C905–C913. 2000. View Article : Google Scholar : PubMed/NCBI
25	Gu R, Jin Y, Zhai Y, Yang L, Zhang C, Li W, Wang L, Kong S, Zhang Y, Yang B and Wang WH: PGE2 inhibits basolateral 50 pS potassium channels in the thick ascending limb of the rat kidney. Kidney Int. 74:478–485. 2008. View Article : Google Scholar : PubMed/NCBI
26	Battula S, Hao S, Pedraza PL, Stier CT and Ferreri NR: Tumor necrosis factor-alpha is an endogenous inhibitor of the Na+-K+-2Cl- cotransporter (NKCC2) isoform A in the thick ascending limb. Am J Physiol Renal Physiol. 301:F94–F100. 2011. View Article : Google Scholar : PubMed/NCBI
27	van Lanschot JJ, Mealy K, Jacobs DO, Evans DA and Wilmore DW: Splenectomy attenuates the inappropriate diuresis associated with tumor necrosis factor administration. Surg Gynecol Obstet. 172:293–297. 1991.PubMed/NCBI
28	Shahid M, Francis J and Majid DS: Tumor necrosis factor-alpha induces renal vasoconstriction as well as natriuresis in mice. Am J Physiol Renal Physiol. 295:F1836–F1844. 2008. View Article : Google Scholar : PubMed/NCBI
29	Nakamura K, Komagiri Y, Kojo T and Kubokawa M: Effects of cytokines on activity of an inwardly rectifying K⁺ channel in cultured human proximal tubule cells. J Iwate Med Assoc. 59:375–385. 2007.
30	Nakamura K, Komagiri Y, Kojo T and Kubokawa M: Delayed and acute effects of interferon-gamma on activity of an inwardly rectifying K+ channel in cultured human proximal tubule cells. Am J Physiol Renal Physiol. 296:F46–F53. 2009. View Article : Google Scholar : PubMed/NCBI
31	Nietsch HH, Roe MW, Fiekers JF, Moore AL and Lidofsky SD: Activation of potassium and chloride channels by tumor necrosis factor. Role in liver cell death. J Biol Chem. 275:20556–20561. 2000. View Article : Google Scholar : PubMed/NCBI
32	Chung CH, Fan J, Lee EY, Kang JS, Lee SJ, Pyagay PE, Khoury CC, Yeo TK, Khayat MF, Wang A and Chen S: Effects of tumor necrosis factor-α on podocyte expression of monocyte chemoattractant protein-1 and in diabetic nephropathy. Nephron Extra. 5:1–18. 2015. View Article : Google Scholar : PubMed/NCBI
33	Kalantarinia K, Awad AS and Siragy HM: Urinary and renal interstitial concentrations of TNF-alpha increase prior to the rise in albuminuria in diabetic rats. Kidney Int. 64:1208–1213. 2003. View Article : Google Scholar : PubMed/NCBI