Basolateral LPS inhibits NHE3 and HCO 3 - absorption through TLR4/MyD88- dependent ERK activation in medullary thick ascending limb

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 6, 2011, Pages

  Watts III, Bruns A ^a   George, Thampi ^a   Sherwood, Edward R ^a   Good, David W ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Acid base balance; Kidney; Na + H + exchange; Sepsis; Toll like receptor 4 signaling

Indexed keywords

ALDOSTERONE; BACTERIUM LIPOPOLYSACCHARIDE; BICARBONATE; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; SODIUM PROTON EXCHANGE PROTEIN; SODIUM PROTON EXCHANGE PROTEIN 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ABSORPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNOBLOTTING; INTRACELLULAR SIGNALING; ION TRANSPORT; KIDNEY PERFUSION; KIDNEY TUBULE; KIDNEY TUBULE ABSORPTION; MALE; MEDULLARY THICK ASCENDING LIMB; MOUSE; NONHUMAN; PH MEASUREMENT; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ABSORPTION; ANIMALS; BICARBONATES; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; KIDNEY TUBULES; LIPOPOLYSACCHARIDES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MYELOID DIFFERENTIATION FACTOR 88; RATS; RATS, SPRAGUE-DAWLEY; RENAL INSUFFICIENCY; SEPSIS; SODIUM-HYDROGEN ANTIPORTER; TOLL-LIKE RECEPTOR 4;

EID: 82455166763     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00237.2011     Document Type: Article

References (88)

1. Alexander RT, Grinstein S. Tethering, recycling and activation of the epithelial sodium-proton exchanger, NHE-3. J Exp Biol 212:1630-1637, 2009.
2. Alpern RJ. Renal acidification mechanisms. In: The Kidney, edited by Brenner BM, Rector Jr FC. Philadelphia, PA: Saunders, 2000, Vol. I, p. 455-519.
3. Amemiya M, Loffing J, Lotscher M, Kaissling B, Alpern RJ, Moe OW. Expression of NHE-3 in the apical membrane of rat renal proximal tubule and thick ascending limb. Kidney Int 48:1206-1215, 1995.
4. Banerjee A, Gerondakis S. Coordinating TLR-activated signaling pathways in cells of the immune system. Immunol Cell Biol 85:420-424, 2007.
5. Banerjee A, Gugasyan R, McMahon M, Gerondakis S. Diverse Tolllike receptors utilize Tpl2 to activate extracellular signal-regulated kinase (ERK) in hemopoietic cells. Proc Natl Acad Sci USA 103:3274-3279, 2006.
6. Baumgart K, Radermacher P, Calzia E, Hauser B. Pathophysiology of tissue acidosis in septic shock: Blocked microcirculation or impaired cellular respiration. Crit Care Med 36:640-642, 2008.
7. Biemesderfer D, Rutherford PA, Nagy T, Pizzonia JH, Abu-Alfa AK, Aronson PS. Monoclonal antibodies for high-resolution localization of NHE3 in adult and neonatal rat kidney. Am J Physiol Renal Physiol 273: F289-F299, 1997.
8. +/H+ exchange in the proximal tubule. Pflügers Arch 458:5-21, 2009.
9. Cetin S, Dunkelbarger J, Li J, Boyle P, Ergun O, Qureshi F, Ford H, Upperman J, Watkins S, Hackam DJ. Endotoxin differentially modulates the basolateral and apical sodium/proton exchangers in enterocytes. Surgery 136:375-383, 2004.
10. Chassin C, Goujon JM, Darche S, duMerle L, Bens M, Cluzeaud F, Werts C, Ogier-Denis E, LeBouguenec C, Buzoni-Gatel D, Vandewalle A. Renal collecting duct epithelial cells react to pyelonephritis-associated Escherichia coli by activating distinct TLR4-dependent and -independent inflammatory pathways. J Immunol 177:4773-4784, 2006.
11. Cohen J. The immunopathogenesis of sepsis. Nature 420:885-891, 2002.
12. Cunningham PN, Wang Y, Guo R, He G, Quigg RJ. Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol 172:2629-2635, 2004.
13. David MD, Cochrane CL, Duncan SK, Schrader JW. Pure lipopolysaccharide or synthetic lipid A induces activation of p21Ras in primary macrophages through a pathway dependent on Src family kinases and PI3K. J Immunol 175:8236-8241, 2005.
14. - absorption through TLR4/MyD88-dependent ERK activation in medullary thick ascending limb." Am J Physiol Cell Physiol (September 21, 2011).doi:10.1152/ajpcell.00350.2011.
15. Doi K, Leelahavanichkul A, Yuen PST, Star RA. Animal models of sepsis and sepsis-induced kidney injury. J Clin Invest 119:2868-2878, 2009.
16. Dong C, Davis RJ, Flavell RA. MAP kinases in the immune response. Annu Rev Immunol 20:55-72, 2002.
17. Donowitz M, Li X. Regulatory binding partners and complexes of NHE3. Physiol Rev 87:825-872, 2007.
18. Dumitru CD, Ceci JD, Tsatsanis C, Kontoyiannis D, Stamatakis K, Lin JH, Patriotis C, Jenkins NA, Copeland NG, Kollias G, Tsichlis PN. TNF- induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103:1071-1083, 2000.
19. El-Achkar TM, Dagher PC. Renal Toll-like receptors: recent advances and implications for disease. Nat Clin Pract Nephrol 2:568-581, 2006.
20. El-Achkar TM, Hosein M, Dagher PC. Pathways of renal injury in systemic gram-negative sepsis. Eur J Clin Invest 38:39-44, 2008.
21. El-Achkar TM, Huang X, Plotkin Z, Sandoval RM, Rhodes G, Dagher PC. Sepsis induces changes in the expression and distribution of Toll-like receptor 4 in the rat kidney. Am J Physiol Renal Physiol 290: F1034- F1043, 2006.
22. Eliopoulos AG, Dumitru CD, Wang CC, Cho J, Tsichlis PN. Induction of COX-2 by LPS in macrophages is regulated by Tpl2-dependent CREB activation signals. EMBO J 21:4831-4840, 2002.
23. + exchange activation mediates the lipopolysaccharide- induced proliferation of human B lymphocytes and is impaired in malignant B-chronic lymphocytic leukemia lymphocytes. J Immunol 142:913-918, 1989.
24. George D, Salmeron A. Cot/Tpl-2 protein kinase as a target for the treatment of inflammatory disease. Curr Topics Med Chem 9:611-622, 2009.
25. Gomez J, Garcia-Vazquez E, Banos R, Canteras M, Ruiz J, Banos V, Herrero JA, Valdes M. Predictors of mortality in patients with methicillin- resistant Staphylococcus aureus bacteremia: the role of empiric antibiotic therapy. Eur J Clin Microbiol Infect Dis 26:239-245, 2007.
26. Good DW. Inhibition of bicarbonate absorption by peptide hormones and cyclic adenosine monophosphate in rat medullary thick ascending limb. J Clin Invest 85:1006-1013, 1990.
27. Good DW. The thick ascending limb as a site of renal bicarbonate reabsorption. Sem Nephrol 13:225-235, 1993.
28. - absorption in thick ascending limb via PI3-kinase. Am J Physiol Cell Physiol 279: C1443-C1454, 2000.
29. +/H+ exchangers. Proc Natl Acad Sci USA 92: 12525- 12529, 1995.
30. +/H+ exchanger. Am J Physiol Cell Physiol 290: C757-C763, 2006.
31. - absorption through parallel phosphatidylinositol 3-kinase-mTOR and ERK pathways in thick ascending limb. J Biol Chem 283:26602-26611, 2008.
32. Good DW, George T, Watts III BA Lipopolysaccharide directly alters renal tubule transport through distinct TLR4-dependent pathways in basolateral and apical membranes. Am J Physiol Renal Physiol 297: F866- F874, 2009.
33. - absorption by bacterial lipoprotein in medullary thick ascending limb. Am J Physiol Renal Physiol 299: F536-F544, 2010.
34. +/H+ exchange in rat medullary thick ascending limb. Am J Physiol Renal Fluid Electrolyte Physiol 270: F691-F699, 1996.
35. +/H+ exchanger null mutant mice. Am J Physiol Renal Physiol 287: F1244-F1249, 2004.
36. Grinevich V, Knepper M, Verbalis J, Reyes I, Aguilera G. Acute endotoxemia in rats induces down-regulation of V2 vasopressin receptors and aquaporin-2 content in the kidney medulla. Kidney Int 65:54-62, 2004.
37. Guha M, Mackman N. LPS induction of gene expression in human monocytes. Cell Signal 13:85-94, 2001.
38. Hall JP, Kurdi Y, Hsu S, Cuzzo J, Liu J, Telliez JP, Seidl KJ, Winkler A, Hu Y, Green N, Askew GR, Tam S, Clark JD, Lin LL. Pharmacologic inhibition of Tpl2 blocks inflammatory responses in primary human monocytes, Synoviocytes, and blood. J Biol Chem 282:33295-33304, 2007.
39. +/H+ exchange isoform activities by enteropathogenic E. coli in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 287: G370-G378, 2004.
40. Hoebe K, Du X, Georgl P, Janssen E, Tabeta K, Kim SO, Goode J, Lin P, Mann N, Mudd S, Crozat K, Sovath S, Han J, Beutler B. Identification of Lps2 as a key transducer of MyD88-independent TIR signaling. Nature 424:743-748, 2003.
41. +/H+ exchanger inhibitors. J Pharmacol Exp Ther 321:345-352, 2007.
42. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115-122, 1999.
43. Kawai T, Akira S. TLR signaling. Cell Death Diff 13:816-825, 2006.
44. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373-384, 2010.
45. Kim BS, Lim SW, Li C, Kim JS, Sun BK, Ahn KO, Han SW, Kim J, Yang CW. Ischemia-reperfusion injury activates innate immunity in rat kidneys. Transplantation 79:1370-1377, 2005.
46. Klenzak J, Himmelfarb J. Sepsis and the kidney. Crit Care Clin 21:211-222, 2005.
47. Kraut JA, Kurtz I. Use of base in the treatment of severe acidemic states. Am J Kidney Dis 38:703-727, 2001.
48. Laghmani K, Borensztein P, Ambuhl P, Froissart M, Bichara M, Moe OW, Alpern RJ, Paillard M. Chronic metabolic acidosis enhances NHE-3 protein abundance and transport activity in the rat thick ascending limb by increasing NHE-3 mRNA. J Clin Invest 99:1-7, 1997.
49. Lee SW, Hong YS, Park DW, Chio SH, Moon SW, Park JS, Kim JY, Baek KJ. Acidosis not hyperlactatemia as a predictor of in hospital mortality in septic emergency patients. Emerg Med J 25:659-665, 2008.
50. Levy EM, Viscoli CM, Horwitz RI. The effect of acute renal failure on mortality. JAMA 275:1489-1494, 1996.
51. Lim SW, Li C, Ahn KO, Moon IS, Ahn C, Lee JR, Yang CW. Cyclosporine-induced renal injury induces Toll-like receptor and maturation of dendritic cells. Transplantation 80:691-699, 2005.
52. Liu W, Ouyang X, Yang J, Liu J, Li Q, Gu Y, Fukata M, Lin T, He JC, Abreu M, Unkeless JC, Mayer L, Xiong H. AP-1 activated by Toll-like receptors regulates expression of IL-23 p19. J Biol Chem 284:24006-24016, 2009.
53. +/H+ exchange-mediated H+ homeostasis. J Neurosci 30: 15210- 15220, 2010.
54. Lombardo E, Alvarez-Barrientos A, Maroto B, Bosca L, Knaus UG. TLR4-mediated survival of macrophages is MyD88 dependent and requires TNF- autocrine signaling. J Immunol 178:3731-3739, 2007.
55. Murphy LO, Blenis J. MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31:268-275, 2006.
56. Nemeth ZH, Deitch EA, Lu Q, Szabo C, Hasko G. NHE blockade inhibits chemokine production and NF-B activation in immunostimulated endothelial cells. Am J Physiol Cell Physiol 283: C396-C403, 2002.
57. +/H+ exchanger blockade inhibits enterocyte inflammatory response and protects against colitis. Am J Physiol Gastrointest Liver Physiol 283: G122-G132, 2002.
58. Olesen ETB, de Seigneux S, Wang G, Lutken SC, Frokiaer J, Kwon TH, Nielsen S. Rapid and segmental specific dysregulation of AQP2, S256-pAQP2 and renal sodium transporters in rats with LPS-induced endotoxaemia. Nephrol Dial Transplant 24:2338-2349, 2009.
59. O'Neill LAJ, Bowie AG. The family of five: TIR-domain-containing adapters in Toll-like receptor signaling. Nat Rev Immunol 7:353-364, 2007.
60. Oppert M, Engel C, Brunkhorst FM, Bogatsch H, Reinhart K, Frei U, Eckardt KU, Loeffler M, John S. Acute renal failure in patients with severe sepsis and septic shock- a significant independent risk factor for mortality: results from the German Prevalence Study. Nephrol Dial Transplant 23:904-909, 2008.
61. Orlowski J, Grinstein S. Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflügers Arch 447:549-565, 2004.
62. Patole PS, Schubert S, Hildinger K, Khandoga S, Khandoga A, Segerer S, Henger A, Kretzler M, Werner M, Krombach F, Schlondorff D, Anders HJ. Toll-like receptor-4: Renal cells and bone marrow cells signal for neutrophil recruitment during pyelonephritis. Kidney Int 68:2582-2587, 2005.
63. Preisig PA. The acid-activated signaling pathway: Starting with Pyk2 and ending with increased NHE3 activity. Kidney Int 72:1324-1329, 2007.
64. Qi HY, Shelhamer JH. Toll-like receptor 4 signaling regulates cytosolic phospholipase A2 activation and lipid generation in lipopolysaccharidestimulated macrophages. J Biol Chem 280:38969-38975, 2005.
65. Rosoff PM, Cantley LC. Lipopolysaccharide and phorbol esters induce differentiation but have opposite effects on phosphatidylinositol turnover and Ca2+ mobilization in 70Z/3 pre-B lymphocytes. J Biol Chem 260:9209-9215, 1985.
66. +/H+ exchanger activity in dendritic cells. Cell Physiol Biochem 26:553-562, 2010.
67. Russell JA, Singer J, Bernard GR, Wheeler A, Fulkerson W, Hudson L, Schein R, Summer W, Wright P, Walley KR. Changing pattern of organ dysfunction in early human sepsis is related to mortality. Crit Care Med 28:3405-3411, 2000.
68. Sataranatarajan K, Feliers D, Mariappan MM, Lee MJ, Jimenez F, Chen Y, Gosh-Choudhury G, Ahuja S, Kasinath BS. Toll-like receptor 4 knockout mice are resistant to diabetic kidney injury (Abstract). J Am Soc Nephrol 19: 107A, 2008.
69. Schmidt C, Hocherl K, Bucher M. Regulation of renal glucose transporters during severe inflammation. Am J Physiol Renal Physiol 292: F804-F811, 2007.
70. Schmidt C, Hocherl K, Schweda F, Kurtz A, Bucher M. Regulation of renal sodium transporters during severe inflammation. J Am Soc Nephrol 18:1072-1083, 2007.
71. Schrier RW, Wang W. Acute renal failure and sepsis. N Engl J Med 351:159-169, 2004.
72. +/H+ exchanger. Nat Genet 19:282-285, 1998.
73. Tsuboi N, Yoshikai Y, Matsuo S, Kikuchi T, Iwami KI, Nagai Y, Takeuchi O, Akira S, Matsuguchi T. Roles of Toll-like receptors in C-C chemokine production by renal tubular epithelial cells. J Immunol 169:2026-2033, 2002.
74. Tsuganezawa T, Sato S, Yamaji Y, Preisig PA, Moe OW, Alpern RJ. Role of c-SRC and ERK in acid-induced activation of NHE3. Kidney Int 62:41-50, 2002.
75. Wang JJ, Zhang SX, Mott R, Chen Y, Knapp RR, Cao W, Ma JX. Anti-inflammatory effects of pigment epithelium-derived factor in diabetic nephropathy. Am J Physiol Renal Physiol 294: F1166-F1173, 2008.
76. Wang W, Li C, Summer SN, Falk S, Wang W, Ljubanovic D, Schrier RJ. Role of AQP1 in endotoxemia-induced acute kidney injury. Am J Physiol Renal Physiol 294: F1473-F1480, 2008.
77. Waterfield MR, Zhang M, Norman LP, Sun SC. NF-B1/p105 regulates lipopolysaccharide-stimulated MAP kinase signaling by governing the stability and function of the Tpl2 kinase. Mol Cell 11:685-694, 2003.
78. +/H+ exchange. J Biol Chem 274:7841-7847, 1999.
79. - absorption through actin cytoskeleton remodeling in renal thick ascending limb. J Biol Chem 280:11439-11447, 2005.
80. - absorption via a nongenomic, ERK-dependent pathway in medullary thick ascending limb. Am J Physiol Renal Physiol 291: F1005- F1013, 2006.
81. - absorption in the medullary thick ascending limb through a two hit mechanism (Abstract). J Am Soc Nephrol 21: 253A, 2010.
82. +/H+ exchange in rat medullary thick ascending limb: pHi-dependence and inhibition by hyperosmolality. J Biol Chem 269:20250-20255, 1994.
83. - absorption in renal thick ascending limb. J Clin Invest 104:1593-1602, 1999.
84. - absorption by nerve growth factor in MTAL. Am J Physiol Renal Physiol 282: F1056-F1063, 2002.
85. Wolfs TGAM, Buurman WA, van Schadewijk A, de Vries B, Daemen MARC, Hiemstra PS, van't Veer C. In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-γ and TNF-α mediated up-regulation during inflammation. J Immunol 168:1286-1293, 2002.
86. Wu H, Chen G, Wybern KR, Yin J, Bertolio P, Eris JM, Alexander SI, Sharland AF, Chadban SJ. TLR4 activation mediates kidney ischemia/ reperfusion injury. J Clin Invest 117,2847-2859, 2007.
87. Zager RA, Johnson ACM, Lund S, Randolph-Habecker J. Toll-like receptor (TLR4) shedding and depletion: acute proximal tubular cell responses to hypoxic and toxic injury. Am J Physiol Renal Physiol 292: F304-F312, 2007.
88. Zhang B, Ramesh G, Uematsu S, Akira S, Reeves WB. TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J Am Soc Nephrol 19:923-932, 2008.