Contribution of renal tubule epithelial cells in the innate immune response during renal bacterial infections and ischemia-reperfusion injury

Chang Gung Medical Journal

Volumn 33, Issue 3, 2010, Pages 225-240

  Mkaddem, Sanae Ben ^a,b   Chassin, Cecilia ^a,b   Vandewalle, Alain ^a,b  

^a CENTRE DE RECHERCHE BIOMÉDICALE BICHAT BEAUJON CRB3   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Inflammation; Ischemia reperfusion injury; Renal tubule epithelial cell; Toll like receptor; Urinary tract infection

Indexed keywords

ARGIPRESSIN; BACTERIUM LIPOPOLYSACCHARIDE; GLYCOPROTEIN GP 96; HEAT SHOCK PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATASE; SERINE THREONINE PROTEIN PHOSPHATASE 5; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; MUCOPROTEIN; TAMM HORSFALL GLYCOPROTEIN; TOLL LIKE RECEPTOR; UMOD PROTEIN, HUMAN;

APOPTOSIS; BACTERIAL INFECTION; BACTERIUM ADHERENCE; BONE MARROW CELL; CELL DAMAGE; DISEASE SEVERITY; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; INFLAMMATION; INNATE IMMUNITY; KIDNEY COLLECTING TUBULE; KIDNEY INFECTION; KIDNEY ISCHEMIA; KIDNEY TUBULE EPITHELIUM; NEPHRITIS; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; REPERFUSION INJURY; REVIEW; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI; WATER ABSORPTION; ANIMAL; BACTERIAL TRANSLOCATION; CYTOLOGY; HUMAN; IMMUNOLOGY; KIDNEY DISEASE; KIDNEY TUBULE; PHYSIOLOGY;

ANIMALS; ARGININE VASOPRESSIN; BACTERIAL INFECTIONS; BACTERIAL TRANSLOCATION; EPITHELIAL CELLS; HUMANS; IMMUNITY, INNATE; KIDNEY DISEASES; KIDNEY TUBULES; MUCOPROTEINS; REPERFUSION INJURY; TOLL-LIKE RECEPTORS; URINARY TRACT INFECTIONS; UROMODULIN;

EID: 77954500551     PISSN: 20720939     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (152)

1. Brown P, Ki M, Foxman B. Acute pyelonephritis among adults: cost of illness and considerations for the economic evaluation of therapy. Pharmacoeconomics 2005;23:1123-42.
2. Johnson JR, Russo TA. Molecular epidemiology of extraintestinal pathogenic (uropathogenic) Escherichia coli. Int J Med Microbiol 2005;295: 383-404.
3. Freedman AL. Urologic diseases in North America Project: trends in resource utilization for urinary tract infections in children. J Urol 2005;173: 949-54.
4. Abbott KC, Swanson SJ, Richter ER, Bohen EM, Agodoa LY, Peters TG, Barbour G, Lipnick R, Cruess DF. Late urinary tract infection after renal transplantation in the United States. Am J Kidney Dis 2004;44: 353-62.
5. Pellé G, Vimont S, Levy PP, Hertig A, Ouali N, Chassin C, Arlet G, Rondeau E, Vandewalle A. Acute pyelonephritis represents a risk factor impairing long-term kidney graft function. Am J Transplant 2007;7: 899-907.
6. de Souza RM, Olsburgh J. Urinary tract infection in the renal transplant patient. Nat Clin Pract Nephrol 2008;4: 252-64.
7. Säemann M, Hörl WH. Urinary tract infection in renal transplant recipients. Eur J Clin Invest 2008;38 Suppl 2: 58-65.
8. Clermont O, Lavollay M, Vimont S, Deschamps C, Forestier C, Branger C, Denamur E, Arlet G. The CTX-M-15-producing Escherichia coli diffusing clone belongs to a highly virulent B2 phylogenetic subgroup. J Antimicrob Chemother 2008;61: 1024-8.
9. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 2003;301: 105-7.
10. Justice SS, Hunstad DA, Seed PC, Hultgren SJ. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc Natl Acad Sci USA 2006;103: 19884-9.
11. Wright KJ, Seed PC, Hultgren SJ. Development of intra-cellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 2007;9: 2230-41.
12. Kamath NS, John GT, Neelakantan N, Kirubakaran MG, Jacob CK. Acute graft pyelonephritis following renal transplantation. Transpl Infect Dis 2006;8: 140-7.
13. Gribar SC, Anand RJ, Sodhi CP, Hackam DJ. The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J Leukoc Biol 2008;83: 493-8.
14. Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol 2004;4: 499-511.
15. O'Neill LA, Bowie AG. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 2007;7: 353-64.
16. Werts C, Girardin SE, Philpott DJ. TIR, CARD and PYRIN: three domains for an antimicrobial triad. Cell Death Differ 2006;13: 798-815.
17. Franchi L, Warner N, Viani K, Nuñez G. Function of Nod-like receptors in microbial recognition and host defense. Immunol Rev 2009;227: 106-28.
18. Ip WK, Takahashi K, Ezekowitz RA, Stuart LM. Mannose-binding lectin and innate immunity. Immunol Rev 2009;230: 9-21.
19. Gribar SC, Richardson WM, Sodhi CP, Hackam DJ. No longer an innocent bystander: epithelial toll-like receptor signaling in the development of mucosal inflammation. Mol Med 2008;14: 645-59.
20. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007;81: 1-5.
21. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998;282: 2085-8.
22. Baeuerle PA, Baltimore D. I kappa B: a specific inhibitor of the NF-kappa B transcription factor. Science 1988;242: 540-6.
23. Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 1995;267: 1485-8.
24. Ninomiya-Tsuji J, Kishimoto K, Hiyama A, Inoue J, Cao Z, Matsumoto K. The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 1999;398: 252-6.
25. An H, Yu Y, Zhang M, Xu H, Qi R, Yan X, Liu S, Wang W, Guo Z, Guo J, Qin Z, Cao X. Involvement of ERK, p38 and NF-kappaB signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells. Immunology 2002;106: 38-45.
26. Schieven GL. The biology of p38 kinase: a central role in inflammation. Curr Top Med Chem 2005;5: 921-8.
27. Hoebe K, Du X, Georgel 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 signalling. Nature 2003;424: 743-8.
28. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okae M, Takeda M, Akira S. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 2003;301: 640-3.
29. Vandewalle A. Toll-like receptors and renal bacterial infections. Chang Gung Med J 2008;31: 525-37.
30. Tsuboi N, Yoshikai Y, Matsuo S, Kikuchi T, Iwami K, 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 2002;169: 2026-33.
31. Wolfs TG, Buurman WA, van Schadewijk A, de Vries B, Daemen MA, Hiemstra PS, van't Veer C. In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-gamma and TNF-alpha mediated up-regulation during inflammation. J Immunol 2002;168: 1286-93.
32. Yang CW, Hung CC, Wu MS, Tian YC, Chang CT, Pan MJ, Vandewalle A. Toll-like receptor 2 mediates early inflammation by leptospiral outer membrane proteins in proximal tubule cells. Kidney Int 2006;69: 815-22.
33. Chowdhury P, Sacks SH, Sheerin NS. Toll-like receptors TLR2 and TLR4 initiate the innate immune response of the renal tubular epithelium to bacterial products. Clin Exp Immunol 2006;145: 346-56.
34. Chassin C, Goujon JM, Darche S, du Merle L, Bens M, Cluzeaud F, Werts C, Ogier-Denis E, Le Bouguénec 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 2006;177: 4773-84.
35. Shigeoka AA, Holscher TD, King AJ, Hall FW, Kiosses WB, Tobias PS, Mackman N, McKay DB. TLR2 is constitutively expressed within the kidney and participates in ischemic renal injury through both MyD88-dependent and -independent pathways. J Immunol 2007;178: 6252-8.
36. El-Achkar TM, Huang X, Plotkin Z, Sandoval RM, Rhodes GJ, Dagher PC. Sepsis induces changes in the expression and distribution of Toll-like receptor 4 in the rat kidney. Am J Physiol Renal Physiol 2006;290:F1034-43.
37. Bäckhed F, Söderhäll M, Ekman P, Normark S, Richter-Dahlfors A. Induction of innate immune responses by Escherichia coli and purified lipopolysaccharide correlate with organ-and cell-specific expression of Toll-like receptors within the human urinary tract. Cell Microbiol 2001;3: 153-8.
38. Samuelsson P, Hang L, Wullt B, Irjala H, Svandborg C. Toll-like receptor 4 expression and cytokine responses in the human urinary tract mucosa. Infect Immun 2004;72: 3179-86.
39. Andersen-Nissen E, Hawn TR, Smith KD, Nachman A, Lampano AE, Uematsu S, Akira S, Aderem A. Cutting edge: Tlr5-/-mice are more susceptible to Escherichia coli urinary tract infection. J Immunol 2007;178: 4717-20.
40. Zhang D, Zhang G, Hayden MS, Greenblatt MB, Bussey C, Flavell RA, Ghosh S. A toll-like receptor that prevents infection by uropathogenic bacteria. Science 2004;303: 1522-6.
41. Yarovinsky F, Zhang D, Andersen JF, Bannenberg GL, Serhan CN, Hayden MS, Hieny S, Sutterwala FS, Flavell RA, Ghosh S, Sher A. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 2005;308: 1626-9.
42. Patole PS, Gröne HJ, Segerer S, Ciubar R, Belemezova E, Henger A, Kretzler M, Schlöndorff D, Anders HJ. Viral double-stranded RNA aggravates lupus nephritis through Toll-like receptor 3 on glomerular mesangial cells and antigen-presenting cells. J Am Soc Nephrol 2005;16: 1326-38.
43. Anders HJ, Vielhauer V, Eis V, Linde Y, Kretzler M, Perez de Lema G, Strutz F, Bauer S, Rutz M, Wagner H, Gröne HJ, Schlöndorff D. Activation of toll-like receptor-9 induces progression of renal disease in MRL-Fas(lpr) mice. FASEB J 2004;18: 534-6.
44. Pawar RD, Patole PS, Zecher D, Segerer S, Kretzler M, Schlöndorff D, Anders HJ. Toll-like receptor-7 modulates immune complex glomerulonephritis. J Am Soc Nephrol 2006;17: 141-9.
45. Giorgini A, Brown HJ, Lock HR, Nimmerjahn F, Ravetch JV, Verbeek JS, Sacks SH, Robson MG. Fc gamma RIII and Fc gamma RIV are indispensable for acute glomerular inflammation induced by switch variant monoclonal antibodies. J Immunol 2008;181: 8745-52.
46. Brown HJ, Lock HR, Wolfs TG, Buurman WA, Sacks SH, Robson MG. Toll-like receptor 4 ligation on intrinsic renal cells contributes to the induction of antibody-mediated glomerulonephritis via CXCL1 and CXCL2. J Am Soc Nephrol 2007;18: 1732-9.
47. Qureshi ST, Lariviere L, Leveque G, Clermont S, Moore KJ, Gros P, Malo D. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J Exp Med 1999;189: 615-25.
48. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999;162: 3749-52.
49. Arbour NC, Lorenz E, Schutte BC, Zabner J, Kline JN, Jones M, Frees K, Watt JL, Schwartz DA. TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat Genet 2000;25: 187-91.
50. Schilling JD, Martin SM, Hung CS, Lorenz RG, Hultgren SJ. Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc Natl Acad Sci USA 2003;100: 4203-8.
51. Patole PS, Schubert S, Hildinger K, Khandoga S, Khandoga A, Segerer S, Henger A, Kretzler M, Werner M, Krombach F, Schlöndorff D, Anders HJ. Toll-like receptor-4: renal cells and bone marrow cells signal for neutrophil recruitment during pyelonephritis. Kidney Int 2005;68: 2582-7.
52. Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ. Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 2006;176: 3070-9.
53. Ruemmele FM, Beaulieu JF, Dionne S, Levy E, Seidman EG, Cerf-Bensussan N, Lentze MJ. Lipopolysaccharide modulation of normal enterocyte turnover by toll-like receptors is mediated by endogenously produced tumour necrosis factor alpha. Gut 2002;51: 842-8.
54. Cario E, Podolsky DK. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 2000;68: 7010-7.
55. Otte JM, Cario E, Podolsky DK. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 2004;126: 1054-70.
56. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 2002;195: 559-70.
57. Jilling T, Simon D, Lu J, Meng FJ, Li D, Schy R, Thomson RB, Soliman A, Arditi M, Caplan MS. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 2006;177: 3273-82.
58. Neal MD, Leaphart C, Levy R, Prince J, Billiar TR, Watkins S, Li J, Cetin S, Ford H, Schreiber A, Hackam DJ. Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 2006;176: 3070-9.
59. Bergsten G, Wullt B, Svanborg C. Escherichia coli, fimbriae, bacterial persistence and host response induction in the human urinary tract. Int J Med Microb 2005;295:487-502.
60. Connell I, Agace W, Klemm P, Schembri M, Marild S, Svanborg C. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci USA 1996;93: 9827-32.
61. Leffler H, Svanborg-Edén C. Chemical identification of a glycosphingolipid receptor for Escherichia coli attaching to human urinary tract epithelial cells and agglutinating human erythrocytes. FEMS Microbiol Lett 1980;8:117-82.
62. Roberts JA, Marklund BI, Ilver D, Hasla D, Kaack MB, Baskin G, Louis M, Mollby R, Winberg J, Normark S. The Gal(alpha 1-4)Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. Proc Natl Acad Sci USA 1994;91: 11889-93.
63. Nowicki B, Moulds J, Hull R, Hull S. A hemagglutinin of uropathogenic Escherichia coli recognizes the Dr blood group antigen. Infect Immun 1988;56: 1057-60.
64. Schilling JD, Mulvey MA, Vincent CD, Lorenz RG, Hultgren SJ. Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism. J Immunol 2001;166: 1148-55.
65. Fischer H, Yamamoto M, Akira S, Beutler B, Svanborg C. Mechanism of pathogen-specific TLR4 activation in the mucosa: fimbriae, recognition receptors and adaptor protein selection. Eur J Immunol 2006;36: 267-77.
66. Chassin C, Hornef MW, Bens M, Lotz M, Goujon JM, Vimont S, Arlet G, Hertig A, Rondeau E, Vandewalle A. Hormonal control of the renal immune response and antibacterial host defense by arginine vasopressin. J Exp Med 2007;204: 2837-52.
67. Knepper MA, Star RA. Vasopressin: friend or foe? Nat Med 2008;14: 14-6.
68. Martinez JJ, Mulvey MA, Schilling JD, Pinkne JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 2000;19: 2803-12.
69. Schilling JD, Mulvey MA, Vincent CD, Lorenz RG, Hultgren SJ. Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism. J Immunol 2001;166: 1148-55.
70. Wullt B, Bergsten G, Connell H, Rollano P, Gebratsedik N, Hang L, Svanborg C. P-fimbriae trigger mucosal responses to Escherichia coli in the human urinary tract. Cell Microbiol 2001;3: 255-64.
71. Duncan MJ, Li G, Shin JS, Carson JL, Abraham SN. Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem 2004;279: 18944-51.
72. Anderson RG. The caveolae membrane system. Annu Rev Biochem 1998;67: 199-225.
73. Kurzchalia TV, Parton RG. Membrane microdomains and caveolae. Curr Opin Cell Biol 1999;11: 424-31.
74. Triantafilou M, Miyake K, Golenbock DT, Triantafilou K. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J Cell Sci 2002;115: 2603-11.
75. Hornef MW, Normark BH, Vandewalle A, Normark S. Intracellular recognition of lipopolysaccharide by toll-like receptor 4 in intestinal epithelial cells. J Exp Med 2003;198: 1225-35.
76. Chassin C, Vimont S, Cluzeaud F, Bens M, Goujon JM, Fernandez B, Hertig A, Rondeau E, Arlet G, Hornef MW, Vandewalle A. TLR4 facilitates translocation of bacteria across renal collecting duct cells. J Am Soc Nephrol 2008;19: 2364-74.
77. Ries F, Klastersky J. Nephrotoxicity induced by cancer chemotherapy with special emphasis on cisplatin toxicity. Am J Kidney Dis 1986;13: 368-79.
78. Ramesh G, Zhang B, Uematsu S, Akira S, Reeves WB. Endotoxin and cisplatin synergistically induce renal dysfunction and cytokine production in mice. Am J Physiol Renal Physiol 2007;293:F 325-32.
79. Zhang B, Ramesh G, Uematsu S, Akira S, Reeves WB. TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J Am Soc Nephrol 2008;19: 923-32.
80. Zasloff M. Antimicrobial peptides, innate immunity, and the normally sterile urinary tract. J Am Soc Nephrol 2007;18: 2810-6.
81. Rehaume LM, Hancock RE. Neutrophil-derived defensins as modulators of innate immune function. Crit Rev Immunol 2008;28: 185-200.
82. Bevins CL. Paneth cell defensins: key effector molecules of innate immunity. Biochem Soc Trans 2006;34: 263-6.
83. Donovan KL, Topley N. What are renal defensins defending? Nephron Exp Nephrol 2003;93:e 125-8.
84. Malm J, Sørensen O, Persson T, Frohm-Nilsson M, Johansson B, Bjartell A, Lilja H, Ståhle-Bäckdahl M, Borregaard N, Egesten A. The human cationic antimicrobial protein (hCAP-18) is expressed in the epithelium of human epididymis, is present in seminal plasma at high concentrations, and is attached to spermatozoa. Infect Immun 2000;68: 4297-302.
85. Gallo RL, Kim KJ, Bernfield M, Kozak CA, Zanetti M, Merluzzi L, Gennaro R. Identification of CRAMP, a cathelin-related antimicrobial peptide expressed in the embryonic and adult mouse. J Biol Chem 1997;272: 13088-93.
86. Sørensen OE, Follin P, Johnsen AH, Calafat J, Tjabringa GS, Hiemstra PS, Borregaard N. Human cathelicidin, hCAP-18, is processed to the antimicrobial peptide LL-37 by extracellular cleavage with proteinase 3. Blood 2001;97: 3951-9.
87. Pestonjamasp VK, Huttner KH, Gallo RL. Processing site and gene structure for the murine antimicrobial peptide CRAMP. Peptides 2001;22: 1643-50.
88. Chromek M, Slamová Z, Bergman P, Kovács L, Podracká L, Ehrán I, Hökfelt T, Gudmundsson GH, Gallo RL, Agerberth B, Brauner A. The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 2006;12: 636-41.
89. Serafini-Cessi F, Malagolini N, Cavallone D. TammHorsfall glycoprotein: biology and clinical relevance. Am J Kidney Dis 2003;42: 658-76.
90. Su SJ, Chang KL, Lin TM, Huang YH, Yeh TM. Uromodulin and Tamm-Horsfall protein induce human monocytes to secrete TNF and express tissue factor. J Immunol 1997;158: 3449-56.
91. Kreft B, Jabs WJ, Laskay T, Klinger M, Solbach W, Kumar S, van Zandbergen G. Polarized expression of Tamm-Horsfall protein by renal tubular epithelial cells activates human granulocytes. Infect Immun 2002;70: 2650-6.
92. Säemann MD, Weichhart T, Zeyda M, Staffler G, Schunn M, Stuhlmeier KM, Sobanov Y, Stulnig TM, Akira S, von Gabain A, von Ahsen U, Hörl WH, Zlabinger GJ. Tamm-Horsfall glycoprotein links innate immune cell activation with adaptive immunity via a Toll-like receptor-4-dependent mechanism. J Clin Invest 2005;115:468-75.
93. Bates JM, Raffi HM, Prasadan K, Mascarenhas R, Laszik Z, Maeda N, Hultgren SJ, Kumar S. Tamm-Horsfall protein knockout mice are more prone to urinary tract infection: rapid communication. Kidney Int 2004;65: 791-7.
94. El-Achkar TM, Wu XR, Rauchman M, McCracken R, Kiefer S, Dagher PC. Tamm-Horsfall protein protects the kidney from ischemic injury by decreasing inflammation and altering TLR4 expression. Am J Physiol Renal Physiol 2008;295:F 534-44.
95. Abrink M, Larsson E, Gobl A, Hellman L. Expression of lactoferrin in the kidney: implications for innate immunity and iron metabolism. Kidney Int 2000;57: 2004-10.
96. Berger T, Togawa A, Duncan GS, Elia AJ, You-Ten A, Wakeham A, Fong HE, Cheung CC, Mak TW. Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci USA 2006;103: 1834-9.
97. Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 2009;60: 379-406.
98. Srikrishna G, Freeze HH. Endogenous damage-associated molecular pattern molecules at the crossroads of inflammation and cancer. Neoplasia 2009;11: 615-28.
99. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004;279: 7370-7.
100. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005;201: 1135-43.
101. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ, Tracey KJ, Yang H. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2. Shock 2006;26: 174-9.
102. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 2002;277: 15107-12.
103. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, Stevenson MA, Calderwood SK. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem 2002;277: 15028-34.
104. Ohashi K, Burkart V, Flohé S, Kolb H. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J Immunol 2000;164: 558-61.
105. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 2001;167: 2887-94.
106. Okamura Y, Watari M, Jerud ES, Young DW, Ishizaka ST, Rose J, Chow JC, Strauss JF 3rd. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem 2001;276: 10229-33.
107. Guillot L, Balloy V, McCormack FX, Golenbock DT, Chignard M, Si-Tahar M. Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. J Immunol 2002;168: 5989-92.
108. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, Chertov O, Shirakawa AK, Farber JM, Segal DM, Oppenheim JJ, Kwak LW. Toll-like receptor 4- dependent activation of dendritic cells by beta-defensin 2. Science 2002;298: 1025-9.
109. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003;425: 516-21.
110. Termeer C, Benedix F, Sleeman J, Fieber C, Voith U, Ahrens T, Miyake K, Freudenberg M, Galanos C, Simon JC. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002;195:99-111.
111. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, Krzyzankova M, Marsche G, Young MF, Mihalik D, Götte M, Malle E, Schaefer RM, Gröne HJ. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 2005;115: 2223-33.
112. Johnson GB, Brunn GJ, Kodaira Y, Platt JL. Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 2002;168: 5233-9.
113. Ishii KJ, Suzuki K, Coban C, Takeshita F, Itoh Y, Matoba H, Kohn LD, Klinman DM. Genomic DNA released by dying cells induces the maturation of APCs. J Immunol 2001;167: 2602-7.
114. Karikó K, Ni H, Capodici J, Lamphier M, Weissman D. mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 2004;279: 12542-50.
115. Thomas JO, Travers AA. HMG1 and 2, and related 'architectural' DNA-binding proteins. Trends Biochem Sci 2001;26: 167-74.
116. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418: 191-5.
117. Rucci A, Palumbo R, Bianchi ME. HMGB1: a signal of necrosis. Autoimmunity 2007;40: 285-9.
118. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 2005;201: 1135-43.
119. Zhai Y, Shen XD, O'Connell R, Gao F, Lassman C, Busuttil RW, Cheng G, Kupiec-Weglinski JW. Cutting edge: TLR4 activation mediates liver ischemia/reperfusion inflammatory response via IFN regulatory factor 3dependent MyD88-independent pathway. J Immunol 2004;173: 7115-9.
120. Oyama J, Blais Jr C, Liu X, Pu M, Kobzik L, Kelly RA, Bourcier T. Reduced myocardial ischemia-reperfusion injury in toll-like receptor 4-deficient mice. Circulation 2004;109: 784-9.
121. Barsness KA, Arcaroli J, Harken AH, Abraham E, Banerjee A, Reznikov L, McIntyre RC. Hemorrhageinduced acute lung injury is TLR-4 dependent. Am J Physiol Regul Integr Comp Physiol 2004;287:R 592-9.
122. Prince JM, Levy RM, Yang R, Mollen KP, Fink MP, Vodovotz Y, Billiar TR. Toll-like receptor-4 signaling mediates hepatic injury and systemic inflammation in hemorrhagic shock. J Am Coll Surg 2006;202: 407-17.
123. Leemans JC, Stokman G, Claessen N, Rouschop KM, Teske GJ, Kirschning CJ, Akira S, van der Poll T, Weening JJ, Florquin S. Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest 2005;115: 2894-903.
124. Wu H, Chen G, Wyburn KR, Yin J, Bertolino P, Eris JM, Alexander SI, Sharland AF, Chadban SJ. TLR4 activation mediates kidney ischemia/reperfusion injury. J Clin Invest 2007;117: 2847-59.
125. 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 2005;79: 1370-7.
126. Shigeoka AA, Holscher TD, King AJ, Hall FW, Kiosses WB, Tobias PS, Mackman N, McKay DB. TLR2 is constitutively expressed within the kidney and participates in ischemic renal injury through both MyD88-dependent and -independent pathways. J Immunol 2007;178:6252-8.
127. Chakraborti T, Das S, Mondal M, Roychoudhury S, Chakraborti S. Oxidant, mitochondria and calcium: an overview. Cell Signal 1999;11: 77-85.
128. Nakano H, Nakajima A, Sakon-Komazawa S, Piao JH, Xue X, Okumura K. Reactive oxygen species mediate crosstalk between NF-kappaB and JNK. Cell Death Differ 2006;13: 730-7.
129. Matsuzawa A, IchijoH. Stress-responsive protein kinases in redox-regulated apoptosis signaling. Antioxid Redox Signal 2005;7: 472-81.
130. Ichijo H, Nishida E, Irie K, ten Dijke P, Saitoh M, Moriguchi T, Takagi M, Matsumoto K, Miyazono K, Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 1997;275: 90-4.
131. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, Takeda K, Minowa O, Miyazono K, Noda T, Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001;2: 222-8.
132. Wang X, McCullough KD, Franke TF, Holbrook NJ. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 2000;275: 14624-31.
133. Stefanelli C, Tantini B, Fattori M, Stanic' I, Pignatti C, Clo C, Guarnieri C, Caldarera CM, Mackintosh CA, Pegg AE, Flamigni F. Caspase activation in etoposidetreated fibroblasts is correlated to ERK phosphorylation and both events are blocked by polyamine depletion. FEBS Lett 2002;527: 223-8.
134. Sarró E, Tornavaca O, Plana M, Meseguer A, Itarte E. Phosphoinositide 3-kinase inhibitors protect mouse kidney cells from cyclosporine-induced cell death. Kidney Int 2008;73: 77-85.
135. Guyton KZ, Liu Y, Gorospe M, Xu Q, Holbrook NJ. Activation of mitogen-activated protein kinase by H2O2. Role in cell survival following oxidant injury. J Biol Chem 1996;271: 4138-42.
136. Hung CC, Ichimura T, Stevens JL, Bonventre JV. Protection of renal epithelial cells against oxidative injury by endoplasmic reticulum stress preconditioning is mediated by ERK1/2 activation. J Biol Chem 2003;278: 29317-26.
137. Hu P, Han Z, Couvillon AD, Exton JH. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J Biol Chem 2004;279: 49420-9.
138. Mkaddem SB, Werts C, Goujon JM, Bens M, Pedruzzi E, Ogier-Denis E, Vandewalle A. Heat shock protein gp96 interacts with protein phosphatase 5 and controls toll-like receptor 2 (TLR2)-mediated activation of extracellular signal-regulated kinase (ERK) 1/2 in post-hypoxic kidney cells. J Biol Chem 2009;284: 12541-9.
139. von Kriegsheim A, Pitt A, Grindlay GJ, Kolch W, Dhillon AS. Regulation of the Raf-MEK-ERK pathway by protein phosphatase 5. Nat Cell Biol 2006;8: 1011-6.
140. Randow F, Seed B. Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability. Nat Cell Biol 2001;3: 891-6.
141. Yang Y, Liu B, Dai J, Srivastava PK, Zammit DJ, Lefrançois L, Li Z. Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 2007;26:215-26.
142. Cunningham PN, Wang Y, Guo R, He G, Quigg RJ. Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J Immunol 2004;172: 2629-35.
143. Ducloux D, Deschamps M, Yannaraki M, Ferrand C, Bamoulid J, Saas P, Kazory A, Chalopin JM, Tiberghien P. Relevance of Toll-like receptor-4 polymorphisms in renal transplantation. Kidney Int 2005;67: 2454-61.
144. Palmer SM, Burch LH, Mir S, Smith SR, Kuo PC, Herczyk WF, Reinsmoen NL, Schwartz DA. Donor polymorphisms in Toll-like receptor-4 influence the development of rejection after renal transplantation. Clin Transplant 2006;20: 30-6.
145. Nogueira E, Ozaki KS, Macusso GD, Quarim RF, Câmara NO, Pacheco-Silva A. Incidence of donor and recipient toll-like receptor-4 polymorphisms in kidney transplantation. Transplant Proc 2007;39: 412-4.
146. Braudeau C, Ashton-Chess J, Giral M, Dugast E, Louis S, Pallier A, Braud C, Moreau A, Renaudin K, Soulillou JP, Brouard S. Contrasted blood and intragraft toll-like receptor 4 mRNA profiles in operational tolerance versus chronic rejection in kidney transplant recipients. Transplantation 2008;86: 130-6.
147. Krüger B, Krick S, Dhillon N, Lerner SM, Ames S, Bromberg JS, Lin M, Walsh L, Vella J, Fischereder M, Krämer BK, Colvin RB, Heeger PS, Murphy BT, Schröppel B. Donor Toll-like receptor 4 contributes to ischemia and reperfusion injury following human kidney transplantation. Proc Natl Acad Sci USA 2009;106:3390-5.
148. Lane MC, Lockatell V, Monterosso G, Lamphier D, Weinert J, Hebel JR, Johnson DE, Mobley HL. Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect Immun 2005;73: 7644-56.
149. Lane MC, Alteri CJ, Smith SN, Mobley HL. Expression of flagella is coincident with uropathogenic Escherichia coli ascension to the upper urinary tract. Proc Natl Acad Sci USA 2007;104: 16669-74.
150. Wright KJ, Seed PC, Hultgren SJ. Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun 2005;73: 7657-68.
151. Pichon C, Háchard C, du Merle L, Chaudray C, Bonne I, Guadagnini S, Vandewalle A, Le Bouguénec C. Uropathogenic Escherichia coli AL511 requires flagellum to enter renal collecting duct cells. Cell Microbiol 2009;11: 616-28.
152. Hawn TR, Scholes D, Li SS, Wang H, Yang Y, Roberts PL, Stapleton AE, Janer M, Aderem A, Stamm WE, Zhao LP, Hooton TM. Toll-like receptor polymorphisms and susceptibility to urinary tract infections in adult women. PLoS One 2009;4:e5990.