Toll-like receptors and their role in renal pathologies

Inflammation and Allergy - Drug Targets

Volumn 11, Issue 6, 2012, Pages 464-477

  Eleftheriadis, Theodoros ^a   Pissas, Georgios ^a   Liakopoulos, Vassilios ^a   Stefanidis, Ioannis ^a   Lawson, Brian R ^b  

^a UNIVERSITY OF THESSALY   (Greece)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Fibrosis; Glomerulonephritis; Ischemia reperfusion injury; Kidney; Sepsis; Toll like receptors; Urinary tract infection

Indexed keywords

CD14 ANTIGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; PATTERN RECOGNITION RECEPTOR; RANTES; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 11; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNINDEXED DRUG;

ANTIGEN EXPRESSION; ARTICLE; GENETIC PREDISPOSITION; HAZARD; HEPATITIS C VIRUS; HUMAN; IMMUNOPATHOGENESIS; KIDNEY DISEASE; KIDNEY FAILURE; KIDNEY FIBROSIS; KIDNEY ISCHEMIA; MAJOR HISTOCOMPATIBILITY COMPLEX; MEMBRANOPROLIFERATIVE GLOMERULONEPHRITIS; MOLECULAR RECOGNITION; NONHUMAN; REPERFUSION INJURY; SEPSIS; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; URINARY TRACT INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; HUMANS; IMMUNITY, INNATE; KIDNEY; KIDNEY DISEASES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84870280094     PISSN: 18715281     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152812803589994     Document Type: Article

References (117)

1. Eleftheriadis, T.; Lawson, B.R. Toll-like receptors and kidney diseases. Inflamm. Allergy Drug Targets, 2009, 8(3), 191-201.
2. Poltorak, A.; He, X.; Smirnova, I.; Liu, M.Y.; 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(5396), 2085-2088.
3. Kawai, T.; Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunolo., 2010, 11(5), 373-384.
4. Janeway, C.A. Jr. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today, 1992, 13(1), 11-16.
5. Matzinger, P. The danger model: a renewed sense of self. Science, 2002, 296(5566), 301-305.
6. Baccala, R.; Gonzalez-Quintial, R.; Lawson, B.R.; Stern, M.E.; Kono, D.H.; Beutler, B.; Theofilopoulos, A.N. Sensors of the innate immune system: their mode of action. Nat. Rev. Rheumatol., 2009, 5(8), 448-456.
7. Garraud, O.; Cognasse, F. Platelet Toll-like receptor expression: the link between danger ligands and inflammation. Inflamm. Allergy Drug Targets, 2010, 9(5), 322-333.
8. Eleftheriadis, T.; Liakopoulos, V.; Lawson, B.; Antoniadi, G.; Stefanidis, I.; Galaktidou, G. Lipopolysaccharide and hypoxia significantly alters interleukin-8 and macrophage chemoattractant protein-1 production by human fibroblasts but not fibrosis related factors. Hippokratia, 2011, 15(3), 238-243.
9. Imani Fooladi, A.A.; Mousavi, S.F.; Seghatoleslami, S.; Yazdani, S.; Nourani, M.R. Toll-like receptors: role of inflammation and commensal bacteria. Inflamm. Allergy Drug Targets, 2011, 10(3), 198-207.
10. Fallach, R.; Shainberg, A.; Avlas, O.; Fainblut, M.; Chepurko, Y.; Porat, E.; Hochhauser, E. Cardiomyocyte Toll-like receptor 4 is involved in heart dysfunction following septic shock or myocardial ischemia. J. Mol. Cellular Cardiol., 2010, 48(6), 1236-1244.
11. Tsung, A.; Sahai, R.; Tanaka, H.; Nakao, A.; Fink, M.P.; Lotze, M.T.; Yang, H.; Li, J.; Tracey, K.J.; Geller, D.A.; Billiar, T.R. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Medi., 2005, 201(7), 1135-1143.
12. Guillot, L.; Medjane, S.; Le-Barillec, K.; Balloy, V.; Danel, C.; Chignard, M.; Si-Tahar, M. Response of human pulmonary epithelial cells to lipopolysaccharide involves Toll-like receptor 4 (TLR4)-dependent signaling pathways: evidence for an intracellular compartmentalization of TLR4. J. Biol. Chem., 2004, 279(4), 2712-2718.
13. Theofilopoulos, A.N.; Kono, D.H.; Beutler, B.; Baccala, R. Intracellular nucleic acid sensors and autoimmunity. J. Interferon Cytokine Res., 2011, 31(12), 867-886.
14. Salaun, B.; Romero, P.; Lebecque, S. Toll-like receptors' twoedged sword: when immunity meets apoptosis. Eur. J. Immunol., 2007, 37(12), 3311-3318.
15. Ioannou, S.; Voulgarelis, M. Toll-like receptors, tissue injury, and tumourigenesis. Mediators Inflamm., 2010, 2010.
16. Macedo, L.; Pinhal-Enfield, G.; Alshits, V.; Elson, G.; Cronstein, B.N.; Leibovich, S.J. Wound healing is impaired in MyD88-deficient mice: a role for MyD88 in the regulation of wound healing by adenosine A2A receptors. Am. J. Pathol., 2007, 171(6), 1774-1788.
17. Farrar, C.A.; Keogh, B.; McCormack, W.; O'Shaughnessy, A.; Parker, A.; Reilly, M.; Sacks, S.H. Inhibition of TLR2 promotes graft function in a murine model of renal transplant ischemiareperfusion injury. FASEB, 2012, 26(2), 799-807.
18. Kumar, H.; Kawai, T.; Akira, S. Pathogen recognition by the innate immune system. Int. Rev. Immunol., 2011, 30(1), 16-34.
19. Beg, A.A. Endogenous ligands of Toll-like receptors: implications for regulating inflammatory and immune responses. Trends Immunol., 2002, 23(11), 509-512.
20. Atkinson, T.J. Toll-like receptors, transduction-effector pathways, and disease diversity: evidence of an immunobiological paradigm explaining all human illness? Int. Rev. Immunol., 2008, 27(4), 255-281.
21. Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell, 2010, 140(6), 805-820.
22. Aliprantis, A.O.; Yang, R.B.; Weiss, D.S.; Godowski, P.; Zychlinsky, A. The apoptotic signaling pathway activated by Tolllike receptor-2. EMBO J., 2000, 19(13), 3325-3336.
23. Kaiser, W.J.; Offermann, M.K. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol., 2005, 174(8), 4942-4952.
24. Zhang, Y.; Peng, T.; Zhu, H.; Zheng, X.; Zhang, X.; Jiang, N.; Cheng, X.; Lai, X.; Shunnar, A.; Singh, M.; Riordan, N.; Bogin, V.; Tong, N.; Min, W.P. Prevention of hyperglycemia-induced myocardial apoptosis by gene silencing of Toll-like receptor-4. J. Transl. Med., 2010, 8, 133.
25. 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(2), 267-277.
26. Scherberich, J.E.; Hartinger, A. Impact of Toll-like receptor signalling on urinary tract infection. Int. J. Antimicrob. Agents, 2008, 31 Suppl 1, S9-S14.
27. Chassin, C.; Vimont, S.; Cluzeaud, F.; Bens, M.; Goujon, J.M.; Fernandez, B.; Hertig, A.; Rondeau, E.; Arlet, G.; Hornef, M.W.; Vandewalle, A. TLR4 facilitates translocation of bacteria across renal collecting duct cells. J. Am. Soc. Nephrol., 2008, 19(12), 2364-2374.
28. Schilling, J.D.; Mulvey, M.A.; Vincent, C.D.; Lorenz, R.G.; Hultgren, S.J. Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharidedependent mechanism. J. Immunol., 2001, 166(2), 1148-1155.
29. Schilling, J.D.; Martin, S.M.; Hung, C.S.; Lorenz, R.G.; Hultgren, S.J. Toll-like receptor 4 on stromal and hematopoietic cells mediates innate resistance to uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA., 2003, 100(7), 4203-4208.
30. Patole, P.S.; Schubert, S.; Hildinger, K.; Khandoga, S.; Khandoga, A.; Segerer, S.; Henger, A.; Kretzler, M.; Werner, M.; Krombach, F.; Schlondorff, D.; Anders, H.J. Toll-like receptor-4: renal cells and bone marrow cells signal for neutrophil recruitment during pyelonephritis. Kidney intl., 2005, 68(6), 2582-2587.
31. Chassin, C.; Goujon, J.M.; Darche, S.; du Merle, L.; Bens, M.; Cluzeaud, F.; Werts, C.; Ogier-Denis, E.; Le Bouguenec, 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(7), 4773-4784.
32. Andersen-Nissen, E.; Hawn, T.R.; Smith, K.D.; Nachman, A.; Lampano, A.E.; Uematsu, S.; Akira, S.; Aderem, A. Cutting edge: Tlr5-/- mice are more susceptible to Escherichia coli urinary tract infection. J. Immunol., 2007, 178(8), 4717-4720.
33. Zhang, D.; Zhang, G.; Hayden, M.S.; Greenblatt, M.B.; Bussey, C.; Flavell, R.A.; Ghosh, S. A toll-like receptor that prevents infection by uropathogenic bacteria. Science, 2004, 303(5663), 1522-1526.
34. Cirl, C.; Wieser, A.; Yadav, M.; Duerr, S.; Schubert, S.; Fischer, H.; Stappert, D.; Wantia, N.; Rodriguez, N.; Wagner, H.; Svanborg, C.; Miethke, T. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domaincontaining proteins. Nat. Med., 2008, 14(4), 399-406.
35. Yadav, M.; Zhang, J.; Fischer, H.; Huang, W.; Lutay, N.; Cirl, C.; Lum, J.; Miethke, T.; Svanborg, C. Inhibition of TIR domain signaling by TcpC: MyD88-dependent and independent effects on Escherichia coli virulence. PLoS Pathogens, 2010, 6(9), e1001120.
36. Justice, S.S.; Hunstad, D.A.; Seed, P.C.; Hultgren, S.J. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc. Natl. Acad. Sci. USA, 2006, 103(52), 19884-19889.
37. Ragnarsdottir, B.; Samuelsson, M.; Gustafsson, M.C.; Leijonhufvud, I.; Karpman, D.; Svanborg, C. Reduced toll-like receptor 4 expression in children with asymptomatic bacteriuria. The Journal of infectious diseases, 2007, 196(3), 475-484.
38. Ragnarsdottir, B.; Jonsson, K.; Urbano, A.; Gronberg-Hernandez, J.; Lutay, N.; Tammi, M.; Gustafsson, M.; Lundstedt, A.C.; Leijonhufvud, I.; Karpman, D.; Wullt, B.; Truedsson, L.; Jodal, U.; Andersson, B.; Svanborg, C. Toll-like receptor 4 promoter polymorphisms: common TLR4 variants may protect against severe urinary tract infection. PloS one, 2010, 5(5), e10734.
39. Karoly, E.; Fekete, A.; Banki, N.F.; Szebeni, B.; Vannay, A.; Szabo, A.J.; Tulassay, T.; Reusz, G.S. Heat shock protein 72 (HSPA1B) gene polymorphism and Toll-like receptor (TLR) 4 mutation are associated with increased risk of urinary tract infection in children. Pediatr. Res., 2007, 61(3), 371-374.
40. Yin, X.; Hou, T.; Liu, Y.; Chen, J.; Yao, Z.; Ma, C.; Yang, L.; Wei, L. Association of Toll-like receptor 4 gene polymorphism and expression with urinary tract infection types in adults. PloS One, 2010, 5(12), e14223.
41. Tabel, Y.; Berdeli, A.; Mir, S. Association of TLR2 gene Arg753Gln polymorphism with urinary tract infection in children. Int. J. Immunogenet, 2007, 34(6), 399-405.
42. Saemann, M.D.; Weichhart, T.; Zeyda, M.; Staffler, G.; Schunn, M.; Stuhlmeier, K.M.; Sobanov, Y.; Stulnig, T.M.; Akira, S.; von Gabain, A.; von Ahsen, U.; Horl, W.H.; Zlabinger, G.J. Tamm-Horsfall glycoprotein links innate immune cell activation with adaptive immunity via a Toll-like receptor-4-dependent mechanism. J. Clin. Invest., 2005, 115(2), 468-475.
43. Raffi, H.S.; Bates, J.M. Jr.; Laszik, Z.; Kumar, S. Tamm-Horsfall protein acts as a general host-defense factor against bacterial cystitis. Am. J. Nephrol., 2005, 25(6), 570-578.
44. Schrier, R.W.; Wang, W. Acute renal failure and sepsis. New Engl. J. Med., 2004, 351(2), 159-169.
45. Cohen, J. The immunopathogenesis of sepsis. Nature, 2002, 420(6917), 885-891.
46. Sutton, T.A. Alteration of microvascular permeability in acute kidney injury. Microvascular Res., 2009, 77(1), 4-7.
47. Le Dorze, M.; Legrand, M.; Payen, D.; Ince, C. The role of the microcirculation in acute kidney injury. Curr. Opin. Crit. Care, 2009, 15(6), 503-508.
48. Good, D.W.; George, T.; Watts, B.A. 3rd, Lipopolysaccharide directly alters renal tubule transport through distinct TLR4-dependent pathways in basolateral and apical membranes. Am. J. Physiol. Renal Physiol., 2009, 297(4), F866-874.
49. Watts, B.A. 3rd; George, T.; Sherwood, E.R.; Good, D.W. Basolateral LPS inhibits NHE3 and HCOFormula absorption through TLR4/MyD88-dependent ERK activation in medullary thick ascending limb. Am. J. Physiol. Renal Physiol., 2011, 301(6), C1296-C1306.
50. Marino, M.W.; Dunn, A.; Grail, D.; Inglese, M.; Noguchi, Y.; Richards, E.; Jungbluth, A.; Wada, H.; Moore, M.; Williamson, B.; Basu, S.; Old, L.J. Characterization of tumor necrosis factordeficient mice. Proc. Natl. Acad. Sci. USA, 1997, 94(15), 8093-8098.
51. Abraham, E.; Wunderink, R.; Silverman, H.; Perl, T.M.; Nasraway, S.; Levy, H.; Bone, R.; Wenzel, R.P.; Balk, R.; Allred, R.; et al. Efficacy and safety of monoclonal antibody to human tumor necrosis factor alpha in patients with sepsis syndrome. A randomized, controlled, double-blind, multicenter clinical trial. TNF-alpha MAb Sepsis Study Group. JAMA, 1995, 273(12), 934-941.
52. Fisher, C.J. Jr.; Agosti, J.M.; Opal, S.M.; Lowry, S.F.; Balk, R.A.; Sadoff, J.C.; Abraham, E.; Schein, R.M.; Benjamin, E. Treatment of septic shock with the tumor necrosis factor receptor:Fc fusion protein. The Soluble TNF Receptor Sepsis Study Group. New Engl. J. Med., 1996, 334(26), 1697-1702.
53. Knotek, M.; Rogachev, B.; Wang, W.; Ecder, T.; Melnikov, V.; Gengaro, P.E.; Esson, M.; Edelstein, C.L.; Dinarello, C.A.; Schrier, R.W. Endotoxemic renal failure in mice: Role of tumor necrosis factor independent of inducible nitric oxide synthase. Kidney int., 2001, 59(6), 2243-2249.
54. Rodrigues, C.E.; Sanches, T.R.; Volpini, R.A.; Shimizu, M.H.; Kuriki, P.S.; Camara, N.O.; Seguro, A.C.; Andrade, L. Effects of continuous erythropoietin receptor activator in sepsis-induced acute kidney injury and multi-organ dysfunction. PloS one, 2012, 7(1), e29893.
55. Nakamura, A.; Niimi, R.; Yanagawa, Y. Protection from sepsisinduced acute renal failure by adenoviral-mediated gene transfer of beta2-adrenoceptor. PLoS One, 2010, 25(3), 730-737.
56. Dear, J.W.; Yasuda, H.; Hu, X.; Hieny, S.; Yuen, P.S.; Hewitt, S.M.; Sher, A.; Star, R.A. Sepsis-induced organ failure is mediated by different pathways in the kidney and liver: acute renal failure is dependent on MyD88 but not renal cell apoptosis. Kidney int., 2006, 69(5), 832-836.
57. Wang, J.E.; Dahle, M.K.; Yndestad, A.; Bauer, I.; McDonald, M.C.; Aukrust, P.; Foster, S.J.; Bauer, M.; Aasen, A.O.; Thiemermann, C. Peptidoglycan of Staphylococcus aureus causes inflammation and organ injury in the rat. Crit. Care Med., 2004, 32(2), 546-552.
58. Good, D.W.; George, T.; Watts, B.A. 3rd, Toll-like receptor 2 mediates inhibition of HCO(3)(-) absorption by bacterial lipoprotein in medullary thick ascending limb. Am. J. Physiol. Renal Physiol., 2010, 299(3), F536-F544.
59. Cunningham, P.N.; Wang, Y.; Guo, R.; He, G.; Quigg, R.J. Role of Toll-like receptor 4 in endotoxin-induced acute renal failure. J. Immunol., 2004, 172(4), 2629-2635.
60. Shimazu, R.; Akashi, S.; Ogata, H.; Nagai, Y.; Fukudome, K.; Miyake, K.; Kimoto, M. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med., 1999, 189(11), 1777-1782.
61. Kitchens, R.L. Role of CD14 in cellular recognition of bacterial lipopolysaccharides. Chem. Immunol., 2000, 74, 61-82.
62. Bussolati, B.; David, S.; Cambi, V.; Tobias, P.S.; Camussi, G. Urinary soluble CD14 mediates human proximal tubular epithelial cell injury induced by LPS. Int. J. Mol. Med., 2002, 10(4), 441-449.
63. El-Achkar, T.M.; Huang, X.; Plotkin, Z.; Sandoval, R.M.; Rhodes, G.J.; Dagher, P.C. Sepsis induces changes in the expression and distribution of Toll-like receptor 4 in the rat kidney. American journal of physiology. Renal physiol., 2006, 290(5), F1034-1043.
64. Nakamura, A.; Niimi, R.; Yanagawa, Y. Renal beta(2)-adrenoceptor modulates the lipopolysaccharide transport system in sepsis-induced acute renal failure. Inflammation, 2009, 32(1), 12-19.
65. Pugin, J.; Stern-Voeffray, S.; Daubeuf, B.; Matthay, M.A.; Elson, G.; Dunn-Siegrist, I. Soluble MD-2 activity in plasma from patients with severe sepsis and septic shock. Blood, 2004, 104(13), 4071-4079.
66. Yasuda, H.; Leelahavanichkul, A.; Tsunoda, S.; Dear, J.W.; Takahashi, Y.; Ito, S.; Hu, X.; Zhou, H.; Doi, K.; Childs, R.; Klinman, D.M.; Yuen, P.S.; Star, R.A. Chloroquine and inhibition of Toll-like receptor 9 protect from sepsis-induced acute kidney injury. Am. J. Physiol. Renal Physiol., 2008, 294(5), F1050-F1058.
67. Barton, G.M.; Kagan, J.C.; Medzhitov, R. Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat. Immunol., 2006, 7(1), 49-56.
68. Zeerleder, S.; Zwart, B.; Wuillemin, W.A.; Aarden, L.A.; Groeneveld, A.B.; Caliezi, C.; van Nieuwenhuijze, A.E.; van Mierlo, G.J.; Eerenberg, A.J.; Lammle, B.; Hack, C.E. Elevated nucleosome levels in systemic inflammation and sepsis. Crit. Care Med., 2003, 31(7), 1947-1951.
69. Martins, G.A.; Kawamura, M.T.; Carvalho Mda, G. Detection of DNA in the plasma of septic patients. Ann. N Y Acad. Sci., 2000, 906, 134-140.
70. McKay, D.B. Intracellular pattern recognition receptors and renal ischemia. Crit. Rev. Immunol., 2011, 31(4), 297-306.
71. Friedewald, J.J.; Rabb, H. Inflammatory cells in ischemic acute renal failure. Kidney Int., 2004, 66(2), 486-491.
72. Burne, M.J.; Daniels, F.; El Ghandour, A.; Mauiyyedi, S.; Colvin, R.B.; O'Donnell, M.P.; Rabb, H. Identification of the CD4(+) T cell as a major pathogenic factor in ischemic acute renal failure. J. Clin. Invest., 2001, 108(9), 1283-1290.
73. Wolfs, T.G.; Buurman, W.A.; van Schadewijk, A.; de Vries, B.; Daemen, M.A.; Hiemstra, P.S.; 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(3), 1286-1293.
74. Shigeoka, A.A.; Holscher, T.D.; King, A.J.; Hall, F.W.; Kiosses, W.B.; Tobias, P.S.; Mackman, N.; McKay, D.B. TLR2 is constitutively expressed within the kidney and participates in ischemic renal injury through both MyD88-dependent and - independent pathways. J. Immunol., 2007, 178(10), 6252-6258.
75. Leemans, J.C.; Stokman, G.; Claessen, N.; Rouschop, K.M.; Teske, G.J.; Kirschning, C.J.; Akira, S.; van der Poll, T.; Weening, J.J.; Florquin, S. Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J. C. Invest., 2005, 115(10), 2894-2903.
76. Wu, H.; Chen, G.; Wyburn, K.R.; Yin, J.; Bertolino, P.; Eris, J.M.; Alexander, S.I.; Sharland, A.F.; Chadban, S.J. TLR4 activation mediates kidney ischemia/reperfusion injury. J. Clin. Invest., 2007, 117(10), 2847-2859.
77. Rusai, K.; Sollinger, D.; Baumann, M.; Wagner, B.; Strobl, M.; Schmaderer, C.; Roos, M.; Kirschning, C.; Heemann, U.; Lutz, J. Toll-like receptors 2 and 4 in renal ischemia/reperfusion injury. Pediatr. Nephrol., 2010, 25(5), 853-860.
78. Wang, S.; Schmaderer, C.; Kiss, E.; Schmidt, C.; Bonrouhi, M.; Porubsky, S.; Gretz, N.; Schaefer, L.; Kirschning, C.J.; Popovic, Z.V.; Grone, H.J. Recipient Toll-like receptors contribute to chronic graft dysfunction by both MyD88- and TRIF-dependent signaling. Dis. Models Mech., 2010, 3(1-2), 92-103.
79. Kim, B.S.; Lim, S.W.; Li, C.; Kim, J.S.; Sun, B.K.; Ahn, K.O.; Han, S.W.; Kim, J.; Yang, C.W. Ischemia-reperfusion injury activates innate immunity in rat kidneys. Transplantation, 2005, 79(10), 1370-1377.
80. Kruger, B.; Krick, S.; Dhillon, N.; Lerner, S.M.; Ames, S.; Bromberg, J.S.; Lin, M.; Walsh, L.; Vella, J.; Fischereder, M.; Kramer, B.K.; Colvin, R.B.; Heeger, P.S.; Murphy, B.T.; Schroppel, B. Donor Toll-like receptor 4 contributes to ischemia and reperfusion injury following human kidney transplantation. Proc. Natl. Acad. Sci. USA, 2009, 106(9), 3390-3395.
81. El-Achkar, T.M.; Wu, X.R.; Rauchman, M.; McCracken, R.; Kiefer, S.; Dagher, P.C. Tamm-Horsfall protein protects the kidney from ischemic injury by decreasing inflammation and altering TLR4 expression. Am. J. Physiol. Renal Physiol., 2008, 295(2), F534-544.
82. Kuo, M.C.; Patschan, D.; Patschan, S.; Cohen-Gould, L.; Park, H.C.; Ni, J.; Addabbo, F.; Goligorsky, M.S. Ischemia-Induced Exocytosis of Weibel-Palade Bodies Mobilizes Stem Cells. J. Am. Soc. Nephrol., 2008, 19, 2321-2330.
83. Reiser, J.; von Gersdorff, G.; Loos, M.; Oh, J.; Asanuma, K.; Giardino, L.; Rastaldi, M.P.; Calvaresi, N.; Watanabe, H.; Schwarz, K.; Faul, C.; Kretzler, M.; Davidson, A.; Sugimoto, H.; Kalluri, R.; Sharpe, A.H.; Kreidberg, J.A.; Mundel, P., Induction of B7-1 in podocytes is associated with nephrotic syndrome. J. Clin. Invest., 2004, 113(10), 1390-1397.
84. Wornle, M.; Schmid, H.; Banas, B.; Merkle, M.; Henger, A.; Roeder, M.; Blattner, S.; Bock, E.; Kretzler, M.; Grone, H.J.; Schlondorff, D. Novel role of toll-like receptor 3 in hepatitis Cassociated glomerulonephritis. Am. J. Pathol., 2006, 168(2), 370-385.
85. Merkle, M.; Ribeiro, A.; Wornle, M. TLR3-dependent regulation of cytokines in human mesangial cells: a novel role for IP-10 and TNF-alpha in hepatitis C-associated glomerulonephritis. Am. J. Physiol. Renal Physiol., 2011, 301 (1), F57-F69.
86. Anders, H.J.; Vielhauer, V.; Eis, V.; Linde, Y.; Kretzler, M.; Perez de Lema, G.; Strutz, F.; Bauer, S.; Rutz, M.; Wagner, H.; Grone, H.J.; Schlondorff, D. Activation of toll-like receptor-9 induces progression of renal disease in MRL-Fas(lpr) mice. FASEB J., 2004, 18(3), 534-536.
87. Patole, P.S.; Zecher, D.; Pawar, R.D.; Grone, H.J.; Schlondorff, D.; Anders, H.J. G-rich DNA suppresses systemic lupus. J. Am. Soc. Nephrol., 2005, 16 (11), 3273-3280.
88. Graham, K.L.; Lee, L.Y.; Higgins, J.P.; Steinman, L.; Utz, P.J.; Ho, P.P. Treatment with a toll-like receptor inhibitory GpG oligonucleotide delays and attenuates lupus nephritis in NZB/W mice. Autoimmunity, 2010, 43 (2), 140-155.
89. Pawar, R.D.; Patole, P.S.; Ellwart, A.; Lech, M.; Segerer, S.; Schlondorff, D.; Anders, H.J. Ligands to nucleic acid-specific tolllike receptors and the onset of lupus nephritis. J. Am. Soc. Nephrol., 2006, 17(12), 3365-3373.
90. Christensen, S.R.; Kashgarian, M.; Alexopoulou, L.; Flavell, R.A.; Akira, S.; Shlomchik, M.J. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J. Exp. Med., 2005, 202(2), 321-331.
91. Yu, P.; Wellmann, U.; Kunder, S.; Quintanilla-Martinez, L.; Jennen, L.; Dear, N.; Amann, K.; Bauer, S.; Winkler, T.H.; Wagner, H. Toll-like receptor 9-independent aggravation of glomerulonephritis in a novel model of SLE. Int. Immunol., 2006, 18(8), 1211-1219.
92. Machida, H.; Ito, S.; Hirose, T.; Takeshita, F.; Oshiro, H.; Nakamura, T.; Mori, M.; Inayama, Y.; Yan, K.; Kobayashi, N.; Yokota, S. Expression of Toll-like receptor 9 in renal podocytes in childhood-onset active and inactive lupus nephritis. Nephrol. Dial. Transplant, 2010, 25(8), 2530-2537.
93. Frieri, M.; Samih, M.A.; Dzhindzhikhashvili, M.; Liu, H.; Balsam, L.; Rubinstein, S. Toll-like receptor 9 and vascular endothelial growth factor levels in human kidneys from lupus nephritis patients. J. Nephrol., 2012, [Epub ahead of print].
94. Patole, P.S.; Grone, H.J.; Segerer, S.; Ciubar, R.; Belemezova, E.; Henger, A.; Kretzler, M.; Schlondorff, D.; Anders, H.J. 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(5), 1326-1338.
95. Sadanaga, A.; Nakashima, H.; Akahoshi, M.; Masutani, K.; Miyake, K.; Igawa, T.; Sugiyama, N.; Niiro, H.; Harada, M. Protection against autoimmune nephritis in MyD88-deficient MRL/lpr mice. Arthritis Rheum., 2007, 56(5), 1618-1628.
96. Akira, S.; Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol., 2004, 4(7), 499-511.
97. Krishnan, J.; Selvarajoo, K.; Tsuchiya, M.; Lee, G.; Choi, S. Tolllike receptor signal transduction. Exp. Mol. Med., 2007, 39(4), 421-438.
98. Baccala, R.; Hoebe, K.; Kono, D.H.; Beutler, B.; Theofilopoulos, A.N. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat. Med., 2007, 13(5), 543-551.
99. Pawar, R.D.; Patole, P.S.; Zecher, D.; Segerer, S.; Kretzler, M.; Schlondorff, D.; Anders, H.J. Toll-like receptor-7 modulates immune complex glomerulonephritis. J. Am. Soc. Nephrol., 2006, 17(1), 141-149.
100. Pawar, R.D.; Ramanjaneyulu, A.; Kulkarni, O.P.; Lech, M.; Segerer, S.; Anders, H.J. Inhibition of Toll-like receptor-7 (TLR-7) or TLR-7 plus TLR-9 attenuates glomerulonephritis and lung injury in experimental lupus. J. Am. Soc. Nephrol., 2007, 18(6), 1721-1731.
101. Savarese, E.; Steinberg, C.; Pawar, R.D.; Reindl, W.; Akira, S.; Anders, H.J.; Krug, A. Requirement of Toll-like receptor 7 for pristane-induced production of autoantibodies and development of murine lupus nephritis. Arthritis Rheum., 2008, 58(4), 1107-1115.
102. Ka, S.M.; Cheng, C.W.; Shui, H.A.; Wu, W.M.; Chang, D.M.; Lin, Y.C.; Chen, A. Mesangial cells of lupus-prone mice are sensitive to chemokine production. Arthritis Res. Therapy, 2007, 9(4), R67.
103. Anders, H.J.; Banas, B.; Linde, Y.; Weller, L.; Cohen, C.D.; Kretzler, M.; Martin, S.; Vielhauer, V.; Schlondorff, D.; Grone, H.J. Bacterial CpG-DNA aggravates immune complex glomerulonephritis: role of TLR9-mediated expression of chemokines and chemokine receptors. J. Am. Soc. Nephrol., 2003, 14(2), 317-326.
104. Fu, Y.; Xie, C.; Chen, J.; Zhu, J.; Zhou, H.; Thomas, J.; Zhou, X.J.; Mohan, C. Innate stimuli accentuate end-organ damage by nephrotoxic antibodies via Fc receptor and TLR stimulation and IL-1/TNF-alpha production. J. Immunol., 2006, 176(1), 632-639.
105. Brown, H.J.; Sacks, S.H.; Robson, M.G. Toll-like receptor 2 agonists exacerbate accelerated nephrotoxic nephritis. J. Am. Soc. Nephrol., 2006, 17(7), 1931-1939.
106. Brown, H.J.; Lock, H.R.; Wolfs, T.G.; Buurman, W.A.; Sacks, S.H.; Robson, M.G. 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(6), 1732-1739.
107. Wynn, T.A. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J. Clin. Invest., 2007, 117(3), 524-529.
108. Meran, S.; Steadman, R. Fibroblasts and myofibroblasts in renal fibrosis. Int. J. Exp. Pathol., 2011, 92(3), 158-167.
109. Eleftheriadis, T.; Antoniadi, G.; Liakopoulos, V.; Antoniadis, N.; Stefanidis, I.; Galaktidou, G. Vitamin D receptor activators and response to injury in kidney diseases. J. Nephrol., 2010, 23(5), 514-524.
110. Chevalier, R.L.; Forbes, M.S.; Thornhill, B.A. Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney int., 2009, 75(11), 1145-1152.
111. Manucha, W.; Valles, P.G. Apoptosis modulated by oxidative stress and inflammation during obstructive nephropathy. Inflamm. Allergy Drug Targets, 2012, 11(4), 303-312.
112. Leemans, J.C.; Butter, L.M.; Pulskens, W.P.; Teske, G.J.; Claessen, N.; van der Poll, T.; Florquin, S. The role of Toll-like receptor 2 in inflammation and fibrosis during progressive renal injury. PloS One, 2009, 4(5), e5704.
113. Pulskens, W.P.; Rampanelli, E.; Teske, G.J.; Butter, L.M.; Claessen, N.; Luirink, I.K.; van der Poll, T.; Florquin, S.; Leemans, J.C. TLR4 promotes fibrosis but attenuates tubular damage in progressive renal injury. J. Am. Soc. Nephrol., 2010, 21(8), 1299-1308.
114. Campbell, M.T.; Hile, K.L.; Zhang, H.; Asanuma, H.; Vanderbrink, B.A.; Rink, R.R.; Meldrum, K.K. Toll-like receptor 4: a novel signaling pathway during renal fibrogenesis. J. Surg. Res., 2011, 168(1), e61-e69.
115. Skuginna, V.; Lech, M.; Allam, R.; Ryu, M.; Clauss, S.; Susanti, H.E.; Rommele, C.; Garlanda, C.; Mantovani, A.; Anders, H.J. Toll-like receptor signaling and SIGIRR in renal fibrosis upon unilateral ureteral obstruction. PloS One, 2011, 6(4), e19204.
116. Correa-Costa, M.; Braga, T.T.; Semedo, P.; Hayashida, C.Y.; Bechara, L.R.; Elias, R.M.; Barreto, C.R.; Silva-Cunha, C.; Hyane, M.I.; Goncalves, G.M.; Brum, P.C.; Fujihara, C.; Zatz, R.; Pacheco-Silva, A.; Zamboni, D.S.; Camara, N.O. Pivotal role of Toll-like receptors 2 and 4, its adaptor molecule MyD88, and inflammasome complex in experimental tubule-interstitial nephritis. PloS One, 2011, 6(12), e29004.
117. Hedayat, M.; Takeda, K.; Rezaei, N. Prophylactic and therapeutic implications of toll-like receptor ligands. Med. Res. Rev., 2012, 32(2), 294-325.