Bacterial lipopeptide triggers massive albuminuria in murine lupus nephritis by activating Toll-like receptor 2 at the glomerular filtration barrier

Immunology

Volumn 128, Issue 1 PART 2, 2009, Pages

  Pawar, Rahul D ^b   Castrezana Lopez, Liliana ^b   Allam, Ramanjaneyulu ^b   Kulkarni, Onkar P ^b   Segerer, Stephan ^b   Radomska, Ewa ^b   Meyer, Tobias N ^c   Schwesinger, Catherine Meyer ^c   Akis, Nese ^d   Gröne, Hermann Josef ^e   Anders, Hans Joachim ^a,b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF HAMBURG   (Germany)

^d ULUDAG UNIVERSITY   (Turkey)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Albuminuria; Autoimmunity; Endothelial cells; Podocytes; Toll like receptors

Indexed keywords

ALBUMIN; AUTOANTIBODY; BACTERIUM LIPOPOLYSACCHARIDE; DNA ANTIBODY; INTERLEUKIN 12; LIPOPEPTIDE; NEPHRIN; TOLL LIKE RECEPTOR 2;

ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL INFECTION; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; ENDOTHELIUM CELL; FEMALE; GLOMERULUS FILTRATION; LUPUS ERYTHEMATOSUS NEPHRITIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PODOCYTE; PRIORITY JOURNAL; SPLENOMEGALY;

ALBUMINURIA; ANIMALS; AUTOANTIBODIES; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; INTERLEUKIN-12; INTERLEUKIN-6; KIDNEY; LIPOPEPTIDES; LIPOPOLYSACCHARIDES; LUPUS NEPHRITIS; MEMBRANE PROTEINS; MICE; MICE, INBRED MRL LPR; MICE, KNOCKOUT; PODOCYTES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR-ALPHA;

EID: 68249147524     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2008.02948.x     Document Type: Article

References (40)

1. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002 20 : 197 216.
2. Hemmi H, Kaisho T, Takeuchi O et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signalling pathway. Nat Immunol 2002 3 : 196 200.
3. Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006 124 : 783 801.
4. Ehlers E, Ravetch JV. Opposing effects of Toll-like receptor stimulation induce autoimmunity or tolerance. Trends Immunol 2007 28 : 74 9.
5. Hawkins BT, Abbruscato TJ, Egleton RD, Brown RC, Huber JD, Campos CR, Davis TP. Nicotine increases in vivo blood-brain barrier permeability and alters cerebral microvascular tight junction protein distribution. Brain Res 2004 1027 : 48 58.
6. Hemmi H, Takeuchi O, Kawai T et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000 408 : 740 5.
7. Pawar RD, Patole PS, Ellwart A, Lech M, Segerer S, Schlondorff D, Anders HJ. Ligands to nucleic acid-specific toll-like receptors and the onset of lupus nephritis. J Am Soc Nephrol 2006 12 : 3365 73.
8. Anders HJ, Vielhauer V, Eis V et al. Activation of toll-like receptor-9 induces progression of renal disease in MRL(Fas)lpr mice. FASEB J 2004 18 : 534 6.
9. Anders HJ, Banas B, Linde Y et al. Bacterial CpG-DNA aggravates immune complex glomerulonephritis: role of TLR9-mediated expression of chemokines and chemokine receptors. J Am Soc Nephrol 2003 14 : 317 26.
10. Pawar RD, Patole PS, Zecher D, Segerer S, Kretzler M, Schlondorff D, Anders HJ. Toll-like receptor-7 modulates immune complex glomerulonephritis. J Am Soc Nephrol 2006 17 : 141 9.
11. Patole PS, Pawar RD, Lech M et al. Expression and regulation of Toll-like receptors in lupus-like immune complex glomerulonephritis of MRL-Fas(lpr) mice. Nephrol Dial Transplant 2006 21 : 3062 73.
12. Tsuboi N, Yoshikai Y, Matsuo S et al. Roles of Toll-like receptors in C-C chemokine production by renal tubular epithelial cells. J Immunol 2002 169 : 2026 33.
13. Wörnle M, Schmid H, Banas B et al. Novel role of Toll-like receptor 3 in hepatitis C-associated glomerulonephritis. Am J Pathol 2006 168 : 370 85.
14. Patole PS, Grone HJ, Segerer S et al. 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.
15. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, Wilson CB, Schroeder L, Aderem A. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci USA 2000 97 : 13766 71.
16. Triantafilou M, Gamper FGJ, Haston RM, Mouratis MA, Morath S, Hartung T, Triantafilou K. Membrane sorting of Toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J Biol Chem 2006 281 : 31002 11.
17. Aliprantis AO, Yang RB, Mark MR et al. Cell activation and apoptosis by bacterial lipopeptides through toll-like receptor-2. Science 1999 285 : 736 9.
18. Poltorak A, He X, Smirnova I et al. Defective LPS signalling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998 282 : 2085 8.
19. Brown HJ, Lock HR, Sacks SH, Robson MG. TLR2 stimulation of intrinsic renal cells in the induction of immune-mediated glomerulonephritis. J Immunol 2006 177 : 1925 31.
20. Fu Y, Xie C, Chen J, Zhu J, Zhou H, Thomas J, Zhou XJ, 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 : 632 9.
21. Brown HJ, Sacks SH, Robson MG. Toll-like receptor 2 agonists exacerbate accelerated nephrotoxic nephritis. J Am Soc Nephrol 2006 7 : 1931 9.
22. Akis N, Madaio MP. Isolation, culture, and characterization of endothelial cells from mouse glomeruli. Kidney Int 2004 65 : 2223 7.
23. Mundel P, Reiser J, Borja AZM, Pavenstädt H, Davidson GR, Kriz W, Zeller R. Rearrangements of the cytoskeleton and cell contacts induce process formation during differentiation of conditionally immortalized mouse podocyte cell lines. Exp Cell Res 1997 236 : 248 58.
24. Shankland SJ, Pippin JW, Reiser J, Mundel P. Podocytes in culture: past, present, and future. Kidney Int 2007 72 : 26 36.
25. Satchell SC, Buchatska O, Khan SB et al. Interferon-beta reduces proteinuria in experimental glomerulonephritis. J Am Soc Nephrol 2007 18 : 2875 84.
26. Austin HA, Muenz LR, Joyce KM, Antonovych TT, Balow JE. Diffuse proliferative lupus nephritis: identification of specific pathologic features affecting renal outcome. Kidney Int 1984 25 : 689 95.
27. Weening JJ, D'agati VD, Schwartz MM et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 2004 65 : 521 30.
28. Tryggvason K, Patrakka J, Wartiovaara J. Hereditary proteinuria syndromes and mechanisms of proteinuria. N Engl J Med 2006 354 : 1387 401.
29. Kalluri R. Proteinuria with and without renal glomerular podocyte effacement. J Am Soc Nephrol 2006 17 : 2383 9.
30. Mitu GM, Wang S, Hirschberg RR. BMP7 is a podocyte survival factor and rescues podocytes from diabetic injury. Am J Physiol Renal Physiol 2007 293 : F1641 8.
31. Iwasaki A, Medzitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004 10 : 987 95.
32. Camici M. Renal glomerular permselectivity and vascular endothelium. Biomed Pharmacother 2005 59 : 30 7.
33. Reiser J, von Gersdorff G, Loos M et al. Induction of B7-1 in podocytes is associated with nephrotic syndrome. J Clin Invest 2004 113 : 1390 7.
34. Reiser J, Kritz W, Kretzler M, Mundel P. The glomerular slit diaphragm is a modified adherence junction. J Am Soc Nephrol 2000 11 : 1 8.
35. Yanagida-Asanuma E, Asanuma K, Kim K et al. Synaptopodin protects against proteinuria by disrupting Cdc42:IRSp53:Mena signalling complexes in kidney podocytes. Am J Pathol 2007 171 : 415 27.
36. Wang W, Dentler WL, Borchardt RT. VEGF increases BMEC monolayer permeability by affecting occludin expression and tight junction assembly. Am J Physiol Heart Circ Physiol 2001 280 : H434 40.
37. Lee HS, Namkoong K, Kim DH, Kim KJ, Cheong YH, Kim SS, Lee WB, Kim KY. Hydrogen peroxide-induced alterations of tight junction proteins in bovine brain microvascular endothelial cells. Microvasc Res 2004 68 : 231 8.
38. van Eijk L, Nooteboom A, Hendriks T, Sprong T, Netea M, Smits P, van der Hoeven J, Pickkers P. Plasma obtained during human endotoxemia increases endothelial albumin permeability in vitro. Shock 2006 25 : 358 62.
39. Angelini DJ, Hyun SW, Grigoryev DN et al. TNF- increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am J Pathol 2005 167 : 1161 72.
40. Brooks TA, Hawkins BT, Huber JD, Egleton RD, Davis TP. Chronic inflammatory pain leads to increased blood-brain barrier permeability and tight junction protein alterations. Am J Physiol Heart Circ Physiol 2005 289 : H738 43.