Bacterial peptidoglycan-associated lipoprotein: A naturally occurring toll-like receptor 2 agonist that is shed into serum and has synergy with lipopolysaccharide

Journal of Infectious Diseases

Volumn 191, Issue 6, 2005, Pages 939-948

  Liang, Michael D ^a   Bagchi, Aranya ^c   Warren, H Shaw ^b,c   Tehan, Megan M ^c   Trigilio, James A ^c   Beasley Topliffe, Laura K ^c   Tesini, Brenda L ^c   Lazzaroni, Jean Claude ^e   Fenton, Matthew J ^d   Hellman, Judith ^b,c  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOPOLYSACCHARIDE; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ARTICLE; CIRCULATION; CYTOKINE PRODUCTION; ESCHERICHIA COLI; GRAM NEGATIVE SEPSIS; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; SERUM;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CELL LINE; DRUG SYNERGISM; ESCHERICHIA COLI; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; HUMANS; LIPOPOLYSACCHARIDES; LIPOPROTEINS; MACROPHAGE ACTIVATION; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDOGLYCAN; RECEPTORS, CELL SURFACE; SEPSIS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTORS;

EID: 20044369519     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/427815     Document Type: Article

References (58)

1. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001; 2:675-80.
2. Rock FL, Hardiman G, Timans JC, Kastelein RA, Bazan JF. A family of human receptors structurally related to Drosophila Toll. Proc Natl Acad Sci USA 1998; 95:588-93.
3. Poltorak A, He X, Smirnova I, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in TLR4 gene. Science 1998; 282:2085-8.
4. Qureshi ST, Lariviere L, Leveque G, et al. Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (TLR4). J Exp Med 1999; 189:615-25.
5. Rhee SH, Hwang D. Murine Toll-like receptor 4 confers lipopolysaccharide responsiveness as determined by activation of NF κB and expression of the inducible cyclooxygenase. J Biol Chem 2000; 275:34035-40.
6. Tapping RI, Akashi S, Miyake K, Godowski PJ, Tobias PS. Toll-like receptor 4, but not Toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J Immunol 2000; 165:5780-7.
7. Takeuchi O, Hoshino K, Kawai T, et al. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999; 11:443-51.
8. Schwandner R, Dziarski R, Wesche H, Rothe M, Kirschning CJ. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J Biol Chem 1999; 274:17406-9.
9. Means TK, Lien E, Yoshimura A, Wang S, Golenbock DT, Fenton MJ. The CD14 ligands lipoarabinomannan and lipopolysaccharide differ in their requirement for Toll-like receptors. J Immunol 1999; 163:6748-55.
10. Hirschfeld M, Weis JJ, Toshchakov V, et al. Signaling by Toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect Immun 2001; 69:1477-82.
11. Werts C, Tapping RI, Mathison JC, et al. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat Immunol 2001; 2:346-52.
12. Hayashi F, Smith KD, Ozinsky A, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001; 410:1099-103.
13. Brightbill HD, Libraty DH, Krutzik SR, et al. Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 1999; 285:732-5.
14. Aliprantis AO, Yang RB, Mark MR, et al. Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science 1999; 285:736-9.
15. Hirschfeld M, Kirschning CJ, Schwandner R, et al. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by Toll-like receptor 2. J Immunol 1999; 163:2382-6.
16. Lee HK, Lee J, Tobias PS. Two lipoproteins extracted from Escherichia coli K-12 LCD25 lipopolysaccharide are the major components responsible for Toll-like receptor 2-mediated signaling. J Immunol 2002; 168:4012-7.
17. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000; 408:740-5.
18. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001; 413:732-8.
19. Ozinsky A, Underhill DM, Fontenot JD, et al. 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.
20. Zhang D, Zhang G, Hayden MS, et al. A Toll-like receptor that prevents infection by uropathogenic bacteria. Science 2004; 303:1522-6.
21. Jones BW, Means TK, Heldwein KA, et al. Different Toll-like receptor agonists induce distinct macrophage responses. J Leukoc Biol 2001; 69:1036-44.
22. Vogel SN, Fenton M. Toll-like receptor 4 signalling: new perspectives on a complex signal-transduction problem. Biochem Soc Trans 2003; 31:664-8.
23. Yamamoto M, Sato S, Hemmi H, et al. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 2003; 301:640-3.
24. Wietek C, Miggin SM, Jefferies CA, O'Neill LA. Interferon regulatory factor-3-mediated activation of the interferon-sensitive response element by Toll-like receptor (TLR) 4 but not TLR3 requires the p65 subunit of NF-κ. J Biol Chem 2003; 278:50923-31.
25. Beutler B, Milsark IW, Cerami AC. Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 1985; 229:869-71.
26. Galanos C, Freudenberg MA. Mechanisms of endotoxin shock and endotoxin hypersensitivity. Immunobiology 1993; 187:346-56.
27. Mizuno T. Structure of peptidolglycan-associated lipoprotein (PAL) of the Proteus mirabilis outer membrane. I. Isolation and characterization of fatty acid-containing peptides from PAL. J Biochem 1981; 89:1051-8.
28. Chen R, Henning U. Nucleotide sequence of the gene for the peptidoglycan-associated lipoprotein of Escherichia coli K12. Eur J Biochem 1987; 163:73-7.
29. Rodriguez-Herva J, Ramos-Gonzalez M, Ramos J. The Pseudomonas putida peptidoglycan-associated outer membrane lipoprotein is involved in maintenance of the integrity of the cell envelope. J Bacteriol 1996; 178:1699-706.
30. Lazzaroni J-C, Portalier R. The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (PAL). Mol Microbiol 1992; 6:735-42.
31. Lazzaroni J, Lefebvre N, Portalier R. Cloning of the excC and excD genes involved in the release of periplasmic proteins by Escherichia coli K12. Mol Gen Genet 1989; 218:460-4.
32. Mizushima S. Post-translational modification and processing of outer membrane prolipoproteins in Escherichia coli. Mol Cell Biochem 1984; 60:5-15.
33. Hellman J, Loiselle PM, Zanzot EM, et al. Release of gram-negative outer membrane proteins into human serum and septic rat blood and their interactions with immunoglobulin in antiserum to Escherichia coli J5. J Infect Dis 2000; 181:1034-43.
34. Hellman J, Loiselle PM, Tehan MM, et al. Outer membrane protein A, peptidoglycan-associated lipoprotein, and murein lipoprotein are released by Escherichia coli bacteria into serum. Infect Immun 2000; 68:2566-72.
35. Hellman J, Warren HS. Outer membrane protein A (OmpA), peptidoglycan-associated lipoprotein (PAL), and murein lipoprotein (MLP) are released in experimental gram-negative sepsis. J Endotoxin Res 2001; 7:69-72.
36. Hellman J, Roberts JDJ, Tehan MM, Allaire JE, Warren HS. Bacterial peptidoglycan-associated lipoprotein is released into the bloodstream in gram-negative sepsis and causes inflammation and death in mice. J Biol Chem 2002; 277:14274-80.
37. Clavel T, Germon P, Vianney A, Portalier R, Lazzaroni JC. TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan- associated proteins Pal, Lpp, and OmpA. Mol Microbiol 1998; 29:359-67.
38. Dubuisson JF, Vianney A, Lazzaroni JC. Mutational analysis of the TolA C-terminal domain of Escherichia coli and genetic evidence for an interaction between TolA and TolB. J Bacteriol 2002; 184:4620-5.
39. Hellman J, Tehan MM, Warren HS. Murein lipoprotein (MLP), Peptidoglycan-associated lipoprotein (PAL), and outer membrane protein A (OmpA) are present in purified rough and smooth LPS. J Infect Dis 2003; 188:286-9.
40. Kirschning CJ, Wesche H, Merrill AT, Rothe M. Human toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J Exp Med 1998; 188:2091-7.
41. Means TK, Wang S, Lien E, Yoshimura A, Golenbock DT, Fenton MJ. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J Immunol 1999; 163:3920-7.
42. Latz E, Visintin A, Lien E, et al. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the Toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction. J Biol Chem 2002; 277:47834-43.
43. Novitsky TJ, Roslansky PF, Siber GR, Warren HS. Turbidometric method for quantifying serum inhibition of Limulus amoebocyte lysate. J Clin Microbiol 1985; 21:211-6.
44. Bierer B, Coligan JE, Margulies DH, Shevach EM, Strober W, eds. Current protocols in immunology. John Wiley and Sons, 2004.
45. Schilling D, Thomas K, Nixdorff K, Vogel SN, Fenton MJ. Toll-like receptor 4 and Toll-IL-1 receptor domain-containing adapter protein (TIRAP)/myeloid differentiation protein 88 adapter-like (Mal) contribute to maximal IL-6 expression in macrophages. J Immunol 2002; 169:5874-80.
46. Hellman J, Zanzot EM, Loiselle PM, et al. Antiserum against Escherichia coli J5 contains antibodies reactive with outer membrane proteins of heterologous gram-negative bacteria. J Infect Dis 1997; 176:1260-8.
47. Fitting C, Dhawan S, Cavaillon JM. Compartmentalization of tolerance to endotoxin. J Infect Dis 2004; 189:1295-303.
48. Sato S, Nomura F, Kawai T, et al. Synergy and cross-tolerance between Toll-like receptor (TLR) 2- and TLR4-mediated signaling pathways. J Immunol 2000; 165:7096-101.
49. Zhang H, Peterson JW, Niesel DW, Klimpel GR. Bacterial lipoprotein and lipopolysaccharide act synergistically to induce lethal shock and proinflammatory cytokine production. J Immunol 1997; 159:4868-78.
50. Wang JE, Jorgensen PF, Ellingsen EA, et al. Peptidoglycan primes for LPS-induced release of proinflammatory cytokines in whole human blood. Shock 2001; 16:178-82.
51. Lehner MD, Morath S, Michelsen KS, Schumann RR, Hartung T. Induction of cross-tolerance by lipopolysaccharide and highly purified lipoteichoic acid via different Toll-like receptors independent of paracrine mediators. J Immunol 2001; 166:5161-7.
52. Schwartz DA, Wohlford-Lenane CL, Quinn TJ, Krieg AM. Bacterial DNA or oligonucleotides containing unmethylated CpG motifs can minimize lipopolysaccharide-induced inflammation in the lower respiratory tract through an IL-12-dependent pathway. J Immunol 1999; 163:224-31.
53. Wang JH, Doyle M, Manning BJ, Di Wu Q, Blankson S, Redmond HP. Induction of bacterial lipoprotein tolerance is associated with suppression of Toll-like receptor 2 expression. J Biol Chem 2002; 277:36068-75.
54. West MA, Bennet T, Clair L. Reprogrammed macrophage tumor necrosis factor and interleukin-1 release with inflammatory pretreatment: differential regulation by endotoxin and zymosan. J Trauma 1995; 39:404-10.
55. d) macrophages. J Immunol 1994; 153:2653-63.
56. Doe WF, Yang ST, Morrison DC, Betz SJ, Henson PM. Macrophage stimulation by bacterial lipopolysaccharides. II. Evidence for differentiation signals delivered by lipid A and by a protein rich fraction of lipopolysaccharides. J Exp Med 1978; 148:557-68.
57. Hirschfeld M, Ma Y, Weis JH, Vogel SN, Weis JJ. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J Immunol 2000; 165:618-22.
58. Jeannin P, Magistrelli G, Goetsch L, et al. Outer membrane protein A (OmpA): a new pathogen-associated molecular pattern that interacts with antigen presenting cells-impact on vaccine strategies. Vaccine 2002; 20(Suppl 4):A23-7.