Peptidoglycan - An endotoxin in its own right?

Shock

Volumn 25, Issue 3, 2006, Pages 227-235

  Myhre, Anders E ^a,b   Aasen, Ansgar O ^a,b   Thiemermann, Christoph ^c   Wang, Jacob E ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Endotoxin; Inflammation; Peptidoglycan; Sepsis

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CELL RECEPTOR; ENDOTOXIN; PEPTIDOGLYCAN; PROTEIN; TOLL LIKE RECEPTOR;

BACTERIAL CELL WALL; BACTERIAL INFECTION; BACTERIAL TRANSLOCATION; CHEMICAL STRUCTURE; ENDOTOXEMIA; GENE ACTIVATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GRAM POSITIVE INFECTION; GRANULOCYTE; HUMAN; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE; MACROPHAGE; MONOCYTE; MULTIPLE ORGAN FAILURE; NONHUMAN; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN; PROTEIN DOMAIN; REVIEW; SEPSIS; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; DRUG EFFECT; GENE EXPRESSION REGULATION; LYMPHOCYTE ACTIVATION;

ENDOTOXINS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LYMPHOCYTE ACTIVATION; MULTIPLE ORGAN FAILURE; PEPTIDOGLYCAN; SEPSIS; SIGNAL TRANSDUCTION;

EID: 33646116564     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.shk.0000191378.55274.37     Document Type: Review

References (118)

1. Beutler B, Rietschel ET: Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3:169-176, 2003.
2. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR: Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 29:1303-1310, 2001.
3. Brun-Buisson C, Doyon F, Carlet J, Dellamonica P, Gouin F, Lepoutre A, Mercier JC, Offenstadt G, Regnier B: Incidence, risk factors, and outcome of severe sepsis and septic shock in adults. A multicenter prospective study in intensive care units. French ICU Group for Severe Sepsis. JAMA 274:968-974, 1995.
4. Cohen J, Abraham E: Microbiologic findings and correlations with serum tumor necrosis factor-alpha in patients with severe sepsis and septic shock. J Infect Dis 180:116-121, 1999.
5. Kobayashi T, Tani T, Yokota T, Kodama M: Detection of peptidoglycan in human plasma using the silkworm larvae plasma test. FEMS Immunol Med Microbiol 28:49-53, 2000.
6. Tabata T, Tani T, Endo Y, Hanasawa K: Bacterial translocation and peptidoglycan translocation by acute ethanol administration. J Gastroenterol 37:726-731, 2002.
7. Shimizu T, Tani T, Endo Y, Hanasawa K, Tsuchiya M, Kodama M: Elevation of plasma peptidoglycan and peripheral blood neutrophil activation during hemorrhagic shock: plasma peptidoglycan reflects bacterial translocation and may affect neutrophil activation. Crit Care Med 30:77-82, 2002.
8. Tsunooka N, Maeyama K, Hamada Y, Imagawa H, Takano S, Watanabe Y, Kawachi K: Bacterial translocation secondary to small intestinal mucosal ischemia during cardiopulmonary bypass. Measurement by diamine oxidase and peptidoglycan. Eur J Cardiothorac Surg 25:275-280, 2004.
9. Shimizu T, Endo Y, Tabata T, Mori T, Hanasawa K, Tsuchiya M, Tani T: Diagnostic and predictive value of the silkworm larvae plasma test for postoperative infection following gastrointestinal surgery. Crit Care Med 33:1288-1295, 2005.
10. Hoijer MA, Melief MJ, van Helden-Meeuwsen CG, Eulderink F, Hazenberg MP: Detection of muramic acid in a carbohydrate fraction of human spleen. Infect Immun 63:1652-1657, 1995.
11. Schrijver IA, Van Meur M, Melief MJ, Wim AC, Buljevac D, Ravid R, Hazenberg MP, Laman JD: Bacterial peptidoglycan and immune reactivity in the central nervous system in multiple sclerosis. Brain 124:1544-1554, 2001.
12. Visser L, Jan de Heer H, Boven LA, van Riel D, van Meurs M, Melief MJ, Zahringer U, van Strijp J, Lambrecht BN, Nieuwenhuis EE, Laman JD: Proinflammatory bacterial peptidoglycan as a cofactor for the development of central nervous system autoimmune disease. J Immunol 174:808-816, 2005.
13. Melief MJ, Hoijer MA, Van Paassen HC, Hazenberg MP: Presence of bacterial flora-derived antigen in synovial tissue macrophages and dendritic cells. Br J Rheumatol 34:1112-1116, 1995.
14. van Langevelde P, van Dissel JT, Ravensbergen E, Appelmelk BJ, Schrijver IA, Groeneveld PH: Antibiotic-induced release of lipoteichoic acid and peptidoglycan from Staphylococcus aureus: quantitative measurements and biological reactivities. Antimicrob Agents Chemother 42:3073-3078, 1998.
15. van Langevelde P, Ravensbergen E, Grashoff P, Beekhuizen H, Groeneveld PH, van Dissel JT: Antibiotic-induced cell wall fragments of Staphylococcus aureus increase endothelial chemokine secretion and adhesiveness for granulocytes. Antimicrob Agents Chemother 43:2984-2989, 1999.
16. Nau R, Eiffert H: Modulation of release of proinflammatory bacterial compounds by antibacterials: potential impact on course of inflammation and outcome in sepsis and meningitis. Clin Microbiol Rev 15:95-110, 2002.
17. Rotta J, Prendergast TJ, Karakawa WW, Harmon CK, Krause RM: Enhanced resistance to streptococcal infection induced in mice by cell wall mucopeptide. J Exp Med 122:877-890, 1965.
18. Rotta J, Bednar B: Biological properties of cell wall mucopeptide of hemolytic streptococci. J Exp Med 130:31-47, 1969.
19. Rotta J: Endotoxin-like properties of the peptidoglycan. Z Immunitatsforsch Exp Klin Immunol 149:230-244, 1975.
20. Johannsen L, Toth LA, Rosenthal RS, Opp MR, Obal F Jr., Cady AB, Krueger JM: Somnogenic, pyrogenic, and hematologic effects of bacterial peptidoglycan. Am J Physiol 258:R182-R186, 1990.
21. Biberstine KJ, Rosenthal RS: Peptidoglycan fragments decrease food intake and body weight gain in rats. Infect Immun 62:3276-3281, 1994.
22. Wang JE, Dahle MK, McDonald M, Foster SJ, Aasen AO, Thiemermann C: Peptidoglycan and lipoteichoic acid in gram-positive bacterial sepsis: receptors, signal transduction, biological effects, and synergism. Shock 20:402-414, 2003.
23. Davies P, Page RC, Allison AC: Changes in cellular enzyme levels and extracellular release of lysosomal acid hydrolases in macrophages exposed to group A streptococcal cell wall substance. J Exp Med 139:1262-1282, 1974.
24. Smialowicz RJ, Schwab JH: Cytotoxicity of rat macrophages activated by persistent or biodegradable bacterial cell walls. Infect Immun 17:599-606, 1977.
25. Takada H, Tsujimoto M, Kato K, Kotani S, Kusumoto S, Inage M, Shiba T, Yano I, Kawata S, Yokogawa K: Macrophage activation by bacterial cell walls and related synthetic compounds. Infect Immun 25:48-53, 1979.
26. Cummings NP, Pabst MJ, Johnston RB Jr.: Activation of macrophages for enhanced release of superoxide anion and greater killing of Candida albicans by injection of muramyl dipeptide. J Exp Med 152:1659-1669, 1980.
27. Vacheron F, Guenounou M, Nauciel C: Induction of interleukin 1 secretion by adjuvant-active peptidoglycans. Infect Immun 42:1049-1054, 1983.
28. Gold MR, Miller CL, Mishell RI: Soluble non-cross-linked peptidoglycan polymers stimulate monocyte-macrophage inflammatory functions. Infect Immun 49:731-741, 1985.
29. Mattsson E, Verhage L, Rollof J, Fleer A, Verhoef J, Van Dijk H: Peptidoglycan and teichoic acid from Staphylococcus epidermidis stimulate human monocytes to release tumour necrosis factor-alpha, interleukin-1 beta and interleukin-6. FEMS Immunol Med Microbiol 7:281-287, 1993.
30. Timmerman CP, Mattsson E, Martinez-Martinez L, De Graaf L, Van Strijp JA, Verbrugh HA, et al.: Induction of release of tumor necrosis factor from human monocytes by staphylococci and staphylococcal peptidoglycans. Infect Immun 61:4167-4172, 1993.
31. Wang JE, Jorgensen PF, Almlof M, Thiemermann C, Foster SJ, Aasen AO, Solberg R: Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor alpha, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infect Immun 68:3965-3970, 2000.
32. Wang ZM, Liu C, Dziarski R: Chemokines are the main proinflammatory mediators in human monocytes activated by Staphylococcus aureus, peptidoglycan, and endotoxin. J Biol Chem 275:20260-20267, 2000.
33. Lawrence C, Nauciel C: Production of interleukin-12 by murine macrophages in response to bacterial peptidoglycan. Infect Immun 66:4947-4949, 1998.
34. Schaub B, Bellou A, Gibbons FK, Velasco G, Campo M, He H, Liang Y, Gillman MW, Gold D, Weiss ST, Perkins DL, Finn PW: TLR2 and TLR4 stimulation differentially induce cytokine secretion in human neonatal, adult, and murine mononuclear cells. J Interferon Cytokine Res 24:543-552, 2004.
35. Dobrina A, Nardon E, Vecile E, Cinco M, Patriarca P: Leptospira icterohemorrhagiae and leptospire peptidoglycans induce endothelial cell adhesiveness for polymorphonuclear leukocytes. Infect Immun 63:2995-2999, 1995.
36. Giese MJ, Shum DC, Rayner SA, Mondino BJ, Berliner JA: Adhesion molecule expression in a rat model of Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci 41:145-153, 2000.
37. Mattsson E, Persson T, Andersson P, Rollof J, Egesten A: Peptidoglycan induces mobilization of the surface marker for activation marker CD66b in human neutrophils but not in eosinophils. Clin Diagn Lab Immunol 10:485-488, 2003.
38. Strassheim D, Asehnoune K, Park JS, Kim JY, He Q, Richter D, Kuhn K, Mitra S, Abraham E: Phosphoinositide 3-kinase and Akt occupy central roles in inflammatory responses of Toll-like receptor 2-stimulated neutrophils. J Immunol 172:5727-5733, 2004.
39. Wang YY, Myhre AE, Pettersen SJ, Dahle MK, Foster SJ, Thiemermann C, Bjornland K, Aasen AO, Wang JE: Peptidoglycan of S.aureus induces enhanced levels of metalloproteinase-9 (MMP-9) in human blood originating from neutrophils. Shock 24:214-218, 2005.
40. Bieneman AP, Chichester KL, Chen YH, Schroeder JT: Toll-like receptor 2 ligands activate human basophils for both IgE-dependent and IgE-independent secretion. J Allergy Clin Immunol 115:295-301, 2005.
41. Stewart-Tull DES: The immunological activities of bacterial peptidoglycans. Annu Rev Microbiol 34:311-340, 1980.
42. Rasanen L, Arvilommi H: Cell walls, peptidoglycans, and teichoic acids of gram-positive bacteria as polyclonal inducers and immunomodulators of proliferative and lymphokine responses of human B and T lymphocytes. Infect Immun 34:712-717, 1981.
43. Dokter WH, Dijkstra AJ, Koopmans SB, Mulder AB, Stulp BK, Halie MR, Keck W, Vellenga E: G(AnH)MTetra, a naturally occurring 1,6-anhydro muramyl dipeptide, induces granulocyte colony-stimulating factor expression in human monocytes: a molecular analysis. Infect Immun 62:2953-2957, 1994.
44. 2. J Immunol 145:2616-2625, 1990.
45. Phipps RP, Stein SH, Roper RL: A new view of prostaglandin E regulation of the immune response. Immunol Today 12:349-352, 1991.
46. Yaqub S, Solhaug V, Vang T, Solberg R, Aasen A, Tasken K, Wang JE: A human whole blood model of LPS-mediated suppression of T cell activation. Med Sci Monit 9:BR120-BR126, 2003.
47. Nakagawa Y, Murai T: Staphylococcal peptidoglycan suppresses production of interleukin-2 by T cells through a T cell-derived factor induced by direct contact between T cells and monocytes. J Infect Dis 188:1284-1294, 2003.
48. Kessler CM, Nussbaum E, Tuazon CU: Disseminated intravascular coagulation associated with Staphylococcus aureus septicemia is mediated by peptidoglycan-induced platelet aggregation. J Infect Dis 164:101-107, 1991.
49. Spika JS, Peterson PK, Wilkinson BJ, Hammerschmidt DE, Verbrugh HA, Verhoef J, Quie PG: Role of peptidoglycan from Staphylococcus aureus in leukopenia, thrombocytopenia, and complement activation associated with bacteremia. J Infect Dis 146:227-234, 1982.
50. Harada K, Kotani S, Takada H, Tsujimoto M, Hirachi Y, Kusumoto S, Shiba T, Kawata S, Yokogawa K, Nishimura H, Kitaura T, Nakajima T: Liberation of serotonin from rabbit blood platelets by bacterial cell walls and related compounds. Infect Immun 37:1181-1190, 1982.
51. Mattsson E, Herwald H, Bjorck L, Egesten A: Peptidoglycan from Staphylococcus aureus induces tissue factor expression and procoagulant activity in human monocytes. Infect Immun 70:3033-3039, 2002.
52. Bokisch VA: Interaction of peptidoglycans with anti-IgGs and with complement. Z Immunitatsforsch Exp Klin Immunol 149:320-330, 1975.
53. Greenblatt J, Boackle RJ, Schwab JH: Activation of the alternate complement pathway by peptidoglycan from streptococcal cell wall. Infect Immun 19:296-303, 1978.
54. Verbrugh HA, van Dijk WC, Peters R, van Erne ME, Daha MR, Peterson PK, Verhoef J: Opsonic recognition of staphylococci mediated by cell wall peptidoglycan: antibody-independent activation of human complement and opsonic activity of peptidoglycan antibodies. J Immunol 124:1167-1173, 1980.
55. Abdulla EM, Schwab JH: Biological properties of streptococcal cell-wall particles. 3. Dermonecrotic reaction to cell-wall mucopeptides. J Bacteriol 91:374-383, 1966.
56. Yoshino S, Cromartie WJ, Schwab JH: Inflammation induced by bacterial cell wall fragments in the rat air pouch. Comparison of rat strains and measurement of arachidonic acid metabolites. Am J Pathol 121:327-336, 1985.
57. Tuomanen E, Liu H, Hengstler B, Zak O, Tomasz A: The induction of meningeal inflammation by components of the pneumococcal cell wall. J Infect Dis 151:859-868, 1985.
58. Burroughs M, Prasad S, Cabellos C, Mendelman PM, Tuomanen E: The biologic activities of peptidoglycan in experimental Haemophilus influenzae meningitis. J Infect Dis 167:464-468, 1993.
59. Martis L, Patel M, Giertych J, Mongoven J, Taminne M, Perrier MA, Mendoza O, Goud N, Costigan A, Denjoy N, Verger C, Owen WF Jr: Aseptic peritonitis due to peptidoglycan contamination of pharmacopoeia standard dialysis solution. Lancet 365:588-594, 2005.
60. Wang JE, Dahle MK, Yndestad A, Bauer I, McDonald MC, Aukrust P, Foster SJ, Bauer M, Aasen AO, Thiemermann C: Peptidoglycan of Staphylococcus aureus causes inflammation and organ injury in the rat. Crit Care Med 32:546-552, 2004.
61. Wang JE, Pettersen S, Stuestol JF, Wang YY, Foster SJ, Thiemermann C, Aasen AO, Bjornland K: Peptidoglycan of S. aureus causes increased levels of matrix metalloproteinases in the rat. Shock 22:376-379, 2004.
62. Kengatharan KM, De KS, Robson C, Foster SJ, Thiemermann C: Mechanism of gram-positive shock: identification of peptidoglycan and lipoteichoic acid moieties essential in the induction of nitric oxide synthase, shock, and multiple organ failure. J Exp Med 188:305-315, 1998.
63. Janusz MJ, Esser RE, Schwab JH: In vivo degradation of bacterial cell wall by the muralytic enzyme mutanolysin. Infect Immun 52:459-467, 1986.
64. Hoijer MA, Melief MJ, Debets R, Hazenberg MP: Inflammatory properties of peptidoglycan are decreased after degradation by human N-acetylmuramyl-L- alanine amidase. Eur Cytokine Netw 8:375-381, 1997.
65. Myhre AE, Stuestol JF, Dahle MK, Overland G, Thiemermann C, Foster SJ, Lilleaasen P, Aasen AO, Wang JE: Organ injury and cytokine release caused by peptidoglycan are dependent on the structural integrity of the glycan chain. Infect Immun 72:1311-1317, 2004.
66. Ganz T, Gabayan V, Liao HI, Liu L, Oren A, Graf T, Cole AM: Increased inflammation in lysozyme M-deficient mice in response to Micrococcus luteus and its peptidoglycan. Blood 101:2388-2392, 2003.
67. Burroughs M, Rozdzinski E, Geelen S, Tuomanen E: A structure-activity relationship for induction of meningeal inflammation by muramyl peptides. J Clin Invest 92:297-302, 1993.
68. Majcherczyk PA, Langen H, Heumann D, Fountoulakis M, Glauser MP, Moreillon P: Digestion of Streptococcus pneumoniae cell walls with its major peptidoglycan hydrolase releases branched stem peptides carrying proinflammatory activity. J Biol Chem 274:12537-12543, 1999.
69. Qi H, Denning TL, Soong L: Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial toll-like receptor activators and skewing of T-cell cytokine profiles. Infect Immun 71:3337-3342, 2003.
70. Hessle CC, Andersson B, Wold AE: Gram-positive and gram-negative bacteria elicit different patterns of pro-inflammatory cytokines in human monocytes. Cytokine 30:311-318, 2005.
71. Freudenberg MA, Galanos C: Induction of tolerance to lipopolysaccharide (LPS)-D-galactosamine lethality by pretreatment with LPS is mediated by macrophages. Infect Immun 56:1352-1357, 1988.
72. Lichtman SN, Wang J, Schwab JH, Lemasters JJ: Comparison of peptidoglycan-polysaccharide and lipopolysaccharide stimulation of Kupffer cells to produce tumor necrosis factor and interleukin-1. Hepatology 19:1013-1022, 1994.
73. Takada H, Galanos C: Enhancement of endotoxin lethality and generation of anaphylactoid reactions by lipopolysaccharides in muramyl-dipeptide-treated mice. Infect Immun 55:409-413, 1987.
74. Wang JE, Jorgensen PF, Ellingsen EA, Almiof M, Thiemermann C, Foster SJ, Aasen AO, Solberg R: Peptidoglycan primes for LPS-induced release of proinflammatory cytokines in whole human blood. Shock 16:178-182, 2001.
75. Parant M, Parant F, Vinit MA, Jupin C, Noso Y, Chedid L: Priming effect of muramyl peptides for induction by lipopolysaccharide of tumor necrosis factor production in mice. J Leukoc Biol 47:164-169, 1990.
76. Wolfert MA, Murray TF, Boons GJ, Moore JN: The origin of the synergistic effect of muramyl dipeptide with endotoxin and peptidoglycan. J Biol Chem 277:39179-39186, 2002.
77. Wray GM, Foster SJ, Hinds CJ, Thiemermann C: A cell wall component from pathogenic and non-pathogenic gram-positive bacteria (peptidoglycan) synergises with endotoxin to cause the release of tumour necrosis factor-alpha, nitric oxide production, shock, and multiple organ injury/dysfunction in the rat. Shock 15:135-142, 2001.
78. Hadley JS, Wang JE, Foster SJ, Thiemermann C, Hinds CJ: Regulation of CD14, TLR2 and TLR4 by PepG in human blood. Infect Immun 73:7613-7619, 2005.
79. de Kimpe SJ, Kengatharan M, Thiemermann C, Vane JR: The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc Natl Acad Sci U S A 92:10359-10363, 1995.
80. Henneke P, Morath S, Uematsu S, Weichert S, Pfitzenmaier M, Takeuchi O, Muller A, Poyart C, Akira S, Berner R, Teti G, Geyer A, Hartung T, Trieu-Cuot P, Kasper DL, Golenbock DT: Role of lipoteichoic acid in the phagocyte response to group B streptococcus. J Immunol 174:6449-6455, 2005.
81. Mattsson E, Rollof J, Verhoef J, Van Dijk H, Fleer A: Serum-induced potentiation of tumor necrosis factor alpha production by human monocytes in response to staphylococcal peptidoglycan: involvement of different serum factors. Infect Immun 62:3837-3843, 1994.
82. Heumann D, Barras C, Severin A, Glauser MP, Tomasz A: Gram-positive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes. Infect Immun 62:2715-2721, 1994.
83. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC: CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431-1433, 1990.
84. Weidemann B, Brade H, Rietschel ET, Dziarski R, Bazil V, Kusumoto S, Flad HD, Ulmer AJ: Soluble peptidoglycan-induced monokine production can be blocked by anti-CD14 monoclonal antibodies and by lipid A partial structures. Infect Immun 62:4709-4715, 1994.
85. Gupta D, Kirkland TN, Viriyakosol S, Dziarski R: CD14 is a cell-activating receptor for bacterial peptidoglycan. J Biol Chem 271:23310-23316, 1996.
86. Dziarski R, Tapping RI, Tobias PS: Binding of bacterial peptidoglycan to CD14. J Biol Chem 273:8680-8690, 1998.
87. Dziarski R, Viriyakosol S, Kirkland TN, Gupta D: Soluble CD14 enhances membrane CD14-mediated responses to peptidoglycan: structural requirements differ from those for responses to lipopolysaccharide. Infect Immun 68:5254-5260, 2000.
88. Haziot A, Hijiya N, Schultz K, Zhang F, Gangloff SC, Goyert SM: CD14 plays no major role in shock induced by Staphylococcus aureus but down-regulates TNF-alpha production. J Immunol 162:4801-4805, 1999.
89. Schwandner R, Dziarski R, Wesche H, Rothe M, Kirschning CJ: Peptido-glycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J Biol Chem 274:17406-17409, 1999.
90. Yoshimura A, Lien E, Ingalls RR, Tuomanen E, Dziarski R, Golenbock D: Cutting edge: recognition of gram-positive bacterial cell wall components by the innate immune system occurs via toll-like receptor 2. J Immunol 163:1-5, 1999.
91. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, Akira S: Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443-451, 1999.
92. Iwaki D, Mitsuzawa H, Murakami S, Sano H, Konishi M, Akino T, Kuroki Y: The extracellular toll-like receptor 2 domain directly binds peptidoglycan derived from Staphylococcus aureus. J Biol Chem 277:24315-24320, 2002.
93. Girardin SE, Travassos LH, Herve M, Blanot D, Boneca IG, Philpott DJ, Sansonetti PJ, Mengin-Lecreulx D: Peptidoglycan molecular requirements allowing detection by NOD1 and NOD2. J Biol Chem 278:41702-41708, 2003.
94. Travassos LH, Girardin SE, Philpott DJ, Blanot D, Nahori MA, Werts C, Boneca IG: Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep 5:1000-1006, 2004.
95. Dziarski R, Gupta D: Staphylococcus aureus peptidoglycan is a toll-like receptor 2 activator: a reevaluation. Infect Immun 73:5212-5216, 2005.
96. Cho JH, Fraser IP, Fukase K, Kusumoto S, Fujimoto Y, Stahl GL, Ezekowitz RA: Human peptidoglycan recognition protein-S is an effector of neutrophil-mediated innate immunity. Blood 106:2551-2558, 2005.
97. Dziarski R, Platt KA, Gelius E, Steiner H, Gupta D: Defect in neutrophil killing and increased susceptibility to infection with nonpathogenic gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice. Blood 102:689-697, 2003.
98. Wang ZM, Li X, Cocklin RR, Wang M, Wang M, Fukase K, Inamura S, Kusumoto S, Gupta D, Dziarski R: Human peptidoglycan recognition protein-L is an N-acetylmuramyl-L-alanine amidase. J Biol Chem 278:49044-49052, 2003.
99. Xu M, Wang Z, Locksley RM: Innate immune responses in peptidoglycan recognition protein L-deficient mice. Mol Cell Biol 2004;24:7949-7957.
100. Dziarski R. Peptidoglycan recognition proteins (PGRPs). Mol Immunol 40:877-886, 2004.
101. Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, Viala J, Tedin K, Taha MK, Labigne A, Zahringer U, Coyle AJ, DiStefano PS, Bertin J, Sansonetti PJ, Philpott DJ: NOD1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300:1584-1587, 2003.
102. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, Thomas G, Philpott DJ, Sansonetti PJ: NOD2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278:8869-8872, 2003.
103. Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L, Ogura Y, Kawasaki A, Fukase K, Kusumoto S, Valvano MA, Foster SJ, Mak TW, Nunez G, Inohara N: An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4:702-707, 2003.
104. Baraich N, Aguirre JE, Reinecker HC, Xavier R, Podolsky DK: Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-{kappa} B activation in muramyl dipeptide recognition. J Cell Biol 170:21-26, 2005.
105. Chin AI, Dempsey PW, Bruhn K, Miller JF, Xu Y, Cheng G: Involvement of receptor-interacting protein 2 in innate and adaptive immune responses. Nature 416:190-194, 2002.
106. Kobayashi K, Inohara N, Hernandez LD, Galan JE, Nunez G, Janeway CA, Medzhitov R, Flavell RA: RICK/Rip2/CARDIAK mediates signalling for receptors of the innate and adaptive immune systems. Nature 416:194-199, 2002.
107. Gupta D, Wang Q, Vinson C, Dziarski R: Bacterial peptidoglycan induces CD14-dependent activation of transcription factors CREB/ATF and AP-1. J Biol Chem 274:14012-14020, 1999.
108. Martinon F, Agostini L, Meylan E, Tschopp J: Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol 14:1929-1934, 2004.
109. Schrijver IA, Melief MJ, Tak PP, Hazenberg MP, Laman JD: Antigen-presenting cells containing bacterial peptidoglycan in synovial tissues of rheumatoid arthritis patients coexpress costimulatory molecules and cytokines. Arthritis Rheum 43:2160-2168, 2000.
110. Jorgensen PF, Wang JE, Almlof M, Thiemermann C, Foster SJ, Solberg R, Aasen AO: Peptidoglycan and lipoteichoic acid modify monocyte phenotype in human whole blood. Clin Diagn Lab Immunol 8:515-521, 2001.
111. Raymond CR, Wilkie BN: Toll-like receptor, MHC II, B7 and cytokine expression by porcine monocytes and monocyte-derived dendritic cells in response to microbial pathogen-associated molecular patterns. Vet Immunol Immunopathol 107:235-247, 2005.
112. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, Aimer S, Tysk C, O'Morain CA, Gasull M, Binder V, Finkel Y, Cortot A, Modigliani R, Laurent-Puig P, Gower-Rousseau C, Macry J, Colombel JF, Sahbatou M, Thomas G: Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411:599-603, 2001.
113. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, Achkar JP, Brant SR, Bayless TM, Kirschner BS, Hanauer SB, Nunez G, Cho JH: A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411:603-606, 2001.
114. Bonen DK, Ogura Y, Nicolae DL, Inohara N, Saab L, Tanabe T, Chen FF, Foster SJ, Duerr RH, Brant SR, Cho JH, Nunez G: Crohn's disease-associated NOD2 variants share a signaling defect in response to lipopolysaccharide and peptidoglycan. Gastroenterelogy 124:140-146, 2003.
115. Li J, Moran T, Swanson E, Julian C, Harris J, Bonen DK, Hedl M, Nicolae DL, Abraham C, Cho JH: Regulation of IL-8 and IL-1beta expression in Crohn's disease associated NOD2/CARD15 mutations. Hum Mol Genet 13:1715-1725, 2004.
116. Maeda S, Hsu LC, Liu H, Bankston LA, Iimura M, Kagnoff MF, Eckmann L, Karin M: NOD2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing. Science 307:734-738, 2005.
117. Hisamatsu T, Suzuki M, Reinecker HC, Nadeau WJ, McCormick BA, Podolsky DK: CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology 124:993-1000, 2003.
118. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nunez G, Flavell RA: NOD2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307:731-734, 2005.