A polymer-type water-soluble peptidoglycan exhibited both Toll-like receptor 2- and NOD2-agonistic activities, resulting in synergistic activation of human monocytic cells

Innate Immunity

Volumn 14, Issue 5, 2008, Pages 298-308

  Natsuka, Mizuho ^a   Uehara, Akiko ^a   Yang, Shuhua ^a   Echigo, Seishi ^a   Takada, Haruhiko ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Human monocytic cells; Muramyldipeptide (MDP); NOD2; Peptidoglycans; Toll like receptor (TLR)2

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; INTERLEUKIN 8; MURAMYL DIPEPTIDE; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR 2;

ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; MACROPHAGE ACTIVATION; MONOCYTE; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA INTERFERENCE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

CELL LINE, TUMOR; CYTOKINES; HUMANS; LYMPHOCYTE ACTIVATION; MONOCYTES; NOD2 SIGNALING ADAPTOR PROTEIN; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; TOLL-LIKE RECEPTOR 2;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 61349171980     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425908096518     Document Type: Article

References (46)

1. Seidl PH, Schleifer KH. (eds) Biological properties of peptidoglycan. Berlin: Water de Gruyter, 1986; 1-436.
2. Schleifer KH, Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972; 36: 407-477.
3. Ellouz F., Adam A., Ciorbaru R., Lederer E. Minimal structural requirements for adjuvant activity of bacterial peptidoglycan derivatives. Biochem Biophys Res Commun 1974; 59: 1317-1325.
4. Kotani S., Watanabe Y., Kinoshita F. et al. Immunoadjuvant activities of synthetic N-acetyl-muramyl-peptides or -amino acids. Biken J 1975; 18: 105-111.
5. Takada H., Uehara A. Enhancement of TLR-mediated innate immune responses by peptidoglycans through NOD signaling. Curr Pharma Des 2006; 12: 4163-4172.
6. Inohara N., Ogura Y., Fontalba A. et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. J Biol Chem 2003; 278: 5509-5512.
7. Girardin SE, Boneca IG, Viala J. et al. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 2003; 278: 8869-8872.
8. Chamaillard M., Hashimoto M., Horie Y. et al. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 2003; 4: 702-707.
9. Girardin SE, Boneca IG, Carneiro LAM et al. Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science 2003; 300: 1584-1587.
10. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
11. 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: 443-451.
12. Yoshimura A., Lien E., Ingalls RR, Tuomanen E., Dziarski R., Golenbock D. Recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J Immunol 1999; 163: 1-5.
13. 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: 17406-17409.
14. Netea MG, Ferwerda G., de Jong DJ et al. Nucleotide-binding oligomerization domain-2 modulates specific TLR pathways for the induction of cytokine release. J Immunol 2005; 174: 6518-6523.
15. Travassos LH, Girardin SE, Philpott DJ et al. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Report 2004; 5: 1000-1006.
16. Vidal VF, Castéran N., Riendeau CJ et al. Macrophage stimulation with murabutide, an HIV-suppressive muramyl peptide derivative, selectively activates extracellular signal-regulated kinases 1 and 2, C/ EBPβ and STAT1: Role of CD14 and Toll-like receptor 2 and 4. Eur J Immunol 2001; 31: 1962-1971.
17. Yang S., Tamai R., Akashi S. et al. Synergistic effect of muramyldipeptide with lipopolysaccharide or lipoteichoic acid to induce inflammatory cytokines in human monocytic cells in culture. Infect Immun 2001; 69: 2045-2053.
18. Yoshimura A., Takada H., Kaneko T., Kato I., Golenbock D., Hara Y. Structural requirements of muramylpeptides for induction of Toll-like receptor 2-mediated NF-κB activation in CHO cells. J Endotoxin Res 2000; 6: 407-410.
19. Dziarski R., Gupta D. Staphylococcus aureus peptidoglycan is a Toll-like receptor 2 activator: A reevaluation. Infect Immun 2005; 73: 5212-5216.
20. Uehara A., Yang S., Fujimoto Y. et al. Muramyldipeptide and diaminopimelic acid-containing desmuramylpeptides in combination with chemically synthesized Toll-like receptor agonists synergistically induced production of interleukin-8 in a NOD2- and NOD1-dependent manner, respectively, in human monocytic cells in culture. Cell Microbiol 2005; 7: 53-61.
21. Takada H., Tsujimoto M., Kotani S. et al. Mitogenic effects of bacterial cell walls, their fragments, and related synthetic compounds on thymocytes and splenocytes of guinea pigs. Infect Immun 1979; 25: 645-652.
22. Kawata S., Takemura T., Yokogawa K., Kotani S. Isolation of bacteriolytic endopeptidase from a strain of Cytophaga and its application to preparation of hydrosoluble polysaccharide peptide from Staphylococcus epidermidis peptidoglycan. Agric Biol Chem 1984; 48: 2253-2263.
23. Harada K., Kotani S., Takada H. et al. Liberation of serotonin from rabbit blood platelets by bacterial cell walls and related compounds. Infect Immun 1982; 37: 1181-1190.
24. Yokogawa K., Kawata S., Takemura T., Yoshimura Y. Purification and properties of lytic enzymes from Streptomyces globisporus 1829. Agric Biol Chem 1975; 39: 1533-1543.
25. Hashimoto M., Asai Y., Ogawara T. Separation and structural analysis of lipoprotein in a lipopolysaccharide preparation from Porphyromonas gingivalis. IntImmunol 2004; 16: 1431-1437.
26. Kubodera N., Sato K., Nishii Y. Characteristics of 22-oxacalcitriol (OCT) and 2β-(3-hydroxypropoxy)-calcitriol (ED-71). In: Feldman D, Glorieux FH, Pike JW. (eds) Vitamin D. San Diego, CA: Academic Press, 1997; 1071-1086.
27. Uehara A., Sugawara Y., Kurata S. et al. Chemically synthesized pathogen-associated molecular patterns increase the expression of peptidoglycan recognition proteins via Toll-like receptors, NOD1 and NOD2 in human oral epithelial cells. Cell Microbiol 2005; 7: 675-686.
28. Van Heel DA, Ghosh S., Butler M. et al. Synergistic enhancement of Toll-like receptor responses by NOD1 activation. Eur J Immunol 2005; 35: 2471-2476.
29. Fritz JH, Girardin SE, Fitting C. et al. Synergistic stimulation of human monocytes and dendritic cells by Toll-like receptor 4 and NOD1- and NOD2-activating agonists. Eur J Immunol 2005; 35: 2459-2470.
30. Abbott DW, Yang Y., Hutti JE, Madhavarapu S., Kelliher MA, Cantley LC Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol Cell Biol 2007; 27: 6012-6025.
31. Watanabe T., Kitani A., Murray PJ, Strober W. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat Immunol 2004; 5: 800-808.
32. Tada H., Aiba S., Shibata K., Ohteki T., Takada H. Synergistic effect of Nod1 and Nod2 agonists with Toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect Immun 2005; 73: 7967-7976.
33. Martinon F., Agostini L., Meylan E., Tschopp J. Identification of bacterial muramyl dipeptide as activator of the NALP3/Cryopyrin inflammasome. Curr Biol 2004; 14: 1929-1934.
34. Takeuchi O., Kawai T., Mühlradt PF et al. Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int Immunol 2001; 13: 933-940.
35. Morath S., Stadelmaier A., Geyer A., Schmidt RR, Hartung T. Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J Exp Med 2002; 195: 1635-1640.
36. Schröder NWJ, Morath S., Alexander C. et al. Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem 2003; 278: 15587-15594.
37. Zähringer U., Lindner B., Inamura S., Heine H., Alexander C. TLR2 - promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 2008; 213: 205-224.
38. Asai Y., Makimura Y., Kawabata A., Ogawa T. Soluble CD14 discriminates slight structural differences between lipid As that lead to distinct host cell activation. J Immunol 2007; 179: 7674-7683.
39. Kawasaki A., Takada H., Kotani S. et al. Activation of the human complement cascade by bacterial cell walls, peptidoglycans, water-soluble peptidoglycan components, and synthetic muramylpeptides - studies on active components and structural requirements. Microbiol Immunol 1987; 31: 551-569.
40. Myhre AE, Stuestøl JF, Dahle MK et al. Organ injury and cytokine release caused by peptidoglycan are dependent on the structural integrity of the glycan chain. Infect Immun 2004; 72: 1311-1317.
41. Wolfert MA, Murray TF, Boons G. -J, Moore JN The origin of the synergistic effect of muramyl dipeptide with endotoxin and peptidoglycan. J Biol Chem 2002; 277: 39179-39186.
42. Shockman GD, Höltje J-V. Microbial peptidoglycan (murein) hydrolases. In: Ghuysen J-M, Hakenbeck R. (eds) Bacterial Cell Walls. Amsterdam; Elsevier, 1994; 131-166.
43. Karnovsky ML Muramyl peptides in mammalian tissues and their effects at the cellular level. Fed Proc 1986; 45: 2556-2560.
44. Vermeulen MW, Gray GR Processing of Bacillus subtilis peptidoglycan by a mouse macrophage cell line. Infect Immun 1984; 46: 476-483.
45. Johannsen L. Biological properties of bacterial peptidoglycan. APMIS 1993; 101: 337-344.
46. Dziarski R., Gupta D. Mammalian PGRPs: Novel antibacterial proteins. Cell Microbiol 2006; 8: 1059-1069.