Innate immune recognition of microbial cell wall components and microbial strategies to evade such recognitions

Microbiological Research

Volumn 168, Issue 7, 2013, Pages 396-406

  Sukhithasri, V ^a   Nisha, N ^a   Biswas, Lalitha ^a   Anil Kumar, V ^a   Biswas, Raja ^a  

^a AMRITA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

N Deacetylation; N Glycolylation; Nucleotide oligomerization domain protein; O Acetylation; Peptidoglycan

Indexed keywords

BACTERIAL PEPTIDOGLYCAN; MESO-DIAMINOPIMELIC ACID; N-DEACETYLATION; N-GLYCOLYLATION; O-ACETYLATION; PEPTIDOGLYCAN RECOGNITION PROTEIN; PEPTIDOGLYCANS; REACTIVE OXYGEN AND NITROGEN SPECIES;

ACETYLATION; BACTERIA; CELL MEMBRANES; FUNGI; IMMUNE SYSTEM; LEAD COMPOUNDS; NUCLEOTIDES; OLIGOMERIZATION; OLIGOMERS; POLYSACCHARIDES; PROTEINS;

CYTOLOGY;

PEPTIDOGLYCAN;

ANTIMICROBIAL ACTIVITY; BACTERIUM; CELL ORGANELLE; FUNGUS; IMMUNE SYSTEM; MICROBIAL ACTIVITY; ORGANIC ACID; PROTEIN;

ANIMAL; BACTERIAL INFECTION; BACTERIUM; CELL WALL; CHEMISTRY; FUNGUS; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; MYCOSIS; REVIEW;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; CELL WALL; FUNGI; HUMANS; IMMUNITY, INNATE; MYCOSES; PEPTIDOGLYCAN;

BACTERIA (MICROORGANISMS); FUNGI;

EID: 84878478603     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2013.02.005     Document Type: Review

References (92)

1. Araki Y., Fukuoka S., Oba S., Ito E. Enzymatic deacetylation of N-acetylglucosamine residues in peptidoglycan from Bacillus cereus cell walls. Biochem Biophys Res Commun 1971, 45:751-758.
2. Atilano M.L., Yates J., Glittenberg M., Filipe S.R., Ligoxygakis P. Wall teichoic acids of Staphylococcus aureus limit recognition by the Drosophila peptidoglycan recognition protein-SA to promote pathogenicity. PLoS Pathog 2011, 7:e1002421.
3. Aubry C., Goulard C., Nahori M.A., Cayet N., Decalf J., Sachse M., et al. OatA, a peptidoglycan O-acetyltransferase involved in Listeria monocytogenes immune escape, is critical for virulence. J Infect Dis 2011, 204:731-740.
4. Beauvais A., Bruneau J.M., Mol P.C., Buitrago M.J., Legrand R., Latge J.P. Glucan synthase complex of Aspergillus fumigatus. J Bacteriol 2001, 183:2273-2279.
5. Benachour A., Ladjouzi R., Le Jeune A., Hébert L., Thorpe S., Courtin P., et al. The lysozyme-induced peptidoglycan N-acetylglucosamine deacetylase PgdA (EF1843) is required for Enterococcus faecalis virulence. J Bacteriol 2012, 194:6066-6073.
6. Bera A., Herbert S., Jakob A., Vollmer W., Gotz F. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol 2005, 55:778-787.
7. Bera A., Biswas R., Herbert S., Gotz F. The presence of peptidoglycan O-acetyltransferase in various staphylococcal species correlates with lysozyme resistance and pathogenicity. Infect Immun 2006, 74:4598-4604.
8. Bera A., Biswas R., Herbert S., Kulauzovic E., Weidenmaier C., Peschel A., et al. Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J Bacteriol 2007, 189:280-283.
9. Bernard E., Rolain T., Courtin P., Hols P., Chapot-Chartier M.P. Identification of the amidotransferase AsnB1 as being responsible for meso-diaminopimelic acid amidation in Lactobacillus plantarum peptidoglycan. J Bacteriol 2011, 193:6323-6330.
10. Boneca I.G., Dussurget O., Cabanes D., Nahori M.A., Sousa S., Lecuit M., et al. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci U S A 2007, 104:997-1002.
11. Bowman S.M., Free S.J. The structure and synthesis of the fungal cell wall. Bioessays 2006, 28:799-808.
12. Brotz H., Bierbaum G., Leopold K., Reynolds P.E., Sahl H.G. The lantibiotic mersacidin inhibits peptidoglycan synthesis by targeting lipid II. Antimicrob Agents Chemother 1998, 42:154-160.
13. Cabib E., Bowers B., Sburlati A., Silverman S.J. Fungal cell wall synthesis: the construction of a biological structure. Microbiol Sci 1988, 5:370-375.
14. Callewaert L., Aertsen A., Deckers D., Vanoirbeek K.G., Vanderkelen L., Van Herreweghe J.M., et al. A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog 2008, 4:e1000019.
15. Cambi A., Netea M.G., Mora-Montes H.M., Gow N.A., Hato S.V., Lowman D.W., et al. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem 2008, 283:20590-20599.
16. Charrier L., Merlin D. The oligopeptide transporter hPepT1: gateway to the innate immune response. Lab Invest 2006, 86:538-546.
17. Cinel I., Opal S.M. Molecular biology of inflammation and sepsis: a primer. Crit Care Med 2009, 37:291-304.
18. Coulombe F., Divangahi M., Veyrier F., de Léséleuc L., Gleason J.L., Yang Y., et al. Increased NOD2-mediated recognition of N-glycolyl muramyl dipeptide. J Exp Med 2009, 206:1709-1716.
19. Crisostomo M.I., Vollmer W., Kharat A.S., Inhulsen S., Gehre F., Buckenmaier S., et al. Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae. Mol Microbiol 2006, 61:1497-1509.
20. Cummings R.D., Doering T.L. Fungi 2009.
21. Davis K.M., Akinbi H.T., Standish A.J., Weiser J.N. Resistance to mucosal lysozyme compensates for the fitness deficit of peptidoglycan modifications by Streptococcus pneumoniae. PLoS Pathog 2008, 4:e1000241.
22. Diacovich L., Gorvel J.P. Bacterial manipulation of innate immunity to promote infection. Nat Rev Microbiol 2010, 8:117-128.
23. Dillard J.P., Hackett K.T. Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect Immun 2005, 73:5697-5705.
24. Douglas C.M. Fungal beta(1,3)-d-glucan synthesis. Med Mycol 2001, 39(Suppl. 1):55-66.
25. Dziarski R. Peptidoglycan recognition proteins (PGRPs). Mol Immunol 2004, 40:877-886.
26. Dziarski R., Gupta D. Peptidoglycan recognition in innate immunity. J Endotoxin Res 2005, 11:304-310.
27. Dziarski R., Gupta D. The peptidoglycan recognition proteins (PGRPs). Genome Biol 2006, 7:232.
28. Dziarski R., Kashyap D.R., Gupta D. Mammalian peptidoglycan recognition proteins kill bacteria by activating two-component systems and modulate microbiome and inflammation. Microb Drug Resist 2012, 18:280-285.
29. Fahlgren A., Hammarstrom S., Danielsson A., Hammarstrom M.L. Increased expression of antimicrobial peptides and lysozyme in colonic epithelial cells of patients with ulcerative colitis. Clin Exp Immunol 2003, 131:90-101.
30. Fitzner N., Clauberg S., Essmann F., Liebmann J., Kolb-Bachofen V. Human skin endothelial cells can express all 10 TLR genes and respond to respective ligands. Clin Vaccine Immunol 2008, 15:138-146.
31. Gautam A., Vyas R., Tewari R. Peptidoglycan biosynthesis machinery: a rich source of drug targets. Crit Rev Biotechnol 2011, 31:295-336.
32. Girardin S.E., Travassos L.H., Herve M., Blanot D., Boneca I.G., Philpott D.J., et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 2003, 278:41702-41708.
33. Goldblatt D., Levinsky R.J., Turner M.W. Role of cell wall polysaccharide in the assessment of IgG antibodies to the capsular polysaccharides of Streptococcus pneumoniae in childhood. J Infect Dis 1992, 166:632-634.
34. Guariglia-Oropeza V., Helmann J.D. Bacillus subtilis sigma(V) confers lysozyme resistance by activation of two cell wall modification pathways, peptidoglycan O-acetylation and d-alanylation of teichoic acids. J Bacteriol 2011, 193:6223-6232.
35. Hebert L., Courtin P., Torelli R., Sanguinetti M., Chapot-Chartier M.P., Auffray Y., et al. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect Immun 2007, 75:5390-5398.
36. Hong M., Ryan K.R., Arkwright P.D., Gennery A.R., Costigan C., Dominguez M., et al. Pattern recognition receptor expression is not impaired in patients with chronic mucocutanous candidiasis with or without autoimmune polyendocrinopathy candidiasis ectodermal dystrophy. Clin Exp Immunol 2009, 156:40-51.
37. Janssens S., Beyaert R. Role of Toll-like receptors in pathogen recognition. Clin Microbiol Rev 2003, 16:637-646.
38. Kang J.Y., Lee J.O. Structural biology of the Toll-like receptor family. Annu Rev Biochem 2011, 80:917-941.
39. Kashyap D.R., Wang M., Liu L.H., Boons G.J., Gupta D., Dziarski R. Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems. Nat Med 2011, 17:676-683.
40. Kim J.G., Lee S.J., Kagnoff M.F. Nod1 is an essential signal transducer in intestinal epithelial cells infected with bacteria that avoid recognition by toll-like receptors. Infect Immun 2004, 72:1487-1495.
41. Laaberki M.H., Pfeffer J., Clarke A.J., Dworkin J. O-Acetylation of peptidoglycan is required for proper cell separation and S-layer anchoring in Bacillus anthracis. J Biol Chem 2011, 286:5278-5288.
42. Le Bourhis L., Benko S., Girardin S.E. Nod1 and Nod2 in innate immunity and human inflammatory disorders. Biochem Soc Trans 2007, 35:1479-1484.
43. Lebeer S., Vanderleyden J., De Keersmaecker S.C. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat Rev Microbiol 2010, 8:171-184.
44. Lehotzky R.E., Partch C.L., Mukherjee S., Cash H.L., Goldman W.E., Gardner K.H., et al. Molecular basis for peptidoglycan recognition by a bactericidal lectin. Proc Natl Acad Sci U S A 2010, 107:7722-7727.
45. Lemansky P., Hasilik A. Chondroitin sulfate is involved in lysosomal transport of lysozyme in U937 cells. J Cell Sci 2001, 114:345-352.
46. Levitz S.M. Innate recognition of fungal cell walls. PLoS Pathog 2010, 6:e1000758.
47. Li X., Wang S., Wang H., Gupta D. Differential expression of peptidoglycan recognition protein 2 in the skin and liver requires different transcription factors. J Biol Chem 2006, 281:20738-20748.
48. Mahapatra S., Crick D.C., McNeil M.R., Brennan P.J. Unique structural features of the peptidoglycan of Mycobacterium leprae. J Bacteriol 2008, 190:655-661.
49. Martinon F., Tschopp J. NLRs join TLRs as innate sensors of pathogens. Trends Immunol 2005, 26:447-454.
50. McDonald C., Inohara N., Nunez G. Peptidoglycan signaling in innate immunity and inflammatory disease. J Biol Chem 2005, 280:20177-20180.
51. McKenzie C.G., Koser U., Lewis L.E., Bain J.M., Mora-Montes H.M., Barker R.N., et al. Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 2010, 78:1650-1658.
52. Meyrand M., Boughammoura A., Courtin P., Mezange C., Guillot A., Chapot-Chartier M.P. Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 2007, 153:3275-3285.
53. Mogensen T.H. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009, 22:240-273.
54. Moynihan P.J., Clarke A.J. O-Acetylation of peptidoglycan in gram-negative bacteria: identification and characterization of peptidoglycan O-acetyltransferase in Neisseria gonorrhoeae. J Biol Chem 2010, 285:13264-13273.
55. Münch D., Roemer T., Lee S.H., Engeser M., Sahl H.G., Schneider T. Identification and in vitro analysis of the GatD/MurT enzyme-complex catalyzing lipid II amidation in Staphylococcus aureus. PLoS Pathog 2012, 8:e1002509.
56. Nadesalingam J., Dodds A.W., Reid K.B., Palaniyar N. Mannose-binding lectin recognizes peptidoglycan via the N-acetyl glucosamine moiety, and inhibits ligand-induced proinflammatory effect and promotes chemokine production by macrophages. J Immunol 2005, 175:1785-1794.
57. Netea M.G., Gow N.A., Munro C.A., Bates S., Collins C., Ferwerda G., et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 2006, 116:1642-1650.
58. Oosting M., Berende A., Sturm P., Ter Hofstede H.J., de Jong D.J., Kanneganti T.D., et al. Recognition of Borrelia burgdorferi by NOD2 is central for the induction of an inflammatory reaction. J Infect Dis 2012, 201:1849-1858.
59. Pfeffer J.M., Strating H., Weadge J.T., Clarke A.J. Peptidoglycan O acetylation and autolysin profile of Enterococcus faecalis in the viable but nonculturable state. J Bacteriol 2006, 188:902-908.
60. Piris-Gimenez A., Paya M., Lambeau G., Chignard M., Mock M., Touqui L., et al. In vivo protective role of human group IIa phospholipase A2 against experimental anthrax. J Immunol 2005, 175:6786-6791.
61. Raymond J.B., Mahapatra S., Crick D.C., Pavelka M.S. Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J Biol Chem 2005, 280:326-333.
62. Royet J., Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 2007, 5:264-277.
63. Royet J., Gupta D., Dziarski R. Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat Rev Immunol 2011, 11:837-851.
64. Saijo S., Iwakura Y. Dectin-1 and dectin-2 in innate immunity against fungi. Int Immunol 2011, 23:467-472.
65. Schenk M., Belisle J.T., Modlin R.L. TLR2 looks at lipoproteins. Immunity 2009, 31:847-849.
66. Schleifer K.H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 1972, 36:407-477.
67. Schwandner R., Dziarski R., Wesche H., Rothe M., Kirschning C.J. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J Biol Chem 1999, 274:17406-17409.
68. Serrano-Gomez D., Dominguez-Soto A., Ancochea J., Jimenez-Heffernan J.A., Leal J.A., Corbi A.L. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 2004, 173:5635-5643.
69. Severin A., Tabei K., Tomasz A. The structure of the cell wall peptidoglycan of Bacillus cereus RSVF1, a strain closely related to Bacillus anthracis. Microb Drug Resist 2004, 10:77-82.
70. Shahinian S., Bussey H. Beta-1,6-glucan synthesis in Saccharomyces cerevisiae. Mol Microbiol 2000, 35:477-489.
71. Shi L., Takahashi K., Dundee J., Shahroor-Karni S., Thiel S., Jensenius J.C., et al. Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 2004, 199:1379-1390.
72. Slamti L., de Pedro M.A., Guichet E., Picardeau M. Deciphering morphological determinants of the helix-shaped Leptospira. J Bacteriol 2011, 193:6266-6275.
73. Sorbara M.T., Philpott D.J. Peptidoglycan: a critical activator of the mammalian immune system during infection and homeostasis. Immunol Rev 2011, 243:40-60.
74. Steele C., Rapaka R.R., Metz A., Pop S.M., Williams D.L., Gordon S., et al. The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog 2005, 1:e42.
75. Steiner H. Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunol Rev 2004, 198:83-96.
76. Stelter C., Kappeli R., Konig C., Krah A., Hardt W.D., Stecher B., et al. Salmonella-induced mucosal lectin RegIIIbeta kills competing gut microbiota. PloS One 2011, 6:e20749.
77. Strober W., Murray P.J., Kitani A., Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat Rev Immunol 2006, 6:9-20.
78. Sudoh M., Yamazaki T., Masubuchi K., Taniguchi M., Shimma N., Arisawa M., et al. Identification of a novel inhibitor specific to the fungal chitin synthase, Inhibition of chitin synthase 1 arrests the cell growth, but inhibition of chitin synthase 1 and 2 is lethal in the pathogenic fungus Candida albicans. J Biol Chem 2000, 275:32901-32905.
79. Tao M., Scacheri P.C., Marinis J.M., Harhaj E.W., Matesic L.E., Abbott D.W. ITCH K63-ubiquitinates the NOD2 binding protein, RIP2, to influence inflammatory signaling pathways. Curr Biol 2009, 19:1255-1263.
80. Travassos L.H., Girardin S.E., Philpott D.J., Blanot D., Nahori M.A., Werts C., et al. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep 2004, 5:1000-1006.
81. Valimaa H., Tenovuo J., Waris M., Hukkanen V. Human lactoferrin but not lysozyme neutralizes HSV-1 and inhibits HSV-1 replication and cell-to-cell spread. Virol J 2009, 6:53.
82. van Ampting M.T., Loonen L.M., Schonewille A.J., Konings I., Vink C., Iovanna J., et al. Intestinally secreted C-type lectin Reg3b attenuates salmonellosis but not listeriosis in mice. Infect Immun 2012, 80:1115-1120.
83. Veiga P., Bulbarela-Sampieri C., Furlan S., Maisons A., Chapot-Chartier M.P., Erkelenz M., et al. SpxB regulates O-acetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J Biol Chem 2007, 282:19342-19354.
84. Vollmer W., Tomasz A. The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J Biol Chem 2000, 275:20496-20501.
85. Vollmer W., Tomasz A. Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect Immun 2002, 70:7176-7178.
86. Vollmer W. Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 2008, 32:287-306.
87. Wang G., Olczak A., Forsberg L.S., Maier R.J. Oxidative stress-induced peptidoglycan deacetylase in Helicobacter pylori. J Biol Chem 2009, 284:6790-6800.
88. Wang G., Maier S.E., Lo L.F., Maier G., Dosi S., Maier R.J. Peptidoglycan deacetylation in Helicobacter pylori contributes to bacterial survival by mitigating host immune responses. Infect Immun 2010, 78:4660-4666.
89. Weadge J.T., Pfeffer J.M., Clarke A.J. Identification of a new family of enzymes with potential O-acetylpeptidoglycan esterase activity in both Gram-positive and Gram-negative bacteria. BMC Microbiol 2005, 5:49.
90. Weindl G., Wagener J., Schaller M. Epithelial cells and innate antifungal defense. J Dent Res 2010, 89:666-675.
91. Wheeler R.T., Kombe D., Agarwala S.D., Fink G.R. Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 2008, 4:e1000227.
92. Yamamoto M., Takeda K., Akira S. TIR domain-containing adaptors define the specificity of TLR signaling. Mol Immunol 2004, 40:861-868.