Mutations of the Listeria monocytogenes peptidoglycan N-Deacetylase and O-acetylase result in enhanced lysozyme sensitivity, bacteriolysis, and hyperinduction of innate immune pathways

Infection and Immunity

Volumn 79, Issue 9, 2011, Pages 3596-3606

  Rae, Chris S ^a   Geissler, Aimee ^a,b   Adamson, Paul C ^a,c   Portnoy, Daniel A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Wyoming Department of Health   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOZYME; N DEACETYLASE; O ACETYLASE; PEPTIDOGLYCAN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOLYSIS; BONE MARROW CELL; CELL DEATH; CELL GROWTH; CONTROLLED STUDY; CYTOSOL; IN VITRO STUDY; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; MACROPHAGE; NONHUMAN; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL;

ACETYLATION; AMIDOHYDROLASES; ANIMALS; APOPTOSIS; BACTERIOLYSIS; CYTOKINES; FEMALE; IMMUNITY, INNATE; LISTERIA MONOCYTOGENES; MACROPHAGES; MICE; MICE, INBRED C57BL; MURAMIDASE; MUTATION; PEPTIDOGLYCAN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFERASES;

EID: 80052317339     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00077-11     Document Type: Article

References (70)

1. Bera, A., R. Biswas, S. Herbert, and F. Gotz. 2006. The presence of peptidoglycan O-acetyltransferase in various staphylococcal species correlates with lysozyme resistance and pathogenicity. Infect. Immun. 74:4598-4604.
2. Bera, A., S. Herbert, A. Jakob, W. Vollmer, and F. Gotz. 2005. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55:778-787.
3. Boneca, I. G., et al. 2007. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U. S. A. 104:997-1002.
4. Callewaert, L., and C. W. Michiels. 2010. Lysozymes in the animal kingdom. J. Biosci. 35:127-160.
5. Camilli, A., L. G. Tilney, and D. A. Portnoy. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8:143-157.
6. Cohn, Z. A. 1978. Activation of mononuclear phagocytes: fact, fancy, and future. J. Immunol. 121:813-816.
7. Cole, A. M., P. Dewan, and T. Ganz. 1999. Innate antimicrobial activity of nasal secretions. Infect. Immun. 67:3267-3275.
8. Cole, A. M., et al. 2005. Decreased clearance of Pseudomonas aeruginosa from airways of mice deficient in lysozyme M. J. Leukoc. Biol. 78:1081-1085.
9. Crisostomo, M. I., et al. 2006. Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae. Mol. Microbiol. 61:1497-1509.
10. Cross, M., I. Mangelsdorf, A. Wedel, and R. Renkawitz. 1988. Mouse lysozyme M gene: isolation, characterization, and expression studies. Proc. Natl. Acad. Sci. U. S. A. 85:6232-6236.
11. Davis, K. M., H. T. Akinbi, A. J. Standish, and J. N. Weiser. 2008. Resistance to mucosal lysozyme compensates for the fitness deficit of peptidoglycan modifications by Streptococcus pneumoniae. PLoS Pathog. 4:e1000241.
12. Davis, K. M., and J. N. Weiser. 2011. Modifications to the peptidoglycan backbone help bacteria to establish infection. Infect. Immun. 79:562-570.
13. Edelson, B. T., and E. R. Unanue. 2001. Intracellular antibody neutralizes Listeria growth. Immunity 14:503-512.
14. Fawell, S., et al. 1994. Tat-mediated delivery of heterologous proteins into cells. Proc. Natl. Acad. Sci. U. S. A. 91:664-668.
15. Franchi, L., T. D. Kanneganti, G. R. Dubyak, and G. Nunez. 2007. Differential requirement of P2X7 receptor and intracellular K for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 282:18810-18818.
16. Frankel, A. D., and C. O. Pabo. 1988. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55:1189-1193.
17. Ganz, T., et al. 2003. Increased inflammation in lysozyme M-deficient mice in response to Micrococcus luteus and its peptidoglycan. Blood 101:2388-2392.
18. Ginsburg, I. 2002. The role of bacteriolysis in the pathophysiology of inflammation, infection and post-infectious sequelae. APMIS 110:753-770.
19. Gordon, S., J. Todd, and Z. A. Cohn. 1974. In vitro synthesis and secretion of lysozyme by mononuclear phagocytes. J. Exp. Med. 139:1228-1248.
20. Hankiewicz, J., and E. Swierczek. 1974. Lysozyme in human body fluids. Clin. Chim. Acta 57:205-209.
21. Hansen, N. E., and H. Karle. 1971. Blood and bone-marrow lysozyme in neutropenia: an attempt towards pathogenetic classification. Br. J. Haematol. 21:261-270.
22. Hauber, J., M. H. Malim, and B. R. Cullen. 1989. Mutational analysis of the conserved basic domain of human immunodeficiency virus tat protein. J. Virol. 63:1181-1187.
23. Hazrati, E., et al. 2006. Human alpha- and beta-defensins block multiple steps in herpes simplex virus infection. J. Immunol. 177:8658-8666.
24. Herbert, S., et al. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3:e102.
25. Hornung, V., et al. 2009. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 458:514-518.
26. Ishikawa, H., Z. Ma, and G. N. Barber. 2009. STING regulates intracellular DNAmediated, type I interferon-dependent innate immunity. Nature 461:788-792.
27. Jones, S., and D. A. Portnoy. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 62:5608-5613.
28. Kim, S., et al. 2010. Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome. Eur. J. Immunol. 40:1545-1551.
29. Kumar, H., T. Kawai, and S. Akira. 2009. Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 388:621-625.
30. Lamkanfi, M., and T. D. Kanneganti. 2010. Nlrp3: an immune sensor of cellular stress and infection. Int. J. Biochem. Cell Biol. 42:792-795.
31. Leber, J. H., et al. 2008. Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen. PLoS Pathog. 4:e6.
32. Mann, D. A., and A. D. Frankel. 1991. Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J. 10:1733-1739.
33. Mariathasan, S., et al. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440:228-232.
34. Markart, P., et al. 2004. Comparison of the microbicidal and muramidase activities of mouse lysozyme M and P. Biochem. J. 380:385-392.
35. Markart, P., T. R. Korfhagen, T. E. Weaver, and H. T. Akinbi. 2004. Mouse lysozyme M is important in pulmonary host defense against Klebsiella pneumoniae infection. Am. J. Respir. Crit. Care Med. 169:454-458.
36. Martinon, F., A. Mayor, and J. Tschopp. 2009. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27:229-265.
37. Medzhitov, R., and C. Janeway, Jr. 2000. Innate immune recognition: mechanisms and pathways. Immunol. Rev. 173:89-97.
38. Mendiondo, O., H. Suit, and H. Fixler. 1978. Lysozyme levels and macrophage content of tumor tissue in C3H mice bearing fibrosarcoma transplants treated by radiation and Corynebacterium parvum. Int. J. Radiat. Oncol. Biol. Phys. 4:829-834.
39. Munford, R. S., and A. W. Varley. 2006. Shield as signal: lipopolysaccharides and the evolution of immunity to gram-negative bacteria. PLoS Pathog. 2:e67.
40. Myers, J. T., A. W. Tsang, and J. A. Swanson. 2003. Localized reactive oxygen and nitrogen intermediates inhibit escape of Listeria monocytogenes from vacuoles in activated macrophages. J. Immunol. 171:5447-5453.
41. Nagahara, H., et al. 1998. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat. Med. 4:1449-1452.
42. Nash, J. A., T. N. Ballard, T. E. Weaver, and H. T. Akinbi. 2006. The peptidoglycan-degrading property of lysozyme is not required for bactericidal activity in vivo. J. Immunol. 177:519-526.
43. O'Riordan, M., C. H. Yi, R. Gonzales, K. D. Lee, and D. A. Portnoy. 2002. Innate recognition of bacteria by a macrophage cytosolic surveillance pathway. Proc. Natl. Acad. Sci. U. S. A. 99:13861-13866.
44. Ozinsky, A., K. D. Smith, D. Hume, and D. M. Underhill. 2000. Co-operative induction of pro-inflammatory signaling by Toll-like receptors. J. Endotoxin Res. 6:393-396.
45. Ozoren, N., et al. 2006. Distinct roles of TLR2 and the adaptor ASC in IL-1beta/IL-18 secretion in response to Listeria monocytogenes. J. Immunol. 176:4337-4342.
46. Popowska, M., M. Kusio, P. Szymanska, and Z. Markiewicz. 2009. Inactivation of the wall-associated de-N-acetylase (PgdA) of Listeria monocytogenes results in greater susceptibility of the cells to induced autolysis. J. Microbiol. Biotechnol. 19:932-945.
47. Portnoy, D. A., P. S. Jacks, and D. J. Hinrichs. 1988. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J. Exp. Med. 167:1459-1471.
48. Prixova, J. 1975. Serum lysozyme in mice subjected to combined immunosuppression with 6-mercaptopurine and hydrocortisone. Folia Microbiol. (Praha) 20:509-512.
49. Ruben, S., et al. 1989. Structural and functional characterization of human immunodeficiency virus tat protein. J. Virol. 63:1-8.
50. Sauer, J. D., et al. 11 July 2011. Listeria monocytogenes engineered to activate the Nlrc4 inflammasome are severely attenuated and are poor inducers of protective immunity. Proc. Natl. Acad. Sci. U. S. A. [Epub ahead of print.] doi:10.1073/pnas.1019041108.
51. Sauer, J. D., et al. 2011. The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 79:688-694.
52. Sauer, J. D., et al. 2010. Listeria monocytogenes triggers AIM2-mediated pyroptosis upon infrequent bacteriolysis in the macrophage cytosol. Cell Host Microbe 7:412-419.
53. Schnupf, P., and D. A. Portnoy. 2007. Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9:1176-1187.
54. Shimada, J., et al. 2008. Lysozyme M deficiency leads to an increased susceptibility to Streptococcus pneumoniae-induced otitis media. BMC Infect. Dis. 8:134.
55. Shimada, T., et al. 2010. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7:38-49.
56. Stetson, D. B., and R. Medzhitov. 2006. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity 1:93-103.
57. Tan, B. H., et al. 2006. Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J. Immunol. 177:1864-1871.
58. Thedieck, K., et al. 2006. The MprF protein is required for lysinylation of phospholipids in listerial membranes and confers resistance to cationic antimicrobial peptides (CAMPs) on Listeria monocytogenes. Mol. Microbiol. 62:1325-1339.
59. Tilney, L. G., and D. A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608.
60. Torres, D., et al. 2004. Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect. Immun. 72:2131-2139.
61. Travassos, L. H., et al. 2004. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep. 5:1000-1006.
62. Vazquez-Boland, J. A., et al. 2001. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 14:584-640.
63. Vinding, T., J. S. Eriksen, and N. V. Nielsen. 1987. The concentration of lysozyme and secretory IgA in tears from healthy persons with and without contact lens use. Acta Ophthalmol. 65:23-26.
64. Vives, E., P. Brodin, and B. Lebleu. 1997. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J. Biol. Chem. 272:16010-16017.
65. Vollmer, W. 2008. Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol. Rev. 32:287-306.
66. Vollmer, W., and A. Tomasz. 2000. The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J. Biol. Chem. 275:20496-20501.
67. Warren, S. E., et al. 2010. Cutting edge: cytosolic bacterial DNA activates the inflammasome via Aim2. J. Immunol. 185:818-821.
68. Woodward, J. J., A. T. Iavarone, and D. A. Portnoy. 2010. c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328:1703-1705.
69. Zemansky, J., et al. 2009. Development of a mariner-based transposon and identification of Listeria monocytogenes determinants, including the peptidyl-prolyl isomerase PrsA2, that contribute to its hemolytic phenotype. J. Bacteriol. 191:3950-3964.
70. Zipperle, G. F., Jr., J. W. Ezzell, Jr., and R. J. Doyle. 1984. Glucosamine substitution and muramidase susceptibility in Bacillus anthracis. Can. J. Microbiol. 30:553-559.