Peptidoglycan recognition proteins kill bacteria by activating protein-sensing two-component systems

Nature Medicine

Volumn 17, Issue 6, 2011, Pages 676-683

  Kashyap, Des Raj ^a   Wang, Minhui ^a   Liu, Li Hui ^a   Boons, Geert Jan ^b   Gupta, Dipika ^a   Dziarski, Roman ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE NORTHWEST   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HYDROXYL RADICAL; PEPTIDOGLYCAN RECOGNITION PROTEIN; RECO PROTEIN; RNA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BACTERICIDAL ACTIVITY; CELL DIVISION; CELL MEMBRANE PERMEABILITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DAUGHTER CELL; DNA SYNTHESIS; ESCHERICHIA COLI; GENETIC PROCEDURES; INNATE IMMUNITY; MEMBRANE DEPOLARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; RNA SYNTHESIS;

BACILLUS SUBTILIS; BACTERIA; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CARRIER PROTEINS; DNA, BACTERIAL; ESCHERICHIA COLI; HYDROXYL RADICAL; MEMBRANE POTENTIALS; PEPTIDOGLYCAN; RNA, BACTERIAL;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA; POSIBACTERIA;

EID: 79958117263     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2357     Document Type: Article

References (36)

1. Cash, H.L., Whitham, C.V., Behrendt, C.L. & Hooper, L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126-1130 (2006). (Pubitemid 44300239)
2. Stowell, S.R. et al. Innate immune lectins kill bacteria expressing blood group antigen. Nat. Med. 16, 295-301 (2010).
3. Dziarski, R. & Gupta, D. The peptidoglycan recognition proteins (PGRPs). Genome Biol. 7, 232 (2006).
4. Royet, J. & Dziarski, R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defenses. Nat. Rev. Microbiol. 5, 264-277 (2007). (Pubitemid 46443603)
5. Dziarski, R. & Gupta, D. Mammalian PGRPs: novel antibacterial proteins. Cell. Microbiol. 8, 1059-1069 (2006). (Pubitemid 43871642)
6. Kang, D., Liu, G., Lundstrom, A., Gelius, E. & Steiner, H. A peptidoglycan recognition protein in innate immunity conserved from insects to humans. Proc. Natl. Acad. Sci. USA 95, 10078-10082 (1998). (Pubitemid 28415297)
7. Liu, C., Xu, Z., Gupta, D. & Dziarski, R. Peptidoglycan recognition proteins: a novel family of four human innate immunity pattern recognition molecules. J. Biol. Chem. 276, 34686-34694 (2001).
8. Tydell, C.C., Yount, N., Tran, D., Yuan, J. & Selsted, M. Isolation, characterization and antimicrobial properties of bovine oligosaccharide-binding protein. J. Biol. Chem. 277, 19658-19664 (2002).
9. Dziarski, R., Platt, K.A., Gelius, E., Steiner, H. & Gupta, D. Defect in neutrophil killing and increased susceptibility to infection with non-pathogenic Gram-positive bacteria in peptidoglycan recognition protein-S (PGRP-S)-deficient mice. Blood 102, 689-697 (2003). (Pubitemid 36841993)
10. Lu, X. et al. Peptidoglycan recognition proteins are a new class of human bactericidal proteins. J. Biol. Chem. 281, 5895-5907 (2006). (Pubitemid 43847690)
11. Tydell, C.C., Yuan, J., Tran, P. & Selsted, M.E. Bovine peptidoglycan recognition protein-S: antimicrobial activity, localization, secretion and binding properties. J. Immunol. 176, 1154-1162 (2006). (Pubitemid 43099718)
12. Wang, M. et al. Human peptidoglycan recognition proteins require zinc to kill both Gram-positive and Gram-negative bacteria and are synergistic with antibacterial peptides. J. Immunol. 178, 3116-3125 (2007). (Pubitemid 46333193)
13. Gelius, E., Persson, C., Karlsson, J. & Steiner, H. A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-l-alanine amidase activity. Biochem. Biophys. Res. Commun. 306, 988-994 (2003). (Pubitemid 36776228)
14. Wang, Z.-M. et al. Human peptidoglycan recognition protein-L is an N-acetylmuramoyl-l-alanine amidase. J. Biol. Chem. 278, 49044-49052 (2003).
15. Cho, S. et al. Structural insights into the bactericidal mechanism of human peptidoglycan recognition proteins. Proc. Natl. Acad. Sci. USA 104, 8761-8766 (2007). (Pubitemid 47175385)
16. Hancock, R.E.W. & Sahl, H.-G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 24, 1551-1557 (2006). (Pubitemid 44967479)
17. Peschel, A. & Sahl, H.-G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol. 4, 529-536 (2006). (Pubitemid 43905612)
18. Fukushima, T. et al. A new d,l-endopeptidase gene product, YojL (renamed CwlS), plays a role in cell separation with LytE and LytF in Bacillus subtilis. J. Bacteriol. 188, 5541-5550 (2006). (Pubitemid 44157311)
19. Yamamoto, H., Kurosawa, S. & Sekiguchi, J. Localization of the vegetative cell wall hydrolases LytC, LytE and LytF on the Bacillus subtilis cell surface and stability of these enzymes to cell wall-bound or extracellular proteases. J. Bacteriol. 185, 6666-6677 (2003). (Pubitemid 37385887)
20. Blackman, S.A., Smith, T.J. & Foster, S.J. The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144, 73-82 (1998). (Pubitemid 28045214)
21. Kohanski, M.A., Dwyer, D.J., Hayete, B., Lawrence, C.A. & Collins, J.J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130, 797-810 (2007). (Pubitemid 47332566)
22. Hyyryläinen, H.L. et al. A novel two-component regulatory system in Bacillus subtilis for the survival of severe secretion stress. Mol. Microbiol. 41, 1159-1172 (2001).
23. Kohanski, M.A., Dwyer, D.J., Wierzbowski, J., Cottarel, G. & Collins, J.J. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135, 679-690 (2008).
24. DiGiuseppe, P.A. & Silhavy, T.J. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185, 2432-2440 (2003). (Pubitemid 36417966)
25. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J. & Silhavy, T.J. The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev. 9, 387-398 (1995).
26. Nash, J.A., Ballard, T.N., Weaver, T.E. & Akinbi, H.T. The peptidoglycan-degrading property of lysozyme is not required for bactericidal activity in vivo. J. Immunol. 177, 519-526 (2006). (Pubitemid 43939165)
27. Darmon, E. et al. A novel class of heat and secretion stress-responsive genes is controlled by the autoregulated CssRS two-component system of Bacillus subtilis. J. Bacteriol. 184, 5661-5671 (2002).
28. Westers, H. et al. The CssRS two-component regulatory system controls a general secretion stress response in Bacillus subtilis. FEBS J. 273, 3816-3827 (2006). (Pubitemid 44166660)
29. Lim, J.H. et al. Structural basis for preferential recognition of diaminopimelic acid-type peptidoglycan by a subset of peptidoglycan recognition proteins. J. Biol. Chem. 281, 8286-8295 (2006).
30. Touhami, A., Jericho, M.H. & Beveridge, T.J. Atomic force microscopy of cell growth and division in Staphylococcus aureus. J. Bacteriol. 186, 3286-3295 (2004). (Pubitemid 38661523)
31. Yamada, S. et al. An autolysin ring associated with cell separation of Staphylococcus aureus. J. Bacteriol. 178, 1565-1571 (1996). (Pubitemid 26085602)
32. Chang, C.I., Chelliah, Y., Borek, D., Mengin-Lecreulx, D. & Deisenhofer, J. Structure of tracheal cytotoxin in complex with a heterodimeric pattern-recognition receptor. Science 311, 1761-1764 (2006).
33. Kim, M.-S., Byun, M. & Oh, B.-H. Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster. Nat. Immunol. 4, 787-793 (2003). (Pubitemid 36986763)
34. Liu, C., Gelius, E., Liu, G., Steiner, H. & Dziarski, R. Mammalian peptidoglycan recognition protein binds peptidoglycan with high affinity, is expressed in neutrophils and inhibits bacterial growth. J. Biol. Chem. 275, 24490-24499 (2000). (Pubitemid 30626542)
35. Dwyer, D.J., Kohanski, M.A., Hayete, B. & Collins, J.J. Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol. Syst. Biol. 3, 91 (2007).
36. Meijer, W.J. et al. The endogenous Bacillus subtilis (natto) plasmids pTA1015 and pTA1040 contain signal peptidase-encoding genes: identification of a new structural module on cryptic plasmids. Mol. Microbiol. 17, 621-631 (1995).