Peptidoglycan-modifying enzyme Pgp1 is required for helical cell shape and pathogenicity traits in campylobacter jejuni

PLoS Pathogens

Volumn 8, Issue 3, 2012, Pages

  Frirdich, Emilisa ^a   Biboy, Jacob ^b   Adams, Calvin ^a   Lee, Jooeun ^c   Ellermeier, Jeremy ^d   Gielda, Lindsay Davis ^d   DiRita, Victor J ^d   Girardin, Stephen E ^c   Vollmer, Waldemar ^b   Gaynor, Erin C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 8; PEPTIDASE; PEPTIDOGLYCAN; PEPTIDOGLYCAN PEPTIDASE 1; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BIOINFORMATICS; CAMPYLOBACTER JEJUNI; CHICK; CYTOKINE RELEASE; ENZYME ASSAY; EPITHELIUM CELL; GENE DELETION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOST CELL; MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; STRESS; WILD TYPE; ANIMAL; BACTERIAL GENE; BIOSYNTHESIS; CELL LINE; CELL SHAPE; CHICKEN; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI;

ANIMALS; CAMPYLOBACTER JEJUNI; CELL LINE; CELL SHAPE; CHICKENS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; EPITHELIAL CELLS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; PEPTIDE HYDROLASES; PEPTIDOGLYCAN;

EID: 84861214451     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002602     Document Type: Article

References (77)

1. Park SF, (2002) The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol 74: 177-188.
2. Lee MD, Newell DG, (2006) Campylobacter in poultry: filling an ecological niche. Avian Dis 50: 1-9.
3. Newell DG, Wagenaar JA, (2000) Poultry infections and their control at the farm level. In: Nachamkin I, Blaser MJ, editors. Campylobacter Washington, D. C. American Society for Microbiology pp. 497-509.
4. Black RE, Levine MM, Clements ML, Hughes TP, Blaser MJ, (1988) Experimental Campylobacter jejuni infection in humans. J Infect Dis 157: 472-479.
5. Blaser MJ, Engeberg J, (2008) Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In: Szymanski CM, Nachamkin I, Blaser MJ, editors. Campylobacter, 3rd Edition Washington, DC ASM Press pp. 99-122.
6. Hofreuter D, Tsai J, Watson RO, Novik V, Altman B, et al. (2006) Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74: 4694-4707.
7. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
8. Rattee ID, Breur MM, (1974) The Physical Chemistry of Dye Absorption New York Academic Press pp. 180-182.
9. Wood PJ, (1980) Specificity in the interaction of direct dyes with polysaccharides. Carbohydr Res 85: 271-287.
10. McLennan MK, Ringoir DD, Frirdich E, Svensson SL, Wells DH, et al. (2008) Campylobacter jejuni biofilms up-regulated in the absence of the stringent response utilize a calcofluor white-reactive polysaccharide. J Bacteriol 190: 1097-1107.
11. Naito M, Frirdich E, Fields JA, Pryjma M, Li J, et al. (2010) Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J Bacteriol 192: 2182-2192.
12. Vollmer W, Blanot D, de Pedro MA, (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32: 149-167.
13. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, et al. (2010) Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143: 1097-1109.
14. Vollmer W, Bertsche U, (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778: 1714-1734.
15. Vollmer W, Joris B, Charlier P, Foster S, (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32: 259-286.
16. Holtje JV, (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62: 181-203.
17. Amano K, Shibata Y, (1992) Structural studies of peptidoglycans in Campylobacter species. Microbiol Immunol 36: 961-967.
18. Weadge JT, Pfeffer JM, Clarke AJ, (2005) Identification of a new family of enzymes with potential O-acetylpeptidoglycan esterase activity in both Gram-positive and Gram-negative bacteria. BMC Microbiol 5: 49.
19. Sycuro LK, Pincus Z, Gutierrez KD, Biboy J, Stern CA, et al. (2010) Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 141: 822-833.
20. Bonis M, Ecobichon C, Guadagnini S, Prevost MC, Boneca IG, (2010) A M23B-family metallopeptidase of Helicobacter pylori required for cell shape, pole formation and virulence. Mol Microbiol 78: 809-819.
21. Hendrixson DR, Akerley BJ, DiRita VJ, (2001) Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40: 214-224.
22. Sycuro LK, Wyckoff TJ, Biboy J, Born P, Pincus Z, et al. (2012) Multiple peptidoglycan modification networks modulate Helicobacter pylori's cell shape, motility, and colonization potential. PLoS Pathog 8 doi:10.1371/journal.ppat.1002603.
23. Karlyshev AV, Wren BW, (2005) Development and application of an insertional system for gene delivery and expression in Campylobacter jejuni. Appl Environ Microbiol 71: 4004-4013.
24. Glauner B, Holtje JV, Schwarz U, (1988) The composition of the murein of Escherichia coli. J Biol Chem 263: 10088-10095.
25. Bui NK, Gray J, Schwarz H, Schumann P, Blanot D, et al. (2009) The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J Bacteriol 191: 494-505.
26. Clarke AJ, Dupont C, (1992) O-acetylated peptidoglycan: its occurrence, pathobiological significance, and biosynthesis. Can J Microbiol 38: 85-91.
27. Vollmer W, (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32: 287-306.
28. Szymanski CM, King M, Haardt M, Armstrong GD, (1995) Campylobacter jejuni motility and invasion of Caco-2 cells. Infect Immun 63: 4295-4300.
29. van Putten JP, van Alphen LB, Wosten MM, de Zoete MR, (2009) Molecular mechanisms of Campylobacter infection. Curr Top Microbiol Immunol 337: 197-229.
30. den Blaauwen T, de Pedro MA, Nguyen-Disteche M, Ayala JA, (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 32: 321-344.
31. Gerdes K, (2009) RodZ, a new player in bacterial cell morphogenesis. Embo J 28: 171-172.
32. Uehara T, Park JT, (2003) Identification of MpaA, an amidase in Escherichia coli that hydrolyzes the gamma-D-glutamyl-meso-diaminopimelate bond in murein peptides. J Bacteriol 185: 679-682.
33. Arminjon F, Guinand M, Vacheron MJ, Michel G, (1977) Specificity profiles of the membrane-bound gamma-D-glutamyl-(L)meso-diaminopimelateendopeptidase and LD-carboxypeptidase from Bacillus sphaericus 9602. Eur J Biochem 73: 557-565.
34. Garnier M, Vacheron MJ, Guinand M, Michel G, (1985) Purification and partial characterization of the extracellular gamma-D-glutamyl-(L)meso-diaminopimelate endopeptidase I, from Bacillus sphaericus NCTC 9602. Eur J Biochem 148: 539-543.
35. Hourdou ML, Guinand M, Vacheron MJ, Michel G, Denoroy L, et al. (1993) Characterization of the sporulation-related gamma-D-glutamyl-(L)meso-diaminopimelic-acid-hydrolysing peptidase I of Bacillus sphaericus NCTC 9602 as a member of the metallo(zinc) carboxypeptidase A family. Modular design of the protein. Biochem J 292: 563-570.
36. Costa K, Bacher G, Allmaier G, Dominguez-Bello MG, Engstrand L, et al. (1999) The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J Bacteriol 181: 3710-3715.
37. Joshua GW, Guthrie-Irons C, Karlyshev AV, Wren BW, (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152: 387-396.
38. Kalmokoff M, Lanthier P, Tremblay TL, Foss M, Lau PC, et al. (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188: 4312-4320.
39. Moe KK, Mimura J, Ohnishi T, Wake T, Yamazaki W, et al. (2010) The mode of biofilm formation on smooth surfaces by Campylobacter jejuni. J Vet Med Sci 72: 411-416.
40. Al-Sayeqh AF, Loughlin MF, Dillon E, Mellits KH, Connerton IF, (2010) Campylobacter jejuni activates NF-kappaB independently of TLR2, TLR4, Nod1 and Nod2 receptors. Microb Pathog 49: 294-304.
41. Zilbauer M, Dorrell N, Elmi A, Lindley KJ, Schuller S, et al. (2007) A major role for intestinal epithelial nucleotide oligomerization domain 1 (NOD1) in eliciting host bactericidal immune responses to Campylobacter jejuni. Cell Microbiol 9: 2404-2416.
42. Benko S, Philpott DJ, Girardin SE, (2008) The microbial and danger signals that activate Nod-like receptors. Cytokine 43: 368-373.
43. Magalhaes JG, Philpott DJ, Nahori MA, Jehanno M, Fritz J, et al. (2005) Murine Nod1 but not its human orthologue mediates innate immune detection of tracheal cytotoxin. EMBO Rep 6: 1201-1207.
44. Davis KM, Weiser JN, (2011) Modifications to the peptidoglycan backbone help bacteria to establish infection. Infect Immun 79: 562-570.
45. Watson RO, Galan JE, (2008) Campylobacter jejuni survives within epithelial cells by avoiding delivery to lysosomes. PLoS Pathog 4: e14.
46. Lee J, Tattoli I, Wojtal KA, Vavricka SR, Philpott DJ, et al. (2009) pH-dependent internalization of muramyl peptides from early endosomes enables Nod1 and Nod2 signaling. J Biol Chem 284: 23818-23829.
47. Hasegawa M, Yang K, Hashimoto M, Park JH, Kim YG, et al. (2006) Differential release and distribution of Nod1 and Nod2 immunostimulatory molecules among bacterial species and environments. J Biol Chem 281: 29054-29063.
48. Pradipta AR, Fujimoto Y, Hasegawa M, Inohara N, Fukase K, (2010) Characterization of natural human nucleotide-binding oligomerization domain protein 1 (Nod1) ligands from bacterial culture supernatant for elucidation of immune modulators in the environment. J Biol Chem 285: 23607-23613.
49. Dalmasso G, Nguyen HT, Charrier-Hisamuddin L, Yan Y, Laroui H, et al. (2010) PepT1 mediates transport of the proinflammatory bacterial tripeptide L-Ala-{gamma}-D-Glu-meso-DAP in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 299: G687-696.
50. Iyer JK, Coggeshall KM, (2011) Cutting edge: primary innate immune cells respond efficiently to polymeric peptidoglycan, but not to peptidoglycan monomers. J Immunol 186: 3841-3845.
51. Magalhaes JG, Sorbara MT, Girardin SE, Philpott DJ, (2011) What is new with Nods? Curr Opin Immunol 23: 29-34.
52. Kaparakis M, Turnbull L, Carneiro L, Firth S, Coleman HA, et al. (2010) Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol 12: 372-385.
53. de Zoete MR, Keestra AM, Roszczenko P, van Putten JP, (2010) Activation of human and chicken toll-like receptors by Campylobacter spp. Infect Immun 78: 1229-1238.
54. Friis LM, Keelan M, Taylor DE, (2009) Campylobacter jejuni drives MyD88-independent interleukin-6 secretion via Toll-like receptor 2. Infect Immun 77: 1553-1560.
55. Kuijf ML, Samsom JN, van Rijs W, Bax M, Huizinga R, et al. (2010) TLR4-mediated sensing of Campylobacter jejuni by dendritic cells is determined by sialylation. J Immunol 185: 748-755.
56. Li YP, Vegge CS, Brondsted L, Madsen M, Ingmer H, et al. (2011) Campylobacter jejuni induces an anti-inflammatory response in human intestinal epithelial cells through activation of phosphatidylinositol 3-kinase/Akt pathway. Vet Microbiol 148: 75-83.
57. van Mourik A, Steeghs L, van Laar J, Meiring HD, Hamstra HJ, et al. (2010) Altered linkage of hydroxyacyl chains in lipid A of Campylobacter jejuni reduces TLR4 activation and antimicrobial resistance. J Biol Chem 285: 15828-15836.
58. Watson RO, Galan JE, (2005) Signal transduction in Campylobacter jejuni-induced cytokine production. Cell Microbiol 7: 655-665.
59. Hendrixson DR, (2006) A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol Microbiol 61: 1646-1659.
60. Hendrixson DR, (2008) Restoration of flagellar biosynthesis by varied mutational events in Campylobacter jejuni. Mol Microbiol 70: 519-536.
61. Hendrixson DR, DiRita VJ, (2004) Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52: 471-484.
62. Nachamkin I, Yang XH, Stern NJ, (1993) Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Appl Environ Microbiol 59: 1269-1273.
63. Wassenaar TM, van der Zeijst BA, Ayling R, Newell DG, (1993) Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139: 1171-1175.
64. Wosten MM, Wagenaar JA, van Putten JP, (2004) The FlgS/FlgR two-component signal transduction system regulates the fla regulon in Campylobacter jejuni. J Biol Chem 279: 16214-16222.
65. Hanel I, Borrmann E, Muller J, Muller W, Pauly B, et al. (2009) Genomic and phenotypic changes of Campylobacter jejuni strains after passage of the chicken gut. Vet Microbiol 136: 121-129.
66. Martinon F, Agostini L, Meylan E, Tschopp J, (2004) Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol 14: 1929-1934.
67. Laing KJ, Purcell MK, Winton JR, Hansen JD, (2008) A genomic view of the NOD-like receptor family in teleost fish: identification of a novel NLR subfamily in zebrafish. BMC Evol Biol 8: 42.
68. Fernando U, Biswas D, Allan B, Willson P, Potter AA, (2007) Influence of Campylobacter jejuni fliA, rpoN and flgK genes on colonization of the chicken gut. Int J Food Microbiol 118: 194-200.
69. Matz C, van Vliet AH, Ketley JM, Penn CW, (2002) Mutational and transcriptional analysis of the Campylobacter jejuni flagellar biosynthesis gene flhB. Microbiology 148: 1679-1685.
70. Wassenaar TM, Bleumink-Pluym NM, van der Zeijst BA, (1991) Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. Embo J 10: 2055-2061.
71. Hendrixson DR, DiRita VJ, (2003) Transcription of sigma54-dependent but not sigma28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol Microbiol 50: 687-702.
72. Joslin SN, Hendrixson DR, (2009) Activation of the Campylobacter jejuni FlgSR two-component system is linked to the flagellar export apparatus. J Bacteriol 191: 2656-2667.
73. Field LH, Underwood JL, Payne SM, Berry LJ, (1993) Characteristics of an avirulent Campylobacter jejuni strain and its virulence-enhanced variants. J Med Microbiol 38: 293-300.
74. Gaynor EC, Cawthraw S, Manning G, MacKichan JK, Falkow S, et al. (2004) The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J Bacteriol 186: 503-517.
75. Ziprin RL, Hume ME, Andrews K, Droleskey RE, Harvey RB, et al. (2005) News and notes: An atypical Campylobacter coli exhibiting unusual morphology. Curr Microbiol 51: 161-163.
76. Svensson SL, Davis LM, MacKichan JK, Allan BJ, Pajaniappan M, et al. (2009) The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol Microbiol 71: 253-272.
77. Glauner B, (1988) Separation and quantification of muropeptides with high-performance liquid chromatography. Anal Biochem 172: 451-464.