Enzymatic modification of lipid a by arnt protects bordetella bronchiseptica against cationic peptides and is required for transmission

Infection and Immunity

Volumn 82, Issue 2, 2014, Pages 491-499

  Rolin, Olivier ^a   Muse, Sarah J ^a   Safi, Chetan ^a   Elahi, Shokrollah ^b   Gerdts, Volker ^c   Hittle, Lauren E ^d   Ernst, Robert K ^d   Harvill, Eric T ^a   Prestong, Andrew ^e  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^e University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSAMINE; HYPOXIA INDUCIBLE FACTOR 1BETA; LIPID A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARNT GNE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL TRANSMISSION; BORDETELLA BRONCHISEPTICA; BORDETELLA BRONCHISEPTICA INFECTION; GENE LOCUS; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYSTEM;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BORDETELLA BRONCHISEPTICA; BORDETELLA INFECTIONS; DISEASE MODELS, ANIMAL; GLUCOSAMINE; HEXOSYLTRANSFERASES; LIPID A; MICE; MICE, INBRED C57BL; MICROBIAL VIABILITY;

EID: 84892951016     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01260-12     Document Type: Article

References (32)

1. Raetz CR, Reynolds CM, Trent MS, Bishop RE. 2007. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76:295- 329. http://dx.doi.org/10.1146/annurev.biochem.76.010307.145803.
2. Kawai T, Akira S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11:373- 384. http://dx.doi.org/10.1038/ni.1863.
3. Jakubzick C, Tacke F, Llodra J, van Rooijen N, Randolph GJ. 2006. Modulation of dendritic cell trafficking to and from the airways. J. Immunol. 176:3578-3584. http://www.jimmunol.org/content/176/6/3578.abst ract?ijkey=3c1ef3e82db0173c9e2e7e9db48ad1d89be5f477&keytype2=tf _ipsecsha.
4. Miller SI, Ernst RK, Bader MW. 2005. LPS, TLR4 and infectious disease diversity. Nat. Rev. Microbiol. 3:36 - 46. http://dx.doi.org/10 .1038/nrmicro1068.
5. Mattoo S, Cherry JD. 2005. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18:326-382. http: //dx.doi.org/10.1128/CMR.18.2.326-382.2005.
6. Arico B, Scarlato V, Monack DM, Falkow S, Rappuoli R. 1991. Structural and genetic analysis of the bvg locus in Bordetella species. Mol. Microbiol. 5:2481-2491. http://dx.doi.org/10.1111/j.1365-2958.1991.tb02093.x.
7. Merkel TJ, Stibitz S, Keith JM, Leef M, Shahin R. 1998. Contribution of regulation by the bvg locus to respiratory infection of mice by Bordetella pertussis. Infect. Immun. 66:4367-4373.
8. Cotter PA, Miller JF. 1994. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect. Immun. 62:3381-3390.
9. MacArthur I, Jones JW, Goodlett DR, Ernst RK, Preston A. 2011. Role of pagL and lpxO in Bordetella bronchiseptica lipid A biosynthesis. J. Bacteriol. 193:4726-4735. http://dx.doi.org/10.1128/JB.01502-10.
10. Marr N, Hajjar AM, Shah NR, Novikov A, Yam CS, Caroff M, Fernandez RC. 2010. Substitution of the Bordetella pertussis lipid A phosphate groups with glucosamine is required for robust NF-βB activation and release of proinflammatory cytokines in cells expressing human but not murine Toll-like receptor 4-MD-2-CD14. Infect. Immun. 78:2060-2069. http://dx.doi.org/10.1128/IAI.01346-09.
11. Marr N, Tirsoaga A, Blanot D, Fernandez R, Caroff M. 2008. Glucosamine found as a substituent of both phosphate groups in Bordetella lipid A backbones: role of a BvgAS-activated ArnT ortholog. J. Bacteriol. 190: 4281-4290. http://dx.doi.org/10.1128/JB.01875-07.
12. Preston A, Maxim E, Toland E, Pishko EJ, Harvill ET, Caroff M, Maskell DJ. 2003. Bordetella bronchiseptica PagP is a Bvg-regulated lipid A palmitoyl transferase that is required for persistent colonization of the mouse respiratory tract. Mol. Microbiol. 48:725-736. http://dx.doi.org/10 .1046/j.1365-2958.2003.03484.x.
13. Pilione MR, Pishko EJ, Preston A, Maskell DJ, Harvill ET. 2004. pagP is required for resistance to antibody-mediated complement lysis during Bordetella bronchiseptica respiratory infection. Infect. Immun. 72:2837- 2842. http://dx.doi.org/10.1128/IAI.72.5.2837-2842.2004.
14. Trent MS, Ribeiro AA, Lin S, Cotter RJ, Raetz CR. 2001. An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4- amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor. J. Biol. Chem. 276:43122- 43131. http://dx.doi.org/10.1074/jbc.M106961200.
15. Herrera CM, Hankins JV, Trent MS. 2010. Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. Mol. Microbiol. 76:1444-1460. http://dx.doi.org/10 .1111/j.1365-2958.2010.07150.x.
16. Shah NR, Albitar-Nehme S, Kim E, Marr N, Novikov A, Caroff M, Fernandez RC. 2013. Minor modifications to the phosphate groups and the C3= acyl chain length of lipid A in two Bordetella pertussis strains, BP338 and 18-323, independently affect Toll-like receptor 4 protein activation. J. Biol. Chem. 288:11751-11760. http://dx.doi.org/10.1074/jbc .M112.434365.
17. Geurtsen J, Dzieciatkowska M, Steeghs L, Hamstra HJ, Boleij J, Broen K, Akkerman G, El Hassan H, Li J, Richards JC, Tommassen J, van der Ley P. 2009. Identification of a novel lipopolysaccharide core biosynthesis gene cluster in Bordetella pertussis, and influence of core structure and lipid A glucosamine substitution on endotoxic activity. Infect. Immun. 77:2602-2611. http://dx.doi.org/10.1128/IAI.00033-09.
18. Burns VC, Pishko EJ, Preston A, Maskell DJ, Harvill ET. 2003. Role of Bordetella O antigen in respiratory tract infection. Infect. Immun. 71:86- 94. http://dx.doi.org/10.1128/IAI.71.1.86-94.2003.
19. Caroff M, Tacken A, Szabo L. 1988. Detergent-accelerated hydrolysis of bacterial endotoxins and determination of the anomeric configuration of the glycosyl phosphate present in the "isolated lipid A" fragment of the Bordetella pertussis endotoxin. Carbohydr. Res. 175:273-282. http://dx .doi.org/10.1016/0008-6215(88)84149-1.
20. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall KL, Cerdeno-Tarraga AM, Temple L, James K, Harris B, Quail MA, Achtman M, Atkin R, Baker S, Basham D, Bason N, Cherevach I, Chillingworth T, Collins M, Cronin A, Davis P, Doggett J, Feltwell T, Goble A, Hamlin N, Hauser H, Holroyd S, Jagels K, Leather S, Moule S, Norberczak H, O'Neil S, Ormond D, Price C, Rabbinowitsch E, Rutter S, Sanders M, Saunders D, Seeger K, Sharp S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Unwin L, Whitehead S, Barrell BG, Maskell DJ. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:32-40. http://dx.doi.org/10.1038/ng1227.
21. Schweizer HP, Hoang TT. 1995. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158:15- 22. http://dx.doi.org/10.1016/0378-1119(95)00055-B.
22. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat. Biotechnol. 1:784-791. http://dx.doi.org/10.1038 /nbt1183-784.
23. Westphal O, Jann JK. 1965. Bacterial lipopolysaccharides: extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5:83-91.
24. Fischer W, Koch HU, Haas R. 1983. Improved preparation of lipoteichoic acids. Eur. J. Biochem. 133:523-530. http://dx.doi.org/10.1111/j .1432-1033.1983.tb07495.x.
25. Yi EC, Hackett M. 2000. Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 125:651-656. http://dx .doi.org/10.1039/b000368i.
26. Elahi S, Buchanan RM, Attah-Poku S, Townsend HG, Babiuk LA, Gerdts V. 2006. The host defense peptide beta-defensin 1 confers protection against Bordetella pertussis in newborn piglets. Infect. Immun. 74: 2338-2352. http://dx.doi.org/10.1128/IAI.74.4.2338-2352.2006.
27. Doss M, White MR, Tecle T, Hartshorn KL. 2010. Human defensins and LL-37 in mucosal immunity. J. Leukoc. Biol. 87:79-92. http://dx.doi.org /10.1189/jlb.0609382.
28. Song J, Bishop BL, Li G, Duncan MJ, Abraham SN. 2007. TLR4- initiated and cAMP-mediated abrogation of bacterial invasion of the bladder. Cell Host Microbe 1:287-298. http://dx.doi.org/10.1016/j.chom.2007 .05.007.
29. Ganz T. 2004. Defensins: antimicrobial peptides of vertebrates. C R Biol. 327:539-549. http://dx.doi.org/10.1016/j.crvi.2003.12.007.
30. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 27:493-497.
31. Gopinath S, Hotson A, Johns J, Nolan G, Monack D. 2013. The systemic immune state of super-shedder mice is characterized by a unique neutrophil- dependent blunting of TH1 responses. PLoS Pathog. 9:e1003408. http://dx.doi.org/10.1371/journal.ppat.1003408.
32. Rolin O, Smallridge W, Henry M, Goodfield L, Place D, Harvill E. Toll-like receptor 4 limits transmission of Bordetella bronchiseptica. PLoS One, in press.