A transposon site hybridization screen identifies galU and wecBC as important for survival of Yersinia pestis in murine macrophages

Journal of Bacteriology

Volumn 194, Issue 3, 2012, Pages 653-662

  Klein, Kathryn A ^a   Fukuto, Hana S ^a   Pelletier, Mark ^b   Romanov, Galina ^a   Grabenstein, Jens P ^a,d   Palmer, Lance E ^a,c   Ernst, Robert ^b   Bliska, James B ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c SIEMENS CORPORATE RESEARCH   (United States)

^d Carpmaels and Ransford   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; LIPOOLIGOSACCHARIDE; POLYMYXIN B; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE 2 EPIMERASE; URIDINE TRIPHOSPHATE GLUCOSE 1 PHOSPHATE URIDYLYLTRANSFERASE;

ARTICLE; BACTERIAL SURVIVAL; DNA HYBRIDIZATION; DNA MICROARRAY; GEL ELECTROPHORESIS; GENE INSERTION; MACROPHAGE; MASS SPECTROMETRY; PHENOTYPIC VARIATION; PRIORITY JOURNAL; TRANSPOSON; YERSINIA PESTIS;

ANIMALS; BACTERIAL PROTEINS; CARBOHYDRATE DEHYDROGENASES; CARBOHYDRATE EPIMERASES; CELL LINE; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, BACTERIAL; MACROPHAGES; MICE; MICROBIAL VIABILITY; MUTAGENESIS, INSERTIONAL; PLAGUE; UTP-GLUCOSE-1-PHOSPHATE URIDYLYLTRANSFERASE; YERSINIA PESTIS;

ENTEROBACTERIACEAE; MURINAE; YERSINIA PESTIS;

EID: 84855955708     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06237-11     Document Type: Article

References (63)

1. Achtman M, et al. 2004. Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl. Acad. Sci. U. S. A. 101:17837-17842.
2. Anisimov AP, et al. 2010. Yersinia pestis lipopolysaccharide in hostpathogen interactions, p 77-87. In Shafferman, A. Ordentlich, and A. Velan (ed), B. The challenge of highly pathogenic microorganisms: Mechanisms of virulence and novel medical countermeasures. Springer, Heidelberg, London, New York.
3. Barua S, et al. 2002. Involvement of surface polysaccharides in the organic acid resistance of Shiga Toxin-producing Escherichia coli O157:H7. Mol. Microbiol. 43:629-640.
4. Buchau AS, et al. 2010. The host defense peptide cathelicidin is required for NK cell-mediated suppression of tumor growth. J. Immunol. 184: 369-378.
5. Cavanaugh DC, Randall R. 1959. The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of fleaborne plague. J. Immunol. 85:348-363.
6. Chan K, Kim CC, Falkow S. 2005. Microarray-based detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect. Immun. 73:5438-5449.
7. Chang HY, Lee JH, Deng WL, Fu TF, Peng HL. 1996. Virulence and outer membrane properties of a galU mutant of Klebsiella pneumoniae CG43. Microb. Pathog. 20:255-261.
8. Churchill GA. 2002. Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32 Suppl.:490-495.
9. Dean CR, Goldberg JB. 2002. Pseudomonas aeruginosa galU is required for a complete lipopolysaccharide core and repairs a secondary mutation in a PA103 (serogroup O11) wbpM mutant. FEMS Microbiol. Lett. 210: 277-283.
10. Du Y, Rosqvist R, Forsberg A. 2002. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70:1453-1460.
11. El Hamidi A, Tirsoaga A, Novikov A, Hussein A, Caroff M. 2005. Microextraction of bacterial lipid A: easy and rapid method for mass spectrometric characterization. J. Lipid Res. 46:1773-1778.
12. Ernst RK, Guina T, Miller SI. 1999. How intracellular bacteria survive: surface modifications that promote resistance to host innate immune responses. J. Infect. Dis. 179:S326 -S330.
13. Felek S, et al. 2010. Phosphoglucomutase of Yersinia pestis is required for autoaggregation and polymyxin B resistance. Infect. Immun. 78: 1163-1175.
14. Finegold MJ, Petery JJ, Berendt RF, Adams HR. 1968. Studies on the pathogenesis of plague. Blood coagulation and tissue responses of Macaca mulatta following exposure to aerosols of Pasteurella pestis. Am. J. Pathol. 53:99-114.
15. Forgac M. 2007. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8:917-929.
16. Fukuto HS, Svetlanov A, Palmer LE, Karzai AW, Bliska JB. 2010. Global gene expression profiling of Yersinia pestis replicating inside macrophages reveals the roles of a putative stress-induced operon in regulating type III secretion and intracellular cell division. Infect. Immun. 78:3700-3715.
17. Furste JP, et al. 1986. Molecular cloning of the plasmid RP4 primase region in a multi-host range tacP expression vector. Gene 48:119-131.
18. Galvan EM, Lasaro MA, Schifferli DM. 2008. Capsular antigen fraction 1 and Pla modulate the susceptibility of Yersinia pestis to pulmonary antimicrobial peptides such as cathelicidin. Infect. Immun. 76:1456-1464.
19. Gong S, Bearden SW, Geoffroy VA, Fetherston JD, Perry RD. 2001. Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect. Immun. 69:2829-2837.
20. Grabenstein JP. 2005. Stony Brook University, Stony Brook, NY.
21. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB. 2006. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74:3727-3741.
22. Grabenstein JP, Marceau M, Pujol C, Simonet M, Bliska JB. 2004. The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect. Immun. 72:4973-4984.
23. Guo J, Nair MK, Galvan EM, Liu SL, Schifferli DM. 2011. Tn5AraOut mutagenesis for the identification of Yersinia pestis genes involved in resistance towards cationic antimicrobial peptides. Microb. Pathog. 51: 121-132.
24. Hitchen PG, et al. 2002. Structural characterization of lipooligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system. Mol. Microbiol. 44:1637-1650.
25. Horton RM, et al. 1993. Gene splicing by overlap extension. Methods Enzymol. 217:270-279.
26. Inoue T, et al. 2007. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J. Bacteriol. 189:950-957.
27. Ishidoh K, Kominami E. 2002. Processing and activation of lysosomal proteinases. Biol. Chem. 383:1827-1831.
28. Jiang SS, et al. 2010. Characterization of UDP-glucose dehydrogenase and UDP-glucose pyrophosphorylase mutants of Proteus mirabilis: defectiveness in polymyxin B resistance, swarming, and virulence. Antimicrob. Agents Chemother. 54:2000-2009.
29. Knirel YA, et al. 2007. Relationship of the lipopolysaccharide structure of Yersinia pestis to resistance to antimicrobial factors. Adv. Exp. Med. Biol. 603:88-96.
30. Krauss JH, Weckesser J, Mayer H. 1988. Electrophoretic Analysis of Lipopolysaccharides of Purple Nonsulfur Bacteria. Int. J. Syst. Bacteriol. 38:157-163.
31. Lathem WW, Crosby SD, Miller VL, Goldman WE. 2005. Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl. Acad. Sci. U. S. A. 102: 17786-17791.
32. Liberati NT, et al. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838.
33. Lilo S, Zheng Y, Bliska JB. 2008. Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector YopJ. Infect. Immun. 76:3911-3923.
34. Lukaszewski RA, et al. 2005. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73:7142-7150.
35. Marolda CL, Valvano MA. 1996. The GalF protein of Escherichia coli is not a UDP-glucose pyrophosphorylase but interacts with the GalU protein possibly to regulate cellular levels of UDP-glucose. Mol. Microbiol. 22:827-840.
36. Miller JH. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Murry JP, Sassetti CM, Lane JM, Xie Z, Rubin EJ. 2008. Transposon site hybridization in Mycobacterium tuberculosis. Methods Mol. Biol. 416: 45-59.
38. Nesper J, et al. 2001. Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect. Immun. 69:435-445.
39. Oyston PCF, et al. 2000. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68:3419-3425.
40. Palmer LE, Hobbie S, Galan JE, Bliska JB. 1998. YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF production and the downregulation of the MAP kinases p38 and JNK. Mol. Microbiol. 27:953-965.
41. Perry RD, Fetherston JD. 1997. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
42. Pujol C, Bliska JB. 2003. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect. Immun. 71:5892-5899.
43. Pujol C, Grabenstein JP, Perry RD, Bliska JB. 2005. Replication of Yersinia pestis in interferon gamma-activated macrophages requires ripA, a gene encoded in the pigmentation locus. Proc. Natl. Acad. Sci. U. S. A. 102:12909-12914.
44. Pujol C, et al. 2009. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect. Immun. 77:2551-2561.
45. Ramos-Morales F, Prieto AI, Beuzon CR, Holden DW, Casadesus J. 2003. Role for Salmonella enterica enterobacterial common antigen in bile resistance and virulence. J. Bacteriol. 185:5328-5332.
46. Rebeil R, Ernst RK, Gowen BB, Miller SI, Hinnebusch BJ. 2004. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 52:1363-1373.
47. Rosenberger CM, Gallo RL, Finlay BB. 2004. Interplay between antibacterial effectors: a macrophage antimicrobial peptide impairs intracellular Salmonella replication. Proc. Natl. Acad. Sci. U. S. A. 101:2422-2427.
48. Rotz LD, Khan AS, Lillibridge SR, Ostroff SM, Hughes JM. 2002. Public health assessment of potential biological terrorism agents. Emerg. Infect. Dis. 8:225-230.
49. Rubin EJ, et al. 1999. In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc. Natl. Acad. Sci. U. S. A. 96: 1645-1650.
50. Sassetti CM, Boyd DH, Rubin EJ. 2001. Comprehensive identification of conditionally essential genes in mycobacteria. Proc. Natl. Acad. Sci. U. S. A. 98:12712-12717.
51. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Biotechnology. 1:784-791.
52. Simonet M, Falkow S. 1992. Invasin expression in Yersinia pseudotuberculosis. Infect. Immun. 60:4414-4417.
53. Skurnik M, et al. 2007. Characterization and biological role of the O-polysaccharide gene cluster of Yersinia enterocolitica serotype O:9. J. Bacteriol. 189:7244-7253.
54. Skurnik M, Venho R, Bengoechea JA, Moriyon I. 1999. The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity. Mol. Microbiol. 31:1443-1462.
55. Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl. Genet. Mol. Biol. 3:Article3.
56. Straley SC, Harmon PA. 1984. Growth in mouse peritoneal macrophages of Yersinia pestis lacking established virulence determinants. Infect. Immun. 45:649-654.
57. Straley SC, Harmon PA. 1984. Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect. Immun. 45:655-659.
58. 't Hoen PA, de Kort F, van Ommen GJ, den Dunnen JT. 2003. Fluorescent labelling of cRNA for microarray applications. Nucleic Acids Res. 31:e20.
59. Tsai CM, Frasch CE. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
60. Viboud GI, Bliska JB. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59: 69-89.
61. Vieira OV, Botelho RJ, Grinstein S. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366:689-704.
62. Vilches S, et al. 2007. Mesophilic Aeromonas UDP-glucose pyrophosphorylase (GalU) mutants show two types of lipopolysaccharide structures and reduced virulence. Microbiology 153:2393-2404.
63. Winfield MD, Latifi T, Groisman EA. 2005. Transcriptional regulation of the 4-amino-4-deoxy-L-arabinose biosynthetic genes in Yersinia pestis. J. Biol. Chem. 280:14765-14772.