The role of the phoPQ operon in the pathogenesis of the fully virulent CO92 strain of Yersinia pestis and the IP32953 strain of Yersinia pseudotuberculosis

Microbial Pathogenesis

Volumn 50, Issue 6, 2011, Pages 314-321

  Bozue, Joel ^a   Mou, Sherry ^a,b   Moody, Krishna L ^a   Cote, Christopher K ^a   Trevino, Sylvia ^a   Fritz, David ^a   Worsham, Patricia ^a  

^a UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Macrophages; PhoP; PhoQ; Plague; Yersinia pestis; Yersinia pseudotuberculosis

Indexed keywords

BACTERIAL PROTEIN; PROTEIN PHOPQ; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENE DELETION; GENE LOSS; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; LD 50; MACROPHAGE; MOUSE; NONHUMAN; OPERON; PATHOGENESIS; PHOPQ GENE; PLAGUE; PRIORITY JOURNAL; WILD TYPE; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTION;

ANIMALS; BACTERIAL PROTEINS; GASTROINTESTINAL DISEASES; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VARIATION; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MUTATION; OPERON; PLAGUE; VIRULENCE; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

MURINAE; MUS; NEGIBACTERIA; YERSINIA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 79960725668     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2011.02.005     Document Type: Article

References (54)

1. Worsham P.L., McGovern T.W., Vietri N.J., Friedlander A.M. Plague. Medical aspects of biological warfare 2007, 91-119. Office of The Surgeon General, Washington, DC. Z.F. Dembek (Ed.).
2. Perry R.D., Fetherston J.D. Yersinia pestis - etiologic agent of plague. Clin Microbiol Rev 1997, 10:35-66.
3. Bercovier H., Mollaret H.H., Alonso J.M., Brault J., Fanning G.R., Steigerwalt A.G., et al. Intra- and interspecies relatedness of Yersinia pestis by DNA hybridization and its relationship to Yersinia pseudotuberculosis. Curr Microbiol 1980, 4:225-229.
4. Skurnik M., Peippo A., Ervela E. Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol Microbiol 2000, 37:316-330.
5. Achtman M., Zurth K., Morelli G., Torrea G., Guiyoule A., Carniel E. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 1999, 96:14043-14048.
6. Putzker M., Sauer H., Sobe D. Plague and other human infections caused by Yersinia species. Clin Lab 2001, 47:453-466.
7. Cornelis G.R., Biot T., Lambert de Rouvroit C., Michiels T., Mulder B., Sluiters C., et al. The Yersinia yop regulon. Mol Microbiol 1989, 3:1455-1459.
8. Straley S.C. The low-Ca2+ response virulence regulon of human-pathogenic Yersiniae. Microb Pathog 1991, 10:87-91.
9. Welkos S.L., Davis K.M., Pitt L.M., Worsham P.L., Freidlander A.M. Studies on the contribution of the F1 capsule-associated plasmid pFra to the virulence of Yersinia pestis. Contrib Microbiol Immunol 1995, 13:299-305.
10. Sodeinde O.A., Goguen J.D. Genetic analysis of the 9.5-kilobase virulence plasmid of Yersinia pestis. Infect Immun 1988, 56:2743-2748.
11. Sodeinde O.A., Subrahmanyam Y.V., Stark K., Quan T., Bao Y., Goguen J.D. A surface protease and the invasive character of plague. Science 1992, 258:1004-1007.
12. Groisman E.A., Chiao E., Lipps C.J., Heffron F. Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci U S A 1989, 86:7077-7081.
13. Vescovi E.G., Ayala Y.M., Di Cera E., Groisman E.A. Characterization of the bacterial sensor protein PhoQ. Evidence for distinct binding sites for Mg2+ and Ca2+. J Biol Chem 1997, 272:1440-1443.
14. Moon K., Gottesman S. A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 2009, 74:1314-1330.
15. Soncini F.C., Garcia Vescovi E., Solomon F., Groisman E.A. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 1996, 178:5092-5099.
16. Bearson B.L., Wilson L., Foster J.W. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J Bacteriol 1998, 180:2409-2417.
17. Zhou D., Han Y., Qiu J., Qin L., Guo Z., Wang X., et al. Genome-wide transcriptional response of Yersinia pestis to stressful conditions simulating phagolysosomal environments. Microbes Infect 2006, 8:2669-2678.
18. Fisher M.L., Castillo C., Mecsas J. Intranasal inoculation of mice with Yersinia pseudotuberculosis causes a lethal lung infection that is dependent on Yersinia outer proteins and PhoP. Infect Immun 2007, 75:429-442.
19. Grabenstein J.P., Fukuto H.S., Palmer L.E., Bliska J.B. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 2006, 74:3727-3741.
20. Grabenstein J.P., Marceau M., Pujol C., Simonet M., Bliska J.B. The response regulator PhoP of Yersinia pseudotuberculosis is important for replication in macrophages and for virulence. Infect Immun 2004, 72:4973-4984.
21. Oyston P.C., Dorrell N., Williams K., Li S.R., Green M., Titball R.W., et al. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 2000, 68:3419-3425.
22. Rebeil R., Ernst R.K., Gowen B.B., Miller S.I., Hinnebusch B.J. Variation in lipid A structure in the pathogenic Yersiniae. Mol Microbiol 2004, 52:1363-1373.
23. Groisman E.A., Parra-Lopez C., Salcedo M., Lipps C.J., Heffron F. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci U S A 1992, 89:11939-11943.
24. Garcia Vescovi E., Soncini F.C., Groisman E.A. Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 1996, 84:165-174.
25. Donnenberg M.S., Kaper J.B. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 1991, 59:4310-4317.
26. Conchas R.F., Carniel E. A highly efficient electroporation system for transformation of Yersinia. Gene 1990, 87:133-137.
27. Surgalla M.J., Beesley E.D. Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl Microbiol 1969, 18:834-837.
28. Chain P.S., Carniel E., Larimer F.W., Lamerdin J., Stoutland P.O., Regala W.M., et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 2004, 101:13826-13831.
29. Hitchen P.G., Prior J.L., Oyston P.C., Panico M., Wren B.W., Titball R.W., et al. Structural characterization of lipo-oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system. Mol Microbiol 2002, 44:1637-1650.
30. Sun Y.C., Koumoutsi A., Darby C. The response regulator PhoP negatively regulates Yersinia pseudotuberculosis and Yersinia pestis biofilms. FEMS Microbiol Lett 2009, 290:85-90.
31. Erickson D.L., Jarrett C.O., Wren B.W., Hinnebusch B.J. Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis. J Bacteriol 2006, 188:1113-1119.
32. Joshua G.W., Karlyshev A.V., Smith M.P., Isherwood K.E., Titball R.W., Wren B.W. A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 2003, 149:3221-3229.
33. Pujol C., Bliska J.B. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect Immun 2003, 71:5892-5899.
34. Pujol C., Klein K.A., Romanov G.A., Palmer L.E., Cirota C., Zhao Z., et al. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect Immun 2009, 77:2251-2261.
35. Straley S.C., Harmon P.A. Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect Immun 1984, 45:655-659.
36. Lukaszewski R.A., Kenny D.J., Taylor R., Rees D.G., Hartley M.G., Oyston P.C. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect Immun 2005, 73:7142-7150.
37. Friedlander A.M., Welkos S.L., Worsham P.L., Andrews G.P., Heath D.G., Anderson G.W., et al. Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin Infect Dis 1995, 21:S178-S181.
38. Welkos S., Pitt M.L., Martinez M., Friedlander A., Vogel P., Tammariello R. Determination of the virulence of the pigmentation-deficient and pigmentation-plasminogen activator-deficient strains of Yersinia pestis in non-human primate and mouse models of pneumonic plague. Vaccine 2002, 20:2206-2214.
39. Cathelyn J.S., Crosby S.D., Lathem W.W., Goldman W.E., Miller V.L. RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci U S A 2006, 103:13514-13519.
40. Doll J.M., Zeitz P.S., Ettestad P., Bucholtz A.L., Davis T., Gage K. Cat-transmitted fatal pneumonic plague in a person who traveled from Colorado to Arizona. Am J Trop Med Hyg 1994, 51:109-114.
41. Lambert M.A., Smith S.G. The PagN protein of Salmonella enterica serovar Typhimurium is an adhesin and invasin. BMC Microbiol 2008, 8:142.
42. Winfield M.D., Latifi T., Groisman E.A. Transcriptional regulation of the 4-amino-4-deoxy-L-arabinose biosynthetic genes in Yersinia pestis. J Biol Chem 2005, 280:14765-14772.
43. O'Loughlin J.L., Spinner J.L., Minnich S.A., Kobayashi S.D. Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect Immun 2010, 78:773-782.
44. Schild S., Lamprecht A.K., Fourestier C., Lauriano C.M., Klose K.E., Reidl J. Characterizing lipopolysaccharide and core lipid A mutant O1 and O139 Vibrio cholerae strains for adherence properties on mucus-producing cell line HT29-Rev MTX and virulence in mice. Int J Med Microbiol 2005, 295:243-251.
45. Clements A., Gaboriaud F., Duval J.F., Farn J.L., Jenney A.W., Lithgow T., et al. The major surface-associated saccharides of Klebsiella pneumoniae contribute to host cell association. PLoS One 2008, 3:e3817.
46. Worsham P.L., Roy C. Pestoides F, a Yersinia pestis strain lacking plasminogen activator, is virulent by the aerosol route. Adv Exp Med Biol 2003, 529:129-131.
47. Welkos S.L., Friedlander A.M., Davis K.J. Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain C092. Microb Pathog 1997, 23:211-223.
48. Straley S.C., Harmon P.A. Growth in mouse peritoneal macrophages of Yersinia pestis lacking established virulence determinants. Infect Immun 1984, 45:649-654.
49. Wang R.F., Kushner S.R. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 1991, 100:195-199.
50. McCarron R.M., Goroff D.K., Luhr J.E., Murphy M.A., Herscowitz H.B. Methods for the collection of peritoneal and alveolar macrophages. Methods Enzymol 1984, 108:274-284.
51. Anderson G.W., Leary S.E., Williamson E.D., Titball R.W., Welkos S.L., Worsham P.L., et al. Recombinant V antigen protects mice against pneumonic and bubonic plague caused by F1-capsule-positive and -negative strains of Yersinia pestis. Infect Immun 1996, 64:4580-4585.
52. Glynn A., Roy C.J., Powell B.S., Adamovicz J.J., Freytag L.C., Clements J.D. Protection against aerosolized Yersinia pestis challenge following homologous and heterologous prime-boost with recombinant plague antigens. Infect Immun 2005, 73:5256-5261.
53. Davis K.J., Vogel P., Fritz D.L., Steele K.E., Pitt M.L., Welkos S.L., et al. Bacterial filamentation of Yersinia pestis by beta-lactam antibiotics in experimentally infected mice. Arch pathology Laboratory Medicine 1997, 121:865-868.
54. Sun Y.C., Hinnebusch B.J., Darby C. Experimental evidence for negative selection in the evolution of a Yersinia pestis pseudogene. Proc Natl Acad Sci U S A 2008, 105:8097-8101.