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. 1995 Jul;177(13):3843–3854. doi: 10.1128/jb.177.13.3843-3854.1995

Mutations in yscC, yscD, and yscG prevent high-level expression and secretion of V antigen and Yops in Yersinia pestis.

G V Plano 1, S C Straley 1
PMCID: PMC177105  PMID: 7601852

Abstract

The Yersinia pestis low-Ca2+ response stimulon is responsible for the temperature- and Ca(2+)-regulated expression and secretion of plasmid pCD1-encoded antihost proteins (V antigen and Yops). We have previously shown that lcrD and yscR encode proteins that are essential for high-level expression and secretion of V antigen and Yops at 37 degrees C in the absence of Ca2+. In this study, we constructed and characterized mutants with in-frame deletions in yscC, yscD, and yscG of the ysc operon that contains yscA through yscM. All three mutants lost the Ca2+ requirement for growth at 37 degrees c, expressed only basal levels of V antigen and YopM in the presence or absence of Ca2+, and failed to secrete these proteins to the culture supernatant. Overproduction of YopM in these mutants failed to restore YopM export, showing that the mutations had a direct effect on secretion. The protein products of yscC, yscD, and yscG were identified and localized by immunoblot analysis. YscC was localized to the outer membrane of Y. pestis, while YscD was found in the inner membrane. YscG was distributed equally between the soluble and total membrane fractions. Double mutants were characterized to assess where YscC and YscD act in low-Ca2+ response (LCR) regulation. lcrH::cat-yscC and lcrH::cat-yscD double mutants were constitutively induced for expression of V antigen and YopM; however, these proteins were not exported. This finding showed that the ysc mutations did not directly decrease induction of LCR stimulon genes. In contrast, lcrE-yscC, lcrG-yscC, lcrE-yscD, and lcrG-yscD double mutants as well as an lcrE-lcrD double mutant expressed only basal levels of V antigen and YopM and also failed to secrete these proteins to the culture supernatant. These results indicated that a functional LCR secretion system was necessary for high-level expression of LCR stimulon proteins in the lcrE and lcrG mutants but not in an lcrH::cat mutant. Possible models of regulation which incorporate these results are discussed.

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Selected References

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  1. Allaoui A., Woestyn S., Sluiters C., Cornelis G. R. YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion. J Bacteriol. 1994 Aug;176(15):4534–4542. doi: 10.1128/jb.176.15.4534-4542.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andrews G. P., Maurelli A. T. mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-response protein, LcrD, of Yersinia pestis. Infect Immun. 1992 Aug;60(8):3287–3295. doi: 10.1128/iai.60.8.3287-3295.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ben-Gurion R., Shafferman A. Essential virulence determinants of different Yersinia species are carried on a common plasmid. Plasmid. 1981 Mar;5(2):183–187. doi: 10.1016/0147-619x(81)90019-6. [DOI] [PubMed] [Google Scholar]
  4. Bergman T., Erickson K., Galyov E., Persson C., Wolf-Watz H. The lcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium. J Bacteriol. 1994 May;176(9):2619–2626. doi: 10.1128/jb.176.9.2619-2626.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bergman T., Håkansson S., Forsberg A., Norlander L., Macellaro A., Bäckman A., Bölin I., Wolf-Watz H. Analysis of the V antigen lcrGVH-yopBD operon of Yersinia pseudotuberculosis: evidence for a regulatory role of LcrH and LcrV. J Bacteriol. 1991 Mar;173(5):1607–1616. doi: 10.1128/jb.173.5.1607-1616.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bischoff D. S., Ordal G. W. Identification and characterization of FliY, a novel component of the Bacillus subtilis flagellar switch complex. Mol Microbiol. 1992 Sep;6(18):2715–2723. doi: 10.1111/j.1365-2958.1992.tb01448.x. [DOI] [PubMed] [Google Scholar]
  8. Bischoff D. S., Weinreich M. D., Ordal G. W. Nucleotide sequences of Bacillus subtilis flagellar biosynthetic genes fliP and fliQ and identification of a novel flagellar gene, fliZ. J Bacteriol. 1992 Jun;174(12):4017–4025. doi: 10.1128/jb.174.12.4017-4025.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bliska J. B., Galán J. E., Falkow S. Signal transduction in the mammalian cell during bacterial attachment and entry. Cell. 1993 Jun 4;73(5):903–920. doi: 10.1016/0092-8674(93)90270-z. [DOI] [PubMed] [Google Scholar]
  10. Bliska J. B., Guan K. L., Dixon J. E., Falkow S. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1187–1191. doi: 10.1073/pnas.88.4.1187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brubaker R. R. The V antigen of yersiniae: an overview. Contrib Microbiol Immunol. 1991;12:127–133. [PubMed] [Google Scholar]
  12. Bölin I., Portnoy D. A., Wolf-Watz H. Expression of the temperature-inducible outer membrane proteins of yersiniae. Infect Immun. 1985 Apr;48(1):234–240. doi: 10.1128/iai.48.1.234-240.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cornelis G. R., Biot T., Lambert de Rouvroit C., Michiels T., Mulder B., Sluiters C., Sory M. P., Van Bouchaute M., Vanooteghem J. C. The Yersinia yop regulon. Mol Microbiol. 1989 Oct;3(10):1455–1459. doi: 10.1111/j.1365-2958.1989.tb00129.x. [DOI] [PubMed] [Google Scholar]
  14. Cornelis G. R., Sluiters C., Delor I., Geib D., Kaniga K., Lambert de Rouvroit C., Sory M. P., Vanooteghem J. C., Michiels T. ymoA, a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions. Mol Microbiol. 1991 May;5(5):1023–1034. doi: 10.1111/j.1365-2958.1991.tb01875.x. [DOI] [PubMed] [Google Scholar]
  15. Cornelis G., Sluiters C., de Rouvroit C. L., Michiels T. Homology between virF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. J Bacteriol. 1989 Jan;171(1):254–262. doi: 10.1128/jb.171.1.254-262.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cotton R. G. Detection of single base changes in nucleic acids. Biochem J. 1989 Oct 1;263(1):1–10. doi: 10.1042/bj2630001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Echols H., Lu C., Burgers P. M. Mutator strains of Escherichia coli, mutD and dnaQ, with defective exonucleolytic editing by DNA polymerase III holoenzyme. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2189–2192. doi: 10.1073/pnas.80.8.2189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fenselau S., Balbo I., Bonas U. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):390–396. doi: 10.1094/mpmi-5-390. [DOI] [PubMed] [Google Scholar]
  19. Ferber D. M., Brubaker R. R. Plasmids in Yersinia pestis. Infect Immun. 1981 Feb;31(2):839–841. doi: 10.1128/iai.31.2.839-841.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fields K. A., Plano G. V., Straley S. C. A low-Ca2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis. J Bacteriol. 1994 Feb;176(3):569–579. doi: 10.1128/jb.176.3.569-579.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Forsberg A., Rosqvist R., Wolf-Watz H. Regulation and polarized transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis. Trends Microbiol. 1994 Jan;2(1):14–19. doi: 10.1016/0966-842x(94)90339-5. [DOI] [PubMed] [Google Scholar]
  22. Forsberg A., Viitanen A. M., Skurnik M., Wolf-Watz H. The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis. Mol Microbiol. 1991 Apr;5(4):977–986. doi: 10.1111/j.1365-2958.1991.tb00773.x. [DOI] [PubMed] [Google Scholar]
  23. Fowler J. M., Brubaker R. R. Physiological basis of the low calcium response in Yersinia pestis. Infect Immun. 1994 Dec;62(12):5234–5241. doi: 10.1128/iai.62.12.5234-5241.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Galyov E. E., Håkansson S., Wolf-Watz H. Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol. 1994 Aug;176(15):4543–4548. doi: 10.1128/jb.176.15.4543-4548.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Galán J. E., Ginocchio C., Costeas P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol. 1992 Jul;174(13):4338–4349. doi: 10.1128/jb.174.13.4338-4349.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Genin S., Boucher C. A. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol Gen Genet. 1994 Apr;243(1):112–118. doi: 10.1007/BF00283883. [DOI] [PubMed] [Google Scholar]
  27. Goguen J. D., Yother J., Straley S. C. Genetic analysis of the low calcium response in Yersinia pestis mu d1(Ap lac) insertion mutants. J Bacteriol. 1984 Dec;160(3):842–848. doi: 10.1128/jb.160.3.842-848.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gough C. L., Genin S., Zischek C., Boucher C. A. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):384–389. doi: 10.1094/mpmi-5-384. [DOI] [PubMed] [Google Scholar]
  29. Groisman E. A., Ochman H. Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J. 1993 Oct;12(10):3779–3787. doi: 10.1002/j.1460-2075.1993.tb06056.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Haddix P. L., Straley S. C. Structure and regulation of the Yersinia pestis yscBCDEF operon. J Bacteriol. 1992 Jul;174(14):4820–4828. doi: 10.1128/jb.174.14.4820-4828.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hoe N. P., Goguen J. D. Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J Bacteriol. 1993 Dec;175(24):7901–7909. doi: 10.1128/jb.175.24.7901-7909.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hsia R. C., Small P. L., Bavoil P. M. Characterization of virulence genes of enteroinvasive Escherichia coli by TnphoA mutagenesis: identification of invX, a gene required for entry into HEp-2 cells. J Bacteriol. 1993 Aug;175(15):4817–4823. doi: 10.1128/jb.175.15.4817-4823.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hughes K. T., Gillen K. L., Semon M. J., Karlinsey J. E. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science. 1993 Nov 19;262(5137):1277–1280. doi: 10.1126/science.8235660. [DOI] [PubMed] [Google Scholar]
  34. Hwang I., Lim S. M., Shaw P. D. Cloning and characterization of pathogenicity genes from Xanthomonas campestris pv. glycines. J Bacteriol. 1992 Mar;174(6):1923–1931. doi: 10.1128/jb.174.6.1923-1931.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kado C. I., Liu S. T. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol. 1981 Mar;145(3):1365–1373. doi: 10.1128/jb.145.3.1365-1373.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kihara M., Homma M., Kutsukake K., Macnab R. M. Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences. J Bacteriol. 1989 Jun;171(6):3247–3257. doi: 10.1128/jb.171.6.3247-3257.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
  38. LAWTON W. D., ERDMAN R. L., SURGALLA M. J. BIOSYNTHESIS AND PURIFICATION OF V AND W ANTIGEN IN PASTEURELLA PESTIS. J Immunol. 1963 Aug;91:179–184. doi: 10.21236/ad0299868. [DOI] [PubMed] [Google Scholar]
  39. Lambert de Rouvroit C., Sluiters C., Cornelis G. R. Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Mol Microbiol. 1992 Feb;6(3):395–409. [PubMed] [Google Scholar]
  40. Leung K. Y., Straley S. C. The yopM gene of Yersinia pestis encodes a released protein having homology with the human platelet surface protein GPIb alpha. J Bacteriol. 1989 Sep;171(9):4623–4632. doi: 10.1128/jb.171.9.4623-4632.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lindler L. E., Klempner M. S., Straley S. C. Yersinia pestis pH 6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect Immun. 1990 Aug;58(8):2569–2577. doi: 10.1128/iai.58.8.2569-2577.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Malakooti J., Komeda Y., Matsumura P. DNA sequence analysis, gene product identification, and localization of flagellar motor components of Escherichia coli. J Bacteriol. 1989 May;171(5):2728–2734. doi: 10.1128/jb.171.5.2728-2734.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Michiels T., Cornelis G. R. Secretion of hybrid proteins by the Yersinia Yop export system. J Bacteriol. 1991 Mar;173(5):1677–1685. doi: 10.1128/jb.173.5.1677-1685.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Michiels T., Vanooteghem J. C., Lambert de Rouvroit C., China B., Gustin A., Boudry P., Cornelis G. R. Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol. 1991 Aug;173(16):4994–5009. doi: 10.1128/jb.173.16.4994-5009.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Michiels T., Wattiau P., Brasseur R., Ruysschaert J. M., Cornelis G. Secretion of Yop proteins by Yersiniae. Infect Immun. 1990 Sep;58(9):2840–2849. doi: 10.1128/iai.58.9.2840-2849.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Miller S., Pesci E. C., Pickett C. L. A Campylobacter jejuni homolog of the LcrD/FlbF family of proteins is necessary for flagellar biogenesis. Infect Immun. 1993 Jul;61(7):2930–2936. doi: 10.1128/iai.61.7.2930-2936.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Miller V. L., Mekalanos J. J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988 Jun;170(6):2575–2583. doi: 10.1128/jb.170.6.2575-2583.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mullis K. B., Faloona F. A. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–350. doi: 10.1016/0076-6879(87)55023-6. [DOI] [PubMed] [Google Scholar]
  49. Ohnishi K., Kutsukake K., Suzuki H., Lino T. A novel transcriptional regulation mechanism in the flagellar regulon of Salmonella typhimurium: an antisigma factor inhibits the activity of the flagellum-specific sigma factor, sigma F. Mol Microbiol. 1992 Nov;6(21):3149–3157. doi: 10.1111/j.1365-2958.1992.tb01771.x. [DOI] [PubMed] [Google Scholar]
  50. Perry R. D., Harmon P. A., Bowmer W. S., Straley S. C. A low-Ca2+ response operon encodes the V antigen of Yersinia pestis. Infect Immun. 1986 Nov;54(2):428–434. doi: 10.1128/iai.54.2.428-434.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Perry R. D., Pendrak M. L., Schuetze P. Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J Bacteriol. 1990 Oct;172(10):5929–5937. doi: 10.1128/jb.172.10.5929-5937.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Plano G. V., Barve S. S., Straley S. C. LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J Bacteriol. 1991 Nov;173(22):7293–7303. doi: 10.1128/jb.173.22.7293-7303.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Plano G. V., Straley S. C. Multiple effects of lcrD mutations in Yersinia pestis. J Bacteriol. 1993 Jun;175(11):3536–3545. doi: 10.1128/jb.175.11.3536-3545.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Price S. B., Cowan C., Perry R. D., Straley S. C. The Yersinia pestis V antigen is a regulatory protein necessary for Ca2(+)-dependent growth and maximal expression of low-Ca2+ response virulence genes. J Bacteriol. 1991 Apr;173(8):2649–2657. doi: 10.1128/jb.173.8.2649-2657.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Price S. B., Leung K. Y., Barve S. S., Straley S. C. Molecular analysis of lcrGVH, the V antigen operon of Yersinia pestis. J Bacteriol. 1989 Oct;171(10):5646–5653. doi: 10.1128/jb.171.10.5646-5653.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Price S. B., Straley S. C. lcrH, a gene necessary for virulence of Yersinia pestis and for the normal response of Y. pestis to ATP and calcium. Infect Immun. 1989 May;57(5):1491–1498. doi: 10.1128/iai.57.5.1491-1498.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Protsenko O. A., Anisimov P. I., Mozharov O. T., Konnov N. P., Popov Iu A. Vyiavlenie i kharakteristika plazmid chumnogo mikroba, determiniruiushchikh sintez pestitsina I, antigena fraktsiia I i ékzotoksina "myshinogo" toksina. Genetika. 1983 Jul;19(7):1081–1090. [PubMed] [Google Scholar]
  58. Ramakrishnan G., Zhao J. L., Newton A. The cell cycle-regulated flagellar gene flbF of Caulobacter crescentus is homologous to a virulence locus (lcrD) of Yersinia pestis. J Bacteriol. 1991 Nov;173(22):7283–7292. doi: 10.1128/jb.173.22.7283-7292.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Reisner B. S., Straley S. C. Yersinia pestis YopM: thrombin binding and overexpression. Infect Immun. 1992 Dec;60(12):5242–5252. doi: 10.1128/iai.60.12.5242-5252.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Rimpiläinen M., Forsberg A., Wolf-Watz H. A novel protein, LcrQ, involved in the low-calcium response of Yersinia pseudotuberculosis shows extensive homology to YopH. J Bacteriol. 1992 May;174(10):3355–3363. doi: 10.1128/jb.174.10.3355-3363.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Rosqvist R., Forsberg A., Rimpiläinen M., Bergman T., Wolf-Watz H. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol. 1990 Apr;4(4):657–667. doi: 10.1111/j.1365-2958.1990.tb00635.x. [DOI] [PubMed] [Google Scholar]
  62. Rosqvist R., Forsberg A., Wolf-Watz H. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun. 1991 Dec;59(12):4562–4569. doi: 10.1128/iai.59.12.4562-4569.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Rosqvist R., Magnusson K. E., Wolf-Watz H. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 1994 Feb 15;13(4):964–972. doi: 10.1002/j.1460-2075.1994.tb06341.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Salmond G. P., Reeves P. J. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem Sci. 1993 Jan;18(1):7–12. doi: 10.1016/0968-0004(93)90080-7. [DOI] [PubMed] [Google Scholar]
  65. Sanders L. A., Van Way S., Mullin D. A. Characterization of the Caulobacter crescentus flbF promoter and identification of the inferred FlbF product as a homolog of the LcrD protein from a Yersinia enterocolitica virulence plasmid. J Bacteriol. 1992 Feb;174(3):857–866. doi: 10.1128/jb.174.3.857-866.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Sasakawa C., Komatsu K., Tobe T., Suzuki T., Yoshikawa M. Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a. J Bacteriol. 1993 Apr;175(8):2334–2346. doi: 10.1128/jb.175.8.2334-2346.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Skryzpek E., Straley S. C. LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis. J Bacteriol. 1993 Jun;175(11):3520–3528. doi: 10.1128/jb.175.11.3520-3528.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Skrzypek E., Haddix P. L., Plano G. V., Straley S. C. New suicide vector for gene replacement in yersiniae and other gram-negative bacteria. Plasmid. 1993 Mar;29(2):160–163. doi: 10.1006/plas.1993.1019. [DOI] [PubMed] [Google Scholar]
  70. Straley S. C., Bowmer W. S. Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun. 1986 Feb;51(2):445–454. doi: 10.1128/iai.51.2.445-454.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Straley S. C., Plano G. V., Skrzypek E., Haddix P. L., Fields K. A. Regulation by Ca2+ in the Yersinia low-Ca2+ response. Mol Microbiol. 1993 Jun;8(6):1005–1010. doi: 10.1111/j.1365-2958.1993.tb01644.x. [DOI] [PubMed] [Google Scholar]
  72. Straley S. C., Skrzypek E., Plano G. V., Bliska J. B. Yops of Yersinia spp. pathogenic for humans. Infect Immun. 1993 Aug;61(8):3105–3110. doi: 10.1128/iai.61.8.3105-3110.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Une T., Brubaker R. R. In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Infect Immun. 1984 Mar;43(3):895–900. doi: 10.1128/iai.43.3.895-900.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Van Gijsegem F., Genin S., Boucher C. Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol. 1993 Aug;1(5):175–180. doi: 10.1016/0966-842x(93)90087-8. [DOI] [PubMed] [Google Scholar]
  75. Venkatesan M. M., Buysse J. M., Oaks E. V. Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus. J Bacteriol. 1992 Mar;174(6):1990–2001. doi: 10.1128/jb.174.6.1990-2001.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Viitanen A. M., Toivanen P., Skurnik M. The lcrE gene is part of an operon in the lcr region of Yersinia enterocolitica O:3. J Bacteriol. 1990 Jun;172(6):3152–3162. doi: 10.1128/jb.172.6.3152-3162.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Wattiau P., Bernier B., Deslée P., Michiels T., Cornelis G. R. Individual chaperones required for Yop secretion by Yersinia. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10493–10497. doi: 10.1073/pnas.91.22.10493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wattiau P., Cornelis G. R. SycE, a chaperone-like protein of Yersinia enterocolitica involved in Ohe secretion of YopE. Mol Microbiol. 1993 Apr;8(1):123–131. doi: 10.1111/j.1365-2958.1993.tb01209.x. [DOI] [PubMed] [Google Scholar]
  79. Woestyn S., Allaoui A., Wattiau P., Cornelis G. R. YscN, the putative energizer of the Yersinia Yop secretion machinery. J Bacteriol. 1994 Mar;176(6):1561–1569. doi: 10.1128/jb.176.6.1561-1569.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Yother J., Goguen J. D. Isolation and characterization of Ca2+-blind mutants of Yersinia pestis. J Bacteriol. 1985 Nov;164(2):704–711. doi: 10.1128/jb.164.2.704-711.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]

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