Interaction between Yersinia pestis and the host immune system

Infection and Immunity

Volumn 76, Issue 5, 2008, Pages 1804-1811

  Li, Bei ^a   Yang, Ruifu ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CYTOKINE; PATTERN RECOGNITION RECEPTOR; PROTEIN DERIVATIVE; PROTEIN LCRV; TOLL LIKE RECEPTOR 4; YERSINIA OUTER PROTEIN E;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; BACTERIAL IMMUNITY; BACTERIAL VIRULENCE; CELL MATURATION; CELLULAR IMMUNITY; CHEMOTAXIS; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; HOST PATHOGEN INTERACTION; HUMAN; HUMORAL IMMUNITY; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; INFECTION RESISTANCE; INFLAMMATION; INNATE IMMUNITY; LEUKOCYTE; MACROPHAGE; MAMMAL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SERUM; SHORT SURVEY; T LYMPHOCYTE ACTIVATION; YERSINIA PESTIS; YERSINIOSIS; IMMUNOLOGY; PLAGUE; REVIEW;

HOST-PATHOGEN INTERACTIONS; HUMANS; PLAGUE; YERSINIA PESTIS;

EID: 42949122126     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01517-07     Document Type: Short Survey

References (97)

1. Aepfelbacher, M., and J. Heesemann. 2001. Modulation of Rho GTPases and the actin cytoskeleton by Yersinia outer proteins (Yops). Int. J. Med. Microbiol. 291:269-276.
2. Aepfelbacher, M., R. Zumbihl, and J. Heesemann. 2005. Modulation of Rho GTPases and the actin cytoskeleton by YopT of Yersinia. Curr. Top. Microbiol. Immunol. 291:167-175.
3. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
4. Alonso, A., N. Bottini, S. Bruckner, S. Rahmouni, S. Williams, S. P. Schoenberger, and T. Mustelin. 2004. Lck dephosphorylation at Tyr-394 and inhibition of T-cell antigen receptor signaling by Yersinia phosphatase YopH. J. Biol. Chem. 279:4922-4928.
5. Anderson, G. W., Jr., S. E. Leary, E. D. Williamson, R. W. Titball, S. L. Welkos, P. L. Worsham, and A. M. Friedlander. 1996. Recombinant V antigen protects mice against pneumonic and bubonic plague caused by F1-capsule-positive and -negative strains of Yersinia pestis. Infect. Immun. 64:4580-4585.
6. Andersson, K., N. Carballeira, K. E. Magnusson, C. Persson, O. Stendahl, H. Wolf-Watz, and M. Fallman. 1996. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signaling associated with phagocytosis. Mol. Microbiol. 20:1057-1069.
7. Andrews, G. P., D. G. Heath, G. W. Anderson, Jr., S. L. Welkos, and A. M. Friedlander. 1996. Fraction 1 capsular antigen (F1) purification from Yersinia pestis CO92 and from an Escherichia coli recombinant strain and efficacy against lethal plague challenge. Infect. Immun. 64:2180-2187.
8. Andrews, G. P., S. T. Strachan, G. E. Benner, A. K. Sample, G. W. Anderson, Jr., J. J. Adamovicz, S. L. Welkos, J. K. Pullen, and A. M. Friedlander. 1999. Protective efficacy of recombinant Yersinia outer proteins against bubonic plague caused by encapsulated and nonencapsulated Yersinia pestis. Infect. Immun. 67:1533-1537.
9. Anisimov, A. P., S. V. Dentovskaya, G. M. Titareva, I. V. Bakhteeva, R. Z. Shaikhutdinova, S. V. Balakhonov, B. Lindner, N. A. Kocharova, S. N. Senchenkova, O. Holst, G. B. Pier, and Y. A. Knirel. 2005. Intraspecies and temperature-dependent variations in susceptibility of Yersinia pestis to the bactericidal action of serum and to polymyxin B. Infect. Immun. 73:7324-7331.
10. Bacarese-Hamilton, T., A. Ardizzoni, J. Gray, and A. Crisanti. 2004. Protein arrays for serodiagnosis of disease. Methods Mol. Biol. 264:271-283.
11. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245-252.
12. Bartra, S. S., K. L. Styer, D. M. O'Bryant, M. L. Nilles, B. J. Hinnebusch, A. Aballay, and G. V. Piano. 2008. Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein. Infect. Immun. 76:612-622.
13. Benner, G. E., G. P. Andrews, W. R. Byrne, S. D. Strachan, A. K. Sample, D. G. Heath, and A. M. Friedlander. 1999. Immune response to Yersinia outer proteins and other Yersinia pestis antigens after experimental plague infection in mice. Infect. Immun. 67:1922-1928.
14. Biedzka-Sarek, M., R. Venho, and M. Skurnik. 2005. Role of YadA, Ail, and lipopolysaccharide in serum resistance of Yersinia enterocolitica serotype O:3. Infect. Immun. 73:2232-2244.
15. Bliska, J. B., and S. Falkow. 1992. Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc. Natl. Acad. Sci. USA 89:3561-3565.
16. Bohn, E., S. Muller, J. Lauber, R. Geffers, N. Speer, C. Spieth, J. Krejci, B. Manncke, J. Buer, A. Zell, and I. B. Autenrieth. 2004. Gene expression patterns of epithelial cells modulated by pathogenicity factors of Yersinia enterocolitica. Cell Microbiol. 6:129-141.
17. Boland, A., and G. R. Cornelis. 1998. Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect. Immun. 66:1878-1884.
18. Bossi, P., and F. Bricaire. 2003. The plague, possible bioterrorist act. Presse Med. 32:804-807. (In French.)
19. Broussard, L. A. 2001. Biological agents: weapons of warfare and bioterrorism. Mol. Diagn. 6:323-333.
20. Brubaker, R. R. 2007. How the structural gene products of Yersinia pestis relate to virulence. Future Microbiol. 2:377-385.
21. Bruckner, S., S. Rhamouni, L. Tautz, J. B. Denault, A. Alonso, B. Becattini, G. S. Salvesen, and T. Mustelin. 2005. Yersinia phosphatase induces mitochondrially dependent apoptosis of T cells. J. Biol. Chem. 280:10388-10394.
22. Cornelis, G. R. 2002. Yersinia type III secretion: send in the effectors. J. Cell Biol. 158:401-408.
23. Cornelis, G. R. 2002. The Yersinia Ysc-Yop virulence apparatus. Int. J. Med. Microbiol. 291:455-462.
24. Cornelis, G. R., and H. Wolf-Watz. 1997. The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
25. Covert, B. A., J. S. Spencer, I. M. Orme, and J. T. Belisle. 2001. The application of proteomics in defining the T-cell antigens of Mycobacterium tuberculosis. Proteomics 1:574-586.
26. DeBord, K. L., D. M. Anderson, M. M. Marketon, K. A. Overheim, R. W. DePaolo, N. A. Ciletti, B. Jabri, and O. Schneewind. 2006. Immunogenicity and protective immunity against bubonic plague and pneumonic plague by immunization of mice with the recombinant V10 antigen, a variant of LcrV. Infect. Immun. 74:4910-4914.
27. DeLeo, F. R., and B. J. Hinnebusch. 2005. A plague upon the phagocytes. Nat. Med. 11:927-928.
28. Denecker, G., S. Totemeyer, L. J. Mota, P. Troisfontaines, I. Lambermont, C. Youta, I. Stainier, M. Ackermann, and G. R. Cornelis. 2002. Effect of low-and high-virulence Yersinia enterocolitica strains on the inflammatory response of human umbilical vein endothelial cells. Infect. Immun. 70:3510-3520.
29. Du, Y., R. Rosqvist, and A. Forsberg. 2002. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70:1453-1460.
30. Dziarski, R. 2006. Deadly plague versus mild-mannered TLR4. Nat. Immunol. 7:1017-1019.
31. Easterbrook, T. J., K. Reddin, A. Robinson, and N. Modi. 1995. Studies on the immunogenicity of the Pla protein from Yersinia pestis. Contrib. Microbiol. Immunol. 13:214-215.
32. Elvin, S. J., and E. D. Williamson. 2004. Stat 4 but not Stat 6 mediated immune mechanisms are essential in protection against plague. Microb. Pathog. 37:177-184.
33. Elvin, S. J., E. D. Williamson, J. C. Scott, J. N. Smith, G. Perez De Lema, S. Chilla, P. Clapham, K. Pfeffer, D. Schlondorff, and B. Luckow. 2004. Evolutionary genetics: ambiguous role of CCR5 in Yersinia pestis infection. Nature 430:417.
34. Goodin, J. L., R. W. Raab, R. L. McKown, G. L. Coffman, B. S. Powell, J. T. Enama, J. A. Ligon, and G. P. Andrews. 2005. Yersinia pestis outer membrane type III secretion protein YscC: expression, purification, characterization, and induction of specific antiserum. Protein Expr. Purif. 40:152-163.
35. Green, S. P., E. L. Hartland, R. M. Robins-Browne, and W. A. Phillips. 1995. Role of YopH in the suppression of tyrosine phosphorylation and respiratory burst activity in murine macrophages infected with Yersinia enterocolitica. J. Leukoc. Biol. 57:972-977.
36. Grosdent, N., I. Maridonneau-Parini, M. P. Sory, and G. R. Cornelis. 2002. Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect. Immun. 70:4165-4176.
37. Hill, J., C. D. Underwood, L. Sundberg, H. Astrom, S. E. Leary, A. Forsberg, and R. W. Titball. 2003. Immunological characterisation of sub-units of the Yersinia type III secretion apparatus. Adv. Exp. Med. Biol. 529:415-417.
38. Huang, X., and L. E. Lindler. 2004. The pH 6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect. Immun. 72:7212-7219.
39. Iriarte, M., and G. R. Cornelis. 1998. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29:915-929.
40. Juris, S. J., F. Shao, and J. E. Dixon. 2002. Yersinia effectors target mammalian signalling pathways. Cell Microbiol. 4:201-211.
41. Kerschen, E. J., D. A. Cohen, A. M. Kaplan, and S. C. Straley. 2004. The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect. Immun. 72:4589-4602.
42. Lawton, D. G., C. Longstaff, B. A. Wallace, J. Hill, S. E. Leary, R. W. Titball, and K. A. Brown. 2002. Interactions of the type III secretion pathway proteins LcrV and LcrG from Yersinia pestis are mediated by coiled-coil domains. J. Biol. Chem. 277:38714-38722.
43. Leary, S. E., K. F. Griffin, E. E. Galyov, J. Hewer, E. D. Williamson, A. Holmstrom, Forsberg, and R. W. Titball. 1999. Yersinia outer proteins (YOPS) E, K and N are antigenic but non-protective compared to V antigen, in a murine model of bubonic plague. Microb. Pathog. 26:159-169.
44. Leary, S. E., K. F. Griffin, H. S. Gannory, E. D. Williamson, and R. W. Titball. 1997. Expression of an F1/V fusion protein in attenuated Salmonella typhimurium and protection of mice against plague. Microb. Pathog. 23:167-179.
45. Leary, S. E., E. D. Williamson, K. F. Griffin, P. Russell, S. M. Eley, and R. W. Titball. 1995. Active immunization with recombinant V antigen from Yersinia pestis protects mice against plague. Infect. Immun. 63:2854-2858.
46. Lee, H. K., and A. Iwasaki. 2007. Innate control of adaptive immunity: dendritic cells and beyond. Semin. Immunol. 19:48-55.
47. Li, B., L. Jiang, Q. Song, J. Yang, Z. Chen, Z. Guo, D. Zhou, Z. Du, Y. Song, J. Wang, H. Wang, S. Yu, and R. Yang. 2005. Protein microarray for profiling antibody responses to Yersinia pestis live vaccine. Infect. Immun. 73:3734-3739.
48. Li, B., D. Zhou, Z. Wang, Z. Song, H. Wang, M. Li, and R. Yang. 2008. Antibody profiling in plague patients by protein microarray. Microbes Infect. 10:45-51.
49. Lindler, L. E., and B. D. Tall. 1993. Yersinia pestis pH 6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol. Microbiol. 8:311-324.
50. Lukaszewski, R. A., D. J. Kenny, R. Taylor, D. G. Rees, M. G. Hartley, and P. C. Oyston. 2005. Pathogenesis of Yersinia pestis infection in BALB/c mice: effects on host macrophages and neutrophils. Infect. Immun. 73:7142-7150.
51. Makoveichuk, E., P. Cherepanov, S. Lundberg, A. Forsberg, and G. Olivecrona. 2003. pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. J. Lipid Res. 44:320-330.
52. Marketon, M. M., R. W. DePaolo, K. L. DeBord, B. Jabri, and O. Schneewind. 2005. Plague bacteria target immune cells during infection. Science 309:1739-1741.
53. Matson, J. S., K. A. Durick, D. S. Bradley, and M. L. Nilles. 2005. Immunization of mice with YscF provides protection from Yersinia pestis infections. BMC Microbiol. 5:38.
54. McDonald, C., P. O. Vacratsis, J. B. Bliska, and J. E. Dixon. 2003. The yersinia virulence factor YopM forms a novel protein complex with two cellular kinases. J. Biol. Chem. 278:18514-18523.
55. Miller, S. I., R. K. Ernst, and M. W. Bader. 2005. LPS, TLR4 and infectious disease diversity. Nat. Rev. Microbiol. 3:36-46.
56. Montminy, S. W., N. Khan, S. McGrath, M. J. Walkowicz, F. Sharp, J. E. Conlon, K. Fukase, S. Kusumoto, C. Sweet, K. Miyake, S. Akira, R. J. Cotter, J. D. Goguen, and E. Lien. 2006. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7:1066-1073.
57. Murphy, B. S., C. R. Wulff, B. A. Garvy, and S. C. Straley. 2007. Yersinia pestis YadC: a novel vaccine candidate against plague. Adv. Exp. Med. Biol. 603:400-414.
58. Navarro, L., N. M. Alto, and J. E. Dixon. 2005. Functions of the Yersinia effector proteins in inhibiting host immune responses. Curr. Opin. Microbiol. 8:21-27.
59. Neuman de Vegvar, H. E., and W. H. Robinson. 2004. Microarray profiling of antiviral antibodies for the development of diagnostics, vaccines, and therapeutics. Clin. Immunol. 111:196-201.
60. Overheim, K. A., R. W. Depaolo, K. L. Debord, E. M. Morrin, D. M. Anderson, N. M. Green, R. R. Brubaker, B. Jabri, and O. Schneewind. 2005. LcrV plague vaccine with altered immunomodulatory properties. Infect. Immun. 73:5152-5159.
61. Oyston, P. C., N. Dorrell, K. Williams, S. R. Li, M. Green, R. W. Titball, and B. W. Wren. 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.
62. Parent, M. A., K. N. Berggren, L. W. Kummer, L. B. Wilhelm, F. M. Szaba, I. K. Mullarky, and S. T. Smiley. 2005. Cell-mediated protection against pulmonary Yersinia pestis infection. Infect. Immun. 73:7304-7310.
63. Parent, M. A., L. B. Wilhelm, L. W. Kummer, F. M. Szaba, I. K. Mullarky, and S. T. Smiley. 2006. Gamma interferon, tumor necrosis factor alpha, and nitric oxide synthase 2, key elements of cellular immunity, perform critical protective functions during humoral defense against lethal pulmonary Yersinia pestis infection. Infect. Immun. 74:3381-3386.
64. Pasare, C., and R. Medzhitov. 2005. Toll-like receptors: linking innate and adaptive immunity. Adv. Exp. Med. Biol. 560:11-18.
65. + phenotype of Yersinia enterocolitica. Infect. Immun. 40:166-171.
66. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis: etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
67. Pettersson, J., A. Holmstrom, J. Hill, S. Leary, E. Frithz-Lindsten, A. von Euler-Matell, E. Carlsson, R. Titball, A. Forsberg, and H. Wolf-Watz. 1999. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol. Microbiol. 32:961-976.
68. Philipovskiy, A. V., and S. T. Smiley. 2007. Vaccination with live Yersinia pestis primes CD4 and CD8 T cells that synergistically protect against lethal pulmonary Y. pestis infection. Infect. Immun. 75:878-885.
69. Pouliot, K., N. Pan, S. Wang, S. Lu, E. Lien, and J. D. Goguen. 2007. Evaluation of the role of LcrV-Toll-like receptor 2-mediated immunomodulation in the virulence of Yersinia pestis. Infect. Immun. 75:3571-3580.
70. Price, S. B., M. D. Freeman, and K. S. Yen. 1995. Transcriptional analysis of the Yersinia pestis pH 6 antigen gene. J. Bacteriol. 177:5997-6000.
71. Prior, J. L., P. G. Hitchen, D. E. Williamson, A. J. Reason, H. R. Morris, A. Dell, B. W. Wren, and R. W. Titball. 2001. Characterization of the lipopolysaccharide of Yersinia pestis. Microb. Pathog. 30:49-57.
72. Pujol, C., and J. B. Bliska. 2003. The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect. Immun. 71:5892-5899.
73. Pujol, C., and J. B. Bliska. 2005. Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin. Immunol. 114:216-226.
74. Rebeil, R., R. K. Ernst, C. O. Jarrett, K. N. Adams, S. I. Miller, and B. J. Hinnebusch. 2006. Characterization of late acyltransferase genes of Yersinia pestis and their role in temperature-dependent lipid A variation. J. Bacteriol. 188:1381-1388.
75. Reithmeier-Rost, D., J. Hill, S. J. Elvin, D. Williamson, S. Dittmann, A. Schmid, G. Wilharm, and A. Sing. 2007. The weak interaction of LcrV and TLR2 does not contribute to the virulence of Yersinia pestis. Microbes Infect. 9:997-1002.
76. Robinson, W. H. 2006. Antigen arrays for antibody profiling. Curr. Opin. Chem. Biol. 10:67-72.
77. Rosqvist, R., A. Forsberg, M. Rimpilainen, T. Bergman, and H. Wolf-Watz. 1990. The cytotoxic protein YopE of Yersinia obstructs the primary host defense. Mol. Microbiol. 4:657-667.
78. Sabhnani, L., M. Manocha, D. Tomar, D. Shashikiran, and D. N. Rao. 2003. Yersinia pestis F1 antigen: a correlation between antibody titres and subclass distribution with differential avidity in different inbred mouse strains. Int. Immunopharmacol. 3:1413-1418.
79. Schoppet, M., A. Bubert, and H. I. Huppertz. 2000. Dendritic cell function is perturbed by Yersinia enterocolitica infection in vitro. Clin. Exp. Immunol. 122:316-323.
80. Simpson, W. J., R. E. Thomas, and T. G. Schwan. 1990. Recombinant capsular antigen (fraction 1) from Yersinia pestis induces a protective antibody response in BALB/c mice. Am. J. Trop. Med. Hyg. 43:389-396.
81. Sing, A., D. Rost, N. Tvardovskaia, A. Roggenkamp, A. Wiedemann, C. J. Kirschning, M. Aepfelbacher, and J. Heesemann. 2002. Yersinia V-antigen exploits Toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196:1017-1024.
82. Sodhi, A., R. K. Sharma, and H. V. Batra. 2005. Yersinia rLcrV and rYopB inhibits the activation of murine peritoneal macrophages in vitro. Immunol. Lett. 99:146-152.
83. Straley, S. C., and P. A. Harmon. 1984. Yersinia pestis grows within phagolysosomes in mouse peritoneal macrophages. Infect. Immun. 45:655-659.
84. Swietnicki, W., B. S. Powell, and J. Goodin. 2005. Yersinia pestis Yop secretion protein F: purification, characterization, and protective efficacy against bubonic plague. Protein Expr. Purif. 42:166-172.
85. Takahashi, K., and T. Kawai. 2007. Pathogen recognition by Toll-like receptor. Nippon Rinsho. 65(Suppl. 2, Pt. 1):53-57. (In Japanese.)
86. Tan, L., and C. Darby. 2005. Yersinia pestis is viable with endotoxin composed of only lipid A. J. Bacteriol. 187:6599-6600.
87. Tanabe, M., H. S. Atkins, D. N. Harland, S. J. Elvin, A. J. Stagg, O. Mirza, R. W. Titball, B. Byrne, and K. A. Brown. 2006. The ABC transporter protein OppA provides protection against experimental Yersinia pestis infection. Infect. Immun. 74:3687-3691.
88. Trulzsch, K., G. Geginat, T. Sporleder, K. Ruckdeschel, R. Hoffmann, J. Heesemann, and H. Russmann. 2005. Yersinia outer protein P inhibits CD8 T-cell priming in the mouse infection model. J. Immunol. 174:4244-4251.
89. Une, T., and R. R. Brubaker. 1984. In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Infect. Immun. 43:895-900.
90. Velan, B., E. Bar-Haim, A. Zauberman, E. Mamroud, A. Shafferman, and S. Cohen. 2006. Discordance in the effects of Yersinia pestis on the dendritic cell functions manifested by induction of maturation and paralysis of migration. Infect. Immun. 74:6365-6376.
91. Welkos, S., A. Friedlander, D. McDowell, J. Weeks, and S. Tobery. 1998. V antigen of Yersinia pestis inhibits neutrophil chemotaxis. Microb. Pathog. 24:185-196.
92. Williamson, E. D., S. M. Eley, K. F. Griffin, M. Green, P. Russell, S. E. Leary, P. C. Oyston, T. Easterbrook, K. M. Reddin, and A. Robinson. 1995. A new improved sub-unit vaccine for plague: the basis of protection. FEMS Immunol. Med. Microbiol. 12:223-230.
93. Williamson, E. D., P. M. Vesey, K. J. Gillhespy, S. M. Eley, M. Green, and R. W. Titball. 1999. An IgG1 titre to the F1 and V antigens correlates with protection against plague in the mouse model. Clin. Exp. Immunol. 116:107-114.
94. Yao, T., J. Mecsas, J. I. Healy, S. Falkow, and Y. Chien. 1999. Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, yopH. J. Exp. Med. 190:1343-1350.
95. Zauberman, A., S. Cohen, E. Mamroud, Y. Flashner, A. Tidhar, R. Ber, E. Elhanany, A. Shafferman, and B. Velan. 2006. Interaction of Yersinia pestis with macrophages: limitations in YopJ-dependent apoptosis. Infect. Immun. 74:3239-3250.
96. Zhou, D., Y. Han, and R. Yang. 2006. Molecular and physiological insights into plague transmission, virulence, and etiology. Microbes Infect. 8:273-284.
97. Zhou, D., Z. Tong, Y. Song, Y. Han, D. Pei, X. Pang, J. Zhai, M. Li, B. Cui, Z. Qi, L. Jin, R. Dai, Z. Du, J. Wang, Z. Guo, P. Huang, and R. Yang. 2004. Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J. Bacteriol. 186:5147-5152.