Insight into bacterial virulence mechanisms against host immune response via the yersinia pestis-human protein-protein interaction network

Infection and Immunity

Volumn 79, Issue 11, 2011, Pages 4413-4424

  Yang, Huiying ^a   Ke, Yuehua ^a   Wang, Jian ^b   Tan, Yafang ^a   Myeni, Sebenzile K ^c   Li, Dong ^b   Shi, Qinghai ^a   Yan, Yanfeng ^a   Chen, Hui ^b   Guo, Zhaobiao ^a   Yuan, Yanzhi ^b   Yang, Xiaoming ^b   Yang, Ruifu ^a   Du, Zongmin ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ARTICLE; BACTERIAL VIRULENCE; CELL FUNCTION; CYTOSKELETON; EPITHELIUM CELL; EPSTEIN BARR VIRUS; FOCAL ADHESION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LEUKOCYTE MIGRATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; YERSINIA PESTIS;

BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; PLAGUE; PROTEIN BINDING; VIRULENCE; YERSINIA PESTIS;

EID: 80855129283     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05622-11     Document Type: Article

References (83)

1. Agar, S. L., et al. 2009. Characterization of the rat pneumonic plague model: infection kinetics following aerosolization of Yersinia pestis CO92. Microbes Infect. 11:205-214.
2. Aili, M., E. L. Isaksson, B. Hallberg, H. Wolf-Watz, and R. Rosqvist. 2006. Functional analysis of the YopE GTPase-activating protein (GAP) activity of Yersinia pseudotuberculosis. Cell. Microbiol. 8:1020-1033.
3. Andersson, K., et al. 1996. YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol. Microbiol. 20:1057-1069.
4. Aoki-Kinoshita, K. F., and M. Kanehisa. 2007. Gene annotation and pathway mapping in KEGG. Methods Mol. Biol. 396:71-92.
5. Applewhite, D. A., et al. 2007. Ena/VASP proteins have an anti-capping independent function in filopodia formation. Mol. Biol. Cell 18:2579-2591.
6. Assenov, Y., F. Ramirez, S. E. Schelhorn, T. Lengauer, and M. Albrecht. 2008. Computing topological parameters of biological networks. Bioinformatics 24:282-284.
7. Bader, G. D., D. Betel, and C. W. Hogue. 2003. BIND: the Biomolecular Interaction Network Database. Nucleic Acids Res. 31:248-250.
8. Barz, C., T. N. Abahji, K. Trulzsch, and J. Heesemann. 2000. The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac-1. FEBS Lett. 482:139-143.
9. Barzik, M. 2005. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J. Biol. Chem. 280:28653-28662.
10. Black, D. S., and J. B. Bliska. 1997. Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J. 16:2730-2744.
11. Black, D. S., A. Marie-Cardine, B. Schraven, and J. B. Bliska. 2000. The Yersinia tyrosine phosphatase YopH targets a novel adhesion-regulated signalling complex in macrophages. Cell. Microbiol. 2:401-414.
12. Boquet, P. 2000. Small GTP binding proteins and bacterial virulence. Microbes Infect. 2:837-843.
13. Breitkreutz, B. J., et al. 2008. The BioGRID Interaction Database: 2008 update. Nucleic Acids Res. 36:D637-D640.
14. Brubaker, R. R. 2003. Interleukin-10 and inhibition of innate immunity to yersiniae: roles of Yops and LcrV (V antigen). Infect. Immun. 71:3673-3681.
15. Bubeck, S. S., A. M. Cantwell, and P. H. Dube. 2007. Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice. Infect. Immun. 75:697-705.
16. Busso, D., B. Delagoutte-Busso, and D. Moras. 2005. Construction of a set Gateway-based destination vectors for high-throughput cloning and expression screening in Escherichia coli. Anal. Biochem. 343:313-321.
17. Butler, T. 2009. Plague into the 21st century. Clin. Infect. Dis. 49:736-742.
18. Calderwood, M. A., et al. 2007. Epstein-Barr virus and virus human protein interaction maps. Proc. Natl. Acad. Sci. U. S. A. 104:7606-7611.
19. Chatr-Aryamontri, A., et al. 2007. MINT: the Molecular INTeraction database. Nucleic Acids Res. 35:D572-D574.
20. Cornelis, G. R., et al. 1998. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62:1315-1352.
21. Cornelis, G. R. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811-825.
22. de Chassey, B., et al. 2008. Hepatitis C virus infection protein network. Mol. Syst. Biol. 4:230.
23. Deleuil, F., L. Mogemark, M. S. Francis, H. Wolf-Watz, and M. Fallman. 2003. Interaction between the Yersinia protein tyrosine phosphatase YopH and eukaryotic Cas/Fyb is an important virulence mechanism. Cell. Microbiol. 5:53-64.
24. 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.
25. Dukuzumuremyi, J. M., et al. 2000. The Yersinia protein kinase A is a host factor inducible RhoA/Rac-binding virulence factor. J. Biol. Chem. 275: 35281-35290.
26. Dyer, M. D., T. M. Murali, and B. W. Sobral. 2008. The landscape of human proteins interacting with viruses and other pathogens. PLoS Pathog. 4:e32.
27. Dyer, M. D., et al. 2010. The human-bacterial pathogen protein interaction networks of Bacillus anthracis, Francisella tularensis, and Yersinia pestis. PLoS One 5:e12089.
28. Goh, K. I., E. Oh, H. Jeong, B. Kahng, and D. Kim. 2002. Classification of scale-free networks. Proc. Natl. Acad. Sci. U. S. A. 99:12583-12588.
29. Gomez, T. M., and E. Robles. 2004. The great escape; phosphorylation of Ena/VASP by PKA promotes filopodial formation. Neuron 42:1-3.
30. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
31. Han, Y., et al. 2005. DNA microarray analysis of the heat- and cold-shock stimulons in Yersinia pestis. Microbes Infect. 7:335-348.
32. Han, Y., et al. 2007. Comparative transcriptomics in Yersinia pestis: a global view of environmental modulation of gene expression. BMC Microbiol. 7:96.
33. Hentschke, M., wet al. 2010. Yersinia virulence factor YopM induces sustained RSK activation by interfering with dephosphorylation. PLoS One 5:e13165.
34. Higashide, W., S. Dai, V. P. Hombs, and D. Zhou. 2002. Involvement of SipA in modulating actin dynamics during Salmonella invasion into cultured epithelial cells. Cell. Microbiol. 4:357-365.
35. Huang, D. W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57.
36. Jeong, H., S. P. Mason, A. L. Barabasi, and Z. N. Oltvai. 2001. Lethality and centrality in protein networks. Nature 411:41-42.
37. Juris, S. J., A. E. Rudolph, D. Huddler, K. Orth, and J. E. Dixon. 2000. A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc. Natl. Acad. Sci. U. S. A. 97:9431-9436.
38. Juris, S. J., F. Shao, and J. E. Dixon. 2002. Yersinia effectors target mammalian signalling pathways. Cell. Microbiol. 4:201-211.
39. Kerrien, S., et al. 2007. IntAct-open source resource for molecular interaction data. Nucleic Acids Res. 35:D561-D565.
40. Krause, M., E. W. Dent, J. E. Bear, J. J. Loureiro, and F. B. Gertler. 2003. Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19:541-564.
41. LaCount, D. J., et al. 2005. A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438:103-107.
42. Lathem, W. W., S. D. Crosby, V. L. Miller, and W. E. Goldman. 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.
43. Lemaitre, N., F. Sebbane, D. Long, and B. J. Hinnebusch. 2006. Yersinia pestis YopJ suppresses tumor necrosis factor alpha induction and contributes to apoptosis of immune cells in the lymph node but is not required for virulence in a rat model of bubonic plague. Infect. Immun. 74:5126-5131.
44. Li, B., et al. 2005. Protein microarray for profiling antibody responses to Yersinia pestis live vaccine. Infect. Immun. 73:3734-3739.
45. Li, B., et al. 2009. High-throughput identification of new protective antigens from a Yersinia pestis live vaccine by enzyme-linked immunospot assay. Infect. Immun. 77:4356-4361.
46. Li, S., et al. 2004. A map of the interactome network of the metazoan C. elegans. Science 303:540-543.
47. Liu, H., et al. 2009. Transcriptional profiling of a mice plague model: insights into interaction between Yersinia pestis and its host. J. Basic Microbiol. 49:92-99.
48. Lu, Z., K. B. Cohen, and L. Hunter. 2007. GeneRIF quality assurance as summary revision. Pac. Symp. Biocomput. 269-280.
49. MacIntyre, S., et al. 2001. An extended hydrophobic interactive surface of Yersinia pestis Caf1M chaperone is essential for subunit binding and F1 capsule assembly. Mol. Microbiol. 39:12-25.
50. Maere, S., K. Heymans, and M. Kuiper. 2005. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448-3449.
51. McCoy, M. W., M. L. Marre, C. F. Lesser, and J. Mecsas. 2010. The C-terminal tail of Yersinia pseudotuberculosis YopM is critical for interacting with RSK1 and for virulence. Infect. Immun. 78:2584-2598.
52. Mejia, E., J. B. Bliska, and G. I. Viboud. 2008. Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog. 4:e3.
53. Mukherjee, S., et al. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312:1211-1214.
54. Navarro, L., et al. 2007. Identification of a molecular target for the Yersinia protein kinase A. Mol. Cell 26:465-477.
55. Noel, B. L., S. Lilo, D. Capurso, J. Hill, and J. B. Bliska. 2009. Yersinia pestis can bypass protective antibodies to LcrV and activation with gamma interferon to survive and induce apoptosis in murine macrophages. Clin. Vaccine Immunol. 16:1457-1466.
56. Ohta, Y., N. Suzuki, S. Nakamura, J. H. Hartwig, and T. P. Stossel. 1999. The small GTPase RalA targets filamin to induce filopodia. Proc. Natl. Acad. Sci. U. S. A. 96:2122-2128.
57. Pal Sharma, C., and W. H. Goldmann. 2004. Phosphorylation of actinbinding protein (ABP-280; filamin) by tyrosine kinase p56lck modulates actin filament cross-linking. Cell Biol. Int. 28:935-941.
58. Parkhill, J., et al. 2001. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527.
59. Parrish, J. R., et al. 2007. A proteome-wide protein interaction map for Campylobacter jejuni. Genome Biol. 8:R130.
60. Peri, S., et al. 2004. Human protein reference database as a discovery resource for proteomics. Nucleic Acids Res. 32:D497-D501.
61. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
62. Persson, C., N. Carballeira, H. Wolf-Watz, and M. Fallman. 1997. The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J. 16:2307-2318.
63. Prehna, G., M. I. Ivanov, J. B. Bliska, and C. E. Stebbins. 2006. Yersinia virulence depends on mimicry of host Rho-family nucleotide dissociation inhibitors. Cell 126:869-880.
64. Pujol, C., and J. B. Bliska. 2005. Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin. Immunol. 114:216-226.
65. Pujol, C., et al. 2009. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect. Immun. 77:2251-2261.
66. Rual, J. F., et al. 2005. Towards a proteome-scale map of the human protein- protein interaction network. Nature 437:1173-1178.
67. Shao, F., et al. 2003. Biochemical characterization of the Yersinia YopT protease: cleavage site and recognition elements in Rho GTPases. Proc. Natl. Acad. Sci. U. S. A. 100:904-909.
68. Simon, S. I., and C. E. Green. 2005. Molecular mechanics and dynamics of leukocyte recruitment during inflammation. Annu. Rev. Biomed. Eng. 7:151-185.
69. Sing, A., et al. 2002. Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196: 1017-1024.
70. Song, Y., et al. 2004. Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11:179-197.
71. Stelzl, U., et al. 2005. A human protein-protein interaction network: a resource for annotating the proteome. Cell 122:957-968.
72. Trasak, C., et al. 2007. Yersinia protein kinase YopO is activated by a novel G-actin binding process. J. Biol. Chem. 282:2268-2277.
73. Uetz, P., et al. 2006. Herpesviral protein networks and their interaction with the human proteome. Science 311:239-242.
74. Vastrik, I., et al. 2007. Reactome: a knowledge base of biologic pathways and processes. Genome Biol. 8:R39.
75. Velan, B., et al. 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.
76. Von Pawel-Rammingen, U., et al. 2000. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36:737-748.
77. Walhout, A. J., et al. 2000. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol.
78. Welch, W. J. 1990. Construction of permutation tests. J. Am. Stat. Assoc. 85:693-698.
79. Wentworth, J. K., G. Pula, and A. W. Poole. 2006. Vasodilator-stimulated phosphoprotein (VASP) is phosphorylated on Ser157 by protein kinase C-dependent and -independent mechanisms in thrombin-stimulated human platelets. Biochem. J. 393:555-564.
80. Xenarios, I., et al. 2002. DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions. Nucleic Acids Res. 30:303-305.
81. Ye, Z., et al. 2009. Gr1+ cells control growth of YopM-negative Yersinia pestis during systemic plague. Infect. Immun. 77:3791-3806.
82. Zhou, D., et al. 2006. Genome-wide transcriptional response of Yersinia pestis to stressful conditions simulating phagolysosomal environments. Microbes Infect. 8:2669-2678.
83. Zumbihl, R., et al. 1999. The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J. Biol. Chem. 274:29289-29293.