5.9
CiteScore
5.9
Impact Factor
Volume 41 Issue 7
Jul.  2014
Turn off MathJax
Article Contents

Transcriptomic Response to Yersinia pestis: RIG-I Like Receptor Signaling Response Is Detrimental to the Host against Plague

doi: 10.1016/j.jgg.2014.05.006
More Information
  • Corresponding author: E-mail address: zongmindu@gmail.com (Zongmin Du); E-mail address: ruifuyang@gmail.com (Ruifu Yang)
  • Received Date: 2014-04-24
  • Accepted Date: 2014-05-14
  • Rev Recd Date: 2014-05-09
  • Available Online: 2014-06-02
  • Publish Date: 2014-07-20
  • Bacterial pathogens have evolved various mechanisms to modulate host immune responses for successful infection. In this study, RNA-sequencing technology was used to analyze the responses of human monocytes THP1 to Yersinia pestis infection. Over 6000 genes were differentially expressed over the 12 h infection. Kinetic responses of pathogen recognition receptor signaling pathways, apoptosis, antigen processing, and presentation pathway and coagulation system were analyzed in detail. Among them, RIG-I-like receptor (RLR) signaling pathway, which was established for antiviral defense, was significantly affected. Mice lacking MAVS, the adaptor of the RLR signaling pathway, were less sensitive to infection and exhibited lower IFN-β production, higher Th1-type cytokines IFN-γ and IL-12 production, and lower Th2-type cytokines IL-4 and IL-13 production in the serum compared with wild-type mice. Moreover, infection of pathogenic bacteria other than Y. pestis also altered the expression of the RLR pathway, suggesting that the response of RLR pathway to bacterial infection is a universal mechanism.
  • These authors contribute equally to this work.
  • loading
  • [1]
    Abramov, V.M., Khlebnikov, V.S., Vasiliev, A.M. et al. J. Proteome Res., 6 (2007),pp. 2222-2231
    [2]
    Bergsbaken, T., Cookson, B.T. Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis PLoS Pathog., 3 (2007),p. e161
    [3]
    Bergsbaken, T., Cookson, B.T. Innate immune response during Yersinia infection: critical modulation of cell death mechanisms through phagocyte activation J. Leukoc. Biol., 86 (2009),pp. 1153-1158
    [4]
    Boldrick, J.C., Alizadeh, A.A., Diehn, M. et al. Stereotyped and specific gene expression programs in human innate immune responses to bacteria Proc. Natl. Acad. Sci. USA, 99 (2002),pp. 972-977
    [5]
    Chiliveru, S., Birkelund, S., Paludan, S.R. Induction of interferon-stimulated genes by Chlamydia pneumoniae in fibroblasts is mediated by intracellular nucleotide-sensing receptors PLoS ONE, 5 (2010),p. e10005
    [6]
    Chiu, Y.H., Macmillan, J.B., Chen, Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway Cell, 138 (2009),pp. 576-591
    [7]
    Comer, J.E., Sturdevant, D.E., Carmody, A.B. et al. Infect. Immun., 78 (2010),pp. 5086-5098
    [8]
    Cornelis, G.R., Boland, A., Boyd, A.P. et al. The virulence plasmid of Yersinia, an antihost genome Microbiol. Mol. Biol. Rev., 62 (1998),pp. 1315-1352
    [9]
    Decker, T., Muller, M., Stockinger, S. The yin and yang of type I interferon activity in bacterial infection Nat. Rev. Immunol., 5 (2005),pp. 675-687
    [10]
    Depaolo, R.W., Tang, F., Kim, I. et al. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis Cell Host Microbe, 4 (2008),pp. 350-361
    [11]
    Duewell, P., Kono, H., Rayner, K.J. et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals Nature, 464 (2010),pp. 1357-1361
    [12]
    Durfee, L.A., Lyon, N., Seo, K. et al. The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15 Mol. Cell, 38 (2010),pp. 722-732
    [13]
    Galindo, C.L., Moen, S.T., Kozlova, E.V. et al. Comp. Funct. Genomics, 2009 (2009),p. 914762
    [14]
    Gordon, S. Alternative activation of macrophages Nat. Rev. Immunol., 3 (2003),pp. 23-35
    [15]
    Gordon, S., Martinez, F.O. Alternative activation of macrophages: mechanism and functions Immunity, 32 (2010),pp. 593-604
    [16]
    Grayson, T.H., Cooper, L.F., Wrathmell, A.B. et al. Host responses to Renibacterium salmoninarum and specific components of the pathogen reveal the mechanisms of immune suppression and activation Immunology, 106 (2002),pp. 273-283
    [17]
    Guinet, F., Ave, P., Jones, L. et al. PLoS ONE, 3 (2008),p. e1688
    [18]
    Han, Y., Zhou, D., Pang, X. et al. Microbiol. Immunol., 48 (2004),pp. 791-805
    [19]
    Huang da, W., Sherman, B.T., Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc, 4 (2009),pp. 44-57
    [20]
    Huang, Q., Liu, D., Majewski, P. et al. The plasticity of dendritic cell responses to pathogens and their components Science, 294 (2001),pp. 870-875
    [21]
    Imaizumi, T., Sashinami, H., Mori, F. et al. Listeria monocytogenes induces the expression of retinoic acid-inducible gene-I Microbiol. Immunol., 50 (2006),pp. 811-815
    [22]
    Jenner, R.G., Young, R.A. Insights into host responses against pathogens from transcriptional profiling Nat. Rev. Microbiol., 3 (2005),pp. 281-294
    [23]
    Kanneganti, T.D., Lamkanfi, M., Nunez, G. Intracellular NOD-like receptors in host defense and disease Immunity, 27 (2007),pp. 549-559
    [24]
    Kato, H., Takeuchi, O., Sato, S. et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature, 441 (2006),pp. 101-105
    [25]
    Kawahara, K., Tsukano, H., Watanabe, H. et al. Infect. Immun., 70 (2002),pp. 4092-4098
    [26]
    Kobayashi, S.D., Voyich, J.M., Buhl, C.L. et al. Global changes in gene expression by human polymorphonuclear leukocytes during receptor-mediated phagocytosis: cell fate is regulated at the level of gene expression Proc. Natl. Acad. Sci. USA, 99 (2002),pp. 6901-6906
    [27]
    Kobayashi, S.D., Braughton, K.R., Whitney, A.R. et al. Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils Proc. Natl. Acad. Sci. USA, 100 (2003),pp. 10948-10953
    [28]
    Kong, L., Sun, L., Zhang, H. et al. An essential role for RIG-I in toll-like receptor-stimulated phagocytosis Cell Host Microbe, 6 (2009),pp. 150-161
    [29]
    Korhonen, T.K., Haiko, J., Laakkonen, L. et al. Front. Cell Infect. Microbiol., 3 (2013),p. 35
    [30]
    Krishnan, J., Selvarajoo, K., Tsuchiya, M. et al. Toll-like receptor signal transduction Exp. Mol. Med., 39 (2007),pp. 421-438
    [31]
    Kukkonen, M., Lahteenmaki, K., Suomalainen, M. et al. Mol. Microbiol., 40 (2001),pp. 1097-1111
    [32]
    Lathem, W.W., Crosby, S.D., Miller, V.L. et al. Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 17786-17791
    [33]
    Lathem, W.W., Price, P.A., Miller, V.L. et al. A plasminogen-activating protease specifically controls the development of primary pneumonic plague Science, 315 (2007),pp. 509-513
    [34]
    Leary, S.E., Griffin, K.F., Galyov, E.E. et al. 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 (1999),pp. 159-169
    [35]
    Li, R., Yu, C., Li, Y. et al. SOAP2: an improved ultrafast tool for short read alignment Bioinformatics, 25 (2009),pp. 1966-1967
    [36]
    Li, X.D., Chiu, Y.H., Ismail, A.S. et al. Mitochondrial antiviral signaling protein (MAVS) monitors commensal bacteria and induces an immune response that prevents experimental colitis Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 17390-17395
    [37]
    Lin, J.S., Szaba, F.M., Kummer, L.W. et al. J. Immunol., 187 (2011),pp. 897-904
    [38]
    Liu, H., Wang, H., Qiu, J. et al. J. Basic Microbiol., 49 (2009),pp. 92-99
    [39]
    Lukaszewski, R.A., Kenny, D.J., Taylor, R. et al. Infect. Immun., 73 (2005),pp. 7142-7150
    [40]
    Monack, D.M., Mecsas, J., Ghori, N. et al. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 10385-10390
    [41]
    Monack, D.M., Mecsas, J., Bouley, D. et al. Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice J. Exp. Med., 188 (1998),pp. 2127-2137
    [42]
    Mortazavi, A., Williams, B.A., McCue, K. et al. Mapping and quantifying mammalian transcriptomes by RNA-seq Nat. Meth., 5 (2008),pp. 621-628
    [43]
    Mukherjee, S., Keitany, G., Li, Y. et al. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation Science, 312 (2006),pp. 1211-1214
    [44]
    Musson, J.A., Morton, M., Walker, N. et al. J. Biol. Chem., 281 (2006),pp. 26129-26135
    [45]
    Nakajima, R., Brubaker, R.R. Infect. Immun., 61 (1993),pp. 23-31
    [46]
    Nau, G.J., Richmond, J.F., Schlesinger, A. et al. Human macrophage activation programs induced by bacterial pathogens Proc. Natl. Acad. Sci. USA, 99 (2002),pp. 1503-1508
    [47]
    Nguyen, H., Hiscott, J., Pitha, P.M. The growing family of interferon regulatory factors Cytokine Growth Factor Rev., 8 (1997),pp. 293-312
    [48]
    Opitz, B., Vinzing, M., van Laak, V. et al. J. Biol. Chem., 281 (2006),pp. 36173-36179
    [49]
    Parent, M.A., Wilhelm, L.B., Kummer, L.W. et al. Infect. Immun., 74 (2006),pp. 3381-3386
    [50]
    Patel, A.A., Lee-Lewis, H., Hughes-Hanks, J. et al. Opposing roles for interferon regulatory factor-3 (IRF-3) and type I interferon signaling during plague PLoS Pathog., 8 (2012),p. e1002817
    [51]
    Pereira, M.S., Morgantetti, G.F., Massis, L.M. et al. J. Immunol., 187 (2011),pp. 6447-6455
    [52]
    Perry, R.D., Fetherston, J.D. Clin. Microbiol. Rev., 10 (1997),pp. 35-66
    [53]
    Philipovskiy, A.V., Cowan, C., Wulff-Strobel, C.R. et al. Infect. Immun., 73 (2005),pp. 1532-1542
    [54]
    Pouliot, K., Pan, N., Wang, S. et al. Infect. Immun., 75 (2007),pp. 3571-3580
    [55]
    Price, P.A., Jin, J., Goldman, W.E. Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 3083-3088
    [56]
    Rogers, J.V., Choi, Y.W., Giannunzio, L.F. et al. Microb. Pathog., 43 (2007),pp. 67-77
    [57]
    Satoh, T., Kato, H., Kumagai, Y. et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 1512-1517
    [58]
    Schafer, S.L., Lin, R., Moore, P.A. et al. Regulation of type I interferon gene expression by interferon regulatory factor-3 J. Biol. Chem., 273 (1998),pp. 2714-2720
    [59]
    Schroder, K., Tschopp, J. The inflammasomes Cell, 140 (2010),pp. 821-832
    [60]
    Sharma, R.K., Sodhi, A., Batra, H.V. Mol. Immunol., 42 (2005),pp. 695-701
    [61]
    Shim, H.K., Musson, J.A., Harper, H.M. et al. Immunology, 119 (2006),pp. 385-392
    [62]
    Sing, A., Reithmeier-Rost, D., Granfors, K. et al. A hypervariable N-terminal region of Yersinia LcrV determines Toll-like receptor 2-mediated IL-10 induction and mouse virulence Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 16049-16054
    [63]
    Sun, Q., Sun, L., Liu, H.H. et al. The specific and essential role of MAVS in antiviral innate immune responses Immunity, 24 (2006),pp. 633-642
    [64]
    Takaoka, A., Wang, Z., Choi, M.K. et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response Nature, 448 (2007),pp. 501-505
    [65]
    Takeuchi, O., Akira, S. Innate immunity to virus infection Immunol. Rev., 227 (2009),pp. 75-86
    [66]
    Unterholzner, L., Keating, S.E., Baran, M. et al. IFI16 is an innate immune sensor for intracellular DNA Nat. Immunol., 11 (2010),pp. 997-1004
    [67]
    von Delwig, A., Musson, J.A., Shim, H.K. et al. Distribution of productive antigen-processing activity for MHC class II presentation in macrophages Scand J. Immunol., 62 (2005),pp. 243-250
    [68]
    Waddell, S.J., Butcher, P.D., Stoker, N.G. RNA profiling in host-pathogen interactions Curr. Opin. Microbiol., 10 (2007),pp. 297-302
    [69]
    Wang, Z., Gerstein, M., Snyder, M. RNA-Seq: a revolutionary tool for transcriptomics Nat. Rev. Genet., 10 (2009),pp. 57-63
    [70]
    West, A.P., Koblansky, A.A., Ghosh, S. Recognition and signaling by toll-like receptors Annu. Rev. Cell. Dev. Biol., 22 (2006),pp. 409-437
    [71]
    Yamanaka, H., Hoyt, T., Yang, X. et al. Infect. Immun., 76 (2008),pp. 4564-4573
    [72]
    Yoneyama, M., Fujita, T. RNA recognition and signal transduction by RIG-I-like receptors Immunol. Rev., 227 (2009),pp. 54-65
    [73]
    Yoneyama, M., Kikuchi, M., Natsukawa, T. et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat. Immunol., 5 (2004),pp. 730-737
    [74]
    Zhang, X., Wu, J., Du, F. et al. The cytosolic DNA Sensor cGAS forms an oligomeric complex with DNA and undergoes switch-like conformational changes in the activation loop Cell Rep., 6 (2014),pp. 421-430
    [75]
    Zhang, Y., Bliska, J.B. Role of macrophage apoptosis in the pathogenesis of Yersinia Curr. Top. Microbiol. Immunol., 289 (2005),pp. 151-173
    [76]
    Zhang, Y., Mena, P., Romanov, G. et al. Infect. Immun., 80 (2012),pp. 206-214
    [77]
    Zhao, C., Denison, C., Huibregtse, J.M. et al. Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 10200-10205
    [78]
    Zhao, Y., Yang, J., Shi, J. et al. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus Nature, 477 (2011),pp. 596-600
    [79]
    Zheng, Y., Lilo, S., Mena, P. et al. YopJ-induced caspase-1 activation in Yersinia-infected macrophages: independent of apoptosis, linked to necrosis, dispensable for innate host defense PLoS ONE, 7 (2012),p. e36019
    [80]
    Zheng, Y., Lilo, S., Brodsky, I.E. et al. A Yersinia effector with enhanced inhibitory activity on the NF-kappaB pathway activates the NLRP3/ASC/caspase-1 inflammasome in macrophages PLoS Pathog., 7 (2011),p. e1002026
    [81]
    Zhou, H., Monack, D.M., Kayagaki, N. et al. Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation J. Exp. Med., 202 (2005),pp. 1327-1332
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (85) PDF downloads (0) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return