Posttranscriptional regulation of the Yersinia pestis Cyclic AMP receptor protein Crp and impact on virulence

mBio

Volumn 5, Issue 1, 2014, Pages

  Lathem, Wyndham W ^a   Schroeder, Jay A ^a   Bellows, Lauren E ^a,c   Ritzert, Jeremy T ^a   Koo, Jovanka T ^a,d   Price, Paul A ^b,e   Caulfield, Adam J ^a   Goldman, William E ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d WHEATON COLLEGE   (United States)

^e BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CYCLIC AMP BINDING PROTEIN; MESSENGER RNA; PROTEIN HFQ; PROTEIN PLA; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CONTROLLED STUDY; CRP GENE; FEMALE; GENE; GENE EXPRESSION; IN VIVO STUDY; MOUSE; NONHUMAN; PLA GENE; PLAGUE; PNEUMONIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS REGULATION; TEMPERATURE; TRANSCRIPTION REGULATION; YERSINIA PESTIS;

ANIMALS; CYCLIC AMP RECEPTOR PROTEIN; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MICE, INBRED C57BL; PLAGUE; TEMPERATURE; VIRULENCE; YERSINIA PESTIS;

EID: 84903362673     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01038-13     Document Type: Article

References (65)

1. Perry RD, Fetherston JD. 1997. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
2. Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, Gage KL, Leirs H, Rahalison L. 2008. Plague: past, present, and future. PLoS Med. 5:e3. http://dx.doi.org/10.1371/journal.pmed.1000003.
3. Lathem WW, Crosby SD, Miller VL, Goldman WE. 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. http://dx.doi.org/10.1073/pnas.0506840102.
4. Bubeck SS, Cantwell AM, Dube PH. 2007. Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice. Infect. Immun. 75:697-705. http://dx.doi.org/10.1128/IAI.00403-06.
5. Price PA, Jin J, Goldman WE. 2012. Pulmonary infection by Yersinia pestis rapidly establishes a permissive environment for microbial proliferation. Proc. Natl. Acad. Sci. U. S. A. 109:3083-3088. http://dx.doi.org/ 10.1073/pnas.1112729109.
6. Lathem WW, Price PA, Miller VL, Goldman WE. 2007. A plasminogenactivating protease specifically controls the development of primary pneumonic plague. Science 315:509-513. http://dx.doi.org/10.1126/ science.1137195.
7. Degen JL, Bugge TH, Goguen JD. 2007. Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost. 5(Suppl 1):24-31. http:// dx.doi.org/10.1111/j.1538-7836.2007.02519.x.
8. Korhonen TK, Haiko J, Laakkonen L, Järvinen HM, Westerlund-Wikström B. 2013. Fibrinolytic and coagulative activities of Yersinia pestis. Front. Cell. Infect. Microbiol. 3:35. http://dx.doi.org/10.3389/ fcimb.2013.00035.
9. Caulfield AJ, Lathem WW. 2012. Substrates of the plasminogen activator protease of Yersinia pestis. Adv. Exp. Med. Biol. 954:253-260. http:// dx.doi.org/10.1007/978-1-4614-3561-7_32.
10. Lawrenz MB, Pennington J, Miller VL. 2013. Acquisition of omptin reveals cryptic virulence function of autotransporter YapE in Yersinia pestis. Mol. Microbiol. 89:276-287. http://dx.doi.org/10.1111/mmi.12273.
11. Järvinen HM, Laakkonen L, Haiko J, Johansson T, Juuti K, Suomalainen M, Buchrieser C, Kalkkinen N, Korhonen TK. 2013. Human single-chain urokinase is activated by the omptins PgtE of Salmonella enterica and Pla of Yersinia pestis despite mutations of active site residues. Mol. Microbiol. 89:507-517. http://dx.doi.org/10.1111/mmi.12293.
12. Chromy BA, Choi MW, Murphy GA, Gonzales AD, Corzett CH, Chang BC, Fitch JP, McCutchen-Maloney SL. 2005. Proteomic characterization of Yersinia pestis virulence. J. Bacteriol. 187:8172-8180. http://dx.doi.org/ 10.1128/JB.187.23.8172-8180.2005.
13. Eren E, van den Berg B. 2012. Structural basis for activation of an integral membrane protease by lipopolysaccharide. J. Biol. Chem. 287: 23971-23976. http://dx.doi.org/10.1074/jbc.M112.376418.
14. Kukkonen M, Suomalainen M, Kyllönen P, Lähteenmäki K, Lång H, Virkola R, Helander IM, Holst O, Korhonen TK. 2004. Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica. Mol. Microbiol. 51:215-225.
15. Kim TJ, Chauhan S, Motin VL, Goh EB, Igo MM, Young GM. 2007. Direct transcriptional control of the plasminogen activator gene of Yersinia pestis by the cyclic AMP receptor protein. J. Bacteriol. 189: 8890-8900. http://dx.doi.org/10.1128/JB.00972-07.
16. Botsford JL, Harman JG. 1992. Cyclic AMP in prokaryotes. Microbiol. Rev. 56:100-122.
17. Zhan L, Han Y, Yang L, Geng J, Li Y, Gao H, Guo Z, Fan W, Li G, Zhang L, Qin C, Zhou D, Yang R. 2008. The cyclic AMP receptor protein, CRP, is required for both virulence and expression of the minimal CRP regulon in Yersinia pestis biovar Microtus. Infect. Immun. 76: 5028-5037. http://dx.doi.org/10.1128/IAI.00370-08.
18. Fic E, Bonarek P, Gorecki A, Kedracka-Krok S, Mikolajczak J, Polit A, Tworzydlo M, Dziedzicka-Wasylewska M, Wasylewski Z. 2009. cAMP receptor protein from Escherichia coli as a model of signal transduction in proteins-a review. J. Mol. Microbiol. Biotechnol. 17:1-11. http:// dx.doi.org/10.1159/000178014.
19. Busby S, Ebright RH. 1999. Transcription activation by catabolite activator protein (CAP). J. Mol. Biol. 293:199-213. http://dx.doi.org/ 10.1006/jmbi.1999.3161.
20. Saier MH. 1998. Multiple mechanisms controlling carbon metabolism in bacteria. Biotechnol. Bioeng. 58:170-174. http://dx.doi.org/10.1002/ (SICI)1097-0290(19980420)58:2/3.
21. Crasnier M. 1996. Cyclic AMP and catabolite repression. Res. Microbiol. 147:479-482. http://dx.doi.org/10.1016/0923-2508(96)84002-2.
22. Silva AJ, Benitez JA. 2004. Transcriptional regulation of Vibrio cholerae hemagglutinin/protease by the cyclic AMP receptor protein and RpoS. J. Bacteriol. 186:6374-6382. http://dx.doi.org/10.1128/JB.186.19.6374-6382.2004.
23. Müller CM, Aberg A, Straseviçiene J, Emody L, Uhlin BE, Balsalobre C. 2009. Type 1 fimbriae, a colonization factor of uropathogenic Escherichia coli, are controlled by the metabolic sensor CRP-cAMP. PLoS Pathog. 5:e1000303. http://dx.doi.org/10.1371/journal.ppat.1000303.
24. Petersen S, Young GM. 2002. Essential role for cyclic AMP and its receptor protein in Yersinia enterocolitica virulence. Infect. Immun. 70: 3665-3672. http://dx.doi.org/10.1128/IAI.70.7.3665-3672.2002.
25. Zhan L, Yang L, Zhou L, Li Y, Gao H, Guo Z, Zhang L, Qin C, Zhou D, Yang R. 2009. Direct and negative regulation of the sycO-ypkA-yopJ operon by cyclic AMP receptor protein (CRP) in Yersinia pestis. BMC Microbiol. 9:178. http://dx.doi.org/10.1186/1471-2180-9-178.
26. Heroven AK, Sest M, Pisano F, Scheb-Wetzel M, Steinmann R, Böhme K, Klein J, Münch R, Schomburg D, Dersch P. 2012. Crp induces switching of the CsrB and CsrC RNAs in Yersinia pseudotuberculosis and links nutritional status to virulence. Front. Cell Infect. Microbiol. 2:158. http://dx.doi.org/10.3389/fcimb.2012.00158.
27. Sun W, Roland KL, Kuang X, Branger CG, Curtiss R. 2010. Yersinia pestis with regulated delayed attenuation as a vaccine candidate to induce protective immunity against plague. Infect. Immun. 78:1304-1313. http://dx.doi.org/10.1128/IAI.01122-09.
28. Ishizuka H, Hanamura A, Inada T, Aiba H. 1994. Mechanism of the down-regulation of cAMP receptor protein by glucose in Escherichia coli: role of autoregulation of the crp gene. EMBO J. 13:3077-3082.
29. González-Gil G, Kahmann R, Muskhelishvili G. 1998. Regulation of crp transcription by oscillation between distinct nucleoprotein complexes. EMBO J. 17:2877-2885. http://dx.doi.org/10.1093/emboj/17.10.2877.
30. Berthoumieux S, de Jong H, Baptist G, Pinel C, Ranquet C, Ropers D, Geiselmann J. 2013. Shared control of gene expression in bacteria by transcription factors and global physiology of the cell. doi:10.1038/ msb.2012.70. Mol. Syst. Biol. 9:634. PubMed.
31. Aiba H. 1985. Transcription of the Escherichia coli adenylate cyclase gene is negatively regulated by cAMP-cAMP receptor protein. J. Biol. Chem. 260:3063-3070.
32. Hanamura A, Aiba H. 1991. Molecular mechanism of negative autoregulation of Escherichia coli crp gene. Nucleic Acids Res. 19:4413-4419. http://dx.doi.org/10.1093/nar/19.16.4413.
33. Zhang Y, Wang L, Han Y, Yan Y, Tan Y, Zhou L, Cui Y, Du Z, Wang X, Bi Y, Yang H, Song Y, Zhang P, Zhou D, Yang R. 2013. Autoregulation of PhoP/PhoQ and positive regulation of the cyclic AMP receptor protein-cyclic AMP complex by PhoP in Yersinia pestis. J. Bacteriol. 195: 1022-1030. http://dx.doi.org/10.1128/JB.01530-12.
34. Qu S, Zhang Y, Liu L, Wang L, Han Y, Yang R, Zhou D, Liu M. 2013. CyclicAMPreceptor protein is a repressor of adenylyl cyclase gene cyaA in Yersinia pestis. Can. J. Microbiol. 59:304-310. http://dx.doi.org/10.1139/ cjm-2012-0705.
35. Rajkowitsch L, Schroeder R. 2007. Dissecting RNA chaperone activity. RNA 13:2053-2060. http://dx.doi.org/10.1261/rna.671807.
36. Aiba H. 2007. Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol. 10:134-139. http://dx.doi.org/10.1016/ j.mib.2007.03.010.
37. Chao Y, Vogel J. 2010. The role of Hfq in bacterial pathogens. Curr. Opin. Microbiol. 13:24-33. http://dx.doi.org/10.1016/j.mib.2010.01.001.
38. Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, Benhammou J, Thompson KM, FitzGerald PC, Sowa NA, FitzGerald DJ. 2006. Small RNA regulators and the bacterial response to stress. Cold Spring Harb. Symp. Quant. Biol. 71:1-11. http://dx.doi.org/10.1101/ sqb.2006.71.016.
39. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69-82. http://dx.doi.org/10.1016/j.cell.2004.06.009.
40. Sittka A, Pfeiffer V, Tedin K, Vogel J. 2007. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol. Microbiol. 63:193-217. http://dx.doi.org/10.1111/j.1365-2958.2006.05489.x.
41. Geng J, Song Y, Yang L, Feng Y, Qiu Y, Li G, Guo J, Bi Y, Qu Y, Wang W, Wang X, Guo Z, Yang R, Han Y. 2009. Involvement of the posttranscriptional regulator Hfq in Yersinia pestis virulence. PLoS One 4:e6213. http://dx.doi.org/10.1371/journal.pone.0006213.
42. Schiano CA, Bellows LE, Lathem WW. 2010. The small RNA chaperone Hfq is required for the virulence of Yersinia pseudotuberculosis. Infect. Immun. 78:2034-2044. http://dx.doi.org/10.1128/IAI.01046-09.
43. Koo JT, Alleyne TM, Schiano CA, Jafari N, Lathem WW. 2011. Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersiniaspecific small, noncoding RNAs required for virulence. Proc. Natl. Acad. Sci. U. S. A. 108:E709-E717. http://dx.doi.org/10.1073/pnas.1101655108.
44. Schiano CA, Lathem WW. 2012. Post-transcriptional regulation of gene expression in Yersinia species. Front Cell. Infect. Microbiol. 2:129. http:// dx.doi.org/10.3389/fcimb.2012.00129.
45. Dennis JJ, Zylstra GJ. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of Gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
46. Bellows LE, Koestler BJ, Karaba SM, Waters CM, Lathem WW. 2012. Hfq-dependent, co-ordinate control of cyclic diguanylate synthesis and catabolism in the plague pathogen Yersinia pestis. Mol. Microbiol. 86: 661-674. http://dx.doi.org/10.1111/mmi.12011.
47. Bai G, Golubov A, Smith EA, McDonough KA. 2010. The importance of the small RNA chaperone Hfq for growth of epidemic Yersinia pestis, but not Yersinia pseudotuberculosis, with implications for plague biology. J. Bacteriol. 192:4239-4245. http://dx.doi.org/10.1128/JB.00504-10.
48. Ishizuka H, Hanamura A, Kunimura T, Aiba H. 1993. A lowered concentration of cAMP receptor protein caused by glucose is an important determinant for catabolite repression in Escherichia coli. Mol. Microbiol. 10:341-350. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01960.x.
49. Balsalobre C, Johansson J, Uhlin BE. 2006. Cyclic AMP-dependent osmoregulation of crp gene expression in Escherichia coli. J. Bacteriol. 188: 5935-5944. http://dx.doi.org/10.1128/JB.00235-06.
50. Zhang J, Sprung R, Pei J, Tan X, Kim S, Zhu H, Liu CF, Grishin NV, Zhao Y. 2009. Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Mol. Cell. Proteomics 8:215-225. http://dx.doi.org/10.1074/mcp.M800187-MCP200.
51. Yu BJ, Kim JA, Moon JH, Ryu SE, Pan JG. 2008. The diversity of lysine-acetylated proteins in Escherichia coli. J. Microbiol. Biotechnol. 18: 1529-1536.
52. Gao H, Zhang Y, Yang L, Liu X, Guo Z, Tan Y, Han Y, Huang X, Zhou D, Yang R. 2011. Regulatory effects of cAMP receptor protein (CRP) on porin genes and its own gene in Yersinia pestis. BMC Microbiol. 11:40. http://dx.doi.org/10.1186/1471-2180-11-40.
53. Groisman EA, Mouslim C. 2006. Sensing by bacterial regulatory systems in host and non-host environments. Nat. Rev. Microbiol. 4:705-709. http://dx.doi.org/10.1038/nrmicro1478.
54. Lutz R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res. 25:1203-1210. http://dx.doi.org/ 10.1093/nar/25.6.1203.
55. Zuker M. 1989. Computer prediction of RNA structure. Methods Enzymol. 180:262-288.
56. Sledjeski DD, Gupta A, Gottesman S. 1996. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli. EMBO J. 15:3993-4000.
57. Majdalani N, Hernandez D, Gottesman S. 2002. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol. 46:813-826. http://dx.doi.org/10.1046/j.1365-2958.2002.03203.x.
58. Achtman M, Zurth K, Morelli G, Torrea G, Guiyoule A, Carniel E. 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. U. S. A. 96:14043-14048. http://dx.doi.org/10.1073/pnas.96.24.14043.
59. Ligon BL. 2006. Plague: a review of its history and potential as a biological weapon. Semin. Pediatr. Infect. Dis. 17:161-170. http://dx.doi.org/ 10.1053/j.spid.2006.07.002.
60. Vadyvaloo V, Jarrett C, Sturdevant D, Sebbane F, Hinnebusch BJ. 2007. Analysis of Yersinia pestis gene expression in the flea vector. Adv. Exp. Med. Biol. 603:192-200. http://dx.doi.org/10.1007/978-0-387-72124-8_16.
61. Sebbane F, Lemaître N, Sturdevant DE, Rebeil R, Virtaneva K, Porcella SF, Hinnebusch BJ. 2006. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. U. S. A. 103:11766-11771. http://dx.doi.org/10.1073/ pnas.0601182103.
62. Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, Sterzenbach T, Tsolis RM, Roth JR, Bäumler AJ. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl. Acad. Sci. U. S. A. 108:17480-17485. http://dx.doi.org/10.1073/pnas.1107857108.
63. Biosystems, Applied. 1997. ABI Prism 7700 sequence detection system user bulletin 2. Applied Biosystems, Grand Island, NY.
64. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP. 2005. A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2:443-448. http:// dx.doi.org/10.1038/nmeth765.
65. Houppert AS, Bohman L, Merritt PM, Cole CB, Caulfield AJ, Lathem WW, Marketon MM. 2013. RfaL is required for Yersinia pestis type III secretion and virulence. Infect. Immun. 81:1186-1197. http://dx.doi.org/ 10.1128/IAI.01417-12.