The ribosome binding site of a mini-ORF protects a T3SS mRNA from degradation by RNase E

Molecular Microbiology

Volumn 86, Issue 5, 2012, Pages 1167-1182

  Lodato, Patricia B ^a   Hsieh, Ping Kun ^b   Belasco, Joel G ^b   Kaper, James B ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE E; STRUCTURAL PROTEIN; TRANSLOCON;

ARTICLE; BINDING SITE; CYTOSOL; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENZYME DEGRADATION; INTESTINE EPITHELIUM CELL; NONHUMAN; OPEN READING FRAME; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; RIBOSOME; SEQUENCE ANALYSIS;

AU RICH ELEMENTS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; BINDING SITES; CODON; ECTHYMA, CONTAGIOUS; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA STABILITY; RNA, BACTERIAL; RNA, MESSENGER;

ESCHERICHIA COLI;

EID: 84870247169     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12050     Document Type: Article

References (66)

1. Agaisse, H., and Lereclus, D. (1996) STAB-SD: a Shine-Dalgarno sequence in the 5′ untranslated region is a determinant of mRNA stability. Mol Microbiol 20: 633-643.
2. Anupama, K., Leela, J.K., and Gowrishankar, J. (2011) Two pathways for RNase E action in Escherichia coli in vivo and bypass of its essentiality in mutants defective for Rho-dependent transcription termination. Mol Microbiol 82: 1330-1348.
3. Apirion, D. (1978) Isolation, genetic mapping and some characterization of a mutation in Escherichia coli that affects the processing of ribonuleic acid. Genetics 90: 659-671.
4. Baga, M., Goransson, M., Normark, S., and Uhlin, B.E. (1988) Processed mRNA with differential stability in the regulation of E. coli pilin gene expression. Cell 52: 197-206.
5. Baker, K.E., and Mackie, G.A. (2003) Ectopic RNase E sites promote bypass of 5′-end-dependent mRNA decay in Escherichia coli. Mol Microbiol 47: 75-88.
6. Bardey, V., Vallet, C., Robas, N., Charpentier, B., Thouvenot, B., Mougin, A., etal. (2005) Characterization of the molecular mechanisms involved in the differential production of erythrose-4-phosphate dehydrogenase, 3-phosphoglycerate kinase and class II fructose-1, 6-bisphosphate aldolase in Escherichia coli. Mol Microbiol 57: 1265-1287.
7. Bechhofer, D.H. (2009) Messenger RNA decay and maturation in Bacillus subtilis. Prog Mol Biol Transl Sci 85: 231-273.
8. Bhatt, S., Edwards, A.N., Nguyen, H.T., Merlin, D., Romeo, T., and Kalman, D. (2009) The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli. Infect Immun 77: 3552-3568.
9. Bouvet, P., and Belasco, J.G. (1992) Control of RNase E-mediated RNA degradation by 5′-terminal base pairing in E. coli. Nature 360: 488-491.
10. Bouvier, M., and Carpousis, A.J. (2011) A tale of two mRNA degradation pathways mediated by RNase E. Mol Microbiol 82: 1305-1310.
11. Bricker, A.L., and Belasco, J.G. (1999) Importance of a 5′ stem-loop for longevity of papA mRNA in Escherichia coli. J Bacteriol 181: 3587-3590.
12. Callaghan, A.J., Marcaida, M.J., Stead, J.A., McDowall, K.J., Scott, W.G., and Luisi, B.F. (2005) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature 437: 1187-1191.
13. Cam, K., Rome, G., Krisch, H.M., and Bouche, J.P. (1996) RNase E processing of essential cell division genes mRNA in Escherichia coli. Nucleic Acids Res 24: 3065-3070.
14. Campellone, K.G., Roe, A.J., Lobner-Olesen, A., Murphy, K.C., Magoun, L., Brady, M.J., etal. (2007) Increased adherence and actin pedestal formation by dam-deficient enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 63: 1468-1481.
15. Celesnik, H., Deana, A., and Belasco, J.G. (2007) Initiation of RNA decay in Escherichia coli by 5′ pyrophosphate removal. Mol Cell 27: 79-90.
16. Dasanayake, D., Richaud, M., Cyr, N., Caballero-Franco, C., Pittroff, S., Finn, R.M., etal. (2011) The N-terminal amphipathic region of the Escherichia coli type III secretion system protein EspD is required for membrane insertion and function. Mol Microbiol 81: 734-750.
17. Deana, A., Celesnik, H., and Belasco, J.G. (2008) The bacterial enzyme RppH triggers messenger RNA degradation by 5′ pyrophosphate removal. Nature 451: 355-358.
18. Emory, S.A., Bouvet, P., and Belasco, J.G. (1992) A 5′-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev 6: 135-148.
19. Garrey, S.M., and Mackie, G.A. (2011) Roles of the 5′-phosphate sensor domain in RNase E. Mol Microbiol 80: 1613-1624.
20. Garrey, S.M., Blech, M., Riffell, J.L., Hankins, J.S., Stickney, L.M., Diver, M., etal. (2009) Substrate binding and active site residues in RNases E and G: role of the 5′-sensor. J Biol Chem 284: 31843-31850.
21. Griffin, P.M., Ostroff, S.M., Tauxe, R.V., Greene, K.D., Wells, J.G., Lewis, J.H., and Blake, P.A. (1988) Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann Intern Med 109: 705-712.
22. Hamada, D., Hamaguchi, M., Suzuki, K.N., Sakata, I., and Yanagihara, I. (2010) Cytoskeleton-modulating effectors of enteropathogenic and enterohemorrhagic Escherichia coli: a case for EspB as an intrinsically less-ordered effector. FEBS J 277: 2409-2415.
23. Hambraeus, G., Karhumaa, K., and Rutberg, B. (2002) A 5′ stem-loop and ribosome binding but not translation are important for the stability of Bacillus subtilis aprE leader mRNA. Microbiology 148: 1795-1803.
24. Hansen, A.M., and Kaper, J.B. (2009) Hfq affects the expression of the LEE pathogenicity island in enterohaemorrhagic Escherichia coli. Mol Microbiol 73: 446-465.
25. Huang, H., Liao, J., and Cohen, S.N. (1998) Poly(A)- and poly(U)-specific RNA 3′ tail shortening by E. coli ribonuclease E. Nature 391: 99-102.
26. Ide, T., Laarmann, S., Greune, L., Schillers, H., Oberleithner, H., and Schmidt, M.A. (2001) Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol 3: 669-679.
27. Iizumi, Y., Sagara, H., Kabe, Y., Azuma, M., Kume, K., Ogawa, M., etal. (2007) The enteropathogenic E. coli effector EspB facilitates microvillus effacing and antiphagocytosis by inhibiting myosin function. Cell Host Microbe 2: 383-392.
28. Islam, M.S., Shaw, R.K., Frankel, G., Pallen, M.J., and Busby, S.J. (2012) Translation of a minigene in the 5′ leader sequence of the enterohaemorrhagic Escherichia coli LEE1 transcription unit affects expression of the neighbouring downstream gene. Biochem J 441: 247-253.
29. Jiang, X., and Belasco, J.G. (2004) Catalytic activation of multimeric RNase E and RNase G by 5′-monophosphorylated RNA. Proc Natl Acad Sci USA 101: 9211-9216.
30. Jimenez, R., Cruz-Migoni, S.B., Huerta-Saquero, A., Bustamante, V.H., and Puente, J.L. (2010) Molecular characterization of GrlA, a specific positive regulator of ler expression in enteropathogenic Escherichia coli. J Bacteriol 192: 4627-4642.
31. Kaper, J.B., Nataro, J.P., and Mobley, H.L. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
32. Kendall, M.M., Gruber, C.C., Rasko, D.A., Hughes, D.T., and Sperandio, V. (2011) Hfq virulence regulation in enterohemorrhagic Escherichia coli O157:H7 strain 86-24. J Bacteriol 193: 6843-6851.
33. Kime, L., Jourdan, S.S., Stead, J.A., Hidalgo-Sastre, A., and McDowall, K.J. (2010) Rapid cleavage of RNA by RNase E in the absence of 5′ monophosphate stimulation. Mol Microbiol 76: 590-604.
34. Knutton, S., Rosenshine, I., Pallen, M.J., Nisan, I., Neves, B.C., Bain, C., etal. (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17: 2166-2176.
35. Ko, J.H., and Lee, Y. (2006) RNA-conjugated template-switching RT-PCR method for generating an Escherichia coli cDNA library for small RNAs. J Microbiol Methods 64: 297-304.
36. Kokoska, R.J., and Steege, D.A. (1998) Appropriate expression of filamentous phage f1 DNA replication genes II and X requires RNase E-dependent processing and separate mRNAs. J Bacteriol 180: 3245-3249.
37. Koslover, D.J., Callaghan, A.J., Marcaida, M.J., Garman, E.F., Martick, M., Scott, W.G., and Luisi, B.F. (2008) The crystal structure of the Escherichia coli RNase E apoprotein and a mechanism for RNA degradation. Structure 16: 1238-1244.
38. Kozak, M. (2005) Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361: 13-37.
39. Kresse, A.U., Rohde, M., and Guzman, C.A. (1999) The EspD protein of enterohemorrhagic Escherichia coli is required for the formation of bacterial surface appendages and is incorporated in the cytoplasmic membranes of target cells. Infect Immun 67: 4834-4842.
40. Kresse, A.U., Beltrametti, F., Muller, A., Ebel, F., and Guzman, C.A. (2000) Characterization of SepL of enterohemorrhagic Escherichia coli. J Bacteriol 182: 6490-6498.
41. Lodato, P.B., and Kaper, J.B. (2009) Post-transcriptional processing of the LEE4 operon in enterohaemorrhagic Escherichia coli. Mol Microbiol 71: 273-290.
42. Luo, W., and Donnenberg, M.S. (2011) Interactions and predicted host membrane topology of the enteropathogenic Escherichia coli translocator protein EspB. J Bacteriol 193: 2972-2980.
43. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S., and Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92: 1664-1668.
44. McDowall, K.J., Hernandez, R.G., Lin-Chao, S., and Cohen, S.N. (1993) The ams-1 and rne-3071 temperature-sensitive mutations in the ams gene are in close proximity to each other and cause substitutions within a domain that resembles a product of the Escherichia coli mre locus. J Bacteriol 175: 4245-4249.
45. McDowall, K.J., Lin-Chao, S., and Cohen, S.N. (1994) A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. J Biol Chem 269: 10790-10796.
46. Mackie, G.A. (1998) Ribonuclease E is a 5′-end-dependent endonuclease. Nature 395: 720-723.
47. Mathy, N., Benard, L., Pellegrini, O., Daou, R., Wen, T., and Condon, C. (2007) 5′-to-3′ exoribonuclease activity in bacteria: role of RNase J1 in rRNA maturation and 5′ stability of mRNA. Cell 129: 681-692.
48. Mellies, J.L., Barron, A.M., and Carmona, A.M. (2007) Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun 75: 4199-4210.
49. Nakanishi, N., Abe, H., Ogura, Y., Hayashi, T., Tashiro, K., Kuhara, S., etal. (2006) ppGpp with DksA controls gene expression in the locus of enterocyte effacement (LEE) pathogenicity island of enterohaemorrhagic Escherichia coli through activation of two virulence regulatory genes. Mol Microbiol 61: 194-205.
50. Nilsson, P., and Uhlin, B.E. (1991) Differential decay of a polycistronic Escherichia coli transcript is initiated by RNase E-dependent endonucleolytic processing. Mol Microbiol 5: 1791-1799.
51. O'Connell, C.B., Creasey, E.A., Knutton, S., Elliott, S., Crowther, L.J., Luo, W., etal. (2004) SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol 52: 1613-1625.
52. Richards, J., Liu, Q., Pellegrini, O., Celesnik, H., Yao, S., Bechhofer, D.H., etal. (2011) An RNA pyrophosphohydrolase triggers 5′-exonucleolytic degradation of mRNA in Bacillus subtilis. Mol Cell 43: 940-949.
53. Roe, A.J., Yull, H., Naylor, S.W., Woodward, M.J., Smith, D.G., and Gally, D.L. (2003) Heterogeneous surface expression of EspA translocon filaments by Escherichia coli O157:H7 is controlled at the posttranscriptional level. Infect Immun 71: 5900-5909.
54. Sawers, R.G. (2005) Evidence for novel processing of the anaerobically inducible dicistronic focA-pfl mRNA transcript in Escherichia coli. Mol Microbiol 58: 1441-1453.
55. Schmidt, M.A. (2010) LEEways: tales of EPEC, ATEC and EHEC. Cell Microbiol 12: 1544-1552.
56. Sekiya, K., Ohishi, M., Ogino, T., Tamano, K., Sasakawa, C., and Abe, A. (2001) Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci USA 98: 11638-11643.
57. Shakhnovich, E.A., Davis, B.M., and Waldor, M.K. (2009) Hfq negatively regulates type III secretion in EHEC and several other pathogens. Mol Microbiol 74: 347-363.
58. Sharp, J.S., and Bechhofer, D.H. (2005) Effect of 5′-proximal elements on decay of a model mRNA in Bacillus subtilis. Mol Microbiol 57: 484-495.
59. Shaw, R.K., Daniell, S., Ebel, F., Frankel, G., and Knutton, S. (2001) EspA filament-mediated protein translocation into red blood cells. Cell Microbiol 3: 213-222.
60. Shine, J., and Dalgarno, L. (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71: 1342-1346.
61. Steitz, J.A., and Jakes, K. (1975) How ribosomes select initiator regions in mRNA: base pair formation between the 3′ terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc Natl Acad Sci USA 72: 4734-4738.
62. Tamura, M., Lee, K., Miller, C.A., Moore, C.J., Shirako, Y., Kobayashi, M., and Cohen, S.N. (2006) RNase E maintenance of proper FtsZ/FtsA ratio required for nonfilamentous growth of Escherichia coli cells but not for colony-forming ability. J Bacteriol 188: 5145-5152.
63. Tree, J.J., Wolfson, E.B., Wang, D., Roe, A.J., and Gally, D.L. (2009) Controlling injection: regulation of type III secretion in enterohaemorrhagic Escherichia coli. Trends Microbiol 17: 361-370.
64. Walsh, A.P., Tock, M.R., Mallen, M.H., Kaberdin, V.R., von Gabain, G.A., and McDowall, K.J. (2001) Cleavage of poly(A) tails on the 3′-end of RNA by ribonuclease E of Escherichia coli. Nucleic Acids Res 29: 1864-1871.
65. Walters, M., and Sperandio, V. (2006) Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect Immun 74: 5445-5455.
66. Wang, D., Roe, A.J., McAteer, S., Shipston, M.J., and Gally, D.L. (2008) Hierarchal type III secretion of translocators and effectors from Escherichia coli O157:H7 requires the carboxy terminus of SepL that binds to Tir. Mol Microbiol 69: 1499-1512.