Identifying and characterizing Hfq-RNA interactions

Methods

Volumn 63, Issue 2, 2013, Pages 144-159

  Faner, M A ^a   Feig, A L ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Hfq; NcRNA; Protein RNA interactions; SRNA

Indexed keywords

MESSENGER RNA; PROTEIN HFQ; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; BASE PAIRING; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; REGULATORY MECHANISM; REGULATORY RNA SEQUENCE; RIBOSOME; RNA DEGRADATION; SALMONELLA TYPHIMURIUM; STRESS;

ESCHERICHIA COLI; SALMONELLA TYPHIMURIUM;

(ARN)(X); 2-METHYLNICOTINIC ACID IMIDIZOLIDE; 5′ PHOSPHATE DEPENDENT TERMINATOR ENDONUCLEASE; 5′ RAPID AMPLIFICATION OF CDNA ENDS; 5′RACE; CLIP; CLR; CO-IP; COIMMUNOPRECIPITATION; CONTEXT LIKELIHOOD OF RELATEDNESS; CROSS-LINKING AND IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY GEL SHIFT ASSAY; EMSA; HFQ; HIGH THROUGH-PUT SEQUENCING; HTS; ISOTHERMAL TITRATION CALORIMETRY; ITC; LC-MS; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MALDI-TOF; MAST; MATRIX-ASSISTED LASER DESORPTION/IONIZATION TIME-OF-FLIGHT; MEME; MOTIF ALIGNMENT AND SEARCH TOOL; MULTIPLE EM FOR MOTIF ELICITATION; N-METHYLISATOIC ANHYDRIDE; NAI; NCRNA; NMIA; PROTEIN-RNA INTERACTIONS; QRT-PCR; QUANTITATIVE REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; RIBONUCLEOPROTEIN; RNP; RT; SELECTIVE 2′-HYDROXYL ACYLATION ANALYZED BY PRIMER EXTENSION; SELEX; SHAPE; SMALL REGULATORY RNAS; SPR; SRNA; SRNAS; SURFACE PLASMON RESONANCE; SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENT; TBE; TEX; TRIS/BORATE/EDTA; WHERE A IS ADENINE, R IS ADENINE OR GUANOSINE, AND N IS ANY NUCLEOTIDE;

BACTERIA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; IMMUNOPRECIPITATION; MODELS, MOLECULAR; PROTEIN BINDING; PROTEOMICS; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; SELEX APTAMER TECHNIQUE;

EID: 84885151374     PISSN: 10462023     EISSN: 10959130     Source Type: Journal    
DOI: 10.1016/j.ymeth.2013.04.023     Document Type: Article

References (130)

1. Storz G., Vogel J., Wassarman K.M. Mol. Cell 2011, 43:880-891.
2. Berezikov E. Nat. Rev. Genet. 2011, 12:846-860.
3. Waters L.S., Storz G. Cell 2009, 136:615-628.
4. Grundy F.J., Henkin T.M. Crit. Rev. Biochem. Mol. Biol. 2006, 41:329-338.
5. Brantl S. Curr. Opin. Microbiol. 2007, 10:102-109.
6. Aiba H. Curr. Opin. Microbiol. 2007, 10:134-139.
7. Fender A., Elf J., Hampel K., Zimmermann B., Wagner E.G. Genes Dev. 2010, 24:2621-2626.
8. Maki K., Morita T., Otaka H., Aiba H. Mol. Microbiol. 2010, 76:782-792.
9. Soper T., Mandin P., Majdalani N., Gottesman S., Woodson S.A. Proc. Natl. Acad. Sci. USA 2010, 107:9602-9607.
10. Doetsch M., Stampfl S., Furtig B., Beich-Frandsen M., Saxena K., Lybecker M., Schroeder R. Nucleic Acids Res. 2013, 41:487-497.
11. Lee T., Feig A. The RNA-protein complexes of E. coli Hfq: form and function. Non-Protein Coding RNAs 2008, 249-272. Elsevier, New York. N. Walter, S. Woodson, R. Batey (Eds.).
12. Chao Y., Vogel J. Curr. Opin. Microbiol. 2012, 13:24-33.
13. Ansong C., Yoon H., Porwollik S., Mottaz-Brewer H., Petritis B.O., Jaitly N., Adkins J.N., McClelland M., Heffron F., Smith R.D. PLoS One 2009, 4:e4809.
14. Christiansen J.K., Larsen M.H., Ingmer H., Sogaard-Andersen L., Kallipolitis B.H. J. Bacteriol. 2004, 186:3355-3362.
15. Tsui H.C., Leung H.C., Winkler M.E. Mol. Microbiol. 1994, 13:35-49.
16. Sittka A., Pfeiffer V., Tedin K., Vogel J. Mol. Microbiol. 2007, 63:193-217.
17. Ding Y., Davis B.M., Waldor M.K. Mol. Microbiol. 2004, 53:345-354.
18. Horstmann N., Orans J., Valentin-Hansen P., Shelburne S.A., Brennan R.G. Nucleic Acids Res. 2012, 40:11023-11035.
19. Mikulecky P.J., Kaw M.K., Brescia C.C., Takach J.C., Sledjeski D.D., Feig A.L. Nat. Struct. Mol. Biol. 2004, 11:1206-1214.
20. Link T.M., Valentin-Hansen P., Brennan R.G. Proc. Natl. Acad. Sci. USA 2009, 106:19292-19297.
21. Schumacher M.A., Pearson R.F., Moller T., Valentin-Hansen P., Brennan R.G. EMBO J. 2002, 21:3546-3556.
22. Brescia C.C., Mikulecky P.J., Feig A.L., Sledjeski D.D. RNA 2003, 9:33-43.
23. Otaka H., Ishikawa H., Morita T., Aiba H. Proc. Natl. Acad. Sci. USA 2011, 108:13059-13064.
24. Sauer E., Weichenrieder O. Proc. Natl. Acad. Sci. USA 2011, 108:13065-13070.
25. Soper T.J., Woodson S.A. RNA 2008, 14:1907-1917.
26. Salim N.N., Feig A.L. PLoS One 2010, 5:e13028.
27. Chen C.Y., Shyu A.B. Trends Biochem. Sci. 1995, 20:465-470.
28. Someya T., Baba S., Fujimoto M., Kawai G., Kumasaka T., Nakamura K. Nucleic Acids Res. 2012, 40:1856-1867.
29. Beich-Frandsen M., Vecerek B., Konarev P.V., Sjoblom B., Kloiber K., Hammerle H., Rajkowitsch L., Miles A.J., Kontaxis G., Wallace B.A., Svergun D.I., Konrat R., Blasi U., Djinovic-Carugo K. Nucleic Acids Res. 2011, 39:4900-4915.
30. Sauer E., Schmidt S., Weichenrieder O. Proc. Natl. Acad. Sci. USA 2012, 109:9396-9401.
31. Vincent H.A., Henderson C.A., Ragan T.J., Garza-Garcia A., Cary P.D., Gowers D.M., Malfois M., Driscoll P.C., Sobott F., Callaghan A.J. J. Mol. Biol. 2012, 420:56-69.
32. Beisel C.L., Storz G. FEMS Microbiol. Rev. 2010, 34:866-882.
33. Papenfort K., Vogel J. Res. Microbiol. 2009, 160:278-287.
34. Adamson D.N., Lim H.N. PLoS Comput. Biol. 2011, 7:e1002138.
35. Chao Y., Papenfort K., Reinhardt R., Sharma C.M., Vogel J. EMBO J. 2012, 31:4005-4019.
36. Sittka A., Lucchini S., Papenfort K., Sharma C.M., Rolle K., Binnewies T.T., Hinton J.C., Vogel J. PLoS Genet. 2008, 4:e1000163.
37. Majdalani N., Vanderpool C.K., Gottesman S. Crit. Rev. Biochem. Mol. Biol. 2005, 40:93-113.
38. Zhang A., Wassarman K.M., Rosenow C., Tjaden B.C., Storz G., Gottesman S. Mol. Microbiol. 2003, 50:1111-1124.
39. Hussein R., Lim H.N. Proc. Natl. Acad. Sci. USA 2011, 108:1110-1115.
40. Moon K., Gottesman S. Mol. Microbiol. 2011, 82:1545-1562.
41. Butland G., Peregrin-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., Starostine A., Richards D., Beattie B., Krogan N., Davey M., Parkinson J., Greenblatt J., Emili A. Nature 2005, 433:531-537.
42. Carabetta V.J., Silhavy T.J., Cristea I.M. J. Bacteriol. 2010, 192:3713-3721.
43. Hu P., Janga S.C., Babu M., Diaz-Mejia J.J., Butland G., Yang W., Pogoutse O., Guo X., Phanse S., Wong P., Chandran S., Christopoulos C., Nazarians-Armavil A., Nasseri N.K., Musso G., Ali M., Nazemof N., Eroukova V., Golshani A., Paccanaro A., Greenblatt J.F., Moreno-Hagelsieb G., Emili A. PLoS Biol. 2009, 7:e96.
44. Mohanty B.K., Maples V.F., Kushner S.R. Mol. Microbiol. 2004, 54:905-920.
45. Morita T., Maki K., Aiba H. Genes Dev. 2005, 19:2176-2186.
46. Carmichael G.G., Weber K., Niveleau A., Wahba A.J. J. Biol. Chem. 1975, 250:3607-3612.
47. Kajitani M., Kato A., Wada A., Inokuchi Y., Ishihama A. J. Bacteriol. 1994, 176:531-534.
48. Masse E., Vanderpool C.K., Gottesman S. J. Bacteriol. 2005, 187:6962-6971.
49. Papenfort K., Pfeiffer V., Mika F., Lucchini S., Hinton J.C., Vogel J. Mol. Microbiol. 2006, 62:1674-1688.
50. Vanderpool C.K., Gottesman S. Mol. Microbiol. 2004, 54:1076-1089.
51. Vogel J., Luisi B.F. Nat. Rev. Microbiol. 2011, 9:578-589.
52. Christiansen J.K., Nielsen J.S., Ebersbach T., Valentin-Hansen P., Sogaard-Andersen L., Kallipolitis B.H. RNA 2006, 12:1383-1396.
53. Vogel J., Bartels V., Tang T.H., Churakov G., Slagter-Jager J.G., Huttenhofer A., Wagner E.G. Nucleic Acids Res. 2003, 31:6435-6443.
54. Zhang A., Wassarman K.M., Ortega J., Steven A.C., Storz G. Mol. Cell 2002, 9:11-22.
55. Sonnleitner E., Sorger-Domenigg T., Madej M.J., Findeiss S., Hackermuller J., Huttenhofer A., Stadler P.F., Blasi U., Moll I. Microbiology 2008, 154:3175-3187.
56. Ramos C.G., Grilo A.M., da Costa P.J., Leitao J.H. Genomics 2012, 101:139-184.
57. Messer L.I., Currey K.M., O'Neill B.J., Maizel J.V., Levin J.G., Gerwin B.I. Virology 1985, 146:146-152.
58. Wassarman K.M., Repoila F., Rosenow C., Storz G., Gottesman S. Genes Dev. 2001, 15:1637-1651.
59. Vanderpool C.K., Balasubramanian D., Lloyd C.R. Biochimie 2011, 93:1943-1949.
60. Chi S.W., Zang J.B., Mele A., Darnell R.B. Nature 2009, 460:479-486.
61. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.C., Munschauer M., Ulrich A., Wardle G.S., Dewell S., Zavolan M., Tuschl T. Cell 2010, 141:129-141.
62. Milek M., Wyler E., Landthaler M. Semin. Cell. Dev. Biol. 2012, 23:206-212.
63. Ule J., Jensen K., Mele A., Darnell R.B. Methods 2005, 37:376-386.
64. 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. PLoS One 2009, 4:e6213.
65. Roscetto E., Angrisano T., Costa V., Casalino M., Forstner K.U., Sharma C.M., Di Nocera P.P., De Gregorio E. J. Bacteriol. 2012, 194:5864-5874.
66. Guisbert E., Rhodius V.A., Ahuja N., Witkin E., Gross C.A. J. Bacteriol. 2007, 189:1963-1973.
67. Barra-Bily L., Fontenelle C., Jan G., Flechard M., Trautwetter A., Pandey S.P., Walker G.C., Blanco C. J. Bacteriol. 2010, 192:1719-1729.
68. Lorenz C., Gesell T., Zimmermann B., Schoeberl U., Bilusic I., Rajkowitsch L., Waldsich C., von Haeseler A., Schroeder R. Nucleic Acids Res. 2010, 38:3794-3808.
69. Altuvia S., Weinstein-Fischer D., Zhang A., Postow L., Storz G. Cell 1997, 90:43-53.
70. Balbontin R., Fiorini F., Figueroa-Bossi N., Casadesus J., Bossi L. Mol. Microbiol. 2010, 78:380-394.
71. Kierzek E., Kierzek R., Turner D.H., Catrina I.E. Biochemistry 2006, 45:581-593.
72. Papenfort K., Bouvier M., Mika F., Sharma C.M., Vogel J. Proc. Natl. Acad. Sci. USA 2010, 107:20435-20440.
73. Salim N.N., Faner M.A., Philip J.A., Feig A.L. Nucleic Acids Res. 2012, 40:8021-8032.
74. Soper T.J., Doxzen K., Woodson S.A. RNA 2011, 17:1544-1550.
75. Lease R.A., Woodson S.A. J. Mol. Biol. 2004, 344:1211-1223.
76. Olejniczak M. Biochemistry 2011, 50:4427-4440.
77. Lee T., Feig A.L. RNA 2008, 14:514-523.
78. Kawamoto H., Koide Y., Morita T., Aiba H. Mol. Microbiol. 2006, 61:1013-1022.
79. Jing M., Bowser M.T. Anal. Chim. Acta 2011, 686:9-18.
80. Katsamba P.S., Park S., Laird-Offringa I.A. Methods 2002, 26:95-104.
81. Feig A.L. Methods Enzymol. 2009, 468:409-422.
82. Perrin Polarisation de la lumiere de fluorescence vie moyenne des molecules dans l'etat excite. J. Phys. Radium 1926, 7:390-401.
83. Arluison V., Mutyam S.K., Mura C., Marco S., Sukhodolets M.V. Protein Sci. 2007, 16:1830-1841.
84. Sun X., Wartell R.M. Biochemistry 2006, 45:4875-4887.
85. Updegrove T.B., Correia J.J., Chen Y., Terry C., Wartell R.M. RNA 2011, 17:489-500.
86. Wang W., Wang L., Zou Y., Zhang J., Gong Q., Wu J., Shi Y. Genes Dev. 2011, 25:2106-2117.
87. Geissmann T.A., Touati D. EMBO J. 2004, 23:396-405.
88. Desnoyers G., Morissette A., Prevost K., Masse E. EMBO J. 2009, 28:1551-1561.
89. Lindell M., Romby P., Wagner E.G. RNA 2002, 8:534-541.
90. Merino E.J., Wilkinson K.A., Coughlan J.L., Weeks K.M. J. Am. Chem. Soc. 2005, 127:4223-4231.
91. Mitra S., Shcherbakova I.V., Altman R.B., Brenowitz M., Laederach A. Nucleic Acids Res. 2008, 36:e63.
92. Wilkinson K.A., Gorelick R.J., Vasa S.M., Guex N., Rein A., Mathews D.H., Giddings M.C., Weeks K.M. PLoS Biol. 2008, 6:e96.
93. Vasa S.M., Guex N., Wilkinson K.A., Weeks K.M., Giddings M.C. RNA 2008, 14:1979-1990.
94. Reuter J.S., Mathews D.H. BMC Bioinf. 2010, 11:129.
95. Lucks J.B., Mortimer S.A., Trapnell C., Luo S., Aviran S., Schroth G.P., Pachter L., Doudna J.A., Arkin A.P. Proc. Natl. Acad. Sci. USA 2011, 108:11063-11068.
96. Spitale R.C., Crisalli P., Flynn R.A., Torre E.A., Kool E.T., Chang H.Y. Nat. Chem. Biol. 2013, 9:18-20.
97. Fratczak A., Kierzek R., Kierzek E. Biochemistry 2011, 50:7647-7665.
98. Chen S., Zhang A., Blyn L.B., Storz G. J. Bacteriol. 2004, 186:6689-6697.
99. Jorgensen M.G., Nielsen J.S., Boysen A., Franch T., Moller-Jensen J., Valentin-Hansen P. Mol. Microbiol. 2012, 84:36-50.
100. Frohlich K.S., Papenfort K., Berger A.A., Vogel J. Nucleic Acids Res. 2012, 40:3623-3640.
101. Sharma C.M., Papenfort K., Pernitzsch S.R., Mollenkopf H.J., Hinton J.C., Vogel J. Mol. Microbiol. 2011, 81:1144-1165.
102. Bailey T.L., Gribskov M. J. Comput. Biol. 1998, 5:211-221.
103. Tjaden B. Nucleic Acids Res. 2008, 36:W109-W113.
104. Li W., Ying X., Lu Q., Chen L. Genomics Proteomics Bioinf. 2012, 10:276-284.
105. Hebrard M., Kroger C., Srikumar S., Colgan A., Handler K., Hinton J.C. RNA Biol. 2012, 9:437-445.
106. Postic G., Dubail I., Frapy E., Dupuis M., Dieppedale J., Charbit A., Meibom K.L. PLoS One 2012, 7:e41999.
107. Zhao Y., Li H., Hou Y., Cha L., Cao Y., Wang L., Ying X., Li W. Biochem. Biophys. Res. Commun. 2008, 372:346-350.
108. Busch A., Richter A.S., Backofen R. Bioinformatics 2008, 24:2849-2856.
109. Eggenhofer F., Tafer H., Stadler P.F., Hofacker I.L. Nucleic Acids Res. 2011, 39:W149-W154.
110. Ying X., Cao Y., Wu J., Liu Q., Cha L., Li W. PLoS One 2011, 6:e22705.
111. Modi S.R., Camacho D.M., Kohanski M.A., Walker G.C., Collins J.J. Proc. Natl. Acad. Sci. USA 2011, 108:15522-15527.
112. Mika F., Busse S., Possling A., Berkholz J., Tschowri N., Sommerfeldt N., Pruteanu M., Hengge R. Mol. Microbiol. 2012, 84:51-65.
113. Faith J.J., Hayete B., Thaden J.T., Mogno I., Wierzbowski J., Cottarel G., Kasif S., Collins J.J., Gardner T.S. PLoS Biol. 2007, 5:e8.
114. Masse E., Gottesman S. Proc. Natl. Acad. Sci. USA 2002, 99:4620-4625.
115. Argaman L., Hershberg R., Vogel J., Bejerano G., Wagner E.G., Margalit H., Altuvia S. Curr. Biol. 2001, 11:941-950.
116. Udekwu K.I., Darfeuille F., Vogel J., Reimegard J., Holmqvist E., Wagner E.G. Genes Dev. 2005, 19:2355-2366.
117. Mandin P., Gottesman S. EMBO J. 2010, 29:3094-3107.
118. De Lay N., Gottesman S. Mol. Microbiol. 2012, 86:524-538.
119. Mandin P., Gottesman S. Mol. Microbiol. 2009, 72:551-565.
120. Ulbrandt N.D., Newitt J.A., Bernstein H.D. Cell 1997, 88:187-196.
121. Papenfort K., Pfeiffer V., Lucchini S., Sonawane A., Hinton J.C., Vogel J. Mol. Microbiol. 2008, 68:890-906.
122. Bouvier M., Sharma C.M., Mika F., Nierhaus K.H., Vogel J. Mol. Cell 2008, 32:827-837.
123. Guillier M., Gottesman S. Nucleic Acids Res. 2008, 36:6781-6794.
124. Wadler C.S., Vanderpool C.K. Proc. Natl. Acad. Sci. USA 2007, 104:20454-20459.
125. Hershberg R., Altuvia S., Margalit H. Nucleic Acids Res. 2003, 31:1813-1820.
126. Jin Y., Watt R.M., Danchin A., Huang J.D. BMC Genomics 2009, 10:165.
127. Hobbs E.C., Astarita J.L., Storz G. J. Bacteriol. 2010, 192:59-67.
128. Urban J.H., Vogel J. Nucleic Acids Res. 2007, 35:1018-1037.
129. Majdalani N., Cunning C., Sledjeski D., Elliott T., Gottesman S. Proc. Natl. Acad. Sci. USA 1998, 95:12462-12467.
130. Zimmermann B., Bilusic I., Lorenz C., Schroeder R. Methods 2010, 52:125-132.