Поиск РНК-модифицирующих ферментов Escherichia coli тема диссертации и автореферата по ВАК РФ 02.00.10, кандидат химических наук Головина, Анна Янковна

• Головина, Анна Янковна
• кандидат химических наук
• 2010

Оглавление диссертации кандидат химических наук Головина, Анна Янковна

Список сокращений

Введение

1. Обзор литературы.

1.1. Разнообразие модификаций РНК в клетке

1.2. РНК-метилтрансферазы бактерий: их структура и функции.

1.2.1. т5С и m5U метилтрансферазы

1.2.2. N-метилтрансферазы т6А метилтрансферазы m2G метилтрансферазы т'G метилтрансферазы

1.2.3. SPOUT-суперсемейство метилтрансфераз

1.2.4. SAM-радикальное суперсемейство метилтрансфераз

Введение диссертации (часть автореферата) на тему «Поиск РНК-модифицирующих ферментов Escherichia coli»

Нуклеиновые кислоты были открыты еще в конце 19 века, и сейчас ни один исследователь не может представить себе существование живой клетки без РНК. В 50-х годах 20 века группа русских учёных под предводительством Белозерского и Спирина показала, что большую часть РНК клетки составляет рибосомная РНК, обеспечивающая синтез всех белков. Не менее важное место в жизнедеятельности живых организмов занимают транспортная, матричная и другие малые'РНК. Для осуществления нормального функционирования, поддержания необходимой структуры, эффективности и специфичности взаимодействия со своими мишенями многие РНК (в особенности рРНК и тРНК) претерпевают множественные химические превращения, затрагивающие, как правило, азотистые основания и рибозу в нуклеотидах. За данные превращения ответственно огомное количество разнообразных специфических ферментов, причем в некоторых бактериальных геномах представленность их генов достигает 1% [1]. Жизненную необходимость модификаций РНК доказывает также существование различных механизмов контроля качества в клетке, которые приводят к быстрой деградации тРНК при её неполной модификации [2,3].

Функции многих модифицированных нуклеотидов бактериальных РНК до сих пор остаются неясными, и зачастую это связано с отсутствием каких-либо данных о ферментах, осуществляющих их. Знание о генах, кодирующих тот или иной фермент, дает возможность «включать» и «выключать» в клетке соответствующую модификацию, и такие манипуляции позволяют собрать исчерпывающую информацию о ее функции.

Альтернативный способ изучения влияния модифицированных нуклеотидов на функционирование рибосомы заключается в мутагенезе модифицируемых остатков. Мутации нуклеотида-мишени, как правило, приводят к отсутствию модификации. Такие мутации часто детальны для клетки. Гены мутантных рРНК можно экспрессировать только одновременно с генами рРНК дикого типа. В связи с этим, для дальнейшего изучения свойств рибосом, несущих летальные мутации в рРНК, возникает необходимость создать способ выделения рибосом, несущих в себе соответствующую летальную мутацию из смеси с рибосомами дикого типа.

Данная работа посвящена исследованию функций трех гипотетических метилтрансфераз Е. coli: YibK, YafE и YfiC, а также разработке удобного инструментария для выделения 30S субчастиц, которые могут содержать любые мутации, необходимые для изучения нуклеотидов, особо важных для функционирования рибосомы Е. coli.

1. Обзор литературы

Заключение диссертации по теме «Биоорганическая химия», Головина, Анна Янковна

4. Выводы

1. Метилтрансферазы YafE и YibK Е. coli способны метилировать 30S субчастицы рибосомы in vitro, но модификация нуклеотида m2G1516 16S РНК не осуществляется белками YafE и YibK

2. Белок YfiC осуществляет SAM-зависимое метилирование нуклеотида A3 7 тРНК(Уа' Е. coli с образованием остатка т6А.

3. Метилирование TPHKiVal с образованием ш6А37 способствует выживанию клеток при осмотическом и окислительном стрессе.

4. Вставка стрептавидин-связывающего аптамера в спираль 33а 16S рРНК позволяет выделять функционально-активные 30S субчастицы в чистом виде с помощью аффинной хроматографии.

Список литературы диссертационного исследования кандидат химических наук Головина, Анна Янковна, 2010 год

1. Bjôrk G.R., Ericson J.U., Gustafsson C.E., Hagervall T.G., Jônsson Y .H., Wikstrôm P.M. Transfer RNA modification. Annu. Rev. Biochem. (1987). 56: cc. 263-287.

2. Kadaba S., Krueger A., Trice T., Krecic A.M., Hinnebusch A.G., Anderson J. Nuclear surveillance and degradation of hypomodified initiator tRNAMet in S. cerevisiae. Genes Dev. (2004). 18: cc. 1227-1240.

3. Alexandrov A., Chernyakov I., Gu W., Hiley S.L., Hughes T.R., Grayhack E.J., Phizicky E.M. Rapid tRNA decay can result from lack of nonessential modifications. Mol. Cell. (2006). 21: cc. 87-96.

4. Rozenski J., Crain P.P., McCloskey J.A. The RNA Modification Database: 1999 update. Nucleic Acids Res. (1999). 27: cc. 196-197.

5. Sprinzl M., Horn C., Brown M., Ioudovitch A., Steinberg S. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. (1998). 26: cc. 148-153.

6. Dunin-Horkawicz S., Czerwoniec A., Gajda M.J., Feder M., Grosjean H., Bujnicki J.M. MODOMICS: a database of RNA modification pathways. Nucleic Acids Res. (2006). 34: cc. D145-149.

7. Andersen N.M., Douthwaite S. YebU is a m5C Methyltransferase Specific for 16 S rRNA Nucleotide 1407. Journal of Molecular Biology. (2006). 359: cc. 777-786.

8. Tran E., Brown J., Maxwell E.S. Evolutionary origins of the RNA-guided nucleotide-modiflcation complexes: from the primitive translation apparatus? Trends Biochem. Sci. (2004). 29: cc. 343-350.

9. Lafontaine D.L., Tollervey D. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci. (1998). 23: cc. 383-388.

10. Kiss T. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J. (2001). 20: cc. 3617-3622.

11. Sergiev P.V., Bogdanov A.A., Dontsova O.A. Ribosomal RNA guanine-(N2)-methytransferases and their targets. Nucleic Acids Res. (2007). 35: cc. 2295-2301.

12. Cantoni G.L. Biological methylation: selected aspects. Annu. Rev. Biochem. (1975). 44: cc. 435-451.

13. Demirci H., Larsen L.H.G., Hansen T., Rasmussen A., Cadambi A., Gregory S.T., Kirpekar F., Jogl G. Multi-site-specific 16S rRNA methyltransferase RsmF from Thermus thermophilus. RNA. (2010). 16: cc. 1584-1596.

14. Anantharaman V., Koonin E.V., Aravind L. SPOUT: a class of methyltransferases that includes spoU and trmD RNA methylase superfamilies, and novel superfamilies of predicted prokaryotic RNA methylases. J. Mol. Microbiol. Biotechnol. (2002). 4: cc. 71-75.

15. Michel G., Sauvé V., Larocque R., Li Y., Matte A., Cygler M. The structure of the RlmB 23S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot. Structure. (2002). 10: cc. 1303-1315.

16. Ahn H.J., Kim H., Yoon H., Lee B.I., Suh S.W., Yang J.K. Crystal structure of tRNA(ml G37)methytransferase: insights into tRNA recognition. EMBO J. (2003). 22: cc. 2593-2603.

17. Urbonavicius J., Qian Q., Durand J.M., Hagervall T.G., Bjôrk G.R. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. (2001). 20: cc. 4863-4873.

18. Christian T., Evilia C., Williams S., Hou Y. Distinct origins of tRNA(mlG37) methyltransferase. J. Mol. Biol. (2004). 339: cc. 707-719.

19. Purta E., van Vliet F., Tkaczuk K., Dunin-Horkawicz S., Mori H., Droogmans L., Bujnicki J. The yfhQ gene of Escherichia coli encodes a tRNA:Cm32/Um32 methyltransferase. BMC Molecular Biology. (2006). 7: cc. 23.

20. Goto-Ito S., Ito T., Ishii R., Muto Y., Bessho Y., Yokoyama S. Crystal structure of archaeal tRNA(m( 1 )G37)methyltransferase aTrm5. Proteins. (2008). 72: cc. 1274-1289.

21. Pôsfai J., Bhagwat A.S., Pôsfai G., Roberts R.J. Predictive motifs derived from cytosine methyltransferases. Nucleic Acids Res. (1989). 17: cc. 2421-2435.

22. Agarwalla S., Kealey J.T., Santi D.V., Stroud R.M. Characterization of the 23 S ribosomal RNA m5U1939 methyltransferase from Escherichia coli. J. Biol. Chem. (2002). 277: cc. 8835-8840.

23. Madsen C.T., Mengel-Jorgensen J., Kirpekar F., Douthwaite S. Identifying the methyltransferases for m(5)U747 and m(5)U1939 in 23S rRNA using MALDI mass spectrometry. Nucleic Acids Res. (2003). 31: cc. 4738-4746.

24. Kealey J.T., Gu X., Santi D.V. Enzymatic mechanism of tRNA (m5U54)methyItransferase. Biochimie. (1994). 76: cc. 1133-1142.

25. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H.D., Noller II.F. Crystal Structure of the Ribosome at 5.5 A Resolution. Science. (2001). 292: cc. 883-896.

26. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The Complete Atomic Structure of the Large Ribosomal Subunit at 2.4 A Resolution. Science. (2000). 289: cc. 905-920.

27. Liu M., Douthwaite S. Resistance to the macrolide antibiotic tylosin is conferred by single methylations at 23S rRNA nucleotides G748 and A2058 acting in synergy. Proc. Natl. Acad. Sci. U.S.A. (2002). 99: cc. 14658-14663.

28. Hansen L.H., Mauvais P., Douthwaite S. The macrolide-ketolide antibiotic binding site is formed by structures in domains II and V of 23S ribosomal RNA. Mol. Microbiol. (1999). 31:cc. 623-631.

29. Xiong L., Shah S., Mauvais P., Mankin A.S. A ketolide resistance mutation in domain II of 23S rRNA reveals the proximity of hairpin 35 to the peptidyl transferase centre. Mol. Microbiol. (1999). 31: cc. 633-639.

30. Gu X., Ivanetich K.M., Santi D.V. Recognition of the T-arm of tRNA by tRNA (m5U54)-methyltransferase is not sequence specific. Biochemistry. (1996). 35: cc. 11652-11659.

31. Alian A., Lee T.T., Griner S.L., Stroud R.M., Finer-Moore J. Structure of a TrmA-RNA complex: A consensus RNA fold contributes to substrate selectivity and catalysis in m5U methyltransferases. Proc Natl Acad Sci USA. (2008). 105: cc. 6876-6881.

32. Kealey J.T., Lee S., Floss H.G., Santi D.V. Stereochemistry of methyl transfer catalyzed by tRNA (m5U54)-methyltransferase--evidence for a single displacement mechanism. Nucleic Acids Res. (1991). 19: cc. 6465-6468.

33. Ivanetich K.M., Santi D.V. 5,6-dihydropyrimidine adducts in the reactions and interactions of pyrimidines with proteins. Prog. Nucleic Acid Res. Mol. Biol. (1992). 42: cc. 127-156.

34. Lee T.T., Agarwalla S., Stroud R.M. A unique RNA Fold in the RumA-RNA-cofactor ternary complex contributes to substrate selectivity and enzymatic function. Cell. (2005). 120: cc. 599-611.

35. Lee T.T., Agarwalla S., Stroud R.M. Crystal Structure of RumA, an Iron-Sulfur Cluster Containing E. coli Ribosomal RNA 5-Methyluridine Methyltransferase. Structure. (2004). 12: cc. 397-407.

36. Sticht H., Rosch P. The structure of iron-sulfur proteins. Progress in Biophysics and Molecular Biology. (1998). 70: cc. 95-136.

37. Reinisch K.M., Chen L., Verdine G.L., Lipscomb W.N. The crystal structure of Haelll methyltransferase convalently complexed to DNA: an extrahelical cytosine and rearranged base pairing. Cell. (1995). 82: cc. 143-153.

38. Foster P.G., Nunes C.R., Greene P., Moustakas D., Stroud R.M. The first structure of an RNA m5C methyltransferase, Fmu, provides insight into catalytic mechanism and specific binding of RNA substrate. Structure. (2003). 11: cc. 1609-1620.

39. Tscherne J.S., Nurse K., Popienick P., Michel H., Sochacki M., Ofengand J. Purification, Cloning, and Characterization of the 16S RNA m5C967 Methyltransferase from Escherichia colij. Biochemistry. (1999). 38: cc. 1884-1892.

40. Gu X.R., Gustafsson C., Ku J., Yu M., Santi D.V. Identification of the 16S rRNA m5C967 Methyltransferase from Escherichia coli"j\ Biochemistry. (1999). 38: cc. 4053-4057.

41. Purta E., O'Connor M., Bujnicki J.M., Douthwaite S. YccW is the m5C methyltransferase specific for 23S rRNA nucleotide 1962. J. Mol. Biol. (2008). 383: cc. 641-651.

42. Reid R., Greene P. J., Santi D.V. Exposition of a family of RNA m(5)C methyltransferases from searching genomic and proteomic sequences. Nucleic Acids Res. (1999). 27: cc. 31383145.

43. Bujnicki J.M., Feder M., Ayres C.L., Redman K.L. Sequence-structure-function studies of tRNA:m5C methyltransferase Trm4p and its relationship to DNA:m5C and RNA:m5U methyltransferases. Nucleic Acids Res. (2004). 32: cc. 2453-2463.

44. Liu Y., Santi D.V. m5C RNA and m5C DNA methyl transferases use different cysteine residues as catalysts. Proc. Natl. Acad. Sei. U.S.A. (2000). 97: cc. 8263-8265.

45. Goedecke K., Pignot M., Goody R.S., Scheidig A.J., Weinhold E. Structure of the N6-adenine DNA methyltransferase Mbull.TaqI in complex with DNA and a cofactor analog. Nat Struct Mol Biol. (2001). 8: cc. 121-125.

46. Newby Z.E.R., Lau E.Y., Bruice T.C. A theoretical examination of the factors controlling the catalytic efficiency of the DNA-(adenine-N6)-methyltransferase from Thermus aquaticus. Proc. Natl. Acad. Sei. U.S.A. (2002). 99: cc. 7922-7927.

47. Hou Y., Perona J.J. Stereochemical mechanisms of tRNA methyltransferases. FEBS Lett. (2010). 584: cc. 278-286.

48. Heiser T.L., Davies J.E., Dahlberg J.E. Change in methylation of 16S ribosomal RNA associated with mutation to kasugamycin resistance in Escherichia coli. Nature New Biol. (1971). 233: cc. 12-14.

49. Schuwirth B.S., Day J.M., Hau C.W., Janssen G.R., Dahlberg A.E., Cate J.H.D., Vila-Sanjurjo A. Structural analysis of kasugamycin inhibition of translation. Nat. Struct. Mol. Biol. (2006). 13: cc. 879-886.

50. O'Farrell H.C., Scarsdale J.N., Rife J.P. Crystal structure of KsgA, a universally conserved rRNA adenine dimethyltransferase in Escherichia coli. J. Mol. Biol. (2004). 339: cc. 337353.

51. Kimura S., Suzuki T. Fine-tuning of the ribosomal decoding center by conserved methyl-modifications in the Escherichia coli 16S rRNA. Nucleic Acids Res. (2010). 38: cc. 13411352.

52. Czerwoniec A., Dunin-Horkawicz S., Purta E., Kaminska K.H., Kasprzak J.M., Bujnicki J.M., Grosjean H., Rother K. MODOMICS: a database of RNA modification pathways. 2008 update. Nucleic Acids Res. (2009). 37: cc. D118-121.

53. Ihsanawati, Nishimoto M., Higashijima K., Shirouzu M., Grosjean H., Bessho Y., Yokoyama S. Crystal Structure of tRNA N2,N2-Guanosine Dimethyltransferase Trml from Pyrococcus horikoshii. Journal of Molecular Biology. (2008). 383: cc. 871-884.

54. Purushothaman S.K., Bujnicki J.M., Grosjean H., Lapeyre B. Trmllp and Trmll2p Arc both Required for the Formation of 2-Methylguanosine at Position 10 in Yeast tRNA. Mol Cell Biol. (2005). 25: cc. 4359-4370.

55. Schubert H.L., Blumenthal R.M., Cheng X. Many paths to methyltransfer: a chronicle of convergence. Trends in Biochemical Sciences. (2003). 28: cc. 329-335.

56. Bujnicki J.M., Leach R.A., Debski J., Rychlewski L. Bioinformatic analyses of the tRNA: (guanine 26, N2,N2)-dimethyltransferase (Trml) family. J. Mol. Microbiol. Biotechnol. (2002). 4: cc. 405-415.

57. Tscherne J.S., Nurse K., Popienick P., Ofengand J. Purification, cloning, and characterization of the 16 S RNA m2G1207 methyltransferase from Escherichia coli. J. Biol. Chem. (1999). 274: cc. 924-929.

58. Sergiev P.V., Lesnyak D.V., Bogdanov A.A., Dontsova O.A. Identification of Escherichia coli m2G methyltransferases: II. The ygjO gene encodes a methyltransferase specific for Gl 835 of the 23 S rRNA. J. Mol. Biol. (2006). 364: cc. 26-31.

59. Lesnyak D.V., Sergiev P.V., Bogdanov A.A., Dontsova O.A. Identification of Escherichia coli m2G methyltransferases: I. the ycbY gene encodes a methyltransferase specific for G2445 of the 23 S rRNA. J. Mol. Biol. (2006). 364: cc. 20-25.

60. Ogle J.M., Brodersen D.E., Clemons W.M., Tarry M.J., Carter A.P., Ramakrishnan V. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science. (2001). 292: cc. 897-902.

61. Kubarenko A., Sergiev P., Wintermeyer W., Dontsova O., Rodnina M.V. Involvement of Helix 34 of 16 S rRNA in Decoding and Translocation on the Ribosome. Journal of Biological Chemistry. (2006). 281: cc. 35235 -35244.

62. Agafonov D.E., Kolb V.A., Spirin A.S. Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep. (2001). 2: cc. 399-402.

63. Sunita S., Purta E., Durawa M., Tkaczuk K.L., Swaathi J., Bujnicki J.M., Sivaraman J. Functional specialization of domains tandemly duplicated within 16S rRNA methyltransferase RsmC. Nucleic Acids Res. (2007). 35: cc. 4264-4274.

64. Demirci H., Gregory S.T., Dahlberg A.E., Jogi G. Crystal Structure of the Thermus thermophilus 16 S rRNA Methyltransferase RsmC in Complex with Cofactor and Substrate Guanosine. J Biol Chem. (2008). 283: cc. 26548-26556.

65. Huang L., Hung L., Odell M., Yokota H., Kim R., Kim S. Structure-based experimental confirmation of biochemical function to a methyltransferase, MJ0882, from hyperthermophile Methanococcus jannaschii. J. Struct. Funct. Genomics. (2002). 2: cc. 121-127.

66. Gustafsson C., Persson B.C. Identification of the rrmA gene encoding the 23S rRNA mlG745 methyltransferase in Escherichia coli and characterization of an mlG745-deficient mutant. J. Bacteriol. (1998). 180: cc. 359-365.

67. Maidak B.L., Olsen G.J., Larsen N., Overbeek R., McCaughey M.J., Woese C.R. The Ribosomal Database Project (RDP). Nucleic Acids Res. (1996). 24: cc. 82-85.

68. Takeda H., Toyooka T., Ikeuchi Y., Yokobori S., Okadome K., Takano F., Oshima T., Suzuki T., Endo Y., Hori H. The substrate specificity of tRNA (mlG37) methyltransferase (TrmD) from Aquifex aeolicus. Genes Cells. (2006). 11: cc. 1353-1365.

69. Lee C., Kramer G., Graham D.E., Appling D.R. Yeast mitochondrial initiator tRNA is methylated at guanosine 37 by the Trm5-encoded tRNA (guanine-Nl-)-methyltransferase. J. Biol. Chem. (2007). 282: cc. 27744-27753.

70. Christian T., Hou Y. Distinct determinants of tRNA recognition by the TrmD and Trm5 methyltransferases. J. Mol. Biol. (2007). 373: cc. 623-632.

71. Goto-Ito S., Ito T., Kuratani M., Bessho Y., Yokoyama S. Tertiary structure checkpoint at anticodon loop modification in tRNA functional maturation. Nat. Struct. Mol. Biol. (2009). 16:cc. 1109-1115.

72. Tkaczuk K.L., Dunin-Horkawicz S., Purta E., Bujnicki J.M. Structural and evolutionary bio informatics of the SPOUT superfamily of methyltransferases. BMC Bio informatics. 8: cc. 73-73.

73. Lovgren J.M., Wikstrom P.M. The rlmB gene is essential for formation of Gm2251 in 23 S rRNA but not for ribosome maturation in Escherichia coli. J. Bacteriol. (2001). 183: cc. 6957-6960.

74. Purta E., Kaminska K.H., Kasprzak J.M., Bujnicki J.M., Douthwaite S. YbeA is the m3Psi methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA. RNA. (2008). 14: cc. 2234-2244.

75. Basturea G.N., Rudd K.E., Deutscher M.P. Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA. (2006). 12: cc. 426434.

76. Watanabe K., Nureki O., Fukai S., Ishii R., Okamoto H., Yokoyama S., Endo Y., Hori H. Roles of Conserved Amino Acid Sequence Motifs in the SpoU (TrmH) RNA Methyltransferase Family. Journal ofBiological Chemistry. (2005). 280: cc. 10368 -10377.

77. Elkins P.A., Watts J.M., Zalacain M., van Thiel A., Yitazka P.R., Redlak M., Andraos-Selim C., Rastinejad F., Holmes W.M. Insights into catalysis by a knotted TrmD tRNA methyltransferase. J. Mol. Biol. (2003). 333: cc. 931-949.

78. Mallam A.L., Jackson S.E. A comparison of the folding of two knotted proteins: YbeA and YibK. J. Mol. Biol. (2007). 366: cc. 650-665.

79. Moss M., Frey P.A. The role of S-adenosylmethionine in the lysine 2,3-aminomutase reaction. J. Biol. Chem. (1987). 262: cc. 14859-14862.

80. Baraniak J., Moss M.L., Frey P.A. Lysine 2,3-aminomutase. Support for a mechanism of hydrogen transfer involving S-adenosylmethionine. J. Biol. Chem. (1989). 264: cc. 13571360.

81. Ballinger M.D., Frey P.A., Reed G.H. Structure of a substrate radical intermediate in the reaction of lysine 2,3-aminomutase. Biochemistry. (1992). 31: cc. 10782-10789.

82. Ballinger M.D., Reed G.H., Frey P.A. An organic radical in the lysine 2,3-aminomutase reaction. Biochemistry. (1992). 31: cc. 949-953.

83. Eliasson R., Fontecave M., Jörnvall H., Krook M., Pontis E., Reichard P. The anaerobic ribonucleoside triphosphate reductase from Escherichia coli requires S-adenosylmethionine as a cofactor. Proc. Natl. Acad. Sei. Ü.S.A. (1990). 87: cc. 3314-3318.

84. Eliasson R., Pontis E., Fontecave M., Gerez C., Harder J., Jornvall H., Krook M., Reichard P. Characterization of components of the anaerobic ribonucleotide reductase system from Escherichia coli. J. Biol. Chem. (1992). 267: cc. 25541-25547.

85. King D.S., Reichard P. Mass spectrometric determination of the radical scission site in the anaerobic ribonucleotide reductase of Escherichia coli. Biochem. Biophys. Res. Commun. (1995). 206: cc. 731-735.

86. Ugulava N.B., Gibney B.R., Jarrett J.T. Biotin synthase contains two distinct iron-sulfur cluster binding sites: chemical and spectroelectrochemical analysis of iron-sulfur cluster interconversions. Biochemistry. (2001). 40: cc. 8343-8351.

87. Ugulava N.B., Sacanell C.J., Jarrett J.T. Spectroscopic changes during a single turnover of biotin synthase: destruction of a 2Fe-2S. cluster accompanies sulfur insertion. Biochemistry. (2001). 40: cc. 8352-8358.

88. Tse Sum Bui B., Benda R., Schiinemann V., Florentin D., Trautwein A.X., Marquet A. Fate of the (2Fe-2S)(2+) cluster of Escherichia coli biotin synthase during reaction: a Mossbauer characterization. Biochemistry. (2003). 42: cc. 8791-8798.

89. Cicchillo R.M., Lee K., Baleanu-Gogonea C., Nesbitt N.M., Krebs C„ Booker S.J. Escherichia coli lipoyl synthase binds two distinct 4Fe-4S. clusters per polypeptide. Biochemistry. (2004). 43: cc. 11770-11781.

90. Tse Sum Bui B., Lotierzo M., Escalettes F., Florentin D., Marquet A. Further investigation on the turnover of Escherichia coli biotin synthase with dethiobiotin and 9-mercaptodethiobiotin as substrates. Biochemistry. (2004). 43: cc. 16432-16441.

91. Layer G., Moser J., Heinz D.W., Jahn D., Schubert W. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of Radical SAM enzymes. EMBO J. (2003). 22: cc. 6214-6224.

92. Layer G., Kervio E., Morlock G., Heinz D.W., Jahn D., Retey J., Schubert W. Structural and functional comparison of HemN to other radical SAM enzymes. Biol. Chem. (2005). 386: cc. 971-980.

93. Pierrel F., Douki T., Fontecave M., Atta M. MiaB protein is a bifunctional radical-S-adenosylmethionine enzyme involved in thiolation and methylation of tRNA. J. Biol. Chem. (2004). 279: cc. 47555-47563.

94. Chatterjee A., Li Y„ Zhang Y., Grove T.L., Lee M., Krebs C., Booker S.J., Begley T.P., Ealick S.E. Reconstitution of ThiC in thiamine pyrimidine biosynthesis expands the radical SAM superfamily. Nat. Chem. Biol. (2008). 4: cc. 758-765.

95. Frey P.A., Magnusson O.T. S-Adenosylmethionine: a wolf in sheep's clothing, or a rich man's adenosylcobalamin? Chem. Rev. (2003). 103: cc. 2129-2148.

96. Frey P.A., Hegeman A.D., Ruzicka F.J. The Radical SAM Superfamily. Crit. Rev. Biochem. Mol. Biol. (2008). 43: cc. 63-88.

97. Booker S.J. Anaerobic functionalization of unactivated C-H bonds. Curr Opin Chem Biol. (2009). 13: cc. 58-73.

98. Toh S., Xiong L., Bae T., Mankin A.S. The methyltransferase YfgB/RlmN is responsible for modification of adenosine 2503 in 23S rRNA. RNA. (2008). 14: cc. 98-106.

99. Yan F., LaMarre J.M., Röhrich R., Wiesner J., Jomaa H., Mankin A.S., Fujimori D.G. RlmN and Cfr are radical SAM enzymes involved in methylation of ribosomal RNA. J. Am. Chem. Soc. (2010). 132: cc. 3953-3964.

100. Xiang Z. Advances in Homology Protein Structure Modeling. Curr Protein Pept Sei. (2006). 7: cc. 217-227.

101. Mallam A.L., Jackson S.E. Folding studies on a knotted protein. J. Mol. Biol. (2005). 346: cc. 1409-1421.

102. Mallam A.L., Jackson S.E. Probing nature's knots: the folding pathway of a knotted homodimeric protein. J. Mol. Biol. (2006). 359: cc. 1420-1436.

103. Gloss L.M. Tying the knot that binds. Structure. (2007). 15: cc. 2-4.

104. Mallam A.L., Jackson S.E. The dimerization of an alpha/beta-knotted protein is essential for structure and function. Structure. (2007). 15: cc. 111-122.

105. Wallin S., Zeldovich K.B., Shakhnovich E.I. The folding mechanics of a knotted protein. J. Mol. Biol. (2007). 368: cc. 884-893.

106. Mallam A.L., Morris E.R., Jackson S.E. Exploring knotting mechanisms in protein folding. Proc. Natl. Acad. Sei. U.S.A. (2008). 105: cc. 18740-18745.

107. Sulkowska J.I., Sulkowski P., Onuchic J. Dodging the crisis of folding proteins with knots. Proc. Natl. Acad. Sei. U.S.A. (2009). 106: cc. 3119-3124.

108. Tuszynska I., Bujnicki J.M. Predicting atomic details of the unfolding pathway for YibK, a knotted protein from the SPOUT superfamily. J. Biomol. Struct. Dyn. (2010). 27: cc. 511520.

109. Jeltsch A. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem. (2002). 3: cc. 274-293.

110. Weber A., Kögl S.A., Jung K. Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. (2006). 188: cc. 71657175.

111. Blankenborn D., Phillips J., Slonczewski J.L. Acid- and Base-Induced Proteins during Aerobic and Anaerobic Growth of Escherichia coli Revealed by Two-Dimensional Gel Electrophoresis. J Bacteriol. (1999). 181: cc. 2209-2216.

112. Kannan G., Wilks J.C., Fitzgerald D.M., Jones B.D., BonDurant S.S., Slonczewski J.L. Rapid acid treatment of Escherichia coli: transcriptomic response and recovery. BMC Microbiol. 8: cc. 37-37.

113. Almeida C.C., Romao C.V., Lindley P.F., Teixeira M., Saraiva L.M. The role of the hybrid cluster protein in oxidative stress defense. J. Biol. Chem. (2006). 281: cc. 32445-32450.

114. Samaha R.R., Green R., Noller H.F. A base pair between tRNA and 23S rRNA in the peptidyl transferase centre of the ribosome. Nature. (1995). 377: cc. 309-314.

115. Green R., Noller H.F. In vitro complementation analysis localizes 23S rRNA posttranscriptional modifications that are required for Escherichia coli 50S ribosomal subunit assembly and function. RNA. (1996). 2: cc. 1011 -1021.

116. Green R., Noller H.F. Reconstitution of functional 50S ribosomes from in vitro transcripts of Bacillus stearothermophilus 23S rRNA. Biochemistry. (1999). 38: cc. 1772-1779.

117. Khaitovich P., Tenson T., Kloss P., Mankin A.S. Reconstitution of functionally active Thermus aquaticus large ribosomal subunits with in vitro-transcribed rRNA. Biochemistry. (1999). 38: cc. 1780-1788.

118. Leonov A.A., Sergiev P.V., Bogdanov A.A., Brimacombe R., Dontsova O.A. Affinity purification of ribosomes with a lethal G2655C mutation in 23 S rRNA that affects the translocation. J. Biol. Chem. (2003). 278: cc. 25664-25670.

119. Youngman E.M., Green R. Affinity purification of in vivo-assembled ribosomes for in vitro biochemical analysis. Methods. (2005). 36: cc. 305-312.

120. Youngman E.M., Brunelle J.L., Kochaniak A.B., Green R. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell. (2004). 117: cc. 589-599.

121. Cochella L., Brunelle J.L., Green R. Mutational analysis reveals two independent molecular requirements during transfer RNA selection on the ribosome. Nat. Struct. Mol. Biol. (2007). 14: cc. 30-36.

122. Bachler M., Schroeder R., von Ahsen U. StreptoTag: a novel method for the isolation of RNA-binding proteins. RNA. (1999). 5: cc. 1509-1516.

123. Afonina E., Chichkova N., Bogdanova S., Bogdanov A. 30S ribosomal subunits with fragmented 16S RNA: a new approach for structure and function study of ribosomes. Biochimie. (1991). 73: cc. 777-787.

124. Miyauchi K., Ohara T., Suzuki T. Automated parallel isolation of multiple species of non-coding RNAs by the reciprocal circulating chromatography method. Nucleic Acids Res. (2007). 35: cc. e24.

125. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained Polyacrylamide gels. Anal. Chem. (1996). 68: cc. 850-858.

126. Kunkel T.A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sei. U.S.A. (1985). 82: cc. 488-492.

127. Douthwaite S., Powers T., Lee J.Y., Noller H.F. Defining the structural requirements for a helix in 23 S ribosomal RNA that confers erythromycin resistance. J. Mol. Biol. (1989). 209:cc. 655-665.

128. Ellwood M., Nomura M. Chromosomal locations of the genes for rRNA in Escherichia coli K-12. J. Bacteriol. (1982). 149: cc. 458-468.

129. Shimizu Y., Inoue A., Tomari Y., Suzuki T., Yokogawa T., Nishikawa K., Ueda T. Cellfree translation reconstituted with purified components. Nat. Biotechno1. (2001). 19: cc. 751-755.

130. NIRENBERG M., LEDER P. RNA CODEWORDS AND PROTEIN SYNTHESIS. THE EFFECT OF TRINUCLEOTIDES UPON THE BINDING OF SRNA TO RIBOSOMES. Science. (1964). 145: cc. 1399-1407.