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RNA-binding Sm-like proteins of bacteria and archaea. Similarity and difference in structure and function

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Abstract

RNA-binding proteins play a significant role in many processes of RNA metabolism, such as splicing and processing, regulation of DNA transcription and RNA translation, etc. Among the great number of RNA-binding proteins, so-called RNA-chaperones occupy an individual niche; they were named for their ability to assist RNA molecules to gain their accurate native spatial structure. When binding with RNAs, they possess the capability of altering (melting) their secondary structure, thus providing a possibility for formation of necessary intramolecular contacts between individual RNA sites for proper folding. These proteins also have an additional helper function in RNA-RNA and RNA-protein interactions. Members of such class of the RNA-binding protein family are Sm and Sm-like proteins (Sm-Like, LSm). The presence of these proteins in bacteria, archaea, and eukaryotes emphasizes their biological significance. These proteins are now attractive for researchers because of their implication in many processes associated with RNAs in bacterial and archaeal cells. This review is focused on a comparison of architecture of bacterial and archaeal LSm proteins and their interaction with different RNA molecules.

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Abbreviations

H-NS:

histone-like heat-stable nucleoid-structuring protein

K d :

apparent dissociation constant

LSm:

Smlike protein

snRNA:

small nuclear RNA

sRNA:

small regulatory RNA

REFERENCES

  1. Rajkowitsch, L., Chen, D., Stampfl, S., Semrad, K., Waldsich, C., and Mayer, O. (2007) RNA Biol., 4, 118–130.

    PubMed  CAS  Google Scholar 

  2. Wilusz, C. J., and Wilusz, J. (2005) Nat. Struct. Mol. Biol., 12, 1031–1036.

    PubMed  CAS  Google Scholar 

  3. Tharun, S. (2009) Int. Rev. Cell Mol. Biol., 272, 149–189.

    PubMed  CAS  Google Scholar 

  4. Fischer, S., Benz, J., Spath, B., Maier, L., Straub, J., and Granzow, M. (2010) J. Biol. Chem., 285, 34429–34438.

    PubMed  CAS  Google Scholar 

  5. Chao, Y., and Vogel, J. (2010) Curr. Opin. Microbiol., 13, 24–33.

    PubMed  CAS  Google Scholar 

  6. Valentin-Hansen, P., Eriksen, M., and Udesen, C. (2004) Mol. Microbiol., 51, 1525–1533.

    PubMed  CAS  Google Scholar 

  7. Notman, D. D., Kurata, N., and Tan, E. M. (1975) Ann. Int. Med., 83, 464–469.

    PubMed  CAS  Google Scholar 

  8. Lerner, M. R., and Steitz, J. A. (1979) Proc. Natl. Acad. Sci. USA, 76, 5495–5499.

    PubMed  CAS  Google Scholar 

  9. Luhrmann, R., Kastner, B., and Bach, M. (1990) Biochim. Biophys. Acta, 1087, 265–292.

    PubMed  CAS  Google Scholar 

  10. Hermann, H., Fabrizio, P., Raker, V. A., Foulaki, K., Hornig, H., and Brahms, H. (1995) EMBO J., 14, 2076–2088.

    PubMed  CAS  Google Scholar 

  11. He, W., and Parker, R. (2000) Curr. Opin. Cell Biol., 12, 346–350.

    PubMed  CAS  Google Scholar 

  12. Yong, J., Golembe, T. J., Battle, D. J., Pellizzoni, L., and Dreyfuss, G. (2004) Mol. Cell. Biol., 24, 2747–2756.

    PubMed  CAS  Google Scholar 

  13. Pomeranz Krummel, D. A., Oubridge, C., Leung, A. K. W., Li, J., and Nagai, K. (2009) Nature, 458, 475–480.

    PubMed  CAS  Google Scholar 

  14. Shapiro, L., Franze de Fernandez, M. T., and August, J. T. (1968) Nature, 220, 478–480.

    PubMed  CAS  Google Scholar 

  15. Franze de Fernandez, M. T., Eoyang, L., and August, J. T. (1968) Nature, 219, 588–590.

    PubMed  CAS  Google Scholar 

  16. Franze de Fernandez, M. T., Hayward, W. S., and August, J. T. (1972) J. Biol. Chem., 247, 824–831.

    PubMed  CAS  Google Scholar 

  17. Kajitani, M., and Ishihama, A. (1991) Nucleic Acids Res., 19, 1063–1066.

    PubMed  CAS  Google Scholar 

  18. Schuppli, D., Miranda, G., Tsui, H. C., Winkler, M. E., Sogo, J. M., and Weber, H. (1997) Proc. Natl. Acad. Sci. USA, 94, 10239–10242.

    PubMed  CAS  Google Scholar 

  19. Tsui, H. C., Feng, G., and Winkler, M. E. (1997) J. Bacteriol., 179, 7476–7487.

    PubMed  CAS  Google Scholar 

  20. Zhang, A., Wassarman, K. M., Ortega, J., Steven, A. C., and Storz, G. (2002) Mol. Cell, 9, 11–22.

    PubMed  Google Scholar 

  21. Moller, T., Franch, T., Hojrup, P., Keene, D. R., Bachinger, H. P., and Brennan, R. G. (2002) Mol. Cell, 9, 23–30.

    PubMed  CAS  Google Scholar 

  22. Sun, X., Zhulin, I., and Wartell, R. M. (2002) Nucleic Acids Res., 30, 3662–3671.

    PubMed  CAS  Google Scholar 

  23. Schumacher, M. A., Pearson, R. F., Moller, T., Valentin-Hansen, P., and Brennan, R. G. (2002) EMBO J., 21, 3546–3556.

    PubMed  CAS  Google Scholar 

  24. Sauter, C., Basquin, J., and Suck, D. (2003) Nucleic Acids Res., 31, 4091–4098.

    PubMed  CAS  Google Scholar 

  25. Moskaleva, O., Melnik, B., Gabdulkhakov, A., Garber, M., Nikonov, S., and Stolboushkina, E. (2010) Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 66, 760–764.

    PubMed  Google Scholar 

  26. Nikulin, A., Stolboushkina, E., Perederina, A., Vassilieva, I., Blaesi, U., and Moll, I. (2005) Acta Crystallogr. D Biol. Crystallogr., 61, 141–146.

    PubMed  Google Scholar 

  27. Boggild, A., Overgaard, M., Valentin-Hansen, P., and Brodersen, D. E. (2009) FEBS J., 276, 3904–3915.

    PubMed  Google Scholar 

  28. Dienst, D., Duhring, U., Mollenkopf, H., Vogel, J., Golecki, J., and Hess, W. R. (2008) Microbiology, 154, 3134–3143.

    PubMed  CAS  Google Scholar 

  29. Seraphin, B. (1995) EMBO J., 14, 2089–2098.

    PubMed  CAS  Google Scholar 

  30. Murzin, A. G. (1993) EMBO J., 12, 861–867.

    PubMed  CAS  Google Scholar 

  31. Musacchio, A., Gibson, T., Lehto, V. P., and Saraste, M. (1992) FEBS Lett., 307, 55–61.

    PubMed  CAS  Google Scholar 

  32. Brennan, R. G., and Link, T. M. (2007) Curr. Opin. Microbiol., 10, 125–133.

    PubMed  CAS  Google Scholar 

  33. Tsui, H. C., Leung, H. C., and Winkler, M. E. (1994) Mol. Microbiol., 13, 35–49.

    PubMed  CAS  Google Scholar 

  34. Sonnleitner, E., Moll, I., and Blasi, U. (2002) Microbiology, 148, 883–891.

    PubMed  CAS  Google Scholar 

  35. Arluison, V., Folichon, M., Marco, S., Derreumaux, P., Pellegrini, O., and Seguin, J. (2004) Eur. J. Biochem., 271, 1258–1265.

    PubMed  CAS  Google Scholar 

  36. Sittka, A., Sharma, C. M., Rolle, K., and Vogel, J. (2009) RNA Biol., 6, 266–275.

    PubMed  CAS  Google Scholar 

  37. Nielsen, J. S., Lei, L. K., Ebersbach, T., Olsen, A. S., Klitgaard, J. K., and Valentin-Hansen, P. (2010) Nucleic Acids Res., 38, 907–919.

    PubMed  CAS  Google Scholar 

  38. Nielsen, J. S., Boggild, A., Andersen, C. B. F., Nielsen, G., Boysen, A., and Brodersen, D. E. (2007) RNA, 13, 2213–2223.

    PubMed  CAS  Google Scholar 

  39. Vecerek, B., Rajkowitsch, L., Sonnleitner, E., Schroeder, R., and Blasi, U. (2008) Nucleic Acids Res., 36, 133–143.

    PubMed  CAS  Google Scholar 

  40. Olsen, A. S., Moller-Jensen, J., Brennan, R. G., and Valentin-Hansen, P. (2010) J. Mol. Biol., 404, 173–182.

    PubMed  CAS  Google Scholar 

  41. Vassilieva, Yu. M., and Garber, M. B. (2002) Mol. Biol. (Moscow), 36, 785–791.

    CAS  Google Scholar 

  42. Soper, T., Mandin, P., Majdalani, N., Gottesman, S., and Woodson, S. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 9602–9607.

    PubMed  CAS  Google Scholar 

  43. Basineni, S. R., Madhugiri, R., Kolmsee, T., Hengge, R., and Klug, G. (2009) RNA Biol., 6, 584–594.

    PubMed  CAS  Google Scholar 

  44. Sledjeski, D. D., Whitman, C., and Zhang, A. (2001) J. Bacteriol., 183, 1997–2005.

    PubMed  CAS  Google Scholar 

  45. Nogueira, T., and Springer, M. (2000) Curr. Opin. Microbiol., 3, 154–158.

    PubMed  CAS  Google Scholar 

  46. Aiba, H. (2007) Curr. Opin. Microbiol., 10, 134–139.

    PubMed  CAS  Google Scholar 

  47. Gorke, B., and Vogel, J. (2008) Genes Dev., 22, 2914–2925.

    PubMed  Google Scholar 

  48. Urban, J. H., and Vogel, J. (2007) Nucleic Acids Res., 35, 1018–1037.

    PubMed  CAS  Google Scholar 

  49. Argaman, L., and Altuvia, S. (2000) J. Mol. Biol., 300, 1101–1112.

    PubMed  CAS  Google Scholar 

  50. Zhang, A., Altuvia, S., Tiwari, A., Argaman, L., Hengge-Aronis, R., and Storz, G. (1998) EMBO J., 17, 6061–6068.

    PubMed  CAS  Google Scholar 

  51. Altuvia, S., Zhang, A., Argaman, L., Tiwari, A., and Storz, G. (1998) EMBO J., 17, 6069–6075.

    PubMed  CAS  Google Scholar 

  52. Lease, R. A., and Belfort, M. (2000) Mol. Microbiol., 38, 667–672.

    PubMed  CAS  Google Scholar 

  53. Sledjeski, D. D., Gupta, A., and Gottesman, S. (1996) EMBO J., 15, 3993–4000.

    PubMed  CAS  Google Scholar 

  54. Vecerek, B., Beich-Frandsen, M., Resch, A., and Blasi, U. (2010) Nucleic Acids Res., 38, 1284–1293.

    PubMed  CAS  Google Scholar 

  55. Muffler, A., Fischer, D., and Hengge-Aronis, R. (1996) Genes Dev., 10, 1143–1151.

    PubMed  CAS  Google Scholar 

  56. Brown, L., and Elliott, T. (1996) J. Bacteriol., 178, 3763–3770.

    PubMed  CAS  Google Scholar 

  57. Dong, T., and Schellhorn, H. E. (2009) Mol. Genet. Genom., 281, 19–33.

    CAS  Google Scholar 

  58. Loewen, P. C., and Hengge-Aronis, R. (1994) Annu. Rev. Microbiol., 48, 53–80.

    PubMed  CAS  Google Scholar 

  59. Hengge-Aronis, R. (2000) Adv. Exp. Med. Biol., 485, 85–93.

    PubMed  CAS  Google Scholar 

  60. Hengge-Aronis, R. (1996) Mol. Microbiol., 21, 887–893.

    PubMed  CAS  Google Scholar 

  61. Hengge-Aronis, R., Lange, R., Henneberg, N., and Fischer, D. (1993) J. Bacteriol., 175, 259–265.

    PubMed  CAS  Google Scholar 

  62. Hengge-Aronis, R. (1993) Cell, 72, 165–168.

    PubMed  CAS  Google Scholar 

  63. Fang, F. C., Libby, S. J., Buchmeier, N. A., Loewen, P. C., Switala, J., and Harwood, J. (1992) Proc. Natl. Acad. Sci. USA, 89, 11978–11982.

    PubMed  CAS  Google Scholar 

  64. Webb, C., Moreno, M., Wilmes-Riesenberg, M., Curtiss, R. III., and Foster, J. W. (1999) Mol. Microbiol., 34, 112–123.

    PubMed  CAS  Google Scholar 

  65. Jorgensen, F., Bally, M., Chapon-Herve, V., Michel, G., Lazdunski, A., and Williams, P. (1999) Microbiology, 145, 835–844.

    PubMed  CAS  Google Scholar 

  66. Suh, S. J., Silo-Suh, L., Woods, D. E., Hassett, D. J., West, S. E., and Ohman, D. E. (1999) J. Bacteriol., 181, 3890–3897.

    PubMed  CAS  Google Scholar 

  67. Badger, J. L., and Miller, V. L. (1995) J. Bacteriol., 177, 5370–5373.

    PubMed  CAS  Google Scholar 

  68. Lange, R., and Hengge-Aronis, R. (1994) Genes Dev., 8, 1600–1612.

    PubMed  CAS  Google Scholar 

  69. Yamashino, T., Ueguchi, C., and Mizuno, T. (1995) EMBO J., 14, 594–602.

    PubMed  CAS  Google Scholar 

  70. Muffler, A., Traulsen, D. D., Fischer, D., Lange, R., and Hengge-Aronis, R. (1997) J. Bacteriol., 179, 297–300.

    PubMed  CAS  Google Scholar 

  71. Vecerek, B., Moll, I., and Blasi, U. (2005) RNA, 11, 976–984.

    PubMed  CAS  Google Scholar 

  72. Vytvytska, O., Jakobsen, J. S., Balcunaite, G., Andersen, J. S., Baccarini, M., and von Gabain, A. (1998) Proc. Natl. Acad. Sci. USA, 95, 14118–14123.

    PubMed  CAS  Google Scholar 

  73. Hajnsdorf, E., and Regnier, P. (2000) Proc. Natl. Acad. Sci. USA, 97, 1501–1505.

    PubMed  CAS  Google Scholar 

  74. Folichon, M., Arluison, V., Pellegrini, O., Huntzinger, E., Regnier, P., and Hajnsdorf, E. (2003) Nucleic Acids Res., 31, 7302–7310.

    PubMed  CAS  Google Scholar 

  75. Takada, A., Wachi, M., and Nagai, K. (1999) Biochem. Biophys. Res. Commun., 266, 579–583.

    PubMed  CAS  Google Scholar 

  76. Wachi, M., Takada, A., and Nagai, K. (1999) Biochem. Biophys. Res. Commun., 264, 525–529.

    PubMed  CAS  Google Scholar 

  77. Vytvytska, O., Moll, I., Kaberdin, V. R., von Gabain, A., and Blasi, U. (2000) Genes Dev., 14, 1109–1118.

    PubMed  CAS  Google Scholar 

  78. Udekwu, K. I., Darfeuille, F., Vogel, J., Reimegard, J., Holmqvist, E., and Wagner, E. G. H. (2005) Genes Dev., 19, 2355–2366.

    PubMed  CAS  Google Scholar 

  79. De Haseth, P. L., and Uhlenbeck, O. C. (1980) Biochemistry, 19, 6146–6151.

    PubMed  Google Scholar 

  80. Mikulecky, P. J., Kaw, M. K., Brescia, C. C., Takach, J. C., Sledjeski, D. D., and Feig, A. L. (2004) Nat. Struct. Mol. Biol., 11, 1206–1214.

    PubMed  CAS  Google Scholar 

  81. Sun, X., and Wartell, R. M. (2006) Biochemistry, 45, 4875–4887.

    PubMed  CAS  Google Scholar 

  82. Link, T. M., Valentin-Hansen, P., and Brennan, R. G. (2009) Proc. Natl. Acad. Sci. USA, 106, 19292–19297.

    PubMed  CAS  Google Scholar 

  83. Lease, R. A., and Woodson, S. A. (2004) J. Mol. Biol., 344, 1211–1223.

    PubMed  CAS  Google Scholar 

  84. Updegrove, T. B., Correia, J. J., Chen, Y., Terry, C., and Wartell, R. M. (2011) RNA, 17, 489–500.

    PubMed  CAS  Google Scholar 

  85. Azam, T. A., and Ishihama, A. (1999) J. Biol. Chem., 274, 33105–33113.

    PubMed  CAS  Google Scholar 

  86. Ishihama, A. (1999) Genes Cells, 4, 135–143.

    PubMed  CAS  Google Scholar 

  87. Takada, A., Wachi, M., Kaidow, A., Takamura. M., and Nagai, K. (1997) Biochem. Biophys. Res. Commun., 236, 576–579.

    PubMed  CAS  Google Scholar 

  88. Updegrove, T. B., Correia, J. J., Galletto, R., Bujalowski, W., and Wartell, R. M. (2010) Biochim. Biophys. Acta, 1799, 588–596.

    PubMed  CAS  Google Scholar 

  89. Vlahovicek, K., Kajan, L., and Pongor, S. (2003) Nucleic Acids Res., 31, 3686–3687.

    PubMed  CAS  Google Scholar 

  90. Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S., and Seraphin, B. (1999) EMBO J., 18, 3451–3462.

    PubMed  CAS  Google Scholar 

  91. Toro, I., Thore, S., Mayer, C., Basquin, J., Seraphin, B., and Suck, D. (2001) EMBO J., 20, 2293–2303.

    PubMed  CAS  Google Scholar 

  92. Achsel, T., Stark, H., and Luhrmann, R. (2001) Proc. Natl. Acad. Sci. USA, 98, 3685–3689.

    PubMed  CAS  Google Scholar 

  93. Collins, B. M., Harrop, S. J., Kornfeld, G. D., Dawes, I. W., Curmi, P. M., and Mabbutt, B. C. (2001) J. Mol. Biol., 309, 915–923.

    PubMed  CAS  Google Scholar 

  94. Mura, C., Cascio, D., Sawaya, M. R., and Eisenberg, D. S. (2001) Proc. Natl. Acad. Sci. USA, 98, 5532–5537.

    PubMed  CAS  Google Scholar 

  95. Toro, I., Basquin, J., Teo-Dreher, H., and Suck, D. (2002) J. Mol. Biol., 320, 129–142.

    PubMed  Google Scholar 

  96. Kilic, T., Sanglier, S., van Dorsselaer, A., and Suck, D. (2006) Protein Sci., 15, 2310–2317.

    PubMed  CAS  Google Scholar 

  97. Mura, C., Kozhukhovsky, A., Gingery, M., Phillips, M., and Eisenberg, D. (2003) Protein Sci., 12, 832–847.

    PubMed  CAS  Google Scholar 

  98. Mura, C., Phillips, M., Kozhukhovsky, A., and Eisenberg, D. (2003) Proc. Natl. Acad. Sci. USA, 100, 4539–4544.

    PubMed  CAS  Google Scholar 

  99. Soppa, J., Straub, J., Brenneis, M., Jellen-Ritter, A., Heyer, R., and Fischer, S. (2009) Biochem. Soc. Trans., 37, 133–136.

    PubMed  CAS  Google Scholar 

  100. Straub, J., Brenneis, M., Jellen-Ritter, A., Heyer, R., Soppa, J., and Marchfelder, A. (2009) RNA Biol., 6, 281–292.

    PubMed  CAS  Google Scholar 

  101. Arluison, V., Mura, C., Guzman, M. R., Liquier, J., Pellegrini, O., and Gingery, M. (2006) J. Mol. Biol., 356, 86–96.

    PubMed  CAS  Google Scholar 

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Original Russian Text © V. N. Murina, A. D. Nikulin, 2011, published in Uspekhi Biologicheskoi Khimii, 2011, Vol. 51, pp. 133–164.

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Murina, V.N., Nikulin, A.D. RNA-binding Sm-like proteins of bacteria and archaea. Similarity and difference in structure and function. Biochemistry Moscow 76, 1434–1449 (2011). https://doi.org/10.1134/S0006297911130050

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