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.
Similar content being viewed by others
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
Rajkowitsch, L., Chen, D., Stampfl, S., Semrad, K., Waldsich, C., and Mayer, O. (2007) RNA Biol., 4, 118–130.
Wilusz, C. J., and Wilusz, J. (2005) Nat. Struct. Mol. Biol., 12, 1031–1036.
Tharun, S. (2009) Int. Rev. Cell Mol. Biol., 272, 149–189.
Fischer, S., Benz, J., Spath, B., Maier, L., Straub, J., and Granzow, M. (2010) J. Biol. Chem., 285, 34429–34438.
Chao, Y., and Vogel, J. (2010) Curr. Opin. Microbiol., 13, 24–33.
Valentin-Hansen, P., Eriksen, M., and Udesen, C. (2004) Mol. Microbiol., 51, 1525–1533.
Notman, D. D., Kurata, N., and Tan, E. M. (1975) Ann. Int. Med., 83, 464–469.
Lerner, M. R., and Steitz, J. A. (1979) Proc. Natl. Acad. Sci. USA, 76, 5495–5499.
Luhrmann, R., Kastner, B., and Bach, M. (1990) Biochim. Biophys. Acta, 1087, 265–292.
Hermann, H., Fabrizio, P., Raker, V. A., Foulaki, K., Hornig, H., and Brahms, H. (1995) EMBO J., 14, 2076–2088.
He, W., and Parker, R. (2000) Curr. Opin. Cell Biol., 12, 346–350.
Yong, J., Golembe, T. J., Battle, D. J., Pellizzoni, L., and Dreyfuss, G. (2004) Mol. Cell. Biol., 24, 2747–2756.
Pomeranz Krummel, D. A., Oubridge, C., Leung, A. K. W., Li, J., and Nagai, K. (2009) Nature, 458, 475–480.
Shapiro, L., Franze de Fernandez, M. T., and August, J. T. (1968) Nature, 220, 478–480.
Franze de Fernandez, M. T., Eoyang, L., and August, J. T. (1968) Nature, 219, 588–590.
Franze de Fernandez, M. T., Hayward, W. S., and August, J. T. (1972) J. Biol. Chem., 247, 824–831.
Kajitani, M., and Ishihama, A. (1991) Nucleic Acids Res., 19, 1063–1066.
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.
Tsui, H. C., Feng, G., and Winkler, M. E. (1997) J. Bacteriol., 179, 7476–7487.
Zhang, A., Wassarman, K. M., Ortega, J., Steven, A. C., and Storz, G. (2002) Mol. Cell, 9, 11–22.
Moller, T., Franch, T., Hojrup, P., Keene, D. R., Bachinger, H. P., and Brennan, R. G. (2002) Mol. Cell, 9, 23–30.
Sun, X., Zhulin, I., and Wartell, R. M. (2002) Nucleic Acids Res., 30, 3662–3671.
Schumacher, M. A., Pearson, R. F., Moller, T., Valentin-Hansen, P., and Brennan, R. G. (2002) EMBO J., 21, 3546–3556.
Sauter, C., Basquin, J., and Suck, D. (2003) Nucleic Acids Res., 31, 4091–4098.
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.
Nikulin, A., Stolboushkina, E., Perederina, A., Vassilieva, I., Blaesi, U., and Moll, I. (2005) Acta Crystallogr. D Biol. Crystallogr., 61, 141–146.
Boggild, A., Overgaard, M., Valentin-Hansen, P., and Brodersen, D. E. (2009) FEBS J., 276, 3904–3915.
Dienst, D., Duhring, U., Mollenkopf, H., Vogel, J., Golecki, J., and Hess, W. R. (2008) Microbiology, 154, 3134–3143.
Seraphin, B. (1995) EMBO J., 14, 2089–2098.
Murzin, A. G. (1993) EMBO J., 12, 861–867.
Musacchio, A., Gibson, T., Lehto, V. P., and Saraste, M. (1992) FEBS Lett., 307, 55–61.
Brennan, R. G., and Link, T. M. (2007) Curr. Opin. Microbiol., 10, 125–133.
Tsui, H. C., Leung, H. C., and Winkler, M. E. (1994) Mol. Microbiol., 13, 35–49.
Sonnleitner, E., Moll, I., and Blasi, U. (2002) Microbiology, 148, 883–891.
Arluison, V., Folichon, M., Marco, S., Derreumaux, P., Pellegrini, O., and Seguin, J. (2004) Eur. J. Biochem., 271, 1258–1265.
Sittka, A., Sharma, C. M., Rolle, K., and Vogel, J. (2009) RNA Biol., 6, 266–275.
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.
Nielsen, J. S., Boggild, A., Andersen, C. B. F., Nielsen, G., Boysen, A., and Brodersen, D. E. (2007) RNA, 13, 2213–2223.
Vecerek, B., Rajkowitsch, L., Sonnleitner, E., Schroeder, R., and Blasi, U. (2008) Nucleic Acids Res., 36, 133–143.
Olsen, A. S., Moller-Jensen, J., Brennan, R. G., and Valentin-Hansen, P. (2010) J. Mol. Biol., 404, 173–182.
Vassilieva, Yu. M., and Garber, M. B. (2002) Mol. Biol. (Moscow), 36, 785–791.
Soper, T., Mandin, P., Majdalani, N., Gottesman, S., and Woodson, S. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 9602–9607.
Basineni, S. R., Madhugiri, R., Kolmsee, T., Hengge, R., and Klug, G. (2009) RNA Biol., 6, 584–594.
Sledjeski, D. D., Whitman, C., and Zhang, A. (2001) J. Bacteriol., 183, 1997–2005.
Nogueira, T., and Springer, M. (2000) Curr. Opin. Microbiol., 3, 154–158.
Aiba, H. (2007) Curr. Opin. Microbiol., 10, 134–139.
Gorke, B., and Vogel, J. (2008) Genes Dev., 22, 2914–2925.
Urban, J. H., and Vogel, J. (2007) Nucleic Acids Res., 35, 1018–1037.
Argaman, L., and Altuvia, S. (2000) J. Mol. Biol., 300, 1101–1112.
Zhang, A., Altuvia, S., Tiwari, A., Argaman, L., Hengge-Aronis, R., and Storz, G. (1998) EMBO J., 17, 6061–6068.
Altuvia, S., Zhang, A., Argaman, L., Tiwari, A., and Storz, G. (1998) EMBO J., 17, 6069–6075.
Lease, R. A., and Belfort, M. (2000) Mol. Microbiol., 38, 667–672.
Sledjeski, D. D., Gupta, A., and Gottesman, S. (1996) EMBO J., 15, 3993–4000.
Vecerek, B., Beich-Frandsen, M., Resch, A., and Blasi, U. (2010) Nucleic Acids Res., 38, 1284–1293.
Muffler, A., Fischer, D., and Hengge-Aronis, R. (1996) Genes Dev., 10, 1143–1151.
Brown, L., and Elliott, T. (1996) J. Bacteriol., 178, 3763–3770.
Dong, T., and Schellhorn, H. E. (2009) Mol. Genet. Genom., 281, 19–33.
Loewen, P. C., and Hengge-Aronis, R. (1994) Annu. Rev. Microbiol., 48, 53–80.
Hengge-Aronis, R. (2000) Adv. Exp. Med. Biol., 485, 85–93.
Hengge-Aronis, R. (1996) Mol. Microbiol., 21, 887–893.
Hengge-Aronis, R., Lange, R., Henneberg, N., and Fischer, D. (1993) J. Bacteriol., 175, 259–265.
Hengge-Aronis, R. (1993) Cell, 72, 165–168.
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.
Webb, C., Moreno, M., Wilmes-Riesenberg, M., Curtiss, R. III., and Foster, J. W. (1999) Mol. Microbiol., 34, 112–123.
Jorgensen, F., Bally, M., Chapon-Herve, V., Michel, G., Lazdunski, A., and Williams, P. (1999) Microbiology, 145, 835–844.
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.
Badger, J. L., and Miller, V. L. (1995) J. Bacteriol., 177, 5370–5373.
Lange, R., and Hengge-Aronis, R. (1994) Genes Dev., 8, 1600–1612.
Yamashino, T., Ueguchi, C., and Mizuno, T. (1995) EMBO J., 14, 594–602.
Muffler, A., Traulsen, D. D., Fischer, D., Lange, R., and Hengge-Aronis, R. (1997) J. Bacteriol., 179, 297–300.
Vecerek, B., Moll, I., and Blasi, U. (2005) RNA, 11, 976–984.
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.
Hajnsdorf, E., and Regnier, P. (2000) Proc. Natl. Acad. Sci. USA, 97, 1501–1505.
Folichon, M., Arluison, V., Pellegrini, O., Huntzinger, E., Regnier, P., and Hajnsdorf, E. (2003) Nucleic Acids Res., 31, 7302–7310.
Takada, A., Wachi, M., and Nagai, K. (1999) Biochem. Biophys. Res. Commun., 266, 579–583.
Wachi, M., Takada, A., and Nagai, K. (1999) Biochem. Biophys. Res. Commun., 264, 525–529.
Vytvytska, O., Moll, I., Kaberdin, V. R., von Gabain, A., and Blasi, U. (2000) Genes Dev., 14, 1109–1118.
Udekwu, K. I., Darfeuille, F., Vogel, J., Reimegard, J., Holmqvist, E., and Wagner, E. G. H. (2005) Genes Dev., 19, 2355–2366.
De Haseth, P. L., and Uhlenbeck, O. C. (1980) Biochemistry, 19, 6146–6151.
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.
Sun, X., and Wartell, R. M. (2006) Biochemistry, 45, 4875–4887.
Link, T. M., Valentin-Hansen, P., and Brennan, R. G. (2009) Proc. Natl. Acad. Sci. USA, 106, 19292–19297.
Lease, R. A., and Woodson, S. A. (2004) J. Mol. Biol., 344, 1211–1223.
Updegrove, T. B., Correia, J. J., Chen, Y., Terry, C., and Wartell, R. M. (2011) RNA, 17, 489–500.
Azam, T. A., and Ishihama, A. (1999) J. Biol. Chem., 274, 33105–33113.
Ishihama, A. (1999) Genes Cells, 4, 135–143.
Takada, A., Wachi, M., Kaidow, A., Takamura. M., and Nagai, K. (1997) Biochem. Biophys. Res. Commun., 236, 576–579.
Updegrove, T. B., Correia, J. J., Galletto, R., Bujalowski, W., and Wartell, R. M. (2010) Biochim. Biophys. Acta, 1799, 588–596.
Vlahovicek, K., Kajan, L., and Pongor, S. (2003) Nucleic Acids Res., 31, 3686–3687.
Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S., and Seraphin, B. (1999) EMBO J., 18, 3451–3462.
Toro, I., Thore, S., Mayer, C., Basquin, J., Seraphin, B., and Suck, D. (2001) EMBO J., 20, 2293–2303.
Achsel, T., Stark, H., and Luhrmann, R. (2001) Proc. Natl. Acad. Sci. USA, 98, 3685–3689.
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.
Mura, C., Cascio, D., Sawaya, M. R., and Eisenberg, D. S. (2001) Proc. Natl. Acad. Sci. USA, 98, 5532–5537.
Toro, I., Basquin, J., Teo-Dreher, H., and Suck, D. (2002) J. Mol. Biol., 320, 129–142.
Kilic, T., Sanglier, S., van Dorsselaer, A., and Suck, D. (2006) Protein Sci., 15, 2310–2317.
Mura, C., Kozhukhovsky, A., Gingery, M., Phillips, M., and Eisenberg, D. (2003) Protein Sci., 12, 832–847.
Mura, C., Phillips, M., Kozhukhovsky, A., and Eisenberg, D. (2003) Proc. Natl. Acad. Sci. USA, 100, 4539–4544.
Soppa, J., Straub, J., Brenneis, M., Jellen-Ritter, A., Heyer, R., and Fischer, S. (2009) Biochem. Soc. Trans., 37, 133–136.
Straub, J., Brenneis, M., Jellen-Ritter, A., Heyer, R., Soppa, J., and Marchfelder, A. (2009) RNA Biol., 6, 281–292.
Arluison, V., Mura, C., Guzman, M. R., Liquier, J., Pellegrini, O., and Gingery, M. (2006) J. Mol. Biol., 356, 86–96.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © V. N. Murina, A. D. Nikulin, 2011, published in Uspekhi Biologicheskoi Khimii, 2011, Vol. 51, pp. 133–164.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0006297911130050