Skip to main content
SpringerLink
Log in

Diversity of LSM Family Proteins: Similarities and Differences

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Members of the Lsm protein family are found in all three domains of life: bacteria, archaea, and eukarya. They are involved in numerous processes associated with RNA processing and gene expression regulation. A common structural feature of all Lsm family proteins is the presence of the Sm fold consisting of a five-stranded β-sheet and an α-helix at the N-terminus. Heteroheptameric eukaryotic Sm and Lsm proteins participate in the formation of spliceosomes and mRNA decapping. Homohexameric bacterial Lsm protein, Hfq, is involved in the regulation of transcription of different mRNAs by facilitating their interactions with small regulatory RNAs. Furthermore, recently obtained data indicate a new role of Hfq as a ribosome biogenesis factor, as it mediates formation of the productive structure of the 17S rRNA 3′- and 5′-sequences, facilitating their further processing by RNases. Lsm archaeal proteins (SmAPs) form homoheptamers and likely interact with single-stranded uridine-rich RNA elements, although the role of these proteins in archaea is still poorly understood. In this review, we discuss the structural features of the Lsm family proteins from different life domains and their structure–function relationships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

Abbreviations

Sm:

Smith antigen

Lsm protein:

Like-Sm (Sm-like) protein

SmAP:

Sm archaeal protein

Hfq:

Qβ host factor, replicase (host factor I participating in the replication of Qβ bacteriophage)

snRNA:

small nuclear RNA

sRNA:

small regulatory RNA

snRNP:

small nuclear ribonucleoprotein

References

  1. Mura, C., Randolph, P. S., Patterson, J., and Cozen, A. E. (2013) Archaeal and eukaryotic homologs of Hfq, RNA Biol., 10, 636-651.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Wilusz, C. J., and Wilusz, J. (2005) Eukaryotic Lsm proteins: lessons from bacteria, Nat. Struct. Mol. Biol., 12, 1031-1036.

    CAS  PubMed  Google Scholar 

  3. Notman, D. D., Kurata, N., and Tan, E. M. (1975) Profiles of antinuclear antibodies in systemic rheumatic diseases, Ann. Intern. Med., 83, 464-469.

    CAS  PubMed  Google Scholar 

  4. Thore, S., Mayer, C., Sauter, C., Weeks, S., and Suck, D. (2003) Crystal structures of the Pyrococcus abyssi Sm core and its complex with RNA: common features of RNA binding in archaea and eukarya, J. Biol. Chem., 278, 1239-1247.

    CAS  PubMed  Google Scholar 

  5. Sun, X. (2002) Predicted structure and phyletic distribution of the RNA-binding protein Hfq, Nucleic Acids Res., 30, 3662-3671.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Møller, T., Franch, T., Højrup, P., Keene, D. R., Bächinger, H. P., et al. (2002) Hfq: a bacterial Sm-like protein that mediates RNA–RNA interaction, Mol. Cell, 9, 23-30.

    PubMed  Google Scholar 

  7. Murina, V., Lekontseva, N., and Nikulin, A. (2013) Hfq binds ribonucleotides in three different RNA-binding sites, Acta Crystallogr. Sec. D Biol. Crystallogr., 69, 1504-1513.

    CAS  Google Scholar 

  8. Wassarman, K. M., Repoila, F., Rosenow, C., Storz, G., and Gottesman, S. (2001) Identification of novel small RNAs using comparative genomics and microarrays, Genes Dev., 15, 1637-1651.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S., and Séraphin, B. (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin, EMBO J., 18, 3451-3462.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Mura, C., Phillips, M., Kozhukhovsky, A., and Eisenberg, D. (2003) Structure and assembly of an augmented Sm-like archaeal protein 14-mer, Proc. Natl. Acad. Sci. USA, 100, 4539-4544.

    CAS  PubMed  Google Scholar 

  11. Collins, B. M., Harrop, S. J., Kornfeld, G. D., Dawes, I. W., Curmi, P. M.., and Mabbutt, B. C. (2001) Crystal structure of a heptameric Sm-like protein complex from archaea: implications for the structure and evolution of snRNPs, J. Mol. Biol., 309, 915-923.

    CAS  PubMed  Google Scholar 

  12. Törö, I., Thore, S., Mayer, C., Basquin, J., Séraphin, B., and Suck, D. (2001) RNA binding in an Sm core domain: X-ray structure and functional analysis of an archaeal Sm protein complex, EMBO J., 20, 2293-22303.

    PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Kambach, C., Walke, S., Young, R., Avis, J. M., De La Fortelle, E., et al. (1999) Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs, Cell, 96, 375-387.

    CAS  PubMed  Google Scholar 

  15. Mura, C., Cascio, D., Sawaya, M. R., and Eisenberg, D. S. (2001) The crystal structure of a heptameric archaeal Sm protein: implications for the eukaryotic snRNP core, Proc. Natl. Acad. Sci. USA, 98, 5532-5537.

    CAS  PubMed  Google Scholar 

  16. Schumacher, M. A., Pearson, R. F., Møller, T., Valentin-Hansen, P., and Brennan, R. G. (2002) Structures of the pleiotropic translational regulator Hfq and an Hfq–RNA complex: a bacterial Sm-like protein, EMBO J., 21, 3546-3556.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Sauter, C., Basquin, J., and Suck, D. (2003) Sm-like proteins in Eubacteria: the crystal structure of the Hfq protein from Escherichia coli, Nucleic Acids Res., 31, 4091-4098.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Nikulin, A., Stolboushkina, E., Perederina, A., Vassilieva, I., Blaesi, U., et al. (2005) Structure of Pseudomonas aeruginosa Hfq protein, Acta Crystallogr. Sec. D Biol. Crystallogr., 61, 141-146.

    Google Scholar 

  19. Das, D., Kozbial, P., Axelrod, H. L., Miller, M. D., McMullan, D., et al. (2009) Crystal structure of a novel Sm-like protein of putative cyanophage origin at 2.60 Å resolution, Proteins, 75, 296-307.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Törö, I., Basquin, J., Teo-Dreher, H., and Suck, D. (2002) Archaeal Sm proteins form heptameric and hexameric complexes: crystal structures of the Sm1 and Sm2 proteins from the hyperthermophile Archaeoglobus fulgidus, J. Mol. Biol., 320, 129-142.

    PubMed  Google Scholar 

  21. Wu, D., Jiang, S., Bowler, M. W., and Song, H. (2012) Crystal structures of Lsm3, Lsm4 and Lsm5/6/7 from Schizosaccharomyces pombe, PLoS One, 7, e36768.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Naidoo, N., Harrop, S. J., Sobti, M., Haynes, P. A, Szymczyna, B. R., et al. (2008) Crystal structure of Lsm3 octamer from Saccharomyces cerevisiae: implications for Lsm ring organisation and recruitment, J. Mol. Biol., 377, 1357-1371.

    CAS  PubMed  Google Scholar 

  23. Weichenrieder, O. (2014) A trade-off between optimal sequence readout and RNA backbone conformation RNA binding by Hfq and ring-forming (L)Sm proteins, RNA Biol., 11, 537-549.

    PubMed  PubMed Central  Google Scholar 

  24. Weber, G., Trowitzsch, S., Kastner, B., Lührmann, R., and Wahl, M. C. (2010) Functional organization of the Sm core in the crystal structure of human U1 snRNP, EMBO J., 29, 4172-4184.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Wilusz, C. J., and Wilusz, J. (2013) Lsm proteins and Hfq, RNA Biol., 10, 592-601.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Vogel, J., and Luisi, B. F. (2011) Hfq and its constellation of RNA, Nat. Rev. Microbiol., 9, 578-589.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Wagner, E. G. H. (2013) Cycling of RNAs on Hfq, RNA Biol., 10, 619-626.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Tharun, S. (2008) Roles of eukaryotic Lsm proteins in the regulation of mRNA function, Int. Rev. Cell Mol. Biol., 272, 149-189.

    Google Scholar 

  29. Walke, S., Bragado-Nilsson, E., Séraphin, B., and Nagai, K. (2001) Stoichiometry of the Sm proteins in yeast spliceosomal snRNPs supports the heptamer ring model of the core domain, J. Mol. Biol., 308, 49-58.

    CAS  PubMed  Google Scholar 

  30. Licht, K., Medenbach, J., Luhrmann, R., Kambach, C., and Bindereif, A. (2008) 3′-cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor p110 through LSm proteins, RNA, 14, 1532-1538.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Zaric, B., Chami, M., Rémigy, H., Engel, A., Ballmer-Hofer, K., et al. (2005) Reconstitution, of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function, J. Biol. Chem., 280, 16066-16075.

    CAS  PubMed  Google Scholar 

  32. Rinke, J., and Steitz, J. A. (1985) Association of the lupus antigen La with a subset of U6 snRNA molecules, Nucleic Acids Res., 13, 2617-2629.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Shchepachev, V., Wischnewski, H., Missiaglia, E., Soneson, C., and Azzalin, C. M. (2012) Mpn1, mutated in poikiloderma with neutropenia protein 1, is a conserved 3′-to-5′ RNA exonuclease processing U6 small nuclear RNA, Cell Rep., 2, 855-865.

    CAS  PubMed  Google Scholar 

  34. Achsel, T., Stark, H., and Lührmann, R. (2001) The Sm domain is an ancient RNA-binding motif with oligo(U) specificity, Proc. Natl. Acad. Sci. USA, 98, 3685-3689.

    CAS  PubMed  Google Scholar 

  35. Zhou, L., Hang, J., Zhou, Y., Wan, R., Lu, G., et al. (2014) Crystal structures of the Lsm complex bound to the 3′ end sequence of U6 small nuclear RNA, Nature, 506, 116-120.

    CAS  PubMed  Google Scholar 

  36. Tharun, S., He, W., Mayes, A. E., Lennertz, P., Beggs, J. D., and Parker, R. (2000) Yeast Sm-like proteins function in mRNA decapping and decay, Nature, 404, 515-518.

    CAS  PubMed  Google Scholar 

  37. Chen, C.-Y. A., and Shyu, A.-B. (2011) Mechanisms of deadenylation-dependent decay, Wiley Interdiscip. Rev. RNA, 2, 167-183.

    CAS  PubMed  Google Scholar 

  38. Chowdhury, A., Mukhopadhyay, J., and Tharun, S. (2007) The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs, RNA, 13, 998-1016.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Braun, J. E., Tritschler, F., Haas, G., Igreja, C., Truffault, V., et al. (2010) The C-terminal α-α superhelix of Pat is required for mRNA decapping in metazoa, EMBO J., 29, 2368-2380.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhou, L., Zhou, Y., Hang, J., Wan, R., Lu, G., et al. (2014) Crystal structure and biochemical analysis of the heptameric Lsm1-7 complex, Cell Res., 24, 497-500.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Wu, D., Muhlrad, D., Bowler, M. W., Jiang, S., Liu, Z., et al. (2014) Lsm2 and Lsm3 bridge the interaction of the Lsm1-7 complex with Pat1 for decapping activation, Cell Res., 24, 233-246.

    CAS  PubMed  Google Scholar 

  42. Rissland, O. S., and Norbury, C. J. (2009) Decapping is preceded by 3′ uridylation in a novel pathway of bulk mRNA turnover, Nat. Struct. Mol. Biol., 16, 616-623.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Morozov, I. Y., Jones, M. G., Razak, A. A., Rigden, D. J., and Caddick, M. X. (2010) CUCU modification of mRNA promotes decapping and transcript degradation in Aspergillus nidulans, Mol. Cel. Biol., 30, 460-469.

    CAS  Google Scholar 

  44. Morozov, I. Y., Jones, M. G., Gould, P. D., Crome, V., Wilson, J. B., et al. (2012) mRNA 3′-tagging is induced by nonsense-mediated decay and promotes ribosome dissociation, Mol. Cel. Biol., 32, 2585-2595.

    CAS  Google Scholar 

  45. Franze de Fernandez, M. T., Hayward, W. S., and August, J. T. (1972) Bacterial proteins required for replication of phage Q ribonucleic acid. Purification and properties of host factor I, a ribonucleic acid-binding protein, J. Biol. Chem., 247, 824-831.

    CAS  PubMed  Google Scholar 

  46. Sauer, E. (2013) Structure and RNA-binding properties of the bacterial LSm protein Hfq, RNA Biol., 10, 610-618.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Updegrove, T. B., Zhang, A., and Storz, G. (2016) Hfq: the flexible RNA matchmaker, Curr. Opin. Microbiol., 30, 133-138.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Otaka, H., Ishikawa, H., Morita, T., and Aiba, H. (2011) PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action, Proc. Natl. Acad. Sci. USA, 108, 13059-13064.

    CAS  PubMed  Google Scholar 

  49. Wang, W., Wang, L., Wu, J., Gong, Q., and Shi, Y. (2013) Hfq-bridged ternary complex is important for translation activation of rpoS by DsrA, Nucleic Acids Res., 41, 5938-5948.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Sauer, E., and Weichenrieder, O. (2011) Structural basis for RNA 3′-end recognition by Hfq, Proc. Natl. Acad. Sci. USA, 108, 13065-13070.

    CAS  PubMed  Google Scholar 

  51. Zhang, A., Schu, D. J., Tjaden, B. C., Storz, G., and Gottesman, S. (2013) Mutations in interaction surfaces differentially impact E. coli Hfq association with small RNAs and their mRNA targets, J. Mol. Biol., 425, 3678-3697.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Panja, S., Santiago-Frangos, A., Schu, D. J., Gottesman, S., and Woodson, S. A. (2015) Acidic residues in the Hfq chaperone increase the selectivity of sRNA binding and annealing, J. Mol. Biol., 427, 3491-3500.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Link, T. M., Valentin-Hansen, P., and Brennan, R. G. (2009) Structure of Escherichia coli Hfq bound to polyriboadenylate RNA, Proc. Natl. Acad. Sci. USA, 106, 19292-19297.

    CAS  PubMed  Google Scholar 

  54. Someya, T., Baba, S., Fujimoto, M., Kawai, G., Kumasaka, T., and Nakamura, K. (2012) Crystal structure of Hfq from Bacillus subtilis in complex with SELEX-derived RNA aptamer: insight into RNA-binding properties of bacterial Hfq, Nucleic Acids Res., 40, 1856-1867.

    CAS  PubMed  Google Scholar 

  55. Schu, D. J., Zhang, A., Gottesman, S., and Storz, G. (2015) Alternative Hfq-sRNA interaction modes dictate alternative mRNA recognition, EMBO J., 34, 2557-2573.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Sauer, E., Schmidt, S., and Weichenrieder, O. (2012) Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition, Proc. Natl. Acad. Sci. USA, 109, 9396-9401.

    CAS  PubMed  Google Scholar 

  57. Sobrero, P., and Valverde, C. (2012) The bacterial protein Hfq: much more than a mere RNA-binding factor, Crit. Rev. Microbiol., 38, 276-299.

    CAS  PubMed  Google Scholar 

  58. Dimastrogiovanni, D., Fröhlich, K. S., Bandyra, K. J., Bruce, H. A., Hohensee, S., et al. (2014) Recognition of the small regulatory RNA RydC by the bacterial Hfq protein, ELife, 3, e05375.

    PubMed Central  Google Scholar 

  59. Robinson, K. E., Orans, J., Kovach, A. R., Link, T. M., and Brennan, R. G. (2014) Mapping Hfq–RNA interaction surfaces using tryptophan fluorescence quenching, Nucleic Acids Res., 42, 2736-2749.

    CAS  PubMed  Google Scholar 

  60. Vincent, H. A., Henderson, C. A., Ragan, T. J., Garza-Garcia, A., Cary, P. D., et al. (2012) Characterization of Vibrio cholerae Hfq provides novel insights into the role of the Hfq C-terminal region, J. Mol. Biol., 420, 56-69.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Lee, T., and Feig, A. L. (2008) The RNA binding protein Hfq interacts specifically with tRNAs, RNA, 14, 514-523.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Zhang, A., Wassarman, K. M., Rosenow, C., Tjaden, B. C., Storz, G., and Gottesman, S. (2003) Global analysis of small RNA and mRNA targets of Hfq, Mol. Microbiol., 50, 1111-1124.

    CAS  PubMed  Google Scholar 

  63. Azam, T. A., Hiraga, S., and Ishihama, A. (2000) Two types of localization of the DNA-binding proteins within the Escherichia coli nucleoid, Genes Cells, 5, 613-626.

    CAS  PubMed  Google Scholar 

  64. Malabirade, A., Jiang, K., Kubiak, K., Diaz-Mendoza, A., Liu, F., et al. (2017) Compaction and condensation of DNA mediated by the C-terminal domain of Hfq, Nucleic Acids Res., 45, 7299-7308.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Andrade, J. M., Pobre, V., Matos, A. M., and Arraiano, C. M. (2012) The crucial role of PNPase in the degradation of small RNAs that are not associated with Hfq, RNA, 18, 844-855.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Moll, I., Leitsch, D., Steinhauser, T., and Bläsi, U. (2003) RNA chaperone activity of the Sm-like Hfq protein, EMBO Rep., 4, 284-289.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Régnier, P., and Hajnsdorf, E. (2013) The interplay of Hfq, poly(A) polymerase I and exoribonucleases at the 3′ ends of RNAs resulting from Rho-independent termination: a tentative model, RNA Biol., 10, 602-609.

    PubMed  PubMed Central  Google Scholar 

  68. Sukhodolets, M. V., and Garges, S. (2003) Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq, Biochemistry, 42, 8022-8034.

    CAS  PubMed  Google Scholar 

  69. Rabhi, M., Espéli, O., Schwartz, A., Cayrol, B., Rahmouni, A. R., et al. (2011) The Sm-like RNA chaperone Hfq mediates transcription antitermination at Rho-dependent terminators, EMBO J., 30, 2805-2816.

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Dos Santos, R. F., Arraiano, C. M., and Andrade, J. M. (2019) New molecular interactions broaden the functions of the RNA chaperone Hfq, Curr. Genet., 65, 1313-1319.

    CAS  PubMed  Google Scholar 

  71. Andrade, J. M., Santos, R. F., Chelysheva, I., Ignatova, Z., and Arraiano, C. M. (2018) The RNA-binding protein Hfq is important for ribosome biogenesis and affects translation fidelity, EMBO J., 37, 1-13.

    Google Scholar 

  72. Strader, M. B., Hervey, W. J., Costantino, N., Fujigaki, S., Chen, C. Y., et al. (2013) A coordinated proteomic approach for identifying proteins that interact with the E. coli ribosomal protein S12, J. Proteome Res., 12, 1289-1299.

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Yusupov, M. M., Yusupova, G. Z., Baucom, A., Lieberman, K., Earnest, T. N., et al. (2001) Crystal structure of the ribosome at 5.5 Å resolution, Science, 292, 883-896.

    CAS  PubMed  Google Scholar 

  74. Cukras, A. R., Southworth, D. R., Brunelle, J. L., Culver, G. M., and Green, R. (2003) Ribosomal proteins S12 and S13 function as control elements for translocation of the mRNA:tRNA complex, Mol. Cell, 12, 321-328.

    CAS  PubMed  Google Scholar 

  75. Nielsen, J. S., Boggild, A., Andersen, C. B. F., Nielsen, G., Boysen, A., et al. (2007) An Hfq-like protein in archaea: crystal structure and functional characterization of the Sm protein from Methanococcus jannaschii, RNA, 13, 2213-2223.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Nikulin, A., Mikhailina, A., Lekontseva, N., Balobanov, V., Nikonova, E., and Tishchenko, S. (2017) Characterization of RNA-binding properties of the archaeal Hfq-like protein from Methanococcus jannaschii, J. Biomol. Struct. Dyn., 35, 1615-1628.

    CAS  PubMed  Google Scholar 

  77. Märtens, B., Hou, L., Amman, F., Wolfinger, M. T., Evguenieva-Hackenberg, E., and Bläsi, U. (2017) The SmAP1/2 proteins of the crenarchaeon Sulfolobus solfataricus interact with the exosome and stimulate A-rich tailing of transcripts, Nucleic Acids Res., 45, 7938-7949.

    PubMed  PubMed Central  Google Scholar 

  78. Märtens, B., Bezerra, G. A., Kreuter, M. J., Grishkovskaya, I., Manica, A., Arkhipova, V., et al. (2015) The heptameric SmAP1 and SmAP2 proteins of the crenarchaeon Sulfolobus Solfataricus bind to common and distinct RNA targets, Life (Basel), 5, 1264-1281.

    Google Scholar 

  79. Fischer, S., Benz, J., Späth, B., Maier, L.-K., Straub, J., et al. (2010) The archaeal Lsm protein binds to small RNAs, J. Biol. Chem., 285, 34429-34438.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Lekontseva, N., Mikhailina, A., Fando, M., Kravchenko, O., Balobanov, V., et al. (2020) Crystal structures and RNA-binding properties of Lsm proteins from archaea Sulfolobus acidocaldarius and Methanococcus vannielii: similarity and difference of the U-binding mode, Biochimie, 175, 1-12.

    CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Russian Science Foundation (project no. 19-74-20186).

Author information

Authors and Affiliations

  1. Institute of Protein Research, Russian Academy of Sciences, 142290, Pushchino, Moscow Region, Russia

    Natalia V. Lekontseva, Elena A. Stolboushkina & Alexey D. Nikulin

Authors
  1. Natalia V. Lekontseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena A. Stolboushkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexey D. Nikulin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalia V. Lekontseva.

Ethics declarations

The authors declare no conflict of interest in financial or any other sphere. This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lekontseva, N.V., Stolboushkina, E.A. & Nikulin, A.D. Diversity of LSM Family Proteins: Similarities and Differences. Biochemistry Moscow 86 (Suppl 1), S38–S49 (2021). https://doi.org/10.1134/S0006297921140042

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297921140042

Keywords

Search

Navigation