1loj › Citations

The oligomerization and ligand-binding properties of Sm-like archaeal proteins (SmAPs).

Mura C, Kozhukhovsky A, Gingery M, Phillips M, Eisenberg D
Protein Sci 12 832-47 (2003)
Related entries: 1jbm, 1jri, 1lnx

Cited: 36 times
EuropePMC logo PMID: 12649441

Abstract

Intron splicing is a prime example of the many types of RNA processing catalyzed by small nuclear ribonucleoprotein (snRNP) complexes. Sm proteins form the cores of most snRNPs, and thus to learn principles of snRNP assembly we characterized the oligomerization and ligand-binding properties of Sm-like archaeal proteins (SmAPs) from Pyrobaculum aerophilum (Pae) and Methanobacterium thermautotrophicum (Mth). Ultracentrifugation shows that Mth SmAP1 is exclusively heptameric in solution, whereas Pae SmAP1 forms either disulfide-bonded 14-mers or sub-heptameric states (depending on the redox potential). By electron microscopy, we show that Pae and Mth SmAP1 polymerize into bundles of well ordered fibers that probably form by head-to-tail stacking of heptamers. The crystallographic results reported here corroborate these findings by showing heptamers and 14-mers of both Mth and Pae SmAP1 in four new crystal forms. The 1.9 A-resolution structure of Mth SmAP1 bound to uridine-5'-monophosphate (UMP) reveals conserved ligand-binding sites. The likely RNA binding site in Mth agrees with that determined for Archaeoglobus fulgidus (Afu) SmAP1. Finally, we found that both Pae and Mth SmAP1 gel-shift negatively supercoiled DNA. These results distinguish SmAPs from eukaryotic Sm proteins and suggest that SmAPs have a generic single-stranded nucleic acid-binding activity.

Articles - 1loj mentioned but not cited (2)

  1. The oligomerization and ligand-binding properties of Sm-like archaeal proteins (SmAPs). Mura C, Kozhukhovsky A, Gingery M, Phillips M, Eisenberg D. Protein Sci 12 832-847 (2003)
  2. Crystal structure of a novel Sm-like protein of putative cyanophage origin at 2.60 A resolution. Das D, Kozbial P, Axelrod HL, Miller MD, McMullan D, Krishna SS, Abdubek P, Acosta C, Astakhova T, Burra P, Carlton D, Chen C, Chiu HJ, Clayton T, Deller MC, Duan L, Elias Y, Elsliger MA, Ernst D, Farr C, Feuerhelm J, Grzechnik A, Grzechnik SK, Hale J, Han GW, Jaroszewski L, Jin KK, Johnson HA, Klock HE, Knuth MW, Kumar A, Marciano D, Morse AT, Murphy KD, Nigoghossian E, Nopakun A, Okach L, Oommachen S, Paulsen J, Puckett C, Reyes R, Rife CL, Sefcovic N, Sudek S, Tien H, Trame C, Trout CV, van den Bedem H, Weekes D, White A, Xu Q, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA. Proteins 75 296-307 (2009)


Reviews citing this publication (7)

  1. Hfq structure, function and ligand binding. Brennan RG, Link TM. Curr Opin Microbiol 10 125-133 (2007)
  2. LSm proteins form heptameric rings that bind to RNA via repeating motifs. Khusial P, Plaag R, Zieve GW. Trends Biochem Sci 30 522-528 (2005)
  3. Archaeal and eukaryotic homologs of Hfq: A structural and evolutionary perspective on Sm function. Mura C, Randolph PS, Patterson J, Cozen AE. RNA Biol 10 636-651 (2013)
  4. Insights into RNA-processing pathways and associated RNA-degrading enzymes in Archaea. Clouet-d'Orval B, Batista M, Bouvier M, Quentin Y, Fichant G, Marchfelder A, Maier LK. FEMS Microbiol Rev 42 579-613 (2018)
  5. Evolutionary diversification of the Sm family of RNA-associated proteins. Scofield DG, Lynch M. Mol Biol Evol 25 2255-2267 (2008)
  6. RNA-binding Sm-like proteins of bacteria and archaea. similarity and difference in structure and function. Murina VN, Nikulin AD. Biochemistry (Mosc) 76 1434-1449 (2011)
  7. Unique Archaeal Small RNAs. Gomes-Filho JV, Daume M, Randau L. Annu Rev Genet 52 465-487 (2018)

Articles citing this publication (27)

  1. Escherichia coli Hfq has distinct interaction surfaces for DsrA, rpoS and poly(A) RNAs. Mikulecky PJ, Kaw MK, Brescia CC, Takach JC, Sledjeski DD, Feig AL. Nat Struct Mol Biol 11 1206-1214 (2004)
  2. The origin and early evolution of eukaryotes in the light of phylogenomics. Koonin EV. Genome Biol 11 209 (2010)
  3. Structural and functional analysis of ataxin-2 and ataxin-3. Albrecht M, Golatta M, Wüllner U, Lengauer T. Eur J Biochem 271 3155-3170 (2004)
  4. Novel Sm-like proteins with long C-terminal tails and associated methyltransferases. Albrecht M, Lengauer T. FEBS Lett 569 18-26 (2004)
  5. Spectroscopic observation of RNA chaperone activities of Hfq in post-transcriptional regulation by a small non-coding RNA. Arluison V, Hohng S, Roy R, Pellegrini O, Régnier P, Ha T. Nucleic Acids Res 35 999-1006 (2007)
  6. Mutations in the Saccharomyces cerevisiae LSM1 gene that affect mRNA decapping and 3' end protection. Tharun S, Muhlrad D, Chowdhury A, Parker R. Genetics 170 33-46 (2005)
  7. Unusual arginine formations in protein function and assembly: rings, strings, and stacks. Neves MA, Yeager M, Abagyan R. J Phys Chem B 116 7006-7013 (2012)
  8. An Hfq-like protein in archaea: crystal structure and functional characterization of the Sm protein from Methanococcus jannaschii. Nielsen JS, Bøggild A, Andersen CB, Nielsen G, Boysen A, Brodersen DE, Valentin-Hansen P. RNA 13 2213-2223 (2007)
  9. E. coli DNA associated with isolated Hfq interacts with Hfq's distal surface and C-terminal domain. Updegrove TB, Correia JJ, Galletto R, Bujalowski W, Wartell RM. Biochim Biophys Acta 1799 588-596 (2010)
  10. Three-dimensional structures of fibrillar Sm proteins: Hfq and other Sm-like proteins. Arluison V, Mura C, Guzmán MR, Liquier J, Pellegrini O, Gingery M, Régnier P, Marco S. J Mol Biol 356 86-96 (2006)
  11. The archaeal Lsm protein binds to small RNAs. Fischer S, Benz J, Späth B, Maier LK, Straub J, Granzow M, Raabe M, Urlaub H, Hoffmann J, Brutschy B, Allers T, Soppa J, Marchfelder A. J Biol Chem 285 34429-34438 (2010)
  12. Structure and assembly of an augmented Sm-like archaeal protein 14-mer. Mura C, Phillips M, Kozhukhovsky A, Eisenberg D. Proc Natl Acad Sci U S A 100 4539-4544 (2003)
  13. Regulation by oligomerization in a mycobacterial folate biosynthetic enzyme. Goulding CW, Apostol MI, Sawaya MR, Phillips M, Parseghian A, Eisenberg D. J Mol Biol 349 61-72 (2005)
  14. Hexamer to monomer equilibrium of E. coli Hfq in solution and its impact on RNA annealing. Panja S, Woodson SA. J Mol Biol 417 406-412 (2012)
  15. Crystal structure of Lsm3 octamer from Saccharomyces cerevisiae: implications for Lsm ring organisation and recruitment. Naidoo N, Harrop SJ, Sobti M, Haynes PA, Szymczyna BR, Williamson JR, Curmi PM, Mabbutt BC. J Mol Biol 377 1357-1371 (2008)
  16. The SmAP1/2 proteins of the crenarchaeon Sulfolobus solfataricus interact with the exosome and stimulate A-rich tailing of transcripts. Märtens B, Hou L, Amman F, Wolfinger MT, Evguenieva-Hackenberg E, Bläsi U. Nucleic Acids Res 45 7938-7949 (2017)
  17. Both Sm-domain and C-terminal extension of Lsm1 are important for the RNA-binding activity of the Lsm1-7-Pat1 complex. Chowdhury A, Raju KK, Kalurupalle S, Tharun S. RNA 18 936-944 (2012)
  18. Crystal structure and RNA-binding properties of an Hfq homolog from the deep-branching Aquificae: conservation of the lateral RNA-binding mode. Stanek KA, Patterson-West J, Randolph PS, Mura C. Acta Crystallogr D Struct Biol 73 294-315 (2017)
  19. Analysis of Lsm1p and Lsm8p domains in the cellular localization of Lsm complexes in budding yeast. Reijns MA, Auchynnikava T, Beggs JD. FEBS J 276 3602-3617 (2009)
  20. Unraveling Membrane Perturbations Caused by the Bacterial Riboregulator Hfq. Turbant F, Waeytens J, Campidelli C, Bombled M, Martinez D, Grélard A, Habenstein B, Raussens V, Velez M, Wien F, Arluison V. Int J Mol Sci 23 8739 (2022)
  21. Protein nanorings organized by poly(styrene-block-ethylene oxide) self-assembled thin films. Malmström J, Wason A, Roache F, Yewdall NA, Radjainia M, Wei S, Higgins MJ, Williams DE, Gerrard JA, Travas-Sejdic J. Nanoscale 7 19940-19948 (2015)
  22. The SmAP2 RNA binding motif in the 3'UTR affects mRNA stability in the crenarchaeum Sulfolobus solfataricus. Märtens B, Sharma K, Urlaub H, Bläsi U. Nucleic Acids Res 45 8957-8967 (2017)
  23. Protein subunit interfaces: A statistical analysis of hot spots in Sm proteins. Stojanović SD, Zarić BL, Zarić SD. J Mol Model 16 1743-1751 (2010)
  24. Core spliceosomal Sm proteins as constituents of cytoplasmic mRNPs in plants. Hyjek-Składanowska M, Bajczyk M, Gołębiewski M, Nuc P, Kołowerzo-Lubnau A, Jarmołowski A, Smoliński DJ. Plant J 103 1155-1173 (2020)
  25. The Denaturant- and Mutation-Induced Disassembly of Pseudomonas aeruginosa Hexameric Hfq Y55W Mutant. Marchenkov V, Lekontseva N, Marchenko N, Kashparov I, Murina V, Nikulin A, Filimonov V, Semisotnov G. Molecules 27 3821 (2022)
  26. Supramolecular organization of Hfq-like proteins. Murina VN, Selivanova OM, Mikhaylina AO, Kazakov AS, Nikonova EY, Lekontseva NV, Tishchenko SV, Nikulin AD. Biochemistry (Mosc) 80 441-448 (2015)
  27. The bacterial protein Hfq: Stable modifications and growth phase-dependent changes in SPAM profiles. Troung SF, Sukhodolets MV. J Chromatogr B Analyt Technol Biomed Life Sci 1183 122958 (2021)


Related citations provided by authors (1)

  1. The crystal structure of a heptameric archaeal Sm protein: Implications for the eukaryotic snRNP core. Mura C, Cascio D, Sawaya MR, Eisenberg D Proc. Natl. Acad. Sci. U.S.A. 98 5532-5537 (2001)

Quick links