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Crystal structure of DNA sequence specificity subunit of a type I restriction-modification enzyme and its functional implications.

Kim JS, DeGiovanni A, Jancarik J, Adams PD, Yokota H, Kim R, Kim SH
Proc Natl Acad Sci U S A 102 3248-53 (2005)
Cited: 53 times
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Abstract

Type I restriction-modification enzymes are differentiated from type II and type III enzymes by their recognition of two specific dsDNA sequences separated by a given spacer and cleaving DNA randomly away from the recognition sites. They are oligomeric proteins formed by three subunits: a specificity subunit, a methylation subunit, and a restriction subunit. We solved the crystal structure of a specificity subunit from Methanococcus jannaschii at 2.4-A resolution. Two highly conserved regions (CRs) in the middle and at the C terminus form a coiled-coil of long antiparallel alpha-helices. Two target recognition domains form globular structures with almost identical topologies and two separate DNA binding clefts with a modeled DNA helix axis positioned across the CR helices. The structure suggests that the coiled-coil CRs act as a molecular ruler for the separation between two recognized DNA sequences. Furthermore, the relative orientation of the two DNA binding clefts suggests kinking of bound dsDNA and exposing of target adenines from the recognized DNA sequences.

Reviews - 1yf2 mentioned but not cited (1)

  1. Type I restriction enzymes and their relatives. Loenen WA, Dryden DT, Raleigh EA, Wilson GG. Nucleic Acids Res 42 20-44 (2014)

Articles - 1yf2 mentioned but not cited (15)

  1. The structure of M.EcoKI Type I DNA methyltransferase with a DNA mimic antirestriction protein. Kennaway CK, Obarska-Kosinska A, White JH, Tuszynska I, Cooper LP, Bujnicki JM, Trinick J, Dryden DT. Nucleic Acids Res 37 762-770 (2009)
  2. Crystal structure of DNA sequence specificity subunit of a type I restriction-modification enzyme and its functional implications. Kim JS, DeGiovanni A, Jancarik J, Adams PD, Yokota H, Kim R, Kim SH. Proc Natl Acad Sci U S A 102 3248-3253 (2005)
  3. Characterization and crystal structure of the type IIG restriction endonuclease RM.BpuSI. Shen BW, Xu D, Chan SH, Zheng Y, Zhu Z, Xu SY, Stoddard BL. Nucleic Acids Res 39 8223-8236 (2011)
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  5. Related bifunctional restriction endonuclease-methyltransferase triplets: TspDTI, Tth111II/TthHB27I and TsoI with distinct specificities. Zylicz-Stachula A, Zolnierkiewicz O, Lubys A, Ramanauskaite D, Mitkaite G, Bujnicki JM, Skowron PM. BMC Mol Biol 13 13 (2012)
  6. Structural model for the multisubunit Type IC restriction-modification DNA methyltransferase M.EcoR124I in complex with DNA. Obarska A, Blundell A, Feder M, Vejsadová S, Sisáková E, Weiserová M, Bujnicki JM, Firman K. Nucleic Acids Res 34 1992-2005 (2006)
  7. Functional analysis of MmeI from methanol utilizer Methylophilus methylotrophus, a subtype IIC restriction-modification enzyme related to type I enzymes. Nakonieczna J, Kaczorowski T, Obarska-Kosinska A, Bujnicki JM. Appl Environ Microbiol 75 212-223 (2009)
  8. Shape and subunit organisation of the DNA methyltransferase M.AhdI by small-angle neutron scattering. Callow P, Sukhodub A, Taylor JEN, Kneale GG. J Mol Biol 369 177-185 (2007)
  9. Genome-wide survey of codons under diversifying selection in a highly recombining bacterial species, Helicobacter pylori. Yahara K, Furuta Y, Morimoto S, Kikutake C, Komukai S, Matelska D, Dunin-Horkawicz S, Bujnicki JM, Uchiyama I, Kobayashi I. DNA Res 23 135-143 (2016)
  10. Structural and functional analysis of the engineered type I DNA methyltransferase EcoR124I(NT). Taylor JEN, Callow P, Swiderska A, Kneale GG. J Mol Biol 398 391-399 (2010)
  11. Crystal structure of a novel domain of the motor subunit of the Type I restriction enzyme EcoR124 involved in complex assembly and DNA binding. Grinkevich P, Sinha D, Iermak I, Guzanova A, Weiserova M, Ludwig J, Mesters JR, Ettrich RH. J Biol Chem 293 15043-15054 (2018)
  12. Oligomerization of a retroviral matrix protein is facilitated by backbone flexibility on nanosecond time scale. Srb P, Vlach J, Prchal J, Grocký M, Ruml T, Lang J, Hrabal R. J Phys Chem B 115 2634-2644 (2011)
  13. DNA recognition by the SwaI restriction endonuclease involves unusual distortion of an 8 base pair A:T-rich target. Shen BW, Heiter DF, Lunnen KD, Wilson GG, Stoddard BL. Nucleic Acids Res 45 1516-1528 (2017)
  14. Cloning, crystallization and preliminary X-ray diffraction analysis of an intact DNA methyltransferase of a type I restriction-modification enzyme from Vibrio vulnificus. Huynh Thi Yen L, Park SY, Kim JS. Acta Crystallogr F Struct Biol Commun 70 489-492 (2014)
  15. The extremophile Picrophilus torridus carries a DNA adenine methylase M.PtoI that is part of a Type I restriction-modification system. Gulati P, Singh A, Goel M, Saha S. Front Microbiol 14 1126750 (2023)


Reviews citing this publication (10)

  1. The biology of restriction and anti-restriction. Tock MR, Dryden DT. Curr Opin Microbiol 8 466-472 (2005)
  2. Coiled-coils: The long and short of it. Truebestein L, Leonard TA. Bioessays 38 903-916 (2016)
  3. Adenine methylation in eukaryotes: Apprehending the complex evolutionary history and functional potential of an epigenetic modification. Iyer LM, Zhang D, Aravind L. Bioessays 38 27-40 (2016)
  4. Small angle neutron and X-ray scattering in structural biology: recent examples from the literature. Neylon C. Eur Biophys J 37 531-541 (2008)
  5. Structures in systems biology. Beltrao P, Kiel C, Serrano L. Curr Opin Struct Biol 17 378-384 (2007)
  6. DNA mimicry by proteins and the control of enzymatic activity on DNA. Dryden DT. Trends Biotechnol 24 378-382 (2006)
  7. Structure-based inference of molecular functions of proteins of unknown function from Berkeley Structural Genomics Center. Shin DH, Hou J, Chandonia JM, Das D, Choi IG, Kim R, Kim SH. J Struct Funct Genomics 8 99-105 (2007)
  8. Understanding the cell in terms of structure and function: insights from structural genomics. Rigden DJ. Curr Opin Biotechnol 17 457-464 (2006)
  9. EcoR124I: from plasmid-encoded restriction-modification system to nanodevice. Youell J, Firman K. Microbiol Mol Biol Rev 72 365-77, table of contents (2008)
  10. DNA mimicry by proteins as effective mechanism for regulation of activity of DNA-dependent enzymes. Zavilgelsky GB, Rastorguev SM. Biochemistry (Mosc) 72 913-9, 4 p. following 982 (2007)

Articles citing this publication (27)

  1. Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. Waldron DE, Lindsay JA. J Bacteriol 188 5578-5585 (2006)
  2. Highlights of the DNA cutters: a short history of the restriction enzymes. Loenen WA, Dryden DT, Raleigh EA, Wilson GG, Murray NE. Nucleic Acids Res 42 3-19 (2014)
  3. Predicting DNA-binding sites of proteins from amino acid sequence. Yan C, Terribilini M, Wu F, Jernigan RL, Dobbs D, Honavar V. BMC Bioinformatics 7 262 (2006)
  4. The MmeI family: type II restriction-modification enzymes that employ single-strand modification for host protection. Morgan RD, Dwinell EA, Bhatia TK, Lang EM, Luyten YA. Nucleic Acids Res 37 5208-5221 (2009)
  5. Impact of target site distribution for Type I restriction enzymes on the evolution of methicillin-resistant Staphylococcus aureus (MRSA) populations. Roberts GA, Houston PJ, White JH, Chen K, Stephanou AS, Cooper LP, Dryden DT, Lindsay JA. Nucleic Acids Res 41 7472-7484 (2013)
  6. A coiled-coil domain acts as a molecular ruler to regulate O-antigen chain length in lipopolysaccharide. Hagelueken G, Clarke BR, Huang H, Tuukkanen A, Danciu I, Svergun DI, Hussain R, Liu H, Whitfield C, Naismith JH. Nat Struct Mol Biol 22 50-56 (2015)
  7. Structure and operation of the DNA-translocating type I DNA restriction enzymes. Kennaway CK, Taylor JEN, Song CF, Potrzebowski W, Nicholson W, White JH, Swiderska A, Obarska-Kosinska A, Callow P, Cooper LP, Roberts GA, Artero JB, Bujnicki JM, Trinick J, Kneale GG, Dryden DT. Genes Dev 26 92-104 (2012)
  8. Crystal structure of a putative type I restriction-modification S subunit from Mycoplasma genitalium. Calisto BM, Pich OQ, Piñol J, Fita I, Querol E, Carpena X. J Mol Biol 351 749-762 (2005)
  9. Nonequilibrium dynamics of helix reorganization observed by transient 2D IR spectroscopy. Tucker MJ, Abdo M, Courter JR, Chen J, Brown SP, Smith AB, Hochstrasser RM. Proc Natl Acad Sci U S A 110 17314-17319 (2013)
  10. HsdR subunit of the type I restriction-modification enzyme EcoR124I: biophysical characterisation and structural modelling. Obarska-Kosinska A, Taylor JEN, Callow P, Orlowski J, Bujnicki JM, Kneale GG. J Mol Biol 376 438-452 (2008)
  11. Hyperthermophilic DNA methyltransferase M.PabI from the archaeon Pyrococcus abyssi. Watanabe M, Yuzawa H, Handa N, Kobayashi I. Appl Environ Microbiol 72 5367-5375 (2006)
  12. Translocation-coupled DNA cleavage by the Type ISP restriction-modification enzymes. Chand MK, Nirwan N, Diffin FM, van Aelst K, Kulkarni M, Pernstich C, Szczelkun MD, Saikrishnan K. Nat Chem Biol 11 870-877 (2015)
  13. The fragment structure of a putative HsdR subunit of a type I restriction enzyme from Vibrio vulnificus YJ016: implications for DNA restriction and translocation activity. Uyen NT, Park SY, Choi JW, Lee HJ, Nishi K, Kim JS. Nucleic Acids Res 37 6960-6969 (2009)
  14. Residues of E. coli topoisomerase I conserved for interaction with a specific cytosine base to facilitate DNA cleavage. Narula G, Tse-Dinh YC. Nucleic Acids Res 40 9233-9243 (2012)
  15. Genome-wide DNA methylation analysis of Haloferax volcanii H26 and identification of DNA methyltransferase related PD-(D/E)XK nuclease family protein HVO_A0006. Ouellette M, Jackson L, Chimileski S, Papke RT. Front Microbiol 6 251 (2015)
  16. Structural insights into assembly, operation and inhibition of a type I restriction-modification system. Gao Y, Cao D, Zhu J, Feng H, Luo X, Liu S, Yan XX, Zhang X, Gao P. Nat Microbiol 5 1107-1118 (2020)
  17. Structure of HsdS subunit from Thermoanaerobacter tengcongensis sheds lights on mechanism of dynamic opening and closing of type I methyltransferase. Gao P, Tang Q, An X, Yan X, Liang D. PLoS One 6 e17346 (2011)
  18. Structural basis underlying complex assembly and conformational transition of the type I R-M system. Liu YP, Tang Q, Zhang JZ, Tian LF, Gao P, Yan XX. Proc Natl Acad Sci U S A 114 11151-11156 (2017)
  19. Structural insights into DNA sequence recognition by Type ISP restriction-modification enzymes. Kulkarni M, Nirwan N, van Aelst K, Szczelkun MD, Saikrishnan K. Nucleic Acids Res 44 4396-4408 (2016)
  20. Crystal structure of the R-protein of the multisubunit ATP-dependent restriction endonuclease NgoAVII. Tamulaitiene G, Silanskas A, Grazulis S, Zaremba M, Siksnys V. Nucleic Acids Res 42 14022-14030 (2014)
  21. Removal of a frameshift between the hsdM and hsdS genes of the EcoKI Type IA DNA restriction and modification system produces a new type of system and links the different families of Type I systems. Roberts GA, Chen K, Cooper LP, White JH, Blakely GW, Dryden DT. Nucleic Acids Res 40 10916-10924 (2012)
  22. A model for the evolution of prokaryotic DNA restriction-modification systems based upon the structural malleability of Type I restriction-modification enzymes. Bower EKM, Cooper LP, Roberts GA, White JH, Luyten Y, Morgan RD, Dryden DTF. Nucleic Acids Res 46 9067-9080 (2018)
  23. Structural characterization of a modification subunit of a putative type I restriction enzyme from Vibrio vulnificus YJ016. Park SY, Lee HJ, Song JM, Sun J, Hwang HJ, Nishi K, Kim JS. Acta Crystallogr D Biol Crystallogr 68 1570-1577 (2012)
  24. A Type I Restriction Modification System Influences Genomic Evolution Driven by Horizontal Gene Transfer in Paenibacillus polymyxa. Chen Z, Shen M, Mao C, Wang C, Yuan P, Wang T, Sun D. Front Microbiol 12 709571 (2021)
  25. Characterisation of Phage Susceptibility Variation in Salmonellaenterica Serovar Typhimurium DT104 and DT104b. Mohammed M, Orzechowska B. Microorganisms 9 865 (2021)
  26. Crystallization and preliminary X-ray diffraction analysis of the HsdR subunit of a putative type I restriction enzyme from Vibrio vulnificus YJ016. Uyen NT, Nishi K, Park SY, Choi JW, Lee HJ, Kim JS. Acta Crystallogr Sect F Struct Biol Cryst Commun 64 926-928 (2008)
  27. Molecular insights into DNA recognition and methylation by non-canonical type I restriction-modification systems. Zhu J, Gao Y, Wang Y, Zhan Q, Feng H, Luo X, Li P, Liu S, Hou H, Gao P. Nat Commun 13 6391 (2022)


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