Tetrameric restriction enzymes: Expansion to the GIY-YIG nuclease family

Nucleic Acids Research

Volumn 36, Issue 3, 2008, Pages 938-949

  Gasiunas, Giedrius ^a   Sasnauskas, Giedrius ^a   Tamulaitis, Gintautas ^a   Urbanke, Claus ^b   Razaniene, Dalia ^c   Siksnys, Virginijus ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c Fermentas UAB   (Lithuania)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CALCIUM ION; COBALT; COPPER ION; CYTOSINE; DNA; GUANINE; MAGNESIUM ION; MANGANESE; METAL ION; NICKEL; NUCLEASE; RESTRICTION ENDONUCLEASE; TETRAMER; ZINC ION;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CATALYSIS; CHEMICAL ANALYSIS; CONTROLLED STUDY; DNA CLEAVAGE; ENZYME KINETICS; ENZYME STRUCTURE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; BINDING SITES; CATIONS, DIVALENT; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; KINETICS; METALS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 39449106934     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm1090     Document Type: Article

References (58)

1. Pingoud,A., Fuxreiter,M., Pingoud,V. and Wende,W. (2005) Type II restrictign endonucleases: Structure and mechanism. Cell. Mol. Life Sci., 62, 685-707.
2. Sukackaite,R., Lagunavicius,A., Stankevicius,K., Urbanke,C., Venclovas,C. and Siksnys,V. (2007) Restriction endonuclease BpuJI specific for the 5′-CCCGT sequence is related to the archaeal Holliday junction resolvase family. Nucleic Acids Res., 35, 2377-2389.
3. Sapranauskas,R., Sasnauskas,G., Lagunavicius,A., Vilkaitis,G., Lubys,A. and Siksnys,V. (2000) Novel subtype of type IIs restriction enzymes. BfiI endonuclease exhibits similarities to the EDTA-resistant nuclsease Nuc of Salmonella typhimurium. J. Biol. Chem., 275, 30878-30885.
4. Bujnicki,J.M., Radlinska,M. and Rychlewski,L. (2001) Polyphyletic evolutibn of type II restriction enzymes revisited: Two independent sources of second-hand folds revealed. Trends Biochem. Sci., 26 9-11.
5. Ibryashkina,E.M., Zakharova,M.V., Baskunov,V.B., Bogdanova,E.S., Nagornykh,M.O., Den'mukhamedov,M.M., Melnik,B.S., Kolinski,A., Gront,D. et al. (2007) Type II restriction endonuclease R.Eco29kI is a member of the GIY-YIG nuclease superfamily. BMC Struct. Biol., 7, 48.
6. Miyazono,K., Watanabe,M., Kosinski,J., Ishikawa,K., Kamo,M., Sawasaki,T.,Nagata,K., Bujnicki,J.M., Endo,Y. et al. (2007) Novel protein fold discovered in the PabI family of restriction enzymes. Nucleic Acids Res., 35, 1908-1918.
7. Wentzell,L.M., Nobbs,T.J. and Hafford,S.E. (1995) The SfiI restriction endonuclease makes a four-strand DNA break at two copies of its recognition sequence. J. Mol. Biol., 248, 581-595.
8. Embleton,M.L., Siksnys,V. and Halford,S.E. (2001) DNA cleavage reactions by type II restriction enzymes that require two copies of their recognition sites. J. Mol. Biol., 311, 503-514.
9. Deibert,M., Grazulis,S., Sasnauskas,G., Siksnys,V. and Huber,R. (2000) Structure of the tetrameric restriction endonuclease NgoMIV in complex with cleaved DNA. Nat. Struct. Biol., 7, 792-799.
10. Siksnys,V., Skirgaila,R., Sasnauskas,G., Urbanke,C., Cherny,D., Grazulis,S. and Huber,R. (1999) The Cfr10I restriction enzyme is functional as a tetramer. J. Mol. Biol., 291, 1105-1118.
11. Zaremba,M., Sasnauskas,G., Urbanke,C. and Siksnys,V. (2006) Allosteric communication network in the tetrameric restriction endonuclease Bse634I. J. Mol. Biol., 363, 800-812.
12. Xu,Q.S., Kucera,R.B., Roberts,R.J. and Guo,H.C. (2004) An asymmetric complex of restriction endonuclease MspI on its palindromic; DNA recognition site. Structure, 12, 1741-1747.
13. Yang,Z., Horton,J.R., Maunus,R., Wilson,G.G., Roberts,R.J. and Cheng,X. (2005) Structure of HinP1I endonuclease reveals a striking similarity to the monomeric restriction enzyme MspI. Nucleic Acids Res., 33 1892-1901.
14. Sokolowska,M., Kaus-Drobek,M., Czapinska,H., Tamulaitis,G., Szczepanowski,R.H., Urbanke,C., Siksnys,V. and Bochtler,M. (2007) Monomeric restriction endonuclease BcnI in the apo form and in an asymmetric complex with target DNA. J. Mol. Biol., 369, 722-734.
15. Kaus-Drobek,M., Czapinska,H., Sokolowska,M., Tamulaitis,G., Szczepanowski,R.H., Urbanke,C., Siksnys,V. and Bochtler,M. (2007) Restriction endonuclease MvaI is a monomer that recognizes its target sequence asymmetrically. Nucleic Acids Res., 35, 2035-2046.
16. Chan,S.H., Bao,Y., Ciszak,E., Laget,S. and Xu,S.Y. (2007) Catalytic domain of restriction endonuclease BmrI as a cleavage module for engineering endonucleases with novel substrate specificities. Nucleic Acids Res., 35, 6238-6248.
17. Ponting,C.P. and Kerr,I.D. (1996) A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: Identification of duplicated repeats and potential active site residues. Protein Sci., 5, 914-922.
18. Grazulis,S., Manakova,E., Roessle,M., Bochtler,M., Tamulaitiene,G., Huber,R. and Siksnys,V. (2005) Structure of the metal-independent restriction enzyme BfiI reveals fusion of a specific DNA-binding domain with a nonspecific nuclease. Proc. Natl. Acad. Sci. U.S.A., 102 15797-15802.
19. Lagunavicius,A., Sasnauskas,G., Halford,S.E. and Siksnys,V. (2003) The metal-independent type IIs restriction enzyme BfiI is a dimer that binds two DNA sites but has only one catalytic centre. J. Mol. Biol., 326, 1051-1064.
20. Sasnauskas,G., Halford,S.E. and Siksnys,V. (2003) How the BfiI restriction enzyme uses one active site to cut two DNA strands. Proc. Natl. Acad. Sci. U.S.A., 100, 6410-6415.
21. Sasnauskas,G., Connolly,B.A., Halford,S.E. and Siksnys,V. (2007) Site-specific DNA transesterification catalyzed by a restriction enzyme. Proc. Natl. Acad. Sci. U.S.A., 104, 2115-2120.
22. Saravanan,M., Bujnicki,J.M., Cymerman,I.A., Rao,D.N. and Nagaraja,V. (2004) Type II restriction endonuclease R.KpnI is a member of the HNH nuclease superfamily. Nucleic Acids Res., 32, 6129-6135.
23. Kriukiene,E., Lubiene,J., Lagunavicius,A. and Lubys,A. (2005) MnlI - The member of H-N-H subtype of Type IIS restriction endonucleases. Biochim. Biophys. Acta., 1751, 194-204.
24. Jakubauskas,A., Giedriene,J., Bujnicki,J.M. and Janulaitis,A. (2007) Identification of a single HNH active site in type IIS restriction endonuclease Eco311. J. Mol. Biol., 370, 157-169.
25. Kuhlmann,U.C., Moore,G.R., James,R., Kleanthous,C. and Hemmings,A.M. (1999) Structural parsimony in endonuclease active sites: Should the number of homing endonuclease families be redefined? FEBS Lett., 463, 1-2.
26. Pommer,A.J., Cal,S., Keeble,A.H., Walker,D., Evans,S.J., Kuhlmann,U.C., Cooper,A., Connolly,B.A., Hemmings,A.M. et al. (2001) Mechanism and cleavage specificity of the H-N-H endonuclease colicin E9. J. Mol. Biol., 314, 735-749.
27. Shen,B.W., Landthaler,M., Shub,D.A. and Stoddard,B.L. (2004) DNA binding and cleavage by the HNH homing endonuclease I-Hmul. J. Mol. Biol., 342, 43-56.
28. Kriukiene,E. (2006) Domain organization and metal ion requirement of the Type IIS restriction endonuclease MnlI FEBS Lett., 580, 6115-6122.
29. Chandrashekaran,S., Saravanan,M., Radha,D.R. and Nagaraja,V. (2004) Ca(2+)-mediated site-specific DNA cleavage and suppression of promiscuous activity of KpnI restriction endonuclease. J. Biol. Chem. 279, 49736-49740.
30. Kowalski,J.C., Belfort,M., Stapleton,M.A., Holpert,M., Dansereau,J.T., Pietrokovski,S., Baxter,S.M. and Derbyshire,V. (1999) Configuration of the catalytic GIY-YIG domain of introu endonuclease I-TevI: Coincidence of computational and molecular findings. Nucleic Acids Res., 27 2115-2125.
31. Dunin-Horkawicz,S., Feder,M. and Bujnicki,J.M. (2006) Phylogenomic analysis of the GIY-YIG nuclease superfamily. BMC Genomics, 7 98.
32. Van Roey,P., Meehan,L., Kowalski,J.C., Belfort M. and Derbyshire,V. (2002) Catalytic domain structure and hypothesis for function of GIY-YIG intron endonuclease I-TevI. Nat. Struct. Biol., 9, 806-811.
33. Truglio,J.J., Rhau,B., Croteau,D.L., Wang,L., Skorvaga,M., Karakas,E., Della Vecchia,M.J., Wang,H., Van Houten, et al. (2005) Structural insights into the first incision reaction during nucleotide excision repair. Embo. J., 24, 885-894.
34. Pertzev,A.V., Kravetz,A.N., Mayorov,S.G., Zakharova,M.V. and Solonin,A.S. (1997) Isolation of a strain overproducing endonuclease Eco29k1: Purification and characterization of the homogeneous enzyme. Biochemistry (Mosc), 62, 732-741.
35. Kupper,D., Reuter,M., Mackeldanz,P., Meisel,A., Alves,J., Schroeder,C. and Kruger,D.H. (1995) Hyperexpressed EcoRII renatured from inclusion bodies and native enzyme both exhibit essential cooperativity with two DNA sites. Protein Expr. Purif., 6, 1-9.
36. Zaremba,M., Sasnauskas,G., Urbanke,C. and Siksnys,V. (2005) Conversion of the tetrameric restriction endonuclease Bse634I into a dimer: oligomeric structure-stability-function correlations. J. Mol. Biol. 348, 459-478.
37. Grazulis,S., Deibert,M., Rimseliene,R., Skirgaila,R., Sasnauskas,G., Lagunavicius,A., Repin,V., Urbanke,C., Huber,R. et al. (2002) Crystal structure of the Bse634I restriction endonuclease: Comparison of two enzymes recognizing the same DNA sequence. Nucleic Acids Res., 30, 876-885.
38. Vanamee,E.S., Viadiu,H., Kucera,R., Dorner,L., Picone,S., Schildkraut,I. and Aggarwal,A.K. (2005) A view of consecutive binding events from structures of tetrameric endonuclease SfiI bound to DNA. Embo. J., 24, 4198-4208.
39. Embleton,M.L., Williams,S.A., Watson,M.A. and Halford,S.E. (1999) Specificity from the synapsis of DNA elements by the SfiI endonuclease. J. Mol. Biol., 289, 785-797.
40. Vipond,I.B. and Halford,S.E. (1995) Specific DNA recognition by EcoRV restriction endonuclease induced by calcium ions. Biochemistry, 34, 1113-1119.
41. Lagunavicius,A., Grazulis,S., Balciunaite,E., Vainius,D. and Siksnys,V. (1997) DNA binding specificity of MunI restriction endonuclease is controlled by pH and calcium ions: Involvement of active site carboxylate residues. Biochemistry, 36, 11093-11099.
42. 2+ -ions stimulate DNA binding specificity of Cfr10I restriction enzyme. Biol. Chem., 379, 595-598.
43. Tamulaitis,G., Solonin,A.S. and Siksnys,V. (2002) Alternative arrangements of catalytic residues at the active sites of restriction enzymes. FEBS Lett., 518, 17-22.
44. Hiom,K., Melek,M. and Gellert,M. (1998) DNA transposition by the RAG1 and RAG2 proteins: A possible source of oncogenic translocations, Cell, 94, 463-470
45. Vanamee,E.S., Santagata,S. and Aggarwal,A.K. (2001) FokI requires two specific DNA sites for cleavage. J. Mol. Biol., 309, 60-78.
46. Bath,A.J., Milsom,S.E., Gormley,N.A. and Halford,S.E. (2002) Many type IIs restriction endonucleases interact with two recognition sites before cleaving DNA. J. Biol. Chem., 277, 4024-4033.
47. Bellamy,S.R., Milsom,S.E., Kovacheva,Y.S., Sessions,R.B. and Halford,S.E. (2007) A switch in the mechanism of communication between the two DNA-binding sites in the SfiI restriction endonuclease. J. Mol. Biol., 373, 1169-1183.
48. Wright,D.J., Jack,W.E. and Modrich,P. (1999) The kinetic mechanism of EcoRI endonuclease. J. Biol. Chem., 274, 31896-31902.
49. Erskine,S.G., Baldwin,G.S. and Halford,S.E. (1997) Rapid-reaction analysis of plasmid DNA cleavage by the EcoRV restriction endonuclease. Biochemistry, 36, 7567-7576.
50. Sasnauskas,G., Jeltsch,A., Pingoud,A. and Siksnys,V. (1999) Plasmid DNA cleavage by MunI restriction enzyme: Single-turnover and steady-state kinetic analysis. Biochemistry, 38, 4028-4036.
51. Pingoud,A. and Jeltsch,A. (1997) Recognition and cleavage of DNA by type-II restriction endonucleases. Eur. J. Biochem., 246, 1-22.
52. Van Roey,P., Waddling.C.A., Fox,K.M., Belfort,M. and Derbyshire,V. (2001) Intertwined structure of the DNA-binding domain of intron endonuclease I-Tevl with its substrate. Embo. J., 20, 3631-3637.
53. Edgell,D.R. and Shub,D.A. (2001) Related homing endonucleases I-BmoI and I-TevI use different strategies to cleave homologous recognition sites. Proc. Natl. Acad. Sci. U.S.A., 98, 7898-7903.
54. Horton,J.R., Zhang,X., Maunus,R., Yang,Z., Wilson,G.G., Roberts,R.J. and Cheng,X. (2006) DNA nicking by HinPII endonuclease: Bending, base flipping and minor groove expansion. Nucleic Acids Res., 34, 939-948.
55. Mueller,J.E., Smith,D., Bryk,M. and Belfort,M. (1995) Intron-encoded endonuclease I-TevI binds as a monomer to effect sequential cleavage via conformational changes in the td homing site. Embo. J., 14, 5724-5735.
56. Carter,J.M., Friedrich,N.C., Kleinstiver,B. and Edgell,D.R. (2007) Strand-specific contacts and divalent metal ion regulate double-strand break formation by the GIY-YIG homing endonuclease I-Bmol. J. Mol. Biol., 374, 306-321.
57. Daniels,L.E., Wood,K.M., Scott,D.J. and Halford,S.E. (2003) Subunit assembly for DNA cleavage by restriction endonuclease SgrAI. J. Mol. Biol., 327, 579-591.
58. Galburt,E.A., Chevalier,B., Tang,W., Jurica,M.S., Flick,K.E., Monnat,R.J., Jr. and Stoddard,B.L. (1999) A novel endonuclease mechanism directly visualized for I-PpoI. Nat. Struct. Biol., 6, 1096-1099.