Promiscuous restriction is a cellular defense strategy that confers fitness advantage to bacteria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 20, 2012, Pages

  Vasu, Kommireddy ^a   Nagamalleswari, Easa ^a   Nagaraja, Valakunja ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

DNA cleavage; Evolution; Genome protection; KpnI; Promiscuous activity

Indexed keywords

BACTERIAL DNA; KPNI PROTEIN; MUTANT PROTEIN; RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIOPHAGE; CATALYSIS; CONTROLLED STUDY; DNA CLEAVAGE; DNA RESTRICTION; DNA SEQUENCE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; IN VIVO STUDY; KLEBSIELLA PNEUMONIAE; MOLECULAR RECOGNITION; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN METABOLISM;

BACTERIOPHAGES; BIOLOGICAL EVOLUTION; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA RESTRICTION-MODIFICATION ENZYMES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GENETIC FITNESS; HOST-PATHOGEN INTERACTIONS; KLEBSIELLA PNEUMONIAE; OLIGONUCLEOTIDES;

BACTERIA (MICROORGANISMS);

EID: 84861211375     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1119226109     Document Type: Article

References (58)

1. Khersonsky O, Roodveldt C, Tawfik DS (2006) Enzyme promiscuity: Evolutionary and mechanistic aspects. Curr Opin Chem Biol 10:498-508. (Pubitemid 44375065)
2. Jensen RA (1976) Enzyme recruitment in evolution of new function. Annu Rev Microbiol 30:409-425.
3. O'Brien PJ, Herschlag D (1999) Catalytic promiscuity and the evolution of new enzymatic activities. Chem Biol 6:R91-R105. (Pubitemid 29368405)
4. Aharoni A, et al. (2005) The 'evolvability' of promiscuous protein functions. Nat Genet 37:73-76. (Pubitemid 40070942)
5. Yoshikuni Y, Ferrin TE, Keasling JD (2006) Designed divergent evolution of enzyme function. Nature 440:1078-1082.
6. Zhu Z, et al. (2009) Patent US 2009/0029376 A1.
7. Khersonsky O, Tawfik DS (2010) Enzyme promiscuity: A mechanistic and evolutionary perspective. Annu Rev Biochem 79:471-505.
8. Pingoud A, Fuxreiter M, Pingoud V, Wende W (2005) Type II restriction endonucleases: Structure and mechanism. Cell Mol Life Sci 62:685-707.
9. ArberW, Linn S (1969) DNA modification and restriction. Annu Rev Biochem 38:467-500.
10. Tock MR, Dryden DTF (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466-472. (Pubitemid 41021909)
11. Cowan JA, ed (2004) Role of Metal Ions in Promoting DNA Binding and Cleavage by restriction Endonucleases (Springer, Berlin), pp 339-360.
12. Thielking V, Alves J, Fliess A, Maass G, Pingoud A (1990) Accuracy of the EcoRI restriction endonuclease: Binding and cleavage studies with oligodeoxynucleotide substrates containing degenerate recognition sequences. Biochemistry 29:4682-4691. (Pubitemid 20172686)
13. Sapienza PJ, Dela Torre CA, McCoy, WH, 4th, Jana SV, Jen-Jacobson L (2005) Thermodynamic and kinetic basis for the relaxed DNA sequence specificity of "promiscuous" mutant EcoRI endonucleases. J Mol Biol 348:307-324. (Pubitemid 40462098)
14. Chandrashekaran S, Saravanan M, Radha DR, 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. (Pubitemid 39577777)
15. Saravanan M, Vasu K, Kanakaraj R, Rao DN, Nagaraja V (2007) R.KpnI, an HNH superfamily REase, exhibits differential discrimination at non-canonical sequences in the presence of Ca2+ and Mg2+. Nucleic Acids Res 35:2777-2786. (Pubitemid 47073688)
16. Cowan JA (2002) Structural and catalytic chemistry of magnesium-dependent enzymes. Biometals 15:225-235.
17. SaravananM, Vasu K, Nagaraja V (2008) Evolution of sequence specificity in a restriction endonuclease by a point mutation. Proc Natl Acad Sci USA 105:10344-10347.
18. Alatossava T, Jütte H, Kuhn A, Kellenberger E (1985) Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187. J Bacteriol 162:413-419. (Pubitemid 15095883)
19. Arber W (1965) Host specificity of DNA produced by Escherichia coli V. The role of methionine in the production of host specificity. J Mol Biol 11:247-256.
20. Bickle TA, Krüger DH (1993) Biology of DNA restriction. Microbiol Rev 57:434-450. (Pubitemid 23170101)
21. Krüger DH, Barcak GJ, Smith HO (1988) Abolition of DNA recognition site resistance to the restriction endonuclease EcoRII. Biomed Biochim Acta 47:K1-K5.
22. Wilson GG, Murray NE (1991) Restriction and modification systems. Annu Rev Genet 25:585-627. (Pubitemid 21903734)
23. Chatterjee DK, Hammond AW, Blakesley RW, Adams SM, Gerard GF (1991) Genetic organization of theKpnI restriction-modificationsystem. Nucleic Acids Res 19:6505-6509.
24. Hawley DK, McClure WR (1983) Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res 11:2237-2255.
25. Chandrashekaran S, Babu P, Nagaraja V (1999) Characterization of DNA binding activities of over-expressed kpnI restriction endonuclease and modification methylase. J Biosci 24:269-277. (Pubitemid 29426006)
26. Asakura Y, Kobayashi I (2009) From damaged genome to cell surface: Transcriptome changes during bacterial cell death triggered by loss of a restriction-modification gene complex. Nucleic Acids Res 37:3021-3031.
27. Keatch SA, Leonard PG, Ladbury JE, Dryden DTF (2005) StpA protein from Escherichia coli condenses supercoiled DNA in preference to linear DNA and protects it from digestion by DNase I and EcoKI. Nucleic Acids Res 33:6540-6546. (Pubitemid 41806418)
28. Makovets S, Powell LM, Titheradge AJ, Blakely GW, Murray NE (2004) Is modification sufficient to protect a bacterial chromosome from a resident restriction endonuclease? Mol Microbiol 51:135-147. (Pubitemid 38031077)
29. Dillon SC, Dorman CJ (2010) Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8:185-195.
30. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749-790. (Pubitemid 14059150)
31. Pingoud A, et al. (1984) Effect of polyamines and basic proteins on cleavage of DNA by restriction endonucleases. Biochemistry 23:5697-5703. (Pubitemid 15189721)
32. Tabor CW, Tabor H (1976) 1,4-Diaminobutane (putrescine), spermidine, and spermine. Annu Rev Biochem 45:285-306.
33. Jeltsch A, Urbanke C (2004) Sliding or hopping? How restriction enzymes find their way on DNA restriction endonucleases. Nucleic Acids and Molecular Biology, ed Pingoud AM (Springer, Berlin), Vol 14, pp 95-110.
34. Gowers DM, Halford SE (2003) Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J 22:1410-1418. (Pubitemid 36362704)
35. Bickle TA (2004) Restricting restriction. Mol Microbiol 51:3-5.
36. Zheng Y, et al. (2010) A unique family of Mrr-like modification-dependent restriction endonucleases. Nucleic Acids Res 38:5527-5534.
37. Chinen A, Naito Y, Handa N, Kobayashi I (2000) Evolution of sequence recognition by restriction-modification enzymes: Selective pressure for specificity decrease. Mol Biol Evol 17:1610-1619.
38. Karlin S, Mrázek J, Campbell AM (1997) Compositional biases of bacterial genomes and evolutionary implications. J Bacteriol 179:3899-3913. (Pubitemid 27259908)
39. Blaisdell BE, Campbell AM, Karlin S (1996) Similarities and dissimilarities of phage genomes. Proc Natl Acad Sci USA 93:5854-5859. (Pubitemid 26190767)
40. Gelfand MS, Koonin EV (1997) Avoidance of palindromic words in bacterial and archaeal genomes: A close connection with restriction enzymes. Nucleic Acids Res 25: 2430-2439. (Pubitemid 27303704)
41. Sharp PM (1986) Molecular evolution of bacteriophages: Evidence of selection against the recognition sites of host restriction enzymes. Mol Biol Evol 3:75-83.
42. Warren RA(1980)Modified bases in bacteriophage DNAs. Annu RevMicrobiol 34:137-158.
43. SwintonD, et al. (1983) Purification and characterization of the unusual deoxynucleoside, alpha-N-(9-beta-D-2′-deoxyribofuranosylpurin-6-yl) glycinamide, specified by the phage Mu modification function. Proc Natl Acad Sci USA 80:7400-7404. (Pubitemid 14178010)
44. Brouns SJ, et al. (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960-964.
45. Cardinale CJ, et al. (2008) Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science 320:935-938. (Pubitemid 351929589)
46. Horvath P, et al. (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190:1401-1412. (Pubitemid 351215023)
47. Dorman CJ (2009) Nucleoid-associated proteins and bacterial physiology. Adv Appl Microbiol 67:47-64.
48. Luijsterburg MS, White MF, van Driel R, Dame RT (2008) The major architects of chromatin: Architectural proteins in bacteria, archaea and eukaryotes. Crit Rev Biochem Mol Biol 43:393-418.
49. Keatch SA, Su TJ, Dryden DTF (2004) Alleviation of restriction by DNA condensation and non-specific DNA binding ligands. Nucleic Acids Res 32:5841-5850. (Pubitemid 39619167)
50. Cromie GA, Leach DR (2001) Recombinational repair of chromosomal DNA doublestrand breaks generated by a restriction endonuclease. Mol Microbiol 41:873-883. (Pubitemid 34208996)
51. Heitman J, Zinder ND, Model P (1989) Repair of the Escherichia coli chromosome after in vivo scission by the EcoRI endonuclease. Proc Natl Acad Sci USA 86:2281-2285. (Pubitemid 19102492)
52. Smith MD, Longo M, Gerard GF, Chatterjee DK (1992) Cloning and characterization of genes for the PvuI restriction and modification system. Nucleic Acids Res 20:5743-5747.
53. Tímár E, Venetianer P, Kiss A (2008) In vivo DNA protection by relaxed-specificity SinI DNA methyltransferase variants. J Bacteriol 190:8003-8008.
54. Wei H, Therrien C, Blanchard A, Guan S, Zhu Z (2008) The Fidelity Index provides a systematic quantitation of star activity of DNA restriction endonucleases. Nucleic Acids Res 36:e50.
55. Murray IA, Stickel SK, Roberts RJ (2010) Sequence-specific cleavage of RNA by Type II restriction enzymes. Nucleic Acids Res 38:8257-8268.
56. Lagerbäck P, Andersson E, Malmberg C, Carlson K (2009) Bacteriophage T4 endonuclease II, a promiscuous GIY-YIG nuclease, binds as a tetramer to two DNA substrates. Nucleic Acids Res 37:6174-6183.
57. Osuna R, Finkel SE, Johnson RC (1991) Identification of two functional regions in Fis: The N-terminus is required to promote Hin-mediated DNA inversion but not lambda excision. EMBO J 10:1593-1603. (Pubitemid 21905625)
58. Joseph N, Sawarkar R, Rao DN (2004) DNA mismatch correction in Haemophilus influenzae: Characterization of MutL, MutH and their interaction. DNA Repair (Amst) 3:1561-1577. (Pubitemid 39335689)