Evidence that the insertion events of IS2 transposition are biased towards abrupt compositional shifts in target DNA and modulated by a diverse set of culture parameters

Applied Microbiology and Biotechnology

Volumn 98, Issue 15, 2014, Pages 6609-6619

  Gonçalves, Geisa A L ^a,g   Oliveira, Pedro H ^b,c   Gomes, Ana G ^d   Prather, Kristala L J ^e,g   Lewis, Leslie A ^f   Prazeres, Duarte M F ^a,g   Monteiro, Gabriel A ^a,g  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^b INSTITUT PASTEUR   (France)

^c CNRS   (France)

^d INSTITUTO POLITÉCNICO DE SETÚBAL   (Portugal)

^e Massachusetts Institute of Technology Cambridge   (United States)

^f CITY UNIVERSITY OF NEW YORK   (United States)

^g MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Bacteria; Biopharmaceuticals; Culture growth; GC skew; Genetic instability; Insertion sequence

Indexed keywords

BACTERIA; BIOLOGY; BIOTECHNOLOGY;

BIOPHARMACEUTICALS; CULTURE GROWTH; GC SKEW; GENETIC INSTABILITY; INSERTION SEQUENCES;

DNA;

BACTERIAL DNA; PLASMID DNA; MINICIRCLE DNA; TRANSPOSON; VIRUS DNA;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; CONTROLLED STUDY; CULTURE TECHNIQUE; DNA CONFORMATION; DNA STRUCTURE; DNA TRANSPOSITION; ESCHERICHIA COLI; GENE AMPLIFICATION; GENE INSERTION; GENE INSERTION SEQUENCE; GENE TARGETING; GFP GENE; GROWTH CURVE; NONHUMAN; PLASMID; REPORTER GENE; BACTERIOPHAGE; CELL DENSITY; CULTURE MEDIUM; GENE SWITCHING; GENE EXPRESSION REGULATION; GENETICS; TRANSPOSON;

BACTERIUM; BIOASSAY; DNA; DRUG; GENE; GENETIC ANALYSIS; PLASMID; RECOMBINATION;

BACTERIOPHAGES; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; DNA, VIRAL; ESCHERICHIA COLI; MUTAGENESIS, INSERTIONAL; PLASMIDS;

EID: 84905023433     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5695-6     Document Type: Article

References (61)

1. Azzoni AR, Ribeiro SC, Monteiro GA, Prazeres DMF (2007) The impact of polyadenylation signals on plasmid nuclease-resistance and transgene expression. J Gene Med 9:392-402. doi:10.1002/jgm.1031 (Pubitemid 46796585)
2. Bernard N, Ferain T, Garmyn D, Hols P, Delcour J (1991) Cloning of the D-lactate dehydrogenase gene from Lactobacillus delbrueckii subsp. bulgaricus by complementation in Escherichia coli. FEBS Lett 290(1-2):61-64. doi:10.1016/0014-5793(91)81226-X
3. Boyd AC, Popp F, Michaelis U, Davidson H, Davidson-Smith H, Doherty A, McLachlan G, Porteous DJ, Seeber S (1999) Insertion of natural intron 6a-6b into a human cDNA-derived gene therapy vector for cystic fibrosis improves plasmid stability and permits facile RNA/DNA discrimination. J Gene Med 1(5): 312-321. doi: 10.1002/(SICI)1521-2254(199909/10)1:5<312::AID
4. Brukner I, Sànchez R, Suck D, Pongor S (1995) Sequence-dependent bending propensity of DNA as revealed by DNase I: parameters for trinucleotides. EMBO J 14(1812-1818)
5. Carnes AE, Hodgson CPA,Williams J (2006) Inducible Escherichia coli fermentation for increased plasmid DNA production. Biotechnol Appl Biochem 45:155-166. doi:10.1042/BA20050223 (Pubitemid 44690220)
6. Chandler M, Mahillon J (2002) Insertion sequences revisited. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. ASM Press, Washington DC, pp 305-366
7. Cohen SP, Hachler H, Levy SB (1993) Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J Bacteriol 175(5):1484-1492. doi:10.1053/rvsc.2001.0537 (Pubitemid 23081826)
8. Cress WD, Nevins JR (1996) A role for a bent DNA structure in E2F-mediated transcription activation. Mol Cell Biol 16(5):2119-2127 (Pubitemid 26123732)
9. Du P, Yang Y, Wang H, Liu D, Gao GF, Chen C (2011) A large scale comparative genomic analysis reveals insertion sites for newly acquired genomic islands in bacterial genomes. BMC Microbiol 11:135. doi:10.1186/1471-2180-11-135
10. Eichenbaum Z, Livneh Z (1998) UV light induces IS10 transposition in Escherichia coli. Genetics 149(3):1173-1181 (Pubitemid 28334515)
11. Gabrielian A, Vlahovicek K, Pongor S (1997) Distribution of sequence-dependent curvature in genomic DNA sequences. FEBS Lett 406(1-2):69-74. doi:10.1016/S0014-5793(97)00236-6 (Pubitemid 27156960)
12. Gaffe J, McKenzie C, Maharjan RP, Coursange E, Ferenci T, Schneider D (2011) Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 72(4):398-412. doi:10.1007/s00239-011-9439-2
13. Gamas P, Chandler MG, Prentki P, Galas DJ (1987) Escherichia coli integration host factor binds specifically to the ends of the insertion sequence IS1 and to its major insertion hot-spot in pBR322. J Mol Biol 195(2):261-272. doi:10.1016/0022-2836(87)90648-6 (Pubitemid 17106690)
14. Gimenes F, Takeda KI, Fiorini A, Gouveia FS, Fernandez MA (2008) Intrinsically bent DNA in replication origins and gene promoters. Genet Mol Res 7(2):549-558
15. Gomez-Gomez JM, Blazquez J, Baquero F, Martinez JL (1997) H-NS and RpoS regulate emergence of Lac Ara+mutants of Escherichia coli MCS2. J Bacteriol 179(14):4620-4622 (Pubitemid 27299081)
16. Guynet C, Achard A, Hoang BT, Barabas O, Hickman AB, Dyda F, Chandler M (2009) Resetting the site: redirecting integration of an insertion sequence in a predictable way. Mol Cell 34(5):612-619. doi:10.1016/j.molcel.2009.05.017
17. Hallet B, Rezsohazy R, Mahillon J, Delcour J (1994) IS231A insertion specificity - consensus sequence and DNA bending at the target site. MolMicrobiol 14(1):131-139. doi:10.1111/j.1365-2958.1994.tb01273.x (Pubitemid 24312826)
18. Hirsch HJ, Starlinger P, Brachet P (1972) Two kinds of insertions in bacterial genes. Mol General Genet 119(3):191-206. doi:10.1007/BF00333858
19. Ilves H, Horak R, Kivisaar M (2001) Involvement of sigma(S) in starvation-induced transposition of Pseudomonas putida transposon Tn4652. J Bacteriol 183(18):5445-5448. doi:10.1128/JB.183.18.5445-5448.2001 (Pubitemid 32802620)
20. Kharat AS, Coursange E, Noirclerc-Savoye M, Lacoste J, BlotM(2006) IS1 transposition is enhanced by translation errors and by bacterial growth at extreme glucose levels. Acta Biochimica Polonica 53(4):729-738 (Pubitemid 46090120)
21. Kobori S, Ko Y, KatoM(2009) A target site for spontaneous insertion of IS10 element in pUC19DNA located within intrinsically bent DNA. Open Microbiol J 3:146-150. doi:10.2174/1874285800903010146
22. Kolter R, Siegele DA, Tormo A (1993) The stationary phase of the bacterial life cycle. Annual Review of Microbiology 47:855-874. doi:10.1146/annurev.mi.47.100193.004231 (Pubitemid 23302955)
23. Kusakabe T, Sugimoto Y, Maeda T, Nakajima Y, Miyano M, Nishikawa J, Tone S, Kawaguchi Y, Koga K, Ohyama T (2001) Linearization and integration of DNA into cells preferentially occurs at intrinsically curved regions from human LINE-1 repetitive element. Gene 274(1-2):271-281. doi:10.1016/S0378-1119(01) 00631-X (Pubitemid 32817145)
24. Lewis LA, Grindley ND (1997) Two abundant intramolecular transposition products, resulting from reactions initiated at a single end, suggest that IS2 transposes by an unconventional pathway. Mol Microbiol 25(3):517-529. doi:10.1046/j.1365-2958.1997.4871848.x (Pubitemid 27373580)
25. Lewis LA, Gopaul S, Marsh C (1994a) The non-random pattern of insertion of IS2 into the hemB gene of Escherichia coli. Microbiol Immunol 38(6):461-465. doi:10.1111/j.1348-0421.1994.tb01808.x (Pubitemid 24234768)
26. Lewis LA, Lewis D, Persaud V, Gopaul S, Turner B (1994b) Transposition of IS2 into the hemB gene of Escherichia coli K-12. J Bacteriol 176(7):2114-2120 (Pubitemid 24103566)
27. Lewis LA, Gadura N, Greene M, Saby R, Grindley ND (2001) The basis of asymmetry in IS2 transposition. Mol Microbiol 42(4):887-901. doi:10.1046/j.1365-2958.2001.02662.x (Pubitemid 33078374)
28. Lewis LA, Cylin E, Lee HK, Saby R, Wong W, Grindley ND (2004) The left end of IS2: a compromise between transpositional activity and an essential promoter function that regulates the transposition pathway. J Bacteriol 186(3):858-865. doi:10.1128/JB.186.3.858-865. 2004 (Pubitemid 38129665)
29. Lewis LA, Astatke M, Umekubo PT, Alvi S, Saby R, Afrose J (2011) Soluble expression, purification and characterization of the full length IS2 transposase. Mob DNA 2:14. doi:10.1186/1759-8753-2-14
30. Lewis LA, Astatke M, Umekubo PT, Alvi S, Saby R, Afrose J, Oliveira PH, Monteiro GA, Prazeres DM (2012) Protein-DNA interactions define the mechanistic aspects of circle formation and insertion reactions in IS 2 transposition. Mob DNA 3(1):1. doi:10.1186/1759-8753-3-1
31. Listner K, Bentley LK, Chartrain M (2006) A simple method for the production of plasmid DNA in bioreactors. Meth Mol Med 127:295-309. doi:10.1385/1-59745-168-1:295
32. Muller HP, Varmus HE (1994) DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes. EMBO J 13(19):4704-4714
33. Nagy Z, Chandler M (2004) Regulation of transposition in bacteria. Res Microbiol 155(5):387-398. doi:10.1016/j.resmic.2004.01.008 (Pubitemid 38786466)
34. Oliveira PH, Prather KJ, Prazeres DM, Monteiro GA (2009a) Structural instability of plasmid biopharmaceuticals: challenges and implications. Trends Biotechnol 27(9):503-511. doi:10.1016/j.tibtech.2009.06.004
35. Oliveira PH, Prazeres DM, Monteiro GA (2009b) Deletion formation mutations in plasmid expression vectors are unfavored by runaway amplification conditions and differentially selected under kanamycin stress. J Biotechnol 143(4):231-238. doi:10.1016/j.jbiotec.2009.08.002
36. Oliveira PH, Prazeres DM, Monteiro GA (2012) Structural and segregational instability in plasmid biology. In: Gonzalez FER, Lopez MI (ed) Plasmids: genetics, applications and health. Nova Publishers, NY, pp. 79-100
37. Pedersen AG, Baldi P, Chauvin Y, Brunak S (1998) DNA structure in human RNA polymerase II promoters. J Mol Biol 281(4):663-673. doi:10.1006/jmbi.1998. 1972 (Pubitemid 28383138)
38. Polard P, Prere MF, Chandler M, Fayet O (1991) Programmed translational frameshifting and initiation at an AUU codon in gene expression of bacterial insertion sequence IS911. J Mol Biol 222(3):465-477. doi:10.1016/0022-2836(91) 90490-W
39. Porollo AA, Adamczak R, Meller J (2004) POLYVIEW: a flexible visualization tool for structural and functional annotations of proteins. Bioinformatics 20(15):2460-2462. doi:10.1093/bioinformatics/bth248 (Pubitemid 39429919)
40. Prather KL, Edmonds MC, Herod JW (2006) Identification and characterization of IS1 transposition in plasmid amplification mutants of E. coli clones producing DNA vaccines. Appl Microbiol Biotechnol 73(4):815-826. doi:10.1007/s00253-006-0532-1 (Pubitemid 44833028)
41. Pribil PA, Haniford DB (2003) Target DNA bending is an important specificity determinant in target site selection in Tn10 transposition. J Mol Biol 330(2):247-259. doi:10.1016/S0022-2836(03)00588-6 (Pubitemid 36773699)
42. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16(6):276-277. doi:10.1016/S0168- 9525(00)02024-2
43. Rijavec M, Budic M, Mrak P, Muller-Premru M, Podlesek Z, Zgur-Bertok D (2007) Prevalence of ColE1-like plasmids and colicin K production among uropathogenic Escherichia coli strains and quantification of inhibitory activity of colicin K. Appl Environ Microbiol 73(3):1029-1032. doi:10.1128/AEM.01780-06 (Pubitemid 46233527)
44. Schneeberger RG, Zhang K, Tatarinova T, Troukhan M, Kwok SF, Drais J, Klinger K, Orejudos F,Macy K, Bhakta A, Burns J, Subramanian G, Donson J, Flavell R, Feldmann KA (2005) Agrobacterium TDNA integration in Arabidopsis is correlated with DNA sequence compositions that occur frequently in gene promoter regions. Funct Integr Genomics 5(4):240-253. doi:10.1007/s10142-005-0138-1 (Pubitemid 41435175)
45. Sekine Y, Eisaki N, Ohtsubo E (1994) Translational control in production of transposase and in transposition of insertion sequence IS3. J Mol Biol 235(5):1406-1420. doi:10.1006/jmbi.1994.1097 (Pubitemid 24150395)
46. Sengstag C, Arber W (1983) IS2 insertion is a major cause of spontaneous mutagenesis of the bacteriophage P1: non-random distribution of target sites. EMBO J 2(1):67-71
47. Sengstag C, Arber W (1987) A cloned DNA fragment from bacteriophage P1 enhances IS2 insertion. Mol General Genet 206(2):344-351. doi:10.1007/BF00333593 (Pubitemid 17013202)
48. Sengstag C, Shepherd JC, Arber W (1983) The sequence of the bacteriophage P1 genome region serving as hot target for IS2 insertion. EMBO J 2(10):1777-1781
49. Studier FW, Daegelen P, Lenski RE, Maslov S, Kim JF (2009) Understanding the differences between genome sequences of Escherichia coli B strains REL606 and BL21(DE3) and comparison of the E. coli B and K-12 genomes. JMol Biol 394(4):653-680. doi:10.1016/j.jmb.2009.09.021
50. 2 intermediate. Mol General Genet 251(3):281-289. doi:10.1007/BF02172518
51. Szeverenyi I, Hodel A, Arber W, Olasz F (1996b) Vector for IS element entrapment and functional characterization based on turning on expression of distal promoterless genes. Gene 174(1):103-110. doi:10.1016/0378-1119(96)00407-6 (Pubitemid 26326857)
52. Twiss E, Coros AM, Tavakoli NP, Derbyshire KM (2005) Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol Microbiol 57(6):1593-1607. doi:10.1111/j.1365-2958. 2005.04794.x (Pubitemid 41337389)
53. van der Heijden I, Gomez-Eerland R, van den Berg JH, Oosterhuis K, Schumacher TN, Haanen JB, Beijnen JH, Nuijen B (2013) Transposon leads to contamination of clinical pDNA vaccine. Vaccine 31(32):3274-3280. doi:10.1016/j.vaccine.2013.05.022
54. Vivas P, Velmurugu Y, Kuznetsov SV, Rice PA, Ansari A (2012) Mapping the transition state for DNA bending by IHF. J Mol Biol 418(5):300-315. doi:10.1016/j.jmb.2012.02.028
55. Vlahovicek K, Kajan L, Pongor S (2003) DNA analysis servers: plot.it, bend.it, model.it and IS. Nucleic Acids Res 31(13):3686-3687 (Pubitemid 37442223)
56. Vogele K, Schwartz E, Welz C, Schiltz E, Rak B (1991) High-level ribosomal frameshifting directs the synthesis of IS150 gene products. Nucleic Acids Res 19(16):4377-4385. doi:10.1093/nar/gkg559 (Pubitemid 21912813)
57. Weber H, Polen T, Heuveling J, Wendisch VF, Hengge R (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J Bacteriol 187(5):1591-1603. doi:10.1128/JB.187.5.1591-1603.2005 (Pubitemid 40289359)
58. Whiteway J, Koziarz P, Veall J, Sandhu N, Kumar P, Hoecher B, Lambert IB (1998) Oxygen-insensitive nitroreductases: analysis of the roles of nfsA and nfsB in development of resistance to 5-nitrofuran derivatives in Escherichia coli. J Bacteriol 180(21):5529-5539 (Pubitemid 28489842)
59. Yang S, Sleight SC, Sauro HM (2013) Rationally designed bidirectional promoter improves the evolutionary stability of synthetic genetic circuits. Nucleic Acids Res 41(1):e33. doi:10.1093/nar/gks972
60. Zhang Z, Saier MH Jr (2009) A novel mechanism of transposon-mediated gene activation. PLoS Genet 5(10):e1000689. doi:10.1371/journal.pgen.1000689
61. Zhang J, Guo D, Chang Y, You C, Li X, Dai X,Weng Q, Zhang J, Chen G, Li X, Liu H, Han B, Zhang Q, Wu C (2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13 804 T-DNA flanking sequences from an enhancer-trap mutant library. Plant J 49(5):947-959. doi:10.1111/j.1365-313X.2006.03001.x (Pubitemid 46279276) a Tecnologia