General Information/IS and Gene Expression
Another important aspect of IS impact on their bacterial hosts is their ability to modulate gene expression. In addition to acting as vectors for gene transmission from one replicon to another in the form composite transposons (two IS flanking any gene; Fig.2.3) and tIS (Fig.8.1) and their ability to interrupt genes, it has been known for some time[1][2] that IS can also activate gene expression. This capacity has recently received much attention due to the increase in resistance to various antibacterials[3][4][5], a worrying public health threat[6][7].
They can accomplish this in two ways: either by providing internal promoters whose transcripts escape into neighboring DNA[2][8][9][10] or by hybrid promoter formation. Many IS carry -35 promoter components oriented towards the flanking DNA (Fig.18.1). In a number of cases this plays an important part in their transposition since a significant number of IS transposes using an excised transposon circle (Fig.18.1) with abutted left and right ends. For these IS, the other end carries a -10 element oriented inwards towards the Tpase gene. Together with the -35, this generates a strong promoter on formation of the circle junction to drive Tpase expression required for catalysis of integration (Fig.18.2) [11][12][13][14]. Thus, if integration occurs next to a resident -10 sequence, the IS -35 sequence can contribute to a hybrid promoter to drive expression of neighboring genes [see [15]]. At present, this phenomenon had been reported to occur with over 30 different IS in more than 17 bacterial species[16][17] (Table IS and Gene Expression below). Indeed, specific vector plasmids have been designed to identify activating insertions (e.g. [18]).
IS activity can affect efflux mechanisms resulting in increased resistance: IS1 or IS10 insertion can up-regulate the AcrAB-TolC pump in Salmonella enterica[19]; IS1 or IS2 insertion upstream of AcrEF[20][21] and IS186 insertional inactivation of the AcrAB repressor, AcrR, in Escherichia coli [20], all lead to increased resistance to fluoroquinolones. Insertional inactivation of specific porins can also play a significant role[22].
IS and Gene Expression
Bibliography
- ↑ Reif HJ, Saedler H . IS1 is involved in deletion formation in the gal region of E. coli K12. - Mol Gen Genet: 1975, 137(1);17-28 [PubMed:1101028] [DOI]
- ↑ 2.0 2.1 2.2 2.3 Glansdorff N, Charlier D, Zafarullah M . Activation of gene expression by IS2 and IS3. - Cold Spring Harb Symp Quant Biol: 1981, 45 Pt 1;153-6 [PubMed:6271458] [DOI]
- ↑ 3.0 3.1 Aubert D, Naas T, Héritier C, Poirel L, Nordmann P . Functional characterization of IS1999, an IS4 family element involved in mobilization and expression of beta-lactam resistance genes. - J Bacteriol: 2006 Sep, 188(18);6506-14 [PubMed:16952941] [DOI]
- ↑ 4.0 4.1 Aubert D, Naas T, Nordmann P . IS1999 increases expression of the extended-spectrum beta-lactamase VEB-1 in Pseudomonas aeruginosa. - J Bacteriol: 2003 Sep, 185(17);5314-9 [PubMed:12923109] [DOI]
- ↑ 5.0 5.1 5.2 5.3 5.4 Sóki J, Eitel Z, Urbán E, Nagy E, ESCMID Study Group on Anaerobic Infections . Molecular analysis of the carbapenem and metronidazole resistance mechanisms of Bacteroides strains reported in a Europe-wide antibiotic resistance survey. - Int J Antimicrob Agents: 2013 Feb, 41(2);122-5 [PubMed:23158541] [DOI]
- ↑ McKenna M . Antibiotic resistance: the last resort. - Nature: 2013 Jul 25, 499(7459);394-6 [PubMed:23887414] [DOI]
- ↑ Mole B . MRSA: Farming up trouble. - Nature: 2013 Jul 25, 499(7459);398-400 [PubMed:23887415] [DOI]
- ↑ 8.0 8.1 Charlier D, Piette J, Glansdorff N . IS3 can function as a mobile promoter in E. coli. - Nucleic Acids Res: 1982 Oct 11, 10(19);5935-48 [PubMed:6292860] [DOI]
- ↑ Zafarullah M, Charlier D, Glansdorff N . Insertion of IS3 can "turn-on" a silent gene in Escherichia coli. - J Bacteriol: 1981 Apr, 146(1);415-7 [PubMed:6260746] [DOI]
- ↑ Simons RW, Hoopes BC, McClure WR, Kleckner N . Three promoters near the termini of IS10: pIN, pOUT, and pIII. - Cell: 1983 Sep, 34(2);673-82 [PubMed:6311437] [DOI]
- ↑ Chandler M, Fayet O, Rousseau P, Ton Hoang B, Duval-Valentin G . Copy-out-Paste-in Transposition of IS911: A Major Transposition Pathway. - Microbiol Spectr: 2015 Aug, 3(4); [PubMed:26350305] [DOI]
- ↑ Ton-Hoang B, Bétermier M, Polard P, Chandler M . Assembly of a strong promoter following IS911 circularization and the role of circles in transposition. - EMBO J: 1997 Jun 2, 16(11);3357-71 [PubMed:9214651] [DOI]
- ↑ Perkins-Balding D, Duval-Valentin G, Glasgow AC . Excision of IS492 requires flanking target sequences and results in circle formation in Pseudoalteromonas atlantica. - J Bacteriol: 1999 Aug, 181(16);4937-48 [PubMed:10438765] [DOI]
- ↑ Duval-Valentin G, Normand C, Khemici V, Marty B, Chandler M . Transient promoter formation: a new feedback mechanism for regulation of IS911 transposition. - EMBO J: 2001 Oct 15, 20(20);5802-11 [PubMed:11598022] [DOI]
- ↑ 15.0 15.1 Prentki P, Teter B, Chandler M, Galas DJ . Functional promoters created by the insertion of transposable element IS1. - J Mol Biol: 1986 Oct 5, 191(3);383-93 [PubMed:3029382] [DOI]
- ↑ Depardieu F, Podglajen I, Leclercq R, Collatz E, Courvalin P . Modes and modulations of antibiotic resistance gene expression. - Clin Microbiol Rev: 2007 Jan, 20(1);79-114 [PubMed:17223624] [DOI]
- ↑ Siguier P, Gourbeyre E, Chandler M . Bacterial insertion sequences: their genomic impact and diversity. - FEMS Microbiol Rev: 2014 Sep, 38(5);865-91 [PubMed:24499397] [DOI]
- ↑ Szeverényi I, Hodel A, Arber W, Olasz F . Vector for IS element entrapment and functional characterization based on turning on expression of distal promoterless genes. - Gene: 1996 Sep 26, 174(1);103-10 [PubMed:8863735] [DOI]
- ↑ 19.0 19.1 19.2 Olliver A, Vallé M, Chaslus-Dancla E, Cloeckaert A . Overexpression of the multidrug efflux operon acrEF by insertional activation with IS1 or IS10 elements in Salmonella enterica serovar typhimurium DT204 acrB mutants selected with fluoroquinolones. - Antimicrob Agents Chemother: 2005 Jan, 49(1);289-301 [PubMed:15616308] [DOI]
- ↑ 20.0 20.1 20.2 Jellen-Ritter AS, Kern WV . Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants Selected with a fluoroquinolone. - Antimicrob Agents Chemother: 2001 May, 45(5);1467-72 [PubMed:11302812] [DOI]
- ↑ Kobayashi K, Tsukagoshi N, Aono R . Suppression of hypersensitivity of Escherichia coli acrB mutant to organic solvents by integrational activation of the acrEF operon with the IS1 or IS2 element. - J Bacteriol: 2001 Apr, 183(8);2646-53 [PubMed:11274125] [DOI]
- ↑ Wolter DJ, Hanson ND, Lister PD . Insertional inactivation of oprD in clinical isolates of Pseudomonas aeruginosa leading to carbapenem resistance. - FEMS Microbiol Lett: 2004 Jul 1, 236(1);137-43 [PubMed:15212803] [DOI]
- ↑ 23.0 23.1 23.2 Barany F, Boeke JD, Tomasz A . Staphylococcal plasmids that replicate and express erythromycin resistance in both Streptococcus pneumoniae and Escherichia coli. - Proc Natl Acad Sci U S A: 1982 May, 79(9);2991-5 [PubMed:6283551] [DOI]
- ↑ Saedler H, Reif HJ, Hu S, Davidson N . IS2, a genetic element for turn-off and turn-on of gene activity in E. coli. - Mol Gen Genet: 1974, 132(4);265-89 [PubMed:4610339] [DOI]
- ↑ Nevers P, Saedler H . Transposable genetic elements as agents of gene instability and chromosomal rearrangements. - Nature: 1977 Jul 14, 268(5616);109-15 [PubMed:339095] [DOI]
- ↑ Jaurin B, Normark S . Insertion of IS2 creates a novel ampC promoter in Escherichia coli. - Cell: 1983 Mar, 32(3);809-16 [PubMed:6187472] [DOI]
- ↑ Blount ZD, Barrick JE, Davidson CJ, Lenski RE . Genomic analysis of a key innovation in an experimental Escherichia coli population. - Nature: 2012 Sep 27, 489(7417);513-8 [PubMed:22992527] [DOI]
- ↑ Bongers RS, Hoefnagel MH, Starrenburg MJ, Siemerink MA, Arends JG, Hugenholtz J, Kleerebezem M . IS981-mediated adaptive evolution recovers lactate production by ldhB transcription activation in a lactate dehydrogenase-deficient strain of Lactococcus lactis. - J Bacteriol: 2003 Aug, 185(15);4499-507 [PubMed:12867459] [DOI]
- ↑ Safi H, Barnes PF, Lakey DL, Shams H, Samten B, Vankayalapati R, Howard ST . IS6110 functions as a mobile, monocyte-activated promoter in Mycobacterium tuberculosis. - Mol Microbiol: 2004 May, 52(4);999-1012 [PubMed:15130120] [DOI]
- ↑ Luo Y, Yang J, Ye L, Guo L, Zhao Q, Chen R, Chen Y, Han X, Zhao J, Tian S, Han L . Characterization of KPC-2-producing Escherichia coli, Citrobacter freundii, Enterobacter cloacae, Enterobacter aerogenes, and Klebsiella oxytoca isolates from a Chinese Hospital. - Microb Drug Resist: 2014 Aug, 20(4);264-9 [PubMed:24433026] [DOI]
- ↑ Ciampi MS, Schmid MB, Roth JR . Transposon Tn10 provides a promoter for transcription of adjacent sequences. - Proc Natl Acad Sci U S A: 1982 Aug, 79(16);5016-20 [PubMed:6289329] [DOI]
- ↑ Simons RW, Hoopes BC, McClure WR, Kleckner N . Three promoters near the termini of IS10: pIN, pOUT, and pIII. - Cell: 1983 Sep, 34(2);673-82 [PubMed:6311437] [DOI]
- ↑ Rothstein SJ, Reznikoff WS . The functional differences in the inverted repeats of Tn5 are caused by a single base pair nonhomology. - Cell: 1981 Jan, 23(1);191-9 [PubMed:6260374] [DOI]
- ↑ 34.0 34.1 Poirel L, Decousser JW, Nordmann P . Insertion sequence ISEcp1B is involved in expression and mobilization of a bla(CTX-M) beta-lactamase gene. - Antimicrob Agents Chemother: 2003 Sep, 47(9);2938-45 [PubMed:12936998] [DOI]
- ↑ 35.0 35.1 Corvec S, Caroff N, Espaze E, Giraudeau C, Drugeon H, Reynaud A . AmpC cephalosporinase hyperproduction in Acinetobacter baumannii clinical strains. - J Antimicrob Chemother: 2003 Oct, 52(4);629-35 [PubMed:12951337] [DOI]
- ↑ Segal H, Nelson EC, Elisha BG . Genetic environment and transcription of ampC in an Acinetobacter baumannii clinical isolate. - Antimicrob Agents Chemother: 2004 Feb, 48(2);612-4 [PubMed:14742218] [DOI]
- ↑ Héritier C, Poirel L, Nordmann P . Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. - Clin Microbiol Infect: 2006 Feb, 12(2);123-30 [PubMed:16441449] [DOI]
- ↑ Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, Pitt TL . The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. - FEMS Microbiol Lett: 2006 May, 258(1);72-7 [PubMed:16630258] [DOI]
- ↑ 39.0 39.1 Carlson PE Jr, Horzempa J, O'Dee DM, Robinson CM, Neophytou P, Labrinidis A, Nau GJ . Global transcriptional response to spermine, a component of the intramacrophage environment, reveals regulation of Francisella gene expression through insertion sequence elements. - J Bacteriol: 2009 Nov, 191(22);6855-64 [PubMed:19749055] [DOI]
- ↑ Tolmasky ME, Crosa JH . Iron transport genes of the pJM1-mediated iron uptake system of Vibrio anguillarum are included in a transposonlike structure. - Plasmid: 1995 May, 33(3);180-90 [PubMed:7568465] [DOI]
- ↑ Haggoud A, Reysset G, Azeddoug H, Sebald M . Nucleotide sequence analysis of two 5-nitroimidazole resistance determinants from Bacteroides strains and of a new insertion sequence upstream of the two genes. - Antimicrob Agents Chemother: 1994 May, 38(5);1047-51 [PubMed:8067736] [DOI]
- ↑ 42.0 42.1 Podglajen I, Breuil J, Collatz E . Insertion of a novel DNA sequence, 1S1186, upstream of the silent carbapenemase gene cfiA, promotes expression of carbapenem resistance in clinical isolates of Bacteroides fragilis. - Mol Microbiol: 1994 Apr, 12(1);105-14 [PubMed:8057831] [DOI]
- ↑ Podglajen I, Breuil J, Casin I, Collatz E . Genotypic identification of two groups within the species Bacteroides fragilis by ribotyping and by analysis of PCR-generated fragment patterns and insertion sequence content. - J Bacteriol: 1995 Sep, 177(18);5270-5 [PubMed:7545155] [DOI]
- ↑ 44.0 44.1 44.2 Scordilis GE, Ree H, Lessie TG . Identification of transposable elements which activate gene expression in Pseudomonas cepacia. - J Bacteriol: 1987 Jan, 169(1);8-13 [PubMed:3025189] [DOI]
- ↑ Leelaporn A, Firth N, Byrne ME, Roper E, Skurray RA . Possible role of insertion sequence IS257 in dissemination and expression of high- and low-level trimethoprim resistance in staphylococci. - Antimicrob Agents Chemother: 1994 Oct, 38(10);2238-44 [PubMed:7840551] [DOI]
- ↑ Simpson AE, Skurray RA, Firth N . An IS257-derived hybrid promoter directs transcription of a tetA(K) tetracycline resistance gene in the Staphylococcus aureus chromosomal mec region. - J Bacteriol: 2000 Jun, 182(12);3345-52 [PubMed:10852863] [DOI]
- ↑ Chen TL, Wu RC, Shaio MF, Fung CP, Cho WL . Acquisition of a plasmid-borne blaOXA-58 gene with an upstream IS1008 insertion conferring a high level of carbapenem resistance to Acinetobacter baumannii. - Antimicrob Agents Chemother: 2008 Jul, 52(7);2573-80 [PubMed:18443121] [DOI]
- ↑ Lee KY, Hopkins JD, Syvanen M . Direct involvement of IS26 in an antibiotic resistance operon. - J Bacteriol: 1990 Jun, 172(6);3229-36 [PubMed:2160941] [DOI]
- ↑ Naas T, Philippon L, Poirel L, Ronco E, Nordmann P . An SHV-derived extended-spectrum beta-lactamase in Pseudomonas aeruginosa. - Antimicrob Agents Chemother: 1999 May, 43(5);1281-4 [PubMed:10223953] [DOI]
- ↑ Bräu B, Pilz U, Piepersberg W . Genes for gentamicin-(3)-N-acetyltransferases III and IV: I. Nucleotide sequence of the AAC(3)-IV gene and possible involvement of an IS140 element in its expression. - Mol Gen Genet: 1984, 193(1);179-87 [PubMed:6318050] [DOI]
- ↑ Rogers MB, Bennett TK, Payne CM, Smith CJ . Insertional activation of cepA leads to high-level beta-lactamase expression in Bacteroides fragilis clinical isolates. - J Bacteriol: 1994 Jul, 176(14);4376-84 [PubMed:7517394] [DOI]
- ↑ Naas T, Cuzon G, Villegas MV, Lartigue MF, Quinn JP, Nordmann P . Genetic structures at the origin of acquisition of the beta-lactamase bla KPC gene. - Antimicrob Agents Chemother: 2008 Apr, 52(4);1257-63 [PubMed:18227185] [DOI]
- ↑ Dalrymple B . Novel rearrangements of IS30 carrying plasmids leading to the reactivation of gene expression. - Mol Gen Genet: 1987 May, 207(2-3);413-20 [PubMed:3039299] [DOI]
- ↑ Rudant E, Courvalin P, Lambert T . Characterization of IS18, an element capable of activating the silent aac(6')-Ij gene of Acinetobacter sp. 13 strain BM2716 by transposition. - Antimicrob Agents Chemother: 1998 Oct, 42(10);2759-61 [PubMed:9756793] [DOI]
- ↑ Zander E, Chmielarczyk A, Heczko P, Seifert H, Higgins PG . Conversion of OXA-66 into OXA-82 in clinical Acinetobacter baumannii isolates and association with altered carbapenem susceptibility. - J Antimicrob Chemother: 2013 Feb, 68(2);308-11 [PubMed:23014718] [DOI]
- ↑ Rasmussen JL, Odelson DA, Macrina FL . Complete nucleotide sequence of insertion element IS4351 from Bacteroides fragilis. - J Bacteriol: 1987 Aug, 169(8);3573-80 [PubMed:3038844] [DOI]
- ↑ Maki H, Murakami K . Formation of potent hybrid promoters of the mutant llm gene by IS256 transposition in methicillin-resistant Staphylococcus aureus. - J Bacteriol: 1997 Nov, 179(22);6944-8 [PubMed:9371438] [DOI]
- ↑ Couto I, Wu SW, Tomasz A, de Lencastre H . Development of methicillin resistance in clinical isolates of Staphylococcus sciuri by transcriptional activation of the mecA homologue native to s. - J Bacteriol: 2003 Jan, 185(2);645-53 [PubMed:12511511] [DOI]
- ↑ Hübner A, Hendrickson W . A fusion promoter created by a new insertion sequence, IS1490, activates transcription of 2,4,5-trichlorophenoxyacetic acid catabolic genes in Burkholderia cepacia AC1100. - J Bacteriol: 1997 Apr, 179(8);2717-23 [PubMed:9098071] [DOI]
- ↑ DeShazer D, Wood GE, Friedman RL . Molecular characterization of catalase from Bordetella pertussis: identification of the katA promoter in an upstream insertion sequence. - Mol Microbiol: 1994 Oct, 14(1);123-30 [PubMed:7830550] [DOI]
- ↑ Vandecraen J, Monsieurs P, Mergeay M, Leys N, Aertsen A, Van Houdt R . Zinc-Induced Transposition of Insertion Sequence Elements Contributes to Increased Adaptability of Cupriavidus metallidurans. - Front Microbiol: 2016, 7;359 [PubMed:27047473] [DOI]
- ↑ 62.0 62.1 62.2 62.3 Podglajen I, Breuil J, Rohaut A, Monsempes C, Collatz E . Multiple mobile promoter regions for the rare carbapenem resistance gene of Bacteroides fragilis. - J Bacteriol: 2001 Jun, 183(11);3531-5 [PubMed:11344163] [DOI]
- ↑ 63.0 63.1 63.2 63.3 Kato N, Yamazoe K, Han CG, Ohtsubo E . New insertion sequence elements in the upstream region of cfiA in imipenem-resistant Bacteroides fragilis strains. - Antimicrob Agents Chemother: 2003 Mar, 47(3);979-85 [PubMed:12604530] [DOI]
- ↑ López de Felipe F, Magni C, de Mendoza D, López P . Transcriptional activation of the citrate permease P gene of Lactococcus lactis biovar diacetylactis by an insertion sequence-like element present in plasmid pCIT264. - Mol Gen Genet: 1996 Mar 7, 250(4);428-36 [PubMed:8602160] [DOI]
- ↑ Cascio GL, Macaccaro L, Centonze AR, Sóki J, Fontana R, Mazzariol A . A new insertion sequence element containing a cfiA gene in the first imipenem-resistant Bacteroides fragilis strain isolated in Italy. - Int J Antimicrob Agents: 2009 Dec, 34(6);610-1 [PubMed:19744834] [DOI]
- ↑ Karim A, Poirel L, Nagarajan S, Nordmann P . Plasmid-mediated extended-spectrum beta-lactamase (CTX-M-3 like) from India and gene association with insertion sequence ISEcp1. - FEMS Microbiol Lett: 2001 Jul 24, 201(2);237-41 [PubMed:11470367] [DOI]
- ↑ Cao V, Lambert T, Nhu DQ, Loan HK, Hoang NK, Arlet G, Courvalin P . Distribution of extended-spectrum beta-lactamases in clinical isolates of Enterobacteriaceae in Vietnam. - Antimicrob Agents Chemother: 2002 Dec, 46(12);3739-43 [PubMed:12435670] [DOI]
- ↑ Lartigue MF, Poirel L, Aubert D, Nordmann P . In vitro analysis of ISEcp1B-mediated mobilization of naturally occurring beta-lactamase gene blaCTX-M of Kluyvera ascorbata. - Antimicrob Agents Chemother: 2006 Apr, 50(4);1282-6 [PubMed:16569841] [DOI]
- ↑ Wachino J, Yamane K, Kimura K, Shibata N, Suzuki S, Ike Y, Arakawa Y . Mode of transposition and expression of 16S rRNA methyltransferase gene rmtC accompanied by ISEcp1. - Antimicrob Agents Chemother: 2006 Sep, 50(9);3212-5 [PubMed:16940134] [DOI]
- ↑ Demuth DR, Duan Y, Jenkinson HF, McNab R, Gil S, Lamont RJ . Interruption of the Streptococcus gordonii M5 sspA/sspB intergenic region by an insertion sequence related to IS1167 of Streptococcus pneumoniae. - Microbiology (Reading): 1997 Jun, 143 ( Pt 6);2047-2055 [PubMed:9202480] [DOI]
- ↑ Kallastu A, Hõrak R, Kivisaar M . Identification and characterization of IS1411, a new insertion sequence which causes transcriptional activation of the phenol degradation genes in Pseudomonas putida. - J Bacteriol: 1998 Oct, 180(20);5306-12 [PubMed:9765560] [DOI]
- ↑ Al Safadi R, Amor S, Hery-Arnaud G, Spellerberg B, Lanotte P, Mereghetti L, Gannier F, Quentin R, Rosenau A . Enhanced expression of lmb gene encoding laminin-binding protein in Streptococcus agalactiae strains harboring IS1548 in scpB-lmb intergenic region. - PLoS One: 2010 May 24, 5(5);e10794 [PubMed:20520730] [DOI]