期刊论文详细信息
BMC Microbiology
Tetracycline accelerates the temporally-regulated invasion response in specific isolates of multidrug-resistant Salmonella enterica serovar Typhimurium
Bradley L Bearson2  Shawn MD Bearson1  Brian W Brunelle1 
[1] Food Safety and Enteric Pathogens Research Unit, National Animal Disease Center, ARS, USDA, Ames, IA 50010, USA;Agroecosystems Management Research Unit, National Laboratory for Agriculture and the Environment, ARS, USDA, Ames, IA 50010, USA
关键词: DT193;    DT104;    Typhimurium;    Tetracycline;    Salmonella;    Invasion;    Drug-resistant;    Antibiotics;   
Others  :  1143068
DOI  :  10.1186/1471-2180-13-202
 received in 2013-04-16, accepted in 2013-09-02,  发布年份 2013
PDF
【 摘 要 】

Background

Multidrug-resistant (MDR) Salmonella isolates are associated with increased morbidity compared to antibiotic-sensitive strains and are an important health and safety concern in both humans and animals. Salmonella enterica serovar Typhimurium is a prevalent cause of foodborne disease, and a considerable number of S. Typhimurium isolates from humans and livestock are resistant to three or more antibiotics. The majority of these MDR S. Typhimurium isolates are resistant to tetracycline, a commonly used and clinically and agriculturally relevant antibiotic. Because exposure of drug-resistant bacteria to antibiotics can affect cellular processes associated with virulence, such as invasion, we investigated the effect tetracycline had on the invasiveness of tetracycline-resistant MDR S. Typhimurium isolates.

Results

The isolates selected and tested were from two common definitive phage types of S. Typhimurium, DT104 and DT193, and were resistant to tetracycline and at least three other antibiotics. Although Salmonella invasiveness is temporally regulated and normally occurs during late-log growth phase, tetracycline exposure induced the full invasive phenotype in a cell culture assay during early-log growth in several DT193 isolates. No changes in invasiveness due to tetracycline exposure occurred in the DT104 isolates during early-log growth or in any of the isolates during late-log growth. Real-time PCR was used to test expression of the virulence genes hilA, prgH, and invF, and these genes were significantly up-regulated during early-log growth in most isolates due to tetracycline exposure; however, increased virulence gene expression did not always correspond with increased invasion, and therefore was not an accurate indicator of elevated invasiveness. This is the first report to assess DT193 isolates, as well as the early-log growth phase, in response to tetracycline exposure, and it was the combination of both parameters that was necessary to observe the induced invasion phenotype.

Conclusions

In this report, we demonstrate that the invasiveness of MDR S. Typhimurium can be modulated in the presence of tetracycline, and this effect is dependent on growth phase, antibiotic concentration, and strain background. Identifying the conditions necessary to establish an invasive phenotype is important to elucidate the underlying factors associated with increased virulence of MDR Salmonella.

【 授权许可】

   
2013 Brunelle et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150328225549811.pdf 435KB PDF download
Figure 3. 50KB Image download
Figure 2. 101KB Image download
Figure 1. 85KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】
  • [1]Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM: Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 2011, 17(1):7-15.
  • [2]Service ER: Foodborne Illness Cost Calculator: Salmonella. Washington, D.C: United States Department of Agriculture; 2009.
  • [3]CDC: National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Human Isolates Final Report, 2010. Atlanta, Georgia: US Department of Health and Human Services, CDC; 2012.
  • [4]CDC: Investigation Update: Multistate Outbreak of Human Salmonella Typhimurium Infections Linked to Ground Beef. 2012. http://www.cdc.gov/salmonella/typhimurium-groundbeef/020112/index.html webcite
  • [5]Evans S, Davies R: Case control study of multiple-resistant Salmonella typhimurium DT104 infection of cattle in Great Britain. Vet Rec 1996, 139(23):557-558.
  • [6]Varma JK, Greene KD, Ovitt J, Barrett TJ, Medalla F, Angulo FJ: Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984–2002. Emerg Infect Dis 2005, 11(6):943-946.
  • [7]Barza M: Potential mechanisms of increased disease in humans from antimicrobial resistance in food animals. Clin Infect Dis 2002, 34(Suppl 3):S123-125.
  • [8]Molbak K: Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clin Infect Dis 2005, 41(11):1613-1620.
  • [9]Blickwede M, Goethe R, Wolz C, Valentin-Weigand P, Schwarz S: Molecular basis of florfenicol-induced increase in adherence of Staphylococcus aureus strain Newman. J Antimicrob Chemother 2005, 56(2):315-323.
  • [10]Deneve C, Bouttier S, Dupuy B, Barbut F, Collignon A, Janoir C: Effects of subinhibitory concentrations of antibiotics on colonization factor expression by moxifloxacin-susceptible and moxifloxacin-resistant Clostridium difficile strains. Antimicrob Agents Chemother 2009, 53(12):5155-5162.
  • [11]Kuroda H, Kuroda M, Cui L, Hiramatsu K: Subinhibitory concentrations of beta-lactam induce haemolytic activity in Staphylococcus aureus through the SaeRS two-component system. FEMS Microbiol Lett 2007, 268(1):98-105.
  • [12]Shen L, Shi Y, Zhang D, Wei J, Surette MG, Duan K: Modulation of secreted virulence factor genes by subinhibitory concentrations of antibiotics in Pseudomonas aeruginosa. J Microbiol 2008, 46(4):441-447.
  • [13]Weir EK, Martin LC, Poppe C, Coombes BK, Boerlin P: Subinhibitory concentrations of tetracycline affect virulence gene expression in a multi-resistant Salmonella enterica subsp. enterica serovar Typhimurium DT104. Microbes Infect 2008, 10(8):901-907.
  • [14]Carlson SA, Willson RM, Crane AJ, Ferris KE: Evaluation of invasion-conferring genotypes and antibiotic-induced hyperinvasive phenotypes in multiple antibiotic resistant Salmonella typhimurium DT104. Microb Pathog 2000, 28(6):373-378.
  • [15]FDA: National Antimicrobial Resistance Monitoring System – Enteric Bacteria (NARMS): 2009 Executive Report. Rockville, MD: U.S. Department of Health and Human Services, Food and Drug Administration; 2011.
  • [16]Boyd D, Peters GA, Cloeckaert A, Boumedine KS, Chaslus-Dancla E, Imberechts H, Mulvey MR: Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J Bacteriol 2001, 183(19):5725-5732.
  • [17]Carlson SA, Sharma VK, McCuddin ZP, Rasmussen MA, Franklin SK: Involvement of a Salmonella genomic island 1 gene in the rumen protozoan-mediated enhancement of invasion for multiple-antibiotic-resistant Salmonella enterica serovar Typhimurium. Infect Immun 2007, 75(2):792-800.
  • [18]Rasmussen MA, Carlson SA, Franklin SK, McCuddin ZP, Wu MT, Sharma VK: Exposure to rumen protozoa leads to enhancement of pathogenicity of and invasion by multiple-antibiotic-resistant Salmonella enterica bearing SGI1. Infect Immun 2005, 73(8):4668-4675.
  • [19]Saini S, Slauch JM, Aldridge PD, Rao CV: Role of cross talk in regulating the dynamic expression of the flagellar Salmonella pathogenicity island 1 and type 1 fimbrial genes. J Bacteriol 2010, 192(21):5767-5777.
  • [20]Ibarra JA, Knodler LA, Sturdevant DE, Virtaneva K, Carmody AB, Fischer ER, Porcella SF, Steele-Mortimer O: Induction of Salmonella pathogenicity island 1 under different growth conditions can affect Salmonella-host cell interactions in vitro. Microbiology 2010, 156(Pt 4):1120-1133.
  • [21]Thijs IM, De Keersmaecker SC, Fadda A, Engelen K, Zhao H, McClelland M, Marchal K, Vanderleyden J: Delineation of the Salmonella enterica serovar Typhimurium HilA regulon through genome-wide location and transcript analysis. J Bacteriol 2007, 189(13):4587-4596.
  • [22]Lee CA, Jones BD, Falkow S: Identification of a Salmonella typhimurium invasion locus by selection for hyperinvasive mutants. Proc Natl Acad Sci USA 1992, 89(5):1847-1851.
  • [23]Adaska JM, Silva AJ, Berge AC, Sischo WM: Genetic and phenotypic variability among Salmonella enterica serovar Typhimurium isolates from California dairy cattle and humans. Appl Environ Microbiol 2006, 72(10):6632-6637.
  • [24]Bergeron N, Corriveau J, Letellier A, Daigle F, Quessy S: Characterization of Salmonella Typhimurium isolates associated with septicemia in swine. Can J Vet Res 2010, 74(1):11-17.
  • [25]Dechet AM, Scallan E, Gensheimer K, Hoekstra R, Gunderman-King J, Lockett J, Wrigley D, Chege W, Sobel J: Outbreak of multidrug-resistant Salmonella enterica serotype Typhimurium Definitive Type 104 infection linked to commercial ground beef, northeastern United States, 2003–2004. Clin Infect Dis 2006, 42(6):747-752.
  • [26]Gebreyes WA, Altier C: Molecular characterization of multidrug-resistant Salmonella enterica subsp. enterica serovar Typhimurium isolates from swine. J Clin Microbiol 2002, 40(8):2813-2822.
  • [27]Gebreyes WA, Thakur S, Davies PR, Funk JA, Altier C: Trends in antimicrobial resistance, phage types and integrons among Salmonella serotypes from pigs, 1997–2000. J Antimicrob Chemother 2004, 53(6):997-1003.
  • [28]Glenn LM, Lindsey RL, Frank JF, Meinersmann RJ, Englen MD, Fedorka-Cray PJ, Frye JG: Analysis of antimicrobial resistance genes detected in multidrug-resistant Salmonella enterica serovar Typhimurium isolated from food animals. Microb Drug Resist 2011, 17(3):407-418.
  • [29]Ng LK, Mulvey MR, Martin I, Peters GA, Johnson W: Genetic characterization of antimicrobial resistance in Canadian isolates of Salmonella serovar Typhimurium DT104. Antimicrob Agents Chemother 1999, 43(12):3018-3021.
  • [30]Brazas MD, Hancock RE: Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance. Drug Discov Today 2005, 10(18):1245-1252.
  • [31]Goh EB, Yim G, Tsui W, McClure J, Surette MG, Davies J: Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci U S A 2002, 99(26):17025-17030.
  • [32]Kamensek S, Zgur-Bertok D: Global transcriptional responses to the bacteriocin colicin M in Escherichia coli. BMC Microbiol 2013, 13:42. BioMed Central Full Text
  • [33]Yim G, de la Cruz F, Spiegelman GB, Davies J: Transcription modulation of Salmonella enterica serovar Typhimurium promoters by sub-MIC levels of rifampin. J Bacteriol 2006, 188(22):7988-7991.
  • [34]Chopra I, Roberts M: Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 2001, 65(2):232-260. second page, table of contents
  • [35]Banos RC, Vivero A, Aznar S, Garcia J, Pons M, Madrid C, Juarez A: Differential regulation of horizontally acquired and core genome genes by the bacterial modulator H-NS. PLoS Genet 2009, 5(6):e1000513.
  • [36]Gal-Mor O, Gibson DL, Baluta D, Vallance BA, Finlay BB: A novel secretion pathway of Salmonella enterica acts as an antivirulence modulator during salmonellosis. PLoS Pathog 2008, 4(4):e1000036.
  • [37]Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor; 1982.
  • [38]Chang HR, Loo LH, Jeyaseelan K, Earnest L, Stackebrandt E: Phylogenetic relationships of Salmonella typhi and Salmonella typhimurium based on 16S rRNA sequence analysis. Int J Syst Bacteriol 1997, 47(4):1253-1254.
  • [39]Brunelle BW, Bearson SMD, Bearson BL: Salmonella enterica serovar Typhimurium DT104 invasion is not enhanced by sub-Inhibitory concentrations of the antibiotic florfenicol. Vet Sci Technol 2011, 2:1.
  • [40]Golding GR, Olson AB, Doublet B, Cloeckaert A, Christianson S, Graham MR, Mulvey MR: The effect of the Salmonella genomic island 1 on in vitro global gene expression in Salmonella enterica serovar Typhimurium LT2. Microbes Infect 2007, 9(1):21-27.
  • [41]Elsinghorst EA: Measurement of invasion by gentamicin resistance. Methods Enzymol 1994, 236:405-420.
  • [42]Ramakers C, Ruijter JM, Deprez RH, Moorman AF: Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 2003, 339(1):62-66.
  • [43]Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(9):e45.
  文献评价指标  
  下载次数:15次 浏览次数:7次