Impact of antibiotic treatments on the expression of the R plasmid tra genes and on the host innate immune activity during pRAS1 bearing Aeromonas hydrophila infection in zebrafish (Danio rerio)

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Cantas, Leon ^a,b   Midtlyng, Paul J ^a   Sørum, Henning ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b Norwegian Veterinary Alliance ^*  (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; FLUMEQUINE; INTERLEUKIN 1BETA; INTERLEUKIN 8; MESSENGER RNA; PLACEBO; RNA 16S; SULFONAMIDE; TETRACYCLINE; TRIMETHOPRIM; TUMOR NECROSIS FACTOR ALPHA; ANTIINFECTIVE AGENT; QUINOLONE DERIVATIVE;

AEROMONAS HYDROPHILA; AEROMONAS HYDROPHILA INFECTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; FEMALE; GENE DOSAGE; GENE EXPRESSION; INCU PLASMID; INNATE IMMUNITY; INTESTINE FLORA; MALE; MOUTH INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRAS1 BACTERIAL GENE; R PLASMID; TRAD BACTERIAL GENE; VIRB11 BACTERIAL GENE; VIRD4 BACTERIAL GENE; ZEBRA FISH; ANIMAL; ANIMAL DISEASE; BACTERIUM CONJUGATION; DRUG EFFECT; FISH DISEASE; GENE EXPRESSION REGULATION; GENETICS; GRAM NEGATIVE INFECTION; HORIZONTAL GENE TRANSFER; IMMUNOLOGY; INTESTINE; METAGENOME; MICROBIOLOGY; MULTIDRUG RESISTANCE; R FACTOR;

AEROMONAS HYDROPHILA; BACTERIA (MICROORGANISMS); DANIO RERIO;

AEROMONAS HYDROPHILA; ANIMALS; ANTI-BACTERIAL AGENTS; CONJUGATION, GENETIC; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; FISH DISEASES; FLUOROQUINOLONES; GENE EXPRESSION REGULATION, BACTERIAL; GENE TRANSFER, HORIZONTAL; GRAM-NEGATIVE BACTERIAL INFECTIONS; IMMUNITY, INNATE; INTESTINES; MALE; METAGENOME; R FACTORS; RNA, RIBOSOMAL, 16S; TETRACYCLINE; TRIMETHOPRIM; ZEBRAFISH;

EID: 84858325370     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-37     Document Type: Article

References (78)

1. Zebrafish embryos as a model host for the real time analysis of Salmonella typhimurium infections. van der Sar AM, Musters RJ, van Eeden FJ, Appelmelk BJ, Vandenbroucke-Grauls CM, Bitter W, Cell Microbiol 2003 5 601 611 10.1046/j.1462-5822.2003.00303.x 12925130 (Pubitemid 37080671)
2. A guide for the laboratory use of zebrafish (Danio rerio). Westerfield M, University of Oregon Press 2000
3. Real-time visualization of Mycobacterium macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Davis JM, Clay H, Lewis JL, Ghori N, Herbomel P, Ramakrishnan L, Immunity 2002 17 693 702 10.1016/S1074-7613(02)00475-2 12479816 (Pubitemid 35477789)
4. Streptococcus zebrafish model of bacterial pathogenesis. Neely MN, Pfeifer JD, Caparon M, Infect Immun 2000 70 3904 3914
5. Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Pressley ME, Phelan PE, Witten PE, Mellon MT, Kim CH, Dev Comp Immunol 2005 29 501 513 10.1016/j.dci.2004.10.007 15752547 (Pubitemid 40326987)
6. A star with stripes: zebrafish as an infection model. van der Sar AM, Appelmelk BJ, Vandenbroucke-Grauls CM, Bitter W, Trends Microbiol 2004 12 451 457 10.1016/j.tim.2004.08.001 15381194 (Pubitemid 39286123)
7. Adherence, haemagglutination, and cell surface characteristics of motile aeromonads virulent for fish. Del Corral F, Shotts EB Jr, Brown J, J Fish Dis 1990 13 255 268 10.1111/j.1365-2761.1990.tb00782.x
8. Pathogenicity factors and virulence for rainbow trout (Salmo gairdneri) of motile Aeromonas spp. isolated from a river. Paniagua C, Rivero O, Anguita J, Naharro G, J Clin Microbiol 1990 28 350 355 2312678 (Pubitemid 20050950)
9. Aeromonas hydrophila isolated from food and drinking water: hemagglutination, hemolysis, and cytotoxicity for a human intestinal cell line (HT-29). Handfield M, Simard P, Couillard M, Letarte R, Appl Environ Microbiol 1996 62 3459 3461 8795237 (Pubitemid 26304141)
10. Immune response of zebrafish (Danio rerio) against a newly isolated bacterial pathogen Aeromonas hydrophila. Rodriguez I, Novoa B, Figueras A, Fish and Shellfish Immun 2008 25 239 249 10.1016/j.fsi.2008.05.002
11. High mortality in Zebrafish (Danio rerio). Pullium JK, Dillehay DL, Webb S, Contemp Top Lab Anim Sci 1999 38 80 83 12086431 (Pubitemid 129618883)
12. Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions. Janda JM, Abbott SL, Clin Infect Dis 1998 27 332 244 10.1086/514652 9709884
13. Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp. Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P, Emerg Infect Dis 2008 14 231 237 10.3201/eid1402.070677 18258115 (Pubitemid 351213672)
14. Integron-containing IncU R plasmids pRAS1 and pAr-32 from the fish pathogen Aeromonas salmonicida. Sørum H, L'Abée-Lund TM, Solberg A, Wold A, Antimicrob Agents Chemother 2003 47 1285 1290 10.1128/AAC.47.4.1285- 1290.2003 12654659 (Pubitemid 36368586)
15. Characterization of conjugative R plasmids belonging to the new Incompatibility group IncU. Tschäpe H, Tietze E, Koch C, J Gener Microbiol 1981 127 155 160 (Pubitemid 12169883)
16. Transfer of multiple drug resistance plasmids between bacteria of diverse origins in natural microenvironments. Kruse H, Sørum H, Appl Environ Microbiol 1994 60 4015 4021 11865872 (Pubitemid 24335854)
17. Complete nucleotide sequence of the conjugative tetracycline resistance plasmid pFBAOT6, a member of a group of IncU plasmids with global ubiquity. Rhodes G, Parkhill J, Bird C, Ambrose K, Jones MC, Huys G, Swings J, Pickup RW, Appl Environ Microbiol 2004 70 7497 7510 10.1128/AEM.70.12.7497-7510.2004 15574953 (Pubitemid 39643817)
18. Genomic and functional characterization of the modular Broad-Host-Range RA3 plasmid, the Archetype of the IncU group. Kulinska A, Czeredys M, Hayes F, Jagura-Burdzy G, Appl Environ Microbiol 2008 74 4119 4132 10.1128/AEM.00229-08 18502921 (Pubitemid 351962438)
19. Short and long peptidoglycan recognition proteins (PGRPs) in zebrafish, with findings of multiple PGRP homologs in teleost fish. Chang MX, Nie P, Wei LL, Mol Immunol 2007 44 3005 3023 10.1016/j.molimm.2006.12.029 17296228 (Pubitemid 46412480)
20. Zebrafish ribonucleases are bactericidal: implications for the origin of the vertebrate RNase A superfamily. Cho S, Zhang J, Mol Biol Evol 2007 24 1259 1268 10.1093/molbev/msm047 17347156 (Pubitemid 47343651)
21. Intestinal differentiation in zebrafish requires Cdx1b, a functional equivalent of mammalian Cdx2. Flores MV, Hall CJ, Davidson AJ, Singh PP, Mahagaonkar AA, Zon LI, Crosier KE, Crosier PS, Gastroenterology 2008 135 5 1665 1675 10.1053/j.gastro.2008.07.024 18804112
22. Zebrafish peptidoglycan recognition proteins are bactericidal amidases essential for defense against bacterial infections. Li X, Wang S, Qi J, Echtenkamp SF, Chatterjee R, Wang M, Boons GJ, Dziarski R, Gupta D, Immunity 2007 27 518 529 10.1016/j.immuni.2007.07.020 17892854 (Pubitemid 47418675)
23. Fish immunology. Lieschke GJ, Trede NS, Curr Biol 2009 19 678 682 10.1016/j.cub.2009.06.068
24. Topographical distribution of antimicrobial genes in the zebrafish intestine. Oehlers SH, Flores MV, Chen T, Chris JH, Crosier KE, Crosier PS, Develop Comp Immun 2011 35 385 391 10.1016/j.dci.2010.11.008
25. Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: Striking similarities and obvious differences with mammals. Lin B, Chen S, Cao Z, Lin Y, Mo D, Zhang H, et al. Mol Immunol 2007 44 295 301 10.1016/j.molimm.2006.03.001 16630661 (Pubitemid 44308357)
26. Characterisation of class 1 integrons associated with R-plasmids in clinical Aeromonas salmonicida isolates from various geographic areas. Schmidt AS, Bruun MS, Larsen JL, Dalsgaard I, J Antimicrob Chemother 2001 47 735 743 10.1093/jac/47.6.735 11389105 (Pubitemid 32519821)
27. The culturable intestinal microbiota of triploid and diploid juvenile Atlantic salmon (Salmo salar)-a comparison of composition and drug resistance. Cantas L, Fraser TWK, Fjelldal PG, Mayer I, Sørum H, BMC Vet Res 2011 7 71 10.1186/1746-6148-7-71 22094054
28. Culturable gut microbiota diversity in Zebrafish. Cantas L, Sørby JRT, Aleström P, Sørum H, Zebrafish 2012 9 1 26 37
29. Primer3 on the WWW for general users and for biologist programmers. Rozen S, Skaletsky H, Methods Mol Biol 2000 132 365 386 10547847
30. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C[T]] method. Livak KJ, Schmittgen TD, Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609 (Pubitemid 34164012)
31. Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish (Clarias gariepinus). Bogerd J, Blomenrohr M, Andersson E, van der Putten HHAGM, Tensen CP, Vischer HF, Biological Reproduction 2001 64 1633 1643 10.1095/biolreprod64. 6.1633 (Pubitemid 32493478)
32. Quantification of total bacteria, enterobacteria and lactobacilli populations in pig digesta by real-time PCR. Castillo M, Martin-Orue SM, Manzanilla EG, Badiola I, Martin M, Gasa J, Vet Microbiol 2006 114 165 170 10.1016/j.vetmic.2005.11.055 16384658
33. Statistical analysis of real-time PCR data. Yuan JS, Reed A, Chen F, Stewart JCN, BMC Bioinfor 2006 7 85 10.1186/1471-2105-7-85 (Pubitemid 43362095)
34. The cytotoxic enterotoxin of Aeromonas hydrophila induces proinflammatory cytokine production and activates arachidonic acid metabolism in macrophages. Chopra AK, Xu X, Ribardo D, Gonzalez M, Kuhl K, Peterson JW, et al. Infect Immun 2000 68 2808 2818 10.1128/IAI.68.5.2808-2818.2000 10768977 (Pubitemid 30253860)
35. Early cell signaling by the cytotoxic enterotoxin of Aeromonas hydrophila in macrophages. Ribardo DA, Kuhl KR, Boldogh I, Peterson JW, Houston CW, Chopra AK, Microb Pathog 2002 32 149 163 10.1006/mpat.2001.0490 12079405 (Pubitemid 34743888)
36. Identification of Aeromonas hydrophila cytotoxic enterotoxin-induced genes in macrophages using microarrays. Galindo CL, Sha J, Ribardo DA, Fadl AA, Pillai L, Chopra AK, J Biol Chem 2003 278 40198 40212 10.1074/jbc.M305788200 12824169 (Pubitemid 37248588)
37. Serum amyloid A, the major vertebrate acute-phase reactant. Uhlar CM, Whitehead AS, Eur J Biochem 1999 265 501 523 10.1046/j.1432-1327.1999.00657.x 10504381 (Pubitemid 29488982)
38. Complement: central to innate immunity and bridging to adaptive responses. Morgan BP, Marchbank KJ, Longhi MP, Harris CL, Gallimore AM, Immunol Lett 2005 97 171 179 10.1016/j.imlet.2004.11.010 15752555 (Pubitemid 40326948)
39. Structure and biology of complement protein C3, a connecting link between innate and acquired immunity. Sahu A, Lambris JD, Immunol Rev 2001 180 35 48 10.1034/j.1600-065X.2001.1800103.x 11414361 (Pubitemid 32472850)
40. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Rawls JF, Mahowald MA, Ley RE, Jeffrey IG, Cell 2006 127 423 433 10.1016/j.cell.2006.08.043 17055441 (Pubitemid 44572375)
41. Contamination and sensitivity issues with a real-time universal 16S rRNA PCR. Corless CE, Guiver M, Borrow R, Edwards-Jones V, Kaczmarski EB, Fox AJ, J Clin Microbiol 2000 38 1747 1752 10790092 (Pubitemid 30253908)
42. Evaluation of the Applied Biosystems automated Taqman polymerase chain reaction system for the detection of meningococcal DNA. Guiver M, Borrow R, Marsh J, Gray SJ, Kaczmarski EB, Howells D, Boseley P, Fox AJ, FEMS Immunol Med Microbiol 2000 28 173 179 10.1111/j.1574-695X.2000.tb01473.x 10799809 (Pubitemid 30224639)
43. Quantitative real-time PCR for Porphyromonas gingivalis and total bacteria. Lyons SR, Griffen AL, Leys EJ, J Clin Microbiol 2000 38 2362 2365 10835003 (Pubitemid 30414365)
44. Determination of bacterial load by real-time PCR using a broad-range [universal] probe and primers set. Nadkarni MA, Martin FE, Jacques NA, Hunter N, Microbiol 2002 148 257 266 (Pubitemid 34083204)
45. Rapid identification of Yersinia enterocolitica in blood by the 5' nuclease PCR assay. Sen K, J Clin Microbiol 2000 38 1953 1958 10790127 (Pubitemid 30253943)
46. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, Achkar JP, Brant SR, Bayless TM, Kirschner BS, Hanauer SB, Nunez G, Cho JH, Nature 2001 411 603 606 10.1038/35079114 11385577 (Pubitemid 32531409)
47. Quantification of intestinal bacterial populations by Real-Time PCR with a universal primer set and minor groove binder probes: a global approach to the enteric flora. Ott SJ, Musfeldt M, Ullmann U, Hampe J, Schreiber S, J Clin Microb 2004 42 2566 2572 10.1128/JCM.42.6.2566-2572.2004 (Pubitemid 38747505)
48. Intestinal microbial changes and disease as a result of antimicrobial use. Finegold SM, Pediatr Infect Dis 1986 5 88 90 10.1097/00006454-198601001- 00015
49. Fecal microbiota of horses in the clinical setting: potential effects of penicillin and general anesthesia. Grønvold AM, L'Abée-Lund TM, Strand E, Sørum H, Yannarell AC, Mackie RI, FEMS Microbiol Ecol 2009 71 313 326 20002181
50. Changes in fecal microbiota of healthy dogs administered amoxicillin. Grønvold AM, L'Abée-Lund TM, Sørum H, Skancke E, Yannarell AC, Mackie RI, Vet Microbiol 2010 145 366 372 10.1016/j.vetmic.2010.03.023 20434851
51. Structural basis of specific Tra-Tra recognition during F plasmid-mediated bacterial conjugation. Lu J, Wong JJ, Edwards RA, Manchak J, Frost LS, Glover JN, Mol Microbiol 2008 70 89 99 10.1111/j.1365-2958.2008.06391. x 18717787
52. The virD gene is required for virulence while virD3 and orf5 are not required for virulence of Agrobacterium tumefaciens. Lin TX, Kado CI, Mol Microbiol 1993 9 803 812 10.1111/j.1365-2958.1993.tb01739.x 8231811 (Pubitemid 23253505)
53. Molecular characterization of the virD operon from Agrobacterium tumefaciens. Porter SG, Yanofsky MF, Nester EW, Nucleic Acids Res 1987 15 7503 7517 10.1093/nar/15.18.7503 3658701
54. Selective pressure affects transfer and establishment of a Lactobacillus plantarum resistance plasmid in the gastrointestinal environment. Feld L, Schjørring S, Hammer K, Licht TR, Danielsen M, Krogfelt K, Wilcks A, J Antimicrob Chemother 2008 61 845 852 10.1093/jac/dkn033 18238887 (Pubitemid 351426069)
55. Conjugative gene transfer in the gastrointestinal environment. Licht TR, Wilcks A, Adv Appl Microbiol 2006 58 77 95 16509443
56. Transfer in marine sediments of naturally occurring plasmid pRAS1 encoding multiple antibiotic resistance. Sandaa RA, Enger Appl Environ Microbiol 1994 60 4234 4238 16349453 (Pubitemid 24370784)
57. Evidence of increased spread and establishment of plasmid RP4 in the intestine under sub-inhibitory tetracycline concentrations. Licht TR, Struve C, Christensen BB, Poulsen RL, Molin S, Krogfelt KA, FEMS Microbiol Ecol 2003 44 217 223 10.1016/S0168-6496(03)00016-3 19719638 (Pubitemid 36423416)
58. Factors affecting transfer frequency of pAM beta 1 from Streptococcus faecalis to Lactobacillus plantarum. Sasaki Y, Taketomo N, Sasaki T, J Bacteriol 1988 170 5939 5942 3142863 (Pubitemid 19004378)
59. Inhibition of mutation and combating the evolution of antibiotic resistance. Cirz RT, Chin JK, Andes DR, de Crécy-Lagard V, Craig WA, Romesberg F, PLoS Biol 2005 3 176 10.1371/journal.pbio.0030176 (Pubitemid 41032212)
60. Effects of subinhibitory concentrations of antibiotics on SOS and DNA repair gene expression in Staphylococcus aureus. Mesak LR, Miao V, Davies J, Antimicrob Agents Chemother 2008 8 3394 3397
61. Antibacterial agents. Yao J, Moellering RJ, Manual of Clinical Microbiology Washington, DC: ASM Press, Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH, 2003 1039 1073
62. SOS-induction of the RP4 plasmid tet-determinant. Skavronskaia AG, Aleshkin GI, Tiganova IG, Rusina O, Andreeva IV, Mol Gen Mikrobiol Virusol 1988 8 17 23 2848194
63. SOS response induction by Beta-Lactams and bacterial defense against antibiotic lethality. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, et al. Science 2004 305 1629 1631 10.1126/science.1101630 15308764 (Pubitemid 39296359)
64. After 30 years of study, the bacterial SOS response still surprises us. Michel B, PLoS Biol 2005 3 255 10.1371/journal.pbio.0030255 (Pubitemid 41032183)
65. Resistance gene transfer in anaerobes: new insights, new problems. Salyers AA, Shoemaker NB, Clin Infect Dis 1996 23 36 43 10.1093/clinids/23. Supplement-1.S36
66. The SOS response controls integron recombination. Guerin E, Cambray G, Sanchez-Alberola N, Campoy S, Erill I, Da Re S, Gonzalez-Zorn B, Barbé J, Ploy MC, Mazel D, Science 2009 324 1034 10.1126/science.1172914 19460999
67. Genomic analysis of LexA binding reveals the permissive nature of the Escherichia coli genome and identifies unconventional target sites. Wade JT, Reppas NB, Church GM, Struhl K, Genes Dev 2005 19 2619 2630 10.1101/gad.1355605 16264194 (Pubitemid 41565981)
68. The immune system of cyprinid fish: The immunosuppressive effect of antibiotic oxytetracycline in carp. Rijkers GT, Teunissen AG, van Oostreom R, van Muiswinkel WB, Aquaculture 1980 19 177 189 10.1016/0044-8486(80)90018-6
69. The influence of antibiotics on the immune system: Immuno-pharmocokinetic investigations on the primary anti-SRBC response in carp, Cyprinus carpio L., after oxytetracycline injection. Grondel JL, Nouws JFM, van Muiswinkel WB, J Fish Dis 1987 10 35 43 10.1111/j.1365-2761.1987.tb00716.x
70. Protection against endotoxic shock and lipopolysaccharide-induced local inflammation by tetracycline: Correlation with inhibition of cytokine secretion. Shapira L, Soskolne WA, Houri Y, Barak V, Halabi A, Stabholz A, Infect Immun 1996 64 825 828 8641787 (Pubitemid 26065554)
71. Influence of flumequine on in vivo mitogen responses of European eel (Anguilla anguilla L., 1758) lymphoid cells. van der Heijden MHT, Booms GHR, Tanck MWT, Romboutb JHWM, Boona JH, Vet Immun Immunopat 1995 47 143 152 10.1016/0165-2427(94)05397-B
72. A study on the effect of enrofloxacin on the immune cells of experimental mice. Lu Y, Pan ZJH, He S, Journal of Foshan University Natural Science 2009
73. Complement evasion of pathogens: common strategies are shared by diverse organisms. Zipfel PF, Wurzner R, Skerka C, Mol Immun 2007 44 3850 3857 10.1016/j.molimm.2007.06.149 (Pubitemid 47332624)
74. The biochemistry and genetics of capsular polysaccharide production in bacteria. Roberts IS, Ann Rev Microbiol 1996 50 285 315 10.1146/annurev.micro. 50.1.285 (Pubitemid 26337465)
75. Effect of tetracycline on transfer and establishment of the tetracycline-inducible conjugative transposon Tn91 in the guts of gnotobiotic rats. Bahl MI, Sørensen SJ, Hansen LH, Licht TR, Appl Environ Microbiol 2004 70 758 764 10.1128/AEM.70.2.758-764.2004 14766552 (Pubitemid 38568196)
76. Conjugative transfer facilitates stable maintenance of IncP- plasmid pKJK5 in Escherichia coli cells colonizing the gastrointestinal tract of the germfree rat. Bahl MI, Hansen LH, Licht TR, Sørensen SJ, Appl Environ Microbiol 2007 73 341 343 10.1128/AEM.01971-06 17085707 (Pubitemid 46079970)
77. In vivo transfer of plasmid pRAS1 between Aeromonas salmonicida and Aeromonas hydrophila in artificially infected Cyprinus carpio L. Bello-Lopez JM, Fernandez-Rendon E, Curiel-Quesada E, J Fish Dis 2010 33 251 259 10.1111/j.1365-2761.2009.01118.x 20059637
78. Influence of reagents formulation on real-time PCR parameters. Burgos JS, Ramirez C, Tenorio R, Sastre I, Bullido MJ, Mol Cell Probe 2002 16 257 260 10.1006/mcpr.2002.0419