Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence

Microbiology (United Kingdom)

Volumn 159, Issue PART7, 2013, Pages 1471-1486

  Santander, Javier ^a   Martin, Taylor ^b   Loh, Amanda ^b   Pohlenz, Camilo ^c   Gatlin, Delbert M ^c,d   Curtiss, Roy ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d TEXAS A AND M UNIVERSITY SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPOLYSACCHARIDE; POLYPEPTIDE ANTIBIOTIC AGENT; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE; URIDINE DIPHOSPHATE GLUCURONIC ACID;

ANTIBIOTIC RESISTANCE; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM COLONY; BIOFILM; CATFISH; CONTROLLED STUDY; EDWARDSIELLA ICTALURI; ENTERITIS; GENE DELETION; LYMPHOID TISSUE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; SYNTHESIS; ZEBRA FISH;

ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; AQUACULTURE; CATFISHES; DRUG RESISTANCE, BACTERIAL; EDWARDSIELLA ICTALURI; ENTEROBACTERIACEAE INFECTIONS; FISH DISEASES; GASTROINTESTINAL TRACT; INFLAMMATION; URIDINE DIPHOSPHATE GLUCOSE DEHYDROGENASE; VIRULENCE;

DANIO RERIO; EDWARDSIELLA (ENTEROBACTERIA); EDWARDSIELLA ICTALURI; ENTEROBACTERIACEAE; ICTALURUS PUNCTATUS;

EID: 84879805378     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.066639-0     Document Type: Article

References (83)

1. Aguirre, A., Lejona, S., Véscovi, E. G. & Soncini, F. C. (2000). Phosphorylated PmrA interacts with the promoter region of ugd in Salmonella enterica serovar typhimurium. J Bacteriol 182, 3874-3876.
2. Ali, S. A., Sarto, I. & Steinkasserer, A. (1997). Production of PCR mimics for any semiquantitative PCR application. Biotechniques 22, 1060-1062.
3. Bader, M. W., Sanowar, S., Daley, M. E., Schneider, A. R., Cho, U., Xu, W., Klevit, R. E., Le Moual, H. & Miller, S. I. (2005). Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122, 461-472.
4. Banemann, A. Deppisch, H. & Gross, R. (1998). The lipopolysac-charide of Bordetella bronchiseptica acts as a protective shield against antimicrobial peptides. Infect Immun 66, 5607-5612.
5. Bao, B. Peatman, E. Li, P. He, C. & Liu, Z. (2005). Catfish hepcidin gene is expressed in a wide range of tissues and exhibits tissue-specific upregulation after bacterial infection. Dev Comp Immunol 29, 939-950.
6. Bao, B., Peatman, E., Xu, P., Li, P., Zeng, H., He, C. & Liu, Z. (2006). The catfish liver-expressed antimicrobial peptide 2 (LEAP-2) gene is expressed in a wide range of tissues and developmentally regulated. Mol Immunol 43, 367-377.
7. Berczi, I., Bertók, L. & Bereznai, T. (1966). Comparative studies on the toxicity of Escherichia coli lipopolysaccharide endotoxin in various animal species. Can J Microbiol 12, 1070-1071.
8. Bertani, G. (1951). Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62, 293-300.
9. Bertolini, J. M., Cipriano, R. C., Pyle, S. W. & McLaughlin, J. J. (1990). Serological investigation of the fish pathogen Edwardsiella ictaluri, cause of enteric septicemia of catfish. J Wildl Dis 26, 246-252.
10. Bly, J. E. & Clem, L. W. (1991). Temperature-mediated processes in teleost immunity: in vitro immunosuppression induced by in vivo low temperature in channel catfish. Vet Immunol Immunopathol 28, 365-377.
11. Booth, N. J., Beekman, J. B. & Thune, R. L. (2009). Edwardsiella ictaluri encodes an acid-activated urease that is required for intracellular replication in channel catfish (Ictalurus punctatus) macrophages. Appl Environ Microbiol 75, 6712-6720.
12. Bowser, P. R. & Plumb, J. A. (1980). Fish cell lines: establishment of a line from ovaries of channel catfish. In Vitro 16, 365-368.
13. Breazeale, S. D., Ribeiro, A. A. & Raetz, C. R. (2002). Oxidative decarboxylation of UDP-glucuronic acid in extracts of polymyxin- resistant Escherichia coli. Origin of lipid A species modified with 4- amino-4-deoxy-L-arabinose. J Biol Chem 277, 2886-2896.
14. Brogden, K. A. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3, 238-250.
15. 2+ sensing by a novel PhoP- PhoQ two-component system for regulation of virulence in Edwardsiella tarda. J Biol Chem 285, 38876-38888.
16. Chandler, D. E. & Roberson, R. W. (2009). Bioimaging: Current Concepts in Light and Electron Microscopy. Sudbury, MA: Jones and Bartlett Publishers.
17. Clerton, P., Troutaud, D. & Deschaux, P. (1998). The chemilumin- escence response of leucocytes isolated from the gut of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 8, 73-76.
18. CLSI, Clinical and Laboratory Standards Institute. (2005a). Methods for antimicrobial disk susceptibility testing of bacteria isolated from aquatic animals; Proposed guideline. CLSI document M42-P. Wayne, PA: CLSI.
19. CLSI, Clinical and Laboratory Standards Institute. (2005b). Methods for broth dilution susceptibility testing of bacteria isolated from aquatic animals; Proposed guideline. CLSI document M49-P. Wayne, PA: CLSI.
20. De Soyza, A., Ellis, C. D., Khan, C. M., Corris, P. A. & Demarco de Hormaeche, R. (2004). Burkholderia cenocepacia lipopolysaccharide, lipid A, and proinflammatory activity. Am J Respir Crit Care Med 170, 70-77.
21. Dunham, R. A., Warr, G. W., Nichols, A., Duncan, P. L., Argue, B., Middleton, D. & Kucuktas, H. (2002). Enhanced bacterial disease resistance of transgenic channel catfish Ictalurus punctatus possessing cecropin genes. Mar Biotechnol (NY) 4, 338-344.
22. Edwards, R. A., Keller, L. H. & Schifferli, D. M. (1998). Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207, 149-157.
23. Ernst, R. K., Guina, T. & Miller, S. I. (1999). How intracellular bacteria survive: surface modifications that promote resistance to host innate immune responses. J Infect Dis 179 (Suppl 2), S326-S330.
24. Farnaud, S., Spiller, C., Moriarty, L. C., Patel, A., Gant, V., Odell, E. W. & Evans, R. W. (2004). Interactions of lactoferricin-derived peptides with LPS and antimicrobial activity. FEMS Microbiol Lett 233, 193-199.
25. Ganz, T. (2003). The role of antimicrobial peptides in innate immunity. Integr Comp Biol 43, 300-304.
26. Gunn, J. S., Hohmann, E. L. & Miller, S. I. (1996). Transcriptional regulation of Salmonella virulence: a PhoQ periplasmic domain mutation results in increased net phosphotransfer to PhoP. J Bacteriol 178, 6369-6373.
27. Guo, L., Lim, K. B., Gunn, J. S., Bainbridge, B., Darveau, R. P., Hackett, M. & Miller, S. I. (1997). Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276, 250-253.
28. Guo, L., Lim, K. B., Poduje, C. M., Daniel, M., Gunn, J. S., Hackett, M. & Miller, S. I. (1998). Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95, 189-198.
29. Hanson, T. & Sites, D. (2012). Catfish database 2011. http://aurora. auburn.edu/repo/bitstream/handle/11200/44174/2012%20Catfish% 20Database.pdf?sequence=1
30. 31P-NMR study. Mol Microbiol 11, 481-487.
31. Hitchcock, P. J. & Brown, T. M. (1983). Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154, 269-277.
32. Iliev, D. B., Roach, J. C., Mackenzie, S., Planas, J. V. & Goetz, F. W. (2005). Endotoxin recognition: in fish or not in fish? FEBS Lett 579, 6519-6528.
33. Kato, A., Latifi, T. & Groisman, E. A. (2003). Closing the loop: the PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proc Natl Acad Sci U S A 100, 4706-4711.
34. Knirel, Y. A., Dentovskaya, S. V., Bystrova, O. V., Kocharova, N. A., Senchenkova, S. N., Shaikhutdinova, R. Z., Titareva, G. M., Bakhteeva, I. V., Lindner, B. & other authors (2007). Relationship of the lipopolysaccharide structure of Yersinia pestis to resistance to antimicrobial factors. Adv Exp Med Biol 603, 88-96.
35. Kox, L. F., Wosten, M. M. & Groisman, E. A. (2000). A small protein that mediates the activation of a two-component system by another two-component system. EMBO J 19, 1861-1872.
36. Lawrence, M. L., Banes, M. M., Azadi, P. & Reeks, B. Y. (2003). The Edwardsiella ictaluri O polysaccharide biosynthesis gene cluster and the role of O polysaccharide in resistance to normal catfish serum and catfish neutrophils. Microbiology 149, 1409-1421.
37. Llobet, E., Tomás, J. M. & Bengoechea, J. A. (2008). Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 154, 3877-3886.
38. Lv, Y., Zheng, J., Yang, M., Wang, Q. & Zhang, Y. (2012). An Edwardsiella tarda mutant lacking UDP-glucose dehydrogenase shows pleiotropic phenotypes, attenuated virulence, and potential as a vaccine candidate. Vet Microbiol 160, 506-512.
39. McPhee, J. B., Lewenza, S. & Hancock, R. E. (2003). Cationic antimi- crobial peptides activate a two-component regulatory system, PmrA- PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50, 205-217.
40. Merkle, R. K. & Poppe, I. (1994). Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry. Methods Enzymol 230, 1-15.
41. Muyembe, T., Vandepitte, J. & Desmyter, J. (1973). Natural colistin resistance in Edwardsiella tarda. Antimicrob Agents Chemother 4, 521-524.
42. Nummila, K., Kilpelainen, I., Zahringer, U., Vaara, M. & Helander, I. M. (1995). Lipopolysaccharides of polymyxin B-resistant mutants of Escherichia coli are extensively substituted by 2-aminoethyl pyropho- sphate and contain aminoarabinose in lipid A. Mol Microbiol 16, 271-278.
43. Ortega, X. P., Cardona, S. T., Brown, A. R., Loutet, S. A., Flannagan, R. S., Campopiano, D. J., Govan, J. R. & Valvano, M. A. (2007). A putative gene cluster for aminoarabinose biosynthesis is essential for Burkholderia cenocepacia viability. J Bacteriol 189, 3639-3644.
44. Panangala, V. S., Russo, R., van Santen, V. L., Wolfe, K. G. & Klesius, P. H. (2009). Organization and sequence of four flagellin-encoding genes of Edwardsiella ictaluri. Aquaculture Res 40, 1135-1147.
45. Patrzykat, A., Friedrich, C. L., Zhang, L., Mendoza, V. & Hancock, R. E. (2002). Sublethal concentrations of pleurocidin-derived anti- microbial peptides inhibit macromolecular synthesis in Escherichia coli. Antimicrob Agents Chemother 46, 605-614.
46. Peschel, A. & Sahl, H. G. (2006). The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 4, 529-536.
47. Petrie-Hanson, L., Romano, C. L., Mackey, R. B., Khosravi, P., Hohn, C. M. & Boyle, C. R. (2007). Evaluation of zebrafish Danio rerio as a model for enteric septicemia of catfish (ESC). J Aquat Anim Health 19, 151-158.
48. Pohlenz, C., Buentello, A., Mwangi, W. & Gatlin, D. M., III (2012). Arginine and glutamine supplementation to culture media improves the performance of various channel catfish immune cells. Fish Shellfish Immunol 32, 762-768.
49. Pridgeon, J. W., Mu, X. & Klesius, P. H. (2012). Expression profiles of seven channel catfish antimicrobial peptides in response to Edwardsiella ictaluri infection. J Fish Dis 35, 227-237.
50. Raetz, C. R. & Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu Rev Biochem 71, 635-700.
51. Raetz, C. R., Guan, Z., Ingram, B. O., Six, D. A., Song, F., Wang, X. & Zhao, J. (2009). Discovery of new biosynthetic pathways: the lipid A story. J Lipid Res 50 (Suppl), S103-S108.
52. Raetzsch, C. F., Brooks, N. L., Alderman, J. M., Moore, K. S., Hosick, P. A., Klebanov, S., Akira, S., Bear, J. E., Baldwin, A. S. & other authors (2009). Lipopolysaccharide inhibition of glucose production through the Toll-like receptor-4, myeloid differentiation factor 88, and nuclear factor kb pathway. Hepatology 50, 592-600.
53. Rebeil, R., Ernst, R. K., Gowen, B. B., Miller, S. I. & Hinnebusch, B. J. (2004). Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol 52, 1363-1373.
54. Reinhardt, J. F., Fowlston, S., Jones, J. & George, W. L. (1985). Comparative in vitro activities of selected antimicrobial agents against Edwardsiella tarda. Antimicrob Agents Chemother 27, 966-967.
55. Roland, K., Curtiss, R., III & Sizemore, D. (1999). Construction and evaluation of a Dcya Dcrp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis 43, 429-441.
56. Santander, J. & Curtiss, R., III (2010). Intrinsic resistance of Edwardsiella ictaluri to cationic antimicrobial peptides is mediated by UDP-Glc dehydrogenase, an enzyme required for the O- polysaccharide synthesis. In 6th International Symposium on Aquatic Animal Health. Tampa, Florida, USA. http://aquaticpath.phhp.ufl. edu/isaah6/Oral.html#S11
57. Santander, J., Wanda, S. Y., Nickerson, C. A. & Curtiss, R., III (2007). Role of RpoS in fine-tuning the synthesis of Vi capsular polysacchar- ide in Salmonella enterica serotype Typhi. Infect Immun 75, 1382-1392.
58. Santander, J., Xin, W., Yang, Z. & Curtiss, R., III (2010). The aspartate- semialdehyde dehydrogenase of Edwardsiella ictaluri and its use as balanced-lethal system in fish vaccinology. PLoS ONE 5, e15944.
59. Santander, J., Mitra, A. & Curtiss, R., III (2011). Phenotype, virulence and immunogenicity of Edwardsiella ictaluri cyclic adenosine 39,59-monophosphate receptor protein (Crp) mutants in catfish host. Fish Shellfish Immunol 31, 1142-1153.
60. Santander, J., Golden, G., Wanda, S. Y. & Curtiss, R., III (2012). Fur- regulated iron uptake system of Edwardsiella ictaluri and its influence on pathogenesis and immunogenicity in the catfish host. Infect Immun 80, 2689-2703.
61. Secombes, C. J. (1990). Isolation of salmonid macrophages and analysis of their killing activity. In Techniques in Fish Immunology, p. 137e54. Edited by J. S. Stolen, T. C. Fletcher, D. P. Anderson, B. S. Roberson & W. B. van Muiswinkel. Fair Haven, NJ: SOS Publications.
62. Shoemaker, C. A., Klesius, P. H. & Plumb, J. A. (1997). Killing of Edwardsiella ictaluri by macrophages from channel catfish immune and susceptible to enteric septicemia of catfish. Vet Immunol Immunopathol 58, 181-190.
63. Shoemaker, C. A., Klesius, P. H., Arias, C. R. & Evans, J. J. (2009). Uses of modified live vaccines in the aquaculture. J World Aqua Soc 5, 573e85.
64. Shotts, E. B. & Waltman, W. D., II (1990). A medium for the selective isolation of Edwardsiella ictaluri. J Wildl Dis 26, 214-218.
65. Silipo, A., Molinaro, A., Cescutti, P., Bedini, E., Rizzo, R., Parrilli, M. & Lanzetta, R. (2005). Complete structural characterization of the lipid A fraction of a clinical strain of B. cepacia genomovar I lipopolysaccharide. Glycobiology 15, 561-570.
66. Sizemore, D. R., Elsinghorst, E. A., Eck, L. C., Branstrom, A. A., Hoover, D. L., Warren, R. L. & Rubin, F. A. (1997). Interaction of Salmonella typhi strains with cultured human monocyte-derived macrophages. Infect Immun 65, 309-312.
67. Skurnik, M., Venho, R., Bengoechea, J. A. & Moriyón, I. (1999). The lipopolysaccharide outer core of Yersinia enterocolitica serotype O: 3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31, 1443-1462.
68. Stock, I. & Wiedemann, B. (2001). Natural antibiotic susceptibilities of Edwardsiella tarda, E. ictaluri, and E. hoshinae. Antimicrob Agents Chemother 45, 2245-2255.
69. Strominger, J. L. (1957). Microbial uridine-59-pyrophosphate N- acetylamino sugar compounds. I. Biology of the penicillin-induced accumulation. J Biol Chem 224, 509-523.
70. Swain, P., Nayak, S. K., Nanda, P. K. & Dash, S. (2008). Biological effects of bacterial lipopolysaccharide (endotoxin) in fish: a review. Fish Shellfish Immunol 25, 191-201.
71. Tatner, M. F. & Horne, M. T. (1983). Susceptibility and immunity to Vibrio anguillarum in post-hatching rainbow trout fry, Salmo gairdneri Richardson 1836. Dev Comp Immunol 7, 465-472.
72. Tran, A. X., Lester, M. E., Stead, C. M., Raetz, C. R., Maskell, D. J., McGrath, S. C., Cotter, R. J. & Trent, M. S. (2005). Resistance to the antimicrobial peptide polymyxin requires myristoylation of Escherichia coli and Salmonella typhimurium lipid A. J Biol Chem 280, 28186-28194.
73. Trent, M. S., Ribeiro, A. A., Lin, S., Cotter, R. J. & Raetz, C. R. (2001). An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4-amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor. J Biol Chem 276, 43122-43131.
74. Tsai, C. M. & Frasch, C. E. (1982). A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119, 115- 119.
75. Vaara, M., Vaara, T., Jensen, M., Helander, I., Nurminen, M., Rietschel, E. T. & Makela, P. H. (1981). Characterization of the lipopolysaccharide from the polymyxin-resistant pmrA mutants of Salmonella typhimurium. FEBS Lett 129, 145-149.
76. Vinogradov, E., Nossova, L., Perry, M. B. & Kay, W. W. (2005). The structure of the antigenic O-polysaccharide of the lipopolysaccharide of Edwardsiella ictaluri strain MT104. Carbohydr Res 340, 1509- 1513.
77. Wang, Q., Wang, Y., Xu, P. & Liu, Z. (2006). NK-lysin of channel catfish: gene triplication, sequence variation, and expression analysis. Mol Immunol 43, 1676-1686.
78. Whitfield, C. (2006). Biosynthesis and assembly of capsular poly- saccharides in Escherichia coli. Annu Rev Biochem 75, 39-68.
79. Winfield, M. D., Latifi, T. & Groisman, E. A. (2005). Transcriptional regulation of the 4-amino-4-deoxy-L-arabinose biosynthetic genes in Yersinia pestis. J Biol Chem 280, 14765-14772.
80. Wosten, M. M. & Groisman, E. A. (1999). Molecular characterization of the PmrA regulon. J Biol Chem 274, 27185-27190.
81. Xu, P., Bao, B., He, Q., Peatman, E., He, C. & Liu, Z. (2005). Characterization and expression analysis of bactericidal permeability- increasing protein (BPI) antimicrobial peptide gene from channel catfish Ictalurus punctatus. Dev Comp Immunol 29, 865-878.
82. Yi, E. C. & Hackett, M. (2000). Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst (Lond) 125, 651-656.
83. Zanetti, M. (2004). Cathelicidins, multifunctional peptides of the innate immunity. J Leukoc Biol 75, 39-48.