Phenotype, virulence and immunogenicity of Edwardsiella ictaluri cyclic adenosine 3',5'-monophosphate receptor protein (Crp) mutants in catfish host

Fish and Shellfish Immunology

Volumn 31, Issue 6, 2011, Pages 1142-1153

  Santander, Javier ^a,b   Mitra, Arindam ^a   Curtiss, Roy ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Catfish; Crp; Edwardsiella ictaluri; Live attenuated vaccines

Indexed keywords

AVES; BACTERIA (MICROORGANISMS); DANIO RERIO; EDWARDSIELLA ICTALURI; ENTEROBACTERIACEAE; ICTALURUS PUNCTATUS; MAMMALIA; SALMONELLA ENTERICA;

EID: 81255157535     PISSN: 10504648     EISSN: 10959947     Source Type: Journal    
DOI: 10.1016/j.fsi.2011.10.009     Document Type: Article

References (85)

1. Hawke J.P., McWhorter A.C., Steigerwalt A.G., Brenner D.J. Edwardsiella ictaluri sp. nov., the causative agent of enteric septicemia of catfish. Int J Syst Bacteriol 1981, 31:396-440.
2. Shoemaker C.A., Klesius P.H., Arias C.R., Evans J.J. Uses of modified live vaccines in the aquaculture. J World Aqua Soc 2009, 5:573-585.
3. Baldwin T.J., Newton J.C. Pathogenesis of enteric septicemia of channel catfish, caused by Edwardsiella ictaluri: bacteriologic and light and electron microscopic findings. J Aquat Anim Health 1993, 5:189-198.
4. Morrison E.E., Plumb J.A. Olfactory organ of channel catfish as a site of experimental Edwardsiella ictaluri infection. J Aquat Anim Health 1994, 6:101-109.
5. Booth N.J., ElKamel A., Thune R.L. Intracellular replication of Edwardsiella ictaluri in channel catfish macrophages. J Aquat Anim Health 2006, 18:101-108.
6. Menanteau-Ledouble S., Karsi A., Lawrence M.L. Importance of skin abrasion as a primary site of adhesion for Edwardsiella ictaluri and impact on invasion and systematic infection in channel catfish Ictalurus punctatus. Vet Microbiol 2011, 148:425-430.
7. Nusbaum K.E., Morrison E.E. Entry of 35S-labelled Edwardsiella ictaluri into channel catfish. J Aquat Anim Health 1996, 8:146-149.
8. Thune R.L., Collins L.A., Pena M.P. A comparison of immersion, immersion/oral combination and injection methods for the vaccination of channel catfish Ictalurus punctatus against Edwardsiella ictaluri. J World Aqua Soc 1997, 28:193-201.
9. Klesius P.H., Shoemaker C.A. Development and use of modified live Edwardsiella ictaluri vaccine against enteric septicemia of catfish. Adv Vet Med 1999, 41:523-537.
10. Williams M.L., Lawrence M.L. Identification and characterization of a two-component hemolysin from Edwardsiella ictaluri. Vet Microbiol 2005, 108:281-289.
11. Shoemaker C.A., Klesius P.H., Bricker J.M. Efficacy of a modified live Edwardsiella ictaluri vaccine in channel catfish as young as seven days post hatch. Aquaculture 1999, 176:189-193.
12. Jin D.J., Walter W.A., Gross C.A. Characterization of the termination phenotypes of rifampicin-resistant mutants. J Mol Biol 1988, 202:245-253.
13. Jin D.J., Gross C.A. Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J Mol Biol 1988, 202:45-58.
14. Jin D.J., Cashel M., Friedman D.I., Nakamura Y., Walter W.A., Gross C.A. Effects of rifampicin resistant rpoB mutations on antitermination and interaction with nusA in Escherichia coli. J Mol Biol 1988, 204:247-261.
15. Klesius PH, Shoemaker CA. Modified live Edwardsiella ictaluri against enteric septicemia in channel catfish. In: University A, editor. United States Patent; 2000.
16. Arias C.R., Shoemaker C.A., Evans J.J., Klesius P.H. A comparative study of Edwardsiella ictaluri parent (EILO) and E. ictaluri rifampicin-mutant (RE-33) isolates using lipopolysaccharides, outer membrane proteins, fatty acids, Biolog, API 20E and genomic analyses. J Fish Dis 2003, 26:415-421.
17. Busby S., Ebright R.H. Transcription activation by catabolite activator protein (CAP). J Mol Biol 1999, 293:199-213.
18. Grainger D.C., Hurd D., Harrison M., Holdstock J., Busby S.J. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 2005, 102:17693-17698.
19. Botsford J.L., Harman J.G. Cyclic AMP in prokaryotes. Microbiol Rev 1992, 56:100-122.
20. Curtiss R., Kelly S.M. Salmonella typhimurium deletion mutants lacking adenylate cyclase and cyclic AMP receptor protein are avirulent and immunogenic. Infect Immun 1987, 55:3035-3043.
21. Petersen S., Young G.M. Essential role for cyclic AMP and its receptor protein in Yersinia enterocolitica virulence. Infect Immun 2002, 70:3665-3672.
22. Skorupski K., Taylor R.K. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc Natl Acad Sci U S A 1997, 94:265-270.
23. Stapleton M., Haq I., Hunt D.M., Arnvig K.B., Artymiuk P.J., Buxton R.S., et al. Mycobacterium tuberculosis cAMP receptor protein (Rv3676) differs from the Escherichia coli paradigm in its cAMP binding and DNA binding properties and transcription activation properties. J Biol Chem 2010, 285:7016-7027.
24. De Lay N., Gottesman S. The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 2009, 191:461-476.
25. Ahmer B.M., van Reeuwijk J., Watson P.R., Wallis T.S., Heffron F. Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol Microbiol 1999, 31:971-982.
26. Johnston C., Pegues D.A., Hueck C.J., Lee A., Miller S.I. Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 1996, 22:715-727.
27. Eisenstein B.I., Beachey E.H., Solomon S.S. Divergent effects of cyclic adenosine 3',5'-monophosphate on formation of type 1 fimbriae in different K-12 strains of Escherichia coli. J Bacteriol 1981, 145:620-623.
28. O'Byrne C.P., Dorman C.J. The spv virulence operon of Salmonella typhimurium LT2 is regulated negatively by the cyclic AMP (cAMP)-cAMP receptor protein system. J Bacteriol 1994, 176:905-912.
29. Fang F.C., Chen C.Y., Guiney D.G., Xu Y. Identification of sigma S-regulated genes in Salmonella typhimurium: complementary regulatory interactions between sigma S and cyclic AMP receptor protein. J Bacteriol 1996, 178:5112-5120.
30. Kelly S.M., Bosecker B.A., Curtiss R. Characterization and protective properties of attenuated mutants of Salmonella choleraesuis. Infect Immun 1992, 60:4881-4890.
31. Rosu V., Chadfield M.S., Santona A., Christensen J.P., Thomsen L.E., Rubino S., et al. Effects of crp deletion in Salmonella enterica serotype Gallinarum. Acta Vet Scand 2007, 49:14.
32. Zhan L., Han Y., Yang L., Geng J., Li Y., Gao H., et al. The cyclic AMP receptor protein, CRP, is required for both virulence and expression of the minimal CRP regulon in Yersinia pestis biovar microtus. Infect Immun 2008, 76:5028-5037.
33. Thune R.L., Fernandez D.H., Benoit J.L., Kelly-Smith M., Rogge M.L., Booth N.J., et al. Signature-tagged mutagenesis of Edwardsiella ictaluri identifies virulence-related genes, including a Salmonella pathogenicity island 2 class of type III secretion systems. Appl Environ Microbiol 2007, 73:7934-7946.
34. Santander J., Xin W., Yang Z., Curtiss R. The aspartate-semialdehyde dehydrogenase of Edwardsiella ictaluri and its use as balanced-lethal system in fish vaccinology. Plos One 2010, 5:e15944.
35. Bertani G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 1951, 62:293-300.
36. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
37. Soding J., Biegert A., Lupas A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 2005, 33:W244-W248.
38. Santander J., Wanda S.Y., Nickerson C.A., Curtiss R. Role of RpoS in fine-tuning the synthesis of Vi capsular polysaccharide in Salmonella enterica serotype Typhi. Infect Immun 2007, 75:1382-1392.
39. Roland K., Curtiss R., Sizemore D. Construction and evaluation of a delta cya delta crp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis 1999, 43:429-441.
40. Edwards R.A., Keller L.H., Schifferli D.M. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 1998, 207:149-157.
41. Chang A.C., Cohen S.N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 1978, 134:1141-1156.
42. Panangala Victor S., Russo R., van Santen Vicky L., Wolfe Karen G., Klesius Phillip H. Organization and sequence of four flagellin-encoding genes of Edwardsiella ictaluri. Aqua Res 2009, 40:1135-1147.
43. Chandler D.E., Roberson R.W. Bioimaging: current concepts in light and electron microscopy 2009, Jones and Bartlett Publishers, Sudbury, Mass.
44. Sambrook J., Russell W. Molecular cloning; a laboratory manual 2001, Cold Spring Harbor Press.
45. Petrie-Hanson L., Romano C.L., Mackey R.B., Khosravi P., Hohn C.M., Boyle C.R. Evaluation of zebrafish Danio rerio as a model for enteric septicemia of catfish (ESC). J Aquat Anim Health 2007, 19:151-158.
46. Curtiss R. Chromosomal aberrations associated with mutations to bacteriophage resistance in Escherichia coli. J Bacteriol 1965, 89:28-40.
47. Anderson D.P. Fish immunology. Fish immunology 1984, 110-113. China Agriculture Press, Beijing. S.D. Hua (Ed.).
48. Puente J.L., Juarez D., Bobadilla M., Arias C.F., Calva E. The Salmonella ompC gene: structure and use as a carrier for heterologous sequences. Gene 1995, 156:1-9.
49. Yi E.C., Hackett M. Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 2000, 125:651-656.
50. Hitchcock P.J., Brown T.M. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 1983, 154:269-277.
51. Tsai C.M., Frasch C.E. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 1982, 119:115-119.
52. Maki J.L., Dickerson H.W. Systemic and cutaneous mucus antibody responses of channel catfish immunized against the protozoan parasite Ichthyophthirius multifiliis. Clin Diagn Lab Immunol 2003, 10:876-881.
53. Harman J.G. Allosteric regulation of the cAMP receptor protein. Biochim Biophys Acta 2001, 1547:1-17.
54. Chapon C. Expression of malT, the regulator gene of the maltose region in Escherichia coli, is limited both at transcription and translation. EMBO J 1982, 1:369-374.
55. Chapon C. Role of the catabolite activator protein in the maltose regulon of Escherichia coli. J Bacteriol 1982, 150:722-729.
56. Daniel J. Enzyme III stimulation of cyclic AMP synthesis in an Escherichia coli crp mutant. J Bacteriol 1984, 157:940-941.
57. Hohn C., Lee S.R., Pinchuk L.M., Petrie-Hanson L. Zebrafish kidney phagocytes utilize macropinocytosis and Ca+-dependent endocytic mechanisms. Plos One 2009, 4:e4314.
58. Pressley M.E., Phelan P.E., Witten P.E., Mellon M.T., Kim C.H. Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev Comp Immunol 2005, 29:501-513.
59. O'Toole R., Von Hofsten J., Rosqvist R., Olsson P.E., Wolf-Watz H. Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum. Microb Pathog 2004, 37:41-46.
60. Lin B., Chen S., Cao Z., Lin Y., Mo D., Zhang H., et al. Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals. Mol Immunol 2007, 44:295-301.
61. Rombout J.W., Blok L.J., Lamers C.H., Egberts E. Immunization of carp (Cyprinus carpio) with a Vibrio anguillarum bacterin: indications for a common mucosal immune system. Dev Comp Immunol 1986, 10:341-351.
62. Lobb C.J. Secretory immunity induced in catfish, Ictalurus punctatus, following bath immunization. Dev Comp Immunol 1987, 11:727-738.
63. Cain K.D., Jones D.R., Raison R.L. Characterisation of mucosal and systemic immune responses in rainbow trout (Oncorhynchus mykiss) using surface plasmon resonance. Fish Shellfish Immunol 2000, 10:651-666.
64. Esteve C., Birbeck T.H. Secretion of haemolysins and proteases by Aeromonas hydrophila EO63: separation and characterization of the serine protease (caseinase) and the metalloprotease (elastase). J Appl Microbiol 2004, 96:994-1001.
65. Hamuro K., Suetake H., Saha N.R., Kikuchi K., Suzuki Y. A teleost polymeric Ig receptor exhibiting two Ig-like domains transports tetrameric IgM into the skin. J Immunol 2007, 178:5682-5689.
66. Berman H.M., Ten Eyck L.F., Goodsell D.S., Haste N.M., Kornev A., Taylor S.S. The cAMP binding domain: an ancient signaling module. Proc Natl Acad Sci U S A 2005, 102:45-50.
67. Toyoda K., Teramoto H., Inui M., Yukawa H. Genome-wide identification of in vivo binding sites of GlxR, a cyclic AMP receptor protein-type regulator in Corynebacterium glutamicum. J Bacteriol 2011, 193:4123-4133.
68. Kolb A., Igarashi K., Ishihama A., Lavigne M., Buckle M., Buc H. E. coli RNA polymerase, deleted in the C-terminal part of its alpha-subunit, interacts differently with the cAMP-CRP complex at the lacP1 and at the galP1 promoter. Nucleic Acids Res 1993, 21:319-326.
69. Chandler M.S. The gene encoding cAMP receptor protein is required for competence development in Haemophilus influenzae Rd. Proc Natl Acad Sci U S A 1992, 89:1626-1630.
70. Cameron A.D., Redfield R.J. Non-canonical CRP sites control competence regulons in Escherichia coli and many other gamma-proteobacteria. Nucleic Acids Res 2006, 34:6001-6014.
71. Agari Y., Kashihara A., Yokoyama S., Kuramitsu S., Shinkai A. Global gene expression mediated by Thermus thermophilus SdrP, a CRP/FNR family transcriptional regulator. Mol Microbiol 2008, 70:60-75.
72. Rickman L., Scott C., Hunt D.M., Hutchinson T., Menendez M.C., Whalan R., et al. A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol Microbiol 2005, 56:1274-1286.
73. Sun W., Roland K.L., Kuang X., Branger C.G., Curtiss R. Yersinia pestis with regulated delayed attenuation as a vaccine candidate to induce protective immunity against plague. Infect Immun 2010, 78:1304-1313.
74. Kennedy M.J., Yancey R.J., Sanchez M.S., Rzepkowski R.A., Kelly S.M., Curtiss R. Attenuation and immunogenicity of Δcya Δcrp derivatives of Salmonella choleraesuis in pigs. Infect Immun 1999, 67:4628-4636.
75. Wolfgang M.C., Lee V.T., Gilmore M.E., Lory S. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 2003, 4:253-263.
76. de Crecy-Lagard V., Glaser P., Lejeune P., Sismeiro O., Barber C.E., Daniels M.J., et al. A Xanthomonas campestris pv. campestris protein similar to catabolite activation factor is involved in regulation of phytopathogenicity. J Bacteriol 1990, 172:5877-5883.
77. Sheoran A.S., Timoney J.F., Tinge S.A., Sundaram P., Curtiss R. Intranasal immunogenicity of a Δcya Δcrp-pabA mutant of Salmonella enterica serotype Typhimurium for the horse. Vaccine 2001, 19:3787-3795.
78. Flajnik M.F., Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 2010, 11:47-59.
79. Zhang Y.A., Salinas I., Li J., Parra D., Bjork S., Xu Z., et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol 2010, 11:827-835.
80. Frey S.E., Bollen W., Sizemore D., Campbell M., Curtiss R. Bacteremia associated with live attenuated chi8110 Salmonella enterica serovar Typhi ISP1820 in healthy adult volunteers. Clin Immunol 2001, 101:32-37.
81. Tacket C.O., Hone D.M., Curtiss R.I.I.I., Kelly S.M., Losonsky G., Guers L., et al. Comparison of the safety and immunogenicity of delta aroC delta aroD and delta cya delta crp Salmonella typhi strains in adult volunteers. Infect Immun 1992, 60:536-541.
82. Hassan J.O., Curtiss R. Control of colonization by virulent Salmonella typhimurium by oral immunization of chickens with avirulent delta cya delta crp S. typhimurium. Res Microbiol 1990, 141:839-850.
83. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
84. Nei M., Kumar S. Molecular evolution and phylogenetics 2000, Oxford University Press, Oxford; New York.
85. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.