Subspecies Ilia and Illb salmonellae are defective for colonization of murine models of salmonellosis compared to Salmonella enterica subsp. i serovar typhimurium

Journal of Bacteriology

Volumn 191, Issue 8, 2009, Pages 2843-2850

  Katribe, Erin ^a,b   Bogomolnaya, Lydia M ^a   Wingert, Heather ^a   Andrews Polymenis, Helene ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BAGG ALBINO MOUSE; CBA MOUSE; CELL ADHESION; CONTROLLED STUDY; IN VITRO STUDY; INTESTINE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ARIZONAE; SALMONELLA ENTERICA; SALMONELLOSIS; ANIMAL; ANIMAL SALMONELLOSIS; BACTEREMIA; BACTERIAL COUNT; CELL LINE; GASTROINTESTINAL TRACT; LOCOMOTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; SALMONELLA TYPHIMURIUM; VIRULENCE;

ILIA; MAMMALIA; MURINAE; MUS; SALMONELLA; SALMONELLA ENTERICA SUBSP. ARIZONAE; SALMONELLA ENTERICA SUBSP. ENTERICA; VERTEBRATA;

VIRULENCE FACTOR;

ANIMALS; BACTEREMIA; BACTERIAL ADHESION; CELL LINE; COLONY COUNT, MICROBIAL; GASTROINTESTINAL TRACT; LOCOMOTION; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; SALMONELLA ARIZONAE; SALMONELLA ENTERICA; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; VIRULENCE; VIRULENCE FACTORS;

EID: 65249087827     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01223-08     Document Type: Article

References (61)

1. Alvseike, O., and E. Skjerve. 2002. Prevalence of a Salmonella subspecies diarizonae in Norwegian sheep herds. Prev. Vet. Med. 52:277-285.
2. Alvseike, O., T. Vardund, B. Lindstedt, E. Heir, E. Eriksson, and G. Kap- perud. 2004. Molecular epidemiology and population genetics of Salmonella subspecies diarizonae in sheep in Norway and Sweden. Epidemiol. Infect. 132:253-261.
3. Andrews-Polymenis, H. L., W. Rabsch, S. Porwollik, M. McClelland, C. Rosetti, L. G. Adams, and A. J. Baumler. 2004. Host restriction of Salmonella enterica serotype Typhimurium pigeon isolates does not correlate with loss of discrete genes. J. Bacteriol. 186:2619-2628.
4. Bajaj, V., R. L. Lucas, C. Hwang, and C. A. Lee. 1996. Co-odinate regulation of Salmonella typhimurium invasion genes by environmental factors is mediated by control of hilA expression. Mol. Microbiol. 22:703-714.
5. Baumler, A. J., R. M. Tsolis, and F. Heffron. 1996. Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium. Infect. Immun. 64:1862-1865.
6. Bemis, D. A., L. M. Grupka, S. Liamthong, D. W. Folland, J. M. Sykes, and E. C. Ramsay. 2007. Clonal relatedness of Salmonella isolates associated with invasive infections in captive and wild-caught rattlesnakes. Vet. Microbiol. 120:300-307.
7. Boyd, E. F., F.-S. Wang, T. S. Whittam, and R. K. Selander. 1996. Molecular genetic relationship of the salmonellae. Appl. Environ. Microbiol. 62:804-808.
8. Boyd, F. E., and D. L. Hartl. 1998. Salmonella virulence plasmid: modular acquisition of the spv virulence region by an F-plasmid in Salmonella enterica subspecies I and insertion into the chromosome in subspecies II, Ilia, IV, and VII isolates. Genetics 149:1183-1190.
9. Boyle, E. C., N. F. Brown, and B. B. Finlay. 2006. Salmonella enterica serovar Typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function. Cell. Microbiol. 8:1946-1957.
10. Brenner, F. W., R. G. Villar, F. J. Angulo, R. Tauxe, and B. Swaminathan. 2000. Salmonella nomenclature. J. Clin. Microbiol. 38:2465-2467.
11. Briones, V., S. Tellez, J. Goyache, C. Ballesteros, M. del Pilar Lanzarot, L. Dominguez, and J. F. Fernandez-Garayzabal. 2004. Salmonella diversity associated with wild reptiles and amphibians in Spain. Environ. Microbiol. 6:868-871.
12. Buchmeier, N. A., and F. Heffron. 1989. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect. Immun. 57:1-7.
13. Carlson, S. A., M. B. Omary, and B. D. Jones. 2002. Identification of cyto- keratins as accessory mediators of Salmonella entry into eukaryotic cells. Life Sci. 70:1415-1426.
14. Centers for Disease Control and Prevention. 1999. Reptile-associated salmonellosis-selected states, 1996-1998. Morbid. Mortal. Wkly. Rep. 48:1009-1013.
15. Chan, K., S. Baker, C. C. Kim, C. S. Detweiler, G. Dougan, and S. Falkow. 2003. Genomic comparison of Salmonella enterica serovars and Salmonella bongori by use of an S. enterica serovar Typhimurium DNA microarray. J.
16. Bacteriol. 185:553-563.
17. Collier-Hyams, L. S., H. Zeng, J. Sun, A. D. Tomlinson, Z. Q. Bao, H. Chen, J. L. Madara, K. Orth, and A. S. Neish. 2002. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J. Immunol. 169:2846-2850.
18. Coombes, B. K., N. F. Brown, Y. Valdez, J. H. Brumell, and B. Finlay. 2004. Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J. Biol. Chem. 279:49804-49815.
19. Crespo, R., J. S. Jeffrey, R. P. Chin, G. Senties-Cue, and H. L. Shivaprasad. 2004. Phenotypic and genotypic characterization of Salmonella arizonae from an integrated turkey operation. Avian Dis. 48:344-350.
20. Crosa, J. H., D. J. Brenner, W. H. Ewing, and S. Falkow. 1973. Molecular relationships among the salmonelleae. J. Bacteriol. 115:307-315.
21. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
22. Dorsey, C. W., M. C. Laarakker, A. D. Humphries, E. H. Weening, and A. J. Baumler. 2005. Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol. Microbiol. 57:196-211.
23. Ehrbar, K., S. Mirold, A. Friebel, S. Stender, and W. D. Hardt. 2002. Characterization of effector proteins translocated via the SPI1 type III secretion system of Salmonella typhimurium. Int. J. Med. Microbiol. 291:479-485.
24. Fields, P. I., R. V. Swanson, C. G. Haidaris, and F. Heffron. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. USA 83:5189-5193.
25. Galan, J. E., and R. Curtiss III. 1989. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86:6383-6387.
26. Galan, J. E., and R. Curtiss III. 1990. ExpressionofSalmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect. Immun. 58:1879-1885.
27. Hall, M. L., and B. Rowe. 1992. Salmonella arizonae in the United Kingdom from 1966 to 1990. Epidemiol. Infect. 108:59-65.
28. Hansen-Wester, I., and M. Hensel. 2002. Genome-based identification of chromosomal regions specific for Salmonella spp. Infect. Immun. 70:2351-2360.
29. Hayward, R. D., and V. Koronakis. 1999. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18:4926-4934.
30. Hensel, M., J. E. Shea, C. Gleeson, M. D. Jones, E. Dalton, and D. W. Holden. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400-403.
31. Hensel, M., J. E. Shea, S. R. Waterman, R. Mundy, T. Nikolaus, G. Banks, A. Vazquez-Torres, C. Gleeson, F. C. Fang, and D. W. Holden. 1998. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30:163-174.
32. Hernandez, L. D., M. Pypaert, R. A. Flavell, and J. E. Galan. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy.
33. J. Cell Biol. 163:1123-1131.
34. Hersh, D., D. M. Monack, M. R. Smith, N. Ghori, S. Falkow, and A. Zych-linsky. 1999. The salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. USA 96:2396-2401.
35. Jones, R. M., H. Wu, C. Wentworth, L. Luo, L. Collier-Hyams, and A. S. Neish. 2008. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 3:233-244.
36. Kim, H. J., S. H. Park, and H. Y. Kim. 2006. Comparison of Salmonella enterica serovar Typhimurium LT2 and non-LT2 Salmonella genomic sequences and genotyping of salmonellae by using PCR. Appl. Environ. Mi-crobiol. 72:6142-6151.
37. Kingsley, R. A., D. Abi Ghanem, N. Puebla-Osorio, A. M. Keestra, L. Bergh- man, and A. J. Baumler. 2004. Fibronectin binding to the Salmonella enterica serotype Typhimurium ShdA autotransporter protein is inhibited by a monoclonal antibody recognizing the A3 repeat. J. Bacteriol. 186:4931-4939.
38. Kingsley, R. A., A. D. Humphries, E. H. Weening, M. R. De Zoete, S. Winter, A. Papaconstantinopoulou, G. Dougan, and A. J. Baumler. 2003. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: identification of intestinal colonization and persistence determinants. Infect. Immun. 71:629-640.
39. Kingsley, R. A., K. van Amsterdam, N. Kramer, and A. J. Baumler. 2000. The shdA gene is restricted to serotypes of Salmonella enterica subspecies I and contributes to efficient and prolonged fecal shedding. Infect. Immun. 68:2720-2727.
40. Knodler, L. A., B. B. Finlay, and O. Steele-Mortimer. 2005. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J. Biol. Chem. 280:9058-9064.
41. Ledeboer, N. A., J. G. Frye, M. McClelland, and B. D. Jones. 2006. Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect. Immun. 74:3156-3169.
42. Libby, S. J., M. Lesnick, P. Hasegawa, M. Kurth, C. Belcher, J. Fierer, and D. G. Guiney. 2002. Characterization of the spv locus in Salmonella enterica serovar Arizona. Infect. Immun. 70:3290-3294.
43. Mirold, S., K. Ehrbar, A. Weissmuller, R. Prager, H. Tschape, H. Russmann, and W. D. Hardt. 2001. Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2. J. Bacteriol. 183:2348-2358.
44. Norris, F. A., M. P. Wilson, T. S. Wallis, E. E. Galyov, and P. W. Majerus. 1998. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl. Acad. Sci. USA 95:14057-14059.
45. Pasmans, F., A. Martel, F. Boyen, D. Vandekerchove, I. Wybo, F. V. Immer- seel, M. Heyndrickx, J. M. Collard, R. Ducatelle, and F. Haesebrouck. 2005. Characterization of Salmonella isolates from captive lizards. Vet. Microbiol. 110:285-291.
46. Patel, J. C., and J. E. Galan. 2006. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J. Cell Biol. 175:453-463.
47. Porwollik, S., R. M. Wong, and Michael McClelland. 2002. Evolutionary genomics of Salmonella: gene acquisitions revealed by microarray analysis. Proc. Natl. Acad. Sci. 99:8956-8961.
48. Prager, R., S. Mirold, E. Tietze, U. Strutz, B. Knuppel, W. Rabsch, W. D. Hardt, and H. Tschape. 2000. Prevalence and polymorphism of genes encoding translocated effector proteins among clinical isolates of Salmonella enterica. Int. J. Med. Microbiol. 290:605-617.
49. Raffatellu, M., R. P. Wilson, D. Chessa, H. Andrews-Polymenis, Q. T. Tran, S. Lawhon, S. Khare, L. G. Adams, and A. J. Baumler. 2005. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhi- murium invasion of epithelial cells. Infect. Immun. 73:146-154.
50. Scherer, C. A., E. Cooper, and S. I. Miller. 2000. The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol. Microbiol. 37:1133-1145.
51. Schroter, M., P. Roggentin, J. Hofmann, A. Speicher, R. Laufs, and D. Mack. 2004. Pet snakes as a reservoir for Salmonella enterica subsp. diarizonae (serogroup IIIb): a prospective study. Appl. Environ. Microbiol. 70:613-615.
52. Shivaprasad, H. L., P. Cortes, and R. Crespo. 2006. Otitis interna (labyrin- thitis) associated with Salmonella enterica arizonae in turkey poults. Avian Dis. 50:135-138.
53. Toguchi, A., M. Siano, M. Burkart, and R. M. Harshey. 2000. Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
54. Townsend, S. M., N. E. Kramer, R. Edwards, S. Baker, N. Hamlin, M. Simmonds, K. Stevens, S. Maloy, J. Parkhill, G. Dougan, and A. J. Baumler. 2001. Salmonella enterica serotype Typhi possesses a unique repertoire of fimbrial gene sequences. Infect. Immun. 69:2894-2901.
55. Tsolis, R. M., S. M. Townsend, E. A. Miao, S. I. Miller, T. A. Ficht, L. G. Adams, and A. J. Baumler. 1999. Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect. Immun. 67:6385-6393.
56. Washington University. 2008. Salmonella enterica subspecies IIIa (Ari- zonae) serovar 62:z4,z23:-. Washington University Genome Sequencing Center, St. Louis, MO. http://genome.wustl.edu/genome.cgi7GENOME =Salmonella%20enterica%20subspecies%20IIIa%20(Arizonae)%20serovar %2062:z4,z23:-.
57. Washington University. 2008. Salmonella enterica subspecies IIIa (Ari- zonae) serovar 62:z4,z23:-. Washington University Genome Sequencing Center, St. Louis, MO. http://genome.wustl.edu/genome.cgi7GENOME =Salmonella%20enterica%20subspecies%20IIIa%20(Diarizonae)%20serovar %2061:1,v:1,5,(7).
58. Waterman, S. H., G. Juarez, S. J. Carr, and L. Kilman. 1990. Salmonella arizona infections in Latinos associated with rattlesnake folk medicine. Am. J. Public Health 80:286-289.
59. Weening, E. H., J. D. Barker, M. C. Laarakker, A. D. Humphries, R. M. Tsolis, and A. J. Baumler. 2005. The Salmonella enterica serotype Typhi- murium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect. Immun. 73:3358-3366.
60. Weiss, S. H., M. J. Blase, F. P. Paleologo, R. E. Black, A. C. McWorther, M. A. Asbury, G. P. Carter, R. A. Feldman, and D. J. Brenner. 1986. Occurrence and distribution of serotypes of the Arizona subgroup of Salmonella strains in the United States from 1967 to 1976. J. Clin. Microbiol. 23:1056-1064.
61. Zhou, D., L. M. Chen, L. Hernandez, S. B. Shears, and J. E. Galan. 2001. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39:248-259.