Gallbladder epithelium as a niche for chronic salmonella carriage

Infection and Immunity

Volumn 81, Issue 8, 2013, Pages 2920-2930

  Gonzalez Escobedo, Geoffrey ^a   Gunn, John S ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BILE; BIOFILM; CELL DIVISION; CELL SURFACE; CONTROLLED STUDY; EPITHELIUM CELL; GALLBLADDER EPITHELIUM; IN VIVO STUDY; INOCULATION; NEUTROPHIL; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; SALMONELLA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TYPHOID FEVER;

ANIMALS; BIOFILMS; CARRIER STATE; EPITHELIUM; FEMALE; GALLBLADDER; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; SALMONELLA; SALMONELLA INFECTIONS, ANIMAL; TYPHOID FEVER;

EID: 84880663299     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00258-13     Document Type: Article

References (59)

1. Crump JA, Luby SP, Mintz ED. 2004. The global burden of typhoid fever. Bull. World Health Organ. 82:346-353.
2. Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, Brown W, Le M, Berggren R, Parks WT, Fang FC. 1999. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401: 804-808.
3. Levine MM, Black RE, Lanata C. 1982. Precise estimation of the numbers of chronic carriers of Salmonella Typhi in Santiago, Chile, an endemic area. J. Infect. Dis. 146:724-726.
4. Merselis JG, Jr, Kaye D, Connolly CS, Hook EW. 1964. Quantitative bacteriology of the typhoid carrier state. Am. J. Trop. Med. Hyg. 13:425-429.
5. Vogelsang TM, Boe J. 1948. Temporary and chronic carriers of Salmonella Typhi and Salmonella Paratyphi B. J. Hyg. (Lond.) 46:252-261.
6. Dongol S, Thompson CN, Clare S, Nga TV, Duy PT, Karkey A, Arjyal A, Koirala S, Khatri NS, Maskey P, Poudel S, Jaiswal VK, Vaidya S, Dougan G, Farrar JJ, Dolecek C, Basnyat B, Baker S. 2012. The microbiological and clinical characteristics of invasive Salmonella in gallbladders from cholecystectomy patients in Kathmandu, Nepal. PLoS One 7:e47342. doi :10.1371/journal.pone.0047342.
7. Sinnott CR, Teall AJ. 1987. Persistent gallbladder carriage of Salmonella Typhi. Lancet i:976.
8. Shpargel JS, Berardi RS, Lenz D. 1985. Salmonella Typhi carrier state 52 years after illness with typhoid fever: a case study. Am. J. Infect. Control 13:122-123.
9. Caygill CP, Hill MJ, Braddick M, Sharp JC. 1994. Cancer mortality in chronic typhoid and paratyphoid carriers. Lancet 343:83-84.
10. Shukla VK, Singh H, Pandey M, Upadhyay SK, Nath G. 2000. Carcinoma of the gallbladder-is it a sequel of typhoid? Dig. Dis. Sci. 45:900-903.
11. Gonzalez-Escobedo G, Marshall JM, Gunn JS. 2011. Chronic and acute infection of the gall bladder by Salmonella Typhi: understanding the carrier state. Nat. Rev. Microbiol. 9:9-14.
12. Monds RD, O'Toole GA. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17:73-87.
13. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
14. Schioler H, Christiansen ED, Hoybye G, Rasmussen SN, Greibe J. 1983. Biliary calculi in chronic Salmonella carriers and healthy controls: a controlled study. Scand. J. Infect. Dis. 15:17-19.
15. Karaki K, Matsubara Y. 1984. Surgical treatment of chronic biliary typhoid and paratyphoid carriers. Nihon Shokakibyo Gakkai Zasshi. 81: 2978-2985. (In Japanese.)
16. Crawford RW, Rosales-Reyes R, Ramirez-Aguilar Mde L, Chapa-Azuela O, Alpuche-Aranda C, Gunn JS. 2010. Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc. Natl. Acad. Sci. U. S. A. 107:4353-4358.
17. Prouty AM, Schwesinger WH, Gunn JS. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect. Im-mun. 70:2640-2649.
18. Sharma V, Chauhan VS, Nath G, Kumar A, Shukla VK. 2007. Role of bile bacteria in gallbladder carcinoma. Hepatogastroenterology 54:1622-1625.
19. Vaishnavi C, Singh S, Kochhar R, Bhasin D, Singh G, Singh K. 2005. Prevalence of Salmonella enterica serovar Typhi in bile and stool of patients with biliary diseases and those requiring biliary drainage for other purposes. Jpn. J. Infect. Dis. 58:363-365.
20. Menendez A, Arena ET, Guttman JA, Thorson L, Vallance BA, Vogl W, Finlay BB. 2009. Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J. Infect. Dis. 200:1703-1713.
21. Ledeboer NA, Jones BD. 2005. Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar Typhimurium on HEp-2 cells and chicken intestinal epithelium. J. Bacteriol. 187:3214-3226.
22. Finlay BB, Ruschkowski S, Dedhar S. 1991. Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci. 99:283-296.
23. Knodler LA, Vallance BA, Celli J, Winfree S, Hansen B, Montero M, Steele-Mortimer O. 2010. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc. Natl. Acad. Sci. U. S. A. 107:17733-17738.
24. Kuver R, Savard C, Oda D, Lee SP. 1994. PGE generates intracellular cAMP and accelerates mucin secretion by cultured dog gallbladder epithelial cells. Am. J. Physiol. 267:G998-1003.
25. Klinkspoor JH, Kuver R, Savard CE, Oda D, Azzouz H, Tytgat GN, Groen AK, Lee SP. 1995. Model bile and bile salts accelerate mucin secretion by cultured dog gallbladder epithelial cells. Gastroenterology 109:264-274.
26. Yoshida T, Klinkspoor JH, Kuver R, Wrenn SP, Kaler EW, Lee SP. 2000. Cholestan-3β,5a,6β-triol, but not 7-ketocholesterol, suppresses tauro-cholate-induced mucin secretion by cultured dog gallbladder epithelial cells. FEBS Lett. 478:113-118.
27. Klinkspoor JH, Yoshida T, Lee SP. 1998. Bile salts stimulate mucin secretion by cultured dog gallbladder epithelial cells independent of their detergent effect. Biochem. J. 332:257-262.
28. Choi J, Klinkspoor JH, Yoshida T, Lee SP. 1999. Lipopolysaccharide from Escherichia colt stimulates mucin secretion by cultured dog gallbladder epithelial cells. Hepatology 29:1352-1357.
29. Malik R, Lee SK, Savard CE, Oda D, Wong WS, Chan BY, Lee SP. 1997. The effect of N-methyl-W-nitro-N-nitrosoguanidine on cultured dog gallbladder epithelial cells. Hepatology 26:1296-1302.
30. Wagner C, Polke M, Gerlach RG, Linke D, Stierhof YD, Schwarz H, Hensel M. 2011. Functional dissection of SiiE, a giant non-fimbrial adhe-sin of Salmonella enterica. Cell. Microbiol. 13:1286-1301.
31. Bishop A, House D, Perkins T, Baker S, Kingsley RA, Dougan G. 2008. Interaction of Salmonella enterica serovar Typhi with cultured epithelial cells: roles of surface structures in adhesion and invasion. Microbiology 154:1914-1926.
32. Raffatellu M, Wilson RP, Chessa D, Andrews-Polymenis H, Tran QT, Lawhon S, Khare S, Adams LG, Baumler AJ. 2005. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect. Immun. 73:146-154.
33. Begley M, Gahan CG, Hill C. 2005. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29:625-651.
34. Zen Y, Harada K, Sasaki M, Tsuneyama K, Katayanagi K, Yamamoto Y, Nakanuma Y. 2002. Lipopolysaccharide induces overexpression of MUC2 and MUC5AC in cultured biliary epithelial cells: possible key phenomenon of hepatolithiasis. Am. J. Pathol. 161:1475-1484.
35. Prouty AM, Brodsky IE, Falkow S, Gunn JS. 2004. Bile-salt-mediated induction of antimicrobial and bile resistance in Salmonella Typhimurium. Microbiology 150:775-783.
36. Prouty AM, Brodsky IE, Manos J, Belas R, Falkow S, Gunn JS. 2004. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41:177-185.
37. Prouty AM, Gunn JS. 2000. Salmonella enterica serovar Typhimurium invasion is repressed in the presence of bile. Infect. Immun. 68:6763-6769.
38. Crawford RW, Gibson DL, Kay WW, Gunn JS. 2008. Identification of a bile-induced exopolysaccharide required for Salmonella biofilm formation on gallstone surfaces. Infect. Immun. 76:5341-5349.
39. de Jong HK, Parry CM, van der Poll T, Wiersinga WJ. 2012. Host-pathogen interaction in invasive salmonellosis. PLoS Pathog. 8:e1002933. doi: 10.1371/journal.ppat.1002933.
40. Sivula CP, Bogomolnaya LM, Andrews-Polymenis HL. 2008. A comparison of cecal colonization of Salmonella enterica serotype Typhimurium in white leghorn chicks and Sa/mone/Za-resistant mice. BMC Microbiol. 8:182. doi: 10.1186/1471-2180-8-182.
41. Boddicker JD, Ledeboer NA, Jagnow J, Jones BD, Clegg S. 2002. Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol. Microbiol. 45:1255-1265.
42. Dwyer BE, Newton KL, Kisiela D, Sokurenko EV, Clegg S. 2011. Single nucleotide polymorphisms of fimH associated with adherence and biofilm formation by serovars of Salmonella enterica. Microbiology 157:3162-3171.
43. Ledeboer NA, Frye JG, McClelland M, Jones BD. 2006. Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafifimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect. Immun. 74:3156-3169.
44. Norris TL, Kingsley RA, Bumler AJ. 1998. Expression and transcrip-tional control of the Salmonella Typhimurium lpf fimbrial operon by phase variation. Mol. Microbiol. 29:311-320.
45. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, Baumler AJ. 2005. The Salmonella enterica serotype Typhimurium lpf bcf, stb, sic, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect. Immun. 73:3358-3366.
46. Crawford RW, Reeve KE, Gunn JS. 2010. Flagellated but not hyperfim-briated Salmonella enterica serovar Typhimurium attaches to and forms biofilms on cholesterol-coated surfaces. J. Bacteriol. 192:2981-2990.
47. Jonas K, Tomenius H, Kader A, Normark S, Romling U, Belova LM, Melefors O.2007. Roles of curli, cellulose and BapAin Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol. 7:70. doi: 10.1186/1471-2180-7-70.
48. Jain S, Chen J. 2007. Attachment and biofilm formation by various sero-types of Salmonella as influenced by cellulose production and thin aggregative fimbriae biosynthesis. J. Food Prot. 70:2473-2479.
49. Austin JW, Sanders G, Kay WW, Collinson SK. 1998. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162:295-301.
50. Romling U, Sierralta WD, Eriksson K, Normark S. 1998. Multicellular and aggregative behaviour of Salmonella Typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249-264.
51. Sukupolvi S, Lorenz RG, Gordon JI, Bian Z, Pfeifer JD, Normark SJ, Rhen M. 1997. Expression of thin aggregative fimbriae promotes interaction of Salmonella Typhimurium SR-11 with mouse small intestinal epithelial cells. Infect. Immun. 65:5320-5325.
52. Barak JD, Gorski L, Naraghi-Arani P, Charkowski AO. 2005. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microbiol. 71:5685-5691.
53. S)-regulated genes in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182:5749-5756.
54. S). Mol. Microbiol. 39:1533-1545.
55. Beraud M, Kolb A, Monteil V, D'Alayer J, Norel F. 2010. A proteomic analysis reveals differential regulation of the yciGFE(katN) locus by YncC and HNS in Salmonella and Escherichia coli K-12. Mol. Cell. Proteomics 9:2601-2616.
56. Prouty AM, Gunn JS. 2003. Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass. Infect. Immun. 71:7154-7158.
57. Finzi L, Barbu V, Burgel PR, Mergey M, Kirkwood KS, Wick EC, Scoazec JY, Peschaud F, Paye F, Nadel JA, Housset C. 2006. MUC5AC, a gel-forming mucin accumulating in gallstone disease, is overproduced via an epidermal growth factor receptor pathway in the human gallbladder. Am. J. Pathol. 169:2031-2041.
58. Chang HJ, Suh JI, Kwon SY. 1999. Gallstone formation and gallbladder mucosal changes in mice fed a lithogenic diet. J. Korean Med. Sci. 14:286-292.
59. Mathur SK, Duhan A, Singh S, Aggarwal M, Aggarwal G, Sen R, Singh S, Garg S. 2012. Correlation of gallstone characteristics with mucosal changes in gall bladder. Trop. Gastroenterol. 33:39-44.