Obacunone represses salmonella pathogenicity Islands 1 and 2 in an envz-dependent fashion

Applied and Environmental Microbiology

Volumn 78, Issue 19, 2012, Pages 7012-7022

  Vikram, Amit ^a,b   Jayaprakasha, Guddadarangavvanahally K ^a   Jesudhasan, Palmy R ^a   Pillai, Suresh D ^a   Patil, Bhimanagouda S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CDNA MICROARRAYS; CELL-CELL SIGNALING; CITRUS SPECIES; ESCHERICHIA COLI O157:H7; FOOD-BORNE PATHOGENS; HYDROGENASES; INFECTION ASSAYS; INFECTION MODELS; MALTOSE TRANSPORTERS; MICROARRAY DATA; PHENOTYPIC DATA; S. TYPHIMURIUM; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TRITERPENOIDS;

ESCHERICHIA COLI; LEAD COMPOUNDS; MALTOSE;

SALMONELLA;

BACTERIAL PROTEIN; BENZOXEPIN DERIVATIVE; LIMONOID; MALTOSE; OBACUNONE; VIRULENCE FACTOR;

COLIFORM BACTERIUM; ENZYME ACTIVITY; FRUIT; INHIBITION; ISLAND; PATHOGEN; PATHOGENICITY; SIGNALING; TERPENE; VIRULENCE;

ARTICLE; BIOSYNTHESIS; CELL STRAIN CACO 2; CHEMISTRY; CITRUS; DRUG ANTAGONISM; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENOMIC ISLAND; HUMAN; METABOLISM; MICROARRAY ANALYSIS; MICROBIOLOGY; SALMONELLA TYPHIMURIUM;

BACTERIAL PROTEINS; BENZOXEPINS; CACO-2 CELLS; CITRUS; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENOMIC ISLANDS; HUMANS; LIMONINS; MALTOSE; MICROARRAY ANALYSIS; SALMONELLA TYPHIMURIUM; VIRULENCE FACTORS;

CITRUS; ESCHERICHIA COLI; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; VIBRIO HARVEYI;

EID: 84868346167     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01326-12     Document Type: Article

References (61)

1. Bajaj V, Hwang C, Lee CA. 1995. hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes. Mol. Microbiol. 18:715-727.
2. Bajaj V, Lucas RL, Hwang C, Lee CA. 1996. Co-ordinate regulation of Salmonella Typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22:703-714.
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Methodol. 57:289-300.
4. Boos W, Shuman H. 1998. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol. Mol. Biol. Rev. 62:204-229.
5. Brawn LC, Hayward RD, Koronakis V. 2007. Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 1:63-75.
6. Bustamante VH, et al. 2008. HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc. Natl. Acad. Sci. U. S. A. 105:14591-14596.
7. Case CC, Bukau B, Granett S, Villarejo MR, Boos W. 1986. Contrasting mechanisms of envZ control of mal and pho regulon genes in Escherichia coli. J. Bacteriol. 166:706-712.
8. Centers for Disease Control and Prevention. 2010. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-10 states, 2009. MMWR Morb. Mortal. Wkly. Rep. 59: 418-430.
9. Clatworthy AE, Pierson E, Hung DT. 2007. Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol. 3:541-548.
10. Darwin KH, Miller VL. 2001. Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella Typhimurium. EMBO J. 20:1850-1862.
11. Deiwick J, Nikolaus T, Erdogan S, Hensel M. 1999. Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol. Microbiol. 31:1759-1773.
12. Economic Research Service. 2012. Food availability (per capita) data system. Economic Research Service, US Department of Agriculture, Washington, DC. http://www.ers.usda.gov/Data/FoodConsumption/.
13. Garmendia J, Beuzon CR, Ruiz-Albert J, Holden DW. 2003. The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella Typhimurium SPI-2 type III secretion system. Microbiology 149: 2385-2396.
14. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
15. Hasegawa S, Bennett RD, Verdon CP. 1980. Limonoids in citrus seeds: origin and relative concentration. J. Agric. Food Chem. 28:922-925.
16. Hautefort I, et al. 2008. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell. Microbiol. 10:958-984.
17. Herman Z, Fong CH, Ou P, Hasegawa S. 1990. Limonoid glucosides in orange juices by HPLC. J. Agric. Food Chem. 38:1860-1861.
18. Hsu W-J, Berhow M, Robertson GH, Hasegawa S. 1998. Limonoids and flavonoids in juices of Oroblanco and Melogold grapefruit hybrids. J. Food Sci. 63:57-60.
19. Jones SA, et al. 2008. Glycogen and maltose utilization by Escherichia coli O157:H7 in the mouse intestine. Infect. Immun. 76:2531-2540.
20. Keyser P, Elofsson M, Rosell S, Wolf-Watz H. 2008. Virulence blockers as alternatives to antibiotics: type III secretion inhibitors against Gramnegative bacteria. J. Intern. Med. 264:17-29.
21. Kosarewicz A, Königsmaier L, Marlovits TC. 2012. The blueprint of the type-3 injectisome. Philos. Trans. R. Soc. B Biol. Sci. 367:1140-1154.
22. Lawhon SD, et al. 2003. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48:1633-1645.
23. Lee AK, Detweiler CS, Falkow S. 2000. OmpR regulates the twocomponent system SsrA-SsrB in Salmonella pathogenicity island 2. J. Bacteriol. 182:771-781.
24. -ΔΔCT method. Methods 25: 402-408.
25. prgH from Salmonella pathogenicity island 1 (SPI1). J. Bacteriol. 183:4876-4885.
26. Lucas RL, Lee CA. 2001. Roles of hilC and hilD in regulation of hilA expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 183: 2733-2745.
27. Lucas RL, et al. 2000. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182:1872-1882.
28. Maier RJ, Olczak A, Maier S, Soni S, Gunn J. 2004. Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 72:6294-6299.
29. Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L. 2004. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79:727-747.
30. Manners GD, Jacob RA, Breksa AP III, Schoch TK, Hasegawa S. 2003. Bioavailability of citrus limonoids in humans. J. Agric. Food Chem. 51: 4156-4161.
31. Martínez LC, et al. 2011. Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol. Microbiol. 80:1637-1656.
32. Menon NK, et al. 1990. Cloning and sequencing of a putative Escherichia coli [NiFe] hydrogenase-1 operon containing six open reading frames. J. Bacteriol. 172:1969-1977.
33. Miao EA, Miller SI. 2000. A conserved amino acid sequence directing intracellular type III secretion by Salmonella Typhimurium. Proc. Natl. Acad. Sci. U. S. A. 97:7539-7544.
34. Miller EG, Porter JL, Binnie WH, Guo IY, Hasegawa S. 2004. Further studies on the anticancer activity of citrus limonoids. J. Agric. Food Chem. 52:4908-4912.
35. Miller J. 1972. Assay of β-galactosidase, p 352-355. In Miller JH (ed), Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Neidhardt FC, Bloch PL, Smith DF. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
37. O'Callaghan D, Charbit A. 1990. High efficiency transformation of Salmonella typhimurium and Salmonella typhi by electroporation. Mol. Gen. Genet. 223:156-158.
38. Ochman H, Soncini FC, Solomon F, Groisman EA. 1996. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl. Acad. Sci. U. S. A. 93:7800-7804.
39. Ozaki Y, et al. 1995. Limonoid glucosides in fruit, juice and processing by-products of Satsuma mandarin (Citrus unshiu Marcov.). J. Food Sci. 60:186-189.
40. Pfeifer CG, Marcus SL, Steele-Mortimer O, Knodler LA, Finlay BB. 1999. Salmonella typhimurium virulence genes are induced upon bacterial invasion into phagocytic and nonphagocytic cells. Infect. Immun. 67: 5690-5698.
41. Poulose SM, Harris ED, Patil BS. 2006. Antiproliferative effects of citrus limonoids against human neuroblastoma and colonic adenocarcinoma cells. Nutr. Cancer 56:103-112.
42. Poulose SM, Harris ED, Patil BS. 2005. Citrus limonoids induce apoptosis in human neuroblastoma cells and have radical scavenging activity. J. Nutr. 135:870-877.
43. Quackenbush J. 2002. Microarray data normalization and transformation. Nat. Genet. 32:496-501.
44. Raibaud O, Roa M, Braun-Breton C, Schwartz M. 1979. Structure of the malB region in Escherichia coli K12. I. Genetic map of malK-lambdaB operon. Mol. Gen. Genet. 174:241-248.
45. Rakeman JL, Bonifield HR, Miller SI. 1999. A HilA-independent pathway to Salmonella Typhimurium invasion gene transcription. J. Bacteriol. 181:3096-3104.
46. Rhen M, Maskell D, Mastroeni P, Threlfall J (ed). 2007. Salmonella: molecular biology and pathogenesis. Horizon Press, Norwich, Norfolk, United Kingdom.
47. Rossmann R, Sawers G, Böck A. 1991. Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol. Microbiol. 5:2807-2814.
48. Rozen S, Skaletsky HJ. 2000. Primer3 on theWWWfor general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
49. Silhavy TJ, et al. 1979. Structure of the malB region in Escherichia coli K12. II. Genetic map of malE, F,Goperon. Mol. Gen. Genet. 174:249-259.
50. Sittka A, Pfeiffer V, Tedin K, Vogel J. 2007. The RNA chaperone Hfq is essential for the virulence of Salmonella Typhimurium. Mol. Microbiol. 63:193-217.
51. Sperandio V. 2007. Novel approaches to bacterial infection therapy by interfering with bacteria-to-bacteria signaling. Expert Rev. Anti Infect. Ther. 5:271-276.
52. Tanaka T, et al. 2001. Inhibition of azoxymethane-induced colon carcinogenesis in male F344 rats by the citrus limonoids obacunone and limonin. Carcinogenesis 22:193-198.
53. Valdivia RH, Falkow S. 1997. Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277:2007-2011.
54. Vikram A, et al. 2011. Citrus flavonoid represses Salmonella pathogenicity island 1 and motility in S. Typhimurium LT2. Int. J. Food Microbiol. 145:28-36.
55. Vikram A, Jesudhasan PR, Jayaprakasha GK, Pillai SD, Patil BS. 2011. Citrus limonoids interfere with Vibrio harveyi cell-cell signaling and biofilm formation by modulating response regulator luxO. Microbiology 157: 99-110.
56. Vikram A, Jesudhasan PR, Jayaprakasha GK, Pillai SD, Patil BS. 2010. Grapefruit bioactive limonoids modulate E. coli O157:H7 TTSS and biofilm. Int. J. Food Microbiol. 140:109-116.
57. Voetsch AC, et al. 2004. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin. Infect. Dis. 38:S127-S134.
58. Wilmes-Riesenberg MR, Foster JW, Curtiss R. 1997. An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect. Immun. 65:203-210.
59. Zbell AL, Benoit SL, Maier RJ. 2007. Differential expression of NiFe uptake-type hydrogenase genes in Salmonella enterica serovar Typhimurium. Microbiology 153:3508-3516.
60. 2 in Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 75:1456-1459.
61. Zhao S, et al. 2009. β-Lactam resistance in Salmonella strains isolated from retail meats in the United States by the National Antimicrobial Resistance Monitoring System between 2002 and 2006. Appl. Environ. Microbiol. 75:7624-7630.