Salmonella promotes virulence by repressing cellulose production

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 16, 2015, Pages 5183-5188

  Pontes, Mauricio H ^a,b,c   Lee, Eun Jin ^a,b,c,d   Choi, Jeongjoon ^a,b   Groisman, Eduardo A ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

^d Kyung Hee University   (South Korea)

Author keywords

ATP; Biofilm; Magnesium

Indexed keywords

CELLULOSE; GUANOSINE PHOSPHATE; PROTEIN BCSA; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CELLULOSE SYNTHASE; GLUCOSYLTRANSFERASE; MAGNESIUM;

ANIMAL CELL; ARTICLE; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BCSA GENE; BIOFILM; CONTROLLED STUDY; FEMALE; GENE; GENE INACTIVATION; MACROPHAGE; MGTC GENE; MOUSE; MUTANT; NONHUMAN; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SYNTHESIS; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRACELLULAR SPACE; METABOLISM; MICROBIOLOGY; MUTATION; PHAGOCYTE; VIRULENCE;

SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACTERIAL PROTEINS; CELLULOSE; GLUCOSYLTRANSFERASES; INTRACELLULAR SPACE; MACROPHAGES; MAGNESIUM; MICE; MUTATION; PHAGOCYTES; SALMONELLA TYPHIMURIUM; VIRULENCE;

EID: 84928732488     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1500989112     Document Type: Article

References (44)

1. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71(1):37-78.
2. Foreman-Wykert AK, Miller JF (2003) Hypervirulence and pathogen fitness. Trends Microbiol 11(3):105-108.
3. Parsons DA, Heffron F (2005) sciS, an icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence. Infect Immun 73(7):4338-4345.
4. Mouslim C, Hilbert F, Huang H, Groisman EA (2002) Conflicting needs for a Salmonella hypervirulence gene in host and non-host environments. Mol Microbiol 45(4):1019-1027.
5. Choi J, Groisman EA (2013) The lipopolysaccharide modification regulator PmrA limits Salmonella virulence by repressing the type three-secretion system Spi/Ssa. Proc Natl Acad Sci USA 110(23):9499-9504.
6. Klemm D, Heublein B, Fink HP, Bohn A (2005) Cellulose: Fascinating biopolymer and sustainable raw material. Angew Chem Int Ed Engl 44(22):3358-3393.
7. Zorraquino V, et al. (2013) Coordinated cyclic-di-GMP repression of Salmonella motility through YcgR and cellulose. J Bacteriol 195(3):417-428.
8. Solano C, et al. (2002) Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol Microbiol 43(3):793-808.
9. Serra DO, Richter AM, Hengge R (2013) Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol 195(24):5540-5554.
10. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U (2001) The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39(6):1452-1463.
11. Coburn B, Grassl GA, Finlay BB (2007) Salmonella, the host and disease: A brief review. Immunol Cell Biol 85(2):112-118.
12. Fields PI, Swanson RV, Haidaris CG, Heffron F (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83(14):5189-5193.
13. Buchmeier NA, Heffron F (1991) Inhibition of macrophage phagosome-lysosome fusion by Salmonella typhimurium. Infect Immun 59(7):2232-2238.
14. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47(1):103-118.
15. Blanc-Potard AB, Groisman EA (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16(17):5376-5385.
16. Lee EJ, Pontes MH, Groisman EA (2013) A bacterial virulence protein promotes pathogenicity by inhibiting the bacterium's own F1Fo ATP synthase. Cell 154(1):146-156.
17. Okuno D, Iino R, Noji H (2011) Rotation and structure of FoF1-ATP synthase. J Biochem 149(6):655-664.
18. Turner AK, et al. (2003) Contribution of proton-translocating proteins to the virulence of Salmonella enterica serovars Typhimurium, Gallinarum, and Dublin in chickens and mice. Infect Immun 71(6):3392-3401.
19. Soncini FC, García Véscovi E, Solomon F, Groisman EA (1996) Molecular basis of the magnesium-deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178(17):5092-5099.
20. Buchmeier N, et al. (2000) A parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica. Mol Microbiol 35(6):1375-1382.
21. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB (2006) Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 74(7):3727-3741.
22. Lavigne JP, O'callaghan D, Blanc-Potard AB (2005) Requirement of MgtC for Brucella suis intramacrophage growth: A potential mechanism shared by Salmonella enterica and Mycobacterium tuberculosis for adaptation to a low-Mg2+ environment. Infect Immun 73(5):3160-3163.
23. Maloney KE, Valvano MA (2006) The mgtC gene of Burkholderia cenocepacia is required for growth under magnesium limitation conditions and intracellular survival in macrophages. Infect Immun 74(10):5477-5486.
24. Rang C, et al. (2007) Dual role of the MgtC virulence factor in host and non-host environments. Mol Microbiol 63(2):605-622.
25. Storer AC, Cornish-Bowden A (1976) Concentration of MgATP2- and other ions in solution: Calculation of the true concentrations of species present in mixtures of associating ions. Biochem J 159(1):1-5.
26. Koebmann BJ, Westerhoff HV, Snoep JL, Nilsson D, Jensen PR (2002) The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J Bacteriol 184(14):3909-3916.
27. Omadjela O, et al. (2013) BcsA and BcsB form the catalytically active core of bacterial cellulose synthase sufficient for in vitro cellulose synthesis. Proc Natl Acad Sci USA 110(44):17856-17861.
28. Brown RM, et al. (1983) The biosynthesis and degradation of cellulose. J Appl Polym Sci 37:33-78.
29. Ross P, et al. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325(6101):279-281.
30. Sudarsan N, et al. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321(5887):411-413.
31. Blake AW, et al. (2006) Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J Biol Chem 281(39):29321-29329.
32. Lee EJ, Choi J, Groisman EA (2014) Control of a Salmonella virulence operon by proline-charged tRNA(Pro). Proc Natl Acad Sci USA 111(8):3140-3145.
33. Heithoff DM, et al. (1999) Coordinate intracellular expression of Salmonella genes induced during infection. J Bacteriol 181(3):799-807.
34. Simm R, Morr M, Kader A, Nimtz M, Römling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53(4):1123-1134.
35. Matthysse AG, et al. (2005) The effect of cellulose overproduction on binding and biofilm formation on roots by Agrobacterium tumefaciens. Mol Plant Microbe Interact 18(9):1002-1010.
36. Bassis CM, Visick KL (2010) The cyclic-di-GMP phosphodiesterase BinA negatively regulates cellulose-containing biofilms in Vibrio fischeri. J Bacteriol 192(5):1269-1278.
37. Tamayo R, Pratt JT, Camilli A (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61:131-148.
38. Lamprokostopoulou A, Monteiro C, Rhen M, Römling U (2010) Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar Typhimurium at the mucosal lining. Environ Microbiol 12(1):40-53.
39. Ahmad I, et al. (2011) Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS ONE 6(12):e28351.
40. Prouty AM, Gunn JS (2003) Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation on gallstones and on glass. Infect Immun 71(12):7154-7158.
41. Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183(6):1835-1842.
42. Zwir I, Latifi T, Perez JC, Huang H, Groisman EA (2012) The promoter architectural landscape of the Salmonella PhoP regulon. Mol Microbiol 84(3):463-485.
43. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97(12):6640-6645.
44. Davis RW, Bolstein D, Roth JR (1980) Advanced Bacterial Genetics (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).