Physiological levels of glucose induce membrane vesicle secretion and affect the lipid and protein composition of Yersinia pestis cell surfaces

Applied and Environmental Microbiology

Volumn 79, Issue 14, 2013, Pages 4509-4514

  Kolodziejek, Anna M ^a,b   Caplan, Allan B ^a   Bohach, Gregory A ^a,c   Paszczynski, Andrzej J ^a   Minnich, Scott A ^a   Hovde, Carolyn J ^a  

^a UNIVERSITY OF IDAHO   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Mississippi State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACES; EXTRACELLULAR; MEMBRANE VESICLES; PHYSIOLOGICAL LEVELS; PROTEIN COMPOSITION; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

CELL MEMBRANES; GLUCOSE; PROTEINS;

PHYSIOLOGY;

GLUCOSE; VIRULENCE FACTOR;

BIOFILM; CARBOHYDRATE; GLUCOSE; GROWTH RATE; LIPID; MEMBRANE; SECRETION; TEMPERATURE EFFECT;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BIOFILM; CELL MEMBRANE; CHEMISTRY; EVOLUTION; FLEA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRULENCE; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

AMINO ACID SEQUENCE; ANIMALS; BIOFILMS; BIOLOGICAL EVOLUTION; CELL MEMBRANE; GLUCOSE; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; SIPHONAPTERA; VIRULENCE; VIRULENCE FACTORS; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84879812602     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00675-13     Document Type: Article

References (51)

1. Perry RD, Fetherston JD. 1997. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
2. Achtman M, Zurth K, Morelli G, Torrea G, Guiyoule A, Carniel E. 1999. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. U. S. A. 96:14043-14048.
3. Rosenzweig JA, Chopra AK. 2012. The future of plague vaccines: hopes raised by a surrogate, live-attenuated recombinant vaccine candidate. Expert Rev. Vaccines 11:659-661.
4. Williamson ED. 2009. Plague. Vaccine 27(Suppl 4):D56-D60.
5. Kolodziejek AM, Schnider DR, Rohde HN, Wojtowicz AJ, Bohach GA, Minnich SA, Hovde CJ. 2010. Outer membrane protein X (Ail) contributes to Yersinia pestis virulence in pneumonic plague and its activity is dependent on the lipopolysaccharide core length. Infect. Immun. 78: 5233-5243.
6. Kolodziejek AM, Sinclair DJ, Seo KS, Schnider DR, Deobald CF, Rohde HN, Viall AK, Minnich SS, Hovde CJ, Minnich SA, Bohach GA. 2007. Phenotypic characterization of OmpX, an Ail homologue of Yersinia pestis KIM. Microbiology 153:2941-2951.
7. Spinner JL, Hinnebusch BJ. 2012. The life stage of Yersinia pestis in the flea vector confers increased resistance to phagocytosis and killing by murine polymorphonuclear leukocytes. Adv. Exp. Med. Biol. 954:159-163.
8. Vadyvaloo V, Jarrett C, Sturdevant DE, Sebbane F, Hinnebusch BJ. 2010. Transit through the flea vector induces a pretransmission innate immunity resistance phenotype in Yersinia pestis. PLoS Pathog. 6:e1000783. doi:10.1371/journal.ppat.1000783.
9. Burrows TW, Bacon GA. 1956. The basis of virulence in Pasteurella pestis: the development of resistance to phagocytosis in vitro. Br. J. Exp. Pathol. 37:286-299.
10. Chiang SL, Taylor RK, Koomey M, Mekalanos JJ. 1995. Single amino acid substitutions in the N-terminus of Vibrio cholerae TcpA affect colonization, autoagglutination, and serum resistance. Mol. Microbiol. 17: 1133-1142.
11. Guerry P, Ewing CP, Schirm M, Lorenzo M, Kelly J, Pattarini D, Majam G, Thibault P, Logan S. 2006. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60:299- 311.
12. Kapperud G, Lassen J. 1983. Relationship of virulence-associated autoagglutination to hemagglutinin production in Yersinia enterocolitica and Yersinia enterocolitica-like bacteria. Infect. Immun. 42:163-169.
13. Laird WJ, Cavanaugh DC. 1980. Correlation of autoagglutination and virulence of yersiniae. J. Clin. Microbiol. 11:430-432.
14. Polakof S, Mommsen TP, Soengas JL. 2011. Glucosensing and glucose homeostasis: from fish to mammals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 160:123-149.
15. Allan ND, Kooi C, Sokol PA, Beveridge TJ. 2003. Putative virulence factors are released in association with membrane vesicles from Burkholderia cepacia. Can. J. Microbiol. 49:613-624.
16. Amano A, Takeuchi H, Furuta N. 2010. Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect. 12:791-798.
17. Beveridge TJ. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:4725-4733.
18. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64:163-184.
19. Wang D, Zetterstrom CE, Gabrielsen M, Beckham KS, Tree JJ, Macdonald SE, Byron O, Mitchell TJ, Gally DL, Herzyk P, Mahajan A, Uvell H, Burchmore R, Smith BO, Elofsson M, Roe AJ. 2011. Identification of bacterial target proteins for the salicylidene acylhydrazide class of virulence- blocking compounds. J. Biol. Chem. 286:29922-29931.
20. Gao L, Weck MN, Michel A, Pawlita M, Brenner H. 2009. Association between chronic atrophic gastritis and serum antibodies to 15 Helicobacter pylori proteins measured by multiplex serology. Cancer Res. 69:2973- 2980.
21. Garduno RA, Garduno E, Hoffman PS. 1998. Surface-associated hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect. Immun. 66:4602-4610.
22. Hildebrand GJ, Ng J, Von Metz EK, Eisler DM. 1966. Studies on the mechanism of circulatory failure induced in rats by Pasteurella pestis murine toxin. J. Infect. Dis. 116:615-629.
23. Hu Y, Coates AR. 2009. Acute and persistent Mycobacterium tuberculosis infections depend on the thiol peroxidase TpX. PLoS One 4:e5150. doi:10 .1371/journal.pone.0005150.
24. Reffuveille F, Connil N, Sanguinetti M, Posteraro B, Chevalier S, Auffray Y, Rince A. 2012. Involvement of peptidylprolyl cis/trans isomerases in Enterococcus faecalis virulence. Infect. Immun. 80:1728-1735.
25. Hinnebusch BJ, Rudolph AE, Cherepanov P, Dixon JE, Schwan TG, Forsberg A. 2002. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296:733-735.
26. Joshi MC, Sharma A, Kant S, Birah A, Gupta GP, Khan SR, Bhatnagar R, Banerjee N. 2008. An insecticidal GroEL protein with chitin binding activity from Xenorhabdus nematophila. J. Biol. Chem. 283:28287-28296.
27. Khan MN, Shukla D, Bansal A, Mustoori S, Ilavazhagan G. 2009. Immunogenicity and protective efficacy of GroEL (hsp60) of Streptococcus pneumoniae against lethal infection in mice. FEMS Immunol. Med. Microbiol. 56:56-62.
28. Miyoshi A, Bermudez-Humaran LG, Ribeiro LA, Le Loir Y, Oliveira SC, Langella P, Azevedo V. 2006. Heterologous expression of Brucella abortus GroEL heat-shock protein in Lactococcus lactis. Microb. Cell Fact. 5:14.
29. Noll A, Autenrieth IB. 1996. Immunity against Yersinia enterocolitica by vaccination with Yersinia HSP60 immunostimulating complexes or Yersinia HSP60 plus interleukin-12. Infect. Immun. 64:2955-2961.
30. Watarai M, Kim S, Erdenebaatar J, Makino S, Horiuchi M, Shirahata T, Sakaguchi S, Katamine S. 2003. Cellular prion protein promotes Brucella infection into macrophages. J. Exp. Med. 198:5-17.
31. Ponnusamy D, Hartson SD, Clinkenbeard KD. 2011. Intracellular Yersinia pestis expresses general stress response and tellurite resistance proteins in mouse macrophages. Vet. Microbiol. 150:146-151.
32. Horst SA, Jaeger T, Denkel LA, Rouf SF, Rhen M, Bange FC. 2010. Thiol peroxidase protects Salmonella enterica from hydrogen peroxide stress in vitro and facilitates intracellular growth. J. Bacteriol. 192:2929-2932.
33. Rietsch A, Wolfgang MC, Mekalanos JJ. 2004. Effect of metabolic imbalance on expression of type III secretion genes in Pseudomonas aeruginosa. Infect. Immun. 72:1383-1390.
34. Sieira R, Arocena GM, Bukata L, Comerci DJ, Ugalde RA. 2010. Metabolic control of virulence genes in Brucella abortus: HutC coordinates virB expression and the histidine utilization pathway by direct binding to both promoters. J. Bacteriol. 192:217-224.
35. Bassler BL. 2002. Small talk. Cell-to-cell communication in bacteria. Cell 109:421-424.
36. Bumann D. 2002. Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and twocolour flow cytometry. Mol. Microbiol. 43:1269-1283.
37. Heroven A, Sest M, Pisano F, Scheb-Wetzel M, Böhme K, Klein J, Münch R, Schomburg D, Dersch P. 2012. Crp induces switching of the CsrB and CsrC RNAs in Yersinia pseudotuberculosis and links nutritional status to virulence. Front. Cell. Infect. Microbiol. 2:158.
38. Seo KS, Kim JW, Park JY, Viall AK, Minnich SS, Rohde HN, Schnider DR, Lim SY, Hong JB, Hinnebusch BJ, O'Loughlin JL, Deobald CF, Bohach GA, Hovde CJ, Minnich SA. 2012. Role of a new intimin/invasinlike protein in Yersinia pestis virulence. Infect. Immun. 80:3559-3569.
39. Brickman E, Beckwith J. 1975. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J. Mol. Biol. 96:301-316.
40. Brown RN, Gulig PA. 2008. Regulation of fatty acid metabolism by FadR is essential for Vibrio vulnificus to cause infection of mice. J. Bacteriol. 190:7633-7644.
41. Fozo EM, Scott-Anne K, Koo H, Quivey RG, Jr. 2007. Role of unsaturated fatty acid biosynthesis in virulence of Streptococcus mutans. Infect. Immun. 75:1537-1539.
42. Feodorova VA, Golova AB. 2005. Antigenic and phenotypic modifications of Yersinia pestis under calcium and glucose concentrations simulating the mammalian bloodstream environment. J. Med. Microbiol. 54: 435-441.
43. Wigglesworth VB. 1972. The principles of insect physiology. Chapman & Hall, London, United Kingdom.
44. Rhodes RG, Atoyan JA, Nelson DR. 2010. The chitobiose transporter, chbC, is required for chitin utilization in Borrelia burgdorferi.BMCMicrobiol. 10:21.
45. Montie TC, Kadis S, Ajl SJ. 1970. Microbial toxins, vol 3. Academic Press, New York, NY.
46. Schar M, Meyer KF. 1956. Studies on immunization against plague. XV. The pathophysiologic action of the toxin of Pasteurella pestis in experimental animals. Schweiz. Z. Pathol. Bakteriol. 19:51-70.
47. Hurst MR, Jones SA, Binglin T, Harper LA, Jackson TA, Glare TR. 2011. The main virulence determinant of Yersinia entomophaga MH96 is a broad-host-range toxin complex active against insects. J. Bacteriol. 193: 1966-1980.
48. Nguyen TT, Saxena A, Beveridge TJ. 2003. Effect of surface lipopolysaccharide on the nature of membrane vesicles liberated from the Gramnegative bacterium Pseudomonas aeruginosa. J. Electron Microsc. (Tokyo) 52:465-469.
49. Tashiro Y, Ichikawa S, Shimizu M, Toyofuku M, Takaya N, Nakajima-Kambe T, Uchiyama H, Nomura N. 2010. Variation of physiochemical properties and cell association activity of membrane vesicles with growth phase in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 76:3732- 3739.
50. Lee JC, Lee EJ, Lee JH, Jun SH, Choi CW, Kim SI, Kang SS, Hyun S. 2012. Klebsiella pneumoniae secretes outer membrane vesicles that induce the innate immune response. FEMS Microbiol. Lett. 331:17-24.
51. Staggs TM, Perry RD. 1991. Identification and cloning of a fur regulatory gene in Yersinia pestis. J. Bacteriol. 173:417-425.