A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria

Nature Communications

Volumn 7, Issue , 2016, Pages

  Roier, Sandro ^a   Zingl, Franz G ^a   Cakar, Fatih ^a   Durakovic, Sanel ^a   Kohl, Paul ^a   Eichmann, Thomas O ^a   Klug, Lisa ^b   Gadermaier, Bernhard ^a   Weinzerl, Katharina ^a   Prassl, Ruth ^c   Lass, Achim ^a   Daum, Günther ^b   Reidl, Joachim ^a   Feldman, Mario F ^d   Schild, Stefan ^a  

^a UNIVERSITY OF GRAZ   (Austria)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 OXOACYL ACYL CARRIER PROTEIN REDUCTASE; ABC TRANSPORTER; ACYL CARRIER PROTEIN MALONYLTRANSFERASE; FATTY ACID; FERRIC UPTAKE REGULATOR; IRON; LIPIDOME; LIPOPROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PROTEOME; PROTOPORPHYRIN;

BACTERIUM; BIOGENIC DEPOSIT; FATTY ACID; LIPID; MEMBRANE; MUTATION; PATHOGENICITY; PHOSPHOLIPID; PHYSIOLOGICAL RESPONSE; VIRUS;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BINDING SITE; BIOGENESIS; CELL SIZE; CELLULAR DISTRIBUTION; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DELETION MUTANT; DOWN REGULATION; EPSILONPROTEOBACTERIA; FEMALE; GENE ACTIVATION; GENE CLUSTER; GENE CONTROL; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE MUTATION; GENE REPRESSION; GENETIC ORGANIZATION; HAEMOPHILUS INFLUENZAE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID ANALYSIS; LIPID COMPOSITION; LIPID STORAGE; MEMBRANE COMPONENT; MEMBRANE FORMATION; MOLECULAR WEIGHT; MOUSE; MUTAGENESIS; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SPECIES COMPOSITION; STRESS; SURVIVAL RATE; TRANSPOSON; VIBRIO CHOLERAE; ANIMAL; BAGG ALBINO MOUSE; CYTOPLASM VESICLE; ESCHERICHIA COLI; ORGANELLE BIOGENESIS; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; NEGIBACTERIA; OAT MOSAIC VIRUS; VIBRIO CHOLERAE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CYTOPLASMIC VESICLES; ESCHERICHIA COLI; FEMALE; HAEMOPHILUS INFLUENZAE; MICE, INBRED BALB C; ORGANELLE BIOGENESIS; VIBRIO CHOLERAE;

EID: 84955486191     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10515     Document Type: Article

References (53)

1. Beveridge, T. J. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181, 4725-4733 (1999).
2. Kulp, A. & Kuehn, M. J. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu. Rev. Microbiol. 64, 163-184 (2010).
3. Kulkarni, H. M. & Jagannadham, M. V. Biogenesis and multifaceted roles of outer membrane vesicles from Gram-negative bacteria. Microbiology 160, 2109-2121 (2014).
4. Lee, E. Y., Choi, D. S., Kim, K. P. & Gho, Y. S. Proteomics in Gram-negative bacterial outer membrane vesicles. Mass Spectrom. Rev. 27, 535-555 (2008).
5. Ellis, T. N. & Kuehn, M. J. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74, 81-94 (2010).
6. Mashburn-Warren, L., McLean, R. J. & Whiteley, M. Gram-negative outer membrane vesicles: beyond the cell surface. Geobiology 6, 214-219 (2008).
7. Haurat, M. F., Elhenawy, W. & Feldman, M. F. Prokaryotic membrane vesicles: new insights on biogenesis and biological roles. Biol. Chem. 396, 95-109 (2015).
8. Roier, S. et al. Intranasal immunization with nontypeable Haemophilus influenzae outer membrane vesicles induces cross-protective immunity in mice. PLoS ONe 7, e42664 (2012).
9. Roier, S. et al. Immunogenicity of Pasteurella multocida and Mannheimia haemolytica outer membrane vesicles. Int. J. Med. Microbiol. 303, 247-256 (2013).
10. Schild, S., Nelson, E. J. & Camilli, A. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect. Immun. 76, 4554-4563 (2008).
11. Leitner, D. R. et al. A combined vaccine approach against Vibrio cholerae and ETEC based on outer membrane vesicles. Front. Microbiol. 6, 823 (2015).
12. Acevedo, R. et al. Bacterial outer membrane vesicles and vaccine applications. Front. Immunol. 5, 121 (2014).
13. Rosenthal, J. A., Chen, L., Baker, J. L., Putnam, D. & DeLisa, M. P. Pathogen-like particles: biomimetic vaccine carriers engineered at the nanoscale. Curr. Opin. Biotechnol. 28, 51-58 (2014).
14. Wensink, J. & Witholt, B. Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur. J. Biochem. 116, 331-335 (1981).
15. Deatherage, B. L. et al. Biogenesis of bacterial membrane vesicles. Mol. Microbiol. 72, 1395-1407 (2009).
16. McBroom, A. J., Johnson, A. P., Vemulapalli, S. & Kuehn, M. J. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J. Bacteriol. 188, 5385-5392 (2006).
17. Zhou, L., Srisatjaluk, R., Justus, D. E. & Doyle, R. J. On the origin of membrane vesicles in gram-negative bacteria. FEMS Microbiol. Lett. 163, 223-228 (1998).
18. McBroom, A. J. & Kuehn, M. J. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63, 545-558 (2007).
19. Kadurugamuwa, J. L. & Beveridge, T. J. Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J. Bacteriol. 177, 3998-4008 (1995).
20. Mashburn, L. M. & Whiteley, M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437, 422-425 (2005).
21. Schertzer, J. W. & Whiteley, M. A bilayer-couple model of bacterial outer membrane vesicle biogenesis. MBio 3, e00297-11 (2012).
22. Mashburn-Warren, L. M. & Whiteley, M. Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61, 839-846 (2006).
23. Kulp, A. J. et al. Genome-wide assessment of outer membrane vesicle production in Escherichia coli. PLoS One 10, e0139200 (2015).
24. Malinverni, J. C. & Silhavy, T. J. An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc. Natl. Acad. Sci. USA 106, 8009-8014 (2009).
25. Johnston, J. W. & Apicella, M. A. in Encyclopedia of Microbiology (ed. Schaechter, M.) 153-162 (Academic Press, Elsevier Ltd., 2009).
26. Roier, S. et al. A basis for vaccine development: Comparative characterization of Haemophilus influenzae outer membrane vesicles. Int. J. Med. Microbiol. 305, 298-309 (2015).
27. Song, T. et al. A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol. Microbiol. 70, 100-111 (2008).
28. Sonntag, I., Schwarz, H., Hirota, Y. & Henning, U. Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J. Bacteriol. 136, 280-285 (1978).
29. Nakamura, S. et al. Molecular basis of increased serum resistance among pulmonary isolates of non-typeable Haemophilus influenzae. PLoS Pathog. 7, e1001247 (2011).
30. Carpenter, C. D. et al. The Vps/VacJ ABC transporter is required for intercellular spread of Shigella flexneri. Infect. Immun. 82, 660-669 (2014).
31. Casali, N. & Riley, L. W. A phylogenomic analysis of the Actinomycetales mce operons. BMC Genomics 8, 60 (2007).
32. Schlör, S., Herbert, M., Rodenburg, M., Blass, J. & Reidl, J. Characterization of ferrochelatase (hemH) mutations in Haemophilus influenzae. Infect. Immun. 68, 3007-3009 (2000).
33. Thompson, C. C. & Carabeo, R. A. An optimal method of iron starvation of the obligate intracellular pathogen, Chlamydia trachomatis. Front. Microbiol. 2, 20 (2011).
34. Fillat, M. F. The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch. Biochem. Biophys. 546, 41-52 (2014).
35. Harrison, A. et al. Ferric uptake regulator and its role in the pathogenesis of nontypeable Haemophilus influenzae. Infect. Immun. 81, 1221-1233 (2013).
36. Yu, C. & Genco, C. A. Fur-mediated activation of gene transcription in the human pathogen Neisseria gonorrhoeae. J. Bacteriol. 194, 1730-1742 (2012).
37. Becker, K. W. & Skaar, E. P. Metal limitation and toxicity at the interface between host and pathogen. FEMS Microbiol. Rev. 38, 1235-1249 (2014).
38. Hood, M. I. & Skaar, E. P. Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525-537 (2012).
39. Rao, V. K., Krasan, G. P., Hendrixson, D. R., Dawid, S. & Geme, 3rd J. W. Molecular determinants of the pathogenesis of disease due to non-typable Haemophilus influenzae. FEMS Microbiol. Rev. 23, 99-129 (1999).
40. Hallstrom, T. & Riesbeck, K. Haemophilus influenzae and the complement system. Trends Microbiol. 18, 258-265 (2010).
41. Tan, T. T., Morgelin, M., Forsgren, A. & Riesbeck, K. Haemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J. Infect. Dis. 195, 1661-1670 (2007).
42. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970).
43. Kang, D., Gho, Y. S., Suh, M. & Kang, C. Highly sensitive and fast protein detection with coomassie brilliant blue in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Bull. Kor. Chem. Soc. 23, 1511-1512 (2002).
44. Schlör, S., Kemmer, G. & Reidl, J. Transposon Tn10. Methods Mol. Med. 71, 211-224 (2003).
45. Akerley, B. J. et al. A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc. Natl. Acad. Sci. USA 99, 966-971 (2002).
46. Gerlach, G. et al. Transposon insertion in a serine-specific minor tRNA coding sequence affects intraperitoneal survival of Haemophilus influenzae in the infant rat model. Int. J. Med. Microbiol. 300, 218-228 (2010).
47. Seper, A. et al. Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol. Microbiol. 82, 1015-1037 (2011).
48. Lee, C. H. & Tsai, C. M. Quantification of bacterial lipopolysaccharides by the purpald assay: measuring formaldehyde generated from 2-keto-3-deoxyoctonate and heptose at the inner core by periodate oxidation. Anal. Biochem. 267, 161-168 (1999).
49. Folch, J., Lees, M. & Sloane Stanley, G. H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509 (1957).
50. Broekhuyse, R. M. Phospholipids in tissues of the eye. I. Isolation, characterization and quantitative analysis by two-dimensional thin-layer chromatography of diacyl and vinyl-ether phospholipids. Biochim. Biophys. Acta 152, 307-315 (1968).
51. Knittelfelder, O. L., Weberhofer, B. P., Eichmann, T. O., Kohlwein, S. D. & Rechberger, G. N. A versatile ultra-high performance LC-MS method for lipid profiling. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 951-952, 119-128 (2014).
52. Lichtenegger, S. et al. Characterization of lactate utilization and its implication on the physiology of Haemophilus influenzae. Int. J. Med. Microbiol. 304, 490-498 (2014).
53. Seper, A. et al. Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases. PLoS Pathog. 9, e1003614 (2013).