Pathogenic yersinia promotes its survival by creating an acidic fluid-accessible compartment on the macrophage surface

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Bahnan, Wael ^a,b   Boettner, Douglas R ^a,c   Westermark, Linda ^b   Fällman, Maria ^b   Schesser, Kurt ^a   Abu Kwaik, Yousef ^d  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UMEÅ UNIVERSITY   (Sweden)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; UNCLASSIFIED DRUG; YOPJ PROTEIN;

ACIDITY; ANIMAL CELL; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL COMPONENT; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; HOST PATHOGEN INTERACTION; MACROPHAGE; MOUSE; NONHUMAN; PLASMID; TYPE III SECRETION SYSTEM; YERSINIA CONTAINING ACIDIC COMPARTMENT; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTION; ANIMAL; CELL CULTURE; CELL LINE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; CELL LINE; CELLS, CULTURED; MACROPHAGES; MICE; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

EID: 84943186160     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133298     Document Type: Article

References (29)

1. Galán JE, Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 2006 Nov 30; 444(7119): 567-73. PMID: 17136086
2. Raymond B, Young JC, Pallett M, Endres RG, Clements A, Frankel G. Subversion of trafficking, apoptosis, and innate immunity by type III secretion system effectors. Trends Microbiol. 2013 Aug; 21 (8): 430-41. doi: 10.1016/j.tim.2013.06.008 PMID: 23870533
3. Sarantis H, Balkin DM, DeCamilli P, Isberg RR, Brumell JH, Grinstein S. Yersinia entry into host cells requires Rab5-dependent dephosphorylation of PI(4,5)P2 and membrane scission. Cell Host Microbe. 2012 Feb 16; 11(2): 117-28. doi: 10.1016/j.chom.2012.01.010 PMID: 22341461
4. Viboud GI, Bliska JB. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol. 2005; 59: 69-89. PMID: 15847602
5. Fahlgren A, Westermark L, Akopyan K, Fällman M. Cell type-specific effects of Yersinia pseudotuberculosis virulence effectors. Cell Microbiol. 2009 Dec; 11(12): 1750-67. doi: 10.1111/j.1462-5822.2009.01365.x PMID: 19681909
6. Ray A, Dittel BN. Isolation of mouse peritoneal cavity cells. J Vis Exp. 2010 Jan 28; (35:).
7. Bölin I, Norlander L, Wolf-Watz H. Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun. 1982 Aug; 37(2): 506-12. PMID: 6749681
8. Hâkansson S, Schesser K, Persson C, Galyov EE, Rosqvist R, Homblé F, et al. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 1996 Nov 1; 15(21): 5812-23. PMID: 8918459
9. Galyov EE, Hâkansson S, Wolf-Watz H. Characterization of the operon encoding the YpkASer/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol. 1994 Aug; 176(15): 4543-8. PMID: 8045884
10. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA. 2000; 97: 6640-6645. PMID: 10829079
11. Day JB, Ferracci F, Plano GV. Translocation of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and lcrG deletion mutants measured using a phosphorylatable peptide tag and phosphospecific antibodies. Mol Microbiol. 2003 Feb; 47(3): 807-23. PMID: 12535078
12. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 2001 Jul 27; 106(2): 157-69. PMID: 11511344
13. Mesaki K, Tanabe K, Obayashi M, Oe N, Takei K. Fission of tubular endosomes triggers endosomal acidification and movement. PLoSOne. 2011 May 10; 6(5): e19764. doi: 10.1371/journal.pone.0019764 PMID: 21572956
14. Sory MP, Boland A, Lambermont I, Cornelis GR. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA. 1995 Dec 19; 92(26): 11998-2002 PMID: 8618831
15. Schesser K, Frithz-Lindsten E, Wolf-Watz H. Delineation and mutational analysis of the Yersinia pseudotuberculosis YopE domains which mediate translocation across bacterial and eukaryotic cellular membranes. J Bacteriol. 1996 Dec; 178(24): 7227-33. PMID: 8955406
16. Akopyan K, Edgren T, Wang-Edgren H, Rosqvist R, Fahlgren A, Wolf-Watz H, et al. Translocation of surface-localized effectors in type III secretion. Proc Natl Acad Sci USA. 2011 Jan 25; 108(4): 1639-44. doi: 10.1073/pnas.1013888108 PMID: 21220342
17. Bartra S, Cherepanov P, Forsberg A, Schesser K. The Yersinia YopE and YopH type III effector proteins enhance bacterial proliferation following contact with eukaryotic cells. BMC Microbiol. 2001; 1: e22.
18. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun. 2006 Jul; 74(7): 3727-41. PMID: 16790745
19. Pujol C, Klein KA, Romanov GA, Palmer LE, Cirota C, Zhao Z, et al. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect Immun. 2009 Jun; 77(6): 2251-61. doi: 10.1128/IAI.00068-09 PMID: 19289509
20. Moreau K, Lacas-Gervais S, Fujita N, Sebbane F, Yoshimori T, Simonet M, et al. Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell Microbiol. 2010 Aug; 12 (8): 1108-23. doi: 10.1111/j.1462-5822.2010.01456.x PMID: 20180800
21. Mukherjee S, Keitany G, Li Y, Wang Y, Ball HL, Goldsmith EJ, et al. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science. 2006 May 26; 312(5777): 1211-4. PMID: 16728640
22. Siefker DT, Echeverry A, Brambilla R, Fukata M, Schesser K, Adkins B. Murine neonates infected with Yersinia enterocolitica develop rapid and robust proinflammatory responses in intestinal lymphoid tissues. Infect Immun. 2014 Feb; 82(2): 762-72. doi: 10.1128/IAI.01489-13 PMID: 24478090
23. Erfurth SE, Gröbner S, Kramer U, Gunst DS, Soldanova I, Schaller M, et al. Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells. Infect Immun. 2004 Dec; 72(12): 7045-54 PMID: 15557628
24. Trülzsch K, Geginat G, Sporleder T, Ruckdeschel K, Hoffmann R, Heesemann J, et al. Yersinia outer protein P inhibits CD8T cell priming in the mouse infection model. J Immunol. 2005 Apr 1; 174 (7): 4244-51. PMID: 15778387
25. Skrzypek E, Cowan C, Straley SC. Targeting of the Yersinia pestis YopM protein into HeLa cells and intracellular trafficking to the nucleus. Mol Microbiol. 1998 Dec; 30(5): 1051-65. PMID: 9988481
26. Montecucco C, Rappuoli R. Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol. 2001 Jun; 2(6): 457-66. PMID: 11389469
27. Edgren T, Forsberg A, Rosqvist R, Wolf-Watz H. Type III secretion in Yersinia: injectisome or not? PLoS Pathog. 2012; 8(5): e1002669. doi: 10.1371/journal.ppat.1002669 PMID: 22589714
28. Sandvig K, Olsnes S. Diphtheria toxin entry into cells is facilitated by low pH. J Cell Biol. 1980 Dec; 87(3 Pt 1): 828-32. PMID: 7462324
29. Leka O, Vallese F, Pirazzini M, Berto P, Montecucco C, Zanotti G. Diphtheria toxin conformational switching at acidic pH. FEBS J. 2014 May; 281(9): 2115-22. doi: 10.1111/febs.12783 PMID: 24628974