Early Apoptosis of Macrophages Modulated by Injection of Yersinia pestis YopK Promotes Progression of Primary Pneumonic Plague

PLoS Pathogens

Volumn 9, Issue 4, 2013, Pages

  Peters, Kristen N ^a   Dhariwala, Miqdad O ^a   Hughes Hanks, Jennifer M ^a   Brown, Charles R ^a,b   Anderson, Deborah M ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CASPASE 8; CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN K;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL LOAD; CONTROLLED STUDY; CYTOTOXICITY; DNA SEQUENCE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LUNG INFILTRATE; MACROPHAGE; MALE; MOUSE; NONHUMAN; OPEN READING FRAME; PLAGUE; PNEUMONIA; POINT MUTATION; POLYMERASE CHAIN REACTION; WESTERN BLOTTING; YERSINIA PESTIS;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CASPASE 3; CASPASE 8; DENDRITIC CELLS; ENZYME ACTIVATION; FEMALE; MACROPHAGES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PLAGUE; PROMOTER REGIONS, GENETIC; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84876868010     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003324     Document Type: Article

References (64)

1. Janssen W, Henson P, (2012) Cellular regulation of the inflammatory response. Toxicol Pathol 40: 166-173.
2. Moreira A, Hogaboam C, (2011) Macrophages in allergic asthma: Fine-tuning their pro- and anti-inflammatory actions for disease resolution. J Interfer Cyto Res 31: 485-491.
3. Marriott H, Hellewell P, Cross S, Ince P, Whyte M, et al. (2006) Decreased alveolar macrophage apoptosis is associated with increased pulmonary inflammation in a murine model of pneumococcal pneumonia. J Immunol 177: 6480-6488.
4. Borges V, Vandivier R, McPhillips K, Kench J, Morimoto K, et al. (2009) TNFα inhibits apoptotic cell clearance in the lung, exacerbating acute inflammation. Am J Physiol Lung 297: L586-L595.
5. Pollitzer R (1954) Plague. Geneva, Switzerland: World Health Organization.
6. Fetherston J, Perry R, (1997) Yersinia pestis - etiologic agent of plague. Clin Microbiol Rev 10: 35-66.
7. Bergsbaken T, Cookson BT, (2009) Innate immune response during Yersinia infection: critical modulation of cell death mechanisms through phagocyte activation. J Leukoc Biol 86: 1153-1158.
8. Bubeck SS, Cantwell AM, Dube PH, (2007) Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice. Infect Immun 75: 697-705.
9. Laws T, Davey M, Titball R, Lukaszewski R, (2010) Neutrophils are important in early control of lung infection by Yersinia pestis. Microbes Infect 12: 331-335.
10. Huang X, Nikolich M, Lindler L, (2006) Current trends in plague research: From genomics to virulence. Clin Med Res 4: 189-199.
11. Rosqvist R, Magnusson K, Wolf-Watz H, (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
12. Petersson J, Nordfelth R, Dubinina E, Bergman T, Gustafsson M, et al. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273: 1183-1184.
13. Neyt C, Cornelis G, (1999) Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33: 971-981.
14. Straley S, Cibull M, (1989) Differential clearance and host-pathogen interactions of YopE- and YopK-YopL- Yersinia pestis in BALB/c mice. Infect Immun 57: 1200-1210.
15. Holmstrom A, Rosqvist R, Wolf-Watz H, Forsberg A, (1995) Virulence plasmid-encoded YopK is essential for Yersinia pseudotuberculosis to cause systemic infection in mice. Infect Immun 63: 2269-2276.
16. Nemeth J, Straley S, (1997) Effect of Yersinia pestis YopM on experimental plague. Infect Immun 65: 924-930.
17. Logsdon L, Mecsas J, (2003) Requirement of the Yersinia pseudotuberculosis Effectors YopH and YopE in Colonization and Persistence in Intestinal and Lymph Tissues. Infect Immun 71: 4595-4607.
18. Lemaitre N, Sebbane F, Long D, Hinnebusch B, (2006) Yersinia pestis YopJ suppresses tumor necrosis factor alpha induction and contributes to apoptosis of immune cells in the lymph node but is not required for virulence in a rat model of bubonic plague. Infect Immun 74: 5126-5131.
19. Cantwell A, Bubeck S, Dube P, (2010) YopH inhibits early pro-inflammatory cytokine responses during plague pneumonia. BMC Immunol 11: 29-40.
20. Monack D, Mecsas J, Ghori N, Falkow S, (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci 94: 10385-10390.
21. Mukherjee S, Keitany G, Li Y, Wang Y, Ball H, et al. (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214.
22. Orth K, Xu Z, Mudgett M, Bao Z, Palmer L, et al. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
23. Orth K, Palmer L, Bao Z, Stewart S, Rudolph A, et al. (1999) Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285: 1920-1923.
24. Zauberman A, Cohen S, Mamroud E, Flashner Y, Tidhar A, et al. (2006) Interaction of Yersinia pestis with macrophages: Limitations in YopJ-dependent apoptosis. Infect Immun 74: 3239-3250.
25. Brodsky I, Medzhitov R, (2008) Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog 4: 1-14.
26. Holmstrom A, Pettersson J, Rosqvist R, Hakansson S, Tafazoli F, et al. (1997) YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membran. Mol Microbiol 24: 73-91.
27. Dewoody R, Merritt P, Houppert A, Marketon M, (2011) YopK regulates the Yersinia pestis type III secretion system from within host cells. Mol Microbiol 79: 1445-1461.
28. Garcia J, Ferracci F, Jackson M, Joseph S, Pattis I, et al. (2006) Measurement of effector protein injection by type III and type IV secretion systems by using a 13-residue phophorylatable glycogen synthase kinase tag. Infect Immun 74: 5645-5657.
29. Bergsbaken T, Cookson B, (2007) Macrophage activation redirects Yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PloS Path 3: e161.
30. Shin H, Cornelis G, (2007) Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of pro-inflammatory IL-1β. Cell Microbiol 9: 2893-2902.
31. Lilo S, Zheng Y, Bliska J, (2008) Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector protein YopJ. Infect Immun 76: 3911-3923.
32. Schotte P, Denecker G, Van Den Broeke A, Vandenabeele P, Cornelis G, et al. (2004) Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1β. J Biol Chem 279: 25134-25142.
33. Brodsky I, Palm N, Sadanand S, Ryndak M, Sutterwala F, et al. (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7: 376-387.
34. Montminy S, Khan N, McGrath S, Walkowicz M, Sharp F, et al. (2006) Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat Immunol 7: 1066-1073.
35. Valdimer G, Weng D, Paquette S, Vanaja S, Rathinam V, et al. (2012) The NLRP12 inflammasome recognizes Yersinia pestis. Immunity 37: 96-107.
36. Donnenberg M, Kaper J, (1991) Construction of an eae deletion mutant of Enteropathogenic Escherichia coli by using a positive selection suicide vector. Infect Immun 59: 4310-4317.
37. Marketon M, DePaolo R, DeBord K, Jabri B, Schneewind O, (2005) Plague bacteria target immune cells during infection. Science 309: 1739-1741.
38. Dewoody R, Merritt P, Marketon M, (2013) YopK controls both rate and fidelity of Yop translocation. Mol Microbiol 87: 301-317.
39. Zauberman A, Tidhar A, Levy Y, Bar-Haim E, Halperin G, et al. (2009) Yersinia pestis endowed with increased cytotoxicity is avirulent in a bubonic plague model and induces rapid protection against pneumonic plague. PLoS One 4: e5938.
40. Pandey A, Sodhi A, (2009) Recombinant YopJ induces apoptosis in murine peritoneal macrophages in vitro: involvement of mitochondrial death pathway. Int Immunol 21: 1239-1249.
41. Lavrik I, Krammer P, (2012) Regulation of CD95/Fas signaling at the DISC. Cell Death Diff 19: 36-41.
42. Grobner S, Adkins I, Schulz S, Richter K, Borgmann S, et al. (2007) Catalytically active Yersinia outer protein P induces cleavage of RIP and caspase-8 at the level of the DISC independently of death receptors in dendritic cells. Apoptosis 12: 1813-1825.
43. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, et al. (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J 17: 1675-1687.
44. Zhang Y, Ting A, Marcu K, Bliska J, (2005) Inhibition of MAPK and NF-κB pathways is necessary for rapid apoptosis in macrophages infected with Yersinia. J Immunol 174: 7939-7949.
45. Lee-Lewis H, Anderson D, (2010) Absence of inflammation and pneumonia during infection with non-pigmented Yersinia pestis reveals new role for the pgm locus in pathogenesis. Infect Immun 78: 220-230.
46. Dockrell D, Marriott H, Prince L, Ridger V, Ince P, et al. (2003) Alveolar macrophage apoptosis contributes to pneumococcal clearance in a resolving model of pulmonary infection. J Immunol 171: 5380-5388.
47. Fox S, Leitch A, Duffin R, Haslett C, Rossi A, (2010) Neutrophil apoptosis: Relevance to the innate immune response and inflammatory disease. J Innate Immun 2: 216-227.
48. Eisele N, Brown C, Anderson D, (2012) Phagocytes and humoral immunity to pneumonic plague. Adv Exp Med Biol 954: 165-171.
49. Ye Z, Uittenbogaard A, Cohen D, Kaplan A, Ambati J, et al. (2011) Distinct CCR2(+)Gr1(+) cells control growth of the Yersinia pestis DyopM mutant in liver and spleen during systemic plague. Infect Immun 79: 674-687.
50. Kaufmann T, Strasser A, Jost P, (2012) Fas death receptor signalling: roles of Bid and XIAP. Cell Death Diff 19: 42-50.
51. Janssen W, Barthel L, Muldrow A, Oberley-Deegan R, Kearns M, et al. (2011) Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med 184: 547-560.
52. Laskin D, Weinberger B, Laskin J, (2001) Functional heterogeneity in liver and lung macrophages. J Leuk Biol 70: 163-170.
53. Berghaus L, Moore J, Hurley D, Vandenplas M, Fortes B, et al. (2010) Innate immune responses of primary murine macrophage-lineage cells and RAW 264.7 cells to ligands of Toll-like receptors 2, 3, and 4. Comp Immunol Microbiol Inf Dis 33: 443-454.
54. Sauvonnet N, Lambermont I, van der Bruggen P, Cornelis G, (2002) YopH prevents monocyte chemoattractant protein 1 expression in macrophages and T-cell proliferation through inactivation of the phosphatidylinositol 3-kinase pathway. Mol Microbiol 45: 805-815.
55. Serbina N, Jia T, Hohl T, Pamer E, (2008) Monocyte-mediated defense against microbial pathogens. Ann Rev Immunol 26: 421-452.
56. Lathem W, Crosby S, Miller V, Goldman W, (2005) Progression of primary pneumonic plague: A mouse model of infection, pathology, and bacterial transcriptional activity. Proc Natl Acad Sci 102: 17786-17791.
57. Surgalla M, Beesley E, (1969) Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. App Microbiol 18: 834-837.
58. Welkos S, Friedlander A, Davis K, (1997) Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain CO92. Microb Path 23: 211-223.
59. Anderson D, Schneewind O, (1999) Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ. Mol Microbiol 31: 1139-1148.
60. Hanahan D (1985) DNA Cloning: A practical approach. In: Glover D, editor. McLean, VA: IRL Press. pp. 109.
61. Miller V, Mekalanos J, (1988) A novel suicide vector and its use in construction of insertion mutations: Osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170: 2575-2583.
62. Weeks S, Hill J, Friedlander A, Welkos S, (2002) Anti-V antigen antibody protects macrophages from Yersinia pestis-induced cell death and promotes phagocytosis. Microb Path 32: 227-237.
63. Eisele N, Anderson D, (2009) Dual-function antibodies to Yersinia pestis LcrV required for pulmonary clearance of plague. Clin Vacc Immunol 16: 1720-1727.
64. Reed L, Muench H, (1938) A simple method of estimating fifty percent endpoints. Am J Hyg 27: 493-497.