Dot/Icm type IVB secretion system requirements for coxiella burnetii growth in human macrophages

mBio

Volumn 2, Issue 4, 2011, Pages

  Beare, Paul A ^a   Gilk, Stacey D ^a   Larson, Charles L ^a   Hill, Joshua ^a   Stead, Christopher M ^a   Omsland, Anders ^a   Cockrell, Diane C ^a   Howe, Dale ^a   Voth, Daniel E ^b   Heinzen, Robert A ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN DOT; PROTEIN ICMD; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SECRETION SYSTEM; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL VACUOLE; CONTROLLED STUDY; COXIELLA BURNETII; DOT GENE; DOT ICM TYPE IVB SECRETION SYSTEM; GENE INDUCTION; GENE INSERTION; GENETIC COMPLEMENTATION; GENETIC TRANSFORMATION; HIMAR1 TRANSPOSON; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; ICMB GENE; ICMD GENE; ICMJ GENE; LEISHMANIA; MACROPHAGE; NONHUMAN; PARASITOPHOROUS VACUOLE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SECRETION; TRANSPOSON; WILD TYPE; ANIMAL; CELL LINE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PROTEIN TRANSPORT; Q FEVER;

BACTERIA (MICROORGANISMS); COXIELLA BURNETII; LEGIONELLA PNEUMOPHILA; LEISHMANIA AMAZONENSIS; PROTOZOA;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL LINE; COXIELLA BURNETII; HUMANS; MACROPHAGES; PROTEIN TRANSPORT; Q FEVER; VACUOLES;

EID: 80052630257     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00175-11     Document Type: Article

References (50)

1. Maurin M, Raoult D. 1999. Q fever. Clin. Microbiol. Rev. 12:518-553.
2. Khavkin T, Tabibzadeh SS. 1988. Histologic, immunofluorescence, and electron microscopic study of infectious process in mouse lung after intranasal challenge with Coxiella burnetii. Infect. Immun. 56:1792-1799.
3. Stein A, et al. 2005. Q fever pneumonia: virulence of Coxiella burnetii pathovars in a murine model of aerosol infection. Infect. Immun. 73: 2469-2477.
4. Voth DE, Heinzen RA. 2007. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell. Microbiol. 9:829-840.
5. Howe D, Shannon JG, Winfree S, Dorward DW, Heinzen RA. 2010. Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages. Infect. Immun. 78:3465-3474.
6. Hackstadt T, Williams JC. 1981. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 78:3240-3244.
7. Campoy EM, Zoppino FC, Colombo MI. 2011. The early secretory pathway contributes to the growth of the Coxiella-replicative niche. Infect. Immun. 79:402-413.
8. Gutierrez MG, et al. 2005. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell. Microbiol. 7:981-993.
9. Romano PS, Gutierrez MG, Berón W, Rabinovitch M, Colombo MI. 2007. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell. Microbiol. 9:891-909.
10. Coleman SA, Fischer ER, Howe D, Mead DJ, Heinzen RA. 2004. Temporal analysis of Coxiella burnetii morphological differentiation. J. Bacteriol. 186:7344-7352.
11. Howe D, Melnicáková J, Barák I, Heinzen RA. 2003. Maturation of the Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication. Cell. Microbiol. 5:469-480.
12. Lührmann A, Nogueira CV, Carey KL, Roy CR. 2010. Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc. Natl. Acad. Sci. U. S. A. 107:18997-19001.
13. Lührmann A, Roy CR. 2007. Coxiella burnetii inhibits activation of host cell apoptosis through a mechanism that involves preventing cytochrome c release from mitochondria. Infect. Immun. 75:5282-5289.
14. Voth DE, Heinzen RA. 2009. Sustained activation of Akt and Erk1/2 is required for Coxiella burnetii antiapoptotic activity. Infect. Immun. 77: 205-213.
15. Voth DE, Howe D, Heinzen RA. 2007. Coxiella burnetii inhibits apoptosis in human THP-1 cells and monkey primary alveolar macrophages. Infect. Immun. 75:4263-4271.
16. Wallden K, Rivera-Calzada A, Waksman G. 2010. Type IV secretion systems: versatility and diversity in function. Cell. Microbiol. 12: 1203-1212.
17. Voth DE, Heinzen RA. 2009. Coxiella type IV secretion and cellular microbiology. Curr. Opin. Microbiol. 12:74-80.
18. Isberg RR, O'Connor TJ, Heidtman M. 2009. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat. Rev. Microbiol. 7:13-24.
19. Vogel JP. 2004. Turning a tiger into a house cat: using Legionella pneumophila to study Coxiella burnetii. Trends Microbiol. 12:103-105.
20. Carey KL, Newton HJ, Luhrmann A, Roy CR. 2011. The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication. PLoS Pathog. 7:e1002056.
21. Pan X, Lührmann A, Satoh A, Laskowski-Arce MA, Roy CR. 2008. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320:1651-1654.
22. Voth DE, et al. 2011. The Coxiella burnetii cryptic plasmid is enriched in genes encoding type IV secretion system substrates. J. Bacteriol. 193: 1493-1503.
23. Voth DE, et al. 2009. The Coxiella burnetii ankyrin repeat domaincontaining protein family is heterogeneous, with C-terminal truncationsthat influence Dot/Icm-mediated secretion. J. Bacteriol. 191:4232-4242.
24. Beare PA, Sandoz KM, Omsland A, Rockey DD, Heinzen RA. 2011. Advances in genetic manipulation of obligate intracellular bacterial pathogens. Front. Microbiol. 2:97.
25. Beare PA, et al. 2009. Characterization of a Coxiella burnetii ftsZ mutant generated by Himar1 transposon mutagenesis. J. Bacteriol. 191: 1369-1381.
26. Omsland A, et al. 2011. Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl. Environ. Microbiol. 77:3720-3725.
27. Omsland A, et al. 2009. Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc. Natl. Acad. Sci. U.S.A. 106:4430-4434.
28. Chen C, et al. 2010. Large-scale identification and translocation of type IVsecretion substrates by Coxiella burnetii. Proc. Natl. Acad. Sci. U. S. A. 107:21755-21760.
29. Vincent CD, et al. 2006. Identification of the core transmembrane complexof the Legionella Dot/Icm type IV secretion system. Mol. Microbiol.62:1278-1291.
30. Purcell M, Shuman HA. 1998. The Legionella pneumophila icmGCDJBF genes are required for killing of human macrophages. Infect. Immun. 66:2245-2255.
31. Choi KH, et al. 2005. A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods. 2:443-448.
32. Jin Z, El-Deiry WS. 2005. Overview of cell death signaling pathways. Cancer Biol. Ther. 4:139-163.
33. Antoine JC, Prina E, Lang T, Courret N. 1998. The biogenesis and properties of the parasitophorous vacuoles that harbour Leishmania in murine macrophages. Trends Microbiol. 6:392-401.
34. Veras PS, et al. 1995. Entry and survival of Leishmania amazonensis amastigotes within phagolysosome-like vacuoles that shelter Coxiella burnetii in Chinese hamster ovary cells. Infect. Immun. 63:3502-3506.
35. Mao F, Dam P, Chou J, Olman V, Xu Y. 2009. DOOR: a database for prokaryotic operons. Nucleic Acids Res. 37:D459-D463.
36. Segal G, Feldman M, Zusman T. 2005. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol. Rev. 29:65-81.
37. Segal G, Shuman HA. 1999. Possible origin of the Legionella pneumophila virulence genes and their relation to Coxiella burnetii. Mol. Microbiol. 33:669-670.
38. Seshadri R, et al. 2003. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. U. S. A. 100:5455-5460.
39. Hackstadt T, Williams JC. 1981. Stability of the adenosine 5- triphosphate pool in Coxiella burnetii: influence of pH and substrate. J. Bacteriol. 148:419-425.
40. Coers J, Monahan JJ, Roy CR. 1999. Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat. Cell Biol. 1:451-453.
41. Omsland A, Heinzen RA. Life on the outside: the rescue of Coxiella burnetii from its host cell. Annu. Rev. Microbiol., in press.
42. McConville MJ, de Souza D, Saunders E, Likic VA, Naderer T. 2007. Living in a phagolysosome; metabolism of Leishmania amastigotes. Trends Parasitol. 23:368-375.
43. Schaible UE, et al. 1999. Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J. Cell Sci. 112:681-693.
44. Roy CR, Berger KH, Isberg RR. 1998. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28:663-674.
45. Wiater LA, Dunn K, Maxfield FR, Shuman HA. 1998. Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila. Infect. Immun. 66:4450-4460.
46. Hilbi H, Segal G, Shuman HA. 2001. Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol. Microbiol. 42:603-617.
47. Baca OG, Klassen DA, Aragon AS. 1993. Entry of Coxiella burnetii into host cells. Acta Virol. 37:143-155.
48. Wilson J, et al. 2008. Control of parasitophorous vacuole expansion by LYST/Beige restricts the intracellular growth of Leishmania amazonensis. PLoS Pathog. 4:e1000179.
49. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH. 2010. The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One 5:e8668.
50. Chun KT, Edenberg HJ, Kelley MR, Goebl MG. 1997. Rapid amplification of uncharacterized transposon-taggedDNAsequences from genomic DNA. Yeast 13:233-240.