Coxiella burnetii Type 4B Secretion System-dependent manipulation of endolysosomal maturation is required for bacterial growth


Autoři: Dhritiman Samanta aff001;  Tatiana M. Clemente aff001;  Baleigh E. Schuler aff001;  Stacey D. Gilk aff001
Působiště autorů: Department of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, Indiana, United States of America aff001
Vyšlo v časopise: Coxiella burnetii Type 4B Secretion System-dependent manipulation of endolysosomal maturation is required for bacterial growth. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1007855
Kategorie: Research Article
doi: 10.1371/journal.ppat.1007855

Souhrn

Upon host cell infection, the obligate intracellular bacterium Coxiella burnetii resides and multiplies within the Coxiella–Containing Vacuole (CCV). The nascent CCV progresses through the endosomal maturation pathway into a phagolysosome, acquiring endosomal and lysosomal markers, as well as acidic pH and active proteases and hydrolases. Approximately 24–48 hours post infection, heterotypic fusion between the CCV and host endosomes/lysosomes leads to CCV expansion and bacterial replication in the mature CCV. Initial CCV acidification is required to activate C. burnetii metabolism and the Type 4B Secretion System (T4BSS), which secretes effector proteins required for CCV maturation. However, we found that the mature CCV is less acidic (pH~5.2) than lysosomes (pH~4.8). Further, inducing CCV acidification to pH~4.8 causes C. burnetii lysis, suggesting C. burnetii actively regulates pH of the mature CCV. Because heterotypic fusion with host endosomes/lysosomes may influence CCV pH, we investigated endosomal maturation in cells infected with wildtype (WT) or T4BSS mutant (ΔdotA) C. burnetii. In WT-infected cells, we observed a significant decrease in proteolytically active, LAMP1-positive endolysosomal vesicles, compared to mock or ΔdotA-infected cells. Using a ratiometric assay to measure endosomal pH, we determined that the average pH of terminal endosomes in WT-infected cells was pH~5.8, compared to pH~4.75 in mock and ΔdotA-infected cells. While endosomes progressively acidified from the periphery (pH~5.5) to the perinuclear area (pH~4.7) in both mock and ΔdotA-infected cells, endosomes did not acidify beyond pH~5.2 in WT-infected cells. Finally, increasing lysosomal biogenesis by overexpressing the transcription factor EB resulted in smaller, more proteolytically active CCVs and a significant decrease in C. burnetii growth, indicating host lysosomes are detrimental to C. burnetii. Overall, our data suggest that C. burnetii inhibits endosomal maturation to reduce the number of proteolytically active lysosomes available for heterotypic fusion with the CCV, possibly as a mechanism to regulate CCV pH.

Klíčová slova:

Autophagic cell death – Coxiella burnetii – Dextran – Endosomes – HeLa cells – Lysosomes – Phagosomes – Vesicles


Zdroje

1. Angelakis E, Raoult D. Q Fever. Vet Microbiol. 2010;140(3–4):297–309. Epub 2009/10/31. doi: 10.1016/j.vetmic.2009.07.016 19875249.

2. Romano PS, Gutierrez MG, Beron W, Rabinovitch M, Colombo MI. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol. 2007;9(4):891–909. Epub 2006/11/08. doi: 10.1111/j.1462-5822.2006.00838.x 17087732.

3. Voth DE, Heinzen RA. Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol. 2007;9(4):829–40. Epub 2007/03/27. doi: 10.1111/j.1462-5822.2007.00901.x 17381428.

4. Howe D, Mallavia LP. Coxiella burnetii exhibits morphological change and delays phagolysosomal fusion after internalization by J774A.1 cells. Infect Immun. 2000;68(7):3815–21. Epub 2000/06/17. doi: 10.1128/iai.68.7.3815-3821.2000 10858189.

5. Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect Immun. 1996;64(3):796–809. Epub 1996/03/01. 8641784.

6. Howe D, Shannon JG, Winfree S, Dorward DW, Heinzen RA. Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages. Infect Immun. 2010;78(8):3465–74. Epub 2010/06/03. doi: 10.1128/IAI.00406-10 20515926.

7. Beron W, Gutierrez MG, Rabinovitch M, Colombo MI. Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun. 2002;70(10):5816–21. Epub 2002/09/14. doi: 10.1128/IAI.70.10.5816-5821.2002 12228312.

8. Winchell CG, Graham JG, Kurten RC, Voth DE. Coxiella burnetii type IV secretion-dependent recruitment of macrophage autophagosomes. Infect Immun. 2014;82(6):2229–38. Epub 2014/03/20. doi: 10.1128/IAI.01236-13 24643534.

9. Winchell CG, Dragan AL, Brann KR, Onyilagha FI, Kurten RC, Voth DE. Coxiella burnetii Subverts p62/Sequestosome 1 and Activates Nrf2 Signaling in Human Macrophages. Infect Immun. 2018;86(5). Epub 2018/02/28. doi: 10.1128/IAI.00608-17 29483292.

10. Beare PA, Unsworth N, Andoh M, Voth DE, Omsland A, Gilk SD, et al. Comparative genomics reveal extensive transposon-mediated genomic plasticity and diversity among potential effector proteins within the genus Coxiella. Infect Immun. 2009;77(2):642–56. Epub 2008/12/03. doi: 10.1128/IAI.01141-08 19047403.

11. Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, Nelson WC, et al. Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci U S A. 2003;100(9):5455–60. Epub 2003/04/22. doi: 10.1073/pnas.0931379100 12704232.

12. Beare PA, Gilk SD, Larson CL, Hill J, Stead CM, Omsland A, et al. Dot/Icm Type IVB Secretion System Requirements for Coxiella burnetii Growth in Human Macrophages. mBio. 2011;2:e00175–11-e-11. doi: 10.1128/mBio.00175-11 21862628.

13. Carey KL, Newton HJ, Luhrmann A, Roy CR. 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. 2011;7(5):e1002056. Epub 2011/06/04. doi: 10.1371/journal.ppat.1002056 21637816.

14. Vogel JP. Turning a tiger into a house cat: using Legionella pneumophila to study Coxiella burnetii. Trends Microbiol. 2004;12(3):103–5. doi: 10.1016/j.tim.2004.01.008 15058276

15. Voth DE, Beare PA, Howe D, Sharma UM, Samoilis G, Cockrell DC, et al. The Coxiella burnetii cryptic plasmid is enriched in genes encoding type IV secretion system substrates. J Bacteriol. 2011;193(7):1493–503. Epub 2011/01/11. doi: 10.1128/JB.01359-10 21216993.

16. Howe D, Melnicakova J, Barak I, Heinzen RA. Maturation of the Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication. Cell Microbiol. 2003;5(7):469–80. Epub 2003/06/20. doi: 10.1046/j.1462-5822.2003.00293.x 12814437.

17. Akporiaye ET, Rowatt JD, Aragon AA, Baca OG. Lysosomal response of a murine macrophage-like cell line persistently infected with Coxiella burnetii. Infect Immun. 1983;40(3):1155–62. Epub 1983/06/01. 6852916.

18. Maurin M, Benoliel AM, Bongrand P, Rault D. Phagolysosome of Coxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect Immun. 1992;60(12):5013–6. Epub 1992/12/01. 1452331.

19. Hackstadt T, Williams JC. Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc Natl Acad Sci U S A. 1981;78(5):3240–4. Epub 1981/05/01. doi: 10.1073/pnas.78.5.3240 6942430.

20. Newton HJ, McDonough JA, Roy CR. Effector Protein Translocation by the Coxiella burnetii Dot/Icm Type IV Secretion System Requires Endocytic Maturation of the Pathogen-Occupied Vacuole. PLoS ONE. 2013;8. doi: 10.1371/journal.pone.0054566 23349930.

21. Horwitz MA. The Legionnaires’ disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med. 1983;158(6):2108–26. Epub 1983/12/01. doi: 10.1084/jem.158.6.2108 6644240.

22. Clemens DL, Horwitz MA. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med. 1995;181(1):257–70. Epub 1995/01/01. doi: 10.1084/jem.181.1.257 7807006.

23. Huang B, Hubber A, McDonough JA, Roy CR, Scidmore MA, Carlyon JA. The Anaplasma phagocytophilum-occupied vacuole selectively recruits Rab-GTPases that are predominantly associated with recycling endosomes. Cell Microbiol. 2010;12(9):1292–307. Epub 2010/03/30. doi: 10.1111/j.1462-5822.2010.01468.x 20345488.

24. Magunda F, Thompson CW, Schneider DA, Noh SM. Anaplasma marginale actively modulates vacuolar maturation during intracellular infection of its tick vector, Dermacentor andersoni. Appl Environ Microbiol. 2016;82(15):4715–31. Epub 2016/05/29. doi: 10.1128/AEM.01030-16 27235428.

25. Connor MG, Pulsifer AR, Price CT, Abu Kwaik Y, Lawrenz MB. Yersinia pestis Requires Host Rab1b for Survival in Macrophages. PLoS Pathog. 2015;11(10):e1005241. Epub 2015/10/27. doi: 10.1371/journal.ppat.1005241 26495854.

26. Samanta D, Gilk SD. Measuring pH of the Coxiella burnetii Parasitophorous Vacuole. Curr Protoc Microbiol. 2017;47:6C 3 1–6C 3 11. Epub 2017/11/10. doi: 10.1002/cpmc.38 29120485.

27. Mulye M, Samanta D, Winfree S, Heinzen RA, Gilk SD. Elevated cholesterol in the Coxiella burnetii intracellular niche is bacteriolytic. MBio. 2017;8(1):e02313–16. Epub 2017/03/02. doi: 10.1128/mBio.02313-16 28246364.

28. Mansilla Pareja ME, Bongiovanni A, Lafont F, Colombo MI. Alterations of the Coxiella burnetii Replicative Vacuole Membrane Integrity and Interplay with the Autophagy Pathway. Front Cell Infect Microbiol. 2017;7:112. Epub 2017/05/10. doi: 10.3389/fcimb.2017.00112 28484683.

29. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A. 2006;103(32):11821–7. Epub 2006/08/03. doi: 10.1073/pnas.0601617103 16882731.

30. Rubino M, Miaczynska M, Lippe R, Zerial M. Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem. 2000;275(6):3745–8. Epub 2000/02/08. doi: 10.1074/jbc.275.6.3745 10660521.

31. McBride HM, Rybin V, Murphy C, Giner A, Teasdale R, Zerial M. Oligomeric Complexes Link Rab5 Effectors with NSF and Drive Membrane Fusion via Interactions between EEA1 and Syntaxin 13. Cell. 1999;98(3):377–86. doi: 10.1016/s0092-8674(00)81966-2 10458612

32. Mills IG, Jones AT, Clague MJ. Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol. 1998;8(15):881–4. Epub 1998/08/26. doi: 10.1016/s0960-9822(07)00351-x 9705936.

33. Mills IG, Urbe S, Clague MJ. Relationships between EEA1 binding partners and their role in endosome fusion. J Cell Sci. 2001;114(Pt 10):1959–65. Epub 2001/05/01. 11329382.

34. Simonsen A, Gaullier JM, D’Arrigo A, Stenmark H. The Rab5 effector EEA1 interacts directly with syntaxin-6. J Biol Chem. 1999;274(41):28857–60. Epub 1999/10/03. doi: 10.1074/jbc.274.41.28857 10506127.

35. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature. 1999;397(6720):621–5. Epub 1999/03/02. doi: 10.1038/17618 10050856.

36. Helenius A, Mellman I, Wall D, Hubbard A. Endosomes. Trends in Biochemical Sciences. 1983;8(7):245–50. doi: 10.1016/0968-0004(83)90350-x

37. Huotari J, Helenius A. Endosome maturation. EMBO J. 2011;30(17):3481–500. Epub 2011/09/01. doi: 10.1038/emboj.2011.286 21878991.

38. Maxfield FR, Yamashiro DJ. Endosome acidification and the pathways of receptor-mediated endocytosis. Adv Exp Med Biol. 1987;225:189–98. Epub 1987/01/01. doi: 10.1007/978-1-4684-5442-0_16 2839960.

39. Von Bartheld CS, Altick AL. Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog Neurobiol. 2011;93(3):313–40. Epub 2011/01/11. doi: 10.1016/j.pneurobio.2011.01.003 21216273.

40. Granger BL, Green SA, Gabel CA, Howe CL, Mellman I, Helenius A. Characterization and cloning of lgp110, a lysosomal membrane glycoprotein from mouse and rat cells. J Biol Chem. 1990;265(20):12036–43. Epub 1990/07/15. 2142158.

41. Humphries WHt, Szymanski CJ, Payne CK. Endo-lysosomal vesicles positive for Rab7 and LAMP1 are terminal vesicles for the transport of dextran. PLoS One. 2011;6(10):e26626. Epub 2011/11/01. doi: 10.1371/journal.pone.0026626 22039519.

42. Mrakovic A, Kay JG, Furuya W, Brumell JH, Botelho RJ. Rab7 and Arl8 GTPases are necessary for lysosome tubulation in macrophages. Traffic (Copenhagen, Denmark). 2012;13(12):1667–79. Epub 2012/08/23. doi: 10.1111/tra.12003 22909026.

43. Barrett AJ. Human cathepsin B1. Purification and some properties of the enzyme. Biochemical Journal. 1973;131(4):809–22. doi: 10.1042/bj1310809 4124667.

44. Barrett AJ, Krischke H. Cathepsin B, cathepsin H and cathepsin L. Methods in Enzymology. 1981;80(Part C):535–61.

45. Van Noorden CJ, Boonacker E, Bissell ER, Meijer AJ, van Marle J, Smith RE. Ala-Pro-cresyl violet, a synthetic fluorogenic substrate for the analysis of kinetic parameters of dipeptidyl peptidase IV (CD26) in individual living rat hepatocytes. Anal Biochem. 1997;252(1):71–7. Epub 1997/11/05. doi: 10.1006/abio.1997.2312 9324943.

46. Ghigo E, Colombo MI, Heinzen RA. The Coxiella burnetii parasitophorous vacuole. Adv Exp Med Biol. 2012;984:141–69. Epub 2012/06/20. doi: 10.1007/978-94-007-4315-1_8 22711631.

47. Winfree S, Gilk SD. Quantitative Dextran Trafficking to the Coxiella burnetii Parasitophorous Vacuole. Curr Protoc Microbiol. 2017;46:6C 2 1–6C 2 12. Epub 2017/08/12. doi: 10.1002/cpmc.34 28800156.

48. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132(1):27–42. Epub 2008/01/15. doi: 10.1016/j.cell.2007.12.018 18191218.

49. Kohler LJ, Reed ShC, Sarraf SA, Arteaga DD, Newton HJ, Roy CR. Effector Protein Cig2 Decreases Host Tolerance of Infection by Directing Constitutive Fusion of Autophagosomes with the Coxiella-Containing Vacuole. MBio. 2016;7(4). Epub 2016/07/21. doi: 10.1128/mBio.01127-16 27435465.

50. Latomanski EA, Newton HJ. Interaction between autophagic vesicles and the Coxiella-containing vacuole requires CLTC (clathrin heavy chain). Autophagy. 2018;14(10):1710–25. Epub 2018/07/06. doi: 10.1080/15548627.2018.1483806 29973118.

51. Gutierrez MG, Vazquez CL, Munafo DB, Zoppino FC, Beron W, Rabinovitch M, et al. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol. 2005;7(7):981–93. Epub 2005/06/15. doi: 10.1111/j.1462-5822.2005.00527.x 15953030.

52. Larson CL, Sandoz KM, Cockrell DC, Heinzen RA. Noncanonical Inhibition of mTORC1 by Coxiella burnetii Promotes Replication within a Phagolysosome-Like Vacuole. MBio. 2019;10(1). Epub 2019/02/07. doi: 10.1128/mBio.02816-18 30723133.

53. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol. 2001;152(4):657–68. Epub 2001/03/27. doi: 10.1083/jcb.152.4.657 11266458.

54. Bananis E, Murray JW, Stockert RJ, Satir P, Wolkoff AW. Microtubule and motor-dependent endocytic vesicle sorting in vitro. J Cell Biol. 2000;151(1):179–86. Epub 2000/10/06. doi: 10.1083/jcb.151.1.179 11018063.

55. Johnson DE, Ostrowski P, Jaumouillé V, Grinstein S. The position of lysosomes within the cell determines their luminal pH. Journal of Cell Biology. 2016;212:677–92. doi: 10.1083/jcb.201507112 26975849.

56. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 1990;62(2):317–29. Epub 1990/07/27. doi: 10.1016/0092-8674(90)90369-p 2115402.

57. Laifenfeld D, Patzek LJ, McPhie DL, Chen Y, Levites Y, Cataldo AM, et al. Rab5 mediates an amyloid precursor protein signaling pathway that leads to apoptosis. J Neurosci. 2007;27(27):7141–53. Epub 2007/07/06. doi: 10.1523/JNEUROSCI.4599-06.2007 17611268.

58. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A. Identification of the switch in early-to-late endosome transition. Cell. 2010;141(3):497–508. Epub 2010/05/04. doi: 10.1016/j.cell.2010.03.011 20434987.

59. Yan Q, Lin M, Huang W, Teymournejad O, Johnson JM, Hays FA, et al. Ehrlichia type IV secretion system effector Etf-2 binds to active RAB5 and delays endosome maturation. Proc Natl Acad Sci U S A. 2018;115(38):E8977–E86. Epub 2018/09/06. doi: 10.1073/pnas.1806904115 30181274.

60. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325:473–7. doi: 10.1126/science.1174447 19556463.

61. Nezich CL, Wang C, Fogel AI, Youle RJ. MiT/TFE transcription factors are activated during mitophagy downstream of Parkin and Atg5. J Cell Biol. 2015;210(3):435–50. Epub 2015/08/05. doi: 10.1083/jcb.201501002 26240184.

62. Jones TC, Yeh S, Hirsch JG. The interaction between Toxoplasma gondii and mammalian cells: Mechanism of entry and intracellular fate of the parasite. J Exp Med. 1972;136(5):1157–72. Epub 1972/11/01. doi: 10.1084/jem.136.5.1157 5082671.

63. Friis RR. Interaction of L cells and Chlamydia psittaci: entry of the parasite and host responses to its development. J Bacteriol. 1972;110(2):706–21. Epub 1972/05/01. 4336694.

64. Verma S, Dixit R, Pandey KC. Cysteine Proteases: Modes of Activation and Future Prospects as Pharmacological Targets. Front Pharmacol. 2016;7:107. Epub 2016/05/21. doi: 10.3389/fphar.2016.00107 27199750.

65. Sanman LE, van der Linden WA, Verdoes M, Bogyo M. Bifunctional probes of cathepsin protease activity and pH reveal alterations in endolysosomal pH during bacterial Infection. Cell Chem Biol. 2016;23(7):793–804. Epub 2016/07/19. doi: 10.1016/j.chembiol.2016.05.019 27427229.

66. Miller HE, Hoyt FH, Heinzen RA. Replication of Coxiella burnetii in a lysosome-like vacuole does not require lysosomal hydrolases. Infect Immun. 2019. Epub 2019/08/14. doi: 10.1128/IAI.00493-19 31405956.

67. Omsland A, Cockrell DC, Howe D, Fischer ER, Virtaneva K, Sturdevant DE, et al. Host cell-free growth of the Q fever bacterium Coxiella burnetii. Proc Natl Acad Sci U S A. 2009;106(11):4430–4. Epub 2009/02/28. doi: 10.1073/pnas.0812074106 19246385.

68. Xu L, Shen X, Bryan A, Banga S, Swanson MS, Luo ZQ. Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog. 2010;6(3):e1000822. Epub 2010/03/25. doi: 10.1371/journal.ppat.1000822 20333253.

69. Hawke JP. A bacterium associated with disease of pond cultured channel catfish, Ictalurus punctatus. Journal of the Fisheries Board of Canada. 1979;36(12):1508–12. doi: 10.1139/f79-219

70. Baumgartner WA, Dubytska L, Rogge ML, Mottram PJ, Thune RL. Modulation of vacuolar pH is required for replication of Edwardsiella ictaluri in channel catfish macrophages. Infect Immun. 2014;82(6):2329–36. Epub 2014/03/26. doi: 10.1128/IAI.01616-13 24664505.

71. Scott DR, Weeks D, Hong C, Postius S, Melchers K, Sachs G. The role of internal urease in acid resistance of Helicobacter pylori. Gastroenterology. 1998;114(1):58–70. Epub 1998/01/15. doi: 10.1016/s0016-5085(98)70633-x 9428219.

72. Larson CL, Heinzen RA. High-Content Imaging Reveals Expansion of the Endosomal Compartment during Coxiella burnetii Parasitophorous Vacuole Maturation. Front Cell Infect Microbiol. 2017;7:48. Epub 2017/03/16. doi: 10.3389/fcimb.2017.00048 28293541.

73. Latomanski EA, Newton P, Khoo CA, Newton HJ. The Effector Cig57 Hijacks FCHO-Mediated Vesicular Trafficking to Facilitate Intracellular Replication of Coxiella burnetii. PLoS Pathog. 2016;12(12):e1006101. Epub 2016/12/22. doi: 10.1371/journal.ppat.1006101 28002452.

74. Pearse BM. Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc Natl Acad Sci U S A. 1976;73(4):1255–9. Epub 1976/04/01. doi: 10.1073/pnas.73.4.1255 1063406.

75. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell. 2005;122(5):735–49. Epub 2005/09/07. doi: 10.1016/j.cell.2005.06.043 16143105.

76. Vonderheit A, Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol. 2005;3(7):e233. Epub 2005/06/16. doi: 10.1371/journal.pbio.0030233 15954801.

77. Horiuchi H, Lippe R, McBride HM, Rubino M, Woodman P, Stenmark H, et al. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell. 1997;90(6):1149–59. Epub 1997/10/10. doi: 10.1016/s0092-8674(00)80380-3 9323142.

78. Barr F, Lambright DG. Rab GEFs and GAPs. Curr Opin Cell Biol. 2010;22(4):461–70. Epub 2010/05/15. doi: 10.1016/j.ceb.2010.04.007 20466531.

79. Wurmser AE, Sato TK, Emr SD. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J Cell Biol. 2000;151(3):551–62. Epub 2000/11/04. doi: 10.1083/jcb.151.3.551 11062257.

80. Kinchen JM, Ravichandran KS. Phagosome maturation: going through the acid test. Nat Rev Mol Cell Biol. 2008;9(10):781–95. Epub 2008/09/25. doi: 10.1038/nrm2515 18813294.

81. Alvarez-Dominguez C, Madrazo-Toca F, Fernandez-Prieto L, Vandekerckhove J, Pareja E, Tobes R, et al. Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic (Copenhagen, Denmark). 2008;9(3):325–37. Epub 2007/12/20. doi: 10.1111/j.1600-0854.2007.00683.x 18088303.

82. Mottola G, Boucherit N, Trouplin V, Oury Barry A, Soubeyran P, Mege JL, et al. Tropheryma whipplei, the agent of Whipple’s disease, affects the early to late phagosome transition and survives in a Rab5- and Rab7-positive compartment. PLoS One. 2014;9(2):e89367. Epub 2014/03/04. doi: 10.1371/journal.pone.0089367 24586722.

83. Larson CL, Martinez E, Beare PA, Jeffrey B, Heinzen RA, Bonazzi M. Right on Q: genetics begin to unravel Coxiella burnetii host cell interactions. Future Microbiol. 2016;11:919–39. Epub 2016/07/16. doi: 10.2217/fmb-2016-0044 27418426.

84. Larson CL, Beare PA, Howe D, Heinzen RA. Coxiella burnetii effector protein subverts clathrin-mediated vesicular trafficking for pathogen vacuole biogenesis. Proc Natl Acad Sci U S A. 2013;110(49):E4770–9. Epub 2013/11/20. doi: 10.1073/pnas.1309195110 24248335.

85. Martinez E, Allombert J, Cantet F, Lakhani A, Yandrapalli N, Neyret A, et al. Coxiella burnetii effector CvpB modulates phosphoinositide metabolism for optimal vacuole development. Proc Natl Acad Sci U S A. 2016;113(23):E3260–9. Epub 2016/05/27. doi: 10.1073/pnas.1522811113 27226300.

86. Fratti RA, Chua J, Vergne I, Deretic V. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A. 2003;100(9):5437–42. Epub 2003/04/19. doi: 10.1073/pnas.0737613100 12702770.

87. Puri RV, Reddy PV, Tyagi AK. Secreted acid phosphatase (SapM) of Mycobacterium tuberculosis is indispensable for arresting phagosomal maturation and growth of the pathogen in guinea pig tissues. PLoS One. 2013;8(7):e70514. Epub 2013/08/08. doi: 10.1371/journal.pone.0070514 23923000.

88. Gaspar AH, Machner MP. VipD is a Rab5-activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion. Proc Natl Acad Sci U S A. 2014;111(12):4560–5. Epub 2014/03/13. doi: 10.1073/pnas.1316376111 24616501.

89. Newton HJ, Kohler LJ, McDonough JA, Temoche-Diaz M, Crabill E, Hartland EL, et al. A screen of Coxiella burnetii mutants reveals important roles for Dot/Icm effectors and host autophagy in vacuole biogenesis. PLoS Pathog. 2014;10(7):e1004286. Epub 2014/08/01. doi: 10.1371/journal.ppat.1004286 25080348.

90. Omsland A, Beare PA, Hill J, Cockrell DC, Howe D, Hansen B, et al. Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl Environ Microbiol. 2011;77(11):3720–5. Epub 2011/04/12. doi: 10.1128/AEM.02826-10 21478315.

91. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. Epub 2012/06/30. doi: 10.1038/nmeth.2019 22743772.

92. Vallejo Esquerra E, Yang H, Sanchez SE, Omsland A. Physicochemical and Nutritional Requirements for Axenic Replication Suggest Physiological Basis for Coxiella burnetii Niche Restriction. Front Cell Infect Microbiol. 2017;7:190. Epub 2017/06/18. doi: 10.3389/fcimb.2017.00190 28620582.

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2019 Číslo 12

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Co je dobré vědět o IPF
nový kurz
Autoři:

Nová éra v léčbě migrény
Autoři: MUDr. Eva Medová, MUDr. Tomáš Nežádal, Ph.D.

Imunitní trombocytopenie (ITP) u dospělých pacientů
Autoři: prof. MUDr. Tomáš Kozák, Ph.D., MBA

Význam nutraceutik u kardiovaskulárních onemocnění

Pěnová skleroterapie
Autoři: MUDr. Marek Šlais

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×