Selective fragmentation of the trans-Golgi apparatus by Rickettsia rickettsii
Autoři:
Karin Aistleitner aff001; Tina Clark aff001; Cheryl Dooley aff001; Ted Hackstadt aff001
Působiště autorů:
Host-Parasite Interactions Section, Laboratory of Bacteriology, Rocky Mountain Laboratories, NIAID, NIH, Hamilton, Montana, United States of America
aff001
Vyšlo v časopise:
Selective fragmentation of the trans-Golgi apparatus by Rickettsia rickettsii. PLoS Pathog 16(5): e1008582. doi:10.1371/journal.ppat.1008582
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1008582
Souhrn
Fragmentation of the Golgi apparatus is observed during a number of physiological processes including mitosis and apoptosis, but also occurs in pathological states such as neurodegenerative diseases and some infectious diseases. Here we show that highly virulent strains of Rickettsia rickettsii, the causative agent of Rocky Mountain spotted fever, induce selective fragmentation of the trans-Golgi network (TGN) soon after infection of host cells by secretion of the effector protein Rickettsial Ankyrin Repeat Protein 2 (RARP2). Remarkably, this fragmentation is pronounced for the trans-Golgi network but the cis-Golgi remains largely intact and appropriately localized. Thus R. rickettsii targets specifically the TGN and not the entire Golgi apparatus. Dispersal of the TGN is mediated by the secreted effector protein RARP2, a recently identified type IV secreted effector that is a member of the clan CD cysteine proteases. Site-directed mutagenesis of a predicted cysteine protease active site in RARP2 prevents TGN disruption. General protein transport to the cell surface is severely impacted in cells infected with virulent strains of R. rickettsii. These findings suggest a novel manipulation of cellular organization by an obligate intracellular bacterium to determine interactions with the host cell.
Klíčová slova:
Golgi apparatus – Host cells – Intracellular pathogens – Membrane proteins – Protein transport – Vero cells – Virulence factors – Rickettsia rickettsii
Zdroje
1. Clark TR, Noriea NF, Bublitz DC, Ellison DW, Martens C, Lutter EI, et al. Comparative genome sequencing of Rickettsia rickettsii strains that differ in virulence. Infect Immun. 2015;83:1568–1576. doi: 10.1128/IAI.03140-14 25644009
2. Ricketts HT. Some aspects of Rocky Mountain spotted fever as shown by recent investigations. 1909. Rev Infect Dis. 1991;13:1227–1240. doi: 10.1093/clinids/13.6.1227 1775857
3. Ellison DW, Clark TR, Sturdevant DE, Virtaneva K, Porcella SF, Hackstadt T. Genomic comparison of virulent Rickettsia rickettsii Shiela Smith and avirulent Rickesttia rickettsii Iowa. Infect Immun. 2008;76(2):542–550. doi: 10.1128/IAI.00952-07 18025092
4. Lehman SS, Noriea NF, Aistleitner K, Clark TR, Dooley CA, Nair V, et al. The Rickettsial Ankyrin Repeat Protein 2 Is a Type IV Secreted Effector That Associates with the Endoplasmic Reticulum. MBio. 2018;9 e00975–18. doi: 10.1128/mBio.00975-18 29946049
5. Campadelli G, Brandimarti R, Di Lazzaro C, Ward PL, Roizman B, Torrisi MR. Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus after infection with herpes simplex virus 1. Proc Natl Acad Sci U S A. 1993;90:2798–2802. doi: 10.1073/pnas.90.7.2798 8385343
6. Kornfeld R, Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–64. doi: 10.1146/annurev.bi.54.070185.003215 3896128
7. Virtanen I, Ekblom P, Laurila P. Subcellular compartmentalization of saccharide moieties in cultured normal and malignant cells. Journal of Cell Biology. 1980;85:429–434. doi: 10.1083/jcb.85.2.429 7372714
8. Prescott AR, Lucocq JM, James J, Lister JM, Ponnambalam S. Distinct compartmentalization of TGN46 and beta 1,4-galactosyltransferase in HeLa cells. Eur J Cell Biol. 1997;72:238–246. 9084986
9. Boncompain G, Divoux S, Gareil N, de Forges H, Lescure A, Latreche L, et al. Synchronization of secretory protein traffic in populations of cells. Nat Methods. 2012;9:493–498. doi: 10.1038/nmeth.1928 22406856
10. Escoll P, Mondino S, Rolando M, Buchrieser C. Targeting of host organelles by pathogenic bacteria: a sophisticated subversion strategy. Nat Rev Microbiol. 2016;14:5–19. doi: 10.1038/nrmicro.2015.1 26594043
11. Lippincott-Schwartz J, Zaal KJ. Cell cycle maintenance and biogenesis of the Golgi complex. Histochemistry and cell biology. 2000;114:93–103. doi: 10.1007/s004180000176 11052258
12. Hicks SW, Machamer CE. Golgi structure in stress sensing and apoptosis. Biochimica et Biophysica Acta. 2005;1744:406–414. doi: 10.1016/j.bbamcr.2005.03.002 15979510
13. Niu TK, Pfeifer AC, Lippincott-Schwartz J, Jackson CL. Dynamics of GBF1, a Brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol Biol Cell. 2005;16:1213–1222. doi: 10.1091/mbc.E04-07-0599 15616190
14. Joshi G, Bekier ME 2nd, Wang Y. Golgi fragmentation in Alzheimer's disease. Frontiers in Neuroscience. 2015;9:340. doi: 10.3389/fnins.2015.00340 26441511
15. Beske O, Reichelt M, Taylor MP, Kirkegaard K, Andino R. Poliovirus infection blocks ERGIC-to-Golgi trafficking and induces microtubule-dependent disruption of the Golgi complex. J Cell Sci. 2007;120:3207–3218. doi: 10.1242/jcs.03483 17711878
16. Hansen MD, Johnsen IB, Stiberg KA, Sherstova T, Wakita T, Richard GM, et al. Hepatitis C virus triggers Golgi fragmentation and autophagy through the immunity-related GTPase M. Proc Natl Acad Sci U S A. 2017;114:E3462–e71. doi: 10.1073/pnas.1616683114 28389568
17. McCrossan M, Windsor M, Ponnambalam S, Armstrong J, Wileman T. The trans Golgi network is lost from cells infected with African swine fever virus. J Virol. 2001;75:11755–11765. doi: 10.1128/JVI.75.23.11755-11765.2001 11689656
18. Mousnier A, Swieboda D, Pinto A, Guedan A, Rogers AV, Walton R, et al. Human rhinovirus 16 causes Golgi apparatus fragmentation without blocking protein secretion. J Virol. 2014;88:11671–11685. doi: 10.1128/JVI.01170-14 25100828
19. Netherton CL, McCrossan MC, Denyer M, Ponnambalam S, Armstrong J, Takamatsu HH, et al. African swine fever virus causes microtubule-dependent dispersal of the trans-golgi network and slows delivery of membrane protein to the plasma membrane. J Virol. 2006;80:11385–11392. doi: 10.1128/JVI.00439-06 16956944
20. Burnaevskiy N, Fox TG, Plymire DA, Ertelt JM, Weigele BA, Selyunin AS, et al. Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor IpaJ. Nature. 2013;496:106–109. doi: 10.1038/nature12004 23535599
21. Mounier J, Boncompain G, Senerovic L, Lagache T, Chretien F, Perez F, et al. Shigella effector IpaB-induced cholesterol relocation disrupts the Golgi complex and recycling network to inhibit host cell secretion. Cell Host Microbe. 2012;12:381–389. doi: 10.1016/j.chom.2012.07.010 22980334
22. Truchan HK, VieBrock L, Cockburn CL, Ojugun N, Griffin BP, Wijesinghe DS, et al. Anaplasma phagocytophilium Rab10-dependent parasitism of the trans-Golgi network is critical for completion of the infection cycle. Cell Microbiol. 2015;18:260–281. doi: 10.1111/cmi.12500 26289115
23. Beyer AR, Rodino KG, VieBrock L, Green RS, Tegels BK, Oliver LDJ, et al. Orientia tsutsugamushi Ank9 is a multifunctional effector that utilizes a novel GRIP-like Golgi localization domain for Golgi-to-endoplasmic reticulum trafficking and interacts with host COPB2. Cell Microbiol. 2017;19:e12727.
24. Heuer D, Rejman Lipinski A, Machuy N, Karlas A, Wehrens A, Siedler F, et al. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature. 2009;457:731–735. doi: 10.1038/nature07578 19060882
25. Scidmore MA, Fischer ER, Hackstadt T. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J Cell Biol. 1996;134:363–374. doi: 10.1083/jcb.134.2.363 8707822
26. Brandizzi F, Barlowe C. Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Cell Mol Biol. 2013;14:382392.
27. Gillingham AK, Munro S. Finding the Golgi: Golgin coiled-coil proteins show the way. Trends Cell Biol. 2016;26:399–408. doi: 10.1016/j.tcb.2016.02.005 26972448
28. Boncompain G, Weigel AV. Transport and sorting in the Golgi complex: multiple mechanisms sort diverse cargo. Curr Opin Cell Biol. 2018;50:94–101. doi: 10.1016/j.ceb.2018.03.002 29567348
29. Witkos TM, Lowe M. Recognition and tertering of transport vesicles at the Golgi apparatus. Curr Opin Cell Biol. 2017;47:16–23. doi: 10.1016/j.ceb.2017.02.003 28237810
30. Goud B, Gleeson PA. TGN golgins, Rabs, and cytoskeleton: regulating the Golgi trafficking highways. Trends cell Biol. 2010;20:329–336. doi: 10.1016/j.tcb.2010.02.006 20227882
31. Tang D, Wang Y. Cell cycle regulation of Golgi membrane dynamics. Trends Cell Biol. 2013;23:296–304. doi: 10.1016/j.tcb.2013.01.008 23453991
32. Clements A, Smollett K, Lee SF, Hartland EL, Lowe M, Frankel G. EspG of enteropathogenic and enterohemorrhagic E. coli binds the Golgi matrix protein GM130 and disrupts the Golgi structure and function. Cell Microbiol. 2011;13:1429–1439. doi: 10.1111/j.1462-5822.2011.01631.x 21740499
33. Martin C, Leyton L, Hott M, Arancibia Y, Spichiger C, McNiven MA, et al. Herpes Simplex Virus Type 1 Neuronal Infection Perturbs Golgi Apparatus Integrity through Activation of Src Tyrosine Kinase and Dyn-2 GTPase. Front Cell Infect Microbiol. 2017;7:371. doi: 10.3389/fcimb.2017.00371 28879169
34. Jernigan KK, Bordenstein SR. Ankyrin domains across the Tree of Life. PeerJ. 2014;2:e264. doi: 10.7717/peerj.264 24688847
35. Zhang X, Wang Y. Glycosylation quality control by the Golgi structure. J Mol Biol. 2016;428:3183–3193. doi: 10.1016/j.jmb.2016.02.030 26956395
36. Sahni SK, Narra HP, Sahni A, Walker DH. Recent molecular insights into rickettsial pathogenesis and immunity. Future Microbiology. 2013;8(10):1265–88. doi: 10.2217/fmb.13.102 24059918
37. Walker DH, Olano JP, Feng H. Critical role of cytotoxic T lymphocytes in immune clearance of rickettsial infection. Infect Immun. 2001;69:1841–1846. doi: 10.1128/IAI.69.3.1841-1846.2001 11179362
38. Ambagala APN, Solheim JC, Srikumaran S. Viral interference with MHC class I antigen presentation pathway: the battle continues. Vet Immunol Immunopath. 2005;107:1–15.
39. Antoniou AN, Powis SJ. Pathogen evasion strategies for the major histocompatibility complex class I assembly pathway. Immunology. 2008;124:1–12. doi: 10.1111/j.1365-2567.2008.02804.x 18284468
40. Hansen TH, Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol. 2009;9:503–513. doi: 10.1038/nri2575 19498380
41. van de Weijer ML, Luteijn RD, Wiertz EJHJ. Viral Immune evasion: Lessons in MHC class I antigen presentation. Semin Immuno. 2015;27:125–137.
42. Rodino KG, Adcox HE, Martin RK, Patel V, Conrad DH, Carlyon JA. The obligate intracellular bacterium Oriential tsutsugamushi targets NLRC5 to modulate the major histocompatibility complex class I pathway. Infect Immun. 2019;87:e00876–18. doi: 10.1128/IAI.00876-18 30559222
43. Walker DH. Rickettsiae and rickettsial infections: the current state of knowledge. Clin Inf Dis. 2007;45:S39–44.
44. Anacker RL, Mann RE, Gonzales C. Reactivity of monoclonal antibodies to Rickettsia rickettsii with spotted fever and typhus group rickettsiae. J Clin Microbiol. 1987;25:167–171. 2432081
45. Hackstadt T, Rockey DD, Heinzen RA, Scidmore MA. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 1996;15(5):964–977. 8605892
46. Aistleitner K, Jeske R, Wolfel R, Weissner A, Kikhney J, Moter A, et al. Detection of Coxiella burnetii in heart valve sections by fluorescence in situ hybridization. J Med Microbiol. 2018;67:537–542. doi: 10.1099/jmm.0.000704 29461187
47. Mital J, Miller NJ, Dorward DW, Dooley CA, Hackstadt T. Role for chlamydial inclusion membrane proteins in inclusion membrane structure and biogenesis. PLoS ONE. 2013;8(5):e63426. doi: 10.1371/journal.pone.0063426 23696825
Článek vyšel v časopise
PLOS Pathogens
2020 Číslo 5
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- The hallmarks of COVID-19 disease
- Selective fragmentation of the trans-Golgi apparatus by Rickettsia rickettsii
- Clofazimine enhances the efficacy of BCG revaccination via stem cell-like memory T cells
- Harnessing the natural anti-glycan immune response to limit the transmission of enveloped viruses such as SARS-CoV-2