Yip1A, a Novel Host Factor for the Activation of the IRE1 Pathway of the Unfolded Protein Response during Infection
The genus Brucella is a serious intracellular pathogen that causes brucellosis in a wide range of animals including humans. Infection with Brucella spp. results in a significant economic and health burden due to its high infectivity, chronic nature, and difficulties in vaccine production. Better understanding of the host-pathogen interplay that supports Brucella replication is essential for the development of effective treatments for brucellosis. The unfolded protein response (UPR) has been implicated in the pathogenesis of several viral and bacterial infections. These pathogens modulate individual pathways of the UPR to enable their replication in host cells. Autophagy has also been linked to the survival of several intracellular pathogens. They subvert autophagic machineries of host cells to establish their safe replication niche. In the present study, we show that the activation of the IRE1 pathway of the UPR and the subsequent formation of ER-derived vacuoles are crucial for intracellular survival of B. abortus. In addition, we identified a novel host factor Yip1A that is responsible for these processes. Characterization of the function of Yip1A will provide new insights into the molecular mechanisms by which Brucella spp. replicates in host cells.
Vyšlo v časopise:
Yip1A, a Novel Host Factor for the Activation of the IRE1 Pathway of the Unfolded Protein Response during Infection. PLoS Pathog 11(3): e32767. doi:10.1371/journal.ppat.1004747
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004747
Souhrn
The genus Brucella is a serious intracellular pathogen that causes brucellosis in a wide range of animals including humans. Infection with Brucella spp. results in a significant economic and health burden due to its high infectivity, chronic nature, and difficulties in vaccine production. Better understanding of the host-pathogen interplay that supports Brucella replication is essential for the development of effective treatments for brucellosis. The unfolded protein response (UPR) has been implicated in the pathogenesis of several viral and bacterial infections. These pathogens modulate individual pathways of the UPR to enable their replication in host cells. Autophagy has also been linked to the survival of several intracellular pathogens. They subvert autophagic machineries of host cells to establish their safe replication niche. In the present study, we show that the activation of the IRE1 pathway of the UPR and the subsequent formation of ER-derived vacuoles are crucial for intracellular survival of B. abortus. In addition, we identified a novel host factor Yip1A that is responsible for these processes. Characterization of the function of Yip1A will provide new insights into the molecular mechanisms by which Brucella spp. replicates in host cells.
Zdroje
1. Pappas G, Akritidis N, Bosilkovski M, Tsianos E. Brucellosis. N Engl J Med. 2005;352: 2325–2336. 15930423
2. Starr T, Ng TW, Wehrly TD, Knodler LA, Celli J. Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 2008;9: 678–694. doi: 10.1111/j.1600-0854.2008.00718.x 18266913
3. Celli J, Salcedo SP, Gorvel JP. Brucella coopts the small GTPase Sar1 for intracellular replication. Proc Natl Acad Sci USA. 2005;102: 1673–1678. 15632218
4. Pizarro-Cerda J, Meresse S, Parton RG, van der Goot G, Sola-Landa A, Lopez-Goñi I, et al. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun. 1998;66: 5711–5724. 9826346
5. Pizarro-Cerdá J, Moreno E, Sanguedolce V, Mége J-L, Gorvel JP. Virulent Brucella abortus avoids lysosome fusion and distributes within autophagosome-like compartments. Infect Immun. 1998;66: 2387–2392. 9573138
6. Celli J, de Chastellier C, Franchini DM, Pizarro-Cerda J, Moreno E, Gorvel JP. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med. 2003;198: 545–556. 12925673
7. Hassan IH, Zhang MS, Powers LS, Shao JQ, Baltrusaitis J, Rutkowski DT, et al. Influenza A viral replication is blocked by inhibition of the inositol-requiring enzyme 1 (IRE1) stress pathway. J Biol Chem. 2012;287: 4679–4689. doi: 10.1074/jbc.M111.284695 22194594
8. Tardif KD, Mori K, Kaufman RJ, Siddiqui A. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J Biol Chem. 2004;279: 17158–17164. 14960590
9. Su HL, Liao CL, Lin YL. Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response. J Virol. 2002;76: 4162–4171. 11932381
10. Seimon TA, Kim MJ, Blumenthal A, Koo J, Ehrt S, Wainwright H. Induction of ER stress in macrophages of tuberculosis granulomas. PLoS One. 2010;5(9): e12772. doi: 10.1371/journal.pone.0012772 20856677
11. Baruch M, Belotserkovsky I, Hertzog BB, Ravins M, Dov E, Mclver KS, et al. An extracellular bacterial pathogen modulates host metabolism to regulate its own sensing and proliferation. Cell. 2014;156: 97–108. doi: 10.1016/j.cell.2013.12.007 24439371
12. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74: 739–789. 15952902
13. Qin QM, Pei J, Ancona V, Shaw BD, Ficht TA, de Figueiredo P. RNAi screen of endoplasmic reticulum-associated host factors reveals a role for IRE1alpha in supporting Brucella replication. PLoS Pathog. 2008;4: e1000110. doi: 10.1371/journal.ppat.1000110 18654626
14. de Jong MF, Starr T, Winter MG, den Hartigh AB, Child R, Knodler LA, et al. Sensing of Bacterial Type IV Secretion via the Unfolded Protein Response. mBio. 2013;4: e00418–12. doi: 10.1128/mBio.00418-12 23422410
15. Smith JA, Khan M, Magnani DD, Harms JS, Durward M, Radhakrishnan GK, et al. Brucella induces an unfolded protein response via TcpB that supports intracellular replication in macrophages. PLoS Pathog. 2013;9: e1003785. doi: 10.1371/journal.ppat.1003785 24339776
16. de Jong MF, Sun YH, den Hartigh AB, van Dijl JM, Tsolis RM. Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system. Mol Microbiol. 2008;70: 1378–1396. doi: 10.1111/j.1365-2958.2008.06487.x 19019140
17. de Barsy M, Jamet A, Filopon D, Nicolas C, Laloux G, Rual JF, et al. Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2. Cell Microbiol. 2011;13: 1044–1058. doi: 10.1111/j.1462-5822.2011.01601.x 21501366
18. de Barsy M, Mirabella A, Letesson JJ, De Bolle X. A Brucella abortus cstA mutant is defective for association with endoplasmic reticulum exit sites and displays altered trafficking in HeLa cells. Microbiology. 2012;158: 2610–2618. 22820839
19. Myeni S, Child R, Ng TW, Kupko JJ 3rd, Wehrly TD, Porcella SF, et al. Brucella modulates secretory trafficking via multiple type IV secretion effector proteins. PLoS Pathog. 2013;9: e1003556. doi: 10.1371/journal.ppat.1003556 23950720
20. Fugier E, Salcedo SP, de Chastellier C, Pophillat M, Muller A, Arce-Gorvel V, et al. The glyceraldehyde-3-phosphate dehydrogenase and the small GTPase Rab 2 are crucial for Brucella replication. PLoS Pathog. 2009;5: e1000487. doi: 10.1371/journal.ppat.1000487 19557163
21. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell. 2001;107: 881–91. 11779464
22. Sriburi R, Bommiasamy H, Buldak GL, Robbins GR, Frank M, Jackowski S, et al. Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J Biol Chem. 2007;282: 7024–7034. 17213183
23. D'Arcangelo JG, Stahmer KR, Miller EA. Vesicle-mediated export from the ER: COPII coat function and regulation. Biochim Biophys Acta. 2013;1833: 2464–2472. doi: 10.1016/j.bbamcr.2013.02.003 23419775
24. Tang BL, Ong YS, Huang B, Wei S, Wong ET, Qi R, et al. A membrane protein enriched in endoplasmic reticulum exit sites interacts with COPII. J Biol Chem. 2001;276: 40008–40017. 11489904
25. Korennykh AV, Egea PF, Korostelev AA, Finer-Moore J, Zhang C, Shokat KM, et al. The unfolded protein response signals through high-order assembly of Ire1. Nature. 2009;457: 687–693. doi: 10.1038/nature07661 19079236
26. Li H, Korennykh AV, Behrman SL, Walter P. Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc Natl Acad Sci USA. 2010;107 (37): 16113–16118. doi: 10.1073/pnas.1010580107 20798350
27. Bernales S, McDonald KL, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biology. 2006;4(12): e423. 17132049
28. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 2007;14: 1576–1582. 17612585
29. Graef M, Friedman JR, Graham C, Babu M, Nunnari J. ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell. 2013;24(18): 2918–2931. doi: 10.1091/mbc.E13-07-0381 23904270
30. Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI. Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic. 2010;11: 1246–1261. doi: 10.1111/j.1600-0854.2010.01086.x 20545908
31. Ge L, Melville D, Zhang M, Schekman R. The ER–Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. Elife. 2013;2: e00947. doi: 10.7554/eLife.00947 23930225
32. Wang J, Tan D, Cai Y, Reinisch KM, Walz T, Ferro-Novick S. A requirement for ER-derived COPII vesicles in phagophore initiation. Autophagy. 2014;10: 708–9. doi: 10.4161/auto.28103 24561915
33. Tan D, Cai Y, Wang J, Zhang J, Menon S, Chou H-T, et al. The EM structure of the TRAPPIII complex leads to the identification of a requirement for COPII vesicles on the macroautophagy pathway. Proc Natl Acad Sci USA. 2013;110: 19432–19437. doi: 10.1073/pnas.1316356110 24218626
34. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol. 2008;182:685–701. doi: 10.1083/jcb.200803137 18725538
35. Itakura E, Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy. 2010;6: 764–776. 20639694
36. Koyama-Honda I, Itakura E, Fujiwara TK, Mizushima N. Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy. 2013;9: 1491–9. doi: 10.4161/auto.25529 23884233
37. Jin C, Zhang Y, Zhu H, Ahmed K, Fu C, Yao X. Human Yip1A specifies the localization of Yif1 to the Golgi apparatus. Biochem Biophys Res Commun. 2005;334: 16–22. 15990086
38. Kano F, Yamauchi S, Yoshida Y, Watanabe-Takahashi M, Nishikawa K, Nakamura N, et al. Yip1A regulates the COPI-independent retrograde transport from the Golgi complex to the ER. J Cell Sci. 2009;122: 2218–2227. doi: 10.1242/jcs.043414 19509059
39. Dykstra KM, Pokusa JE, Suhan J, Lee TH. Yip1A structures the mammalian endoplasmic reticulum. Mol Biol Cell. 2010;21: 1556–1568. doi: 10.1091/mbc.E09-12-1002 20237155
40. Chen Y, Machner MP. Targeting of the small GTPase Rab6A’ by the Legionella pneumophila effector LidA. Infect Immun. 2013;81:2226–2235. doi: 10.1128/IAI.00157-13 23569112
41. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 2006;26(24): 9220–9231. 17030611
42. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ. 2008;15: 1460–1471. doi: 10.1038/cdd.2008.81 18551133
43. Arenas GN, Staskevich AS, Aballay A, Mayorga LS. Intracellular trafficking of Brucella abortus in J774 macrophages. Infect Immun. 2000;68: 4255–4263. 10858243
44. Suzuki K. Akioka M, Kondo-Kakuta C, Yamamoto H, Ohsumi Y. Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J Cell Sci. 2013;126: 2534–44. doi: 10.1242/jcs.122960 23549786
45. Orsi A, Razi M, Dooley H, Robinson D, Weston AE, Collinson LM, et al. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, is required for autophagy. Mol Biol Cell. 2012;23(10): 1860–73. doi: 10.1091/mbc.E11-09-0746 22456507
46. Starr T, Child R, Wehrly TD, Hansen B, Hwang S, Lopez-Otein C, et al. Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host & Microbe. 2012;11: 33–45.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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