#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

KSHV activates unfolded protein response sensors but suppresses downstream transcriptional responses to support lytic replication


Autoři: Benjamin P. Johnston aff001;  Eric S. Pringle aff001;  Craig McCormick aff001
Působiště autorů: Department of Microbiology & Immunology, Dalhousie University, Halifax, Nova Scotia, Canada aff001;  Beatrice Hunter Cancer Research Institute, Halifax, Nova Scotia, Canada aff002
Vyšlo v časopise: KSHV activates unfolded protein response sensors but suppresses downstream transcriptional responses to support lytic replication. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008185
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008185

Souhrn

Herpesviruses usurp host cell protein synthesis machinery to convert viral mRNAs into proteins, and the endoplasmic reticulum (ER) to ensure proper folding, post-translational modification and trafficking of secreted and transmembrane viral proteins. Overloading ER folding capacity activates the unfolded protein response (UPR), whereby sensor proteins ATF6, PERK and IRE1 initiate a stress-mitigating transcription program that accelerates catabolism of misfolded proteins while increasing ER folding capacity. Kaposi’s sarcoma-associated herpesvirus (KSHV) can be reactivated from latency by chemical induction of ER stress, which causes accumulation of the XBP1s transcription factor that transactivates the viral RTA lytic switch gene. The presence of XBP1s-responsive elements in the RTA promoter suggests that KSHV evolved a mechanism to respond to ER stress. Here, we report that ATF6, PERK and IRE1 were activated upon reactivation from latency and required for efficient KSHV lytic replication; genetic or pharmacologic inhibition of each UPR sensor diminished virion production. Despite UPR sensor activation during KSHV lytic replication, downstream UPR transcriptional responses were restricted; 1) ATF6 was cleaved to activate the ATF6(N) transcription factor but ATF6(N)-responsive genes were not transcribed; 2) PERK phosphorylated eIF2α but ATF4 did not accumulate; 3) IRE1 caused XBP1 mRNA splicing, but XBP1s protein did not accumulate and XBP1s-responsive genes were not transcribed. Ectopic expression of the KSHV host shutoff protein SOX did not affect UPR gene expression, suggesting that alternative viral mechanisms likely mediate UPR suppression during lytic replication. Complementation of XBP1s deficiency during KSHV lytic replication inhibited virion production in a dose-dependent manner in iSLK.219 cells but not in TREx-BCBL1-RTA cells. However, genetically distinct KSHV virions harvested from these two cell lines were equally susceptible to XBP1s restriction following infection of naïve iSLK cells. This suggests that cell-intrinsic properties of BCBL1 cells may circumvent the antiviral effect of ectopic XBP1s expression. Taken together, these findings indicate that while XBP1s plays an important role in reactivation from latency, it can inhibit virus replication at a later step, which the virus overcomes by preventing its synthesis. These findings suggest that KSHV hijacks UPR sensors to promote efficient viral replication while sustaining ER stress.

Klíčová slova:

DNA transcription – Endoplasmic reticulum – Kaposi's sarcoma-associated herpesvirus – Messenger RNA – Phosphorylation – Transcription factors – Viral replication – Virions


Zdroje

1. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. England; 2007;8: 519–529. doi: 10.1038/nrm2199 17565364

2. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. United States; 2011;334: 1081–1086. doi: 10.1126/science.1209038 22116877

3. Wang M, Kaufman RJ. Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature. England; 2016;529: 326–335. doi: 10.1038/nature17041 26791723

4. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. England; 2012;13: 89–102. doi: 10.1038/nrm3270 22251901

5. Gardner BM, Pincus D, Gotthardt K, Gallagher CM, Walter P. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol. United States; 2013;5: a013169. doi: 10.1101/cshperspect.a013169 23388626

6. Zhang K, Kaufman RJ. Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem. United States; 2004;279: 25935–25938. doi: 10.1074/jbc.R400008200 15070890

7. Okada T, Haze K, Nadanaka S, Yoshida H, Seidah NG, Hirano Y, et al. A serine protease inhibitor prevents endoplasmic reticulum stress-induced cleavage but not transport of the membrane-bound transcription factor ATF6. J Biol Chem. United States; 2003;278: 31024–31032. doi: 10.1074/jbc.M300923200 12782636

8. Ye J, Rawson RB, Komuro R, Chen X, Davé UP, Prywes R, et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell. Elsevier; 2000;6: 1355–64. doi: 10.1016/s1097-2765(00)00133-7 11163209

9. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. England; 1999;397: 271–274. doi: 10.1038/16729 9930704

10. Clemens MJ, Pain VM, Wong ST, Henshaw EC. Phosphorylation inhibits guanine nucleotide exchange on eukaryotic initiation factor 2. Nature. England; 1982;296: 93–95.

11. Krishnamoorthy T, Pavitt GD, Zhang F, Dever TE, Hinnebusch AG. Tight binding of the phosphorylated alpha subunit of initiation factor 2 (eIF2alpha) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol Cell Biol. United States; 2001;21: 5018–5030. doi: 10.1128/MCB.21.15.5018-5030.2001 11438658

12. Merrick WC. Mechanism and regulation of eukaryotic protein synthesis. Microbiol Rev. United States; 1992;56: 291–315. 1620067

13. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell. United States; 2010;40: 228–237. doi: 10.1016/j.molcel.2010.09.028 20965418

14. Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci U S A. United States; 2004;101: 11269–11274. doi: 10.1073/pnas.0400541101 15277680

15. Rzymski T, Milani M, Pike L, Buffa F, Mellor HR, Winchester L, et al. Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene. England; 2010;29: 4424–4435. doi: 10.1038/onc.2010.191 20514020

16. B’chir W, Maurin A-C, Carraro V, Averous J, Jousse C, Muranishi Y, et al. The eIF2alpha/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res. England; 2013;41: 7683–7699. doi: 10.1093/nar/gkt563 23804767

17. Ma Y, Hendershot LM. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem. United States; 2003;278: 34864–34873. doi: 10.1074/jbc.M301107200 12840028

18. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol. Rockefeller University Press; 2001;153: 1011–22. doi: 10.1083/jcb.153.5.1011 11381086

19. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell. United States; 2003;11: 619–633.

20. Lu PD, Harding HP, Ron D. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol. United States; 2004;167: 27–33. doi: 10.1083/jcb.200408003 15479734

21. Han J, Back SH, Hur J, Lin Y-H, Gildersleeve R, Shan J, et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol. England; 2013;15: 481–490. doi: 10.1038/ncb2738 23624402

22. Ma Y, Brewer JW, Diehl JA, Hendershot LM. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J Mol Biol. England; 2002;318: 1351–1365. doi: 10.1016/s0022-2836(02)00234-6 12083523

23. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. England; 2004;11: 381–389. doi: 10.1038/sj.cdd.4401373 14685163

24. Cox JS, Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell. United States; 1996;87: 391–404. doi: 10.1016/s0092-8674(00)81360-4 8898193

25. 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. United States; 2001;107: 881–891. doi: 10.1016/s0092-8674(01)00611-0 11779464

26. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, Okada T, et al. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. United States; 2002;16: 452–466. doi: 10.1101/gad.964702 11850408

27. Jurkin J, Henkel T, Nielsen AF, Minnich M, Popow J, Kaufmann T, et al. The mammalian tRNA ligase complex mediates splicing of XBP1 mRNA and controls antibody secretion in plasma cells. EMBO J. England; 2014;33: 2922–2936. doi: 10.15252/embj.201490332 25378478

28. Lu Y, Liang F-X, Wang X. A synthetic biology approach identifies the mammalian UPR RNA ligase RtcB. Mol Cell. United States; 2014;55: 758–770. doi: 10.1016/j.molcel.2014.06.032 25087875

29. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, et al. XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell. United States; 2007;27: 53–66. doi: 10.1016/j.molcel.2007.06.011 17612490

30. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol. United States; 2009;186: 323–331. doi: 10.1083/jcb.200903014 19651891

31. Hollien J, Weissman JS. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science. United States; 2006;313: 104–107. doi: 10.1126/science.1129631 16825573

32. Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature. 2001;412: 300–307. doi: 10.1038/35085509 11460154

33. Iwakoshi NN, Lee A-H, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol. Nature Publishing Group; 2003;4: 321–329. doi: 10.1038/ni907 12612580

34. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi’s sarcoma. Science. United States; 1994;266: 1865–1869. doi: 10.1126/science.7997879 7997879

35. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM. Kaposi’s sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med. United States; 1995;332: 1186–1191. doi: 10.1056/NEJM199505043321802 7700311

36. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, Babinet P, et al. Kaposi’s sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman’s disease. Blood. United States; 1995;86: 1276–1280. 7632932

37. Coleman CB, Nealy MS, Tibbetts SA. Immature and transitional B cells are latency reservoirs for a gammaherpesvirus. J Virol. United States; 2010;84: 13045–13052. doi: 10.1128/JVI.01455-10 20926565

38. Klein U, Gloghini A, Gaidano G, Chadburn A, Cesarman E, Dalla-Favera R, et al. Gene expression profile analysis of AIDS-related primary effusion lymphoma (PEL) suggests a plasmablastic derivation and identifies PEL-specific transcripts. Blood. United States; 2003;101: 4115–4121. doi: 10.1182/blood-2002-10-3090 12531789

39. Du MQ, Liu H, Diss TC, Ye H, Hamoudi RA, Dupin N, et al. Kaposi sarcoma-associated herpesvirus infects monotypic (IgM lambda) but polyclonal naive B cells in Castleman disease and associated lymphoproliferative disorders. Blood. United States; 2001;97: 2130–2136.

40. Jenner RG, Maillard K, Cattini N, Weiss RA, Boshoff C, Wooster R, et al. Kaposi’s sarcoma-associated herpesvirus-infected primary effusion lymphoma has a plasma cell gene expression profile. Proc Natl Acad Sci U S A. United States; 2003;100: 10399–10404. doi: 10.1073/pnas.1630810100 12925741

41. Yu F, Feng J, Harada JN, Chanda SK, Kenney SC, Sun R. B cell terminal differentiation factor XBP-1 induces reactivation of Kaposi’s sarcoma-associated herpesvirus. FEBS Lett. John Wiley & Sons, Ltd; 2007;581: 3485–3488. doi: 10.1016/j.febslet.2007.06.056 17617410

42. Wilson SJ, Tsao EH, Webb BLJ, Ye H, Dalton-Griffin L, Tsantoulas C, et al. X Box Binding Protein XBP-1s Transactivates the Kaposi’s Sarcoma-Associated Herpesvirus (KSHV) ORF50 Promoter, Linking Plasma Cell Differentiation to KSHV Reactivation from Latency. J Virol. 2007;81: 13578–13586. doi: 10.1128/JVI.01663-07 17928342

43. Dalton-Griffin L, Wilson SJ, Kellam P. X-box binding protein 1 contributes to induction of the Kaposi’s sarcoma-associated herpesvirus lytic cycle under hypoxic conditions. J Virol. United States; 2009;83: 7202–7209. doi: 10.1128/JVI.00076-09 19403667

44. Sun R, Lin SF, Gradoville L, Yuan Y, Zhu F, Miller G. A viral gene that activates lytic cycle expression of Kaposi’s sarcoma-associated herpesvirus. Proc Natl Acad Sci U S A. United States; 1998;95: 10866–10871. doi: 10.1073/pnas.95.18.10866 9724796

45. Lukac DM, Renne R, Kirshner JR, Ganem D. Reactivation of Kaposi’s sarcoma-associated herpesvirus infection from latency by expression of the ORF 50 transactivator, a homolog of the EBV R protein. Virology. United States; 1998;252: 304–312. doi: 10.1006/viro.1998.9486 9878608

46. Liang Y, Chang J, Lynch SJ, Lukac DM, Ganem D. The lytic switch protein of KSHV activates gene expression via functional interaction with RBP-Jkappa (CSL), the target of the Notch signaling pathway. Genes Dev. United States; 2002;16: 1977–1989. doi: 10.1101/gad.996502 12154127

47. Hu D, Wang V, Yang M, Abdullah S, Davis DA, Uldrick TS, et al. Induction of Kaposi’s Sarcoma-Associated Herpesvirus-Encoded Viral Interleukin-6 by X-Box Binding Protein 1. J Virol. United States; 2016;90: 368–378. doi: 10.1128/JVI.01192-15 26491160

48. Aoki Y, Tosato G, Fonville TW, Pittaluga S. Serum viral interleukin-6 in AIDS-related multicentric Castleman disease. Blood. United States; 2001. pp. 2526–2527.

49. Aoki Y, Yarchoan R, Braun J, Iwamoto A, Tosato G. Viral and cellular cytokines in AIDS-related malignant lymphomatous effusions. Blood. United States; 2000;96: 1599–1601. 10942415

50. Polizzotto MN, Uldrick TS, Wang V, Aleman K, Wyvill KM, Marshall V, et al. Human and viral interleukin-6 and other cytokines in Kaposi sarcoma herpesvirus-associated multicentric Castleman disease. Blood. United States; 2013;122: 4189–4198. doi: 10.1182/blood-2013-08-519959 24174627

51. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee A-H, Qian S-B, Zhao H, et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity. United States; 2004;21: 81–93. doi: 10.1016/j.immuni.2004.06.010 15345222

52. Iwakoshi NN, Lee A-H, Vallabhajosyula P, Otipoby KL, Rajewsky K, Glimcher LH. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol. United States; 2003;4: 321–329. doi: 10.1038/ni907 12612580

53. Cheng G, Feng Z, He B. Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2alpha dephosphorylation by the gamma(1)34.5 protein. J Virol. United States; 2005;79: 1379–1388. doi: 10.1128/JVI.79.3.1379-1388.2005 15650164

54. Isler JA, Skalet AH, Alwine JC. Human cytomegalovirus infection activates and regulates the unfolded protein response. J Virol. United States; 2005;79: 6890–6899. doi: 10.1128/JVI.79.11.6890-6899.2005 15890928

55. Siddiquey MNA, Zhang H, Nguyen CC, Domma AJ, Kamil JP. The Human Cytomegalovirus Endoplasmic Reticulum-Resident Glycoprotein UL148 Activates the Unfolded Protein Response. J Virol. United States; 2018;92. doi: 10.1128/JVI.00896-18 30045994

56. Mulvey M, Arias C, Mohr I. Maintenance of endoplasmic reticulum (ER) homeostasis in herpes simplex virus type 1-infected cells through the association of a viral glycoprotein with PERK, a cellular ER stress sensor. J Virol. United States; 2007;81: 3377–3390. doi: 10.1128/JVI.02191-06 17229688

57. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, Jung JU. Global changes in Kaposi’s sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J Virol. United States; 2003;77: 4205–4220. doi: 10.1128/JVI.77.7.4205-4220.2003 12634378

58. Lytton J, Westlin M, Hanley MR. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J Biol Chem. United States; 1991;266: 17067–17071. 1832668

59. Gallagher CM, Garri C, Cain EL, Ang KK-H, Wilson CG, Chen S, et al. Ceapins are a new class of unfolded protein response inhibitors, selectively targeting the ATF6alpha branch. Elife. England; 2016;5. doi: 10.7554/eLife.11878 27435960

60. Wang Y, Shen J, Arenzana N, Tirasophon W, Kaufman RJ, Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem. United States; 2000;275: 27013–27020. doi: 10.1074/jbc.M003322200 10856300

61. Shoulders MD, Ryno LM, Genereux JC, Moresco JJ, Tu PG, Wu C, et al. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep. United States; 2013;3: 1279–1292. doi: 10.1016/j.celrep.2013.03.024 23583182

62. Li M, Baumeister P, Roy B, Phan T, Foti D, Luo S, et al. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol Cell Biol. United States; 2000;20: 5096–5106. doi: 10.1128/mcb.20.14.5096-5106.2000 10866666

63. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell. United States; 2007;13: 351–364. doi: 10.1016/j.devcel.2007.07.005 17765679

64. Meurs E, Chong K, Galabru J, Thomas NS, Kerr IM, Williams BR, et al. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell. United States; 1990;62: 379–390. doi: 10.1016/0092-8674(90)90374-n 1695551

65. Dever TE, Feng L, Wek RC, Cigan AM, Donahue TF, Hinnebusch AG. Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell. United States; 1992;68: 585–596. doi: 10.1016/0092-8674(92)90193-g 1739968

66. Hurst R, Schatz JR, Matts RL. Inhibition of rabbit reticulocyte lysate protein synthesis by heavy metal ions involves the phosphorylation of the alpha-subunit of the eukaryotic initiation factor 2. J Biol Chem. United States; 1987;262: 15939–15945. 3680235

67. Axten JM, Medina JR, Feng Y, Shu A, Romeril SP, Grant SW, et al. Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl)phenyl]acetyl}-2,3-dihydro-1H-indol-5-yl)-7H-pyrrolo[2,3-d]pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J Med Chem. United States; 2012;55: 7193–7207. doi: 10.1021/jm300713s 22827572

68. Harding HP, Zyryanova AF, Ron D. Uncoupling proteostasis and development in vitro with a small molecule inhibitor of the pancreatic endoplasmic reticulum kinase, PERK. J Biol Chem. United States; 2012;287: 44338–44344. doi: 10.1074/jbc.M112.428987 23148209

69. Merlie JP, Sebbane R, Tzartos S, Lindstrom J. Inhibition of glycosylation with tunicamycin blocks assembly of newly synthesized acetylcholine receptor subunits in muscle cells. J Biol Chem. United States; 1982;257: 2694–2701. 7061443

70. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. United States; 1999;13: 1211–1233. doi: 10.1101/gad.13.10.1211 10346810

71. Li B, Yi P, Zhang B, Xu C, Liu Q, Pi Z, et al. Differences in endoplasmic reticulum stress signalling kinetics determine cell survival outcome through activation of MKP-1. Cell Signal. England; 2011;23: 35–45. doi: 10.1016/j.cellsig.2010.07.019 20727407

72. Lee A-H, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol. United States; 2003;23: 7448–7459. doi: 10.1128/MCB.23.21.7448-7459.2003 14559994

73. Glaunsinger B, Ganem D. Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol Cell. United States; 2004;13: 713–723. doi: 10.1016/s1097-2765(04)00091-7 15023341

74. Chandriani S, Ganem D. Host Transcript Accumulation during Lytic KSHV Infection Reveals Several Classes of Host Responses. PLoS One. 2007;2: e811. doi: 10.1371/journal.pone.0000811 17726541

75. Lee YJ, Glaunsinger BA. Aberrant Herpesvirus-Induced Polyadenylation Correlates With Cellular Messenger RNA Destruction. PLoS Biol. 2009;7: e1000107. doi: 10.1371/journal.pbio.1000107 19468299

76. Abernathy E, Gilbertson S, Alla R, Glaunsinger B. Viral Nucleases Induce an mRNA Degradation-Transcription Feedback Loop in Mammalian Cells. Cell Host Microbe. Elsevier; 2015;18: 243–253. doi: 10.1016/j.chom.2015.06.019 26211836

77. Clyde K, Glaunsinger BA. Deep Sequencing Reveals Direct Targets of Gammaherpesvirus-Induced mRNA Decay and Suggests That Multiple Mechanisms Govern Cellular Transcript Escape. PLoS One. 2011;6: e19655. doi: 10.1371/journal.pone.0019655 21573023

78. Glaunsinger B, Chavez L, Ganem D. The exonuclease and host shutoff functions of the SOX protein of Kaposi’s sarcoma-associated herpesvirus are genetically separable. J Virol. 2005;79: 7396–401. doi: 10.1128/JVI.79.12.7396-7401.2005 15919895

79. Sidrauski C, Tsai JC, Kampmann M, Hearn BR, Vedantham P, Jaishankar P, et al. Pharmacological dimerization and activation of the exchange factor eIF2B antagonizes the integrated stress response. Elife. England; 2015;4: e07314. doi: 10.7554/eLife.07314 25875391

80. Sekine Y, Zyryanova A, Crespillo-Casado A, Fischer PM, Harding HP, Ron D. Stress responses. Mutations in a translation initiation factor identify the target of a memory-enhancing compound. Science. United States; 2015;348: 1027–1030. doi: 10.1126/science.aaa6986 25858979

81. Cross BCS, Bond PJ, Sadowski PG, Jha BK, Zak J, Goodman JM, et al. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci U S A. United States; 2012;109: E869–78. doi: 10.1073/pnas.1115623109 22315414

82. Myoung J, Ganem D. Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: maintenance of tight latency with efficient reactivation upon induction. J Virol Methods. Netherlands; 2011;174: 12–21. doi: 10.1016/j.jviromet.2011.03.012 21419799

83. Nishimura K, Ueda K, Sakakibara S, Do E, Ohsaki E, Okuno T, et al. A viral transcriptional activator of Kaposi’s sarcoma-associated herpesvirus (KSHV) induces apoptosis, which is blocked in KSHV-infected cells. Virology. United States; 2003;316: 64–74. doi: 10.1016/s0042-6822(03)00582-8 14599791

84. Vieira J, O’Hearn PM. Use of the red fluorescent protein as a marker of Kaposi’s sarcoma-associated herpesvirus lytic gene expression. Virology. United States; 2004;325: 225–240. doi: 10.1016/j.virol.2004.03.049 15246263

85. Zhang J, He S, Wang Y, Brulois K, Lan K, Jung JU, et al. Herpesviral G protein-coupled receptors activate NFAT to induce tumor formation via inhibiting the SERCA calcium ATPase. PLoS Pathog. United States; 2015;11: e1004768. doi: 10.1371/journal.ppat.1004768 25811856

86. Kaser A, Lee A-H, Franke A, Glickman JN, Zeissig S, Tilg H, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. United States; 2008;134: 743–756. doi: 10.1016/j.cell.2008.07.021 18775308

87. Nakatani Y, Kaneto H, Kawamori D, Yoshiuchi K, Hatazaki M, Matsuoka T, et al. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem. United States; 2005;280: 847–851. doi: 10.1074/jbc.M411860200 15509553

88. Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol. United States; 2012;197: 857–867. doi: 10.1083/jcb.201110131 22733998

89. Smith JA, Turner MJ, DeLay ML, Klenk EI, Sowders DP, Colbert RA. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur J Immunol. Germany; 2008;38: 1194–1203. doi: 10.1002/eji.200737882 18412159

90. Talloczy Z, Virgin HW 4th, Levine B. PKR-dependent autophagic degradation of herpes simplex virus type 1. Autophagy. United States; 2006;2: 24–29. doi: 10.4161/auto.2176 16874088

91. Taylor GS, Mautner J, Munz C. Autophagy in herpesvirus immune control and immune escape. Herpesviridae. England; 2011;2: 2. doi: 10.1186/2042-4280-2-2 21429245

92. Yamaguchi H, Wang H-G. CHOP is involved in endoplasmic reticulum stress-induced apoptosis by enhancing DR5 expression in human carcinoma cells. J Biol Chem. United States; 2004;279: 45495–45502. doi: 10.1074/jbc.M406933200 15322075

93. Houck SA, Ren HY, Madden VJ, Bonner JN, Conlin MP, Janovick JA, et al. Quality control autophagy degrades soluble ERAD-resistant conformers of the misfolded membrane protein GnRHR. Mol Cell. United States; 2014;54: 166–179. doi: 10.1016/j.molcel.2014.02.025 24685158

94. Kroeger H, Miranda E, MacLeod I, Perez J, Crowther DC, Marciniak SJ, et al. Endoplasmic reticulum-associated degradation (ERAD) and autophagy cooperate to degrade polymerogenic mutant serpins. J Biol Chem. United States; 2009;284: 22793–22802. doi: 10.1074/jbc.M109.027102 19549782

95. Lee J-S, Li Q, Lee J-Y, Lee S-H, Jeong JH, Lee H-R, et al. FLIP-mediated autophagy regulation in cell death control. Nat Cell Biol. England; 2009;11: 1355–1362. doi: 10.1038/ncb1980 19838173

96. Liang Q, Chang B, Brulois KF, Castro K, Min C-K, Rodgers MA, et al. Kaposi’s sarcoma-associated herpesvirus K7 modulates Rubicon-mediated inhibition of autophagosome maturation. J Virol. United States; 2013;87: 12499–12503. doi: 10.1128/JVI.01898-13 24027317

97. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. United States; 2005;122: 927–939. doi: 10.1016/j.cell.2005.07.002 16179260

98. Tomlinson CC, Damania B. The K1 protein of Kaposi’s sarcoma-associated herpesvirus activates the Akt signaling pathway. J Virol. United States; 2004;78: 1918–1927. doi: 10.1128/JVI.78.4.1918-1927.2004 14747556

99. Montaner S, Sodhi A, Pece S, Mesri EA, Gutkind JS. The Kaposi’s sarcoma-associated herpesvirus G protein-coupled receptor promotes endothelial cell survival through the activation of Akt/protein kinase B. Cancer Res. United States; 2001;61: 2641–2648. 11289142

100. Zhang P, Su C, Jiang Z, Zheng C. Herpes Simplex Virus 1 UL41 Protein Suppresses the IRE1/XBP1 Signal Pathway of the Unfolded Protein Response via Its RNase Activity. J Virol. United States; 2017;91. doi: 10.1128/JVI.02056-16 27928013

101. Papandreou I, Denko NC, Olson M, Van Melckebeke H, Lust S, Tam A, et al. Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma. Blood. United States; 2011;117: 1311–1314. doi: 10.1182/blood-2010-08-303099 21081713

102. Su A, Wang H, Li Y, Wang X, Chen D, Wu Z. Opposite Roles of RNase and Kinase Activities of Inositol-Requiring Enzyme 1 (IRE1) on HSV-1 Replication. Viruses. Switzerland; 2017;9. doi: 10.3390/v9090235 28832521

103. Xuan B, Qian Z, Torigoi E, Yu D. Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J Virol. United States; 2009;83: 3463–3474. doi: 10.1128/JVI.02307-08 19193809

104. Stahl S, Burkhart JM, Hinte F, Tirosh B, Mohr H, Zahedi RP, et al. Cytomegalovirus downregulates IRE1 to repress the unfolded protein response. PLoS Pathog. United States; 2013;9: e1003544. doi: 10.1371/journal.ppat.1003544 23950715

105. Jheng J-R, Ho J-Y, Horng J-T. ER stress, autophagy, and RNA viruses. Front Microbiol. Frontiers Media SA; 2014;5: 388. doi: 10.3389/fmicb.2014.00388 25140166

106. Tam AB, Koong AC, Niwa M. Ire1 has distinct catalytic mechanisms for XBP1/HAC1 splicing and RIDD. Cell Rep. Elsevier; 2014;9: 850–8. doi: 10.1016/j.celrep.2014.09.016 25437541

107. Livak KJ, Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods. Academic Press; 2001;25: 402–408. doi: 10.1006/meth.2001.1262 11846609

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
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

#ADS_BOTTOM_SCRIPTS#