Analysis of the role of autophagy inhibition by two complementary human cytomegalovirus BECN1/Beclin 1-binding proteins

Autophagy

Volumn 12, Issue 2, 2016, Pages 327-342

  Mouna, Lina ^a   Hernandez, Eva ^a   Bonte, Dorine ^b   Brost, Rebekka ^c   Amazit, Larbi ^d   Delgui, Laura R ^e   Brune, Wolfram ^c   Geballe, Adam P ^f   Beau, Isabelle ^d   Esclatine, Audrey ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b Gustave Roussy Comprehensive Cancer Institute   (France)

^c LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^d Bicêtre Paris Saclay Hospital   (France)

^e Instituto de Histologia y Embriologia   (Argentina)

^f UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Autophagy; BECN1; Cytomegalovirus; EIF2AK2 PKR; IRS1; TRS1

Indexed keywords

PROTEIN IRS1; PROTEIN TRS1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; BECLIN 1; BECN1 PROTEIN, HUMAN; EIF2AK2 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN KINASE R; TRS1 PROTEIN, HUMAN HERPESVIRUS 5; VIRAL PROTEIN;

ARTICLE; AUTOPHAGY; CELL CYCLE; CYTOMEGALOVIRUS INFECTION; HUMAN CYTOMEGALOVIRUS; NONHUMAN; VIRUS MUTANT; VIRUS RECOMBINANT; VIRUS REPLICATION; CHEMISTRY; CYTOMEGALOVIRUS; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELA CELL LINE; HUMAN; MALE; METABOLISM; MUTATION; PROTEIN DOMAIN;

AUTOPHAGY; BECLIN-1; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; EIF-2 KINASE; HELA CELLS; HUMANS; MALE; MUTATION; PROTEIN BINDING; PROTEIN DOMAINS; RECOMBINATION, GENETIC; VIRAL PROTEINS;

EID: 84964528121     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1125071     Document Type: Article

References (57)

1. Richetta C, Faure M. Autophagy in antiviral innate immunity. Cell Microbiol 2013; 15:368-76 ; PMID:23051682; http://dx.doi.org/10.1111/cmi.12043
2. Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013; 13:722-37 ; PMID:24064518; http://dx.doi.org/10.1038/nri3532
3. Deretic V. Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr Opin Immunol 2012; 24:21-31 ; PMID:22118953; http://dx.doi.org/10.1016/j.coi.2011.10.006
4. Richetta C, Gregoire IP, Verlhac P, Azocar O, Baguet J, Flacher M, Tangy F, Rabourdin-Combe C, Faure M. Sustained autophagy contributes to measles virus infectivity. PLoS Pathog 2013; 9:e1003599 ; PMID:24086130; http://dx.doi.org/10.1371/journal.ppat.1003599
5. Bird SW, Maynard ND, Covert MW, Kirkegaard K. Nonlytic viral spread enhanced by autophagy components. Proc Natl Acad Sci U S A 2014; 111:13081-6 ; PMID:25157142; http://dx.doi.org/10.1073/pnas.1401437111
6. Fliss PM, Jowers TP, Brinkmann MM, Holstermann B, Mack C, Dickinson P, Hohenberg H, Ghazal P, Brune W. Viral mediated redirection of NEMO/IKKgamma to autophagosomes curtails the inflammatory cascade. PLoS Pathog 2012; 8:e1002517 ; PMID:22319449; http://dx.doi.org/10.1371/journal.ppat.1002517
7. Tey SK, Khanna R. Autophagy mediates transporter associated with antigen processing-independent presentation of viral epitopes through MHC class I pathway. Blood 2012; 120:994-1004 ; PMID:22723550; http://dx.doi.org/10.1182/blood-2012-01-402404
8. Chaumorcel M, Lussignol M, Mouna L, Cavignac Y, Fahie K, Cotte-Laffitte J, Geballe A, Brune W, Beau I, Codogno P, et al. The human cytomegalovirus protein TRS1 inhibits autophagy via its interaction with Beclin 1. J Virol 2012; 86:2571-84 ; PMID:22205736; http://dx. doi.org/10.1128/JVI.05746-11
9. McFarlane S, Aitken J, Sutherland JS, Nicholl MJ, Preston VG, Preston CM. Early induction of autophagy in human fibroblasts after infection with human cytomegalovirus or herpes simplex virus 1. J Virol 2011; 85:4212-21 ; PMID:21325419; http://dx.doi.org/10.1128/JVI.02435-10
10. Cepeda V, Esteban M, Fraile-Ramos A. Human cytomegalovirus final envelopment on membranes containing both trans-Golgi network and endosomal markers. Cell Microbiol 2010; 12:386-404 ; PMID:19888988; http://dx.doi.org/10.1111/j.1462-5822.2009.01405.x
11. Stern-Ginossar N, Weisburd B, Michalski A, Le VT, Hein MY, Huang SX, Ma M, Shen B, Qian SB, Hengel H, et al. Decoding human cytomegalovirus. Science 2012; 338:1088-93 ; PMID:23180859; http://dx. doi.org/10.1126/science.1227919
12. Romanowski MJ, Shenk T. Characterization of the human cytomegalovirus irs1 and trs1 genes: a second immediate-early transcription unit within irs1 whose product antagonizes transcriptional activation. J Virol 1997; 71:1485-96 ; PMID:8995674
13. Child SJ, Hakki M, De Niro KL, Geballe AP. Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J Virol 2004; 78:197-205 ; PMID:14671101; http://dx.doi.org/10.1128/JVI.78.1.197-205.2004
14. Marshall EE, Bierle CJ, Brune W, Geballe AP. Essential role for either TRS1 or IRS1 in human cytomegalovirus replication. J Virol 2009; 83:4112-20 ; PMID:19211736; http://dx.doi.org/10.1128/JVI.02489-08
15. Hakki M, Geballe AP. Double-stranded RNA binding by human cytomegalovirus pTRS1. J Virol 2005; 79:7311-8 ; PMID:15919885; http://dx.doi.org/10.1128/JVI.79.12.7311-7318.2005
16. Hakki M, Marshall EE, De Niro KL, Geballe AP. Binding and nuclear relocalization of protein kinase R by human cytomegalovirus TRS1. J Virol 2006; 80:11817-26 ; PMID:16987971; http://dx.doi.org/10.1128/JVI.00957-06
17. Bierle CJ, Semmens KM, Geballe AP. Double-stranded RNA binding by the human cytomegalovirus PKR antagonist TRS1. Virology 2013; 442:28-37 ; PMID:23601785; http://dx.doi.org/10.1016/j.virol.2013. 03.024
18. Talloczy Z, Jiang W, Virgin HWt, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B. Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci U S A 2002; 99:190-5 ; PMID:11756670; http://dx.doi.org/10.1073/pnas.012485299
19. Orvedahl A, Alexander D, Talloczy Z, Sun Q, Wei Y, Zhang W, Burns D, Leib DA, Levine B. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 2007; 1:23-35 ; PMID:18005679; http://dx.doi.org/10.1016/j.chom.2006.12.001
20. Lussignol M, Queval C, Bernet-Camard MF, Cotte-Laffitte J, Beau I, Codogno P, Esclatine A. The herpes simplex virus 1 Us11 protein inhibits autophagy through its interaction with the protein kinase PKR. J Virol 2013; 87:859-71 ; PMID:23115300; http://dx.doi.org/10.1128/JVI.01158-12
21. Levine B, Liu R, Dong X, Zhong Q. Beclin orthologs: integrative hubs of cell signaling, membrane trafficking, and physiology. Trends Cell Biol 2015; 25(9):533-44 ; PMID:26071895
22. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39 ; PMID:16179260; http://dx.doi.org/10.1016/j.cell.2005.07.002
23. Chaumorcel M, Souquere S, Pierron G, Codogno P, Esclatine A. Human cytomegalovirus controls a new autophagy-dependent cellular antiviral defense mechanism. Autophagy 2008; 4:46-53 ; PMID:18340111; http://dx.doi.org/10.4161/auto.5184
24. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544 ; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
25. Marshall EE, Geballe AP. Multifaceted evasion of the interferon response by cytomegalovirus. J Interferon Cytokine Res 2009; 29:609-19; http://dx.doi.org/10.1089/jir.2009.0064
26. Terhune S, Torigoi E, Moorman N, Silva M, Qian Z, Shenk T, Yu D. Human cytomegalovirus UL38 protein blocks apoptosis. J Virol 2007; 81:3109-23 ; PMID:17202209; http://dx.doi.org/10.1128/JVI.02124-06
27. Cheng J, Ohsaki Y, Tauchi-Sato K, Fujita A, Fujimoto T. Cholesterol depletion induces autophagy. Biochem Biophys Res Commu 2006; 351:246-52 ; PMID:17056010; http://dx.doi.org/10.1016/j.bbrc.2006. 10.042
28. Liu J, Xia H, Kim M, Xu L, Li Y, Zhang L, Cai Y, Norberg HV, Zhang T, Furuya T, et al. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell 2011; 147:223-34 ; PMID:21962518; http://dx.doi.org/10.1016/j.cell.2011.08.037
29. McKnight NC, Jefferies HB, Alemu EA, Saunders RE, Howell M, Johansen T, Tooze SA. Genome-wide siRNA screen reveals amino acid starvation-induced autophagy requires SCOC and WAC. EMBO J 2012; 31:1931-46 ; PMID:22354037; http://dx.doi.org/10.1038/emboj.2012.36
30. Smith RM, Kosuri S, Kerry JA. Role of human cytomegalovirus tegument proteins in virion assembly. Viruses 2014; 6:582-605 ; PMID:24509811; http://dx.doi.org/10.3390/v6020582
31. Romanowski MJ, Garrido-Guerrero E, Shenk T. pIRS1 and pTRS1 are present in human cytomegalovirus virions. J Virol 1997; 71:5703-5 ; PMID:9188653
32. Blankenship CA, Shenk T. Mutant human cytomegalovirus lacking the immediate-early TRS1 coding region exhibits a late defect. J Virol 2002; 76:12290-9 ; PMID:12414969; http://dx.doi.org/10.1128/JVI.76.23.12290-12299.2002
33. Adamo JE, Schroer J, Shenk T. Human cytomegalovirus TRS1 protein is required for efficient assembly of DNA-containing capsids. J Virol 2004; 78:10221-9 ; PMID:15367587; http://dx.doi.org/10.1128/JVI.78. 19.10221-10229.2004
34. Stasiak PC, Mocarski ES. Transactivation of the cytomegalovirus ICP36 gene promoter requires the a gene product TRS1 in addition to IE1 and IE2. J Virol 1992; 66:1050-8 ; PMID:1370547
35. Strang BL, Geballe AP, Coen DM. Association of human cytomegalovirus proteins IRS1 and TRS1 with the viral DNA polymerase accessory subunit UL44. J Gen Virol 2010; 91:2167-75 ; PMID:20444996; http://dx.doi.org/10.1099/vir.0.022640-0
36. Ziehr B, Lenarcic E, Vincent HA, Cecil C, Garcia B, Shenk T, Moorman NJ. Human cytomegalovirus TRS1 protein associates with the 7-methylguanosine mRNA cap and facilitates translation. Proteomics 2015; 15:1983-94 ; PMID:25894605; http://dx.doi.org/10.1002/pmic.201400616
37. Piya S, White EJ, Klein SR, Jiang H, McDonnell TJ, Gomez-Manzano C, Fueyo J. The E1B19K oncoprotein complexes with Beclin 1 to regulate autophagy in adenovirus-infected cells. PloS One 2011; 6:e29467 ; PMID:22242123; http://dx.doi.org/10.1371/journal. pone.0029467
38. Kyei GB, Dinkins C, Davis AS, Roberts E, Singh SB, Dong C, Wu L, Kominami E, Ueno T, Yamamoto A, et al. Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 2009; 186:255-68 ; PMID:19635843; http://dx.doi.org/10.1083/jcb.200903070
39. Gannage M, Dormann D, Albrecht R, Dengjel J, Torossi T, Ramer PC, Lee M, Strowig T, Arrey F, Conenello G, et al. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 2009; 6:367-80 ; PMID:19837376; http://dx.doi.org/10.1016/j.chom.2009.09.005
40. Gobeil PA, Leib DA. Herpes simplex virus gamma34.5 interferes with autophagosome maturation and antigen presentation in dendritic cells. MBio 2012; 3:e00267-12 ; PMID:23073763; http://dx.doi.org/10.1128/mBio.00267-12
41. Matsunaga K, Saitoh T, Tabata K, Omori H, Satoh T, Kurotori N, Maejima I, Shirahama-Noda K, Ichimura T, Isobe T, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11:385-96 ; PMID:19270696; http://dx.doi.org/10.1038/ncb1846
42. Joubert PE, Werneke SW, de la Calle C, Guivel-Benhassine F, Giodini A, Peduto L, Levine B, Schwartz O, Lenschow DJ, Albert ML. Chikungunya virus-induced autophagy delays caspase-dependent cell death. J Exp Med 2012; 209:1029-47 ; PMID:22508836; http://dx.doi.org/10.1084/jem.20110996
43. Nowag H, Guhl B, Thriene K, Romao S, Ziegler U, Dengjel J, Münz C. Macroautophagy Proteins Assist Epstein Barr Virus Production and Get Incorporated Into the Virus Particles. EBioMedicine 2014; 1:116-25 ; PMID:26137519; http://dx.doi.org/10.1016/j.ebiom.2014.11.007
44. Buckingham EM, Carpenter JE, Jackson W, Grose C. Autophagy and the effects of its inhibition on varicella-zoster virus glycoprotein biosynthesis and infectivity. J Virol 2014; 88:890-902 ; PMID:24198400; http://dx.doi.org/10.1128/JVI.02646-13
45. Bouley SJ, Maginnis MS, Derdowski A, Gee GV, O’Hara BA, Nelson CD, Bara AM, Atwood WJ, Dugan AS. Host cell autophagy promotes BK virus infection. Virology 2014; 456-457:87-95 ; PMID:24889228
46. Li J, Liu Y, Wang Z, Liu K, Wang Y, Liu J, Ding H, Yuan Z. Subversion of cellular autophagy machinery by hepatitis B virus for viral envelopment. J Virol 2011; 85:6319-33 ; PMID:21507968; http://dx.doi.org/10.1128/JVI.02627-10
47. Rodriguez-Rocha H, Gomez-Gutierrez JG, Garcia-Garcia A, Rao XM, Chen L, McMasters KM, Zhou HS. Adenoviruses induce autophagy to promote virus replication and oncolysis. Virology 2011; 416:9-15 ; PMID:21575980; http://dx.doi.org/10.1016/j.virol.2011.04.017
48. Rubinsztein DC, Codogno P, Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012; 11:709-30 ; PMID:22935804; http://dx.doi.org/10.1038/nrd3802
49. Sehgal AR, Konig H, Johnson DE, Tang D, Amaravadi RK, Boyiadzis M, Lotze MT. You eat what you are: autophagy inhibition as a therapeutic strategy in leukemia. Leukemia 2015; 562:40-9.
50. Bampton ET, Goemans CG, Niranjan D, Mizushima N, Tolkovsky AM. The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 2005; 1:23-36 ; PMID:16874023; http://dx.doi.org/10.4161/auto.1.1. 1495
51. Esclatine A, Bellon A, Michelson S, Servin AL, Quero AM, Geniteau-Legendre M. Differentiation-dependent redistribution of heparan sulfate in epithelial intestinal Caco-2 cells leads to basolateral entry of cytomegalovirus. Virology 2001; 289:23-33 ; PMID:11601914; http://dx.doi.org/10.1006/viro.2001.1122
52. Hobom U, Brune W, Messerle M, Hahn G, Koszinowski UH. Fast screening procedures for random transposon libraries of cloned herpesvirus genomes: mutational analysis of human cytomegalovirus envelope glycoprotein genes. J Virol 2000; 74:7720-9 ; PMID:10933677; http://dx.doi.org/10.1128/JVI.74.17.7720-7729.2000
53. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, Court DL, Jenkins NA, Copeland NG. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 2001; 73:56-65 ; PMID:11352566; http://dx.doi.org/10.1006/geno. 2000.6451
54. Kimura S, Fujita N, Noda T, Yoshimori T. Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 2009; 452:1-12 ; PMID:19200872; http://dx.doi.org/10.1016/S0076-6879(08)03601-X
55. Verpooten D, Ma Y, Hou S, Yan Z, He B. Control of TANK-binding kinase 1-mediated signaling by the gamma(1)34.5 protein of herpes simplex virus 1. J Biol Chem 2009; 284:1097-105 ; PMID:19010780; http://dx.doi.org/10.1074/jbc.M805905200
56. Child SJ, Brennan G, Braggin JE, Geballe AP. Species specificity of protein kinase r antagonism by cytomegalovirus TRS1 genes. J Virol 2012; 86:3880-9 ; PMID:22278235; http://dx.doi.org/10.1128/JVI. 06158-11
57. Leruez-Ville M, Ouachee M, Delarue R, Sauget AS, Blanche S, Buzyn A, Rouzioux C. Monitoring cytomegalovirus infection in adult and pediatric bone marrow transplant recipients by a realtime PCR assay performed with blood plasma. J Clin Microbiol 2003; 41:2040-6 ; PMID:12734246; http://dx.doi.org/10.1128/JCM. 41.5.2040-2046.2003