Histone Deacetylase 8 Is Required for Centrosome Cohesion and Influenza A Virus Entry
Influenza A virus (IAV) enters host cells by endocytosis followed by acid-activated penetration from late endosomes (LEs). Using siRNA silencing, we found that histone deacetylase 8 (HDAC8), a cytoplasmic enzyme, efficiently promoted productive entry of IAV into tissue culture cells, whereas HDAC1 suppressed it. HDAC8 enhanced endocytosis, acidification, and penetration of the incoming virus. In contrast, HDAC1 inhibited acidification and penetration. The effects were connected with dramatic alterations in the organization of the microtubule system, and, as a consequence, a change in the behavior of LEs and lysosomes (LYs). Depletion of HDAC8 caused loss of centrosome-associated microtubules and loss of directed centripetal movement of LEs, dispersing LE/LYs to the cell periphery. For HDAC1, the picture was the opposite. To explain these changes, centrosome cohesion emerged as the critical factor. Depletion of HDAC8 caused centrosome splitting, which could also be induced by depleting a centriole-linker protein, rootletin. In both cases, IAV infection was inhibited. HDAC1 depletion reduced the splitting of centrosomes, and enhanced infection. The longer the distance between centrosomes, the lower the level of infection. HDAC8 depletion was also found to inhibit infection of Uukuniemi virus (a bunyavirus) suggesting common requirements among late penetrating enveloped viruses. The results established class I HDACs as powerful regulators of microtubule organization, centrosome function, endosome maturation, and infection by IAV and other late penetrating viruses.
Vyšlo v časopise:
Histone Deacetylase 8 Is Required for Centrosome Cohesion and Influenza A Virus Entry. PLoS Pathog 7(10): e32767. doi:10.1371/journal.ppat.1002316
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002316
Souhrn
Influenza A virus (IAV) enters host cells by endocytosis followed by acid-activated penetration from late endosomes (LEs). Using siRNA silencing, we found that histone deacetylase 8 (HDAC8), a cytoplasmic enzyme, efficiently promoted productive entry of IAV into tissue culture cells, whereas HDAC1 suppressed it. HDAC8 enhanced endocytosis, acidification, and penetration of the incoming virus. In contrast, HDAC1 inhibited acidification and penetration. The effects were connected with dramatic alterations in the organization of the microtubule system, and, as a consequence, a change in the behavior of LEs and lysosomes (LYs). Depletion of HDAC8 caused loss of centrosome-associated microtubules and loss of directed centripetal movement of LEs, dispersing LE/LYs to the cell periphery. For HDAC1, the picture was the opposite. To explain these changes, centrosome cohesion emerged as the critical factor. Depletion of HDAC8 caused centrosome splitting, which could also be induced by depleting a centriole-linker protein, rootletin. In both cases, IAV infection was inhibited. HDAC1 depletion reduced the splitting of centrosomes, and enhanced infection. The longer the distance between centrosomes, the lower the level of infection. HDAC8 depletion was also found to inhibit infection of Uukuniemi virus (a bunyavirus) suggesting common requirements among late penetrating enveloped viruses. The results established class I HDACs as powerful regulators of microtubule organization, centrosome function, endosome maturation, and infection by IAV and other late penetrating viruses.
Zdroje
1. StertzSShawML 2011 Uncovering the global host cell requirements for influenza virus replication via RNAi screening. Microbes Infect 13 516 525
2. WatanabeTWatanabeSKawaokaY 2010 Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 7 427 439
3. TaubenbergerJKKashJC 2010 Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7 440 451
4. MatlinKSReggioHHeleniusASimonsK 1981 Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91 601 613
5. De ContoFCovanSArcangelettiMCOrlandiniGGattiR 2011 Differential infectious entry of human influenza A/NWS/33 virus (H1N1) in mammalian kidney cells. Virus Res 155 221 230
6. RustMJLakadamyaliMZhangFZhuangX 2004 Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 11 567 573
7. de VriesETscherneDMWienholtsMJCobos-JimenezVScholteF 2011 Dissection of the influenza a virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS Pathog 7 e1001329
8. SkehelJJWileyDC 2000 Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69 531 569
9. WhiteJKartenbeckJHeleniusA 1982 Membrane fusion activity of influenza virus. EMBO J 1 217 222
10. LakadamyaliMRustMJBabcockHPZhuangX 2003 Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100 9280 9285
11. BouloSAkarsuHRuigrokRWBaudinF 2007 Nuclear traffic of influenza virus proteins and ribonucleoprotein complexes. Virus Res 124 12 21
12. MartinKHeleniusA 1991 Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67 117 130
13. DoxseySMcCollumDTheurkaufW 2005 Centrosomes in cellular regulation. Annu Rev Cell Dev Biol 21 411 434
14. SluderGNordbergJJ 2004 The good, the bad and the ugly: the practical consequences of centrosome amplification. Curr Opin Cell Biol 16 49 54
15. YangXJSetoE 2003 Collaborative spirit of histone deacetylases in regulating chromatin structure and gene expression. Curr Opin Genet Dev 13 143 153
16. LeeKKWorkmanJL 2007 Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 8 284 295
17. ChoudharyCKumarCGnadFNielsenMLRehmanM 2009 Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325 834 840
18. de RuijterAJvan GennipAHCaronHNKempSvan KuilenburgAB 2003 Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370 737 749
19. EngelSHegerTManciniRHerzogFKartenbeckJ 2011 Role of endosomes in simian virus 40 entry and infection. J Virol 85 4198 4211
20. MaciaEEhrlichMMassolRBoucrotEBrunnerC 2006 Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10 839 850
21. HeleniusAKartenbeckJSimonsKFriesE 1980 On the entry of Semliki forest virus into BHK-21 cells. J Cell Biol 84 404 420
22. MuFTCallaghanJMSteele-MortimerOStenmarkHPartonRG 1995 EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine “fingers” and contains a calmodulin-binding IQ motif. J Biol Chem 270 13503 13511
23. SchroerTA 2004 Dynactin. Annu Rev Cell Dev Biol 20 759 779
24. HirokawaNNodaYTanakaYNiwaS 2009 Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10 682 696
25. KlausnerRD 1989 Sorting and traffic in the central vacuolar system. Cell 57 703 706
26. Dautry-VarsatACiechanoverALodishHF 1983 pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci U S A 80 2258 2262
27. MellmanI 1996 Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12 575 625
28. RhodesCHStieberAGonatasNK 1986 A quantitative electron microscopic study of the intracellular localization of wheat germ agglutinin in retinal neurons. J Comp Neurol 254 287 296
29. HelmuthJABurckhardtCJKoumoutsakosPGreberUFSbalzariniIF 2007 A novel supervised trajectory segmentation algorithm identifies distinct types of human adenovirus motion in host cells. J Struct Biol 159 347 358
30. SbalzariniIFKoumoutsakosP 2005 Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151 182 195
31. PipernoGLeDizetMChangXJ 1987 Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J Cell Biol 104 289 302
32. HubbertCGuardiolaAShaoRKawaguchiYItoA 2002 HDAC6 is a microtubule-associated deacetylase. Nature 417 455 458
33. DelgehyrNSillibourneJBornensM 2005 Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J Cell Sci 118 1565 1575
34. BaheSStierhofYDWilkinsonCJLeissFNiggEA 2005 Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J Cell Biol 171 27 33
35. KhanNJeffersMKumarSHackettCBoldogF 2008 Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 409 581 589
36. MercerJSchelhaasMHeleniusA 2010 Virus entry by endocytosis. Annu Rev Biochem 79 803 833
37. JohannsdottirHKManciniRKartenbeckJAmatoLHeleniusA 2009 Host cell factors and functions involved in vesicular stomatitis virus entry. J Virol 83 440 453
38. WhiteJMatlinKHeleniusA 1981 Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses. J Cell Biol 89 674 679
39. LozachPYManciniRBittoDMeierROestereichL 2010 Entry of bunyaviruses into mammalian cells. Cell Host Microbe 7 488 499
40. MercerJHeleniusA 2008 Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320 531 535
41. LozachPYHuotariJHeleniusA 2011 The Late-penetrating Viruses. Curr Opin Microbiol in press
42. SieczkarskiSBWhittakerGR 2003 Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4 333 343
43. WhittakerGRDigardP 2006 Entry and intracellular transport of influenza virus. KawaokaY Influenza virology: current topics Wymondham (United Kingdom) Caister Academic Press 37 64
44. HaberlandMMokalledMHMontgomeryRLOlsonEN 2009 Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev 23 1625 1630
45. VanniniAVolpariCFilocamoGCasavolaECBrunettiM 2004 Crystal structure of a eukaryotic zinc-dependent histone deacetylase, human HDAC8, complexed with a hydroxamic acid inhibitor. Proc Natl Acad Sci U S A 101 15064 15069
46. WaltregnyDGlenissonWTranSLNorthBJVerdinE 2005 Histone deacetylase HDAC8 associates with smooth muscle alpha-actin and is essential for smooth muscle cell contractility. FASEB J 19 966 968
47. LeeHSenguptaNVillagraARezai-ZadehNSetoE 2006 Histone deacetylase 8 safeguards the human ever-shorter telomeres 1B (hEST1B) protein from ubiquitin-mediated degradation. Mol Cell Biol 26 5259 5269
48. WoodmanPGFutterCE 2008 Multivesicular bodies: co-ordinated progression to maturity. Curr Opin Cell Biol 20 408 414
49. PiperRCKatzmannDJ 2007 Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23 519 547
50. HuotariJHeleniusA 2011 Endosome Maturation. EMBO J 30 3481 3500
51. CollinetCStoterMBradshawCRSamusikNRinkJC 2010 Systems survey of endocytosis by multiparametric image analysis. Nature 464 243 249
52. MeraldiPNiggEA 2001 Centrosome cohesion is regulated by a balance of kinase and phosphatase activities. J Cell Sci 114 3749 3757
53. PielMMeyerPKhodjakovARiederCLBornensM 2000 The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J Cell Biol 149 317 330
54. FryAMMayorTMeraldiPStierhofYDTanakaK 1998 C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J Cell Biol 141 1563 1574
55. PetterssonRKaariainenL 1973 The ribonucleic acids of Uukuniemi virus, a noncubical tick-borne arbovirus. Virology 56 608 619
56. PetersonJRHeleniusA 1999 In vitro reconstitution of calreticulin-substrate interactions. J Cell Sci 112 Pt 16 2775 2784
57. DanielsPSJeffriesSYatesPSchildGCRogersGN 1987 The receptor-binding and membrane-fusion properties of influenza virus variants selected using anti-haemagglutinin monoclonal antibodies. EMBO J 6 1459 1465
58. WebsterRGBrownLEJacksonDC 1983 Changes in the antigenicity of the hemagglutinin molecule of H3 influenza virus at acidic pH. Virology 126 587 599
59. SakaiTOhuchiMImaiMMizunoTKawasakiK 2006 Dual wavelength imaging allows analysis of membrane fusion of influenza virus inside cells. J Virol 80 2013 2018
60. CarpenterAEJonesTRLamprechtMRClarkeCKangIH 2006 CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7 R100
61. PfafflMW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29 e45
62. SaydamNGeorgievONakanoMYGreberUFSchaffnerW 2001 Nucleo-cytoplasmic trafficking of metal-regulatory transcription factor 1 is regulated by diverse stress signals. J Biol Chem 276 25487 25495
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 10
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Severe Acute Respiratory Syndrome Coronavirus Envelope Protein Regulates Cell Stress Response and Apoptosis
- The SARS-Coronavirus-Host Interactome: Identification of Cyclophilins as Target for Pan-Coronavirus Inhibitors
- Biochemical and Structural Insights into the Mechanisms of SARS Coronavirus RNA Ribose 2′-O-Methylation by nsp16/nsp10 Protein Complex
- Evolutionarily Divergent, Unstable Filamentous Actin Is Essential for Gliding Motility in Apicomplexan Parasites