The Dual Role of an ESCRT-0 Component HGS in HBV Transcription and Naked Capsid Secretion

PLoS Pathogens

Volumn 11, Issue 10, 2015, Pages

  Chou, Shu Fan ^a,b   Tsai, Ming Lin ^b   Huang, Jyun Yuan ^b,c   Chang, Ya Shu ^b   Shih, Chiaho ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ESCRT 0 PROTEIN; ESCRT I PROTEIN; ESCRT II PROTEIN; ESCRT III PROTEIN; ESCRT PROTEIN; SINGLE STRANDED DNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; HEPATOCYTE GROWTH FACTOR-REGULATED TYROSINE KINASE SUBSTRATE; PHOSPHOPROTEIN;

AGAR GEL ELECTROPHORESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE EXPRESSION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NORTHERN BLOTTING; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SOUTHERN BLOTTING; VIRUS CAPSID; VIRUS EXPRESSION; VIRUS REPLICATION; VIRUS TRANSCRIPTION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HEPATITIS B; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; RAT; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; CAPSID; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; FLUORESCENT ANTIBODY TECHNIQUE; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; RATS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; TRANSFECTION; VIRUS REPLICATION;

EID: 84946054824     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005123     Document Type: Article

References (89)

1. Ganem D, Prince AM, (2004) Hepatitis B virus infection—natural history and clinical consequences. N Engl J Med 350: 1118–1129. 15014185
2. Ringelhan M, O'Connor T, Protzer U, Heikenwalder M, (2015) The direct and indirect roles of HBV in liver cancer: prospective markers for HCC screening and potential therapeutic targets. J Pathol 235: 355–367. doi: 10.1002/path.4434 25196558
3. Thomas E, Yoneda M, Schiff ER, (2015) Viral Hepatitis: Past and Future of HBV and HDV. Cold Spring Harb Perspect Med 5.
4. Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH, (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vps mutants. Mol Biol Cell 3: 1389–1402. 1493335
5. Hanson PI, Cashikar A, (2012) Multivesicular body morphogenesis. Annu Rev Cell Dev Biol 28: 337–362. doi: 10.1146/annurev-cellbio-092910-154152 22831642
6. Katzmann DJ, Babst M, Emr SD, (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106: 145–155. 11511343
7. Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD, (2002) Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3: 283–289. 12194858
8. Bache KG, Brech A, Mehlum A, Stenmark H, (2003) Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes. J Cell Biol 162: 435–442. 12900395
9. Wollert T, Hurley JH, (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464: 864–869. doi: 10.1038/nature08849 20305637
10. Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD, (2002) Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3: 271–282. 12194857
11. Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH, (2009) Membrane scission by the ESCRT-III complex. Nature 458: 172–177. doi: 10.1038/nature07836 19234443
12. Lata S, Schoehn G, Jain A, Pires R, Piehler J, et al. (2008) Helical structures of ESCRT-III are disassembled by VPS4. Science 321: 1354–1357. doi: 10.1126/science.1161070 18687924
13. Votteler J, Sundquist Wesley I, (2013) Virus Budding and the ESCRT Pathway. Cell Host & Microbe 14: 232–241.
14. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, et al. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107: 55–65. 11595185
15. Morita E, Sandrin V, McCullough J, Katsuyama A, Baci Hamilton I, et al. (2011) ESCRT-III protein requirements for HIV-1 budding. Cell Host Microbe 9: 235–242. doi: 10.1016/j.chom.2011.02.004 21396898
16. Kian Chua P, Lin MH, Shih C, (2006) Potent inhibition of human Hepatitis B virus replication by a host factor Vps4. Virology 354: 1–6. 16920176
17. Watanabe T, Sorensen EM, Naito A, Schott M, Kim S, et al. (2007) Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc Natl Acad Sci U S A 104: 10205–10210. 17551004
18. Lambert C, Doring T, Prange R, (2007) Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol 81: 9050–9060. 17553870
19. Stieler JT, Prange R, (2014) Involvement of ESCRT-II in hepatitis B virus morphogenesis. PLoS One 9: e91279. doi: 10.1371/journal.pone.0091279 24614091
20. Tuttleman JS, Pourcel C, Summers J, (1986) Formation of the pool of covalently closed circular viral DNA in hepadnavirus-infected cells. Cell 47: 451–460. 3768961
21. Shih C, (2012) Chronic Hepatitis B and C. World Scientific Publishing Co Pte Ltd.
22. Gerin JL, Ford EC, Purcell RH, (1975) Biochemical characterization of Australia antigen. Evidence for defective particles of hepatitis B virus. Am J Pathol 81: 651–668. 1211425
23. Kaplan PM, Ford EC, Purcell RH, Gerin JL, (1976) Demonstration of subpopulations of Dane particles. J Virol 17: 885–893. 1255863
24. Sakamoto Y, Yamada G, Mizuno M, Nishihara T, Kinoyama S, et al. (1983) Full and empty particles of hepatitis B virus in hepatocytes from patients with HBsAg-positive chronic active hepatitis. Lab Invest 48: 678–682. 6855194
25. Schormann W, Kraft A, Ponsel D, Bruss V, (2006) Hepatitis B virus particle formation in the absence of pregenomic RNA and reverse transcriptase. J Virol 80: 4187–4190. 16571836
26. Ning X, Nguyen D, Mentzer L, Adams C, Lee H, et al. (2011) Secretion of genome-free hepatitis B virus—single strand blocking model for virion morphogenesis of para-retrovirus. PLoS Pathog 7: e1002255. doi: 10.1371/journal.ppat.1002255 21966269
27. Luckenbaugh L, Kitrinos KM, Delaney WEt, Hu J, (2015) Genome-free hepatitis B virion levels in patient sera as a potential marker to monitor response to antiviral therapy. J Viral Hepat 22: 561–570. doi: 10.1111/jvh.12361 25395045
28. Huovila AP, Eder AM, Fuller SD, (1992) Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment. J Cell Biol 118: 1305–1320. 1522109
29. Patient R, Hourioux C, Sizaret PY, Trassard S, Sureau C, et al. (2007) Hepatitis B virus subviral envelope particle morphogenesis and intracellular trafficking. J Virol 81: 3842–3851. 17267490
30. Doring T, Prange R, (2014) Rab33B and its autophagic Atg5/12/16L1 effector assist in hepatitis B virus naked capsid formation and release. Cell Microbiol.
31. Bardens A, Doring T, Stieler J, Prange R, (2011) Alix regulates egress of hepatitis B virus naked capsid particles in an ESCRT-independent manner. Cell Microbiol 13: 602–619. doi: 10.1111/j.1462-5822.2010.01557.x 21129143
32. Ghoujal B, Milev MP, Ajamian L, Abel K, Mouland AJ, (2012) ESCRT-II's involvement in HIV-1 genomic RNA trafficking and assembly. Biol Cell 104: 706–721. doi: 10.1111/boc.201200021 22978549
33. Mizuno E, Kawahata K, Kato M, Kitamura N, Komada M, (2003) STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol Biol Cell 14: 3675–3689. 12972556
34. Kobayashi H, Tanaka N, Asao H, Miura S, Kyuuma M, et al. (2005) Hrs, a mammalian master molecule in vesicular transport and protein sorting, suppresses the degradation of ESCRT proteins signal transducing adaptor molecule 1 and 2. J Biol Chem 280: 10468–10477. 15640163
35. Nassal M, (1992) The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive-strand DNA synthesis but not for virus assembly. J Virol 66: 4107–4116. 1602535
36. Le Pogam S, Chua PK, Newman M, Shih C, (2005) Exposure of RNA templates and encapsidation of spliced viral RNA are influenced by the arginine-rich domain of human hepatitis B virus core antigen (HBcAg 165–173). J Virol 79: 1871–1887. 15650211
37. Ning B, Shih C, (2004) Nucleolar localization of human hepatitis B virus capsid protein. J Virol 78: 13653–13668. 15564475
38. Arzberger S, Hosel M, Protzer U, (2010) Apoptosis of hepatitis B virus-infected hepatocytes prevents release of infectious virus. J Virol 84: 11994–12001. doi: 10.1128/JVI.00653-10 20719950
39. Shih CH, Li LS, Roychoudhury S, Ho MH, (1989) In vitro propagation of human hepatitis B virus in a rat hepatoma cell line. Proc Natl Acad Sci U S A 86: 6323–6327. 2762328
40. Shih C, Yu MY, Li LS, Shih JW, (1990) Hepatitis B virus propagated in a rat hepatoma cell line is infectious in a primate model. Virology 179: 871–873. 2238476
41. Roychoudhury S, Faruqi AF, Shih C, (1991) Pregenomic RNA encapsidation analysis of eleven missense and nonsense polymerase mutants of human hepatitis B virus. J Virol 65: 3617–3624. 1710285
42. Lanford RE, Notvall L, Lee H, Beames B, (1997) Transcomplementation of nucleotide priming and reverse transcription between independently expressed TP and RT domains of the hepatitis B virus reverse transcriptase. J Virol 71: 2996–3004. 9060659
43. Newman M, Chua PK, Tang FM, Su PY, Shih C, (2009) Testing an electrostatic interaction hypothesis of hepatitis B virus capsid stability by using an in vitro capsid disassembly/reassembly system. J Virol 83: 10616–10626. doi: 10.1128/JVI.00749-09 19656897
44. Chu TH, Liou AT, Su PY, Wu HN, Shih C, (2014) Nucleic acid chaperone activity associated with the arginine-rich domain of human hepatitis B virus core protein. J Virol 88: 2530–2543. doi: 10.1128/JVI.03235-13 24352445
45. Li HC, Huang EY, Su PY, Wu SY, Yang CC, et al. (2010) Nuclear export and import of human hepatitis B virus capsid protein and particles. PLoS Pathog 6: e1001162. doi: 10.1371/journal.ppat.1001162 21060813
46. Chua PK, Tang FM, Huang JY, Suen CS, Shih C, (2010) Testing the balanced electrostatic interaction hypothesis of hepatitis B virus DNA synthesis by using an in vivo charge rebalance approach. J Virol 84: 2340–2351. doi: 10.1128/JVI.01666-09 20015989
47. Hirano S, Kawasaki M, Ura H, Kato R, Raiborg C, et al. (2006) Double-sided ubiquitin binding of Hrs-UIM in endosomal protein sorting. Nat Struct Mol Biol 13: 272–277. 16462748
48. Bishop N, Horman A, Woodman P, (2002) Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J Cell Biol 157: 91–101. 11916981
49. Hasdemir B, Bunnett NW, Cottrell GS, (2007) Hepatocyte growth factor-regulated tyrosine kinase substrate (HRS) mediates post-endocytic trafficking of protease-activated receptor 2 and calcitonin receptor-like receptor. J Biol Chem 282: 29646–29657. 17675298
50. Raiborg C, Bremnes B, Mehlum A, Gillooly DJ, D'Arrigo A, et al. (2001) FYVE and coiled-coil domains determine the specific localisation of Hrs to early endosomes. J Cell Sci 114: 2255–2263. 11493665
51. Matusek T, Wendler F, Poles S, Pizette S, D'Angelo G, et al. (2014) The ESCRT machinery regulates the secretion and long-range activity of Hedgehog. Nature 516: 99–103. doi: 10.1038/nature13847 25471885
52. Baron M, (2012) Endocytic routes to Notch activation. Semin Cell Dev Biol 23: 437–442. doi: 10.1016/j.semcdb.2012.01.008 22285298
53. Lund VK, Delotto R, (2011) Regulation of Toll and Toll-like receptor signaling by the endocytic pathway. Small GTPases 2: 95–98. 21776409
54. Chanut-Delalande H, Jung AC, Baer MM, Lin L, Payre F, et al. (2010) The Hrs/Stam complex acts as a positive and negative regulator of RTK signaling during Drosophila development. PLoS One 5: e10245. doi: 10.1371/journal.pone.0010245 20422006
55. Haag J, Chubinskaya S, Aigner T, (2006) Hgs physically interacts with Smad5 and attenuates BMP signaling. Exp Cell Res 312: 1153–1163. 16516194
56. Gaur NA, Hasek J, Brickner DG, Qiu H, Zhang F, et al. (2013) Vps factors are required for efficient transcription elongation in budding yeast. Genetics 193: 829–851. doi: 10.1534/genetics.112.146308 23335340
57. Irion U, St Johnston D, (2007) bicoid RNA localization requires specific binding of an endosomal sorting complex. Nature 445: 554–558. 17268469
58. Snyder JC, Samson RY, Brumfield SK, Bell SD, Young MJ, (2013) Functional interplay between a virus and the ESCRT machinery in archaea. Proc Natl Acad Sci U S A 110: 10783–10787. doi: 10.1073/pnas.1301605110 23754419
59. Richardson LG, Clendening EA, Sheen H, Gidda SK, White KA, et al. (2014) A unique N-terminal sequence in the Carnation Italian ringspot virus p36 replicase-associated protein interacts with the host cell ESCRT-I component Vps23. J Virol 88: 6329–6344. doi: 10.1128/JVI.03840-13 24672030
60. Barajas D, Martin IF, Pogany J, Risco C, Nagy PD, (2014) Noncanonical role for the host Vps4 AAA+ ATPase ESCRT protein in the formation of Tomato bushy stunt virus replicase. PLoS Pathog 10: e1004087. doi: 10.1371/journal.ppat.1004087 24763736
61. Rusten TE, Stenmark H, (2009) How do ESCRT proteins control autophagy? J Cell Sci 122: 2179–2183. doi: 10.1242/jcs.050021 19535733
62. Sir D, Tian Y, Chen WL, Ann DK, Yen TS, et al. (2010) The early autophagic pathway is activated by hepatitis B virus and required for viral DNA replication. Proc Natl Acad Sci U S A 107: 4383–4388. doi: 10.1073/pnas.0911373107 20142477
63. Tian Y, Sir D, Kuo CF, Ann DK, Ou JH, (2011) Autophagy required for hepatitis B virus replication in transgenic mice. J Virol 85: 13453–13456. doi: 10.1128/JVI.06064-11 21957292
64. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG, (2003) AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114: 689–699. 14505569
65. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, et al. (2003) The protein network of HIV budding. Cell 114: 701–713. 14505570
66. Bouamr F, Houck-Loomis BR, De Los Santos M, Casaday RJ, Johnson MC, et al. (2007) The C-terminal portion of the Hrs protein interacts with Tsg101 and interferes with human immunodeficiency virus type 1 Gag particle production. J Virol 81: 2909–2922. 17182674
67. Takahashi H, Mayers JR, Wang L, Edwardson JM, Audhya A, (2015) Hrs and STAM function synergistically to bind ubiquitin-modified cargoes in vitro. Biophys J 108: 76–84. doi: 10.1016/j.bpj.2014.11.004 25564854
68. Urbe S, Sachse M, Row PE, Preisinger C, Barr FA, et al. (2003) The UIM domain of Hrs couples receptor sorting to vesicle formation. J Cell Sci 116: 4169–4179. 12953068
69. Amano Y, Yamashita Y, Kojima K, Yoshino K, Tanaka N, et al. (2011) Hrs recognizes a hydrophobic amino acid cluster in cytokine receptors during ubiquitin-independent endosomal sorting. J Biol Chem 286: 15458–15472. doi: 10.1074/jbc.M110.191924 21362618
70. Yamashita Y, Kojima K, Tsukahara T, Agawa H, Yamada K, et al. (2008) Ubiquitin-independent binding of Hrs mediates endosomal sorting of the interleukin-2 receptor beta-chain. J Cell Sci 121: 1727–1738. doi: 10.1242/jcs.024455 18445679
71. Mayers JR, Wang L, Pramanik J, Johnson A, Sarkeshik A, et al. (2013) Regulation of ubiquitin-dependent cargo sorting by multiple endocytic adaptors at the plasma membrane. Proc Natl Acad Sci U S A 110: 11857–11862. doi: 10.1073/pnas.1302918110 23818590
72. Tamai K, Tanaka N, Nakano T, Kakazu E, Kondo Y, et al. (2010) Exosome secretion of dendritic cells is regulated by Hrs, an ESCRT-0 protein. Biochem Biophys Res Commun 399: 384–390. doi: 10.1016/j.bbrc.2010.07.083 20673754
73. Tamai K, Shiina M, Tanaka N, Nakano T, Yamamoto A, et al. (2012) Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway. Virology 422: 377–385. doi: 10.1016/j.virol.2011.11.009 22138215
74. Cocucci E, Meldolesi J, (2015) Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol.
75. Wehman AM, Poggioli C, Schweinsberg P, Grant BD, Nance J, (2011) The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Curr Biol 21: 1951–1959. doi: 10.1016/j.cub.2011.10.040 22100064
76. Yuan TT, Sahu GK, Whitehead WE, Greenberg R, Shih C, (1999) The mechanism of an immature secretion phenotype of a highly frequent naturally occurring missense mutation at codon 97 of human hepatitis B virus core antigen. J Virol 73: 5731–5740. 10364324
77. Mabit H, Schaller H, (2000) Intracellular hepadnavirus nucleocapsids are selected for secretion by envelope protein-independent membrane binding. J Virol 74: 11472–11478. 11090143
78. Tuttleman JS, Pugh JC, Summers JW, (1986) In vitro experimental infection of primary duck hepatocyte cultures with duck hepatitis B virus. J Virol 58: 17–25. 3512855
79. Milich DR, McLachlan A, (1986) The nucleocapsid of hepatitis B virus is both a T-cell-independent and a T-cell-dependent antigen. Science 234: 1398–1401. 3491425
80. Milich DR, Chen M, Schodel F, Peterson DL, Jones JE, et al. (1997) Role of B cells in antigen presentation of the hepatitis B core. Proc Natl Acad Sci U S A 94: 14648–14653. 9405667
81. Yang PL, Althage A, Chung J, Chisari FV, (2002) Hydrodynamic injection of viral DNA: a mouse model of acute hepatitis B virus infection. Proc Natl Acad Sci U S A 99: 13825–13830. 12374864
82. Summers J, Mason WS, (1982) Replication of the genome of a hepatitis B—like virus by reverse transcription of an RNA intermediate. Cell 29: 403–415. 6180831
83. Yuan TT, Tai PC, Shih C, (1999) Subtype-independent immature secretion and subtype-dependent replication deficiency of a highly frequent, naturally occurring mutation of human hepatitis B virus core antigen. J Virol 73: 10122–10128. 10559327
84. Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, et al. (2003) HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 162: 425–434. 12900394
85. Janvier K, Pelchen-Matthews A, Renaud JB, Caillet M, Marsh M, et al. (2011) The ESCRT-0 component HRS is required for HIV-1 Vpu-mediated BST-2/tetherin down-regulation. PLoS Pathog 7: e1001265. doi: 10.1371/journal.ppat.1001265 21304933
86. Lv M, Zhang B, Shi Y, Han Z, Zhang Y, et al. (2015) Identification of BST-2/tetherin-induced hepatitis B virus restriction and hepatocyte-specific BST-2 inactivation. Sci Rep 5: 11736. doi: 10.1038/srep11736 26119070
87. Yan R, Zhao X, Cai D, Liu Y, Block T, et al. (2015) Interferon-inducible Protein Tetherin Inhibits Hepatitis B Virus Virion Secretion. J Virol.
88. Aden DP, Fogel A, Plotkin S, Damjanov I, Knowles BB, (1979) Controlled synthesis of HBsAg in a differentiated human liver carcinoma-derived cell line. Nature 282: 615–616. 233137
89. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J, (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858–3863. 6286115