Assembly and remodeling of viral DNA and RNA replicons regulated by cellular molecular chaperones

Biophysical Reviews volume 10, pages445–452(2018)Cite this article

Abstract

A variety of cellular reactions mediated by interactions among proteins and nucleic acids requires a series of proteins called molecular chaperones. The viral genome encodes relatively few kinds of viral proteins and, therefore, host-derived cellular factors are required for virus proliferation. Here we discuss those cellular proteins known as molecular chaperones, which are essential for the assembly of functional viral DNA/RNA replicons. The function of these molecular chaperones in the cellular context is also discussed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Arranz R, Coloma R, Chichon FJ, Conesa JJ, Carrascosa JL, Valpuesta JM, Ortin J, Martin-Benito J (2012) The structure of native influenza virion ribonucleoproteins. Science 338:1634–1637

    CAS  Article  PubMed  Google Scholar 

  2. Asaka MN, Murano K, Nagata K (2008) Sp1-mediated transcription regulation of TAF-Ialpha gene encoding a histone chaperone. Biochem Biophys Res Commun 376:665–670

    CAS  Article  PubMed  Google Scholar 

  3. Bačíková D, Horowitz DS (2005) Genetic and functional interaction of evolutionarily conserved regions of the Prp18 protein and the U5 snRNA. Mol Cell Biol 25:2107–2116

    Article  PubMed  PubMed Central  Google Scholar 

  4. Beresford PJ, Zhang D, Oh DY, Fan Z, Greer EL, Russo ML, Jaju M, Lieberman J (2001) Granzyme a activates an endoplasmic reticulum-associated caspase-independent nuclease to induce single-stranded DNA nicks. J Biol Chem 276:43285–43293

    CAS  Article  PubMed  Google Scholar 

  5. Borer RA, Lehner CF, Eppenberger HM, Nigg EA (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56:379–390

    CAS  Article  PubMed  Google Scholar 

  6. Brennan CM, Gallouzi IE, Steitz JA (2000) Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J Cell Biol 151:1–14

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Canela N, Rodriguez-Vilarrupla A, Estanyol JM, Diaz C, Pujol MJ, Agell N, Bachs O (2003) The SET protein regulates G2/M transition by modulating cyclin B-cyclin-dependent kinase 1 activity. J Biol Chem 278:1158–1164

    CAS  Article  PubMed  Google Scholar 

  8. Chae YC, Kim KB, Kang JY, Kim SR, Jung HS, Seo SB (2014) Inhibition of FoxO1 acetylation by INHAT subunit SET/TAF-Ibeta induces p21 transcription. FEBS Lett 588:2867–2873

    CAS  Article  PubMed  Google Scholar 

  9. Chatterjee PK, Vayda ME, Flint SJ (1986) Adenoviral protein VII packages intracellular viral DNA throughout the early phase of infection. EMBO J 5:1633–1644

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Ellis J (1987) Proteins as molecular chaperones. Nature 328:378–379

    CAS  Article  PubMed  Google Scholar 

  11. Enomoto T, Lichy JH, Ikeda JE, Hurwitz J (1981) Adenovirus DNA replication in vitro: purification of the terminal protein in a functional form. Proc Natl Acad Sci USA 78:6779–6783

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Fleckner J, Zhang M, Valcarcel J, Green MR (1997) U2AF65 recruits a novel human DEAD box protein required for the U2 snRNP-branchpoint interaction. Genes Dev 11:1864–1872

    CAS  Article  PubMed  Google Scholar 

  13. Fong YW, Zhou Q (2001) Stimulatory effect of splicing factors on transcriptional elongation. Nature 414:929–933

    CAS  Article  PubMed  Google Scholar 

  14. Gadad SS, Senapati P, Syed SH et al (2011) The multifunctional protein nucleophosmin (NPM1) is a human linker histone H1 chaperone. Biochemistry 50:2780–2789

    CAS  Article  PubMed  Google Scholar 

  15. Giberson AN, Davidson AR, Parks RJ (2012) Chromatin structure of adenovirus DNA throughout infection. Nucleic Acids Res 40:2369–2376

    CAS  Article  PubMed  Google Scholar 

  16. Goding CR, Russell WC (1983) Adenovirus cores can function as templates in in vitro DNA replication. EMBO J 2:339–344

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Grisendi S, Mecucci C, Falini B, Pandolfi PP (2006) Nucleophosmin and cancer. Nat Rev Cancer 6:493–505

    CAS  Article  PubMed  Google Scholar 

  18. Gyurcsik B, Haruki H, Takahashi T, Mihara H, Nagata K (2006) Binding modes of the precursor of adenovirus major core protein VII to DNA and template activating factor I: implication for the mechanism of remodeling of the adenovirus chromatin. Biochemistry 45:303–313

    CAS  Article  PubMed  Google Scholar 

  19. Haruki H, Gyurcsik B, Okuwaki M, Nagata K (2003) Ternary complex formation between DNA-adenovirus core protein VII and TAF-Ibeta/SET, an acidic molecular chaperone. FEBS Lett 555:521–527

    CAS  Article  PubMed  Google Scholar 

  20. Haruki H, Okuwaki M, Miyagishi M, Taira K, Nagata K (2006) Involvement of template-activating factor I/SET in transcription of adenovirus early genes as a positive-acting factor. J Virol 80:794–801

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Honda A, Ueda K, Nagata K, Ishihama A (1988) RNA polymerase of influenza virus: role of NP in RNA chain elongation. J Biochem (Tokyo) 104:1021–1026

    CAS  Article  Google Scholar 

  22. Hu Y, Gor V, Morikawa K, Nagata K, Kawaguchi A (2017) Cellular splicing factor UAP56 stimulates trimeric NP formation for assembly of functional influenza viral ribonucleoprotein complexes. Sci Rep 7:14053

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ikeda JE, Enomoto T, Hurwitz J (1981) Replication of adenovirus DNA-protein complex with purified proteins. Proc Natl Acad Sci USA 78:884–888

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Ishimi Y, Hirosumi J, Sato W, Sugasawa K, Yokota S, Hanaoka F, Yamada M (1984) Purification and initial characterization of a protein which facilitates assembly of nucleosome-like structure from mammalian cells. Eur J Biochem 142:431–439

    CAS  Article  PubMed  Google Scholar 

  25. Ishimi Y, Kojima M, Yamada M, Hanaoka F (1987) Binding mode of nucleosome-assembly protein (AP-I) and histones. Eur J Biochem 162:19–24

    CAS  Article  PubMed  Google Scholar 

  26. Ito T, Ikehara T, Nakagawa T, Kraus WL, Muramatsu M (2000) p300-mediated acetylation facilitates the transfer of histone H2A-H2B dimers from nucleosomes to a histone chaperone. Genes Dev 14:1899–1907

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Kajitani K, Kato K, Nagata K (2017) Histone H1 chaperone activity of TAF-I is regulated by its subtype-dependent intramolecular interaction. Genes Cells 22:334–347

    CAS  Article  PubMed  Google Scholar 

  28. Kalousi A, Hoffbeck AS, Selemenakis PN, Pinder J, Savage KI, Khanna KK, Brino L, Dellaire G, Gorgoulis VG, Soutoglou E (2015) The nuclear oncogene SET controls DNA repair by KAP1 and HP1 retention to chromatin. Cell Rep 11:149–163

    CAS  Article  PubMed  Google Scholar 

  29. Kato K, Okuwaki M, Nagata K (2011) Role of template activating factor-I as a chaperone in linker histone dynamics. J Cell Sci 124:3254–3265

    CAS  Article  PubMed  Google Scholar 

  30. Kawaguchi A, Nagata K (2007) De novo replication of the influenza virus RNA genome is regulated by DNA replicative helicase, MCM. EMBO J 26:4566–4575

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Kawaguchi A, Momose F, Nagata K (2011) Replication-coupled and host factor-mediated encapsidation of the influenza virus genome by viral nucleoprotein. J Virol 85:6197–6204

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Kawase H, Okuwaki M, Miyaji M, Ohba R, Handa H, Ishimi Y, Fujii-Nakata T, Kikuchi A, Nagata K (1996) NAP-I is a functional homologue of TAF-I that is required for replication and transcription of the adenovirus genome in a chromatin-like structure. Genes Cells 1:1045–1056

    CAS  Article  PubMed  Google Scholar 

  33. Kim JY, Lee KS, Seol JE, Yu K, Chakravarti D, Seo SB (2012) Inhibition of p53 acetylation by INHAT subunit SET/TAF-Ibeta represses p53 activity. Nucleic Acids Res 40:75–87

    CAS  Article  PubMed  Google Scholar 

  34. Komatsu T, Haruki H, Nagata K (2011) Cellular and viral chromatin proteins are positive factors in the regulation of adenovirus gene expression. Nucleic Acids Res 39:889–901

    CAS  Article  PubMed  Google Scholar 

  35. Komatsu T, Dacheux D, Kreppel F, Nagata K, Wodrich H (2015) A method for visualization of incoming adenovirus chromatin complexes in fixed and living cells. PLoS One 10:e0137102

    Article  PubMed  PubMed Central  Google Scholar 

  36. Laskey RA, Honda BM, Mills AD, Finch JT (1978) Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275:416–420

    CAS  Article  PubMed  Google Scholar 

  37. Leith IR, Hay RT, Russell WC (1989) Adenovirus subviral particles and cores can support limited DNA replication. J Gen Virol 70(Pt 12):3235–3248

    CAS  Article  PubMed  Google Scholar 

  38. Linder P, Stutz F (2001) mRNA export: travelling with DEAD box proteins. Curr Biol 11:R961–R963

    CAS  Article  PubMed  Google Scholar 

  39. Long JS, Giotis ES, Moncorge O et al (2016) Species difference in ANP32A underlies influenza a virus polymerase host restriction. Nature 529:101–104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Luo MJ, Zhou Z, Magni K, Christoforides C, Rappsilber J, Mann M, Reed R (2001) Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly. Nature 413:644–647

    CAS  Article  PubMed  Google Scholar 

  41. Mansouri S, Wang S, Frappier L (2013) A role for the nucleosome assembly proteins TAF-Ibeta and NAP1 in the activation of BZLF1 expression and Epstein-Barr virus reactivation. PLoS One 8:e63802

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Matsumoto K, Nagata K, Ui M, Hanaoka F (1993) Template activating factor I, a novel host factor required to stimulate the adenovirus core DNA replication. J Biol Chem 268:10582–10587

    CAS  PubMed  Google Scholar 

  43. McQuibban GA, Commisso-Cappelli CN, Lewis PN (1998) Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1. J Biol Chem 273:6582–6590

    CAS  Article  PubMed  Google Scholar 

  44. Minakuchi M, Sugiyama K, Kato Y, Naito T, Okuwaki M, Kawaguchi A & Nagata K (2017) Pre-mRNA processing factor Prp18 is a stimulatory factor of influenza virus RNA synthesis and possesses nucleoprotein chaperone activity. J Virol 91(3). doi: 10.1128/JVI.01398-16

  45. Miyaji-Yamaguchi M, Okuwaki M, Nagata K (1999) Coiled-coil structure-mediated dimerization of template activating factor-I is critical for its chromatin remodeling activity. J Mol Biol 290:547–557

    CAS  Article  PubMed  Google Scholar 

  46. Moeller A, Kirchdoerfer RN, Potter CS, Carragher B, Wilson IA (2012) Organization of the influenza virus replication machinery. Science 338:1631–1634

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Momose F, Handa H, Nagata K (1996) Identification of host factors that regulate the influenza virus RNA polymerase activity. Biochimie 78:1103–1108

    CAS  Article  PubMed  Google Scholar 

  48. Momose F, Basler CF, O'Neill RE, Iwamatsu A, Palese P, Nagata K (2001) Cellular splicing factor RAF-2p48/NPI-5/BAT1/UAP56 interacts with the influenza virus nucleoprotein and enhances viral RNA synthesis. J Virol 75:1899–1908

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Momose F, Naito T, Yano K, Sugimoto S, Morikawa Y, Nagata K (2002) Identification of Hsp90 as a stimulatory host factor involved in influenza virus RNA synthesis. J Biol Chem 277:45306–45314

    CAS  Article  PubMed  Google Scholar 

  50. Murano K, Okuwaki M, Hisaoka M, Nagata K (2008) Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol Cell Biol 28:3114–3126

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Nagata K, Guggenheimer RA, Enomoto T, Lichy JH, Hurwitz J (1982) Adenovirus DNA replication in vitro: identification of a host factor that stimulates synthesis of the preterminal protein-dCMP complex. Proc Natl Acad Sci USA 79:6438–6442

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Nagata K, Guggenheimer RA, Hurwitz J (1983) Adenovirus DNA replication in vitro: synthesis of full-length DNA with purified proteins. Proc Natl Acad Sci USA 80:4266–4270

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Nagata K, Kawase H, Handa H, Yano K, Yamasaki M, Ishimi Y, Okuda A, Kikuchi A, Matsumoto K (1995) Replication factor encoded by a putative oncogene, set, associated with myeloid leukemogenesis. Proc Natl Acad Sci USA 92:4279–4283

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Nagata K, Saito S, Okuwaki M, Kawase H, Furuya A, Kusano A, Hanai N, Okuda A, Kikuchi A (1998) Cellular localization and expression of template-activating factor I in different cell types. Exp Cell Res 240:274–281

    CAS  Article  PubMed  Google Scholar 

  55. Naito T, Kiyasu Y, Sugiyama K, Kimura A, Nakano R, Matsukage A, Nagata K (2007) An influenza virus replicon system in yeast identified tat-SF1 as a stimulatory host factor for viral RNA synthesis. Proc Natl Acad Sci USA 104:18235–18240

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Ng AK-L, Zhang H, Tan K, Li Z, J-h L, Chan PK-S, Li S-M, Chan W-Y, Au SW-N, Joachimiak A (2008) Structure of the influenza virus a H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J 22:3638–3647

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Ohtomo H, Akashi S, Moriwaki Y, Okuwaki M, Osakabe A, Nagata K, Kurumizaka H, Nishimura Y (2016) C-terminal acidic domain of histone chaperone human NAP1 is an efficient binding assistant for histone H2A-H2B, but not H3-H4. Genes Cells 21:252–263

    CAS  Article  PubMed  Google Scholar 

  58. Okuda M, Horn HF, Tarapore P et al (2000) Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 103:127–140

    CAS  Article  PubMed  Google Scholar 

  59. Okuwaki M, Nagata K (1998) Template activating factor I remodels the chromatin structure and stimulates transcription from the chromatin template. J Biol Chem 273:34511–34518

    CAS  Article  PubMed  Google Scholar 

  60. Okuwaki M, Iwamatsu A, Tsujimoto M, Nagata K (2001a) Identification of nucleophosmin/B23, an acidic nucleolar protein, as a stimulatory factor for in vitro replication of adenovirus DNA complexed with viral basic core proteins. J Mol Biol 311:41–55

    CAS  Article  PubMed  Google Scholar 

  61. Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K (2001b) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276

    CAS  Article  PubMed  Google Scholar 

  62. Okuwaki M, Kato K, Shimahara H, Tate S, Nagata K (2005) Assembly and disassembly of nucleosome core particles containing histone variants by human nucleosome assembly protein I. Mol Cell Biol 25:10639–10651

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Okuwaki M, Kato K, Nagata K (2010) Functional characterization of human nucleosome assembly protein 1-like proteins as histone chaperones. Genes Cells 15:13–27

    CAS  Article  PubMed  Google Scholar 

  64. Okuwaki M, Sumi A, Hisaoka M, Saotome-Nakamura A, Akashi S, Nishimura Y, Nagata K (2012) Function of homo- and hetero-oligomers of human nucleoplasmin/nucleophosmin family proteins NPM1, NPM2 and NPM3 during sperm chromatin remodeling. Nucleic Acids Res 40:4861–4878

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Okuwaki M, Abe M, Hisaoka M, Nagata K (2016) Regulation of cellular dynamics and chromosomal binding site preference of linker histones H1.0 and H1.X. Mol Cell Biol 36:2681–2696

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Pegoraro G, Marcello A, Myers MP, Giacca M (2006) Regulation of adeno-associated virus DNA replication by the cellular TAF-I/set complex. J Virol 80:6855–6864

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Portela A, Digard P (2002) The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol 83:723–734

    CAS  Article  PubMed  Google Scholar 

  68. Pruijn GJ, van Driel W, van der Vliet PC (1986) Nuclear factor III, a novel sequence-specific DNA-binding protein from HeLa cells stimulating adenovirus DNA replication. Nature 322:656–659

    CAS  Article  PubMed  Google Scholar 

  69. Puntener D, Engelke MF, Ruzsics Z, Strunze S, Wilhelm C, Greber UF (2011) Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J Virol 85:481–496

    CAS  Article  PubMed  Google Scholar 

  70. Ruigrok RW, Baudin F (1995) Structure of influenza virus ribonucleoprotein particles. II Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. J Gen Virol 76(Pt 4):1009–1014

    CAS  Article  PubMed  Google Scholar 

  71. Russell WC (2009) Adenoviruses: update on structure and function. J Gen Virol 90:1–20

    CAS  Article  PubMed  Google Scholar 

  72. Saddoughi SA, Gencer S, Peterson YK et al (2013) Sphingosine analogue drug FTY720 targets I2PP2A/SET and mediates lung tumour suppression via activation of PP2A-RIPK1-dependent necroptosis. EMBO Mol Med 5:105–121

    CAS  Article  PubMed  Google Scholar 

  73. Samad MA, Okuwaki M, Haruki H, Nagata K (2007) Physical and functional interaction between a nucleolar protein nucleophosmin/B23 and adenovirus basic core proteins. FEBS Lett 581:3283–3288

    CAS  Article  PubMed  Google Scholar 

  74. Samad MA, Komatsu T, Okuwaki M, Nagata K (2012) B23/nucleophosmin is involved in regulation of adenovirus chromatin structure at late infection stages, but not in virus replication and transcription. J Gen Virol 93:1328–1338

    CAS  Article  PubMed  Google Scholar 

  75. Seo SB, McNamara P, Heo S, Turner A, Lane WS, Chakravarti D (2001) Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 104:119–130

    CAS  Article  PubMed  Google Scholar 

  76. Shimizu K, Handa H, Nakada S, Nagata K (1994) Regulation of influenza virus RNA polymerase activity by cellular and viral factors. Nucleic Acids Res 22:5047–5053

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. Shintomi K, Iwabuchi M, Saeki H, Ura K, Kishimoto T, Ohsumi K (2005) Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs. Proc Natl Acad Sci USA 102:8210–8215

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. Sugase K, Dyson HJ, Wright PE (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447:1021–1025

    CAS  Article  PubMed  Google Scholar 

  79. Sugiyama K, Kawaguchi A, Okuwaki M & Nagata K (2015) pp32 and APRIL are host cell-derived regulators of influenza virus RNA synthesis from cRNA. eLife 4. doi: 10.7554/eLife.08939

  80. Switzer CH, Cheng RY, Vitek TM, Christensen DJ, Wink DA, Vitek MP (2011) Targeting SET/I(2)PP2A oncoprotein functions as a multi-pathway strategy for cancer therapy. Oncogene 30:2504–2513

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  81. Tarus B, Bakowiez O, Chenavas S, Duchemin L, Estrozi L, Bourdieu C, Lejal N, Bernard J, Moudjou M, Chevalier C (2012) Oligomerization paths of the nucleoprotein of influenza a virus. Biochimie 94:776–785

    CAS  Article  PubMed  Google Scholar 

  82. ten Klooster JP, Leeuwen I, Scheres N, Anthony EC, Hordijk PL (2007) Rac1-induced cell migration requires membrane recruitment of the nuclear oncogene SET. EMBO J 26:336–345

    Article  PubMed  PubMed Central  Google Scholar 

  83. Ugai H, Borovjagin AV, Le LP, Wang M, Curiel DT (2007) Thermostability/infectivity defect caused by deletion of the core protein V gene in human adenovirus type 5 is rescued by thermo-selectable mutations in the core protein X precursor. J Mol Biol 366:1142–1160

    CAS  Article  PubMed  Google Scholar 

  84. van Leeuwen H, Okuwaki M, Hong R, Chakravarti D, Nagata K, O'Hare P (2003) Herpes simplex virus type 1 tegument protein VP22 interacts with TAF-I proteins and inhibits nucleosome assembly but not regulation of histone acetylation by INHAT. J Gen Virol 84:2501–2510

    Article  PubMed  Google Scholar 

  85. von Lindern M, van Baal S, Wiegant J, Raap A, Hagemeijer A, Grosveld G (1992) Can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3′ half to different genes: characterization of the set gene. Mol Cell Biol 12:3346–3355

    Article  Google Scholar 

  86. Warren C, Shechter D (2017) Fly fishing for histones: catch and release by histone chaperone intrinsically disordered regions and acidic stretches. J Mol Biol 429:2401–2426

    CAS  Article  PubMed  Google Scholar 

  87. Xue Y, Johnson JS, Ornelles DA, Lieberman J, Engel DA (2005) Adenovirus protein VII functions throughout early phase and interacts with cellular proteins SET and pp32. J Virol 79:2474–2483

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  88. Yamanaka K, Ishihama A, Nagata K (1990) Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. J Biol Chem 265:11151–11155

    CAS  PubMed  Google Scholar 

  89. Ye K (2005) Nucleophosmin/B23, a multifunctional protein that can regulate apoptosis. Cancer Biol Ther 4:918–923

    CAS  Article  PubMed  Google Scholar 

  90. Ye Q, Krug RM, Tao YJ (2006) The mechanism by which influenza a virus nucleoprotein forms oligomers and binds RNA. Nature 444:1078–1082

    CAS  Article  PubMed  Google Scholar 

  91. Ye Q, Guu TS, Mata DA, Kuo RL, Smith B, Krug RM, Tao YJ (2012) Biochemical and structural evidence in support of a coherent model for the formation of the double-helical influenza a virus ribonucleoprotein. MBio 4:e00467–e00412

    Article  PubMed  PubMed Central  Google Scholar 

  92. Zhou Q, Chen D, Pierstorff E, Luo K (1998) Transcription elongation factor p-TEFb mediates tat activation of HIV-1 transcription at multiple stages. EMBO J 17:3681–3691

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge all the collaborators who have contributed to our research projects. In particular, we thank Drs. Fumitaka Momose (Kitasato University) and Tadasuke Naito (Kawasaki Medical School) for their efforts.

Funding

The research work was supported in part by grants-in-aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan (16H05192 for AK and 24115002 for KN).

Author information

Affiliations

  1. Department of Infection Biology, Faculty of Medicine, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, 305-8575, Japan

    Takeshi Sekiya, Kohsuke Kato, Mitsuru Okuwaki & Atsushi Kawaguchi

  2. Graduate School of Comprehensive Human Sciences, University of Tsukuba, Tsukuba, Japan

    Yifan Hu, Kohsuke Kato, Mitsuru Okuwaki & Atsushi Kawaguchi

  3. Transborder Medical Research Center, University of Tsukuba, Tsukuba, Japan

    Atsushi Kawaguchi

  4. Special Laboratory, Department of Infection Biology, Faculty of Medicine, University of Tsukuba, Tsukuba, Japan

    Kyosuke Nagata

Authors
  1. Takeshi Sekiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yifan Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kohsuke Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mitsuru Okuwaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Atsushi Kawaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kyosuke Nagata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Atsushi Kawaguchi or Kyosuke Nagata.

Ethics declarations

Conflict of interest

Takeshi Sekiya declares that he has no conflicts of interest. Yifan Hu declares that he has no conflicts of interest. Kohsuke Kato declares that he has no conflicts of interest. Mitsuru Okuwaki declares that he has no conflicts of interest. Atsushi Kawaguchi declares that he has no conflicts of interest. Kyosuke Nagata declares that he has no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

This article is part of a Special Issue on ‘Biomolecules to Bio-nanomachines–Fumio Arisaka 70th Birthday’ edited by Damien Hall, Junichi Takagi and Haruki Nakamura.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sekiya, T., Hu, Y., Kato, K. et al. Assembly and remodeling of viral DNA and RNA replicons regulated by cellular molecular chaperones. Biophys Rev 10, 445–452 (2018). https://doi.org/10.1007/s12551-017-0333-z

Download citation

Keywords

  • Adenovirus
  • Chromatin
  • Influenza virus
  • Molecular chaperone
  • Ribonucleoprotein