Skip to main content

Nuclear Organization of Replication and Gene Expression in Adenovirus-Infected Cells

  • Chapter
The Molecular Repertoire of Adenoviruses I

Part of the book series: Current Topics in 199/I Microbiology and Immunology ((CT MICROBIOLOGY,volume 199/1))

Abstract

The eukaryotic cell nucleus performs a series of tasks including replication and packaging of DNA and transcription, splicing, polyadenylation, and transport of RNA. Productive infection of cells by viruses is the result of complex interactions between host and viral components that effectively subvert much of the host cell machinery for replication and gene expression of the virus. In a sense, the virus is able to reprogram the host cell, resulting in dramatic changes in host gene expression and allowing for the efficient production of viral particles. Biochemical and genetic analyses of adenovirus-infected cells have provided an enormous amount of information about the interaction of host and viral factors during the infectious program (see Doerfler 1986). Virus infection also alters structural and morphological characteristics of host nuclei (Martinez-Polomo and Granboulan 1967; Martinez-Polomo et al. 1967; Phillips and Raskas 1972; Vlak et al. 1975; Moyne et al. 1978). Adenovirus and herpesvirus replicate and accumulate DNA within distinct nuclear compartments, and host factors have also been shown to localize to these compartments (Walton et al. 1989; Wilcock and Lane 1991 ). Part of the viral reprogramming process is the formation of new virus-dependent nuclear structures and the alteration of existing nuclear structures. The role of the architecture and structural components of the nucleus in the replication and expression of both host and viral genomes is only beginning to be explored.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Adami G, Nevins JR (1988) Splice site selection dominates over poly(A) site choice in RNA production from complex adenovirus transcription units. EMBO J 7: 2107–2116

    CAS  PubMed  Google Scholar 

  • Babich A, Feldman LT, Nevins JR, Darnell JE Jr, Weinberger C (1983) Effect of adenovirus on metabolism of specific host mRNAs: transport control and specific translational discrimination. Mol Cell Biol 3: 1212–1221

    CAS  PubMed  Google Scholar 

  • Beltz GA, Flint SJ (1979) Inhibition of HeLa cell protein synthesis during adenovirus infection: restriction of cellular messenger RNA sequences to the nucleus. J Mol Biol 131: 353–373

    Article  CAS  PubMed  Google Scholar 

  • Beyer AL, Osheim YN (1988) Splice site selection, rate of splicing and alternative splicing on nascent transcripts. Genes Dev 2: 754–765

    Article  CAS  PubMed  Google Scholar 

  • Bosher J, Dawson A, Hay RT (1992) Nuclear factor I is specifically targeted to discrete subnuclear sites in adenovirus type 2-infected cells. J Virol 66: 3140–3150

    CAS  PubMed  Google Scholar 

  • Brasch K, Ochs RL (1992) Nuclear bodies (NBs): a newly “rediscovered” organelle. Exp Cell Res 202: 211–223

    Article  CAS  PubMed  Google Scholar 

  • Bridge E, Carmo-Fonseca M, Lamond AI, Pettersson U (1993) Nuclear organization of splicing small nuclear ribonucleoproteins in adenovirus-infected cells. J Virol 67: 5792–5802

    CAS  PubMed  Google Scholar 

  • Bridge E, Xia D-X, Carmo-Fonseca M, Cardinali B, Lamond AI, Pettersson U (1995) Dynamic organization of splicing factors in adenovirus-infected cells. J Virol 69: 281–290

    CAS  PubMed  Google Scholar 

  • Brison O, Kédinger C, Wilhelm J (1977) Enzymatic properties of viral replication complexes isolated from adenovirus type 2-infected HeLa cell nuclei. J Virol 24: 423–435

    CAS  PubMed  Google Scholar 

  • Brison O, Kédinger C, Chambon P (1979) Adenovirus DNA template for late transcription is not a replicative intermediate. J Virol 32: 91–97

    CAS  PubMed  Google Scholar 

  • Carmo-Fonseca M, Tollervey D, Pepperkok R, Barabino S, Merdes A, Brunner C, Zamore PD, Green MR, Hurt E, Lamond AI (1991 a) Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery. EMBO J 10: 195–206

    CAS  PubMed  Google Scholar 

  • Carmo-Fonseca M, Pepperkok R, Sproat BS, Ansorge W, Swanson MS, Lamond AI (1991b) In vivo detection of snRNP-organelles in the nuclei of mammalian cells. EMBO J 10: 1863–1873

    CAS  PubMed  Google Scholar 

  • Carmo-Fonseca M, Pepperkok R, Carvalho MT, Lamond AI (1992) Transcription dependent localization of the U1, U2, U4/U6 and U5 snRNPs in coiled bodies. J Cell Biol 117: 1–14

    Article  CAS  PubMed  Google Scholar 

  • Carmo-Fonseca M, Ferreira J, Lamond AI (1993) Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis-evidence that the coiled body is a kinetic nuclear structure. J Cell Boil 120: 841–852

    Article  CAS  Google Scholar 

  • Carter KC, Taneja KL, Lawrence JB (1991) Discrete nuclear domains of poly (A) RNA and their relationship to the functional organization of the nucleus. J Cell Biol 115: 1191–1202.

    Article  CAS  PubMed  Google Scholar 

  • Carter KC, Bowman D, Carrington W, Fogarty K, McNeil JA, Fay FS, Lawrence JB (1993) A three- dimensional view of precursor messenger RNA metabolism within the mammalian nucleus. Science 259: 1330–1335

    Article  CAS  PubMed  Google Scholar 

  • Castiglia CL, Flint SJ (1983) Effects of adenovirus infection on RNA synthesis and maturation in HeLa cells. Mol Cell Biol 3: 662–671

    CAS  PubMed  Google Scholar 

  • Challberg M, Kelly T (1989) Animal virus DNA replication. Annu Rev Biochem 58: 671–717

    Article  CAS  PubMed  Google Scholar 

  • Cook PR (1991) The nucleoskeleton and the topology of replication. Cell 66: 627–635

    Article  CAS  PubMed  Google Scholar 

  • Danner D, Leder P (1985) Role of an RNA cleavage/poly (A) addition site in the production of membrane-bound and secreted IgM mRNA. Proc Natl Acad Sci USA 82: 8658–8662

    Article  CAS  PubMed  Google Scholar 

  • Doerfler W (ed) (1986) Adenovirus DNA: the viral genome and its expression. Nijhoff, Boston

    Google Scholar 

  • Dolph PJ, Racaniello V, Villamarin A, Palladino F, Schneider RJ (1988) The adenovirus tripartite leader may eliminate the requirement for cap-binding protein complex during translation initiation. J Virol 62:2059–2066

    CAS  PubMed  Google Scholar 

  • Emeson RB, Hedjran F, Yeakley JM, Guise JW, Rosenfeld MG (1989) Alternative production of calcitonin and CGRP mRNA is regulated at the calcitonin-specific splice acceptor. Nature 341: 76–80

    Article  CAS  PubMed  Google Scholar 

  • Fakan S, Leser G, Martin TE (1984) Ultrastructural distribution of nuclear ribonucleoproteins as visualized by immunocytochemistry on thin sections. J Cell Biol 98: 358–363

    Article  CAS  PubMed  Google Scholar 

  • Flint SJ (1986) Regulation of adenovirus mRNA formation. Adv Virus Res 31: 169–228

    Article  CAS  PubMed  Google Scholar 

  • Fox E, Moen PT Jr, Bodnar JW (1990) Replication of minute virus of mice DNA in adenovirus-infected or adenovirus-transformed cells. Virology 176: 403–412

    Article  CAS  PubMed  Google Scholar 

  • Fox MH, Arndt-Jovin DJ, Jovin TM, Baumann PH, Robert-Nicoud M (1991) Spatial and temporal distribution of DNA replication sites localized by immunofluorescence and confocal microscopy in mouse fibroblasts. J Cell Sci 99: 247–253

    PubMed  Google Scholar 

  • Galli G, Guise J, Tucker PW, Nevins JR (1988) Poly(A) site choice rather than splice site choice governs the regulated production of IgM heavy-chain RNAs. Proc Natl Acad Sci USA 85: 2439–2443

    Article  CAS  PubMed  Google Scholar 

  • Green MR (1991) Biochemical mechanisms of constitutive and regulated pre-mRNA splicing. Annu Rev Cell Biol 7: 559–599

    Article  CAS  PubMed  Google Scholar 

  • Hodge LD, Scharf MD (1969) Effect of adenovirus on host cell DNA synthesis in synchronized cells. Virology 37: 554–564

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Schneider RJ (1991) Adenovirus inhibition of cellular protein synthesis involved inactivation of cap-binding protein. Cell 65: 271–280

    Article  CAS  PubMed  Google Scholar 

  • Jackson DA, Bassim Hassan A, Errington RJ, Cook PR (1993) Visualization of focal sites of transcription within human nuclei. EMBO J 12: 1059–1065

    CAS  PubMed  Google Scholar 

  • Jiménez-Garcia LF, Spector DL (1993) In vivo evidence that transcription of splicing are coordinated by a recruiting mechanism. Cell 73: 47–59

    Article  PubMed  Google Scholar 

  • Jiménez-Garcia LF, Green SR, Mathews MB, Spector DL (1993) Organization of the double-stranded RNA-activated protein kinase DAI and virus-associated VA RNA I in adenovirus-2-infected HeLa cells. J Cell Sci 106: 11–22

    PubMed  Google Scholar 

  • Lamond AI, Carmo-Fonseca M (1993) The coiled body. Trends Cell Biol 3: 198–204

    Article  CAS  PubMed  Google Scholar 

  • Ledinko N (1972) Nucleolar ribosomal precursor RNA and protein synthesis in HEK cultures infected with Ad12. Virology 49: 79–89

    Article  CAS  PubMed  Google Scholar 

  • Leff SE, Evans RM, Rosenfeld MG (1987) Splice commitment dictates neuron-specific alternative RNA processing in calcitonin/CGRP gene expression. Cell 48: 517–524

    Article  CAS  PubMed  Google Scholar 

  • LeMaire MF, Thummel CS (1990) Splicing precedes polyadenylation during Drosophila E74A transcription. Mol Cell Biol 10: 6059–6063

    CAS  PubMed  Google Scholar 

  • Martinez-Palomo A, Granboulan N (1967) Electron microscopy of adenovirus 12 replication. II. High- resolution autoradiography of infected KB cells labeled with tritiated thymidine. J Virol 1: 1010–1018

    CAS  PubMed  Google Scholar 

  • Martinez-Palomo A, Le Buis J, Bernhard W (1967) Electron microscopy of adenovirus 12 replication. I. Fine structural changes in the nucleus of KB cells. J Virol 1: 817–829

    CAS  PubMed  Google Scholar 

  • Matsuguchi M, Puvion-Dutilleul F, Moyne G (1979) Late transcription and simultaneous replication of simian adenovirus 7 DNA as revealed by spreading lytically infected cell cultures. J Gen Virol 42: 443–456

    Article  CAS  PubMed  Google Scholar 

  • Moore MJ, Query CC, Sharp P (1993) Splicing precursors to mRNAs by the spliceosome. In: Gesteland RF, Atkins JF (eds) The RNA world. Cold Spring Harbor Laboratory, New York, pp 303–357

    Google Scholar 

  • Moyne G, Pichard E, Bernard W (1978) Localization of simian adenovirus 7 (SA 7) transcription and replication in lytic infection. An ultracytochemical and autoradiographical study J Gen Virol 40: 77–92

    Article  CAS  PubMed  Google Scholar 

  • Murti KG, Davis DS, Kitchingman GR (1990) Localization of adenovirus-encoded DNA replication proteins in the nucleus by immunogold electron microscopy. J Gen Virol 71: 2847–2857

    Article  CAS  PubMed  Google Scholar 

  • Nakamura H, Morita T, Sato C (1986) Structural organization of replicon domains during DNA synthetic phase in the mammalian nucleus. Exp Cell Res 165: 291–297

    Article  CAS  PubMed  Google Scholar 

  • Nakayasu H, Berezney R (1989) Mapping replication sites in the eukaryotic cell nucleus. J Cell Biol 108: 1–11

    Article  CAS  PubMed  Google Scholar 

  • Nevins JR, Darnell JE Jr (1978) Steps in the processing of Ad2 mRNA: poly(A)+nuclear sequences are conserved and poly(A) addition precedes splicing. Cell 15: 1477–1493

    Article  CAS  PubMed  Google Scholar 

  • Nyman U, Hallman H, Hadlaczky G, Pettersson I, Sharp G, Ringertz NR (1986) Intranuclear localization of snRNP antigens. J Cell Biol 102: 137–144

    Article  CAS  PubMed  Google Scholar 

  • O’Keefe RT, Henderson SC, Spector DL (1992) Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific a satellite DNA sequences. J Cell Biol 116: 1095–1110

    Article  PubMed  Google Scholar 

  • Phillips DM, Raskas HJ (1972) Ultrastructural changes in KB cultures infected with adenovirus type 2. Virology 48: 156–169

    Article  CAS  PubMed  Google Scholar 

  • Pina M, Green M (1969) Biochemical studies on adenovirus multiplication XIV. Macromolecule and enzyme synthesis in cells replicating oncogenic and non-oncogenic human adenoviruses. Virology 38: 573–586

    Article  CAS  PubMed  Google Scholar 

  • Pombo A, Ferreira J, Bridge E, Carmo-Fonesca M (1994) Adenovirus replication and transcription are spatially separated in the nucleus of infected cells. EMBO J 13: 5075–5085

    CAS  PubMed  Google Scholar 

  • Puvion-Dutilleul F (1993) Protocol of electron microscope in situ nucleic hybridization for the exclusive detection of double-stranded DNA sequences in cells containing large amounts of homologous single-stranded DNA and RNA sequence: application to adenovirus type 5 infected HeLa cells. Micros Res Tech 25: 2–11

    Article  CAS  Google Scholar 

  • Puvion-Dutilleul F, Christensen ME (1993) Alterations of fibrillarin distribution and nucleolar ultrastructure induced by adenovirus infection. Eur J Cell Biol 61: 168–176

    CAS  PubMed  Google Scholar 

  • Puvion-Duitilleul F, Pichard E (1992) Segregation of viral double-stranded and single-stranded DNA molecules in nuclei of adenovirus infected cells as revealed by electron microscope in situ hybridization. Biol Cell 76: 139–150

    Article  Google Scholar 

  • Puvion-Dutilleul F, Puvion E (1990a) Analysis by in situ hybridization and autoradiography of sites of replication and storage of single- and double-stranded adenovirus type 5 DNA in lytically infected HeLa cells. J Struct Biol 103: 280–289

    Article  CAS  PubMed  Google Scholar 

  • Puvion-Dutilleul F, Puvion E (1990b) Replicating single-stranded adenovirus type 5 DNA molecules accumulate within well-delimited intranuclear areas of lytically infected HeLa cells. Eur J Cell Biol 52: 379–388

    CAS  PubMed  Google Scholar 

  • Puvion-Dutilleul F, Puvion E (1991) Sites of transcription of adenovirus type 5 genomes in relation to early viral DNA replication in infected HeLa cells. A high resolution in situ hybridization and auto- radiographical study. Biol Cell 71: 135–147

    Article  CAS  PubMed  Google Scholar 

  • Puvion-Dutilleul F, Pédron J, Cajean-Feroldi C (1984) Identification of intranuclear structures containing the 72K DNA-binding protein of human adenovirus type 5. Eur J Cell Biol 34: 313–322

    CAS  PubMed  Google Scholar 

  • Puvion-Dutilleul F, Roussev R, Puvion E (1992) Distribution of viral RNA molecules during the adenovirus type 5 infectious cycle in HeLa cells. J Struct Biol 108: 209–220

    Article  CAS  PubMed  Google Scholar 

  • Raskas HJ, Thomas DC, Green M (1970) Biochemical studies on adenovirus multiplication. XVII. Ribosome synthesis in uninfected and infected KB cells. Virology 40: 893–902

    Article  CAS  PubMed  Google Scholar 

  • Reich NC, Sarnow P, Duprey E, Levine AJ (1983) Monoclonal antibodies which recognize native and denatured forms of the adenovirus DNA-binding protein. Virology 128: 480–484

    Article  CAS  PubMed  Google Scholar 

  • Rosbash M, Singer RH (1993) RNA travel: tracks from DNA to cytoplasm. Cell 75: 399–401

    Article  CAS  PubMed  Google Scholar 

  • Sandler AB, Ketner G (1991) The metabolism of host RNAs in cells infected by an adenovirus E4 mutant. Virology 181: 319–326

    Article  CAS  PubMed  Google Scholar 

  • Sasaguri Y, Sanford T, Aguirre P, Padmanabhan R (1987) Immunological analysis of 140-kDa adenovirus- encoded DNA polymerase in adenovirus type 2-infected HeLa cells using antibodies raised against the protein expressed in Escherichia Coli. Virology 160: 389–399

    Article  CAS  PubMed  Google Scholar 

  • Scheer U, Thiry M, Goessens G (1993) Structure, function and assembly of the nucleous. Trends Cell Biol 3: 236–241

    Article  CAS  PubMed  Google Scholar 

  • Sharp PA (1984) Adenovirus transcription. In: Ginsberg H (ed) The adenoviruses. Plenum, New York, pp 173–204

    Google Scholar 

  • Spector DL (1993) Nuclear organization of pre-RNA processing. Curr Opin Cell Biol 5: 442–448

    Article  CAS  PubMed  Google Scholar 

  • Spector DL, Fu X-D, Maniatis T (1991) Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J 10: 3467–3481

    CAS  PubMed  Google Scholar 

  • Thomas GP, Mathews MB (1980) DNA replication and the early to late transition in adenovirus infection. Cell 22: 523–533

    Article  CAS  PubMed  Google Scholar 

  • Tooze J (ed) (1982) The molecular biology of tumor viruses, vol 2. DNA tumor viruses, 2nd rev edn. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Visa N, Puvion-Dutilleul F, Bachellerie JP, Puvion E (1993a) Intranuclear distribution of U1 and U2 snRNAs visualized by high resolution in situ hybridization: revelation of a novel compartment containing U1 but not U2 snRNA in HeLa. Eur J Cell Biol 60: 308–321

    CAS  PubMed  Google Scholar 

  • Visa N, Puvion-Dutilleul F, Harper F, Bachellerie J-P, Puvion E (1993b) Intranuclear distribution of poly(A) RNA determined by electron microscope hybridization. Exp Cell Res 208: 19–34

    Article  CAS  PubMed  Google Scholar 

  • Vlak JM, Rozij THH, Spies F (1975) Localization of adenovirus DNA replication in KB cells. Virology 65: 535–545

    Article  CAS  PubMed  Google Scholar 

  • Voelkerding K, Klessig DF (1986) Identification of two nuclear subclasses of the adenovirus type 5-encoded DNA-binding protein. J Virol 60: 353–362

    CAS  PubMed  Google Scholar 

  • Wahle E, Keller W (1992) The biochemistry of 3′-end cleavage and polyadenylation of messenger RNA precursors. Annu Rev Biochem 61: 419–440

    Article  CAS  PubMed  Google Scholar 

  • Walton TH, Moen PT Jr, Fox E, Bodnar JW (1989) Interactions of minute virus of mice and adenovirus with host nucleoli. J Virol 63: 3651–3660

    CAS  PubMed  Google Scholar 

  • Wang J, Cao L, Wang Y, Pederson T (1991) Localization of pre-messenger RNA in discrete nuclear sites. Proc Natl Acad Sci USA 88: 7391–7395

    Article  CAS  PubMed  Google Scholar 

  • Wilcock D, Lane DP (1991) Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349: 429–431

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm J, Brison O, Kédinger C, Chambon P (1976) Characterization of adenovirus type 2 transcriptional complexes isolated from infected HeLa cell nuclei. J Virol 19: 61–81

    CAS  PubMed  Google Scholar 

  • Wolgemuth DJ, Hsu M-T (1981) Visualization of nascent RNA transcripts and simultaneous transcription and replication in viral nucleoprotein complexes from adenovirus 2-infected HeLa cells. J Mol Biol 147: 247–268

    Article  CAS  PubMed  Google Scholar 

  • Xing Y, Lawrence JB (1993) Nuclear RNA tracks: structural basis for transcription and splicing? Trends Cell Biol 3: 346–353

    Article  CAS  PubMed  Google Scholar 

  • Xing Y, Johnson CV, Dobner PR, Lawrence JB (1993) Higher level organization of individual gene transcription and RNA splicing. Science 259: 1326–1329

    Article  CAS  PubMed  Google Scholar 

  • Yoder SS, Berget SM (1985) Posttranscriptional control of DHFR gene expression during adenovirus 2 infection. J Virol 54: 72–77

    CAS  PubMed  Google Scholar 

  • Zamore PD, Green MR (1991) Biochemical characterization of U2 snRNP auxiliary factor: an essential pre-mRNA splicing factor with a novel intranuclear distribution. EMBO J 10: 207–214

    CAS  PubMed  Google Scholar 

  • Zhang M, Zamore PD, Carmo-Fonseca M, Lamond AI, Green MR (1992) Cloning and intracellular localization of the U2 small nuclear ribonuclear auxiliary factor small subunit. Proc Natl Acad Sci USA 89: 8769–8773

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1995 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bridge, E., Pettersson, U. (1995). Nuclear Organization of Replication and Gene Expression in Adenovirus-Infected Cells. In: Doerfler, W., Böhm, P. (eds) The Molecular Repertoire of Adenoviruses I. Current Topics in 199/I Microbiology and Immunology, vol 199/1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79496-4_7

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-79496-4_7

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-79498-8

  • Online ISBN: 978-3-642-79496-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics