Parvovirus induced alterations in nuclear architecture and dynamics

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Ihalainen, Teemu O ^a   Niskanen, Einari A ^a   Jylhävä, Juulia ^a,b   Paloheimo, Outi ^a   Dross, Nicolas ^c   Smolander, Hanna ^a,d   Langowski, Jörg ^c   Timonen, Jussi ^a   Vihinen Ranta, Maija ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA; DEXTRAN; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL STRUCTURE; CHROMATIN; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; NONHUMAN; PARVOVIRUS; PARVOVIRUS INFECTION; PROTEIN TRANSPORT; VIRUS CAPSID; VIRUS GENOME; VIRUS REPLICATION; ANIMAL; CAT; CHEMISTRY; CONFOCAL MICROSCOPY; FELINE PANLEUKOPENIA VIRUS; HELA CELL; KIDNEY; METABOLISM; VIROLOGY; VIRUS INFECTION;

CANINE PARVOVIRUS; DNA VIRUSES; EUKARYOTA; MIRIDAE; PARVOVIRUS;

ANIMALS; CATS; CELL NUCLEUS; CHROMATIN; DEXTRANS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENOME, VIRAL; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; KIDNEY; MICROSCOPY, CONFOCAL; PARVOVIRIDAE INFECTIONS; PARVOVIRUS; PARVOVIRUS, CANINE;

EID: 67650115009     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005948     Document Type: Article

References (76)

1. Mettenleiter TC (2002) Herpesvirus assembly and egress. J Virol 76(4): 1537-1547.
2. Berk AJ (2005) Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene 24(52): 7673-7685.
3. Taylor TJ, Knipe DM (2004) Proteomics of herpes simplex virus replication compartments: Association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J Virol 78(11): 5856-5866.
4. Everett RD (2001) DNA viruses and viral proteins that interact with PML nuclear bodies. Oncogene 20(49): 7266-7273.
5. Weitzman MD, Carson CT, Schwartz RA, Lilley CE (2004) Interactions of viruses with the cellular DNA repair machinery. DNA Repair (Amst) 3(8-9): 1165-1173.
6. Lamond AI, Spector DL (2003) Nuclear speckles: A model for nuclear organelles. Nat Rev Mol Cell Biol 4(8): 605-612.
7. Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, et al. (2006) Chromosome territories - a functional nuclear landscape. Curr Opin Cell Biol 18(3): 307-316.
8. Lanctot C, Cheutin T, Cremer M, Cavalli G, Cremer T (2007) Dynamic genome architecture in the nuclear space: Regulation of gene expression in three dimensions. Nat Rev Genet 8(2): 104-115.
9. Cremer C, Munkel C, Granzow M, Jauch A, Dietzel S, et al. (1996) Nuclear architecture and the induction of chromosomal aberrations. Mutat Res 366(2): 97-116.
10. Cremer T, Kreth G, Koester H, Fink RH, Heintzmann R, et al. (2000) Chromosome territories, interchromatin domain compartment, and nuclear matrix: An integrated view of the functional nuclear architecture. Crit Rev Eukaryot Gene Expr 10(2): 179-212.
11. Albiez H, Cremer M, Tiberi C, Vecchio L, Schermelleh L, et al. (2006) Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks. Chromosome Res 14(7): 707-733.
12. Carter DR, Eskiw C, Cook PR (2008) Transcription factories. Biochem Soc Trans 36(Pt 4): 585-589.
13. Handwerger KE, Gall JG (2006) Subnuclear organelles: New insights into form and function. Trends Cell Biol 16(1): 19-26.
14. Misteli T (2007) Beyond the sequence: Cellular organization of genome function. Cell 128(4): 787-800.
15. Tseng Y, Lee JS, Kole TP, Jiang I, Wirtz D (2004) Micro-organization and visco-elasticity of the interphase nucleus revealed by particle nanotracking. J Cell Sci 117(Pt 10): 2159-2167.
16. Guigas G, Kalla C, Weiss M (2007) Probing the nanoscale viscoelasticity of intracellular fluids in living cells. Biophys J 93(1): 316-323.
17. Zeskind BJ, Jordan CD, Timp W, Trapani L, Waller G, et al. (2007) Nucleic acid and protein mass mapping by live-cell deep-ultraviolet microscopy. Nat Methods 4(7): 567-569.
18. Gorisch SM, Wachsmuth M, Toth KF, Lichter P, Rippe K (2005) Histone acetylation increases chromatin accessibility. J Cell Sci 118(Pt 24): 5825-5834.
19. Gorisch SM, Wachsmuth M, Ittrich C, Bacher CP, Rippe K, et al. (2004) Nuclear body movement is determined by chromatin accessibility and dynamics. Proc Natl Acad Sci U S A 101(36): 13221-13226.
20. Tsao J, Chapman MS, Agbandje M, Keller W, Smith K, et al. (1991) The three-dimensional structure of canine parvovirus and its functional implications. Science 251(5000): 1456-1464.
21. Reed AP, Jones EV, Miller TJ (1988) Nucleotide sequence and genome organization of canine parvovirus. J Virol 62(1): 266-276.
22. Parrish CR (1991) Mapping specific functions in the capsid structure of canine parvovirus and feline panleukopenia virus using infectious plasmid clones. Virology 183(1): 195-205.
23. Jindal HK, Yong CB, Wilson GM, Tam P, Astell CR (1994) Mutations in the NTP-binding motif of minute virus of mice (MVM) NS-1 protein uncouple ATPase and DNA helicase functions. J Biol Chem 269(5): 3283-3289.
24. Christensen J, Cotmore SF, Tattersall P (1995) Minute virus of mice transcriptional activator protein NS1 binds directly to the transactivation region of the viral P38 promoter in a strictly ATP-dependent manner. J Virol 69(9): 5422-5430.
25. Christensen J, Cotmore SF, Tattersall P (2001) Minute virus of mice initiator protein NS1 and a host KDWK family transcription factor must form a precise ternary complex with origin DNA for nicking to occur. J Virol 75(15): 7009-7017.
26. Cotmore SF, Christensen J, Nuesch JP, Tattersall P (1995) The NS1 polypeptide of the murine parvovirus minute virus of mice binds to DNA sequences containing the motif [ACCA]2-3. J Virol 69(3): 1652-1660.
27. Nuesch JP, Cotmore SF, Tattersall P (1995) Sequence motifs in the replicator protein of parvovirus MVM essential for nicking and covalent attachment to the viral origin: Identification of the linking tyrosine. Virology 209(1): 122-135.
28. Cziepluch C, Lampel S, Grewenig A, Grund C, Lichter P, et al. (2000) H-1 parvovirus-associated replication bodies: A distinct virus-induced nuclear structure. J Virol 74(10): 4807-4815.
29. Iwahori S, Ikeda M, Kobayashi M (2004) Association of Sf9 cell proliferating cell nuclear antigen with the DNA replication site of autographa californica multicapsid nucleopolyhedrovirus. J Gen Virol 85(Pt 10): 2857-2862.
30. Daikoku T, Kudoh A, Sugaya Y, Iwahori S, Shirata N, et al. (2006) Postreplicative mismatch repair factors are recruited to epstein-barr virus replication compartments. J Biol Chem 281(16): 11422-11430.
31. Christensen J, Cotmore SF, Tattersall P (1997) A novel cellular site-specific DNA-binding protein cooperates with the viral NS1 polypeptide to initiate parvovirus DNA replication. J Virol 71(2): 1405-1416.
32. Nash K, Chen W, McDonald WF, Zhou X, Muzyczka N (2007) Purification of host cell enzymes involved in adeno-associated virus DNA replication. J Virol 81(11): 5777-5787.
33. Dross N, Spriet C, Zwerger M, Muller G, Waldeck W, et al. (2009) Mapping eGFP oligomer mobility in living cell nuclei. PLoS ONE 4(4): e5041.
34. Suikkanen S, Saajarvi K, Hirsimaki J, Valilehto O, Reunanen H, et al. (2002) Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J Virol 76(9): 4401-4411.
35. Ihalainen TO, Niskanen EA, Jylhava J, Turpeinen T, Rinne J, et al. (2007) Dynamics and interactions of parvoviral NS1 protein in the nucleus. Cell Microbiol 9(8): 1946-1959.
36. Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297(5588): 1873-1877.
37. Parker JS, Parrish CR (1997) Canine parvovirus host range is determined by the specific conformation of an additional region of the capsid. J Virol 71(12): 9214-9222.
38. Hauck B, Zhao W, High K, Xiao W (2004) Intracellular viral processing, not single-stranded DNA accumulation, is crucial for recombinant adeno-associated virus transduction. J Virol 78(24): 13678-13686.
39. Parker JS, Murphy WJ, Wang D, O'Brien SJ, Parrish CR (2001) Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J Virol 75(8): 3896-3902.
40. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, et al. (2005) Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 25(21): 9350-9359.
41. Braga J, Desterro JM, Carmo-Fonseca M (2004) Intracellular macromolecular mobility measured by fluorescence recovery after photobleaching with confocal laser scanning microscopes. Mol Biol Cell 15(10): 4749-4760.
42. Sprague BL, Pego RL, Stavreva DA, McNally JG (2004) Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J 86(6): 3473-3495.
43. Christensen J, Tattersall P (2002) Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J Virol 76(13): 6518-6531.
44. Young PJ, Newman A, Jensen KT, Burger LR, Pintel DJ, et al. (2005) Minute virus of mice small non-structural protein NS2 localizes within, but is not required for the formation of, smn-associated autonomous parvovirus-associated replication bodies. J Gen Virol 86(Pt 4): 1009-1014.
45. de Oliveira AP, Glauser DL, Laimbacher AS, Strasser R, Schraner EM, et al. (2008) Live visualization of herpes simplex virus type 1 compartment dynamics. J Virol 82(10): 4974-4990.
46. Blissard GW (1996) Baculovirus - insect cell interactions. Cytotechnology 20(1-3): 73-93.
47. Verschure PJ, van der Kraan I, Manders EM, Hoogstraten D, Houtsmuller AB, et al. (2003) Condensed chromatin domains in the mammalian nucleus are accessible to large macromolecules. EMBO Rep 4(9): 861-866.
48. Gorisch SM, Richter K, Scheuermann MO, Herrmann H, Lichter P (2003) Diffusion-limited compartmentalization of mammalian cell nuclei assessed by microinjected macromolecules. Exp Cell Res 289(2): 282-294.
49. Gilbert L, Toivola J, Valilehto O, Saloniemi T, Cunningham C, et al. (2006) Truncated forms of viral VP2 proteins fused to EGFP assemble into fluorescent parvovirus-like particles. J Nanobiotechnology 4: 13.
50. Riolobos L, Reguera J, Mateu MG, Almendral JM (2006) Nuclear transport of trimeric assembly intermediates exerts a morphogenetic control on the icosahedral parvovirus capsid. J Mol Biol 357(3): 1026-1038.
51. Gilbert L, Toivola J, Lehtomaki E, Donaldson L, Kapyla P, et al. (2004) Assembly of fluorescent chimeric virus-like particles of canine parvovirus in insect cells. Biochem Biophys Res Commun 313(4): 878-887.
52. Seksek O, Biwersi J, Verkman AS (1997) Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J Cell Biol 138(1): 131-142.
53. Seisenberger G, Ried MU, Endress T, Buning H, Hallek M, et al. (2001) Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294(5548): 1929-1932.
54. Muller DE, Siegl G (1983) Maturation of parvovirus LuIII in a subcellular system. II. isolation and characterization of nucleoprotein intermediates. J Gen Virol 64(Pt 5): 1055-1067.
55. Janicki SM, Spector DL (2003) Nuclear choreography: Interpretations from living cells. Curr Opin Cell Biol 15(2): 149-157.
56. Monier K, Armas JC, Etteldorf S, Ghazal P, Sullivan KF (2000) Annexation of the interchromosomal space during viral infection. Nat Cell Biol 2(9): 661-665.
57. Nagamine T, Kawasaki Y, Abe A, Matsumoto S (2008) Nuclear marginalization of host cell chromatin associated with expansion of two discrete virus-induced subnuclear compartments during baculovirus infection. J Virol 82(13): 6409-6418.
58. Oh J, Fraser NW (2008) Temporal association of the herpes simplex virus genome with histone proteins during a lytic infection. J Virol 82(7): 3530-3537.
59. Wachsmuth M, Waldeck W, Langowski J (2000) Anomalous diffusion of fluorescent probes inside living cell nuclei investigated by spatially-resolved fluorescence correlation spectroscopy. J Mol Biol 298(4): 677-689.
60. Kues T, Peters R, Kubitscheck U (2001) Visualization and tracking of single protein molecules in the cell nucleus. Biophys J 80(6): 2954-2967.
61. Richter K, Nessling M, Lichter P (2008) Macromolecular crowding and its potential impact on nuclear function. Biochim Biophys Acta 1783(11): 2100-2107.
62. Wedemeier A, Merlitz H, Wu CX, Langowski J (2007) Modeling diffusional transport in the interphase cell nucleus. J Chem Phys 127(4): 045102.
63. Saxton MJ (1989) Lateral diffusion in an archipelago. distance dependence of the diffusion coefficient. Biophys J 56(3): 615-622.
64. von Hippel PH, Berg OG (1989) Facilitated target location in biological systems. J Biol Chem 264(2): 675-678.
65. Bashir T, Rommelaere J, Cziepluch C (2001) In vivo accumulation of cyclin A and cellular replication factors in autonomous parvovirus minute virus of mice-associated replication bodies. J Virol 75(9): 4394-4398.
66. Marenduzzo D, Finan K, Cook PR (2006) The depletion attraction: An underappreciated force driving cellular organization. J Cell Biol 175(5): 681-686.
67. Braga J, McNally JG, Carmo-Fonseca M (2007) A reaction-diffusion model to study RNA motion by quantitative fluorescence recovery after photobleaching. Biophys J 92(8): 2694-2703.
68. Lukacs GL, Haggie P, Seksek O, Lechardeur D, Freedman N, et al. (2000) Size-dependent DNA mobility in cytoplasm and nucleus. J Biol Chem 275(3): 1625-1629.
69. Cotmore SF, Gottlieb RL, Tattersall P (2007) Replication initiator protein NS1 of the parvovirus minute virus of mice binds to modular divergent sites distributed throughout duplex viral DNA. J Virol 81(23): 13015-13027.
70. Naryzhny SN, Zhao H, Lee H (2005) Proliferating cell nuclear antigen (PCNA) may function as a double homotrimer complex in the mammalian cell. J Biol Chem 280(14): 13888-13894.
71. Solomon DA, Cardoso MC, Knudsen ES (2004) Dynamic targeting of the replication machinery to sites of DNA damage. J Cell Biol 166(4): 455-463.
72. Phair RD, Scaffidi P, Elbi C, Vecerova J, Dey A, et al. (2004) Global nature of dynamic protein-chromatin interactions in vivo: Three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol Cell Biol 24(14): 6393-6402.
73. Cotmore SF, Tattersall P (2005) Genome packaging sense is controlled by the efficiency of the nick site in the right-end replication origin of parvoviruses minute virus of mice and LuIII. J Virol 79(4): 2287-2300.
74. Jackson DA, Pombo A (1998) Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140(6): 1285-1295.
75. Norio P, Schildkraut CL (2004) Plasticity of DNA replication initiation in epstein-barr virus episomes. PLoS Biol 2(6): e152.
76. Yamashita T, Arens M, Green M (1975) Adenovirus deoxyribonucleic acid replication. II. synthesis of viral deoxyribonucleic acid in vitro by a nuclear membrane fraction from infected KB cells. J Biol Chem 250(9): 3273-3279.