1932

Abstract

Parvoviruses are small, rugged, nonenveloped protein particles containing a linear, nonpermuted, single-stranded DNA genome of ∼5 kb. Their limited coding potential requires optimal adaptation to the environment of particular host cells, where entry is mediated by a variable program of capsid dynamics, ultimately leading to genome ejection from intact particles within the host nucleus. Genomes are amplified by a continuous unidirectional strand-displacement mechanism, a linear adaptation of rolling circle replication that relies on the repeated folding and unfolding of small hairpin telomeres to reorient the advancing fork. Progeny genomes are propelled by the viral helicase into the preformed capsid via a pore at one of its icosahedral fivefold axes. Here we explore how the fine-tuning of this unique replication system and the mechanics that regulate opening and closing of the capsid fivefold portals have evolved in different viral lineages to create a remarkably complex spectrum of phenotypes.

Associated Article

There are media items related to this article:
Parvoviruses: Small Does Not Mean Simple: Video 1
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085444
2014-09-29
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085444.html?itemId=/content/journals/10.1146/annurev-virology-031413-085444&mimeType=html&fmt=ahah

Literature Cited

  1. Agbandje-McKenna M, Kleinschmidt J. 1.  2011. AAV capsid structure and cell interactions. Methods Mol. Biol. 807:47–92 [Google Scholar]
  2. Berns KI, Parrish CR. 2.  2013. Parvoviridae. Fields Virology DM Knipe, P Howley 1768–91 Philadelphia: Lippincott Williams & Wilkins, 6th ed.. [Google Scholar]
  3. Halder S, Ng R, Agbandje-McKenna M. 3.  2012. Parvoviruses: structure and infection. Future Virol. 7:253–78 [Google Scholar]
  4. Cotmore SF, Tattersall P. 4.  2007. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 70:183–232 [Google Scholar]
  5. Cotmore SF, Tattersall P. 5.  2013. Parvovirus diversity and DNA damage responses. Cold Spring Harb. Perspect. Biol. 5:a012989 [Google Scholar]
  6. Nuesch JP, Lacroix J, Marchini A, Rommelaere J. 6.  2012. Molecular pathways: rodent parvoviruses—mechanisms of oncolysis and prospects for clinical cancer treatment. Clin. Cancer Res. 18:3516–23 [Google Scholar]
  7. Bleker S, Sonntag F, Kleinschmidt JA. 7.  2005. Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity. J. Virol. 79:2528–40 [Google Scholar]
  8. Plevka P, Hafenstein S, Li L, D'Abramo A, Cotmore SF. 8.  et al. 2011. Structure of a packaging-defective mutant of minute virus of mice indicates that the genome is packaged via a pore at a 5-fold axis. J. Virol. 85:4822–27 [Google Scholar]
  9. King JA, Dubielzig R, Grimm D, Kleinschmidt JA. 9.  2001. DNA helicase–mediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 20:3282–91Identifies the viral helicase as a motor that packages DNA into the preformed protein capsid. [Google Scholar]
  10. Meriluoto M, Hedman L, Tanner L, Simell V, Makinen M. 10.  et al. 2012. Association of human bocavirus 1 infection with respiratory disease in childhood follow-up study, Finland. Emerg. Infect. Dis. 18:264–71 [Google Scholar]
  11. Truyen U, Parrish CR. 11.  2013. Feline panleukopenia virus: its interesting evolution and current problems in immunoprophylaxis against a serious pathogen. Vet. Microbiol. 165:29–32 [Google Scholar]
  12. Bär S, Rommelaere J, Nuesch JP. 12.  2013. Vesicular transport of progeny parvovirus particles through ER and Golgi regulates maturation and cytolysis. PLoS Pathog. 9:e1003605Probes the cellular pathway that mediates active transport of progeny virions out of the parental cell. [Google Scholar]
  13. Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA. 13.  2006. Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J. Virol. 80:11040–54 [Google Scholar]
  14. Cotmore SF, Agbandje-McKenna M, Chiorini JA, Mukha DV, Pintel DJ. 14.  et al. 2014. The family Parvoviridae. Arch. Virol. 159:1239–47 [Google Scholar]
  15. Cotmore SF, Agbandje-McKenna M, Chiorini JA, Gatherer D, Mukha DV. 15.  et al. 2013. Rationalization and extension of the taxonomy of the family Parvoviridae ICTV Official Taxonomy: Updates Since the 8th Report, Code 2013.001a-aaaV, Int. Comm. Taxon. Viruses (ICTV)
  16. Allander T, Tammi MT, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B. 16.  2005. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc. Natl. Acad. Sci. USA 102:12891–96 [Google Scholar]
  17. Jartti T, Hedman K, Jartti L, Ruuskanen O, Allander T, Soderlund-Venermo M. 17.  2012. Human bocavirus—the first 5 years. Rev. Med. Virol. 22:46–64 [Google Scholar]
  18. Jones MS, Kapoor A, Lukashov VV, Simmonds P, Hecht F, Delwart E. 18.  2005. New DNA viruses identified in patients with acute viral infection syndrome. J. Virol. 79:8230–36 [Google Scholar]
  19. Matthews PC, Malik A, Simmons R, Sharp C, Simmonds P, Klenerman P. 19.  2014. PARV4: an emerging tetraparvovirus. PLoS Pathog. 10:e1004036 [Google Scholar]
  20. Fasina O, Pintel DJ. 20.  2013. The adeno-associated virus type 5 small Rep proteins expressed via internal translation initiation are functional. J. Virol. 87:296–303 [Google Scholar]
  21. Guan W, Huang Q, Cheng F, Qiu J. 21.  2011. Internal polyadenylation of the parvovirus B19 precursor mRNA is regulated by alternative splicing. J. Biol. Chem. 286:24793–805 [Google Scholar]
  22. Qiu J, Cheng F, Burger LR, Pintel D. 22.  2006. The transcription profile of Aleutian mink disease virus in CRFK cells is generated by alternative processing of pre-mRNAs produced from a single promoter. J. Virol. 80:654–62 [Google Scholar]
  23. Qiu J, Pintel D. 23.  2008. Processing of adeno-associated virus RNA. Front. Biosci. 13:3101–15 [Google Scholar]
  24. Qiu J, Yoto Y, Tullis G, Pintel DJ. 24.  2005. Parvovirus RNA processing strategies. Parvoviruses JR Kerr, SF Cotmore, ME Bloom, RM Linden, CR Parrish 253–73 London: Hodder Arnold [Google Scholar]
  25. Sukhu L, Fasina O, Burger L, Rai A, Qiu J, Pintel DJ. 25.  2013. Characterization of the nonstructural proteins of the bocavirus minute virus of canines. J. Virol. 87:1098–104Identifies NP1 as the first parvoviral ancillary protein known to influence RNA processing. [Google Scholar]
  26. Kotin RM, Linden RM, Berns KI. 26.  1992. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. EMBO J. 11:5071–78 [Google Scholar]
  27. Miller DG, Trobridge GD, Petek LM, Jacobs MA, Kaul R, Russell DW. 27.  2005. Large-scale analysis of adeno-associated virus vector integration sites in normal human cells. J. Virol. 79:11434–42 [Google Scholar]
  28. Yang J, Zhou W, Zhang Y, Zidon T, Ritchie T, Engelhardt JF. 28.  1999. Concatamerization of adeno-associated virus circular genomes occurs through intermolecular recombination. J. Virol. 73:9468–77 [Google Scholar]
  29. Cotmore SF, Tattersall P. 29.  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. 79:2287–300Packaging strand selection is driven by the efficiency of strand excision, not specific packaging sequences. [Google Scholar]
  30. Cotmore SF, Tattersall P. 30.  2003. Resolution of parvovirus dimer junctions proceeds through a novel heterocruciform intermediate. J. Virol. 77:6245–54 [Google Scholar]
  31. Cotmore SF, Tattersall P. 31.  2006. Parvoviruses. DNA Replication and Human Disease ML DePamphilis 593–608 New York: Cold Spring Harb. Lab. Press [Google Scholar]
  32. Hickman AB, Ronning DR, Perez ZN, Kotin RM, Dyda F. 32.  2004. The nuclease domain of adeno-associated virus Rep coordinates replication initiation using two distinct DNA recognition interfaces. Mol. Cell 13:403–14 [Google Scholar]
  33. James JA, Aggarwal AK, Linden RM, Escalante CR. 33.  2004. Structure of adeno-associated virus type 2 Rep40-ADP complex: insight into nucleotide recognition and catalysis by superfamily 3 helicases. Proc. Natl. Acad. Sci. USA 101:12455–60 [Google Scholar]
  34. Nuesch JP, Cotmore SF, Tattersall P. 34.  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 209:122–35 [Google Scholar]
  35. Tewary SK, Zhao H, Shen W, Qiu J, Tang L. 35.  2013. Structure of the NS1 protein N-terminal origin recognition/nickase domain from the emerging human bocavirus. J. Virol. 87:11487–93 [Google Scholar]
  36. Christensen J, Cotmore SF, Tattersall P. 36.  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. 69:5422–30 [Google Scholar]
  37. Doerig C, Hirt B, Antonietti JP, Beard P. 37.  1990. Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription. J. Virol. 64:387–96 [Google Scholar]
  38. Lackner DF, Muzyczka N. 38.  2002. Studies of the mechanism of transactivation of the adeno-associated virus p19 promoter by Rep protein. J. Virol. 76:8225–35 [Google Scholar]
  39. Zarate-Perez F, Mansilla-Soto J, Bardelli M, Burgner JW II, Villamil-Jarauta M. 39.  et al. 2013. Oligomeric properties of adeno-associated virus Rep68 reflect its multifunctionality. J. Virol. 87:1232–41 [Google Scholar]
  40. Cotmore SF, Gottlieb RL, Tattersall P. 40.  2007. Replication initiator protein NS1 of the parvovirus minute virus of mice binds to modular divergent sites distributed throughout duplex viral DNA. J. Virol. 81:13015–27 [Google Scholar]
  41. Cotmore SF, Tattersall P. 41.  1988. The NS-1 polypeptide of minute virus of mice is covalently attached to the 5′ termini of duplex replicative-form DNA and progeny single strands. J. Virol. 62:851–60 [Google Scholar]
  42. Zadori Z, Szelei J, Tijssen P. 42.  2005. SAT: a late NS protein of porcine parvovirus. J. Virol. 79:13129–38 [Google Scholar]
  43. Huang Q, Luo Y, Cheng F, Best SM, Bloom ME, Qiu J. 43.  2014. Molecular characterization of the small nonstructural proteins of parvovirus Aleutian mink disease virus (AMDV) during infection. Virology 452:23–31 [Google Scholar]
  44. Naeger LK, Cater JE, Pintel DJ. 44.  1990. The small nonstructural protein (NS2) of the parvovirus minute virus of mice is required for efficient DNA replication and infectious virus production in a cell-type-specific manner. J. Virol. 64:6166–75 [Google Scholar]
  45. Ruiz Z, D'Abramo A Jr, Tattersall P. 45.  2006. Differential roles for the C-terminal hexapeptide domains of NS2 splice variants during MVM infection of murine cells. Virology 349:382–95 [Google Scholar]
  46. Brockhaus K, Plaza S, Pintel DJ, Rommelaere J, Salome N. 46.  1996. Nonstructural proteins NS2 of minute virus of mice associate in vivo with 14-3-3 protein family members. J. Virol. 70:7527–34 [Google Scholar]
  47. Bodendorf U, Cziepluch C, Jauniaux JC, Rommelaere J, Salome N. 47.  1999. Nuclear export factor CRM1 interacts with nonstructural proteins NS2 from parvovirus minute virus of mice. J. Virol. 73:7769–79 [Google Scholar]
  48. Eichwald V, Daeffler L, Klein M, Rommelaere J, Salome N. 48.  2002. The NS2 proteins of parvovirus minute virus of mice are required for efficient nuclear egress of progeny virions in mouse cells. J. Virol. 76:10307–19 [Google Scholar]
  49. Engelsma D, Valle N, Fish A, Salome N, Almendral JM, Fornerod M. 49.  2008. A supraphysiological nuclear export signal is required for parvovirus nuclear export. Mol. Biol. Cell 19:2544–52 [Google Scholar]
  50. Miller CL, Pintel DJ. 50.  2002. Interaction between parvovirus NS2 protein and nuclear export factor Crm1 is important for viral egress from the nucleus of murine cells. J. Virol. 76:3257–66 [Google Scholar]
  51. Naumer M, Sonntag F, Schmidt K, Nieto K, Panke C. 51.  et al. 2012. Properties of the adeno-associated virus assembly-activating protein. J. Virol. 86:13038–48 [Google Scholar]
  52. Zhi N, Mills IP, Lu J, Wong S, Filippone C, Brown KE. 52.  2006. Molecular and functional analyses of a human parvovirus B19 infectious clone demonstrates essential roles for NS1, VP1, and the 11-kilodalton protein in virus replication and infectivity. J. Virol. 80:5941–50 [Google Scholar]
  53. Chen AY, Zhang EY, Guan W, Cheng F, Kleiboeker S. 53.  et al. 2010. The small 11 kDa nonstructural protein of human parvovirus B19 plays a key role in inducing apoptosis during B19 virus infection of primary erythroid progenitor cells. Blood 115:1070–80 [Google Scholar]
  54. Chen AY, Cheng F, Lou S, Luo Y, Liu Z. 54.  et al. 2010. Characterization of the gene expression profile of human bocavirus. Virology 403:145–54 [Google Scholar]
  55. Lederman M, Patton JT, Stout ER, Bates RC. 55.  1984. Virally coded noncapsid protein associated with bovine parvovirus infection. J. Virol. 49:315–18 [Google Scholar]
  56. Zadori Z, Szelei J, Lacoste MC, Li Y, Gariepy S. 56.  et al. 2001. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 1:291–302Identifies a phospholipase 2 activity encoded in VP1 N termini that is essential for cell entry. [Google Scholar]
  57. Kronenberg S, Bottcher B, von der Lieth CW, Bleker S, Kleinschmidt JA. 57.  2005. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J. Virol. 79:5296–303 [Google Scholar]
  58. Venkatakrishnan B, Yarbrough J, Domsic J, Bennett A, Bothner B. 58.  et al. 2013. Structure and dynamics of adeno-associated virus serotype 1 VP1-unique N-terminal domain and its role in capsid trafficking. J. Virol. 87:4974–84 [Google Scholar]
  59. Canaan S, Zadori Z, Ghomashchi F, Bollinger J, Sadilek M. 59.  et al. 2004. Interfacial enzymology of parvovirus phospholipases A2. J. Biol. Chem. 279:14502–8 [Google Scholar]
  60. Farr GA, Zhang LG, Tattersall P. 60.  2005. Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc. Natl. Acad. Sci. USA 102:17148–53 [Google Scholar]
  61. Girod A, Wobus CE, Zadori Z, Ried M, Leike K. 61.  et al. 2002. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J. Gen. Virol. 83:973–78 [Google Scholar]
  62. Leisi R, Ruprecht N, Kempf C, Ros C. 62.  2013. Parvovirus B19 uptake is a highly selective process controlled by VP1u, a novel determinant of viral tropism. J. Virol. 87:13161–67 [Google Scholar]
  63. Vihinen-Ranta M, Wang D, Weichert WS, Parrish CR. 63.  2002. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 76:1884–91Antibody microinjection studies show that during cell entry, VP1 N termini are exposed in the cytoplasm. [Google Scholar]
  64. Lombardo E, Ramírez JC, Garcia J, Almendral JM. 64.  2002. Complementary roles of multiple nuclear targeting signals in the capsid proteins of the parvovirus minute virus of mice during assembly and onset of infection. J. Virol. 76:7049–59 [Google Scholar]
  65. Popa-Wagner R, Sonntag F, Schmidt K, King J, Kleinschmidt JA. 65.  2012. Nuclear translocation of adeno-associated virus type 2 capsid proteins for virion assembly. J. Gen. Virol. 93:1887–98 [Google Scholar]
  66. Cohen S, Marr AK, Garcin P, Pante N. 66.  2011. Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle. J. Virol. 85:4863–74 [Google Scholar]
  67. Porwal M, Cohen S, Snoussi K, Popa-Wagner R, Anderson F. 67.  et al. 2013. Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLoS Pathog. 9:e1003671 [Google Scholar]
  68. Lombardo E, Ramírez JC, Agbandje-McKenna M, Almendral JM. 68.  2000. A β-stranded motif drives capsid protein oligomers of the parvovirus minute virus of mice into the nucleus for viral assembly. J. Virol. 74:3804–14 [Google Scholar]
  69. Riolobos L, Reguera J, Mateu MG, Almendral JM. 69.  2006. Nuclear transport of trimeric assembly intermediates exerts a morphogenetic control on the icosahedral parvovirus capsid. J. Mol. Biol. 357:1026–38 [Google Scholar]
  70. Wistuba A, Kern A, Weger S, Grimm D, Kleinschmidt JA. 70.  1997. Subcellular compartmentalization of adeno-associated virus type 2 assembly. J. Virol. 71:1341–52 [Google Scholar]
  71. Agbandje-McKenna M, Llamas-Saiz AL, Wang F, Tattersall P, Rossmann MG. 71.  1998. Functional implications of the structure of the murine parvovirus, minute virus of mice. Structure 6:1369–81X-ray structure of MVM virions identifies a single glycine-rich VP2 sequence traversing the fivefold pores. [Google Scholar]
  72. Gurda BL, Parent KN, Bladek H, Sinkovits RS, DiMattia MA. 72.  et al. 2010. Human bocavirus capsid structure: insights into the structural repertoire of the Parvoviridae. J. Virol. 84:5880–89 [Google Scholar]
  73. Kaufmann B, Simpson AA, Rossmann MG. 73.  2004. The structure of human parvovirus B19. Proc. Natl. Acad. Sci. USA 101:11628–33 [Google Scholar]
  74. McKenna R, Olson NH, Chipman PR, Baker TS, Booth TF. 74.  et al. 1999. Three-dimensional structure of Aleutian mink disease parvovirus: implications for disease pathogenicity. J. Virol. 73:6882–91 [Google Scholar]
  75. Tsao J, Chapman MS, Agbandje M, Keller W, Smith K. 75.  et al. 1991. The three-dimensional structure of canine parvovirus and its functional implications. Science 251:1456–64 [Google Scholar]
  76. Xie Q, Bu W, Bhatia S, Hare J, Somasundaram T. 76.  et al. 2002. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl. Acad. Sci. USA 99:10405–10 [Google Scholar]
  77. Castellanos M, Perez R, Rodriguez-Huete A, Grueso E, Almendral JM, Mateu MG. 77.  2013. A slender tract of glycine residues is required for translocation of the VP2 protein N-terminal domain through the parvovirus MVM capsid channel to initiate infection. Biochem. J. 455:87–94 [Google Scholar]
  78. Kaufmann B, Chipman PR, Kostyuchenko VA, Modrow S, Rossmann MG. 78.  2008. Visualization of the externalized VP2 N termini of infectious human parvovirus B19. J. Virol. 82:7306–12 [Google Scholar]
  79. Ros C, Gerber M, Kempf C. 79.  2006. Conformational changes in the VP1-unique region of native human parvovirus B19 lead to exposure of internal sequences that play a role in virus neutralization and infectivity. J. Virol. 80:12017–24 [Google Scholar]
  80. Maroto B, Valle N, Saffrich R, Almendral JM. 80.  2004. Nuclear export of the nonenveloped parvovirus virion is directed by an unordered protein signal exposed on the capsid surface. J. Virol. 78:10685–94 [Google Scholar]
  81. Cotmore SF, Tattersall P. 81.  2005. Encapsidation of minute virus of mice DNA: aspects of the translocation mechanism revealed by the structure of partially packaged genomes. Virology 336:100–12 [Google Scholar]
  82. Govindasamy L, Gurda BL, Halder S, Van Vliet K, McKenna R. 82.  et al. 2010. MVM capsid dynamics associated with DNA packaging and VP2 externalization for maturation cleavage Presented at XIII Int. Parvovirus Workshop, June 20–24, Helsinki, Finland. Poster P11
  83. Farr GA, Cotmore SF, Tattersall P. 83.  2006. VP2 cleavage and the leucine ring at the base of the fivefold cylinder control pH-dependent externalization of both the VP1 N terminus and the genome of minute virus of mice. J. Virol. 80:161–71 [Google Scholar]
  84. Cotmore SF, Tattersall P. 84.  2012. Mutations at the base of the icosahedral five-fold cylinders of minute virus of mice induce 3′-to-5′ genome uncoating and critically impair entry functions. J. Virol. 86:69–80 [Google Scholar]
  85. Cotmore SF, Hafenstein S, Tattersall P. 85.  2010. Depletion of virion-associated divalent cations induces parvovirus minute virus of mice to eject its genome in a 3′-to-5′ direction from an otherwise intact viral particle. J. Virol. 84:1945–56 [Google Scholar]
  86. López-Bueno A, Mateu MG, Almendral JM. 86.  2003. High mutant frequency in populations of a DNA virus allows evasion from antibody therapy in an immunodeficient host. J. Virol. 77:2701–8 [Google Scholar]
  87. Shackelton LA, Holmes EC. 87.  2006. Phylogenetic evidence for the rapid evolution of human B19 erythrovirus. J. Virol. 80:3666–69 [Google Scholar]
  88. Shackelton LA, Parrish CR, Truyen U, Holmes EC. 88.  2005. High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc. Natl. Acad. Sci. USA 102:379–84 [Google Scholar]
  89. Li L, Cotmore SF, Tattersall P. 89.  2013. Parvoviral left-end hairpin ears are essential during infection for establishing a functional intranuclear transcription template and for efficient progeny genome encapsidation. J. Virol. 87:10501–14Demonstrates that the ears of the MVM left-end hairpin are essential for initiating transcription after cell entry. [Google Scholar]
  90. Tattersall P, Ward DC. 90.  1976. Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature 263:106–9 [Google Scholar]
  91. Ihalainen TO, Niskanen EA, Jylhävä J, Paloheimo O, Dross N. 91.  et al. 2009. Parvovirus induced alterations in nuclear architecture and dynamics. PLoS ONE 4:e5948 [Google Scholar]
  92. Ihalainen TO, Willman SF, Niskanen EA, Paloheimo O, Smolander H. 92.  et al. 2012. Distribution and dynamics of transcription-associated proteins during parvovirus infection. J. Virol. 86:13779–84 [Google Scholar]
  93. Adeyemi RO, Pintel DJ. 93.  2014. Parvovirus-induced depletion of cyclin B1 prevents mitotic entry of infected cells. PLoS Pathog. 10:e1003891 [Google Scholar]
  94. Luo Y, Deng X, Cheng F, Li Y, Qiu J. 94.  2013. SMC1-mediated intra-S-phase arrest facilitates bocavirus DNA replication. J. Virol. 87:4017–32 [Google Scholar]
  95. Luo Y, Kleiboeker S, Deng X, Qiu J. 95.  2013. Human parvovirus B19 infection causes cell cycle arrest of human erythroid progenitors at late S phase that favors viral DNA replication. J. Virol. 87:12766–75 [Google Scholar]
  96. Adeyemi RO, Landry S, Davis ME, Weitzman MD, Pintel DJ. 96.  2010. Parvovirus minute virus of mice induces a DNA damage response that facilitates viral replication. PLoS Pathog. 6:e1001141 [Google Scholar]
  97. Lou S, Luo Y, Cheng F, Huang Q, Shen W. 97.  et al. 2012. Human parvovirus B19 DNA replication induces a DNA damage response that is dispensable for cell cycle arrest at phase G2/M. J. Virol. 86:10748–58 [Google Scholar]
  98. Luo Y, Chen AY, Qiu J. 98.  2011. Bocavirus infection induces a DNA damage response that facilitates viral DNA replication and mediates cell death. J. Virol. 85:133–45 [Google Scholar]
  99. Schwartz RA, Palacios JA, Cassell GD, Adam S, Giacca M, Weitzman MD. 99.  2007. The Mre11/Rad50/Nbs1 complex limits adeno-associated virus transduction and replication. J. Virol. 81:12936–45 [Google Scholar]
  100. Lou HJ, Brister JR, Li JJ, Chen W, Muzyczka N, Tan W. 100.  2004. Adeno-associated virus Rep78/Rep68 promotes localized melting of the Rep binding element in the absence of adenosine triphosphate. ChemBioChem 5:324–32 [Google Scholar]
  101. Willwand K, Moroianu A, Horlein R, Stremmel W, Rommelaere J. 101.  2002. Specific interaction of the nonstructural protein NS1 of minute virus of mice (MVM) with [ACCA]2 motifs in the centre of the right-end MVM DNA palindrome induces hairpin-primed viral DNA replication. J. Gen. Virol. 83:1659–64 [Google Scholar]
  102. Snyder RO, Samulski RJ, Muzyczka N. 102.  1990. In vitro resolution of covalently joined AAV chromosome ends. Cell 60:105–13The first in vitro reconstruction of parvoviral origin activation by its replication initiator protein. [Google Scholar]
  103. Cotmore SF, Tattersall P. 103.  1998. High-mobility group 1/2 proteins are essential for initiating rolling-circle-type DNA replication at a parvovirus hairpin origin. J. Virol. 72:8477–84 [Google Scholar]
  104. Cotmore SF, Tattersall P. 104.  1992. In vivo resolution of circular plasmids containing concatemer junction fragments from minute virus of mice DNA and their subsequent replication as linear molecules. J. Virol. 66:420–31 [Google Scholar]
  105. Christensen J, Cotmore SF, Tattersall P. 105.  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. 75:7009–17 [Google Scholar]
  106. Li L, Cotmore SF, Tattersall P. 106.  2012. Maintenance of the flip sequence orientation of the ears in the parvoviral left-end hairpin is a nonessential consequence of the critical asymmetry in the hairpin stem. J. Virol. 86:12187–97 [Google Scholar]
  107. Nash K, Chen W, Muzyczka N. 107.  2008. Complete in vitro reconstitution of adeno-associated virus DNA replication requires the minichromosome maintenance complex proteins. J. Virol. 82:1458–64 [Google Scholar]
  108. Chapman MS, Rossmann MG. 108.  1995. Single-stranded DNA–protein interactions in canine parvovirus. Structure 3:151–62 [Google Scholar]
  109. Carrasco C, Carreira A, Schaap IAT, Serena PA, Gómez-Herrero J. 109.  et al. 2006. DNA-mediated anisotropic mechanical reinforcement of a virus. Proc. Natl. Acad. Sci. USA 103:13706–11 [Google Scholar]
  110. Carrasco C, Castellanos M, de Pablo PJ, Mateu MG. 110.  2008. Manipulation of the mechanical properties of a virus by protein engineering. Proc. Natl. Acad. Sci. USA 105:4150–55 [Google Scholar]
  111. Deng X, Yan Z, Luo Y, Xu J, Cheng F. 111.  et al. 2013. In vitro modeling of human bocavirus 1 infection of polarized primary human airway epithelia. J. Virol. 87:4097–102 [Google Scholar]
  112. Bär S, Daeffler L, Rommelaere J, Nuesch JPF. 112.  2008. Vesicular egress of non-enveloped lytic parvoviruses depends on gelsolin functioning. PLoS Pathog. 4:e1000126 [Google Scholar]
  113. Nuesch JP, Bär S, Lachmann S, Rommelaere J. 113.  2009. Ezrin-radixin-moesin family proteins are involved in parvovirus replication and spreading. J. Virol. 83:5854–63 [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085444
Loading
/content/journals/10.1146/annurev-virology-031413-085444
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error