Protoparvovirus Knocking at the Nuclear Door
Abstract
:1. Introduction
2. Cytoplasmic Transport
3. Molecular Mechanisms of Nuclear Import
3.1. Nuclear Entry of Viral DNA Genomes
3.2. Nuclear Import of Protoparvoviral Capsids
3.3. Nuclear Entry of Capsid Subunits
4. End of Import-Capsid Disassembly in the Nucleus
5. Concluding Remarks
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Cotmore, S.F.; Agbandje-McKenna, M.; Chiorini, J.A.; Mukha, D.V.; Pintel, D.J.; Qiu, J. The family Parvoviridae. Arch. Virol. 2014, 159, 1239–1247. [Google Scholar] [CrossRef] [PubMed]
- Angelova, A.L.; Geletneky, K.; Nüesch, J.P.; Rommelaere, J. Tumor selectivity of oncolytic parvoviruses: From in vitro and animal models to cancer patients. Front. Bioeng. Biotechnol. 2015, 3. [Google Scholar] [CrossRef] [PubMed]
- Marchini, A.; Bonifati, S.; Scott, E.M.; Angelova, A.L.; Rommelaere, J. Oncolytic parvoviruses: From basic virology to clinical applications. Virol. J. 2015, 12, 6. [Google Scholar] [CrossRef] [PubMed]
- Reed, A.P.; Jones, E.V.; Miller, T.J. Nucleotide sequence and genome organization of canine parvovirus. J. Virol. 1988, 62, 266–276. [Google Scholar] [PubMed]
- Xie, Q.; Chapman, M.S. Canine parvovirus capsid structure, analyzed at 2.9 Å resolution. J. Mol. Biol. 1996, 264, 497–520. [Google Scholar] [CrossRef] [PubMed]
- Cotmore, S.; Tattersal, P. 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. 2014, 79, 2287–2300. [Google Scholar] [CrossRef] [PubMed]
- Hanson, N.D.; Rhode, S.L. Parvovirus NS1 stimulates P4 expression by interaction with the terminal repeats and through DNA amplification. J. Virol. 1991, 65, 4325–4333. [Google Scholar] [PubMed]
- Tullis, G.; Schoborg, R.V.; Pintel, D.J. Characterization of the temporal accumulation of minute virus of mice replicative intermediates. J. Gen. Virol. 1994, 75, 1633–1646. [Google Scholar] [CrossRef] [PubMed]
- Cotmore, S.F.; Gottlieb, R.L.; Tattersall, P. Replication initiator protein NS1 of the parvovirus minute virus of mice binds to modular divergent sites distributed throughout duplex viral DNA. J. Virol. 2007, 81, 13015–13027. [Google Scholar] [CrossRef] [PubMed]
- Moffatt, S.; Yaegashi, N.; Tada, K.; Tanaka, N.; Sugamura, K. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J. Virol. 1998, 72, 3018–3028. [Google Scholar] [PubMed]
- Morita, E.; Nakashima, A.; Asao, H.; Sato, H.; Sugamura, K. Human parvovirus B19 nonstructural protein (NS1) induces cell cycle arrest at G(1) phase. J. Virol. 2003, 77, 2915–2921. [Google Scholar] [CrossRef] [PubMed]
- Op de Beeck, O.D.; Caillet-Fauquet, P. The NS1 protein of the autonomous parvovirus minute virus of mice blocks cellular DNA replication: A consequence of lesions to the chromatin? J. Virol. 1997, 71, 5323–5329. [Google Scholar] [PubMed]
- Nüesch, J.P.F.; Lachmann, S.; Rommelaere, J. Selective alterations of the host cell architecture upon infection with parvovirus minute virus of mice. Virology 2005, 331, 159–174. [Google Scholar] [CrossRef] [PubMed]
- Ihalainen, T.O.; Niskanen, E.A.; Jylhävä, J.; Paloheimo, O.; Dross, N.; Smolander, H.; Langowski, J.; Timonen, J.; Vihinen-Ranta, M. Parvovirus induced alterations in nuclear architecture and dynamics. PLoS ONE 2009, 4, e5948. [Google Scholar] [CrossRef] [PubMed]
- Cotmore, S.F.; Tattersall, P. High-mobility group 1/2 proteins are essential for initiating rolling-circle-type DNA replication at a parvovirus fairpin origin. J. Virol. 1998, 72, 8477–8484. [Google Scholar] [PubMed]
- Cotmore, S.F.; Tattersall, P. A genome-linked copy of the NS-1 polypeptide is located on the outside of infectious parvovirus particles. J. Virol. 1989, 63, 3902–3911. [Google Scholar] [PubMed]
- Bodendorf, U.; Cziepluch, C.; Jauniaux, J.; Rommelaere, J.; Salomé, N. Nuclear export factor CRM1 interacts with nonstructural proteins NS2 from parvovirus minute virus of mice. J. Virol. 1999, 73, 7769–7779. [Google Scholar] [PubMed]
- Miller, C.L.; Pintel, D.J. Interaction between parvovirus NS2 protein and nuclear export factor Crm1 is important for viral egress from the nucleus of murine cells. J. Virol. 2002, 76, 3257–3266. [Google Scholar] [CrossRef] [PubMed]
- López-Bueno, A.; Valle, N.; Gallego, J.M.; Pérez, J.; Almendral, J.M. Enhanced cytoplasmic sequestration of the nuclear export receptor CRM1 by NS2 mutations developed in the host regulates parvovirus fitness. J. Virol. 2004, 78, 10674–10684. [Google Scholar] [CrossRef] [PubMed]
- Engelsma, D.; Valle, N.; Fish, A.; Salomé, N.; Almendral, J.M.; Fornerod, M. A supraphysiological nuclear export signal is required for parvovirus nuclear export. Mol. Biol. Cell 2008, 19, 2544–2552. [Google Scholar] [CrossRef] [PubMed]
- Agbandje-McKenna, M.; Chapman, M.S. Correlating structure with function in the viral capsid. In Parvoviruses; Kerr, J., Cotmore, S.F., Bloom, M.E., Linden, R.M., Parrish, C.R., Eds.; CRC Press: Boca Raton, FL, USA, 2006; pp. 125–139. ISBN 9780340811986. [Google Scholar]
- Lombardo, E.; Ramírez, J.C.; Agbandje McKenna, M.; Almendral, J.M. A β-stranded motif drives capsid protein oligomers of the parvovirus minute virus of mice into the nucleus for viral assembly. J. Virol. 2000, 74, 3804–3814. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Martínez, C.; Grueso, E.; Carroll, M.; Rommelaere, J.; Almendral, J.M. Essential role of the unordered VP2 n-terminal domain of the parvovirus MVM capsid in nuclear assembly and endosomal enlargement of the virion fivefold channel for cell entry. Virology 2012, 432, 45–56. [Google Scholar] [CrossRef] [PubMed]
- Tattersall, P.; Cawte, P.J.; Shatkin, A.J.; Ward, D.C. Three structural polypeptides coded for by minite virus of mice, a parvovirus. J. Virol. 1976, 20, 273–289. [Google Scholar] [PubMed]
- Tsao, J.; Chapman, M.S.; Agbandje, M.; Keller, W.; Simth, K.; Wu, H.; Luo, M.; Smith, T.J.; Rossmann, M.G.; Compans, R.W. The three-dimensional structure of canine parvovirus and its functional implications. Science 1991, 251, 1456–1464. [Google Scholar] [CrossRef] [PubMed]
- Chapman, M.S.; Agbandje-McKenna, M. Atomic structure of viral particles. In Parvoviruses; Kerr, J., Cotmore, S.F., Bloom, M.E., Linden, R.M., Parrish, C.R., Eds.; CRC Press: Boca Raton, FL, USA, 2006; pp. 107–123. ISBN 9780340811986. [Google Scholar]
- Tullis, G.E.; Burger, L.R.; Pintel, D.J. The minor capsid protein VP1 of the autonomous parvovirus minute virus of mice is dispensable for encapsidation of progeny single-stranded DNA but is required for infectivity. J. Virol. 1993, 67, 131–141. [Google Scholar] [PubMed]
- Nelson, C.D.S.; Palermo, L.S.; Hafenstein, S.L.; Parrish, C.R. Different mechanisms of antibody-mediated neutralization of parvoviruses revealed using the Fab fragments of monoclonal antibodies. Virology 2007, 361, 283–293. [Google Scholar] [CrossRef] [PubMed]
- Vihinen-Ranta, M.; Kalela, A.; Mäkinen, P.; Kakkola, L.; Marjomäki, V.; Vuento, M. Intracellular route of canine parvovirus entry. J. Virol. 1998, 72, 802–806. [Google Scholar] [PubMed]
- Parker, J.S.L.; Parrish, C.R. Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J. Virol. 2000, 74, 1919–1930. [Google Scholar] [CrossRef] [PubMed]
- Suikkanen, S.; Sääjärvi, K.; Hirsimäki, J.; Välilehto, O.; Reunanen, H.; Vihinen-Ranta, M.; Vuento, M. Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J. Virol. 2002, 76, 4401–4411. [Google Scholar] [CrossRef] [PubMed]
- Vihinen-Ranta, M.; Suikkanen, S.; Parrish, C.R. Pathways of cell infection by parvoviruses and adeno-associated viruses. J. Virol. 2004, 78, 6709–6714. [Google Scholar] [CrossRef] [PubMed]
- Cureton, D.K.; Harbison, C.E.; Cocucci, E.; Parrish, C.R.; Kirchhausen, T. Limited transferrin receptor clustering allows rapid diffusion of canine parvovirus into clathrin endocytic structures. J. Virol. 2012, 86, 5330–5340. [Google Scholar] [CrossRef] [PubMed]
- Garcin, P.O.; Panté, N. The minute virus of mice exploits different endocytic pathways for cellular uptake. Virology 2015, 482, 157–166. [Google Scholar] [CrossRef] [PubMed]
- Sorkin, A.; von Zastrow, M. Signal transduction and endocytosis: Close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 2002, 3, 600–614. [Google Scholar] [CrossRef] [PubMed]
- Bird, P.I.; Trapani, J.A.; Villadangos, J.A. Endolysosomal proteases and their inhibitors in immunity. Nat. Rev. Immunol. 2009, 9, 871–882. [Google Scholar] [CrossRef] [PubMed]
- Luzio, J.P.; Pryor, P.R.; Bright, N.A. Lysosomes: Fusion and function. Nat. Rev. Mol. Cell Biol. 2007, 8, 622–632. [Google Scholar] [CrossRef] [PubMed]
- Golden, J.W.; Linke, J.; Schmechel, S.; Thoemke, K.; Schiff, L.A. Addition of exogenous protease facilitates reovirus infection in many restrictive cells. J. Virol. 2002, 76, 7430–7443. [Google Scholar] [CrossRef] [PubMed]
- Vihinen-Ranta, M.; Yuan, W.; Parrish, C.R. Cytoplasmic trafficking of the canine parvovirus capsid and its role in infection and nuclear transport. J. Virol. 2000, 74, 4853–4859. [Google Scholar] [CrossRef] [PubMed]
- Lux, K.; Goerlitz, N.; Schlemminger, S.; Perabo, L.; Goldnau, D.; Endell, J.; Leike, K.; Kofler, D.M.; Finke, S.; Hallek, M.; et al. Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J. Virol. 2005, 79, 11776–11787. [Google Scholar] [CrossRef] [PubMed]
- Xiao, P.; Samulski, R.J. Cytoplasmic trafficking, endosomal escape, and perinuclear accumulation of adeno-associated virus type 2 particles are facilitated by microtubule network. J. Virol. 2012, 86, 10462–10473. [Google Scholar] [CrossRef] [PubMed]
- Nicolson, S.C.; Samulski, R.J. Recombinant adeno-associated virus utilizes host cell nuclear import machinery to enter the nucleus. J. Virol. 2014, 88, 4132–4144. [Google Scholar] [CrossRef] [PubMed]
- Mäntylä, E.; Chacko, J.V.; Aho, V.; Parrish, C.R.; Shahin, V.; Kann, M.; Digman, M.A.; Gratton, E.; Vihinen-Ranta, M. Viral highway to nucleus exposed by image correlation analyses. Sci. Rep. 2017. under review. [Google Scholar]
- Rink, J.; Ghigo, E.; Kalaidzidis, Y.; Zerial, M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122, 735–749. [Google Scholar] [CrossRef] [PubMed]
- Huotari, J.; Helenius, A. Endosome maturation. EMBO J. 2011, 30, 3481–3500. [Google Scholar] [CrossRef] [PubMed]
- Foret, L.; Dawson, J.; Villaseñor, R.; Collinet, C.; Deutsch, A.; Brusch, L.; Zerial, M.; Kalaidzidis, Y.; Jülicher, F. A General theoretical framework to infer endosomal network dynamics from quantitative image analysis. Curr. Biol. 2012, 22, 1381–1390. [Google Scholar] [CrossRef] [PubMed]
- Matteoni, R.; Kreis, T.E. Translocation and clustering of endosomes and lysosomes depends on microtubules. J. Cell Biol. 1987, 105, 1253–1265. [Google Scholar] [CrossRef] [PubMed]
- Pangarkar, C.; Dinh, A.; Mitragotri, S. Endocytic pathway rapidly delivers internalized molecules to lysosomes: An analysis of vesicle trafficking, clustering and mass transfer. J. Controll. Release 2012, 162, 76–83. [Google Scholar] [CrossRef] [PubMed]
- Friedman, J.R.; DiBenedetto, J.R.; West, M.; Rowland, A.A.; Voeltz, G.K. Endoplasmic reticulum–endosome contact increases as endosomes traffic and mature. Mol. Biol. Cell 2013, 24, 1030–1040. [Google Scholar] [CrossRef] [PubMed]
- Bandyopadhyay, D.; Cyphersmith, A.; Zapata, J.A.; Kim, Y.J.; Payne, C.K. Lysosome transport as a function of lysosome diameter. PLoS ONE 2014, 9, e86847. [Google Scholar] [CrossRef] [PubMed]
- Su, Q.P.; Du, W.; Ji, Q.; Xue, B.; Jiang, D.; Zhu, Y.; Ren, H.; Zhang, C.; Lou, J.; Yu, L.; et al. Vesicle size regulates nanotube formation in the cell. Sci. Rep. 2016, 6, 24002. [Google Scholar] [CrossRef] [PubMed]
- Zádori, Z.; Szelei, J.; Lacoste, M.; Li, Y.; Gariépy, S.; Raymond, P.; Allaire, M.; Nabi, I.; Tijssen, P. A Viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell 2001, 1, 291–302. [Google Scholar] [CrossRef]
- Cudmore, S.; Cossart, P.; Griffiths, G.; Way, M. Actin-based motility of vaccinia virus. Nature 1995, 378, 636–638. [Google Scholar] [CrossRef] [PubMed]
- Ohkawa, T.; Volkman, L.E.; Welch, M.D. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol. 2010, 190, 187. [Google Scholar] [CrossRef] [PubMed]
- Sodeik, B.; Ebersold, M.W.; Helenius, A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 1997, 136, 1007–1021. [Google Scholar] [CrossRef] [PubMed]
- Brandenburg, B.; Zhuang, X. Virus trafficking-learning from single-virus tracking. Nat. Rev. Microbiol. 2007, 5, 197–208. [Google Scholar] [CrossRef] [PubMed]
- King, S.J.; Schroer, T.A. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2000, 2, 20–24. [Google Scholar] [PubMed]
- Roberts, A.J.; Kon, T.; Knight, P.J.; Sutoh, K.; Burgess, S.A. Functions and mechanics of dynein motor proteins. Nat. Rev. Mol. Cell Biol. 2013, 14, 713–726. [Google Scholar] [CrossRef] [PubMed]
- Bartlett, J.S.; Wilcher, R.; Samulski, R.J. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 2000, 74, 2777–2785. [Google Scholar] [CrossRef] [PubMed]
- Lombardo, E.; Ramírez, J.C.; Garcia, J.; Almendral, J.M. 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. 2002, 76, 7049–7059. [Google Scholar] [CrossRef] [PubMed]
- Kelkar, S.; de, B.P.; Gao, G.; Wilson, J.M.; Crystal, R.G.; Leopold, P.L. A Common mechanism for cytoplasmic dynein-dependent microtubule binding shared among adeno-associated virus and adenovirus serotypes. J. Virol. 2006, 80, 7781–7785. [Google Scholar] [CrossRef] [PubMed]
- Suikkanen, S.; Aaltonen, T.; Nevalainen, M.; Välilehto, O.; Lindholm, L.; Vuento, M.; Vihinen-Ranta, M. Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J. Virol. 2003, 77, 10270–10279. [Google Scholar] [CrossRef] [PubMed]
- Mani, B.; Baltzer, C.; Valle, N.; Almendral, J.M.; Kempf, C.; Ros, C. Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome. J. Virol. 2006, 80, 1015–1024. [Google Scholar] [CrossRef] [PubMed]
- Sonntag, F.; Bleker, S.; Leuchs, B.; Fischer, R.; Kleinschmidt, J. 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. 2006, 80, 11040–11054. [Google Scholar] [CrossRef] [PubMed]
- Bantel-Schaal, U.; Braspenning-Wesch, I.; Kartenbeck, J. Adeno-associated virus type 5 exploits two different entry pathways in human embryo fibroblasts. J. Gen. Virol. 2009, 90, 317–322. [Google Scholar] [CrossRef] [PubMed]
- Grieger, J.C.; Snowdy, S.; Samulski, R.J. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J. Virol. 2006, 80, 5199–5210. [Google Scholar] [CrossRef] [PubMed]
- Harbison, C.E.; Lyi, S.M.; Weichert, W.S.; Parrish, C.R. Early steps in cell infection by parvoviruses: Host-specific differences in cell receptor binding but similar endosomal trafficking. J. Virol. 2009, 83, 10504–10514. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Kim, Y.J.; Ji, M.; Fang, J.; Siriwon, N.; Zhang, L.I.; Wang, P. Enhancing gene delivery of adeno-associated viruses by cell-permeable peptides. Mol. Ther. Methods Clin. Dev. 2014, 1, 12. [Google Scholar] [CrossRef] [PubMed]
- Kural, C.; Kim, H.; Syed, S.; Goshima, G.; Gelfand, V.I.; Selvin, P.R. Kinesin and dynein move a peroxisome in vivo: A tug-of-war or coordinated movement? Science 2005, 308, 1469–1472. [Google Scholar] [CrossRef] [PubMed]
- Castle, M.J.; Perlson, E.; Holzbaur, E.L.F.; Wolfe, J.H. Long-distance axonal transport of AAV9 is driven by dynein and kinesin-2 and is trafficked in a highly motile Rab7-positive compartment. Mol. Ther. 2014, 22, 554–566. [Google Scholar] [CrossRef] [PubMed]
- Kartenbeck, J.; Stukenbrok, H.; Helenius, A. Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 1989, 109, 2721–2729. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Goryaynov, A.; Yang, W. Super-resolution 3D tomography of interactions and competition in the nuclear pore complex. Nat. Struct. Mol. Biol. 2016, 23, 239–247. [Google Scholar] [CrossRef] [PubMed]
- Beck, M.; Hurt, E. The nuclear pore complex: Understanding its function through structural insight. Nat. Rev. Mol. Cell Biol. 2017, 18, 73–89. [Google Scholar] [CrossRef] [PubMed]
- Alber, F.; Dokudovskaya, S.; Veenhoff, L.M.; Zhang, W.; Kipper, J.; Devos, D.; Suprapto, A.; Karni-Schmidt, O.; Williams, R.; Chait, B.T.; et al. The molecular architecture of the nuclear pore complex. Nature 2007, 450, 695–701. [Google Scholar] [CrossRef] [PubMed]
- Cardarelli, F.; Lanzano, L.; Gratton, E. Capturing directed molecular motion in the nuclear pore complex of live cells. Proc. Natl. Acad. Sci. USA 2012, 109, 9863–9868. [Google Scholar] [CrossRef] [PubMed]
- Panté, N.; Kann, M. Nuclear pore complex is able to transport macromolecules with diameters of ~39 nm. Mol. Biol. Cell 2002, 13, 425–434. [Google Scholar] [CrossRef] [PubMed]
- Strawn, L.A.; Shen, T.; Shulga, N.; Goldfarb, D.S.; Wente, S.R. Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat. Cell Biol. 2004, 6, 197–206. [Google Scholar] [CrossRef] [PubMed]
- Frey, S.; Görlich, D. A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 2007, 130, 512–523. [Google Scholar] [CrossRef] [PubMed]
- Patel, S.S.; Belmont, B.J.; Sante, J.M.; Rexach, M.F. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 2007, 129, 83–96. [Google Scholar] [CrossRef] [PubMed]
- Ghavami, A.; van der Giessen, E.; Onck, P.R. Energetics of transport through the nuclear pore complex. PLoS ONE 2016, 11, e0148876. [Google Scholar] [CrossRef] [PubMed]
- Wente, S.R.; Rout, M.P. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2010, 2, a000562. [Google Scholar] [CrossRef] [PubMed]
- Popken, P.; Ghavami, A.; Onck, P.R.; Poolman, B.; Veenhoff, L.M. Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex. Mol. Biol. Cell 2015, 26, 1386–1394. [Google Scholar] [CrossRef] [PubMed]
- Stewart, M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 2007, 8, 195–208. [Google Scholar] [CrossRef] [PubMed]
- Yang, W.; Gelles, J.; Musser, S.M. Imaging of single-molecule translocation through nuclear pore complexes. Proc. Natl. Acad. Sci. USA 2004, 101, 12887–12892. [Google Scholar] [CrossRef] [PubMed]
- Ribbeck, K.; Görlich, D. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 2001, 20, 1320–1330. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Segura, L.M.; Lafarga, M.; Berciano, M.T.; Hernandez, P.; Andres, M.A. Distribution of nuclear pores and chromatin organization in neurons and glial cells of the rat cerebellar cortex. J. Comp. Neurol. 1989, 290, 440–450. [Google Scholar] [CrossRef] [PubMed]
- Goldfarb, D.S.; Gariepy, J.; Schoolnik, G.; Kornberg, R.D. Synthetic peptides as nuclear localization signals. Nature 1986, 322, 641–644. [Google Scholar] [CrossRef] [PubMed]
- Ström, A.; Weiss, K. Importin-β-like nuclear transport receptors. Genome Biol. 2001, 2, reviews3008.1–reviews3008.9. [Google Scholar]
- Jans, D.A.; Ackermann, M.J.; Bischoff, J.R.; Beach, D.H.; Peters, R. p34cdc2-mediated phosphorylation at T124 inhibits nuclear import of SV-40 T antigen proteins. J. Cell Biol. 1991, 115, 1203–1212. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.C.; Brown, K.; Siebenlist, U. Activation of NF-κB requires proteolysis of the inhibitor I κB-α: Signal-induced phosphorylation of I κB-α alone does not release active NF-κB. Proc. Natl. Acad. Sci. USA 1995, 92, 552–556. [Google Scholar] [CrossRef] [PubMed]
- Christie, M.; Chang, C.; Róna, G.; Smith, K.M.; Stewart, A.G.; Takeda, A.A.S.; Fontes, M.R.M.; Stewart, M.; Vértessy, B.G.; Forwood, J.K.; et al. Structural biology and regulation of protein import into the nucleus. J. Mol. Biol. 2016, 428, 2060–2090. [Google Scholar] [CrossRef] [PubMed]
- Rexach, M.; Blobel, G. Protein import into nuclei: Association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 1995, 83, 683–692. [Google Scholar] [CrossRef]
- Stewart, M.; Rhodes, D. Switching affinities in nuclear trafficking. Nat. Struct. Mol. Biol. 1999, 6, 301–304. [Google Scholar] [CrossRef] [PubMed]
- Rux, J.J.; Burnett, R.M. Type-specific epitope locations revealed by X-ray crystallographic study of adenovirus type 5 hexon. Mol. Ther. 2000, 1, 18–30. [Google Scholar] [CrossRef] [PubMed]
- Trotman, L.C.; Mosberger, N.; Fornerod, M.; Stidwill, R.P.; Greber, U.F. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 2001, 3, 1092–1100. [Google Scholar] [CrossRef] [PubMed]
- Greber, U.F.; Willetts, M.; Webster, P.; Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75, 477–486. [Google Scholar] [CrossRef] [Green Version]
- Strunze, S.; Engelke, M.F.; Wang, I.H.; Puntener, D.; Boucke, K.; Schleich, S.; Way, M.; Schoenenberger, P.; Burckhardt, C.J.; Greber, U.F. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 2011, 10, 210–223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Saphire, A.C.S.; Guan, T.; Schirmer, E.C.; Nemerow, G.R.; Gerace, L. Nuclear import of adenovirus DNA in vitro involves the nuclear protein import pathway and HSC70. J. Biol. Chem. 2000, 275, 4298–4304. [Google Scholar] [CrossRef] [PubMed]
- Hindley, C.E.; Lawrence, F.J.; Matthews, D.A. A role for transportin in the nuclear import of adenovirus core proteins and DNA. Traffic 2007, 8, 1313–1322. [Google Scholar] [CrossRef] [PubMed]
- Ojala, P.M.; Sodeik, B.; Ebersold, M.W.; Kutay, U.; Helenius, A. Herpes simplex virus type 1 entry into host cells: Reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol. Cell. Biol. 2000, 20, 4922–4931. [Google Scholar] [CrossRef] [PubMed]
- Copeland, A.M.; Newcomb, W.W.; Brown, J.C. Herpes simplex virus replication: Roles of viral proteins and nucleoporins in capsid-nucleus attachment. J. Virol. 2009, 83, 1660–1668. [Google Scholar] [CrossRef] [PubMed]
- Pasdeloup, D.; Blondel, D.; Isidro, A.L.; Rixon, F.J. Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J. Virol. 2009, 83, 6610–6623. [Google Scholar] [CrossRef] [PubMed]
- Rout, M.P.; Aitchison, J.D.; Suprapto, A.; Hjertaas, K.; Zhao, Y.; Chait, B.T. The yeast nuclear pore complex. J. Cell Biol. 2000, 148, 635–652. [Google Scholar] [CrossRef] [PubMed]
- Booy, F.P.; Newcomb, W.W.; Trus, B.L.; Brown, J.C.; Baker, T.S.; Steven, A.C. Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 1991, 64, 1007–1015. [Google Scholar] [CrossRef]
- Newcomb, W.W.; Cockrell, S.K.; Homa, F.L.; Brown, J.C. Polarized DNA ejection from the herpesvirus capsid. J. Mol. Biol. 2009, 392, 885–894. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Tikoo, S.K.; Babiuk, L.A. Nuclear localization of the ORF2 protein encoded by porcine circovirus type 2. Virology 2001, 285, 91–99. [Google Scholar] [CrossRef] [PubMed]
- Kann, M.; Sodeik, B.; Vlachou, A.; Gerlich, W.H.; Helenius, A. Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex. J. Cell Biol. 1999, 145, 45–55. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.; Wang, J.C.; Pierson, E.E.; Keifer, D.Z.; Delaleau, M.; Gallucci, L.; Cazenave, C.; Kann, M.; Jarrold, M.F.; Zlotnick, A. Importin β can bind hepatitis B virus core protein and empty core-like particles and induce structural changes. PLoS Pathog. 2016, 12, e1005802. [Google Scholar] [CrossRef] [PubMed]
- Schmitz, A.; Schwarz, A.; Foss, M.; Zhou, L.; Rabe, B.; Hoellenriegel, J.; Stoeber, M.; Panté, N.; Kann, M. Nucleoporin 153 arrests the nuclear import of hepatitis B virus capsids in the nuclear basket. PLoS Pathog. 2010, 6, e1000741. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.; Chen, S.; Wang, M.; Cheng, A. The role of nuclear localization signal in parvovirus life cycle. Virol. J. 2017, 14, 80. [Google Scholar] [CrossRef] [PubMed]
- Vihinen-Ranta, M.; Kakkola, L.; Kalela, A.; Vilja, P.; Vuento, M. Characterization of a nuclear localization signal of canine parvovirus capsid proteins. Eur. J. Biochem. 1997, 250, 389–394. [Google Scholar] [CrossRef] [PubMed]
- Vihinen-Ranta, M.; Wang, D.; Weichert, W.S.; Parrish, C.R. The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J. Virol. 2002, 76, 1884–1891. [Google Scholar] [CrossRef] [PubMed]
- Mäntylä, E.; Vihinen-Ranta, M. Analysis of human parvovirus capsid protein NLSs. unpublished.
- Seisenberger, G.; Ried, M.U.; Endress, T.; Büning, H.; Hallek, M.; Bräuchle, C. Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 2001, 294, 1929–1932. [Google Scholar] [CrossRef] [PubMed]
- Porwal, M.; Cohen, S.; Snoussi, K.; Popa-Wagner, R.; Anderson, F.; Dugot-Senant, N.; Wodrich, H.; Dinsart, C.; Kleinschmidt, J.A.; Panté, N.; et al. Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLoS Pathog. 2013, 9. [Google Scholar] [CrossRef] [PubMed]
- Cohen, S.; Panté, N. Pushing the envelope: Microinjection of Minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope. J. Gen. Virol. 2005, 86, 3243–3252. [Google Scholar] [CrossRef] [PubMed]
- Cohen, S.; Marr, A.K.; Garcin, P.; Panté, N. Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle. J. Virol. 2011, 85, 4863–4874. [Google Scholar] [CrossRef] [PubMed]
- Popa-Wagner, R.; Porwal, M.; Kann, M.; Reuss, M.; Weimer, M.; Florin, L.; Kleinschmidt, J.A. Impact of VP1-specific protein sequence motifs on adeno-associated virus type 2 Intracellular trafficking and nuclear entry. J. Virol. 2012, 86, 9163–9174. [Google Scholar] [CrossRef] [PubMed]
- Gil-Ranedo, J.; Hernando, E.; Riolobos, L.; Domínguez, C.; Kann, M.; Almendral, J.M. The mammalian cell cycle regulates parvovirus nuclear capsid assembly. PLoS Pathog. 2015, 11, e1004920105. [Google Scholar] [CrossRef] [PubMed]
- Riolobos, L.; Valle, N.; Hernando, E.; Maroto, B.; Kann, M.; Almendral, J.M. Viral oncolysis that targets Raf-1 signaling control of nuclear transport. J. Virol. 2010, 84, 2090–2099. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, Q.; Bu, W.; Bhatia, S.; Hare, J.; Somasundaram, T.; Azzi, A. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc. Natl. Acad. Sci. USA 2002, 99, 10405–10410. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.S.; Ponnazhagan, S.; Srivastava, A. Rescue and replication of adeno-associated virus type 2 as well as vector DNA sequences from recombinant plasmids containing deletions in the viral inverted terminal repeats: Selective encapsidation of viral genomes in progeny virions. J. Virol. 1996, 70, 1668–1677. [Google Scholar] [PubMed]
- Ben-Asher, E.; Bratosin, S.; Aloni, Y. Intracellular DNA of the parvovirus minute virus of mice is organized in a minichromosome structure. J. Virol. 1982, 41, 1044–1054. [Google Scholar] [PubMed]
- Marcus-Sekura, C.; Carter, B.J. Chromatin-like structure of adeno-associated virus DNA in infected cells. J. Virol. 1983, 48, 79–87. [Google Scholar] [PubMed]
- Penaud-Budloo, M.; Le Guiner, C.; Nowrouzi, A.; Toromanoff, A.; Chérel, Y.; Chenuaud, P.; Schmidt, M.; von Kalle, C.; Rolling, F.; Moullier, P.; et al. Adeno-associated virus vector genomes persist as episomal chromatin in primate muscle. J. Virol. 2008, 82, 7875–7885. [Google Scholar] [CrossRef] [PubMed]
- Mäntylä, E.; Salokas, K.; Oittinen, M.; Aho, V.; Mäntysaari, P.; Palmujoki, L.; Kalliolinna, O.; Ihalainen, T.O.; Niskanen, E.A.; Timonen, J.; et al. Promoter-targeted histone acetylation of chromatinized parvoviral genome is essential for the progress of infection. J. Virol. 2016, 90, 4059–4066. [Google Scholar] [CrossRef] [PubMed]
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mäntylä, E.; Kann, M.; Vihinen-Ranta, M. Protoparvovirus Knocking at the Nuclear Door. Viruses 2017, 9, 286. https://doi.org/10.3390/v9100286
Mäntylä E, Kann M, Vihinen-Ranta M. Protoparvovirus Knocking at the Nuclear Door. Viruses. 2017; 9(10):286. https://doi.org/10.3390/v9100286
Chicago/Turabian StyleMäntylä, Elina, Michael Kann, and Maija Vihinen-Ranta. 2017. "Protoparvovirus Knocking at the Nuclear Door" Viruses 9, no. 10: 286. https://doi.org/10.3390/v9100286