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Structures and Functions of Parvovirus Capsids and the Process of Cell Infection

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Cell Entry by Non-Enveloped Viruses

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 343))

Abstract

To infect a cell, the parvovirus or adeno-associated virus (AAV) genome must be delivered from outside the plasma membrane to the nucleus, and in the process, the capsid must follow a series of binding and trafficking steps and also undergo necessary changes that result in exposure or release the ssDNA genome at the appropriate time and place within the cell. The 25 nm parvovirus capsid is comprised of two or three forms of a single protein, and although it is robust and stable, it is still sufficiently flexible to allow the exposure of several internal components at appropriate times during cell infection. The capsid can also accommodate insertion of peptides into surface loops, and capsid proteins from different viral serotypes can be shuffled to create novel functional variants. The capsids of the different viruses bind to one or more cell receptors, and for at least some viruses, the insertion of additional or alternative receptor binding sequences or structures into the capsid can expand or redirect its tropism. The infection process after cell binding involves receptor-mediated endocytosis followed by viral trafficking through the endosomal systems. That endosomal trafficking may be complex and prolonged for hours or be relatively brief. Generally only a small proportion of the particles taken up enter the cytoplasm after altering the endosomal membrane through the activity of a VP1-encoded phospholipase A2 domain that becomes released to the outside of the viral particle. Modifications to the capsid that can occur within the endosome or cytoplasm include structural changes to expose internal components, ubiquination and proteosomal processing, and possible trafficking of particles on molecular motors. It is still not clear how the genomes enter the nucleus, but nuclear pore-dependent entry of particles or permeabilization of nuclear membranes have been proposed. Those processes control the infection, pathogenesis, and host ranges of the autonomous viruses and determine the effectiveness of gene therapy using AAV capsids.

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References

  • Aasted B, Race RE, Bloom ME (1984) Aleutian disease virus, a parvovirus, is proteolytically degraded during in vivo infection in mink. J Virol 51:7–13

    CAS  PubMed  Google Scholar 

  • Akache B, Grimm D, Shen X, Fuess S, Yant SR, Glazer DS, Park J, Kay MA (2007) A two-hybrid screen identifies cathepsins B and L as uncoating factors for adeno-associated virus 2 and 8. Mol Ther 15:330–339

    Article  CAS  PubMed  Google Scholar 

  • Bantel-Schaal U, Hub B, Kartenbeck J (2002) Endocytosis of adeno-associated virus type 5 leads to accumulation of virus particles in the Golgi compartment. J Virol 76:2340–2349

    Article  CAS  PubMed  Google Scholar 

  • Bar S, Daeffler L, Rommelaere J, Nuesch JP (2008) Vesicular egress of non-enveloped lytic parvoviruses depends on gelsolin functioning. PLoS Pathog 4:e1000126

    Article  PubMed  CAS  Google Scholar 

  • Barbis DP, Chang S-F, Parrish CR (1992) Mutations adjacent to the dimple of canine parvovirus capsid structure affect sialic acid binding. Virology 191:301–308

    Article  CAS  PubMed  Google Scholar 

  • Bartlett JS, Wilcher R, Samulski RJ (2000) Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J Virol 74:2777–2785

    Article  CAS  PubMed  Google Scholar 

  • Bleker S, Sonntag F, Kleinschmidt JA (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 79:2528–2540

    Article  CAS  PubMed  Google Scholar 

  • Boschetti N, Niederhauser I, Kempf C, Stuhler A, Lower J, Blumel J (2004) Different susceptibility of B19 virus and mice minute virus to low pH treatment. Transfusion 44:1079–1086

    Article  CAS  PubMed  Google Scholar 

  • Bruemmer A, Scholari F, Lopez-Ferber M, Conway JF, Hewat EA (2005) Structure of an insect parvovirus (Junonia coenia Densovirus) determined by cryo-electron microscopy. J Mol Biol 347:791–801

    Article  CAS  PubMed  Google Scholar 

  • Brument N, Morenweiser R, Blouin V, Toublanc E, Raimbaud I, Cherel Y, Folliot S, Gaden F, Boulanger P, Kroner-Lux G, Moullier P, Rolling F, Salvetti A (2002) A versatile and scalable two-step ion-exchange chromatography process for the purification of recombinant adeno-associated virus serotypes-2 and -5. Mol Ther 6:678–686

    Article  CAS  PubMed  Google Scholar 

  • Chapman MS (1998) Watching one’s P’s and Q’s: promiscuity, plasticity, and quasiequivalence in a T = 1 virus. Biophys J 74:639–644

    Article  CAS  PubMed  Google Scholar 

  • Chapman MS, Rossmann MG (1993) Structure, sequence, and function correlations among parvoviruses. Virology 194:491–508

    Article  CAS  PubMed  Google Scholar 

  • Chapman MS, Rossmann MG (1995) Single-stranded DNA-protein interactions in canine parvovirus. Structure 3:151–162

    Article  CAS  PubMed  Google Scholar 

  • Clinton G, Hayashi M (1976) The parvovirus MVM: a comparison of heavy and light particle infectivity and their density conversion in vitro. Virology 74:57–63

    Article  CAS  PubMed  Google Scholar 

  • Cohen S, Pante N (2005) Pushing the envelope: microinjection of Minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope. J Gen Virol 86:3243–3252

    Article  CAS  PubMed  Google Scholar 

  • Cohen S, Behzad AR, Carroll JB, Pante N (2006) Parvoviral nuclear import: bypassing the host nuclear-transport machinery. J Gen Virol 87:3209–3213

    Article  CAS  PubMed  Google Scholar 

  • Cotmore SF, Tattersall P (1989) A genome-linked copy of the NS-1 polypeptide is located on the outside of infectious parvovirus particles. J Virol 63:3902–3911

    CAS  PubMed  Google Scholar 

  • Cotmore SF, Tattersall P (2005) Encapsidation of minute virus of mice DNA: aspects of the translocation mechanism revealed by the structure of partially packaged genomes. Virology 336:100–112

    Article  CAS  PubMed  Google Scholar 

  • Cotmore SF, D'Abramo AM, Ticknor CM, Tattersall P (1999) Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 254:169–181

    Article  CAS  PubMed  Google Scholar 

  • Cotmore SF, Hafenstein S, Tattersall P (2009) Depletion of virion-associated divalent cations induces Parvovirus Minute Virus of Mice (MVM) to eject its genome in a 3′-to-5′ direction from otherwise intact viral particles. J Virol. doi:10.1128/JVI.01563-09

    PubMed  Google Scholar 

  • Coura Rdos S, Nardi NB (2007) The state of the art of adeno-associated virus-based vectors in gene therapy. Virol J 4:99

    Article  PubMed  CAS  Google Scholar 

  • Ding W, Zhang L, Yan Z, Engelhardt JF (2005) Intracellular trafficking of adeno-associated viral vectors. Gene Ther 12:873–880

    Article  CAS  PubMed  Google Scholar 

  • Ding W, Zhang LN, Yeaman C, Engelhardt JF (2006) rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol Ther 13(4):671–682

    Article  CAS  PubMed  Google Scholar 

  • Duan D, Yue Y, Yan Z, McCray PB, Engelhardt JF (1998) Polarity influences the efficiency of recombinant adenoassociated virus infection in differentiated airway epithelia. Hum Gene Ther 9:2761–2776

    Article  CAS  PubMed  Google Scholar 

  • Duan D, Li Q, Kao AW, Yue Y, Pessin JE, Engelhardt JF (1999) Dynamin is required for recombinant adeno-associated virus type 2 infection. J Virol 73:10371–10376

    CAS  PubMed  Google Scholar 

  • Farr GA, Tattersall P (2004) A conserved leucine that constricts the pore through the capsid fivefold cylinder plays a central role in parvoviral infection. Virology 323:243–256

    Article  CAS  PubMed  Google Scholar 

  • Farr GA, Zhang LG, Tattersall P (2005) Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc Natl Acad Sci USA 102:17148–17153

    Article  CAS  PubMed  Google Scholar 

  • Farr GA, Cotmore SF, Tattersall P (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 80:161–171

    Article  CAS  PubMed  Google Scholar 

  • Feldherr CM, Akin D (1990) The permeability of the nuclear envelope in dividing and nondividing cell cultures. J Cell Biol 111:1–8

    Article  CAS  PubMed  Google Scholar 

  • Girod A, Ried M, Wobus C, Lahm H, Leike K, Kleinschmidt J, Deleage G, Hallek M (1999) Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2. Nat Med 5:1052–1056

    Article  CAS  PubMed  Google Scholar 

  • Girod A, Wobus CE, Zadori Z, Ried M, Leike K, Tijssen P, Kleinschmidt JA, Hallek M (2002) The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J Gen Virol 83:973–978

    CAS  PubMed  Google Scholar 

  • Govindasamy L, Hueffer K, Parrish CR, Agbandje-McKenna M (2003) Structures of host range-controlling regions of the capsids of canine and feline parvoviruses and mutants. J Virol 77:12211–12221

    Article  CAS  PubMed  Google Scholar 

  • Grieger JC, Samulski RJ (2005) Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and postentry steps. J Virol 79:9933–9944

    Article  CAS  PubMed  Google Scholar 

  • Grieger JC, Snowdy S, Samulski RJ (2006) Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J Virol 80:5199–5210

    Article  CAS  PubMed  Google Scholar 

  • Grieger JC, Johnson JS, Gurda-Whitaker B, Agbandje-McKenna M, Samulski RJ (2007) Surface exposed Adeno-associated virus Vp1-NLS capsid fusion protein rescues infectivity of non-infectious wild-type Vp2/Vp3 and Vp3-only capsids, but not 5-fold pore mutant virions. J Virol 81:7833–7843

    Article  CAS  PubMed  Google Scholar 

  • Grifman M, Trepel M, Speece P, Gilbert LB, Arap W, Pasqualini R, Weitzman MD (2001) Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol Ther 3:964–975

    Article  CAS  PubMed  Google Scholar 

  • Grimm D, Lee JS, Wang L, Desai T, Akache B, Storm TA, Kay MA (2008) In vitro and in vivo gene therapy vector evolution via multispecies interbreeding and retargeting of adeno-associated viruses. J Virol 82:5887–5911

    Article  CAS  PubMed  Google Scholar 

  • Hafenstein S, Palermo LM, Kostyuchenko VA, Xiao C, Morais MC, Nelson CD, Bowman VD, Battisti AJ, Chipman PR, Parrish CR, Rossmann MG (2007) Asymmetric binding of transferrin receptor to parvovirus capsids. Proc Natl Acad Sci USA 104:6585–6589

    Article  CAS  PubMed  Google Scholar 

  • Hafenstein S, Bowman VD, Sun T, Nelson CD, Palermo LM, Chipman PR, Battisti AJ, Parrish CR, Rossmann MG (2009) Structural comparison of different antibodies interacting with parvovirus capsids. J Virol 83:5556–5566

    Article  CAS  PubMed  Google Scholar 

  • Hansen J, Qing K, Srivastava A (2001) Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J Virol 75:4080–4090

    Article  CAS  PubMed  Google Scholar 

  • Harbison CE, Lyi SM, Weichert WS, Parrish CR (2009) Early steps in cell infection by parvoviruses: host-specific differences in cell receptor binding but similar endosomal trafficking. J Virol 83:10504–10514

    Article  CAS  PubMed  Google Scholar 

  • Hirosue S, Senn K, Clement N, Nonnenmacher M, Gigout L, Linden RM, Weber T (2007) Effect of inhibition of dynein function and microtubule-altering drugs on AAV2 transduction. Virology 367:110–118

    Article  CAS  Google Scholar 

  • Hueffer K, Govindasamy L, Agbandje-McKenna M, Parrish CR (2003a) Combinations of two capsid regions controlling canine host range determine canine transferrin receptor binding by canine and feline parvoviruses. J Virol 77:10099–10105

    Article  CAS  PubMed  Google Scholar 

  • Hueffer K, Parker JS, Weichert WS, Geisel RE, Sgro JY, Parrish CR (2003b) The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J Virol 77:1718–1726

    Article  CAS  PubMed  Google Scholar 

  • Hueffer K, Palermo LM, Parrish CR (2004) Parvovirus infection of cells by using variants of the feline transferrin receptor altering clathrin-mediated endocytosis, membrane domain localization, and capsid-binding domains. J Virol 78:5601–5611

    Article  CAS  PubMed  Google Scholar 

  • James JA, Escalante CR, Yoon-Robarts M, Edwards TA, Linden RM, Aggarwal AK (2003) Crystal structure of the SF3 helicase from adeno-associated virus type 2. Structure 11:1025–1035

    Article  CAS  PubMed  Google Scholar 

  • Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA (2001) Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J Virol 75:6884–6893

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann B, Lopez-Bueno A, Mateu MG, Chipman PR, Nelson CD, Parrish CR, Almendral JM, Rossmann MG (2007) Minute virus of mice, a parvovirus, in complex with the Fab fragment of a neutralizing monoclonal antibody. J Virol 81:9851–9858

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann B, Chipman PR, Kostyuchenko VA, Modrow S, Rossmann MG (2008) Visualization of the externalized VP2 N termini of infectious human parvovirus B19. J Virol 82:7306–7312

    Article  CAS  PubMed  Google Scholar 

  • Kelkar S, De BP, Gao G, Wilson JM, Crystal RG, Leopold PL (2006) A common mechanism for cytoplasmic dynein-dependent microtubule binding shared among adeno-associated virus and adenovirus serotypes. J Virol 80:7781–7785

    Article  CAS  PubMed  Google Scholar 

  • Kestler J, Neeb B, Struyf S, Van Damme J, Cotmore SF, D'Abramo A, Tattersall P, Rommelaere J, Dinsart C, Cornelis JJ (1999) cis requirements for the efficient production of recombinant DNA vectors based on autonomous parvoviruses. Hum Gene Ther 10:1619–1632

    Article  CAS  PubMed  Google Scholar 

  • Kontou M, Govindasamy L, Nam HJ, Bryant N, Llamas-Saiz AL, Foces-Foces C, Hernando E, Rubio MP, McKenna R, Almendral JM, Agbandje-McKenna M (2005) Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice. J Virol 79:10931–10943

    Article  CAS  PubMed  Google Scholar 

  • Kronenberg S, Bottcher B, von der Lieth CW, Bleker S, Kleinschmidt JA (2005) A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J Virol 79:5296–5303

    Article  CAS  PubMed  Google Scholar 

  • Lang SI, Boelz S, Stroh-Dege AY, Rommelaere J, Dinsart C, Cornelis JJ (2005) The infectivity and lytic activity of minute virus of mice wild-type and derived vector particles are strikingly different. J Virol 79:289–298

    Article  CAS  PubMed  Google Scholar 

  • Levy HC, Bowman VD, Govindasamy L, McKenna R, Nash K, Warrington K, Chen W, Muzyczka N, Yan X, Baker TS, Agbandje-McKenna M (2009) Heparin binding induces conformational changes in Adeno-associated virus serotype 2. J Struct Biol 165:146–156

    Article  CAS  PubMed  Google Scholar 

  • Li W, Asokan A, Wu Z, Van Dyke T, DiPrimio N, Johnson JS, Govindaswamy L, Agbandje-McKenna M, Leichtle S, Redmond DE, McCown TJ, Petermann KB, Sharpless NE, Samulski RJ (2008) Engineering and selection of shuffled AAV genomes: a new strategy for producing targeted biological nanoparticles. Mol Ther 16:1252–1260

    Article  CAS  PubMed  Google Scholar 

  • Linser P, Bruning H, Armentrout RW (1977) Specific binding sites for a parvovirus, minute virus of mice, on cultured mouse cells. J Virol 41:211–221

    Google Scholar 

  • Lochrie MA, Tatsuno GP, Christie B, McDonnell JW, Zhou S, Surosky R, Pierce GF, Colosi P (2006) Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J Virol 80:821–834

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bueno A, Rubio MP, Bryant N, McKenna R, Agbandje-McKenna M, Almendral JM (2006) Host-selected amino acid changes at the sialic acid binding pocket of the parvovirus capsid modulate cell binding affinity and determine virulence. J Virol 80:1563–1573

    Article  CAS  PubMed  Google Scholar 

  • Lux K, Goerlitz N, Schlemminger S, Perabo L, Goldnau D, Endell J, Leike K, Kofler DM, Finke S, Hallek M, Buning H (2005) Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J Virol 79:11776–11787

    Article  CAS  PubMed  Google Scholar 

  • Mani B, Baltzer C, Valle N, Almendral JM, Kempf C, Ros C (2006) 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 80:1015–1024

    Article  CAS  PubMed  Google Scholar 

  • Mani B, Gerber M, Lieby P, Boschetti N, Kempf C, Ros C (2007) Molecular mechanism underlying B19 virus inactivation and comparison to other parvoviruses. Transfusion 47:1765–1774

    Article  CAS  PubMed  Google Scholar 

  • Mansilla-Soto J, Yoon-Robarts M, Rice WJ, Arya S, Escalante CR, Linden RM (2009) DNA structure modulates the oligomerization properties of the AAV initiator protein Rep68. PLoS Pathog 5:e1000513

    Article  PubMed  CAS  Google Scholar 

  • Maroto B, Valle N, Saffrich R, Almendral JM (2004) Nuclear export of the nonenveloped parvovirus virion is directed by an unordered protein signal exposed on the capsid surface. J Virol 78:10685–10694

    Article  CAS  PubMed  Google Scholar 

  • Marsh M, Helenius A (2006) Virus entry: open sesame. Cell 124:729–740

    Article  CAS  PubMed  Google Scholar 

  • Maxwell IH, Chapman JT, Scherrer LC, Spitzer AL, Leptihn S, Maxwell F, Corsini JA (2001) Expansion of tropism of a feline parvovirus to target a human tumor cell line by display of an alpha(v) integrin binding peptide on the capsid. Gene Ther 8:324–331

    Article  CAS  PubMed  Google Scholar 

  • Michelfelder S, Lee MK, deLima-Hahn E, Wilmes T, Kaul F, Muller O, Kleinschmidt JA, Trepel M (2007) Vectors selected from adeno-associated viral display peptide libraries for leukemia cell-targeted cytotoxic gene therapy. Exp Hematol 35:1766–1776

    Article  CAS  PubMed  Google Scholar 

  • Mueller C, Flotte TR (2008) Clinical gene therapy using recombinant adeno-associated virus vectors. Gene Ther 15:858–863

    Article  CAS  PubMed  Google Scholar 

  • Muller OJ, Kaul F, Weitzman MD, Pasqualini R, Arap W, Kleinschmidt JA, Trepel M (2003) Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat Biotechnol 21:1040–1046

    Article  PubMed  CAS  Google Scholar 

  • Nelson CD, Palermo LM, Hafenstein SL, Parrish CR (2007) Different mechanisms of antibody-mediated neutralization of parvoviruses revealed using the Fab fragments of monoclonal antibodies. Virology 361:283–293

    Article  CAS  PubMed  Google Scholar 

  • Nelson CD, Minkkinen E, Bergkvist M, Hoelzer K, Fisher M, Bothner B, Parrish CR (2008) Detecting small changes and additional peptides in the canine parvovirus capsid structure. J Virol 82:10397–10407

    Article  CAS  PubMed  Google Scholar 

  • O'Donnell J, Taylor KA, Chapman MS (2009) Adeno-associated virus-2 and its primary cellular receptor–Cryo-EM structure of a heparin complex. Virology 385:434–443

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Nonaka-Sarukawa M, Uchibori R, Kinoshita K, Hayashita-Kinoh H, Nitahara-Kasahara Y, Takeda S, Ozawa K (2009) Scalable Purification of Adeno-associated Virus Serotype 1 (AAV1) and AAV8 Vectors, Using Dual Ion-Exchange Adsorptive Membranes. Hum Gene Ther 20:1013–1021

    Article  CAS  PubMed  Google Scholar 

  • Pakkanen K, Karttunen J, Virtanen S, Vuento M (2008) Sphingomyelin induces structural alteration in canine parvovirus capsid. Virus Res 132:187–191

    Article  CAS  PubMed  Google Scholar 

  • Palermo LM, Hueffer K, Parrish CR (2003) Residues in the apical domain of the feline and canine transferrin receptors control host-specific binding and cell infection of canine and feline parvoviruses. J Virol 77:8915–8923

    Article  CAS  PubMed  Google Scholar 

  • Palermo LM, Hafenstein SL, Parrish CR (2006) Purified feline and canine transferrin receptors reveal complex interactions with the capsids of canine and feline parvoviruses that correspond to their host ranges. J Virol 80:8482–8492

    Article  CAS  PubMed  Google Scholar 

  • Pante N, Kann M (2002) Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol Biol Cell 13:425–434

    Article  CAS  PubMed  Google Scholar 

  • Parker JS, Parrish CR (2000) Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J Virol 74:1919–1930

    Article  CAS  PubMed  Google Scholar 

  • 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 75:3896–3902

    Article  CAS  PubMed  Google Scholar 

  • Pasquale GD, Davidson BL, Stein CS, Martins I, Scudiero D, Monks A, Chiorini JA (2003) Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med 9:1306–1312

    Article  PubMed  CAS  Google Scholar 

  • Prasad KM, Trempe JP (1995) The adeno-associated virus Rep78 protein is covalently linked to viral DNA in a preformed virion. Virology 214:360–370

    Article  CAS  PubMed  Google Scholar 

  • Qu G, Bahr-Davidson J, Prado J, Tai A, Cataniag F, McDonnell J, Zhou J, Hauck B, Luna J, Sommer JM, Smith P, Zhou S, Colosi P, High KA, Pierce GF, Wright JF (2007) Separation of adeno-associated virus type 2 empty particles from genome containing vectors by anion-exchange column chromatography. J Virol Methods 140:183–192

    Article  CAS  PubMed  Google Scholar 

  • Rabinowitz JE, Bowles DE, Faust SM, Ledford JG, Cunningham SE, Samulski RJ (2004) Cross-dressing the virion: the transcapsidation of adeno-associated virus serotypes functionally defines subgroups. J Virol 78:4421–4432

    Article  CAS  PubMed  Google Scholar 

  • Reguera J, Carreira A, Riolobos L, Almendral JM, Mateu MG (2004) Role of interfacial amino acid residues in assembly, stability, and conformation of a spherical virus capsid. Proc Natl Acad Sci USA 101:2724–2729

    Article  CAS  PubMed  Google Scholar 

  • Ried MU, Girod A, Leike K, Buning H, Hallek M (2002) Adeno-associated virus capsids displaying immunoglobulin-binding domains permit antibody-mediated vector retargeting to specific cell surface receptors. J Virol 76:4559–4566

    Article  CAS  PubMed  Google Scholar 

  • 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 357:1026–1038

    Article  CAS  PubMed  Google Scholar 

  • Ros C, Kempf C (2004) The ubiquitin-proteasome machinery is essential for nuclear translocation of incoming minute virus of mice. Virology 324:350–360

    Article  CAS  PubMed  Google Scholar 

  • Ros C, Burckhardt CJ, Kempf C (2002) Cytoplasmic trafficking of minute virus of mice: low-pH requirement, routing to late endosomes, and proteasome interaction. J Virol 76:12634–12645

    Article  CAS  PubMed  Google Scholar 

  • Ros C, Gerber M, Kempf C (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 80:12017–12024

    Article  CAS  PubMed  Google Scholar 

  • Rosenfeld SJ, Yoshimoto K, Kajigaya S, Anderson S, Young NS, Field A, Warrener P, Bansal G, Collett MS (1992) Unique region of the minor capsid protein of human parvovirus B19 is exposed on the virion surface. J Clin Invest 89:2023–2029

    Article  CAS  PubMed  Google Scholar 

  • Saikawa T, Anderson S, Momoeda M, Kajigaya S, Young NS (1993) Neutralizing linear epitopes of B19 parvovirus cluster in the VP1 unique and VP1-VP2 junction regions. J Virol 67:3004–3009

    CAS  PubMed  Google Scholar 

  • Sanlioglu S, Benson PK, Yang J, Atkinson EM, Reynolds T, Engelhardt JF (2000) Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J Virol 74:9184–9196

    Article  CAS  PubMed  Google Scholar 

  • Seisenberger G, Ried MU, Endress T, Buning H, Hallek M, Brauchle C (2001) Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294:1929–1932

    Article  CAS  PubMed  Google Scholar 

  • Shi W, Arnold GS, Bartlett JS (2001) Insertional mutagenesis of the adeno-associated virus type 2 (aav2) capsid gene and generation of aav2 vectors targeted to alternative cell-surface receptors. Hum Gene Ther 12:1697–1711

    Article  CAS  PubMed  Google Scholar 

  • Shi X, Fang G, Shi W, Bartlett JS (2006) Insertional mutagenesis at positions 520 and 584 of adeno-associated virus type 2 (AAV2) capsid gene and generation of AAV2 vectors with eliminated heparin- binding ability and introduced novel tropism. Hum Gene Ther 17:353–361

    Article  CAS  PubMed  Google Scholar 

  • Simpson AA, Chipman PR, Baker TS, Tijssen P, Rossmann MG (1998) The structure of an insect parvovirus (Galleria mellonella densovirus) at 3.7 A resolution. Structure 6:1355–1367

    Article  CAS  PubMed  Google Scholar 

  • Simpson AA, Chandrasekar V, Hebert B, Sullivan GM, Rossmann MG, Parrish CR (2000) Host range and variability of calcium binding by surface loops in the capsids of canine and feline parvoviruses. J Mol Biol 300:597–610

    Article  CAS  PubMed  Google Scholar 

  • Smith AE, Helenius A (2004) How viruses enter animal cells. Science 304:237–242

    Article  CAS  PubMed  Google Scholar 

  • Sollner TH (2004) Intracellular and viral membrane fusion: a uniting mechanism. Curr Opin Cell Biol 16:429–435

    Article  CAS  PubMed  Google Scholar 

  • Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA (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 80:11040–11054

    Article  CAS  PubMed  Google Scholar 

  • Stachler MD, Bartlett JS (2006) Mosaic vectors comprised of modified AAV1 capsid proteins for efficient vector purification and targeting to vascular endothelial cells. Gene Ther 13:926–931

    CAS  PubMed  Google Scholar 

  • Strassheim LS, Gruenberg A, Veijalainen P, Sgro J-Y, Parrish CR (1994) Two dominant neutralizing antigenic determinants of canine parvovirus are found on the threefold spike of the virus capsid. Virology 198:175–184

    Article  CAS  PubMed  Google Scholar 

  • Suikkanen S, Saajarvi K, Hirsimaki J, Valilehto O, Reunanen H, Vihinen-Ranta M, Vuento M (2002) Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J Virol 76:4401–4411

    Article  CAS  PubMed  Google Scholar 

  • Suikkanen S, Aaltonen T, Nevalainen M, Valilehto O, Lindholm L, Vuento M, Vihinen-Ranta M (2003a) Exploitation of microtubule cytoskeleton and dynein during parvoviral traffic toward the nucleus. J Virol 77:10270–10279

    Article  CAS  PubMed  Google Scholar 

  • Suikkanen S, Antila M, Jaatinen A, Vihinen-Ranta M, Vuento M (2003b) Release of canine parvovirus from endocytic vesicles. Virology 316:267–280

    Article  CAS  PubMed  Google Scholar 

  • Tullis GE, Burger LR, Pintel DJ (1993) The minor capsid protein VP1 of the autonomous parvovirus minute virus of mice is dispensible for encapsidation of progeny single stranded DNA but is required for infectivity. J Virol 67:131–141

    CAS  PubMed  Google Scholar 

  • Van Vliet K, Blouin V, Agbandje-McKenna M, Snyder RO (2006) Proteolytic mapping of the adeno-associated virus capsid. Mol Ther 14:809–821

    Article  PubMed  CAS  Google Scholar 

  • van Weert AW, Dunn KW, Gueze HJ, Maxfield FR, Stoorvogel W (1995) Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 130:821–834

    Article  PubMed  Google Scholar 

  • Vihinen-Ranta M, Kalela A, Makinen P, Kakkola L, Marjomaki V, Vuento M (1998) Intracellular route of canine parvovirus entry. J Virol 72:802–806

    CAS  PubMed  Google Scholar 

  • Vihinen-Ranta M, Yuan W, Parrish CR (2000) Cytoplasmic trafficking of the canine parvovirus capsid and its role in infection and nuclear transport. J Virol 74:4853–4859

    Article  CAS  PubMed  Google Scholar 

  • Vihinen-Ranta M, Wang D, Weichert WS, Parrish CR (2002) The VP1 N-terminal sequence of canine parvovirus affects nuclear transport of capsids and efficient cell infection. J Virol 76:1884–1891

    Article  CAS  PubMed  Google Scholar 

  • Walters RW, Yi S, Keshavjee S, Brown KE, Welsh MJ, Chiorini JA, Zabner J (2001) Binding of adeno-associated virus type 5 to 2, 3-linked sialic acid is required for gene transfer. J Biol Chem 2766:20610–22061

    Article  Google Scholar 

  • Walters RW, Agbandje-McKenna M, Bowman VD, Moninger TO, Olson NH, Seiler M, Chiorini JA, Baker TS, Zabner J (2004) Structure of adeno-associated virus serotype 5. J Virol 78:3361–3371

    Article  CAS  PubMed  Google Scholar 

  • Warrington KH, Gorbatyuk OS, Harrison JK, Opie SR, Zolotukhin S, Muzyczka N (2004) Adeno-associated virus type 2 VP2 capsid protein is nonessential and can tolerate large peptide insertions at its N terminus. J Virol 78:6595–6609

    Article  CAS  PubMed  Google Scholar 

  • White K, Buning H, Kritz A, Janicki H, McVey J, Perabo L, Murphy G, Odenthal M, Work LM, Hallek M, Nicklin SA, Baker AH (2007) Engineering adeno-associated virus 2 vectors for targeted gene delivery to atherosclerotic lesions. Gene Ther 15:443–451

    Article  PubMed  CAS  Google Scholar 

  • Wu H, Rossmann MG (1993) The canine parvovirus empty capsid structure. J Mol Biol 233:231–244

    Article  CAS  PubMed  Google Scholar 

  • Xiao W, Warrington KH, Hearing P, Hughes J, Muzyczka N (2002) Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J Virol 76:11505–11517

    Article  CAS  PubMed  Google Scholar 

  • Yan Z, Zak R, Luxton GW, Ritchie TC, Bantel-Schaal U, Engelhardt JF (2002) Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J Virol 76:2043–2053

    Article  CAS  PubMed  Google Scholar 

  • Yoon-Robarts M, Blouin AG, Bleker S, Kleinschmidt JA, Aggarwal AK, Escalante CR, Linden RM (2004) Residues within the B' motif are critical for DNA binding by the superfamily 3 helicase Rep40 of adeno-associated virus type 2. J Biol Chem 279:50472–50481

    Article  CAS  PubMed  Google Scholar 

  • Yu CY, Yuan Z, Cao Z, Wang B, Qiao C, Li J, Xiao X (2009) A muscle-targeting peptide displayed on AAV2 improves muscle tropism on systemic delivery. Gene Ther 16:953–962

    Article  CAS  PubMed  Google Scholar 

  • Yunoki M, Tsujikawa M, Urayama T, Sasaki Y, Morita M, Tanaka H, Hattori S, Takechi K, Ikuta K (2003) Heat sensitivity of human parvovirus B19. Vox Sang 84:164–169

    Article  CAS  PubMed  Google Scholar 

  • Zadori Z, Szelei J, Lacoste M-C, Raymond P, Allaire M, Nabi IR, Tijssen P (2001) A viral phospholipase A2 is required for parvovirus infectivity. Dev Cell 1:291–302

    Article  CAS  PubMed  Google Scholar 

  • Zhang HG, Xie J, Dmitriev I, Kashentseva E, Curiel DT, Hsu HC, Mountz JD (2002) Addition of six-His-tagged peptide to the C terminus of adeno-associated virus VP3 does not affect viral tropism or production. J Virol 76:12023–12031

    Article  CAS  PubMed  Google Scholar 

  • Zhong L, Li B, Jayandharan G, Mah CS, Govindasamy L, Agbandje-McKenna M, Herzog RW, Weigel-Van Aken KA, Hobbs JA, Zolotukhin S, Muzyczka N, Srivastava A (2008) Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 381:194–202

    Article  CAS  PubMed  Google Scholar 

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  1. Baker Institute for Animal Health, Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY, 14853, USA

    Colin R. Parrish

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Correspondence to Colin R. Parrish .

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  1. Dept. Molecular Biology, Scripps Research Institute, N. Torrey Pines Rd. 10550, La Jolla, 92037, California, USA

    John E. Johnson

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Parrish, C.R. (2010). Structures and Functions of Parvovirus Capsids and the Process of Cell Infection. In: Johnson, J. (eds) Cell Entry by Non-Enveloped Viruses. Current Topics in Microbiology and Immunology, vol 343. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2010_33

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