Heparin binding induces conformational changes in Adeno-associated virus serotype 2
Open accessAbstract
Adeno-associated virus serotype 2 (AAV2) uses heparan sulfate proteoglycan as a cell surface-attachment receptor. In this study the structures of AAV2 alone and complexed with heparin were determined to approximately 18A resolution using cryo-electron microscopy and three-dimensional image reconstruction. A difference map showed positive density, modeled as heparin, close to the icosahedral twofold axes and between the protrusions that surround the threefold axes of the capsid. Regions of the model near the threefold place the receptor in close proximity to basic residues previously identified as part of the heparin binding site. The region of the model near the twofold axes identifies a second contact site, not previously characterized but which is also possibly configured by heparin binding. The difference map also revealed two significant conformational changes: (I) at the tops of the threefold protrusions, which have become flattened in the complex, and (II) at the fivefold axes where the top of the channel is widened possibly in response to movement of the HI loops in the capsid proteins. Ordered density in the interior of the capsid in the AAV2-heparin complex was interpreted as nucleic acid, consistent with the presence of non-viral DNA in the expressed capsids.
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For AAV2, two critical residues required for binding HS, R585 and R588, reside within VR-VIII, and the 511-NGR-513 motif proposed to play a role in α5β1 co-receptor binding is flanked by VR-I and VR-IV.
“For example, for AAV2, two critical residues required for binding HS, R585 and R588, reside within VR-VIII, and the 511-NGR-513 proposed to play a role in α5β1 co-receptor binding is flanked by VR-I and VR-IV (Asokan et al., 2006; Kern et al., 2003; Levy et al., 2009; Ng et al., 2010; Opie et al., 2003; Shen et al., 2015; Summerford and Samulski, 1998).”
From Structure comparison of the chimeric AAV2.7m8 vector with parental AAV2 (2020) · cites this paper as Levy et al., 2009
The Introduction identifies residues 511-NGR-513 as an α5β1-binding motif, and Results and Discussion calls R585 and R588 the residues most critical for AAV2 heparin binding. The cited paper does not place R585 and R588 within VR-VIII or say that VR-I and VR-IV flank the NGR motif (no page numbers are available in our copy). (LLM, conf=0.87)
Experimental — accuracy not yet measuredDifferent types of contaminating DNA sequences, including fragments of the host cell genome from vector production cells, are copackaged with transgenes in AAV vectors.
“different types of contaminating DNA sequences have been described as being copackaged with the transgenes, including fragments of the host cell genome from the cells that are used during vector production [81].”
From Understanding Capsid Assembly and Genome Packaging for Adeno-Associated Viruses (2017) · cites this paper as [81]
The Results and Discussion section ('AAV2-Hep encapsidates an ordered, dodecahedral cage of DNA'; page unavailable) reports non-viral DNA inside AAV2 virus-like particles and suggests that random DNA fragments may be packaged during assembly. It does not identify those fragments as host-cell genomic DNA or show them copackaged with transgenes in AAV vectors; the particles studied lacked a viral genome. (LLM, conf=0.85)
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Cites
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Self-citationHuman fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2
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MethodSelf-citationIdentification of a heparin-binding motif on adeno-associated virus type 2 capsids
Kern, A., Schmidt, K., Leder, C., Müller, O. J., Wobus, C. E., Bettinger, K., Von der Lieth, C. W., King, J. A., & Kleinschmidt, J. A. (2003) · Journal of Virology · doi:10.1128/jvi.77.20.11072-11081.2003 · Cited by 380 · cited 8× · see citing works
“These mark the closest points to the heparin binding residues identified by mutagenesis (Kern et al., 2003; Opie et al., 2003) in the crystal structure of the AAV2 capsid (Xie et al.”
BackgroundInfluentialOpie, S. R., Warrington, Agbandje-McKenna, M., Zolotukhin, S., & Muzyczka, N. (2003) · Journal of Virology · doi:10.1128/jvi.77.12.6995-7006.2003 · Cited by 364 · cited 8× · see citing works
“In addition, the 2f pos density (Fig. 2A and B) modeled as hep2f (Fig. 2B and C) is difficult to explain on the basis of the heparin binding residues, R484, R487, K527, K532, R585, and R588 (Kern et al., 2003; Opie et al., 2003 ).”
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“The N-terminal sequence unique to VP1 has a phospholipase A2 (PLA2) activity that is essential for infectivity at a step between endocytosis and nuclear entry (Girod et al., 2002) as well as nuclear localization signals.”
BackgroundAdeno-associated virus general transduction vectors: analysis of proviral structures
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Self-citationDNA helicase‐mediated packaging of adeno‐associated virus type 2 genomes into preformed capsids
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“A channel at each fivefold axis (channel) is implicated in packaging of the AAV2 genome and extrusion of the PLA2 activity of the VP1 unique region (Bleker et al., 2005; Sonntag et al., 2006).”
BackgroundHueffer, K., Parker, J. S. L., Weichert, W. S., Geisel, R. E., Sgro, J.-Y., & Parrish, C. R. (2003) · Journal of Virology · doi:10.1128/jvi.77.3.1718-1726.2003 · Cited by 262 · cited 1× · see citing works
“The binding site for the CPV transferrin receptor was mapped by mutagenesis and cryo-reconstruction to the raised portion of the capsid that lies between the icosahedral two- and fivefold axes (Hueffer et al., 2003a,b; Govindasamy et al., 2003; Hafenstein et al., 2007).”
BackgroundStructure of Adeno-Associated Virus Serotype 8, a Gene Therapy Vector
Nam, H.-J., Lane, M. D., Padron, E., Gurda, B. L., McKENNA, R. V., Kohlbrenner, E., Aslanidi, G., Byrne, B. J., Muzyczka, N., Zolotukhin, S., et al. (2007) · Journal of Virology · doi:10.1128/jvi.01304-07 · Cited by 256 · cited 4× · see citing works
“In addition, recent observation of NTs in baculovirus-expressed AAV8 ( Nam et al., 2007 )”
BackgroundMethodInfluentialSelf-citationHepatocyte Growth Factor Receptor Is a Coreceptor for Adeno-Associated Virus Type 2 Infection
Kashiwakura, Y., Tamayose, K., Iwabuchi, K., Hirai, Y., Shimada, T., Matsumoto, K., Nakamura, T., Watanabe, M., Oshimi, K., & Daida, H. (2005) · Journal of Virology · doi:10.1128/jvi.79.1.609-614.2005 · Cited by 246 · cited 1× · see citing works
“Efficient AAV2 infection also requires a co-receptor, such as human fibroblast growth factor receptor 1 (FGFR1), integrins avb5 and a5b1, or hepatocyte growth factor receptor (Asokan et al., 2006; Kashiwakura et al., 2005; Summerford et al., 1999; Qing et al., 1999).”
BackgroundThree-Dimensional Reconstruction of Icosahedral Particles—The Uncommon Line
Fuller, S. D., Butcher, S. J., Cheng, R. H., & Baker, T. S. (1996) · Journal of Structural Biology · doi:10.1006/jsbi.1996.0009 · Cited by 236 · cited 1× · see citing works
“A low resolution 3D map was generated from a selected subset for each set of images using the programs EMSEL and EM3DR (Baker et al., 1999; Fuller et al., 1996).”
MethodSelf-citationQuantification of adeno-associated virus particles and empty capsids by optical density measurement
Sommer, J. Ü. M., Smith, P. H., Parthasarathy, S., Isaacs, J., Vijay, S., Kieran, J., Powell, S. K., McClelland, A., & Wright, J. F. (2003) · Molecular Therapy · doi:10.1016/s1525-0016(02)00019-9 · Cited by 230 · cited 1× · see citing works
“…and three-dimensional (3D) image reconstruction (‘‘cryo-reconstruction”) and X-ray crystallography have been used to determine the structures of several AAV serotypes, including AAV1, AAV2, AAV4, AAV5, AAV7, and AAV8 (Govindasamy et al., 2003; Kronenberg et al., 2001; Miller et al., 2006;…”
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“Efficient AAV2 infection also requires a co-receptor, such as human fibroblast growth factor receptor 1 (FGFR1), integrins avb5 and a5b1, or hepatocyte growth factor receptor (Asokan et al., 2006; Kashiwakura et al., 2005; Summerford et al., 1999; Qing et al., 1999).”
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“The crystal structures of CPV and the immunosuppressive strain of MVM (MVMi) showed the presence of at least 11 ordered ssDNA NTs inside the capsids (Agbandje-Mckenna et al., 1998; Kontou et al., 2005; Xie and Chapman, 1996).”
BackgroundMethodInfluentialSelf-citationStructurally mapping the diverse phenotype of adeno-associated virus serotype 4
Govindasamy, L., Padron, E., McKenna, R., Muzyczka, N., Kaludov, N., Chiorini, J. A., & Agbandje-McKenna, M. (2006) · Journal of Virology · doi:10.1128/jvi.01536-06 · Cited by 205 · see citing works
Self-citationThe structure of human parvovirus B19
Kaufmann, B., Simpson, A. A., & Rossmann, M. G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402992101 · Cited by 204 · cited 1× · see citing works
“However, the HI loop in B19 adopts a radial orientation relative to the capsid surface (Kaufmann et al., 2004), similar to the AAV2–Hep HI loop conformation described above.”
BackgroundLochrie, M. A., Tatsuno, G. P., Christie, B., McDonnell, J. W., Zhou, S., Surosky, R., Pierce, G. F., & Colosi, P. (2006) · Journal of Virology · doi:10.1128/jvi.80.2.821-834.2006 · Cited by 201 · cited 4× · see citing works
“who suggested that primary receptor binding by AAV2 might lead to structural rearrangements close to the twofold axis to facilitate co-receptor attachment (Lochrie et al., 2006).”
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“A channel at each fivefold axis (channel) is implicated in packaging of the AAV2 genome and extrusion of the PLA2 activity of the VP1 unique region (Bleker et al., 2005; Sonntag et al., 2006).”
BackgroundInfluentialKronenberg, S., Böttcher, B., von der Lieth, C. W., Bleker, S., & Kleinschmidt, J. A. (2005) · Journal of Virology · doi:10.1128/jvi.79.9.5296-5303.2005 · Cited by 198 · see citing works
Dynamin Is Required for Recombinant Adeno-Associated Virus Type 2 Infection
Duan, D., Li, Q., Kao, A. W., Yue, Y., Pessin, J. E., & Engelhardt, J. F. (1999) · Journal of Virology · doi:10.1128/jvi.73.12.10371-10376.1999 · Cited by 186 · cited 1× · see citing works
“These co-receptors mediate endocytosis of the virus via clathrin-coated pits (Bartlett et al., 2000; Duan et al., 1999).”
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“Efficient AAV2 infection also requires a co-receptor, such as human fibroblast growth factor receptor 1 (FGFR1), integrins avb5 and a5b1, or hepatocyte growth factor receptor (Asokan et al., 2006; Kashiwakura et al., 2005; Summerford et al., 1999; Qing et al., 1999).”
BackgroundSelf-citationThe structure of pariacoto virus reveals a dodecahedral cage of duplex RNA.
Johnson, J. E., Tang, L., Johnson, K. N., Ball, L. A., Lin, T., & Yeager, M. J. (2001) · Nature Structural Biology · doi:10.1038/83089 · Cited by 165 · cited 1× · see citing works
“The diameter of the electron beam was adjusted to not exceed the limits of the Gatan 2k2 slow-scan CCD detector (0.4 lm on the specimen) to allow images to be recorded without pre-irradiating adjacent regions.”
MethodInfluentialElectron cryo‐microscopy and image reconstruction of adeno‐associated virus type 2 empty capsids
Kronenberg, S., Kleinschmidt, J. A., & Böttcher, B. (2001) · The EMBO Reports · doi:10.1093/embo-reports/kve234 · Cited by 161 · cited 7× · see citing works
“The crystal structures of AAV4 and AAV8 showed the ordering of a single nucleotide (NT) under each threefold axis (Govindasamy et al., 2006; Nam et al., 2007).”
MethodInfluentialVihinen‐Ranta, M., Wang, D., Weichert, W. S., & Parrish, C. R. (2002) · Journal of Virology · doi:10.1128/jvi.76.4.1884-1891.2002 · Cited by 154 · cited 2× · see citing works
“Extrusion and activity of the VP1-N terminal PLA2 domain is essential for efficient infection and is believed to occur during or shortly after virus entry into the cell (Bleker et al., 2005; Farr et al., 2006; Mani et al., 2006; Suikkanen et al., 2003; Vihinen-Ranta et al., 2002).”
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“…Rep-facilitated DNA packaging is proposed to occur with preformed empty capsids through the channel, these observations suggest that small portions of viral genome are pre-packaged during assembly before Rep completes the packaging (Myers and Carter, 1980; Wistuba et al., 1995; King et al., 2001).”
BackgroundFlotte, T. R., Brantly, M., Spencer, L. T., Byrne, B. J., Spencer, C. T., Baker, D. J., & Humphries, M. R. (2004) · Human Gene Therapy · doi:10.1089/10430340460732490 · Cited by 146 · cited 3× · see citing works
“…Baker d, Mavis Agbandje-McKenna a,* a Department of Biochemistry and Molecular Biology, Center for Structural Biology, The McKnight Brain Institute, College of Medicine, 1600 SW Archer Road, P.O. Box 100245, University of Florida, Gainesville, FL 32610, USA b Department of Biological Sciences,…”
BackgroundMethodInfluentialCanine Parvovirus Capsid Structure, Analyzed at 2.9 Å Resolution
Xie, Q., & Chapman, M. S. (1996) · Journal of Molecular Biology · doi:10.1006/jmbi.1996.0657 · Cited by 134 · cited 1× · see citing works
“The crystal structures of CPV and the immunosuppressive strain of MVM (MVMi) showed the presence of at least 11 ordered ssDNA NTs inside the capsids (Agbandje-Mckenna et al., 1998; Kontou et al., 2005; Xie and Chapman, 1996).”
BackgroundThree-dimensional Structure of Calicivirus
Prasad, B. V. V., Matson, D. O., & Smith, A. W. (1994) · Journal of Molecular Biology · doi:10.1006/jmbi.1994.1439 · Cited by 125 · cited 1× · see citing works
“The diameter of the electron beam was adjusted to not exceed the limits of the Gatan 2k2 slow-scan CCD detector (0.4 lm on the specimen) to allow images to be recorded without pre-irradiating adjacent regions.”
MethodInfluentialRelease of canine parvovirus from endocytic vesicles
Suikkanen, S., Antila, M., Jaatinen, A., Vihinen-Ranta, M., & Vuento, M. (2003) · Virology · doi:10.1016/j.virol.2003.08.031 · Cited by 115 · see citing works
Structure of Adeno-Associated Virus Serotype 5
Walters, R. W., Agbandje-McKenna, M., Bowman, V. D., Moninger, T. O., Olson, N. H., Seiler, M., Chiorini, J. A., Baker, T. S., & Zabner, J. (2004) · Journal of Virology · doi:10.1128/jvi.78.7.3361-3371.2004 · Cited by 114 · see citing works
Self-citationMani, B., Baltzer, C., Valle, N., Almendral, J. M., Kempf, C., & Ros, C. (2005) · Journal of Virology · doi:10.1128/jvi.80.2.1015-1024.2006 · Cited by 113 · cited 1× · see citing works
“AAV terminal repeats (TRs) rather than heterologous DNA sequences are known to form the signal used to package AAV (McLaughlin et al., 1988).”
BackgroundHueffer, K., Lakshmanan Govindasamy, A., Agbandje‐McKenna, M., & Parrish, C. R. (2003) · Journal of Virology · doi:10.1128/jvi.77.18.10099-10105.2003 · Cited by 111 · cited 2× · see citing works
“The binding site for the CPV transferrin receptor was mapped by mutagenesis and cryo-reconstruction to the raised portion of the capsid that lies between the icosahedral two- and fivefold axes (Hueffer et al., 2003a,b; Govindasamy et al., 2003; Hafenstein et al., 2007).”
BackgroundSelf-citationStructure of Adeno-Associated Virus Type 4
Padron, E., Bowman, V. D., Kaludov, N. K., Lakshmanan Govindasamy, A., Levy, H. C., Nick, P., McKENNA, R. V., Muzyczka, N., Chiorini, J. A., Baker, T. S., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.8.5047-5058.2005 · Cited by 108 · cited 3× · see citing works
“Cryo-electron microscopy and three-dimensional (3D) image reconstruction (‘‘cryo-reconstruction”) and X-ray crystallography have been used to determine the structures of several AAV serotypes, including AAV1, AAV2, AAV4, AAV5, AAV7, and AAV8 (Govindasamy et al., 2003; Kronenberg et al., 2001; Miller et al., 2006; Nam…”
BackgroundMethodInfluentialSelf-citationAssembly of adeno-associated virus
Myers, M. W., & Carter, B. J. (1980) · Virology · doi:10.1016/0042-6822(80)90071-9 · Cited by 107 · cited 2× · see citing works
“Hence, since Rep-facilitated DNA packaging is proposed to occur with preformed empty capsids through the channel, these observations suggest that small portions of viral genome are pre-packaged during assembly before Rep completes the packaging (Myers and Carter, 1980; Wistuba et al., 1995; King et al., 2001).”
BackgroundChipman, P. R., Agbandje‐McKenna, M., Kajigaya, S., Brown, K. E., Young, N. S., Baker, T. S., & Rossmann, M. G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.7502 · Cited by 106 · cited 3× · see citing works
“Regions of the capsid surface that bind to host-cell receptors have been identified for three autonomous parvoviruses: human parvovirus B19 (B19), canine parvovirus (CPV), and minute virus of mice (MVM) (Chipman et al., 1996; Hafenstein et al., 2007; Lopez-Bueno et al., 2006).”
BackgroundMethodSelf-citationAsymmetric binding of transferrin receptor to parvovirus capsids
Hafenstein, S. L., Palermo, L. M., Kostyuchenko, V. A., Xiao, C., Morais, M. C., Nelson, C. D. S., Bowman, V. D., Battisti, A. J., Chipman, P. R., Parrish, C. R., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701574104 · Cited by 96 · cited 15× · see citing works
“The crystal structures of CPV and the immunosuppressive strain of MVM (MVMi) showed the presence of at least 11 ordered ssDNA NTs inside the capsids (Agbandje-Mckenna et al., 1998; Kontou et al., 2005; Xie and Chapman, 1996).”
BackgroundInfluentialSelf-citationLakshmanan Govindasamy, A., Hueffer, K., Parrish, C. R., & Agbandje‐McKenna, M. (2003) · Journal of Virology · doi:10.1128/jvi.77.22.12211-12221.2003 · Cited by 95 · cited 3× · see citing works
“…and X-ray crystallography have been used to determine the structures of several AAV serotypes, including AAV1, AAV2, AAV4, AAV5, AAV7, and AAV8 (Govindasamy et al., 2003; Kronenberg et al., 2001; Miller et al., 2006; Nam et al., 2007; Padron et al., 2005; Quesada et al., 2007; Walters et…”
BackgroundMethodSelf-citationKontou, M., Lakshmanan Govindasamy, A., Nam, H.-J., Bryant, N. D., Llamas-Saiz, A. L., Foces‐Foces, C., Hernando, E., Rubio, M., McKENNA, R. V., Almendral, J. M., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.17.10931-10943.2005 · Cited by 85 · cited 5× · see citing works
“The crystal structures of CPV and the immunosuppressive strain of MVM (MVMi) showed the presence of at least 11 ordered ssDNA NTs inside the capsids (Agbandje-Mckenna et al., 1998; Kontou et al., 2005; Xie and Chapman, 1996).”
BackgroundInfluentialSelf-citationBiochemical and Physical Characterization of Parvovirus Minute Virus of Mice Virus-like Particles
Hernando, E., Llamas-Saiz, A. L., Foces‐Foces, C., McKENNA, R. V., Portman, I., Agbandje‐McKenna, M., & Almendral, J. M. (2000) · Virology · doi:10.1006/viro.1999.0123 · Cited by 79 · see citing works
Self-citationThe Interaction of Heparin Sulfate and Adeno-Associated Virus 2
Qiu, J., Handa, A., Kirby, M., & Brown, K. E. (2000) · Virology · doi:10.1006/viro.2000.0205 · Cited by 79 · cited 1× · see citing works
“Soluble heparin has been shown to compete with permissive cells for AAV2 binding and de-sulfating heparin reduces binding to AAV2 ( Qiu et al., 2000 ).”
BackgroundLópez-Bueno, A., Rubio, M., Bryant, N. D., McKENNA, R. V., Agbandje‐McKenna, M., & Almendral, J. M. (2006) · Journal of Virology · doi:10.1128/jvi.80.3.1563-1573.2006 · Cited by 79 · see citing works
Self-citationFarr, G. A., Cotmore, S. F., & Tattersall, P. J. (2005) · Journal of Virology · doi:10.1128/jvi.80.1.161-171.2006 · Cited by 71 · cited 3× · see citing works
“Significantly, the fivefold channels of parvovirus capsids have been implicated as conduits for extrusion of the N-terminal portions of VP1 and VP2 (both of which are reported to normally lie inside the capsid and for genome packaging (Bleker et al., 2005; Farr and Tattersall, 2004; Farr et al., 2006).”
BackgroundFarr, G. A., & Tattersall, P. J. (2004) · Virology · doi:10.1016/j.virol.2004.03.006 · Cited by 67 · cited 2× · see citing works
“Significantly, the fivefold channels of parvovirus capsids have been implicated as conduits for extrusion of the N-terminal portions of VP1 and VP2 (both of which are reported to normally lie inside the capsid and for genome packaging (Bleker et al., 2005; Farr and Tattersall, 2004; Farr et al., 2006).”
BackgroundMiller, E. B., Gurda, B. L., Lakshmanan Govindasamy, A., McKENNA, R. V., Zolotukhin, S., Muzyczka, N., & Agbandje‐McKenna, M. (2006) · Acta Crystallographica Section F Structural Biology and Crystallization Communications · doi:10.1107/s1744309106048184 · Cited by 58 · see citing works
Self-citationBowman, V. D., Chase, E. S., Franz, A. W. E., Chipman, P. R., Zhang, X., Perry, K. L., Baker, T. S., & Smith, T. J. (2002) · Journal of Virology · doi:10.1128/jvi.76.23.12250-12258.2002 · Cited by 55 · cited 1× · see citing works
“A total of 2335 particle images was boxed from ten VLP micrographs and 1523 particle images were boxed from eight AAV2–Hep micrographs as previously described (Bowman et al., 2002; Walters et al., 2004).”
MethodSelf-citationIcosahedral Packing of RNA Viral Genomes
Rudnick, J., & Bruinsma, R. (2005) · Physical Review Letters · doi:10.1103/physrevlett.94.038101 · Cited by 51 · cited 2× · see citing works
“A similar mechanism has been proposed for assembly of ssRNA viruses (Rudnick and Bruinsma, 2005; Zlotnick, 1994, 2004).”
BackgroundNony, P., Chadeuf, G., Tessier, J., Moullier, P., & Salvetti, A. (2003) · Journal of Virology · doi:10.1128/jvi.77.1.776-781.2003 · Cited by 51 · cited 2× · see citing works
“Several investigators have shown that AAV DNA and heterologous, chromosomal DNA that contains a Rep binding element and a terminal resolution site, but no TRs, can also be packaged into AAV virions (Huser et al., 2003; Nony et al., 2003).”
BackgroundMethodSurface Loop Dynamics in Adeno-Associated Virus Capsid Assembly
DiPrimio, N., Asokan, A., Lakshmanan Govindasamy, A., Agbandje‐McKenna, M., & Samulski, R. J. (2008) · Journal of Virology · doi:10.1128/jvi.02721-07 · Cited by 49 · cited 2× · see citing works
“Recently, mutagenesis, confocal microscopy, and VP structural alignment studies reported a role for the HI loop in genome packaging (DiPrimio et al., 2008).”
BackgroundSelf-citationAtomic structure of viral particles
Chapman, M. S., & Agbandje‐McKenna, M. (2005) · CRC Press eBooks · doi:10.1201/b13393-13 · Cited by 47 · see citing works
Self-citationViruses and the physics of soft condensed matter
Zlotnick, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406935101 · Cited by 44 · cited 1× · see citing works
“A similar mechanism has been proposed for assembly of ssRNA viruses (Rudnick and Bruinsma, 2005; Zlotnick, 1994, 2004).”
BackgroundHüser, D., Weger, S., & Heilbronn, R. (2003) · Journal of Virology · doi:10.1128/jvi.77.8.4881-4887.2003 · Cited by 29 · cited 2× · see citing works
“Several investigators have shown that AAV DNA and heterologous, chromosomal DNA that contains a Rep binding element and a terminal resolution site, but no TRs, can also be packaged into AAV virions ( Huser et al., 2003; Nony et al., 2003).”
BackgroundReguera, J., Grueso, E., Carreira, A., Sánchez-Martı́nez, C., Almendral, J. M., & Mateu, M. G. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m500867200 · Cited by 27 · cited 1× · see citing works
“The estimated resolution achieved with each reconstruction was defined by the lowest spatial frequency at which the FSC first dropped below 0.5 and the average phase difference exceeded 45 .”
BackgroundInfluentialRNA-protein interactions in spherical viruses
Bink, H. H. J., & Pleij, C. W. A. (2002) · Archives of Virology · doi:10.1007/s00705-002-0891-6 · Cited by 24 · cited 2× · see citing works
“The diameter of the electron beam was adjusted to not exceed the limits of the Gatan 2k2 slow-scan CCD detector (0.4 lm on the specimen) to allow images to be recorded without pre-irradiating adjacent regions.”
BackgroundMethodInfluentialQuesada, O., Gurda, B. L., Lakshmanan Govindasamy, A., McKENNA, R. V., Kohlbrenner, E., Aslanidi, G., Zolotukhin, S., Muzyczka, N., & Agbandje‐McKenna, M. (2007) · Acta Crystallographica Section F Structural Biology and Crystallization Communications · doi:10.1107/s1744309107060289 · Cited by 20 · see citing works
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Virus-like particles in vaccine development
Roldão, A., Mellado, M. C. M., Castilho, L. R., Carrondo, M. J. T., & Alves, P. M. (2010) · Expert Review of Vaccines · doi:10.1586/erv.10.115 · Cited by 851 · see citing works
Pharmacology of Heparin and Related Drugs
Mulloy, B., Hogwood, J., Gray, E., Lever, R., & Page, C. P. (2015) · Pharmacological Reviews · doi:10.1124/pr.115.011247 · Cited by 341 · see citing works
“The second study (Levy et al., 2009), using a partially depolymerized heparin, suffered the same problems, perhaps to a lesser extent; however, both studies agreed on the location of the major heparin binding site in the valleys between protrusions at the 3-fold axis of the icosahedral capsid.”
MethodResultAsokan, A., Conway, J. C., Phillips, J. L., Li, C., Hegge, J., Sinnott, R., Yadav, S. S., DiPrimio, N., Nam, H. J., Agbandje‐McKenna, M., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1599 · Cited by 265 · see citing works
Self-citationCapsid modifications for targeting and improving the efficacy of AAV vectors
Büning, H., & Srivastava, A. (2019) · Molecular Therapy - Methods & Clinical Development · doi:10.1016/j.omtm.2019.01.008 · Cited by 260 · see citing works
“Receptor binding not only enables cell entry, but also primes the capsid for the later release of its genetic payload (uncoating)(46) and prepares the cell for viral particle transport and processing.(46) Since AAV serotypes differ in receptors used for cell attachment and internalization, serotypes other than AAV2, t…”
Intracellular transport of recombinant adeno-associated virus vectors
Nonnenmacher, M., & Weber, T. (2012) · Gene Therapy · doi:10.1038/gt.2012.6 · Cited by 258 · see citing works
Bucher, K., Rodríguez-Bocanegra, E., Dauletbekov, D., & Fischer, M. D. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100915 · Cited by 242 · see citing works
Venkatakrishnan, B., Yarbrough, J., Domsic, J. F., Bennett, A. D., Bothner, B. B., Kozyreva, O. G., Samulski, R. J., Muzyczka, N., McKENNA, R. V., & Agbandje‐McKenna, M. (2013) · Journal of Virology · doi:10.1128/jvi.02524-12 · Cited by 225 · see citing works
Self-citationBasic Biology of Adeno-Associated Virus (AAV) Vectors Used in Gene Therapy
Balakrishnan, B., & Jayandharan, G. (2014) · Current Gene Therapy · doi:10.2174/1566523214666140302193709 · Cited by 225 · see citing works
Engineering Liver-detargeted AAV9 Vectors for Cardiac and Musculoskeletal Gene Transfer
Pulicherla, N., Shen, S., Yadav, S. S., Debbink, K. M., Lakshmanan Govindasamy, A., Agbandje‐McKenna, M., & Asokan, A. (2011) · Molecular Therapy · doi:10.1038/mt.2011.22 · Cited by 223 · see citing works
Self-citationSureau, C., & Salisse, J. (2012) · Hepatology · doi:10.1002/hep.26125 · Cited by 218 · see citing works
AAV Capsid Structure and Cell Interactions
Agbandje-McKenna, M., & Kleinschmidt, J. (2012) · Methods in Molecular Biology · doi:10.1007/978-1-61779-370-7_3 · Cited by 215 · see citing works
Self-citationTwenty-Five Years of Structural Parvovirology
Mietzsch, M., Pénzes, J. J., & Agbandje-McKenna, M. (2019) · Viruses · doi:10.3390/v11040362 · Cited by 197 · see citing works
Self-citationComparative Analysis of Adeno-Associated Virus Capsid Stability and Dynamics
Rayaprolu, V., Kruse, S., Kant, R., Venkatakrishnan, B., Movahed, N., Brooke, D. J., Lins, B., Bennett, A. D., Potter, T., McKENNA, R. V., et al. (2013) · Journal of Virology · doi:10.1128/jvi.01415-13 · Cited by 161 · see citing works
Self-citationResolving Adeno-Associated Viral Particle Diversity With Charge Detection Mass Spectrometry
Pierson, E. E., Keifer, D. Z., Asokan, A., & Jarrold, M. F. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.6b00883 · Cited by 152 · see citing works
Adeno-associated virus (AAV) cell entry: structural insights
Meyer, N., & Chapman, M. S. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2021.09.005 · Cited by 139 · see citing works
Structural Characterization of the Dual Glycan Binding Adeno-Associated Virus Serotype 6
Ng, R., Govindasamy, L., Gurda, B. L., McKENNA, R. V., Kozyreva, O. G., Samulski, R. J., Parent, K. N., Baker, T. S., & Agbandje‐McKenna, M. (2010) · Journal of Virology · doi:10.1128/jvi.01235-10 · Cited by 143 · see citing works
Self-citationIdentification of the Galactose Binding Domain of the Adeno-Associated Virus Serotype 9 Capsid
Bell, C. L., Gurda, B. L., Vliet, K. V., Agbandje‐McKenna, M., & Wilson, J. M. (2012) · Journal of Virology · doi:10.1128/jvi.00448-12 · Cited by 138 · see citing works
Self-citationParvovirus glycan interactions
Huang, L., Halder, S., & Agbandje‐McKenna, M. (2014) · Current Opinion in Virology · doi:10.1016/j.coviro.2014.05.007 · Cited by 136 · see citing works
Self-citationCapsid antibodies to different adeno-associated virus serotypes bind common regions
Gurda, B. L., DiMattia, M. A., Miller, E. B., Bennett, A., McKenna, R., Weichert, W. S., Nelson, C. D., Chen, W.-J., Muzyczka, N., Olson, N. H., et al. (2013) · Journal of Virology · doi:10.1128/jvi.00622-13 · Cited by 127 · see citing works
Self-citationAdeno-associated virus-2 and its primary cellular receptor—Cryo-EM structure of a heparin complex
O’Donnell, J., Taylor, K. A., & Chapman, M. S. (2009) · Virology · doi:10.1016/j.virol.2008.11.037 · Cited by 126 · see citing works
Asuri, P., Bartel, M. A., Vazin, T., Jang, J.-H., Wong, T. B., & Schaffer, D. V. (2012) · Molecular Therapy · doi:10.1038/mt.2011.255 · Cited by 119 · see citing works
Intracellular trafficking of adeno-associated virus (AAV) vectors: challenges and future directions
Riyad, J. M., & Weber, T. (2021) · Gene Therapy · doi:10.1038/s41434-021-00243-z · Cited by 116 · see citing works
Adeno-Associated Virus Structural Biology as a Tool in Vector Development
Drouin, L. M., & Agbandje-McKenna, M. (2013) · Future Virology · doi:10.2217/fvl.13.112 · Cited by 114 · see citing works
Self-citationEngineering the AAV capsid to optimize vector–host-interactions
Büning, H., Huber, A., Zhang, L. N., Meumann, N., & Hacker, U. T. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.08.002 · Cited by 113 · see citing works
Nam, H.-J., Gurda, B. L., McKenna, R., Potter, M., Byrne, B., Salganik, M., Muzyczka, N., & Agbandje-McKenna, M. (2011) · Journal of Virology · doi:10.1128/jvi.05305-11 · Cited by 108 · see citing works
Self-citationGlycan Engagement by Viruses: Receptor Switches and Specificity
Stroh, L. J., & Stehle, T. (2014) · Annual Review of Virology · doi:10.1146/annurev-virology-031413-085417 · Cited by 111 · see citing works
Human parvovirus B19: A review
Rogo, L. D., Mokhtari‐Azad, T., Hamid, K. M., & REZAEI, F. (2014) · Acta Virologica · doi:10.4149/av_2014_03_199 · Cited by 108 · see citing works
Lerch, T. F., Xie, Q., & Chapman, M. S. (2010) · Virology · doi:10.1016/j.virol.2010.03.027 · Cited by 107 · see citing works
“Others have suggested that polysaccharide binding is used by the virus to trigger conformational changes that might be a part of cell entry (Asokan et al., 2006; Levy et al., 2009).”
Shen, S., Horowitz, E. D., Troupes, A. N., Brown, S. M., Pulicherla, N., Samulski, R. J., Agbandje‐McKenna, M., & Asokan, A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.482380 · Cited by 103 · see citing works
Self-citationCharacterization of the Adeno-Associated Virus 1 and 6 Sialic Acid Binding Site
Huang, L.-Y., Patel, A. R., Ng, R., Miller, E. B., Halder, S., McKENNA, R. V., Asokan, A., & Agbandje‐McKenna, M. (2016) · Journal of Virology · doi:10.1128/jvi.00161-16 · Cited by 99 · see citing works
Self-citationStructural insights into adeno-associated virus serotype 5
Govindasamy, L., DiMattia, M. A., Gurda, B. L., Halder, S., McKenna, R., Chiorini, J. A., Muzyczka, N., Zolotukhin, S., & Agbandje-McKenna, M. (2013) · Journal of Virology · doi:10.1128/jvi.00867-13 · Cited by 95 · see citing works
Self-citationHuman Bocavirus Capsid Structure: Insights into the Structural Repertoire of the Parvoviridae
Gurda, B. L., Parent, K. N., Bladek, H., Sinkovits, R. S., DiMattia, M. A., Rence, C., Castro, A., McKENNA, R. V., Olson, N. H., Brown, K. E., et al. (2010) · Journal of Virology · doi:10.1128/jvi.02719-09 · Cited by 94 · see citing works
Self-citationRossi, A., Dupaty, L., Aillot, L., Zhang, L., Gallien, C., Hallek, M., Odenthal, M., Adriouch, S., Salvetti, A., & Büning, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-40071-1 · Cited by 85 · see citing works
Adeno-associated Virus as a Mammalian DNA Vector
Salganik, M., Hirsch, M. L., & Samulski, R. J. (2015) · Microbiology Spectrum · doi:10.1128/microbiolspec.mdna3-0052-2014 · Cited by 88 · see citing works
Understanding Capsid Assembly and Genome Packaging for Adeno-Associated Viruses
Bennett, A., Mietzsch, M., & Agbandje-McKenna, M. (2017) · Future Virology · doi:10.2217/fvl-2017-0011 · Cited by 82 · see citing works
Self-citationBoye, S. L., Bennett, A., Scalabrino, M. L., McCullough, K. T., Van Vliet, K., Choudhury, S., Ruan, Q., Peterson, J., Agbandje-McKenna, M., & Boye, S. E. (2016) · Journal of Virology · doi:10.1128/jvi.00200-16 · Cited by 79 · see citing works
Self-citationChowdhury, E. A., Meno‐Tetang, G. M. L., Chang, H. Y., Wu, S., Huang, H. W., Jamier, T., Chandran, J. S., & Shah, D. K. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.01.017 · Cited by 78 · see citing works
Role of capsid proteins in parvoviruses infection
Tu, M., Liu, F., Chen, S., Wang, M., & Cheng, A. (2015) · Virology Journal · doi:10.1186/s12985-015-0344-y · Cited by 77 · see citing works
Cryoelectron Microscopy Maps of Human Papillomavirus 16 Reveal L2 Densities and Heparin Binding Site
Guan, J., Bywaters, S. M., Brendle, S. A., Ashley, R. E., Makhov, A. M., Conway, J. F., Christensen, N. D., & Hafenstein, S. L. (2017) · Structure · doi:10.1016/j.str.2016.12.001 · Cited by 75 · see citing works
Tran, N. T., Lecomte, E., Saleun, S., Namkung, S., Robin, C., Weber, K., Devine, E., Blouin, V., Adjali, O., Ayuso, E., et al. (2022) · Human Gene Therapy · doi:10.1089/hum.2022.050 · Cited by 74 · see citing works
“It has been demonstrated previously that empty particles may contain small fragments of genomic material, 50 but the contents were unknown.”
Tseng, Y.-S., Gurda, B. L., Chipman, P. R., McKENNA, R. V., Afione, S. A., Chiorini, J. A., Muzyczka, N., Olson, N. H., Baker, T. S., Kleinschmidt, J. A., et al. (2014) · Journal of Virology · doi:10.1128/jvi.02710-14 · Cited by 69 · see citing works
Self-citationComparative Analysis of the Capsid Structures of AAVrh.10, AAVrh.39, and AAV8
Mietzsch, M., Barnes, C., Hull, J. A., Chipman, P. R., Xie, J., Bhattacharya, N., Sousa, D. R., McKENNA, R. V., Gao, G., & Agbandje‐McKenna, M. (2019) · Journal of Virology · doi:10.1128/jvi.01769-19 · Cited by 66 · see citing works
“The previous reports thus support reports of AAV packaging cellular pieces of DNA in the absence of Rep proteins (59).”
ResultSelf-citationCerqueira, C., Liu, Y., Kühling, L., Chai, W., Hafezi, W., Kuppevelt, T. H. V., Kühn, J., Feizi, T., & Schelhaas, M. (2013) · Cellular Microbiology · doi:10.1111/cmi.12150 · Cited by 64 · see citing works
Raupp, C., Naumer, M., Müller, O. J., Gurda, B. L., Agbandje‐McKenna, M., & Kleinschmidt, J. A. (2012) · Journal of Virology · doi:10.1128/jvi.00209-12 · Cited by 63 · see citing works
Self-citationBönsch, C., Zuercher, C., Lieby, P., Kempf, C., & Ros, C. (2010) · Journal of Virology · doi:10.1128/jvi.01143-10 · Cited by 64 · see citing works
Glycan Binding Avidity Determines the Systemic Fate of Adeno-Associated Virus Type 9
Shen, S., Bryant, K. D., Sun, J., Brown, S. M., Troupes, A. N., Pulicherla, N., & Asokan, A. (2012) · Journal of Virology · doi:10.1128/jvi.01155-12 · Cited by 62 · see citing works
Strategies to circumvent humoral immunity to adeno-associated viral vectors
Tse, L. V., Moller-Tank, S., & Asokan, A. (2015) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2015.1035645 · Cited by 61 · see citing works
Adeno-Associated Virus (AAV) Gene Delivery: Dissecting Molecular Interactions upon Cell Entry
Large, E. E., Silveria, M., Zane, G. M., Weerakoon, O., & Chapman, M. S. (2021) · Viruses · doi:10.3390/v13071336 · Cited by 54 · see citing works
“Belief in large-scale glycan-induced conformational change persisted due to hints thereof in an independently determined structure of an AAV2-heparin complex at 18 Å resolution [162].”
BackgroundPénzes, J. J., Chipman, P. R., Bhattacharya, N., Zeher, A., Huang, R. K., McKENNA, R. V., & Agbandje‐McKenna, M. (2021) · Journal of Virology · doi:10.1128/jvi.00843-21 · Cited by 55 · see citing works
Self-citationSynthetic virology: engineering viruses for gene delivery
Guenther, C. M., Kuypers, B. E., Lam, M. T., Robinson, T. M., Zhao, J. X., & Suh, J. (2014) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1287 · Cited by 56 · see citing works
Identification of the heparin binding site on adeno-associated virus serotype 3B (AAV-3B)
Lerch, T. F., & Chapman, M. S. (2011) · Virology · doi:10.1016/j.virol.2011.10.007 · Cited by 54 · see citing works
“Both studies stand in stark contrast to the inference of large induced changes from subtle differences in maps of AAV-2 at much lower (18Å) resolution (Levy et al., 2009).”
ResultTunable Protease-Activatable Virus Nanonodes
Judd, J., Ho, M. L., Tiwari, A., Gomez, E. J., Dempsey, C., Vliet, K. V., Igoshin, O. A., Silberg, J. J., Agbandje‐McKenna, M., & Suh, J. (2014) · ACS Nano · doi:10.1021/nn500550q · Cited by 54 · see citing works
Self-citationParvoviruses: Structure and Infection
Halder, S., Ng, R., & Agbandje‐McKenna, M. (2012) · Future Virology · doi:10.2217/fvl.12.12 · Cited by 53 · see citing works
Self-citationDrouin, L. M., Lins, B., Janssen, M., Bennett, A. D., Chipman, P. R., McKENNA, R. V., Chen, W., Muzyczka, N., Giovanni Cardone, A., Baker, T. S., et al. (2016) · Journal of Virology · doi:10.1128/jvi.00575-16 · Cited by 52 · see citing works
Self-citationNance, M. E., & Duan, D. (2015) · Human Gene Therapy · doi:10.1089/hum.2015.107 · Cited by 50 · see citing works
Judd, J., Wei, F., Nguyen, P. Q., Tartaglia, L. J., Agbandje‐McKenna, M., Silberg, J. J., & Suh, J. (2012) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2012.46 · Cited by 51 · see citing works
Self-citationAslanidi, G., Rivers, A. E., Ortiz, L., Lakshmanan Govindasamy, A., Ling, C., Jayandharan, G. R., Zolotukhin, S., Agbandje‐McKenna, M., & Srivastava, A. (2012) · Vaccine · doi:10.1016/j.vaccine.2012.03.079 · Cited by 48 · see citing works
“The HI loop, which forms interactions between icosahedral five-fold symmetry related VPs and lies on the floor of the depression surrounding this axis, was also proposed to undergo a conformational re-arrangement that opens up the channel located at the icosahedral fivefold axis following heparin binding by AAV2 [41].”
BackgroundSelf-citationCryo-electron Microscopy of Adeno-associated Virus
Stagg, S. M., Yoshioka, C., Davulcu, O., & Chapman, M. S. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00936 · Cited by 47 · see citing works
Cabanes‐Creus, M., Westhaus, A., Navarro, R. G., Baltazar, G., Zhu, E., Amaya, A. K., Liao, S. H. Y., Scott, S., Sallard, E., Dilworth, K. L., et al. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.05.004 · Cited by 45 · see citing works
“Specifically, AAV2, AAV3, AAV6, and AAV13 use residues located in VR-V, VR-VI, and VR-VIII to bind HSPG.(30,36,37).”
BackgroundInfluentialSelf-citationStructures and Functions of Parvovirus Capsids and the Process of Cell Infection
Parrish, C. R. (2010) · Current topics in microbiology and immunology · doi:10.1007/82_2010_33 · Cited by 44 · see citing works
“HSPG binding is associated with surface-exposed patches of positively charged residues, and binding induces small changes in the capsid structure, which are detectable by cryoEM analysis (Levy et al. 2009; O’Donnell et al. 2009) (Fig.”
BackgroundThe structure of AAVrh32.33, a novel gene delivery vector
Mikals, K., Nam, H.-J., Vliet, K. V., Vandenberghe, L. H., Mays, L. E., McKENNA, R. V., Wilson, J. M., & Agbandje‐McKenna, M. (2014) · Journal of Structural Biology · doi:10.1016/j.jsb.2014.03.020 · Cited by 40 · see citing works
Self-citationGlycated AAV vectors: chemical redirection of viral tissue tropism
Horowitz, E. D., Weinberg, M. S., & Asokan, A. (2011) · Bioconjugate Chemistry · doi:10.1021/bc100477g · Cited by 40 · see citing works
Shen, S., Troupes, A. N., Pulicherla, N., & Asokan, A. (2013) · Journal of Virology · doi:10.1128/jvi.02109-13 · Cited by 40 · see citing works
Engineering AAV receptor footprints for gene therapy
Madigan, V. J., & Asokan, A. (2016) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.05.001 · Cited by 37 · see citing works
Xie, Q., Spear, J. M., Noble, A. J., Sousa, D. R., Meyer, N., Davulcu, O., Zhang, F., Linhardt, R. J., Stagg, S. M., & Chapman, M. S. (2017) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2017.02.004 · Cited by 36 · see citing works
Peptide ligands for the affinity purification of adeno‐associated viruses from HEK 293 cell lysates
Chu, W., Shastry, S., Barbieri, E., Prodromou, R., Greback‐Clarke, P., Smith, W. K., Moore, B., Kilgore, R., Cummings, C., Pancorbo, J., et al. (2023) · Biotechnology and Bioengineering · doi:10.1002/bit.28495 · Cited by 33 · see citing works
“…capsid proteins VP1 (~87 kDa), VP2 (~73 kDa), and VP3 (~62 kDa) in the correct ~1:1:10 ratio (DiMattia et al., 2012; Drouin & Agbandje‐McKenna, 2013; Levy et al., 2009) based on the densitometric analysis of the gels, corroborating our interpretative hypothesis that only fully formed capsids are…”
BackgroundArnett, A. L. H., Beutler, L. R., Quintana, A., Allen, J. M., Finn, E. E., Palmiter, R. D., & Chamberlain, J. S. (2012) · Gene Therapy · doi:10.1038/gt.2012.60 · Cited by 33 · see citing works
Structure comparison of the chimeric AAV2.7m8 vector with parental AAV2
Bennett, A., Keravala, A., Makal, V., Kurian, J., Belbellaa, B., Aeran, R., Tseng, Y.-S., Sousa, D., Spear, J., Gasmi, M., et al. (2020) · Journal of Structural Biology · doi:10.1016/j.jsb.2019.107433 · Cited by 33 · see citing works
“For example, for AAV2, two critical residues required for binding HS, R585 and R588, reside within VR-VIII, and the 511-NGR-513 proposed to play a role in α5β1 co-receptor binding is flanked by VR-I and VR-IV (Asokan et al., 2006; Kern et al., 2003; Levy et al., 2009; Ng et al., 2010; Opie et al., 2003; Shen et al., 2…”
BackgroundInfluentialSelf-citationZeng, C., Møller-Tank, S., Asokan, A., & Dragnea, B. G. (2017) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.6b10131 · Cited by 33 · see citing works
Zhang, L., Rossi, A., Lange, L., Meumann, N., Koitzsch, U., Christie, K. A., Nesbit, M. A., Moore, C. B. T., Hacker, U. T., Morgan, M. A., et al. (2019) · Human Gene Therapy · doi:10.1089/hum.2019.027 · Cited by 33 · see citing works
“Given the dependency of AAV2 on HSPG for subsequent steps in cell transduction, such as priming the capsid for co-receptor binding, endosomal escape, and uncoating, 32 it is reasonable to postulate that the low HSPG expression level negatively impacts AAV2 transduction efficiency.”
Barbash, I. M., Cecchini, S., Faranesh, A. Z., Virág, T., Li, L., Yang, Y., Hoyt, R. F., Kornegay, J. N., Bogan, J. R., Garcı́a, L., et al. (2012) · Gene Therapy · doi:10.1038/gt.2012.38 · Cited by 32 · see citing works
Functional Analysis of the Putative Integrin Recognition Motif on Adeno-associated Virus 9
Shen, S., Berry, G. E., Rivera, R. M. C., Cheung, R., Troupes, A. N., Brown, S. M., Kafri, T., & Asokan, A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.608281 · Cited by 26 · see citing works
Choijilsuren, G., Jhou, R., Chou, S.-F., Chang, C.-J., Yang, H., Chen, Y.-Y., Chuang, W., Yu, M., & Shih, C. (2017) · Scientific Reports · doi:10.1038/s41598-017-14573-9 · Cited by 27 · see citing works
Atomic Resolution Structures of Human Bufaviruses Determined by Cryo-Electron Microscopy
Ilyas, M., Mietzsch, M., Kailasan, S., Väisänen, E., Luo, M., Chipman, P. R., Smith, J. K., Kurian, J. J., Sousa, D. R., McKENNA, R. V., et al. (2018) · Viruses · doi:10.3390/v10010022 · Cited by 25 · see citing works
Self-citationConformational Changes in Adeno-Associated Virus Type 1 Induced by Genome Packaging
Gerlach, B., Kleinschmidt, J. A., & Böttcher, B. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.03.062 · Cited by 24 · see citing works
Adeno‐associated virus serotype 2 capsid variants for improved liver‐directed gene therapy
Meumann, N., Cabanes‐Creus, M., Ertelt, M., Navarro, R. G., Lucifora, J., Yuan, Q., Nien‐Huber, K., Abdelrahman, A. M., Vu, X., Zhang, L. N., et al. (2022) · Hepatology · doi:10.1002/hep.32733 · Cited by 25 · see citing works
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Exploiting Natural Diversity of AAV for the Design of Vectors with Novel Properties
Gao, G., Li, Z., & Danos, O. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-370-7_4 · Cited by 22 · see citing works
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Bioengineered Viral Platform for Intramuscular Passive Vaccine Delivery to Human Skeletal Muscle
Paulk, N. K., Pekrun, K., Charville, G. W., Maguire, K., Wosczyna, M. N., Xu, J., Zhang, Y., Lisowski, L., Yoo, B., Vilches-Moure, J. G., et al. (2018) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2018.06.001 · Cited by 19 · see citing works
Multiparametric domain insertional profiling of adeno-associated virus VP1
Hoffmann, M. D., Zdechlik, A. C., He, Y., Nedrud, D. M., Aslanidi, G., Gordon, W. R., & Schmidt, D. (2023) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2023.101143 · Cited by 17 · see citing works
Structural Insight into Non-Enveloped Virus Binding to Glycosaminoglycan Receptors: A Review
Sorin, M. N., Kuhn, J., Stasiak, A. C., & Stehle, T. (2021) · Viruses · doi:10.3390/v13050800 · Cited by 17 · see citing works
“Among the first structures of AAV–GAG complexes are two examples that were solved before the cryoEM “resolution revolution” [17], at lower resolutions of 18 Å [18] and 8 Å [19].”
BackgroundStructural characterization of a bat Adeno-associated virus capsid
Mietzsch, M., Li, Y., Kurian, J. J., Smith, J. K., Chipman, P. R., McKENNA, R. V., Yang, L., & Agbandje‐McKenna, M. (2020) · Journal of Structural Biology · doi:10.1016/j.jsb.2020.107547 · Cited by 17 · see citing works
Self-citationXie, Q., Spilman, M. S., Meyer, N., Lerch, T. F., Stagg, S. M., & Chapman, M. S. (2013) · Journal of Structural Biology · doi:10.1016/j.jsb.2013.09.004 · Cited by 17 · see citing works
Macdonald, J., Marx, J., & Büning, H. (2021) · Human Gene Therapy · doi:10.1089/hum.2021.169 · Cited by 16 · see citing works
“26 The VRs mentioned earlier are primarily found at capsid protrusions, which represent sites of interactions between AAVs and the host cell and define receptor binding and immunogenicity.”
Ye, X., Hu, Y., Qiu, H., & Li, N. (2024) · Protein Science · doi:10.1002/pro.5074 · Cited by 13 · see citing works
Zhang, Y., Chen, Z., Wang, X., Yan, R., Bao, H., Chu, X., Guo, L., Wang, X., Li, Y., Mu, Y., et al. (2024) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.07.023 · Cited by 13 · see citing works
Research Progress on Antiviral Activity of Heparin
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The amazing AAV capsids: Into the structure-verse
Hsi, J., Mietzsch, M., & McKENNA, R. V. (2025) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2025.101629 · Cited by 8 · see citing works
“146 Similarly, a synthetic heparinoid was complexed with the engineered AAV-DJ capsid (see the capsid structures of engineered AAVs section) by cryo-EM at 2.8 Å resolution, showing density for the glycan at the apices of the 3-fold protrusions.”
InfluentialSelf-citationUse of a Lower Dosage Liver-Detargeted AAV Vector to Prevent Hamster Muscular Dystrophy
Rotundo, I. L., Lancioni, A., Savarese, M., D’Orsi, L., Iacomino, M., Nigro, G., Piluso, G., Auricchio, A., & Nigro, V. (2013) · Human Gene Therapy · doi:10.1089/hum.2012.121 · Cited by 6 · see citing works
“424 residue 520 or residues 560–590, corresponding to the heparan sulfate (HS) binding site (Hileman et al., 1998; Summerford and Samulski, 1998; Wu et al., 2000; Shi et al., 2001; Levy et al., 2009) that acts as a primary receptor.”
BackgroundThe Role of Carbohydrates in Viral Infections
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Adeno-associated Virus as a Mammalian DNA Vector
Salganik, M., Hirsch, M. L., & Samulski, R. J. (2015) · ASM Press eBooks · doi:10.1128/9781555819217.ch37 · Cited by 4 · see citing works
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Biologics-device combinations: Enabling prolonged therapies in the posterior segment ocular disease
Zhu, S., Zhang, J., Jiang, X., Peng, C., Liu, H., & Qian, F. (2026) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2026.115773 · Cited by 3 · see citing works
Viral Vectors for Gene Delivery
Dismuke, D. J., Gray, S. J., Hirsch, M. L., Samulski, R. J., & Muzyczka, N. (2010) · Royal Society of Chemistry eBooks · doi:10.1039/9781849732239-00338 · Cited by 3 · see citing works
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“…vectors with wild-type capsids, interactions with extracellular matrix components, such as heparan sulfate proteoglycan (HSPG) for AAV2, initiate cell transduction and facilitate binding to coreceptors, 32 promoting the internalization process, for example, through clathrin-dependent endocytosis.”
Cui, M., Liu, H., Cai, L., Zhang, Q., Yuan, L., Gao, C., Li, C., Xi, J., Li, Y., Wu, C., et al. (2026) · Molecular Therapy Advances · doi:10.1016/j.omta.2026.201806 · Cited by 1 · see citing works
“32,44 The investigation into the mechanisms underlying the enhanced transduction profile of AAV2.”
Nonenveloped Capsid: Mechanisms of Viral Entry
Lins, B., & Agbandje‐McKenna, M. (2014) · Future Virology · doi:10.2217/fvl.14.82 · Cited by 1 · see citing works
Self-citationImmune System Obstacles to In vivo Gene Transfer with Adeno-Associated Virus Vectors
Büning, H., & Mingozzi, F. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800563-7.00004-x · Cited by 1 · see citing works
UNDERSTANDING THE SOLUTION-PHASE BIOPHYSICS AND CONFORMATIONAL DYNAMICS OF VIRUS CAPSIDS
Rayaprolu, V. (2013) · Montana State University ScholarWorks (Montana State University)
- Authors
- Levy, H. C., Bowman, V. D., Govindasamy, L., McKenna, R., Nash, K., Warrington, K., Chen, W., Muzyczka, N., Yan, X., Baker, T. S., & Agbandje-McKenna, M.
- Affiliations
- University of Florida (US)
- Purdue University West Lafayette (US)
- University of California San Diego (US)
- Venue
- Journal of Structural Biology
- Publisher
- Elsevier BV
- Published
- 2009-03
- Volume
- 165
- Issue
- 3
- Pages
- 146-156
- ISSN
- 1047-8477 (ISSN-L)
- PMC
- PMC3694330
- OpenAlex
- W2156683693
- Cited by
- 110
- References
- 76
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 8 · 2020: 3 · 2019: 10 · 2018: 2 · 2017: 5 · 2016: 7 · 2015: 8 · 2014: 10 · 2013: 11 · 2012: 10
- FWCI
- 4.13
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Structural Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (4r37gm033050-27)
- National Heart, Lung, and Blood Institute (P01HL059412, P01HL051811)
- National Institute of General Medical Sciences (R37GM-033050)
- National Institute of Allergy and Infectious Diseases (P01AI045976)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
- Keywords
- AAV2, heparin binding, capsid conformational change, heparan sulfate proteoglycans, capsid structure
- MeSH terms
- Dependovirus, Capsid, Heparin, Image Processing, Computer-Assisted, Models, Molecular, Protein Conformation, Virion, Mutagenesis, Site-Directed, Nucleocapsid, Cryoelectron Microscopy, Capsid Proteins
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