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Hepatocyte Growth Factor Receptor Is a Coreceptor for Adeno-Associated Virus Type 2 Infection
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After the first attachment of virus to the cell surface through a primary receptor, efficient entry of virus requires the presence of a coreceptor. For adeno-associated virus type 2 (AAV2) infection, heparan sulfate proteoglycan is supposed as the primary receptor, and αvβ5 integrin and FGFR1 are reported to act as coreceptors. In this study, we were able to demonstrate that hepatocyte growth factor receptor, c-Met, is also a coreceptor for AAV2 infection. AAV2-mediated transgene analyses revealed that c-Met expression significantly up-regulated transgene expression without increasing AAV2 cell binding. Moreover, a viral overlay assay elucidated the physical interaction between AAV2 and the β subunit of c-Met. These data suggest that c-Met plays the role of coreceptor for AAV2 infection by facilitating AAV2 internalization into the cytoplasm.
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“The early steps of AAV infection involve attachment to a variety of cell surface receptors such as HSPG, FGFR, αvβ5 integrin, and hepatocyte growth factor receptor (c-Met) (Fig. 8I) (9, 25, 31, 39, 40), followed by clathrin-dependent endocytosis (Fig.8II).”
From Packaging Capacity of Adeno-Associated Virus Serotypes: Impact of Larger Genomes on Infectivity and Postentry Steps (2005) · cites this paper as [25]
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“Internalization is enhanced by interactions with one or more of at least six known coreceptors including V5 integrins (63), fibroblast growth factor receptor 1 (53), hepatocyte growth factor receptor ( 35 ), v1 integrin (7), and laminin receptor (3).”
BackgroundAdeno-associated Virus Serotypes: Vector Toolkit for Human Gene Therapy
Wu, Z., Asokan, A., & Samulski, R. J. (2006) · Molecular Therapy · doi:10.1016/j.ymthe.2006.05.009 · Cited by 957
“Subsequent interactions with human fibroblast growth factor receptor 1 (FGFR1) [73], hepatocyte growth factor receptor [74], and integrins aVh5/a5h1 ([75], A.”
BackgroundZhong, L., Li, B., Mah, C. S., Govindasamy, L., Agbandje-McKenna, M., Cooper, M., Herzog, R. W., Zolotukhin, I., Warrington, K. H., Weigel-Van Aken, K. A., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802866105 · Cited by 558
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“However, we hypothesize that since AAV2 uses at least four other receptors (16, 22, 28, 29), blocking one (LamR) might have only marginal effects on AAV2 binding.”
BackgroundGrieger, J. C., & Samulski, R. J. (2005) · Journal of Virology · doi:10.1128/jvi.79.15.9933-9944.2005 · Cited by 419
“8I) (9, 25, 31, 39, 40), followed by clathrin-dependent endocytosis (Fig.”
In vivo tissue-tropism of adeno-associated viral vectors
Srivastava, A. (2016) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.08.003 · Cited by 346
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“AAV2, which has been demonstrated to use integrin V 5, basic fibroblast growth factor receptor, or hepatocyte growth factor receptor as its coreceptor for cell entry (20, 30, 41), was much less sensitive to proteinase K treatment for transduction (Fig.”
BackgroundVarious AAV Serotypes and Their Applications in Gene Therapy: An Overview
Issa, S. S., Shaimardanova, A. A., Solovyeva, V. V., & Rizvanov, A. A. (2023) · Cells · doi:10.3390/cells12050785 · Cited by 339
“The developed strategies suggested different approaches, mainly, capsid modification of AAV3 vectors [76,80,81] and modification of hHGFR expression levels, along with the tyrosine kinase activity associated with it [78].”
BackgroundInfluentialSonntag, F., Bleker, S., Leuchs, B., Fischer, R., & Kleinschmidt, J. A. (2006) · Journal of Virology · doi:10.1128/jvi.01056-06 · Cited by 297
“Infection of cultured cells by adeno-associated virus type 2 (AAV2) is initiated by binding to heparan sulfate proteoglycan as an attachment receptor followed by interaction with either human fibroblast growth factor receptor 1, integrin V 5, or hepatocyte growth factor receptor (35, 50, 62, 63).”
BackgroundNovel properties of tyrosine-mutant AAV2 vectors in the mouse retina
Petrs-Silva, H., Dinculescu, A., Li, Q., Deng, W.-T., Pang, J.-J., Min, S.-H., Chiodo, V., Neeley, A. W., Govindasamy, L., Bennett, A., et al. (2011) · Molecular Therapy · doi:10.1038/mt.2010.234 · Cited by 267
Adeno-associated virus: from defective virus to effective vector
Gonçalves, M. A. F. V. (2005) · Virology Journal · doi:10.1186/1743-422x-2-43 · Cited by 285
“AAV2 virions utilize as primary attachment receptor heparan sulphate proteoglycans [20] while internalisation is aided by the co-receptors αvβ5 integrin heterodimers [21], fibroblast growth factor receptor type 1 [22] and the hepatocyte growth factor receptor, c-Met [23].”
BackgroundEllis, B. L., Hirsch, M. L., Barker, J. C., Connelly, J. P., Steininger, R. J., & Porteus, M. H. (2013) · Virology Journal · doi:10.1186/1743-422x-10-74 · Cited by 252
“In some cases our results did not match perfectly with previous results [23] (for example AAV1, AAV2, AAV5 on C2C12 cells; AAV1, AAV2, AAV5 on CHOK1 cells).”
BackgroundInfluentialIntracellular transport of recombinant adeno-associated virus vectors
Nonnenmacher, M., & Weber, T. (2012) · Gene Therapy · doi:10.1038/gt.2012.6 · Cited by 258
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
Zhong, L., Li, B., Jayandharan, G., Mah, C. S., Govindasamy, L., Agbandje-McKenna, M., Herzog, R. W., Weigel-Van Aken, K. A., Hobbs, J. A., Zolotukhin, S., et al. (2008) · Virology · doi:10.1016/j.virol.2008.08.027 · Cited by 232
“Several fundamental steps in the life cycle of AAV2 vectors, such as viral binding and entry (Kashiwakura et al., 2005; Qing et al., 1999; Summerford et al., 1999; Summerford and Samulski, 1998), intracellular trafficking (Douar et al., 2001; Hansen et al., 2000, 2001; Sanlioglu et al., 2000; Zhao…”
BackgroundAAV 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
Lochrie, 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
“Besides heparan sulfate (48), the v 5 integrin receptor (47), the fibroblast growth factor receptor FGFR1 (37), and the hepatocyte growth factor receptor (24) have also been proposed to be receptors required for AAV-2 transduction.”
BackgroundTwenty-Five Years of Structural Parvovirology
Mietzsch, M., Pénzes, J. J., & Agbandje-McKenna, M. (2019) · Viruses · doi:10.3390/v11040362 · Cited by 197
AAV hybrid serotypes: improved vectors for gene delivery
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“Following this work, several proteinaceous coreceptors, such as fibroblast growth factor receptor 1 (FGFR-1) (18), integrin V 5 (19), and the hepatocyte growth factor receptor (c-Met) (20), were implicated in AAV2 entry.”
BackgroundRecent developments in adeno‐associated virus vector technology
Büning, H., Perabò, L., Coutelle, O., Quadt‐Humme, S., & Hallek, M. J. (2008) · The Journal of Gene Medicine · doi:10.1002/jgm.1205 · Cited by 204
“AAV-1 Not described Not described AAV-2 Heparan sulphate proteoglycan (HSPG) [30] FGFR-1 [170] HGFR, c-met [171] Laminin receptor [172] αvβ5 [173] α5β1 [31] AAV-3 Heparan sulphate proteoglycan (HSPG) [69,174,175] FGFR-1 [174] Laminin receptor [172] AAV-4 O-linked sialic acid [176] AAV-5 N-linked sialic acid [176] Plat…”
BackgroundAsokan, A., Hamra, J. B., Govindasamy, L., Agbandje-McKenna, M., & Samulski, R. J. (2006) · Journal of Virology · doi:10.1128/jvi.00843-06 · Cited by 183
“In addition, AAV also appears to utilize several coreceptors, such as fibroblast growth receptor 1 and hepatocyte growth receptor by AAV2 (21, 31) and platelet-derived growth receptor by AAV5 (5), for successful cellular entry.”
BackgroundGrieger, J. C., Snowdy, S., & Samulski, R. J. (2006) · Journal of Virology · doi:10.1128/jvi.02723-05 · Cited by 172
“7, step 1) (6, 26, 43, 52, 53) followed by clathrin-mediated”
Comparative 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 168
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“…(HSPG) is the primary receptor for AAV2, which can utilize aVb5 integrin, fibroblast growth factor receptor-1, or hepatocyte growth factor receptor as co-receptors for internalization after binding to the cell surface (Kashiwakura et al. 2005; Qing et al. 1999; Summerford and Samulski 1998).”
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“, 1999), hepatocyte growth factor receptor (Kashiwakura et al., 2005) and laminin receptor (Akache et al.”
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“AAV2 6-O- and N-sulfated heparin Fibroblast [108]/hepatocyte [109] growth factor receptor; laminin receptor [110]; integrin αVβ5 [111] and α5β1 [112]”
BackgroundTargeting microglia with lentivirus and AAV: Recent advances and remaining challenges
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“Co-receptors such as the integrins Itgav and Itgb5 [66,67], hepatocyte growth factor receptor (c-MET) [68], and fibroblast growth factor receptor 1 (FGFR1) [69,70] have been implicated in AAV attachment and internalization, from which the integrins are expressed in microglia.”
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“…and integrins αVβ1 and αVβ5, though the latter has been questioned (Akache et al., 2006; Asokan et al., 2006; Blackburn, Steadman, and Johnson, 2005; Kashiwakura et al., 2005; Qing et al., 1999; Qiu and Brown, 1999; Smith, Collaco, and Trempe, 2004; Summerford, Bartlett, and Samulski, 1999).”
BackgroundClinical applications of retinal gene therapy
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“…binding of AAV serotype 2 (AAV2) is heparan sulphate (Summerford and Samulski, 1998), with avb5 integrin (Summerford et al., 1999), fibroblast growth factor-1 (Qing et al., 1999), hepatocyte growth factor (Kashiwakura et al., 2005) and laminin all implicated as coreceptors (Akache et al., 2006).”
BackgroundAn Alternate Route for Adeno-associated Virus (AAV) Entry Independent of AAV Receptor
Dudek, A. M., Pillay, S., Puschnik, A. S., Nagamine, C. M., Cheng, F., Qiu, J., Carette, J. E., & Vandenberghe, L. H. (2018) · Journal of Virology · doi:10.1128/jvi.02213-17 · Cited by 116
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The Role of the Adeno-Associated Virus Capsid in Gene Transfer
Vliet, K. V., Blouin, V., Brument, N., Agbandje‐McKenna, M., & Snyder, R. O. (2008) · Methods in molecular biology · doi:10.1007/978-1-59745-210-6_2 · Cited by 118
“After binding the cell surface, AAV2 can utilize secondary receptors, such as αVβ5 integrin, human fibroblast growth factor receptor-1 (FGFR-1), or hepatocyte growth factor (c-met), which mediate entry [44] [45] [46] [47] .”
BackgroundAdeno-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
Vulchanova, L., Schuster, D. J., Belur, L. R., Riedl, M. S., Podetz-Pedersen, K. M., Kitto, K. F., Wilcox, G. L., McIvor, R. S., & Fairbanks, C. A. (2010) · Molecular Pain · doi:10.1186/1744-8069-6-31 · Cited by 115
“For example, AAV2 utilizes heparan sulfate proteoglycans as receptors and a number of other cell-surface molecules, such as fibroblast growth factor receptor 1 and hepatocyte growth factor receptor, as co-receptors [22-26].”
BackgroundHeparin binding induces conformational changes in Adeno-associated virus serotype 2
Levy, H. C., Bowman, V. D., Govindasamy, L., McKenna, R., Nash, K., Warrington, K., Chen, W., Muzyczka, N., Yan, X., Baker, T. S., et al. (2009) · Journal of Structural Biology · doi:10.1016/j.jsb.2008.12.002 · Cited by 110
“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).”
BackgroundPopa-Wagner, R., Porwal, M., Kann, M., Reuss, M., Weimer, M., Florin, L., & Kleinschmidt, J. A. (2012) · Journal of Virology · doi:10.1128/jvi.00282-12 · Cited by 109
“The infection cycle of AAV2 is initiated by binding to cellular receptors, including heparan sulfate proteoglycan, v 5 integrin, 5 1 integrin, fibroblast growth factor receptor 1, hepatocyte growth factor receptor 1, and 36/67-kDa laminin receptor (1, 4, 31, 46, 53, 54) and subsequent endocytosis into the cell.”
BackgroundAdeno-associated virus 2 bound to its cellular receptor AAVR
Zhang, R., Cao, L., Cui, M., Sun, Z., Hu, M., Zhang, R., Stuart, W. S., Zhao, X., Yang, Z., Li, X., et al. (2019) · Nature Microbiology · doi:10.1038/s41564-018-0356-7 · Cited by 108
Completion of the AAV Structural Atlas: Serotype Capsid Structures Reveals Clade-Specific Features
Mietzsch, M., Jose, A., Chipman, P. R., Bhattacharya, N., Daneshparvar, N., McKENNA, R. V., & Agbandje‐McKenna, M. (2021) · Viruses · doi:10.3390/v13010101 · Cited by 105
“Among the cellular receptors are sialic acids [22–24], heparan sulfate proteoglycans (HSPG) [25–29], terminal galactose [30,31], sulfated N-acetyl-lactosamine [32], AAVR [33], laminin [34], αvβ1 integrin [35], αvβ5 integrin [36], the hepatocyte growth factor receptor [37], the fibroblast growth factor receptor [38], a…”
BackgroundLing, C., Lu, Y., Kalsi, J. K., Jayandharan, G. R., Li, B., Ma, W., Cheng, B., Gee, S. W. Y., McGoogan, K. E., Govindasamy, L., et al. (2010) · Human Gene Therapy · doi:10.1089/hum.2010.075 · Cited by 103
“We next wished to examine whether AAV3 uses murine HGFR as a coreceptor in an animal model in vivo , especially because HGFR has been shown to be a coreceptor for AAV2 (Kashiwakura et al ., 2005), and because transduction by both”
InfluentialHost determinants of adeno-associated viral vector entry
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RNA interference approaches for treatment of HIV-1 infection
Bobbin, M. L., Burnett, J., & Rossi, J. J. (2015) · Genome Medicine · doi:10.1186/s13073-015-0174-y · Cited by 96
“For example, AAV2 targets heparan sulfate proteoglycan, αVβ5 integrin and fibroblast growth receptor 1, which is found on hepatocytes, skeletal muscle cells, smooth muscle cells, and neurons [146].”
BackgroundPipe, S. W., Leebeek, F. W. G., Ferreira, V., Sawyer, E. K., & Pasi, J. (2019) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2019.08.015 · Cited by 92
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“…kinase to the tyrosines on the AAV2 capsid, the surface exposure of which may be determined in part by specific receptor and coreceptor binding as well as by the varied endosomal processing in these tissues (Qing et al., 1999; Kaludov et al., 2001; Kashiwakura et al., 2005; Seiler et al., 2006).”
BackgroundStructure of AAV-DJ, a Retargeted Gene Therapy Vector: Cryo-Electron Microscopy at 4.5 Å Resolution
Lerch, T. F., O’Donnell, J., Meyer, N., Xie, Q., Taylor, K. A., Stagg, S. M., & Chapman, M. S. (2012) · Structure · doi:10.1016/j.str.2012.05.004 · Cited by 88
“(Recent studies suggest that AAV serotypes, all of which vary structurally at VR-I, use several serotype-specific co-receptors for cell entry (Akache et al., 2006; Di Pasquale and Chiorini, 2003; Kashiwakura et al., 2005; Ling et al., 2010; Qing et al., 1999).)”
Stieger, K., Schroeder, J., Provost, N., Mendes-Madeira, A., Belbellaa, B., Meur, G. L., Weber, M., Deschamps, J.-Y., Lorenz, B., Moullier, P., et al. (2009) · Molecular Therapy · doi:10.1038/mt.2008.283 · Cited by 88
A muscle-targeting peptide displayed on AAV2 improves muscle tropism on systemic delivery
Yu, C.-Y., Yuan, Z., Cao, Z., Wang, B., Qiao, C., Li, J., & Xiao, X. (2009) · Gene Therapy · doi:10.1038/gt.2009.59 · Cited by 90
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 93
Akache, B., Grimm, D., Shen, X., Fuess, S., Yant, S. R., Glazer, D. S., Park, J., & Kay, M. A. (2007) · Molecular Therapy · doi:10.1038/sj.mt.6300053 · Cited by 87
“[8] [9] [10] [11] In contrast, AAV5 preferentially attaches to cells by binding to sialic acid and the platelet-derived growth factor receptor, 12, 13 explaining the distinct tissue tropisms displayed by this serotype.”
BackgroundGrieger, J. C., Johnson, J. S., Gurda-Whitaker, B., Agbandje-McKenna, M., & Samulski, R. J. (2007) · Journal of Virology · doi:10.1128/jvi.00580-07 · Cited by 83
“The early steps of AAV2 infection begin with attachment to heparan sulfate proteoglycan and to a variety of cell surface receptors, such as FGFR, V 5 integrin, 5 1 integrin, and hepatocyte growth factor receptor (c-Met) (4, 14, 22, 32, 38, 39), followed by clathrin dependent endocytosis.”
BackgroundRoyo, N. C., Vandenberghe, L. H., Ma, J.-Y., Hauspurg, A. K., Yu, L., Maronski, M., Johnston, J., Dichter, M. A., Wilson, J. M., & Watson, D. J. (2007) · Brain Research · doi:10.1016/j.brainres.2007.11.015 · Cited by 86
Mapping the Structural Determinants Required for AAVrh.10 Transport across the Blood-Brain Barrier
Albright, B. H., Storey, C. M., Murlidharan, G., Castellanos Rivera, R. M., Berry, G. E., Madigan, V. J., & Asokan, A. (2018) · Molecular Therapy · doi:10.1016/j.ymthe.2017.10.017 · Cited by 82
Custom Adeno-Associated Virus Capsids: The Next Generation of Recombinant Vectors with Novel Tropism
Muzyczka, N., & Warrington, K. H. (2005) · Human Gene Therapy · doi:10.1089/hum.2005.16.408 · Cited by 84
Altering AAV tropism with mosaic viral capsids
Gigout, L. I., Rebollo, P., Clement, N., Warrington, K. H., Muzyczka, N., Linden, R. M., & Weber, T. (2005) · Molecular Therapy · doi:10.1016/j.ymthe.2005.03.005 · Cited by 79
López-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 80
“Molecules with specific binding properties or functional activity as parvovirus receptors have been identified for some members of the family, such as the ABP protein for the Aleutian disease virus (28); some globosides and the 5 1 integrin for the human parvovirus B19 (12, 40, 88); transferrin receptors for canine (C…”
BackgroundInfluentialChowdhury, 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 80
Nieuwenhuis, B., Laperrousaz, E., Tribble, J. R., Verhaagen, J., Fawcett, J. W., Martin, K. R. G., Williams, P. A., & Osborne, A. (2023) · Gene Therapy · doi:10.1038/s41434-022-00380-z · Cited by 81
“Comparison of five promoters for transgene expression AAV2 cell entry is primarily achieved by binding heparin sulfate proteoglycans [77–81] and interacting with co-receptors on the cell surface such as the adeno-associated virus receptor [82, 83], the 37/67-kilodalton laminin receptor [84], αVβ5 integrin [85], hepato…”
BackgroundTumor vascular targeting therapy with viral vectors
Liu, Y., & Deisseroth, A. (2005) · Blood · doi:10.1182/blood-2005-10-4114 · Cited by 74
The parvovirus capsid odyssey: from the cell surface to the nucleus
Harbison, C. E., Chiorini, J. A., & Parrish, C. R. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2008.01.012 · Cited by 73
The next step in gene delivery: Molecular engineering of adeno-associated virus serotypes
Wang, J., Faust, S. M., & Rabinowitz, J. E. (2010) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2010.10.017 · Cited by 69
“More recently, Kashiwakura described AAV2 using hepatocyte growth factor as a co-receptor, Asokan showed integrin α5β1 binds AAV2 and that binding increases the efficiency of transduction, andAkache demonstrated that AAV2, 3, 8 and9 bind the 37/67 laminin receptor [29–31].”
BackgroundRetinal gene delivery by adeno-associated virus (AAV) vectors: Strategies and applications
Schön, C., Biel, M., & Michalakis, S. (2015) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2015.01.009 · Cited by 72
“AAV2 is the best characterized serotype and therefore several binding partners on the cell surface were identified including heparan sulfate proteoglycan [53] and different possible co-receptors such as the fibroblast growth factor receptor 1 [54], aVb5 integrin [55], hepatocyte growth factor receptor [56] and laminin…”
BackgroundManini, A., Abati, E., Nuredini, A., Corti, S. P., & Comi, G. P. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2021.814174 · Cited by 76
Comparative 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
“, AAVR (38), laminin (39), v 1 integrin (40), v 5 integrin (41), the hepatocyte growth factor receptor (42), the fibroblast growth factor receptor (43), and platelet-derived growth factor receptor (44).”
BackgroundLee, S. H., Tang, Y.-Q., Rathakrishnan, A., Wang, S. M., Ong, K. C., Manikam, R., Payne, B. J., Jaganath, I. B., & Sekaran, S. D. (2013) · BMC Complementary and Alternative Medicine · doi:10.1186/1472-6882-13-192 · Cited by 66
“The HGF receptor (HGFR) has been implied as a co-receptor for adeno-associated virus type 2 infections [43], and although this has not been shown for dengue virus entry, the HGF per se has been found to be increased in the serum of dengue infected patients [44].”
Michelfelder, S., Lee, M., deLima-Hahn, E., Wilmes, T., Kaul, F., Müller, O. J., Kleinschmidt, J. A., & Trepel, M. (2007) · Experimental Hematology · doi:10.1016/j.exphem.2007.07.018 · Cited by 65
Adeno-Associated Virus 2 at 2.8 ang
Lou, Z. Y., & Zhang, R. (2018) · Worldwide Protein Data Bank · doi:10.2210/pdb6ih9/pdb · Cited by 66
AAVR: A Multi-Serotype Receptor for AAV
Summerford, C., & Samulski, R. J. (2016) · Molecular Therapy · doi:10.1038/mt.2016.49 · Cited by 61
Adeno-associated virus capsid antigen presentation is dependent on endosomal escape
Li, C., He, Y., Nicolson, S., Hirsch, M., Weinberg, M. S., Zhang, P., Kafri, T., & Samulski, R. J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci66611 · Cited by 61
“In the current paradigm, AAV2 transduction is initiated by capsid binding to HSPG as a primary receptor, followed by interaction with coreceptors (19–24).”
Hondermarck, H., Bartlett, N. W., & Nurcombe, V. (2020) · FASEB BioAdvances · doi:10.1096/fba.2020-00015 · Cited by 61
“44 Pharmacological inhibition of the NGF receptor TrkA has been shown to suppress influenza virus replication.”
BackgroundJin, X., Liu, L., Nass, S., O’Riordan, C. R., Pastor, E., & Zhang, X. K. (2017) · Human Gene Therapy Methods · doi:10.1089/hgtb.2016.178 · Cited by 62
López-Gordo, E., Chamberlain, K., Riyad, J. M., Kohlbrenner, E., & Weber, T. (2024) · Viruses · doi:10.3390/v16030442 · Cited by 68
“…have roles in AAV2 binding and transduction (e.g., fi broblast growth factor receptor 1 (FGFR1) [91], α V β 5 and α 5 β 1 integrin [92–94], hepatocyte growth factor receptor (HGFR) [95], and laminin receptor (LR) [96]) but, later, could not be validated as essential factors in transduction [97–99].”
BackgroundCheng, B., Ling, C., Dai, Y., Lu, Y., Glushakova, L. G., Gee, S. W. Y., McGoogan, K. E., Aslanidi, G., Park, M., Stacpoole, P. W., et al. (2011) · Gene Therapy · doi:10.1038/gt.2011.105 · Cited by 59
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 57
“For example, the hepatocyte growth factor receptor (c-MET) and human fibroblast growth factor receptor-1 (FGFR1) were identified as possible protein co-receptors for AAV2 [175,176].”
BackgroundParvoviruses: Structure and Infection
Halder, S., Ng, R., & Agbandje‐McKenna, M. (2012) · Future Virology · doi:10.2217/fvl.12.12 · Cited by 53
Watanabe, M., Nasu, Y., Kashiwakura, Y., Kusumi, N., Tamayose, K., Nagai, A., Sasano, T., Shimada, T., Daida, H., & Kumon, H. (2005) · Human Gene Therapy · doi:10.1089/hum.2005.16.699 · Cited by 53
Self-citationControlled release strategies for rAAV-mediated gene delivery
Rey‐Rico, A., & Cucchiarini, M. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.10.015 · Cited by 52
Wagner, H. J., Weber, W., & Fussenegger, M. (2021) · Advanced Science · doi:10.1002/advs.202004018 · Cited by 52
Cryo-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 48
Attachment of adeno-associated virus type 3H to fibroblast growth factor receptor 1
Blackburn, S. D., Steadman, R., & Johnson, F. B. (2005) · Archives of Virology · doi:10.1007/s00705-005-0650-6 · Cited by 47
“cell entry receptors or coreceptors for AAV-2 include human FGFR-1 [9], αVβ5 integrin [12], and hepatocyte growth factor receptor (c-Met) [ 6 ].”
BackgroundStructural and cellular biology of adeno-associated virus attachment and entry
Zengel, J. R., & Carette, J. E. (2020) · Advances in virus research · doi:10.1016/bs.aivir.2020.01.002 · Cited by 47
AAV-8 and AAV-9 Vectors Cooperate with Serum Proteins Differently Than AAV-1 and AAV-6
Denard, J., Rouillon, J., Léger, T., Garcia, C., Lambert, M. P., Griffith, G., Jenny, C., Camadro, J., Garcı́a, L., & Svinartchouk, F. (2018) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2018.08.001 · Cited by 44
Targeted Gene Therapy for the Treatment of Heart Failure
Rapti, K., Chaanine, A. H., & Hajjar, R. J. (2011) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2011.02.005 · Cited by 43
Characterization of Interactions between Heparin/Glycosaminoglycan and Adeno-Associated Virus
Zhang, F., Aguilera, J. J., Beaudet, J. M., Xie, Q., Lerch, T. F., Davulcu, O., Colón, W., Chapman, M. S., & Linhardt, R. J. (2013) · Biochemistry · doi:10.1021/bi4008676 · Cited by 40
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Sipo, I., Fechner, H., Pinkert, S., Suckau, L., Wang, X., Weger, S., & Poller, W. C. (2007) · Gene Therapy · doi:10.1038/sj.gt.3302987 · Cited by 41
Enhanced transduction of mouse salivary glands with AAV5-based vectors
Katano, H., Kok, M. R., Cotrim, A. P., Yamano, S., Schmidt, M., Afione, S. A., Baum, B. J., & Chiorini, J. A. (2005) · Gene Therapy · doi:10.1038/sj.gt.3302691 · Cited by 39
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
Jayandharan, G. R., Li, Z., Sack, B. K., Rivers, A. E., Li, M., Li, B., Herzog, R. W., & Srivastava, A. (2009) · Human Gene Therapy · doi:10.1089/hum.2009.100 · Cited by 38
“…(Akache et al. , 2006) as opposed to the AAV2 sero-type, for which apart from the primary receptor, heparan sulfate proteoglycan (Summerford and Samulski, 1998), at least six different cellular coreceptors are known to exist (Qing et al. , 1999; Summerford et al. , 1999; Kashiwakura et al. , 2005).”
Viral mechanisms for docking and delivering at nuclear pore complexes
Flatt, J. W., & Greber, U. F. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.05.008 · Cited by 37
Gene Replacement Therapies for Duchenne Muscular Dystrophy Using Adeno-Associated Viral Vectors
Seto, J. T., Ramos, J. N., Muir, L. A., Chamberlain, J. S., & Odom, G. L. (2012) · Current Gene Therapy · doi:10.2174/156652312800840603 · Cited by 37
High-Throughput Dissection of AAV–Host Interactions: The Fast and the Curious
Herrmann, A.-K., & Grimm, D. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.05.022 · Cited by 33
Emmanuel, S. N., Mietzsch, M., Tseng, Y.-S., Smith, J. K., & Agbandje‐McKenna, M. (2020) · Viral Immunology · doi:10.1089/vim.2020.0022 · Cited by 33
“The AAVs utilize various glycan and protein receptors (5,32,56,65,82, 96,100,121,128,132) for cell attachment and entry, and thus differ in tissue tropism (42,102,119).”
Background
Metadata
- Authors
- Kashiwakura, Y., Tamayose, K., Iwabuchi, K., Hirai, Y., Shimada, T., Matsumoto, K., Nakamura, T., Watanabe, M., Oshimi, K., & Daida, H.
- Affiliations
- Juntendo University (JP)
- Nippon Medical School (JP)
- The University of Osaka (JP)
- Okayama University (JP)
- Departments of Cardiology
- Corresponding author
- Tamayose, Kenji
- ORCID
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2005-01
- Volume
- 79
- Issue
- 1
- Pages
- 609-614
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC538679
- OpenAlex
- W2120683337
- Cited by
- 246
- References
- 37
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 8 · 2022: 11 · 2021: 16 · 2020: 10 · 2019: 12 · 2018: 8 · 2017: 13 · 2016: 9 · 2015: 15 · 2014: 8 · 2013: 13 · 2012: 12
- FWCI
- 8.92
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Virology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Viral Infectious Diseases and Gene Expression in Insects
- Keywords
- adeno-associated virus type 2, c-Met, co-receptors, viral entry, heparan sulfate proteoglycans, integrin αvβ5, FGFR1, transgene expression, viral internalization, receptor interaction
- MeSH terms
- Dependovirus, Animals, Cricetinae, HeLa Cells, Humans, Receptors, Virus, Transduction, Genetic, CHO Cells, 3T3 Cells, Hepatocyte Growth Factor, Proto-Oncogene Proteins c-met, Mice
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