Library Selection and Directed Evolution Approaches to Engineering Targeted Viral Vectors

Jang, Jae‐Hyung; Lim, Kwang‐il; Schaffer, David V.

doi:10.1002/bit.21541

Cited by 26Virus-based gene therapy researchRNA Interference and Gene DeliveryNanoparticle-Based Drug Delivery

Library Selection and Directed Evolution Approaches to Engineering Targeted Viral Vectors

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Jang, Jae‐Hyung, Lim, Kwang‐il, Schaffer, David V.·2007·Biotechnology and Bioengineering

DOI 10.1002/bit.21541

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Abstract

Gene therapy, to delivery of genetic material to a patient for therapeutic benefit, has significant promise for translating basic knowledge of disease mechanism into biomedical treatments. The clinical development of the field has been slowed, however, by the need for improvements in the properties and capabilities of gene delivery vehicles. Vehicles based on viruses offer the potential for efficient gene delivery, but because viruses did not evolve to serve human therapeutic needs, many of their properties require significant improvement, including their safety, efficiency, and capacity for targeted gene delivery. Since viruses are highly complex biological entities, engineering such properties at the molecular level can be challenging. However, there has been significant progress in developing approaches that mimic the mechanisms by which viruses arose in the first place. In particular, library‐based selection, the generation of one diverse genetic library and selection for new properties, and directed evolution, based on the multiple rounds of library generation and selection for iterative improvement of function, have strong potential in engineering novel properties into these complex biomolecular assemblies. This review will discuss progress in the application of peptide display, library selection, and directed evolution technologies toward engineering vectors based on retrovirus, adeno‐associated virus, and adenovirus that are capable of targeted delivery to specific cell types. In addition to creating biomedically useful products, these approaches have future potential to yield novel insights into viral structure–function relationships. Biotechnol. Bioeng. 2007;98:515–524. © 2007 Wiley Periodicals, Inc.

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Directed evolution-based vector engineering allows testing of a large variety of rAAV variants in vivo, leading to selection of the most specific for the tissue of interest.
“For instance, the directed evolution-based vector engineering allows the testing of a large variety of rAAV variants in vivo, leading to the selection of the most specific for the tissue of interest [113].”
From Risk mitigation of immunogenicity: a key to personalized retinal gene therapy (2021) · cites this paper as [113]

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Computational Design of a Biologically Active Enzyme
Dwyer, M. A., Looger, L. L., & Hellinga, H. W. (2004) · Science · doi:10.1126/science.1098432 · Cited by 295 · see citing works
Retracted
In Vivo Gene Delivery and Stable Transduction of Nondividing Cells by a Lentiviral Vector
Naldini, L., Blömer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M., & Trono, D. (1996) · Science · doi:10.1126/science.272.5259.263 · Cited by 4,903 · see citing works
Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface
Smith, G. P. (1985) · Science · doi:10.1126/science.4001944 · Cited by 4,143 · see citing works
Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease.
Cavazzana-Calvo, M., Hacein-Bey, S., Basile, G. D. S., Gross, F., Yvon, E., Nusbaum, P., Selz, F., Hue, C., Certain, S., Casanova, J., et al. (2000) · Science · doi:10.1126/science.288.5466.669 · Cited by 2,703 · see citing works
Rapid evolution of a protein in vitro by DNA shuffling
Stemmer, W. P. C. (1994) · Nature · doi:10.1038/370389a0 · Cited by 1,932 · see citing works
Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus
Mann, R., Mulligan, R. C., & Baltimore, D. (1983) · Cell · doi:10.1016/0092-8674(83)90344-6 · Cited by 1,855 · see citing works
Yeast surface display for screening combinatorial polypeptide libraries
Boder, E. T., & Wittrup, K. D. (1997) · Nature Biotechnology · doi:10.1038/nbt0697-553 · Cited by 1,774 · see citing works
The Basic Science of Gene Therapy
Mulligan, R. C. (1993) · Science · doi:10.1126/science.8493530 · Cited by 1,734 · see citing works
Gene therapy - promises, problems and prospects
Verma, I. M., & Somia, N. (1997) · Nature · doi:10.1038/38410 · Cited by 1,681 · see citing works
A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer
Khuri, F. R., Nemunaitis, J. J., Ganly, I., Arseneau, J. C., Tannock, I. F., Romel, L., Gore, M. E., Ironside, J. A. D., MacDougall, R. H., Heise, C. C., et al. (2000) · Nature Medicine · doi:10.1038/78638 · Cited by 1,099 · see citing works
RNA interference in adult mice
McCaffrey, A. P., Meuse, L. A., Pham, T.-T. T., Conklin, D. S., Hannon, G. J., & Kay, M. A. (2002) · Nature · doi:10.1038/418038a · Cited by 1,060 · see citing works
Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain
Kaplitt, M. G., Leone, P., Samulski, R. J., Xiao, X., Pfaff, D. W., O’Malley, K. L., & During, M. J. (1994) · Nature Genetics · doi:10.1038/ng1094-148 · Cited by 1,031 · see citing works
Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector
Kay, M. A., Manno, C. S., Ragni, M. V., Larson, P. J., Couto, L. B., McClelland, A., Glader, B. E., Chew, A. K., Tai, S. J., Herzog, R. W., et al. (2000) · Nature Genetics · doi:10.1038/73464 · Cited by 1,019 · see citing works
Construction and applications of a highly transmissible murine retrovirus shuttle vector
Cepko, C. L., Roberts, B. E., & Mulligan, R. C. (1984) · Cell · doi:10.1016/0092-8674(84)90440-9 · Cited by 973 · see citing works
Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization
Isner, J. M., & Asahara, T. (1999) · Journal of Clinical Investigation · doi:10.1172/jci6889 · Cited by 774 · see citing works
Cd8(+) T-Cell Responses to Adeno-Associated Virus Capsid in Humans
Mingozzi, F., Maus, M. V., Hui, D. J., Sabatino, D. E., Murphy, S. L., Rasko, J. E. J., Ragni, M. V., Manno, C. S., Sommer, J., Jiang, H., et al. (2007) · Nature Medicine · doi:10.1038/nm1549 · Cited by 748 · see citing works
Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression
Samulski, R. J., Chang, L., & Shenk, T. E. (1989) · Journal of Virology · doi:10.1128/jvi.63.9.3822-3828.1989 · Cited by 742 · see citing works
Matrix metalloproteinases in tumour invasion and metastasis
Curran, S., & Murray, G. I. (1999) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199911)189:3 · Cited by 654 · see citing works
Recombinant adeno-associated virus for muscle directed gene therapy
Fisher, K. J., Jooss, K., Alston, J., Yang, Y., Haecker, S. E., High, K., Pathak, R., Raper, S. E., & Wilson, J. M. (1997) · Nature Medicine · doi:10.1038/nm0397-306 · Cited by 654 · see citing works
The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy
Xie, Q., Bu, W., Bhatia, S., Hare, J., Somasundaram, T., Azzi, A., & Chapman, M. S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162250899 · Cited by 612 · see citing works
Quantitative analysis of the packaging capacity of recombinant adeno-associated virus
Dong, J.-Y., Fan, P.-D., & Frizzell, R. A. (1996) · Human Gene Therapy · doi:10.1089/hum.1996.7.17-2101 · Cited by 583 · see citing works
Altering the Tropism of Lentiviral Vectors through Pseudotyping
Cronin, J., Zhang, X.-Y., & Reiser, J. (2005) · Current Gene Therapy · doi:10.2174/1566523054546224 · Cited by 540 · see citing works
Directed evolution of adeno-associated virus yields enhanced gene delivery vectors
Maheshri, N., Koerber, J. T., Kaspar, B. K., & Schaffer, D. V. (2006) · Nature Biotechnology · doi:10.1038/nbt1182 · Cited by 538 · cited 2× · see citing works
“…to the viral envelope (Benedict et al., 1999; Cosset et al., 1995; Russell et al., 1993), as well as non-covalent attachment of adaptor molecules composed of the viral receptor fused to a targeting ligand (Snitkovsky and Young, 1998), have been employed to target retroviruses to new receptors.”
BackgroundMethodSelf-citation
Crystallographic refinement and atomic models of the intact immunoglobulin molecule Kol and its antigen-binding fragment at 3.0 Å and 1.9 Å resolution
Marquart, M., Deisenhofer, J., Huber, R., & Palm, W. (1980) · Journal of Molecular Biology · doi:10.1016/0022-2836(80)90252-1 · Cited by 457 · see citing works
Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors
Müller, O. J., Kaul, F., Weitzman, M. D., Pasqualini, R., Arap, W., Kleinschmidt, J. A., & Trepel, M. (2003) · Nature Biotechnology · doi:10.1038/nbt856 · Cited by 411 · see citing works
Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus
Flannery, J. G., Zolotukhin, S., Vaquero, M. I., LaVail, M. M., Muzyczka, N., & Hauswirth, W. W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6916 · Cited by 407 · see citing works
Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2
Girod, A., Ried, M., Wobus, C., Lahm, H., Leike, K., Kleinschmidt, J., Deléage, G., & Hallek, M. (1999) · Nature Medicine · doi:10.1038/12491 · Cited by 405 · see citing works
Mutational Analysis of the Adeno-Associated Virus Type 2 (AAV2) Capsid Gene and Construction of AAV2 Vectors with Altered Tropism
Wu, P., Xiao, W. S., Conlon, T. J., Hughes, J. A., Agbandje‐McKenna, M., Ferkol, T. W., Flotte, T. R., & Muzyczka, N. (2000) · Journal of Virology · doi:10.1128/jvi.74.18.8635-8647.2000 · Cited by 390 · see citing works
Repeated Adeno-Associated Virus Serotype 2 Aerosol-Mediated Cystic Fibrosis Transmembrane Regulator Gene Transfer to the Lungs of Patients With Cystic Fibrosis
Moss, R. B., Rodman, D. M., Spencer, L. T., Aitken, M. L., Zeitlin, P. L., Waltz, D. A., Milla, C. E., Brody, A. S., Clancy, J. P., Ramsey, B. W., et al. (2004) · CHEST Journal · doi:10.1378/chest.125.2.509 · Cited by 389 · see citing works
Structure of the Prefusion Form of the Vesicular Stomatitis Virus Glycoprotein G
Roche, S., Rey, F. A., Gaudin, Y., & Bressanelli, S. (2007) · Science · doi:10.1126/science.1135710 · Cited by 364 · see citing works
Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding
Opie, 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 · see citing works
Rapid Uncoating of Vector Genomes Is the Key toEfficient Liver Transduction with Pseudotyped Adeno-Associated VirusVectors
Thomas, C. E., Storm, T. A., Huang, Z., & Kay, M. A. (2004) · Journal of Virology · doi:10.1128/jvi.78.6.3110-3122.2004 · Cited by 358 · see citing works
Cloning and Characterization of Adeno-Associated Virus Type 5
Chiorini, J. A., Kim, F., Yang, L. C., & Kotin, R. M. (1999) · Journal of Virology · doi:10.1128/jvi.73.2.1309-1319.1999 · Cited by 332 · see citing works
Targeted adenovirus gene transfer to endothelial and smooth muscle cells by using bispecific antibodies
Wickham, T. J., Segal, D. M., Roelvink, P. W., Carrion, M. E., Lizonová, A., Lee, G. M., & Kovesdi, I. (1996) · Journal of Virology · doi:10.1128/jvi.70.10.6831-6838.1996 · Cited by 288 · see citing works
MEC1 and MEC2: two new cell lines derived from B-chronic lymphocytic leukaemia in prolymphocytoid transformation
Stacchini, A., Aragno, M., Vallario, A., Alfarano, A., Circosta, P., Gottardi, D., Faldella, A., Rege‐Cambrin, G., Thunberg, U., Nilsson, K., et al. (1999) · Leukemia Research · doi:10.1016/s0145-2126(98)00154-4 · Cited by 283 · see citing works
Monoclonal Antibodies against the Adeno-Associated Virus Type 2 (AAV-2) Capsid: Epitope Mapping and Identification of Capsid Domains Involved in AAV-2–Cell Interaction and Neutralization of AAV-2 Infection
Wobus, C. E., Hügle-Dörr, B., Girod, A., Petersen, G., Hallek, M., & Kleinschmidt, J. A. (2000) · Journal of Virology · doi:10.1128/jvi.74.19.9281-9293.2000 · Cited by 273 · cited 2× · see citing works
“…sequence of the capsid, such as virus–cell interactions (Chiorini et al., 1999; Opie et al., 2003) and antibody neutralization (Moskalenko et al., 2000; Wobus et al., 2000), will be extremely challenging to rationally re-design, even with the availability of AAV structures (Xie et al., 2002).”
Background
The cryptic life style of adenoassociated virus
Berns, K. I., & Linden, R. M. (1995) · BioEssays · doi:10.1002/bies.950170310 · Cited by 268 · see citing works
HUMAN GENE THERAPY
Morgan, R. A., & Anderson, W. F. (1993) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.62.070193.001203 · Cited by 265 · see citing works
Epitope Mapping of Human Anti-Adeno-Associated Virus Type 2 Neutralizing Antibodies: Implications for Gene Therapy and Virus Structure
Moskalenko, M., Chen, L., van Roey, M., Donahue, B. A., Snyder, R. O., McArthur, J. G., & Patel, S. D. (2000) · Journal of Virology · doi:10.1128/jvi.74.4.1761-1766.2000 · Cited by 253 · see citing works
Quantitative analysis of the effect of the mutation frequency on the affinity maturation of single chain Fv antibodies
Daugherty, P. S., Chen, G., Iverson, B. L., & Georgiou, G. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.030527597 · Cited by 243 · see citing works
Incorporation of Tumor-Targeting Peptides into Recombinant Adeno-associated Virus Capsids
Grifman, M., Trepel, M., Speece, P., Gilbert, L. B., Arap, W., Pasqualini, R., & Weitzman, M. D. (2001) · Molecular Therapy · doi:10.1006/mthe.2001.0345 · Cited by 241 · see citing works
In vitro selection of viral vectors with modified tropism: the adeno-associated virus display
Perabò, L., Büning, H., Kofler, D. M., Ried, M. U., Girod, A., Wendtner, C., Enssle, J., & Hallek, M. J. (2003) · Molecular Therapy · doi:10.1016/s1525-0016(03)00123-0 · Cited by 232 · see citing works
Targeted adeno-associated virus vector transduction of nonpermissive cells mediated by a bispecific F(ab'γ)2 antibody
Bartlett, J. S., Kleinschmidt, J. A., Boucher, R. C., & Samulski, R. J. (1999) · Nature Biotechnology · doi:10.1038/6185 · Cited by 229 · see citing works
Optimization of DNA shuffling for high fidelity recombination
Zhao, H. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.6.1307 · Cited by 223 · see citing works
Retroviral retargeting by envelopes expressing an N-terminal binding domain
Cosset, F., Morling, F. J., Takeuchi, Y., Weiss, R. A., Collins, M. K., & Russell, S. J. (1995) · Journal of Virology · doi:10.1128/jvi.69.10.6314-6322.1995 · Cited by 221 · see citing works
Efficient and Selective AAV2-Mediated Gene Transfer Directed to Human Vascular Endothelial Cells
Nicklin, S. A., Buening, H., Dishart, K. L., de Alwis, M., Girod, A., Hacker, U., Thrasher, A. J., Ali, R. R., Hallek, M. J., & Baker, A. H. (2001) · Molecular Therapy · doi:10.1006/mthe.2001.0424 · Cited by 219 · see citing works
The three-dimensional structure of an intact monoclonal antibody for canine lymphoma
Harris, L. J., Larson, S. B., Hasel, K. W., Day, J. S., Greenwood, A., & McPherson, A. (1992) · Nature · doi:10.1038/360369a0 · Cited by 217 · see citing works
Immune responses to adeno-associated virus and its recombinant vectors.
Sun, J. Y., Anand-Jawa, V, Chatterjee, S., & Wong, K. K. (2003) · Gene Therapy · doi:10.1038/sj.gt.3302039 · Cited by 215 · see citing works
Retroviral vectors displaying functional antibody fragments
Russell, S. J., Hawkins, R. E., & Winter, G. P. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.5.1081 · Cited by 206 · see citing works
A Targetable, Injectable Adenoviral Vector for Selective Gene Delivery to Pulmonary Endothelium in Vivo
Reynolds, P. N., Zinn, K. R., Gavrilyuk, V. D., Balyasnikova, I. V., Rogers, B. E., Buchsbaum, D. J., Wang, M. H., Miletich, D. J., Grizzle, W. E., Douglas, J. T., et al. (2000) · Molecular Therapy · doi:10.1006/mthe.2000.0205 · Cited by 202 · see citing works
Targeted Gene Delivery to Vascular Tissue In Vivo by Tropism-Modified Adeno-Associated Virus Vectors
White, S. J., Nicklin, S. A., Büning, H., Brosnan, M. J., Leike, K., Papadakis, E. D., Hallek, M. J., & Baker, A. H. (2004) · Circulation · doi:10.1161/01.cir.0000109697.68832.5d · Cited by 193 · see citing works
Insertional Mutagenesis of the Adeno-Associated Virus Type 2 (AAV2) Capsid Gene and Generation of AAV2 Vectors Targeted to Alternative Cell-Surface Receptors
Shi, W., Arnold, G. S., & Bartlett, J. S. (2001) · Human Gene Therapy · doi:10.1089/104303401750476212 · Cited by 167 · see citing works
Impaired Intracellular Trafficking of Adeno-Associated Virus Type 2 Vectors Limits Efficient Transduction of Murine Fibroblasts
Hansen, J. J., Qing, K., Kwon, H., Mah, C. S., & Srivastava, A. (2000) · Journal of Virology · doi:10.1128/jvi.74.2.992-996.2000 · Cited by 147 · see citing works
Phase I Trial of Intramuscular Injection of a Recombinant Adeno-Associated Virus Alpha 1-Antitrypsin (rAAV2-CB-hAAT) Gene Vector to AAT-Deficient Adults
Flotte, 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 · see citing works
Combinatorial engineering of a gene therapy vector: directed evolution of adeno‐associated virus
Perabo, L., Endell, J., King, S., Lux, K., Goldnau, D., Hallek, M., & Büning, H. (2006) · The Journal of Gene Medicine · doi:10.1002/jgm.849 · Cited by 136 · see citing works
Transductional targeting of adenovirus vectors for gene therapy
Glasgow, J. N., Everts, M., & Curiel, D. (2006) · Cancer Gene Therapy · doi:10.1038/sj.cgt.7700928 · Cited by 131 · see citing works
Conjugate-Based Targeting of Recombinant Adeno-Associated Virus Type 2 Vectors by Using Avidin-Linked Ligands
Ponnazhagan, S., Mahendra, G., Kumar, S., Thompson, J. A., & Castillas, M. (2002) · Journal of Virology · doi:10.1128/jvi.76.24.12900-12907.2002 · Cited by 129 · see citing works
Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses
Work, L. M., Büning, H., Ela Hunt, B., Nicklin, S. A., Denby, L., Britton, N., Leike, K., Odenthal, M., Drebber, U., Hallek, M. J., et al. (2006) · Molecular Therapy · doi:10.1016/j.ymthe.2005.11.013 · Cited by 124 · see citing works
Development of Efficient Viral Vectors Selective for Vascular Smooth Muscle Cells
Work, L. M., Nicklin, S. A., Brain, N. J. R., Dishart, K. L., Seggern, D. J. V., Hallek, M. J., Büning, H., & Baker, A. H. (2003) · Molecular Therapy · doi:10.1016/j.ymthe.2003.11.006 · Cited by 115 · see citing works
Transcriptional Targeting in Cancer Gene Therapy
Robson, T., & Hirst, D. G. (2003) · BioMed Research International · doi:10.1155/s1110724303209074 · Cited by 115 · see citing works
Infection Efficiency of Human and Mouse Embryonic Stem Cells Using Adenoviral and Adeno-Associated Viral Vectors
Smith-Arica, J. R., Thomson, A. J., Ansell, R., Chiorini, J. A., Davidson, B. L., & McWhir, J. (2003) · Cloning and Stem Cells · doi:10.1089/153623003321512166 · Cited by 111 · see citing works
Molecular breeding of viruses
Soong, N.-W., Nomura, L. E., Pekrun, K., Reed, M., Sheppard, L., Dawes, G. N., & Stemmer, W. P. C. (2000) · Nature Genetics · doi:10.1038/78132 · Cited by 101 · see citing works
Immune Responses to Recombinant Adeno-Associated Virus Vectors: Putting Preclinical Findings into Perspective
Flotte, T. R. (2004) · Human Gene Therapy · doi:10.1089/1043034041361190 · Cited by 91 · see citing works
Breeding of retroviruses by DNA shuffling for improved stability and processing yields
Powell, S. K., Kaloss, M., Pinkstaff, A., McKee, R. C., Burimski, I., Pensiero, M. N., Otto, E., Stemmer, W. P. C., & Soong, N.-W. (2000) · Nature Biotechnology · doi:10.1038/82391 · Cited by 83 · see citing works
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 80 · see citing works
Metabolic Biotinylation Provides a Unique Platform for the Purification and Targeting of Multiple AAV Vector Serotypes
Arnold, G. S., Sasser, A. K., Stachler, M. D., & Bartlett, J. S. (2006) · Molecular Therapy · doi:10.1016/j.ymthe.2006.02.014 · Cited by 79 · see citing works
Genetic retargeting of adenovirus vectors: functionality of targeting ligands and their influence on virus viability
Magnusson, M. K., Hong, S. S., Henning, P., Boulanger, P. A., & Lindholm, L. (2002) · The Journal of Gene Medicine · doi:10.1002/jgm.285 · Cited by 77 · see citing works
Viral-Mediated Gene Transfer to Mouse Primary Neural Progenitor Cells
Hughes, S. M., Moussavi‐Harami, F., Sauter, S. L., & Davidson, B. L. (2002) · Molecular Therapy · doi:10.1006/mthe.2001.0512 · Cited by 75 · see citing works
Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains
Li, Y., Drone, C., Sat, E. W. Y., & Ghosh, H. P. (1993) · Journal of Virology · doi:10.1128/jvi.67.7.4070-4077.1993 · Cited by 69 · see citing works
The Hypervariable Domain of the Murine Leukemia Virus Surface Protein Tolerates Large Insertions and Deletions, Enabling Development of a Retroviral Particle Display System
Kayman, S. C., Park, H., Saxon, M. E., & Pinter, A. (1999) · Journal of Virology · doi:10.1128/jvi.73.3.1802-1808.1999 · Cited by 68 · see citing works
Cell-specific viral targeting mediated by a soluble retroviral receptor-ligand fusion protein
Astrof, S., & Young, J. A. T. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.7063 · Cited by 67 · see citing works
Differential expression in human cells from the p6 promoter of human parvovirus B19 following plasmid transfection and recombinant adeno-associated virus 2 (AAV) infection: human megakaryocytic leukaemia cells are non-permissive for AAV infection
Ponnazhagan, S., Wang, X.-S., Woody, M. J., Luo, F., Kang, L. Y., Nallari, M. L., Munshi, N. C., Zhou, S. Z., & Srivastava, A. (1996) · Journal of General Virology · doi:10.1099/0022-1317-77-6-1111 · Cited by 64 · see citing works
In vivo selection of protease cleavage sites from retrovirus display libraries
Buchholz, C. J., Peng, K.-W., Morling, F. J., Zhang, J., Cosset, F., & Russell, S. J. (1998) · Nature Biotechnology · doi:10.1038/nbt1098-951 · Cited by 63 · see citing works
Targeting Retroviral Vectors to CD34-Expressing Cells: Binding to CD34 Does Not Catalyze Virus-Cell Fusion
Benedict, C., Tun, R. Y., Rubinstein, D. B., Guillaume, T., Cannon, P. M., & Anderson, W. F. (1999) · Human Gene Therapy · doi:10.1089/10430349950018625 · Cited by 60 · see citing works
Retroviral Display of Functional Binding Domains Fused to the Amino Terminus of Influenza Hemagglutinin
Hatziioannou, T., Delahaye, E., Martin, F., Russell, S. J., & Cosset, F. (1999) · Human Gene Therapy · doi:10.1089/10430349950017860 · Cited by 54 · see citing works
Selection of Novel Vesicular Stomatitis Virus Glycoprotein Variants from a Peptide Insertion Library for Enhanced Purification of Retroviral and Lentiviral Vectors
Yu, J. H., & Schaffer, D. V. (2006) · Journal of Virology · doi:10.1128/jvi.80.7.3285-3292.2006 · Cited by 54 · see citing works
Self-citation
In vitro and in vivo characterisation of endothelial cell selective adenoviral vectors
Nicklin, S. A., White, S. J., Nicol, C. G., Seggern, D. J. V., & Baker, A. H. (2004) · The Journal of Gene Medicine · doi:10.1002/jgm.526 · Cited by 48 · see citing works
Directed evolution of retroviruses activatable by tumour-associated matrix metalloproteases
Schneider, R. M., Medvedovska, Y., Hartl, I., Voelker, B. T., Chadwick, M. P., Russell, S. J., Cichutek, K., & Buchholz, C. J. (2003) · Gene Therapy · doi:10.1038/sj.gt.3302007 · Cited by 41 · see citing works
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Activation conditions determine susceptibility of murine primary T-lymphocytes to retroviral infection
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Phage Display of Adenovirus Type 5 Fiber Knob as a Tool for Specific Ligand Selection and Validation
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Self-citation
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Bupp, K., Sarangi, A., & Roth, M. J. (2005) · Journal of Virology · doi:10.1128/jvi.79.3.1463-1469.2005 · Cited by 18 · see citing works
Selection of feline leukemia virus envelope proteins from a library by functional association with a murine leukemia virus envelope
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Systems for regulated or tissue-specific gene expression
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Antigen-specific membrane fusion mediated by the haemagglutinin protein of influenza A virus: separation of attachment and fusion functions on different molecules
Patterson, S. M., Swainsbury, R., & Routledge, E. G. (1999) · Gene Therapy · doi:10.1038/sj.gt.3300842 · Cited by 9 · see citing works
Claim and Counterclaim on the Human Genome
Marshall, E. (2000) · Science · doi:10.1126/science.288.5464.242b · Cited by 7 · see citing works

Flagged first, then by citations

1 of the 94 references couldn’t be matched to a known paper.

Research works printed but not linked: 2

Fields BN, Knipe DM, Howley PM, Griffin DE. 2001. Fields virology. Philadelphia: Lippincott Williams & Wilkins. 2 v. (xix, 3087, I-72) p.
Russell SJ, Cosset FL. 1999. Modifying the host range properties of retroviral vectors. J Gene Med 1(5):300-311.

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REVIEW Library Selection and Directed Evolution Approaches to Engineering Targeted Viral Vectors
Jang, J.-H., Lim, K.-I., & Schaffer, D. V. (2007)
Self-citation
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Self-citation
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Self-citation
Improved Strategies for Directed Evolution of Adeno-Associated Virus Gene Therapy Vectors
Ojala, D. S. (2017) · eScholarship (California Digital Library)
Directed evolution of new viruses for therapeutic gene delivery
Schaffer, D. V. (2014) · Journal of Nanomedicine & Nanotechnology
Self-citation

Authors: Jang, J., Lim, K., & Schaffer, D. V.
Affiliations: University of California, Berkeley (US)
Corresponding author: Schaffer, David V.
ORCID: Jang, Jae‐Hyung
Lim, Kwang‐il
Schaffer, David V.
Venue: Biotechnology and Bioengineering
Publisher: Wiley
Published: 2007-07-05
Volume: 98
Issue: 3
Pages: 515-524
ISSN: 0006-3592 (ISSN-L)
1097-0290
DOI: 10.1002/bit.21541
OpenAlex: W2163350558
Cited by: 26
References: 94
Citations by year: 2026: 1 · 2024: 1 · 2021: 1 · 2020: 3 · 2018: 1 · 2017: 4 · 2014: 3 · 2013: 4 · 2012: 1
FWCI: 0.21
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Biotechnology and Bioengineering (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
Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
Keywords: viral vectors, gene therapy, gene delivery, library selection, directed evolution, peptide display, retroviruses, adeno-associated virus, adenovirus, targeted gene delivery
MeSH terms: DNA, Viral, Genetic Engineering, Genetic Vectors, Viruses, Gene Library, Gene Targeting, Directed Molecular Evolution

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Library Selection and Directed Evolution Approaches to Engineering Targeted Viral Vectors

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