Virology Journal | |
A survey of ex vivo/in vitro transduction efficiency of mammalian primary cells and cell lines with Nine natural adeno-associated virus (AAV1-9) and one engineered adeno-associated virus serotype | |
Matthew H Porteus4  Robert J Steininger2  Jon P Connelly3  Jenny C Barker3  Matthew L Hirsch1  Brian L Ellis3  | |
[1] Department of Ophthalmology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA;Department of Pharmacology, Green Center for Systems Biology, Simmons Cancer Center, University of Texas Southwestern Medical Center, Dallas, TX, USA;Department of Biochemistry, University of Texas Southwestern Medical Center, Dallas, TX, USA;Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, 75390-9148, USA | |
关键词: ex vivo; Transduction; Cell lines; Progenitor cells; Primary cells; Tropism; Gene therapy; Adeno-associated virus; Serotypes; AAV; | |
Others : 1151440 DOI : 10.1186/1743-422X-10-74 |
|
received in 2012-07-12, accepted in 2013-02-14, 发布年份 2013 | |
【 摘 要 】
Background
The ability to deliver a gene of interest into a specific cell type is an essential aspect of biomedical research. Viruses can be a useful tool for this delivery, particularly in difficult to transfect cell types. Adeno-associated virus (AAV) is a useful gene transfer vector because of its ability to mediate efficient gene transduction in numerous dividing and quiescent cell types, without inducing any known pathogenicity. There are now a number of natural for that designed AAV serotypes that each has a differential ability to infect a variety of cell types. Although transduction studies have been completed, the bulk of the studies have been done in vivo, and there has never been a comprehensive study of transduction ex vivo/in vitro.
Methods
Each cell type was infected with each serotype at a multiplicity of infection of 100,000 viral genomes/cell and transduction was analyzed by flow cytometry + .
Results
We found that AAV1 and AAV6 have the greatest ability to transduce a wide range of cell types, however, for particular cell types, there are specific serotypes that provide optimal transduction.
Conclusions
In this work, we describe the transduction efficiency of ten different AAV serotypes in thirty-four different mammalian cell lines and primary cell types. Although these results may not be universal due to numerous factors such as, culture conditions and/ or cell growth rates and cell heterogeneity, these results provide an important and unique resource for investigators who use AAV as an ex vivo gene delivery vector or who work with cells that are difficult to transfect.
【 授权许可】
2013 Ellis et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150406080323973.pdf | 821KB | download | |
Figure 3. | 88KB | Image | download |
Figure 2. | 102KB | Image | download |
Figure 1. | 18KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
【 参考文献 】
- [1]Daya S, Berns KI: Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 2008, 21:583-593.
- [2]Michelfelder S, Trepel M: Adeno-associated viral vectors and their redirection to cell-type specific receptors. Adv Genet 2009, 67:29-60.
- [3]Sonntag F, Schmidt K, Kleinschmidt JA: A viral assembly factor promotes AAV2 capsid formation in the nucleolus. Proc Natl Acad Sci U S A 2010, 107:10220-10225.
- [4]Ferrari FK, Samulski T, Shenk T, Samulski RJ: Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J Virol 1996, 70:3227-3234.
- [5]McCarty DM, Monahan PE, Samulski RJ: Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 2001, 8:1248-1254.
- [6]Summerford C, Samulski RJ: Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 1998, 72:1438-1445.
- [7]Asokan A, Hamra JB, Govindasamy L, Agbandje-McKenna M, Samulski RJ: Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J Virol 2006, 80:8961-8969.
- [8]Kashiwakura Y, Tamayose K, Iwabuchi K, Hirai Y, Shimada T, Matsumoto K, Nakamura T, Watanabe M, Oshimi K, Daida H: Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J Virol 2005, 79:609-614.
- [9]Kurzeder C, Koppold B, Sauer G, Pabst S, Kreienberg R, Deissler H: CD9 promotes adeno-associated virus type 2 infection of mammary carcinoma cells with low cell surface expression of heparan sulphate proteoglycans. Int J Mol Med 2007, 19:325-333.
- [10]Summerford C, Bartlett JS, Samulski RJ: AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat Med 1999, 5:78-82.
- [11]Qing K, Mah C, Hansen J, Zhou S, Dwarki V, Srivastava A: Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat Med 1999, 5:71-77.
- [12]Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA: The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol 2006, 80:9831-9836.
- [13]Akache B, Grimm D, Shen X, Fuess S, Yant SR, Glazer DS, Park J, Kay MA: A two-hybrid screen identifies cathepsins B and L as uncoating factors for adeno-associated virus 2 and 8. Mol Ther 2007, 15:330-339.
- [14]Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA: Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J Virol 2001, 75:6884-6893.
- [15]Seiler MP, Miller AD, Zabner J, Halbert CL: Adeno-associated virus types 5 and 6 use distinct receptors for cell entry. Hum Gene Ther 2006, 17:10-19.
- [16]Wu Z, Asokan A, Samulski RJ: Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 2006, 14:316-327.
- [17]Wu Z, Miller E, Agbandje-McKenna M, Samulski RJ: Alpha2,3 and alpha2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol 2006, 80:9093-9103.
- [18]Di Pasquale G, Davidson BL, Stein CS, Martins I, Scudiero D, Monks A, Chiorini JA: Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med 2003, 9:1306-1312.
- [19]Zincarelli C, Soltys S, Rengo G, Rabinowitz JE: Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008, 16:1073-1080.
- [20]Ellis BL, Hirsch ML, Porter SN, Samulski RJ, Porteus MH: Zinc-finger nuclease-mediated gene correction using single AAV vector transduction and enhancement by Food and Drug Administration-approved drugs. Gene Ther 2013, 1:35-42.
- [21]Porteus MH, Cathomen T, Weitzman MD, Baltimore D: Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol Cell Biol 2003, 23:3558-3565.
- [22]Smith-Arica JR, Thomson AJ, Ansell R, Chiorini J, Davidson B, McWhir J: Infection efficiency of human and mouse embryonic stem cells using adenoviral and adeno-associated viral vectors. Cloning Stem Cells 2003, 5:51-62.
- [23]Rabinowitz JE, Bowles DE, Faust SM, Ledford JG, Cunningham SE, Samulski RJ: Cross-dressing the virion: the transcapsidation of adeno-associated virus serotypes functionally defines subgroups. J Virol 2004, 78:4421-4432.
- [24]Hauck B, Xiao W: Characterization of tissue tropism determinants of adeno-associated virus type 1. J Virol 2003, 77:2768-2774.
- [25]Bowles DE, Rabinowitz JE, Samulski RJ: Marker rescue of adeno-associated virus (AAV) capsid mutants: a novel approach for chimeric AAV production. J Virol 2003, 77:423-432.
- [26]Choi VW, McCarty DM, Samulski RJ: AAV hybrid serotypes: improved vectors for gene delivery. Curr Gene Ther 2005, 5:299-310.
- [27]Wu Z, Asokan A, Grieger JC, Govindasamy L, Agbandje-McKenna M, Samulski RJ: Single amino acid changes can influence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J Virol 2006, 80:11393-11397.
- [28]Li W, Asokan A, Wu Z, Van Dyke T, DiPrimio N, Johnson JS, Govindaswamy L, Agbandje-McKenna M, Leichtle S, Redmond DE Jr, McCown TJ, Petermann KB, Sharpless NE, Samulski RJ: Engineering and selection of shuffled AAV genomes: a new strategy for producing targeted biological nanoparticles. Mol Ther 2008, 16:1252-1260.
- [29]Asokan A, Conway JC, Phillips JL, Li C, Hegge J, Sinnott R, Yadav S, DiPrimio N, Nam HJ, Agbandje-McKenna M, McPhee S, Wolff J, Samulski RJ: Reengineering a receptor footprint of adeno-associated virus enables selective and systemic gene transfer to muscle. Nat Biotechnol 2010, 28:79-82.
- [30]Gray SJ, Blake BL, Criswell HE, Nicolson SC, Samulski RJ, McCown TJ: Directed evolution of a novel adeno-associated virus (AAV) vector that crosses the seizure-compromised blood-brain barrier (BBB). Mol Ther 2010, 18:570-578.
- [31]Maheshri N, Koerber JT, Kaspar BK, Schaffer DV: Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat Biotechnol 2006, 24:198-204.
- [32]Koerber JT, Maheshri N, Kaspar BK, Schaffer DV: Construction of diverse adeno-associated viral libraries for directed evolution of enhanced gene delivery vehicles. Nat Protoc 2006, 1:701-706.
- [33]Koerber JT, Schaffer DV: Transposon-based mutagenesis generates diverse adeno-associated viral libraries with novel gene delivery properties. Methods Mol Biol 2008, 434:161-170.
- [34]Koerber JT, Jang JH, Schaffer DV: DNA shuffling of adeno-associated virus yields functionally diverse viral progeny. Mol Ther 2008, 16:1703-1709.
- [35]Jang JH, Koerber JT, Gujraty K, Bethi SR, Kane RS, Schaffer DV: Surface immobilization of hexa-histidine-tagged adeno-associated viral vectors for localized gene delivery. Gene Ther 2010, 11:1384-1389.
- [36]Kwon I, Schaffer DV: Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm Res 2008, 25:489-499.
- [37]Russell DW, Hirata RK: Human gene targeting by viral vectors. Nat Genet 1998, 18:325-330.
- [38]Russell DW, Hirata RK, Inoue N: Validation of AAV-mediated gene targeting. Nat Biotechnol 2002, 20:658.
- [39]Miller DG, Wang PR, Petek LM, Hirata RK, Sands MS, Russell DW: Gene targeting in vivo by adeno-associated virus vectors. Nat Biotechnol 2006, 24:1022-1026.
- [40]Khan IF, Hirata RK, Wang PR, Li Y, Kho J, Nelson A, Huo Y, Zavaljevski M, Ware C, Russell DW: Engineering of human pluripotent stem cells by AAV-mediated gene targeting. Mol Ther 2010, 18:1192-1199.
- [41]Miller DG, Petek LM, Russell DW: Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol Cell Biol 2003, 23:3550-3557.
- [42]Hirsch ML, Green L, Porteus MH, Samulski RJ: Self-complementary AAV mediates gene targeting and enhances endonuclease delivery for double-strand break repair. Gene Ther 2010, 9:1175-1180.
- [43]Porteus MH, Carroll D: Gene targeting using zinc finger nucleases. Nat Biotechnol 2005, 23:967-973.
- [44]Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF: Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 2011, 39:e82.
- [45]Li T, Huang S, Zhao X, Wright DA, Carpenter S, Spalding MH, Weeks DP, Yang B: Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 2011, 39:6315-6325.
- [46]Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC: Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol 2011, 29:731-734.
- [47]Sun N, Liang J, Abil Z, Zhao H: Optimized TAL effector nucleases (TALENs) for use in treatment of sickle cell disease. Mol Biosyst 2012, 8:1255-1263.
- [48]Klein RL, Dayton RD, Tatom JB, Henderson KM, Henning PP: AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol Ther 2008, 16:89-96.
- [49]Finn JD, Hui D, Downey HD, Dunn D, Pien GC, Mingozzi F, Zhou S, High KA: Proteasome inhibitors decrease AAV2 capsid derived peptide epitope presentation on MHC class I following transduction. Mol Ther 2010, 18:135-142.
- [50]Hirsch ML, Fagan BM, Dumitru R, Bower JJ, Yadav S, Porteus MH, Pevny LH, Samulski RJ: Viral single-strand DNA induces p53-dependent apoptosis in human embryonic stem cells. PLoS One 2011, 6:e27520.
- [51]Grieger JC, Choi VW, Samulski RJ: Production and characterization of adeno-associated viral vectors. Nat Protoc 2006, 1:1412-1428.
- [52]Morales CP, Holt SE, Ouellette M, Kaur KJ, Yan Y, Wilson KS, White MA, Wright WE, Shay JW: Absence of cancer-associated changes in human fibroblasts immortalized with telomerase. Nat Genet 1999, 21:115-118.
- [53]Ramirez RD, Sheridan S, Girard L, Sato M, Kim Y, Pollack J, Peyton M, Zou Y, Kurie JM, Dimaio JM: Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res 2004, 64:9027-9034.
- [54]Connelly JP, Barker JC, Pruett-Miller S, Porteus MH: Gene Correction by Homologous Recombination With Zinc Finger Nucleases in Primary Cells From a Mouse Model of a Generic Recessive Genetic Disease. Mol Ther 2010, 6:1103-1110.
- [55]Lichti U, Anders J, Yuspa SH: Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc 2008, 3:799-810.
- [56]Meirelles Lda S, Nardi NB: Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br J Haematol 2003, 123:702-711.
- [57]Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, Goodyear LJ, Wagers AJ: Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 2008, 134:37-47.
- [58]Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM: White fat progenitor cells reside in the adipose vasculature. Science 2008, 322:583-586.
- [59]Thurmond DC, Gonelle-Gispert C, Furukawa M, Halban PA, Pessin JE: Glucose-stimulated insulin secretion is coupled to the interaction of actin with the t-SNARE (target membrane soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein) complex. Mol Endocrinol 2003, 17:732-742.