Research Overview


"Fascinating." - Mr. Spock

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Research Overview


"Fascinating." - Mr. Spock

Genome Engineering

For nearly a decade, the primary focus of our lab has been to develop robust, open-source reagents and methods that enable targeted genome engineering across many different cell types and model organisms. Primarily, this effort has involved the engineering and optimization of zinc finger nucleases (ZFNs), TALE nucleases (TALENs), and CRISPR/Cas9 nucleases. Using these three platforms, we (and our collaborators) have created designer genetic mutations with high efficiencies in zebrafish, plants, or human somatic and pluripotent stem cells. These mutations result from repair of nuclease-induced double-stranded DNA breaks by normal cellular repair processes (non-homologous end-joining or homologous recombination). Ongoing projects in the lab are aimed at defining and improving the specificity of these platforms and optimizing the editing capabilities of these methods for eventual therapeutic applications. We are also continuing to explore the development of novel technologies that will enable high-throughput genome editing.

 

Epigenome Engineering

Building off their success as nucleases, we have demonstrated that the utility of zinc fingers, TALEs, and CRISPR/Cas9 proteins can be extended so as to effect targeted changes in gene expression, a strategy we term "epigenome editing." In one strategy, we simply fuse the gene-activating VP64 or p65 domains to an engineered DNA binding domain targeted to an endogenous gene promoter to achieve gene activation. More recently, we have also shown that engineered TALEs can be used to direct histone modifications that can inactivate endogenous gene enhancers (work done with Bradley Bernstein's lab) and to direct demethylation of specific promoter CpGs that can lead to increases in endogenous gene expression. Notably, these studies provide important functional clues into the regulatory roles of epigenetic marks and cis-regulatory elements, and may enable more extensive studies functional analyses of such elements in the future. These capabilities will have important research applications for studying gene regulation and may also provide novel tools for altering the expression of disease-associated genes. 

Publications


“Writing is hard work and bad for the health.” -E.B. White

Publications


“Writing is hard work and bad for the health.” -E.B. White

2016

Benjamin P Kleinstiver*^, Shengdar Q Tsai*, Michelle S Prew, Nhu T Nguyen, Moira M Welch, Jose M Lopez, Zachary R McCaw, Martin J Aryee & J Keith Joung^. Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nature Biotechnology (2016)
        * contributed equally     ^co-corresponding authors

Supriya K. Saha, John D. Gordan, Benjamin P. Kleinstiver, Phuong Vu, Mortada S. Najem, Jia-Chi Yeo, Lei Shi, Yasutaka Kato, Rebecca S. Levin,James T. Webber, Leah J. Damon, Regina K. Egan, Patricia Greninger, Ultan McDermott, Mathew J. Garnett, Roger L. Jenkins,Kimberly M. Rieger-Christ, Travis B. Sullivan, Aram F. Hezel, Andrew S. Liss,Yusuke Mizukami, Lipika Goyal, Cristina R. Ferrone, Andrew X. Zhu,J. Keith Joung, Kevan M. Shokat, Cyril H. Benes & Nabeel Bardeesy. Isocitrate Dehydrogenase Mutations Confer Dasatinib Hypersensitivity and SRC Dependence in Intrahepatic Cholangiocarcinoma. Cancer Discovery (2016) 6; 727.

Shengdar Q Tsai, Ved V Topkar, J Keith Joung & Martin J Aryee. Open-source guideseq software for analysis of GUIDE-seq dataNature Biotechnology (2016)

Shengdar Q Tsai & J Keith Joung. Defining and improving the genome-wide specificities of CRISPR–Cas9 nucleases. Nature Reviews Genetics (2016) 17(5):300-12.

Benjamin P. Kleinstiver*, Vikram Pattanayak*, Michelle S. Prew, Shengdar Q. Tsai, Nhu T. Nguyen, Zongli Zheng & J Keith Joung. High-fidelity CRISPR–Cas9 nucleases with no detectable genome-wide off-target effects. Nature (2016) 529(7587)490-5.
        * contributed equally

2015

J. Keith Joung, Daniel F. Voytas & Joanne Kamens. Accelerating research through reagent repositories: the genome editing exampleGenome Biology (2015) 16:225.

Benjamin P Kleinstiver^, Michelle S Prew, Shengdar Q Tsai, Nhu T Nguyen, Ved V Topkar, Zongli Zheng & J Keith Joung^. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognitionNature Biotechnology (2015) 33(12):1293-8.
     ^co-corresponding authors

Nicolas Wyvekens, Shengdar Tsai, and J Keith Joung. Genome Editing in Human Cells Using CRISPR/Cas Nucleases. Curr Protoc Mol Biol (2015) 112:31.3.1-18. 

Sándor Spisák, Kate Lawrenson, Yanfang Fu, István Csabai, Rebecca T Cottman, Ji-Heui Seo, Christopher Haiman, Ying Han, Romina Lenci, Qiyuan Li, Viktória Tisza, Zoltán Szállási, Zachery T Herbert, Matthew Chabot, Mark Pomerantz, Norbert Solymosi, The GAME-ON/ELLIPSE Consortium, Simon A Gayther, J Keith Joung & Matthew L Freedman. CAUSEL: an epigenome- and genome-editing pipeline for establishing function of noncoding GWAS variantsNature Medicine (2015) 21(11):1357-63.

Basil P Hubbard, Ahmed H Badran, John A Zuris, John P Guilinger, Kevin M Davis, Liwei Chen, Shengdar Q Tsai, Jeffry D Sander, J Keith Joung & David R Liu. Continuous directed evolution of DNA-binding proteins to improve TALEN specificityNature Methods (2015) 12(10):939-42.

J Keith Joung. Unwanted mutations: Standards needed for gene-editing errorsNature (2015) 523(7559):158.

Benjamin P. Kleinstiver, Michelle S. Prew, Shengdar Q. Tsai, Ved V. Topkar, Nhu T. Nguyen, Zongli Zheng, Andrew P. W. Gonzales, Zhuyun Li, Randall T. Peterson, Jing-Ruey Joanna Yeh, Martin J. Aryee & J Keith Joung. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature (2015) 523(7561):481-5.

Nicolas Wyvekens, Ved V. Topkar, Cyd Khayter, J Keith Joung & Shengdar Q Tsai. Dimeric CRISPR RNA-Guided FokI-dCas9 Nucleases Directed by Truncated gRNAs for Highly Specific Genome EditingHum Gene Ther (2015) 26(7):425-31.

Julia M. Rogers, Luis A. Barrera, Deepak Reyon, Jeffry D. Sander, Manolis Kellis, J Keith Joung & Martha L. Bulyk. Context influences on TALE–DNA binding revealed by quantitative profiling. Nature Communications (2015) 6:7440.

Shamim H Rahman, Johannes Kuehle, Christian Reimann, Tafadzwa Mlambo, Jamal Alzubi, Morgan L Maeder, Heimo Riedel, Paul Fisch, Tobias Cantz, Cornelia Rudolph, Claudio Mussolino, J Keith Joung, Axel Schambach & Toni Cathomen. Rescue of DNA-PK Signaling and T-Cell Differentiation by Targeted Genome Editing in a prkdc Deficient iPSC Disease ModelPLoS Genetics (2015) 11(5):e1005239.

Joshua C BlackElnaz AtabakhshJaegil KimKelly M BietteCapucine Van RechemBrendon LaddPaul d BurrowesCarlos DonadoHamid MattooBenjamin P KleinstiverBing SongGrasiella AndrianiJ Keith JoungOthon IliopoulosCristina MontagnaShiv PillaiGad Getz & Johnathan R. Whetstine. Hypoxia drives transient site-specific copy gain and drug-resistant gene expression. Genes & Development (2015) 29(10):1018-31.

Woong Y Hwang, Yanfang Fu, Deepak Reyon, Andrew PW Gonzales, J Keith Joung & Jing-Ruey Joanna Yeh. Targeted Mutagenesis in Zebrafish Using CRISPR RNA-Guided NucleasesMethods in Molecular Biology (2015) 1311:317-34.

[papers missing]

2014

Tsai, Shengdar Q., Nicolas Wyvekens, Cyd Khayter, Jennifer A. Foden, Vishal Thapar, Deepak Reyon, Mathew J. Goodwin, Martin J. Aryee, and J. Keith Joung. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nature Biotechnology  (2014).

Sander, Jeffry D., and J. Keith Joung. CRISPR-Cas systems for editing, regulating and targeting genomesNature Biotechnology  32, no. 4 (2014): 347-355.

Guilinger, John P., Vikram Pattanayak, Deepak Reyon, Shengdar Q. Tsai, Jeffry D. Sander, J. Keith Joung, and David R. Liu. Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificityNature Methods 11, no. 4 (2014): 429-435.

Fu, Y., Sander, J. D., Reyon, D., Cascio, V. M. & Joung, J. K. Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nature Biotechnology. 32, 279–284 (2014). 

2013

Maeder ML, Angstman JF, Richardson ME, Linder SJ, Cascio VM, Tsai SQ, Ho QH, Sander JD, Reyon D,Bernstein BE, Costello JF, Wilkinson MF, Joung JK. Targeted DNA Demethylation and Endogenous Gene Activation Using Programmable TALE-TET1 Fusions. Nat Biotechnol., 2013 Oct 9; doi: 10.1038/nbt2726.

Mendenhall EM, Williamson KE, Reyon D, Zou JY, Ram O, Joung JK, Bernstein BE. Locus-specific editing of histone modifications at endogenous enhancersNat Biotechnol.2013 Sep 8, doi:10.1038/nbt.2701

Qi Y, Li X, Zhang Y, Starker CG, Baltes NJ, Zhang F, Sander JD, Reyon D, Joung JK, Voytas DF.Targeted Deletion and Inversion of Tandemly Arrayed Genes in Arabidopsis thaliana Using Zinc Finger Nucleases. G3 (Bethesda) 2013 Oct 3; 3(10): 1707-15.

Sander JD, Ramirez CL, Linder SJ, Pattanayak V, Shoresh N, Ku M, Foden JA, Reyon D, Bernstein BE,Liu DR, Joung JK. In silico abstraction of zinc finger nuclease cleavage profiles reveals an expanded landscape of off-target sites. Nucleic Acids Res. 2013 Oct 1; 41(19):e181.

Maeder ML, Linder SJ, Cascio VM, Fu Y, Ho QH, Joung JK. CRISPR RNA-guided activation of endogenous human genes. Nat Methods. 2013 Oct; 10 (10): 977-9.

Hwang WY, Fu Y, Reyon D, Maeder ML, Kaini P, Sander JD, Joung JK, Peterson RT, Yeh JR. Heritable and Precise Zebrafish Genome Editing Using a CRISPR-Cas System. PLoS One. 2013 Jul9;8(7):e68708.

Reyon D, Maeder ML, Khayter C, Tsai SQ, Foley JE, Sander JD, Joung JK. Engineering Customized TALE Nucleases (TALENs) and TALE Transcription Factors by Fast Ligation-Based Automatable Solid-Phase High-Throughput (FLASH) Assembly. Curr Protoc Mol Biol. 2013 Jul;Chapter 12:Unit12.16.

Fu Y, Foden JA, Khayter C, Maeder ML, Reyon D, Joung JK*, Sander JD*. High-frequency
off-target mutagenesis induced by CRISPR-Cas nucleases in human cells.
 Nat Biotechnol. 2013 Sep;31(9):822-6. *Co-corresponding authors

Li X, Burnight ER, Cooney AL, Malani N, Brady T, Sander JD, Staber J, Wheelan SJ, Joung JK, McCrayPB Jr, Bushman FD, Sinn PL, Craig NL. piggyBac transposase tools for genome engineering. Proc Natl Acad Sci USA. 2013 June 18; 110(25): E2279-87.

Osborn MJ, Starker CG, McElroy AN, Webber BR, Riddle MJ, Xia L, Defeo AP, Gabriel R, Schmidt M, Von Kalle C, Carlson DF, Maeder ML, Joung JK, Wagner JE, Voytas DF, Blazar BR, Tolar J. TALEN-based Gene Correction for Epidermolysis Bullosa. Mol Ther. 2013 Jun;21(6):1151-9.

Maeder ML, Linder SJ, Reyon D, Angstman JF, Fu Y, Sander JD, Joung JK. Robust, synergistic regulation of human gene expression using TALE activators. Nat Methods. 2013 Mar;10(3): 243-5.

Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR*, Joung JK*. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol. 2013 Mar;31(3):227-9. *Co-corresponding authors

Tremblay JP, Xiao X, Aartsma-Rus A, Barbas C, Blau HM, Bogdanove AJ, Boycott K, Braun S,Breakefield XO, Bueren JA, Buschmann M, Byrne BJ, Calos M, Cathomen T, Chamberlain J, Chuah M,Cornetta K, Davies KE, Dickson JG, Duchateau P, Flotte TR, Gaudet D, Gersbach CA, Gilbert R, Glorioso J, Herzog RW, High KA, Huang W, Huard J, Joung JK, Liu D, Liu D, Lochmüller H, Lustig L, Martens J, Massie B, Mavilio F, Mendell JR, Nathwani A, Ponder K, Porteus M, Puymirat J, Samulski J, Takeda S, Thrasher A, Vandendriessche T, Wei Y, Wilson JM, Wilton SD, Wolfe JH, Gao G. Translating the Genomics Revolution: The Need for an International Gene Therapy Consortium for Monogenic Diseases. Mol Ther. 2013 Feb;21(2):266-268.

2012

Joung JK, Sander JD. TALENs: a widely applicable technology for targeted genome editingNat.Rev. Mol. Cell Biol., 2012, 14: 49-55.

Reyon D, Khayter C, Regan MR, Joung JK*, Sander JD*. Engineering Designer Transcription Activator-Like Effector Nucleases (TALENs) by REAL or REAL-Fast AssemblyCurr Protoc Mol Biol. 2012 Oct;Chapter 12:Unit12.15. *Co-corresponding authors

Hermann M, Maeder ML, Rector K, Ruiz J, Becher B, Bürki K, Khayter C, Aguzzi A, Joung JK, Buch T,Pelczar P. Evaluation of OPEN Zinc Finger Nucleases for Direct Gene Targeting of the ROSA26 Locus in Mouse EmbryosPLoS One. 2012; 7(9): e41796.

Khalil AS, Lu TK, Bashor CJ, Ramirez CL, Pyenson NC, Joung JK, Collins JJ. A synthetic biology framework for programming eukaryotic transcription functionsCell. 2012 Aug
3;150(3):647-58.

Cade L, Reyon D, Hwang WY, Tsai SQ, Patel S, Khayter C, Joung JK, Sander JD, Peterson RT, Yeh JR.Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENsNucleic Acids Res. 2012; 40(16):8001-10.

Moore FE, Reyon D, Sander JD, Martinez SA, Blackburn JS, Khayter C, Ramirez CL, Joung JK, Langenau DM. Improved somatic mutagenesis in zebrafish using transcription activator-like effector nucleases (TALENs)PLoS One. 2012;7(5):e37877.

Reyon D, Tsai SQ, Khayter C, Foden JA, Sander JD*, Joung JK*. FLASH assembly of TALENs for high-throughput genome editingNat Biotechnol. 2012 May; 30(5):460-5. *Co-correspondingauthors

Ramirez CL, Certo MT, Mussolino C, Goodwin MJ, Cradick TJ, McCaffrey AP, Cathomen T, ScharenbergAM, Joung JK. Engineered zinc finger nickases induce homology-directed repair with reduced mutagenic effectsNucleic Acids Res. 2012 Jul;40(12):5560-8.

2011

Sander JD, Maeder ML, Joung JK. Engineering designer nucleases with customized cleavage specificities. Curr Protoc Mol Biol. 2011 Oct;Chapter 12:Unit12.13.

Sander JD, Yeh JR, Peterson RT, Joung JK. Engineering zinc finger nucleases for targeted mutagenesis of zebrafish. Methods Cell Biol. 2011;104:51-8.

Sebastiano V, Maeder ML, Angstman JF, Haddad B, Khayter C, Yeo DT, Goodwin MJ, Hawkins JS,Ramirez CL, Batista LF, Artandi SE, Wernig M*, Joung JK*. In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells. 2011 Nov;29(11):1717-26. *Co-corresponding authors

Pattanayak V, Ramirez CL, Joung JK, Liu DR. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat Methods. 2011 Aug 7;8(9):765-70.

Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK*, Yeh JR*. Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol. 2011 Aug 5;29(8):697-8. *Co-corresponding authors

Lee J, Hirsh AS, Wittner BS, Maeder ML, Singavarapu R, Lang M, Janarthanan S, McDermott U, YajnikV, Ramaswamy S, Joung JK*, Sgroi DC*. Induction of stable drug resistance in human breast cancer cells using a combinatorial zinc finger transcription factor library. PLoS One.2011;6(7):e21112. *Co-corresponding authors

Rahman SH, Maeder ML, Joung JK, Cathomen T. Zinc-finger nucleases for somatic gene therapy: the next frontier. Hum Gene Ther. 2011 Jun 1. [Epub ahead of print]

Curtin SJ, Zhang F, Sander JD, Haun WJ, Starker C, Baltes NJ, Reyon D, Dahlborg EJ, Goodwin MJ,Coffman AP, Dobbs D, Joung JK, Voytas DF, Stupar RM. Targeted mutagenesis of duplicated genes in soybean with zinc-finger nucleases breakthrough technologies. Plant Physiol. 2011Jun;156(2):466-73.

Reyon D, Kirkpatrick JR, Sander JD, Zhang F, Voytas DF, Joung JK, Dobbs D, Coffman CR.ZFNGenome: a comprehensive resource for locating zinc finger nuclease target sites in model organisms. BMC Genomics. 2011 Jan 28;12:83. 

2010

Sander JD, Dahlborg EJ, Goodwin MJ, Cade L, Zhang F, Cifuentes D, Curtin SJ, Blackburn JS,Thibodeau-Beganny S, Qi Y, Pierick CJ, Hoffman E, Maeder ML, Khayter C, Reyon D, Dobbs D,Langenau DM, Stupar RM, Giraldez AJ, Voytas DF, Peterson RT, Yeh JR, Joung JK. Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat Methods. 2010 Dec 12; doi: 10.1038/nmeth.1542.

Sander JD, Reyon D, Maeder ML, Foley JE, Thibodeau-Beganny S, Li X, Regan MR, Dahlborg E, Goodwin MJ, Fu F, Voytas DF, Joung JK, Dobbs D. Predicting success of oligomerized pool engineering (OPEN) for zinc finger target site sequencesBMC Bioinformatics. 2010; 11: 543.

Söllü C, Pars K, Cornu TI, Thibodeau-Beganny S, Maeder ML, Joung JK, Heilbronn R, Cathomen T.Autonomous zinc-finger nuclease pairs for targeted chromosomal deletion. Nucleic Acids Res.2010 Aug 16. Epub ahead of print.

Sander JD, Maeder ML, Reyon D, Voytas DF, Joung JK, Dobbs D. ZiFiT (Zinc Finger Targeter): an updated zinc finger engineering tool. Nucleic Acids Res. 2010 Jul 1;38 Suppl:W462-8.

Zhang F, Maeder ML, Unger-Wallace E, Hoshaw JP, Reyon D, Christian M, Li X, Pierick CJ, Dobbs D,Peterson T, Joung JK, Voytas DF. High frequency targeted mutagenesis in Arabidopsis thaliana using zinc finger nucleases. Proc Natl Acad Sci U S A. 2010 Jun 29;107(26):12028-33.

Thibodeau-Beganny S, Maeder ML, Joung JK. Engineering single Cys2His2 zinc finger domains using a bacterial cell-based two-hybrid selection system. Methods Mol Biol. 2010;649:31-50.

Joung JK, Voytas DF, Cathomen T. Reply to Genome editing with modularly assembled
 zinc-finger nucleases
Nat Methods, 2010, 7: 91-92.

2009

Voytas DF, Joung JK. Plant science. DNA binding made easyScience, 2009, 326: 1491-1492.

Foley JE, Maeder ML, Pearlberg J, Joung JK, Peterson RT, Yeh JR. Targeted mutagenesis in
 zebrafish using customized zinc-finger nucleases
Nat Protocols, 2009, 4: 1855-1867.

Maeder ML, Thibodeau-Beganny S, Sander JD, Voytas DF, Joung JK. Oligomerized Pool ENgineering (OPEN): An "Open-Source" Protocol for Making Customized Zinc Finger ArraysNat Protocols, 2009, 4: 1471-1501.

Zou J, Maeder ML, Mali P, Pruett-Miller SM, Thibodeau-Beganny S, Chou, B-K, Chen G, Ye Z, Park
I-H,  Daley GQ, Porteus MH, Joung JK, Cheng L. Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cellsCell Stem Cell, 2009, 5: 97-110.

Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF. High Frequency  Modification of Plant Genes Using Engineered Zinc Finger NucleasesNature, 2009, 459: 
  442-445.

Foley JE, Yeh J-R Y, Maeder ML, Reyon D, Sander JD, Peterson RT, Joung JK. Rapid Mutation of  Endogenous Zebrafish Genes Using Zinc Finger Nucleases Made by Oligomerized Pool  ENgineering (OPEN)PLoS ONE, 2009, 4: e4348.

Sander JD, Zaback P, Joung JK, Voytas DF, Dobbs D. An affinity-based scoring scheme for  predicting DNA-binding activities of modularly assembled zinc-finger proteinsNucleic AcidsRes., 2009, 37: 506-515.

Fu F, Sander JD, Maeder ML, Thibodeau-Beganny S, Joung JK, Dobbs D, Miller L, Voytas DF. Zinc  Finger Database (ZiFDB): a repository for information on C2H2 zinc fingers and engineered zinc finger arraysNucleic Acids Res., 2009, 35: D279-D283.

2008

Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Jiang T, Foley JE, Winfrey RJ, Townsend JA, Unger-Wallace E, Sander JD, Muller-Lerch F, Fu F, Pearlberg J, Gobel C, Dassie J, Pruett-Miller SM, Porteus MH, Sgroi DC, Iafrate AJ, Dobbs D, McCray PB, Cathomen T,  Voytas DF, Joung JK. Rapid "open-source" engineering of customized zinc-finger nucleases  for highly efficient gene modificationMol Cell, 2008, 31: 294-301.

Ramirez CL, Foley JE, Wright DA, Muller-Lerch F, Rahman SH, Cornu TI, Winfrey RJ, Sander JD, Fu F, Townsend JA, Cathomen T, Voytas DF, Joung JK. Unexpected failure rates for modular  assembly of engineered zinc fingersNat Methods, 2008, 5: 374-375.

Pruett-Miller SM, Connelly JP, Maeder ML, Joung JK, Porteus MH. Comparison of Zinc Finger  Nucleases for Use In Gene Targeting in Mammalian CellsMol Ther., 2008, 16: 707-717.

Cornu TI, Thibodeau-Beganny S, Guhl E, Alwin S, Eichtinger M, Joung JK, Cathomen T. DNA-binding  specificity is a major determinant of the activity and toxicity of zinc-finger nucleasesMol Ther., 2008, 16: 352-8.

2007

Meng X, Thibodeau-Beganny S, Jiang T, Joung JK, Wolfe SA. Profiling the DNA-binding specificities of engineered Cys2His2 zinc finger domains using a rapid cell-based method,Nucleic Acids Res., 2007, 35: e81.

Sander JD, Zaback P, Joung JK, Voytas DF, Dobbs D. Zinc Finger Targeter (ZiFiT): An Engineered  Zinc Finger/Target Site Design ToolNucleic Acids Res., 2007, 35: W599-W605.

2006

Wright DA, Thibodeau-Beganny S, Sander JD, Winfrey RJ, Hirsh AS, Eichtinger M, Fu F, Porteus MH, Dobbs D, Voytas DF, Joung JK. Standardized reagents and protocols for engineering zinc  finger nucleases by modular assemblyNat Protocols, 2006, 1: 1637-1652.

Giesecke AV, Fang R, Joung JK. Synthetic protein-protein interaction domains created by  shuffling Cys2His2 zinc fingersMol Sys Biol., 2006, doi: 10.1038/msb4100053

Meng X, Smith RM, Giesecke AV, Joung JK, Wolfe SA. A counter-selectable marker for
  bacterial-based interaction trap systems
Biotechniques, 2006, 40: 179-184.

2005

Vallet-Galy I, Donovan KE, Fang R, Joung JK, Dove SL. Repression of phase-variable cupA gene  expression by H-NS-like proteins in Pseudomonas aeruginosaProc. Natl. Acad. Sci. USA 2005, 102: 11082-11087.

Serebriiskii IG, Fang R, Latypova E, Hopkins R, Vinson C, Joung JK, Golemis EA. A combined  yeast/bacterial two-hybrid system: development and evaluationMol Cell Proteomics 2005,  4: 819-826.

2004

Nguyen-Hackley DH, Ramm E, Taylor CM, Joung JK, Dervan PB, Pabo CO. Allosteric Inhibition of
  Zinc-Finger Binding in the Major Groove of DNA by Minor-Groove Binding Ligands
 Biochemistry2004; 43: 3880-3890.

Thibodeau SA, Fang R, Joung JK. An optimized high-throughput b-galactosidase assay for  bacterial cell-based reporter systemsBiotechniques 2004; 36: 410-415.

2003

Hurt, JA, Thibodeau SA, Hirsh AS, Pabo CO, Joung JK. Highly specific zinc finger proteins obtained by directed domain shuffling and cell-based selectionProc. Natl. Acad. Sci. USA 2003; 100: 12271-12276.