The following list of publications, authored by Sangamo scientists collaborators and others, contains original research articles and review articles that are relevant to our ZFP technology and its many applications.


Genome editing with engineered zinc finger nucleases.
Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD.

Nat Rev Genet. 2010 Sep;11(9):636-46. Review.PubMed PMID: 20717154.

The discovery of zinc fingers and their applications in generegulation and genome manipulation.
Klug A.

Annu Rev Biochem. 2010;79:213-31. Review. PubMed PMID: 20192761.

Drug discovery with engineered zinc-finger proteins.
Jamieson AC, Miller JC, Pabo CO.

Nat Rev Drug Discov. 2003 May;2(5):361-8. Review. PubMed PMID:12750739.

Design and selection of novel Cys2His2 zinc finger proteins
Pabo, C. O., Peisach, E., and Grant, R. A.

Annu Rev Biochem 70, 313-40. (2001)

Publications Relating to Therapeutic Applications of our ZFN Technology

The following publications relate to the development of ZFP Therapeutics using ZFNs:

Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo.
Holt N, Wang J, Kim K, Friedman G, Wang X, Taupin V, Crooks GM, Kohn DB, Gregory PD, Holmes MC, Cannon PM.

Nat Biotechnol. 2010 Aug;28(8):839-47. Epub 2010 Jul 2. PubMed PMID: 20601939.

Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases.
Perez EE, Wang J, Miller JC, Jouvenot Y, Kim KA, Liu O, Wang N, Lee G, Bartsevich VV, Lee YL, Guschin DY, Rupniewski I, Waite AJ, Carpenito C, Carroll RG, Orange JS, Urnov FD, Rebar EJ, Ando D, Gregory PD, Riley JL, Holmes MC, June CH.

Nat Biotechnol. 2008 Jul;26(7):808-16. Epub 2008 Jun 29. PubMed PMID: 18587387.

Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases.
Moehle, E A; Rock, J M; Lee, Y L Jouvenot, Y; Dekelver, R C; Gregory, P D ; Urnov, F D; Holmes, M C.

Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3055-60. Epub 2007 Feb 20. PubMed PMID: 17360608; PubMed Central PMCID: PMC1802009.

Highly efficient endogenous human gene correction using designed zinc-finger nucleases.
Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, Jamieson AC, Porteus MH, Gregory PD, Holmes MC.

Nature. 2005 Jun2;435(7042):646-51. Epub 2005 Apr 3. PubMed PMID: 15806097.

Publications Relating to Therapeutic Applications of our ZFP TF Technology

The following publications relate to the development of therapeutics based on ZFP TFs:

An engineered zinc finger protein activator of the endogenous glial cell line-derived neurotrophic factor gene provides functional neuroprotection in a rat model of Parkinson's disease.
Laganiere J, Kells AP, Lai JT, Guschin D, Paschon DE, Meng X, Fong LK, Yu Q, Rebar EJ, Gregory PD, Bankiewicz KS, Forsayeth J, Zhang HS.

J Neurosci. 2010 Dec 8;30(49):16469-74. PubMed PMID: 21147986.

Engineered zinc finger protein-mediated VEGF-a activation restores deficient VEGF-A in sensory neurons in experimental diabetes.
Pawson EJ, Duran-Jimenez B, Surosky R, Brooke HE, Spratt SK, Tomlinson DR,
Gardiner NJ. 

Diabetes. 2010 Feb;59(2):509-18. Epub 2009 Nov 23. PubMed PMID: 19934008; PubMed Central PMCID: PMC2809974.

An Engineered Transcription Factor Which Activates VEGF-A Enhances Recovery After
Spinal Cord Injury.

Liu Y, Figley S, Spratt SK, Lee G, Ando D, Surosky R, Fehlings MG. 

Neurobiol Dis. 2010 Feb;37(2):384-93. Epub 2009 Oct 29.
PubMed PMID: 19879362.

Gene transfer of an engineered zinc finger protein enhances the anti-angiogenic defense system.
Yokoi K, Zhang HS, Kachi S, Balaggan KS, Yu Q, Guschin D, Kunis M, Surosky R,Africa LM, Bainbridge JW, Spratt SK, Gregory PD, Ali RR, Campochiaro PA.

Mol Ther. 2007 Nov;15(11):1917-23. Epub 2007 Aug 14. PubMed PMID:17700545.

Regulation of endogenous gene expression using small molecule-controlled engineered zinc-finger protein transcription factors.
Dent CL, Lau G, Drake EA, Yoon A, Case CC, Gregory PD.

Gene Ther. 2007 Sep;14(18):1362-9. Epub 2007 Jul 19. PubMed PMID: 17637799.

Ocular gene transfer with self-complementary AAV vectors.
Yokoi K, Kachi S, Zhang HS, Gregory PD, Spratt SK, Samulski RJ, Campochiaro PA.

Invest Ophthalmol Vis Sci. 2007 Jul;48(7):3324-8. PubMed PMID: 17591905.

Gene transfer of an engineered transcription factor promoting expression of VEGF-A protects against experimental diabetic neuropathy.
Price SA, Dent C, Duran-Jimenez B, Liang Y, Zhang L, Rebar EJ, Case CC, Gregory PD, Martin TJ, Spratt SK, Tomlinson DR.

Diabetes. 2006 Jun;55(6):1847-54. PubMed PMID: 16731852.

Repression of vascular endothelial growth factor A in glioblastoma cells using engineered zinc finger transcription factors.
Snowden AW, Zhang L, Urnov F, Dent C, Jouvenot Y, Zhong X, Rebar EJ, Jamieson AC, Zhang HS, Tan S, Case CC, Pabo CO, Wolffe AP, Gregory PD.

Cancer Res. 2003 Dec 15;63(24):8968-76. PubMed PMID: 14695215

Zinc-finger protein-targeted gene regulation: genomewide single-gene specificity.
Tan S, Guschin D, Davalos A, Lee YL, Snowden AW, Jouvenot Y, Zhang HS, Howes K, McNamara AR, Lai A, Ullman C, Reynolds L, Moore M, Isalan M, Berg LP, Campos B, Qi H, Spratt SK, Case CC, Pabo CO, Campisi J, Gregory PD.

Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):11997-2002. Epub 2003 Sep 26. PubMed PMID: 14514889; PubMed Central PMCID: PMC218702.

Targeted regulation of imprinted genes by synthetic zinc-finger transcription factors.
Jouvenot Y, Ginjala V, Zhang L, Liu PQ, Oshimura M, Feinberg AP, Wolffe AP, Ohlsson R, Gregory PD.

Gene Ther. 2003 Mar;10(6):513-22. PubMed PMID: 12621455.

Gene-specific targeting of H3K9 methylation is sufficient for initiating repression in vivo.
Snowden AW, Gregory PD, Case CC, Pabo CO.

Curr Biol. 2002 Dec 23;12(24):2159-66. PubMed PMID: 12498693.

PPARgamma knockdown by engineered transcription factors: exogenous PPARgamma2 but not PPARgamma1 reactivates adipogenesis.
Ren, D., Collingwood, T. N., Rebar, E. J., Wolffe, A. P., and Camp, H. S.

Genes Dev 16, 27-32(2002).

Induction of angiogenesis in a mouse model using engineered transcription factors
Rebar, E. J., Huang, Y., Hickey, R., Nath, A. K., Meoli, D., Nath, S., Chen, B., Xu, L., Liang, Y., Jamieson, A. C., et al.

Nat Med 8, 1427-32(2002).

Publications Relating to Applications of our ZFN and ZFP TF Technology in Research

Cell Biology Applications

Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells
Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM, Santiago Y, Lee AH, Vo TD, Doyon Y, Miller JC, Paschon DE, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Drubin DG.

Nat Cell Biol. 2011 Feb 6. [Epub ahead of print] PubMed PMID:21297641.

Distinct factors control histone variant H3.3 localization at specific genomic regions.
Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD.

Cell. 2010 Mar 5;140(5):678-91. PubMed PMID: 20211137; PubMed Central PMCID: PMC2885838.

Targeted gene knockout in mammalian cells by using engineered zinc-finger nucleases.
Santiago Y, Chan E, Liu PQ, Orlando S, Zhang L, Urnov FD, Holmes MC, Guschin D, Waite A, Miller JC, Rebar EJ, Gregory PD, Klug A, Collingwood TN.

Proc Natl Acad Sci U S A. 2008 Apr 15;105(15):5809-14. Epub 2008 Mar 21. PubMed PMID: 18359850; PubMed Central PMCID: PMC2299223.

Histone deimination antagonizes arginine methylation.
Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M, Schneider R, Gregory PD, Tempst P, Bannister AJ, Kouzarides T.

Cell. 2004 Sep 3;118(5):545-53.PubMed PMID: 15339660.

Creation of Transgenic Animals

Knockout rats via embryo microinjection of zinc-finger nucleases.
Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Wood A, Cui X, Meng X, Vincent A, Lam S, Michalkiewicz M, Schilling R, Foeckler J, Kalloway S, Weiler H, Ménoret S, Anegon I, Davis GD, Zhang L, Rebar EJ,Gregory PD, Urnov FD, Jacob HJ, Buelow R.

Science. 2009 Jul 24;325(5939):433. PubMed PMID:19628861; PubMed Central PMCID: PMC2831805.

Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases.
Doyon Y, McCammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Amacher SL.

Nat Biotechnol. 2008 Jun;26(6):702-8. Epub 2008 May 25. PubMed PMID: 18500334; PubMed Central PMCID: PMC2674762.

Use of ZFP TFs in Drosophila

Controlling gene expression in Drosophila using engineered zinc finger proteintranscription factors.
Jamieson AC, Guan B, Cradick TJ, Xiao H, Holmes MC, Gregory PD, Carroll PM.

Biochem Biophys Res Commun. 2006 Sep 29;348(3):873-9. Epub 2006 Jul 31. PubMed PMID: 16899226.

Creation of Novel Cell Lines for More Efficient Protein Production

Highly efficient deletion of FUT8 in CHO cell lines using zinc-finger nucleases yields cells that produce completely nonfucosylated antibodies.
Malphettes L, Freyvert Y, Chang J, Liu PQ, Chan E, Miller JC, Zhou Z, Nguyen T, Tsai C, Snowden AW, Collingwood TN, Gregory PD, Cost GJ.

Biotechnol Bioeng. 2010 Aug 1;106(5):774-83. PubMed PMID: 20564614.

Generation of a triple-gene knockout mammalian cell line using engineered zinc-finger nucleases.
Liu PQ, Chan EM, Cost GJ, Zhang L, Wang J, Miller JC, Guschin DY, Reik A, Holmes MC, Mott JE, Collingwood TN, Gregory PD.

Biotechnol Bioeng. 2010 May 1;106(1):97-105. PubMed PMID: 20047187.

BAK and BAX deletion using zinc-finger nucleases yields apoptosis-resistant CHO cells.
Cost GJ, Freyvert Y, Vafiadis A, Santiago Y, Miller JC, Rebar E, Collingwood TN, Snowden A, Gregory PD.

Biotechnol Bioeng. 2010 Feb 1;105(2):330-40. PubMed PMID: 19777580.

ZFP TF’s for Enhanced Protein Production

Enhanced protein production by engineered zinc finger proteins.
Reik A, Zhou Y, Collingwood TN, Warfe L, Bartsevich V, Kong Y, Henning KA, Fallentine BK, Zhang L, Zhong X, Jouvenot Y, Jamieson AC, Rebar EJ, Case CC, Korman A, Li XY, Black A, King DJ, Gregory PD

Biotechnol Bioeng. 2007 Aug 1;97(5):1180-9.PubMed PMID: 17171718.

Isogenic human cell lines for drug discovery: regulation of target gene expression by engineered zinc-finger protein transcription factors.
Liu PQ, Tan S, Mendel MC, Murrills RJ, Bhat BM, Schlag B, Samuel R, Matteo JJ, de la Rosa R, Howes K, Reik A, Case CC, Bex FJ, Young K, Gregory PD.

J Biomol Screen. 2005 Jun;10(4):304-13. PubMed PMID: 15964931.

Use of ZFNs and ZFP TFs in Stem Cells


Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases.
Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, DeKelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ,Gregory PD, Urnov FD, Jaenisch R.

Nat Biotechnol. 2009 Sep;27(9):851-7. Epub 2009 Aug 13. PubMed PMID: 19680244.

Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery.
Lombardo A, Genovese P, Beausejour CM, Colleoni S, Lee YL, Kim KA, Ando D, Urnov FD, Galli C, Gregory PD, Holmes MC, Naldini L.

Nat Biotechnol. 2007 Nov;25(11):1298-306. Epub 2007 Oct 28. PubMed PMID: 17965707.


Engineered zinc finger proteins for controlling stem cell fate.
Bartsevich VV, Miller JC, Case CC, Pabo CO.

Stem Cells. 2003;21(6):632-7. PubMed PMID:14595122.

Use of ZFNs and ZFP TFs Plants


Targeted transgene integration in plant cells using designed zinc finger nucleases.
Cai CQ, Doyon Y, Ainley WM, Miller JC, Dekelver RC, Moehle EA, Rock JM, LeeYL, Garrison R, Schulenberg L, Blue R, Worden A, Baker L, Faraji F, Zhang L, Holmes MC, Rebar EJ, Collingwood TN, Rubin-Wilson B, Gregory PD, Urnov FD, Petolino JF.

Plant Mol Biol. 2009 Apr;69(6):699-709. Epub 2008 Dec 27.PubMed PMID: 19112554.

Precise genome modification in the crop species Zea mays using zinc-finger nucleases.
Shukla VK, Doyon Y, Miller JC, DeKelver RC, Moehle EA, Worden SE, Mitchell JC, Arnold NL, Gopalan S, Meng X, Choi VM, Rock JM, Wu YY, Katibah GE, Zhifang G, McCaskill D, Simpson MA, Blakeslee B, Greenwalt SA, Butler HJ, Hinkley SJ, Zhang L, Rebar EJ, Gregory PD, Urnov FD.

Nature. 2009 May21;459(7245):437-41. Epub 2009 Apr 29. PubMed PMID: 19404259.


Gene regulation in planta by plant-derived engineered zinc finger protein transcription factors.
Holmes-Davis R, Li G, Jamieson AC, Rebar EJ, Liu Q, Kong Y, Case CC, Gregory PD.

Plant Mol Biol. 2005 Feb;57(3):411-23. PubMed PMID:15830130.

ZFN Gene-Editing Topics

Zinc-finger nuclease-driven targeted integration into mammalian genomes using donors with limited chromosomal homology.
Orlando SJ, Santiago Y, DeKelver RC, Freyvert Y, Boydston EA, Moehle EA, Choi VM, Gopalan SM, Lou JF, Li J, Miller JC, Holmes MC, Gregory PD, Urnov FD, Cost GJ.

Nucleic Acids Res. 2010 Aug;38(15):e152. Epub 2010 Jun 8. PubMed PMID: 20530528; PubMed Central PMCID:PMC2926620.

Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome.
DeKelver RC, Choi VM, Moehle EA, Paschon DE, Hockemeyer D, Meijsing SH, Sancak Y, Cui X, Steine EJ, Miller JC, Tam P, Bartsevich VV, Meng X, Rupniewski I,Gopalan SM, Sun HC, Pitz KJ, Rock JM, Zhang L, Davis GD, Rebar EJ, Cheeseman IM, Yamamoto KR, Sabatini DM, Jaenisch R, Gregory PD, Urnov FD.

Genome Res. 2010 Aug;20(8):1133-42. Epub 2010 May 27. PubMed PMID: 20508142; PubMed
Central PMCID: PMC2909576.

Targeted gene addition to human mesenchymal stromal cells as a cell-based plasma-soluble protein delivery platform.
Benabdallah BF, Allard E, Yao S, Friedman G, Gregory PD, Eliopoulos N, Fradette J, Spees JL, Haddad E, Holmes MC, Beauséjour CM.

Cytotherapy. 2010 May;12(3):394-9. PubMed PMID: 20331411.

Engineering of ZFPs, ZFP TFs and ZFNs and Additional Methods

Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures.
Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC.

Nat Methods. 2011 Jan;8(1):74-9. Epub 2010 Dec 5. PubMed PMID: 21131970.

Transient cold shock enhances zinc-finger nuclease-mediated gene disruption.
Doyon Y, Choi VM, Xia DF, Vo TD, Gregory PD, Holmes MC.

Nat Methods. 2010 Jun;7(6):459-60. Epub 2010 May 2. PubMed PMID: 20436476.

An improved zinc-finger nuclease architecture for highly specific genome editing.
Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA, Gregory PD, Pabo CO, Rebar EJ.

Nat Biotechnol. 2007 Jul;25(7):778-85. Epub 2007 Jul 1. PubMed PMID: 17603475.