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Scot Wolfe PhD

TitleProfessor
InstitutionUniversity of Massachusetts Medical School
DepartmentMolecular, Cell and Cancer Biology
AddressUniversity of Massachusetts Medical School
364 Plantation Street, LRB-619
Worcester MA 01605
Phone508-856-3953
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    Other Positions
    InstitutionUMMS - School of Medicine
    DepartmentBiochemistry and Molecular Pharmacology

    InstitutionUMMS - School of Medicine
    DepartmentMolecular, Cell and Cancer Biology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentBiochemistry and Molecular Pharmacology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentBioinformatics and Computational Biology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentInterdisciplinary Graduate Program

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentMD/PhD Program

    InstitutionUMMS - Programs, Centers and Institutes
    DepartmentBioinformatics and Integrative Biology

    InstitutionUMMS - Programs, Centers and Institutes
    DepartmentChemical Biology


    Collapse Biography 
    Collapse education and training
    California Institute of Technology, Pasadena, CA, United StatesBSChemistry & Biology
    Harvard University, Cambridge, MA, United StatesAMChemistry
    Harvard University, Cambridge, MA, United StatesPHDOrganic Chemistry

    Collapse Overview 
    Collapse overview

    Academic Background

    Scot Wolfe received his B.S. in Chemistry and Biology from Caltech in 1990, and his Ph.D. from Harvard in Chemistry in 1996. From 1996-2001 he was a post-doctoral fellow at Massachusetts Institute of Technology where his work was supported in part by the Leukemia and Lymphoma Society. In 2001, Dr. Wolfe joined the faculty of UMMS.

    Engineering precise gene editing systems for application in gene therapy and the analysis of gene regulatory networks

    Scot Wolfe My research program is focused on four inter-related areas (see our lab website for more details https://www.umassmed.edu/wolfe-lab/):

    • Engineering programmable nucleases for the targeted cleavage of a single site within a vertebrate genome for gene therapy
    • Applying programmable nucleases for therapeutic genome editing for beta-hemoglobinopathies (Nat Med & Blood) and pathogneic microduplications (Nature)
    • Improving Cas9/Cpf1 delivery systems for somaitc genome editing 
    • Understanding fundamental aspects of protein-DNA recognition
     
    Creating more precise CRISPR/Cas9 nucleases for gene therapy - We are utilzing our expertise in protein engineering and protein-DNA recognition to create hybrid CRISPR/Cas9 nucleases to achieve single-site cleavage precision within the human genome.  Our new gene editing platforms (Cas9-ZFPs and Cas9-Cas9 fusions) provide dramatic improvements in specificity that make them promising tools to serve as the backbone for new cell-based therapeutics or gene therapy reagents. 
     
    Utilizing CRISPR/Cas9 nucleases for therapeutic applications - We are utilizing CRISPR-Cas systems to improve the efficiency of genome editing in a variety of different cell types.  We are particularly interested in editing in CD34+ hematopoietic stem cells with the goal of therapeutically modifying these cells ex vivo to correct a genetic disorder.  These cells would then be returned to the patient through autologous stem cell transplant.  We have projects focused on Sickle cell disease, beta-thalassemia and Chronic granulotomous disease.  We are also working in collaboration with Charles Emerson (UMMS Wellstone Center) on Limb Girdle Muscular Dystrophy and with Christian Mueller (UMMS-RTI) on Hermansky Pudlak Syndrome.    
     
    Improving delivery systems for CRISPR/Cas9 nucleases for therapeutic applications - We are collaborating the the Khvorova, Sontheimer and Watts laboratories (UMMS-RTI) to improve delivery systems for CRISPR-Cas nucleases in the context of the NIH Somatic Cell Genome Editing program.    
     
    Utilizing CRISPR/Cas9 to inactivate latent HIV provirus in reservoir cells - We are collaborating with Jeremy Luban (UMMS – PMM) to lead a team that is investigating the chromatin architecture of latent HIV provirus in reservoir cells.  This data will be used to develop precise Cas9 nucleases and corresponding delivery systems to selectively inactivate provirus in reservoir cells to provide a path toward a functional cure for HIV.  
     
    CRIPSR-Cas9 systems in Zebrafish - We are collaborating with Nathan Lawson (UMMS – MCCB) to develop new and improved CRISPR-Cas tools for genome engineering in zebrafish.  We have used ZFNs, TALENs and Cas9 to make targeted knockouts of a number of genes of interest.  We are currently working to improve the editing efficiency of CRISPR-based systems for targeted gene knock-outs and knock-ins.  
     
    ZFP transcription factors for NF1 - We are collaborating with labs at UMMS and MGH to develop gene therapy tools to restore Neurofibromin expression. This collaborative project is associated with the Gilbert Family Foundation Gene Therapy Initiative  (https://www.gilbertfamilyfoundation.org/gilbert-nf-research-alliance/gilbert-gene-therapy-initiative/).
     
    Protein-DNA recognition - Our research on protein-DNA recognition is focused primarily on two of the most abundant families of DNA-binding domains in metazoans:

    Cys2His2 Zinc fingers & Homeodomains

    We have performed comprehensive analysis of homeodomain and Cys2His2 zinc finger specificities in D. melanogaster – (fruit fly) in collaboration with Michael Brodsky (UMMS-MCCB) & Gary Stormo (Wash. U). We have coupled this data with specificity data from artificial zinc fingers and homeodomains that we have selected using our bacterial one-hybrid system.  Using this information we can build simple qualitative models of recognition that allow the design of homeodomains with novel DNA-binding specificity.  This dataset can also be used to broadly predict the specificity of homeodomains (http://stormo.wustl.edu/flyhd/) and zinc fingers (http://stormo.wustl.edu/ZFModels/).  We continue to explore aspects of DNA recognition by these DNA-binding domain families to both more broadly and accurately predicting the specificity of naturally-occurring family members in all species and for rationally engineering the specificity of these DNA-binding domains for therapeutic development.
     
    B1H selection systems - We have developed a bacterial one-hybrid system for rapidly characterizing the DNA-binding specificities of sequence-specific transcription factors, both naturally-occurring and engineered. Using this technology have characterized >50% all of the sequence-specific transcription factors in the D. melanogaster genome (FlyFactorSurvey) in collaboration with the laboratory of Michael Brodsky (UMMS – MCCB). This dataset is being used to unravel transcription factor regulatory networks within the fly.  This selection system can also be used to select Cys2His2 Zinc finger proteins and homeodomains with novel DNA-binding specificity for therapeutic applications.


    Collapse Rotation Projects

    Potential Rotation Projects

    Improving the Precision of CRISPR/Cas9 nucleases for gene therapy applications:

    We are working to improve the precision of the CRISPR/Cas9 system to generate nucleases that will cleave at only a single site in the genome.  These engineering efforts focus on increasing the DNA-editing precision of Cas9 and using protein engineering to introduce new properties into the nuclease.  Much of this work is now transitioning to the use of Cas9 (and Cpf1) protein-RNA complexes.  These modified nucleases will then be applied to patient derived cell-culture systems for the targeted repair or inactivation of disease-causing alleles.  With the eventual goal of creating therapeutics for Sickle Cell Disease, HIV, Chronic Granulomatous Disease, Limb Girdle Muscular Dystrophy and other monogenic disorders.

    ex vivo genome editing in CD34+ HSPCs:

    We are developing improved Cas9 proteins for delivery ex vivo into CD34+ HSPCs for therapeutic application to sickle cell disease and beta-thalassemia. The goal is to modify the hematopoietic stem cells of a patient to complement the loss of function of the beta-globin gene and then return these cells to the patient through an autologous transplant. 

    Development of Cys2His2 Zinc fingers proteins (ZFPs) as targeted therapeutics:

    We are developing artificial ZFPs for the regulation of target genes to change their gene expression profiles for therapeutic applications.

    Creation of CRISPR/Cas9-based tools for zebrafish:

    We are developing CRISPR/Cas9 systems for spatial and temporally restricted editing or gene regulation in zebrafish.  These tools will be used to determine the tissue- or cell-type specific function of target genes during development. 



    Collapse Post Docs

    Postdoctoral Fellow Applications are being accepted for TWO positions.

    A position is available to develop new delivery reagents/methods for Cas9-based nucleases for somatic cell genome editing in collaboration with the Khvorova, Sontheimer and Watts labs. This project is associated with the NIH Common Fund Somatic Cell Genome Editing. More information on the specifics of the project can be found at the NIHReporter.

    A position is available to develop Cys2His2 zinc finger proteins (ZFPs) for the treatment of monogenic disorders. This project will focus on the creation of ZFPs with novel DNA-binding specificity to recognize sequence elements within genomic loci of therapeutic interest.  In collaboration with other laboratories, we will evaluate the activity of these ZFP-based gene therapy reagents in vitro and in vivo in relevant disease models.




    Collapse Bibliographic 
    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
    List All   |   Timeline
    1. Métais JY, Doerfler PA, Mayuranathan T, Bauer DE, Fowler SC, Hsieh MM, Katta V, Keriwala S, Lazzarotto CR, Luk K, Neel MD, Perry SS, Peters ST, Porter SN, Ryu BY, Sharma A, Shea D, Tisdale JF, Uchida N, Wolfe SA, Woodard KJ, Wu Y, Yao Y, Zeng J, Pruett-Miller S, Tsai SQ, Weiss MJ. Genome editing of HBG1 and HBG2 to induce fetal hemoglobin. Blood Adv. 2019 Nov 12; 3(21):3379-3392. PMID: 31698466.
      View in: PubMed
    2. Shin M, Nozaki T, Idrizi F, Isogai S, Ogasawara K, Ishida K, Yuge S, Roscoe B, Wolfe SA, Fukuhara S, Mochizuki N, Deguchi T, Lawson ND. Valves Are a Conserved Feature of the Zebrafish Lymphatic System. Dev Cell. 2019 Sep 24. PMID: 31564611.
      View in: PubMed
    3. Sher F, Hossain M, Seruggia D, Schoonenberg VAC, Yao Q, Cifani P, Dassama LMK, Cole MA, Ren C, Vinjamur DS, Macias-Trevino C, Luk K, McGuckin C, Schupp PG, Canver MC, Kurita R, Nakamura Y, Fujiwara Y, Wolfe SA, Pinello L, Maeda T, Kentsis A, Orkin SH, Bauer DE. Rational targeting of a NuRD subcomplex guided by comprehensive in situ mutagenesis. Nat Genet. 2019 Jul; 51(7):1149-1159. PMID: 31253978.
      View in: PubMed
    4. Iyer S, Suresh S, Guo D, Daman K, Chen JCJ, Liu P, Zieger M, Luk K, Roscoe BP, Mueller C, King OD, Emerson CP, Wolfe SA. Precise therapeutic gene correction by a simple nuclease-induced double-stranded break. Nature. 2019 Apr 03. PMID: 30944467.
      View in: PubMed
    5. Wu Y, Zeng J, Roscoe BP, Liu P, Yao Q, Lazzarotto CR, Clement K, Cole MA, Luk K, Baricordi C, Shen AH, Ren C, Esrick EB, Manis JP, Dorfman DM, Williams DA, Biffi A, Brugnara C, Biasco L, Brendel C, Pinello L, Tsai SQ, Wolfe SA, Bauer DE. Highly efficient therapeutic gene editing of human hematopoietic stem cells. Nat Med. 2019 Mar 25. PMID: 30911135.
      View in: PubMed
    6. Liu P, Luk K, Shin M, Idrizi F, Kwok S, Roscoe B, Mintzer E, Suresh S, Morrison K, Frazão JB, Bolukbasi MF, Ponnienselvan K, Luban J, Zhu LJ, Lawson ND, Wolfe SA. Enhanced Cas12a editing in mammalian cells and zebrafish. Nucleic Acids Res. 2019 Mar 20. PMID: 30892626.
      View in: PubMed
    7. Kim D, Luk K, Wolfe SA, Kim JS. Evaluating and Enhancing Target Specificity of Gene-Editing Nucleases and Deaminases. Annu Rev Biochem. 2019 Mar 18. PMID: 30883196.
      View in: PubMed
    8. Xu S, Luk K, Yao Q, Shen AH, Zeng J, Wu Y, Luo HY, Brendel C, Pinello L, Chui DHK, Wolfe SA, Bauer DE. Editing aberrant splice sites efficiently restores ß-globin expression in ß-thalassemia. Blood. 2019 Jan 31. PMID: 30704988.
      View in: PubMed
    9. Bolukbasi MF, Liu P, Luk K, Kwok SF, Gupta A, Amrani N, Sontheimer EJ, Zhu LJ, Wolfe SA. Publisher Correction: Orthogonal Cas9-Cas9 chimeras provide a versatile platform for genome editing. Nat Commun. 2018 12 10; 9(1):5294. PMID: 30531933.
      View in: PubMed
    10. Amrani N, Gao XD, Liu P, Edraki A, Mir A, Ibraheim R, Gupta A, Sasaki KE, Wu T, Donohoue PD, Settle AH, Lied AM, McGovern K, Fuller CK, Cameron P, Fazzio TG, Zhu LJ, Wolfe SA, Sontheimer EJ. NmeCas9 is an intrinsically high-fidelity genome-editing platform. Genome Biol. 2018 Dec 05; 19(1):214. PMID: 30518407.
      View in: PubMed
    11. Bolukbasi MF, Liu P, Luk K, Kwok SF, Gupta A, Amrani N, Sontheimer EJ, Zhu LJ, Wolfe SA. Orthogonal Cas9-Cas9 chimeras provide a versatile platform for genome editing. Nat Commun. 2018 Nov 19; 9(1):4856. PMID: 30451839.
      View in: PubMed
    12. Swygert SG, Senapati S, Bolukbasi MF, Wolfe SA, Lindsay S, Peterson CL. SIR proteins create compact heterochromatin fibers. Proc Natl Acad Sci U S A. 2018 Nov 19. PMID: 30455303.
      View in: PubMed
    13. Pulikkan JA, Hegde M, Ahmad HM, Belaghzal H, Illendula A, Yu J, O'Hagan K, Ou J, Muller-Tidow C, Wolfe SA, Zhu LJ, Dekker J, Bushweller JH, Castilla LH. CBFß-SMMHC Inhibition Triggers Apoptosis by Disrupting MYC Chromatin Dynamics in Acute Myeloid Leukemia. Cell. 2018 Jun 28; 174(1):172-186.e21. PMID: 29958106.
      View in: PubMed
    14. Gao XD, Tu LC, Mir A, Rodriguez T, Ding Y, Leszyk J, Dekker J, Shaffer SA, Zhu LJ, Wolfe SA, Sontheimer EJ. C-BERST: defining subnuclear proteomic landscapes at genomic elements with dCas9-APEX2. Nat Methods. 2018 May 07. PMID: 29735996.
      View in: PubMed
    15. Yin H, Song CQ, Suresh S, Kwan SY, Wu Q, Walsh S, Ding J, Bogorad RL, Zhu LJ, Wolfe SA, Koteliansky V, Xue W, Langer R, Anderson DG. Partial DNA-guided Cas9 enables genome editing with reduced off-target activity. Nat Chem Biol. 2018 Mar; 14(3):311-316. PMID: 29377001.
      View in: PubMed
    16. Ou J, Wolfe SA, Brodsky MH, Zhu LJ. motifStack for the analysis of transcription factor binding site evolution. Nat Methods. 2018 Jan 03; 15(1):8-9. PMID: 29298290.
      View in: PubMed
    17. Yin H, Song CQ, Suresh S, Wu Q, Walsh S, Rhym LH, Mintzer E, Bolukbasi MF, Zhu LJ, Kauffman K, Mou H, Oberholzer A, Ding J, Kwan SY, Bogorad RL, Zatsepin T, Koteliansky V, Wolfe SA, Xue W, Langer R, Anderson DG. Structure-guided chemical modification of guide RNA enables potent non-viral in vivo genome editing. Nat Biotechnol. 2017 Nov 13. PMID: 29131148.
      View in: PubMed
    18. Ma L, Boucher JI, Paulsen J, Matuszewski S, Eide CA, Ou J, Eickelberg G, Press RD, Zhu LJ, Druker BJ, Branford S, Wolfe SA, Jensen JD, Schiffer CA, Green MR, Bolon DN. CRISPR-Cas9-mediated saturated mutagenesis screen predicts clinical drug resistance with improved accuracy. Proc Natl Acad Sci U S A. 2017 Oct 31; 114(44):11751-11756. PMID: 29078326.
      View in: PubMed
    19. Leonard JL, Leonard DM, Wolfe SA, Liu J, Rivera J, Yang M, Leonard RT, Johnson JPS, Kumar P, Liebmann KL, Tutto AA, Mou Z, Simin KJ. Correction: The Dkk3 gene encodes a vital intracellular regulator of cell proliferation. PLoS One. 2017; 12(9):e0184458. PMID: 28863194.
      View in: PubMed
    20. Leonard JL, Leonard DM, Wolfe SA, Liu J, Rivera J, Yang M, Leonard RT, Johnson JPS, Kumar P, Liebmann KL, Tutto AA, Mou Z, Simin KJ. The Dkk3 gene encodes a vital intracellular regulator of cell proliferation. PLoS One. 2017; 12(7):e0181724. PMID: 28738084.
      View in: PubMed
    21. Zhu LJ, Lawrence M, Gupta A, Pagès H, Kucukural A, Garber M, Wolfe SA. GUIDEseq: a bioconductor package to analyze GUIDE-Seq datasets for CRISPR-Cas nucleases. BMC Genomics. 2017 May 15; 18(1):379. PMID: 28506212.
      View in: PubMed
    22. Markert MJ, Zhang Y, Enuameh MS, Reppert SM, Wolfe SA, Merlin C. Genomic Access to Monarch Migration Using TALEN and CRISPR/Cas9-Mediated Targeted Mutagenesis. G3 (Bethesda). 2016 Apr 07; 6(4):905-15. PMID: 26837953.
      View in: PubMed
    23. Brunner D, Burke W, Kuang AQ, LaBombard B, Lipschultz B, Wolfe S. Feedback system for divertor impurity seeding based on real-time measurements of surface heat flux in the Alcator C-Mod tokamak. Rev Sci Instrum. 2016 Feb; 87(2):023504. PMID: 26931846.
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    24. Yin H, Song CQ, Dorkin JR, Zhu LJ, Li Y, Wu Q, Park A, Yang J, Suresh S, Bizhanova A, Gupta A, Bolukbasi MF, Walsh S, Bogorad RL, Gao G, Weng Z, Dong Y, Koteliansky V, Wolfe SA, Langer R, Xue W, Anderson DG. Therapeutic genome editing by combined viral and non-viral delivery of CRISPR system components in vivo. Nat Biotechnol. 2016 Mar; 34(3):328-33. PMID: 26829318.
      View in: PubMed
    25. Bolukbasi MF, Gupta A, Wolfe SA. Creating and evaluating accurate CRISPR-Cas9 scalpels for genomic surgery. Nat Methods. 2016 Jan; 13(1):41-50. PMID: 26716561.
      View in: PubMed
    26. Wang JP, Rancy SK, Lee SK, Feinberg JH, Wolfe SW. Shoulder and Elbow Recovery at 2 and 11 Years Following Brachial Plexus Reconstruction. J Hand Surg Am. 2016 Feb; 41(2):173-9. PMID: 26718077.
      View in: PubMed
    27. Sontheimer EJ, Wolfe SA. Cas9 gets a classmate. Nat Biotechnol. 2015 Dec 09; 33(12):1240-1241. PMID: 26650011.
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    28. Bolukbasi MF, Gupta A, Oikemus S, Derr AG, Garber M, Brodsky MH, Zhu LJ, Wolfe SA. DNA-binding-domain fusions enhance the targeting range and precision of Cas9. Nat Methods. 2015 Dec; 12(12):1150-6. PMID: 26480473.
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    29. Dy CJ, Lee SK, Mancuso CA, Wolfe SW. In Reply. J Hand Surg Am. 2015 Jul; 40(7):1504-5. PMID: 26095057.
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    30. Blatti C, Kazemian M, Wolfe S, Brodsky M, Sinha S. Integrating motif, DNA accessibility and gene expression data to build regulatory maps in an organism. Nucleic Acids Res. 2015 Apr 30; 43(8):3998-4012. PMID: 25791631.
      View in: PubMed
    31. Ma H, Naseri A, Reyes-Gutierrez P, Wolfe SA, Zhang S, Pederson T. Multicolor CRISPR labeling of chromosomal loci in human cells. Proc Natl Acad Sci U S A. 2015 Mar 10; 112(10):3002-7. PMID: 25713381.
      View in: PubMed
    32. Wang JP, Rancy SK, DiCarlo EF, Wolfe SW. Recurrent pigmented villonodular synovitis and multifocal giant cell tumor of the tendon sheath: case report. J Hand Surg Am. 2015 Mar; 40(3):537-41. PMID: 25577961.
      View in: PubMed
    33. Kok FO, Shin M, Ni CW, Gupta A, Grosse AS, van Impel A, Kirchmaier BC, Peterson-Maduro J, Kourkoulis G, Male I, DeSantis DF, Sheppard-Tindell S, Ebarasi L, Betsholtz C, Schulte-Merker S, Wolfe SA, Lawson ND. Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev Cell. 2015 Jan 12; 32(1):97-108. PMID: 25533206.
      View in: PubMed
    34. Dy CJ, Garg R, Lee SK, Tow P, Mancuso CA, Wolfe SW. A systematic review of outcomes reporting for brachial plexus reconstruction. J Hand Surg Am. 2015 Feb; 40(2):308-13. PMID: 25510158.
      View in: PubMed
    35. Weicksel SE, Gupta A, Zannino DA, Wolfe SA, Sagerström CG. Targeted germ line disruptions reveal general and species-specific roles for paralog group 1 hox genes in zebrafish. BMC Dev Biol. 2014 Jun 05; 14:25. PMID: 24902847.
      View in: PubMed
    36. Gupta A, Christensen RG, Bell HA, Goodwin M, Patel RY, Pandey M, Enuameh MS, Rayla AL, Zhu C, Thibodeau-Beganny S, Brodsky MH, Joung JK, Wolfe SA, Stormo GD. An improved predictive recognition model for Cys(2)-His(2) zinc finger proteins. Nucleic Acids Res. 2014 Apr; 42(8):4800-12. PMID: 24523353.
      View in: PubMed
    37. Kok FO, Gupta A, Lawson ND, Wolfe SA. Construction and application of site-specific artificial nucleases for targeted gene editing. Methods Mol Biol. 2014; 1101:267-303. PMID: 24233786.
      View in: PubMed
    38. Kearns NA, Genga RM, Enuameh MS, Garber M, Wolfe SA, Maehr R. Cas9 effector-mediated regulation of transcription and differentiation in human pluripotent stem cells. Development. 2014 Jan; 141(1):219-23. PMID: 24346702.
      View in: PubMed
    39. Cheng Q, Kazemian M, Pham H, Blatti C, Celniker SE, Wolfe SA, Brodsky MH, Sinha S. Computational identification of diverse mechanisms underlying transcription factor-DNA occupancy. PLoS Genet. 2013; 9(8):e1003571. PMID: 23935523.
      View in: PubMed
    40. Kazemian M, Pham H, Wolfe SA, Brodsky MH, Sinha S. Widespread evidence of cooperative DNA binding by transcription factors in Drosophila development. Nucleic Acids Res. 2013 Sep; 41(17):8237-52. PMID: 23847101.
      View in: PubMed
    41. Gupta A, Hall VL, Kok FO, Shin M, McNulty JC, Lawson ND, Wolfe SA. Targeted chromosomal deletions and inversions in zebrafish. Genome Res. 2013 Jun; 23(6):1008-17. PMID: 23478401.
      View in: PubMed
    42. Enuameh MS, Asriyan Y, Richards A, Christensen RG, Hall VL, Kazemian M, Zhu C, Pham H, Cheng Q, Blatti C, Brasefield JA, Basciotta MD, Ou J, McNulty JC, Zhu LJ, Celniker SE, Sinha S, Stormo GD, Brodsky MH, Wolfe SA. Global analysis of Drosophila Cys2-His2 zinc finger proteins reveals a multitude of novel recognition motifs and binding determinants. Genome Res. 2013 Jun; 23(6):928-40. PMID: 23471540.
      View in: PubMed
    43. Zhu C, Gupta A, Hall VL, Rayla AL, Christensen RG, Dake B, Lakshmanan A, Kuperwasser C, Stormo GD, Wolfe SA. Using defined finger-finger interfaces as units of assembly for constructing zinc-finger nucleases. Nucleic Acids Res. 2013 Feb 1; 41(4):2455-65. PMID: 23303772.
      View in: PubMed
    44. Merlin C, Beaver LE, Taylor OR, Wolfe SA, Reppert SM. Efficient targeted mutagenesis in the monarch butterfly using zinc-finger nucleases. Genome Res. 2013 Jan; 23(1):159-68. PMID: 23009861.
      View in: PubMed
    45. Anderson DM, George R, Noyes MB, Rowton M, Liu W, Jiang R, Wolfe SA, Wilson-Rawls J, Rawls A. Characterization of the DNA-binding properties of the Mohawk homeobox transcription factor. J Biol Chem. 2012 Oct 12; 287(42):35351-9. PMID: 22923612.
      View in: PubMed
    46. Shin J, Padmanabhan A, de Groh ED, Lee JS, Haidar S, Dahlberg S, Guo F, He S, Wolman MA, Granato M, Lawson ND, Wolfe SA, Kim SH, Solnica-Krezel L, Kanki JP, Ligon KL, Epstein JA, Look AT. Zebrafish neurofibromatosis type 1 genes have redundant functions in tumorigenesis and embryonic development. Dis Model Mech. 2012 Nov; 5(6):881-94. PMID: 22773753.
      View in: PubMed
    47. Christensen RG, Enuameh MS, Noyes MB, Brodsky MH, Wolfe SA, Stormo GD. Recognition models to predict DNA-binding specificities of homeodomain proteins. Bioinformatics. 2012 Jun 15; 28(12):i84-9. PMID: 22689783.
      View in: PubMed
    48. Gupta A, Christensen RG, Rayla AL, Lakshmanan A, Stormo GD, Wolfe SA. An optimized two-finger archive for ZFN-mediated gene targeting. Nat Methods. 2012 Jun; 9(6):588-90. PMID: 22543349.
      View in: PubMed
    49. Chu SW, Noyes MB, Christensen RG, Pierce BG, Zhu LJ, Weng Z, Stormo GD, Wolfe SA. Exploring the DNA-recognition potential of homeodomains. Genome Res. 2012 Oct; 22(10):1889-98. PMID: 22539651.
      View in: PubMed
    50. Zhu C, Smith T, McNulty J, Rayla AL, Lakshmanan A, Siekmann AF, Buffardi M, Meng X, Shin J, Padmanabhan A, Cifuentes D, Giraldez AJ, Look AT, Epstein JA, Lawson ND, Wolfe SA. Evaluation and application of modularly assembled zinc-finger nucleases in zebrafish. Development. 2011 Oct; 138(20):4555-64. PMID: 21937602.
      View in: PubMed
    51. Lawson ND, Wolfe SA. Forward and reverse genetic approaches for the analysis of vertebrate development in the zebrafish. Dev Cell. 2011 Jul 19; 21(1):48-64. PMID: 21763608.
      View in: PubMed
    52. Christensen RG, Gupta A, Zuo Z, Schriefer LA, Wolfe SA, Stormo GD. A modified bacterial one-hybrid system yields improved quantitative models of transcription factor specificity. Nucleic Acids Res. 2011 Jul; 39(12):e83. PMID: 21507886.
      View in: PubMed
    53. Bussmann J, Wolfe SA, Siekmann AF. Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development. 2011 May; 138(9):1717-26. PMID: 21429983.
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    54. Zhu LJ, Christensen RG, Kazemian M, Hull CJ, Enuameh MS, Basciotta MD, Brasefield JA, Zhu C, Asriyan Y, Lapointe DS, Sinha S, Wolfe SA, Brodsky MH. FlyFactorSurvey: a database of Drosophila transcription factor binding specificities determined using the bacterial one-hybrid system. Nucleic Acids Res. 2011 Jan; 39(Database issue):D111-7. PMID: 21097781.
      View in: PubMed
    55. Gupta A, Meng X, Zhu LJ, Lawson ND, Wolfe SA. Zinc finger protein-dependent and -independent contributions to the in vivo off-target activity of zinc finger nucleases. Nucleic Acids Res. 2011 Jan; 39(1):381-92. PMID: 20843781.
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    56. Kazemian M, Blatti C, Richards A, McCutchan M, Wakabayashi-Ito N, Hammonds AS, Celniker SE, Kumar S, Wolfe SA, Brodsky MH, Sinha S. Quantitative analysis of the Drosophila segmentation regulatory network using pattern generating potentials. PLoS Biol. 2010 Aug 17; 8(8). PMID: 20808951.
      View in: PubMed
    57. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, Ma E, Mane S, Hannon GJ, Lawson ND, Wolfe SA, Giraldez AJ. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science. 2010 Jun 25; 328(5986):1694-8. PMID: 20448148.
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    58. Siekmann AF, Standley C, Fogarty KE, Wolfe SA, Lawson ND. Chemokine signaling guides regional patterning of the first embryonic artery. Genes Dev. 2009 Oct 1; 23(19):2272-7. PMID: 19797767.
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    59. Ince-Cushman A, Rice JE, Reinke M, Greenwald M, Wallace G, Parker R, Fiore C, Hughes JW, Bonoli P, Shiraiwa S, Hubbard A, Wolfe S, Hutchinson IH, Marmar E, Bitter M, Wilson J, Hill K. Observation of self-generated flows in tokamak plasmas with lower-hybrid-driven current. Phys Rev Lett. 2009 Jan 23; 102(3):035002. PMID: 19257362.
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    60. Marx RG, Fives G, Chu SK, Daluiski A, Wolfe SW. Allograft reconstruction for symptomatic chronic complete proximal hamstring tendon avulsion. Knee Surg Sports Traumatol Arthrosc. 2009 Jan; 17(1):19-23. PMID: 18682918.
      View in: PubMed
    61. Noyes MB, Christensen RG, Wakabayashi A, Stormo GD, Brodsky MH, Wolfe SA. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell. 2008 Jun 27; 133(7):1277-89. PMID: 18585360.
      View in: PubMed
    62. Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol. 2008 Jun; 26(6):695-701. PMID: 18500337.
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    63. Noyes MB, Meng X, Wakabayashi A, Sinha S, Brodsky MH, Wolfe SA. A systematic characterization of factors that regulate Drosophila segmentation via a bacterial one-hybrid system. Nucleic Acids Res. 2008 May; 36(8):2547-60. PMID: 18332042.
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    64. 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(11):e81. PMID: 17537811.
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    65. Meng X, Smith RM, Giesecke AV, Joung JK, Wolfe SA. Counter-selectable marker for bacterial-based interaction trap systems. Biotechniques. 2006 Feb; 40(2):179-84. PMID: 16526407.
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    66. Meng X, Wolfe SA. Identifying DNA sequences recognized by a transcription factor using a bacterial one-hybrid system. Nat Protoc. 2006; 1(1):30-45. PMID: 17406209.
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    67. Meng X, Brodsky MH, Wolfe SA. A bacterial one-hybrid system for determining the DNA-binding specificity of transcription factors. Nat Biotechnol. 2005 Aug; 23(8):988-94. PMID: 16041365.
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    68. Wolfe SA. Mapping key elements of a protein motif. Chem Biol. 2004 Jul; 11(7):889-91. PMID: 15271344.
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    69. Wolfe SA, Grant RA, Pabo CO. Structure of a designed dimeric zinc finger protein bound to DNA. Biochemistry. 2003 Nov 25; 42(46):13401-9. PMID: 14621985.
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    70. Fernández MJ, Adrio JL, Piret JM, Wolfe S, Ro S, Demain AL. Stimulatory effect of growth in the presence of alcohols on biotransformation of penicillin G into cephalosporin-type antibiotics by resting cells of Streptomyces clavuligerus NP1. Appl Microbiol Biotechnol. 1999 Oct; 52(4):484-8. PMID: 10570794.
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    71. Cho H, Adrio JL, Luengo JM, Wolfe S, Ocran S, Hintermann G, Piret JM, Demain AL. Elucidation of conditions allowing conversion of penicillin G and other penicillins to deacetoxycephalosporins by resting cells and extracts of Streptomyces clavuligerus NP1. Proc Natl Acad Sci U S A. 1998 Sep 29; 95(20):11544-8. PMID: 9751702.
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    72. Wolfe SW, Gupta A, Crisco JJ. Kinematics of the scaphoid shift test. J Hand Surg Am. 1997 Sep; 22(5):801-6. PMID: 9330136.
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    73. Zhang J, Wolfe S, Demain AL. Biochemical studies on the activity of delta-(L-alpha-aminoadipyl)-L-cysteinyl-D-valine synthetase from Streptomyces clavuligerus. Biochem J. 1992 May 1; 283 ( Pt 3):691-8. PMID: 1590759.
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    74. Xiao XF, Wolfe S, Demain AL. Purification and characterization of cephalosporin 7 alpha-hydroxylase from Streptomyces clavuligerus. Biochem J. 1991 Dec 1; 280 ( Pt 2):471-4. PMID: 1747122.
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    75. Owen TA, Holthuis J, Markose E, van Wijnen AJ, Wolfe SA, Grimes SR, Lian JB, Stein GS. Modifications of protein-DNA interactions in the proximal promoter of a cell-growth-regulated histone gene during onset and progression of osteoblast differentiation. Proc Natl Acad Sci U S A. 1990 Jul; 87(13):5129-33. PMID: 2367528.
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    76. Jhang J, Wolfe S, Demain AL. Phosphate regulation of ACV synthetase and cephalosporin biosynthesis in Streptomyces clavuligerus. FEMS Microbiol Lett. 1989 Jan 15; 48(2):145-50. PMID: 2721913.
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    77. Zhang JY, Wolfe S, Demain AL. Effect of ammonium as nitrogen source on production of delta-(L-alpha-aminoadipyl)-L-cysteinyl-D-valine synthetase by Cephalosporium acremonium C-10. J Antibiot (Tokyo). 1987 Dec; 40(12):1746-50. PMID: 3429339.
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