Lim Lab | Papers

Synthetic organizer cells guide development via spatial and biochemical instructions
Yamada T, Trentesaux C, Brunger JM, Xiao Y, Stevens AJ, Martyn I, Kasparek P, Shroff NP, Aguilar A, Bruneau BG, Boffelli D, Klein OD, Lim WA.
Cell. 2024 Dec 11. doi: 10.1016/j.cell.2024.11.017. PMID: 39706189.
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Engineering synthetic suppressor T cells that execute locally targeted immunoprotective programs
Reddy NR, Maachi H, Xiao Y, Simic MS, Yu W, Tonai Y, Cabanillas DA, Serrano-Wu E, Pauerstein PT, Tamaki W, Allen GM, Parent AV, Hebrok M, Lim WA.
Science. 2024 Dec 6;386(6726):eadl4793. doi: 10.1126/science.adl4793. PMID: 39636990.
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Programming tissue-sensing T cells that deliver therapies to the brain
Simic MS, Watchmaker PB, Gupta S, Wang Y, Sagan SA, Duecker J, Shepherd C, Diebold D, Pineo-Cavanaugh P, Haegelin J, Zhu R, Ng B, Yu W, Tonai Y, Cardarelli L, Reddy NR, Sidhu SS, Troyanskaya O, Hauser SL, Wilson MR, Zamvil SS, Okada H, Lim WA.
Science. 2024 Dec 6;386(6726):eadl4237. doi: 10.1126/science.adl4237. PMID: 39636984.
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Degron-based bioPROTACs for controlling signaling in CAR T cells
Kim MS, Bhargava HK, Shavey GE, Lim WA, El-Samad H, Ng AH.
ACS Synthetic Biology. 2024
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CAR-T Cell-Mediated B-Cell Depletion in Central Nervous System Autoimmunity
Gupta S, Simic M, Sagan SA, Shepherd C, Duecker J, Sobel RA, Dandekar R, Wu GF, Wu W, Pak JE, Hauser SL, Lim W, Wilson MR, Zamvil SS.
Neurol Neuroimmunol Neuroinflamm. 2023
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Instructional materials that control cellular activity through synthetic Notch receptors
Lee JC, Brien HJ, Walton BL, Eidman ZM, Toda S, Lim WA, Brunger JM.
Biomaterials. 2023
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Harnessing synthetic biology to engineer organoids and tissues
Trentesaux C, Yamada T, Klein OD, Lim WA.
Cell Stem Cell. 2023
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Synthetic cytokine circuits that drive T cells into immune-excluded tumors
Allen GM, Frankel NW, Reddy NR, Bhargava HK, Yoshida MA, Stark SR, Purl M, Lee J, Yee JL, Yu W, Li AW, Garcia KC, El-Samad H, Roybal KT, Spitzer MH, Lim WA.
Science. 2022
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Programming Multicellular Assembly with Synthetic Cell Adhesion Molecules
Stevens AJ, Harris AR, Gerdts J, Kim KH, Trentesaux C, Ramirez JT, McKeithan WL, Fattahi F, Klein OD, Fletcher DA, Lim WA.
Nature. 2022
PDF. UCSF Press Release.
Decoding CAR T cell phenotype using combinatorial signaling motif libraries and machine learning
Daniels KG, Wang S, Simic MS, Bhargava HK, Capponi S, Tonai Y, Yu W, Bianco S, Lim WA.
Science. 2022
PDF. UCSF Press Release.
The emerging era of cell engineering: Harnessing the modularity of cells to program complex biological function
Lim WA.
Science. 2022
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Rethinking cancer targeting strategies in the era of smart cell therapeutics
Allen GM, Lim WA.
Nat Rev Cancer. 2022
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SynNotch-CAR T cells overcome challenges of specificity, heterogeneity, and persistence in treating glioblastoma
Choe JH, Watchmaker PB, Simic MS, Gilbert RD, Li AW, Krasnow NA, Downey KM, Yu W, Carrera DA, Celli A, Cho J, Briones JD, Duecker JM, Goretsky YE, Dannenfelser R, Cardarelli L, Troyanskaya O, Sidhu SS, Roybal KT, Okada H, Lim WA.
Sci Transl Med. 2021
PDF. PRESS UCSF.
T cell circuits that sense antigen density with an ultrasensitive threshold
Hernandez-Lopez RA, Yu W, Cabral KA, Creasey OA, Lopez Pazmino MDP, Tonai Y, De Guzman A, Mäkelä A, Saksela K, Gartner ZJ, Lim WA.
Science. 2021
PDF. FEATURED IN Cell Research. FEATURED IN Signal Transduction and Targeted Therapy
T cells selectively filter oscillatory signals on the minutes timescale
O'Donoghue GP, Bugaj LJ, Anderson W, Daniels KG, Rawlings DJ, Lim WA.
Proc Natl Acad Sci U S A. 2021
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DNA scaffolds enable efficient and tunable functionalization of biomaterials for immune cell modulation
Huang X, Williams JZ, Chang R, Li Z, Burnett CE, Hernandez-Lopez R, Setiady I, Gai E, Patterson DM, Yu W, Roybal KT, Lim WA, Desai TA.
Nat Nanotechnol. 2021
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Precise T cell recognition programs designed by transcriptionally linking multiple receptors
Williams JZ, Allen GM, Shah D, Sterin IS, Kim KH, Garcia VP, Shavey GE, Yu W, Puig-Saus C, Tsoi J, Ribas A, Roybal KT, Lim WA.
Science. 2020
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Engineering cytokines and cytokine circuits
Li AW, Lim WA.
Science. 2020
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Engineering synthetic morphogen systems that can program multicellular patterning
Toda S, McKeithan WL, Hakkinen TJ, Lopez P, Klein OD, Lim WA.
Science. 2020
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Discriminatory Power of Combinatorial Antigen Recognition in Cancer T Cell Therapies
Dannenfelser R, Allen GM, VanderSluis B, Koegel AK, Levinson S, Stark SR, Yao V, Tadych A, Troyanskaya OG, Lim WA.
Cell Syst. 2020
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Simple Rules Determine Distinct Patterns of Branching Morphogenesis
Yu W, Marshall WF, Metzger RJ, Brakeman PR, Morsut L, Lim W, Mostov KE.
Cell Syst. 2019
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The Design Principles of Biochemical Timers: Circuits that Discriminate between Transient and Sustained Stimulation
Gerardin J, Reddy NR, Lim WA.
Cell Syst. 2019
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High-throughput multicolor optogenetics in microwell plates
Bugaj LJ, Lim WA.
Nat Protoc. 2019
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Engineering cell-cell communication networks: programming multicellular behaviors
Toda S, Frankel NW, Lim WA.
Curr Opin Chem Biol. 2019
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Programming self-organizing multicellular structures with synthetic cell-cell signaling
Toda S, Blauch LR, Tang SKY, Morsut L, Lim WA.
Science. 2018
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Building a Stable Relationship: Ensuring Homeostasis among Cell Types within a Tissue
Frankel NW, Lim WA.
Cell. 2018
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Design of Tunable Oscillatory Dynamics in a Synthetic NF-κB Signaling Circuit
Zhang ZB, Wang QY, Ke YX, Liu SY, Ju JQ, Lim WA, Tang C, Wei P.
Cell Syst. 2017
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Tracing Information Flow from Erk to Target Gene Induction Reveals Mechanisms of Dynamic and Combinatorial Control
Wilson MZ, Ravindran PT, Lim WA, Toettcher JE.
Mol Cell. 2017
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Synthetic Immunology: Hacking Immune Cells to Expand Their Therapeutic Capabilities
Roybal KT, Lim WA.
Annu Rev Immunol. 2017
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CRISPR/Cas9-mediated PD-1 disruption enhances anti-tumor efficacy of human chimeric antigen receptor T cells
Rupp LJ, Schumann K, Roybal KT, Gate RE, Ye CJ, Lim WA, Marson A.
Sci Rep. 2017
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The Principles of Engineering Immune Cells to Treat Cancer
Lim WA, June CH.
Cell. 2017
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Interrogating cellular perception and decision making with optogenetic tools
Bugaj LJ, O'Donoghue GP, Lim WA.
J Cell Biol. 2017
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Engineering Therapeutic T Cells: From Synthetic Biology to Clinical Trials
Esensten JH, Bluestone JA, Lim WA.
Annu Rev Pathol. 2017
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Engineering dynamical control of cell fate switching using synthetic phospho-regulons
Gordley RM, Williams RE, Bashor CJ, Toettcher JE, Yan S, Lim WA.
Proc Natl Acad Sci U S A. 2016
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Complex transcriptional modulation with orthogonal and inducible dCas9 regulators
Gao Y, Xiong X, Wong S, Charles EJ, Lim WA, Qi LS.
Nat Methods. 2016
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Engineering T Cells with Customized Therapeutic Response Programs Using Synthetic Notch Receptors
Roybal KT, Williams JZ, Morsut L, Rupp LJ, Kolinko I, Choe JH, Walker WJ, McNally KA, Lim WA.
Cell. 2016
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Cellular perception and misperception: Internal models for decision-making shaped by evolutionary experience
Mitchell A, Lim W.
Bioessays. 2016
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Modular engineering of cellular signaling proteins and networks
Gordley RM, Bugaj LJ, Lim WA.
Curr Opin Struct Biol. 2016
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CRISPR/Cas9 for Human Genome Engineering and Disease Research
Xiong X, Chen M, Lim WA, Zhao D, Qi LS.
Annu Rev Genomics Hum Genet. 2016
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Nucleosome breathing and remodeling constrain CRISPR-Cas9 function
Isaac RS, Jiang F, Doudna JA, Lim WA, Narlikar GJ, Almeida R.
Elife. 2016
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Precision Tumor Recognition by T Cells With Combinatorial Antigen-Sensing Circuits
Roybal KT, Rupp LJ, Morsut L, Walker WJ, McNally KA, Park JS, Lim WA.
Cell. 2016
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Engineering Customized Cell Sensing and Response Behaviors Using Synthetic Notch Receptors
Morsut L, Roybal KT, Xiong X, Gordley RM, Coyle SM, Thomson M, Lim WA.
Cell. 2016
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Mapping the functional versatility and fragility of Ras GTPase signaling circuits through in vitro network reconstitution
Coyle SM, Lim WA.
Elife. 2016
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Expanding the CRISPR imaging toolset with Staphylococcus aureus Cas9 for simultaneous imaging of multiple genomic loci
Chen B, Hu J, Almeida R, Liu H, Balakrishnan S, Covill-Cooke C, Lim WA, Huang B.
Nucleic Acids Res. 2016
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Beyond editing: repurposing CRISPR-Cas9 for precision genome regulation and interrogation
Dominguez AA, Lim WA, Qi LS.
Nat Rev Mol Cell Biol. 2016
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Oscillatory stress stimulation uncovers an Achilles' heel of the yeast MAPK signaling network
Mitchell A, Wei P, Lim WA.
Science. 2015
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Remote control of therapeutic T cells through a small molecule-gated chimeric receptor
Wu CY, Roybal KT, Puchner EM, Onuffer J, Lim WA.
Science. 2015
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Synthetic biology approaches to engineer T cells
Wu CY, Rupp LJ, Roybal KT, Lim WA.
Curr Opin Immunol. 2015
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Differential genetic interactions of yeast stress response MAPK pathways
Martin H, Shales M, Fernandez-Piñar P, Wei P, Molina M, Fiedler D, Shokat KM, Beltrao P, Lim W, Krogan NJ.
Mol Syst Biol. 2015
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Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds
Zalatan JG, Lee ME, Almeida R, Gilbert LA, Whitehead EH, La Russa M, Tsai JC, Weissman JS, Dueber JE, Qi LS, Lim WA.
Cell. 2015
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Specific gene repression by CRISPRi system transferred through bacterial conjugation
Ji W, Lee D, Wong E, Dadlani P, Dinh D, Huang V, Kearns K, Teng S, Chen S, Haliburton J, Heimberg G, Heineike B, Ramasubramanian A, Stevens T, Helmke KJ, Zepeda V, Qi LS, Lim WA.
ACS Synth Biol. 2014
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Sending mixed messages for cell population control
Youk H, Lim WA.
Cell. 2014
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Synthetic control of mammalian-cell motility by engineering chemotaxis to an orthogonal bioinert chemical signal
Park JS, Rhau B, Hermann A, McNally KA, Zhou C, Gong D, Weiner OD, Conklin BR, Onuffer J, Lim WA.
Proc Natl Acad Sci U S A. 2014
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Secreting and sensing the same molecule allows cells to achieve versatile social behaviors
Youk H, Lim WA.
Science. 2014
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Using optogenetics to interrogate the dynamic control of signal transmission by the Ras/Erk module
Toettcher JE, Weiner OD, Lim WA.
Cell. 2013
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CRISPR interference (CRISPRi) for sequence-specific control of gene expression
Larson MH, Gilbert LA, Wang X, Lim WA, Weissman JS, Qi LS.
Nat Protoc. 2013
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Actin dynamics rapidly reset chemoattractant receptor sensitivity following adaptation in neutrophils
Dandekar SN, Park JS, Peng GE, Onuffer JJ, Lim WA, Weiner OD.
Philos Trans R Soc Lond B Biol Sci. 2013
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Counting molecules in single organelles with superresolution microscopy allows tracking of the endosome maturation trajectory
Puchner EM, Walter JM, Kasper R, Huang B, Lim WA.
Proc Natl Acad Sci U S A. 2013
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Exploitation of latent allostery enables the evolution of new modes of MAP kinase regulation
Coyle SM, Flores J, Lim WA.
Cell. 2013
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CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes
Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA, Torres SE, Stern-Ginossar N, Brandman O, Whitehead EH, Doudna JA, Lim WA, Weissman JS, Qi LS.
Cell. 2013
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Improved blue, green, and red fluorescent protein tagging vectors for S. cerevisiae
Lee S, Lim WA, Thorn KS.
PLoS One. 2013
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Cell-based therapeutics: the next pillar of medicine
Fischbach MA, Bluestone JA, Lim WA.
Sci Transl Med. 2013
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Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression
Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, Lim WA.
Cell. 2013
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Bridging cross-cultural gaps in scientific exchange through innovative team challenge workshops
Lee CM, Gong S, Tang C, Lim WA.
Quant Biol. 2013
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Design principles of regulatory networks: searching for the molecular algorithms of the cell
Lim WA, Lee CM, Tang C.
Mol Cell. 2013
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Designing synthetic regulatory networks capable of self-organizing cell polarization
Chau AH, Walter JM, Gerardin J, Tang C, Lim WA.
Cell. 2012
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Conformational control of the Ste5 scaffold protein insulates against MAP kinase misactivation
Zalatan JG, Coyle SM, Rajan S, Sidhu SS, Lim WA.
Science. 2012
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Bacterial virulence proteins as tools to rewire kinase pathways in yeast and immune cells
Wei P, Wong WW, Park JS, Corcoran EE, Peisajovich SG, Onuffer JJ, Weiss A, Lim WA.
Nature. 2012
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Systematic functional prioritization of protein posttranslational modifications
Beltrao P, Albanèse V, Kenner LR, Swaney DL, Burlingame A, Villén J, Lim WA, Fraser JS, Frydman J, Krogan NJ.
Cell. 2012
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Control of protein signaling using a computationally designed GTPase/GEF orthogonal pair
Kapp GT, Liu S, Stein A, Wong DT, Reményi A, Yeh BJ, Fraser JS, Taunton J, Lim WA, Kortemme T.
Proc Natl Acad Sci U S A. 2012
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Light-based feedback for controlling intracellular signaling dynamics
Toettcher JE, Gong D, Lim WA, Weiner OD.
Nat Methods. 2011
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Recruitment interactions can override catalytic interactions in determining the functional identity of a protein kinase
Won AP, Garbarino JE, Lim WA.
Proc Natl Acad Sci U S A. 2011
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Light control of plasma membrane recruitment using the Phy-PIF system
Toettcher JE, Gong D, Lim WA, Weiner OD.
Methods Enzymol. 2011
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Scaffold proteins: hubs for controlling the flow of cellular information
Good MC, Zalatan JG, Lim WA.
Science. 2011
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The promise of optogenetics in cell biology: interrogating molecular circuits in space and time
Toettcher JE, Voigt CA, Weiner OD, Lim WA.
Nat Methods. 2011
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Phosphotyrosine signaling: evolving a new cellular communication system
Lim WA, Pawson T.
Cell. 2010
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The minimal autoinhibited unit of the guanine nucleotide exchange factor intersectin
Ahmad KF, Lim WA.
PLoS One. 2010
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Designing customized cell signalling circuits
Lim WA.
Nat Rev Mol Cell Biol. 2010
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Rapid diversification of cell signaling phenotypes by modular domain recombination
Peisajovich SG, Garbarino JE, Wei P, Lim WA.
Science. 2010
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Rewiring cells: synthetic biology as a tool to interrogate the organizational principles of living systems
Bashor CJ, Horwitz AA, Peisajovich SG, Lim WA.
Annu Rev Biophys. 2010
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Spatiotemporal control of cell signalling using a light-switchable protein interaction
Levskaya A, Weiner OD, Lim WA, Voigt CA.
Nature. 2009
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Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species
Beltrao P, Trinidad JC, Fiedler D, Roguev A, Lim WA, Shokat KM, Burlingame AL, Krogan NJ.
PLoS Biol. 2009
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The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation
Good M, Tang G, Singleton J, Reményi A, Lim WA.
Cell. 2009
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Frederic M Richards 1925-2009
Lim WA.
Nat Struct Mol Biol. 2009
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The pathogen protein EspF(U) hijacks actin polymerization using mimicry and multivalency
Sallee NA, Rivera GM, Dueber JE, Vasilescu D, Mullins RD, Mayer BJ, Lim WA.
Nature. 2008
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Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages
Pincus D, Letunic I, Bork P, Lim WA.
Proc Natl Acad Sci U S A. 2008
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Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics
Bashor CJ, Helman NC, Yan S, Lim WA.
Science. 2008
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Synthetic biology: lessons from the history of synthetic organic chemistry
Yeh BJ, Lim WA.
Nat Chem Biol. 2007
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Rewiring cellular morphology pathways with synthetic guanine nucleotide exchange factors
Yeh BJ, Rutigliano RJ, Deb A, Bar-Sagi D, Lim WA.
Nature. 2007
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Engineering synthetic signaling proteins with ultrasensitive input/output control
Dueber JE, Mirsky EA, Lim WA.
Nat Biotechnol. 2007
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Engineering modular protein interaction switches by sequence overlap
Sallee NA, Yeh BJ, Lim WA.
J Am Chem Soc. 2007
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Docking interactions in protein kinase and phosphatase networks
Reményi A, Good MC, Lim WA.
Curr Opin Struct Biol. 2006
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Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits
Bhattacharyya RP, Reményi A, Yeh BJ, Lim WA.
Annu Rev Biochem. 2006
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The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway
Bhattacharyya RP, Reményi A, Good MC, Bashor CJ, Falick AM, Lim WA.
Science. 2006
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The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network
Reményi A, Good MC, Bhattacharyya RP, Lim WA.
Mol Cell. 2005
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A general model for preferential hetero-oligomerization of LIN-2/7 domains: mechanism underlying directed assembly of supramolecular signaling complexes
Petrosky KY, Ou HD, Löhr F, Dötsch V, Lim WA.
J Biol Chem. 2005
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A polybasic motif allows N-WASP to act as a sensor of PIP(2) density
Papayannopoulos V, Co C, Prehoda KE, Snapper S, Taunton J, Lim WA.
Mol Cell. 2005
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Rewiring cell signaling: the logic and plasticity of eukaryotic protein circuitry
Dueber JE, Yeh BJ, Bhattacharyya RP, Lim WA.
Curr Opin Struct Biol. 2004
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Sho1 and Pbs2 act as coscaffolds linking components in the yeast high osmolarity MAP kinase pathway
Zarrinpar A, Bhattacharyya RP, Nittler MP, Lim WA.
Mol Cell. 2004
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Optimization of specificity in a cellular protein interaction network by negative selection
Zarrinpar A, Park SH, Lim WA.
Nature. 2003
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Reprogramming control of an allosteric signaling switch through modular recombination
Dueber JE, Yeh BJ, Chak K, Lim WA.
Science. 2003
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The structure and function of proline recognition domains
Zarrinpar A, Bhattacharyya RP, Lim WA.
Sci STKE. 2003
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Complex inheritance of familial hypercholanemia with associated mutations in TJP2 and BAAT
Carlton VE, Harris BZ, Puffenberger EG, Batta AK, Knisely AS, Robinson DL, Strauss KA, Shneider BL, Lim WA, Salen G, Morton DH, Bull LN.
Nat Genet. 2003
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Role of electrostatic interactions in PDZ domain ligand recognition
Harris BZ, Lau FW, Fujii N, Guy RK, Lim WA.
Biochemistry. 2003
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Rewiring MAP kinase pathways using alternative scaffold assembly mechanisms
Park SH, Zarrinpar A, Lim WA.
Science. 2003
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Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/Enabled and a Netrin-independent UNC-40/DCC function
Yu TW, Hao JC, Lim W, Tessier-Lavigne M, Bargmann CI.
Nat Neurosci. 2002
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Coordinated folding and association of the LIN-2, -7 (L27) domain. An obligate heterodimerization involved in assembly of signaling and cell polarity complexes
Harris BZ, Venkatasubrahmanyam S, Lim WA.
J Biol Chem. 2002
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The modular logic of signaling proteins: building allosteric switches from simple binding domains
Lim WA.
Curr Opin Struct Biol. 2002
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Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins
McGee AW, Dakoji SR, Olsen O, Bredt DS, Lim WA, Prehoda KE.
Mol Cell. 2001
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Mechanism and role of PDZ domains in signaling complex assembly
Harris BZ, Lim WA.
J Cell Sci. 2001
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An analysis of the interactions between the Sem-5 SH3 domain and its ligands using molecular dynamics, free energy calculations, and sequence analysis
Wang W, Lim WA, Jakalian A, Wang J, Wang J, Luo R, Bayly CI, Kollman PA.
J Am Chem Soc. 2001
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Energetic determinants of internal motif recognition by PDZ domains
Harris BZ, Hillier BJ, Lim WA.
Biochemistry. 2001
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Integration of multiple signals through cooperative regulation of the N-WASP-Arp2/3 complex
Prehoda KE, Scott JA, Mullins RD, Lim WA.
Science. 2000
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Improving SH3 domain ligand selectivity using a non-natural scaffold
Nguyen JT, Porter M, Amoui M, Miller WT, Zuckermann RN, Lim WA.
Chem Biol. 2000
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PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain
Christopherson KS, Hillier BJ, Lim WA, Bredt DS.
J Biol Chem. 1999
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Structure of the enabled/VASP homology 1 domain-peptide complex: a key component in the spatial control of actin assembly
Prehoda KE, Lee DJ, Lim WA.
Cell. 1999
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Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex
Hillier BJ, Christopherson KS, Prehoda KE, Bredt DS, Lim WA.
Science. 1999
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Exploiting the basis of proline recognition by SH3 and WW domains: design of N-substituted inhibitors
Nguyen JT, Turck CW, Cohen FE, Zuckermann RN, Lim WA.
Science. 1998
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Lim Lab| Books

Cell Signaling: Principles and Mechanisms.
Lim WA, Mayer BJ, Pawson T. Morales M, editor.
New York, NY, USA: Garland Science; 2014