Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins

Guntas, Gurkan; Hallett, Ryan A.; Zimmerman, Seth P.; Williams, Tishan; Yumerefendi, Hayretin; Bear, James E.; Kuhlman, Brian

doi:10.1073/pnas.1417910112

Title: Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins

Journal Article · Mon Dec 22 00:00:00 EST 2014 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1417910112· OSTI ID:1168516

Guntas, Gurkan ^[1]; Hallett, Ryan A. ^[1]; Zimmerman, Seth P. ^[1]; Williams, Tishan ^[1]; Yumerefendi, Hayretin ^[1]; Bear, James E. ^[2]; Kuhlman, Brian ^[3]

Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biochemistry & Biophysics
Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Cell Biology & Physiology. Lineberger Comprehensive Cancer Center. Howard Hughes Medical Inst.
Univ. of North Carolina, Chapel Hill, NC (United States). Dept. of Biochemistry & Biophysics. Lineberger Comprehensive Cancer Center

The discovery of light-inducible protein–protein interactions has allowed for the spatial and temporal control of a variety of biological processes. To be effective, a photodimerizer should have several characteristics: it should show a large change in binding affinity upon light stimulation, it should not cross-react with other molecules in the cell, and it should be easily used in a variety of organisms to recruit proteins of interest to each other. In this study, to create a switch that meets these criteria we have embedded the bacterial SsrA peptide in the C-terminal helix of a naturally occurring photoswitch, the light-oxygen-voltage 2 (LOV2) domain from Avena sativa. In the dark the SsrA peptide is sterically blocked from binding its natural binding partner, SspB. When activated with blue light, the C-terminal helix of the LOV2 domain undocks from the protein, allowing the SsrA peptide to bind SspB. Without optimization, the switch exhibited a twofold change in binding affinity for SspB with light stimulation. Here, we describe the use of computational protein design, phage display, and high-throughput binding assays to create an improved light inducible dimer (iLID) that changes its affinity for SspB by over 50-fold with light stimulation. A crystal structure of iLID shows a critical interaction between the surface of the LOV2 domain and a phenylalanine engineered to more tightly pin the SsrA peptide against the LOV2 domain in the dark. Finally, we demonstrate the functional utility of the switch through light-mediated subcellular localization in mammalian cell culture and reversible control of small GTPase signaling.

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Research Organization:: University of North Carolina, Chapel Hill, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); Human Frontier Science Program (HFSP) (France)

Grant/Contract Number:: W-31-109-Eng-38; GM093208

OSTI ID:: 1168516

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 1; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 355 works

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Improvement of phycocyanobilin synthesis for genetically encoded phytochrome-based optogenetics Uda, Youichi; Miura, Haruko; Goto, Yuhei bioRxiv https://doi.org/10.1101/2020.01.15.908343	posted_content	January 2020
Dynein–Dynactin–NuMA clusters generate cortical spindle-pulling forces as a multi-arm ensemble Okumura, Masako; Natsume, Toyoaki; Kanemaki, Masato T. eLife, Vol. 7 https://doi.org/10.7554/elife.36559	journal	May 2018
Optogenetics reveals Cdc42 local activation by scaffold-mediated positive feedback and Ras GTPase Lamas, Iker; Merlini, Laura; Vještica, Aleksandar bioRxiv https://doi.org/10.1101/710855	posted_content	August 2019
Induction of Signal Transduction by Using Non-Channelrhodopsin-Type Optogenetic Tools Ueda, Yoshibumi; Sato, Moritoshi ChemBioChem, Vol. 19, Issue 12 https://doi.org/10.1002/cbic.201700635	journal	May 2018
Optimized second-generation CRY2–CIB dimerizers and photoactivatable Cre recombinase Taslimi, Amir; Zoltowski, Brian; Miranda, Jose G. Nature Chemical Biology, Vol. 12, Issue 6 https://doi.org/10.1038/nchembio.2063	journal	April 2016
Near-infrared optogenetic pair for protein regulation and spectral multiplexing Redchuk, Taras A.; Omelina, Evgeniya S.; Chernov, Konstantin G. Nature Chemical Biology, Vol. 13, Issue 6 https://doi.org/10.1038/nchembio.2343	journal	March 2017
Light-induced nuclear export reveals rapid dynamics of epigenetic modifications Yumerefendi, Hayretin; Lerner, Andrew Michael; Zimmerman, Seth Parker Nature Chemical Biology, Vol. 12, Issue 6 https://doi.org/10.1038/nchembio.2068	journal	April 2016
Designing protein structures and complexes with the molecular modeling program Rosetta Kuhlman, Brian Journal of Biological Chemistry, Vol. 294, Issue 50 https://doi.org/10.1074/jbc.aw119.008144	journal	November 2019
Targeted mutagenesis: A sniper-like diversity generator in microbial engineering Zheng, Xiang; Xing, Xin-Hui; Zhang, Chong Synthetic and Systems Biotechnology, Vol. 2, Issue 2 https://doi.org/10.1016/j.synbio.2017.07.001	journal	June 2017
Optogenetic Control of Protein Function: From Intracellular Processes to Tissue Morphogenesis Guglielmi, Giorgia; Falk, Henning Johannes; De Renzis, Stefano Trends in Cell Biology, Vol. 26, Issue 11 https://doi.org/10.1016/j.tcb.2016.09.006	journal	November 2016
Optical Control of Peroxisomal Trafficking Spiltoir, Jessica I.; Strickland, Devin; Glotzer, Michael ACS Synthetic Biology, Vol. 5, Issue 7 https://doi.org/10.1021/acssynbio.5b00144	journal	November 2015
A Phytochrome-Derived Photoswitch for Intracellular Transport Adrian, Max; Nijenhuis, Wilco; Hoogstraaten, Rein I. ACS Synthetic Biology, Vol. 6, Issue 7 https://doi.org/10.1021/acssynbio.6b00333	journal	March 2017
A bacterial phytochrome-based optogenetic system controllable with near-infrared light Kaberniuk, Andrii A.; Shemetov, Anton A.; Verkhusha, Vladislav V. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3864	journal	May 2016
Control of microtubule dynamics using an optogenetic microtubule plus end–F-actin cross-linker Adikes, Rebecca C.; Hallett, Ryan A.; Saway, Brian F. Journal of Cell Biology, Vol. 217, Issue 2 https://doi.org/10.1083/jcb.201705190	journal	December 2017
Optimized light-inducible transcription in mammalian cells using Flavin Kelch-repeat F-box1/GIGANTEA and CRY2/CIB1 Quejada, Jose R.; Park, Seon-Hye E.; Awari, Daniel W. Nucleic Acids Research, Vol. 45, Issue 20 https://doi.org/10.1093/nar/gkx804	journal	October 2017
An engineered photoswitchable mammalian pyruvate kinase Gehrig, Stefanie; Macpherson, Jamie A.; Driscoll, Paul C. The FEBS Journal, Vol. 284, Issue 18 https://doi.org/10.1111/febs.14175	journal	August 2017
The rise of photoresponsive protein technologies applications in vivo: a spotlight on zebrafish developmental and cell biology Chow, Renee Wei-Yan; Vermot, Julien F1000Research, Vol. 6 https://doi.org/10.12688/f1000research.10617.1	journal	April 2017
Signaling in T cells – is anything the m(a)TOR with the picture(s)? Boothby, Mark F1000Research, Vol. 5 https://doi.org/10.12688/f1000research.7027.1	journal	February 2016
Predicting individual-level income from Facebook profiles Matz, Sandra C.; Menges, Jochen I.; Stillwell, David J. PLOS ONE, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pone.0214369	journal	March 2019
Photoreceptor engineering Ziegler, Thea; Möglich, Andreas Humboldt-Universität zu Berlin https://doi.org/10.18452/20825	text	January 2015
KRASmutations in blood circulating cell-free DNA: a pancreatic cancer case-control Le Calvez-Kelm, Florence; Foll, Matthieu; Wozniak, Magdalena B. Oncotarget, Vol. 7, Issue 48 https://doi.org/10.18632/oncotarget.12386	journal	October 2016
Hydrogels With Tunable Mechanical Properties Based on Photocleavable Proteins Xiang, Dongfang; Wu, Xin; Cao, Wei Frontiers in Chemistry, Vol. 8 https://doi.org/10.3389/fchem.2020.00007	journal	January 2020
Flash-and-Freeze: Coordinating Optogenetic Stimulation with Rapid Freezing to Visualize Membrane Dynamics at Synapses with Millisecond Resolution Watanabe, Shigeki Frontiers in Synaptic Neuroscience, Vol. 8 https://doi.org/10.3389/fnsyn.2016.00024	journal	August 2016
Mice endometrium receptivity in early pregnancy is impaired by maternal hyperinsulinemia Li, Runqin; Wu, Juan; He, Junlin Molecular Medicine Reports, Vol. 15, Issue 5 https://doi.org/10.3892/mmr.2017.6322	journal	March 2017
Controlling Organization and Forces in Active Matter Through Optically-Defined Boundaries Ross, Tyler D.; Lee, Heun Jin; Qu, Zijie arXiv https://doi.org/10.48550/arxiv.1812.09418	text	January 2018

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