Irreversible light-activated SpyLigation mediates split-protein assembly in 4D

Brizzia G. Munoz-Robles, Cole A. DeForest

Published: 2024-01-22 DOI: 10.1038/s41596-023-00938-0

LASL

SpyLigation

split-protein assembly

photocaging

protein activation

AI 解读

Supplementary information

Reporting Summary

Genetic manipulation and immortalized culture of ex vivo primary human germinal center B cells

The cell-line-derived subcutaneous tumor model in preclinical cancer research

Subcellular patch-clamp techniques for single-bouton stimulation and simultaneous pre- and postsynaptic recording at cortical synapses

NovoSpaRc: flexible spatial reconstruction of single-cell gene expression with optimal transport

Genome-wide pooled CRISPR screening in neurospheres

High-throughput cultivation and identification of bacteria from the plant root microbiota

Viral crosslinking and solid-phase purification enables discovery of ribonucleoprotein complexes on incoming RNA virus genomes

Mitochondrial single-cell ATAC-seq for high-throughput multi-omic detection of mitochondrial genotypes and chromatin accessibility

Addendum: Micro-CT acquisition and image processing to track and characterize pulmonary nodules in mice

Multiplexed single-cell proteomics using SCoPE2

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Shekhawat, S. S. & Ghosh, I. Split-protein systems: beyond binary protein–protein interactions. Curr. Opin. Chem. Biol. 15, 789–797 (2011).
Michnick, S. W., Ear, P. H., Manderson, E. N., Remy, I. & Stefan, E. Universal strategies in research and drug discovery based on protein-fragment complementation assays. Nat. Rev. Drug Discov. 6, 569–582 (2007).
Fink, T. et al. Design of fast proteolysis-based signaling and logic circuits in mammalian cells. Nat. Chem. Biol. 15, 115–122 (2019).
Rihtar, E. et al. Chemically inducible split protein regulators for mammalian cells. Nat. Chem. Biol. 19, 64–71 (2023).
Gao, Y. et al. Complex transcriptional modulation with orthogonal and inducible dCas9 regulators. Nat. Methods 13, 1043–1049 (2016).
Farrar, M. A., Alberola-lla, J. & Perlmutter, R. M. Activation of the Raf-1 kinase cascade by coumermycin-induced dimerization. Nature 383, 178–181 (1996).
Spencer, D. M., Wandless, T. J., Schreiber, S. L. & Crabtree, G. R. Controlling signal transduction with synthetic ligands. Science 262, 1019–1024 (1993).
Kawano, F., Suzuki, H., Furuya, A. & Sato, M. Engineered pairs of distinct photoswitches for optogenetic control of cellular proteins. Nat. Commun. 6, 6256 (2015).
Levskaya, A., Weiner, O. D., Lim, W. A. & Voigt, C. A. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 461, 997–1001 (2009).
Kennedy, M. J. et al. Rapid blue-light–mediated induction of protein interactions in living cells. Nat. Methods 7, 973–975 (2010).
Ruskowitz, E. R. et al. Spatiotemporal functional assembly of split protein pairs through a light-activated SpyLigation. Nat. Chem. 15, 694–704 (2023).
Zakeri, B. et al. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc. Natl Acad. Sci. USA 109, E690–7 (2012).
Keeble, A. H. & Howarth, M. Power to the protein: enhancing and combining activities using the Spy toolbox. Chem. Sci. 11, 7281–7291 (2020).
Keeble, A. H. & Howarth, M. in Methods in Enzymology vol. 617 443–461 (Elsevier, 2019).
Hoorens, M. W. H. & Szymanski, W. Reversible, spatial and temporal control over protein activity using light. Trends Biochem. Sci. 43, 567–575 (2018).
Ruskowitz, E. R. & DeForest, C. A. Proteome-wide analysis of cellular response to ultraviolet light for biomaterial synthesis and modification. ACS Biomater. Sci. Eng. 5, 2111–2116 (2019).
Chin, J. W. Expanding and reprogramming the genetic code. Nature 550, 53–60 (2017).
Chen, P. R. et al. A facile system for encoding unnatural amino acids in mammalian cells. Angew. Chem. Int. Ed. 48, 4052–4055 (2009).
Young, T. S., Ahmad, I., Yin, J. A. & Schultz, P. G. An enhanced system for unnatural amino acid mutagenesis in E. coli. J. Mol. Biol. 395, 361–374 (2010).
Yanagisawa, T. et al. Multistep engineering of Pyrrolysyl–tRNA synthetase to genetically encode Nɛ-(o-Azidobenzyloxycarbonyl) lysine for site-specific protein modification. Chem. Biol. 15, 1187–1197 (2008).
Serfling, R. et al. Designer tRNAs for efficient incorporation of non-canonical amino acids by the pyrrolysine system in mammalian cells. Nucleic Acids Res. 46, 1–10 (2018).
To, T.-L., Zhang, Q. & Shu, X. Structure-guided design of a reversible fluorogenic reporter of protein-protein interactions: design of a reversible fluorogenic reporter of PPIs. Protein Sci. 25, 748–753 (2016).
Hall, M. P. et al. Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. ACS Chem. Biol. 7, 1848–1857 (2012).
Guimaraes, C. P. et al. Site-specific C-terminal and internal loop labeling of proteins using sortase-mediated reactions. Nat. Protoc. 8, 1787–1799 (2013).
Mao, H., Hart, S. A., Schink, A. & Pollok, B. A. Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc. 126, 2670–2671 (2004).
Shadish, J. A., Benuska, G. M. & DeForest, C. A. Bioactive site-specifically modified proteins for 4D patterning of gel biomaterials. Nat. Mater. 18, 1005–1014 (2019).
Gawade, P. M., Shadish, J. A., Badeau, B. A. & DeForest, C. A. Logic‐based delivery of site‐ specifically modified proteins from environmentally responsive hydrogel biomaterials. Adv. Mater. 31, 1902462 (2019).
Batalov, I., Stevens, K. R. & DeForest, C. A. Photopatterned biomolecule immobilization to guide three-dimensional cell fate in natural protein-based hydrogels. Proc. Natl Acad. Sci. USA 118, e2014194118 (2021).
Agard, N. J., Prescher, J. A. & Bertozzi, C. R. A strain-promoted [3 + 2] azide−alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126, 15046–15047 (2004).
DeForest, C. A., Polizzotti, B. D. & Anseth, K. S. Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments. Nat. Mater. 8, 659–664 (2009).
Arakawa, C. K., Badeau, B. A., Zheng, Y. & DeForest, C. A. Multicellular vascularized engineered tissues through user‐programmable biomaterial photodegradation. Adv. Mater. 29, 1703156 (2017).
Badeau, B. A., Comerford, M. P., Arakawa, C. K., Shadish, J. A. & DeForest, C. A. Engineered modular biomaterial logic gates for environmentally triggered therapeutic delivery. Nat. Chem. 10, 251–258 (2018).
Szymczak, A. L. et al. Correction of multi-gene deficiency in vivo using a single ‘self-cleaving’ 2A peptide–based retroviral vector. Nat. Biotechnol. 22, 589–594 (2004).
Roberts, P. J. et al. Rho family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J. Biol. Chem. 283, 25150–25163 (2008).
Keeble, A. H. et al. Approaching infinite affinity through engineering of peptide–protein interaction. Proc. Natl Acad. Sci. USA 116, 26523–26533 (2019).
Keeble, A. H. et al. DogCatcher allows loop-friendly protein–protein ligation. Cell Chem. Biol. 29, 339–350.e10 (2022).
Wu, X.-L., Liu, Y., Liu, D., Sun, F. & Zhang, W.-B. An intrinsically disordered peptide-peptide stapler for highly efficient protein ligation both in vivo and in vitro. J. Am. Chem. Soc. 140, 17474–17483 (2018).
Fierer, J. O., Veggiani, G. & Howarth, M. SpyLigase peptide–peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture. Proc. Natl Acad. Sci. USA 111, E1176–E1181 (2014).
Buldun, C. M., Jean, J. X., Bedford, M. R. & Howarth, M. Snoopligase catalyzes peptide– peptide locking and enables solid-phase conjugate isolation. J. Am. Chem. Soc. 140, 3008–3018 (2018).
Lorand, L. & Graham, R. M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4, 140–156 (2003).
Fegan, A., White, B., Carlson, J. C. T. & Wagner, C. R. Chemically controlled protein assembly: techniques and applications. Chem. Rev. 110, 3315–3336 (2010).
Sun, J. & Sadelain, M. The quest for spatio-temporal control of CAR T cells. Cell Res. 25, 1281–1282 (2015).
Barlow, A. D., Nicholson, M. L. & Herbert, T. P. Evidence for rapamycin toxicity in pancreatic β-cells and a review of the underlying molecular mechanisms. Diabetes 62, 2674–2682 (2013).
Hartzell, E. J., Terr, J. & Chen, W. Engineering a Blue Light Inducible SpyTag System (BLISS). J. Am. Chem. Soc. 143, 8572–8577 (2021).
Wong, S., Mosabbir, A. A. & Truong, K. An engineered split intein for photoactivated protein trans-splicing. PLoS ONE 10, e0135965 (2015).
Cadet, J., Sage, E. & Douki, T. Ultraviolet radiation-mediated damage to cellular DNA. Mutat. Res. Mol. Mech. Mutagen. 571, 3–17 (2005).
Lawrence, K. P. et al. The UV/visible radiation boundary region (385–405 nm) damages skin cells and induces “dark” cyclobutane pyrimidine dimers in human skin in vivo. Sci. Rep. 8, 12722 (2018).
Kozmin, S. et al. UVA radiation is highly mutagenic in cells that are unable to repair 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 102, 13538–13543 (2005).
Zhang, W. et al. Optogenetic control with a photocleavable protein, PhoCl. Nat. Methods 14, 391–394 (2017).
Coin, I., Beyermann, M. & Bienert, M. Solid-phase peptide synthesis: from standard procedures to the synthesis of difficult sequences. Nat. Protoc. 2, 3247–3256 (2007).
Kawada, Y., Kodama, T., Miyashita, K., Imanishi, T. & Obika, S. Synthesis and evaluation of novel caged DNA alkylating agents bearing 3,4-epoxypiperidine structure. Org. Biomol. Chem. 10, 5102 (2012).
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
Baek, M. et al. Accurate prediction of protein structures and interactions using a three-track neural network. Science 373, 871–876 (2021).
Dolberg, T. B. et al. Computation-guided optimization of split protein systems. Nat. Chem. Biol. 17, 531–539 (2021).
Chen, X., Zaro, J. L. & Shen, W.-C. Fusion protein linkers: property, design and functionality. Adv. Drug Deliv. Rev. 65, 1357–1369 (2013).
Phillips-Jones, M. K., Hill, L. S., Atkinson, J. & Martin, R. Context effects on misreading and suppression at UAG codons in human cells. Mol. Cell. Biol. 15, 6593–6600 (1995).
Beier, H. Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res. 29, 4767–4782 (2001).
Shadish, J. A. & DeForest, C. A. Site-selective protein modification: from functionalized proteins to functional biomaterials. Matter 2, 50–77 (2020).
Stoien, J. D. & Wang, R. J. Effect of near-ultraviolet and visible light on mammalian cells in culture. II. Formation of toxic photoproducts in tissue culture medium by blacklight. Proc. Natl Acad. Sci. USA 71, 3961–3965 (1974).
DeForest, C. A. & Tirrell, D. A. A photoreversible protein-patterning approach for guiding stem cell fate in three-dimensional gels. Nat. Mater. 14, 523–531 (2015).

Irreversible light-activated SpyLigation mediates split-protein assembly in 4D

Supplementary information

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