ACS Publications. Most Trusted. Most Cited. Most Read

OR SEARCH CITATIONS

My Activity
Publications
CONTENT TYPES

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Am. Chem. Soc. 2020, 142, 11, 5078-5086
RETURN TO ISSUEPREVArticleNEXT

Tyrosinase-Mediated Oxidative Coupling of Tyrosine Tags on Peptides and Proteins

  • Alan M. Marmelstein
    Alan M. Marmelstein
    Department of Chemistry, University of California at Berkeley, Berkeley, California 94720, United States
    More by Alan M. Marmelstein
  • , 
  • Marco J. Lobba
    Marco J. Lobba
    Department of Chemistry, University of California at Berkeley, Berkeley, California 94720, United States
    More by Marco J. Lobba
  • , 
  • Casey S. Mogilevsky
    Casey S. Mogilevsky
    Department of Chemistry, University of California at Berkeley, Berkeley, California 94720, United States
    More by Casey S. Mogilevsky
  • , 
  • Johnathan C. Maza
    Johnathan C. Maza
    Department of Chemistry, University of California at Berkeley, Berkeley, California 94720, United States
    More by Johnathan C. Maza
    Orcidhttp://orcid.org/0000-0003-2898-8770
  • , 
  • Daniel D. Brauer
    Daniel D. Brauer
    Department of Chemistry, University of California at Berkeley, Berkeley, California 94720, United States
    More by Daniel D. Brauer
  • , and 
  • Matthew B. Francis*
    Matthew B. Francis
    Department of Chemistry, University of California at Berkeley, Berkeley, California 94720, United States
    Materials Sciences Division, Lawrence Berkeley National Laboratories, Berkeley, California 94720, United States
    *[email protected]
    More by Matthew B. Francis
    Orcidhttp://orcid.org/0000-0003-2837-2538
Cite this: J. Am. Chem. Soc. 2020, 142, 11, 5078–5086
Publication Date (Web):February 24, 2020
https://doi.org/10.1021/jacs.9b12002
Copyright © 2020 American Chemical Society
Request reuse permissions

    Article Views

    8218

    Altmetric

    -

    Citations

    49
    LEARN ABOUT THESE METRICS
    Other access options
    Get e-Alerts
    Supporting Info (1)»
    SUBJECTS:

    Abstract

    Abstract Image

    Oxidative coupling (OC) through o-quinone intermediates has been established as an efficient and site-selective way to modify protein N-termini and the unnatural amino acid p-aminophenylalanine (paF). Recently, we reported that the tyrosinase-mediated oxidation of phenol-tagged cargo molecules is a particularly convenient method of generating o-quinones in situ. The coupling partners can be easily prepared and stored, the reaction takes place under mild conditions (phosphate buffer, pH 6.5, 4 to 23 °C), and dissolved oxygen is the only oxidant required. Here, we show an important extension of this chemistry for the activation of tyrosine residues that project into solution from the N or C-termini of peptide and protein substrates. Generating the o-quinone electrophiles from tyrosine allows greater flexibility in choosing the nucleophilic coupling partner and expands the scope of the reaction to include C-terminal positions. We also introduce a new bacterial tyrosinase enzyme that shows improved activation for some tyrosine substrates. The efficacy of several secondary amines and aniline derivatives was evaluated in the coupling reactions, providing important information for coupling partner design. This strategy was used to modify the C-termini of an antibody scFv construct and of Protein L, a human IgG kappa light chain binding protein. The use of the modified proteins as immunolabeling agents was also demonstrated.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.9b12002.

    • Experimental procedures, full mass spectra of key proteins before and after coupling, NMR spectra of the small molecule oxidative coupling product, flow cytometry gating schemes and statistics, and other relevant data (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 49 publications.

    1. Hao Zhu, Jae Hoon Oh, Yuna Matsuda, Takeharu Mino, Mamoru Ishikawa, Hideki Nakamura, Muneo Tsujikawa, Hiroshi Nonaka, Itaru Hamachi. Tyrosinase-Based Proximity Labeling in Living Cells and In Vivo. Journal of the American Chemical Society 2024, 146 (11) , 7515-7523. https://doi.org/10.1021/jacs.3c13183
    2. Wendy Cao, Johnathan C. Maza, Natalia Chernyak, John A. Flygare, Shane W. Krska, F. Dean Toste, Matthew B. Francis. Modification of Cysteine-Substituted Antibodies Using Enzymatic Oxidative Coupling Reactions. Bioconjugate Chemistry 2023, 34 (3) , 510-517. https://doi.org/10.1021/acs.bioconjchem.2c00576
    3. Page N. Daniels, Wilfred A. van der Donk. Substrate Specificity of the Flavoenzyme BhaC1 That Converts a C-Terminal Trp to a Hydroxyquinone. Biochemistry 2023, 62 (2) , 378-387. https://doi.org/10.1021/acs.biochem.2c00206
    4. Amanda J. Bischoff, Conner C. Harper, Evan R. Williams, Matthew B. Francis. Characterizing Heterogeneous Mixtures of Assembled States of the Tobacco Mosaic Virus Using Charge Detection Mass Spectrometry. Journal of the American Chemical Society 2022, 144 (51) , 23368-23378. https://doi.org/10.1021/jacs.2c09160
    5. Xingyu Ji, Nanlin Zhu, Yanjie Ma, Jia Liu, Youhong Hu. Protein C-Terminal Tyrosine Conjugation via Recyclable Immobilized BmTYR. ACS Omega 2022, 7 (44) , 40532-40539. https://doi.org/10.1021/acsomega.2c05794
    6. Johnathan C. Maza, Derek M. García-Almedina, Lydia E. Boike, Noah X. Hamlish, Daniel K. Nomura, Matthew B. Francis. Tyrosinase-Mediated Synthesis of Nanobody–Cell Conjugates. ACS Central Science 2022, 8 (7) , 955-962. https://doi.org/10.1021/acscentsci.1c01265
    7. Joshua A. Walker, Noah Hamlish, Avery Tytla, Daniel D. Brauer, Matthew B. Francis, Alanna Schepartz. Redirecting RiPP Biosynthetic Enzymes to Proteins and Backbone-Modified Substrates. ACS Central Science 2022, 8 (4) , 473-482. https://doi.org/10.1021/acscentsci.1c01577
    8. Katsuya Maruyama, Takashi Ishiyama, Yohei Seki, Kentaro Sakai, Takaya Togo, Kounosuke Oisaki, Motomu Kanai. Protein Modification at Tyrosine with Iminoxyl Radicals. Journal of the American Chemical Society 2021, 143 (47) , 19844-19855. https://doi.org/10.1021/jacs.1c09066
    9. Casey S. Mogilevsky, Marco J. Lobba, Daniel D. Brauer, Alan M. Marmelstein, Johnathan C. Maza, Jamie M. Gleason, Jennifer A. Doudna, Matthew B. Francis. Synthesis of Multi-Protein Complexes through Charge-Directed Sequential Activation of Tyrosine Residues. Journal of the American Chemical Society 2021, 143 (34) , 13538-13547. https://doi.org/10.1021/jacs.1c03079
    10. Bauke Albada, Jordi F. Keijzer, Han Zuilhof, Floris van Delft. Oxidation-Induced “One-Pot” Click Chemistry. Chemical Reviews 2021, 121 (12) , 7032-7058. https://doi.org/10.1021/acs.chemrev.0c01180
    11. Alexandra V. Ramsey, Amanda J. Bischoff, Matthew B. Francis. Enzyme Activated Gold Nanoparticles for Versatile Site-Selective Bioconjugation. Journal of the American Chemical Society 2021, 143 (19) , 7342-7350. https://doi.org/10.1021/jacs.0c11678
    12. Marco J. Lobba, Christof Fellmann, Alan M. Marmelstein, Johnathan C. Maza, Elijah N. Kissman, Stephanie A. Robinson, Brett T. Staahl, Cole Urnes, Rachel J. Lew, Casey S. Mogilevsky, Jennifer A. Doudna, Matthew B. Francis. Site-Specific Bioconjugation through Enzyme-Catalyzed Tyrosine–Cysteine Bond Formation. ACS Central Science 2020, 6 (9) , 1564-1571. https://doi.org/10.1021/acscentsci.0c00940
    13. Michael B. Geeson, Gonçalo J. L. Bernardes. Protein–Protein Conjugates: Tyrosine Delivers. ACS Central Science 2020, 6 (9) , 1473-1475. https://doi.org/10.1021/acscentsci.0c01008
    14. Simon Edelmann, Jean-Philip Lumb. A para- to meta-isomerization of phenols. Nature Chemistry 2024, 9 https://doi.org/10.1038/s41557-024-01512-1
    15. Suwei Dong, Ji-Shen Zheng, Yiming Li, Huan Wang, Gong Chen, Yongxiang Chen, Gemin Fang, Jun Guo, Chunmao He, Honggang Hu, Xuechen Li, Yanmei Li, Zigang Li, Man Pan, Shan Tang, Changlin Tian, Ping Wang, Bian Wu, Chuanliu Wu, Junfeng Zhao, Lei Liu. Recent advances in chemical protein synthesis: method developments and biological applications. Science China Chemistry 2024, 67 (4) , 1060-1096. https://doi.org/10.1007/s11426-024-1950-1
    16. Wei Huang, Scott T. Laughlin. Cell-selective bioorthogonal labeling. Cell Chemical Biology 2024, 31 (3) , 409-427. https://doi.org/10.1016/j.chembiol.2023.09.010
    17. Hongfei Chen, Hong‐Chai Fabio Wong, Jiaming Qiu, Biquan Li, Dingdong Yuan, Hao Kong, Yishu Bao, Yu Zhang, Zhiyi Xu, Ying‐Lung Steve Tse, Jiang Xia. Site‐Selective Tyrosine Reaction for Antibody‐Cell Conjugation and Targeted Immunotherapy. Advanced Science 2024, 11 (5) https://doi.org/10.1002/advs.202305012
    18. Hwaseok Hong, Uk-Jae Lee, Seul Hoo Lee, Hyun Kim, Gyu-Min Lim, Sang-Hyuk Lee, Hyeoncheol Francis Son, Byung-Gee Kim, Kyung-Jin Kim. Highly efficient site-specific protein modification using tyrosinase from Streptomyces avermitilis: Structural insight. International Journal of Biological Macromolecules 2024, 255 , 128313. https://doi.org/10.1016/j.ijbiomac.2023.128313
    19. Xiaoxuan Ma, Jian Jiang, Xiaoye An, Wanting Zu, Chi Ma, Zhuo Zhang, Yaci Lu, Lijing Zhao, Lisheng Wang. Advances in research based on antibody-cell conjugation. Frontiers in Immunology 2023, 14 https://doi.org/10.3389/fimmu.2023.1310130
    20. Sébastien Depienne, Mohammed Bouzelha, Emmanuelle Courtois, Karine Pavageau, Pierre-Alban Lalys, Maia Marchand, Dimitri Alvarez-Dorta, Steven Nedellec, Laura Marín-Fernández, Cyrille Grandjean, Mohammed Boujtita, David Deniaud, Mathieu Mével, Sébastien G. Gouin. Click-electrochemistry for the rapid labeling of virus, bacteria and cell surfaces. Nature Communications 2023, 14 (1) https://doi.org/10.1038/s41467-023-40534-0
    21. Susanta Bhunia, Manasa Purushotham, Ganesh Karan, Bishwajit Paul, Modhu Sudan Maji. Exploring Chemical Modifications of Aromatic Amino Acid Residues in Peptides. Synthesis 2023, 55 (22) , 3701-3724. https://doi.org/10.1055/a-2091-8062
    22. Shengping Zhang, Luis M. De Leon Rodriguez, Freda F. Li, Margaret A. Brimble. Recent developments in the cleavage, functionalization, and conjugation of proteins and peptides at tyrosine residues. Chemical Science 2023, 14 (29) , 7782-7817. https://doi.org/10.1039/D3SC02543H
    23. Soumya Jyoti Singha Roy, Conor Loynd, Delilah Jewel, Sarah E. Canarelli, Elise D. Ficaretta, Quan A. Pham, Eranthie Weerapana, Abhishek Chatterjee. Photoredox‐Catalyzed Labeling of Hydroxyindoles with Chemoselectivity (PhotoCLIC) for Site‐Specific Protein Bioconjugation. Angewandte Chemie 2023, 135 (27) https://doi.org/10.1002/ange.202300961
    24. Soumya Jyoti Singha Roy, Conor Loynd, Delilah Jewel, Sarah E. Canarelli, Elise D. Ficaretta, Quan A. Pham, Eranthie Weerapana, Abhishek Chatterjee. Photoredox‐Catalyzed Labeling of Hydroxyindoles with Chemoselectivity (PhotoCLIC) for Site‐Specific Protein Bioconjugation. Angewandte Chemie International Edition 2023, 62 (27) https://doi.org/10.1002/anie.202300961
    25. Cindy Rodriguez, Samantha Delaney, Joni Sebastiano, Samantha M. Sarrett, Mike A. Cornejo, Sarah Thau, Meena M. Hosny, Brian M. Zeglis. Site-selective radiolabeling using mushroom tyrosinase and the strain-promoted oxidation-controlled 1,2-quinone cycloaddition. RSC Advances 2023, 13 (26) , 17705-17709. https://doi.org/10.1039/D3RA03486K
    26. Jing Dai, Kiera B. Wilhelm, Amanda J. Bischoff, Jose H. Pereira, Michel T. Dedeo, Derek M. García‐Almedina, Paul D. Adams, Jay T. Groves, Matthew B. Francis. A Membrane‐Associated Light‐Harvesting Model is Enabled by Functionalized Assemblies of Gene‐Doubled TMV Proteins. Small 2023, 19 (20) https://doi.org/10.1002/smll.202207805
    27. Yeke Ni, Yu Wang, Alethea B. Tabor, John M. Ward, Helen C. Hailes. The use of tyrosinases in a chemoenzymatic cascade as a peptide ligation strategy. RSC Chemical Biology 2023, 4 (2) , 132-137. https://doi.org/10.1039/D2CB00237J
    28. Niklas Henrik Fischer, Maria Teresa Oliveira, Frederik Diness. Chemical modification of proteins – challenges and trends at the start of the 2020s. Biomaterials Science 2023, 11 (3) , 719-748. https://doi.org/10.1039/D2BM01237E
    29. Thomas A. King, Laura Rodríguez Pérez, Sabine L. Flitsch. Application of Biocatalysis for Protein Bioconjugation. 2023https://doi.org/10.1016/B978-0-32-390644-9.00122-0
    30. Jingyuan Liu, Mahesha M. Poojary, Mikkel B. Thygesen, Mogens L. Andersen, Marianne N. Lund. Temperature affects the kinetics but not the products of the reaction between 4-methylbenzoquinone and lysine. Food Research International 2023, 163 , 112187. https://doi.org/10.1016/j.foodres.2022.112187
    31. Xiaokang Ren, Luyang Zhao, Chengqian Yuan, Mengqian Shi, Ruirui Xing, Xuehai Yan. Enzyme-driven oxygen-fuelled pathway selectivity of tyrosine-containing peptide oxidation evolution. Chemical Engineering Journal 2022, 450 , 138293. https://doi.org/10.1016/j.cej.2022.138293
    32. Nina Declas, John R. J. Maynard, Laure Menin, Natalia Gasilova, Sebastian Götze, Jakob L. Sprague, Pierre Stallforth, Stefan Matile, Jerome Waser. Tyrosine bioconjugation with hypervalent iodine. Chemical Science 2022, 13 (43) , 12808-12817. https://doi.org/10.1039/D2SC04558C
    33. Hyunbin Choi, Kyueui Lee. Crosslinking Mechanisms of Phenol, Catechol, and Gallol for Synthetic Polyphenols: A Comparative Review. Applied Sciences 2022, 12 (22) , 11626. https://doi.org/10.3390/app122211626
    34. Mikail D. Levasseur, Raphael Hofmann, Thomas G. W. Edwardson, Svenja Hehn, Manutsawee Thanaburakorn, Jeffrey W. Bode, Donald Hilvert. Post‐Assembly Modification of Protein Cages by Ubc9‐Mediated Lysine Acylation. ChemBioChem 2022, 23 (20) https://doi.org/10.1002/cbic.202200332
    35. Hao‐Ran Jia, Ya‐Xuan Zhu, Yi Liu, Yuxin Guo, Sayed Mir Sayed, Xiao‐Yu Zhu, Xiaotong Cheng, Fu‐Gen Wu. Direct chemical editing of Gram‐positive bacterial cell walls via an enzyme‐catalyzed oxidative coupling reaction. Exploration 2022, 2 (5) https://doi.org/10.1002/EXP.20220010
    36. Xiaolin Pei, Zhiyuan Luo, Li Qiao, Qinjie Xiao, Pengfei Zhang, Anming Wang, Roger A. Sheldon. Putting precision and elegance in enzyme immobilisation with bio-orthogonal chemistry. Chemical Society Reviews 2022, 51 (16) , 7281-7304. https://doi.org/10.1039/D1CS01004B
    37. Chuan Wan, Yuena Wang, Chenshan Lian, Qi Chang, Yuhao An, Jiean Chen, Jinming Sun, Zhanfeng Hou, Dongyan Yang, Xiaochun Guo, Feng Yin, Rui Wang, Zigang Li. Histidine-specific bioconjugation via visible-light-promoted thioacetal activation. Chemical Science 2022, 13 (28) , 8289-8296. https://doi.org/10.1039/D2SC02353A
    38. Shengping Zhang, Luis M. De Leon Rodriguez, Freda F. Li, Renjie Huang, Ivanhoe K. H. Leung, Paul W. R. Harris, Margaret A. Brimble. A novel tyrosine hyperoxidation enables selective peptide cleavage. Chemical Science 2022, 13 (9) , 2753-2763. https://doi.org/10.1039/D1SC06216F
    39. Shinichi Sato. Protein Chemical Modification Using Highly Reactive Species and Spatial Control of Catalytic Reactions. Chemical and Pharmaceutical Bulletin 2022, 70 (2) , 95-105. https://doi.org/10.1248/cpb.c21-00915
    40. Eduardo Fuentes-Lemus, Per Hägglund, Camilo López-Alarcón, Michael J. Davies. Oxidative Crosslinking of Peptides and Proteins: Mechanisms of Formation, Detection, Characterization and Quantification. Molecules 2022, 27 (1) , 15. https://doi.org/10.3390/molecules27010015
    41. Karl D. Brune, Ilva Liekniņa, Grigorij Sutov, Alexander R. Morris, Dejana Jovicevic, Gints Kalniņš, Andris Kazāks, Rihards Kluga, Sabine Kastaljana, Anna Zajakina, Juris Jansons, Dace Skrastiņa, Karīna Spunde, Alexander A. Cohen, Pamela J. Bjorkman, Howard R. Morris, Edgars Suna, Kaspars Tārs. N‐Terminal Modification of Gly‐His‐Tagged Proteins with Azidogluconolactone. ChemBioChem 2021, 22 (22) , 3199-3207. https://doi.org/10.1002/cbic.202100381
    42. Joshua A. Baccile, Peter J. Voorhees, Anthony J. Chillo, Madeline Berry, Robin Morgenstern, Tyler J. Schwertfeger, Francis M. Rossi, Christian D. S. Nelson. Site‐Specific Small Molecule Labeling of an Internal Loop in JC Polyomavirus Pentamers Using the π‐Clamp‐Mediated Cysteine Conjugation. ChemBioChem 2021, 22 (21) , 3037-3041. https://doi.org/10.1002/cbic.202100188
    43. Augustine George, Mohan Indhu, Sundarapandian Ashokraj, Ganesh Shanmugam, Ponesakki Ganesan, Numbi Ramudu Kamini, Niraikulam Ayyadurai. Genetically encoded dihydroxyphenylalanine coupled with tyrosinase for strain promoted labeling. Bioorganic & Medicinal Chemistry 2021, 50 , 116460. https://doi.org/10.1016/j.bmc.2021.116460
    44. Fahimeh Tabatabaei, Morteza Rasoulianboroujeni, Amir Yadegari, Sanaz Tajik, Keyvan Moharamzadeh, Lobat Tayebi. Osteo-mucosal engineered construct: In situ adhesion of hard-soft tissues. Materials Science and Engineering: C 2021, 128 , 112255. https://doi.org/10.1016/j.msec.2021.112255
    45. Arnab Chowdhury, Saurav Chatterjee, Akumlong Pongen, Dhanjit Sarania, Nitesh Mani Tripathi, Anupam Bandyopadhyay. Site-Selective, Chemical Modification of Protein at Aromatic Side Chain and Their Emergent Applications. Protein & Peptide Letters 2021, 28 (7) , 788-808. https://doi.org/10.2174/0929866528666210129152535
    46. Kai Zhang, Lei Zhou, Tingting Zhang, Zhenqiang Fan, Minhao Xie, Yuedi Ding, Hao Li. Peptide based Biosensing of Protein Functional Control Indicates Novel Mechanism of Cancerous Development under Oxidative Stress. Sensors and Actuators B: Chemical 2021, 329 , 129121. https://doi.org/10.1016/j.snb.2020.129121
    47. Peter A. Szijj, Kristina A. Kostadinova, Richard J. Spears, Vijay Chudasama. Tyrosine bioconjugation – an emergent alternative. Organic & Biomolecular Chemistry 2020, 18 (44) , 9018-9028. https://doi.org/10.1039/D0OB01912G
    48. Dimitri Alvarez Dorta, David Deniaud, Mathieu Mével, Sébastien G. Gouin. Tyrosine Conjugation Methods for Protein Labelling. Chemistry – A European Journal 2020, 26 (63) , 14257-14269. https://doi.org/10.1002/chem.202001992
    49. Susan L. Knox, Angela Steinauer, Garrett Alpha-Cobb, Adam Trexler, Elizabeth Rhoades, Alanna Schepartz. Quantification of protein delivery in live cells using fluorescence correlation spectroscopy. 2020, 477-505. https://doi.org/10.1016/bs.mie.2020.05.007
    Download PDF

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect