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CryoEM and AI reveal a structure of SARS-CoV-2 Nsp2, a multifunctional protein involved in key host processes
View ORCID ProfileMeghna Gupta, View ORCID ProfileCaleigh M. Azumaya, View ORCID ProfileMichelle Moritz, View ORCID ProfileSergei Pourmal, View ORCID ProfileAmy Diallo, View ORCID ProfileGregory E. Merz, View ORCID ProfileGwendolyn Jang, View ORCID ProfileMehdi Bouhaddou, View ORCID ProfileAndrea Fossati, View ORCID ProfileAxel F. Brilot, View ORCID ProfileDevan Diwanji, View ORCID ProfileEvelyn Hernandez, View ORCID ProfileNadia Herrera, View ORCID ProfileHuong T. Kratochvil, View ORCID ProfileVictor L. Lam, View ORCID ProfileFei Li, View ORCID ProfileYang Li, View ORCID ProfileHenry C. Nguyen, View ORCID ProfileCarlos Nowotny, View ORCID ProfileTristan W. Owens, View ORCID ProfileJessica K. Peters, View ORCID ProfileAlexandrea N. Rizo, View ORCID ProfileUrsula Schulze-Gahmen, Amber M. Smith, View ORCID ProfileIris D. Young, View ORCID ProfileZanlin Yu, View ORCID ProfileDaniel Asarnow, View ORCID ProfileChristian Billesbølle, View ORCID ProfileMelody G. Campbell, View ORCID ProfileJen Chen, View ORCID ProfileKuei-Ho Chen, View ORCID ProfileUn Seng Chio, View ORCID ProfileMiles Sasha Dickinson, Loan Doan, View ORCID ProfileMingliang Jin, View ORCID ProfileKate Kim, View ORCID ProfileJunrui Li, View ORCID ProfileYen-Li Li, View ORCID ProfileEdmond Linossi, View ORCID ProfileYanxin Liu, View ORCID ProfileMegan Lo, View ORCID ProfileJocelyne Lopez, View ORCID ProfileKyle E. Lopez, View ORCID ProfileAdamo Mancino, View ORCID ProfileFrank R. Moss III, View ORCID ProfileMichael D. Paul, View ORCID ProfileKomal Ishwar Pawar, View ORCID ProfileAdrian Pelin, View ORCID ProfileThomas H. Pospiech Jr., View ORCID ProfileCristina Puchades, View ORCID ProfileSoumya Govinda Remesh, View ORCID ProfileMaliheh Safari, View ORCID ProfileKaitlin Schaefer, View ORCID ProfileMing Sun, Mariano C Tabios, View ORCID ProfileAye C. Thwin, View ORCID ProfileErron W. Titus, View ORCID ProfileRaphael Trenker, View ORCID ProfileEric Tse, View ORCID ProfileTsz Kin Martin Tsui, View ORCID ProfileFeng Wang, View ORCID ProfileKaihua Zhang, View ORCID ProfileYang Zhang, View ORCID ProfileJianhua Zhao, View ORCID ProfileFengbo Zhou, View ORCID ProfileYuan Zhou, View ORCID ProfileLorena Zuliani-Alvarez, QCRG Structural Biology Consortium, View ORCID ProfileDavid A Agard, Yifan Cheng, View ORCID ProfileJames S Fraser, Natalia Jura, View ORCID ProfileTanja Kortemme, Aashish Manglik, Daniel R. Southworth, View ORCID ProfileRobert M Stroud, View ORCID ProfileDanielle L Swaney, View ORCID ProfileNevan J Krogan, View ORCID ProfileAdam Frost, Oren S Rosenberg, View ORCID ProfileKliment A Verba
doi: https://doi.org/10.1101/2021.05.10.443524
Meghna Gupta
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Caleigh M. Azumaya
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Michelle Moritz
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Sergei Pourmal
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Amy Diallo
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Gregory E. Merz
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Gwendolyn Jang
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Mehdi Bouhaddou
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Andrea Fossati
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Axel F. Brilot
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Devan Diwanji
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Evelyn Hernandez
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Nadia Herrera
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Huong T. Kratochvil
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Victor L. Lam
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Fei Li
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Yang Li
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Henry C. Nguyen
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Carlos Nowotny
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Tristan W. Owens
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Jessica K. Peters
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Alexandrea N. Rizo
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Ursula Schulze-Gahmen
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Amber M. Smith
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Iris D. Young
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Zanlin Yu
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Daniel Asarnow
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Christian Billesbølle
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Melody G. Campbell
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
6Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA
Jen Chen
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Kuei-Ho Chen
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Un Seng Chio
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Miles Sasha Dickinson
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Loan Doan
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Mingliang Jin
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Kate Kim
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Junrui Li
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Yen-Li Li
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Edmond Linossi
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Yanxin Liu
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Megan Lo
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Jocelyne Lopez
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Kyle E. Lopez
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Adamo Mancino
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Frank R. Moss III
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Michael D. Paul
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Komal Ishwar Pawar
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Adrian Pelin
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Thomas H. Pospiech Jr.
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Cristina Puchades
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Soumya Govinda Remesh
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Maliheh Safari
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Kaitlin Schaefer
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Ming Sun
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
7Beam Therapeutics, Cambridge, MA 02139, USA
Mariano C Tabios
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Aye C. Thwin
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Erron W. Titus
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Raphael Trenker
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Eric Tse
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Tsz Kin Martin Tsui
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Feng Wang
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Kaihua Zhang
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Yang Zhang
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Jianhua Zhao
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Fengbo Zhou
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
Yuan Zhou
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Lorena Zuliani-Alvarez
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
David A Agard
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
Yifan Cheng
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
9Howard Hughes Medical Institute, San Francisco, CA 94158, USA
James S Fraser
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
Natalia Jura
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
11Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA
Tanja Kortemme
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
10Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, CA 94158, USA
12The University of California, Berkeley–University of California, San Francisco Graduate Program in Bioengineering, University of California, San Francisco, CA 94158, USA
Aashish Manglik
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
13Department of Pharmaceutical Chemistry, University of California, San Francisco, CA 94158, USA
Daniel R. Southworth
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
Robert M Stroud
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
Danielle L Swaney
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
Nevan J Krogan
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
4Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA
5J. David Gladstone Institutes, San Francisco, CA 94158, USA
16Department of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
Adam Frost
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
14Chan-Zuckerberg Biohub, San Francisco, CA 94158, USA
Oren S Rosenberg
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
8Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94158, USA
14Chan-Zuckerberg Biohub, San Francisco, CA 94158, USA
15Department of Medicine, University of California, San Francisco, CA 94143, USA
Kliment A Verba
1QBI Coronavirus Research Group Structural Biology Consortium, University of California, San Francisco, CA 94158, USA
2Quantitative Biosciences Institute (QBI) COVID-19 Research Group (QCRG), San Francisco, CA 94158, USA
3QBI, University of California, San Francisco, CA 94158, USA
13Department of Pharmaceutical Chemistry, University of California, San Francisco, CA 94158, USA
Abstract
The SARS-CoV-2 protein Nsp2 has been implicated in a wide range of viral processes, but its exact functions, and the structural basis of those functions, remain unknown. Here, we report an atomic model for full-length Nsp2 obtained by combining cryo-electron microscopy with deep learning-based structure prediction from AlphaFold2. The resulting structure reveals a highly-conserved zinc ion-binding site, suggesting a role for Nsp2 in RNA binding. Mapping emerging mutations from variants of SARS-CoV-2 on the resulting structure shows potential host-Nsp2 interaction regions. Using structural analysis together with affinity tagged purification mass spectrometry experiments, we identify Nsp2 mutants that are unable to interact with the actin-nucleation-promoting WASH protein complex or with GIGYF2, an inhibitor of translation initiation and modulator of ribosome-associated quality control. Our work suggests a potential role of Nsp2 in linking viral transcription within the viral replication-transcription complexes (RTC) to the translation initiation of the viral message. Collectively, the structure reported here, combined with mutant interaction mapping, provides a foundation for functional studies of this evolutionary conserved coronavirus protein and may assist future drug design.
Competing Interest Statement
J.S.F. is a founder of Keyhole Therapeutics and a shareholder of Relay Therapeutics and Keyhole Therapeutics. The Fraser laboratory has received sponsored research support from Relay Therapeutics. The Krogan Laboratory has received research support from Vir Biotechnology and F. Hoffmann-La Roche. N.K. has consulting agreements with Maze Therapeutics and Interline Therapeutics, and is a shareholder of Tenaya Therapeutics. A.F. is a shareholder of Relay Therapeutics. A.F. has received sponsored research support from Relay Therapeutics. Other authors declare no competing interests.
Copyright
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
Posted May 12, 2021.
CryoEM and AI reveal a structure of SARS-CoV-2 Nsp2, a multifunctional protein involved in key host processes
Meghna Gupta, Caleigh M. Azumaya, Michelle Moritz, Sergei Pourmal, Amy Diallo, Gregory E. Merz, Gwendolyn Jang, Mehdi Bouhaddou, Andrea Fossati, Axel F. Brilot, Devan Diwanji, Evelyn Hernandez, Nadia Herrera, Huong T. Kratochvil, Victor L. Lam, Fei Li, Yang Li, Henry C. Nguyen, Carlos Nowotny, Tristan W. Owens, Jessica K. Peters, Alexandrea N. Rizo, Ursula Schulze-Gahmen, Amber M. Smith, Iris D. Young, Zanlin Yu, Daniel Asarnow, Christian Billesbølle, Melody G. Campbell, Jen Chen, Kuei-Ho Chen, Un Seng Chio, Miles Sasha Dickinson, Loan Doan, Mingliang Jin, Kate Kim, Junrui Li, Yen-Li Li, Edmond Linossi, Yanxin Liu, Megan Lo, Jocelyne Lopez, Kyle E. Lopez, Adamo Mancino, Frank R. Moss III, Michael D. Paul, Komal Ishwar Pawar, Adrian Pelin, Thomas H. Pospiech Jr., Cristina Puchades, Soumya Govinda Remesh, Maliheh Safari, Kaitlin Schaefer, Ming Sun, Mariano C Tabios, Aye C. Thwin, Erron W. Titus, Raphael Trenker, Eric Tse, Tsz Kin Martin Tsui, Feng Wang, Kaihua Zhang, Yang Zhang, Jianhua Zhao, Fengbo Zhou, Yuan Zhou, Lorena Zuliani-Alvarez, QCRG Structural Biology Consortium, David A Agard, Yifan Cheng, James S Fraser, Natalia Jura, Tanja Kortemme, Aashish Manglik, Daniel R. Southworth, Robert M Stroud, Danielle L Swaney, Nevan J Krogan, Adam Frost, Oren S Rosenberg, Kliment A Verba
bioRxiv 2021.05.10.443524; doi: https://doi.org/10.1101/2021.05.10.443524
CryoEM and AI reveal a structure of SARS-CoV-2 Nsp2, a multifunctional protein involved in key host processes
Meghna Gupta, Caleigh M. Azumaya, Michelle Moritz, Sergei Pourmal, Amy Diallo, Gregory E. Merz, Gwendolyn Jang, Mehdi Bouhaddou, Andrea Fossati, Axel F. Brilot, Devan Diwanji, Evelyn Hernandez, Nadia Herrera, Huong T. Kratochvil, Victor L. Lam, Fei Li, Yang Li, Henry C. Nguyen, Carlos Nowotny, Tristan W. Owens, Jessica K. Peters, Alexandrea N. Rizo, Ursula Schulze-Gahmen, Amber M. Smith, Iris D. Young, Zanlin Yu, Daniel Asarnow, Christian Billesbølle, Melody G. Campbell, Jen Chen, Kuei-Ho Chen, Un Seng Chio, Miles Sasha Dickinson, Loan Doan, Mingliang Jin, Kate Kim, Junrui Li, Yen-Li Li, Edmond Linossi, Yanxin Liu, Megan Lo, Jocelyne Lopez, Kyle E. Lopez, Adamo Mancino, Frank R. Moss III, Michael D. Paul, Komal Ishwar Pawar, Adrian Pelin, Thomas H. Pospiech Jr., Cristina Puchades, Soumya Govinda Remesh, Maliheh Safari, Kaitlin Schaefer, Ming Sun, Mariano C Tabios, Aye C. Thwin, Erron W. Titus, Raphael Trenker, Eric Tse, Tsz Kin Martin Tsui, Feng Wang, Kaihua Zhang, Yang Zhang, Jianhua Zhao, Fengbo Zhou, Yuan Zhou, Lorena Zuliani-Alvarez, QCRG Structural Biology Consortium, David A Agard, Yifan Cheng, James S Fraser, Natalia Jura, Tanja Kortemme, Aashish Manglik, Daniel R. Southworth, Robert M Stroud, Danielle L Swaney, Nevan J Krogan, Adam Frost, Oren S Rosenberg, Kliment A Verba
bioRxiv 2021.05.10.443524; doi: https://doi.org/10.1101/2021.05.10.443524
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