RNA-Puzzles Round V: blind predictions of 23 RNA structures

Fan Bu; Yagoub Adam; Ryszard W Adamiak; Maciej Antczak; Belisa Rebeca H de Aquino; Nagendar Goud Badepally; Robert T Batey; Eugene F Baulin; Pawel Boinski; Michal J Boniecki; Janusz M Bujnicki; Kristy A Carpenter; Jose Chacon; Shi-Jie Chen; Wah Chiu; Pablo Cordero; Naba Krishna Das; Rhiju Das; Wayne K Dawson; Frank DiMaio; Feng Ding; Anne-Catherine Dock-Bregeon; Nikolay V Dokholyan; Ron O Dror; Stanisław Dunin-Horkawicz; Stephan Eismann; Eric Ennifar; Reza Esmaeeli; Masoud Amiri Farsani; Adrian R Ferré-D'Amaré; Caleb Geniesse; George E Ghanim; Horacio V Guzman; Iris V Hood; Lin Huang; Dharm Skandh Jain; Farhang Jaryani; Lei Jin; Astha Joshi; Masha Karelina; Jeffrey S Kieft; Wipapat Kladwang; Sebastian Kmiecik; Deepak Koirala; Markus Kollmann; Rachael C Kretsch; Mateusz Kurciński; Jun Li; Shuang Li; Marcin Magnus; BenoÎt Masquida; S Naeim Moafinejad; Arup Mondal; Sunandan Mukherjee; Thi Hoang Duong Nguyen; Grigory Nikolaev; Chandran Nithin; Grace Nye; Iswarya P N Pandaranadar Jeyeram; Alberto Perez; Phillip Pham; Joseph A Piccirilli; Smita Priyadarshini Pilla; Radosław Pluta; Simón Poblete; Almudena Ponce-Salvatierra; Mariusz Popenda; Lukasz Popenda; Fabrizio Pucci; Ramya Rangan; Angana Ray; Aiming Ren; Joanna Sarzynska; Congzhou Mike Sha; Filip Stefaniak; Zhaoming Su; Krishna C Suddala; Marta Szachniuk; Raphael Townshend; Robert J Trachman 3rd; Jian Wang; Wenkai Wang; Andrew Watkins; Tomasz K Wirecki; Yi Xiao; Peng Xiong; Yiduo Xiong; Jianyi Yang; Joseph David Yesselman; Jinwei Zhang; Yi Zhang; Zhenzhen Zhang; Yuanzhe Zhou; Tomasz Zok; Dong Zhang; Sicheng Zhang; Adriana Żyła; Eric Westhof; Zhichao Miao

doi:10.1038/s41592-024-02543-9

RNA-Puzzles Round V: blind predictions of 23 RNA structures

Nat Methods. 2024 Dec 2. doi: 10.1038/s41592-024-02543-9. Online ahead of print.

Authors

Fan Bu^{1

2}, Yagoub Adam^{3

4}, Ryszard W Adamiak^{5

6}, Maciej Antczak^{5

6}, Belisa Rebeca H de Aquino⁷, Nagendar Goud Badepally⁷, Robert T Batey⁸, Eugene F Baulin⁷, Pawel Boinski⁶, Michal J Boniecki⁷, Janusz M Bujnicki⁷, Kristy A Carpenter⁹, Jose Chacon^{10

11}, Shi-Jie Chen¹², Wah Chiu¹³, Pablo Cordero^{10

14}, Naba Krishna Das¹⁵, Rhiju Das^{10

16

17}, Wayne K Dawson⁷, Frank DiMaio^{18

19}, Feng Ding²⁰, Anne-Catherine Dock-Bregeon²¹, Nikolay V Dokholyan²², Ron O Dror^{23

24

25

26}, Stanisław Dunin-Horkawicz⁷, Stephan Eismann^{27

28}, Eric Ennifar²⁹, Reza Esmaeeli³⁰, Masoud Amiri Farsani⁷, Adrian R Ferré-D'Amaré³¹, Caleb Geniesse^{10

32}, George E Ghanim³³, Horacio V Guzman³⁴, Iris V Hood³⁵, Lin Huang³⁶, Dharm Skandh Jain⁷, Farhang Jaryani⁷, Lei Jin¹², Astha Joshi⁷, Masha Karelina^{17

23}, Jeffrey S Kieft^{37

38}, Wipapat Kladwang^{10

16}, Sebastian Kmiecik³⁹, Deepak Koirala¹⁵, Markus Kollmann⁴⁰, Rachael C Kretsch¹⁷, Mateusz Kurciński³⁹, Jun Li¹², Shuang Li³⁵, Marcin Magnus^{7

41}, BenoÎt Masquida⁴², S Naeim Moafinejad⁷, Arup Mondal³⁰, Sunandan Mukherjee⁷, Thi Hoang Duong Nguyen³³, Grigory Nikolaev⁷, Chandran Nithin^{7

39}, Grace Nye¹⁶, Iswarya P N Pandaranadar Jeyeram⁷, Alberto Perez³⁰, Phillip Pham¹⁶, Joseph A Piccirilli^{43

44}, Smita Priyadarshini Pilla⁴⁵, Radosław Pluta⁷, Simón Poblete^{46

47}, Almudena Ponce-Salvatierra⁷, Mariusz Popenda⁵, Lukasz Popenda⁴⁸, Fabrizio Pucci⁴⁹, Ramya Rangan^{17

28}, Angana Ray⁷, Aiming Ren⁵⁰, Joanna Sarzynska⁵, Congzhou Mike Sha²², Filip Stefaniak⁷, Zhaoming Su⁵¹, Krishna C Suddala³⁵, Marta Szachniuk^{5

6}, Raphael Townshend^{23

28}, Robert J Trachman 3rd³¹, Jian Wang²², Wenkai Wang⁵², Andrew Watkins^{10

53}, Tomasz K Wirecki⁷, Yi Xiao⁵⁴, Peng Xiong^{2

55}, Yiduo Xiong⁵⁴, Jianyi Yang⁵², Joseph David Yesselman^{16

56}, Jinwei Zhang³⁵, Yi Zhang⁵⁴, Zhenzhen Zhang²⁰, Yuanzhe Zhou¹², Tomasz Zok⁶, Dong Zhang¹², Sicheng Zhang¹², Adriana Żyła⁷, Eric Westhof^{57

58}, Zhichao Miao^{59

60

61}

Affiliations

¹ GMU-GIBH Joint School of Life Sciences, The Guangdong-Hong Kong-Macao Joint Laboratory for Cell Fate Regulation and Diseases, Guangzhou National Laboratory, Guangzhou Medical University, Guangzhou, China.
² School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Hefei, China.
³ Inter-institutional Graduate Program on Bioinformatics, Department of Computer Science and Mathematics, FFCLRP, University of São Paulo, Ribeirão Preto, Brazil.
⁴ Covenant University Bioinformatics Research (CUBRe), Covenant University, Ota, Nigeria.
⁵ Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznan, Poland.
⁶ Institute of Computing Science, Poznan University of Technology, Poznan, Poland.
⁷ Laboratory of Bioinformatics and Protein Engineering, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland.
⁸ Department of Biochemistry, University of Colorado at Boulder, Boulder, CO, USA.
⁹ Department of Biomedical Data Science, Stanford University, Stanford, CA, USA.
¹⁰ Department of Biochemistry, Stanford University, Stanford, CA, USA.
¹¹ Department of Cell and Developmental Biology, University of California San Diego, San Diego, CA, USA.
¹² Department of Physics, Department of Biochemistry and Institute for Data Science and Informatics, University of Missouri, Columbia, MO, USA.
¹³ Department of Bioengineering and James H. Clark Center, Stanford University, Stanford, CA, USA.
¹⁴ Stripe, South San Francisco, CA, USA.
¹⁵ Department of Chemistry and Biochemistry, University of Maryland Baltimore County, Baltimore, MD, USA.
¹⁶ Howard Hughes Medical Institute, Stanford University, Stanford, CA, USA.
¹⁷ Biophysics program, Stanford University, Stanford, CA, USA.
¹⁸ Department of Biochemistry, University of Washington, Seattle, WA, USA.
¹⁹ Institute for Protein Design, University of Washington, Seattle, WA, USA.
²⁰ Department of Physics and Astronomy, Clemson University, Clemson, SC, USA.
²¹ Laboratory of Integrative Biology of Marine Models (LBI2M), Sorbonne University-CNRS UMR8227, Roscoff, France.
²² Department of Pharmacology, Penn State College of Medicine, Hershey, PA, USA.
²³ Department of Computer Science, Stanford University, Stanford, CA, USA.
²⁴ Department of Structural Biology, Stanford University, Stanford, CA, USA.
²⁵ Department of Molecular and Cellular Physiology, Stanford University, Stanford, CA, USA.
²⁶ Institute for Computational and Mathematical Engineering, Stanford University, Stanford, CA, USA.
²⁷ Department of Applied Physics, Stanford University, Stanford, CA, USA.
²⁸ Atomic AI, South San Francisco, CA, USA.
²⁹ Architecture et Réactivité de l'ARN, Institut de Biologie Moléculaire et Cellulaire du CNRS, Université de Strasbourg, Strasbourg, France.
³⁰ Department of Chemistry and Quantum Theory Project, University of Florida, Gainesville, FL, USA.
³¹ Laboratory of Nucleic Acids, National Heart, Lung and Blood Institute, Bethesda, MD, USA.
³² Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
³³ Medical Research Council Laboratory of Molecular Biology, Cambridge, UK.
³⁴ Instituto de Ciencia de Materials de Barcelona, ICMAB-CSIC, Bellaterra E-08193, Spain & Departamento de Física Teórica de la Materia Condensada, Universidad Autónoma de Madrid, Madrid, Spain.
³⁵ Laboratory of Molecular Biology, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD, USA.
³⁶ Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Guangdong-Hong Kong Joint Laboratory for RNA Medicine, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University Guangzhou, Guangdong, China.
³⁷ Department of Biochemistry and Molecular Genetics, University of Colorado Denver School of Medicine, Aurora, CO, USA.
³⁸ New York Structural Biology Center, New York, NY, USA.
³⁹ Laboratory of Computational Biology, Biological and Chemical Research Center, Faculty of Chemistry, University of Warsaw, Warsaw, Poland.
⁴⁰ Department of Computer Science, Heinrich Heine University of Düsseldorf, Düsseldorf, Germany.
⁴¹ Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA, USA.
⁴² UMR 7156, CNRS - Université de Strasbourg, IPCB, Strasbourg, France.
⁴³ Department of Biochemistry and Molecular Biology, The University of Chicago, Chicago, IL, USA.
⁴⁴ Department of Chemistry, The University of Chicago, Chicago, IL, USA.
⁴⁵ Laboratory of Computational Biology, Biological and Chemical Research Center, University of Warsaw, Warsaw, Poland.
⁴⁶ Facultad de Ingeniería, Arquitectura y Diseño, Universidad San Sebastián, Santiago, Chile.
⁴⁷ Centro BASAL Ciencia & Vida, Universidad San Sebastián, Santiago, Chile.
⁴⁸ NanoBioMedical Centre, Adam Mickiewicz University, Poznan, Poland.
⁴⁹ Computational Biology and Bioinformatics, Université Libre de Bruxelles, Brussels, Belgium.
⁵⁰ Life Sciences Institute, Zhejiang University, Hangzhou, China.
⁵¹ The State Key Laboratory of Biotherapy, West China Hospital, Chengdu, China.
⁵² MOE Frontiers Science Center for Nonlinear Expectations, Research Center for Mathematics and Interdisciplinary Sciences, Shandong University, Qingdao, China.
⁵³ Prescient Design, Genentech Research and Early Development, South San Francisco, CA, USA.
⁵⁴ School of Physics and Key Laboratory of Molecular Biophysics of the Ministry of Education, Huazhong University of Science and Technology, Wuhan, China.
⁵⁵ Department of Biomedical Engineering, Suzhou Institute for Advanced Research, University of Science and Technology of China, Suzhou, China.
⁵⁶ Department of Chemistry, University of Nebraska, Lincoln, NE, USA.
⁵⁷ Architecture et Réactivité de l'ARN, Institut de Biologie Moléculaire et Cellulaire du CNRS, Université de Strasbourg, Strasbourg, France. e.westhof@ibmc-cnrs.unistra.fr.
⁵⁸ Engineering Research Center of Clinical Functional Materials and Diagnosis & Treatment Devices of Zhejiang Province, Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou, China. e.westhof@ibmc-cnrs.unistra.fr.
⁵⁹ GMU-GIBH Joint School of Life Sciences, The Guangdong-Hong Kong-Macao Joint Laboratory for Cell Fate Regulation and Diseases, Guangzhou National Laboratory, Guangzhou Medical University, Guangzhou, China. miao_zhichao@gzlab.ac.cn.
⁶⁰ Shanghai Key Laboratory of Anesthesiology and Brain Functional Modulation, Clinical Research Center for Anesthesiology and Perioperative Medicine, Translational Research Institute of Brain and Brain-Like Intelligence, Shanghai Fourth People's Hospital, School of Medicine, Tongji University, Shanghai, China. miao_zhichao@gzlab.ac.cn.
⁶¹ European Bioinformatics Institute, European Molecular Biology Laboratory, Wellcome Genome Campus, Cambridge, UK. miao_zhichao@gzlab.ac.cn.

PMID: 39623050
DOI: 10.1038/s41592-024-02543-9

Abstract

RNA-Puzzles is a collective endeavor dedicated to the advancement and improvement of RNA three-dimensional structure prediction. With agreement from structural biologists, RNA structures are predicted by modeling groups before publication of the experimental structures. We report a large-scale set of predictions by 18 groups for 23 RNA-Puzzles: 4 RNA elements, 2 Aptamers, 4 Viral elements, 5 Ribozymes and 8 Riboswitches. We describe automatic assessment protocols for comparisons between prediction and experiment. Our analyses reveal some critical steps to be overcome to achieve good accuracy in modeling RNA structures: identification of helix-forming pairs and of non-Watson-Crick modules, correct coaxial stacking between helices and avoidance of entanglements. Three of the top four modeling groups in this round also ranked among the top four in the CASP15 contest.

Abstract

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