Structural basis of sequence-specific RNA recognition by the antiviral factor APOBEC3G

Yang, Hanjing; Kim, Kyumin; Li, Shuxing; Pacheco, Josue; Chen, Xiaojiang S.

doi:10.1038/s41467-022-35201-9

Structural basis of sequence-specific RNA recognition by the antiviral factor APOBEC3G

Journal Article · 01 December 2022 · Nat. Commun.

DOI:https://doi.org/10.1038/s41467-022-35201-9· OSTI ID:1902366

Yang, Hanjing; Kim, Kyumin; Li, Shuxing; Pacheco, Josue; Chen, Xiaojiang S.

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: DOE - Office Of Science; NCI; NIH

OSTI ID:: 1902366

Journal Information:: Nat. Commun., Journal Name: Nat. Commun. Vol. 13

Country of Publication:: United States

Language:: ENGLISH

References (64)

Retroviruses drive the rapid evolution of mammalian APOBEC3 genes Ito, Jumpei; Gifford, Robert J.; Sato, Kei Proceedings of the National Academy of Sciences, Vol. 117, Issue 1 https://doi.org/10.1073/pnas.1914183116	journal	December 2019
APOBEC3G restricts early HIV-1 replication in the cytoplasm of target cells Anderson, Jenny L.; Hope, Thomas J. Virology, Vol. 375, Issue 1 https://doi.org/10.1016/j.virol.2008.01.042	journal	May 2008
Antiviral Function of APOBEC3G Can Be Dissociated from Cytidine Deaminase Activity Newman, Edmund N. C.; Holmes, Rebecca K.; Craig, Heather M. Current Biology, Vol. 15, Issue 2 https://doi.org/10.1016/j.cub.2004.12.068	journal	January 2005
Structural Determinants of the APOBEC3G N-Terminal Domain for HIV-1 RNA Association Fukuda, Hirofumi; Li, Songling; Sardo, Luca Frontiers in Cellular and Infection Microbiology, Vol. 9 https://doi.org/10.3389/fcimb.2019.00129	journal	May 2019
Hypermutation of HIV-1 DNA in the Absence of the Vif Protein Lecossier, D. Science, Vol. 300, Issue 5622 https://doi.org/10.1126/science.1083338	journal	May 2003
Correcting pervasive errors in RNA crystallography through enumerative structure prediction Chou, Fang-Chieh; Sripakdeevong, Parin; Dibrov, Sergey M. Nature Methods, Vol. 10, Issue 1 https://doi.org/10.1038/nmeth.2262	journal	December 2012
Crystal Structure of a Soluble APOBEC3G Variant Suggests ssDNA to Bind in a Channel that Extends between the Two Domains Maiti, Atanu; Myint, Wazo; Delviks-Frankenberry, Krista A. Journal of Molecular Biology, Vol. 432, Issue 23 https://doi.org/10.1016/j.jmb.2020.10.020	journal	November 2020
The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA Zhang, Hui; Yang, Bin; Pomerantz, Roger J. Nature, Vol. 424, Issue 6944 https://doi.org/10.1038/nature01707	journal	May 2003
Association of Potent Human Antiviral Cytidine Deaminases with 7SL RNA and Viral RNP in HIV-1 Virions Zhang, Wenyan; Du, Juan; Yu, Kevin Journal of Virology, Vol. 84, Issue 24 https://doi.org/10.1128/JVI.01632-10	journal	October 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
A Guanosine-Centric Mechanism for RNA Chaperone Function Grohman, J. K.; Gorelick, R. J.; Lickwar, C. R. Science, Vol. 340, Issue 6129 https://doi.org/10.1126/science.1230715	journal	March 2013
APOBEC3G Restricts HIV-1 to a Greater Extent than APOBEC3F and APOBEC3DE in Human Primary CD4 ⁺ T Cells and Macrophages Chaipan, Chawaree; Smith, Jessica L.; Hu, Wei-Shau Journal of Virology, Vol. 87, Issue 1 https://doi.org/10.1128/JVI.00676-12	journal	January 2013
APOBEC3G cytosine deamination hotspots are defined by both sequence context and single-stranded DNA secondary structure Holtz, Colleen M.; Sadler, Holly A.; Mansky, Louis M. Nucleic Acids Research, Vol. 41, Issue 12 https://doi.org/10.1093/nar/gkt246	journal	April 2013
E-MSD: the European Bioinformatics Institute Macromolecular Structure Database Boutselakis, H. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg065	journal	January 2003
The Antiviral and Cancer Genomic DNA Deaminase APOBEC3H Is Regulated by an RNA-Mediated Dimerization Mechanism Shaban, Nadine M.; Shi, Ke; Lauer, Kate V. Molecular Cell, Vol. 69, Issue 1 https://doi.org/10.1016/j.molcel.2017.12.010	journal	January 2018
Structure of the HIV-1 Nucleocapsid Protein Bound to the SL3 -RNA Recognition Element De Guzman, R. N. Science, Vol. 279, Issue 5349 https://doi.org/10.1126/science.279.5349.384	journal	January 1998
RNA-binding residues in the N-terminus of APOBEC3G influence its DNA sequence specificity and retrovirus restriction efficiency Bélanger, Kasandra; Langlois, Marc-André Virology, Vol. 483 https://doi.org/10.1016/j.virol.2015.04.019	journal	September 2015
Extremely High Mutation Rate of HIV-1 In Vivo Cuevas, José M.; Geller, Ron; Garijo, Raquel PLOS Biology, Vol. 13, Issue 9 https://doi.org/10.1371/journal.pbio.1002251	journal	September 2015
Binding of RNA by APOBEC3G controls deamination-independent restriction of retroviruses Bélanger, Kasandra; Savoie, Mathieu; Rosales Gerpe, María Carla Nucleic Acids Research, Vol. 41, Issue 15 https://doi.org/10.1093/nar/gkt527	journal	June 2013
APOBEC3G Inhibits Elongation of HIV-1 Reverse Transcripts Bishop, Kate N.; Verma, Mohit; Kim, Eun-Young PLoS Pathogens, Vol. 4, Issue 12 https://doi.org/10.1371/journal.ppat.1000231	journal	December 2008
Understanding the structural basis of HIV-1 restriction by the full length double-domain APOBEC3G Yang, Hanjing; Ito, Fumiaki; Wolfe, Aaron D. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14377-y	journal	January 2020
Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein Sheehy, Ann M.; Gaddis, Nathan C.; Choi, Jonathan D. Nature, Vol. 418, Issue 6898 https://doi.org/10.1038/nature00939	journal	July 2002
NMR Studies of Retroviral Genome Packaging Boyd, Patricia S.; Brown, Janae B.; Brown, Joshua D. Viruses, Vol. 12, Issue 10 https://doi.org/10.3390/v12101115	journal	September 2020
Crystal structures of APOBEC3G N-domain alone and its complex with DNA Xiao, Xiao; Li, Shu-Xing; Yang, Hanjing Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12193	journal	August 2016
Characterization of APOBEC3G binding to 7SL RNA Bach, Daniel; Peddi, Shyam; Mangeat, Bastien Retrovirology, Vol. 5, Issue 1 https://doi.org/10.1186/1742-4690-5-54	journal	July 2008
Human and Rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H Demonstrate a Conserved Capacity To Restrict Vif-Deficient HIV-1 Hultquist, J. F.; Lengyel, J. A.; Refsland, E. W. Journal of Virology, Vol. 85, Issue 21 https://doi.org/10.1128/JVI.05238-11	journal	August 2011
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Architecture and secondary structure of an entire HIV-1 RNA genome Watts, Joseph M.; Dang, Kristen K.; Gorelick, Robert J. Nature, Vol. 460, Issue 7256 https://doi.org/10.1038/nature08237	journal	August 2009
Stem-loop structure preference for site-specific RNA editing by APOBEC3A and APOBEC3G Sharma, Shraddha; Baysal, Bora E. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.4136	journal	December 2017
Promiscuous RNA Binding Ensures Effective Encapsidation of APOBEC3 Proteins by HIV-1 Apolonia, Luis; Schulz, Reiner; Curk, Tomaž PLOS Pathogens, Vol. 11, Issue 1 https://doi.org/10.1371/journal.ppat.1004609	journal	January 2015
Insights into the Structures and Multimeric Status of APOBEC Proteins Involved in Viral Restriction and Other Cellular Functions Chen, Xiaojiang S. Viruses, Vol. 13, Issue 3 https://doi.org/10.3390/v13030497	journal	March 2021
Structure of the HIV-1 RNA packaging signal Keane, S. C.; Heng, X.; Lu, K. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.aaa9266	journal	May 2015
APOBEC3 proteins can copackage and comutate HIV-1 genomes Desimmie, Belete A.; Burdick, Ryan C.; Izumi, Taisuke Nucleic Acids Research, Vol. 44, Issue 16 https://doi.org/10.1093/nar/gkw653	journal	July 2016
The RNA Binding Specificity of Human APOBEC3 Proteins Resembles That of HIV-1 Nucleocapsid York, Ashley; Kutluay, Sebla B.; Errando, Manel PLOS Pathogens, Vol. 12, Issue 8 https://doi.org/10.1371/journal.ppat.1005833	journal	August 2016
Functions and consequences of AID/APOBEC-mediated DNA and RNA deamination Pecori, Riccardo; Di Giorgio, Salvatore; Paulo Lorenzo, J. Nature Reviews Genetics, Vol. 23, Issue 8 https://doi.org/10.1038/s41576-022-00459-8	journal	March 2022
Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome Yu, Qin; König, Renate; Pillai, Satish Nature Structural & Molecular Biology, Vol. 11, Issue 5 https://doi.org/10.1038/nsmb758	journal	April 2004
Suppression of HIV-1 Infection by APOBEC3 Proteins in Primary Human CD4 ⁺ T Cells Is Associated with Inhibition of Processive Reverse Transcription as Well as Excessive Cytidine Deamination Gillick, Kieran; Pollpeter, Darja; Phalora, Prabhjeet Journal of Virology, Vol. 87, Issue 3 https://doi.org/10.1128/JVI.02587-12	journal	November 2012
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
The A-nucleotide preference of HIV-1 in the context of its structured RNA genome van Hemert, Formijn J.; van der Kuyl, Antoinette C.; Berkhout, Ben RNA Biology, Vol. 10, Issue 2 https://doi.org/10.4161/rna.22896	journal	February 2013
Multiple, Switchable Protein:RNA Interactions Regulate Human Immunodeficiency Virus Type 1 Assembly Bieniasz, Paul; Telesnitsky, Alice Annual Review of Virology, Vol. 5, Issue 1 https://doi.org/10.1146/annurev-virology-092917-043448	journal	September 2018
Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts Mangeat, Bastien; Turelli, Priscilla; Caron, Gersende Nature, Vol. 424, Issue 6944 https://doi.org/10.1038/nature01709	journal	May 2003
Potential Intra- and Intermolecular Interactions Involving the Unique-5′ Region of the HIV-1 5′-UTR Spriggs, Shardell; Garyu, Lianko; Connor, Ryan Biochemistry, Vol. 47, Issue 49 https://doi.org/10.1021/bi8014373	journal	November 2008
The double-domain cytidine deaminase APOBEC3G is a cellular site-specific RNA editing enzyme Sharma, Shraddha; Patnaik, Santosh K.; Taggart, Robert T. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep39100	journal	December 2016
Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G Iwatani, Yasumasa; Chan, Denise S. B.; Wang, F. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm750	journal	October 2007
Macromolecular complexes in crystals and solutions Krissinel, Evgeny Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007232	journal	March 2011
Structure of the Vif-binding domain of the antiviral enzyme APOBEC3G Kouno, Takahide; Luengas, Elizabeth M.; Shigematsu, Megumi Nature Structural & Molecular Biology, Vol. 22, Issue 6 https://doi.org/10.1038/nsmb.3033	journal	May 2015
Functional Analysis and Structural Modeling of Human APOBEC3G Reveal the Role of Evolutionarily Conserved Elements in the Inhibition of Human Immunodeficiency Virus Type 1 Infection and Alu Transposition Bulliard, Yannick; Turelli, Priscilla; Röhrig, Ute F. Journal of Virology, Vol. 83, Issue 23 https://doi.org/10.1128/JVI.01491-09	journal	September 2009
Unpaired Guanosines in the 5′ Untranslated Region of HIV-1 RNA Act Synergistically To Mediate Genome Packaging Nikolaitchik, Olga A.; Somoulay, Xayathed; Rawson, Jonathan M. O. Journal of Virology, Vol. 94, Issue 21 https://doi.org/10.1128/JVI.00439-20	journal	October 2020
HIV restriction factor APOBEC3G binds in multiple steps and conformations to search and deaminate single-stranded DNA Morse, Michael; Naufer, M. Nabuan; Feng, Yuqing eLife, Vol. 8 https://doi.org/10.7554/eLife.52649	journal	December 2019
APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase Suspene, R. Nucleic Acids Research, Vol. 32, Issue 8 https://doi.org/10.1093/nar/gkh554	journal	April 2004
High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition Chiu, Y. -L.; Witkowska, H. E.; Hall, S. C. Proceedings of the National Academy of Sciences, Vol. 103, Issue 42 https://doi.org/10.1073/pnas.0604524103	journal	October 2006
PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Dolinsky, T. J.; Nielsen, J. E.; McCammon, J. A. Nucleic Acids Research, Vol. 32, Issue Web Server, p. W665-W667 https://doi.org/10.1093/nar/gkh381	journal	July 2004
Mitochondrial hypoxic stress induces widespread RNA editing by APOBEC3G in natural killer cells Sharma, Shraddha; Wang, Jianmin; Alqassim, Emad Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1651-1	journal	February 2019
Oligomerization transforms human APOBEC3G from an efficient enzyme to a slowly dissociating nucleic acid-binding protein Chaurasiya, Kathy R.; McCauley, Micah J.; Wang, Wei Nature Chemistry, Vol. 6, Issue 1 https://doi.org/10.1038/nchem.1795	journal	November 2013
Structural basis of chimpanzee APOBEC3H dimerization stabilized by double-stranded RNA Matsuoka, Tatsuya; Nagae, Takayuki; Ode, Hirotaka Nucleic Acids Research, Vol. 46, Issue 19 https://doi.org/10.1093/nar/gky676	journal	July 2018
PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations Dolinsky, T. J.; Czodrowski, P.; Li, H. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm276	journal	May 2007
RNA-Dependent Oligomerization of APOBEC3G Is Required for Restriction of HIV-1 Huthoff, Hendrik; Autore, Flavia; Gallois-Montbrun, Sarah PLoS Pathogens, Vol. 5, Issue 3 https://doi.org/10.1371/journal.ppat.1000330	journal	March 2009
NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the Ψ-RNA packaging signal. implications for genome recognition 1 1Edited by P. Wright Amarasinghe, Gaya K.; De Guzman, Roberto N.; Turner, Ryan B. Journal of Molecular Biology, Vol. 301, Issue 2 https://doi.org/10.1006/jmbi.2000.3979	journal	August 2000
The biased nucleotide composition of the HIV genome: a constant factor in a highly variable virus van der Kuyl, Antoinette C.; Berkhout, Ben Retrovirology, Vol. 9, Issue 1 https://doi.org/10.1186/1742-4690-9-92	journal	November 2012
APOBEC3H structure reveals an unusual mechanism of interaction with duplex RNA Bohn, Jennifer A.; Thummar, Keyur; York, Ashley Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01309-6	journal	October 2017
Retroviral restriction by APOBEC proteins Harris, Reuben S.; Liddament, Mark T. Nature Reviews Immunology, Vol. 4, Issue 11 https://doi.org/10.1038/nri1489	journal	November 2004
The Cellular Antiviral Protein APOBEC3G Interacts with HIV-1 Reverse Transcriptase and Inhibits Its Function during Viral Replication Wang, Xiaoxia; Ao, Zhujun; Chen, Liyu Journal of Virology, Vol. 86, Issue 7 https://doi.org/10.1128/JVI.06594-11	journal	April 2012
Deep sequencing of HIV-1 reverse transcripts reveals the multifaceted antiviral functions of APOBEC3G Pollpeter, Darja; Parsons, Maddy; Sobala, Andrew E. Nature Microbiology, Vol. 3, Issue 2 https://doi.org/10.1038/s41564-017-0063-9	journal	November 2017
Inhibition of \batchmode \documentclass[fleqn,10pt,legalpaper]{article} \usepackage{amssymb} \usepackage{amsfonts} \usepackage{amsmath} \pagestyle{empty} \begin{document} \(\mathrm{tRNA}_{3}^{\mathrm{Lys}}\) \end{document}-Primed Reverse Transcription by Human APOBEC3G during Human Immunodeficiency Virus Type 1 Replication Guo, Fei; Cen, Shan; Niu, Meijuan Journal of Virology, Vol. 80, Issue 23 https://doi.org/10.1128/JVI.01038-06	journal	December 2006

Similar Records

Structural basis for protein-RNA recognition in telomerase

Journal Article · 2014 · Nature Structural & Molecular Biology · OSTI ID:1497125

STRUCTURAL BASIS FOR 5 -END-SPECIFIC RECOGNITION OF GUIDE RNA BY THE A. FULGIDU PIWI PROTEIN

Journal Article · 2004 · REP. PROG. PHYS. · OSTI ID:884397

SPECIFICITY OF RNA-RNA HELIX RECOGNITION

Journal Article · 2001 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:15009233

Structural basis of sequence-specific RNA recognition by the antiviral factor APOBEC3G

Citation Formats

References (64)

Similar Records

Related Subjects