Structural determinants of APOBEC3B non-catalytic domain for molecular assembly and catalytic regulation

Xiao, Xiao; Yang, Hanjing; Arutiunian, Vagan; Fang, Yao; Besse, Guillaume; Morimoto, Cherie; Zirkle, Brett; Chen, Xiaojiang S.

doi:10.1093/nar/gkx362

Structural determinants of APOBEC3B non-catalytic domain for molecular assembly and catalytic regulation

Journal Article · Tue May 30 00:00:00 EDT 2017 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkx362· OSTI ID:1372228

Xiao, Xiao ^[1]; Yang, Hanjing ^[1]; Arutiunian, Vagan ^[1]; Fang, Yao ^[2]; Besse, Guillaume ^[3]; Morimoto, Cherie ^[1]; Zirkle, Brett ^[1]; Chen, Xiaojiang S. ^[1]

Univ. of Southern California, Los Angeles, CA (United States)
Univ. of Southern California, Los Angeles, CA (United States); Third Military Medical University (China); 161 Hospital, Wuhan (China)
Univ. of Southern California, Los Angeles, CA (United States); Universite Blaise Pascal, Clermont-Ferrand (France)

The catalytic activity of human cytidine deaminase APOBEC3B (A3B) has been correlated with kataegic mutational patterns within multiple cancer types. The molecular basis of how the N-terminal non-catalytic CD1 regulates the catalytic activity and consequently, biological function of A3B remains relatively unknown. Here, we report the crystal structure of a soluble human A3B-CD1 variant and delineate several structural elements of CD1 involved in molecular assembly, nucleic acid interactions and catalytic regulation of A3B. We show that (i) A3B expressed in human cells exists in hypoactive high-molecular-weight (HMW) complexes, which can be activated without apparent dissociation into low-molecular-weight (LMW) species after RNase A treatment. (ii) Multiple surface hydrophobic residues of CD1 mediate the HMW complex assembly and affect the catalytic activity, including one tryptophan residue W127 that likely acts through regulating nucleic acid binding. (iii) One of the highly positively charged surfaces on CD1 is involved in RNA-dependent attenuation of A3B catalysis. (iv) Surface hydrophobic residues of CD1 are involved in heterogeneous nuclear ribonucleoproteins (hnRNPs) binding to A3B. The structural and biochemical insights described here suggest that unique structural features on CD1 regulate the molecular assembly and catalytic activity of A3B through distinct mechanisms.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH)

OSTI ID:: 1372228

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 12 Vol. 45; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Increased APOBEC3B Predicts Worse Outcomes in Lung Cancer: A Comprehensive Retrospective Study Yan, Shumei; He, Fan; Gao, Bei Journal of Cancer, Vol. 7, Issue 6 https://doi.org/10.7150/jca.14030	journal	January 2016

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Evaluation of APOBEC3B Recognition Motifs by NMR Reveals Preferred Substrates Liu, Manjuan; Mallinger, Aurélie; Tortorici, Marcello ACS Chemical Biology, Vol. 13, Issue 9 https://doi.org/10.1021/acschembio.8b00639	journal	August 2018
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
Understanding the Structure, Multimerization, Subcellular Localization and mC Selectivity of a Genomic Mutator and Anti-HIV Factor APOBEC3H Ito, Fumiaki; Yang, Hanjing; Xiao, Xiao Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21955-0	journal	February 2018
Enzyme cycling contributes to efficient induction of genome mutagenesis by the cytidine deaminase APOBEC3B Adolph, Madison B.; Love, Robin P.; Feng, Yuqing Nucleic Acids Research, Vol. 46, Issue 22 https://doi.org/10.1093/nar/gky1115	journal	November 2018
APOBEC3B reporter myeloma cell lines identify DNA damage response pathways leading to APOBEC3B expression Yamazaki, Hiroyuki; Shirakawa, Kotaro; Matsumoto, Tadahiko https://doi.org/10.1101/781112	posted_content	September 2019
Human APOBEC3B interacts with the heterogenous nuclear ribonucleoprotein A3 in cancer cells Mishra, Nawneet; Reddy, K. Sony; Timilsina, Uddhav Journal of Cellular Biochemistry, Vol. 119, Issue 8 https://doi.org/10.1002/jcb.26855	journal	April 2018
Conformational Switch Regulates the DNA Cytosine Deaminase Activity of Human APOBEC3B Shi, Ke; Demir, Özlem; Carpenter, Michael A. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-17694-3	journal	December 2017
A panel of eGFP reporters for single base editing by APOBEC-Cas9 editosome complexes Martin, A. St.; Salamango, D. J.; Serebrenik, A. A. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-36739-9	journal	January 2019
The DNA deaminase APOBEC3B interacts with the cell-cycle protein CDK4 and disrupts CDK4-mediated nuclear import of Cyclin D1 McCann, Jennifer L.; Klein, Madeline M.; Leland, Evelyn M. Journal of Biological Chemistry, Vol. 294, Issue 32 https://doi.org/10.1074/jbc.ra119.008443	journal	August 2019
APOBEC3A is a prominent cytidine deaminase in breast cancer Cortez, Luis M.; Brown, Amber L.; Dennis, Madeline A. PLOS Genetics, Vol. 15, Issue 12 https://doi.org/10.1371/journal.pgen.1008545	journal	December 2019
APOBEC3B reporter myeloma cell lines identify DNA damage response pathways leading to APOBEC3B expression Yamazaki, Hiroyuki; Shirakawa, Kotaro; Matsumoto, Tadahiko PLOS ONE, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pone.0223463	journal	January 2020

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