The Antiviral and Cancer Genomic DNA Deaminase APOBEC3H Is Regulated by an RNA-Mediated Dimerization Mechanism

Shaban, Nadine M.; Shi, Ke; Lauer, Kate V.; Carpenter, Michael A.; Richards, Christopher M.; Salamango, Daniel; Wang, Jiayi; Lopresti, Michael W.; Banerjee, Surajit; Levin-Klein, Rena; Brown, William L.; Aihara, Hideki; Harris, Reuben S.

doi:10.1016/j.molcel.2017.12.010

Title: The Antiviral and Cancer Genomic DNA Deaminase APOBEC3H Is Regulated by an RNA-Mediated Dimerization Mechanism

Journal Article · Thu Dec 28 00:00:00 EST 2017 · Molecular Cell

DOI:https://doi.org/10.1016/j.molcel.2017.12.010· OSTI ID:1432879

Shaban, Nadine M. ^[1]; Shi, Ke ^[1]; Lauer, Kate V. ^[1]; Carpenter, Michael A. ^[1]; Richards, Christopher M. ^[1]; Salamango, Daniel ^[1]; Wang, Jiayi ^[1]; Lopresti, Michael W. ^[1]; Banerjee, Surajit ^[2]; Levin-Klein, Rena ^[1]; Brown, William L. ^[1]; Aihara, Hideki ^[1]; Harris, Reuben S. ^[1]

Univ. of Minnesota, Minneapolis, MN (United States)
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS), Northeastern Collaborative Access Team (NE-CAT); Cornell Univ., Ithaca, NY (United States)

Human APOBEC3H and homologous single-stranded DNA cytosine deaminases are unique to mammals. These DNA-editing enzymes function in innate immunity by restricting the replication of viruses and transposons. APOBEC3H also contributes to cancer mutagenesis. Here, in this paper, we address the fundamental nature of RNA in regulating human APOBEC3H activities. APOBEC3H co-purifies with RNA as an inactive protein, and RNase A treatment enables strong DNA deaminase activity. RNA-binding-defective mutants demonstrate clear separation of function by becoming DNA hypermutators. Biochemical and crystallographic data demonstrate a mechanism in which double-stranded RNA mediates enzyme dimerization. Additionally, APOBEC3H separation-of-function mutants show that RNA binding is required for cytoplasmic localization, packaging into HIV-1 particles, and antiviral activity. Overall, these results support a model in which structured RNA negatively regulates the potentially harmful DNA deamination activity of APOBEC3H while, at the same time, positively regulating its antiviral activity.

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

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); Prospect Creek Foundation; University of Minnesota

Grant/Contract Number:: AC02-06CH11357; NIGMS R01-GM118000; NIGMS R35-GM118047; NCI R21-CA206309; T32-HL007062; T32-AI83196; T90-DE022732; NIGMS P41-GM103403; S10 RR029205

OSTI ID:: 1432879

Journal Information:: Molecular Cell, Vol. 69, Issue 1; ISSN 1097-2765

Publisher:: Cell Press - ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 45 works

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Genetic and mechanistic basis for APOBEC3H alternative splicing, retrovirus restriction, and counteraction by HIV-1 protease Ebrahimi, Diako; Richards, Christopher M.; Carpenter, Michael A. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06594-3	journal	October 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
APOBEC restriction goes nuclear Malim, Michael H.; Pollpeter, Darja Nature Microbiology, Vol. 4, Issue 1 https://doi.org/10.1038/s41564-018-0323-3	journal	December 2018
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

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59 BASIC BIOLOGICAL SCIENCES
APOBEC3
HDNA cytosine deaminase
HIV-1
retrovirus restriction factor
ribonucleoprotein complex
RNA duplex
structural virology

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