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      Perspective: APOBEC mutagenesis in drug resistance and immune escape in HIV and cancer evolution

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          Abstract

          The apolipoprotein B mRNA-editing enzyme, catalytic polypeptide-like (APOBEC) mutational signature has only recently been detected in a multitude of cancers through next-generation sequencing. In contrast, APOBEC has been a focus of virology research for over a decade. Many lessons learnt regarding APOBEC within virology are likely to be applicable to cancer. In this review, we explore the parallels between the role of APOBEC enzymes in HIV and cancer evolution. We discuss data supporting the role of APOBEC mutagenesis in creating HIV genome heterogeneity, drug resistance, and immune escape variants. We hypothesize similar functions of APOBEC will also hold true in cancer.

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          Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme.

          M Muramatsu, K Kinoshita, S Fagarasan … (2000)
          Induced overexpression of AID in CH12F3-2 B lymphoma cells augmented class switching from IgM to IgA without cytokine stimulation. AID deficiency caused a complete defect in class switching and showed a hyper-IgM phenotype with enlarged germinal centers containing strongly activated B cells before or after immunization. AID-/- spleen cells stimulated in vitro with LPS and cytokines failed to undergo class switch recombination although they expressed germline transcripts. Immunization of AID-/- chimera with 4-hydroxy-3-nitrophenylacetyl (NP) chicken gamma-globulin induced neither accumulation of mutations in the NP-specific variable region gene nor class switching. These results suggest that AID may be involved in regulation or catalysis of the DNA modification step of both class switching and somatic hypermutation.
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            The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA.

            Hui Zhang, Bin Yang, Roger Pomerantz … (2003)
            High mutation frequency during reverse transcription has a principal role in the genetic variation of primate lentiviral populations. It is the main driving force for the generation of drug resistance and the escape from immune surveillance. G to A hypermutation is one of the characteristics of primate lentiviruses, as well as other retroviruses, during replication in vivo and in cell culture. The molecular mechanisms of this process, however, remain to be clarified. Here, we demonstrate that CEM15 (also known as apolipoprotein B mRNA editing enzyme, catalytic polypeptide-like 3G; APOBEC3G), an endogenous inhibitor of human immunodeficiency virus type 1 (HIV-1) replication, is a cytidine deaminase and is able to induce G to A hypermutation in newly synthesized viral DNA. This effect can be counteracted by the HIV-1 virion infectivity factor (Vif). It seems that this viral DNA mutator is a viral defence mechanism in host cells that may induce either lethal hypermutation or instability of the incoming nascent viral reverse transcripts, which could account for the Vif-defective phenotype. Importantly, the accumulation of CEM15-mediated non-lethal hypermutation in the replicating viral genome could potently contribute to the genetic variation of primate lentiviral populations.
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              Comprehensive Transcriptional Analysis of Early-Stage Urothelial Carcinoma

              Jakob Hedegaard, Philippe Lamy, Iver Nordentoft … (2016)
              Non-muscle-invasive bladder cancer (NMIBC) is a heterogeneous disease with widely different outcomes. We performed a comprehensive transcriptional analysis of 460 early-stage urothelial carcinomas and showed that NMIBC can be subgrouped into three major classes with basal- and luminal-like characteristics and different clinical outcomes. Large differences in biological processes such as the cell cycle, epithelial-mesenchymal transition, and differentiation were observed. Analysis of transcript variants revealed frequent mutations in genes encoding proteins involved in chromatin organization and cytoskeletal functions. Furthermore, mutations in well-known cancer driver genes (e.g., TP53 and ERBB2) were primarily found in high-risk tumors, together with APOBEC-related mutational signatures. The identification of subclasses in NMIBC may offer better prognostication and treatment selection based on subclass assignment.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Ann Oncol
                Journal ID (iso-abbrev): Ann. Oncol
                Journal ID (publisher-id): annonc
                Title: Annals of Oncology
                Publisher: Oxford University Press
                ISSN (Print): 0923-7534
                ISSN (Electronic): 1569-8041
                Publication date (Print): March 2018
                Publication date (Electronic): 08 January 2018
                Publication date PMC-release: 08 January 2018
                Volume: 29
                Issue: 3
                Pages: 563-572
                Affiliations
                [1 ]CRUK Lung Cancer Centre of Excellence, UCL Cancer Institute, London, UK
                [2 ]Translational Cancer Therapeutics Laboratory, The Francis Crick Institute, London, UK
                [3 ]Danish Cancer Society Research Center, Copenhagen, Denmark, UK
                [4 ]Science for Life Laboratory, Stockholm, Sweden
                [5 ]Division of Genome Biology, Department of Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
                [6 ]Cancer Immunology Unit, UCL Cancer Institute, London, UK
                [7 ]International AIDS Vaccine Initiative (IAVI), New York, USA
                [8 ]Masonic Cancer Center, Minneapolis, USA
                [9 ]Institute for Molecular Virology, Minneapolis, USA
                [10 ]Center for Genome Engineering, Minneapolis, USA
                [11 ]Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, USA
                [12 ]Howard Hughes Medical Institute, University of Minnesota, Minneapolis, USA
                Author notes
                Correspondence to: Prof. Reuben S. Harris, Howard Hughes Medical Institute, University of Minnesota, Minneapolis, MN 55455, USA. Tel: +1-612-624-0457; Fax: +1-612-625-2163; E-mail: rsh@ 123456umn.edu

                Prof. Charles Swanton, Translational Cancer Therapeutics Laboratory, The Francis Crick Institute, 1 Midland Road, London NW1 1AT, UK. Tel: +44-0-2072693463; Fax: +44-0-2072693463; E-mail: charles.swanton@ 123456crick.ac.uk

                S. Venkatesan and R. Rosenthal contributed equally as first authors.

                R. S. Harris and C. Swanton contributed equally as senior authors.

                Article
                Publisher ID: mdy003
                DOI: 10.1093/annonc/mdy003
                PMC ID: 5888943
                PubMed ID: 29324969
                SO-VID: 7f397ad8-a955-4044-80a4-127dd9922c35
                Copyright © © The Author(s) 2018. Published by Oxford University Press on behalf of the European Society for Medical Oncology.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Pages: 10
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: NIAID R37 AI064046 and NCI R21 CA206309
                Funded by: Cancer Research UK 10.13039/501100000289
                Award ID: FC001169
                Funded by: Wellcome Trust 10.13039/100004440
                Award ID: FC001169
                Categories
                Subject: Reviews
                Subject: Editor's Choice

                ScienceOpen disciplines: Oncology & Radiotherapy
                Keywords: apobec,immune escape,drug resistance,human immunodeficiency virus,intratumour heterogeneity
                Data availability:
                ScienceOpen disciplines: Oncology & Radiotherapy
                Keywords: apobec, immune escape, drug resistance, human immunodeficiency virus, intratumour heterogeneity

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