Mackenzie K Wyllie, Clare K Morris, Nicholas H Moeller, Henry A M Schares, Ramkumar Moorthy, Christopher A Belica, Michael J Grillo, Özlem Demir, Alex M Ayoub, Michael A Carpenter, Hideki Aihara, Reuben S Harris, Rommie E Amaro, Daniel A Harki
{"title":"糖构象对 APOBEC3A 和 APOBEC3B 酶单链 DNA 选择性的影响","authors":"Mackenzie K Wyllie, Clare K Morris, Nicholas H Moeller, Henry A M Schares, Ramkumar Moorthy, Christopher A Belica, Michael J Grillo, Özlem Demir, Alex M Ayoub, Michael A Carpenter, Hideki Aihara, Reuben S Harris, Rommie E Amaro, Daniel A Harki","doi":"10.1021/acschembio.4c00540","DOIUrl":null,"url":null,"abstract":"<p><p>The APOBEC3 family of polynucleotide cytidine deaminases has diverse roles as viral restriction factors and oncogenic mutators. These enzymes convert cytidine to uridine in single-stranded (ss)DNA, inducing genomic mutations that promote drug resistance and tumor heterogeneity. Of the seven human APOBEC3 members, APOBEC3A (A3A) and APOBEC3B (A3B) are most implicated in driving pro-tumorigenic mutations. How these enzymes engage and selectively deaminate ssDNA over RNA is not well understood. We previously conducted molecular dynamics (MD) simulations that support the role of sugar conformation as a key molecular determinant in nucleic acid recognition by A3B. We hypothesize that A3A and A3B selectively deaminate substrates in the 2'-<i>endo</i> (DNA) conformation and show reduced activity for 3'-<i>endo</i> (RNA) conformation substrates. Consequently, we have characterized A3A- and A3B-binding and deaminase activity with chimeric oligonucleotides containing cytidine analogues that promote either the 2'-<i>endo</i> or 3'-<i>endo</i> conformation. Using fluorescence polarization and gel-based deamination assays, we determined that sugar conformation preferentially impacts the ability of these enzymes to deaminate substrates and less so binding to substrates. Using MD simulations, we identify specific active site interactions that promote selectivity based on the 2'-<i>endo</i> conformation. These findings help inform the biological functions of A3A and A3B in providing antiviral innate immunity and pathogenic functions in cancer.</p>","PeriodicalId":11,"journal":{"name":"ACS Chemical Biology","volume":" ","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2024-12-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"The Impact of Sugar Conformation on the Single-Stranded DNA Selectivity of APOBEC3A and APOBEC3B Enzymes.\",\"authors\":\"Mackenzie K Wyllie, Clare K Morris, Nicholas H Moeller, Henry A M Schares, Ramkumar Moorthy, Christopher A Belica, Michael J Grillo, Özlem Demir, Alex M Ayoub, Michael A Carpenter, Hideki Aihara, Reuben S Harris, Rommie E Amaro, Daniel A Harki\",\"doi\":\"10.1021/acschembio.4c00540\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The APOBEC3 family of polynucleotide cytidine deaminases has diverse roles as viral restriction factors and oncogenic mutators. These enzymes convert cytidine to uridine in single-stranded (ss)DNA, inducing genomic mutations that promote drug resistance and tumor heterogeneity. Of the seven human APOBEC3 members, APOBEC3A (A3A) and APOBEC3B (A3B) are most implicated in driving pro-tumorigenic mutations. How these enzymes engage and selectively deaminate ssDNA over RNA is not well understood. We previously conducted molecular dynamics (MD) simulations that support the role of sugar conformation as a key molecular determinant in nucleic acid recognition by A3B. We hypothesize that A3A and A3B selectively deaminate substrates in the 2'-<i>endo</i> (DNA) conformation and show reduced activity for 3'-<i>endo</i> (RNA) conformation substrates. Consequently, we have characterized A3A- and A3B-binding and deaminase activity with chimeric oligonucleotides containing cytidine analogues that promote either the 2'-<i>endo</i> or 3'-<i>endo</i> conformation. Using fluorescence polarization and gel-based deamination assays, we determined that sugar conformation preferentially impacts the ability of these enzymes to deaminate substrates and less so binding to substrates. Using MD simulations, we identify specific active site interactions that promote selectivity based on the 2'-<i>endo</i> conformation. These findings help inform the biological functions of A3A and A3B in providing antiviral innate immunity and pathogenic functions in cancer.</p>\",\"PeriodicalId\":11,\"journal\":{\"name\":\"ACS Chemical Biology\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2024-12-16\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"ACS Chemical Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1021/acschembio.4c00540\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"ACS Chemical Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1021/acschembio.4c00540","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
The Impact of Sugar Conformation on the Single-Stranded DNA Selectivity of APOBEC3A and APOBEC3B Enzymes.
The APOBEC3 family of polynucleotide cytidine deaminases has diverse roles as viral restriction factors and oncogenic mutators. These enzymes convert cytidine to uridine in single-stranded (ss)DNA, inducing genomic mutations that promote drug resistance and tumor heterogeneity. Of the seven human APOBEC3 members, APOBEC3A (A3A) and APOBEC3B (A3B) are most implicated in driving pro-tumorigenic mutations. How these enzymes engage and selectively deaminate ssDNA over RNA is not well understood. We previously conducted molecular dynamics (MD) simulations that support the role of sugar conformation as a key molecular determinant in nucleic acid recognition by A3B. We hypothesize that A3A and A3B selectively deaminate substrates in the 2'-endo (DNA) conformation and show reduced activity for 3'-endo (RNA) conformation substrates. Consequently, we have characterized A3A- and A3B-binding and deaminase activity with chimeric oligonucleotides containing cytidine analogues that promote either the 2'-endo or 3'-endo conformation. Using fluorescence polarization and gel-based deamination assays, we determined that sugar conformation preferentially impacts the ability of these enzymes to deaminate substrates and less so binding to substrates. Using MD simulations, we identify specific active site interactions that promote selectivity based on the 2'-endo conformation. These findings help inform the biological functions of A3A and A3B in providing antiviral innate immunity and pathogenic functions in cancer.
期刊介绍:
ACS Chemical Biology provides an international forum for the rapid communication of research that broadly embraces the interface between chemistry and biology.
The journal also serves as a forum to facilitate the communication between biologists and chemists that will translate into new research opportunities and discoveries. Results will be published in which molecular reasoning has been used to probe questions through in vitro investigations, cell biological methods, or organismic studies.
We welcome mechanistic studies on proteins, nucleic acids, sugars, lipids, and nonbiological polymers. The journal serves a large scientific community, exploring cellular function from both chemical and biological perspectives. It is understood that submitted work is based upon original results and has not been published previously.