MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma
Abstract
The oncogenic transcription factor MYC and its binding partner MAX regulate gene expression by binding to DNA at enhancer-box (E-box) elements 5'-CACGTG-3'. In mammalian genomes, the central E-box CpG has the potential to be methylated at the 5-position of cytosine (5mC), or to undergo further oxidation to the 5-hydroxymethyl (5hmC), 5-formyl (5fC), or 5-carboxyl (5caC) forms. We find that MAX exhibits the greatest affinity for a 5caC or unmodified C-containing E-box, and much reduced affinities for the corresponding 5mC, 5hmC or 5fC forms. Crystallization of MAX with a 5caC modified E-box oligonucleotide revealed that MAX Arg36 recognizes 5caC using a 5caC–Arg–Guanine triad, with the next nearest residue to the carboxylate group being Arg60. In an analysis of >800 primary multiple myelomas, MAX alterations occurred at a frequency of ~3%, more than half of which were single nucleotide substitutions affecting a basic clamp-like interface important for DNA interaction. Among these, arginines 35, 36 and 60 were the most frequently altered. In vitro binding studies showed that whereas mutation of Arg36 (R36W) or Arg35 (R35H/L) completely abolished DNA binding, mutation of Arg60 (R60Q) significantly reduced DNA binding, but retained a preference for the 5caC modified E-box. Interestingly, MAX alterations define a subsetmore »
- Authors:
-
- Emory Univ. School of Medicine, Atlanta, GA (United States)
- Emory Univ. School of Medicine, Atlanta, GA (United States); Univ. of Texas MD Anderson Cancer Center, Houston, TX (United States)
- Emory Univ. School of Medicine, Atlanta, GA (United States); The Winship Cancer Inst. of Emory Univ., Atlanta, GA (United States)
- Emory Univ. School of Medicine, Atlanta, GA (United States); The Winship Cancer Inst. of Emory University, Atlanta, GA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH)
- OSTI Identifier:
- 1356410
- Grant/Contract Number:
- GM049245-23; CA077337-15
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 45; Journal Issue: 5; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Wang, Dongxue, Hashimoto, Hideharu, Zhang, Xing, Barwick, Benjamin G., Lonial, Sagar, Boise, Lawrence H., Vertino, Paula M., and Cheng, Xiaodong. MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma. United States: N. p., 2016.
Web. doi:10.1093/nar/gkw1184.
Wang, Dongxue, Hashimoto, Hideharu, Zhang, Xing, Barwick, Benjamin G., Lonial, Sagar, Boise, Lawrence H., Vertino, Paula M., & Cheng, Xiaodong. MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma. United States. https://doi.org/10.1093/nar/gkw1184
Wang, Dongxue, Hashimoto, Hideharu, Zhang, Xing, Barwick, Benjamin G., Lonial, Sagar, Boise, Lawrence H., Vertino, Paula M., and Cheng, Xiaodong. Mon .
"MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma". United States. https://doi.org/10.1093/nar/gkw1184. https://www.osti.gov/servlets/purl/1356410.
@article{osti_1356410,
title = {MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma},
author = {Wang, Dongxue and Hashimoto, Hideharu and Zhang, Xing and Barwick, Benjamin G. and Lonial, Sagar and Boise, Lawrence H. and Vertino, Paula M. and Cheng, Xiaodong},
abstractNote = {The oncogenic transcription factor MYC and its binding partner MAX regulate gene expression by binding to DNA at enhancer-box (E-box) elements 5'-CACGTG-3'. In mammalian genomes, the central E-box CpG has the potential to be methylated at the 5-position of cytosine (5mC), or to undergo further oxidation to the 5-hydroxymethyl (5hmC), 5-formyl (5fC), or 5-carboxyl (5caC) forms. We find that MAX exhibits the greatest affinity for a 5caC or unmodified C-containing E-box, and much reduced affinities for the corresponding 5mC, 5hmC or 5fC forms. Crystallization of MAX with a 5caC modified E-box oligonucleotide revealed that MAX Arg36 recognizes 5caC using a 5caC–Arg–Guanine triad, with the next nearest residue to the carboxylate group being Arg60. In an analysis of >800 primary multiple myelomas, MAX alterations occurred at a frequency of ~3%, more than half of which were single nucleotide substitutions affecting a basic clamp-like interface important for DNA interaction. Among these, arginines 35, 36 and 60 were the most frequently altered. In vitro binding studies showed that whereas mutation of Arg36 (R36W) or Arg35 (R35H/L) completely abolished DNA binding, mutation of Arg60 (R60Q) significantly reduced DNA binding, but retained a preference for the 5caC modified E-box. Interestingly, MAX alterations define a subset of myeloma patients with lower MYC expression and a better overall prognosis. Together these data indicate that MAX can act as a direct epigenetic sensor of E-box cytosine modification states and that local CpG modification and MAX variants converge to modulate the MAX-MYC transcriptional network.},
doi = {10.1093/nar/gkw1184},
journal = {Nucleic Acids Research},
number = 5,
volume = 45,
place = {United States},
year = {Mon Nov 28 00:00:00 EST 2016},
month = {Mon Nov 28 00:00:00 EST 2016}
}
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Characteristic profiles of DNA epigenetic modifications in colon cancer and its predisposing conditions—benign adenomas and inflammatory bowel disease
journal, May 2018
- Dziaman, Tomasz; Gackowski, Daniel; Guz, Jolanta
- Clinical Epigenetics, Vol. 10, Issue 1