MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma

Wang, Dongxue; Hashimoto, Hideharu; Zhang, Xing; Barwick, Benjamin G.; Lonial, Sagar; Boise, Lawrence H.; Vertino, Paula M.; Cheng, Xiaodong

doi:10.1093/nar/gkw1184

Title: MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma

Journal Article · Mon Nov 28 00:00:00 EST 2016 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkw1184· OSTI ID:1356410

Wang, Dongxue ^[1]; Hashimoto, Hideharu ^[1]; Zhang, Xing ^[2]; Barwick, Benjamin G. ^[1]; Lonial, Sagar ^[3]; Boise, Lawrence H. ^[3]; Vertino, Paula M. ^[4]; Cheng, Xiaodong ^[2]

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)

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH)

Grant/Contract Number:: GM049245-23; CA077337-15

OSTI ID:: 1356410

Journal Information:: Nucleic Acids Research, Vol. 45, Issue 5; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 44 works

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