Structural and mechanistic basis of mammalian Nudt12 RNA deNADding

Grudzien-Nogalska, Ewa; Wu, Yixuan; Jiao, Xinfu; Cui, Huijuan; Mateyak, Maria K.; Hart, Ronald P.; Tong, Liang; Kiledjian, Megerditch

doi:10.1038/s41589-019-0293-7

Title: Structural and mechanistic basis of mammalian Nudt12 RNA deNADding

Journal Article · 17 May 2019 · Nature Chemical Biology

DOI: https://doi.org/10.1038/s41589-019-0293-7 · OSTI ID:1531008

Grudzien-Nogalska, Ewa ^[1]; Wu, Yixuan ^[2]; Jiao, Xinfu ^[1]; Cui, Huijuan ^[1]; Mateyak, Maria K. ^[1]; Hart, Ronald P. ^[1];

^[2];

^[1]

Rutgers Univ., Piscataway, NJ (United States)
Columbia Univ., New York, NY (United States)

We recently demonstrated that mammalian cells harbor nicotinamide adenine dinucleotide (NAD)-capped messenger RNAs that are hydrolyzed by the DXO deNADding enzyme. Here, we report that the Nudix protein Nudt12 is a second mammalian deNADding enzyme structurally and mechanistically distinct from DXO and targeting different RNAs. Here, the crystal structure of mouse Nudt12 in complex with the deNADding product AMP and three Mg²⁺ ions at 1.6 Å resolution provides insights into the molecular basis of the deNADding activity in the NAD pyrophosphate. Disruption of the Nudt12 gene stabilizes transfected NAD-capped RNA in cells, and its endogenous NAD-capped mRNA targets are enriched in those encoding proteins involved in cellular energetics. Furthermore, exposure of cells to nutrient or environmental stress manifests changes in NAD-capped RNA levels that are selectively responsive to Nudt12 or DXO, respectively, indicating an association of deNADding to cellular metabolism.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH); NIH-ORIP HEI

Grant/Contract Number:: AC02-06CH11357; GM118093; S10OD012018; GM126488; P41 GM103403; S10 RR029205

OSTI ID:: 1531008

Journal Information:: Nature Chemical Biology, Vol. 15, Issue 6; ISSN 1552-4450

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 34 works

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Identification of a quality-control mechanism for mRNA 5′-end capping Jiao, Xinfu; Xiang, Song; Oh, ChanSeok Nature, Vol. 467, Issue 7315 https://doi.org/10.1038/nature09338	journal	August 2010
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The mechanism of RNA 5′ capping with NAD+, NADH and desphospho-CoA Bird, Jeremy G.; Zhang, Yu; Tian, Yuan Nature, Vol. 535, Issue 7612 https://doi.org/10.1038/nature18622	journal	July 2016
Capture and sequencing of NAD-capped RNA sequences with NAD captureSeq Winz, Marie-Luise; Cahová, Hana; Nübel, Gabriele Nature Protocols, Vol. 12, Issue 1 https://doi.org/10.1038/nprot.2016.163	journal	December 2016
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IRF-3-dependent and augmented target genes during viral infection Andersen, J.; VanScoy, S.; Cheng, T-F Genes & Immunity, Vol. 9, Issue 2 https://doi.org/10.1038/sj.gene.6364449	journal	December 2007
Mammalian NADH diphosphatases of the Nudix family: cloning and characterization of the human peroxisomal NUDT12 protein Abdelraheim, Salama R.; Spiller, David G.; McLENNAN, Alexander G. Biochemical Journal, Vol. 374, Issue 2 https://doi.org/10.1042/bj20030441	journal	September 2003
Identification of NAD ⁺ capped mRNAs in Saccharomyces cerevisiae Walters, Robert W.; Matheny, Tyler; Mizoue, Laura S. Proceedings of the National Academy of Sciences, Vol. 114, Issue 3 https://doi.org/10.1073/pnas.1619369114	journal	December 2016
Mutational analysis of a Dcp2-binding element reveals general enhancement of decapping by 5′-end stem-loop structures Li, You; Ho, Eric S.; Gunderson, Samuel I. Nucleic Acids Research, Vol. 37, Issue 7 https://doi.org/10.1093/nar/gkp087	journal	February 2009
Superior 5' homogeneity of RNA from ATP-initiated transcription under the T7 2.5 promoter Coleman, T. M. Nucleic Acids Research, Vol. 32, Issue 1 https://doi.org/10.1093/nar/gnh007	journal	January 2004
Tissue-specific regulation of SIRT1 by calorie restriction Chen, D.; Bruno, J.; Easlon, E. Genes & Development, Vol. 22, Issue 13 https://doi.org/10.1101/gad.1650608	journal	July 2008
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Multiple Nudix family proteins possess mRNA decapping activity Song, M. -G.; Bail, S.; Kiledjian, M. RNA, Vol. 19, Issue 3 https://doi.org/10.1261/rna.037309.112	journal	January 2013
Functional characterization of the mammalian mRNA decapping enzyme hDcp2 Piccirillo, C. RNA, Vol. 9, Issue 9 https://doi.org/10.1261/rna.5690503	journal	September 2003
Edc3 Function in Yeast and Mammals Is Modulated by Interaction with NAD-Related Compounds Walters, Robert W.; Shumilin, Igor A.; Yoon, Je-Hyun G3: Genes\|Genomes\|Genetics, Vol. 4, Issue 4 https://doi.org/10.1534/g3.114.010470	journal	February 2014
Bioconductor : open software development for computational biology and bioinformatics C., Gentleman, Robert; J., Carey, Vincent; M., Bates, Douglas BioMed Central https://doi.org/10.21256/zhaw-1907	text	January 2004
Open Source Software for the Analysis of Microarray Data Dudoit, Sandrine; Gentleman, Robert C.; Quackenbush, John BioTechniques, Vol. 34, Issue 3S https://doi.org/10.2144/mar03dudoit	journal	March 2003

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