Evolution of a histone variant involved in compartmental regulation of NAD metabolism.
Journal
Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
07
04
2021
accepted:
28
10
2021
entrez:
10
12
2021
pubmed:
11
12
2021
medline:
7
1
2022
Statut:
ppublish
Résumé
NAD metabolism is essential for all forms of life. Compartmental regulation of NAD
Identifiants
pubmed: 34887560
doi: 10.1038/s41594-021-00692-5
pii: 10.1038/s41594-021-00692-5
doi:
Substances chimiques
Chromatin
0
Histones
0
MACROH2A1 protein, human
0
NAD
0U46U6E8UK
PARP1 protein, human
EC 2.4.2.30
Poly (ADP-Ribose) Polymerase-1
EC 2.4.2.30
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1009-1019Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Covarrubias, A. J., Perrone, R., Grozio, A. & Verdin, E. NAD
pubmed: 33353981
doi: 10.1038/s41580-020-00313-x
Rajman, L., Chwalek, K. & Sinclair, D. A. Therapeutic potential of NAD-boosting molecules: the in vivo evidence. Cell Metab. 27, 529–547 (2018).
pubmed: 29514064
pmcid: 6342515
doi: 10.1016/j.cmet.2018.02.011
Xiao, W., Wang, R. S., Handy, D. E. & Loscalzo, J. NAD(H) and NADP(H) redox couples and cellular energy metabolism. Antioxid. Redox Signal 28, 251–272 (2018).
pubmed: 28648096
pmcid: 5737637
doi: 10.1089/ars.2017.7216
Palazzo, L., Mikolčević, P., Mikoč, A. & Ahel, I. ADP-ribosylation signalling and human disease. Open Biol. https://doi.org/10.1098/rsob.190041 (2019).
Cambronne, X. A. & Kraus, W. L. Location, location, location: compartmentalization of NAD
pubmed: 32595066
pmcid: 7502477
doi: 10.1016/j.tibs.2020.05.010
Strømland, Ø. et al. Keeping the balance in NAD metabolism. Biochem. Soc. Trans. 47, 119–130 (2019).
pubmed: 30626706
doi: 10.1042/BST20180417
Cantó, C., Menzies, K. J. & Auwerx, J. NAD
pubmed: 26118927
pmcid: 4487780
doi: 10.1016/j.cmet.2015.05.023
Altmeyer, M. & Hottiger, M. O. Poly(ADP-ribose) polymerase 1 at the crossroad of metabolic stress and inflammation in aging. Aging 1, 458–469 (2009).
pubmed: 20157531
pmcid: 2806023
doi: 10.18632/aging.100052
Bai, P. et al. PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metab. 13, 461–468 (2011).
pubmed: 21459330
pmcid: 3086520
doi: 10.1016/j.cmet.2011.03.004
Pirinen, E. et al. Pharmacological inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab. 19, 1034–1041 (2014).
pubmed: 24814482
pmcid: 4047186
doi: 10.1016/j.cmet.2014.04.002
Posavec-Marjanović, M. et al. MacroH2A1.1 regulates mitochondrial respiration by limiting nuclear NAD
pubmed: 28991266
pmcid: 5791885
doi: 10.1038/nsmb.3481
Luo, X. et al. PARP-1 controls the adipogenic transcriptional program by PARylating C/EBPβ and modulating its transcriptional activity. Mol. Cell 65, 260–271 (2017).
pubmed: 28107648
pmcid: 5258183
doi: 10.1016/j.molcel.2016.11.015
Ryu, K. W. et al. Metabolic regulation of transcription through compartmentalized NAD
Hurtado-Bagès, S. et al. The histone variant macroH2A1 regulates key genes for myogenic cell fusion in a splice-isoform dependent manner. Cells 9, 1109 (2020).
Oláh, G. et al. Differentiation-associated downregulation of poly(ADP-ribose) polymerase-1 expression in myoblasts serves to increase their resistance to oxidative stress. PLoS ONE 10, e0134227 (2015).
Rack, J. G. M., Perina, D. & Ahel, I. Macrodomains: structure, function, evolution and catalytic activities. Annu. Rev. Biochem. 85, 431–54 (2016).
pubmed: 26844395
doi: 10.1146/annurev-biochem-060815-014935
Karras, G. I. et al. The macro domain is an ADP-ribose binding module. EMBO J. 24, 1911–1920 (2005).
pubmed: 15902274
pmcid: 1142602
doi: 10.1038/sj.emboj.7600664
Singh, H. R. et al. A poly-ADP-ribose trigger releases the auto-inhibition of a chromatin remodeling oncogene. Mol. Cell 68, 860–871.e7 (2017).
pubmed: 29220653
doi: 10.1016/j.molcel.2017.11.019
Timinszky, G. et al. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16, 923–929 (2009).
pubmed: 19680243
doi: 10.1038/nsmb.1664
Jankevicius, G. et al. A family of macrodomain proteins reverses cellular mono-ADP-ribosylation. Nat. Struct. Mol. Biol. 20, 508–514 (2013).
pubmed: 23474712
pmcid: 7097781
doi: 10.1038/nsmb.2523
Rosenthal, F. et al. Macrodomain-containing proteins are new mono-ADP-ribosylhydrolases. Nat. Struct. Mol. Biol. 20, 502–507 (2013).
pubmed: 23474714
doi: 10.1038/nsmb.2521
Buschbeck, M. & Hake, S. B. Variants of core histones and their roles in development, stem cells and cancer. Nat. Publ. Gr. https://doi.org/10.1038/nrm.2016.166 (2017).
Kustatscher, G., Hothorn, M., Pugieux, C., Scheffzek, K. & Ladurner, A. G. Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12, 624–625 (2005).
pubmed: 15965484
doi: 10.1038/nsmb956
Kozlowski, M. et al. MacroH2A histone variants limit chromatin plasticity through two distinct mechanisms. EMBO Rep. 19, e44445 (2018).
Chen, H. et al. MacroH2A1.1 and PARP-1 cooperate to regulate transcription by promoting CBP-mediated H2B acetylation. Nat. Struct. Mol. Biol. 21, 981–989 (2014).
pubmed: 25306110
pmcid: 4221384
doi: 10.1038/nsmb.2903
Ouararhni, K. et al. The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev. 20, 3324–3336 (2006).
pubmed: 17158748
pmcid: 1686608
doi: 10.1101/gad.396106
Rivera-Casas, C., Gonzalez-Romero, R., Cheema, M. S., Ausió, J. & Eirín-López, J. M. The characterization of macroH2A beyond vertebrates supports an ancestral origin and conserved role for histone variants in chromatin. Epigenetics 11, 415–425 (2016).
pubmed: 27082816
pmcid: 4939916
doi: 10.1080/15592294.2016.1172161
Torruella, G. et al. Phylogenomics reveals convergent evolution of lifestyles in close relatives of animals and fungi. Curr. Biol. 25, 2404–2410 (2015).
pubmed: 26365255
doi: 10.1016/j.cub.2015.07.053
Sebé-Pedrós, A. et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2013, e01287 (2013).
Allen, M. D., Buckle, A. M., Cordell, S. C., Löwe, J. & Bycroft, M. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J. Mol. Biol. 330, 503–511 (2003).
pubmed: 12842467
doi: 10.1016/S0022-2836(03)00473-X
Sebé-Pedrós, A. et al. High-throughput proteomics reveals the unicellular roots of animal phosphosignaling and cell differentiation. Dev. Cell 39, 186–197 (2016).
pubmed: 27746046
doi: 10.1016/j.devcel.2016.09.019
Douet, J. et al. MacroH2A histone variants maintain nuclear organization and heterochromatin architecture. J. Cell Sci. 130, 1570–1582 (2017).
pubmed: 28283545
Catara, G., Corteggio, A., Valente, C., Grimaldi, G. & Palazzo, L. Targeting ADP-ribosylation as an antimicrobial strategy. Biochem. Pharmacol. 167, 13–26 (2019).
pubmed: 31176616
pmcid: 7172630
doi: 10.1016/j.bcp.2019.06.001
Chen, W., Smeekens, J. M. & Wu, R. Systematic study of the dynamics and half-lives of newly synthesized proteins in human cells. Chem. Sci. 7, 1393–1400 (2016).
pubmed: 29910897
doi: 10.1039/C5SC03826J
Commerford, S. L., Carsten, A. L. & Cronkite, E. P. Histone turnover within nonproliferating cells. Proc. Natl Acad. Sci. USA 79, 1163–1165 (1982).
pubmed: 6951165
pmcid: 345921
doi: 10.1073/pnas.79.4.1163
Fornasiero, E. F. et al. Precisely measured protein lifetimes in the mouse brain reveal differences across tissues and subcellular fractions. Nat. Commun. https://doi.org/10.1038/s41467-018-06519-0 (2018).
Mathieson, T. et al. Systematic analysis of protein turnover in primary cells. Nat. Commun. 9, 689 (2018).
Pillai, A. S. et al. Origin of complexity in haemoglobin evolution. Nature 581, 480–485 (2020).
pubmed: 32461643
pmcid: 8259614
doi: 10.1038/s41586-020-2292-y
Huh, J. W., Shima, J. & Ochi, K. ADP-ribosylation of proteins in Bacillus subtilis and its possible importance in sporulation. J. Bacteriol. 178, 4935–4941 (1996).
pubmed: 8759858
pmcid: 178277
doi: 10.1128/jb.178.16.4935-4941.1996
Setlow, P. & Kornberg, A. Biochemical studies of bacterial sporulation and germination. J. Biol. Chem. 245, 3637–3644 (1970).
pubmed: 4394282
doi: 10.1016/S0021-9258(18)62974-6
Setlow, R. & Setlow, P. Levels of oxidized and reduced pyridine nucleotides in dormant spores and during growth, sporulation, and spore germination of Bacillus megaterium. J. Bacteriol. 129, 857–865 (1977).
pubmed: 14113
pmcid: 235022
doi: 10.1128/jb.129.2.857-865.1977
Berger, F., Lau, C., Dahlmann, M. & Ziegler, M. Subcellular compartmentation and differential catalytic properties of the three human nicotinamide mononucleotide adenylyltransferase isoforms. J. Biol. Chem. 280, 36334–36341 (2005).
pubmed: 16118205
doi: 10.1074/jbc.M508660200
Cambronne, X. A. et al. Biosensor reveals multiple sources for mitochondrial NAD
pubmed: 27313049
pmcid: 6530784
doi: 10.1126/science.aad5168
Simonet, N. G. et al. SirT7 auto-ADP-ribosylation regulates glucose starvation response through mH2A1. Sci. Adv. https://doi.org/10.1101/719559 (2020).
Creppe, C. et al. MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol. Cell. Biol. 32, 1442–1452 (2012).
pubmed: 22331466
pmcid: 3318583
doi: 10.1128/MCB.06323-11
Sporn, J. C. & Jung, B. Differential regulation and predictive potential of macroH2A1 isoforms in colon cancer. Am. J. Pathol. 180, 2516–2526 (2012).
pubmed: 22542848
pmcid: 3717782
doi: 10.1016/j.ajpath.2012.02.027
Sebé-Pedrós, A. et al. The dynamic regulatory genome of capsaspora and the origin of animal multicellularity. Cell 165, 1224–1237 (2016).
pubmed: 27114036
pmcid: 4877666
doi: 10.1016/j.cell.2016.03.034
Bockwoldt, M. et al. Identification of evolutionary and kinetic drivers of NAD-dependent signaling. Proc. Natl Acad. Sci. USA 116, 15957–15966 (2019).
pubmed: 31341085
pmcid: 6689970
doi: 10.1073/pnas.1902346116
Morowitz, H. J. A theory of biochemical organization, metabolic pathways, and evolution. Complexity 4, 39–53 (1999).
doi: 10.1002/(SICI)1099-0526(199907/08)4:6<39::AID-CPLX8>3.0.CO;2-2
Pehrson, J. R., Changolkar, L. N., Costanzi, C. & Leu, N. A. Mice without macroH2A histone variants. Mol. Cell. Biol. 34, 4523–4533 (2014).
pubmed: 25312643
pmcid: 4248737
doi: 10.1128/MCB.00794-14
Sebastian, R. et al. Epigenetic regulation of DNA repair pathway choice by MacroH2A1 splice variants ensures genome stability. Mol. Cell 79, 836–845.e7 (2020).
pubmed: 32649884
pmcid: 7483679
doi: 10.1016/j.molcel.2020.06.028
Lavigne, M. D. et al. Composite macroH2A/NRF-1 nucleosomes suppress noise and generate robustness in gene expression. Cell Rep. https://doi.org/10.1016/j.celrep.2015.04.022 (2015).
Afgan, E. et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res. 44, W3–W10 (2016).
pubmed: 27137889
pmcid: 4987906
doi: 10.1093/nar/gkw343
Brown, M. W. et al. Phylogenomics places orphan protistan lineages in a novel eukaryotic super-group. Genome Biol. Evol. 10, 427–433 (2018).
pubmed: 29360967
pmcid: 5793813
doi: 10.1093/gbe/evy014
de Mendoza, A., Suga, H., Permanyer, J., Irimia, M. & Ruiz-Trillo, I. Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals. eLife 4, e08904 (2015).
Dudin, O. et al. A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization. eLife 8, e49801 (2019).
Grau-Bové, X. et al. Dynamics of genomic innovation in the unicellular ancestry of animals. eLife 6, e26036 (2017).
Hehenberger, E. et al. Novel predators reshape holozoan phylogeny and reveal the presence of a two-component signaling system in the ancestor of animals. Curr. Biol. 27, 2043–2050.e6 (2017).
pubmed: 28648822
doi: 10.1016/j.cub.2017.06.006
Richter, D., Berney, C., Strassert, J., Burki, F. & de Vargas, C. EukProt: a database of genome-scale predicted proteins across the diversity of eukaryotic life. Preprint at bioRxiv https://doi.org/10.1101/2020.06.30.180687 (2020).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2-A multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009).
pubmed: 19151095
pmcid: 2672624
doi: 10.1093/bioinformatics/btp033
Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: a sequence logo generator. Genome Res 14, 1188–1190 (2004).
pubmed: 15173120
pmcid: 419797
doi: 10.1101/gr.849004
Bawono, P. & Heringa, J. PRALINE: a versatile multiple sequence alignment toolkit. Methods Mol. Biol. 1079, 245–262 (2014).
pubmed: 24170407
doi: 10.1007/978-1-62703-646-7_16
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
Le, S. Q. & Gascuel, O. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25, 1307–1320 (2008).
pubmed: 18367465
doi: 10.1093/molbev/msn067
Hedges, S. B., Dudley, J. & Kumar, S. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971–2972 (2006).
pubmed: 17021158
doi: 10.1093/bioinformatics/btl505
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Suga, H. et al. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat. Commun. 4, 2325 (2013).
Liao, Y., Smyth, G. K. & Shi, W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
Huerta-Cepas, J. et al. EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314 (2019).
pubmed: 30418610
doi: 10.1093/nar/gky1085
Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30 (2000).
pubmed: 10592173
pmcid: 102409
doi: 10.1093/nar/28.1.27
Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016).
pubmed: 26585406
doi: 10.1016/j.jmb.2015.11.006
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 236 (2019).
Ruiz, P. D. & Gamble, M. J. MacroH2A1 chromatin specification requires its docking domain and acetylation of H2B lysine 20. Nat. Commun. 9, 5143 (2018).
Mayer, M. & Meyer, B. Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angew. Chem. 38, 1784–1788 (1999).
doi: 10.1002/(SICI)1521-3773(19990614)38:12<1784::AID-ANIE1784>3.0.CO;2-Q
Aretz, J. et al. Allosteric inhibition of a mammalian lectin. J. Am. Chem. Soc. 140, 14915–14925 (2018).
pubmed: 30303367
doi: 10.1021/jacs.8b08644
Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125–132 (2010).
pubmed: 20124692
pmcid: 2815665
doi: 10.1107/S0907444909047337
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
pubmed: 15572765
doi: 10.1107/S0907444904019158
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493
Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352–367 (2012).
pubmed: 22505256
pmcid: 3322595
doi: 10.1107/S0907444912001308
Moriarty, N. W., Grosse-Kunstleve, R. W. & Adams, P. D. Electronic ligand builder and optimization workbench (eLBOW): a tool for ligand coordinate and restraint generation. Acta Crystallogr. D Biol. Crystallogr. 65, 1074–1080 (2009).
pubmed: 19770504
pmcid: 2748967
doi: 10.1107/S0907444909029436
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Wallace, A. C., Laskowski, R. A. & Thornton, J. M. Ligplot: a program to generate schematic diagrams of protein–ligand interactions. Protein Eng. Des. Sel. 8, 127–134 (1995).
doi: 10.1093/protein/8.2.127
Ashkenazy, H. et al. ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 44, W344–W350 (2016).
pubmed: 27166375
pmcid: 4987940
doi: 10.1093/nar/gkw408
Sporn, J. C. et al. Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 28, 3423–3428 (2009).
pubmed: 19648962
doi: 10.1038/onc.2009.26
Fackelmayer, F., Dahm, K., Renz, A., Ramsperger, U. & Richter, A. Nucleic-acid-binding properties of hnRNP-U/SAF-A, a nuclear-matrix protein which binds DNA and RNA in vivo and in vitro. Eur. J. Biochem. 221, 749–757 (1994).
pubmed: 8174554
doi: 10.1111/j.1432-1033.1994.tb18788.x