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Research Article

Impact of Nuclear De Novo NAD+ Synthesis via Histone Dynamics on DNA Repair during Cellular Senescence To Prevent Tumorigenesis

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Article: e00379-22 | Received 01 Sep 2022, Accepted 27 Sep 2022, Published online: 24 Feb 2023

REFERENCES

  • Demarest TG, Babbar M, Okur MN, Dan X, Croteau DL, Fakouri NB, Mattson MP, Bohr VA. 2019. NAD+ metabolism in aging and cancer. Annu Rev Cancer Biol 3:105–130. https://doi.org/10.1146/annurev-cancerbio-030518-055905.
  • Xie N, Zhang L, Gao W, Huang C, Huber PE, Zhou X, Li C, Shen G, Zou B. 2020. NAD(+) metabolism: pathophysiologic mechanisms and therapeutic potential. Signal Transduct Target Ther 5:227. https://doi.org/10.1038/s41392-020-00311-7.
  • Canto C, Menzies KJ, Auwerx J. 2015. NAD(+) metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab 22:31–53. https://doi.org/10.1016/j.cmet.2015.05.023.
  • Yaku K, Okabe K, Nakagawa T. 2018. NAD metabolism: implications in aging and longevity. Ageing Res Rev 47:1–17. https://doi.org/10.1016/j.arr.2018.05.006.
  • Shi H, Enriquez A, Rapadas M, Martin E, Wang R, Moreau J, Lim CK, Szot JO, Ip E, Hughes JN, Sugimoto K, Humphreys DT, McInerney-Leo AM, Leo PJ, Maghzal GJ, Halliday J, Smith J, Colley A, Mark PR, Collins F, Sillence DO, Winlaw DS, Ho JWK, Guillemin GJ, Brown MA, Kikuchi K, Thomas PQ, Stocker R, Giannoulatou E, Chapman G, Duncan EL, Sparrow DB, Dunwoodie SL. 2017. NAD deficiency, congenital malformations, and niacin supplementation. N Engl J Med 377:544–552. https://doi.org/10.1056/NEJMoa1616361.
  • Liu L, Su X, Quinn WJ, III, Hui S, Krukenberg K, Frederick DW, Redpath P, Zhan L, Chellappa K, White E, Migaud M, Mitchison TJ, Baur JA, Rabinowitz JD. 2018. Quantitative analysis of NAD synthesis-breakdown fluxes. Cell Metab 27:1067–1080.E5. https://doi.org/10.1016/j.cmet.2018.03.018.
  • Poyan Mehr A, Tran MT, Ralto KM, Leaf DE, Washco V, Messmer J, Lerner A, Kher A, Kim SH, Khoury CC, Herzig SJ, Trovato ME, Simon-Tillaux N, Lynch MR, Thadhani RI, Clish CB, Khabbaz KR, Rhee EP, Waikar SS, Berg AH, Parikh SM. 2018. De novo NAD(+) biosynthetic impairment in acute kidney injury in humans. Nat Med 24:1351–1359. https://doi.org/10.1038/s41591-018-0138-z.
  • Katsyuba E, Mottis A, Zietak M, De Franco F, van der Velpen V, Gariani K, Ryu D, Cialabrini L, Matilainen O, Liscio P, Giacche N, Stokar-Regenscheit N, Legouis D, de Seigneux S, Ivanisevic J, Raffaelli N, Schoonjans K, Pellicciari R, Auwerx J. 2018. De novo NAD(+) synthesis enhances mitochondrial function and improves health. Nature 563:354–359. https://doi.org/10.1038/s41586-018-0645-6.
  • Tummala KS, Gomes AL, Yilmaz M, Grana O, Bakiri L, Ruppen I, Ximenez-Embun P, Sheshappanavar V, Rodriguez-Justo M, Pisano DG, Wagner EF, Djouder N. 2014. Inhibition of de novo NAD(+) synthesis by oncogenic URI causes liver tumorigenesis through DNA damage. Cancer Cell 26:826–839. https://doi.org/10.1016/j.ccell.2014.10.002.
  • Fjeld CC, Birdsong WT, Goodman RH. 2003. Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor. Proc Natl Acad Sci USA 100:9202–9207. https://doi.org/10.1073/pnas.1633591100.
  • Katoh Y, Ikura T, Hoshikawa Y, Tashiro S, Ito T, Ohta M, Kera Y, Noda T, Igarashi K. 2011. Methionine adenosyltransferase II serves as a transcriptional corepressor of Maf oncoprotein. Mol Cell 41:554–566. https://doi.org/10.1016/j.molcel.2011.02.018.
  • Ikura M, Furuya K, Fukuto A, Matsuda R, Adachi J, Matsuda T, Kakizuka A, Ikura T. 2016. Coordinated regulation of TIP60 and poly(ADP-ribose) polymerase 1 in damaged-chromatin dynamics. Mol Cell Biol 36:1595–1607. https://doi.org/10.1128/MCB.01085-15.
  • Zhang T, Berrocal JG, Frizzell KM, Gamble MJ, DuMond ME, Krishnakumar R, Yang T, Sauve AA, Kraus WL. 2009. Enzymes in the NAD+ salvage pathway regulate SIRT1 activity at target gene promoters. J Biol Chem 284:20408–20417. https://doi.org/10.1074/jbc.M109.016469.
  • Zhang T, Berrocal JG, Yao J, DuMond ME, Krishnakumar R, Ruhl DD, Ryu KW, Gamble MJ, Kraus WL. 2012. Regulation of poly(ADP-ribose) polymerase-1-dependent gene expression through promoter-directed recruitment of a nuclear NAD+ synthase. J Biol Chem 287:12405–12416. https://doi.org/10.1074/jbc.M111.304469.
  • Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, Scully R, Qin J, Nakatani Y. 2000. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:463–473. https://doi.org/10.1016/s0092-8674(00)00051-9.
  • Ikura T, Tashiro S, Kakino A, Shima H, Jacob N, Amunugama R, Yoder K, Izumi S, Kuraoka I, Tanaka K, Kimura H, Ikura M, Nishikubo S, Ito T, Muto A, Miyagawa K, Takeda S, Fishel R, Igarashi K, Kamiya K. 2007. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol 27:7028–7040. https://doi.org/10.1128/MCB.00579-07.
  • Ikura M, Furuya K, Matsuda S, Matsuda R, Shima H, Adachi J, Matsuda T, Shiraki T, Ikura T. 2015. Acetylation of histone H2AX at Lys 5 by the TIP60 histone acetyltransferase complex is essential for the dynamic binding of NBS1 to damaged chromatin. Mol Cell Biol 35:4147–4157. https://doi.org/10.1128/MCB.00757-15.
  • Bogan KL, Brenner C. 2008. Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu Rev Nutr 28:115–130. https://doi.org/10.1146/annurev.nutr.28.061807.155443.
  • Hu L, Ibrahim K, Stucki M, Frapolli M, Shahbeck N, Chaudhry FA, Gorg B, Haussinger D, Penberthy WT, Ben-Omran T, Haberle J. 2015. Secondary NAD+ deficiency in the inherited defect of glutamine synthetase. J Inherit Metab Dis 38:1075–1083. https://doi.org/10.1007/s10545-015-9846-4.
  • Matsuda S, Adachi J, Ihara M, Tanuma N, Shima H, Kakizuka A, Ikura M, Ikura T, Matsuda T. 2016. Nuclear pyruvate kinase M2 complex serves as a transcriptional coactivator of arylhydrocarbon receptor. Nucleic Acids Res 44:636–647. https://doi.org/10.1093/nar/gkv967.
  • Tang J, Cho NW, Cui G, Manion EM, Shanbhag NM, Botuyan MV, Mer G, Greenberg RA. 2013. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 20:317–325. https://doi.org/10.1038/nsmb.2499.
  • Aymard F, Bugler B, Schmidt CK, Guillou E, Caron P, Briois S, Iacovoni JS, Daburon V, Miller KM, Jackson SP, Legube G. 2014. Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat Struct Mol Biol 21:366–374. https://doi.org/10.1038/nsmb.2796.
  • Zheng D, Ezzeddine N, Chen CY, Zhu W, He X, Shyu AB. 2008. Deadenylation is prerequisite for P-body formation and mRNA decay in mammalian cells. J Cell Biol 182:89–101. https://doi.org/10.1083/jcb.200801196.
  • Suda Y, Tachikawa H, Yokota A, Nakanishi H, Yamashita N, Miura Y, Takahashi N. 2003. Saccharomyces cerevisiae QNS1 codes for NAD(+) synthetase that is functionally conserved in mammals. Yeast 20:995–1005. https://doi.org/10.1002/yea.1008.
  • Kalderon D, Roberts BL, Richardson WD, Smith AE. 1984. A short amino acid sequence able to specify nuclear location. Cell 39:499–509. https://doi.org/10.1016/0092-8674(84)90457-4.
  • Wojcik M, Seidle HF, Bieganowski P, Brenner C. 2006. Glutamine-dependent NAD+ synthetase. How a two-domain, three-substrate enzyme avoids waste. J Biol Chem 281:33395–33402. https://doi.org/10.1074/jbc.M607111200.
  • Lukas C, Melander F, Stucki M, Falck J, Bekker-Jensen S, Goldberg M, Lerenthal Y, Jackson SP, Bartek J, Lukas J. 2004. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J 23:2674–2683. https://doi.org/10.1038/sj.emboj.7600269.
  • Zahradka P, Ebisuzaki K. 1982. A shuttle mechanism for DNA-protein interactions. The regulation of poly(ADP-ribose) polymerase. Eur J Biochem 127:579–585.
  • Ferro AM, Olivera BM. 1982. Poly(ADP-ribosylation) in vitro. Reaction parameters and enzyme mechanism. J Biol Chem 257:7808–7813. https://doi.org/10.1016/S0021-9258(18)34453-3.
  • Langelier MF, Pascal JM. 2013. PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr Opin Struct Biol 23:134–143. https://doi.org/10.1016/j.sbi.2013.01.003.
  • He J, Hu B, Shi X, Weidert ER, Lu P, Xu M, Huang M, Kelley EE, Xie W. 2013. Activation of the aryl hydrocarbon receptor sensitizes mice to nonalcoholic steatohepatitis by deactivating mitochondrial sirtuin deacetylase Sirt3. Mol Cell Biol 33:2047–2055. https://doi.org/10.1128/MCB.01658-12.
  • Stein LR, Imai S. 2012. The dynamic regulation of NAD metabolism in mitochondria. Trends Endocrinol Metab 23:420–428. https://doi.org/10.1016/j.tem.2012.06.005.
  • Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD, Jr, Chen LB. 1991. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA 88:3671–3675. https://doi.org/10.1073/pnas.88.9.3671.
  • Wiley CD, Campisi J. 2021. The metabolic roots of senescence: mechanisms and opportunities for intervention. Nat Metab 3:1290–1301. https://doi.org/10.1038/s42255-021-00483-8.
  • Petr MA, Tulika T, Carmona-Marin LM, Scheibye-Knudsen M. 2020. Protecting the aging genome. Trends Cell Biol 30:117–132. https://doi.org/10.1016/j.tcb.2019.12.001.
  • Krenning L, van den Berg J, Medema RH. 2019. Life or death after a break: what determines the choice? Mol Cell 76:346–358. https://doi.org/10.1016/j.molcel.2019.08.023.
  • Caron MC, Sharma AK, O'Sullivan J, Myler LR, Ferreira MT, Rodrigue A, Coulombe Y, Ethier C, Gagne JP, Langelier MF, Pascal JM, Finkelstein IJ, Hendzel MJ, Poirier GG, Masson JY. 2019. Poly(ADP-ribose) polymerase-1 antagonizes DNA resection at double-strand breaks. Nat Commun 10:2954. https://doi.org/10.1038/s41467-019-10741-9.
  • Helleday T, Bryant HE, Schultz N. 2005. Poly(ADP-ribose) polymerase (PARP-1) in homologous recombination and as a target for cancer therapy. Cell Cycle 4:1176–1178. https://doi.org/10.4161/cc.4.9.2031.
  • Yoshino Y, Endo S, Chen Z, Qi H, Watanabe G, Chiba N. 2019. Evaluation of site-specific homologous recombination activity of BRCA1 by direct quantitation of gene editing efficiency. Sci Rep 9:1644. https://doi.org/10.1038/s41598-018-38311-x.
  • Helleday T. 2010. Homologous recombination in cancer development, treatment and development of drug resistance. Carcinogenesis 31:955–960. https://doi.org/10.1093/carcin/bgq064.
  • Carr AM, Lambert S. 2013. Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J Mol Biol 425:4733–4744. https://doi.org/10.1016/j.jmb.2013.04.023.
  • Cifone MA, Fidler IJ. 1980. Correlation of patterns of anchorage-independent growth with in vivo behavior of cells from a murine fibrosarcoma. Proc Natl Acad Sci USA 77:1039–1043. https://doi.org/10.1073/pnas.77.2.1039.
  • Chan ASL, Narita M. 2019. Short-term gain, long-term pain: the senescence life cycle and cancer. Genes Dev 33:127–143. https://doi.org/10.1101/gad.320937.118.
  • Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, d'Adda di Fagagna F, Bernard D, Hernando E, Gil J. 2008. Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133:1006–1018. https://doi.org/10.1016/j.cell.2008.03.038.
  • Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ, Peeper DS. 2008. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133:1019–1031. https://doi.org/10.1016/j.cell.2008.03.039.
  • Huang Z, Xie N, Illes P, Di Virgilio F, Ulrich H, Semyanov A, Verkhratsky A, Sperlagh B, Yu SG, Huang C, Tang Y. 2021. From purines to purinergic signalling: molecular functions and human diseases. Signal Transduct Target Ther 6:162. https://doi.org/10.1038/s41392-021-00553-z.
  • Ikeda T, Uno M, Honjoh S, Nishida E. 2017. The MYST family histone acetyltransferase complex regulates stress resistance and longevity through transcriptional control of DAF-16/FOXO transcription factors. EMBO Rep 18:1716–1726. https://doi.org/10.15252/embr.201743907.

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