Роль гидролаз семейства NUDIX в метаболизме NAD и ADP-рибозы у млекопитающих

Сноски

* Адресат для корреспонденции.

Финансирование

Работа выполнена при финансовой поддержке РНФ (проект 18-74-00081) и РФФИ (проект 19-34-60039).

Конфликт интересов

Авторы заявляют об отсутствии конфликта интересов.

Соблюдение этических норм

Настоящая статья не содержит описания каких-либо исследований с участием людей или животных в качестве объектов.

Список литературы

1. McLennan, A. G. (2006) The Nudix hydrolase superfamily, Cell. Mol. Life Sci., 63, 123-143, doi: 10.1007/s00018-005-5386-7.

2. Carreras-Puigvert, J., Zitnik, M., Jemth, A. S., Carter, M., Unterlass, J. E. et al. (2017) A comprehensive structural, biochemical and biological profiling of the human NUDIX hydrolase family, Nat. Commun., 8, 1541, doi: 10.1038/s41467-017-01642-w.

3. Rai, P., and Sobol, R. W. (2019) Mechanisms of MTH1 inhibition-induced DNA strand breaks: the slipperyslope from the oxidized nucleotide pool to genotoxic damage, DNA Rep., 77, 18-26, doi: 10.1016/j.dnarep.2019.03.001.

4. Ishibashi, T., Hayakawa, H., and Sekiguchi, M. (2003) A novel mechanism for preventing mutations caused by oxidation of guanine nucleotides, EMBO Rep., 4, 479-483, doi: 10.1038/sj.embor.embor838.

5. Cai, J. P., Ishibashi, T., Takagi, Y., Hayakawa, H., and Sekiguchi, M. (2003) Mouse MTH2 protein which prevents mutations caused by 8-oxoguanine nucleotides, Biochem. Biophys. Res. Commun., 305, 1073-1077, doi: 10.1016/s0006-291x(03)00864-7.

6. Ishibashi, T., Hayakawa, H., Ito, R., Miyazawa, M., Yamagata, Y., and Sekiguchi, M. (2005) Mammalian enzymes for preventing transcriptional errors caused by oxidative damage, Nucleic Acids Res., 33, 3779-3784, doi: 10.1093/nar/gki682.

7. Grudzien-Nogalska, E., and Kiledjian, M. (2017) New insights into decapping enzymes and selective mRNA decay, Wiley Interdisc. rev. RNA, 8, doi: 10.1002/wrna.1379.

8. Lu, G., Zhang, J., Li, Y., Li, Z., Zhang, N., Xu, X., Wang, T., Guan, Z., Gao, G. F., and Yan, J. (2011) hNUDT16: a universal decapping enzyme for small nucleolar RNA and cytoplasmic mRNA, Protein Cell, 2, 64-73, doi: 10.1007/s13238-011-1009-2.

9. Gasmi, L., and McLennan, A. G. (2001) The mouse Nudt7 gene encodes a peroxisomal nudix hydrolase specific for coenzyme A and its derivatives, Biochemi. J., 357, 33-38, doi: 10.1042/0264-6021:3570033.

10. Shumar, S. A., Kerr, E. W., Geldenhuys, W. J., Montgomery, G. E., Fagone, P., Thirawatananond, P., Saavedra, H., Gabelli, S. B., and Leonardi, R. (2018) Nudt19 is a renal CoA diphosphohydrolase with biochemical and regulatory properties that are distinct from the hepatic Nudt7 isoform, J. Biol. Chem., 293, 4134-4148, doi: 10.1074/jbc.RA117.001358.

11. Kerr, E. W., Shumar, S. A., and Leonardi, R. (2019) Nudt8 is a novel CoA diphosphohydrolase that resides in the mitochondria, FEBS Lett., 593, 1133-1143, doi: 10.1002/1873-3468.13392.

12. Ying, W. (2008) NAD⁺/NADH and NADP⁺/NADPH in cellular functions and cell death: regulation and biological consequences, Antioxid. Redox Signal., 10, 179-206, doi: 10.1089/ars.2007.1672.

13. Kulikova, V. A., Gromyko, D. V., and Nikiforov, A. A. (2018) The regulatory role of NAD in human and animal cells, Biochemistry (Moscow), 83, 800-812, doi: 10.1134/S0006297918070040.

14. Stromland, O., Niere, M., Nikiforov, A. A., VanLinden, M. R., Heiland, I., and Ziegler, M. (2019) Keeping the balance in NAD metabolism, Biochem. Soc. Trans., 47, 119-130, doi: 10.1042/BST20180417.

15. Yang, Y., and Sauve, A. A. (2016) NAD(+) metabolism: Bioenergetics, signaling and manipulation for therapy, Biochim. Biophys. Acta, 1864, 1787-1800, doi: 10.1016/j.bbapap.2016.06.014.

16. Gupte, R., Liu, Z., and Kraus, W. L. (2017) PARPs and ADP-ribosylation: recent advances linking molecular functions to biological outcomes, Genes Dev., 31, 101-126, doi: 10.1101/gad.291518.116.

17. Cohen, M. S., and Chang, P. (2018) Insights into the biogenesis, function, and regulation of ADP-ribosylation, Nat. Chem. Biol., 14, 236-243, doi: 10.1038/nchembio.2568.

18. Rack, J. G. M., Palazzo, L., and Ahel, I. (2020) (ADP-ribosyl)hydrolases: structure, function, and biology, Genes Dev., 34, 263-284, doi: 10.1101/gad.334631.119.

19. Talhaoui, I., Lebedeva, N. A., Zarkovic, G., Saint-Pierre, C., Kutuzov, M. M., Sukhanova, M. V., Matkarimov, B. T., Gasparutto, D., Saparbaev, M. K., Lavrik, O. I., and Ishchenko, A. A. (2016) Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro, Nucl. Acids Res., 44, 9279-9295, doi: 10.1093/nar/gkw675.

20. Munnur, D., and Ahel, I. (2017) Reversible mono-ADP-ribosylation of DNA breaks, FEBS J., 284, 4002-4016, doi: 10.1111/febs.14297.

21. Munnur, D., Bartlett, E., Mikolcevic, P., Kirby, I. T., Rack, J. G. M., Mikoc, A., Cohen, M. S., and Ahel, I. (2019) Reversible ADP-ribosylation of RNA, Nucl. Acids Res., 47, 5658-5669, doi: 10.1093/nar/gkz305.

22. Houtkooper, R. H., Pirinen, E., and Auwerx, J. (2012) Sirtuins as regulators of metabolism and healthspan, Nat. Rev. Mol. Cell Biol., 13, 225-238, doi: 10.1038/nrm3293.

23. Tanner, K. G., Landry, J., Sternglanz, R., and Denu, J. M. (2000) Silent information regulator 2 family of NAD- dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose, Proc. Natl. Acad. Sci. USA, 97, 14178-14182, doi: 10.1073/pnas.250422697.

24. Sassone-Corsi, P. (2016) The Epigenetic and Metabolic Language of the Circadian Clock, in A Time for Metabolism and Hormones (Sassone-Corsi, P., and Christen, Y. eds.) Cham (CH), pp. 1-11

25. Imai, S., and Guarente, L. (2014) NAD⁺ and sirtuins in aging and disease, Trends Cell. Biol., 24, 464-471, doi: 10.1016/j.tcb.2014.04.002.

26. Cao, Y., Jiang, X., Ma, H., Wang, Y., Xue, P., and Liu, Y. (2016) SIRT1 and insulin resistance, J. Diabetes Complic., 30, 178-183, doi: 10.1016/j.jdiacomp.2015.08.022.

27. Grubisha, O., Rafty, L. A., Takanishi, C. L., Xu, X., Tong, L., Perraud, A. L., Scharenberg, A. M., and Denu, J. M. (2006) Metabolite of SIR2 reaction modulates TRPM2 ion channel, J. Biolog. Chem., 281, 14057-14065, doi: 10.1074/jbc.M513741200.

28. Chen, D., Vollmar, M., Rossi, M. N., Phillips, C., Kraehenbuehl, R., Slade, D., Mehrotra, P. V., von Delft, F., Crosthwaite, S. K., Gileadi, O., Denu, J. M., and Ahel, I. (2011) Identification of macrodomain proteins as novel O-acetyl-ADP-ribose deacetylases, J. Biolog. Chem., 286, 13261-13271, doi: 10.1074/jbc.M110.206771.

29. Ono, T., Kasamatsu, A., Oka, S., and Moss, J. (2006) The 39-kDa poly(ADP-ribose) glycohydrolase ARH3 hydrolyzes O-acetyl-ADP-ribose, a product of the Sir2 family of acetyl-histone deacetylases, Proc. Natl. Acad. Sci. USA, 103, 16687-16691, doi: 10.1073/pnas.0607911103.

30. Lee, H. C., and Zhao, Y. J. (2019) Resolving the topological enigma in Ca²⁺ signaling by cyclic ADP-ribose and NAADP, J. Biolog. Chem., 294, 19831-19843, doi: 10.1074/jbc.REV119.009635.

31. Guse, A. H. (2015) Calcium mobilizing second messengers derived from NAD, Biochim. Biophys. Acta, 1854, 1132-1137, doi: 10.1016/j.bbapap.2014.12.015.

32. Sumoza-Toledo, A., and Penner, R. (2011) TRPM2: a multifunctional ion channel for calcium signalling, J. Physiol., 589, 1515-1525, doi: 10.1113/jphysiol.2010.201855.

33. Jiao, X., Doamekpor, S. K., Bird, J. G., Nickels, B. E., Tong, L., Hart, R. P., and Kiledjian, M. (2017) 5′-End nicotinamide adenine dinucleotide cap in human cells promotes RNA decay through DXO-mediated deNADding, Cell, 168, 1015-1027, doi: 10.1016/j.cell.2017.02.019.

34. Luscher, B., Butepage, M., Eckei, L., Krieg, S., Verheugd, P., and Shilton, B. H. (2018) ADP-ribosylation, a multifaceted posttranslational modification involved in the control of cell physiology in health and disease, Chem. Rev., 118, 1092-1136, doi: 10.1021/acs.chemrev.7b00122.

35. Nikiforov, A., Kulikova, V., and Ziegler, M. (2015) The human NAD metabolome: functions, metabolism and compartmentalization, Crit. Rev. Biochem. Mol. Biol., 50, 284-297, doi: 10.3109/10409238.2015.1028612.

36. Katsyuba, E., Romani, M., Hofer, D., and Auwerx, J. (2020) NAD⁺ homeostasis in health and disease, Nat. Metab., 2, doi: 10.1038/s42255-019-0161-5.

37. Dolle, C., Skoge, R. H., Vanlinden, M. R., and Ziegler, M. (2013) NAD biosynthesis in humans – enzymes, metabolites and therapeutic aspects, Curr. Top. Med. Chem., 13, 2907-2917, doi: 10.2174/15680266113136660206.

38. Yang, Y., Zhang, N., Zhang, G., and Sauve, A. A. (2020) NRH salvage and conversion to NAD⁺ requires NRH kinase activity by adenosine kinase, Nat. Metab., 2, 364-379, doi: 10.1038/s42255-020-0194-9.

39. Frick, D. N., and Bessman, M. J. (1995) Cloning, purification, and properties of a novel NADH pyrophosphatase. Evidence for a nucleotide pyrophosphatase catalytic domain in MutT-like enzymes, J. Biolog. Chem., 270, 1529-1534, doi: 10.1074/jbc.270.4.1529.

40. Shimizu, M., Masuo, S., Fujita, T., Doi, Y., Kamimura, Y., and Takaya, N. (2012) Hydrolase controls cellular NAD, sirtuin, and secondary metabolites, Mol. Cell. Biol., 32, 3743-3755, doi: 10.1128/MCB.00032-12.

41. Xu, W., Dunn, C. A., and Bessman, M. J. (2000) Cloning and characterization of the NADH pyrophosphatases from Caenorhabditis elegans and Saccharomyces cerevisiae, members of a Nudix hydrolase subfamily, Biochem. Biophys. Res. Commun., 273, 753-758, doi: 10.1006/bbrc.2000.2999.

42. AbdelRaheim, S. R., Cartwright, J. L., Gasmi, L., and McLennan, A. G. (2001) The NADH diphosphatase encoded by the Saccharomyces cerevisiae NPY1 Nudix hydrolase gene is located in peroxisomes, Arch. Biochem. Biophys., 388, 18-24, doi: 10.1006/abbi.2000.2268.

43. AbdelRaheim, S. R., Spiller, D. G., and McLennan, A. G. (2003) Mammalian NADH diphosphatases of the Nudix family: cloning and characterization of the human peroxisomal NUDT12 protein, Biochem. J., 374, 329-335, doi: 10.1042/BJ20030441.

44. Dunn, C. A., O’Handley, S. F., Frick, D. N., and Bessman, M. J. (1999) Studies on the ADP-ribose pyrophosphatase subfamily of the nudix hydrolases and tentative identification of trgB, a gene associated with tellurite resistance, J. Biol. Chem., 274, 32318-32324, doi: 10.1074/jbc.274.45.32318.

45. Lin, S., Gasmi, L., Xie, Y., Ying, K., Gu, S., Wang, Z., Jin, H., Chao, Y., Wu, C., Zhou, Z., Tang, R., Mao, Y., and McLennan, A. G. (2002) Cloning, expression and characterisation of a human Nudix hydrolase specific for adenosine 5′-diphosphoribose (ADP-ribose), Biochim. Biophys. Acta, 1594, 127-135, doi: 10.1016/s0167-4838(01)00296-5.

46. Tong, L., Lee, S., and Denu, J. M. (2009) Hydrolase regulates NAD⁺ metabolites and modulates cellular redox, J. Biolog. Chem., 284, 11256-11266, doi: 10.1074/jbc.M809790200.

47. Adam-Vizi, V., and Chinopoulos, C. (2006) Bioenergetics and the formation of mitochondrial reactive oxygen species, Trends Pharmacolog. Sci., 27, 639-645, doi: 10.1016/j.tips.2006.10.005.

48. Jamieson, D. J. (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae, Yeast, 14, 1511-1527, doi: 10.1002/(SICI)1097-0061(199812)14:16<1511::AID-YEA356>3.0.CO;2-S.

49. Abdelraheim, S. R., Spiller, D. G., and McLennan, A. G. (2017) Mouse Nudt13 is a mitochondrial Nudix hydrolase with NAD(P)H pyrophosphohydrolase activity, Protein J., 36, 425-432, doi: 10.1007/s10930-017-9734-x.

50. Wu, H., Li, L., Chen, K. M., Homolka, D., Gos, P., Fleury-Olela, F., McCarthy, A. A., and Pillai, R. S. (2019) Decapping enzyme NUDT12 partners with BLMH for cytoplasmic surveillance of NAD-capped RNAs, Cell Rep., 29, 4422-4434, doi: 10.1016/j.celrep.2019.11.108.

51. Wanders, R. J., Waterham, H. R., and Ferdinandusse, S. (2015) Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum, Front. Cell Dev. Biol., 3, 83, doi: 10.3389/fcell.2015.00083.

52. Agrimi, G., Russo, A., Scarcia, P., and Palmieri, F. (2012) The human gene SLC25A17 encodes a peroxisomal transporter of coenzyme A, FAD and NAD⁺, Biochem. J., 443, 241-247, doi: 10.1042/BJ20111420.

53. Antonenkov, V. D., and Hiltunen, J. K. (2012) Transfer of metabolites across the peroxisomal membrane, Biochim. Biophys. Acta, 1822, 1374-1386, doi: 10.1016/j.bbadis.2011.12.011.

54. Antonenkov, V. D., Sormunen, R. T., and Hiltunen, J. K. (2004) The rat liver peroxisomal membrane forms a permeability barrier for cofactors but not for small metabolites in vitro, J. Cell Sci., 117, 5633-5642, doi: 10.1242/jcs.01485.

55. Rokka, A., Antonenkov, V. D., Soininen, R., Immonen, H. L., Pirila, P. L., Bergmann, U., Sormunen, R. T., Weckstrom, M., Benz, R., and Hiltunen, J. K. (2009) Pxmp2 is a channel-forming protein in Mammalian peroxisomal membrane, PLoS One, 4, e5090, doi: 10.1371/journal.pone.0005090.

56. Ramanathan, A., Robb, G. B., and Chan, S. H. (2016) mRNA capping: biological functions and applications, Nucleic Acids Res., 44, 7511-7526, doi: 10.1093/nar/gkw551.

57. Grudzien-Nogalska, E., Wu, Y., Jiao, X., Cui, H., Mateyak, M. K., Hart, R. P., Tong, L., and Kiledjian, M. (2019) Structural and mechanistic basis of mammalian Nudt12 RNA deNADding, Nat. Chem. Biol., 15, 575-582, doi: 10.1038/s41589-019-0293-7.

58. Alano, C. C., Tran, A., Tao, R., Ying, W., Karliner, J. S., and Swanson, R. A. (2007) Differences among cell types in NAD(+) compartmentalization: a comparison of neurons, astrocytes, and cardiac myocytes, J. Neurosci. Res., 85, 3378-3385, doi: 10.1002/jnr.21479.

59. Stein, L. R., and Imai, S. (2012) The dynamic regulation of NAD metabolism in mitochondria, Trends Edocrinol. Metab., 23, 420-428, doi: 10.1016/j.tem.2012.06.005.

60. Wallace, D. C. (2009) Mitochondria, bioenergetics, and the epigenome in eukaryotic and human evolution, Cold Spring Harb. Symp. Quant. Biol., 74, 383-393, doi: 10.1101/sqb.2009.74.031.

61. Dolle, C., Rack, J. G., and Ziegler, M. (2013) NAD and ADP-ribose metabolism in mitochondria, FEBS J., 280, 3530-3541, doi: 10.1111/febs.12304.

62. Yang, H., Yang, T., Baur, J. A., Perez, E., Matsui, T., Carmona, J. J., Lamming, D. W., Souza-Pinto, N. C., Bohr, V. A., Rosenzweig, A., de Cabo, R., Sauve, A. A., and Sinclair, D. A. (2007) Nutrient-sensitive mitochondrial NAD⁺ levels dictate cell survival, Cell, 130, 1095-1107, doi: 10.1016/j.cell.2007.07.035.

63. Pittelli, M., Formentini, L., Faraco, G., Lapucci, A., Rapizzi, E., Cialdai, F., Romano, G., Moneti, G., Moroni, F., and Chiarugi, A. (2010) Inhibition of nicotinamide phosphoribosyltransferase: cellular bioenergetics reveals a mitochondrial insensitive NAD pool, J. Biol. Chem., 285, 34106-34114, doi: 10.1074/jbc.M110.136739.

64. Barile, M., Passarella, S., Danese, G., and Quagliariello, E. (1996) Rat liver mitochondria can synthesize nicotinamide adenine dinucleotide from nicotinamide mononucleotide and ATP via a putative matrix nicotinamide mononucleotide adenylyltransferase, Biochem. Mol. Biol. Intern., 38, 297-306.

65. Nikiforov, A., Dolle, C., Niere, M., and Ziegler, M. (2011) Pathways and subcellular compartmentation of NAD biosynthesis in human cells: from entry of extracellular precursors to mitochondrial NAD generation, J. Biol. Chem., 286, 21767-21778, doi: 10.1074/jbc.M110.213298.

66. Davila, A., Liu, L., Chellappa, K., Redpath, P., Nakamaru-Ogiso, E., Paolella, L. M., Zhang, Z., Migaud, M. E., Rabinowitz, J. D., and Baur, J. A. (2018) Nicotinamide adenine dinucleotide is transported into mammalian mitochondria, Elife, 7, doi: 10.7554/eLife.33246.

67. Cambronne, X. A., Stewart, M. L., Kim, D., Jones-Brunette, A. M., Morgan, R. K., Farrens, D. L., Cohen, M. S., and Goodman, R. H. (2016) Biosensor reveals multiple sources for mitochondrial NAD(+), Science, 352, 1474-1477, doi: 10.1126/science.aad5168.

68. Sharma, S., Grudzien-Nogalska, E., Hamilton, K., Jiao, X., Yang, J., Tong, L., and Kiledjian, M. (2020) Mammalian Nudix proteins cleave nucleotide metabolite caps on RNAs, Nucleic Acids Res., 48, 6788-6798, doi: 10.1093/nar/gkaa402.

69. Wright, R. H., Lioutas, A., Le Dily, F., Soronellas, D., Pohl, A., Bonet, J., Nacht, A. S., Samino, S., Font-Mateu, J., Vicent, G. P., Wierer, M., Trabado, M. A., Schelhorn, C., Carolis, C., Macias, M. J., Yanes, O., Oliva, B., and Beato, M. (2016) ADP-ribose-derived nuclear ATP synthesis by NUDIX5 is required for chromatin remodeling, Science, 352, 1221-1225, doi: 10.1126/science.aad9335.

70. Gasmi, L., Cartwright, J. L., and McLennan, A. G. (1999) Cloning, expression and characterization of YSA1H, a human adenosine 5′-diphosphosugar pyrophosphatase possessing a MutT motif, Biochem. J., 344 Pt. 2, 331-337.

71. Page, B. D. G., Valerie, N. C. K., Wright, R. H. G., Wallner, O., Isaksson, R., Carter, M., Rudd, S. G., Loseva, O., Jemth, A. S., Almlof, I., Font-Mateu, J., Llona-Minguez, S., Baranczewski, P., Jeppsson, F., Homan, E., Almqvist, H., Axelsson, H., Regmi, S., Gustavsson, A. L., Lundback, T. et al. (2018) Targeted NUDT5 inhibitors block hormone signaling in breast cancer cells, Nat. Commun., 9, 250, doi: 10.1038/s41467-017-02293-7.

72. Yoon, B., Yang, E. G., and Kim, S. Y. (2018) The ADP-ribose reactive NUDIX hydrolase isoforms can modulate HIF-1alpha in cancer cells, Biochem. Biophys. Res. Commun., 504, 321-327, doi: 10.1016/j.bbrc.2018.08.185.

73. Formentini, L., Macchiarulo, A., Cipriani, G., Camaioni, E., Rapizzi, E., Pellicciari, R., Moroni, F., and Chiarugi, A. (2009) Poly(ADP-ribose) catabolism triggers AMP-dependent mitochondrial energy failure, J. Biol. Chem., 284, 17668-17676, doi: 10.1074/jbc.M109.002931.

74. Nury, H., Dahout-Gonzalez, C., Trezeguet, V., Lauquin, G. J., Brandolin, G., and Pebay-Peyroula, E. (2006) Relations between structure and function of the mitochondrial ADP/ATP carrier, Annu. Rev. Biochem., 75, 713-741, doi: 10.1146/annurev.biochem.75.103004.142747.

75. Hardie, D. G., Ross, F. A., and Hawley, S. A. (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis, Nat. Rev. Mol. Cell Biol., 13, 251-262, doi: 10.1038/nrm3311.

76. Gowans, G. J., Hawley, S. A., Ross, F. A., and Hardie, D. G. (2013) AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation, Cell Metab., 18, 556-566, doi: 10.1016/j.cmet.2013.08.019.

77. Rafty, L. A., Schmidt, M. T., Perraud, A. L., Scharenberg, A. M., and Denu, J. M. (2002) Analysis of O-acetyl-ADP-ribose as a target for Nudix ADP-ribose hydrolases, J. Biol. Chem., 277, 47114-47122, doi: 10.1074/jbc.M208997200.

78. Pickup, K. E., Pardow, F., Carbonell-Caballero, J., Lioutas, A., Villanueva-Canas, J. L., Wright, R. H. G., and Beato, M. (2019) Expression of oncogenic drivers in 3D cell culture depends on nuclear ATP synthesis by NUDT5, Cancers, 11, doi: 10.3390/cancers11091337.

79. Perraud, A. L., Shen, B., Dunn, C. A., Rippe, K., Smith, M. K., Bessman, M. J., Stoddard, B. L., and Scharenberg, A. M. (2003) NUDT9, a member of the Nudix hydrolase family, is an evolutionarily conserved mitochondrial ADP-ribose pyrophosphatase, J. Biol. Chem., 278, 1794-1801, doi: 10.1074/jbc.M205601200.

80. Ahuja, N., Schwer, B., Carobbio, S., Waltregny, D., North, B. J., Castronovo, V., Maechler, P., and Verdin, E. (2007) Regulation of insulin secretion by SIRT4, a mitochondrial ADP-ribosyltransferase, J. Biol. Chem., 282, 33583-33592, doi: 10.1074/jbc.M705488200.

81. Haigis, M. C., Mostoslavsky, R., Haigis, K. M., Fahie, K., Christodoulou, D. C., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Karow, M., Blander, G., Wolberger, C., Prolla, T. A., Weindruch, R., Alt, F. W., and Guarente, L. (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells, Cell, 126, 941-954, doi: 10.1016/j.cell.2006.06.057.

82. Zhang, J., Zhang, J., Benovic, J. L., Sugai, M., Wetzker, R., Gout, I., and Rittenhouse, S. E. (1995) Sequestration of a G-protein beta gamma subunit or ADP-ribosylation of Rho can inhibit thrombin-induced activation of platelet phosphoinositide 3-kinases, J. Biol. Chem., 270, 6589-6594, doi: 10.1074/jbc.270.12.6589.

83. Jacobson, E. L., Cervantes-Laurean, D., and Jacobson, M. K. (1997) ADP-ribose in glycation and glycoxidation reactions, Adv. Exp. Med. Biol., 419, 371-379, doi: 10.1007/978-1-4419-8632-0_49.

84. Perraud, A. L., Takanishi, C. L., Shen, B., Kang, S., Smith, M. K., Schmitz, C., Knowles, H. M., Ferraris, D., Li, W., Zhang, J., Stoddard, B. L., and Scharenberg, A. M. (2005) Accumulation of free ADP-ribose from mitochondria mediates oxidative stress-induced gating of TRPM2 cation channels, J. Biol. Chem., 280, 6138-6148, doi: 10.1074/jbc.M411446200.

85. Zharova, T. V., and Vinogradov, A. D. (1997) A competitive inhibition of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) by ADP-ribose, Biochim. Biophys. Acta, 1320, 256-264, doi: 10.1016/s0005-2728(97)00029-7.

86. Palazzo, L., Thomas, B., Jemth, A. S., Colby, T., Leidecker, O., Feijs, K. L., Zaja, R., Loseva, O., Puigvert, J. C., Matic, I., Helleday, T., and Ahel, I. (2015) Processing of protein ADP-ribosylation by Nudix hydrolases, Biochem. J., 468, 293-301, doi: 10.1042/BJ20141554.

87. Thirawatananond, P., McPherson, R. L., Malhi, J., Nathan, S., Lambrecht, M. J., Brichacek, M., Hergenrother, P. J., Leung, A. K. L., and Gabelli, S. B. (2019) Structural analyses of NudT16-ADP-ribose complexes direct rational design of mutants with improved processing of poly(ADP-ribosyl)ated proteins, Sci. Rep., 9, 5940, doi: 10.1038/s41598-019-39491-w.

88. Zhang, F., Lou, L., Peng, B., Song, X., Reizes, O., Almasan, A., and Gong, Z. (2020) Nudix hydrolase NUDT16 regulates 53BP1 protein by reversing 53BP1 ADP-ribosylation, Cancer Res., 80, 999-1010, doi: 10.1158/0008-5472.CAN-19-2205.

89. Ward, I. M., Minn, K., van Deursen, J., and Chen, J. (2003) p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice, Mol. Cell. Biol., 23, 2556-2563, doi: 10.1128/mcb.23.7.2556-2563.2003.

90. Belousova, E. A., Kutuzov, M. M., Ivankina, P. A., Ishchenko, A. A., and Lavrik, O. I. (2018) A new DNA break repair pathway involving PARP3 and base excision repair proteins, Dokl. Biochem. Biophys., 482, 233-237, doi: 10.1134/S1607672918050010.