A New Vision of Mitochondrial Unfolded Protein Response to the Sirtuin Family

Author(s): Huidan Weng, Yihong Ma, Lina Chen, Guoen Cai, Zhiting Chen, Shaochuan Zhang*, Qinyong Ye*

Journal Name: Current Neuropharmacology

Volume 18 , Issue 7 , 2020


DOI : 10.2174/1570159X18666200123165002

  Journal Home
Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Mitochondrial damage is involved in many pathophysiological processes, such as tumor development, metabolism, and neurodegenerative diseases. The mitochondrial unfolded protein response (mtUPR) is the first stress-protective response initiated by mitochondrial damage, and it repairs or clears misfolded proteins to alleviate this damage. Studies have confirmed that the sirtuin family is essential for the mitochondrial stress response; in particular, SIRT1, SIRT3, and SIRT7 participate in the mtUPR in different axes. This article summarizes the associations of sirtuins with the mtUPR as well as specific molecular targets related to the mtUPR in different disease models, which will provide new inspiration for studies on mitochondrial stress, mitochondrial function protection, and mitochondria-related diseases, such as neurodegenerative diseases.

Keywords: SIRT, mitochondrial unfolded protein response, mitochondrial stress, AMPK, FOXO3A, CHOP, PARP, mitochondrial protein quality control.

[1]
Hamon, M. P.; Bulteau, A. L.; Friguet, B. Mitochondrial proteases and protein quality control in ageing and longevity. Ageing Res Rev, 2015, 23(Pt A), 56-66.
[http://dx.doi.org/10.1016/j.arr.2014.12.010]
[2]
Liang, R.; Ghaffari, S. Mitochondria and FOXO3 in stem cell homeostasis, a window into hematopoietic stem cell fate determination. J. Bioenerg. Biomembr., 2017, 49(4), 343-346.
[http://dx.doi.org/10.1007/s10863-017-9719-7] [PMID: 28639090]
[3]
Naresh, N.U.; Haynes, C.M. Signaling and Regulation of the Mitochondrial Unfolded Protein Response. Cold Spring Harb. Perspect. Biol., 2019, 11(6)a033944
[http://dx.doi.org/10.1101/cshperspect.a033944] [PMID: 30617048]
[4]
Andreux, P.A.; Houtkooper, R.H.; Auwerx, J. Pharmacological approaches to restore mitochondrial function. Nat. Rev. Drug Discov., 2013, 12(6), 465-483.
[http://dx.doi.org/10.1038/nrd4023] [PMID: 23666487]
[5]
Mora, A.L.; Bueno, M.; Rojas, M. Mitochondria in the spotlight of aging and idiopathic pulmonary fibrosis. J. Clin. Invest., 2017, 127(2), 405-414.
[http://dx.doi.org/10.1172/JCI87440] [PMID: 28145905]
[6]
Jovaisaite, V.; Auwerx, J. The mitochondrial unfolded protein response—synchronizing genomes. Curr. Opin. Cell Biol., 2015, 33, 74-81.
[http://dx.doi.org/10.1016/j.ceb.2014.12.003] [PMID: 25543897]
[7]
Münch, C. The different axes of the mammalian mitochondrial unfolded protein response. BMC Biol., 2018, 16(1), 81.
[http://dx.doi.org/10.1186/s12915-018-0548-x] [PMID: 30049264]
[8]
Aldridge, J.E.; Horibe, T.; Hoogenraad, N.J. Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS One, 2007, 2(9)e874
[http://dx.doi.org/10.1371/journal.pone.0000874] [PMID: 17849004]
[9]
Pakos-Zebrucka, K.; Koryga, I.; Mnich, K.; Ljujic, M.; Samali, A.; Gorman, A.M. The integrated stress response. EMBO Rep., 2016, 17(10), 1374-1395.
[http://dx.doi.org/10.15252/embr.201642195] [PMID: 27629041]
[10]
Papa, L.; Germain, D. Estrogen receptor mediates a distinct mitochondrial unfolded protein response. J. Cell Sci., 2011, 124(Pt 9), 1396-1402.
[http://dx.doi.org/10.1242/jcs.078220] [PMID: 21486948]
[11]
Kenny, T.C.; Germain, D. From discovery of the CHOP axis and targeting ClpP to the identification of additional axes of the UPRmt driven by the estrogen receptor and SIRT3. J. Bioenerg. Biomembr., 2017, 49(4), 297-305.
[http://dx.doi.org/10.1007/s10863-017-9722-z] [PMID: 28799020]
[12]
Kang, B.H.; Plescia, J.; Song, H.Y.; Meli, M.; Colombo, G.; Beebe, K.; Scroggins, B.; Neckers, L.; Altieri, D.C. Combinatorial drug design targeting multiple cancer signaling networks controlled by mitochondrial Hsp90. J. Clin. Invest., 2009, 119(3), 454-464.
[http://dx.doi.org/10.1172/JCI37613] [PMID: 19229106]
[13]
Bernstein, S.H.; Venkatesh, S.; Li, M.; Lee, J.; Lu, B.; Hilchey, S.P.; Morse, K.M.; Metcalfe, H.M.; Skalska, J.; Andreeff, M.; Brookes, P.S.; Suzuki, C.K. The mitochondrial ATP-dependent Lon protease: a novel target in lymphoma death mediated by the synthetic triterpenoid CDDO and its derivatives. Blood, 2012, 119(14), 3321-3329.
[http://dx.doi.org/10.1182/blood-2011-02-340075] [PMID: 22323447]
[14]
Moon, J.; Kim, H.R.; Shin, M.G. Rejuvenating aged hematopoietic stem cells through improvement of mitochondrial function. Ann. Lab. Med., 2018, 38(5), 395-401.
[http://dx.doi.org/10.3343/alm.2018.38.5.395] [PMID: 29797808]
[15]
Lerrer, B.; Gertler, A.A.; Cohen, H.Y. The complex role of SIRT6 in carcinogenesis. Carcinogenesis, 2016, 37(2), 108-118.
[http://dx.doi.org/10.1093/carcin/bgv167] [PMID: 26717993]
[16]
Wątroba, M.; Dudek, I.; Skoda, M.; Stangret, A.; Rzodkiewicz, P.; Szukiewicz, D. Sirtuins, epigenetics and longevity. Ageing Res. Rev., 2017, 40, 11-19.
[http://dx.doi.org/10.1016/j.arr.2017.08.001] [PMID: 28789901]
[17]
Rose, G.; Santoro, A.; Salvioli, S. Mitochondria and mitochondria-induced signalling molecules as longevity determinants. BMC Biol., 2017, 16(1), 81.
[http://dx.doi.org/10.1016/j.mad.2016.12.002]
[18]
Dahlmans, D.; Houzelle, A.; Schrauwen, P.; Hoeks, J. Mitochondrial dynamics, quality control and miRNA regulation in skeletal muscle: implications for obesity and related metabolic disease. Clin. Sci. (Lond.), 2016, 130(11), 843-852.
[http://dx.doi.org/10.1042/CS20150780] [PMID: 27129097]
[19]
Mendelsohn, A.R.; Larrick, J.W. The NAD+/PARP1/SIRT1 Axis in Aging. Rejuvenation Res., 2017, 20(3), 244-247.
[http://dx.doi.org/10.1089/rej.2017.1980] [PMID: 28537485]
[20]
Gariani, K.; Menzies, K.J.; Ryu, D.; Wegner, C.J.; Wang, X.; Ropelle, E.R.; Moullan, N.; Zhang, H.; Perino, A.; Lemos, V.; Kim, B.; Park, Y.K.; Piersigilli, A.; Pham, T.X.; Yang, Y.; Ku, C.S.; Koo, S.I.; Fomitchova, A.; Cantó, C.; Schoonjans, K.; Sauve, A.A.; Lee, J.Y.; Auwerx, J. Eliciting the mitochondrial unfolded protein response by nicotinamide adenine dinucleotide repletion reverses fatty liver disease in mice. Hepatology, 2016, 63(4), 1190-1204.
[http://dx.doi.org/10.1002/hep.28245] [PMID: 26404765]
[21]
Jukarainen, S.; Heinonen, S.; Rämö, J.T.; Rinnankoski-Tuikka, R.; Rappou, E.; Tummers, M.; Muniandy, M.; Hakkarainen, A.; Lundbom, J.; Lundbom, N.; Kaprio, J.; Rissanen, A.; Pirinen, E.; Pietiläinen, K.H.; Obesity Is Associated With Low, N.A.D. Obesity is associated with low nad(+)/sirt pathway expression in adipose tissue of bmi-discordant monozygotic twins. J. Clin. Endocrinol. Metab., 2016, 101(1), 275-283.
[http://dx.doi.org/10.1210/jc.2015-3095] [PMID: 26574954]
[22]
O’Callaghan, C.; Vassilopoulos, A. Sirtuins at the crossroads of stemness, aging, and cancer. Aging Cell, 2017, 16(6), 1208-1218.
[http://dx.doi.org/10.1111/acel.12685] [PMID: 28994177]
[23]
Zhang, H.; Menzies, K.J.; Auwerx, J. The role of mitochondria in stem cell fate and aging. Development, 2018, 145(8)dev143420
[http://dx.doi.org/10.1242/dev.143420] [PMID: 29654217]
[24]
Mouchiroud, L.; Houtkooper, R.H.; Moullan, N.; Katsyuba, E.; Ryu, D.; Cantó, C.; Mottis, A.; Jo, Y.S.; Viswanathan, M.; Schoonjans, K.; Guarente, L.; Auwerx, J. The NAD(+)/Sirtuin pathway modulates longevity through activation of mitochondrial UPR and FOXO signaling. Cell, 2013, 154(2), 430-441.
[http://dx.doi.org/10.1016/j.cell.2013.06.016] [PMID: 23870130]
[25]
Imai, S.; Guarente, L. NAD+ and sirtuins in aging and disease. Trends Cell Biol., 2014, 24(8), 464-471.
[http://dx.doi.org/10.1016/j.tcb.2014.04.002] [PMID: 24786309]
[26]
Cho, E.H. SIRT3 as a Regulator of non-alcoholic fatty liver disease. J. Lifestyle Med., 2014, 4(2), 80-85.
[http://dx.doi.org/10.15280/jlm.2014.4.2.80] [PMID: 26064858]
[27]
Liu, J.P.; Chen, R. Stressed SIRT7: facing a crossroad of senescence and immortality. Clin. Exp. Pharmacol. Physiol., 2015, 42(6), 567-569.
[http://dx.doi.org/10.1111/1440-1681.12423] [PMID: 25970806]
[28]
Jensen, M.B.; Jasper, H. Mitochondrial proteostasis in the control of aging and longevity. Cell Metab., 2014, 20(2), 214-225.
[http://dx.doi.org/10.1016/j.cmet.2014.05.006] [PMID: 24930971]
[29]
Imai, S.I.; Guarente, L. It takes two to tango: NAD+ and sirtuins in aging/longevity control. Aging Mech. Dis., 2016, 2, 16017.
[http://dx.doi.org/10.1038/npjamd.2016.17] [PMID: 28721271]
[30]
Calabrese, V.; Cornelius, C.; Mancuso, C.; Pennisi, G.; Calafato, S.; Bellia, F.; Bates, T.E.; Giuffrida Stella, A.M.; Schapira, T.; Dinkova Kostova, A.T.; Rizzarelli, E. Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem. Res., 2008, 33(12), 2444-2471.
[http://dx.doi.org/10.1007/s11064-008-9775-9] [PMID: 18629638]
[31]
Pillai, V.B.; Sundaresan, N.R.; Jeevanandam, V.; Gupta, M.P. Mitochondrial SIRT3 and heart disease. Cardiovasc. Res., 2010, 88(2), 250-256.
[http://dx.doi.org/10.1093/cvr/cvq250] [PMID: 20685942]
[32]
Houtkooper, R.H.; Mouchiroud, L.; Ryu, D.; Moullan, N.; Katsyuba, E.; Knott, G.; Williams, R.W.; Auwerx, J. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature, 2013, 497(7450), 451-457.
[http://dx.doi.org/10.1038/nature12188] [PMID: 23698443]
[33]
Pirinen, E.; Cantó, C.; Jo, Y.S.; Morato, L.; Zhang, H.; Menzies, K.J.; Williams, E.G.; Mouchiroud, L.; Moullan, N.; Hagberg, C.; Li, W.; Timmers, S.; Imhof, R.; Verbeek, J.; Pujol, A.; van Loon, B.; Viscomi, C.; Zeviani, M.; Schrauwen, P.; Sauve, A.A.; Schoonjans, K.; Auwerx, J. Pharmacological Inhibition of poly(ADP-ribose) polymerases improves fitness and mitochondrial function in skeletal muscle. Cell Metab., 2014, 19(6), 1034-1041.
[http://dx.doi.org/10.1016/j.cmet.2014.04.002] [PMID: 24814482]
[34]
Gao, Z.; Ye, J. Inhibition of transcriptional activity of c-JUN by SIRT1. Biochem. Biophys. Res. Commun., 2008, 376(4), 793-796.
[http://dx.doi.org/10.1016/j.bbrc.2008.09.079] [PMID: 18823944]
[35]
Luna, A.; Aladjem, M.I.; Kohn, K.W. SIRT1/PARP1 crosstalk: connecting DNA damage and metabolism. Genome Integr., 2013, 4(1), 6.
[http://dx.doi.org/10.1186/2041-9414-4-6] [PMID: 24360018]
[36]
Mikó, E.; Kovács, T.; Fodor, T.; Bai, P. Methods to Assess the Role of Poly(ADP-Ribose) Polymerases in Regulating Mitochondrial Oxidation. Methods Mol. Biol., 2017, 1608, 185-200.
[http://dx.doi.org/10.1007/978-1-4939-6993-7_13] [PMID: 28695511]
[37]
Cantó, C.; Auwerx, J. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol., 2009, 20(2), 98-105.
[http://dx.doi.org/10.1097/MOL.0b013e328328d0a4] [PMID: 19276888]
[38]
De, I.; Dogra, N.; Singh, S. The mitochondrial unfolded protein response: role in cellular homeostasis and disease. Curr. Mol. Med., 2017, 17(9), 587-597.
[http://dx.doi.org/10.2174/1566524018666180308110130] [PMID: 29521229]
[39]
Ge, J.; Zhang, C.; Sun, Y-C.; Zhang, Q.; Lv, M-W.; Guo, K.; Li, J-L. Cadmium exposure triggers mitochondrial dysfunction and oxidative stress in chicken (Gallus gallus) kidney via mitochondrial UPR inhibition and Nrf2-mediated antioxidant defense activation. Sci. Total Environ., 2019, 689, 1160-1171.
[http://dx.doi.org/10.1016/j.scitotenv.2019.06.405] [PMID: 31466156]
[40]
Lehmann, S.; Costa, A.C.; Celardo, I.; Loh, S.H.; Martins, L.M. Parp mutations protect against mitochondrial dysfunction and neurodegeneration in a PARKIN model of Parkinson’s disease. Cell Death Dis., 2016, 7e2166
[http://dx.doi.org/10.1038/cddis.2016.72] [PMID: 27031963]
[41]
Tan, M.; Tang, C.; Zhang, Y.; Cheng, Y.; Cai, L.; Chen, X.; Gao, Y.; Deng, Y.; Pan, M. SIRT1/PGC-1α signaling protects hepatocytes against mitochondrial oxidative stress induced by bile acids. Free Radic. Res., 2015, 49(8), 935-945.
[http://dx.doi.org/10.3109/10715762.2015.1016020] [PMID: 25789761]
[42]
Wang, S.; Wan, T.; Ye, M.; Qiu, Y.; Pei, L.; Jiang, R.; Pang, N.; Huang, Y.; Liang, B.; Ling, W.; Lin, X.; Zhang, Z.; Yang, L. Nicotinamide riboside attenuates alcohol induced liver injuries via activation of SirT1/PGC-1α/mitochondrial biosynthesis pathway. Redox Biol., 2018, 17, 89-98.
[http://dx.doi.org/10.1016/j.redox.2018.04.006] [PMID: 29679894]
[43]
Lagouge, M.; Argmann, C.; Gerhart-Hines, Z.; Meziane, H.; Lerin, C.; Daussin, F.; Messadeq, N.; Milne, J.; Lambert, P.; Elliott, P.; Geny, B.; Laakso, M.; Puigserver, P.; Auwerx, J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell, 2006, 127(6), 1109-1122.
[http://dx.doi.org/10.1016/j.cell.2006.11.013] [PMID: 17112576]
[44]
Mihaela, T.; Savu, D.I.; Moisoi, N. Intracellular and intercellular signalling mechanisms following DNA damage are modulated by pink1. Oxid. Med. Cell. Longev., 2018, 2018, 1-15.
[45]
Bai, P.; Nagy, L.; Fodor, T.; Liaudet, L.; Pacher, P. Poly(ADP-ribose) polymerases as modulators of mitochondrial activity. Trends Endocrinol. Metab., 2015, 26(2), 75-83.
[http://dx.doi.org/10.1016/j.tem.2014.11.003] [PMID: 25497347]
[46]
Tang, B.L. Sirt1 and the Mitochondria. Mol. Cells, 2016, 39(2), 87-95.
[http://dx.doi.org/10.14348/molcells.2016.2318] [PMID: 26831453]
[47]
Price, N.L.; Gomes, A.P.; Ling, A.J.; Duarte, F.V.; Martin-Montalvo, A.; North, B.J.; Agarwal, B.; Ye, L.; Ramadori, G.; Teodoro, J.S.; Hubbard, B.P.; Varela, A.T.; Davis, J.G.; Varamini, B.; Hafner, A.; Moaddel, R.; Rolo, A.P.; Coppari, R.; Palmeira, C.M.; de Cabo, R.; Baur, J.A.; Sinclair, D.A. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab., 2012, 15(5), 675-690.
[http://dx.doi.org/10.1016/j.cmet.2012.04.003] [PMID: 22560220]
[48]
Gomes, A.P.; Price, N.L.; Ling, A.J.Y.; Moslehi, J.J.; Montgomery, M.K.; Rajman, L.; White, J.P.; Teodoro, J.S.; Wrann, C.D.; Hubbard, B.P.; Mercken, E.M.; Palmeira, C.M.; de Cabo, R.; Rolo, A.P.; Turner, N.; Bell, E.L.; Sinclair, D.A.; Declining, N.A.D. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell, 2013, 155(7), 1624-1638.
[http://dx.doi.org/10.1016/j.cell.2013.11.037] [PMID: 24360282]
[49]
Kitada, M.; Ogura, Y.; Monno, I.; Koya, D. Sirtuins and type 2 diabetes: role in inflammation, oxidative stress, and mitochondrial function. Front. Endocrinol. (Lausanne), 2019, 10, 187-187.
[http://dx.doi.org/10.3389/fendo.2019.00187] [PMID: 30972029]
[50]
Singh, C.K.; Chhabra, G.; Ndiaye, M.A.; Garcia-Peterson, L.M.; Mack, N.J.; Ahmad, N. The role of sirtuins in antioxidant and redox signaling. Antioxid. Redox Signal., 2018, 28(8), 643-661.
[http://dx.doi.org/10.1089/ars.2017.7290] [PMID: 28891317]
[51]
Liu, G.; Park, S.H.; Imbesi, M.; Nathan, W.J.; Zou, X.; Zhu, Y.; Jiang, H.; Parisiadou, L.; Gius, D. Loss of NAD-dependent protein deacetylase sirtuin-2 alters mitochondrial protein acetylation and dysregulates mitophagy. Antioxid. Redox Signal., 2017, 26(15), 849-863.
[http://dx.doi.org/10.1089/ars.2016.6662] [PMID: 27460777]
[52]
Xu, W-N.; Yang, R-Z.; Zheng, H-L.; Yu, W.; Zheng, X-F.; Li, B.; Jiang, S-D.; Jiang, L-S. PGC-1α acts as an mediator of Sirtuin2 to protect annulus fibrosus from apoptosis induced by oxidative stress through restraining mitophagy. Int. J. Biol. Macromol., 2019, 136, 1007-1017.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.06.163] [PMID: 31238070]
[53]
Zhou, S.; Tang, X.; Chen, H.Z. Sirtuins and insulin resistance. Front. Endocrinol., 2018, 9, 748.
[http://dx.doi.org/10.3389/fendo.2018.00748] [PMID: 30574122]
[54]
Xu, D.; Wu, L.; Jiang, X.; Yang, L.; Cheng, J.; Chen, H.; Hua, R.; Geng, G.; Yang, L.; Li, Q. SIRT2 inhibition results in meiotic arrest, mitochondrial dysfunction, and disturbance of redox homeostasis during bovine oocyte maturation. Int. J. Mol. Sci., 2019, 20(6)E1365
[http://dx.doi.org/10.3390/ijms20061365] [PMID: 30889926]
[55]
Pehar, M.; Harlan, B.A.; Killoy, K.M.; Vargas, M.R. Nicotinamide adenine dinucleotide metabolism and neurodegeneration. Antioxid. Redox Signal., 2018, 28(18), 1652-1668.
[http://dx.doi.org/10.1089/ars.2017.7145] [PMID: 28548540]
[56]
Gomes, P.; Leal, H.; Mendes, A.F.; Reis, F.; Cavadas, C. Dichotomous Sirtuins: Implications for drug discovery in neurodegenerative and cardiometabolic diseases. Trends Pharmacol. Sci., 2019, 40(12), 1021-1039.
[http://dx.doi.org/10.1016/j.tips.2019.09.003] [PMID: 31704173]
[57]
Lu, Z.; Chen, Y.; Aponte, A.M.; Battaglia, V.; Gucek, M.; Sack, M.N. Prolonged fasting identifies heat shock protein 10 as a Sirtuin 3 substrate: elucidating a new mechanism linking mitochondrial protein acetylation to fatty acid oxidation enzyme folding and function. J. Biol. Chem., 2015, 290(4), 2466-2476.
[http://dx.doi.org/10.1074/jbc.M114.606228] [PMID: 25505263]
[58]
Papa, L.; Germain, D. SirT3 regulates the mitochondrial unfolded protein response. Mol. Cell. Biol., 2014, 34(4), 699-710.
[http://dx.doi.org/10.1128/MCB.01337-13] [PMID: 24324009]
[59]
Srivastava, S. Emerging therapeutic roles for NAD(+) metabolism in mitochondrial and age-related disorders. Clin. Transl. Med., 2016, 5(1), 25-25.
[http://dx.doi.org/10.1186/s40169-016-0104-7] [PMID: 27465020]
[60]
Kenny, T.C.; Craig, A.J.; Villanueva, A.; Germain, D. Mitohormesis primes tumor invasion and metastasis. Cell Rep., 2019, 27(8), 2292-2303.e6.
[http://dx.doi.org/10.1016/j.celrep.2019.04.095] [PMID: 31116976]
[61]
Kenny, T.C.; Hart, P.; Ragazzi, M.; Sersinghe, M.; Chipuk, J.; Sagar, M.A.K.; Eliceiri, K.W.; LaFramboise, T.; Grandhi, S.; Santos, J.; Riar, A.K.; Papa, L.; D’Aurello, M.; Manfredi, G.; Bonini, M.G.; Germain, D. Selected mitochondrial DNA landscapes activate the SIRT3 axis of the UPRmt to promote metastasis. Oncogene, 2017, 36(31), 4393-4404.
[http://dx.doi.org/10.1038/onc.2017.52] [PMID: 28368421]
[62]
Chang, G.; Chen, Y.; Zhang, H.; Zhou, W. Trans sodium crocetinate alleviates ischemia/reperfusion-induced myocardial oxidative stress and apoptosis via the SIRT3/FOXO3a/SOD2 signaling pathway. Int. Immunopharmacol., 2019, 71, 361-371.
[http://dx.doi.org/10.1016/j.intimp.2019.03.056] [PMID: 30952100]
[63]
He, J.; Liu, X.; Su, C.; Wu, F.; Sun, J.; Zhang, J.; Yang, X.; Zhang, C.; Zhou, Z.; Zhang, X.; Lin, X.; Tao, J. Inhibition of mitochondrial oxidative damage improves reendothelialization capacity of endothelial progenitor cells via sirt3 (sirtuin 3)-enhanced sod2 (superoxide dismutase 2) deacetylation in hypertension. Arterioscler. Thromb. Vasc. Biol., 2019, 39(8), 1682-1698.
[http://dx.doi.org/10.1161/ATVBAHA.119.312613] [PMID: 31189433]
[64]
Gao, J.; Feng, Z.; Wang, X.; Zeng, M.; Liu, J.; Han, S.; Xu, J.; Chen, L.; Cao, K.; Long, J.; Li, Z.; Shen, W.; Liu, J. SIRT3/SOD2 maintains osteoblast differentiation and bone formation by regulating mitochondrial stress. Cell Death Differ., 2018, 25(2), 229-240.
[http://dx.doi.org/10.1038/cdd.2017.144] [PMID: 28914882]
[65]
Gomez, M.; Germain, D. Cross talk between SOD1 and the mitochondrial UPR in cancer and neurodegeneration. Mol. Cell. Neurosci., 2019, 98, 12-18.
[http://dx.doi.org/10.1016/j.mcn.2019.04.003] [PMID: 31028834]
[66]
Xu, M.; Xue, R.Q.; Lu, Y.; Yong, S.Y.; Wu, Q.; Cui, Y.L.; Zuo, X.T.; Yu, X.J.; Zhao, M.; Zang, W.J. Choline ameliorates cardiac hypertrophy by regulating metabolic remodelling and UPRmt through SIRT3-AMPK pathway. Cardiovasc. Res., 2019, 115(3), 530-545.
[http://dx.doi.org/10.1093/cvr/cvy217] [PMID: 30165480]
[67]
Lin, S.; Xing, H.; Zang, T.; Ruan, X.; Wo, L.; He, M. Sirtuins in mitochondrial stress: Indispensable helpers behind the scenes. Ageing Res. Rev., 2018, 44, 22-32.
[http://dx.doi.org/10.1016/j.arr.2018.03.006] [PMID: 29580919]
[68]
Bergström, S.; Danielsson, H.; Samuelsson, B. The enzymatic formation of prostaglandin E2 from arachidonic acid prostaglandins and related factors 32. Biochimica et Biophysica Acta (BBA) -. General Subjects, 1964, 90(1), 207-210.
[http://dx.doi.org/10.1016/0304-4165(64)90145-X]
[69]
Zhou, L.; Wang, F.; Sun, R.; Chen, X.; Zhang, M.; Xu, Q.; Wang, Y.; Wang, S.; Xiong, Y.; Guan, K-L.; Yang, P.; Yu, H.; Ye, D. SIRT5 promotes IDH2 desuccinylation and G6PD deglutarylation to enhance cellular antioxidant defense. EMBO Rep., 2016, 17(6), 811-822.
[http://dx.doi.org/10.15252/embr.201541643] [PMID: 27113762]
[70]
Ryu, D.; Jo, Y.S.; Lo Sasso, G.; Stein, S.; Zhang, H.; Perino, A.; Lee, J.U.; Zeviani, M.; Romand, R.; Hottiger, M.O.; Schoonjans, K.; Auwerx, J. A SIRT7-dependent acetylation switch of GABPβ1 controls mitochondrial function. Cell Metab., 2014, 20(5), 856-869.
[http://dx.doi.org/10.1016/j.cmet.2014.08.001] [PMID: 25200183]
[71]
Li, L.; Shi, L.; Yang, S.; Yan, R.; Zhang, D.; Yang, J.; He, L.; Li, W.; Yi, X.; Sun, L.; Liang, J.; Cheng, Z.; Shi, L.; Shang, Y.; Yu, W. SIRT7 is a histone desuccinylase that functionally links to chromatin compaction and genome stability. Nat. Commun., 2016, 7, 12235-12235.
[http://dx.doi.org/10.1038/ncomms12235] [PMID: 27436229]
[72]
Fang, E.F.; Scheibye-Knudsen, M.; Chua, K.F.; Mattson, M.P.; Croteau, D.L.; Bohr, V.A. Nuclear DNA damage signalling to mitochondria in ageing. Nat. Rev. Mol. Cell Biol., 2016, 17(5), 308-321.
[http://dx.doi.org/10.1038/nrm.2016.14] [PMID: 26956196]
[73]
Mohrin, M.; Shin, J.; Liu, Y.; Brown, K.; Luo, H.; Xi, Y.; Haynes, C.M.; Chen, D. Stem cell aging. A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science, 2015, 347(6228), 1374-1377.
[http://dx.doi.org/10.1126/science.aaa2361] [PMID: 25792330]
[74]
Mohrin, M.; Chen, D. The mitochondrial metabolic checkpoint and aging of hematopoietic stem cells. Curr. Opin. Hematol., 2016, 23(4), 318-324.
[http://dx.doi.org/10.1097/MOH.0000000000000244] [PMID: 26945277]
[75]
Yang, Y.; Cheung, H.H.; Tu, J.; Miu, K.K.; Chan, W.Y. New insights into the unfolded protein response in stem cells. Oncotarget, 2016, 7(33), 54010-54027.
[http://dx.doi.org/10.18632/oncotarget.9833] [PMID: 27304053]
[76]
Ajami, M.; Pazoki-Toroudi, H.; Amani, H.; Nabavi, S.F.; Braidy, N.; Vacca, R.A.; Atanasov, A.G.; Mocan, A.; Nabavi, S.M. Therapeutic role of sirtuins in neurodegenerative disease and their modulation by polyphenols. Neurosci. Biobehav. Rev., 2017, 73, 39-47.
[http://dx.doi.org/10.1016/j.neubiorev.2016.11.022] [PMID: 27914941]
[77]
Ocampo, A.; Izpisua Belmonte, J.C. Stem cells. Holding your breath for longevity. Science, 2015, 347(6228), 1319-1320.
[http://dx.doi.org/10.1126/science.aaa9608] [PMID: 25792319]
[78]
He, C.; Hart, P.C.; Germain, D.; Bonini, M.G. SOD2 and the mitochondrial upr: partners regulating cellular phenotypic transitions. Trends Biochem. Sci., 2016, 41(7), 568-577.
[http://dx.doi.org/10.1016/j.tibs.2016.04.004] [PMID: 27180143]
[79]
Tang, B.L. SIRT7 and hepatic lipid metabolism. Front. Cell Dev. Biol., 2015, 3, 1-1.
[http://dx.doi.org/10.3389/fcell.2015.00001] [PMID: 25654079]
[80]
Chiang, W-C.; Tishkoff, D.X.; Yang, B.; Wilson-Grady, J.; Yu, X.; Mazer, T.; Eckersdorff, M.; Gygi, S.P.; Lombard, D.B.; Hsu, A-L.C. C. elegans SIRT6/7 homolog SIR-2.4 promotes DAF-16 relocalization and function during stress. PLoS Genet., 2012, 8(9), e1002948-e1002948.
[http://dx.doi.org/10.1371/journal.pgen.1002948] [PMID: 23028355]
[81]
Haigis, M.C.; Guarente, L.P. Mammalian sirtuins--emerging roles in physiology, aging, and calorie restriction. Genes Dev., 2006, 20(21), 2913-2921.
[http://dx.doi.org/10.1101/gad.1467506] [PMID: 17079682]
[82]
Lu, S-P.; Lin, S-J. Regulation of yeast sirtuins by NAD(+) metabolism and calorie restriction. Biochim. Biophys. Acta, 2010, 1804(8), 1567-1575.
[http://dx.doi.org/10.1016/j.bbapap.2009.09.030] [PMID: 19818879]
[83]
Dai, H.; Sinclair, D.A.; Ellis, J.L.; Steegborn, C. Sirtuin activators and inhibitors: Promises, achievements, and challenges. Pharmacol. Ther., 2018, 188, 140-154.
[http://dx.doi.org/10.1016/j.pharmthera.2018.03.004] [PMID: 29577959]
[84]
Wood, J.G.; Schwer, B.; Wickremesinghe, P.C.; Hartnett, D.A.; Burhenn, L.; Garcia, M.; Li, M.; Verdin, E.; Helfand, S.L. Sirt4 is a mitochondrial regulator of metabolism and lifespan in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 2018, 115(7)(Suppl. 1), 1564-1569.
[http://dx.doi.org/10.1073/pnas.1720673115] [PMID: 29378963]
[85]
Fusco, S.; Maulucci, G.; Pani, G. Sirt1: def-eating senescence? Cell Cycle, 2012, 11(22), 4135-4146.
[http://dx.doi.org/10.4161/cc.22074] [PMID: 22983125]
[86]
Chang, H.C.; Guarente, L. SIRT1 and other sirtuins in metabolism. Trends Endocrinol. Metab., 2014, 25(3), 138-145.
[http://dx.doi.org/10.1016/j.tem.2013.12.001] [PMID: 24388149]
[87]
Teng, Y.B.; Jing, H.; Aramsangtienchai, P.; He, B.; Khan, S.; Hu, J.; Lin, H.; Hao, Q. Efficient demyristoylase activity of SIRT2 revealed by kinetic and structural studies. Sci. Rep., 2015, 5, 8529.
[http://dx.doi.org/10.1038/srep08529] [PMID: 25704306]
[88]
Lombard, D.B.; Tishkoff, D.X.; Bao, J. Mitochondrial sirtuins in the regulation of mitochondrial activity and metabolic adaptation. Handb. Exp. Pharmacol., 2011, 206, 163-188.
[http://dx.doi.org/10.1007/978-3-642-21631-2_8] [PMID: 21879450]
[89]
Zhu, Y.; Yan, Y.; Principe, D.R.; Zou, X.; Vassilopoulos, A.; Gius, D. SIRT3 and SIRT4 are mitochondrial tumor suppressor proteins that connect mitochondrial metabolism and carcinogenesis. Cancer Metab., 2014, 2, 15-15.
[http://dx.doi.org/10.1186/2049-3002-2-15] [PMID: 25332769]
[90]
Hirschey, M.D.; Zhao, Y. Metabolic Regulation by lysine malonylation, succinylation, and glutarylation. Mol. Cell. Proteomics, 2015, 14(9), 2308-2315.
[http://dx.doi.org/10.1074/mcp.R114.046664] [PMID: 25717114]
[91]
Tsai, Y-C.; Greco, T.M.; Cristea, I.M. Sirtuin 7 plays a role in ribosome biogenesis and protein synthesis. Mol. Cell. Proteomics, 2014, 13(1), 73-83.
[http://dx.doi.org/10.1074/mcp.M113.031377] [PMID: 24113281]
[92]
Jiang, H.; Khan, S.; Wang, Y.; Charron, G.; He, B.; Sebastian, C.; Du, J.; Kim, R.; Ge, E.; Mostoslavsky, R.; Hang, H.C.; Hao, Q.; Lin, H. SIRT6 regulates TNF-α secretion through hydrolysis of long-chain fatty acyl lysine. Nature, 2013, 496(7443), 110-113.
[http://dx.doi.org/10.1038/nature12038] [PMID: 23552949]
[93]
Kupis, W.; Pałyga, J.; Tomal, E.; Niewiadomska, E. The role of sirtuins in cellular homeostasis. J. Physiol. Biochem., 2016, 72(3), 371-380.
[http://dx.doi.org/10.1007/s13105-016-0492-6] [PMID: 27154583]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 18
ISSUE: 7
Year: 2020
Published on: 28 July, 2020
Page: [613 - 623]
Pages: 11
DOI: 10.2174/1570159X18666200123165002
Price: $65

Article Metrics

PDF: 25
HTML: 3
PRC: 1



Related Article(s)

Most Downloaded Article(s)