Acknowledgement
This work was supported by the Basic Study and Interdisciplinary R&D Foundation Fund from the University of Seoul (2021-2022) granted to E.S.H.
References
- Ahmad, I.M., Aykin-Burns, N., Sim, J.E., Walsh, S.A., Higashikubo, R., Buettner, G.R., Venkataraman, S., Mackey, M.A., Flanagan, S.W., Oberley, L.W., et al. (2005). Mitochondrial O2*- and H2O2 mediate glucose deprivation-induced stress in human cancer cells. J. Biol. Chem. 280, 4254-4263. https://doi.org/10.1074/jbc.M411662200
- Alexander, A. and Walker, C.L. (2010). Differential localization of ATM is correlated with activation of distinct downstream signaling pathways. Cell Cycle 9, 3685-3686. https://doi.org/10.4161/cc.9.18.13253
- Alzamora, R., Thali, R.F., Gong, F., Smolak, C., Li, H., Baty, C.J., Bertrand, C.A., Auchli, Y., Brunisholz, R.A., Neumann, D., et al. (2010). PKA regulates vacuolar H+-ATPase localization and activity via direct phosphorylation of the a subunit in kidney cells. J. Biol. Chem. 285, 24676-24685. https://doi.org/10.1074/jbc.M110.106278
- Aman, Y., Schmauck-Medina, T., Hansen, M., Morimoto, R.I., Simon, A.K., Bjedov, I., Palikaras, K., Simonsen, A., Johansen, T., Tavernarakis, N., et al. (2021). Autophagy in healthy aging and disease. Nat. Aging 1, 634-650. https://doi.org/10.1038/s43587-021-00098-4
- Ashrafi, G. and Schwarz, T.L. (2013). The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 20, 31-42. https://doi.org/10.1038/cdd.2012.81
- Brenmoehl, J. and Hoeflich, A. (2013). Dual control of mitochondrial biogenesis by sirtuin 1 and sirtuin 3. Mitochondrion 13, 755-761. https://doi.org/10.1016/j.mito.2013.04.002
- Buzzai, M., Bauer, D.E., Jones, R.G., Deberardinis, R.J., Hatzivassiliou, G., Elstrom, R.L., and Thompson, C.B. (2005). The glucose dependence of Akttransformed cells can be reversed by pharmacologic activation of fatty acid beta-oxidation. Oncogene 24, 4165-4173. https://doi.org/10.1038/sj.onc.1208622
- Chan, C.Y. and Parra, K.J. (2014). Yeast phosphofructokinase-1 subunit Pfk2p is necessary for pH homeostasis and glucose-dependent vacuolar ATPase reassembly. J. Biol. Chem. 289, 19448-19457. https://doi.org/10.1074/jbc.M114.569855
- Curnock, R., Yalci, K., Palmfeldt, J., Jaattela, M., Liu, B., and Carroll, B. (2023). TFEB-dependent lysosome biogenesis is required for senescence. EMBO J. 42, e111241.
- Dehay, B., Martinez-Vicente, M., Ramirez, A., Perier, C., Klein, C., Vila, M., and Bezard, E. (2012). Lysosomal dysfunction in Parkinson disease: ATP13A2 gets into the groove. Autophagy 8, 1389-1391. https://doi.org/10.4161/auto.21011
- Fethiere, J., Venzke, D., Diepholz, M., Seybert, A., Geerlof, A., Gentzel, M., Wilm, M., and Bottcher, B. (2004). Building the stator of the yeast vacuolarATPase: specific interaction between subunits E and G. J. Biol. Chem. 279, 40670-40676. https://doi.org/10.1074/jbc.M407086200
- Foster, D.W. (2012). Malonyl-CoA: the regulator of fatty acid synthesis and oxidation. J. Clin. Invest. 122, 1958-1959. https://doi.org/10.1172/JCI63967
- Hardie, D.G. (2003). Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144, 5179-5183. https://doi.org/10.1210/en.2003-0982
- Hariharan, N., Maejima, Y., Nakae, J., Paik, J., Depinho, R.A., and Sadoshima, J. (2010). Deacetylation of FoxO by Sirt1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ. Res. 107, 1470-1482. https://doi.org/10.1161/CIRCRESAHA.110.227371
- He, Y., She, H., Zhang, T., Xu, H., Cheng, L., Yepes, M., Zhao, Y., and Mao, Z. (2018). p38 MAPK inhibits autophagy and promotes microglial inflammatory responses by phosphorylating ULK1. J. Cell Biol. 217, 315-328. https://doi.org/10.1083/jcb.201701049
- Huang, R., Xu, Y., Wan, W., Shou, X., Qian, J., You, Z., Liu, B., Chang, C., Zhou, T., Lippincott-Schwartz, J., et al. (2015). Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol. Cell 57, 456-466. https://doi.org/10.1016/j.molcel.2014.12.013
- Ikenaka, K., Kawai, K., Katsuno, M., Huang, Z., Jiang, Y.M., Iguchi, Y., Kobayashi, K., Kimata, T., Waza, M., Tanaka, F., et al. (2013). dnc-1/dynactin 1 knockdown disrupts transport of autophagosomes and induces motor neuron degeneration. PLoS One 8, e54511.
- Jang, S.Y., Kang, H.T., and Hwang, E.S. (2012). Nicotinamide-induced mitophagy: event mediated by high NAD+/NADH ratio and SIRT1 protein activation. J. Biol. Chem. 287, 19304-19314. https://doi.org/10.1074/jbc.M112.363747
- Jelluma, N., Yang, X., Stokoe, D., Evan, G.I., Dansen, T.B., and Haas-Kogan, D.A. (2006). Glucose withdrawal induces oxidative stress followed by apoptosis in glioblastoma cells but not in normal human astrocytes. Mol. Cancer Res. 4, 319-330. https://doi.org/10.1158/1541-7786.MCR-05-0061
- Jung, T., Bader, N., and Grune, T. (2007). Lipofuscin: formation, distribution, and metabolic consequences. Ann. N. Y. Acad. Sci. 1119, 97-111. https://doi.org/10.1196/annals.1404.008
- Juricic, P., Lu, Y.X., Leech, T., Drews, L.F., Paulitz, J., Lu, J., Nespital, T., Azami, S., Regan, J.C., Funk, E., et al. (2022). Long-lasting geroprotection from brief rapamycin treatment in early adulthood by persistently increased intestinal autophagy. Nat. Aging 2, 824-836. https://doi.org/10.1038/s43587-022-00278-w
- Kane, P.M. (1995). Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo. J. Biol. Chem. 270, 17025-17032. https://doi.org/10.1016/S0021-9258(17)46944-4
- Kang, H.T. and Hwang, E.S. (2009). Nicotinamide enhances mitochondria quality through autophagy activation in human cells. Aging Cell 8, 426-438. https://doi.org/10.1111/j.1474-9726.2009.00487.x
- Kang, H.T., Park, J.T., Choi, K., Kim, Y., Choi, H.J.C., Jung, C.W., Lee, Y.S., and Park, S.C. (2017). Chemical screening identifies ATM as a target for alleviating senescence. Nat. Chem. Biol. 13, 616-623. https://doi.org/10.1038/nchembio.2342
- Karabiyik, C., Vicinanza, M., Son, S.M., and Rubinsztein, D.C. (2021). Glucose deprivation induces autophagy via ULK1-mediated activation of PIKfyve in an AMPK-dependent manner. Dev. Cell 56, 1961-1975.e5. https://doi.org/10.1016/j.devcel.2021.05.010
- Khanna, K.K., Lavin, M.F., Jackson, S.P., and Mulhern, T.D. (2001). ATM, a central controller of cellular responses to DNA damage. Cell Death Differ. 8, 1052-1065. https://doi.org/10.1038/sj.cdd.4400874
- Kim, H.J., Han, Y.H., Kim, J.Y., and Lee, M.O. (2021). RORalpha enhances lysosomal acidification and autophagic flux in the hepatocytes. Hepatol. Commun. 5, 2121-2138. https://doi.org/10.1002/hep4.1785
- Kimura, S., Noda, T., and Yoshimori, T. (2007). Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460. https://doi.org/10.4161/auto.4451
- Kwak, J.Y., Ham, H.J., Kim, C.M., and Hwang, E.S. (2015). Nicotinamide exerts antioxidative effects on senescent cells. Mol. Cells 38, 229-235. https://doi.org/10.14348/molcells.2015.2253
- Lee, B.Y., Han, J.A., Im, J.S., Morrone, A., Johung, K., Goodwin, E.C., Kleijer, W.J., DiMaio, D., and Hwang, E.S. (2006). Senescence-associated betagalactosidase is lysosomal beta-galactosidase. Aging Cell 5, 187-195. https://doi.org/10.1111/j.1474-9726.2006.00199.x
- Lee, I.H., Cao, L., Mostoslavsky, R., Lombard, D.B., Liu, J., Bruns, N.E., Tsokos, M., Alt, F.W., and Finkel, T. (2008). A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. U. S. A. 105, 3374-3379. https://doi.org/10.1073/pnas.0712145105
- Lee, Y.J., Galoforo, S.S., Berns, C.M., Chen, J.C., Davis, B.H., Sim, J.E., Corry, P.M., and Spitz, D.R. (1998). Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J. Biol. Chem. 273, 5294-5299. https://doi.org/10.1074/jbc.273.9.5294
- Leprivier, G. and Rotblat, B. (2020). How does mTOR sense glucose deprivation? AMPK is the usual suspect. Cell Death Discov. 6, 27.
- Li, X., Yu, W., Qian, X., Xia, Y., Zheng, Y., Lee, J.H., Li, W., Lyu, J., Rao, G., Zhang, X., et al. (2017). Nucleus-translocated ACSS2 promotes gene transcription for lysosomal biogenesis and autophagy. Mol. Cell 66, 684-697.e9. https://doi.org/10.1016/j.molcel.2017.04.026
- Liu, Y., Song, X.D., Liu, W., Zhang, T.Y., and Zuo, J. (2003). Glucose deprivation induces mitochondrial dysfunction and oxidative stress in PC12 cell line. J. Cell. Mol. Med. 7, 49-56. https://doi.org/10.1111/j.1582-4934.2003.tb00202.x
- Lu, M., Ammar, D., Ives, H., Albrecht, F., and Gluck, S.L. (2007). Physical interaction between aldolase and vacuolar H+-ATPase is essential for the assembly and activity of the proton pump. J. Biol. Chem. 282, 24495-24503. https://doi.org/10.1074/jbc.M702598200
- Manchester, J., Kong, X., Lowry, O.H., and Lawrence, J.C., Jr. (1994). Ras signaling in the activation of glucose transport by insulin. Proc. Natl. Acad. Sci. U. S. A. 91, 4644-4648. https://doi.org/10.1073/pnas.91.11.4644
- McGuire, C.M. and Forgac, M. (2018). Glucose deprivation increases V-ATPase assembly and activity in mammalian cells through AMP kinase and phosphatidylinositide 3-kinase/Akt signaling. J. Biol. Chem. 293, 9113-9123. https://doi.org/10.1074/jbc.RA117.001327
- Miwa, S., Kashyap, S., Chini, E., and von Zglinicki, T. (2022). Mitochondrial dysfunction in cell senescence and aging. J. Clin. Invest. 132, e158447.
- Morselli, E., Maiuri, M.C., Markaki, M., Megalou, E., Pasparaki, A., Palikaras, K., Criollo, A., Galluzzi, L., Malik, S.A., Vitale, I., et al. (2010). Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis. 1, e10.
- Moruno, F., Perez-Jimenez, E., and Knecht, E. (2012). Regulation of autophagy by glucose in Mammalian cells. Cells 1, 372-395. https://doi.org/10.3390/cells1030372
- Nakamura, S. and Yoshimori, T. (2018). Autophagy and longevity. Mol. Cells 41, 65-72.
- Ntsapi, C., Swart, C., Lumkwana, D., and Loos, B. (2016). Autophagic flux failure in neurodegeneration: identifying the defect and compensating flux offset. In Autophagy in Current Trends in Cellular Physiology and Pathology, N.V. Gorbunov and M. Schneider, eds. (Rijeka: IntechOpen), pp. 157-176.
- Oh, C.K., Dolatabadi, N., Cieplak, P., Diaz-Meco, M.T., Moscat, J., Nolan, J.P., Nakamura, T., and Lipton, S.A. (2022). S-Nitrosylation of p62 Inhibits autophagic flux to promote alpha-synuclein secretion and spread in Parkinson's disease and Lewy body dementia. J. Neurosci. 42, 3011-3024. https://doi.org/10.1523/JNEUROSCI.1508-21.2022
- Parra, K.J. and Kane, P.M. (1998). Reversible association between the V1 and V0 domains of yeast vacuolar H+-ATPase is an unconventional glucose-induced effect. Mol. Cell. Biol. 18, 7064-7074. https://doi.org/10.1128/MCB.18.12.7064
- Ploumi, C., Daskalaki, I., and Tavernarakis, N. (2017). Mitochondrial biogenesis and clearance: a balancing act. FEBS J. 284, 183-195. https://doi.org/10.1111/febs.13820
- Ramirez-Peinado, S., Leon-Annicchiarico, C.L., Galindo-Moreno, J., Iurlaro, R., Caro-Maldonado, A., Prehn, J.H.M., Ryan, K.M., and Munoz-Pinedo, C. (2013). Glucose-deprived cells do not engage in prosurvival autophagy. J. Biol. Chem. 288, 30387-30398. https://doi.org/10.1074/jbc.M113.490581
- Salminen, A. and Kaarniranta, K. (2012). AMP-activated protein kinase (AMPK) controls the aging process via an integrated signaling network. Ageing Res. Rev. 11, 230-241. https://doi.org/10.1016/j.arr.2011.12.005
- Shi, G., Lee, J.R., Grimes, D.A., Racacho, L., Ye, D., Yang, H., Ross, O.A., Farrer, M., McQuibban, G.A., and Bulman, D.E. (2011). Functional alteration of PARL contributes to mitochondrial dysregulation in Parkinson's disease. Hum. Mol. Genet. 20, 1966-1974. https://doi.org/10.1093/hmg/ddr077
- Shi, G. and McQuibban, G.A. (2017). The mitochondrial rhomboid protease PARL is regulated by PDK2 to integrate mitochondrial quality control and metabolism. Cell Rep. 18, 1458-1472. https://doi.org/10.1016/j.celrep.2017.01.029
- Smardon, A.M. and Kane, P.M. (2007). RAVE is essential for the efficient assembly of the C subunit with the vacuolar H(+)-ATPase. J. Biol. Chem. 282, 26185-26194. https://doi.org/10.1074/jbc.M703627200
- Son, Y., Cheong, Y.K., Kim, N.H., Chung, H.T., Kang, D.G., and Pae, H.O. (2011). Mitogen-activated protein kinases and reactive oxygen species: how can ROS activate MAPK pathways? J. Signal Transduct. 2011, 792639.
- Son, Y., Kim, S., Chung, H.T., and Pae, H.O. (2013). Reactive oxygen species in the activation of MAP kinases. Methods Enzymol. 528, 27-48. https://doi.org/10.1016/B978-0-12-405881-1.00002-1
- Song, S.B. and Hwang, E.S. (2018). A rise in ATP, ROS, and mitochondrial content upon glucose withdrawal correlates with a dysregulated mitochondria turnover mediated by the activation of the protein deacetylase SIRT1. Cells 8, 11.
- Song, S.B. and Hwang, E.S. (2020). High levels of ROS impair lysosomal acidity and autophagy flux in glucose-deprived fibroblasts by activating ATM and Erk pathways. Biomolecules 10, 761.
- Song, S.B., Shim, W., and Hwang, E.S. (2023). Lipofuscin granule accumulation requires autophagy activation. Mol. Cells 46, 486-495. https://doi.org/10.14348/molcells.2023.0019
- Swerdlow, R.H. (2009). Mitochondrial medicine and the neurodegenerative mitochondriopathies. Pharmaceuticals (Basel) 2, 150-167. https://doi.org/10.3390/ph2030150
- Twig, G., Elorza, A., Molina, A.J., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G., et al. (2008). Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446. https://doi.org/10.1038/sj.emboj.7601963
- Wang, S., Li, H., Yuan, M., Fan, H., and Cai, Z. (2022). Role of AMPK in autophagy. Front. Physiol. 13, 1015500.
- Wong, Y.C. and Holzbaur, E.L. (2014). The regulation of autophagosome dynamics by huntingtin and HAP1 is disrupted by expression of mutant huntingtin, leading to defective cargo degradation. J. Neurosci. 34, 1293-1305. https://doi.org/10.1523/JNEUROSCI.1870-13.2014
- Yoo, S. and Jung, Y. (2018). A molecular approach to mitophagy and mitochondrial dynamics. Mol. Cells 41, 18-26.
- Zhang, X.J., Chen, S., Huang, K.X., and Le, W.D. (2013). Why should autophagic flux be assessed? Acta Pharmacol. Sin. 34, 595-599. https://doi.org/10.1038/aps.2012.184
- Zorov, D.B., Juhaszova, M., and Sollott, S.J. (2014). Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 94, 909-950. https://doi.org/10.1152/physrev.00026.2013