Distinct designer diamines promote mitophagy, and thereby enhance healthspan in C. elegans and protect human cells against oxidative damage

References

• Kowald A, Kirkwood TBL. Accumulation of defective mitochondria through delayed degradation of damaged organelles and its possible role in the ageing of post-mitotic and dividing cells. J Theor Biol. 2000;202(2):145–160.
   PubMed Web of Science ®Google Scholar
• Palikaras K, Lionaki E, Tavernarakis N. Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans. Nature. 2015;521(7553):525–528. PubMed PMID: 25896323
   PubMed Web of Science ®Google Scholar
• Palikaras K, Lionaki E, Tavernarakis N. Coupling mitogenesis and mitophagy for longevity.Autophagy.2015;11(8):1428–1430; Epub 2015/06/18. PubMed PMID: 26083448; PubMed Central PMCID: PMCPMC4590656.
   PubMed Web of Science ®Google Scholar
• Onishi M, Yamano K, Sato M, et al.Molecular mechanisms and physiological functions of mitophagy.EMBO J.2021;40(3):e104705; Epub 2021/01/14. PubMed PMID: 33438778; PubMed Central PMCID: PMCPMC7849173.
   PubMed Web of Science ®Google Scholar
• Yamashita S-I, Kanki T. How autophagy eats large mitochondria: autophagosome formation coupled with mitochondrial fragmentation. Autophagy. 2017;13(5):980–981.
   PubMed Web of Science ®Google Scholar
• Diot A, Morten K, Poulton J. Mitophagy plays a central role in mitochondrial ageing.Mamm Genome.2016;27(7–8):381–395; Epub 2016/06/29. PubMed PMID: 27352213; PubMed Central PMCID: PMCPMC4935730.
   PubMed Web of Science ®Google Scholar
• Fang EF, Hou Y, Palikaras K, et al. Mitophagy inhibits amyloid-beta and tau pathology and reverses cognitive deficits in models of Alzheimer’s disease. Nat Neurosci. 2019;22(3):401–412. Epub 2019/02/12 PubMed PMID: 30742114.
   PubMed Web of Science ®Google Scholar
• Liu J, Liu W, Li R, et al.Mitophagy in Parkinson’s disease: from pathogenesis to treatment.Cells.2019;8(7):712; Epub 2019/07/25. PubMed PMID: 31336937; PubMed Central PMCID: PMCPMC6678174.
   PubMed Web of Science ®Google Scholar
• Clark EH, Vazquez de la Torre A, Hoshikawa T, et al. Targeting mitophagy in Parkinson’s disease. J Biol Chem. 2020;296:100209. Epub 2020/12/30. PubMed PMID: 33372898; PubMed Central PMCID: PMCPMC7948953.
   PubMed Web of Science ®Google Scholar
• Drummond MJ, Addison O, Brunker L, et al. Downregulation of E3 ubiquitin ligases and mitophagy-related genes in skeletal muscle of physically inactive, frail older women: a cross-sectional comparison. J Gerontol A Biol Sci Med Sci. 2014;69(8):1040–1048. Epub 2014/02/15 PubMed PMID: 24526667; PubMed Central PMCID: PMCPMC4111292.
   PubMed Web of Science ®Google Scholar
• Bellanti F, Lo Buglio A, Vendemiale G. Mitochondrial impairment in Sarcopenia. Biology (Basel). 2021;10(1). DOI:10.3390/biology10010031 Epub 2021/01/10 PubMed PMID: 33418869; PubMed Central PMCID: PMCPMC7825073.
   PubMedGoogle Scholar
• Qi Y, Qiu Q, Gu X, et al. ATM mediates spermidine-induced mitophagy via PINK1 and Parkin regulation in human fibroblasts. Sci Rep. 2016;6(1):24700.
   PubMedGoogle Scholar
• Yang X, Zhang M, Dai Y, et al. Spermidine inhibits neurodegeneration and delays aging via the PINK1-PDR1-dependent mitophagy pathway in C. elegans. Aging (Albany NY). 2020;12(17):16852–16866. Epub 2020/09/10 PubMed PMID: 32902411; PubMed Central PMCID: PMCPMC7521492.
   PubMedGoogle Scholar
• Palikaras K, Princz A, Tavernarakis N. Mitophagy modulators. In: Rattan SIS, editor. Encyclopedia of biomedical Gerontology. Oxford: Academic Press; 2020. p. 433–446.
   Google Scholar
• Eisenberg T, Abdellatif M, Schroeder S, et al. Cardioprotection and lifespan extension by the natural polyamine spermidine. Nat Med. 2016;22(12):1428–1438.
   PubMed Web of Science ®Google Scholar
• Schroeder S, Hofer SJ, Zimmermann A, et al. Dietary spermidine improves cognitive function. Cell Rep. 2021;35(2):108985.
   PubMed Web of Science ®Google Scholar
• Eisenberg T, Knauer H, Schauer A, et al. Induction of autophagy by spermidine promotes longevity. Nat Cell Biol. 2009;11(11):1305–1314.
   PubMed Web of Science ®Google Scholar
• Minois N, Carmona-Gutierrez D, Bauer MA, et al. Spermidine promotes stress resistance in Drosophila melanogaster through autophagy-dependent and -independent pathways. Cell Death Dis. 2012;3(10):e401. Epub 2012/10/13 PubMed PMID: 23059820; PubMed Central PMCID: PMCPMC3481127.
   PubMedGoogle Scholar
• Igarashi K, Ueda S, Yoshida K, et al.Polyamines in renal failure.Amino Acids.2006;31(4):477–483; Epub 2006/03/24. PubMed PMID: 16554974.
   PubMed Web of Science ®Google Scholar
• Pegg AE. Toxicity of polyamines and their metabolic products.Chem Res Toxicol.2013;26(12):1782–1800; Epub 2013/11/15. PubMed PMID: 24224555.
   PubMed Web of Science ®Google Scholar
• Cochemé HM, Murphy MP. Complex I is the major site of mitochondrial superoxide production by Paraquat*. J Biol Chem. 2008;283(4):1786–1798.
   PubMed Web of Science ®Google Scholar
• Yoneda T, Benedetti C, Urano F, et al.Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones.J Cell Sci.2004;117(Pt 18):4055–4066; Epub 2004/07/29. PubMed PMID: 15280428.
   PubMed Web of Science ®Google Scholar
• Fang EF, Palikaras K, Sun N, et al. In vitro and in vivo detection of mitophagy in human cells, C. Elegans, and mice. J Vis Exp. 2017; 129. Epub 2017/12/30. 10.3791/56301. PubMed PMID: 29286376; PubMed Central PMCID: PMCPMC5755444.
   Web of Science ®Google Scholar
• Palikaras K, Tavernarakis N. In vivo mitophagy monitoring in Caenorhabditis elegans to determine mitochondrial homeostasis. Biol Protoc. 2017;7(7). DOI:10.21769/BioProtoc.2215 Epub 2017/04/14 PubMed PMID: 28405595; PubMed Central PMCID: PMCPMC5386141.
   PubMedGoogle Scholar
• Koentjoro B, Park JS, Sue CM. Nix restores mitophagy and mitochondrial function to protect against PINK1/Parkin-related Parkinson’s disease.Sci Rep.2017;7(1):44373; Epub 2017/03/11. PubMed PMID: 28281653; PubMed Central PMCID: PMCPMC5345073.
   PubMedGoogle Scholar
• Nahapetyan H, Moulis M, Grousset E, et al. Altered mitochondrial quality control in Atg7-deficient VSMCs promotes enhanced apoptosis and is linked to unstable atherosclerotic plaque phenotype. Cell Death Dis. 2019;10(2):119.
   PubMedGoogle Scholar
• Lee SH, Du J, Stitham J, et al. Inducing mitophagy in diabetic platelets protects against severe oxidative stress. EMBO Mol Med. 2016;8(7):779–795. Epub 2016/05/26 PubMed PMID: 27221050; PubMed Central PMCID: PMCPMC4931291.
   PubMed Web of Science ®Google Scholar
• Schaar CE, Dues DJ, Spielbauer KK, et al. Mitochondrial and cytoplasmic ROS have opposing effects on lifespan. PLoS Genet. 2015;11(2):e1004972. Epub 2015/02/12 PubMed PMID: 25671321; PubMed Central PMCID: PMCPMC4335496.
   PubMed Web of Science ®Google Scholar
• Head BP, Zulaika M, Ryazantsev S, et al.A novel mitochondrial outer membrane protein, MOMA-1, that affects cristae morphology in Caenorhabditis elegans.Mol Biol Cell.2011;22(6):831–841; Epub 2011/01/21. PubMed PMID: 21248201; PubMed Central PMCID: PMCPMC3057707.
   PubMed Web of Science ®Google Scholar
• Cabreiro F, Au C, Leung KY, et al. Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell. 2013;153(1):228–239. Epub 2013/04/02 PubMed PMID: 23540700; PubMed Central PMCID: PMCPMC3898468
   PubMed Web of Science ®Google Scholar
• Palmisano NJ, Meléndez A. Autophagy in C. elegans development. Dev Biol. 2019;447(1):103–125.
   PubMed Web of Science ®Google Scholar
• Manil-Ségalen M, Lefebvre C, Jenzer C, et al. The C. elegans LC3 acts downstream of GABARAP to Degrade autophagosomes by interacting with the HOPS Subunit VPS39. Dev Cell. 2014;28(1):43–55.
   PubMed Web of Science ®Google Scholar
• Kumsta C, Chang JT, Lee R, et al. The autophagy receptor p62/SQST-1 promotes proteostasis and longevity in C. elegans by inducing autophagy. Nat Commun. 2019;10(1):5648.
   PubMedGoogle Scholar
• Konstantinidis G, Tavernarakis N. Molecular basis of neuronal autophagy in ageing: insights from Caenorhabditis elegans.Cells.2021;10(3):694; Epub 2021/04/04. PubMed PMID: 33800981; PubMed Central PMCID: PMCPMC8004021.
   PubMed Web of Science ®Google Scholar
• Zhou X, Zhao X, Zhou W, et al. Impaired placental mitophagy and oxidative stress are associated with dysregulated BNIP3 in preeclampsia. Sci Rep. 2021;11(1):20469.
   PubMed Web of Science ®Google Scholar
• Lizama-Manibusan B, McLaughlin B. Redox modification of proteins as essential mediators of CNS autophagy and mitophagy.FEBS Lett.2013;587(15):2291–2298; Epub 2013/06/19. PubMed PMID: 23773928; PubMed Central PMCID: PMCPMC5125300.
   PubMed Web of Science ®Google Scholar
• Miedel MT, Graf NJ, Stephen KE, et al. A Pro-Cathepsin L mutant is a luminal substrate for endoplasmic-reticulum-associated degradation in C. elegans. PloS one. 2012;7(7):e40145.
   PubMed Web of Science ®Google Scholar
• Lin K, Dorman JB, Rodan A, et al.daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans.Science.1997;278(5341):1319–1322; Epub 1997/11/21. PubMed PMID: 9360933.
   PubMed Web of Science ®Google Scholar
• Lin K, Hsin H, Libina N, et al.Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling.Nat Genet.2001;28(2):139–145; Epub 2001/05/31. PubMed PMID: 11381260.
   PubMed Web of Science ®Google Scholar
• Xu X, Kim SK, Copenhaver GP. The GATA transcription factor egl-27 delays aging by promoting stress resistance in Caenorhabditis elegans. PLoS Genet. 2012;8(12):e1003108.
   PubMed Web of Science ®Google Scholar
• Mair W, Dillin A. Aging and survival: the genetics of life span extension by dietary restriction.Annu Rev Biochem.2008;77(1):727–754; Epub 2008/04/01. PubMed PMID: 18373439.
   PubMedGoogle Scholar
• Lakowski B, Hekimi S. The genetics of caloric restriction in Caenorhabditis elegans.Proc Natl Acad Sci U S A.1998;95(22):13091–13096; Epub 1998/10/28. PubMed PMID: 9789046; PubMed Central PMCID: PMCPMC23719.
   PubMed Web of Science ®Google Scholar
• Houthoofd K, Braeckman BP, Lenaerts I, et al. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Exp Gerontol. 2002;37(12):1359–1369.
   PubMed Web of Science ®Google Scholar
• Bar DZ, Charar C, Dorfman J, et al. Cell size and fat content of dietary-restricted Caenorhabditis elegans are regulated by ATX-2, an mTOR repressor. Proc Natl Acad Sci U S A. 2016;113(32):E4620–9. Epub 2016/07/28 PubMed PMID: 27457958; PubMed Central PMCID: PMCPMC4987808.
   PubMed Web of Science ®Google Scholar
• Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283(16):10892–10903. Epub 2008/02/19 PubMed PMID: 18281291; PubMed Central PMCID: PMCPMC2447655.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Shao Z, Zhai Z, et al. The HIF-1 hypoxia-inducible factor modulates lifespan in C. elegans. PLoS One. 2009;4(7):e6348. PubMed PMID: 19633713; PubMed Central PMCID: PMC2711329.
   PubMed Web of Science ®Google Scholar
• Jiang H, Guo R, Powell-Coffman JA. The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia.Proc Natl Acad Sci U S A.2001;98(14):7916–7921; Epub 2001/06/28. PubMed PMID: 11427734; PubMed Central PMCID: PMCPMC35443.
   PubMed Web of Science ®Google Scholar
• Lapierre LR, De Magalhaes Filho CD, McQuary PR, et al. The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans. Nat Commun. 2013;4(1):2267.
   PubMedGoogle Scholar
• Hansen M, Chandra A, Mitic LL, et al.A role for autophagy in the extension of lifespan by dietary restriction in C. elegans.PLoS Genet.2008;4(2):e24; Epub 2008/02/20. PubMed PMID: 18282106; PubMed Central PMCID: PMCPMC2242811.
   PubMed Web of Science ®Google Scholar
• Nhan JD, Turner CD, Anderson SM, et al. Redirection of SKN-1 abates the negative metabolic outcomes of a perceived pathogen infection. Proc Natl Acad Sci U S A. 2019;116(44):22322–22330. Epub 2019/10/16 PubMed PMID: 31611372; PubMed Central PMCID: PMCPMC6825279.
   PubMed Web of Science ®Google Scholar
• Tang L, Dodd W, Choe K. Isolation of a hypomorphic skn-1 Allele that does not require a balancer for maintenance.G3 (Bethesda).2015;6(3):551–558; Epub 2015/12/31. PubMed PMID: 26715089; PubMed Central PMCID: PMCPMC4777118.
   PubMedGoogle Scholar
• Inoue H, Hisamoto N, An JH, et al. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev. 2005;19(19):2278–2283. PubMed PMID: 16166371; PubMed Central PMCID: PMCPMC1240035.
   PubMed Web of Science ®Google Scholar
• Chikka Madhusudana R, Anbalagan C, Dvorak K, et al. The mitochondria-regulated immune pathway activated in the C. elegans intestine is neuroprotective. Cell Rep. 2016;16(9):2399–2414.
   PubMed Web of Science ®Google Scholar
• Yang W, Hekimi S, Tissenbaum HA. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol. 2010;8(12):e1000556. PubMed PMID: 21151885; PubMed Central PMCID: PMC2998438.
   PubMed Web of Science ®Google Scholar
• Robinson KM, Janes MS, Pehar M, et al. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci U S A. 2006;103(41):15038–15043. PubMed PMID: WOS:000241247300012.
   PubMed Web of Science ®Google Scholar
• Kwon YJ, Guha S, Tuluc F, et al. High-throughput BioSorter quantification of relative mitochondrial content and membrane potential in living Caenorhabditis elegans. Mitochondrion. 2018;40:42–50. Epub 2017/10/08. PubMed PMID: 28986305; PubMed Central PMCID: PMCPMC5858966.
   PubMed Web of Science ®Google Scholar
• Presley AD, Fuller KM, Arriaga EA. MitoTracker Green labeling of mitochondrial proteins and their subsequent analysis by capillary electrophoresis with laser-induced fluorescence detection.J Chromatogr B Analyt Technol Biomed Life Sci.2003;793(1):141–150; Epub 2003/07/26. PubMed PMID: 12880861.
   PubMed Web of Science ®Google Scholar
• Koopman M, Michels H, Dancy BM, et al. A screening-based platform for the assessment of cellular respiration in Caenorhabditis elegans. Nat Protoc. 2016;11(10):1798–1816.
   PubMed Web of Science ®Google Scholar
• Kim H, Perentis RJ, Caldwell GA, et al. Gene-by-environment interactions that disrupt mitochondrial homeostasis cause neurodegeneration in C. elegans Parkinson’s models. Cell Death Dis. 2018;9(5):555.
   PubMedGoogle Scholar
• Panel M, Ghaleh B, Morin D. Mitochondria and aging: a role for the mitochondrial transition pore?Aging Cell.2018;17(4):e12793; Epub 2018/06/12. PubMed PMID: 29888494; PubMed Central PMCID: PMCPMC6052406.
   PubMed Web of Science ®Google Scholar
• Velarde MC. Mitochondrial and sex steroid hormone crosstalk during aging.Longev Healthspan.2014;3(1):2; Epub 2014/02/06. PubMed PMID: 24495597; PubMed Central PMCID: PMCPMC3922316.
   PubMedGoogle Scholar
• Ikeda M, Ide T, Fujino T, et al. Overexpression of TFAM or twinkle increases mtDNA copy number and facilitates cardioprotection associated with limited mitochondrial oxidative stress. PloS one. 2015;10(3):e0119687. Epub 2015/03/31 PubMed PMID: 25822152; PubMed Central PMCID: PMCPMC4379048.
   PubMed Web of Science ®Google Scholar
• Barros MH, Bandy B, Tahara EB, et al.Higher respiratory activity decreases mitochondrial reactive oxygen release and increases life span in Saccharomyces cerevisiae.J Biol Chem.2004;279(48):49883–49888; Epub 2004/09/24. PubMed PMID: 15383542.
   PubMed Web of Science ®Google Scholar
• Morcos M, Du X, Pfisterer F, et al. Glyoxalase-1 prevents mitochondrial protein modification and enhances lifespan in Caenorhabditis elegans. Aging Cell. 2008;7(2):260–269. Epub 2008/01/29 PubMed PMID: 18221415.
   PubMed Web of Science ®Google Scholar
• Caldeira da Silva CC, Cerqueira FM, Barbosa LF, et al. Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity. Aging Cell. 2008;7(4):552–560.
   PubMed Web of Science ®Google Scholar
• Avery L, Horvitz HR. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans.J Exp Zool.1990;253(3):263–270; Epub 1990/03/01. PubMed PMID: 2181052.
   PubMedGoogle Scholar
• Rodolfo C, Campello S, Cecconi F. Mitophagy in neurodegenerative diseases. Neurochem Int. 2018;117:156–166.
   PubMed Web of Science ®Google Scholar
• Morley JF, Brignull HR, Weyers JJ, et al.The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans.Proc Natl Acad Sci U S A.2002;99(16):10417–10422; Epub 2002/07/18. PubMed PMID: 12122205; PubMed Central PMCID: PMCPMC124929.
   PubMed Web of Science ®Google Scholar
• Machiela E, Dues DJ, Senchuk MM, et al. Oxidative stress is increased in C. elegans models of Huntington’s disease but does not contribute to polyglutamine toxicity phenotypes. Neurobiol Dis. 2016;96:1–11.
   PubMed Web of Science ®Google Scholar
• Gidalevitz T, Krupinski T, Garcia S, et al.Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity.PLoS Genet.2009;5(3):e1000399; Epub 2009/03/07. PubMed PMID: 19266020; PubMed Central PMCID: PMCPMC2642731.
   PubMed Web of Science ®Google Scholar
• Jonsson PA, Ernhill K, Andersen PM, et al. Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain. 2004;127(Pt 1):73–88. Epub 2003/10/10 PubMed PMID: 14534160.
   PubMedGoogle Scholar
• Palikaras K, Tavernarakis N. Mitophagy in neurodegeneration and aging. Front Genet. 2012;3:297. Epub 2012/12/26. PubMed PMID: 23267366; PubMed Central PMCID: PMCPMC3525948.
   PubMedGoogle Scholar
• Boukamp P, Petrussevska RT, Breitkreutz D, et al.Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line.J Cell Biol.1988;106(3):761–771; Epub 1988/03/01. PubMed PMID: 2450098.
   PubMed Web of Science ®Google Scholar
• Pietrocola F, Lachkar S, Enot DP, et al. Spermidine induces autophagy by inhibiting the acetyltransferase EP300. Cell Death Differ. 2015;22(3):509–516. Epub 2014/12/20 PubMed PMID: 25526088; PubMed Central PMCID: PMCPMC4326581.
   PubMed Web of Science ®Google Scholar
• Karni R, Jove R, Levitzki A. Inhibition of pp60c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors. Oncogene. 1999;18(33):4654–4662.
   PubMed Web of Science ®Google Scholar
• Cui X, Zuo P, Zhang Q, et al. Chronic systemic D-galactose exposure induces memory loss, neurodegeneration, and oxidative damage in mice: protective effects of R-alpha-lipoic acid. J Neurosci Res. 2006;84(3):647–654. Epub 2006/05/20 PubMed PMID: 16710848.
   PubMed Web of Science ®Google Scholar
• Delwing-de Lima D, Hennrich SB, Delwing-Dal Magro D, et al. The effect of d-galactose induced oxidative stress on in vitro redox homeostasis in rat plasma and erythrocytes. Biomed Pharmacother. 2017;86:686–693.
   PubMed Web of Science ®Google Scholar
• Liu YY, Nagpure BV, Wong PT, et al.Hydrogen sulfide protects SH-SY5Y neuronal cells against d-galactose induced cell injury by suppression of advanced glycation end products formation and oxidative stress.Neurochem Int.2013;62(5):603–609; Epub 2013/01/01. PubMed PMID: 23274001.
   PubMed Web of Science ®Google Scholar
• Di Rita A, D’Acunzo P, Simula L, et al. AMBRA1-mediated mitophagy counteracts oxidative stress and apoptosis induced by neurotoxicity in human neuroblastoma SH-SY5Y cells. Front Cell Neurosci. 2018;12(92). DOI:10.3389/fncel.2018.00092
   PubMedGoogle Scholar
• Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays.J Immunol Methods.1983;65(1–2):55–63; Epub 1983/12/16. PubMed PMID: 6606682.
   PubMed Web of Science ®Google Scholar
• Rahimi VB, Askari VR, Mousavi SH. Ellagic acid reveals promising anti-aging effects against d-galactose-induced aging on human neuroblastoma cell line, SH-SY5Y: a mechanistic study. Biomed Pharmacother. 2018;108:1712–1724. Epub 2018/10/31. PubMed PMID: 30372874.
   PubMed Web of Science ®Google Scholar
• Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. Fifth edition. ed. Oxford: Oxford University Press; 2015. p. xxxviii, 905 pages, 16 unnumbered pages of plates p.
   Google Scholar
• Nahdi AMTA, John A, Raza H. Elucidation of molecular mechanisms of streptozotocin-induced oxidative stress, apoptosis, and mitochondrial dysfunction in Rin-5F Pancreatic β-Cells. Oxid Med Cell Longev. 2017;2017:7054272.
   PubMed Web of Science ®Google Scholar
• Chen H, Li X, Epstein PN. MnSOD and Catalase Transgenes Demonstrate That Protection of Islets From Oxidative Stress Does Not Alter Cytokine Toxicity. Diabetes. 2005;54(5):1437–1446.
   PubMed Web of Science ®Google Scholar
• Hohmeier HE, Mulder H, Chen G, et al.Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion.Diabetes.2000;49(3):424–430; Epub 2000/06/27. PubMed PMID: 10868964.
   PubMed Web of Science ®Google Scholar
• Rose SD, Collingwood MA, Behlke MA. Optimizing knockdown of gene expression using the TriFECTa™ Dicer-substrate RNAi reagent system. Nat Methods. 2006;3(9):V–VII.
   Google Scholar
• Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)(1). Autophagy. 2021;17(1):1–382. Epub 2021/02/27 PubMed PMID: 33634751; PubMed Central PMCID: PMCPMC7996087.
   PubMed Web of Science ®Google Scholar
• Rojansky R, Cha M-Y, Chan DC. Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. eLife. 2016;5:e17896.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Hilliard G, Ferguson T, et al.Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha.J Biol Chem.2003;278(18):15911–15916; Epub 2003/02/28. PubMed PMID: 12606543.
   PubMed Web of Science ®Google Scholar
• Cervellati F, Cervellati C, Romani A, et al. Hypoxia induces cell damage via oxidative stress in retinal epithelial cells. Free Radic Res. 2014;48(3):303–312.
   PubMed Web of Science ®Google Scholar
• Rider JE, Hacker A, Mackintosh CA, et al.Spermine and spermidine mediate protection against oxidative damage caused by hydrogen peroxide.Amino Acids.2007;33(2):231–240; Epub 2007/03/31. PubMed PMID: 17396215.
   PubMed Web of Science ®Google Scholar
• Madeo F, Eisenberg T, Pietrocola F, et al. Spermidine in health and disease. Science. 2018;359(6374). DOI:10.1126/science.aan2788 Epub 2018/01/27 PubMed PMID: 29371440
   PubMed Web of Science ®Google Scholar
• Zhang William B, Sinha Drew B, Pittman William E, et al. Extended Twilight among Isogenic C. elegans Causes a Disproportionate Scaling between Lifespan and Health. Cell Syst. 2016;3(4):333–45.e4.
   PubMed Web of Science ®Google Scholar
• Tan S, Wong E. Mitophagy Transcriptome: mechanistic Insights into Polyphenol-Mediated Mitophagy. Oxid Med Cell Longev. 2017;2017:9028435.
   PubMed Web of Science ®Google Scholar
• Papa L, Germain D. SirT3 regulates the mitochondrial unfolded protein response.Mol Cell Biol.2014;34(4):699–710; Epub 2013/12/11. PubMed PMID: 24324009; PubMed Central PMCID: PMCPMC3911493.
   PubMed Web of Science ®Google Scholar
• Audesse AJ, Dhakal S, Hassell LA, et al.FOXO3 directly regulates an autophagy network to functionally regulate proteostasis in adult neural stem cells.PLoS Genet.2019;15(4):e1008097; Epub 2019/04/12. PubMed PMID: 30973875; PubMed Central PMCID: PMCPMC6478346.
   PubMed Web of Science ®Google Scholar
• Koh H, Kim H, Kim MJ, et al.Silent information regulator 2 (Sir2) and Forkhead box O (FOXO) complement mitochondrial dysfunction and dopaminergic neuron loss in Drosophila PTEN-induced kinase 1 (PINK1) null mutant.J Biol Chem.2012;287(16):12750–12758; Epub 2012/03/02. PubMed PMID: 22378780; PubMed Central PMCID: PMCPMC3339960.
   PubMed Web of Science ®Google Scholar
• Mei Y, Zhang Y, Yamamoto K, et al.FOXO3a-dependent regulation of Pink1 (Park6) mediates survival signaling in response to cytokine deprivation.Proc Natl Acad Sci U S A.2009;106(13):5153–5158; Epub 2009/03/12. PubMed PMID: 19276113; PubMed Central PMCID: PMCPMC2654023.
   PubMed Web of Science ®Google Scholar
• Wang S, Chen Y, Li X, et al. Emerging role of transcription factor EB in mitochondrial quality control. Biomed Pharmacother. 2020;128:110272.
   PubMed Web of Science ®Google Scholar
• Lin -X-X, Sen I, Janssens GE, et al. DAF-16/FOXO and HLH-30/TFEB function as combinatorial transcription factors to promote stress resistance and longevity. Nat Commun. 2018;9(1):4400.
   PubMedGoogle Scholar
• Shen JL, Fortier TM, Wang R, et al. Vps13D functions in a Pink1-dependent and Parkin-independent mitophagy pathway. J Cell Biol. 2021;220(11). DOI:10.1083/jcb.202104073 Epub 2021/08/31 PubMed PMID: 34459871; PubMed Central PMCID: PMCPMC8406608.
   Web of Science ®Google Scholar
• Igarashi R, Yamashita S-I, Yamashita T, et al. Gemcitabine induces Parkin-independent mitophagy through mitochondrial-resident E3 ligase MUL1-mediated stabilization of PINK1. Sci Rep. 2020;10(1):1465.
   PubMed Web of Science ®Google Scholar
• Livshits L, Gross E. A method for measuring sulfide toxicity in the nematode Caenorhabditis elegans. MethodsX. 2017;4:250–255.
   PubMedGoogle Scholar
• Asfari M, Janjic D, Meda P, et al. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology. 1992;130(1):167–178.
   PubMed Web of Science ®Google Scholar
• Romero-Afrima L, Zelmanovich V, Abergel Z, et al. Ferritin is regulated by a neuro-intestinal axis in the nematode Caenorhabditis elegans. UNSP 101359. 10.1016/j.redox.2019.101359. PubMed PMID: WOS:000501490700032 Redox Biol. 2020;28.
   Web of Science ®Google Scholar
• Abergel R, Livshits L, Shaked M, et al.Synergism between soluble guanylate cyclase signaling and neuropeptides extends lifespan in the nematode Caenorhabditis elegans.Aging Cell.2017;16(2):401–413; Epub 2017/01/06. PubMed PMID: 28054425; PubMed Central PMCID: PMCPMC5334569.
   PubMed Web of Science ®Google Scholar
• Livshits L, Chatterjee AK, Karbian N, et al. Mechanisms of defense against products of cysteine catabolism in the nematode Caenorhabditis elegans. Free Radic Biol Med. 2017;104:346–359. Epub 2017/02/10. PubMed PMID: 28179109.
   PubMed Web of Science ®Google Scholar
• Mattout A, Pike Brietta L, Towbin Benjamin D, et al. An EDMD Mutation in C. elegans Lamin Blocks Muscle-Specific Gene Relocation and Compromises Muscle Integrity. Curr Biol. 2011;21(19):1603–1614.
   PubMed Web of Science ®Google Scholar
• Abramoff MD, Magelhaes PJ, Ram SJ. Image Processing with ImageJ. Biophotonics Int. 2004;11(7):36–42.
   Google Scholar
• Abergel Z, Chatterjee AK, Zuckerman B, et al. Regulation of Neuronal Oxygen Responses in C. elegans Is Mediated through Interactions between Globin 5 and the H-NOX Domains of Soluble Guanylate Cyclases. J Neurosci. 2016;36(3):963–978. PubMed PMID: 26791224; PubMed Central PMCID: PMC4719025.
   PubMed Web of Science ®Google Scholar
• Cohen E, Bieschke J, Perciavalle RM, et al.Opposing activities protect against age-onset proteotoxicity.Science.2006;313(5793):1604–1610; Epub 2006/08/12. PubMed PMID: 16902091.
   PubMed Web of Science ®Google Scholar
• Lee SJ, Hwang AB, Kenyon C. Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr Biol. 2010;20(23):2131–2136. PubMed PMID: 21093262; PubMed Central PMCID: PMC3058811.
   PubMed Web of Science ®Google Scholar
• Palikaras K, Tavernarakis N. Intracellular Assessment of ATP Levels in Caenorhabditis elegans. Biol Protoc. 2016;6(23). DOI:10.21769/BioProtoc.2048 Epub 2017/02/15 PubMed PMID: 28194429; PubMed Central PMCID: PMCPMC5303341
   Google Scholar
• Runwal G, Stamatakou E, Siddiqi FH, et al.LC3-positive structures are prominent in autophagy-deficient cells.Sci Rep.2019;9(1):10147; Epub 2019/07/14. PubMed PMID: 31300716; PubMed Central PMCID: PMCPMC6625982.
   PubMed Web of Science ®Google Scholar
• Gross E, Soltesz Z, Oda S, et al. GLOBIN-5-Dependent O2 Responses Are Regulated by PDL-1/PrBP That Targets Prenylated Soluble Guanylate Cyclases to Dendritic Endings. J Neurosci. 2014;34(50):16726–16738. PubMed PMID: 25505325; PubMed Central PMCID: PMC4261097.
   PubMed Web of Science ®Google Scholar
• Mello CC, Kramer JM, Stinchcomb D, et al. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991;10(12):3959–3970. PubMed PMID: 1935914; PubMed Central PMCID: PMC453137.
   PubMed Web of Science ®Google Scholar
• Gibson DG, Young L, Chuang R-Y, et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6(5):343–345.
   PubMed Web of Science ®Google Scholar