Iron-Starvation-Induced Mitophagy Mediates Lifespan Extension upon Mitochondrial Stress in C. elegans

Current Biology

Volumn 25, Issue 14, 2015, Pages 1810-1822

  Schiavi, Alfonso ^b,c   Maglioni, Silvia ^a,b   Palikaras, Konstantinos ^d   Shaik, Anjumara ^a,b   Strappazzon, Flavie ^c,f   Brinkmann, Vanessa ^b   Torgovnick, Alessandro ^b   Castelein, Natascha ^h   De Henau, Sasha ^h   Braeckman, Bart P ^h   Cecconi, Francesco ^c,f,g   Tavernarakis, Nektarios ^d,e   Ventura, Natascia ^a,b,c  

^a Department of Orthopedic Surgery   (Germany)

^b IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^e UNIVERSITY OF CRETE   (Greece)

^f IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^g DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^h GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

CAENORHABDITIS ELEGANS PROTEIN; FRATAXIN; IRON; IRON BINDING PROTEIN;

ANAEROBIC GROWTH; ANIMAL; CAENORHABDITIS ELEGANS; DEFICIENCY; DIET RESTRICTION; DRUG EFFECTS; GENETICS; LONGEVITY; METABOLISM; MITOPHAGY; PHYSIOLOGY;

ANAEROBIOSIS; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FASTING; IRON; IRON-BINDING PROTEINS; LONGEVITY; MITOCHONDRIAL DEGRADATION;

EID: 84937514081     PISSN: 09609822     EISSN: 18790445     Source Type: Journal    
DOI: 10.1016/j.cub.2015.05.059     Document Type: Article

References (56)

1. V. Campuzano, L. Montermini, M.D. Moltò, L. Pianese, M. Cossée, F. Cavalcanti, E. Monros, F. Rodius, F. Duclos, A. Monticelli, and et al. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion Science 271 1996 1423 1427
2. N. Ventura, and S.L. Rea Caenorhabditis elegans mitochondrial mutants as an investigative tool to study human neurodegenerative diseases associated with mitochondrial dysfunction Biotechnol. J. 2 2007 584 595
3. C. Dell'agnello, S. Leo, A. Agostino, G. Szabadkai, C. Tiveron, A. Zulian, A. Prelle, P. Roubertoux, R. Rizzuto, and M. Zeviani Increased longevity and refractoriness to Ca(2+)-dependent neurodegeneration in Surf1 knockout mice Hum. Mol. Genet. 16 2007 431 444
4. N. Ventura, S.L. Rea, and R. Testi Long-lived C. elegans mitochondrial mutants as a model for human mitochondrial-associated diseases Exp. Gerontol. 41 2006 974 991
5. E. Munkácsy, and S.L. Rea The paradox of mitochondrial dysfunction and extended longevity Exp. Gerontol. 56 2014 221 233
6. A. Schiavi, A. Torgovnick, A. Kell, E. Megalou, N. Castelein, I. Guccini, L. Marzocchella, S. Gelino, M. Hansen, F. Malisan, and et al. Autophagy induction extends lifespan and reduces lipid content in response to frataxin silencing in C. elegans Exp. Gerontol. 48 2013 191 201
7. J. Durieux, S. Wolff, and A. Dillin The cell-non-autonomous nature of electron transport chain-mediated longevity Cell 144 2011 79 91
8. R. Mehta, K.A. Steinkraus, G.L. Sutphin, F.J. Ramos, L.S. Shamieh, A. Huh, C. Davis, D. Chandler-Brown, and M. Kaeberlein Proteasomal regulation of the hypoxic response modulates aging in C. elegans Science 324 2009 1196 1198
9. Y. Zhang, Z. Shao, Z. Zhai, C. Shen, and J.A. Powell-Coffman The HIF-1 hypoxia-inducible factor modulates lifespan in C. elegans PLoS ONE 4 2009 e6348
10. A.C. Epstein, J.M. Gleadle, L.A. McNeill, K.S. Hewitson, J. O'Rourke, D.R. Mole, M. Mukherji, E. Metzen, M.I. Wilson, A. Dhanda, and et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation Cell 107 2001 43 54
11. V. Samokhvalov, B.A. Scott, and C.M. Crowder Autophagy protects against hypoxic injury in C. elegans Autophagy 4 2008 1034 1041
12. K. Wang, and D.J. Klionsky Mitochondria removal by autophagy Autophagy 7 2011 297 300
13. H. Zhang, M. Bosch-Marce, L.A. Shimoda, Y.S. Tan, J.H. Baek, J.B. Wesley, F.J. Gonzalez, and G.L. Semenza Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia J. Biol. Chem. 283 2008 10892 10903
14. A. Schiavi, and N. Ventura The interplay between mitochondria and autophagy and its role in the aging process Exp. Gerontol. 56 2014 147 153
15. K. Palikaras, and N. Tavernarakis Mitophagy in neurodegeneration and aging Front. Genet. 3 2012 297
16. D.P. Narendra, and R.J. Youle Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control Antioxid. Redox Signal. 14 2011 1929 1938
17. W. Springer, T. Hoppe, E. Schmidt, and R. Baumeister A Caenorhabditis elegans Parkin mutant with altered solubility couples alpha-synuclein aggregation to proteotoxic stress Hum. Mol. Genet. 14 2005 3407 3423
18. J. Sämann, J. Hegermann, E. von Gromoff, S. Eimer, R. Baumeister, and E. Schmidt Caenorhabditits elegans LRK-1 and PINK-1 act antagonistically in stress response and neurite outgrowth J. Biol. Chem. 284 2009 16482 16491
19. A.S. Bess, T.L. Crocker, I.T. Ryde, and J.N. Meyer Mitochondrial dynamics and autophagy aid in removal of persistent mitochondrial DNA damage in Caenorhabditis elegans Nucleic Acids Res. 40 2012 7916 7931
20. M. Yasuda, C. D'Sa-Eipper, X.L. Gong, and G. Chinnadurai Regulation of apoptosis by a Caenorhabditis elegans BNIP3 homolog Oncogene 17 1998 2525 2530
21. Y. Tian, Z. Li, W. Hu, H. Ren, E. Tian, Y. Zhao, Q. Lu, X. Huang, P. Yang, X. Li, and et al. C. elegans screen identifies autophagy genes specific to multicellular organisms Cell 141 2010 1042 1055
22. J.P. Pursiheimo, K. Rantanen, P.T. Heikkinen, T. Johansen, and P.M. Jaakkola Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62 Oncogene 28 2009 334 344
23. B. Guo, X. Huang, P. Zhang, L. Qi, Q. Liang, X. Zhang, J. Huang, B. Fang, W. Hou, J. Han, and H. Zhang Genome-wide screen identifies signaling pathways that regulate autophagy during Caenorhabditis elegans development EMBO Rep. 15 2014 705 713
24. K. Okatsu, K. Saisho, M. Shimanuki, K. Nakada, H. Shitara, Y.S. Sou, M. Kimura, S. Sato, N. Hattori, M. Komatsu, and et al. p62/SQSTM1 cooperates with Parkin for perinuclear clustering of depolarized mitochondria Genes Cells 15 2010 887 900
25. K. Palikaras, and N. Tavernarakis Mitochondrial homeostasis: the interplay between mitophagy and mitochondrial biogenesis Exp. Gerontol. 56 2014 182 188
26. M.L. Huang, E.M. Becker, M. Whitnall, Y. Suryo Rahmanto, P. Ponka, and D.R. Richardson Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant Proc. Natl. Acad. Sci. USA 106 2009 16381 16386
27. N.V. Kirienko, D.R. Kirienko, J. Larkins-Ford, C. Wählby, G. Ruvkun, and F.M. Ausubel Pseudomonas aeruginosa disrupts Caenorhabditis elegans iron homeostasis, causing a hypoxic response and death Cell Host Microbe 13 2013 406 416
28. S.J. Lee, A.B. Hwang, and C. Kenyon Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity Curr. Biol. 20 2010 2131 2136
29. G. Bellot, R. Garcia-Medina, P. Gounon, J. Chiche, D. Roux, J. Pouysségur, and N.M. Mazure Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains Mol. Cell. Biol. 29 2009 2570 2581
30. I. Papandreou, A.L. Lim, K. Laderoute, and N.C. Denko Hypoxia signals autophagy in tumor cells via AMPK activity, independent of HIF-1, BNIP3, and BNIP3L Cell Death Differ. 15 2008 1572 1581
31. A. Dillin, A.L. Hsu, N. Arantes-Oliveira, J. Lehrer-Graiwer, H. Hsin, A.G. Fraser, R.S. Kamath, J. Ahringer, and C. Kenyon Rates of behavior and aging specified by mitochondrial function during development Science 298 2002 2398 2401
32. M.H. Khan, M. Ligon, L.R. Hussey, B. Hufnal, R. Farber 2nd, E. Munkacsy, A. Rodriguez, A. Dillow, E. Kahlig, and S.L. Rea TAF-4 is required for the life extension of isp-1, clk-1 and tpk-1 Mit mutants Aging (Albany NY) 5 2013 741 758
33. A. Meléndez, Z. Tallóczy, M. Seaman, E.L. Eskelinen, D.H. Hall, and B. Levine Autophagy genes are essential for dauer development and life-span extension in C. elegans Science 301 2003 1387 1391
34. H. Jiang, R. Guo, and J.A. Powell-Coffman The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia Proc. Natl. Acad. Sci. USA 98 2001 7916 7921
35. C. Shen, D. Nettleton, M. Jiang, S.K. Kim, and J.A. Powell-Coffman Roles of the HIF-1 hypoxia-inducible factor during hypoxia response in Caenorhabditis elegans J. Biol. Chem. 280 2005 20580 20588
36. D. Hoogewijs, N.B. Terwilliger, K.A. Webster, J.A. Powell-Coffman, S. Tokishita, H. Yamagata, T. Hankeln, T. Burmester, K.T. Rytkönen, M. Nikinmaa, and et al. From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia Integr. Comp. Biol. 47 2007 552 577
37. D. Hoogewijs, E. Geuens, S. Dewilde, A. Vierstraete, L. Moens, S. Vinogradov, and J.R. Vanfleteren Wide diversity in structure and expression profiles among members of the Caenorhabditis elegans globin protein family BMC Genomics 8 2007 356
38. S.J. Romney, B.S. Newman, C. Thacker, and E.A. Leibold HIF-1 regulates iron homeostasis in Caenorhabditis elegans by activation and inhibition of genes involved in iron uptake and storage PLoS Genet. 7 2011 e1002394
39. N. Gabrielli, J. Ayté, and E. Hidalgo Cells lacking pfh1, a fission yeast homolog of mammalian frataxin protein, display constitutive activation of the iron starvation response J. Biol. Chem. 287 2012 43042 43051
40. Y.I. Kim, J.H. Cho, O.J. Yoo, and J. Ahnn Transcriptional regulation and life-span modulation of cytosolic aconitase and ferritin genes in C.elegans J. Mol. Biol. 342 2004 421 433
41. B.L. Gourley, S.B. Parker, B.J. Jones, K.B. Zumbrennen, and E.A. Leibold Cytosolic aconitase and ferritin are regulated by iron in Caenorhabditis elegans J. Biol. Chem. 278 2003 3227 3234
42. H. Puccio, D. Simon, M. Cossée, P. Criqui-Filipe, F. Tiziano, J. Melki, C. Hindelang, R. Matyas, P. Rustin, and M. Koenig Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits Nat. Genet. 27 2001 181 186
43. S.L. Rea, N. Ventura, and T.E. Johnson Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans PLoS Biol. 5 2007 e259
44. W. Yang, and S. Hekimi Two modes of mitochondrial dysfunction lead independently to lifespan extension in Caenorhabditis elegans Aging Cell 9 2010 433 447
45. J.A. Butler, N. Ventura, T.E. Johnson, and S.L. Rea Long-lived mitochondrial (Mit) mutants of Caenorhabditis elegans utilize a novel metabolism FASEB J. 24 2010 4977 4988
46. N. Dasgupta, A.M. Patel, B.A. Scott, and C.M. Crowder Hypoxic preconditioning requires the apoptosis protein CED-4 in C. elegans Curr. Biol. 17 2007 1954 1959
47. H.K. Park, K. Chu, K.H. Jung, S.T. Lee, J.J. Bahn, M. Kim, S.K. Lee, and J.K. Roh Autophagy is involved in the ischemic preconditioning Neurosci. Lett. 451 2009 16 19
48. G.F. Allen, R. Toth, J. James, and I.G. Ganley Loss of iron triggers PINK1/Parkin-independent mitophagy EMBO Rep. 14 2013 1127 1135
49. N.V. Kirienko, F.M. Ausubel, and G. Ruvkun Mitophagy confers resistance to siderophore-mediated killing by Pseudomonas aeruginosa Proc. Natl. Acad. Sci. USA 112 2015 1821 1826
50. S. Maglioni, A. Schiavi, A. Runci, A. Shaik, and N. Ventura Mitochondrial stress extends lifespan in C. elegans through neuronal hormesis Exp. Gerontol. 56 2014 89 98
51. L.G. Luhachack, O. Visvikis, A.C. Wollenberg, A. Lacy-Hulbert, L.M. Stuart, and J.E. Irazoqui EGL-9 controls C. elegans host defense specificity through prolyl hydroxylation-dependent and -independent HIF-1 pathways PLoS Pathog. 8 2012 e1002798
52. S.F. Leiser, and M. Kaeberlein The hypoxia-inducible factor HIF-1 functions as both a positive and negative modulator of aging Biol. Chem. 391 2010 1131 1137
53. L.R. Lapierre, C.D. De Magalhaes Filho, P.R. McQuary, C.C. Chu, O. Visvikis, J.T. Chang, S. Gelino, B. Ong, A.E. Davis, J.E. Irazoqui, and et al. The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans Nat. Commun. 4 2013 2267
54. I. Guccini, D. Serio, I. Condò, A. Rufini, B. Tomassini, A. Mangiola, G. Maira, C. Anile, D. Fina, F. Pallone, and et al. Frataxin participates to the hypoxia-induced response in tumors Cell Death Dis. 2 2011 e123
55. N. Ventura, S.L. Rea, A. Schiavi, A. Torgovnick, R. Testi, and T.E. Johnson p53/CEP-1 increases or decreases lifespan, depending on level of mitochondrial bioenergetic stress Aging Cell 8 2009 380 393
56. S. Maglioni, N. Arsalan, L. Franchi, A. Hurd, A.W. Opipari, G.D. Glick, and N. Ventura An automated phenotype-based microscopy screen to identify pro-longevity interventions acting through mitochondria in C. elegans Biochim Biophys Acta. 2015 10.1016/j.bbabio.2015.05.004 Published online May 12, 2015