Succinate Dehydrogenase Upregulation Destabilize Complex I and Limits the Lifespan of gas-1 Mutant

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Pujol, Claire ^a   Bratic Hench, Ivana ^a,b   Sumakovic, Marija ^a   Hench, Jürgen ^c   Mourier, Arnaud ^d   Baumann, Linda ^a   Pavlenko, Victor ^a   Trifunovic, Aleksandra ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME REGULATION; ENZYME STABILITY; GAS 1 GENE; GENE; LIFESPAN; LONGEVITY; MITOCHONDRION; NONHUMAN; POINT MUTATION; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ENZYME STABILITY; LONGEVITY; MITOCHONDRIA; MUTATION; NADH DEHYDROGENASE; REACTIVE OXYGEN SPECIES; SUCCINATE DEHYDROGENASE; UP-REGULATION;

CAENORHABDITIS ELEGANS;

EID: 84875484178     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059493     Document Type: Article

References (47)

1. Janssen RJ, Nijtmans LG, van den Heuvel LP, Smeitink JA, (2006) Mitochondrial complex I: structure, function and pathology. J Inherit Metab Dis 29: 499-515.
2. Wang J, Wilhelmsson H, Graff C, Li H, Oldfors A, et al. (1999) Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet 21: 133-137.
3. Hance N, Ekstrand MI, Trifunovic A, (2005) Mitochondrial DNA polymerase gamma is essential for mammalian embryogenesis. Hum Mol Genet 14: 1775-1783.
4. Feng J, Bussiere F, Hekimi S, (2001) Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev Cell 1: 633-644.
5. Lee SS, Lee RY, Fraser AG, Kamath RS, Ahringer J, et al. (2003) A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat Genet 33: 40-48.
6. Dillin A, Hsu AL, Arantes-Oliveira N, Lehrer-Graiwer J, Hsin H, et al. (2002) Rates of behavior and aging specified by mitochondrial function during development. Science 298: 2398-2401.
7. Rea SL, Ventura N, Johnson TE, (2007) Relationship Between Mitochondrial Electron Transport Chain Dysfunction, Development, and Life Extension in Caenorhabditis elegans. PLoS Biol 5: e259.
8. Huang J, Lemire BD, (2009) Mutations in the C. elegans succinate dehydrogenase iron-sulfur subunit promote superoxide generation and premature aging. J Mol Biol 387: 559-569.
9. Kayser EB, Morgan PG, Hoppel CL, Sedensky MM, (2001) Mitochondrial expression and function of GAS-1 in Caenorhabditis elegans. J Biol Chem 276: 20551-20558.
10. Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, et al. (2010) Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 12: 1431-1470.
11. Tuppen HA, Hogan VE, He L, Blakely EL, Worgan L, et al. (2010) The p.M292T NDUFS2 mutation causes complex I-deficient Leigh syndrome in multiple families. Brain 133: 2952-2963.
12. Falk MJ, Rosenjack JR, Polyak E, Suthammarak W, Chen Z, et al. (2009) Subcomplex Ilambda specifically controls integrated mitochondrial functions in Caenorhabditis elegans. PLoS One 4: e6607.
13. Falk MJ, Zhang Z, Rosenjack JR, Nissim I, Daikhin E, et al. (2008) Metabolic pathway profiling of mitochondrial respiratory chain mutants in C. elegans. Mol Genet Metab 93: 388-397.
14. Hartman PS, Ishii N, Kayser EB, Morgan PG, Sedensky MM, (2001) Mitochondrial mutations differentially affect aging, mutability and anesthetic sensitivity in Caenorhabditis elegans. Mech Ageing Dev 122: 1187-1201.
15. Butler JA, Ventura N, Johnson TE, Rea SL, (2010) Long-lived mitochondrial (Mit) mutants of Caenorhabditis elegans utilize a novel metabolism. FASEB J 24: 4977-4988.
16. Hunte C, Zickermann V, Brandt U, (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science. 329: 448-451.
17. Goldberg GS, Kaczmarczyk W, (1993) A chicken genomic DNA fragment that hybridizes to the murine Hox-3.1 homeobox is likely to encode the NADH ubiquinone oxidoreductase subunit B15. Gene 133: 233-235.
18. Hirst J, (2009) Towards the molecular mechanism of respiratory complex I. Biochem J. 425: 327-339.
19. Hench J, Bratic Hench I, Pujol C, Ipsen S, Brodesser S, et al. (2011) A tissue-specific approach to the analysis of metabolic changes in Caenorhabditis elegans. PLoS One 6: e28417.
20. Kuramochi T, Hirawake H, Kojima S, Takamiya S, Furushima R, et al. (1994) Sequence comparison between the flavoprotein subunit of the fumarate reductase (complex II) of the anaerobic parasitic nematode, Ascaris suum and the succinate dehydrogenase of the aerobic, free-living nematode, Caenorhabditis elegans. Mol Biochem Parasitol 68: 177-187.
21. Kondo M, Senoo-Matsuda N, Yanase S, Ishii T, Hartman PS, et al. (2005) Effect of oxidative stress on translocation of DAF-16 in oxygen-sensitive mutants, mev-1 and gas-1 of Caenorhabditis elegans. Mech Ageing Dev 126: 637-641.
22. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT, (2008) Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol 28: 718-731.
23. Back P, Matthijssens F, Vlaeminck C, Braeckman BP, Vanfleteren JR, (2010) Effects of sod gene overexpression and deletion mutation on the expression profiles of reporter genes of major detoxification pathways in Caenorhabditis elegans. Exp Gerontol 45: 603-610.
24. Lee SJ, Hwang AB, Kenyon C, (2010) Inhibition of respiration extends C. elegans life span via reactive oxygen species that increase HIF-1 activity. Curr Biol 20: 2131-2136.
25. Semenza GL, (2012) Hypoxia-inducible factors in physiology and medicine. Cell 148: 399-408.
26. Koivunen P, Hirsila M, Remes AM, Hassinen IE, Kivirikko KI, et al. (2007) Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 282: 4524-4532.
27. Benedetti C, Haynes CM, Yang Y, Harding HP, Ron D, (2006) Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 174: 229-239.
28. Yoneda T, Benedetti C, Urano F, Clark SG, Harding HP, et al. (2004) Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J Cell Sci 117: 4055-4066.
29. Zhao Q, Wang J, Levichkin IV, Stasinopoulos S, Ryan MT, et al. (2002) A mitochondrial specific stress response in mammalian cells. EMBO J 21: 4411-4419.
30. Durieux J, Wolff S, Dillin A, (2011) The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144: 79-91.
31. Genova ML, Bianchi C, Lenaz G, (2005) Supercomplex organization of the mitochondrial respiratory chain and the role of the Coenzyme Q pool: pathophysiological implications. Biofactors 25: 5-20.
32. Acin-Perez R, Fernandez-Silva P, Peleato ML, Perez-Martos A, Enriquez JA, (2008) Respiratory active mitochondrial supercomplexes. Mol Cell 32: 529-539.
33. Winge DR, (2012) Sealing the mitochondrial respirasome. Mol Cell Biol 32: 2647-2652.
34. Stiernagle T (2006) Maintenance of C. elegans. WormBook: 1-11.
35. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J, (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.
36. Bianchi L, Driscoll M (2006) Culture of embryonic C. elegans cells for electrophysiological and pharmacological analyses. WormBook: 1-15.
37. Kaplan EL, Meier P, (1958) Nonparametric estimation from incomplete observation. J Am Stat Assoc 53: 457-481.
38. Bratic I, Hench J, Trifunovic A, (2010) Caenorhabditis elegans as a model system for mtDNA replication defects. Methods 51: 437-443.
39. Levine RL, Garland D, Oliver CN, Amici A, Climent I, et al. (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186: 464-478.
40. Yasuda K, Ishii T, Suda H, Akatsuka A, Hartman PS, et al. (2006) Age-related changes of mitochondrial structure and function in Caenorhabditis elegans. Mech Ageing Dev 127: 763-770.
41. van den Ecker D, van den Brand MA, Bossinger O, Mayatepek E, Nijtmans LG, et al. (2010) Blue native electrophoresis to study mitochondrial complex I in C. elegans. Anal Biochem 407: 287-289.
42. Steinberg TH, (2009) Protein gel staining methods: an introduction and overview. Methods Enzymol 463: 541-563.
43. Carroll J, Fearnley IM, Shannon RJ, Hirst J, Walker JE, (2003) Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol Cell Proteomics 2: 117-126.
44. Grad LI, Lemire BD, (2006) Riboflavin enhances the assembly of mitochondrial cytochrome c oxidase in C. elegans NADH-ubiquinone oxidoreductase mutants. Biochim Biophys Acta 1757: 115-122.
45. Acin-Perez R, Bayona-Bafaluy MP, Fernandez-Silva P, Moreno-Loshuertos R, Perez-Martos A, et al. (2004) Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol Cell 13: 805-815.
46. Senoo-Matsuda N, Yasuda K, Tsuda M, Ohkubo T, Yoshimura S, et al. (2001) A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J Biol Chem 276: 41553-41558.
47. Yang W, Hekimi S, (2010) Two modes of mitochondrial dysfunction lead independently to lifespan extension in Caenorhabditis elegans. Aging Cell 9: 433-447.