A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans

PLoS Genetics

Volumn 5, Issue 4, 2009, Pages

  Cristina, David ^a   Cary, Michael ^a   Lunceford, Adam ^b   Clarke, Catherine ^b   Kenyon, Cynthia ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; UBIQUINONE; CAENORHABDITIS ELEGANS PROTEIN;

AGING; ARTICLE; BEHAVIOR; CAENORHABDITIS ELEGANS; CELL PROTECTION; CONTROLLED STUDY; GENE EXPRESSION; GENE LOSS; GENE SWITCHING; INHIBITION KINETICS; LIFESPAN; MAMMAL CELL; MICROBIAL RESPIRATION; MUTANT; NONHUMAN; PHENOTYPE; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; UPREGULATION; YEAST; ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; CELL RESPIRATION; GENE EXPRESSION REGULATION; GENETICS; LONGEVITY; METABOLISM; MITOCHONDRION; MUTATION; PHYSIOLOGY;

CAENORHABDITIS ELEGANS; MAMMALIA;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL RESPIRATION; GENE EXPRESSION REGULATION; LONGEVITY; MITOCHONDRIA; MODELS, ANIMAL; MUTATION;

EID: 66149087761     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000450     Document Type: Article

References (40)

1. Kirchman PA, Kim S, Lai CY, Jazwinski SM (1999) Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae. Genetics 152: 179-190.
2. 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.
3. 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.
4. 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.
5. Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299: 1351-1354.
6. Dell'agnello C, Leo S, Agostino A, Szabadkai G, Tiveron C, et al. (2007) Increased longevity and refractoriness to Ca(2+)-dependent neurodegeneration in Surf1 knockout mice. Hum Mol Genet 16: 431-444.
7. Lakowski B, Hekimi S (1996) Determination of life-span in Caenorhabditis elegans by four clock genes. Science 272: 1010-1013.
8. Ewbank JJ, Barnes TM, Lakowski B, Lussier M, Bussey H, et al. (1997) Structural and functional conservation of the Caenorhabditis elegans timing gene clk-1. Science 275: 980-983.
9. Kayser EB, Sedensky MM, Morgan PG, Hoppel CL (2004) Mitochondrial oxidative phosphorylation is defective in the long-lived mutant clk-1. J Biol Chem 279: 54479-54486.
10. Braeckman BP, Houthoofd K, De Vreese A, Vanfleteren JR (1999) Apparent uncoupling of energy production and consumption in long-lived Clk mutants of Caenorhabditis elegans. Curr Biol 9: 493-496.
11. Felkai S, Ewbank JJ, Lemieux J, Labbe JC, Brown GG, et al. (1999) CLK-1 controls respiration, behavior and aging in the nematode Caenorhabditis elegans. EMBO J 18: 1783-1792.
12. Jonassen T, Larsen PL, Clarke CF (2001) A dietary source of coenzyme Q is essential for growth of long-lived Caenorhabditis elegans clk-1 mutants. Proc Natl Acad Sci U S A 98: 421-426.
13. Larsen PL, Clarke CF (2002) Extension of life-span in Caenorhabditis elegans by a diet lacking coenzyme Q. Science 295: 120-123.
14. Branicky R, Nguyen PA, Hekimi S (2006) Uncoupling the pleiotropic phenotypes of clk-1 with tRNA missense suppressors in Caenorhabditis elegans. Mol Cell Biol 26: 3976-3985.
15. Padilla S, Jonassen T, Jimenez-Hidalgo MA, Fernandez-Ayala DJ, Lopez-Lluch G, et al. (2004) Demethoxy-Q, an intermediate of coenzyme Q biosynthesis, fails to support respiration in Saccharomyces cerevisiae and lacks antioxidant activity. J Biol Chem 279: 25995-26004.
16. Liu X, Jiang N, Hughes B, Bigras E, Shoubridge E, et al. (2005) Evolutionary conservation of the clk-1-dependent mechanism of longevity: loss of mclk1 increases cellular fitness and lifespan in mice. Genes Dev 19: 2424-2434.
17. Lapointe J, Hekimi S (2008) Early mitochondrial dysfunction in long-lived Mclk1+/2 mice. J Biol Chem 283: 26217-26227.
18. 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.
19. Branicky R, Shibata Y, Feng J, Hekimi S (2001) Phenotypic and suppressor analysis of defecation in clk-1 mutants reveals that reaction to changes in temperature is an active process in Caenorhabditis elegans. Genetics 159: 997-1006.
20. Branicky R, Hekimi S (2005) Specification of muscle neurotransmitter sensitivity by a Paired-like homeodomain protein in Caenorhabditis elegans. Development 132: 4999-5009.
21. Shibata Y, Branicky R, Landaverde IO, Hekimi S (2003) Redox regulation of germline and vulval development in Caenorhabditis elegans. Science 302: 1779-1782.
22. Yang W, Li J, Hekimi S (2007) A Measurable Increase in Oxidative Damage Due to Reduction in Superoxide Detoxification Fails to Shorten the Life Span of Long-Lived Mitochondrial Mutants of Caenorhabditis elegans. Genetics 177: 2063-2074.
23. Liao X, Butow RA (1993) RTG1 and RTG2: two yeast genes required for a novel path of communication from mitochondria to the nucleus. Cell 72: 61-71.
24. Parikh VS, Morgan MM, Scott R, Clements LS, Butow RA (1987) The mitochondrial genotype can influence nuclear gene expression in yeast. Science 235: 576-580.
25. Epstein CB, Waddle JA, Hale Wt, Dave V, Thornton J, et al. (2001) Genomewide responses to mitochondrial dysfunction. Mol Biol Cell 12: 297-308.
26. Traven A, Wong JM, Xu D, Sopta M, Ingles CJ (2001) Interorganellar communication. Altered nuclear gene expression profiles in a yeast mitochondrial dna mutant. J Biol Chem 276: 4020-4027.
27. Butow RA, Avadhani NG (2004) Mitochondrial signaling: the retrograde response. Mol Cell 14: 1-15.
28. Miceli MV, Jazwinski SM (2005) Common and cell type-specific responses of human cells to mitochondrial dysfunction. Exp Cell Res 302: 270-280.
29. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
30. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
31. Biswas G, Adebanjo OA, Freedman BD, Anandatheerthavarada HK, Vijayasarathy C, et al. (1999) Retrograde Ca2+ signaling in C2C12 skeletal myocytes in response to mitochondrial genetic and metabolic stress: a novel mode of inter-organelle crosstalk. EMBO J 18: 522-533.
32. Huang CG, Lamitina T, Agre P, Strange K (2007) Functional analysis of the quaporin gene family in Caenorhabditis elegans. Am J Physiol Cell Physiol 292: C1867-1873.
33. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, et al. (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-283.
34. Lenaz G (2001) The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 52: 159-164.
35. 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.
36. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA (2008) Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70: 611-625.
37. Wong A, Boutis P, Hekimi S (1995) Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing. Genetics 139: 1247-1259.
38. Ishii N, Takahashi K, Tomita S, Keino T, Honda S, et al. (1990) A methyl viologen-sensitive mutant of the nematode Caenorhabditis elegans. Mutat Res 37: 165-171.
39. DeRisi JL, Iyer VR, Brown PO (1997) Exploring the metabolic and genetic ontrol of gene expression on a genomic scale. Science 278: 680-686.
40. Storey JD, Siegmund D (2001) Approximate p-values for local sequence alignments: numerical studies. J Comput Biol 8: 549-556.