Functional Loss of Two Ceramide Synthases Elicits Autophagy-Dependent Lifespan Extension in C. elegans

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Mosbech, Mai Britt ^a   Kruse, Rikke ^a   Harvald, Eva Bang ^a   Olsen, Anne Sofie Braun ^a   Gallego, Sandra Fernandez ^a   Hannibal Bach, Hans Kristian ^a   Ejsing, Christer S ^a   Færgeman, Nils J ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; CERAMIDE GLUCOSYLTRANSFERASE; SPHINGOLIPID; TRANSCRIPTION FACTOR;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DIET RESTRICTION; FEEDING BEHAVIOR; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; GENE SILENCING; GENETIC TRANSCRIPTION; HEAT TOLERANCE; LIFE EXTENSION; LIPOGENESIS; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; REPRODUCTION;

ANIMALS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; LIPID METABOLISM; LONGEVITY; OXIDOREDUCTASES; PHENOTYPE; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 84880478801     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070087     Document Type: Article

References (41)

1. Bartke N, Hannun YA, (2009) Bioactive sphingolipids: metabolism and function. J Lipid Res 50 (Suppl):: S91-96.
2. Pitson SM, (2011) Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem Sci 36: 97-107.
3. Hannun YA, Obeid LM, (2011) Many ceramides. The Journal of biological chemistry 286: 27855-27862.
4. Stiban J, Tidhar R, Futerman AH, (2010) Ceramide synthases: roles in cell physiology and signaling. Adv Exp Med Biol 688: 60-71.
5. Mullen TD, Spassieva S, Jenkins RW, Kitatani K, Bielawski J, et al. (2011) Selective knockdown of ceramide synthases reveals complex interregulation of sphingolipid metabolism. J Lipid Res 52: 68-77.
6. Spassieva S, Seo JG, Jiang JC, Bielawski J, Alvarez-Vasquez F, et al. (2006) Necessary role for the Lag1p motif in (dihydro)ceramide synthase activity. The Journal of biological chemistry 281: 33931-33938.
7. Tedesco P, Jiang J, Wang J, Jazwinski SM, Johnson TE, (2008) Genetic analysis of hyl-1, the C. elegans homolog of LAG1/LASS1. Age (Dordr) 30: 43-52.
8. Deng X, Yin X, Allan R, Lu DD, Maurer CW, et al. (2008) Ceramide biogenesis is required for radiation-induced apoptosis in the germ line of C. elegans. Science 322: 110-115.
9. Marza E, Simonsen KT, Faergeman NJ, Lesa GM, (2009) Expression of ceramide glucosyltransferases, which are essential for glycosphingolipid synthesis, is only required in a small subset of C. elegans cells. J Cell Sci 122: 822-833.
10. Menuz V, Howell KS, Gentina S, Epstein S, Riezman I, et al. (2009) Protection of C. elegans from anoxia by HYL-2 ceramide synthase. Science 324: 381-384.
11. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, et al. (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301: 1387-1391.
12. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M, et al. (2008) A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet 4: e24.
13. Panowski SH, Wolff S, Aguilaniu H, Durieux J, Dillin A, (2007) PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans. Nature 447: 550-555.
14. Greer EL, Brunet A, (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8: 113-127.
15. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M, et al. (2008) A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS genetics 4: e24.
16. Bishop NA, Guarente L, (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447: 545-549.
17. Lakowski B, Hekimi S, (1998) The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci U S A 95: 13091-13096.
18. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R, (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
19. Curtis R, O'Connor G, DiStefano PS, (2006) Aging networks in Caenorhabditis elegans: AMP-activated protein kinase (aak-2) links multiple aging and metabolism pathways. Aging Cell 5: 119-126.
20. Seglen PO, Gordon PB, (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79: 1889-1892.
21. Mordier S, Deval C, Bechet D, Tassa A, Ferrara M, (2000) Leucine limitation induces autophagy and activation of lysosome-dependent proteolysis in C2C12 myotubes through a mammalian target of rapamycin-independent signaling pathway. J Biol Chem 275: 29900-29906.
22. Lavieu G, Scarlatti F, Sala G, Levade T, Ghidoni R, et al. (2007) Is autophagy the key mechanism by which the sphingolipid rheostat controls the cell fate decision? Autophagy 3: 45-47.
23. Lavieu G, Scarlatti F, Sala G, Carpentier S, Levade T, et al. (2006) Regulation of autophagy by sphingosine kinase 1 and its role in cell survival during nutrient starvation. J Biol Chem 281: 8518-8527.
24. Munoz MJ, (2003) Longevity and heat stress regulation in Caenorhabditis elegans. Mech Ageing Dev 124: 43-48.
25. D'Mello N P, Childress AM, Franklin DS, Kale SP, Pinswasdi C, et al. (1994) Cloning and characterization of LAG1, a longevity-assurance gene in yeast. J Biol Chem 269: 15451-15459.
26. Huang X, Liu J, Dickson RC, (2012) Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet 8: e1002493.
27. Jiang JC, Kirchman PA, Zagulski M, Hunt J, Jazwinski SM, (1998) Homologs of the yeast longevity gene LAG1 in Caenorhabditis elegans and human. Genome Res 8: 1259-1272.
28. Guillas I, Jiang JC, Vionnet C, Roubaty C, Uldry D, et al. (2003) Human homologues of LAG1 reconstitute Acyl-CoA-dependent ceramide synthesis in yeast. J Biol Chem 278: 37083-37091.
29. Hars ES, Qi H, Ryazanov AG, Jin S, Cai L, et al. (2007) Autophagy regulates ageing in C. elegans. Autophagy 3: 93-95.
30. Lapierre LR, Hansen M, (2012) Lessons from C. elegans: signaling pathways for longevity. Trends Endocrinol Metab 23: 637-644.
31. Mair W, Dillin A, (2008) Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem 77: 727-754.
32. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, et al. (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17: 1646-1656.
33. Ponnusamy S, Meyers-Needham M, Senkal CE, Saddoughi SA, Sentelle D, et al. (2010) Sphingolipids and cancer: ceramide and sphingosine-1-phosphate in the regulation of cell death and drug resistance. Future Oncol 6: 1603-1624.
34. Beljanski V, Knaak C, Smith CD, (2010) A novel sphingosine kinase inhibitor induces autophagy in tumor cells. J Pharmacol Exp Ther 333: 454-464.
35. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
36. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
37. Kamath RS, Ahringer J, (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
38. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
39. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, et al. (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc Natl Acad Sci U S A 106: 2136-2141.
40. Sampaio JL, Gerl MJ, Klose C, Ejsing CS, Beug H, et al. (2011) Membrane lipidome of an epithelial cell line. Proc Natl Acad Sci U S A 108: 1903-1907.
41. Klose C, Surma MA, Gerl MJ, Meyenhofer F, Shevchenko A, et al. (2012) Flexibility of a eukaryotic lipidome-insights from yeast lipidomics. PLoS One 7: e35063.