Sphingolipid metabolism regulates development and lifespan in Caenorhabditis elegans

Mechanisms of Ageing and Development

Volumn 143-144, Issue , 2014, Pages 9-18

  Cutler, Roy G ^a   Thompson, Kenneth W ^a   Camandola, Simonetta ^a   Mack, Kendra T ^a   Mattson, Mark P ^a,b  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ceramide; Gangliosides; Longevity; Oxidative stress; Sphingomyelin

Indexed keywords

CERAMIDE; CERAMIDE GLUCOSYLTRANSFERASE; FATTY ACID; GANGLIOSIDE; GANGLIOSIDE GM1; SERINE PALMITOYL TRANSFERASE; SMALL INTERFERING RNA; SPHINGOLIPID; SPHINGOMYELIN; THERMOZYMOCIDIN; TRANSFERASE; UNCLASSIFIED DRUG; GLUCOSYLTRANSFERASE; SERINE PALMITOYLTRANSFERASE;

AGING; ARTICLE; BIOACCUMULATION; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DRUG DETERMINATION; EGG LAYING; ENZYME ACTIVITY; ENZYME ASSAY; FATTY ACID DESATURATION; GROWTH INHIBITION; GROWTH RATE; LIFESPAN; LIPID ANALYSIS; LIPOGENESIS; MOLECULAR DYNAMICS; NONHUMAN; PARASITE DEVELOPMENT; PARASITE IDENTIFICATION; REPRODUCTION; RNA INTERFERENCE; SPHINGOLIPID METABOLISM; TRANSCRIPTION ELONGATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL SURVIVAL; GENETICS; LONGEVITY; METABOLISM; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL SURVIVAL; CERAMIDES; GANGLIOSIDES; GLUCOSYLTRANSFERASES; LONGEVITY; SERINE C-PALMITOYLTRANSFERASE; SIGNAL TRANSDUCTION; SPHINGOLIPIDS;

EID: 84919392954     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2014.11.002     Document Type: Article

References (47)

1. Bielawska A., Greenberg M.S., Perry D., Jayadev S., Shayman J.A., McKay C., Hannun Y.A. (1S, 2R)-D-erythro-2-(N-myristoylamino)-1-phenyl-1-propanol as an inhibitor of ceramidase. J. Biol. Chem. 1996, 271:12646-12654.
2. Bismuth J., Lin P., Yao Q., Chen C. Ceramide a common pathway for atherosclerosis?. Atherosclerosis 2008, 196:497-504.
3. Bobryshev Y.V., Golovanova N.K., Tra D., Samovilova N.N., Gracheva E.V., Efremov E.E., Sobolev A.Y., Yurchenko Y.V., Lor R.S., Cao W., Lu J., Saito M., Prokazova N.V. Expression of GM3 synthase in human atherosclerotic lesions. Atherosclerosis 2006, 184:63-71.
4. Cutler R.G., Pedersen W.A., Camandola S., Rothstein J.D., Mattson M.P. Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis. Ann. Neurol. 2002, 52:448-457.
5. Cutler R.G., Haughey N.J., Tammara A., McArthur J.C., Nath A., Reid R., Vargas D.L., Pardo C.A., Mattson M.P. Dysregulation of sphingolipid and sterol metabolism by ApoE4 in HIV dementia. Neurology 2004, 63:626-630.
6. Erdreich-Epstein A., Tran L.B., Cox O.T., Huang E.Y., Laug W.E., Shimada H., Millard M. Endothelial apoptosis induced by inhibition of integrins alphaVbeta3 and alphaVbeta5 involves ceramide metabolic pathways. Blood 2005, 105:4353-4361.
7. Euling S.Y., Selevan S.G., Pescovitz O.H., Skakkebaek N.E. Role of environmental factors in the timing of puberty. Pediatrics 2008, 121:S167-S171.
8. Fielenbach N., Antebi A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev. 2008, 22:2149-2165.
9. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
10. Gami M.S., Wolkow C.A. Studies of Caenorhabditis elegans DAF-2/insulin signaling reveal targets for pharmacological manipulation of lifespan. Aging Cell 2006, 5:31-37.
11. Gerisch B., Weitzel C., Kober-Eisermann C., Rottiers V., Antebi A. A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev. Cell 2001, 1:841-851.
12. Gerstbrein B., Stamatas G., Kollias N., Driscoll M. In vivo spectrofluorimetry reveals endogenous biomarkers that report healthspan and dietary restriction in Caenorhabditis elegans. Aging Cell 2005, 4:127-137.
13. Gulbins E., Kolesnick R. Raft ceramide in molecular medicine. Oncogene 2003, 22:7070-7077.
14. Hanada K., Nishijima M., Fujita T., Kobayashi S. Specificity of inhibitors of serine palmitoyltransferase (SPT), a key enzyme in sphingolipid biosynthesis, in intact cells. A novel evaluation system using an SPT-defective mammalian cell mutant. Biochem. Pharmacol. 2000, 59:1211-1216.
15. Hannun Y.A., Obeid L.M. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 2008, 9:139-150.
16. Hayashi H., Kimura N., Yamaguchi H., Hasegawa K., Yokoseki T., Shibata M., Yamamoto N., Michikawa M., Yoshikawa Y., Terao K., Matsuzaki K., Lemere C.A., Selkoe D.J., Naiki H., Yanagisawa K. A seed for Alzheimer amyloid in the brain. J. Neurosci. 2004, 24:4894-4902.
17. Henderson S.T., Johnson T.E. daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr. Biol. 2001, 11:1975-1980.
18. Holland W.L., Bikman B.T., Wang L.P., Yuguang G., Sargent K.M., Bulchand S., Knotts T.A., Shui G., Clegg D.J., Wenk M.R., Pagliassotti M.J., Scherer P.E., Summers S.A. Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest. 2011, 121:1858-1870.
19. Hsin H., Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 1999, 399:362-366.
20. Huang X., Liu J., Dickson R.C. Down-regulating sphingolipid synthesis increases yeast lifespan. PLoS Genet. 2012, 8(2):e1002493.
21. Inokuchi J., Momosaki K., Shimeno H., Nagamatsu A., Radin N.S. Effects of D-threo-PDMP, an inhibitor of glucosylceramide synthetase, on expression of cell surface glycolipid antigen and binding to adhesive proteins by B16 melanoma cells. J. Cell. Physiol. 1989, 141:573-583.
22. Johnson T.E., Mitchell D.H., Kline S., Kemal R., Foy J. Arresting development arrests aging in the nematode Caenorhabditis elegans. Mech. Ageing Dev. 1984, 28:23-40.
23. Kimura K.D., Tissenbaum H.A., Liu Y., Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 1997, 277:942-946.
24. Kirkwood T.B., Rose M.R. Evolution of senescence: late survival sacrificed for reproduction. Philos. Trans. R. Soc. London B Biol. Sci. 1991, 332:15-24.
25. Kolesnick R.N., Tilly J.L. A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J. 2005, 19:860-862.
26. Li Z., Hailemariam T.K., Zhou H., Li Y., Duckworth D.C., Peake D.A., Zhang Y., Kuo M.S., Cao G., Jiang X.C. Inhibition of sphingomyelin synthase (SMS) affects intracellular sphingomyelin accumulation and plasma membrane lipid organization. Biophys. Acta 2007, 1771:1186-1194.
27. Lightle S.A., Oakley J.I., Nikolova-Karakashian M.N. Activation of sphingolipid turnover and chronic generation of ceramide and sphingosine in liver during aging. Mech. Ageing Dev. 2000, 120:111-125.
28. Lin X., Hengartner M.O., Kolesnick R. Caenorhabditis elegans contains two distinct acid sphingomyelinases. J. Biol. Chem. 1998, 273:14374-14379.
29. Liu J., Huang X., Withers B.R., Blalock E., Liu K., Dickson R.C. Reducing sphingolipid synthesis orchestrates global changes to extend yeast lifespan. Aging Cell 2013, 12:3-841.
30. Lochnit G., Bongaarts R., Geyer R. Searching new targets for anthelminthic strategies: interference with glycosphingolipid biosynthesis and phosphorylcholine metabolism affects development of Caenorhabditis elegans. Int. J. Parasitol. 2005, 35:911-9236.
31. Lopez P.H., Schnaar R.L. Gangliosides in cell recognition and membrane protein regulation. Curr. Opin. Struct. Biol. 2009, 19:549-557.
32. Marza E., Simonsen K.T., Færgeman N.J., Lesa G.M. Expression of ceramide glucosyltransferases, which are essential for glycosphingolipid synthesis, is only required in a small subset of C. elegans cells. J. Cell Sci. 2009, 122:122-833.
33. Mattison J.A., Lane M.A., Roth G.S., Ingram D.K. Calorie restriction in rhesus monkeys. Exp. Gerontol. 2003, 38:35-46.
34. Merrill A.H., Jones D.D. An update of the enzymology and regulation of sphingomyelin metabolism. Biochim. Biophys. Acta 1990, 1044:1-12.
35. Miyake Y., Kozutsumi Y., Nakamura S., Fujita T., Kawasaki T. Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem. Biophys. Res. Commun. 1995, 211:396-403.
36. Mooradian A.D. Dyslipidemia in type 2 diabetes mellitus. Nat. Clin. Pract. Endocrinol. Metab. 2009, 5:150-159.
37. Mukhopadhyay A., Tissenbaum H.A. Reproduction and longevity: secrets revealed by C. elegans. Trends Cell Biol. 2007, 17:65-71.
38. Ricklefs R.E. Embryo development and ageing in birds and mammals. Proc. Biol. Sci. 2006, 273:2077-2082.
39. Schenck M., Carpinteiro A., Grassmé H., Lang F., Gulbins E. Ceramide physiological and pathophysiological aspects. Arch. Biochem. Biophys. 2007, 462:171-175.
40. Stommel A., Berlet H.H., Debuch H. Buoyant density and lipid composition of purified myelin of aging human brain. Mech. Ageing Dev. 1989, 48:1-14.
41. Straczkowski M., Kowalska I. The role of skeletal muscle sphingolipids in the development of insulin resistance. Rev. Diabet Stud. 2008, 5:13-24.
42. Tatar M., Bartke A., Antebi A. The endocrine regulation of aging by insulin-like signals. Science 2003, 299:1346-1351.
43. Uemura K., Sugiyama E., Taketomi T. Effects of an inhibitor of glucosylceramide synthase on glycosphingolipid synthesis and neurite outgrowth in murine neuroblastoma cell lines. J. Biochem. 1991, 110:96-102.
44. Venable M.E., Webb-Froehlich L.M., Sloan E.F., Thomley J.E. Shift in sphingolipid metabolism leads to an accumulation of ceramide in senescence. Mech. Ageing Dev. 2006, 127:473-480.
45. Watts J.L., Browse J. Dietary manipulation implicates lipid signaling in the regulation of germ cell maintenance in C. elegans. Dev. Biol. 2006, 292:381-392.
46. Wu M., Singh S.B., Wang J., Chung C.C., Salituro G., Karanam B.V., Lee S.H., Powles M., Ellsworth K.P., Lassman M.E., Miller C., Myers R.W., Tota M.R., Zhang B.B., Li C. Antidiabetic and antisteatotic effects of the selective fatty acid synthase (FAS) inhibitor platensimycin in mouse models of diabetes. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5378-5383.
47. Yappert M.C., Rujoi M., Borchman D., Vorobyov I., Estrada R. Glycero- versus sphingo-phospholipids: correlations with human and non-human mammalian lens growth. Exp. Eye Res. 2003, 76:725-734.