DAF-16 and δ 9 desaturase genes promote cold tolerance in long-lived Caenorhabditis elegans age-1 mutants

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Savory, Fiona R ^a   Sait, Steven M ^a   Hope, Ian A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOMEDIN C; ACYL COENZYME A DESATURASE; AGE 1 PROTEIN, C ELEGANS; AGE-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; DAF 16 PROTEIN, C ELEGANS; DAF-16 PROTEIN, C ELEGANS; GREEN FLUORESCENT PROTEIN; INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; CAENORHABDITIS ELEGANS; CELLULAR DISTRIBUTION; COLD STRESS; COLD TOLERANCE; CONTROLLED STUDY; DAF 16 GENE; DELTA 9 DESATURASE GENE; DEVELOPMENTAL STAGE; FAT 5 GENE; FAT 6 GENE; FAT 7 GENE; GENE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE TARGETING; GENETIC VARIABILITY; LOW TEMPERATURE PROCEDURES; NONHUMAN; PHENOTYPIC VARIATION; SIGNAL TRANSDUCTION; SURVIVAL RATE; TEMPERATURE DEPENDENCE; TRANSCRIPTION REGULATION; TRANSITION TEMPERATURE; WILD TYPE; WORM; ACCLIMATIZATION; ANIMAL; COLD; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; RNA INTERFERENCE; TEMPERATURE; TIME;

CAENORHABDITIS ELEGANS;

ACCLIMATIZATION; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; COLD TEMPERATURE; GREEN FLUORESCENT PROTEINS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEAROYL-COA DESATURASE; TEMPERATURE; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 80052537036     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024550     Document Type: Article

References (76)

1. Kenyon C, (2010) The genetics of ageing. Nature 464: 504-512.
2. Friedman DB, Johnson TE, (1988) Three mutants that extend both mean and maximum life span of the nematode, Caenorhabditis elegans, define the age-1 gene. J Gerontol 43: 102-109.
3. 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.
4. Larsen PL, (1993) Aging and resistance to oxidative damage in Caenorhabditis elegans. Proc Natl Acad Sci U S A 90: 8905-8909.
5. Lithgow GJ, White TM, Hinerfeld DA, Johnson TE, (1994) Thermotolerance of a long-lived mutant of Caenorhabditis elegans. J Gerontol 49: B270-B276.
6. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, et al. (2001) Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292: 104-106.
7. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292: 107-110.
8. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, et al. (2003) IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421: 182-187.
9. Bonafe M, Barbieri M, Marchegiani F, Olivieri F, Ragno E, et al. (2003) Polymorphic variants of Insulin-Like Growth Factor I (IGF-I) receptor and phosphoinositide 3-kinase genes affect IGF-I plasma levels and human longevity. J Clin Endocrinol Metab 88: 3299-3304.
10. van Heemst D, Beekman M, Mooijaart SP, Heijmans BT, Brandt BW, et al. (2005) Reduced insulin/IGF-1 signalling and human longevity. Aging Cell 4: 79-85.
11. Henderson S, Johnson T, (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Current Biology 11: 1975-1980.
12. Lin K, Hsin H, Libina N, Kenyon C, (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nature Genetics 28: 139-145.
13. Lee SS, Kennedy S, Tolonen AC, Ruvkun G, (2003) DAF-16 target genes that control C. elegans life-span and metabolism. Science 300: 644-647.
14. 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.
15. Vanfleteren JR, (1993) Oxidative stress and ageing in Caenorhabditis elegans. J Biochem 292: 605-608.
16. Murakami S, Johnson TE, (1996) A genetic pathway conferring life extension and resistance to UV stress in Caenorhabditis elegans. Genetics 143: 1207-1218.
17. Barsyte D, Lovejoy DA, Lithgow GJ, (2001) Longevity and heavy metal resistance in daf-2 and age-1 long-lived mutants of Caenorhabditis elegans. The FASEB Journal 15: 627-634.
18. Scott BA, Avidan MS, Crowder CM, (2002) Regulation of hypoxic death in C. elegans by the insulin/IGF receptor homolog DAF-2. Science 296: 2388-2391.
19. Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, et al. (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300: 1921.
20. Lamitina ST, Strange K, (2005) Transcriptional targets of DAF-16 insulin signaling pathway protect C. elegans from extreme hypertonic stress. Am J Physiol Cell Physiol 288: 467-474.
21. Luckinbill LS, (1998) Selection for longevity confers resistance to low-temperature stress in Drosophila melanogaster. J Gerontol A Bio Sci Med Sci 53: B147-153.
22. Norry FM, Loeschcke VR, (2002) Longevity and resistance to cold stress in cold-stress selected lines and their controls in Drosophila melanogaster. J Evol Biol 15: 775-783.
23. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, et al. (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102: 3105-3110.
24. Lindquist S, (1986) The heat-shock response. Ann Rev Biochem 55: 1151-1191.
25. Hazel JR, (1995) Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Ann Rev Physiol 57: 19-42.
26. Cossins AR, (1994) Homeoviscous adaptation of biological membranes and its functional significance. In: Cossins A, editors. Temperature adaptation of biological membranes Portland Press pp. 63-76.
27. Tiku PE, Gracey AY, Macartney AI, Beynon RJ, Cossins AR, (1996) Cold-induced expression of Δ9 desaturase in carp by transcriptional and post-translational mechanisms. Science 271: 815-818.
28. Uemura M, Joseph RA, Steponkus PL, (1995) Cold acclimation of Arabidopsis thaliana: Effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiol 109: 15-30.
29. Wada H, Combos Z, Murata N, (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347: 200-203.
30. Ishizaki-Nishizawa O, Fujii T, Azuma M, Sekiguchi K, Murata N, et al. (1996) Low temperature resistance of higher plants is significantly enhanced by a non-specific cyanobacterial desaturase. Nature Biotechnol 14: 1003-1006.
31. Brock T, Browse J, Watts J, (2007) Fatty acid desaturation and the regulation of adiposity in Caenorhabditis elegans. Genetics 176: 865-875.
32. Gracey AY, Fraser EJ, Li W, Fang Y, Brass A, et al. (2004) Coping with cold: an integrative, multi-tissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci USA 101: 16970-16975.
33. Murray P, Hayward SAL, Govan GG, Gracey AY, Cossins AR, (2007) An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans. Proc Natl Acad Sci U S A 104: 5489-5494.
34. Schuster E, McElwee JJ, Tullet JMA, Doonan R, Matthijssens F, et al. (2010) DamID in C. elegans reveals longevity-associated targets of DAF-16/FoxO. Molecular Systems Biol 6: 399.
35. McElwee JJ, Schuster E, Blanc E, Thomas JH, Gems D, (2004) Shared transcriptional signature in Caenorhabditis elegans dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J Biol Chem 279: 44533-44543.
36. McElwee J, Schuster E, Blanc E, Thornton J, Gems D, (2006) Diapause-associated metabolic traits reiterated in long-lived daf-2 mutants in the nematode Caenorhabditis elegans. Mechanisms of Ageing and Development 127: 458-472.
37. Wang J, Kim SK, (2003) Global analysis of dauer gene expression in Caenorhabditis elegans. Development 130: 1621-1634.
38. Dusenbery DB, Barr J, (1980) Thermal limits and chemotaxis in mutants of the nematode Caenorhabditis elegans defective in thermotaxis. J Comp Physiol 137: 353-356.
39. Lyons JM, Keith AD, Thomason IJ, (1975) Temperature-induced phase transitions in nematode lipids and their influence on respiration. J Nematol 7: 98-104.
40. Watts JL, Browse J, (2000) A palmitoyl-CoA specific Δ9 fatty acid desaturase from Caenorhabditis elegans. Biochem Biophys Res Commun 272: 263-269.
41. Brock TJ, Browse J, Watts JL, (2006) Genetic regulation of unsaturated fatty acid composition in C. elegans. PLoS Genet 2: 997-1005.
42. David RJ, Gibert P, Pla E, Petavy G, Karan D, et al. (1998) Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. J Therm Biol 23: 291-299.
43. Schmookler Reis RJS, Xu LL, Lee H, Chae M, Thaden JJ, et al. (2011) Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants. Aging 3: 125-147.
44. Honda Y, Tanaka M, Honda S, (2010) Trehalose extends longevity in the nematode Caenorhabditis elegans. Aging Cell 9: 558-569.
45. Schade B, Jansen G, Whiteway M, Entian KD, Thomas DY, (2004) Cold adaptation in budding yeast. Molec Biol Cell 15: 5492-5502.
46. Jagdale GB, Grewal PS, Salminen SO, (2005) Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. J Parasitol 91: 988-994.
47. Benoit JB, Lopez-Martinez G, Elnitsky MA, Lee RE, Denlinger DL, (2009) Dehyration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. Comp Biochem Physiol A 152: 518-523.
48. Khani A, Moharramipour S, Barzegar M, (2007) Cold tolerance and trehalose accumulation in overwintering larvae of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). Eur J Entomology 104: 385-392.
49. Overgaard J, Sørensen JG, Søren OP, Loeschcke V, Holmstrup M, (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 51: 1173-1182.
50. Lee RE, Chen CP, Denlinger DL, (1987) A rapid cold-hardening process in insects. Science 238: 1415-1417.
51. Boggs JM, Rangaraj G, (1985) Phase transitions and fatty acid spin label behavior in interdigitated lipid phases induced by glycerol. Biochim Biophys Acta 816: 221-233.
52. Crowe JH, Hoekstra FA, Crowe LM, (1992) Anhydrobiosis. Ann Rev Physiol 54: 579-599.
53. Pacheco A, Pereira C, Almeida MJ, Sousa MJ, (2009) Small heat-shock protein Hsp12 contributes to yeast tolerance to freezing stress. Microbiology 155: 2021-2028.
54. Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SAL, et al. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci U S A 104: 11130-11137.
55. Joanisse DR, Storey KB, (1996) Oxidative stress and antioxidants in overwintering larvae of cold-hardy goldenrod gall insects. J Exp Biol 199: 1483-1491.
56. Dai F, Huang Y, Zhou M, Zhang G, (2009) The influence of cold acclimation on antioxidative enzymes and antioxidants in sensitive and tolerant barley cultivars. Biologia Plantarum 53: 257-262.
57. Thomashow MF, (1999) Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Physiol Plant Mol Biol 50: 571-599.
58. Henderson ST, Bonafe M, Johnson TE, (2006) daf-16 protects the nematode Caenorhabditis elegans during food deprivation. J Gerontol A Biol Sci Med Sci 61: 444-60.
59. Horikawa M, Sakamoto K, (2009) Fatty-acid metabolism is involved in stress-resistance mechanisms of Caenorhabditis elegans. Biochem Biophys Res Comm 390: 1402-1407.
60. Wolf M, Nunes F, Henkel A, Heinick A, Paul RJ, (2008) The MAP kinase JNK-1 of Caenorhabditis elegans: location, activation and influences over temperature-dependent insulin-like signalling, stress responses and fitness. J Cell Physiol 214: 721-229.
61. Gasparetti AL, de Souza CT, Pereira-da-Silva M, Oliviera RLGS, Saad MJA, et al. (2003) Cold exposure induces tissue-specific modulation of the insulin-signalling pathway in Rattus norvegicus. J Physiol 552: 149-162.
62. Torsoni AM, Carvalheira JB, Pereira-Da-Silva M, de Carvalho-Filho MA, Saad MJA, et al. (2003) Molecular and functional resistance to insulin in hypothalamus of rats exposed to cold. Am J Physiol Endo 285: E216-E223.
63. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, et al. (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2: e183.
64. Kültz D, (2005) Molecular and evolutionary basis of the cellular stress response. Ann Rev Physiol 67: 225-257.
65. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, et al. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421: 268-272.
66. van Gilst MR, Hadjivassiliou H, Jolly A, Yamamoto KR, (2005) Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol 3: 301-312.
67. Yang F, Vought BW, Satterlee JS, Walker AK, Sun ZYJ, et al. (2006) An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442: 700-704.
68. Bale JS, Hayward SAL, (2010) Insect overwintering in a changing climate. J Exp Biol 213: 980-994.
69. Denlinger DL, (2002) Regulation of diapause. Ann Rev Entomol 47: 93-122.
70. Sim C, Denlinger DL, (2008) Insulin signalling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc Natl Acad Sci U S A 105: 6777-6781.
71. Williams KD, Busto M, Suster ML, So AKC, Ben-Shahar Y, et al. (2006) Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proc Natl Acad Sci U S A 103: 15911-15915.
72. Golden JW, Riddle DL, (1984) The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food and temperature. Dev Biol 102: 368-378.
73. Kamath RS, Ahringer J, (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
74. R Development Core Team (2010) R: A language and environment for statistical computing. Available: http://www.R-project.org Accessed 2011 Jun 16.
75. Breslow NE, Clayton DG, (1993) Approximate inference in generalized linear mixed models. J Am Stat Assoc 88: 9-25.
76. Agresti A, (2002) Categorical data analysis New York Wiley-Interscience Publishers.