PAQR-2 Regulates Fatty Acid Desaturation during Cold Adaptation in

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C.
elegans PAQR-2 is homologous to the insulin-sensitizing adiponectin receptors in mammals, and essential for adaptation to growth at 15°C, a low but usually acceptable temperature for this organism. By screening for novel paqr-2 suppressors, we identified mutations in genes involved in phosphatidylcholine synthesis (cept-1, pcyt-1 and sams-1) and fatty acid metabolism (ech-7, hacd-1, mdt-15, nhr-49 and sbp-1). We then show genetic evidence that paqr-2, phosphatidylcholines, sbp-1 and Δ9-desaturases form a cold adaptation pathway that regulates the increase in unsaturated fatty acids necessary to retain membrane fluidity at low temperatures. This model is supported by the observations that the paqr-2 suppressors normalize the levels of saturated fatty acids, and that low concentrations of detergents that increase membrane fluidity can rescue the paqr-2 mutant.

Vyšlo v časopise: PAQR-2 Regulates Fatty Acid Desaturation during Cold Adaptation in. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003801
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003801

Souhrn

Zdroje

1. HazelJR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57 : 19–42.

2. GuschinaIA, HarwoodJL (2006) Mechanisms of temperature adaptation in poikilotherms. FEBS Lett 580 : 5477–5483 doi:10.1016/j.febslet.2006.06.066

3. CrockettEL (2008) The cold but not hard fats in ectotherms: consequences of lipid restructuring on susceptibility of biological membranes to peroxidation, a review. J Comp Physiol, B 178 : 795–809 doi:10.1007/s00360-008-0275-7

4. HaywardSAL, MurrayPA, GraceyAY, CossinsAR (2007) Beyond the lipid hypothesis: mechanisms underlying phenotypic plasticity in inducible cold tolerance. Adv Exp Med Biol 594 : 132–142 doi:_10.1007/978-0-387-39975-1_12

5. BrockTJ, BrowseJ, WattsJL (2007) Fatty acid desaturation and the regulation of adiposity in Caenorhabditis elegans. Genetics 176 : 865–875 doi:10.1534/genetics.107.071860

6. OhtsuT, KimuraMT, KatagiriC (1998) How Drosophila species acquire cold tolerance–qualitative changes of phospholipids. Eur J Biochem 252 : 608–611.

7. SavoryFR, SaitSM, HopeIA (2011) DAF-16 and Δ9 desaturase genes promote cold tolerance in long-lived Caenorhabditis elegans age-1 mutants. PLoS ONE 6: e24550 doi:10.1371/journal.pone.0024550

8. OvergaardJ, SørensenJG, PetersenSO, LoeschckeV, HolmstrupM (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 51 : 1173–1182 doi:10.1016/j.jinsphys.2005.06.007

9. PeiJ, MillayDP, OlsonEN, GrishinNV (2011) CREST–a large and diverse superfamily of putative transmembrane hydrolases. Biol Direct 6 : 37 doi:10.1186/1745-6150-6-37

10. ColinetH, LeeSF, HoffmannA (2010) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277 : 174–185 doi:10.1111/j.1742-4658.2009.07470.x

11. TanakaT, IkitaK, AshidaT, MotoyamaY, YamaguchiY, et al. (1996) Effects of growth temperature on the fatty acid composition of the free-living nematode Caenorhabditis elegans. Lipids 31 : 1173–1178.

12. SvenssonE, OlsenL, MörckC, BrackmannC, EnejderA, et al. (2011) The Adiponectin Receptor Homologs in C. elegans Promote Energy Utilization and Homeostasis. PLoS ONE 6: e21343.

13. YamauchiT, KamonJ, ItoY, TsuchidaA, YokomizoT, et al. (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423 : 762–769 doi:10.1038/nature01705

14. YamauchiT, NioY, MakiT, KobayashiM, TakazawaT, et al. (2007) Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 13 : 332–339 doi:10.1038/nm1557

15. HollandWL, MillerRA, WangZV, SunK, BarthBM, et al. (2011) Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat Med 17 : 55–63 doi:10.1038/nm.2277

16. MurrayP, HaywardSAL, GovanGG, GraceyAY, CossinsAR (2007) An explicit test of the phospholipid saturation hypothesis of acquired cold tolerance in Caenorhabditis elegans. Proc Natl Acad Sci USA 104 : 5489–5494 doi:10.1073/pnas.0609590104

17. van GilstMR, HadjivassiliouH, JollyA, YamamotoKR (2005) Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans. PLoS Biol 3: e53 doi:10.1371/journal.pbio.0030053

18. PatharePP, LinA, BornfeldtKE, TaubertS, van GilstMR (2012) Coordinate regulation of lipid metabolism by novel nuclear receptor partnerships. PLoS Genet 8: e1002645 doi:10.1371/journal.pgen.1002645

19. WalkerA, JacobsR, WattsJ, RottiersV (2011) A Conserved SREBP-1/Phosphatidylcholine Feedback Circuit Regulates Lipogenesis in Metazoans. Cell 147 : 840–852.

20. WangZ, SherwoodDR (2011) Dissection of genetic pathways in C. elegans. Methods Cell Biol 106 : 113–157 doi:10.1016/B978-0-12-544172-8.00005-0

21. ZurynS, Le GrasS, JametK, JarriaultS (2010) A strategy for direct mapping and identification of mutations by whole-genome sequencing. Genetics 186 : 427–430 doi:10.1534/genetics.110.119230

22. SarinS, PrabhuS, O'MearaMM, Pe'erI, HobertO (2008) Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nat Methods 5 : 865–867 doi:10.1038/nmeth.1249

23. YangF, VoughtBW, SatterleeJS, WalkerAK, Jim SunZ-Y, et al. (2006) An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442 : 700–704 doi:10.1038/nature04942

24. TaubertS, van GilstMR, HansenM, YamamotoKR (2006) A Mediator subunit, MDT-15, integrates regulation of fatty acid metabolism by NHR-49-dependent and -independent pathways in C. elegans. Genes Dev 20 : 1137–1149 doi:10.1101/gad.1395406

25. AthertonHJ, JonesOAH, MalikS, MiskaEA, GriffinJL (2008) A comparative metabolomic study of NHR-49 in Caenorhabditis elegans and PPAR-alpha in the mouse. FEBS Lett 582 : 1661–1666 doi:10.1016/j.febslet.2008.04.020

26. McKayRM, McKayJP, AveryL, GraffJM (2003) C. elegans: a model for exploring the genetics of fat storage. Dev Cell 4 : 131–142.

27. BrockTJ, BrowseJ, WattsJL (2006) Genetic regulation of unsaturated fatty acid composition in C. elegans. PLoS Genet 2: e108 doi:10.1371/journal.pgen.0020108

28. HenriksenJR, AndresenTL, FeldborgLN, DuelundL, IpsenJH (2010) Understanding Detergent Effects on Lipid Membranes: A Model Study of Lysolipids. Biophysj 98 : 2199–2205 doi:10.1016/j.bpj.2010.01.037

29. AhyayauchH, BennounaM, AlonsoA, GoñiFM (2010) Detergent Effects on Membranes at Subsolubilizing Concentrations: Transmembrane Lipid Motion, Bilayer Permeabilization, and Vesicle Lysis/Reassembly Are Independent Phenomena. Langmuir 26 : 7307–7313 doi:10.1021/la904194a

30. YodaM, NakanoY, TobeT, ShiodaS, Choi-MiuraNH, et al. (2001) Characterization of mouse GBP28 and its induction by exposure to cold. Int J Obes Relat Metab Disord 25 : 75–83.

31. ImbeaultP, DépaultI, HamanF (2009) Cold exposure increases adiponectin levels in men. Metab Clin Exp 58 : 552–559 doi:10.1016/j.metabol.2008.11.017

32. KleinI, Sanchez-AlavezM, TabareanI, SchaeferJ, HolmbergKH, et al. (2011) AdipoR1 and 2 are expressed on warm sensitive neurons of the hypothalamic preoptic area and contribute to central hyperthermic effects of adiponectin. Brain Res 1423 : 1–9 doi:10.1016/j.brainres.2011.09.019

33. WongGW, WangJ, HugC, TsaoT-S, LodishHF (2004) A family of Acrp30/adiponectin structural and functional paralogs. Proc Natl Acad Sci USA 101 : 10302–10307.

34. Sulston JE, Hodgkin JA (1988) Methods. In: Wood WB, editor. The Nematode Caernorhabditis elegans. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. pp. 587–606.

35. BigelowH, DoitsidouM, SarinS, HobertO (2009) MAQGene: software to facilitate C. elegans mutant genome sequence analysis. Nat Methods 6 : 549 doi:10.1038/nmeth.f.260

36. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9 : 671–675 doi:10.1038/nmeth.2089

37. FolchJ, LeesM, Sloane StanleyGH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226 : 497–509.

38. JungHR, SylvänneT, KoistinenKM, TarasovK, KauhanenD, et al. (2011) High throughput quantitative molecular lipidomics. Biochim Biophys Acta 1811 : 925–934 doi:10.1016/j.bbalip.2011.06.025

39. EjsingCS, SampaioJL, SurendranathV, DuchoslavE, EkroosK, et al. (2009) Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proceedings of the National Academy of Sciences 106 : 2136–2141 doi:10.1073/pnas.0811700106

40. EkroosK, EjsingCS, BahrU, KarasM, SimonsK, et al. (2003) Charting molecular composition of phosphatidylcholines by fatty acid scanning and ion trap MS3 fragmentation. J Lipid Res 44 : 2181–2192 doi:10.1194/jlr.D300020-JLR200

41. MurphyRC, JamesPF, McAnoyAM, KrankJ, DuchoslavE, et al. (2007) Detection of the abundance of diacylglycerol and triacylglycerol molecular species in cells using neutral loss mass spectrometry. Anal Biochem 366 : 59–70 doi:10.1016/j.ab.2007.03.012