Activation of the endoplasmic reticulum unfolded protein response by lipid disequilibrium without disturbed proteostasis in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 22, 2014, Pages

  Hou, Nicole S ^a,b,c   Gutschmidt, Aljona ^d,e   Choi, Daniel Y ^a,b   Pather, Keouna ^a,b   Shi, Xun ^f   Watts, Jennifer L ^f   Hoppe, Thorsten ^d,e   Taubert, Stefan ^a,b,c  

^a Centre for Molecular Medicine and Therapeutics   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF COLOGNE   (Germany)

^f WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

C. elegans; Cardiolipin; MED15; Mediator complex

Indexed keywords

ACYL COENZYME A DESATURASE; MEDIATOR COMPLEX; MEDIATOR COMPLEX SUBUNIT MDT 15; MEMBRANE LIPID; MEMBRANE PHOSPHOLIPID; PHOSPHATIDYLCHOLINE; S ADENOSYL METHIONINE SYNTHETASE; SYNTHETASE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FATTY ACID DESATURATION; GENE INACTIVATION; GENE MUTATION; IN VIVO STUDY; LIPID HOMEOSTASIS; MEMBRANE FLUIDITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN MISFOLDING; UNFOLDED PROTEIN RESPONSE;

C. ELEGANS; CARDIOLIPIN; MED15; MEDIATOR COMPLEX;

ACYL COENZYME A; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARDIOLIPINS; ENDOPLASMIC RETICULUM; FATTY ACIDS; HOMEOSTASIS; LIPIDS; MITOCHONDRIA; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PROTEOSTASIS DEFICIENCIES; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 84901832063     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318262111     Document Type: Article

References (55)

1. Conaway RC, Conaway JW (2011) Function and regulation of the Mediator complex. Curr Opin Genet Dev 21(2):225-230.
2. Malik S, Roeder RG (2010) The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 11(11):761-772.
3. Yang F, et al. (2006) An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442(7103):700-704. (Pubitemid 44215326)
4. Taubert S, Van Gilst MR, Hansen M, Yamamoto KR (2006) A Mediator subunit, MDT-15, integrates regulation of fatty acidmetabolismby NHR-49-dependent and -independent pathways in C. elegans. Genes Dev 20(9):1137-1149.
5. Taubert S, Hansen M, Van Gilst MR, Cooper SB, Yamamoto KR (2008) The Mediator subunit MDT-15 confers metabolic adaptation to ingested material. PLoS Genet 4(2):e1000021.
6. Fire A, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391(6669):806-811. (Pubitemid 28099681)
7. Goh GYS, et al. (2013) The conserved Mediator subunit MDT-15 is required for oxidative stress responses in C. elegans. Aging Cell.
8. Brock TJ, Browse J, Watts JL (2006) Genetic regulation of unsaturated fatty acid composition in C. elegans. PLoS Genet 2(7):e108.
9. Watts JL, Browse J (2002) Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc Natl Acad Sci USA 99(9):5854-5859. (Pubitemid 34493229)
10. Hagen RM, Rodriguez-Cuenca S, Vidal-Puig A (2010) An allostatic control of membrane lipid composition by SREBP1. FEBS Lett 584(12):2689-2698.
11. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112-124. (Pubitemid 351158912)
12. Ariyama H, Kono N, Matsuda S, Inoue T, Arai H (2010) Decrease in membrane phospholipid unsaturation induces unfolded protein response. J Biol Chem 285(29):22027-22035.
13. Fu S, et al. (2011) Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473(7348):528-531.
14. Lagace TA, Ridgway ND (2013) The role of phospholipids in the biological activity and structure of the endoplasmic reticulum. Biochim Biophys Acta 1833(11):2499-2510.
15. Cao SS, Kaufman RJ (2013) Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin Ther Targets 17(4):437-448.
16. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8(7):519-529. (Pubitemid 46985379)
17. Wang S, Kaufman RJ (2012) The impact of the unfolded protein response on human disease. J Cell Biol 197(7):857-867.
18. Gardner BM, Walter P (2011) Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333(6051):1891-1894.
19. Pineau L, et al. (2009) Lipid-induced ER stress: Synergistic effects of sterols and saturated fatty acids. Traffic 10(6):673-690.
20. Ozcan U, et al. (2006) Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313(5790):1137-1140. (Pubitemid 44300242)
21. Volmer R, van der Ploeg K, Ron D (2013) Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci USA 110(12):4628-4633.
22. Kitai Y, et al. (2013) Membrane lipid saturation activates IRE1α without inducing clustering. Genes Cells 18(9):798-809.
23. Pellegrino MW, Nargund AM, Haynes CM (2013) Signaling the mitochondrial unfolded protein response. Biochim Biophys Acta 1833(2):410-416.
24. Heifetz A, Keenan RW, Elbein AD (1979) Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl-phosphate Glc-NAc-1-phosphate transferase. Biochemistry 18(11):2186-2192.
25. Glover-Cutter KM, Lin S, Blackwell TK (2013) Integration of the unfolded protein and oxidative stress responses through SKN-1/Nrf. PLoS Genet 9(9):e1003701.
26. Calfon M, et al. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415(6867):92-96. (Pubitemid 34062456)
27. Deguil J, et al. (2011) Modulation of lipid-induced ER stress by fatty acid shape. Traffic 12(3):349-362.
28. Shen X, et al. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107(7):893-903. (Pubitemid 34084980)
29. Shen X, Ellis RE, Sakaki K, Kaufman RJ (2005) Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet 1(3):e37.
30. Struwe WB, et al. (2009) Modeling a congenital disorder of glycosylation type I in C. elegans: a genome-wide RNAi screen for N-glycosylation-dependent loci. Glycobiology 19(12):1554-1562.
31. Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39(3):257-288. (Pubitemid 30224706)
32. Schipanski A, et al. (2013) A novel interaction between aging and ER overload in a protein conformational dementia. Genetics 193(3):865-876.
33. Natarajan B, Gaur R, Hemmingsson O, Kao G, Naredi P (2013) Depletion of the ER chaperone ENPL-1 sensitizes C. elegans to the anticancer drug cisplatin. Worm 2(1):e24059.
34. Melo JA, Ruvkun G (2012) Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 149(2):452-466.
35. Miedel MT, et al. (2012) A pro-cathepsin L mutant is a luminal substrate for endoplasmic-reticulum-associated degradation in C. elegans. PLoS ONE 7(7):e40145.
36. Zwaal RR, et al. (2001) The sarco-endoplasmic reticulum Ca2+ ATPase is required for development and muscle function in Caenorhabditis elegans. J Biol Chem 276(47):43557-43563.
37. Sakaki K, et al. (2012) RNA surveillance is required for endoplasmic reticulum homeostasis. Proc Natl Acad Sci USA 109(21):8079-8084.
38. Thibault G, et al. (2012) The membrane stress response buffers lethal effects of lipid disequilibrium by reprogramming the protein homeostasis network. Mol Cell 48(1):16-27.
39. Walker AK, et al. (2011) A conserved SREBP-1/phosphatidylcholine feedback circuit regulates lipogenesis in metazoans. Cell 147(4):840-852.
40. Satouchi K, Hirano K, Sakaguchi M, Takehara H, Matsuura F (1993) Phospholipids from the free-living nematode Caenorhabditis elegans. Lipids 28(9):837-840. (Pubitemid 23277649)
41. Watts JL, Browse J (2000) A palmitoyl-CoA-specific delta9 fatty acid desaturase from Caenorhabditis elegans. Biochem Biophys Res Commun 272(1):263-269. (Pubitemid 30444932)
42. Cnop M, et al. (2007) Selective inhibition of eukaryotic translation initiation factor 2 alpha dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic beta-cell dysfunction and apoptosis. J Biol Chem 282(6):3989-3997. (Pubitemid 47084497)
43. Wei Y, Wang D, Topczewski F, Pagliassotti MJ (2006) Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 291(2):E275-E281. (Pubitemid 44035286)
44. Sakamoto T, et al. (2012) Deficiency of cardiolipin synthase causes abnormal mitochondrial function and morphology in germ cells of Caenorhabditis elegans. J Biol Chem 287(7):4590-4601.
45. Wei Y, Wang D, Gentile CL, Pagliassotti MJ (2009) Reduced endoplasmic reticulum luminal calcium links saturated fatty acid-mediated endoplasmic reticulum stress and cell death in liver cells. Mol Cell Biochem 331(1-2):31-40.
46. Cho JH, Bandyopadhyay J, Lee J, Park CS, Ahnn J (2000) Two isoforms of sarco/endoplasmic reticulum calcium ATPase (SERCA) are essential in Caenorhabditis elegans. Gene 261(2):211-219. (Pubitemid 32146491)
47. Hansen M, Hsu A-L, Dillin A, Kenyon C (2005) New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet 1(1):119-128.
48. Henis-Korenblit S, et al. (2010) Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc Natl Acad Sci USA 107(21):9730-9735.
49. Hou NS, Taubert S (2012) Function and Regulation of Lipid Biology in Caenorhabditis elegans Aging. Front Physiol 3:143.
50. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71-94.
51. Simmer F, et al. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 12(15):1317-1319. (Pubitemid 34869882)
52. Yoneda T, et al. (2004) Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. J Cell Sci 117(Pt 18):4055-4066. (Pubitemid 39328294)
53. Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157(3):1217-1226. (Pubitemid 32225014)
54. Kamath RS, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421(6920):231-237. (Pubitemid 36139121)
55. Shi X, et al. (2013) Regulation of lipid droplet size and phospholipid composition by stearoyl-CoA desaturase. J Lipid Res 54(9):2504-2514.