Using natural variation in Drosophila to discover previously unknown endoplasmic reticulum stress genes

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

Volumn 110, Issue 22, 2013, Pages 9013-9018

  Chow, Clement Y ^a   Wolfner, Mariana F ^a   Clark, Andrew G ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUNICAMYCIN; X BOX BINDING PROTEIN 1;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; MICROARRAY ANALYSIS; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; DATABASES, GENETIC; DROSOPHILA; ENDOPLASMIC RETICULUM STRESS; GENETIC ASSOCIATION STUDIES; GENETIC VARIATION; HUMANS; SPECIES SPECIFICITY; SURVIVAL RATE; TUNICAMYCIN;

EID: 84878459113     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307125110     Document Type: Article

References (51)

1. Dermitzakis ET (2012) Cellular genomics for complex traits. Nat Rev Genet 13(3):215-220.
2. Mackay TF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482(7384):173-178.
3. Mackay TF, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: Challenges and prospects. Nat Rev Genet 10(8):565-577.
4. Bernales S, Papa FR, Walter P (2006) Intracellular signaling by the unfolded protein response. Annu Rev Cell Dev Biol 22:487-508.
5. Teske BF, et al. (2011) The eIF2 kinase PERK and the integrated stress response facilitate activation of ATF6 during endoplasmic reticulum stress. Mol Biol Cell 22(22):4390-4405.
6. Zhao L, Ackerman SL (2006) Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol 18(4):444-452.
7. Delépine M, et al. (2000) EIF2AK3, encoding translation initiation factor 2-Alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 25(4):406-409.
8. Harding HP, et al. (2001) Diabetes mellitus and exocrine pancreatic dysfunction in perk-/-mice reveals a role for translational control in secretory cell survival. Mol Cell 7(6):1153-1163.
9. Ladiges WC, et al. (2005) Pancreatic beta-cell failure and diabetes in mice with a deletion mutation of the endoplasmic reticulum molecular chaperone gene P58IPK. Diabetes 54(4):1074-1081.
10. Ozcan U, et al. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306(5695):457-461.
11. Scheuner D, et al. (2005) Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 11(7):757-764.
12. Boden G, et al. (2008) Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 57(9):2438-2444.
13. Shimazawa M, et al. (2010) An inducer of VGF protects cells against ER stress-induced cell death and prolongs survival in the mutant SOD1 animal models of familial ALS. PLoS ONE 5(12):e15307.
14. Wang L, Popko B, Roos RP (2011) The unfolded protein response in familial amyotrophic lateral sclerosis. Hum Mol Genet 20(5):1008-1015.
15. Dombroski BA, et al. (2010) Gene expression and genetic variation in response to endoplasmic reticulum stress in human cells. Am J Hum Genet 86(5):719-729.
16. Girardot F, Monnier V, Tricoire H (2004) Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 5(1):74.
17. Hollien J, et al. (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186(3):323-331.
18. Hollien J, Weissman JS (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313(5783):104-107.
19. Gaddam D, Stevens N, Hollien J (2013) Comparison of mRNA localization and regulation during endoplasmic reticulum stress in Drosophila cells. Mol Biol Cell 24(1):14-20.
20. Stone EA, Ayroles JF (2009) Modulated modularity clustering as an exploratory tool for functional genomic inference. PLoS Genet 5(5):e1000479.
21. Ayroles JF, et al. (2009) Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41(3):299-307.
22. Jordan KW, et al. (2012) Genome-wide association for sensitivity to chronic oxidative stress in Drosophila melanogaster. PLoS ONE 7(6):e38722.
23. Weber AL, et al. (2012) Genome-wide association analysis of oxidative stress resistance in Drosophila melanogaster. PLoS ONE 7(4):e34745.
24. Fraser HB, Moses AM, Schadt EE (2010) Evidence for widespread adaptive evolution of gene expression in budding yeast. Proc Natl Acad Sci USA 107(7):2977-2982.
25. Orr HA (1998) Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149(4):2099-2104.
26. Schwartz DR, et al. (1999) The neutral cysteine protease bleomycin hydrolase is essential for epidermal integrity and bleomycin resistance. Proc Natl Acad Sci USA 96(8): 4680-4685.
27. He Y, et al. (2010) Emerging roles for XBP1, a sUPeR transcription factor. Gene Expr 15(1):13-25.
28. Senesi S, et al. (2010) Hexose-6-phosphate dehydrogenase in the endoplasmic reticulum. Biol Chem 391(1):1-8.
29. Chen X, et al. (2008) Endoplasmic reticulum Ca2+ dysregulation and endoplasmic reticulum stress following in vitro neuronal ischemia: role of Na+-K+-Cl-cotransporter. J Neurochem 106(4):1563-1576.
30. Morgenstern R, Zhang J, Johansson K (2011) Microsomal glutathione transferase 1: Mechanism and functional roles. Drug Metab Rev 43(2):300-306.
31. Maclean KN, et al. (2012) Cystathionine protects against endoplasmic reticulum stress-induced lipid accumulation, tissue injury, and apoptotic cell death. J Biol Chem 287(38):31994-32005.
32. Simmen T, et al. (2005) PACS-2 controls endoplasmic reticulum- mitochondria communication and Bid-mediated apoptosis. EMBO J 24(4):717-729.
33. Lavery GG, et al. (2008) Deletion of hexose-6-phosphate dehydrogenase activates the unfolded protein response pathway and induces skeletal myopathy. J Biol Chem 283(13):8453-8461.
34. Ma Z, Liu Z, Huang X (2012) Membrane phospholipid asymmetry counters the adverse effects of sterol overloading in the Golgi membrane of Drosophila. Genetics 190(4): 1299-1308.
35. SchröderM, Sutcliffe L (2010) Consequences of stress in the secretory pathway: The ER stress response and its role in the metabolic syndrome. Methods Mol Biol 648:43-62.
36. Jogl G, Hsiao YS, Tong L (2004) Structure and function of carnitine acyltransferases. Ann N Y Acad Sci 1033:17-29.
37. Min KT, Benzer S (1999) Preventing neurodegeneration in the Drosophila mutant bubblegum. Science 284(5422):1985-1988.
38. Steinberg SJ, Morgenthaler J, Heinzer AK, Smith KD, Watkins PA (2000) Very longchain acyl-CoA synthetases. Human "bubblegum" represents a new family of proteins capable of activating very long-chain fatty acids. J Biol Chem 275(45):35162-35169.
39. Basseri S, Austin RC (2012) Endoplasmic reticulum stress and lipid metabolism: Mechanisms and therapeutic potential. Biochem Res Int 2012:841362.
40. Mourikis P, Hurlbut GD, Artavanis-Tsakonas S (2006) Enigma, a mitochondrial protein affecting lifespan and oxidative stress response in Drosophila. Proc Natl Acad Sci USA 103(5):1307-1312.
41. Colgan SM, Hashimi AA, Austin RC (2011) Endoplasmic reticulum stress and lipid dysregulation. Expert Rev Mol Med 13:e4.
42. Malhotra JD, Kaufman RJ (2007) Endoplasmic reticulum stress and oxidative stress: A vicious cycle or a double-edged sword? Antioxid Redox Signal 9(12):2277-2293.
43. Kimball SR (1999) Eukaryotic initiation factor eIF2. Int J Biochem Cell Biol 31(1):25-29.
44. Prostko CR, Brostrom MA, Brostrom CO (1993) Reversible phosphorylation of eukaryotic initiation factor 2 alpha in response to endoplasmic reticular signaling. Mol Cell Biochem 127-128:255-265.
45. 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.
46. Cui Z, Houweling M (2002) Phosphatidylcholine and cell death. Biochim Biophys Acta 1585(2-3):87-96.
47. Fu S, et al. (2011) Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature 473(7348):528-531.
48. Fu S, Watkins SM, Hotamisligil GS (2012) The role of endoplasmic reticulum in hepatic lipid homeostasis and stress signaling. Cell Metab 15(5):623-634.
49. Qi H, et al. (2004) Megator, an essential coiled-coil protein that localizes to the putative spindle matrix during mitosis in Drosophila. Mol Biol Cell 15(11):4854-4865.
50. Goffin L, et al. (2006) The unfolded protein response transducer Ire1p contains a nuclear localization sequence recognized by multiple beta importins. Mol Biol Cell 17(12):5309-5323.
51. Rutkowski DT, et al. (2008) UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 15(6):829-840.