How does protein misfolding in the endoplasmic reticulum affect lipid metabolism in the liver?

Current Opinion in Lipidology

Volumn 25, Issue 2, 2014, Pages 125-132

  Wang, Shiyu ^a   Kaufman, Randal J ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Endoplasmic reticulum stress; Lipid metabolism; The unfolded protein response

Indexed keywords

LIPID; LIVER PROTEIN;

DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; LIPID LIVER LEVEL; LIPID METABOLISM; LIPOTOXICITY; LIVER CELL; LIVER DISEASE; METABOLIC DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

ANIMALS; ENDOPLASMIC RETICULUM; HUMANS; LIPID METABOLISM; LIVER; PROTEIN BIOSYNTHESIS; PROTEINS; UNFOLDED PROTEIN RESPONSE;

EID: 84897026394     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0000000000000056     Document Type: Review

References (66)

1. Shibata Y, Voeltz GK, Rapoport TA. Rough sheets and smooth tubules. Cell 2006; 126:435-439.
2. McNew JA, Sondermann H, Lee T, et al. GTP-dependent membrane fusion. Annu Rev Cell Dev Biol 2013; 29:529-550.
3. Fu S, Watkins SM, Hotamisligil GS. The role of endoplasmic reticulum in hepatic lipid homeostasis and stress signaling. Cell Metab 2012; 15:623-634.
4. Andrews TM, Tata Jr. Protein synthesis by membrane-bound and free ribosomes of the developing rat cerebral cortex. Biochem J 1971; 124:883-889.
5. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74:739-789.
6. Ordonez A, Snapp EL, Tan L, et al. Endoplasmic reticulum polymers impair luminal protein mobility and sensitize to cellular stress in alpha1-Antitrypsin deficiency. Hepatology 2013; 57:2049-2060.
7. Lomas DA, Evans DL, Finch JT, Carrell RW. The mechanism of Z alpha 1-Antitrypsin accumulation in the liver. Nature 1992; 357:605-607.
8. Silverman GA, Pak SC, Perlmutter DH. Disorders of protein misfolding: Alpha-1-Antitrypsin deficiency as prototype. J Pediatr 2013; 163:320-326.
9. Simha V, Garg A. Lipodystrophy: Lessons in lipid and energy metabolism. Curr Opin Lipidol 2006; 17:162-169.
10. Fagone P, Jackowski S. Membrane phospholipid synthesis and endoplasmic reticulum function. J Lipid Res 2009; 50 (Suppl):S311-316.
11. Yokoyama C, Wang X, Briggs MR, et al. SREBP-1, a basic-helix-loop- helixleucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 1993; 75:187-197.
12. Hinz U, Giebel B, Campos-Ortega JA. The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 1994; 76:77-87.
13. Brown MS, Goldstein JL. The SREBP pathway: Regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997; 89:331-340.
14. Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS. Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: A delicate balance. Cell Metab 2008; 8:512-521.
15. Liu Q, Siloto RM, Lehner R, et al. Acyl-CoA:diacylglycerol acyltransferase: Molecular biology, biochemistry and biotechnology. Prog Lipid Res 2012; 51:350-377.
16. Gimeno RE, Cao J. Thematic review series: Glycerolipids. Mammalian glycerol-3-phosphate acyltransferases-new genes for an old activity. J Lipid Res 2008; 49:2079-2088.
17. Lagace TA, Ridgway ND. The role of phospholipids in the biological activity and structure of the endoplasmic reticulum. Biochim Biophys Acta 2013; 1833:2499-2510.
18. Olofsson SO, Bostrom P, Andersson L, et al. Triglyceride containing lipid droplets and lipid droplet-Associated proteins. Curr Opin Lipidol 2008; 19:441-447.
19. Reue K. A thematic review series: Lipid droplet storage and metabolism-from yeast to man. J Lipid Res 2011; 52:1865-1868.
20. Nielsen S, Karpe F. Determinants of VLDL-Triglycerides production. Curr Opin Lipidol 2012; 23:321-326.
21. Tiwari S, Siddiqi SA. Intracellular trafficking and secretion of VLDL. Arterioscler Thromb Vasc Biol 2012; 32:1079-1086.
22. Hussain MM, Shi J, Dreizen P. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J Lipid Res 2003; 44:22-32.
23. Rutledge AC, Su Q, Adeli K. Apolipoprotein B100 biogenesis: A complex array of intracellular mechanisms regulating folding, stability, and lipoprotein assembly. Biochem Cell Biol 2010; 88:251-267.
24. Olofsson SO, Boren J. Apolipoprotein B secretory regulation by degradation. Arterioscler Thromb Vasc Biol 2012; 32:1334-1338.
25. Hassing HC, Surendran RP, Mooij HL, et al. Pathophysiology of hypertriglyceridemia. Biochim Biophys Acta 2012; 1821:826-832.
26. Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol 2012; 197:857-867.
27. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010; 140:900-917.
28. Yoshida H, Matsui T, Yamamoto A, et al. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001; 107:881-891.
29. Yamamoto K, Sato T, Matsui T, et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 2007; 13:365-376.
30. Harding HP, Zhang Y, Bertolotti A, et al. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 2000; 5:897-904.
31. Scheuner D, Song B, McEwen E, et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 2001; 7:1165-1176.
32. Shi Y, Vattem KM, Sood R, et al. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 1998; 18:7499-7509.
33. Rutkowski DT, Arnold SM, Miller CN, et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-Apoptotic mRNAs and proteins. PLoS Biol 2006; 4:e374.
34. Rutkowski DT, Wu J, Back SH, et al. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 2008; 15:829-840.
35. Zhang K, Wang S, Malhotra J, et al. The unfolded protein response transducer IRE1alpha prevents ER stress-induced hepatic steatosis. EMBO J 2011; 30:1357-1375.
36. Werstuck GH, Lentz SR, Dayal S, et al. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Invest 2001; 107:1263-1273.
37. Kammoun HL, Chabanon H, Hainault I, et al. GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 2009; 119:1201-1215.
38. Qiu W, Su Q, Rutledge AC, et al. Glucosamine-induced endoplasmic reticulum stress attenuates apolipoprotein B100 synthesis via PERK signaling. J Lipid Res 2009; 50:1814-1823.
39. Qiu W, Zhang J, Dekker MJ, et al. Hepatic autophagy mediates endoplasmic reticulum stress-induced degradation of misfolded apolipoprotein B. Hepatology 2011; 53:1515-1525.
40. Fisher EA. The degradation of apolipoprotein B100: Multiple opportunities to regulate VLDL triglyceride production by different proteolytic pathways. Biochim Biophys Acta 2012; 1821:778-781.
41. Deng J, Liu S, Zou L, et al. Lipolysis response to endoplasmic reticulum stress in adipose cells. J Biol Chem 2012; 287:6240-6249.
42. Jha P, Claudel T, Baghdasaryan A, et al. Role of adipose triglyceride lipase (PNPLA2) in protection from hepatic inflammation in mouse models of steatohepatitis and endotoxemia. Hepatology 2014. [Epub ahead of print].
43. Jo H, Choe SS, Shin KC, et al. Endoplasmic reticulum stress induces hepatic steatosis via increased expression of the hepatic very low-density lipoprotein receptor. Hepatology 2013; 57:1366-1377.
44. Han D, Lerner AG, Vande Walle L, et al. IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 2009; 138:562-575.
45. Hollien J, Lin JH, Li H, et al. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009; 186:323-331.
46. So JS, Hur KY, Tarrio M, et al. Silencing of lipid metabolism genes through IRE1alpha-mediated mRNA decay lowers plasma lipids in mice. Cell Metab 2012; 16:487-499.
47. Lee AH, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 2008; 320:1492-1496.
48. Zhou Y, Lee J, Reno CM, et al. Regulation of glucose homeostasis through a XBP-1-FoxO1 interaction. Nat Med 2011; 17:356-365.
49. Park SW, Zhou Y, Lee J, et al. The regulatory subunits of PI3K, p85alpha and p85beta, interact with XBP-1 and increase its nuclear translocation. Nat Med 2010; 16:429-437.
50. Zeng L, Lu M, Mori K, et al. ATF6 modulates SREBP2-mediated lipogenesis. EMBO J 2004; 23:950-958.
51. Zhang K, Shen X,WuJ, et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 2006; 124:587-599.
52. Lee JH, Giannikopoulos P, Duncan SA, et al. The transcription factor cyclic AMP-responsive element-binding protein H regulates triglyceride metabolism. Nat Med 2011; 17:812-815.
53. Zhang C, Wang G, Zheng Z, et al. Endoplasmic reticulum-Tethered transcription factor cAMP responsive element-binding protein, hepatocyte specific, regulates hepatic lipogenesis, fatty acid oxidation, and lipolysis upon metabolic stress in mice. Hepatology 2012; 55:1070-1082.
54. Wu J, Rutkowski DT, Dubois M, et al. ATF6alpha optimizes long-Term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007; 13:351-364.
55. Harding HP, Novoa I, Zhang Y, et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000; 6:1099-1108.
56. Harding HP, Zhang Y, Zeng H, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 2003; 11:619-633.
57. Marciniak SJ, Yun CY, Oyadomari S, et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 2004; 18:3066-3077.
58. Han J, Back SH, Hur J, et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 2013; 15:481-490.
59. Xiao G, Zhang T, Yu S, et al. ATF4 protein deficiency protects against high fructose-induced hypertriglyceridemia in mice. J Biol Chem 2013; 288:25350-25361.
60. Chikka MR, McCabe DD, Tyra HM, Rutkowski DT. C/EBP homologous protein (CHOP) contributes to suppression of metabolic genes during endoplasmic reticulum stress in the liver. J Biol Chem 2013; 288:4405-4415.
61. Wang S, Chen Z, Lam V, et al. IRE1alpha-XBP1 s induces PDI expression to increase MTP activity for hepatic VLDL assembly and lipid homeostasis. Cell Metab 2012; 16:473-486.
62. Otoda T, Takamura T, Misu H, et al. Proteasome dysfunction mediates obesity-induced endoplasmic reticulum stress and insulin resistance in the liver. Diabetes 2013; 62:811-824.
63. B'Chir W, Maurin AC, Carraro V, et al. The eIF2alpha/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res 2013; 41:7683-7699.
64. Guo W, Wong S, Xie W, et al. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab 2007; 293:E576-586.
65. Pineau L, Colas J, Dupont S, et al. Lipid-induced ER stress: Synergistic effects of sterols and saturated fatty acids. Traffic 2009; 10:673-690.
66. Volmer R, van der Ploeg K, Ron D. Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci U S A 2013; 110:4628-4633.