Microsome-associated lumenal lipid droplets in the regulation of lipoprotein secretion

Current Opinion in Lipidology

Volumn 24, Issue 2, 2013, Pages 160-170

  Yao, Zemin ^a   Zhou, Hu ^b   Figeys, Daniel ^a   Wang, Yuwei ^a   Sundaram, Meenakshi ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

apoC III; hypertriglyceridemia; lipogenesis; nonalcoholic fatty liver disease; VLDL

Indexed keywords

CAVEOLIN 1; FAT DROPLET; LIVER X RECEPTOR; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SPHINGOMYELIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; VERY LOW DENSITY LIPOPROTEIN;

ADIPOGENESIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FATTY LIVER; HOMEOSTASIS; HUMAN; HYPERTRIGLYCERIDEMIA; LIPOGENESIS; LIPOPROTEIN SECRETION; LIVER CELL; LIVER DISEASE; LIVER REGENERATION; LOSS OF FUNCTION MUTATION; MICROSOME; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW;

ABETALIPOPROTEINEMIA; ANIMALS; APOLIPOPROTEIN C-III; CYTOSOL; ENDOPLASMIC RETICULUM; FATTY LIVER; HOMEOSTASIS; HUMANS; LIPOGENESIS; LIPOPROTEINS, VLDL; LIVER; MICE; MICROSOMES; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRIGLYCERIDES;

MAMMALIA;

EID: 84875217960     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0b013e32835aebe7     Document Type: Review

References (56)

1. Sundaram M, Yao Z. Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr Metab (Lond) 2010; 7: 35-51.
2. Yao Z, Wang Y. Apolipoprotein C-III and hepatic triglyceride-rich lipoprotein production. Curr Opin Lipidol 2012; 23: 206-212.
3. Browning JD, Horton JD. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest 2004; 114: 147-152.
4. 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.
5. Li Y, Na K, Lee HJ, et al. Contribution of sams-1 and pmt-1 to lipid homoeostasis in adult Caenorhabditis elegans. J Biochem 2011; 149: 529-538. This is one of the first study that demonstrated, in Caenorhabditis elegans, that S adenosylmethionine synthetase (SAMS) and phosphoethanolamine N-methyltransferase play a role in triglyceride synthesis and lipid droplet formation.
6. Walker AK, Jacobs RL, Watts JL, et al. A conserved SREBP-1/ phosphatidylcholine feedback circuit regulates lipogenesis in metazoans. Cell 2011; 147: 840-852. This study showed that the blockage of phosphatidylcholine synthesis, in Caenorhabditis elegans, mouse liver, and human cells, results in activation of SREBP-1, triglyceride synthesis, and lipid droplet formation.
7. Guo Y, Walther TC, Rao M, et al. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization. Nature 2008; 453: 657-661.
8. Horl G, Wagner A, Cole LK, et al. Sequential synthesis and methylation of phosphatidylethanolamine promote lipid droplet biosynthesis and stability in tissue culture and in vivo. J Biol Chem 2011; 286: 17338-17350.
9. Brasaemle DL, Wolins NE. Packaging of fat: an evolving model of lipid droplet assembly and expansion. J Biol Chem 2012; 287: 2273-2279.
10. Yao ZM, Vance DE. The active synthesis of phosphatidylcholine is required for very low density lipoprotein secretion from rat hepatocytes. J Biol Chem 1988; 263: 2998-3004.
11. Yu S, Matsusue K, Kashireddy P, et al. Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferatoractivated receptor gamma1 (PPARgamma1) overexpression. J Biol Chem 2003; 278: 498-505.
12. Matsusue K, Haluzik M, Lambert G, et al. Liver-specific disruption of PPARgamma in leptin-deficient mice improves fatty liver but aggravates diabetic phenotypes. J Clin Invest 2003; 111: 737-747.
13. Gavrilova O, Haluzik M, Matsusue K, et al. Liver peroxisome proliferatoractivated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J Biol Chem 2003; 278: 34268-34276.
14. Lee JS, Mendez R, Heng HH, et al. Pharmacological ER stress promotes hepatic lipogenesis and lipid droplet formation. Am J Transl Res 2012; 4: 102-113.
15. Bai L, Jia Y, Viswakarma N, et al. Transcription coactivator mediator subunit MED1 is required for the development of fatty liver in the mouse. Hepatology 2011; 53: 1164-1174. This study shows that MED1 (also known as PBP or TRAP220) acts as a PPARgspecific mediator in promoting hepatic adipogenesis and steatosis.
16. Flach RJ, Qin H, Zhang L, et al. Loss of mitogen-activated protein kinase phosphatase-1 protects from hepatic steatosis by repression of cell deathinducing DNA fragmentation factor A (DFFA)-like effector C (CIDEC)/fatspecific protein 27. J Biol Chem 2011; 286: 22195-22202.
17. Zhou J, Febbraio M, Wada T, et al. Hepatic fatty acid transporter Cd36 is a common target of LXR, PXR, and PPARgamma in promoting steatosis. Gastroenterology 2008; 134: 556-567.
18. Lisanti MP, Scherer PE, Vidugiriene J, et al. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J Cell Biol 1994; 126: 111-126.
19. Fernandez MA, Albor C, Ingelmo-Torres M, et al. Caveolin-1 is essential for liver regeneration. Science 2006; 313: 1628-1632.
20. Fernandez-Rojo M, Restall C, Ferguson C, et al. Caveolin-1 orchestrates the balance between glucose and lipid-dependent energy metabolism: implications for liver regeneration. Hepatology 2012; 55: 1574-1584. This study demonstrates that expression of CAV1 in mice is required for hepatic lipid storage during fasting, liver regeneration, and diet-induced steatosis in mouse models that have low activities of the pentose phosphate pathway that is required for efficient lipogenesis.
21. Mayoral R, Valverde AM, Llorente IC, et al. Impairment of transforming growth factor beta signaling in caveolin-1-deficient hepatocytes: role in liver regeneration. J Biol Chem 2010; 285: 3633-3642.
22. Mitsutake S, Zama K, Yokota H, et al. Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, fatty liver, and type 2 diabetes. J Biol Chem 2011; 286: 28544-28555. This study shows that inactivation of sphingomyelin synthase 2, the enzyme located in plasma membrane lipid microdomains, prevents large and mature lipid droplet formation in mouse liver.
23. Fon TK, Rozman D. Nonalcoholic Fatty liver disease: focus on lipoprotein and lipid deregulation. J Lipids 2011; 783976.
24. Gross DA, Zhan C, Silver DL. Direct binding of triglyceride to fat storageinducing transmembrane proteins 1 and 2 is important for lipid droplet formation. Proc Natl Acad Sci U S A 2011; 108: 19581-19586.
25. Matsusue K, Kusakabe T, Noguchi T, et al. Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab 2008; 7: 302-311.
26. Gong J, Sun Z, Wu L, et al. Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites. J Cell Biol 2011; 195: 953-963.
27. Jambunathan S, Yin J, Khan W, et al. FSP27 promotes lipid droplet clustering and then fusion to regulate triglyceride accumulation. PLoS One 2011; 6: e28614.
28. Xu L, Zhou L, Li P. CIDE proteins and lipid metabolism. Arterioscler Thromb Vasc Biol 2012; 32: 1094-1098.
29. Yang H, Galea A, Sytnyk V, et al. Controlling the size of lipid droplets: lipid and protein factors. Curr Opin Cell Biol 2012; 24: 509-516.
30. Krahmer N, Guo Y, Wilfling F, et al. Phosphatidylcholine synthesis for lipid droplet expansion is mediated by localized activation of CTP: phosphocholine cytidylyltransferase. Cell Metab 2011; 14: 504-515.
31. Murphy S, Martin S, Parton RG. Quantitative analysis of lipid droplet fusion: inefficient steady state fusion but rapid stimulation by chemical fusogens. PLoS One 2010; 5: e15030.
32. Sturley SL, Hussain MM. Lipid droplet formation on opposing sides of the endoplasmic reticulum. J Lipid Res 2012; 53: 1800-1810.
33. Okumura T. Role of lipid droplet proteins in liver steatosis. J Physiol Biochem 2011; 67: 629-636.
34. Hsieh K, Lee YK, Londos C, et al. Perilipin family members preferentially sequester to either triacylglycerol-or cholesteryl ester-specific intracellular lipid storage droplets. J Cell Sci 2012 [Epub ahead of print]. doi: 10.1242/jcs.104943.
35. Wang H, Bell M, Sreenevasan U, et al. Unique regulation of adipose triglyceride lipase (ATGL) by perilipin 5, a lipid droplet-associated protein. J Biol Chem 2011; 286: 15707-15715.
36. Hussain MM, Rava P, Walsh M, et al. Multiple functions of microsomal triglyceride transfer protein. Nutr Metab (Lond) 2012; 9: 14.
37. Minehira K, Young SG, Villanueva CJ, et al. Blocking VLDL secretion causes hepatic steatosis but does not affect peripheral lipid stores or insulin sensitivity in mice. J Lipid Res 2008; 49: 2038-2044.
38. Liao W, Hui TY, Young SG, et al. Blocking microsomal triglyceride transfer protein interferes with apoB secretion without causing retention or stress in the ER. J Lipid Res 2003; 44: 978-985.
39. Brown JM, Betters JL, Lord C, et al. CGI-58 knockdown in mice causes hepatic steatosis but prevents diet-induced obesity and glucose intolerance. J Lipid Res 2010; 51: 3306-3315.
40. Mantzaris MD, Tsianos EV, Galaris D. Interruption of triacylglycerol synthesis in the endoplasmic reticulum is the initiating event for saturated fatty acidinduced lipotoxicity in liver cells. FEBS J 2011; 278: 519-530.
41. Klemm EJ, Spooner E, Ploegh HL. Dual role of ancient ubiquitous protein 1 (AUP1) in lipid droplet accumulation and endoplasmic reticulum (ER) protein quality control. J Biol Chem 2011; 286: 37602-37614. This study shows that, in HeLa cells, AUP1 is located both to the lipid droplets and ER, thus suggesting a link between lipid storage and ER protein quality control.
42. Wang CW, Lee SC. The ubiquitin-like (UBX)-domain-containing protein Ubx2/Ubxd8 regulates lipid droplet homeostasis. J Cell Sci 2012; 125: 2930-2939.
43. Ohsaki Y, Cheng J, Fujita A, et al. Cytoplasmic lipid droplets are sites of convergence of proteasomal and autophagic degradation of apolipoprotein B. Mol Biol Cell 2006; 17: 2674-2683.
44. Bouchoux J, Beilstein F, Pauquai T, et al. The proteome of cytosolic lipid droplets isolated from differentiated Caco-2/TC7 enterocytes reveals cellspecific characteristics. Biol Cell 2011; 103: 499-517.
45. Forte TM, Shu X, Ryan RO. The ins (cell) and outs (plasma) of apolipoprotein A-V. J Lipid Res 2009; 50 (Suppl): S150-S155.
46. Suzuki M, Otsuka T, Ohsaki Y, et al. Derlin-1 and UBXD8 are engaged in dislocation and degradation of lipidated ApoB-100 at lipid droplets. Mol Biol Cell 2012; 23: 800-810. This study provides new evidence that intracellular degradation of newly synthesized apoB-100 involves cytosolic lipid droplets.
47. Ploegh HL. A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum. Nature 2007; 448: 435-438.
48. Blade AM, Fabritius MA, Hou L, et al. Biogenesis of apolipoprotein A-V and its impact on VLDL triglyceride secretion. J Lipid Res 2011; 52: 237-244. This study shows that secretion of apoA-V is inversely related to hepatic triglyceride synthesis, and the retarded apoA-V secretion was associated with increased presentation of apoA-V on cytosolic lipid droplets.
49. Olzmann JA, Kopito RR. Lipid droplet formation is dispensable for endoplasmic reticulum-associated degradation. J Biol Chem 2011; 286: 27872-27874.
50. Ye J. Hepatitis C virus: a new class of virus associated with particles derived from very low-density lipoproteins. Arterioscler Thromb Vasc Biol 2012; 32: 1099-1103.
51. Qin W, Sundaram M, Wang Y, et al. Missense Mutation in APOC3 within the C-terminal Lipid-binding Domain of Human apoC-III Results in Impaired Assembly and Secretion of Triacylglycerol-rich Very Low Density Lipoproteins. Evidence that apoC-III plays a major role in the formation of lipid precursors within the microsomal lumen. J Biol Chem 2011; 286: 27769-27780. This study reveals a functional domain within the carboxyl terminus of human apoC-III that plays a role in the formation of microsome-associated lumenal lipid droplets.
52. Sundaram M, Zhong S, Bou Khalil M, et al. Expression of apolipoprotein C-III in McA-RH7777 cells enhances VLDL assembly and secretion under lipid-rich conditions. J Lipid Res 2010; 51: 150-161.
53. Sundaram M, Zhong S, Bou Khalil M, et al. Functional analysis of the missense APOC3 mutation Ala23Thr associated with human hypotriglyceridemia. J Lipid Res 2010; 51: 1524-1534.
54. Zhou H, Wang F, Wang Y, et al. Improved recovery and identification of membrane proteins from rat hepatic cells using a centrifugal proteomic reactor. Mol Cell Proteomics 2011; doi: 10.1074/mcp.O111.008425.
55. Wang H, Gilham D, Lehner R. Proteomic and lipid characterization of apolipoprotein B-free luminal lipid droplets from mouse liver microsomes: implications for very low density lipoprotein assembly. J Biol Chem 2007; 282: 33218-33226.
56. Sundaram M, Yao Z. Intrahepatic role of exchangeable apolipoproteins in lipoprotein assembly and secretion. Arterioscler Thromb Vasc Biol 2012; 32: 1073-1078.