Hypoxia-inducible Lipid Droplet-associated (HILPDA) is a novel Peroxisome Proliferator-activated Receptor (PPAR) target involved in hepatic triglyceride secretion

Journal of Biological Chemistry

Volumn 289, Issue 28, 2014, Pages 19279-19293

  Mattijssen, Frits ^a   Georgiadi, Anastasia ^a   Andasarie, Tresty ^a   Szalowska, Ewa ^a   Zota, Annika ^b   Krones Herzig, Anja ^b   Heier, Christoph ^c   Ratman, Dariusz ^d   De Bosscher, Karolien ^d   Qi, Ling ^e   Zechner, Rudolf ^c   Herzig, Stephan ^b   Kersten, Sander ^a,e  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY OF GRAZ   (Austria)

^d GHENT UNIVERSITY   (Belgium)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DIGITAL STORAGE; DROPS; GENES; MAMMALS; METABOLISM; PHYSIOLOGY; VIRUSES;

ADENO-ASSOCIATED VIRUS; CHROMATIN IMMUNOPRECIPITATION; FATTY ACID OXIDATION; LIVER TRIGLYCERIDES; MICROARRAY ANALYSIS; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; RESPONSE ELEMENTS; TRANSCRIPTION START SITE;

TRANSCRIPTION;

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASE PAIRING; BODY WEIGHT; CONTROLLED STUDY; ENZYME ACTIVITY; FATTY ACID OXIDATION; FATTY LIVER; GENE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOXIA INDUCIBLE LIPID DROPLET ASSOCIATED GENE; LIPID ANALYSIS; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIPOLYSIS; LIPOPROTEIN SECRETION; LIVER CELL; LIVER SLICE; MALE; METABOLIC REGULATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSCRIPTION INITIATION SITE;

HIG2; LIPID DROPLETS; LIPOPROTEIN SECRETION; LIVER METABOLISM; LIVER SLICES; NUCLEAR RECEPTOR; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR (PPAR); PPRE; STEATOSIS; VLDL;

ANIMALS; ANTICHOLESTEREMIC AGENTS; CELL LINE; HUMANS; LIPOGENESIS; LIVER; MICE; MICE, KNOCKOUT; NEOPLASM PROTEINS; PPAR ALPHA; PYRIMIDINES; RATS; RATS, WISTAR; RESPONSE ELEMENTS; RNA, MESSENGER; TRIGLYCERIDES;

EID: 84904186695     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.570044     Document Type: Article

References (56)

1. McPherson, P. A., and McEneny, J. (2012) The biochemistry of ketogenesis and its role in weight management, neurological disease and oxidative stress. J. Physiol. Biochem. 68, 141-151
2. Sun, Z., and Lazar, M. A. (2013) Dissociating fatty liver and diabetes. Trends Endocrinol. Metab. 24, 4-12
3. Pawlak, M., Lefebvre, P., and Staels, B. (2012) General molecular biology and architecture of nuclear receptors. Curr. Top. Med. Chem. 12, 486-504
4. Nakamura, M. T., Cheon, Y., Li, Y., and Nara, T. Y. (2004) Mechanisms of regulation of gene expression by fatty acids. Lipids 39, 1077-1083 (Pubitemid 40129050)
5. Chawla, A., Repa, J. J., Evans, R. M., and Mangelsdorf, D. J. (2001) Nuclear receptors and lipid physiology: opening the X-files. Science 294, 1866-1870 (Pubitemid 33101573)
6. Sonoda, J., Pei, L., and Evans, R. M. (2008) Nuclear receptors: decoding metabolic disease. FEBS Lett. 582, 2-9 (Pubitemid 350297241)
7. Kersten, S., Desvergne, B., and Wahli, W. (2000) Roles of PPARs in health and disease. Nature 405, 421-424 (Pubitemid 30367411)
8. Schupp, M., and Lazar, M. A. (2010) Endogenous ligands for nuclear receptors: digging deeper. J. Biol. Chem. 285, 40409-40415
9. Lalloyer, F., and Staels, B. (2010) Fibrates, glitazones, and peroxisome proliferator-activated receptors. Arterioscler. Thromb. Vasc. Biol. 30, 894-899
10. Dreyer, C., Krey, G., Keller, H., Givel, F., Helftenbein, G., and Wahli, W. (1992) Control of the peroxisomal β-oxidation pathway by a novel family of nuclear hormone receptors. Cell 68, 879-887
11. Poulsen, L., Siersbæk, M., and Mandrup, S. (2012) PPARs: fatty acid sensors controlling metabolism. Semin. Cell Dev. Biol. 23, 631-639
12. Tontonoz, P., and Spiegelman, B. M. (2008) Fat and beyond: the diverse biology of PPARγ. Annu. Rev. Biochem. 77, 289-312
13. Kleiner, S., Nguyen-Tran, V., Baré, O., Huang, X., Spiegelman, B., and Wu, Z. (2009) PPARδ agonism activates fatty acid oxidation via PGC-1α but does not increase mitochondrial gene expression and function. J. Biol. Chem. 284, 18624-18633
14. Roberts, L. D., Murray, A. J., Menassa, D., Ashmore, T., Nicholls, A. W., and Griffin, J. L. (2011) The contrasting roles of PPARδ and PPARγ in regulating the metabolic switch between oxidation and storage of fats in white adipose tissue. Genome Biol. 12, R75
15. Mandard, S., Müller, M., and Kersten, S. (2004) Peroxisome proliferator-activated receptor α target genes. Cell Mol. Life Sci. 61, 393-416 (Pubitemid 38316578)
16. Peters, J. M., Hennuyer, N., Staels, B., Fruchart, J. C., Fievet, C., Gonzalez, F. J., and Auwerx, J. (1997) Alterations in lipoprotein metabolism in peroxisome proliferator-activated receptor α-deficient mice. J. Biol. Chem. 272, 27307-27312 (Pubitemid 27452695)
17. Aoyama, T., Peters, J. M., Iritani, N., Nakajima, T., Furihata, K., Hashimoto, T., and Gonzalez, F. J. (1998) Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor α (PPARα). J. Biol. Chem. 273, 5678-5684 (Pubitemid 28124039)
18. Kersten, S., Seydoux, J., Peters, J. M., Gonzalez, F. J., Desvergne, B., and Wahli, W. (1999) Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J. Clin. Invest. 103, 1489-1498
19. Yu, S., Matsusue, K., Kashireddy, P., Cao, W. Q., Yeldandi, V., Yeldandi, A. V., Rao, M. S., Gonzalez, F. J., and Reddy, J. K. (2003) Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor γ1 (PPARγ1) overexpression. J. Biol. Chem. 278, 498-505 (Pubitemid 36043602)
20. Rakhshandehroo, M., Hooiveld, G., Müller, M., and Kersten, S. (2009) Comparative analysis of gene regulation by the transcription factor PPARα between mouse and human. PLoS One 4, e6796
21. Lichtenstein, L., Mattijssen, F., de Wit, N. J., Georgiadi, A., Hooiveld, G. J., van der Meer, R., He, Y., Qi, L., Köster, A., Tamsma, J. T., Tan, N. S., Müller, M., and Kersten, S. (2010) Angptl4 protects against severe proinflammatory effects of saturated fat by inhibiting fatty acid uptake into mesenteric lymph node macrophages. Cell Metab. 12, 580-592
22. Haemmerle, G., Lass, A., Zimmermann, R., Gorkiewicz, G., Meyer, C., Rozman, J., Heldmaier, G., Maier, R., Theussl, C., Eder, S., Kratky, D., Wagner, E. F., Klingenspor, M., Hoefler, G., and Zechner, R. (2006) Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312, 734-737
23. Gimm, T., Wiese, M., Teschemacher, B., Deggerich, A., Schödel, J., Knaup, K. X., Hackenbeck, T., Hellerbrand, C., Amann, K., Wiesener, M. S., Höning, S., Eckardt, K. U., and Warnecke, C. (2010) Hypoxia-inducible protein 2 is a novel lipid droplet protein and a specific target gene of hypoxia-inducible factor-1. FASEB J. 24, 4443-4458
24. Patsouris, D., Reddy, J. K., Müller, M., and Kersten, S. (2006) Peroxisome proliferator-activated receptor α mediates the effects of high-fat diet on hepatic gene expression. Endocrinology 147, 1508-1516 (Pubitemid 43244386)
25. Hashimoto, T., Cook, W. S., Qi, C., Yeldandi, A. V., Reddy, J. K., and Rao, M. S. (2000) Defect in peroxisome proliferator-activated receptor α-inducible fatty acid oxidation determines the severity of hepatic steatosis in response to fasting. J. Biol. Chem. 275, 28918-28928
26. Podvinec, M., Kaufmann, M. R., Handschin, C., and Meyer, U. A. (2002) NUBIScan, an in silico approach for prediction of nuclear receptor response elements. Mol. Endocrinol. 16, 1269-1279 (Pubitemid 34621075)
27. Kenny, P. A., Enver, T., and Ashworth, A. (2005) Receptor and secreted targets of Wnt-1/β-catenin signalling in mouse mammary epithelial cells. BMC Cancer 5, 3
28. 1 switch gene 2 is a novel PPAR target gene. Biochem. J. 392, 313-324
29. 1 switch gene 2 is an important regulator of hepatic triglyceride metabolism. PLoS One 8, e72315
30. 1 switch gene 2 enhances adipose lipolysis, alters hepatic energy balance, and alleviates high fat diet-induced liver steatosis. Diabetes 63, 934-946
31. 1 switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab. 11, 194-205
32. Ahrens, M., Ammerpohl, O., von Schönfels, W., Kolarova, J., Bens, S., Itzel, T., Teufel, A., Herrmann, A., Brosch, M., Hinrichsen, H., Erhart, W., Egberts, J., Sipos, B., Schreiber, S., Häsler, R., Stickel, F., Becker, T., Krawczak, M., Röcken, C., Siebert, R., Schafmayer, C., and Hampe, J. (2013) DNA methylation analysis in nonalcoholic fatty liver disease suggests distinct disease-specific and remodeling signatures after bariatric surgery. Cell Metab. 18, 296-302
33. Tiwari, S., and Siddiqi, S. A. (2012) Intracellular trafficking and secretion of VLDL. Arterioscler. Thromb. Vasc. Biol. 32, 1079-1086
34. Gordon, D. A., and Jamil, H. (2000) Progress towards understanding the role of microsomal triglyceride transfer protein in apolipoprotein-B lipoprotein assembly. Biochim. Biophys. Acta 1486, 72-83 (Pubitemid 30336793)
35. Gusarova, V., Brodsky, J. L., and Fisher, E. A. (2003) Apolipoprotein B100 exit from the endoplasmic reticulum (ER) is COPII-dependent, and its lipidation to very low density lipoprotein occurs post-ER. J. Biol. Chem. 278, 48051-48058 (Pubitemid 37523255)
36. Yamaguchi, J., Gamble, M. V., Conlon, D., Liang, J. S., and Ginsberg, H. N. (2003) The conversion of apoB100 low density lipoprotein/high density lipoprotein particles to apoB100 very low density lipoproteins in response to oleic acid occurs in the endoplasmic reticulum and not in the Golgi in McA RH7777 cells. J. Biol. Chem. 278, 42643-42651 (Pubitemid 37310538)
37. Qin, W., Sundaram, M., Wang, Y., Zhou, H., Zhong, S., Chang, C. C., Manhas, S., Yao, E. F., Parks, R. J., McFie, P. J., Stone, S. J., Jiang, Z. G., Wang, C., Figeys, D., Jia, W., and Yao, Z. (2011) 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. 286, 27769-27780
38. Li, X., Ye, J., Zhou, L., Gu, W., Fisher, E. A., and Li, P. (2012) Opposing roles of cell death-inducing DFF45-like effector B and perilipin 2 in controlling hepatic VLDL lipidation. J. Lipid Res. 53, 1877-1889
39. Strong, A., Ding, Q., Edmondson, A. C., Millar, J. S., Sachs, K. V., Li, X., Kumaravel, A., Wang, M. Y., Ai, D., Guo, L., Alexander, E. T., Nguyen, D., Lund-Katz, S., Phillips, M. C., Morales, C. R., Tall, A. R., Kathiresan, S., Fisher, E. A., Musunuru, K., and Rader, D. J. (2012) Hepatic sortilin regulates both apolipoprotein B secretion and LDL catabolism. J. Clin. Invest. 122, 2807-2816
40. Magnusson, B., Asp, L., Boström, P., Ruiz, M., Stillemark-Billton, P., Lindén, D., Borén, J., and Olofsson, S. O. (2006) Adipocyte differentiation-related protein promotes fatty acid storage in cytosolic triglycerides and inhibits secretion of very low-density lipoproteins. Arterioscler. Thromb. Vasc. Biol. 26, 1566-1571 (Pubitemid 44288984)
41. Webster, K. A. (2003) Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia. J. Exp. Biol. 206, 2911-2922
42. Semenza, G. L. (2011) Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harb. Symp. Quant. Biol. 76, 347-353
43. Gordon, G. B., Barcza, M. A., and Bush, M. E. (1977) Lipid accumulation of hypoxic tissue culture cells. Am. J. Pathol. 88, 663-678 (Pubitemid 8202944)
44. Sanderson, L. M., Degenhardt, T., Koppen, A., Kalkhoven, E., Desvergne, B., Müller, M., and Kersten, S. (2009) Peroxisome proliferator-activated receptor β/δ (PPARβ/δ) but not PPARα serves as a plasma free fatty acid sensor in liver. Mol. Cell. Biol. 29, 6257-6267
45. Ip, E., Farrell, G., Hall, P., Robertson, G., and Leclercq, I. (2004) Administration of the potent PPARα agonist, Wy-14,643, reverses nutritional fibrosis and steatohepatitis in mice. Hepatology 39, 1286-1296 (Pubitemid 38569050)
46. Ip, E., Farrell, G. C., Robertson, G., Hall, P., Kirsch, R., and Leclercq, I. (2003) Central role of PPARα-dependent hepatic lipid turnover in dietary steatohepatitis in mice. Hepatology 38, 123-132 (Pubitemid 36775803)
47. Kashireddy, P. V., and Rao, M. S. (2004) Lack of peroxisome proliferator-activated receptor α in mice enhances methionine and choline deficient diet-induced steatohepatitis. Hepatol. Res. 30, 104-110 (Pubitemid 41115272)
48. Kong, L., Ren, W., Li, W., Zhao, S., Mi, H., Wang, R., Zhang, Y., Wu, W., Nan, Y., and Yu, J. (2011) Activation of peroxisome proliferator activated receptor α ameliorates ethanol induced steatohepatitis in mice. Lipids Health Dis. 10, 246
49. Rakhshandehroo, M., Sanderson, L. M., Matilainen, M., Stienstra, R., Carlberg, C., de Groot, P. J., Müller, M., and Kersten, S. (2007) Comprehensive analysis of PPARα-dependent regulation of hepatic lipid metabolism by expression profiling. PPAR Res. 2007, 26839
50. Shiri-Sverdlov, R., Wouters, K., van Gorp, P. J., Gijbels, M. J., Noel, B., Buffat, L., Staels, B., Maeda, N., van Bilsen, M., and Hofker, M. H. (2006) Early diet-induced non-alcoholic steatohepatitis in APOE2 knock-in mice and its prevention by fibrates. J. Hepatol. 44, 732-741
51. Shah, A., Rader, D. J., and Millar, J. S. (2010) The effect of PPAR-α agonism on apolipoprotein metabolism in humans. Atherosclerosis 210, 35-40
52. Kersten, S. (2008) Peroxisome proliferator activated receptors and lipoprotein metabolism. PPAR Res. 2008, 132960
53. Edvardsson, U., Ljungberg, A., Lindén, D., William-Olsson, L., Peilot-Sjögren, H., Ahnmark, A., and Oscarsson, J. (2006) PPARα activation increases triglyceride mass and adipose differentiation-related protein in hepatocytes. J. Lipid Res. 47, 329-340 (Pubitemid 43276918)
54. Lindén, D., Lindberg, K., Oscarsson, J., Claesson, C., Asp, L., Li, L., Gustafsson, M., Borén, J., and Olofsson, S. O. (2002) Influence of peroxisome proliferator-activated receptor α agonists on the intracellular turnover and secretion of apolipoprotein (Apo) B-100 and ApoB-48. J. Biol. Chem. 277, 23044-23053 (Pubitemid 34967291)
55. Lindén, D., Alsterholm, M., Wennbo, H., and Oscarsson, J. (2001) PPARα deficiency increases secretion and serum levels of apolipoprotein B-containing lipoproteins. J. Lipid Res. 42, 1831-1840 (Pubitemid 33116714)
56. Tordjman, K., Bernal-Mizrachi, C., Zemany, L., Weng, S., Feng, C., Zhang, F., Leone, T. C., Coleman, T., Kelly, D. P., and Semenkovich, C. F. (2001) PPARα deficiency reduces insulin resistance and atherosclerosis in apoE-null mice. J. Clin. Invest. 107, 1025-1034 (Pubitemid 32323412)