PNPLA3 mediates hepatocyte triacylglycerol remodeling

Journal of Lipid Research

Volumn 55, Issue 4, 2014, Pages 739-746

  Ruhanen, Hanna ^a,b   Perttilä, Julia ^a   Hölttä Vuori, Maarit ^a,c   Zhou, You ^a   Yki Järvinen, Hannele ^a,b   Ikonen, Elina ^a,c   Käkelä, Reijo ^b   Olkkonen, Vesa M ^a,c  

^a MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Adiponutrin; Lipase; Lipid droplet; Lipidomics; Nonalcoholic fatty liver disease; Patatin like phospholipase domain containing 3

Indexed keywords

CARBON 13; DEUTERIUM; FAT DROPLET; GLYCEROL; LIPIDOME; LIVER PROTEIN; MONOUNSATURATED FATTY ACID; OLEIC ACID; PHOSPHATIDYLCHOLINE; PNPLA3 PROTEIN; SATURATED FATTY ACID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ADIPONUTRIN, HUMAN; FATTY ACID; MEMBRANE PROTEIN; PHOSPHOLIPID; TRIACYLGLYCEROL LIPASE;

ARTICLE; CELL COMPOSITION; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IN VITRO STUDY; INCUBATION TIME; ISOTOPE LABELING; LIPID COMPOSITION; LIPOGENESIS; LIVER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; WILD TYPE; ENZYMOLOGY; LIPID METABOLISM; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT; TUMOR CELL LINE;

CELL LINE, TUMOR; FATTY ACIDS; HEPATOCYTES; HUMANS; LIPASE; LIPID DROPLETS; LIPID METABOLISM; MEMBRANE PROTEINS; MUTATION, MISSENSE; PHOSPHOLIPIDS; PROTEIN TRANSPORT; TRIGLYCERIDES;

EID: 84897430331     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M046607     Document Type: Article

References (35)

1. Cohen, J. C., J. D. Horton, and H. H. Hobbs. 2011. Human fatty liver disease: old questions and new insights. Science. 332: 1519-1523.
2. Younossi, Z. M., M. Stepanova, M. Afendy, Y. Fang, Y. Younossi, H. Mir, and M. Srishord. 2011. Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008. Clin. Gastroenterol. Hepatol. 9: 524-530.
3. Kotronen, A., J. Westerbacka, R. Bergholm, K. H. Pietiläinen, and H. Yki-Järvinen. 2007. Liver fat in the metabolic syndrome. J. Clin. Endocrinol. Metab. 92: 3490-3497.
4. Romeo, S., J. Kozlitina, C. Xing, A. Pertsemlidis, D. Cox, L. A. Pennacchio, E. Boerwinkle, J. C. Cohen, and H. H. Hobbs. 2008. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat. Genet. 40: 1461-1465.
5. Sookoian, S., and C. J. Pirola. 2011. Meta-analysis of the influence of I148M variant of patatin-like phospholipase domain containing 3 gene (PNPLA3) on the susceptibility and histological severity of nonalcoholic fatty liver disease. Hepatology. 53: 1883-1894.
6. He, S., C. McPhaul, J. Z. Li, R. Garuti, L. Kinch, N. V. Grishin, J. C. Cohen, and H. H. Hobbs. 2010. A sequence variation (I148M) in PNPLA3 associated with nonalcoholic fatty liver disease disrupts triglyceride hydrolysis. J. Biol. Chem. 285: 6706-6715.
7. Jenkins, C. M., D. J. Mancuso, W. Yan, H. F. Sims, B. Gibson, and R. W. Gross. 2004. Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J. Biol. Chem. 279: 48968-48975.
8. Lake, A. C., Y. Sun, J. L. Li, J. E. Kim, J. W. Johnson, D. Li, T. Revett, H. H. Shih, W. Liu, J. E. Paulsen, et al. 2005. Expression, regulation, and triglyceride hydrolase activity of Adiponutrin family members. J. Lipid Res. 46: 2477-2487.
9. Huang, Y., J. C. Cohen, and H. H. Hobbs. 2011. Expression and characterization of a PNPLA3 protein isoform (I148M) associated with nonalcoholic fatty liver disease. J. Biol. Chem. 286: 37085-37093.
10. Moldes, M., G. Beauregard, M. Faraj, N. Peretti, P. H. Ducluzeau, M. Laville, R. Rabasa-Lhoret, H. Vidal, and K. Clement. 2006. Adiponutrin gene is regulated by insulin and glucose in human adipose tissue. Eur. J. Endocrinol. 155: 461-468.
11. Rae-Whitcombe, S. M., D. Kennedy, M. Voyles, and M. P. Thompson. 2010. Regulation of the promoter region of the human adiponutrin/ PNPLA3 gene by glucose and insulin. Biochem. Biophys. Res. Commun. 402: 767-772.
12. Soronen, J., P. P. Laurila, J. Naukkarinen, I. Surakka, S. Ripatti, M. Jauhiainen, V. M. Olkkonen, and H. Yki-Järvinen. 2012. Adipose tissue gene expression analysis reveals changes in inflammatory, mitochondrial respiratory and lipid metabolic pathways in obese insulin-resistant subjects. BMC Med. Genomics. 5: 9.
13. Huang, Y., S. He, J. Z. Li, Y. K. Seo, T. F. Osborne, J. C. Cohen, and H. H. Hobbs. 2010. A feed-forward loop amplifies nutritional regulation of PNPLA3. Proc. Natl. Acad. Sci. USA. 107: 7892-7897.
14. Dubuquoy, C., C. Robichon, F. Lasnier, C. Langlois, I. Dugail, F. Foufelle, J. Girard, A. F. Burnol, C. Postic, and M. Moldes. 2011. Distinct regulation of adiponutrin/PNPLA3 gene expression by the transcription factors ChREBP and SREBP1c in mouse and human hepatocytes. J. Hepatol. 55: 145-153.
15. Perttilä, J., C. Huaman-Samanez, S. Caron, K. Tanhuanpää, B. Staels, H. Yki-Järvinen, and V. M. Olkkonen. 2012. PNPLA3 is regulated by glucose in human hepatocytes, and its I148M mutant slows down triglyceride hydrolysis. Am. J. Physiol. Endocrinol. Metab. 302: E1063-E1069.
16. Qiao, A., J. Liang, Y. Ke, C. Li, Y. Cui, L. Shen, H. Zhang, A. Cui, X. Liu, C. Liu, et al. 2011. Mouse patatin-like phospholipase domaincontaining 3 influences systemic lipid and glucose homeostasis. Hepatology. 54: 509-521.
17. Kumari, M., G. Schoiswohl, C. Chitraju, M. Paar, I. Cornaciu, A. Y. Rangrez, N. Wongsiriroj, H. M. Nagy, P. T. Ivanova, S. A. Scott, et al. 2012. Adiponutrin functions as a nutritionally regulated lysophosphatidic acid acyltransferase. Cell Metab. 15: 691-702.
18. Basantani, M. K., M. T. Sitnick, L. Cai, D. S. Brenner, N. P. Gardner, J. Z. Li, G. Schoiswohl, K. Yang, M. Kumari, R. W. Gross, et al. 2011. Pnpla3/Adiponutrin deficiency in mice does not contribute to fatty liver disease or metabolic syndrome. J. Lipid Res. 52: 318-329.
19. Chen, W., B. Chang, L. Li, and L. Chan. 2010. Patatin-like phospholipase domain-containing 3/adiponutrin deficiency in mice is not associated with fatty liver disease. Hepatology. 52: 1134-1142.
20. Kumashiro, N., T. Yoshimura, J. L. Cantley, S. K. Majumdar, F. Guebre-Egziabher, R. Kursawe, D. F. Vatner, I. Fat, M. Kahn, D. M. Erion, et al. 2013. Role of patatin-like phospholipase domaincontaining 3 on lipid-induced hepatic steatosis and insulin resistance in rats. Hepatology. 57: 1763-1772.
21. Pirazzi, C., M. Adiels, M. A. Burza, R. M. Mancina, M. Levin, M.Stahlman, M. R. Taskinen, M. Orho-Melander, J. Perman, A. Pujia, et al. 2012. Patatin-like phospholipase domain-containing 3 (PNPLA3) I148M (rs738409) affects hepatic VLDL secretion in humans and in vitro. J. Hepatol. 57: 1276-1282.
22. Li, J. Z., Y. Huang, R. Karaman, P. T. Ivanova, H. A. Brown, T. Roddy, J. Castro-Perez, J. C. Cohen, and H. H. Hobbs. 2012. Chronic overexpression of PNPLA3I148M in mouse liver causes hepatic steatosis. J. Clin. Invest. 122: 4130-4144.
23. Chamoun, Z., F. Vacca, R. G. Parton, and J. Gruenberg. 2013. PNPLA3/adiponutrin functions in lipid droplet formation. Biol Cell. 105: 219-233
24. Nakabayashi, H., K. Taketa, K. Miyano, T. Yamane, and J. Sato. 1982. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42: 3858-3863.
25. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226: 497-509.
26. Käkelä, R., P. Somerharju, and J. Tyynelä. 2003. Analysis of phospholipid molecular species in brains from patients with infantile and juvenile neuronal-ceroid lipofuscinosis using liquid chromatography-electrospray ionization mass spectrometry. J. Neurochem. 84: 1051-1065.
27. Haimi, P., A. Uphoff, M. Hermansson, and P. Somerharju. 2006. Software tools for analysis of mass spectrometric lipidome data. Anal. Chem. 78: 8324-8331.
28. Käkelä, R., A. Käkelä, S. Kahle, P. H. Becker, A. Kelly, and R. Furness. 2005. Fatty acid signatures in plasma of captive herring gulls as indicators of demersal or pelagic fish diet. Mar. Ecol. Prog. Ser. 293: 191-200.
29. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
30. Hölttä-Vuori, M., V. T. Salo, Y. Ohsaki, M. L. Suster, and E. Ikonen. 2013. Alleviation of seipinopathy-related ER stress by triglyceride storage. Hum. Mol. Genet. 22: 1157-1166.
31. Wold, S., and M. Sjöström. 1977. SIMCA: a method for analyzing chemical data in terms of similarity and analogy. In Chemometrics: Theory and Application. B. Kowalski, editor. American Chemical Society, Washington, DC. 243-282.
32. Lankester, D. L., A. M. Brown, and V. A. Zammit. 1998. Use of cytosolic triacylglycerol hydrolysis products and of exogenous fatty acid for the synthesis of triacylglycerol secreted by cultured rat hepatocytes. J. Lipid Res. 39: 1889-1895.
33. Yamashita, A., Y. Hayashi, Y. Nemoto-Sasaki, M. Ito, S. Oka, T. Tanikawa, K. Waku, and T. Sugiura. 2014. Acyltransferases and transacylases that determine the fatty acid composition of glycerolipids and the metabolism of bioactive lipid mediators in mammalian cells and model organisms. Prog. Lipid Res. 53: 18-81.
34. Pérez-Chacón, G., A. M. Astudillo, D. Balgoma, M. A. Balboa, and J. Balsinde. 2009. Control of free arachidonic acid levels by phospholipases A2 and lysophospholipid acyltransferases. Biochim. Biophys. Acta. 1791: 1103-1113.
35. Raclot, T. 2003. Selective mobilization of fatty acids from adipose tissue triaclyglycerols. Prog. Lipid Res. 42: 257-288.