Role of long-chain acyl-CoA synthetase 4 in formation of polyunsaturated lipid species in hepatic stellate cells

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 2, 2015, Pages 220-230

  Tuohetahuntila, Maidina ^a   Spee, Bart ^b   Kruitwagen, Hedwig S ^b   Wubbolts, Richard ^a   Brouwers, Jos F ^a   Van De Lest, Chris H ^a   Molenaar, Martijn R ^a   Houweling, Martin ^a   Helms, J Bernd ^a   Vaandrager, Arie B ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Arachidonic acid; Eicosanoid; Heavy isotope labeling; Lipidomics; Phosphatidylcholine; Prostaglandin

Indexed keywords

ARACHIDONIC ACID; FAT DROPLET; ICOSANOID; LIPID; LONG CHAIN FATTY ACID COENZYME A LIGASE; PHOSPHATIDYLCHOLINE; POLYUNSATURATED FATTY ACID; ROSIGLITAZONE; SMALL INTERFERING RNA; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ACSL4 PROTEIN, RAT; ENZYME INHIBITOR; LONG-CHAIN-FATTY-ACID-COA LIGASE; TRIACYLGLYCEROL; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIPID COMPOSITION; MALE; NONHUMAN; PROSTAGLANDIN RELEASE; PROTEIN FAMILY; RAT; SPECIES; STELLATE CELL; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; METABOLISM; RNA INTERFERENCE; TIME; WISTAR RAT;

ANIMALS; ARACHIDONIC ACID; CELL LINE; COENZYME A LIGASES; ENZYME INHIBITORS; FATTY ACIDS, UNSATURATED; HEPATIC STELLATE CELLS; HUMANS; MALE; PHOSPHATIDYLCHOLINES; RATS, WISTAR; RNA INTERFERENCE; THIAZOLIDINEDIONES; TIME FACTORS; TRANSFECTION; TRIGLYCERIDES; UP-REGULATION;

EID: 84919934611     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.12.003     Document Type: Article

References (38)

1. W.S. Blaner, S.M. O'Byrne, N. Wongsiriroj, J. Kluwe, D.M. D'Ambrosio, H. Jiang, R.F. Schwabe, E.M.C. Hillman, R. Piantedosi, J. Libien, Hepatic stellate cell lipid droplets: a specialized lipid droplet for retinoid storage, Biochim. Biophys. Acta 1791 (2009) 467-473, http://dx.doi.org/10.1016/j.bbalip.2008.11.001.
2. S.L. Friedman, Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver, Physiol. Rev. 88 (2008) 125-172, http://dx.doi.org/10.1152/physrev.00013.2007.
3. N. Uyama, Y. Shimahara, N. Kawada, S. Seki, H. Okuyama, Y. Iimuro, Y. Yamaoka, Regulation of cultured rat hepatocyte proliferation by stellate cells, J. Hepatol. 36 (2002) 590-599.
4. M. Sato, T. Sato, N. Kojima, K. Imai, N. Higashi, D.R.Wang, H. Senoo, 3-D structure of extracellular matrix regulates gene expression in cultured hepatic stellate cells to induce process elongation, Comp. Hepatol. 3 (Suppl. 1) (2004) S4, http://dx.doi.org/10.1186/1476-5926-2-S1-S4.
5. M. Okuno, H. Moriwaki, S. Imai, Y. Muto, N. Kawada, Y. Suzuki, S. Kojima, Retinoids exacerbate rat liver fibrosis by inducing the activation of latent TGF-beta in liver stellate cells, Hepatology 26 (1997) 913-921, http://dx.doi.org/10.1053/jhep.1997.v26.pm0009328313.
6. S.L. Friedman, Liver fibrosis - from bench to bedside, J. Hepatol. 38 (Suppl. 1) (2003) S38-S53.
7. N. Testerink, M. Ajat, M. Houweling, J.F. Brouwers, V.V. Pully, H.J. vanManen, C. Otto, J.B. Helms, A.B. Vaandrager, Replacement of retinyl esters by polyunsaturated triacylglycerol species in lipid droplets of hepatic stellate cells during activation, PLoS ONE 7 (2012) e34945, http://dx.doi.org/10.1371/journal.pone.0034945.
8. L.O. Li, E.L. Klett, R.A. Coleman, Acyl-CoA synthesis, lipid metabolism and lipotoxicity, Biochim. Biophys. Acta 1801 (2010) 246-251, http://dx.doi.org/10.1016/j.bbalip.2009.09.024.
9. D.G. Mashek, L.O. Li, R.A. Coleman, Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet, J. Lipid Res. 47 (2004-2010), http://dx.doi.org/10.1194/jlr.M600150-JLR200.
10. P.C. Calder, R.F. Grimble, Polyunsaturated fatty acids, inflammation and immunity, Eur. J. Clin. Nutr. 56 (Suppl. 3) (2002) S14-S19, http://dx.doi.org/10.1038/sj.ejcn.1601478.
11. H. Harizi, J.B. Corcuff, N. Gualde, Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology, Trends Mol. Med. 14 (2008) 461-469, http://dx. doi.org/10.1016/j.molmed.2008.08.005.
12. S.A. Farber, E.S. Olson, J.D. Clark, M.E. Halpern, Characterization of Ca2+-dependent phospholipase A2 activity during zebra fish embryogenesis, J. Biol. Chem. 274 (1999) 19338-19346.
13. L. Riccalton-Banks, R. Bhandari, J. Fry, K.M. Shakesheff, A simple method for the simultaneous isolation of stellate cells and hepatocytes from rat liver tissue, Mol. Cell. Biochem. 248 (2003) 97-102.
14. F.G. van Steenbeek, L. Van den Bossche, G.C. Grinwis, A. Kummeling, I.H. van Gils, M.J. Koerkamp, D. van Leenen, F.C. Holstege, L.C. Penning, J. Rothuizen, P.A. Leegwater, B. Spee, Aberrant gene expression in dogs with portosystemic shunts, PLoS ONE 8 (2013) e57662, http://dx.doi.org/10.1371/journal.pone.0057662.
15. E.G. Bligh,W.J. Dyer, A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol. 37 (1959) 911-917.
16. K. Retra, O.B. Bleijerveld, R.A. van Gesteil, A.G.M. Tielens, J.J. van Hellemond, J.F. Brouwers, A simple and universal method for the separation and identification of phospholipid molecular species, Rapid Commun. Mass Spectrom. 22 (2008) 1853-1862, http://dx.doi.org/10.1002/rcm.3562.
17. M. Kates, Techniques of lipidology: isolation, analysis and identification of lipids, in: R.H. Burdon, P.H. Van Knippenberg (Eds.), In Laboratory Techniques in Biochemistry and Molecular Biology, 2nd ed., 125, Elsevier, Amsterdam, 1986.
18. H. Aardema, F. Lolicato, C.H. van de Lest, J.F. Brouwers, A.B. Vaandrager, H.T. van Tol, B.A. Roelen, P.L. Vos, J.B.Helms, B.M. Gadella, Bovine cumulus cells protectmaturing oocytes from increased fatty acid levels by massive intracellular lipid storage, Biol. Reprod. 88 (2013) 164 1-164 15, http://dx.doi.org/10.1095/biolreprod.112.106062.
19. J.C. de Grauw, C.H. van de Lest, P.R. van Weeren, A targeted lipidomics approach to the study of eicosanoid release in synovial joints, Arthritis Res. Ther. 13 (2011) R123, http://dx.doi.org/10.1186/ar3427.
20. D.L. Golej, B. Askari, F. Kramer, S. Barnhart, A. Vivekanandan-Giri, S. Pennathur, K.E. Bornfeldt, Long-chain acyl-CoA synthetase 4 modulates prostaglandin E(2) release from human arterial smooth muscle cells, J. Lipid Res. 52 (2011) 782-793, http://dx.doi.org/10.1194/jlr.M013292.
21. B. Askari, J.E. Kanter, A.M. Sherrid, D.L. Golej, A.T. Bender, J. Liu, W.A. Hsueh, J.A. Beavo, R.A. Coleman, K.E. Bornfeldt, Rosiglitazone inhibits acyl-CoA synthetase activity and fatty acid partitioning to diacylglycerol and triacylglycerol via a peroxisome proliferator-activated receptor-gamma-independent mechanism in human arterial smooth muscle cells and macrophages, Diabetes 56 (2007) 1143-1152, http://dx.doi.org/10.2337/db06-0267.
22. F.J. Eng, S.L. Friedman, I. Fibrogenesis, New insights into hepatic stellate cell activation: the simple becomes complex, Am. J. Physiol. Gastrointest. Liver Physiol. 279 (2000) G7-G11.
23. L. Al-Alem, R.C. Southard,M.W. Kilgore, T.E. Curry, Specific thiazolidinediones inhibit ovarian cancer cell line proliferation and cause cell cycle arrest in a PPARgamma independent manner, PLoS ONE 6 (2011) e16179, http://dx.doi.org/10.1371/journal. pone.0016179.
24. H.E. Ferguson, A. Kulkarni, G.M. Lehmann, T.M. Garcia-Bates, T.H. Thatcher, K.R. Huxlin, R.P. Phipps, P.J. Sime, Electrophilic peroxisome proliferator-activated receptor-gamma ligands have potent antifibrotic effects in human lung fibroblasts, Am. J. Respir. Cell Mol. Biol. 41 (2009) 722-730, http://dx.doi.org/10.1165/rcmb. 2009-0006OC.
25. E.L. Klett, S. Chen, M.L. Edin, L.O. Li, O. Ilkayeva, D.C. Zeldin, C.B. Newgard, R.A. Coleman, Diminished Acyl-CoA synthetase isoform 4 activity in INS 832/13 cells reduces cellular epoxyeicosatrienoic acid levels and results in impaired glucosestimulated insulin secretion, J. Biol. Chem. 288 (2013) 21618-21629, http://dx.doi. org/10.1074/jbc.M113.481077.
26. D.G. Mashek, L.O. Li, R.A. Coleman, Long-chain acyl-CoA synthetases and fatty acid channeling, Futur. Lipidol. 2 (2007) 465-476.
27. F. Wilfling, H. Wang, J.T. Haas, N. Krahmer, T.J. Gould, A. Uchida, J.X. Cheng, M. Graham, R. Christiano, F. Frohlich, X. Liu, K.K. Buhman, R.A. Coleman, J. Bewersdorf, R.V. Farese Jr., T.C. Walther, Triacylglycerol synthesis enzymesmediate lipid droplet growth by relocalizing from the ER to lipid droplets, Dev. Cell 24 (2013) 384-399, http://dx.doi.org/10.1016/j.devcel.2013.01.013.
28. P. Liu, Y. Ying, Y. Zhao, D.I. Mundy, M. Zhu, R.G. Anderson, Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traf fic, J. Biol. Chem. 279 (2004) 3787-3792, http://dx.doi.org/10.1074/jbc. M311945200.
29. D.L. Brasaemle, G. Dolios, L. Shapiro, R. Wang, Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes, J. Biol. Chem. 279 (2004) 46835-46842, http://dx.doi.org/10.1074/jbc. M409340200.
30. E. Umlauf, E. Csaszar, M. Moertelmaier, G.J. Schuetz, R.G. Parton, R. Prohaska, Association of stomatin with lipid bodies, J. Biol. Chem. 279 (2004) 23699-23709, http://dx.doi.org/10.1074/jbc.M310546200.
31. S.Y. Cho, E.S. Shin, P.J. Park, D.W. Shin, H.K. Chang, D. Kim, H.H. Lee, J.H. Lee, S.H. Kim, M.J. Song, I.S. Chang, O.S. Lee, T.R. Lee, Identification of mouse Prp19p as a lipid droplet-associated protein and its possible involvement in the biogenesis of lipid droplets, J. Biol. Chem. 282 (2007) 2456-2465, http://dx.doi.org/10.1074/jbc. M608042200.
32. H. Shindou, D. Hishikawa, T. Harayama, M. Eto, T. Shimizu, Generation of membrane diversity by lysophospholipid acyltransferases, J. Biochem. 154 (2013) 21-28, http://dx.doi.org/10.1093/jb/mvt048.
33. A. Galli, D.W. Crabb, E. Ceni, R. Salzano, T. Mello, G. Svegliati-Baroni, F. Ridolfi, L. Trozzi, C. Surrenti, A. Casini, Antidiabetic thiazolidinediones inhibit collagen synthesis and hepatic stellate cell activation in vivo and in vitro, Gastroenterology 122 (2002) 1924-1940.
34. T.Miyahara, L. Schrum, R. Rippe, S. Xiong, H.F. Yee Jr., K. Motomura, F.A. Anania, T.M. Willson, H. Tsukamoto, Peroxisome proliferator-activated receptors and hepatic stellate cell activation, J. Biol. Chem. 275 (2000) 35715-35722, http://dx.doi.org/ 10.1074/jbc.M006577200.
35. P.T. Bozza, K.G. Magalhaes, P.F. Weller, Leukocyte lipid bodies - biogenesis and functions in in flammation, Biochim. Biophys. Acta 1791 (2009) 540-551, http://dx.doi.org/10.1016/j.bbalip.2009.01.005.
36. H.J. van Manen, Y.M. Kraan, D. Roos, C. Otto, Single-cell Raman and fluorescence microscopy reveal the association of lipid bodies with phagosomes in leukocytes, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10159-10164, http://dx.doi.org/10.1073/pnas. 0502746102.
37. P.M. Maloberti, A.B. Duarte, U.D. Orlando,M.E. Pasqualini, A.R. Solano, C. Lopez-Otin, E.J. Podesta, Functional interaction between acyl-CoA synthetase 4, lipooxygenases and cyclooxygenase-2 in the aggressive phenotype of breast cancer cells, PLoS ONE 5 (2010) e15540, http://dx.doi.org/10.1371/journal.pone.0015540.
38. H.S. Chou, C.C. Hsieh, H.R. Yang, L. Wang, Y. Arakawa, K. Brown, Q. Wu, F. Lin, M. Peters, J.J. Fung, L. Lu, S. Qian, Hepatic stellate cells regulate immune response by way of induction of myeloid suppressor cells in mice, Hepatology 53 (2011) 1007-1019, http://dx.doi.org/10.1002/hep.24162.