Fish oil and fenofibrate prevented phosphorylation-dependent hepatic sortilin 1 degradation in western diet-fed mice

Journal of Biological Chemistry

Volumn 289, Issue 32, 2014, Pages 22437-22449

  Li, Jibiao ^a   Bi, Lipeng ^a   Hulke, Michelle ^a   Li, Tiangang ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; PHYSIOLOGY;

DOWN-REGULATION; FENOFIBRATE; FISH OIL; IN-VIVO; PLASMA LIPID;

NUTRITION;

ANTILIPEMIC AGENT; FENOFIBRATE; FISH OIL; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; SERINE; SORTILIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADVERSE EFFECTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CHEMISTRY; DEFICIENCY; DIABETES MELLITUS, TYPE 2; GENE SILENCING; GENETICS; HEPG2 CELL LINE; HUMAN; KNOCKOUT MOUSE; LIPID METABOLISM; LIVER; MALE; METABOLISM; MOUSE; MOUSE MUTANT; OBESITY; PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN STABILITY; WESTERN DIET;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; DIABETES MELLITUS, TYPE 2; DIET, WESTERN; FENOFIBRATE; FISH OILS; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HUMANS; HYPOLIPIDEMIC AGENTS; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; OBESITY; PHOSPHORYLATION; PPAR ALPHA; PROTEIN STABILITY; PROTEOLYSIS; RNA, MESSENGER; SERINE;

EID: 84905851432     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.548933     Document Type: Article

References (50)

1. Reaven, G. M. (2002) MultipleCHDrisk factors in type 2 diabetes: beyond hyperglycaemia. Diabetes Obes. Metab. 4, S13-S18
2. Adiels, M., Borén, J., Caslake, M. J., Stewart, P., Soro, A., Westerbacka, J., Wennberg, B., Olofsson, S. O., Packard, C., and Taskinen, M. R. (2005) Overproduction of VLDL1 driven by hyperglycemia is a dominant feature of diabetic dyslipidemia. Arterioscler. Thromb. Vasc. Biol. 25, 1697-1703
3. Boden, G., and Shulman, G. I. (2002) Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and beta-cell dysfunction. Eur. J. Clin. Invest. 32, 14-23
4. Cohen, J. C., Horton, J. D., and Hobbs, H. H. (2011) Human fatty liver disease: old questions and new insights. Science 332, 1519-1523
5. Choi, S. H., and Ginsberg, H. N. (2011) Increased very low density lipoprotein (VLDL) secretion, hepatic steatosis, and insulin resistance. Trends Endocrinol. Metab. 22, 353-363
6. Eguchi, K., Manabe, I., Oishi-Tanaka, Y., Ohsugi, M., Kono, N., Ogata, F., Yagi, N., Ohto, U., Kimoto, M., Miyake, K., Tobe, K., Arai, H., Kadowaki, T., and Nagai, R. (2012) Saturated fatty acid and TLR signaling link beta cell dysfunction and islet inflammation. Cell Metab. 15, 518-533
7. Shi, H., Kokoeva, M. V., Inouye, K., Tzameli, I., Yin, H., and Flier, J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025
8. Holland, W. L., Bikman, B. T., Wang, L. P., Yuguang, G., Sargent, K. M., Bulchand, S., Knotts, T. A., Shui, G., Clegg, D. J., Wenk, M. R., Pagliassotti, M. J., Scherer, P. E., and Summers, S. A. (2011) Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice. J. Clin. Invest. 121, 1858-1870
9. Ding, Y., Subramanian, S., Montes, V. N., Goodspeed, L., Wang, S., Han, C., Teresa, A. S., 3rd, Kim, J., O'Brien, K. D., and Chait, A. (2012) Toll-like receptor 4 deficiency decreases atherosclerosis but does not protect against inflammation in obese low-density lipoprotein receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 32, 1596-1604
10. Cusi, K. (2012) Role of obesity and lipotoxicity in the development of nonalcoholic steatohepatitis: pathophysiology and clinical implications. Gastroenterology 142, 711-725.e6
11. Griffin, M. E., Marcucci, M. J., Cline, G. W., Bell, K., Barucci, N., Lee, D., Goodyear, L. J., Kraegen, E. W., White, M. F., and Shulman, G. I. (1999) Free fatty acid-induced insulin resistance is associated with activation of protein kinase C α and alterations in the insulin signaling cascade. Diabetes 48, 1270-1274
12. Lewis, G. F., and Steiner, G. (1996) Acute effects of insulin in the control of VLDL production in humans. Implications for the insulin-resistant state. Diabetes Care 19, 390-393
13. Taghibiglou, C., Rashid-Kolvear, F., Van Iderstine, S. C., Le-Tien, H., Fantus, I. G., Lewis, G. F., and Adeli, K. (2002) Hepatic very low density lipoprotein-apoB overproduction is associated with attenuated hepatic insulin signaling and overexpression of protein-tyrosine phosphatase 1B in a fructose-fed hamster model of insulin resistance. J. Biol. Chem. 277, 793-803
14. Steinberg, H. O., and Baron, A. D. (2002) Vascular function, insulin resistance and fatty acids. Diabetologia 45, 623-634
15. Tripathy, D., Aljada, A., and Dandona, P. (2003) Free fatty acids (FFA) and endothelial dysfunction; role of increased oxidative stress and inflammation.-to: Steinberg et al. (2002) Vascular function, insulin resistance and fatty acids. Diabetologia 46, 300-301
16. Liu, L., Li, Y., Guan, C., Li, K., Wang, C., Feng, R., and Sun, C. (2010) Free fatty acid metabolic profile and biomarkers of isolated post-challenge diabetes and type 2 diabetes mellitus based on GC-MS and multivariate statistical analysis. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 878, 2817-2825
17. Musunuru, K., Strong, A., Frank-Kamenetsky, M., Lee, N. E., Ahfeldt, T., Sachs, K. V., Li, X., Li, H., Kuperwasser, N., Ruda, V. M., Pirruccello, J. P., Muchmore, B., Prokunina-Olsson, L., Hall, J. L., Schadt, E. E., Morales, C. R., Lund-Katz, S., Phillips, M. C., Wong, J., Cantley, W., Racie, T., Ejebe, K. G., Orho-Melander, M., Melander, O., Koteliansky, V., Fitzgerald, K., Krauss, R. M., Cowan, C. A., Kathiresan, S., and Rader, D. J. (2010) From noncoding variant to phenotype via SORT1 at the 1p13 cholesterol locus. Nature 466, 714-719
18. Linsel-Nitschke, P., Heeren, J., Aherrahrou, Z., Bruse, P., Gieger, C., Illig, T., Prokisch, H., Heim, K., Doering, A., Peters, A., Meitinger, T., Wichmann, H. E., Hinney, A., Reinehr, T., Roth, C., Ortlepp, J. R., Soufi, M., Sattler, A. M., Schaefer, J., Stark, K., Hengstenberg, C., Schaefer, A., Schreiber, S., Kronenberg, F., Samani, N. J., Schunkert, H., and Erdmann, J. (2010) Genetic variation at chromosome 1p13.3 affects sortilin mRNA expression, cellular LDL-uptake and serum LDL levels which translates to the risk of coronary artery disease. Atherosclerosis 208, 183-189
19. Kathiresan, S., Melander, O., Guiducci, C., Surti, A., Burtt, N. P., Rieder, M. J., Cooper, G. M., Roos, C., Voight, B. F., Havulinna, A. S., Wahlstrand, B., Hedner, T., Corella, D., Tai, E. S., Ordovas, J. M., Berglund, G., Vartiainen, E., Jousilahti, P., Hedblad, B., Taskinen, M. R., Newton-Cheh, C., Salomaa, V., Peltonen, L., Groop, L., Altshuler, D. M., and Orho-Melander, M. (2008) Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat. Genet. 40, 189-197
20. Myocardial Infarction Genetics Consortium, Kathiresan, S., Voight, B. F., Purcell, S., Musunuru, K., Ardissino, D., Mannucci, P. M., Anand, S., Engert, J. C., Samani, N. J., Schunkert, H., Erdmann, J., Reilly, M. P., Rader, D. J., Morgan, T., Spertus, J. A., Stoll, M., Girelli, D., McKeown, P. P., Patterson, C. C., Siscovick, D. S., O'Donnell, C. J., Elosua, R., Peltonen, L., Salomaa, V., Schwartz, S. M., Melander, O., Altshuler, D., Ardissino, D., Merlini, P. A., Berzuini, C., Bernardinelli, L., Peyvandi, F., Tubaro, M., Celli, P., Ferrario, M., Fetiveau, R., Marziliano, N., Casari, G., Galli, M., Ribichini, F., Rossi, M., Bernardi, F., Zonzin, P., Piazza, A., Mannucci, P. M., Schwartz, S. M., Siscovick, D. S., Yee, J., Friedlander, Y., Elosua, R., Marrugat, J., Lucas, G., Subirana, I., Sala, J., Ramos, R., Kathiresan, S., Meigs, J. B., Williams, G., Nathan, D. M., MacRae, C. A., O'Donnell, C. J., Salomaa, V., Havulinna, A. S., Peltonen, L., Melander, O., Berglund, G., Voight, B. F., Kathiresan, S., Hirschhorn, J. N., Asselta, R., Duga, S., Spreafico, M., Musunuru, K., Daly, M. J., Purcell, S., Voight, B. F., Purcell, S., Nemesh, J., Korn, J. M., McCarroll, S. A., Schwartz, S. M., Yee, J., Kathiresan, S., Lucas, G., Subirana, I., Elosua, R., Surti, A., Guiducci, C., Gianniny, L., Mirel, D., Parkin, M., Burtt, N., Gabriel, S. B., Samani, N. J., Thompson, J. R., Braund, P. S., Wright, B. J., Balmforth, A. J., Ball, S. G., Hall, A., Wellcome Trust Case Control, C., Schunkert, H., Erdmann, J., Linsel-Nitschke, P., Lieb, W., Ziegler, A., Konig, I., Hengstenberg, C., Fischer, M., Stark, K., Grosshennig, A., Preuss, M., Wichmann, H. E., Schreiber, S., Schunkert, H., Samani, N. J., Erdmann, J., Ouwehand, W., Hengstenberg, C., Deloukas, P., Scholz, M., Cambien, F., Reilly, M. P., Li, M., Chen, Z., Wilensky, R., Matthai, W., Qasim, A., Hakonarson, H. H., Devaney, J., Burnett, M. S., Pichard, A. D., Kent, K. M., Satler, L., Lindsay, J. M., Waksman, R., Knouff, C. W., Waterworth, D. M., Walker, M. C., Mooser, V., Epstein, S. E., Rader, D. J., Scheffold, T., Berger, K., Stoll, M., Huge, A., Girelli, D., Martinelli, N., Olivieri, O., Corrocher, R., Morgan, T., Spertus, J. A., McKeown, P., Patterson, C. C., Schunkert, H., Erdmann, E., Linsel-Nitschke, P., Lieb, W., Ziegler, A., Konig, I. R., Hengstenberg, C., Fischer, M., Stark, K., Grosshennig, A., Preuss, M., Wichmann, H. E., Schreiber, S., Holm, H., Thorleifsson, G., Thorsteinsdottir, U., Stefansson, K., Engert, J. C., Do, R., Xie, C., Anand, S., Kathiresan, S., Ardissino, D., Mannucci, P. M., Siscovick, D., O'Donnell, C. J., Samani, N. J., Melander, O., Elosua, R., Peltonen, L., Salomaa, V., Schwartz, S. M., and Altshuler, D. (2009) Genome-wide association of early-onset myocardial infarction with single nucleotide polymorphisms and copy number variants. Nat. Genet. 41, 334-341
21. Hermey, G. (2009) The Vps10p-domain receptor family. Cell Mol. Life Sci. 66, 2677-2689
22. Nielsen, M. S., Jacobsen, C., Olivecrona, G., Gliemann, J., and Petersen, C. M. (1999) Sortilin/neurotensin receptor-3 binds and mediates degradation of lipoprotein lipase. J. Biol. Chem. 274, 8832-8836
23. Nilsson, S. K., Christensen, S., Raarup, M. K., Ryan, R. O., Nielsen, M. S., and Olivecrona, G. (2008) Endocytosis of apolipoprotein A-V by members of the low density lipoprotein receptor and the VPS10p domain receptor families. J. Biol. Chem. 283, 25920-25927
24. 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
25. Kjolby, M., Andersen, O. M., Breiderhoff, T., Fjorback, A. W., Pedersen, K. M., Madsen, P., Jansen, P., Heeren, J., Willnow, T. E., and Nykjaer, A. (2010) Sort1, encoded by the cardiovascular risk locus 1p13.3, is a regulator of hepatic lipoprotein export. Cell Metab. 12, 213-223
26. Gustafsen, C., Kjolby, M., Nyegaard, M., Mattheisen, M., Lundhede, J., Buttenschøn, H., Mors, O., Bentzon, J. F., Madsen, P., Nykjaer, A., and Glerup, S. (2014) The hypercholesterolemia-risk gene SORT1 facilitates PCSK9 secretion. Cell Metab. 19, 310-318
27. Bi, L., Chiang, J. Y., Ding, W. X., Dunn, W., Roberts, B., and Li, T. (2013) Saturated fatty acids activate ERK signaling to down-regulate hepatic sortilin 1 in obese and diabetic mice. J. Lipid Res. 54, 2754-2762
28. Murali, G., Milne, G. L., Webb, C. D., Stewart, A. B., McMillan, R. P., Lyle, B. C., Hulver, M. W., and Saraswathi, V. (2012) Fish oil and indomethacin in combination potently reduce dyslipidemia and hepatic steatosis in LDLR(/) mice. J. Lipid Res. 53, 2186-2197
29. Mikami, N., Hosokawa, M., and Miyashita, K. (2012) Dietary combination of fish oil and taurine decreases fat accumulation and ameliorates blood glucose levels in type 2 diabetic/obese KK-A(y) mice. J. Food Sci. 77, H114-H120
30. Neschen, S., Morino, K., Dong, J., Wang-Fischer, Y., Cline, G. W., Romanelli, A. J., Rossbacher, J. C., Moore, I. K., Regittnig, W., Munoz, D. S., Kim, J. H., and Shulman, G. I. (2007) n-3 Fatty acids preserve insulin sensitivity in vivo in a peroxisome proliferator-activated receptor-dependent manner. Diabetes 56, 1034-1041
31. Oosterveer, M. H., Grefhorst, A., van Dijk, T. H., Havinga, R., Staels, B., Kuipers, F., Groen, A. K., and Reijngoud, D. J. (2009) Fenofibrate simultaneously induces hepatic fatty acid oxidation, synthesis, and elongation in mice. J. Biol. Chem. 284, 34036-34044
32. Choi, S. E., Lee, S. M., Lee, Y. J., Li, L. J., Lee, S. J., Lee, J. H., Kim, Y., Jun, H. S., Lee, K. W., and Kang, Y. (2009) Protective role of autophagy in palmitate-induced INS-1 beta-cell death. Endocrinology 150, 126-134
33. Li, T., Owsley, E., Matozel, M., Hsu, P., Novak, C. M., and Chiang, J. Y. (2010) Transgenic expression of cholesterol 7-hydroxylase in the liver prevents high-fat diet-induced obesity and insulin resistance in mice. Hepatology 52, 678-690
34. Pan, M., Cederbaum, A. I., Zhang, Y. L., Ginsberg, H. N., Williams, K. J., and Fisher, E. A. (2004) Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J. Clin. Invest. 113, 1277-1287
35. Bordin, P., Bodamer, O. A., Venkatesan, S., Gray, R. M., Bannister, P. A., and Halliday, D. (1998) Effects of fish oil supplementation on apolipoprotein B100 production and lipoprotein metabolism in normolipidaemic males. Eur. J. Clin. Nutr. 52, 104-109
36. Park, Y., and Harris, W. S. (2003)-3 fatty acid supplementation accelerates chylomicron triglyceride clearance. J. Lipid Res. 44, 455-463
37. Zuliani, G., Galvani, M., Leitersdorf, E., Volpato, S., Cavalieri, M., and Fellin, R. (2009) The role of polyunsaturated fatty acids (PUFA) in the treatment of dyslipidemias. Curr. Pharm. Des. 15, 4087-4093
38. Motojima, K., Passilly, P., Peters, J. M., Gonzalez, F. J., and Latruffe, N. (1998) Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor α and α activators in a tissueand inducer-specific manner. J. Biol. Chem. 273, 16710-16714
39. Forman, B. M., Chen, J., and Evans, R. M. (1997) Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors α and. Proc. Natl. Acad. Sci. U.S.A. 94, 4312-4317
40. Calder, P. C. (2012) The role of marine-3 (n-3) fatty acids in inflammatory processes, atherosclerosis and plaque stability. Mol. Nutr. Food Res. 56, 1073-1080
41. Yaqoob, P., and Shaikh, S. R. (2010) The nutritional and clinical significance of lipid rafts. Curr. Opin. Clin. Nutr. Metab. Care 13, 156-166
42. Dumaresq-Doiron, K., Jules, F., and Lefrancois, S. (2013) Sortilin turnover is mediated by ubiquitination. Biochem. Biophys. Res. Commun. 433, 90-95
43. Ai, D., Baez, J. M., Jiang, H., Conlon, D. M., Hernandez-Ono, A., Frank-Kamenetsky, M., Milstein, S., Fitzgerald, K., Murphy, A. J., Woo, C. W., Strong, A., Ginsberg, H. N., Tabas, I., Rader, D. J., and Tall, A. R. (2012) Activation of ER stress and mTORC1 suppresses hepatic sortilin-1 levels in obese mice. J. Clin. Invest. 122, 1677-1687
44. Weitz, D., Weintraub, H., Fisher, E., and Schwartzbard, A. Z. (2010) Fish oil for the treatment of cardiovascular disease. Cardiol. Rev. 18, 258-263
45. Adkins, Y., and Kelley, D. S. (2010) Mechanisms underlying the cardioprotective effects of-3 polyunsaturated fatty acids. J. Nutr. Biochem. 21, 781-792
46. Fedor, D., and Kelley, D. S. (2009) Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr. Opin. Clin. Nutr. Metab. Care 12, 138-146
47. Denys, A., Hichami, A., and Khan, N. A. (2001) Eicosapentaenoic acid and docosahexaenoic acid modulate MAP kinase (ERK1/ERK2) signaling in human T cells. J. Lipid Res. 42, 2015-2020
48. Whyte, C., Thies, F., Peyrol, L., and Balcerzak, D. (2012) N-3 long-chain polyunsaturated fatty acids inhibit smooth muscle cell migration by modulating urokinase plasminogen activator receptor through MEK/ERK-dependent and-independent mechanisms. J. Nutr. Biochem. 23, 1378-1383
49. Gervois, P., and Mansouri, R. M. (2012) PPAR as a therapeutic target in inflammation-associated diseases. Expert Opin. Ther. Targets 16, 1113-1125
50. Klingenberg, R., Gerdes, N., Badeau, R. M., Gisterå, A., Strodthoff, D., Ketelhuth, D. F., Lundberg, A. M., Rudling, M., Nilsson, S. K., Olivecrona, G., Zoller, S., Lohmann, C., Lüscher, T. F., Jauhiainen, M., Sparwasser, T., and Hansson, G. K. (2013) Depletion of FOXP3 regulatory T cells promotes hypercholesterolemia and atherosclerosis. J. Clin. Invest. 123, 1323-1334