High-fructose feeding promotes accelerated degradation of hepatic LDL receptor and hypercholesterolemia in hamsters via elevated circulating PCSK9 levels

Atherosclerosis

Volumn 239, Issue 2, 2015, Pages 364-374

  Dong, Bin ^a   Singh, Amar Bahadur ^a   Azhar, Salman ^a   Seidah, Nabil G ^b   Liu, Jingwen ^a  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Dyslipidemia; Hamsters; High fructose diet; LDL receptor; PCSK9

Indexed keywords

FRUCTOSE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; PLASMA PROTEIN; PROPROTEIN CONVERTASE SUBTILISIN KEXIN TYPE 9; SORTILIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; CHOLESTEROL; PCSK9 PROTEIN, MOUSE; SERINE PROTEINASE;

ANIMAL EXPERIMENT; ARTICLE; ATHEROGENIC DIET; CHOLESTEROL BLOOD LEVEL; DYSLIPIDEMIA; GENE EXPRESSION; HAMSTER; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERCHOLESTEROLEMIA; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEK293 CELL LINE; HUMAN; INSULIN RESISTANCE; LIVER; MESOCRICETUS; METABOLISM;

ANIMALS; CHOLESTEROL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRICETINAE; DIET, ATHEROGENIC; DYSLIPIDEMIAS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FRUCTOSE; HEK293 CELLS; HUMANS; INSULIN RESISTANCE; LIVER; MALE; MESOCRICETUS; MICE; MICE, INBRED C57BL; PROPROTEIN CONVERTASES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LDL; SERINE ENDOPEPTIDASES;

EID: 84922575455     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2015.01.013     Document Type: Article

References (43)

1. Horton J.D., Cohen J.C., Hobbs H.H. Molecular biology of PCSK9: its role in LDL metabolism. Trends Biochem. Sci. 2006, 32:71-77.
2. Benjannet S., Rhainds D., Hamelin J., Nassoury N., Seidah N.G. The proprotein convertase (PC) PCSK9 is inactivated by furin and/or PC5/6A: functional consequences of natural mutations and post-translational modifications. J.Biol. Chem. 2006, 281:30561-30572.
3. Essalmani R., Susan-Resiga D., Chamberland A., et al. Invivo evidence that furin from hepatocytes inactivates PCSK9. J.Biol. Chem. 2011, 286:4257-4263.
4. Lipari M.T., Li W., Moran P., et al. Furin-cleaved proprotein convertase subtilisin/kexin type 9 (PCSK9) is active and modulates low density lipoprotein receptor and serum cholesterol levels. J.Biol. Chem. 2012, 287:43482-43491.
5. Grefhorst A., McNutt M.C., Lagace T.A., Horton J.D. Plasma PCSK9 preferentially reduces liver LDL receptors in Mice. J.Lipid Res. 2008, 49:1303-1311.
6. Lambert G., Ancellin N., Charlton F., et al. Plasma PCSK9 concentration correlate with LDL and total cholesterol in diabetic patients and are decreased by fenofibrate treatment. Clin. Chem. 2008, 54:1038-1045.
7. Lakoski S.G., Lagace T.A., Cohen J.C., Horton J.D., Hobbs H.H. Genetic and metabolic determinants of plasma PCSK9 levels. J.Clin. Endocrinol. Metab. 2009, 94:2537-2543.
8. Seidah N.G. PCSK9 as a therapeutic target of dyslipidemia. Expert Opin. Ther. Targets 2009, 13:19-28.
9. Hooper A.J., Burnett J.R. Anti-PCSK9 therapies for the treatment of hypercholesterolemia. Expert Opin. Biol. Ther. 2013, 13:429-435.
10. Graham M.J., Lemonidis K.M., Whipple C.P., et al. Antisense inhibition of proprotein convertase subtilisin/kexin type 9 reduces serum LDL in hyperlipidemic mice. J.Lipid Res. 2007, 48:763-767.
11. Frank-Kamenetsky M., Grefhouse A., Anderson N.N., et al. Therapeutic RNAi targeting PCSK9 acutely lowers plasma cholestertol in rodents and LDL cholesterol in nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11915-11920.
12. Ling H., Burns T.L., Hilleman D.E. An update on the clinical development of proprotein convertase subtilisin kexin 9 inhibitors, novel therapeutic agents for lowering low-density lipoprotein cholesterol. Cardiovasc. Ther. 2014, 32:82-88.
13. Cariou B., Langhi C., Le B.M., et al. Plasma PCSK9 concentrations during an oral fat load and after short term high-fat, high-fat high-protein and high-fructose diets. Nutr. Metab. (Lond.) 2013, 10:4.
14. Tappy L., Le K.A. Metabolic effects of fructose and the worldwide increase in obesity. Physiol. Rev. 2010, 90:23-46.
15. Koo H.Y., Miyashita M., Cho B.H., Nakamura M.T. Replacing dietary glucose with fructose increases ChREBP activity and SREBP-1 protein in rat liver nucleus. Biochem. Biophys. Res. Commun. 2009, 390:285-289.
16. Saravanan M., Pandikumar P., Saravanan S., Toppo E., Pazhanivel N., Ignacimuthu S. Lipolytic and antiadipogenic effects of (3,3-dimethylallyl) halfordinol on 3T3-L1 adipocytes and High fat and fructose diet induced obese C57/BL6J mice. Eur.J Pharmacol. 2014, 740:714-721.
17. Cheng Q., Zhang X., Wang O., et al. Anti-diabetic effects of the ethanol extract of a functional formula diet in mice fed with a fructose/fat-rich combination diet. J.Sci. Food Agric. 2015, 95:401-408.
18. Nunes P.M., Wright A.J., Veltien A., et al. Dietary lipids do not contribute to the higher hepatic triglyceride levels of fructose- compared to glucose-fed mice. FASEB J. 2014, 28:1988-1997.
19. Dissard R., Klein J., Caubet C., et al. Long term metabolic syndrome induced by a high fat high fructose diet leads to minimal renal injury in C57BL/6 mice. PLoS One 2013, 8:e76703.
20. Debosch B.J., Chen Z., Finck B.N., Chi M., Moley K.H. Glucose transporter-8 (GLUT8) mediates glucose intolerance and dyslipidemia in high-fructose diet-fed male mice. Mol. Endocrinol. 2013, 27:1887-1896.
21. Singh A.B., Kan C.F., Shende V., Dong B., Liu J. Anovel posttranscriptional mechanism for dietary cholesterol-mediated suppression of liver LDL receptor expression. J.Lipid Res. 2014, 55:1397-1407.
22. Briand F., Thieblemont Q., Muzotte E., Sulpice T. High-fat and fructose intake induces insulin resistance, dyslipidemia, and liver steatosis and alters invivo macrophage-to-feces reverse cholesterol transport in hamsters. J.Nutr. 2012, 142:704-709.
23. Hayashi A.A., Webb J., Choi J., et al. Intestinal SR-BI is upregulated in insulin-resistant states and is associated with overproduction of intestinal apoB48-containing lipoproteins. Am. J Physiol. Gastrointest. Liver Physiol. 2011, 301:G326-G337.
24. Hsieh J., Hayashi A.A., Webb J., Adeli K. Postprandial dyslipidemia in insulin resistance: mechanisms and role of intestinal insulin sensitivity. Atheroscler. Suppl. 2008, 9:7-13.
25. Basciano H., Miller A.E., Naples M., et al. Metabolic effects of dietary cholesterol in an animal model of insulin resistance and hepatic steatosis. Am. J Physiol. Endocrinol. Metab. 2009, 297:E462-E473.
26. Dong B., Singh A.B., Kan F.C., Liu J. CETP inhibitors downregulate hepatic LDL receptor and PCSK9 expression invitro and invivo through a SREBP2 dependent mechanism. Atherosclerosis 2014, 235:449-462.
27. Wu M., Dong B., Cao A., Li H., Liu J. Delineation of molecular pathways that regulate hepatic PCSK9 and LDL receptor expression during fasting in normolipidemic hamsters. Atherosclerosis 2012, 224:401-410.
28. Havel R.J., Eder H.A., Bragdon J.H. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J.Clin. Invest. 1955, 34:1345-1353.
29. Faergeman O., Sata T., Kane J.P., Havel R.J. Metabolism of apoprotein B of plasma very low density lipoproteins in the rat. J.Clin. Invest. 1975, 56:1396-1403.
30. Rashid S., Curtis D.E., Garuti R., et al. Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. PNAS 2005, 102:5374-5379.
31. Kosenko T., Golder M., Leblond G., Weng W., Lagace T.A. Low density lipoprotein binds to proprotein convertase subtilisin/kexin type-9 (PCSK9) in human plasma and inhibits PCSK9-mediated low density lipoprotein receptor degradation. J.Biol. Chem. 2013, 288:8279-8288.
32. Lambert G., Jarnoux A.L., Pineau T., et al. Fasting induces hyperlipidemia in mice overexpressing proprotein convertase subtilisin kexin type 9: lack of modulation of very-low-density lipoprotein hepatic output by the low-density lipoprotein receptor. Endocrinology 2006, 147:4985-4995.
33. Tavori H., Fan D., Blakemore J.L., et al. Serum proprotein convertase subtilisin/kexin type 9 and cell surface low-density lipoprotein receptor: evidence for a reciprocal regulation. Circulation 2013, 127:2403-2413.
34. Zaid A., Roubtsova A., Essalmani R., et al. Proprotein convertase subtilisin/kexin type 9 (PCSK9): hepatocyte-specific low-density lipoprotein receptor degradation and critical role in mouse liver regeneration. Hepatology 2008, 48:646-654.
35. Jeong H.J., Lee H.-S., Kim K.-S., Kim Y.-K., Yoon D., Park S.W. Sterol-dependent regulation of proprotein convertase subtilisin/kexin type 9 expression by sterol-regulatory element binding protein-2. J.Lipid Res. 2008, 49:399-409.
36. Li H., Dong B., Park S.W., Lee H.S., Chen W., Liu J. Hepatocyte nuclear factor 1alpha plays a critical role in PCSK9 gene transcription and regulation by the natural hypocholesterolemic compound berberine. J.Biol. Chem. 2009, 284:28885-28895.
37. Zelcer N., Hong C., Boyadjian R., Tontonoz P. LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science 2009, 325:100-104.
38. Gustafsen C., Kjolby M., Nyegaard M., et al. The hypercholesterolemia-risk gene SORT1 facilitates PCSK9 secretion. Cell Metab. 2014, 19:310-318.
39. Sun H., Samarghandi A., Zhang N., Yao Z., Xiong M., Teng B.B. Proprotein convertase subtilisin/kexin type 9 interacts with apolipoprotein B and prevents its intracellular degradation, irrespective of the low-density lipoprotein receptor. Arterioscler. Thromb. Vasc. Biol. 2012, 32:1585-1595.
40. Luo Y., Warren L., Xia D., et al. Function and distribution of circulating human PCSK9 expressed extrahepatically in transgenic mice. J.Lipid Res. 2009, 50:1581-1588.
41. Maxwell K.N., Breslow J.L. Adenoviral-mediated expression of Pcsk9 in mice results in a low-density lipoprotein receptor knockout phenotype. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7100-7105.
42. Han B., Eacho P.I., Knierman M.D., et al. Isolation and characterization of the circulating truncated form of PCSK9. J.Lipid Res. 2014, 55:1505-1514.
43. Simopoulos A.P. Dietary omega-3 fatty acid deficiency and high fructose intake in the development of metabolic syndrome, brain metabolic abnormalities, and non-alcoholic fatty liver disease. Nutrients 2013, 5:2901-2923.