The association of human apolipoprotein C-III sialylation proteoforms with plasma triglycerides

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Yassine, Hussein N ^a   Trenchevska, Olgica ^b   Ramrakhiani, Ambika ^a   Parekh, Aarushi ^a   Koska, Juraj ^c   Walker, Ryan W ^a   Billheimer, Dean ^e   Reaven, Peter D ^c   Yen, Frances T ^f   Nelson, Randall W ^b   Goran, Michael I ^d   Nedelkov, Dobrin ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c CARL T HAYDEN VA MEDICAL CENTER   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ARIZONA   (United States)

^f UNIVERSITÉ DE LORRAINE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN C3; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; N ACETYLGALACTOSAMINE; TRIACYLGLYCEROL;

ADOLESCENT; AMINO ACID SYNTHESIS; ARTICLE; BLOOD SAMPLING; BODY MASS; CHILD; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GLUCOSE TOLERANCE TEST; GLYCOSYLATION; HISPANIC; HUMAN; HYPERTRIGLYCERIDEMIA; IMMUNOASSAY; INSULIN SENSITIVITY; MALE; MASS SPECTROMETRY; OBESITY; SIALYLATION; TRIACYLGLYCEROL BLOOD LEVEL; BLOOD; BODY WEIGHT; INSULIN RESISTANCE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY;

ADOLESCENT; APOLIPOPROTEIN C-III; BODY WEIGHT; CHILD; FEMALE; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MALE; OBESITY; OVERWEIGHT; TRIGLYCERIDES;

EID: 84956671120     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0144138     Document Type: Article

References (44)

1. Wang C-S, McConathy WJ, Kloer HU, Alaupovic P. Modulation of lipoprotein lipase activity by apolipoproteins. Effect of apolipoprotein C-III. Journal of Clinical Investigation. 1985; 75(2):384. PMID: 3973011
2. Breyer ED, Le N-A, Li X, Martinson D, Brown WV. Apolipoprotein C-III displacement of apolipoprotein E from VLDL: effect of particle size. Journal of lipid research. 1999; 40(10):1875-82. PMID: 10508207
3. Fredenrich A, Giroux L, Tremblay M, Krimbou L, Davignon J, Cohn J. Plasma lipoprotein distribution of apoC-III in normolipidemic and hypertriglyceridemic subjects: comparison of the apoC-III to apoE ratio in different lipoprotein fractions. Journal of lipid research. 1997; 38(7):1421-32. PMID: 9254067
4. Windler E, Havel RJ. Inhibitory effects of C apolipoproteins from rats and humans on the uptake of triglyceride-rich lipoproteins and their remnants by the perfused rat liver. Journal of lipid research. 1985; 26(5):556-65. PMID: 4020294
5. Ito Y, Azrolan N, O'Connell A, Walsh A, Breslow JL. Hypertriglyceridemia as a result of human apo CIII gene expression in transgenic mice. Science. 1990; 249(4970):790-3. PMID: 2167514
6. Crosby J, Peloso GM, Auer PL, Crosslin DR, Stitziel NO, Lange LA, et al. Loss-of-function mutations in APOC3, triglycerides, and coronary disease. The New England journal of medicine. 2014; 371(1):22-31. Epub 2014/06/19. doi: 10.1056/NEJMoa1307095 PMID: 24941081; PubMed Central PMCID: PMCPMC4180269.
7. Batal R, Tremblay M, Barrett PHR, Jacques H, Fredenrich A, Mamer O, et al. Plasma kinetics of apoC-III and apoE in normolipidemic and hypertriglyceridemic subjects. Journal of lipid research. 2000; 41(5):706-18. PMID: 10787431
8. Zheng C, Khoo C, Ikewaki K, Sacks FM. Rapid turnover of apolipoprotein C-III-containing triglyceride-rich lipoproteins contributing to the formation of LDL subfractions. Journal of lipid research. 2007; 48(5):1190-203. Epub 2007/02/23. doi: 10.1194/jlr.P600011-JLR200 PMID: 17314277.
9. Caron S, Verrijken A, Mertens I, Samanez CH, Mautino G, Haas JT, et al. Transcriptional activation of apolipoprotein CIII expression by glucose may contribute to diabetic dyslipidemia. Arteriosclerosis, thrombosis, and vascular biology. 2011; 31(3):513-9. doi: 10.1161/ATVBAHA.110.220723 PMID: 21183731
10. Li WW, Dammerman MM, Smith JD, Metzger S, Breslow JL, Leff T. Common genetic variation in the promoter of the human apo CIII gene abolishes regulation by insulin and may contribute to hypertriglyceridemia. Journal of Clinical Investigation. 1995; 96(6):2601. PMID: 8675624
11. Chen M, Breslow JL, Li W, Leff T. Transcriptional regulation of the apoC-III gene by insulin in diabetic mice: correlation with changes in plasma triglyceride levels. Journal of lipid research. 1994; 35(11):1918-24. Epub 1994/11/01. PMID: 7868970.
12. Graham MJ, Lee RG, Bell TA, Fu W, Mullick AE, Alexander VJ, et al. Antisense oligonucleotide inhibition of apolipoprotein C-III reduces plasma triglycerides in rodents, nonhuman primates, and humans. Circulation research. 2013; 112(11):1479-90. doi: 10.1161/CIRCRESAHA.111.300367 PMID: 23542898
13. Gaudet D, Alexander VJ, Baker BF, Brisson D, Tremblay K, Singleton W, et al. Antisense Inhibition of Apolipoprotein C-III in Patients with Hypertriglyceridemia. New England Journal of Medicine. 2015; 373(5):438-47. doi: 10.1056/NEJMoa1400283 PMID: 26222559
14. Brewer HB, Shulman R, Herbert P, Ronan R, Wehrly K. The complete amino acid sequence of alanine apolipoprotein (apoC-III), an apolipoprotein from human plasma very low density lipoproteins. Journal of Biological Chemistry. 1974; 249(15):4975-84. PMID: 4846755
15. Vaith P, Assmann G, Uhlenbruck G. Characterization of the oligosaccharide side chain of apolipoprotein C-III from human plasma very low density lipoproteins. Biochimica et Biophysica Acta (BBA)-General Subjects. 1978; 541(2):234-40.
16. Zannis VI, Breslow JL. Genetic mutations affecting human lipoprotein metabolism. Advances in Human Genetics 14: Springer; 1985. p. 125-215. PMID: 2986430
17. Kashyap M, Srivastava L, Hynd B, Gartside P, Perisutti G. Quantitation of human apolipoprotein C-III and its subspecie by radioimmunoassay and analytical isoelectric focusing: abnormal plasma triglyceride-rich lipoprotein apolipoprotein C-III subspecie concentrations in hypertriglyceridemia. Journal of lipid research. 1981; 22(5):800-10. PMID: 7288286
18. Mauger J-F, Couture P, Bergeron N, Lamarche B. Apolipoprotein C-III isoforms: kinetics and relative implication in lipid metabolism. Journal of lipid research. 2006; 47(6):1212-8. PMID: 16495512
19. Roghani A, Zannis V. Mutagenesis of the glycosylation site of human ApoCIII. O-linked glycosylation is not required for ApoCIII secretion and lipid binding. Journal of Biological Chemistry. 1988; 263(34):17925-32. PMID: 3192519
20. Millar JS. The sialylation of plasma lipoproteins. Atherosclerosis. 2001; 154(1):1-13. PMID: 11137077
21. Bosello O, Cominacini L, Zocca I, Garbin U, Ferrari F, Davoli A. Effects of severe caloric restriction on the degree of sialylation of apoprotein C-III in obese women. Annals of nutrition and metabolism. 1985; 29(1):33-9. PMID: 3977292
22. Harvey SB, Zhang Y, Wilson-Grady J, Monkkonen T, Nelsestuen GL, Kasthuri RS, et al. O-glycoside biomarker of apolipoprotein C3: responsiveness to obesity, bariatric surgery, and therapy with metformin, to chronic or severe liver disease and to mortality in severe sepsis and graft vs host disease. Journal of proteome research. 2008; 8(2):603-12.
23. Witztum JL, Schonfeld G. Carbohydrate diet-induced changes in very low density lipoprotein composition and structure. Diabetes. 1978; 27(12):1215-29. Epub 1978/12/01. PMID: 214369.
24. Falko JM, Schonfeld G, Witztum JL, Kolar JB, Salmon P. Effects of short-term high carbohydrate, fat-free diet on plasma levels of Apo C-II and Apo C-III and on the Apo C subspecies in human plasma lipoproteins. Metabolism: clinical and experimental. 1980; 29(7):654-61. Epub 1980/07/01. PMID: 7382829.
25. Lindbohm N, Gylling H, Miettinen TE, Miettinen TA. Sialic acid content of LDL and lipoprotein metabolism in combined hyperlipidemia and primary moderate hypercholesterolemia. Clinica Chimica Acta. 1999; 285(1-2):69-84. doi: 10.1016/S0009-8981(99)00107-2
26. Savinova OV, Fillaus K, Jing L, Harris WS, Shearer GC. Reduced Apolipoprotein Glycosylation in Patients with the Metabolic Syndrome. PloS one. 2014; 9(8):e104833. doi: 10.1371/journal.pone.0104833 PMID: 25118169
27. Mann CJ, Troussard AA, Yen FT, Hannouche N, Najib J, Fruchart JC, et al. Inhibitory effects of specific apolipoprotein C-III isoforms on the binding of triglyceride-rich lipoproteins to the lipolysis-stimulated receptor. The Journal of biological chemistry. 1997; 272(50):31348-54. PMID: 9395464.
28. Holleboom AG, Karlsson H, Lin RS, Beres TM, Sierts JA, Herman DS, et al. Heterozygosity for a loss-of-function mutation in GALNT2 improves plasma triglyceride clearance in man. Cell Metab. 2011; 14(6):811-8. Epub 2011/12/14. doi: 10.1016/j.cmet.2011.11.005 PMID: 22152306; PubMed Central PMCID: PMCPMC3523677.
29. Catapano AL. Activation of lipoprotein lipase by apolipoprotein C-II is modulated by the COOH terminal region of apolipoprotein C-III. Chemistry and Physics of Lipids. 1987; 45(1):39-47. doi: 10.1016/0009-3084(87)90038-7 PMID: 3446410
30. Nelson RW, Borges CR. Mass spectrometric immunoassay revisited. J Am Soc Mass Spectrom. 2011; 22(6):960-8. doi: 10.1007/s13361-011-0094-z PMID: 21953037.
31. Nelson RW, Krone JR, Bieber AL, Williams P. Mass spectrometric immunoassay. Anal Chem. 1995; 67(7):1153-8. Epub 1995/04/01. PMID: 15134097.
32. Yassine HN, Trenchevska O, He H, Borges CR, Nedelkov D, Mack W, et al. Serum amyloid a truncations in type 2 diabetes mellitus. PloS one. 2015; 10(1):e0115320. Epub 2015/01/22. doi: 10.1371/journal.pone.0115320 PMID: 25607823.
33. Trenchevska O, Schaab MR, Nelson RW, Nedelkov D. Development of multiplex mass spectrometric immunoassay for detection and quantification of apolipoproteins CI, C- II, C-III and their proteoforms. Methods. 2015.
34. Must A, Anderson S. PEDIATRIC MINI REVIEW Body mass index in children and adolescents: considerations for population-based applications. International journal of obesity. 2006; 30:590-4.
35. Cruz ML, Bergman RN, Goran MI. Unique effect of visceral fat on insulin sensitivity in obese Hispanic children with a family history of type 2 diabetes. Diabetes care. 2002; 25(9):1631-6. PMID: 12196439
36. Harduin-Lepers A, Vallejo-Ruiz V, Krzewinski-Recchi MA, Samyn-Petit B, Julien S, Delannoy P. The human sialyltransferase family. Biochimie. 2001; 83(8):727-37. Epub 2001/09/01. PMID: 11530204.
37. Willer CJ, Sanna S, Jackson AU, Scuteri A, Bonnycastle LL, Clarke R, et al. Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nature genetics. 2008; 40(2):161-9. doi: 10.1038/ng.76 PMID: 18193043
38. Katrine T-BS, Vakhrushev SY, Kong Y, Steentoft C, Nudelman AS, Pedersen NB, et al. Probing isoform-specific functions of polypeptide GalNAc-transferases using zinc finger nuclease glycoengineered SimpleCells. Proceedings of the National Academy of Sciences. 2012; 109(25):9893-8.
39. Marucci A, di Mauro L, Menzaghi C, Prudente S, Mangiacotti D, Fini G, et al. GALNT2 expression is reduced in patients with type 2 diabetes: possible role of hyperglycemia. PloS one. 2013; 8(7):e70159. doi: 10.1371/journal.pone.0070159 PMID: 23894607
40. Savinova OV, Fillaus K, Harris WS, Shearer GC. Effects of niacin and omega-3 fatty acids on the apolipoproteins in overweight patients with elevated triglycerides and reduced HDL cholesterol. Atherosclerosis. 2015; 240(2):520-5. doi: 10.1016/j.atherosclerosis.2015.04.793 PMID: 25932792
41. Holdsworth G, Stocks J, Dodson P, Galton DJ. An abnormal triglyceride-rich lipoprotein containing excess sialylated apolipoprotein C-III. The Journal of clinical investigation. 1982; 69(4):932-9. Epub 1982/04/01. PMID: 7076853; PubMed Central PMCID: PMCPMC370147.
42. Hiukka A, Ståhlman M, Pettersson C, Levin M, Adiels M, Teneberg S, et al. ApoCIII-enriched LDL in type 2 diabetes displays altered lipid composition, increased susceptibility for sphingomyelinase, and increased binding to biglycan. Diabetes. 2009; 58(9):2018-26. doi: 10.2337/db09-0206 PMID: 19502413
43. Wada Y, Azadi P, Costello CE, Dell A, Dwek RA, Geyer H, et al. Comparison of the methods for profiling glycoprotein glycans - HUPO Human Disease Glycomics/Proteome Initiative multi-institutional study. Glycobiology. 2007; 17(4):411-22. PMID: 17223647
44. Bondarenko PV, Cockrill SL, Watkins LK, Cruzado ID, Macfarlane RD. Mass spectral study of polymorphism of the apolipoproteins of very low density lipoprotein. Journal of lipid research. 1999; 40(3):543-55. PMID: 10064743