Reduced apolipoprotein glycosylation in patients with the metabolic syndrome

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Savinova, Olga V ^a   Fillaus, Kristi ^a   Jing, Linhong ^b   Harris, William S ^c   Shearer, Gregory C ^a,c  

^a SANFORD RESEARCH   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN; HIGH DENSITY LIPOPROTEIN; INTERMEDIATE DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; SAA4 PROTEIN, HUMAN; SERUM AMYLOID A; VERY LOW DENSITY LIPOPROTEIN;

ADULT; BLOOD; CASE CONTROL STUDY; CHEMISTRY; CLASSIFICATION; FEMALE; GLYCOSYLATION; HUMAN; MALE; METABOLIC SYNDROME X; METABOLISM; MIDDLE AGED;

ADULT; APOLIPOPROTEINS; CASE-CONTROL STUDIES; FEMALE; GLYCOSYLATION; HUMANS; LIPOPROTEINS, HDL; LIPOPROTEINS, IDL; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; MALE; METABOLIC SYNDROME X; MIDDLE AGED; SERUM AMYLOID A PROTEIN;

EID: 84905851466     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104833     Document Type: Article

References (66)

1. Ford ES, Giles WH, Mokdad AH (2004) Increasing prevalence of the metabolic syndrome among u.s. Adults. Diabetes Care 27: 2444-2449. (Pubitemid 39281399)
2. Lim S, Shin H, Song JH, Kwak SH, Kang SM, et al. (2011) Increasing prevalence of metabolic syndrome in Korea: the Korean National Health and Nutrition Examination Survey for 1998-2007. Diabetes Care 34: 1323-1328.
3. Mozumdar A, Liguori G (2011) Persistent increase of prevalence of metabolic syndrome among U.S. adults: NHANES III to NHANES 1999-2006. Diabetes Care 34: 216-219.
4. Nestel P, Lyu R, Low LP, Sheu WH, Nitiyanant W, et al. (2007) Metabolic syndrome: recent prevalence in East and Southeast Asian populations. Asia Pac J Clin Nutr 16: 362-367. (Pubitemid 46750768)
5. Beltran-Sanchez H, Harhay MO, Harhay MM, McElligott S (2013) Prevalence and trends of metabolic syndrome in the adult U.S. population, 1999-2010. J Am Coll Cardiol 62: 697-703.
6. Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, et al. (2010) The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol 56: 1113-1132.
7. Galassi A, Reynolds K, He J (2006) Metabolic syndrome and risk of cardiovascular disease: a meta-analysis. Am J Med 119: 812-819. (Pubitemid 44415613)
8. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, et al. (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120: 1640-1645.
9. Mahley RW, Innerarity TL, Rall SC Jr, Weisgraber KH (1984) Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res 25: 1277-1294. (Pubitemid 15150638)
10. Mahley RW, Innerarity TL, Weisgraber KH, Rall SC Jr, Hui DY, et al. (1986) Cellular and molecular biology of lipoprotein metabolism: characterization of lipoprotein receptor-ligand interactions. Cold Spring Harb Symp Quant Biol 51 Pt 2: 821-828. (Pubitemid 17078597)
11. McQueen MJ, Hawken S, Wang X, Ounpuu S, Sniderman A, et al. (2008) Lipids, lipoproteins, and apolipoproteins as risk markers of myocardial infarction in 52 countries (the INTERHEART study): a case-control study. Lancet 372: 224-233. (Pubitemid 351978112)
12. Walldius G, Jungner I, Holme I, Aastveit AH, Kolar W, et al. (2001) High apolipoprotein B, low apolipoprotein A-I, and improvement in the prediction of fatal myocardial infarction (AMORIS study): a prospective study. Lancet 358: 2026-2033. (Pubitemid 34084825)
13. Lee SJ, Campos H, Moye LA, Sacks FM (2003) LDL containing apolipoprotein CIII is an independent risk factor for coronary events in diabetic patients. Arterioscler Thromb Vasc Biol 23: 853-858. (Pubitemid 36566177)
14. Williams K, Sniderman AD, Sattar N, D'Agostino R Jr, Wagenknecht LE, et al. (2003) Comparison of the associations of apolipoprotein B and low-density lipoprotein cholesterol with other cardiovascular risk factors in the Insulin Resistance Atherosclerosis Study (IRAS). Circulation 108: 2312-2316. (Pubitemid 37413535)
15. Corsetti JP, Zareba W, Moss AJ, Sparks CE (2004) Apolipoprotein B determines risk for recurrent coronary events in postinfarction patients with metabolic syndrome. Atherosclerosis 177: 367-373. (Pubitemid 39505270)
16. Onat A, Hergenc G, Sansoy V, Fobker M, Ceyhan K, et al. (2003) Apolipoprotein C-III, a strong discriminant of coronary risk in men and a determinant of the metabolic syndrome in both genders. Atherosclerosis 168: 81-89. (Pubitemid 36555814)
17. Onat A, Can G, Ornek E, Ayhan E, Erginel-Unaltuna N, et al. (2013) High serum apolipoprotein E determines hypertriglyceridemic dyslipidemias, coronary disease and apoA-I dysfunctionality. Lipids 48: 51-61.
18. Vaisar T, Pennathur S, Green PS, Gharib SA, Hoofnagle AN, et al. (2007) Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J Clin Invest 117: 746-756. (Pubitemid 46348533)
19. Davidsson P, Hulthe J, Fagerberg B, Olsson BM, Hallberg C, et al. (2005) A proteomic study of the apolipoproteins in LDL subclasses in patients with the metabolic syndrome and type 2 diabetes. J Lipid Res 46: 1999-2006. (Pubitemid 41248497)
20. Rabbani N, Chittari MV, Bodmer CW, Zehnder D, Ceriello A, et al. (2010) Increased glycation and oxidative damage to apolipoprotein B100 of LDL cholesterol in patients with type 2 diabetes and effect of metformin. Diabetes 59: 1038-1045.
21. Halim A, Ruetschi U, Larson G, Nilsson J (2013) LC-MS/MS characterization of O-glycosylation sites and glycan structures of human cerebrospinal fluid glycoproteins. J Proteome Res 12: 573-584.
22. Lee Y, Kockx M, Raftery MJ, Jessup W, Griffith R, et al. (2010) Glycosylation and sialylation of macrophage-derived human apolipoprotein E analyzed by SDS-PAGE and mass spectrometry: evidence for a novel site of glycosylation on Ser290. Mol Cell Proteomics 9: 1968-1981.
23. Wernette-Hammond ME, Lauer SJ, Corsini A, Walker D, Taylor JM, et al. (1989) Glycosylation of human apolipoprotein E. The carbohydrate attachment site is threonine 194. J Biol Chem 264: 9094-9101. (Pubitemid 19151641)
24. Nilsson J, Ruetschi U, Halim A, Hesse C, Carlsohn E, et al. (2009) Enrichment of glycopeptides for glycan structure and attachment site identification. Nat Methods 6: 809-811.
25. Schjoldager KT, Vakhrushev SY, Kong Y, Steentoft C, Nudelman AS, et al. (2012) Probing isoform-specific functions of polypeptide GalNAc-transferases using zinc finger nuclease glycoengineered SimpleCells. Proc Natl Acad Sci U S A 109: 9893-9898.
26. Steentoft C, Vakhrushev SY, Vester-Christensen MB, Schjoldager KT, Kong Y, et al. (2011) Mining the O-glycoproteome using zinc-finger nuclease-glycoengineered SimpleCell lines. Nat Methods 8: 977-982.
27. Millar JS (2001) The sialylation of plasma lipoproteins. Atherosclerosis 154: 1-13.
28. Kockx M, Dinnes DL, Huang KY, Sharpe LJ, Jessup W, et al. (2012) Cholesterol accumulation inhibits ER to Golgi transport and protein secretion: studies of apolipoprotein E and VSVGt. Biochem J 447: 51-60.
29. de Beer MC, Yuan T, Kindy MS, Asztalos BF, Roheim PS, et al. (1995) Characterization of constitutive human serum amyloid A protein (SAA4) as an apolipoprotein. J Lipid Res 36: 526-534.
30. Whitehead AS, de Beer MC, Steel DM, Rits M, Lelias JM, et al. (1992) Identification of novel members of the serum amyloid A protein superfamily as constitutive apolipoproteins of high density lipoprotein. J Biol Chem 267: 3862-3867.
31. Tertov VV, Sobenin IA, Tonevitsky AG, Orekhov AN, Smirnov VN (1990) Isolation of atherogenic modified (desialylated) low density lipoprotein from blood of atherosclerotic patients: separation from native lipoprotein by affinity chromatography. Biochem Biophys Res Commun 167: 1122-1127. (Pubitemid 20113297)
32. Orekhov AN, Tertov VV, Mukhin DN, Mikhailenko IA (1989) Modification of low density lipoprotein by desialylation causes lipid accumulation in cultured cells: discovery of desialylated lipoprotein with altered cellular metabolism in the blood of atherosclerotic patients. Biochem Biophys Res Commun 162: 206-211. (Pubitemid 19185847)
33. Tertov VV, Orekhov AN, Sobenin IA, Morrisett JD, Gotto AM Jr, et al. (1993) Carbohydrate composition of protein and lipid components in sialic acid-rich and -poor low density lipoproteins from subjects with and without coronary artery disease. J Lipid Res 34: 365-375. (Pubitemid 23095364)
34. Millar JS, Anber V, Shepherd J, Packard CJ (1999) Sialic acid-containing components of lipoproteins influence lipoprotein-proteoglycan interactions. Atherosclerosis 145: 253-260. (Pubitemid 29359131)
35. Atkinson KR, Blumenstein M, Black MA, Wu SH, Kasabov N, et al. (2009) An altered pattern of circulating apolipoprotein E3 isoforms is implicated in preeclampsia. J Lipid Res 50: 71-80.
36. Atger V, Beyne P, Frommherz K, Roullet JB, Drueke T (1989) Presence of Apo B48, and relative Apo CII deficiency and Apo CIII enrichment in uremic very-low density lipoproteins. Ann Biol Clin (Paris) 47: 497-501. (Pubitemid 19277136)
37. Harake B, Caines PS, Thibert RJ, Cheung RM (1991) A simple micromethod for rapid assessment of the distribution of apolipoprotein C isoforms in very-lowdensity lipoprotein. Clin Biochem 24: 255-260.
38. Harvey SB, Zhang Y, Wilson-Grady J, Monkkonen T, Nelsestuen GL, et al. (2009) 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. J Proteome Res 8: 603-612.
39. Schumaker VN, Puppione DL (1986) Sequential flotation ultracentrifugation. Methods Enzymol 128: 155-170. (Pubitemid 16100890)
40. Shearer GC, Newman JW, Hammock BD, Kaysen GA (2005) Graded effects of proteinuria on HDL structure in nephrotic rats. J Am Soc Nephrol 16: 1309-1319. (Pubitemid 41716515)
41. Sun HY, Chen SF, Lai MD, Chang TT, Chen TL, et al. (2010) Comparative proteomic profiling of plasma very-low-density and low-density lipoproteins. Clin Chim Acta 411: 336-344.
42. Stahlman M, Davidsson P, Kanmert I, Rosengren B, Boren J, et al. (2008) Proteomics and lipids of lipoproteins isolated at low salt concentrations in D2O/sucrose or in KBr. J Lipid Res 49: 481-490. (Pubitemid 351213633)
43. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76: 4350-4354. (Pubitemid 9256559)
44. Hochberg Y, Benjamini Y (1990) More powerful procedures for multiple significance testing. Stat Med 9: 811-818. (Pubitemid 20343989)
45. Pitsavos C, Panagiotakos DB, Skoumas J, Papadimitriou L, Stefanadis C (2008) Risk stratification of apolipoprotein B, apolipoprotein A1, and apolipoprotein B/AI ratio on the prevalence of the metabolic syndrome: the ATTICA study. Angiology 59: 335-341. (Pubitemid 351793161)
46. Sierra-Johnson J, Somers VK, Kuniyoshi FH, Garza CA, Isley WL, et al. (2006) Comparison of apolipoprotein-B/apolipoprotein-AI in subjects with versus without the metabolic syndrome. Am J Cardiol 98: 1369-1373. (Pubitemid 44666643)
47. Brunzell JD, Ayyobi AF (2003) Dyslipidemia in the metabolic syndrome and type 2 diabetes mellitus. Am J Med 115 Suppl 8A: 24S-28S.
48. Adiels M, Olofsson SO, Taskinen MR, Boren J (2008) Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol 28: 1225-1236.
49. Chan DC, Ng TW, Watts GF (2012) Apolipoprotein A-II: evaluating its significance in dyslipidaemia, insulin resistance, and atherosclerosis. Ann Med 44: 313-324.
50. Tailleux A, Duriez P, Fruchart JC, Clavey V (2002) Apolipoprotein A-II, HDL metabolism and atherosclerosis. Atherosclerosis 164: 1-13. (Pubitemid 34765632)
51. Huff MW, Strong WL (1987) Separation and isolation of human apolipoproteins C-II, C-III0, C-III1, and C-III2 by chromatofocusing on the Fast Protein Liquid Chromatography system. J Lipid Res 28: 1118-1123. (Pubitemid 17124415)
52. Maeda H, Hashimoto RK, Ogura T, Hiraga S, Uzawa H (1987) Molecular cloning of a human apoC-III variant: Thr 74 - Ala 74 mutation prevents O-glycosylation. J Lipid Res 28: 1405-1409. (Pubitemid 18025874)
53. Roghani A, Zannis VI (1988) Mutagenesis of the glycosylation site of human ApoCIII. O-linked glycosylation is not required for ApoCIII secretion and lipid binding. J Biol Chem 263: 17925-17932. (Pubitemid 19005067)
54. Zanni EE, Kouvatsi A, Hadzopoulou-Cladaras M, Krieger M, Zannis VI (1989) Expression of ApoE gene in Chinese hamster cells with a reversible defect in O-glycosylation. Glycosylation is not required for apoE secretion. J Biol Chem 264: 9137-9140. (Pubitemid 19157543)
55. Yamada T, Wada A, Yamaguchi T, Itoh Y, Kawai T (1997) Automated measurement of a constitutive isotype of serum amyloid A/SAA4 and comparison with other apolipoproteins. J Clin Lab Anal 11: 363-368. (Pubitemid 27513671)
56. Yamada T, Miyake N, Itoh K, Igari J (2001) Further characterization of serum amyloid A4 as a minor acute phase reactant and a possible nutritional marker. Clin Chem Lab Med 39: 7-10. (Pubitemid 32186271)
57. Hiukka A, Stahlman M, Pettersson C, Levin M, Adiels M, et al. (2009) ApoCIII-enriched LDL in type 2 diabetes displays altered lipid composition, increased susceptibility for sphingomyelinase, and increased binding to biglycan. Diabetes 58: 2018-2026.
58. Willer CJ, Sanna S, Jackson AU, Scuteri A, Bonnycastle LL, et al. (2008) Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat Genet 40: 161-169. (Pubitemid 351171403)
59. Kathiresan S, Melander O, Guiducci C, Surti A, Burtt NP, et al. (2008) Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat Genet 40: 189-197. (Pubitemid 351171402)
60. Schjoldager KT, Vester-Christensen MB, Bennett EP, Levery SB, Schwientek T, et al. (2010) O-Glycosylation Modulates Proprotein Convertase Activation of Angiopoietin-like Protein 3: Possible Role of Polypeptide Galnac-Transferase-2 In Regulation of Concentrations of Plasma Lipids. J Biol Chem 285: 36293-36303.
61. D'Avila F, Tringali C, Papini N, Anastasia L, Croci G, et al. (2013) Identification of lysosomal sialidase NEU1 and plasma membrane sialidase NEU3 in human erythrocytes. J Cell Biochem 114: 204-211.
62. Tertov VV, Kaplun VV, Sobenin IA, Boytsova EY, Bovin NV, et al. (2001) Human plasma trans-sialidase causes atherogenic modification of low density lipoprotein. Atherosclerosis 159: 103-115. (Pubitemid 33016627)
63. Anber V, Millar JS, McConnell M, Shepherd J, Packard CJ (1997) Interaction of very-low-density, intermediate-density, and low-density lipoproteins with human arterial wall proteoglycans. Arterioscler Thromb Vasc Biol 17: 2507-2514. (Pubitemid 28015987)
64. Shearer GC, Pottala JV, Hansen SN, Brandenburg V, Harris WS (2012) Effects of prescription niacin and omega-3 fatty acids on lipids and vascular function in metabolic syndrome: a randomized controlled trial. J Lipid Res.
65. Borja MS, Zhao L, Hammerson B, Tang C, Yang R, et al. (2013) HDL-apoA-I exchange: rapid detection and association with atherosclerosis. PLoS One 8: e71541.
66. Bantscheff M, Lemeer S, Savitski MM, Kuster B (2012) Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal Bioanal Chem 404: 939-965.