Proteomic analysis of HDL from inbred mouse strains implicates APOE associated with HDL in reduced cholesterol efflux capacity via the ABCA1 pathway

Journal of Lipid Research

Volumn 57, Issue 2, 2016, Pages 246-257

  Pamir, Nathalie ^a   Hutchins, Patrick ^a   Ronsein, Graziella ^a   Vaisar, Tomas ^a   Reardon, Catherine A ^b   Getz, Godfrey S ^b   Lusis, Aldons J ^c   Heinecke, Jay W ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apolipoprotein E; Atherosclerosis; Atp binding cassette transporter a1; Cardiovascular risk; High density lipoprotein; Mass spectrometry

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN A1; APOLIPOPROTEIN C3; APOLIPOPROTEIN D; APOLIPOPROTEIN E; AQUAPORIN 4; COMPLEMENT COMPONENT C3; HIGH DENSITY LIPOPROTEIN; RETINOL BINDING PROTEIN 4; SERINE PROTEINASE INHIBITOR; SERUM AMYLOID A; ABCA1 PROTEIN, MOUSE; CHOLESTEROL;

ANIMAL EXPERIMENT; ARTICLE; CARDIOVASCULAR DISEASE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; INBRED MOUSE STRAIN; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MACROPHAGE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; ULTRACENTRIFUGATION; ANIMAL; ATHEROSCLEROSIS; BIOSYNTHESIS; CELL LINE; GENETICS; HUMAN; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; ATP BINDING CASSETTE TRANSPORTER 1; CELL LINE; CHOLESTEROL; HUMANS; LIPID METABOLISM; LIPOPROTEINS, HDL; MACROPHAGES; MICE; MICE, INBRED STRAINS; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84964370968     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M063701     Document Type: Article

References (56)

1. Gordon , D. J. , J. L. Probstfield , R. J. Garrison , J. D. Neaton , W. P. Castelli , J. D. Knoke , D. R. Jacobs , S. Bangdiwala , and H. A. Tyroler . 1989 . High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies. Circulation . 79 : 8 - 15 .
2. Heinecke , J. W. 2012 . The not-so-simple HDL story: a new era for quantifying HDL and cardiovascular risk? Nat. Med. 18 : 1346 - 1347 .
3. Kingwell , B. A. , M. J. Chapman , A. Kontush , and N. E. Miller . 2014 . HDL-targeted therapies: progress, failures and future. Nat. Rev. Drug Discov. 13 : 445 - 464 .
4. Rader , D. J. , E. T. Alexander , G. L. Weibel , J. Billheimer , and G. H. Rothblat . 2009 . The role of reverse cholesterol transport in animals and humans and relationship to atherosclerosis. J. Lipid Res. 50 ( Suppl ): S189 - S194 .
5. Yvan-Charvet , L. , N. Wang , and A. R. Tall . 2010 . Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 30 : 139 - 143 .
6. Oram , J. F. , and J. W. Heinecke . 2005 . ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol. Rev. 85 : 1343 - 1372 .
7. Du , X-M. , M-J. Kim , L. Hou , W. Le Goff , M. J. Chapman , M. Van Eck , L. K. Curtiss , J. R. Burnett , S. P. Cartland , C. M. Quinn , et al . 2015 . HDL particle size is a critical determinant of ABCA1-mediated macrophage cellular cholesterol export. Circ. Res. 116 : 1133 - 1142 .
8. Ferrans , V. J. , and D. S. Fredrickson . 1975 . The pathology of Tangier disease. A light and electron microscopic study. Am. J. Pathol. 78 : 101 - 158 .
9. Lawn , R. M. , D. P. Wade , M. R. Garvin , X. Wang , K. Schwartz , J. G. Porter , J. J. Seilhamer , A. M. Vaughan , and J. F. Oram . 1999 . The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J. Clin. Invest. 104 : R25 - R31 .
10. de la Llera-Moya , M. , D. Drazul-Schrader , B. F. Asztalos , M. Cuchel , D. J. Rader , and G. H. Rothblat . 2010 . The ability to promote efflux via ABCA1 determines the capacity of serum specimens with similar high-density lipoprotein cholesterol to remove cholesterol from macrophages. Arterioscler. Thromb. Vasc. Biol. 30 : 796 - 801 .
11. Khera , A. V. , M. Cuchel , M. de la Llera-Moya , A. Rodrigues , M. F. Burke , K. Jafri , B. C. French , J. A. Phillips , M. L. Mucksavage , R. L. Wilensky , et al . 2011 . Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N. Engl. J. Med. 364 : 127 - 135 .
12. Sankaranarayanan , S. , G. Kellner-Weibel , M. de la Llera-Moya , M. C. Phillips , B. F. Asztalos , R. Bittman , and G. H. Rothblat . 2011 . A sensitive assay for ABCA1-mediated cholesterol efflux using BODIPY-cholesterol. J. Lipid Res. 52 : 2332 - 2340 .
13. Rohatgi , A. , A. Khera , J. D. Berry , E. G. Givens , C. R. Ayers , K. E. Wedin , I. J. Neeland , I. S. Yuhanna , D. R. Rader , J. A. de Lemos , et al . 2014 . HDL cholesterol efflux capacity and incident cardiovascular events. N. Engl. J. Med. 371 : 2383 - 2393 .
14. Saleheen , D. , R. Scott , S. Javad , W. Zhao , A. Rodrigues , A. Picataggi , D. Lukmanova , M. L. Mucksavage , R. Luben , J. Billheimer , et al . 2015 . Association of HDL cholesterol efflux capacity with incident coronary heart disease events: a prospective case-control study. Lancet Diabetes Endocrinol. 3 : 507 - 513 .
15. Vaisar , T. , S. Pennathur , P. S. Green , S. A. Gharib , A. N. Hoofnagle , M. C. Cheung , J. Byun , S. Vuletic , S. Kassim , P. Singh , et al . 2007 . Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J. Clin. Invest. 117 : 746 - 756 .
16. Shah , A. S. , L. Tan , J. L. Long , and W. S. Davidson . 2013 . Proteomic diversity of high density lipoproteins: our emerging understanding of its importance in lipid transport and beyond. J. Lipid Res. 54 : 2575 - 2585 .
17. Davidson , W. S. , R. A. G. D. Silva , S. Chantepie , W. R. Lagor , M. J. Chapman , and A. Kontush . 2009 . Proteomic analysis of defined HDL subpopulations reveals particle-specific protein clusters: relevance to antioxidative function. Arterioscler. Thromb. Vasc. Biol. 29 : 870 - 876 .
18. Cheung , M. C. , T. Vaisar , X. Han , J. W. Heinecke , and J. J. Albers . 2010 . Phospholipid transfer protein in human plasma associates with proteins linked to immunity and inflammation. Biochemistry . 49 : 7314 - 7322 .
19. Mu , J. L. , J. K. Naggert , K. L. Svenson , G. B. Collin , J. H. Kim , C. McFarland , P. M. Nishina , D. M. Levine , K. J. Williams , and B. Paigen . 1999 . Quantitative trait loci analysis for the differences in susceptibility to atherosclerosis and diabetes between inbred mouse strains C57BL/6J and C57BLKS/J. J. Lipid Res. 40 : 1328 - 1335 .
20. Shao , B. , X. Fu , T. O. McDonald , P. S. Green , K. Uchida , K. D. O'Brien , J. F. Oram , and J. W. Heinecke . 2005 . Acrolein impairs ATP binding cassette transporter A1-dependent cholesterol export from cells through site-specific modification of apolipoprotein A-I. J. Biol. Chem. 280 : 36386 - 36396 .
21. Green , P. S. , T. Vaisar , S. Pennathur , J. J. Kulstad , A. B. Moore , S. Marcovina , J. Brunzell , R. H. Knopp , X-Q. Zhao , and J. W. Heinecke . 2008 . Combined statin and niacin therapy remodels the high-density lipoprotein proteome. Circulation . 118 : 1259 - 1267 .
22. Keller , A. , A. I. Nesvizhskii , E. Kolker , and R. Aebersold . 2002 . Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74 : 5383 - 5392 .
23. Nesvizhskii , A. I. , A. Keller , E. Kolker , and R. Aebersold . 2003 . A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75 : 4646 - 4658 .
24. Wain , H. M. , E. A. Bruford , R. C. Lovering , M. J. Lush , M. W. Wright , and S. Povey . 2002 . Guidelines for human gene nomenclature. Genomics . 79 : 464 - 470 .
25. Davisson , M. T. 1994 . Rules and guidelines for nomenclature of mouse genes. International Committee on Standardized Genetic Nomenclature for Mice. Gene . 147 : 157 - 160 .
26. Rappsilber , J. , and M. Mann . 2002 . What does it mean to identify a protein in proteomics? Trends Biochem. Sci. 27 : 74 - 78 .
27. Liu , H. , R. G. Sadygov , and J. R. Yates . 2004 . A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76 : 4193 - 4201 .
28. Fu , X. , S. A. Gharib , P. S. Green , M. L. Aitken , D. A. Frazer , D. R. Park , T. Vaisar , and J. W. Heinecke . 2008 . Spectral index for assessment of differential protein expression in shotgun proteomics. J. Proteome Res. 7 : 845 - 854 .
29. Hutchins , P. M. , G. E. Ronsein , J. S. Monette , N. Pamir , J. Wimberger , Y. He , G. M. Anantharamaiah , D. S. Kim , J. E. Ranchalis , G. P. Jarvik , et al . 2014 . Quantification of HDL particle concentration by calibrated ion mobility analysis. Clin. Chem. 60 : 1393 - 1401 .
30. Rosenson , R. S. , H. B. Brewer , M. J. Chapman , S. Fazio , M. M. Hussain , A. Kontush , R. M. Krauss , J. D. Otvos , A. T. Remaley , and E. J. Schaefer . 2011 . HDL measures, particle heterogeneity, proposed nomenclature, and relation to atherosclerotic cardiovascular events. Clin. Chem. 57 : 392 - 410 .
31. LeBoeuf , R. C. , D. L. Puppione , V. N. Schumaker , and A. J. Lusis . 1983 . Genetic control of lipid transport in mice. I. Structural properties and polymorphisms of plasma lipoproteins. J. Biol. Chem. 258 : 5063 - 5070 .
32. Lusis , A. J. , B. A. Taylor , R. W. Wangenstein , and R. C. LeBoeuf . 1983 . Genetic control of lipid transport in mice. II. Genes controlling structure of high density lipoproteins. J. Biol. Chem. 258 : 5071 - 5078 .
33. Frazer , K. A. , E. Eskin , H. M. Kang , M. A. Bogue , D. A. Hinds , E. J. Beilharz , R. V. Gupta , J. Montgomery , M. M. Morenzoni , G. B. Nilsen , et al . 2007 . A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature . 448 : 1050 - 1053 .
34. Vaisar , T. , C. Tang , I. Babenko , P. Hutchins , J. Wimberger , A. F. Suffredini , and J. W. Heinecke . 2015 . Inflammatory remodeling of the HDL proteome impairs cholesterol efflux capacity. J. Lipid Res. 56 : 1519 - 1530 .
35. Gordon , S. M. , J. Deng , L. J. Lu , and W. S. Davidson . 2010 . Proteomic characterization of human plasma high density lipoprotein fractionated by gel filtration chromatography. J. Proteome Res. 9 : 5239 - 5249 .
36. Gordon , S. M. , H. Li , X. Zhu , A. S. Shah , L. J. Lu , and W. S. Davidson . 2015 . A comparison of the mouse and human lipoproteome: suitability of the mouse model for studies of human lipoproteins. J. Proteome Res. 14 : 2686 - 2695 .
37. Weng , W. , and J. L. Breslow . 1996 . Dramatically decreased high density lipoprotein cholesterol, increased remnant clearance, and insulin hypersensitivity in apolipoprotein A-II knockout mice suggest a complex role for apolipoprotein A-II in atherosclerosis susceptibility. Proc. Natl. Acad. Sci. USA . 93 : 14788 - 14794 .
38. Rader , D. J. , and G. K. Hovingh . 2014 . HDL and cardiovascular disease. Lancet . 384 : 618 - 625 .
39. Linton , M. F. , J. B. Atkinson , and S. Fazio . 1995 . Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science . 267 : 1034 - 1037 .
40. Doolittle , M. H. , R. C. LeBoeuf , C. H. Warden , L. M. Bee , and A. J. Lusis . 1990 . A polymorphism affecting apolipoprotein A-II translational efficiency determines high density lipoprotein size and composition. J. Biol. Chem. 265 : 16380 - 16388 .
41. Hedrick , C. C. , L. W. Castellani , H. Wong , and A. J. Lusis . 2001 . In vivo interactions of apoA-II, apoA-I, and hepatic lipase contributing to HDL structure and antiatherogenic functions. J. Lipid Res. 42 : 563 - 570 .
42. Sontag , T. J. , P. A. Krishack , J. R. Lukens , C. V. Bhanvadia , G. S. Getz , and C. A. Reardon . 2014 . Apolipoprotein A-I protection against atherosclerosis is dependent on genetic background. Arterioscler. Thromb. Vasc. Biol. 34 : 262 - 269 .
43. Warden , C. H. , C. C. Hedrick , J. H. Qiao , L. W. Castellani , and A. J. Lusis . 1993 . Atherosclerosis in transgenic mice overexpressing apolipoprotein A-II. Science . 261 : 469 - 472 .
44. Heinecke , J. W. 2015 . Small HDL promotes cholesterol efflux by the ABCA1 pathway in macrophages: implications for therapies targeted to HDL. Circ. Res. 116 : 1101 - 1103 .
45. Ridker , P. M. , N. Rifai , M. A. Pfeffer , F. M. Sacks , L. A. Moye , S. Goldman , G. C. Flaker , and E. Braunwald . 1998 . Inflammation, pravastatin, and the risk of coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events (CARE) Investigators. Circulation . 98 : 839 - 844 .
46. Huang , Z. H. , C. Y. Lin , J. F. Oram , and T. Mazzone . 2001 . Sterol efflux mediated by endogenous macrophage ApoE expression is independent of ABCA1. Arterioscler. Thromb. Vasc. Biol. 21 : 2019 - 2025 .
47. Von Eckardstein , A. , C. Langer , T. Engel , I. Schaukal , A. Cignarella , J. Reinhardt , S. Lorkowski , Z. Li , X. Zhou , P. Cullen , et al . 2001 . ATP binding cassette transporter ABCA1 modulates the secretion of apolipoprotein E from human monocyte-derived macrophages. FASEB J. 15 : 1555 - 1561 .
48. Remaley , A. T. , J. A. Stonik , S. J. Demosky , E. B. Neufeld , A. V. Bocharov , T. G. Vishnyakova , T. L. Eggerman , A. P. Patterson , N. J. Duverger , S. Santamarina-Fojo , et al . 2001 . Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem. Biophys. Res. Commun. 280 : 818 - 823 .
49. Remaley , A. T. , U. K. Schumacher , J. A. Stonik , B. D. Farsi , H. Nazih , and H. B. Brewer . 1997 . Decreased reverse cholesterol transport from Tangier disease fibroblasts. Acceptor specificity and effect of brefeldin on lipid efflux. Arterioscler. Thromb. Vasc. Biol. 17 : 1813 - 1821 .
50. Murphy , A. J. , M. Akhtari , S. Tolani , T. Pagler , N. Bijl , C-L. Kuo , M. Wang , M. Sanson , S. Abramowicz , C. Welch , et al . 2011 . ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J. Clin. Invest. 121 : 4138 - 4149 .
51. Sacks , F. M. , P. Alaupovic , L. A. Moye , T. G. Cole , B. Sussex , M. J. Stampfer , M. A. Pfeffer , and E. Braunwald . 2000 . VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation . 102 : 1886 - 1892 .
52. Mahley , R. W. , Y. Huang , and K. H. Weisgraber . 2006 . Putting cholesterol in its place: apoE and reverse cholesterol transport. J. Clin. Invest. 116 : 1226 - 1229 .
53. Yvan-Charvet , L. , M. Ranalletta , N. Wang , S. Han , N. Terasaka , R. Li , C. Welch , and A. R. Tall . 2007 . Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J. Clin. Invest. 117 : 3900 - 3908 .
54. Lee-Rueckert , M. 2006 . Absence of endogenous phospholipid transfer protein impairs ABCA1-dependent efflux of cholesterol from macrophage foam cells. J. Lipid Res. 47 : 1725 - 1732 .
55. Lagor , W. R. , and D. J. Rader . 2011 . Phospholipidation of HDL-how much is too much? Clin. Chem. 57 : 4 - 6 .
56. Yang , Q. , T. E. Graham , N. Mody , F. Preitner , O. D. Peroni , J. M. Zabolotny , K. Kotani , L. Quadro , and B. B. Kahn . 2005 . Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature . 436 : 356 - 362 .