Network-Based Analysis on Orthogonal Separation of Human Plasma Uncovers Distinct High Density Lipoprotein Complexes

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3082-3094

  Li, Hailong ^a,b   Gordon, Scott M ^c   Zhu, Xiaoting ^b   Deng, Jingyuan ^b   Swertfeger, Debi K ^b   Davidson, W Sean ^c   Lu, L Jason ^b  

^a JIANGHAN UNIVERSITY   (China)

^b CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

apolipoprotein; comigration pattern; high density lipoprotein; human plasma; maximal clique; particle fractionation; protein network; proteomics; subspecies

Indexed keywords

APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD ANALYSIS; BLOOD LEVEL; CARDIOVASCULAR DISEASE; CHROMATOGRAPHY; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FRACTIONATION; GENE INACTIVATION; HUMAN; MOLECULAR WEIGHT; MOUSE; NONHUMAN; ORTHOGONAL CHROMATOGRAPHY; PLASMA; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEPARATION TECHNIQUE; ADULT; ANIMAL; BIOLOGICAL MODEL; BLOOD; ELECTROSPRAY MASS SPECTROMETRY; GENETICS; ION EXCHANGE CHROMATOGRAPHY; ISOELECTRIC FOCUSING; KNOCKOUT MOUSE; MALE; METABOLISM; PARTICLE SIZE; PROCEDURES; PROTEIN ANALYSIS; PROTEOMICS; SIZE EXCLUSION CHROMATOGRAPHY; TANDEM MASS SPECTROMETRY;

ADULT; ANIMALS; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, ION EXCHANGE; FEMALE; HUMANS; ISOELECTRIC FOCUSING; LIPOPROTEINS, HDL; MALE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PARTICLE SIZE; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEOMICS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

EID: 84938816591     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00419     Document Type: Article

References (53)

1. Mahmood, S. S.; Levy, D.; Vasan, R. S.; Wang, T. J. The Framingham Heart Study and the epidemiology of cardiovascular disease: A historical perspective Lancet 2014, 383 (9921) 999-1008
2. Alwan, A. Global Status Report on Noncommunicable Diseases 2010; World Health Organization: Geneva, Switzerland, 2011.
3. Rezaee, F.; Casetta, B.; Levels, J. H.; Speijer, D.; Meijers, J. C. Proteomic analysis of high-density lipoprotein Proteomics 2006, 6 (2) 721-30
4. Vaisar, T.; Pennathur, S.; Green, P. S.; Gharib, S. A.; Hoofnagle, A. N.; Cheung, M. C.; Byun, J.; Vuletic, S.; Kassim, S.; Singh, P.; Chea, H.; Knopp, R. H.; Brunzell, J.; Geary, R.; Chait, A.; Zhao, X. Q.; Elkon, K.; Marcovina, S.; Ridker, P.; Oram, J. F.; Heinecke, J. W. Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL J. Clin. Invest. 2007, 117 (3) 746-56
5. Karlsson, H.; Leanderson, P.; Tagesson, C.; Lindahl, M. Lipoproteomics II: Mapping of proteins in high-density lipoprotein using two-dimensional gel electrophoresis and mass spectrometry Proteomics 2005, 5 (5) 1431-45
6. Heller, M.; Stalder, D.; Schlappritzi, E.; Hayn, G.; Matter, U.; Haeberli, A. Mass spectrometry-based analytical tools for the molecular protein characterization of human plasma lipoproteins Proteomics 2005, 5 (10) 2619-30
7. Davidson, W. S.; Silva, R. A.; Chantepie, S.; Lagor, W. R.; Chapman, M. J.; Kontush, A. Proteomic analysis of defined HDL subpopulations reveals particle-specific protein clusters: Relevance to antioxidative function Arterioscler., Thromb., Vasc. Biol. 2009, 29 (6) 870-6
8. Gordon, S. M.; Deng, J.; Lu, L. J.; Davidson, W. S. Proteomic characterization of human plasma high density lipoprotein fractionated by gel filtration chromatography J. Proteome Res. 2010, 9 (10) 5239-49
9. Gordon, S. M.; Deng, J.; Tomann, A. B.; Shah, A. S.; Lu, L. J.; Davidson, W. S. Multidimensional coseparation analysis reveals protein-protein interactions defining plasma lipoprotein subspecies Mol. Cell Proteomics 2013, 12 (11) 3123-34
10. Riwanto, M.; Rohrer, L.; Roschitzki, B.; Besler, C.; Mocharla, P.; Mueller, M.; Perisa, D.; Heinrich, K.; Altwegg, L.; von Eckardstein, A.; Luscher, T. F.; Landmesser, U. Altered activation of endothelial anti- and proapoptotic pathways by high-density lipoprotein from patients with coronary artery disease: Role of high-density lipoprotein-proteome remodeling Circulation 2013, 127 (8) 891-904
11. Sreckovic, I.; Birner-Gruenberger, R.; Obrist, B.; Stojakovic, T.; Scharnagl, H.; Holzer, M.; Scholler, M.; Philipose, S.; Marsche, G.; Lang, U.; Desoye, G.; Wadsack, C. Distinct composition of human fetal HDL attenuates its antioxidative capacity Biochim. Biophys. Acta 2013, 1831 (4) 737-46
12. Link, J. J.; Rohatgi, A.; de Lemos, J. A. HDL cholesterol: Physiology, pathophysiology, and management Curr. Probl. Cardiol. 2007, 32 (5) 268-314
13. Shah, A. S.; Tan, L.; Long, J. L.; Davidson, W. S. Proteomic diversity of high-density lipoproteins: Our emerging understanding of its importance in lipid transport and beyond J. Lipid Res. 2013, 54 (10) 2575-85
14. Glomset, J. A. The plasma lecithins:cholesterol acyltransferase reaction J. Lipid Res. 1968, 9 (2) 155-67
15. Mackness, M. I.; Arrol, S.; Durrington, P. N. Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein FEBS Lett. 1991, 286 (1-2) 152-4
16. Nofer, J. R.; Assmann, G. Atheroprotective effects of high-density lipoprotein-associated lysosphingolipids Trends Cardiovasc. Med. 2005, 15 (7) 265-71
17. Wadham, C.; Albanese, N.; Roberts, J.; Wang, L.; Bagley, C. J.; Gamble, J. R.; Rye, K. A.; Barter, P. J.; Vadas, M. A.; Xia, P. High-density lipoproteins neutralize C-reactive protein proinflammatory activity Circulation 2004, 109 (17) 2116-22
18. Kulkarni, S.; Woollard, K. J.; Thomas, S.; Oxley, D.; Jackson, S. P. Conversion of platelets from a proaggregatory to a proinflammatory adhesive phenotype: Role of PAF in spatially regulating neutrophil adhesion and spreading Blood 2007, 110 (6) 1879-86
19. Kuvin, J. T.; Harati, N. A.; Pandian, N. G.; Bojar, R. M.; Khabbaz, K. R. Postoperative cardiac tamponade in the modern surgical era Ann. Thorac. Surg. 2002, 74 (4) 1148-53
20. Asztalos, B. F.; Schaefer, E. J. High-density lipoprotein subpopulations in pathologic conditions Am. J. Cardiol. 2003, 91 (7A) 12E-7E
21. Rifkin, M. R. Identification of the trypanocidal factor in normal human serum: High-density lipoprotein Proc. Natl. Acad. Sci. U. S. A. 1978, 75 (7) 3450-4
22. Raper, J.; Fung, R.; Ghiso, J.; Nussenzweig, V.; Tomlinson, S. Characterization of a novel trypanosome lytic factor from human serum Infect. Immun. 1999, 67 (4) 1910-6
23. Sawle, A.; Higgins, M. K.; Olivant, M. P.; Higgins, J. A. A rapid single-step centrifugation method for determination of HDL, LDL, and VLDL cholesterol, and TG, and identification of predominant LDL subclass J. Lipid Res. 2002, 43 (2) 335-43
24. vant Hooft, F.; Havel, R. J. Metabolism of apolipoprotein E in plasma high density lipoproteins from normal and cholesterol-fed rats J. Biol. Chem. 1982, 257 (18) 10996-1001
25. Havugimana, P. C.; Hart, G. T.; Nepusz, T.; Yang, H.; Turinsky, A. L.; Li, Z.; Wang, P. I.; Boutz, D. R.; Fong, V.; Phanse, S.; Babu, M.; Craig, S. A.; Hu, P.; Wan, C.; Vlasblom, J.; Dar, V. U.; Bezginov, A.; Clark, G. W.; Wu, G. C.; Wodak, S. J.; Tillier, E. R.; Paccanaro, A.; Marcotte, E. M.; Emili, A. A census of human soluble protein complexes Cell 2012, 150 (5) 1068-81
26. Spirin, V.; Mirny, L. A. Protein complexes and functional modules in molecular networks Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (21) 12123-8
27. Bader, G. D.; Hogue, C. W. An automated method for finding molecular complexes in large protein interaction networks BMC Bioinf. 2003, 4 (1) 2
28. Lu, L. J.; Xia, Y.; Paccanaro, A.; Yu, H.; Gerstein, M. Assessing the limits of genomic data integration for predicting protein networks Genome Res. 2005, 15 (7) 945-953
29. Lin, C. C.; Juan, H. F.; Hsiang, J. T.; Hwang, Y. C.; Mori, H.; Huang, H. C. Essential core of protein-protein interaction network in Escherichia coli J. Proteome Res. 2009, 8 (4) 1925-31
30. Bron, C.; Kerbosch, J. Finding all cliques of an undirected graph [H] Commun. ACM 1973, 16 (9) 575-7
31. Gordon, S. M.; Hofmann, S.; Askew, D. S.; Davidson, W. S. High-density lipoprotein: Its not just about lipid transport anymore Trends Endocrinol. Metab. 2011, 22 (1) 9-15
32. Eisenberg, S. High density lipoprotein metabolism J. Lipid Res. 1984, 25 (10) 1017-58
33. Prasad, T. K.; Goel, R.; Kandasamy, K.; Keerthikumar, S.; Kumar, S.; Mathivanan, S.; Telikicherla, D.; Raju, R.; Shafreen, B.; Venugopal, A. Human protein reference database-2009 update Nucleic Acids Res. 2009, 37 (Suppl. 1) D767-72
34. Santos, R. D.; Schaefer, E. J.; Asztalos, B. F.; Polisecki, E.; Wang, J.; Hegele, R. A.; Martinez, L. R.; Miname, M. H.; Rochitte, C. E.; Da Luz, P. L.; Maranhao, R. C. Characterization of high density lipoprotein particles in familial apolipoprotein A-I deficiency J. Lipid Res. 2008, 49 (2) 349-57
35. Zhang, M.; Lu, L. J. Investigating the validity of current network analysis on static conglomerate networks by protein network stratification BMC Bioinf. 2010, 11, 466
36. Franceschini, A.; Szklarczyk, D.; Frankild, S.; Kuhn, M.; Simonovic, M.; Roth, A.; Lin, J.; Minguez, P.; Bork, P.; von Mering, C. STRING v9. 1: Protein-protein interaction networks, with increased coverage and integration Nucleic Acids Res. 2013, 41 (D1) D808-15
37. Schamaun, O.; Olaisen, B.; Mevag, B.; Gedde-Dahl, T., Jr.; Ehnholm, C.; Teisberg, P. The two apolipoprotein loci apo A-I and apo A-IV are closely linked in man Hum. Genet. 1984, 68 (2) 181-4
38. Ordovas, J. M.; Schaefer, E. J. Genetic determinants of plasma lipid response to dietary intervention: The role of the APOA1/C3/A4 gene cluster and the APOE gene Br. J. Nutr. 2000, 83 (Suppl. 1) S127-36
39. Puppione, D. L. Higher primates, but not New World monkeys, have a duplicate set of enhancers flanking their apoC-I genes Comp. Biochem. Physiol., Part D: Genomics Proteomics 2014, 11, 45-8
40. Karten, B.; Campenot, R. B.; Vance, D. E.; Vance, J. E. Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia J. Biol. Chem. 2006, 281 (7) 4049-57
41. Monaco, H. L. The transthyretin-retinol-binding protein complex Biochim. Biophys. Acta 2000, 1482 (1-2) 65-72
42. Sousa, M. M.; Berglund, L.; Saraiva, M. J. Transthyretin in high-density lipoproteins: Association with apolipoprotein A-I J. Lipid Res. 2000, 41 (1) 58-65
43. Liz, M. A.; Faro, C. J.; Saraiva, M. J.; Sousa, M. M. Transthyretin, a new cryptic protease J. Biol. Chem. 2004, 279 (20) 21431-8
44. Lee, M.; Kovanen, P. T.; Tedeschi, G.; Oungre, E.; Franceschini, G.; Calabresi, L. Apolipoprotein composition and particle size affect HDL degradation by chymase: Effect on cellular cholesterol efflux J. Lipid Res. 2003, 44 (3) 539-46
45. Liz, M. A.; Gomes, C. M.; Saraiva, M. J.; Sousa, M. M. ApoA-I cleaved by transthyretin has reduced ability to promote cholesterol efflux and increased amyloidogenicity J. Lipid Res. 2007, 48 (11) 2385-95
46. Boucher, J.; Ramsamy, T. A.; Braschi, S.; Sahoo, D.; Neville, T. A.; Sparks, D. L. Apolipoprotein A-II regulates HDL stability and affects hepatic lipase association and activity J. Lipid Res. 2004, 45 (5) 849-58
47. Duverger, N.; Murry-Brelier, A.; Latta, M.; Reboul, S.; Castro, G.; Mayaux, J. F.; Fruchart, J. C.; Taylor, J. M.; Steinmetz, A.; Denefle, P. Functional characterization of human recombinant apolipoprotein AIV produced in Escherichia coli Eur. J. Biochem. 1991, 201 (2) 373-83
48. de Haan, W.; Out, R.; Berbee, J. F.; van der Hoogt, C. C.; van Dijk, K. W.; van Berkel, T. J.; Romijn, J. A.; Jukema, J. W.; Havekes, L. M.; Rensen, P. C. Apolipoprotein CI inhibits scavenger receptor BI and increases plasma HDL levels in vivo Biochem. Biophys. Res. Commun. 2008, 377 (4) 1294-8
49. Gordon, S.; Li, H.; Zhu, X.; Shah, A.; Lu, L. J.; Davidson, W. S. A comparison of the mouse and human lipoproteome: Suitability of the mouse model for studies of human lipoproteins J. Proteome Res. 2015, 14 (6) 2686-95
50. Camus, M. C.; Chapman, M. J.; Forgez, P.; Laplaud, P. M. Distribution and characterization of the serum lipoproteins and apoproteins in the mouse, Mus musculus J. Lipid Res. 1983, 24 (9) 1210-28
51. Al-Sarraf, A.; Al-Ghofaili, K.; Sullivan, D. R.; Wasan, K. M.; Hegele, R.; Frohlich, J. Complete Apo AI deficiency in an Iraqi Mandaean family: Case studies and review of the literature J. Clin. Lipidol. 2010, 4 (5) 420-6
52. Huang, Y.; Wu, Z.; Riwanto, M.; Gao, S.; Levison, B. S.; Gu, X.; Fu, X.; Wagner, M. A.; Besler, C.; Gerstenecker, G.; Zhang, R.; Li, X. M.; DiDonato, A. J.; Gogonea, V.; Tang, W. H.; Smith, J. D.; Plow, E. F.; Fox, P. L.; Shih, D. M.; Lusis, A. J.; Fisher, E. A.; DiDonato, J. A.; Landmesser, U.; Hazen, S. L. Myeloperoxidase, paraoxonase-1, and HDL form a functional ternary complex J. Clin. Invest. 2013, 123 (9) 3815-28
53. Phillips, M. C. New insights into the determination of HDL structure by apolipoproteins: Thematic review series: high density lipoprotein structure, function, and metabolism J. Lipid Res. 2013, 54 (8) 2034-48