Mapping oxidations of apolipoprotein B-100 in human low-density lipoprotein by liquid chromatography-tandem mass spectrometry

Analytical Biochemistry

Volumn 404, Issue 2, 2010, Pages 109-117

  Chakraborty, Sourav ^a   Cai, Yang ^a,b   Tarr, Matthew A ^a  

^a UNIVERSITY OF NEW ORLEANS   (United States)

^b CHILDREN S HOSPITAL   (United States)

Author keywords

Hydroxyl radical; LC MS MS; LDL; Natural variants; Oxidative mapping

Indexed keywords

AMINO ACIDS; BIOINFORMATICS; DISEASES; FREE RADICALS; LIPOPROTEINS; LIQUID CHROMATOGRAPHY; MAPPING; MASS SPECTROMETRY; PEPTIDES; SEARCH ENGINES;

ATHEROSCLEROTIC LESIONS; ELEVATED CONCENTRATIONS; HYDROXYL RADICALS; LC-MS/MS; LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY (LC MS/MS); LIQUID CHROMATOGRAPHY-TANDEM MASS SPECTROMETRY; LOW DENSITY LIPOPROTEINS; NATURAL VARIANTS;

OXIDATION;

APOLIPOPROTEIN B100; HYDROXYL RADICAL; LYSINE; PHENYLALANINE; PROLINE; TRYPTOPHAN; TYROSINE; AMINO ACID; LOW DENSITY LIPOPROTEIN; PEPTIDE; TRYPSIN;

ALGORITHM; AQUEOUS SOLUTION; ARTICLE; HUMAN; LIPID ANALYSIS; LIPID BILAYER; LIPID OXIDATION; LIPOPROTEIN METABOLISM; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN CONFORMATION; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CHEMISTRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PEPTIDE MAPPING; PROCEDURES;

AMINO ACID SEQUENCE; AMINO ACIDS; APOLIPOPROTEIN B-100; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HUMANS; HYDROXYL RADICAL; LIPOPROTEINS, LDL; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PEPTIDE MAPPING; PEPTIDES; TANDEM MASS SPECTROMETRY; TRYPSIN;

EID: 77954455981     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2010.05.005     Document Type: Article

References (67)

1. Available from UniProt Knowlegebase (entry name APOB_HUMAN): http://srs.ebi.ac.uk/srsbin/cgi-bin/wgetz?-e.
2. Goldstein J.L., Brown M.S., Anderson R.G.W., Russell D.W., Schneider W.J. Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1985, 1:1-39.
3. Steinberg D., Parthasarathy S., Carew T.E., Khoo J.C., Witztum J.L. Low-density lipoprotein and atherogenesis. N. Engl. J. Med. 1989, 321:1196-1197.
4. Heinecke J.W. Mechanisms of oxidative damage of low density lipoprotein in human atherosclerosis. Curr. Opin. Lipidol. 1997, 8:268-274.
5. Heinecke J.W. Oxidized amino acids: culprits in human atherosclerosis and indicators of oxidative stress. Free Radic. Biol. Med. 2002, 32:1090-1101.
6. Itabe H. Oxidized low-density lipoproteins: what is understood and what remains to be clarified. Biol. Pharm. Bull. 2003, 26:1-9.
7. Stocker R., Keaney J.F. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 2004, 84:1381-1478.
8. Navab M., Ananthramaiah G.M., Reddy S.T., Van Lenten B.J., Ansell B., Fonarow G.C., Vahabzadeh K., Hama S., Hough G., Kamranpour N., Berliner J.A., Lusis A., Fogelman A.M. The oxidation hypothesis of atherogenesis: the role of oxidized phospholipids and HDL. J. Lipid Res. 2004, 45:993-1007.
9. Olsson U., Camejo G., Hurt-Camejo E., Elfsber K., Wiklund O., Bondjers G. Possible functional interactions of apolipoprotein B-100 segments that associate with cell proteoglycans and the apoB/E receptor. Arterioscler. Thromb. Vasc. Biol. 1997, 17:149-155.
10. Lundstam U., Hurt-Camejo E., Olsson G., Sartipy P., Camejo G., Wiklund O. Proteoglycans contribution to association of Lp(a) and LDL with smooth muscle cell extracellular matrix. Arterioscler. Thromb. Vasc. Biol. 1999, 19:1162-1167.
11. Halliwell B. Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 1991, 91:14S-22S.
12. Darley-Usmar V., Halliwell B. Blood radicals: reactive nitrogen species, reactive oxygen species, transition metal ions, and the vascular system. Pharm. Res. 1996, 13:649-662.
13. Fu S., Davies M.J., Stocker R., Dean R.T. Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque. Biochem. J. 1998, 333:519-525.
14. Stadtman E.R., Berlett B.S. Fenton chemistry: amino acid oxidation. J. Biol. Chem. 1991, 266:17201-17211.
15. Stadtman E.R., Levine R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 2003, 25:207-218.
16. Witztum J.L., Steinberg D. The oxidative modification hypothesis of atherosclerosis: does it hold for humans?. Trends Cardiovasc. Med. 2001, 11:93-102.
17. Segrest J.P., Jones M.K., De Loof H., Dashti N. Structure of apolipoprotein B-100 in low density lipoproteins. J. Lipid Res. 2001, 42:1346-1367.
18. Kriško A., Etchebest C. Theoretical model of human apolipoprotein B100 tertiary structure. Proteins: Struct. Funct. Bioinform. 2007, 66:342-358.
19. Esterbauer H., Gebicki J., Puhl H., Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic. Biol. Med. 1992, 13:341-390.
20. Gieseg S.P., Esterbauer H. Low density lipoprotein is saturable by pro-oxidant copper. FEBS Lett. 1994, 343:188-194.
21. Dean R.T., Fu S., Stocker R., Davies M.J. Biochemistry and pathology of radical-mediated protein oxidation. Biochem. J. 1997, 324:1-18.
22. Obama T., Kato R., Masuda Y., Takahashi K., Aiuchi T., Itabe H. Analysis of modified apolipoprotein B-100 structures formed in oxidized low-density lipoprotein using LC-MS/MS. Proteomics 2007, 7:2132-2141.
23. Pietzsch J. Measurement of 5-hydroxy-2-aminovaleric acid as a specific marker of iron-mediated oxidation of proline and arginine side-chain residues of low-density lipoprotein apolipoprotein B-100. Biochem. Biophys. Res. Commun. 2000, 270:852-857.
24. Pietzsch J., Bergmann R. Analysis of 6-hydroxy-2-aminocaproic acid (HACA) as a specific marker of protein oxidation: The use of N(O,S)-ethoxycarbonyl trifluoroethyl ester derivatives and gas chromatography/mass spectrometry. Amino Acids 2004, 26:45-51.
25. Uchida K., Toyokuni S., Nishikawa K., Kawakishi S., Oda H., Hiai H., Stadtman E.R. Michael addition-type 4-hydroxy-2-nonenal adducts in modified low-density lipoproteins: markers for atherosclerosis. Biochemistry (Mosc.) 1994, 33:12487-12494.
26. Uchida K., Kanematsu M., Morimitsu Y., Osawa T., Noguchi N., Niki E. Acrolein is a product of lipid peroxidation reaction: formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J. Biol. Chem. 1998, 273:16058-16066.
27. Sayre L.M., Arora P.K., Iyer R.S., Salomon R.G. Pyrrole formation from 4-hydroxynonenal and primary amines. Chem. Res. Toxicol. 1993, 6:19-22.
28. Bolgar M.S., Yang C.-Y., Gaskell S.J. First direct evidence for lipid/protein conjugation in oxidized human low density lipoprotein. J. Biol. Chem. 1996, 271:27999-28001.
29. Sharp J.S., Becker J.M., Hettich R.L. Protein surface mapping by chemical oxidation: structural analysis by mass spectrometry. Anal. Biochem. 2003, 313:216-225.
30. Sharp J.S., Becker J.M., Hettich R.L. Analysis of protein solvent accessible surfaces by photochemical oxidation and mass spectrometry. Anal. Chem. 2004, 76:672-683.
31. Aye T.T., Low T.Y., Sze S.K. Nanosecond laser-induced photochemical oxidation method for protein surface mapping with mass spectrometry. Anal. Chem. 2005, 77:5814-5822.
32. Sharp J.S., Tomer K.B. Effects of anion proximity in peptide primary sequence on the rate and mechanism of leucine oxidation. Anal. Chem. 2006, 78:4885-4893.
33. Shao B., Bergt C., Fu X., Green P., Voss J.C., Oda M.N., Oram J.F., Heinecke J.W. Tyrosine 192 in apolipoprotein A-I is the major site of nitration and chlorination by myeloperoxidase, but only chlorination markedly impairs ABCA1-dependent cholesterol transport. J. Biol. Chem. 2005, 280:5983-5993.
34. Shao B., Fu X., McDonald T.O., Green P.S., Uchida K., O'Brien K.D., Oram J.F., Heinecke J.W. Acrolein impairs ATP binding cassette transporter A1-dependent cholesterol export from cells through site-specific modification of apolipoprotein A-I. J. Biol. Chem. 2005, 280:36386-36396.
35. Bolgar M.S., Gaskell S.J. Determination of the sites of 4-hydroxy-2-nonenal adduction to protein by electrospray tandem mass spectrometry. Anal. Chem. 1996, 68:2325-2330.
36. Karlsson H., Leanderson P., Tagesson C., Lindahl M. Lipoproteomics: I. Mapping of proteins in low-density lipoprotein using two-dimensional gel electrophoresis and mass spectrometry. Proteomics 2005, 5:551-565.
37. 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, 5:2619-2630.
38. Carlsson P., Olofsson S.O., Bondjers G., Darnfors C., Wiklund O., Bjursell G. Molecular cloning of human apolipoprotein B cDNA. Nucleic Acids Res. 1985, 13:8813-8826.
39. Wei C.F., Chen S.H., Yang C.Y., Marcel Y.L., Milne R.W., Li W.H., Sparrow J.T., Gotto A.M., Chan L. Molecular cloning and expression of partial cDNAs and deduced amino acid sequence of a carboxyl-terminal fragment of human apolipoprotein B-100. Proc. Natl. Acad. Sci. USA 1985, 82:7265-7269.
40. Carlsson P., Darnfors C., Olofsson S.O., Bjursell G. Analysis of the human apolipoprotein B gene: complete structure of the B-74 region. Gene 1986, 49:29-51.
41. Chen S.H., Yang C.Y., Chen P.F., Setzer D., Tanimura M., Li W.H., Gotto A.M., Chan L. The complete cDNA and amino acid sequence of human apolipoprotein B-100. J. Biol. Chem. 1986, 261:12918-12921.
42. Cladaras C., Hadzopoulou-Cladaras M., Nolte R.T., Atkinson D., Zannis V.I. The complete sequence and structural analysis of human apolipoprotein B-100: relationship between apoB-100 and apoB-48 forms. EMBO J. 1986, 5:3495-3507.
43. Law S.W., Grant S.M., Higuchi K., Hospattankar A., Lackner K., Lee N., Brewer H.B. Human liver apolipoprotein B-100 cDNA: complete nucleic acid and derived amino acid sequence. Proc. Natl. Acad. Sci. USA 1986, 83:8142-8146.
44. Pfitzner R., Wagener R., Stoffel W. Isolation, expression, and characterization of a human apolipoprotein B 100-specific cDNA clone. Biol. Chem. 1986, 367:1077-1083.
45. Yang C.Y., Chen S.H., Gianturco S.H., Bradley W.A., Sparrow J.T., Tanimura M., Li W.H., Sparrow D.A., De Loof H., Rosseneu M., Lee F.-S., Gu Z.-W., Gotto A.M., Chan L. Sequence, structure, receptor-binding domains, and internal repeats of human apolipoprotein B-100. Nature (Lond.) 1986, 323:738-742.
46. Ludwig E.H., Blackhart B.D., Pierotti V.R., Caiati L., Fortier C., Knott T., Scott J., Mahley R.W., Levy-Wilson B., McCarthy B.J. DNA sequence of the human apolipoprotein B gene. DNA 1987, 6:363-372.
47. Navajas M., Laurent A.M., Moreel J.F., Ragab A., Cambou J.P., Cuny G., Cambien F., Roizes G. Detection by denaturing gradient gel electrophoresis of a new polymorphism in the apolipoprotein B gene. Hum. Genet. 1990, 86:91-93.
48. Zhou X., Mopper K. Determination of photochemically produced hydroxyl radicals in seawater and freshwater. Mar. Chem. 1990, 30:71-88.
49. Lindsey M.E., Xu G., Lu J., Tarr M.A. Enhanced Fenton degradation of hydrophobic organics by simultaneous iron and pollutant complexation with cyclodextrins. Sci. Total Environ. 2003, 307:215-229.
50. Goshe M.B., Blonder J., Smith R.D. Affinity labeling of highly hydrophobic integral membrane proteins for proteome-wide analysis. J. Proteome Res. 2003, 2:153-161.
51. Blonder J., Goshe M.B., Moore R.J., Pasa-Tolic L., Masselon C.D., Lipton M.S., Smith R.D. Enrichment of integral membrane proteins for proteomic analysis using liquid chromatography-tandem mass spectrometry. J. Proteome Res. 2002, 1:351-360.
52. Requena J.R., Levine R.L., Stadtman E.R. Recent advances in the analysis of oxidized proteins. Amino Acids 2003, 25:221-226.
53. Liu Z., Minkler P.E., Sayre L.M. Mass spectroscopic characterization of protein modification by 4-hydroxy-2-(E)-nonenal and 4-oxo-2-(E)-nonenal. Chem. Res. Toxicol. 2003, 16:901-911.
54. Hardman D.A., Protter A.A., Chen G.C., Schilling J.W., Sato K.Y., Lau K., Yamanaka M., Mikita T., Miller J., Crisp T., McEnroe G., Scarborough R.M., Kane J.P. Structural comparison of human apolipoproteins B-48 and B-100. Biochemistry (Mosc.) 1987, 26:5478-5486.
55. Steen H., Mann M. The abc's (and xyz's) of peptide sequencing. Nat. Rev. Mol. Cell Biol. 2004, 5:699-711.
56. Jurgens G., Hoff H.F., Chisolm G.M., Esterbauer H. Modification of human serum low-density lipoprotein by oxidation: characterization and pathophysiological implications. Chem. Phys. Lipids 1987, 45:315-336.
57. Hambly D.M., Gross M.L. Laser flash photolysis of hydrogen peroxide to oxidize protein solvent-accessible residues on the microsecond timescale. J. Am. Soc. Mass Spectrom. 2005, 16:2057-2063.
58. Chehin R., Rengel D., Milicua J.C.G., Goni F.M., Arrondo J.L.R., Pifat G. Early stages of LDL oxidation: apolipoprotein B structural changes monitored by infrared spectroscopy. J. Lipid Res. 2001, 42:778-782.
59. Jayaraman S., Gantz D.L., Gursky O. Effects of oxidation on the structure and stability of human low-density lipoprotein. Biochemistry (Mosc.) 2007, 46:5790-5797.
60. Oorni K., Pentikainen M.O., Ala-Korpela M., Kovanen P.T. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: Molecular mechanisms and effects on matrix interactions. J. Lipid Res. 2000, 41:1703-1714.
61. Heinecke J.W., Rosen H., Chait A. Iron and copper promote modification of low density lipoprotein by human arterial smooth muscle cells in culture. J. Clin. Invest. 1984, 74:1890-1894.
62. 2 induce apoptosis through Fenton chemistry independent of the cellular thiol state. Free Radic. Biol. Med. 2001, 30:1008-1018.
63. Collot-Teixeira S., Martin J., McDermott-Roe C., Poston R., McGregor J.L. CD36 and macrophages in atherosclerosis. Cardiovasc. Res. 2007, 75:468-477.
64. Kar N.S., Ashraf M.Z., Valiyaveettil M., Podrez E.A. Mapping and characterization of the binding site for specific oxidized phospholipids and oxidized low density lipoprotein of scavenger receptor CD36. J. Biol. Chem. 2008, 283:8765-8771.
65. Wild B., Green B., Stephens A. The potential of electrospray ionization mass spectrometry for the diagnosis of hemoglobin variants found in newborn screening. Blood Cells Mol. Dis. 2004, 33:308-317.
66. Bellelli A., Brunori M., Miele A., Panetta G., Vallone B. The allosteric properties of hemoglobin: insights from natural and site directed mutants. Curr. Protein Pept. Sci. 2006, 7:17-45.
67. Fisher E., Scharnagl H., Hoffmann M.M., Kusterer K., Wittmann D., Wieland H., Gross W., Marz W. Mutations in the apolipoprotein (apo) B-100 receptor-binding region: detection of apo B-100 (Arg3500→Trp) associated with two new haplotypes and evidence that apo B-100 (Glu3405→Gln) diminishes receptor-mediated uptake of LDL. Clin. Chem. 1999, 45:1026-1038.