Haptoglobin binding to apolipoprotein A-I prevents damage from hydroxyl radicals on its stimulatory activity of the enzyme lecithin-cholesterol acyl-transferase

Biochemistry

Volumn 46, Issue 39, 2007, Pages 11158-11168

  Salvatore, Alfonso ^a   Cigliano, Luisa ^a   Bucci, Enrico M ^b,c   Corpillo, Davide ^b   Velasco, Silvia ^b   Carlucci, Alessandro ^a   Pedone, Carlo ^a,d   Abrescia, Paolo ^a,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b Laboratorio Integrato Metodologie Avanzate   (Italy)

^c CNR   (Italy)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; ELECTROPHORESIS; ENZYME ACTIVITY; ESTERIFICATION; MACROPHAGES; OXIDATIVE STRESS;

HAPTOGLOBINS; HYDROXYL RADICALS; HYDROXYPROLINES; INFLAMMATIONS; PLASMA PROTEINS;

PROTEINS;

APOLIPOPROTEIN A1; CARRAGEENAN; HAPTOGLOBIN; HEMOGLOBIN; HIGH DENSITY LIPOPROTEIN; HYDROXYL RADICAL; HYDROXYPROLINE; LIPOSOME; MONOMER; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; RESIN;

AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL ESTERIFICATION; CONTROLLED STUDY; DISEASE MODEL; ELECTROPHORESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; INFLAMMATION; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN IMMOBILIZATION; PROTEIN PROTEIN INTERACTION; REACTION ANALYSIS; SWISS WEBSTER MOUSE;

ANIMALS; APOLIPOPROTEIN A-I; APOLIPOPROTEIN C-II; APOLIPOPROTEINS D; BLOTTING, WESTERN; CHROMATOGRAPHY, AFFINITY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HAPTOGLOBINS; HUMANS; HYDROXYL RADICAL; KINETICS; LIPOPROTEINS, HDL; MALE; MICE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PHOSPHATIDYLCHOLINE-STEROL O-ACYLTRANSFERASE; PROTEIN BINDING; TANDEM MASS SPECTROMETRY; TIME FACTORS;

MUS;

EID: 34848833578     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7006349     Document Type: Article

References (55)

1. Lewis, G. F., and Rader, D. (2005) New Insights into the Regulation of HDL Metabolism and Reverse Cholesterol Transport, Circ. Res. 96, 1221-1232.
2. Linsel-Nitschke, P., and Tall, A. R. (2005) HDL as a target in the treatment of atherosclerotic cardiovascular disease, Nat. Rev. 4, 193-205.
3. Acton, S., Rigotti, A., Landshultz, K. T., Xu, S., Hobbs, H. H., and Krieger, M. (1996) Identification of scavenger receptor SR-BI as high density lipoprotein receptor, Science 271, 518-520.
4. Xu, S., Laccotripe, M., Huang, X., Rigotti, A., Zannis, V. I., and Krieger, M. (1997) Apolipoproteins of HDL can directly mediate binding to the scavenger receptor SR-BI, an HDL receptor that mediates selective lipid uptake, J. Lipid. Res. 38, 1289-1298.
5. Temel, R. E., Trigatti, B., DeMattos, R. B., Azhar. S., Krieger, M., and Williams, D. L. (1997) Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells, Proc. Natl. Acad. Sci. 94, 13600-13605.
6. Plump, A. S., Erickson, S. K., Weng, W., Partin, J. S., Breslow, J. L., and Williams, D. L. (1996) Apolipoprotein A-I is required for cholesteryl ester accumulation in steroidogenic cells and for normal adrenal steroid production, J. Clin. Invest. 97, 2660-2671.
7. Sorci-Thomas, M. G., and Thomas, M. J. (2002) The effects of altered apolipoprotein A-I structure on plasma HDL concentration, Trends Cardiovasc. Med. 12, 121-128.
8. Francis, G. A. (2000) High density lipoprotein oxidation: in vitro susceptibility and potential in vivo consequences, Biochim. Biophys. Acta 1483, 217-235.
9. Marsche, G., Hammer, A., Oskolkova, O., Kozarsky, K. F., Sattler, W., and Malle, E. (2002) Hypochlorite-modified high density lipoprotein, a high affinity ligand to scavenger receptor class B, type I, impairs high density lipoprotein-dependent selective lipid uptake and reverse cholesterol transport, J. Biol. Chem. 277, 32172-32179.
10. Shao, B., Oda, M. N., Bergt, C., Fu, X., Green, P. S., Brot, N., Oram, J. F., and Heinecke, J. W. (2006) Myeloperoxidase impairs ABCA1-dependent cholesterol efflux through methionine oxidation and site-specific tyrosine chlorination of apolipoprotein A-I, J. Biol. Chem. 281, 9001-9004.
11. Shao, B., Bergt, C., Fu, X., Green, P. S., Voss, J. C., Oda, M. N., Oram, J. F., and Heinecke, J. W. (2005) 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. 280, 5983-5993.
12. Zheng, L., Nukuna, B., Brennan, M. L., Sun, M., Goormastic, M., Settle, M., Schmitt, D., Fu, X., Thomson, L., Fox, P. L., Ischiropoulos, H., Smith, J. D., Kinter, M., and Hazen, S. L. (2004) Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease, J. Clin. Invest. 114, 529-541.
13. Libby, P., Ridker, P. M., and Maseri, A. (2002) Inflammation and atherosclerosis, Circulation 105, 1135-1143.
14. Hansson, G. K., and Libby, P. (2006) The immune response in atherosclerosis: a double-edged sword, Nat. Rev. Immunol. 6, 508-519.
15. Halliwell, B., Gutteridge, J. M. C. (2000) Free Radicals in biology and medicine; Oxford University Press, New York.
16. Langlois, M. R., and Delanghe, J. R. (1996) Biological and clinical significance of haptoglobin polymorphism in humans, Clin. Chem. 42, 1589-1600.
17. Sutton, H. E. (1970) The haptoglobins, Prog. Med. Genet. 7, 163-216.
18. Moestrup, S. K., and Moller, H. J. (2004) CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response, Ann. Med. 36, 347-354.
19. Sayed, M. H., Sadrzadeh, S. M., Graf, E., Panter, S. S., Hallaway, P. E., and Eaton, J. W. (1984) Hemoglobin. A biologic fenton reagent, J. Biol. Chem. 259, 14354-14356.
20. Taniyama, Y., and Griendling, K. K. (2003) Reactive oxygen species in the vasculature. Molecular and cellular mechanisms, Hypertension 42, 1075-1081.
21. Halliwell, B., Clement, M. V., and Long, L. H. (2000) Hydrogen peroxide in the human body, FEBS Lett. 486, 10-13.
22. Elahi, M. M., and Matata, B. M. (2006) Free radicals in blood: evolving concepts in the mechanism of ischemic heart disease, Arch. Biochem. Biophys. 450, 78-88.
23. Aruoma, O. I., and Halliwell, B. (1987) Superoxide-dependent and ascorbate-dependent formation of hydroxyl radicals from hydrogen peroxide in the presence of iron. Are lactoferrin and transferrin promoters of hydroxyl-radical generation?, Biochem. J. 241, 273-278.
24. Rademacher, B. E., and Steele, W. J. (1987) A general method for the isolation of haptoglobin 1-1, 1-2 and 2-2 from human plasma, Anal. Biochem. 160, 119-126.
25. Kunitake, S. T., Carilli, C. T., Lau, K., Protter, A. A., Naya-Vigne, J., and Kane, J. P. (1994) Identification of proteins associated with apolipoprotein A-I -containing lipoproteins purified by selected -affinity immunosorption, Biochemistry 33, 1988-1993.
26. Spagnuolo, M. S., Cigliano, L., and Abrescia, P. (2003) The binding of haptoglobin to apolipoprotein A-I: influence of hemoglobin and cancanavalin A, Biol. Chem. 384, 1593-1596.
27. Spagnuolo, M. S., Cigliano, L., D'Andrea, L. D., Pedone, C., and Abrescia, P. (2005) Assignment of the binding site for haptoglobin on apolipoprotein A-I, J. Biol. Chem. 280, 1193-1198.
28. Cho, K. H., Durbin, D. M., and Jonas, A. (2001) Role of individual amino acids of apolipoprotein A-I in the activation of lecithin: cholesterol acyltransferase and in HDL rearrangements, J. Lipid Res. 42, 379-389.
29. Cigliano, L., Spagnuolo, M. S., Cuomo, G., Valentini, G., Niglio, A., and Abrescia, P. (2005) Apolipoprotein A-I-dependent cholesterol esterification in patients with rheumatoid arthritis, Life Sei. 77, 108-120.
30. Wolfe, F. (1997) Comparative usefulness of C-reactive protein and erythrocyte sedimentation rate in patients with rheumatoid arthritis, J. Rheumatol. 24, 1477-1485.
31. Goodson, N. (2002) Coronary artery disease and rheumatoid arthritis, Curr. Opin. Rheumatol. 14, 115-120.
32. Schumaker, V. N., and Puppione, D. L. (1986) Sequential flotation ultracentrifugation, Methods Enzymol. 128, 155-170.
33. Miller, N. J., Rice-Evans, C., Davies, M. J., Gopinathan, V., and Milner, A. (1993) A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates, Clin. Sci. (London) 84, 407-412.
34. Cigliano, L., Spagnuolo, M. S., and Abrescia, P. (2003) Quantitative variations of the isoforms in haptoglobin 1-2 and 2-2 individual phenotypes, Arch. Biochem. Biophys. 416, 227-237.
35. Towbin, H., Staehelin, T., and 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.
36. Posadas, I., Bucci, M., Roviezzo, F., Rossi, A., Parente, L., Sautebin, L., and Cirino, G. (2004) Carrageenan-induced mouse paw oedema is biphasic, age-weight dependent and displays differential nitric oxide cyclooxygenase-2 expression. Br. J. Pharmacol. 142, 331-338.
37. Brewer, H. B., Jr., Ronan, R., Meng, M., and Bishop, C. (1986) Isolation and characterization of apolipoproteins A-I, A-II, and A-IV, Methods Enzymol. 128, 223-246.
38. Delanghe, J., Allcock, K., Langlois, M., Claeys, L., and De Buyzere, M. (2000) Fast determination of haptoglobin phenotype and calculation of hemoglobin binding capacity using high pressure gel permeation chromatography, Clin. Chim. Acta 291, 43-51.
39. Rezaee, F., Casetta, B., Levels, J. H., Speijer, D., and Meijers, J. C. (2006) Proteomic analysis of high-density lipoprotein, Proteomics 6, 721-730.
40. Crawford, J. H., Chacko, B. K., Kevil, C. G., and Patel, R. P. (2004) The red blood cell and vascular function in health and disease, Antioxid. Redox Signaling 6, 992-999.
41. Panzenbock, U., Kritharides, L., Raftery, M., Rye, K. A., and Stocker, R. (2000) Oxidation of methionine residues to methionine sulfoxides does not decrease potential antiatherogenic properties of apolipoprotein A-I, J. Biol. Chem. 275, 19536-19544.
42. Agil, A., Fuller, C. J., and Jialal, I. (1995) Susceptibility of plasma to ferrous iron/hydrogen peroxide-mediated oxidation: demonstration of a possible Fenton reaction, Clin. Chem. 4, 220-225.
43. Macdonald, D. L., Terry, T. L., Agellon, L. B., Nation, P. N., and Francis, G. A. (2003) Administration of tyrosyl radical-oxidized HDL inhibits the development of atherosclerosis in apolipoprotein E-deficient mice, Arterioscler. Thromb. Vasc. Biol. 23, 1583-1588.
44. Wang, X. L., Dudman, N. P., Wang, J., and Wilcken, D. E. (1989) Mechanisms responsible for increasing immunoreactivity of apolipoprotein A-I with storage: the role of oxidation, Clin. Chem. 35, 2082-2086.
45. Karlsson, H., Leanderson, P., Tagesson, C., and Lindahl, M. (2005) Lipoproteomics II: Mapping of proteins in high-density lipoprotein using two-dimensional gel electrophoresis and mass spectrometry, Proteomics 5, 1431-1445.
46. Schuessler, H., and Schilling, K. (1984) Oxygen effect in the radiolysis of proteins. Part 2. Bovine serum albumin, Int. J. Radiat. Biol. Relat. Stud. Phys., Chem. Med. 45, 267-281.
47. Requena, J. R., Levine, R. L., and Stadtman, E. R. (2003) Recent advances in the analysis of oxidized proteins, Amino Acids 25, 221-226.
48. Amici, A., Levine, R. L., Tsai, L., and Stadtman, E. R. (1989) Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions, J. Biol. Chem. 264, 3341-3346.
49. Fu, S., Dean, R., Southan, M., and Truscott, R. (1998) The hydroxyl radical in lens nuclear cataractogenesis, J. Biol. Chem. 273, 28603-28609.
50. Balestrieri, M., Cigliano, L., De Simone, M. L., Dale, B., and Abrescia, P. (2001) Haptoglobin inhibits lecithin-cholesterol acyltransferase in human ovarian follicular fluid, Mol. Reprod. Dev. 59, 186-191.
51. Langlois, M. R., Delanghe, J. R., De Buyzere, M. L., Bernard, D. R., and Ouyang, J. (1997) Effect of haptoglobin on the metabolism of vitamin C, Am. J. Clin. Nutr. 66, 606-610.
52. Bernard, D., Christophe, A., Delanghe, J., De Buyzere, M., and Comhaire, F. (2003) The effect of supplementation with an antioxidant preparation on LDL-oxidation is determined by haptoglobin polymorphism. Redox Rep. 8, 41-46.
53. Rees, D., Sloane, T., Jessup, W., Dean, R. T., and Kritharides, L. (1999) Apolipoprotein A-I stimulates secretion of apolipoprotein E by foam cell macrophages, J. Biol. Chem. 274, 27925-27933.
54. Curtiss, L. K., Valenta, D. T., Hime, N. J., and Rye, K. A. (2006) What is so special about apolipoprotein AI in reverse cholesterol transport?, Arterioscler. Thromb. Vasc. Biol. 26, 12-19.
55. Ramet, M. E., Ramet, M., Lu, Q., Nickerson, M., Savolainen, M. J., Malzone, A., and Karas, R. H. (2003) High-density lipoprotein increases the abundance of eNOS protein in human vascular endothelial cells by increasing its half-life, J. Am. Coll. Cardiol. 41, 2288-2297.