Acidity increases the uptake of native LDL by human monocyte-derived macrophages

Atherosclerosis

Volumn 217, Issue 2, 2011, Pages 401-406

  Plihtari, Riia ^a   Kovanen, Petri T ^a   Öörni, Katariina ^a  

^a WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

Acidic pH; LDL; Macrophage; Proteoglycan

Indexed keywords

GLYCOSAMINOGLYCAN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEPARIN LYASE; LOW DENSITY LIPOPROTEIN; N ACETYLGALACTOSAMINE 4 SULFATASE; PROTEOGLYCAN;

ACIDITY; ARTICLE; ATHEROGENESIS; CELL DIFFERENTIATION; CELL PH; CELL SURFACE; CONTROLLED STUDY; FOAM CELL; GRANULOCYTE; HUMAN; HUMAN CELL; LIPID STORAGE; MACROPHAGE; MONOCYTE; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION;

BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELLS, CULTURED; CHLORATES; CHONDROITINASES AND CHONDROITIN LYASES; HEPARIN LYASE; HUMANS; HYDROGEN-ION CONCENTRATION; LIPOPROTEINS, LDL; MACROPHAGES; PINOCYTOSIS; PROTEOGLYCANS; TIME FACTORS; UP-REGULATION;

EID: 79960696690     PISSN: 00219150     EISSN: 18791484     Source Type: Journal    
DOI: 10.1016/j.atherosclerosis.2011.04.013     Document Type: Article

References (44)

1. Hansson G.K. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005, 352:1685-1695.
2. Pentikäinen M.O., Öörni K., Ala-Korpela M., Kovanen P.T. Modified LDL - trigger of atherosclerosis and inflammation in the arterial intima. J Intern Med 2000, 247:359-370.
3. Brown M.S., Goldstein J.L. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu Rev Biochem 1983, 52:223-261.
4. Bostrom P., Magnusson B., Svensson P.A., et al. Hypoxia converts human macrophages into triglyceride-loaded foam cells. Arterioscler Thromb Vasc Biol 2006, 26:1871-1876.
5. Nissen S.E., Yock P. Intravascular ultrasound - novel pathophysiological insights and current clinical applications. Circulation 2001, 103:604-616.
6. Torres F., Leunig I., Yuan M., Intaglietta F., Jain M. Noninvasive measurement of microvascular R.K. interstitial oxygen profiles in a human tumor in S.C.I.D. mice. Proc Natl Acad Sci U S A 1994, 91:2081-2085.
7. Sluimer J.C., Gasc J.M., van Wanroij J.L., et al. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol 2008, 51:1258-1265.
8. Sluimer J.C., Daemen M.J. Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. J Pathol 2009, 218:7-29.
9. Leppänen O., Bjornheden T., Evaldsson M., Boren J., Wiklund O., Levin M. ATP depletion in macrophages in the core of advanced rabbit atherosclerotic plaques in vivo. Atherosclerosis 2006, 188:323-330.
10. Naghavi M., John R., Naguib S., et al. pH Heterogeneity of human and rabbit atherosclerotic plaques; a new insight into detection of vulnerable plaque. Atherosclerosis 2002, 164:27-35.
11. Haka A.S., Grosheva I., Chiang E., et al. Macrophages create an acidic extracellular hydrolytic compartment to digest aggregated lipoproteins. Mol Biol Cell 2009, 20:4932-4940.
12. Yao L.Y., Moody C., Schonherr E., Wight T.N., Sandell L.J. Identification of the proteoglycan versican in aorta and smooth muscle cells by DNA sequence analysis, in situ hybridization and immunohistochemistry. Matrix Biol 1994, 14:213-225.
13. Wegrowski Y., Milard A.L., Kotlarz G., Toulmonde E., Maquart F.X., Bernard J. Cell surface proteoglycan expression during maturation of human monocytes-derived dendritic cells and macrophages. Clin Exp Immunol 2006, 144:485-493.
14. Camejo G., Rosengren B., Olson U., et al. Molecular basis of the association of arterial proteoglycans with low density lipoproteins: its effect on the structure of the lipoprotein particle. Eur Heart J 1990, 11(Suppl. E):164-173.
15. Camejo G., Lalaguna F., Lopez F., Starosta R. Characterization and properties of a lipoprotein-complexing proteoglycan from human aorta. Atherosclerosis 1980, 35:307-320.
16. Sneck M., Kovanen P.T., Oorni K. Decrease in pH strongly enhances binding of native, proteolyzed, lipolyzed, and oxidized low density lipoprotein particles to human aortic proteoglycans. J Biol Chem 2005, 280:37449-37454.
17. Öörni K., Kovanen P.T. Enhanced extracellular lipid accumulation in acidic environments. Curr Opin Lipidol 2006, 17:534-540.
18. Vijayagopal P., Srinivasan S.R., Radhakrishnamurthy B., Berenson G.S. Human monocyte-derived macrophages bind low-density-lipoprotein-proteoglycan complexes by a receptor different from the low-density-lipoprotein receptor. Biochem J 1993, 289(Pt 3):837-844.
19. Boyanovsky B.B., Shridas P., Simons M., van der Westhuyzen D.R., Webb N.R. Syndecan-4 mediates macrophage uptake of group V secretory phospholipase A2-modified LDL. J Lipid Res 2009, 50:641-650.
20. Kruth H.S., Jones N.L., Huang W., et al. Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein. J Biol Chem 2005, 280:2352-2360.
21. Lähdesmäki K., Plihtari R., Soininen P., et al. Phospholipase A(2)-modified LDL particles retain the generated hydrolytic products and are more atherogenic at acidic pH. Atherosclerosis 2009, 207:352-359.
22. Havel R.J., Eder H.A., Bragdon J.H. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Cli Invest 1955, 34:1345-1353.
23. Radding C.M., Steinberg D. Studies on the synthesis and secretion of serum lipoproteins by rat liver slices. J Clin Invest 1960, 39:1560-1569.
24. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem 1951, 193:265-275.
25. Saren P., Welgus H.G., Kovanen P.T. TNF-alpha and IL-1beta selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol 1996, 157:4159-4165.
26. Xu X.X., Tabas I. Sphingomyelinase enhances low density lipoprotein uptake and ability to induce cholesteryl ester accumulation in macrophages. J Biol Chem 1991, 266:24849-24858.
27. Turnbull J.E., Lyon M., Gallagher J.T. Structural analysis of glycosaminoglycans. Extracellular matrix: a practical approach 1999, 199-220. Oxford University Press, New York, USA. M.A. Haralson, J.R. Hassell (Eds.).
28. Bolton A.E., Hunter W.M. The labelling of proteins to high specific radioactivities by conjugation to a 125I-containing acylating agent. Biochem J 1973, 133:529-539.
29. Wooton-Kee C.R., Boyanovsky B.B., Nasser M.S., de Villiers W.J., Webb N.R. Group V sPLA2 hydrolysis of low-density lipoprotein results in spontaneous particle aggregation and promotes macrophage foam cell formation. Arterioscler Thromb Vasc Biol 2004, 24:762-767.
30. Boyanovsky B.B., van der Westhuyzen D.R., Webb N.R. Group V secretory phospholipase A2-modified low density lipoprotein promotes foam cell formation by a SR-A- and CD36-independent process that involves cellular proteoglycans. J Biol Chem 2005, 280:32746-32752.
31. Öörni K., Pentikäinen 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.
32. Kruth H.S., Huang W., Ishii I., Zhang W.Y. Macrophage foam cell formation with native low density lipoprotein. J Biol Chem 2002, 277:34573-34580.
33. Waldo S.W., Li Y., Buono C., et al. Heterogeneity of human macrophages in culture and in atherosclerotic plaques. Am J Pathol 2008, 172:1112-1126.
34. Bjornheden T., Bondjers G. Oxygen consumption in aortic tissue from rabbits with diet-induced atherosclerosis. Arteriosclerosis 1987, 7:238-247.
35. Bjornheden T., Levin M., Evaldsson M., Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol 1999, 19:870-876.
36. Punturieri A., Filippov S., Allen E., et al. Regulation of elastinolytic cysteine proteinase activity in normal and cathepsin K-deficient human macrophages. J Exp Med 2000, 192:789-799.
37. Asplund A., Stillemark-Billton P., Larsson E., et al. Hypoxic regulation of secreted proteoglycans in macrophages. Glycobiology 2010, 20:33-40.
38. Gigli M., Consonni A., Ghiselli G., Rizzo V., Naggi A., Torri G. Heparin binding to human plasma low-density lipoproteins: dependence on heparin sulfation degree and chain length. Biochemistry 1992, 31:5996-6003.
39. Ji Z.S., Mahley R.W. Lactoferrin binding to heparan sulfate proteoglycans and the LDL receptor-related protein Further evidence supporting the importance of direct binding of remnant lipoproteins to HSPG. Arterioscler Thromb 1994, 14:2025-2031.
40. Andres J.L., Stanley K., Cheifetz S., Massague J. Membrane-anchored and soluble forms of betaglycan, a polymorphic proteoglycan that binds transforming growth factor-beta. J Cell Biol 1989, 109:3137-3145.
41. Godyna S., Liau G., Popa I., Stefansson S., Argraves W.S. Identification of the low density lipoprotein receptor-related protein (LRP) as an endocytic receptor for thrombospondin-1. J Cell Biol 1995, 129:1403-1410.
42. Moestrup S.K., Kaltoft K., Sottrup-Jensen L., Gliemann J. The human alpha 2-macroglobulin receptor contains high affinity calcium binding sites important for receptor conformation and ligand recognition. J Biol Chem 1990, 265:12623-12628.
43. Williams S.E., Ashcom J.D., Argraves W.S., Strickland D.K. A novel mechanism for controlling the activity of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J Biol Chem 1992, 267:9035-9040.
44. Ling T.Y., Chen C.L., Huang Y.H., Liu I.H., Huang S.S., Huang J.S. Identification and characterization of the acidic pH binding sites for growth regulatory ligands of low density lipoprotein receptor-related protein-1. J Biol Chem 2004, 279:38736-38748.