Native low-density lipoprotein uptake by macrophage colony-stimulating factor-differentiated human macrophages is mediated by macropinocytosis and micropinocytosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 30, Issue 10, 2010, Pages 2022-2031

  Anzinger, Joshua J ^a   Chang, Janet ^a   Xu, Qing ^a   Buono, Chiara ^a   Li, Yifu ^a   Leyva, Francisco J ^a   Park, Bum Chan ^a   Greene, Lois E ^a   Kruth, Howard S ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

atherosclerosis; LDL; macrophages; macropinocytosis; micropinocytosis

Indexed keywords

2,3 DIHYDRO 2 OXO 3 (4,5,6,7 TETRAHYDRO 1H INDOL 2 YLMETHYLENE) 1H INDOLE 5 SULFONIC ACID DIMETHYLAMIDE; BAFILOMYCIN A1; CHOLESTEROL; COLONY STIMULATING FACTOR 1; LOW DENSITY LIPOPROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; INDOLE DERIVATIVE; MACROLIDE; SULFONAMIDE;

ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL DIFFERENTIATION; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIPID TRANSPORT; MACROPHAGE; PINOCYTOSIS; PRIORITY JOURNAL; ACTIVE TRANSPORT; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; IMMUNOELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY;

BIOLOGICAL TRANSPORT, ACTIVE; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; INDOLES; LIPOPROTEINS, LDL; MACROLIDES; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICROSCOPY, IMMUNOELECTRON; PINOCYTOSIS; SULFONAMIDES;

EID: 77957699953     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.210849     Document Type: Article

References (61)

1. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999; 340:115-126.
2. Steinberg D. The LDL modification hypothesis of atherogenesis: an update. J Lipid Res. 2009;50(suppl):S376-S381.
3. Hoff HF, Gaubatz JW, Gotto AM Jr. Apo B concentration in the normal human aorta. Biochem Biophys Res Commun. 1978;85:1424-1430.
4. Smith EB. Transport, interactions and retention of plasma proteins in the intima: the barrier function of the internal elastic lamina. Eur Heart J. 1990;11(suppl E):72-81.
5. Smith EB, Ashall C. Low-density lipoprotein concentration in interstitial fluid from human atherosclerotic lesions: relation to theories of endothe-lial damage and lipoprotein binding. Biochim Biophys Acta. 1983;754: 249-257.
6. Kruth HS, Jones NL, Huang W, Zhao B, Ishii I, Chang J, Combs CA, Malide D, Zhang WY. Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein. J Biol Chem. 2005;280:2352-2360.
7. Zhao B, Li Y, Buono C, Waldo SW, Jones NL, Mori M, Kruth HS. Constitutive receptor-independent low density lipoprotein uptake and cholesterol accumulation by macrophages differentiated from human monocytes with macrophage-colony-stimulating factor (M-CSF). J Biol Chem. 2006;281:15757-15762.
8. Buono C, Anzinger JJ, Amar M, Kruth HS. Fluorescent pegylated nano-particles demonstrate fluid-phase pinocytosis by macrophages in mouse atherosclerotic lesions. J Clin Invest. 2009;119:1373-1381.
9. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem. 2009;78:857-902.
10. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature. 2003;422:37-44.
11. Clinton SK, Underwood R, Hayes L, Sherman ML, Kufe DW, Libby P. Macrophage colony-stimulating factor gene expression in vascular cells and in experimental and human atherosclerosis. Am J Pathol. 1992;140: 301-316.
12. Qiao JH, Tripathi J, Mishra NK, Cai Y, Tripathi S, Wang XP, Imes S, Fishbein MC, Clinton SK, Libby P, Lusis AJ, Rajavashisth TB. Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteo-petrotic mice. Am J Pathol. 1997;150:1687-1699.
13. Waldo SW, Li Y, Buono C, Zhao B, Billings EM, Chang J, Kruth HS. Heterogeneity of human macrophages in culture and in atherosclerotic plaques. Am J Pathol. 2008;172:1112-1126.
14. Akagawa KS. Functional heterogeneity of colony-stimulating factor-induced human monocyte-derived macrophages. Int J Hematol. 2002;76:27-34.
15. Goldstein JL, Basu SK, Brown MS. Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 1983;98: 241-260.
16. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265-275.
17. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem. 1957; 226:497-509.
18. Gamble W, Vaughan M, Kruth HS, Avigan J. Procedure for determination of free and total cholesterol in micro-or nanogram amounts suitable for studies with cultured cells. J Lipid Res. 1978;19:1068-1070.
19. Lang T, de Chastellier C. Fluid phase and mannose receptor-mediated uptake of horseradish peroxidase in mouse bone marrow-derived macro-phages: biochemical and ultrastructural study. Biol Cell. 1985;53: 149-154.
20. Yamaguchi Y, Dalle-Molle E, Hardison WG. Hepatocyte horseradish peroxidase uptake is saturable and inhibited by mannose-terminal glyco-proteins. Am J Physiol. 1993;264:G880-G885.
21. Kruth HS, Skarlatos SI, Lilly K, Chang J, Ifrim I. Sequestration of acetylated LDL and cholesterol crystals by human monocyte-derived macrophages. J Cell Biol. 1995;129:133-145.
22. Blake RA, Broome MA, Liu X, Wu J, Gishizky M, Sun L, Courtneidge SA. SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol Cell Biol. 2000;20:9018-9027.
23. Guo W, Castaigne JG, Mooney N, Charron D, Al-Daccak R. Signaling through HLA-DR induces PKC beta-dependent B cell death outside rafts. Eur J Immunol. 2003;33:928-938.
24. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor: study of Lck-and FynT-dependent T cell activation. J Biol Chem. 1996;271:695-701.
25. Yan SR, Novak MJ. Src-family kinase-p53/Lyn p56 plays an important role in TNF-alpha-stimulated production of O2-by human neutrophils adherent to fibrinogen. Inflammation. 1999;23:167-178.
26. Bae YS, Lee JH, Choi SH, Kim S, Almazan F, Witztum JL, Miller YI. Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein: toll-like receptor 4-and spleen tyrosine kinase-dependent activation of NADPH oxidase 2. Circ Res. 2009;104: 210-218, 221.
27. Choi SH, Harkewicz R, Lee JH, Boullier A, Almazan F, Li AC, Witztum JL, Bae YS, Miller YI. Lipoprotein accumulation in macrophages via toll-like receptor-4-dependent fluid phase uptake. Circ Res. 2009;104: 1355-1363.
28. Radhakrishna H, Klausner RD, Donaldson JG. Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. J Cell Biol. 1996;134:935-947.
29. Garrett WS, Chen LM, Kroschewski R, Ebersold M, Turley S, Trombetta S, Galan JE, Mellman I. Developmental control of endocytosis in dendritic cells by Cdc42. Cell. 2000;102:325-334.
30. West MA, Prescott AR, Eskelinen EL, Ridley AJ, Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol. 2000;10:839-848.
31. Sun P, Yamamoto H, Suetsugu S, Miki H, Takenawa T, Endo T. Small GTPase Rah/Rab34 is associated with membrane ruffles and macropi-nosomes and promotes macropinosome formation. J Biol Chem. 2003; 278:4063-4071.
32. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992;70:401-410.
33. Steinman RM, Brodie SE, Cohn ZA. Membrane flow during pinocytosis: a stereologic analysis. J Cell Biol. 1976;68:665-687.
34. Chinnapen DJ, Chinnapen H, Saslowsky D, Lencer WI. Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol Lett. 2007;266:129-137.
35. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol. 1995;5: 424-428.
36. Kasahara K, Nakayama Y, Sato I, Ikeda K, Hoshino M, Endo T, Yamaguchi N. Role of Src-family kinases in formation and trafficking of macropinosomes. J Cell Physiol. 2007;211:220-232.
37. Mettlen M, Platek A, Van Der Smissen P, Carpentier S, Amyere M, Lanzetti L, de Diesbach P, Tyteca D, Courtoy PJ. Src triggers circular ruffling and macropinocytosis at the apical surface of polarized MDCK cells. Traffic. 2006;7:589-603.
38. Veithen A, Amyere M, Van Der Smissen P, Cupers P, Courtoy PJ. Regulation of macropinocytosis in v-Src-transformed fibroblasts: cyclic AMP selectively promotes regurgitation of macropinosomes. J Cell Sci. 1998;111(pt 16):2329-2335.
39. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem J. 2007;408:297-315.
40. Racoosin EL, Swanson JA. Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J Exp Med. 1989;170:1635-1648.
41. Racoosin EL, Swanson JA. M-CSF-induced macropinocytosis increases solute endocytosis but not receptor-mediated endocytosis in mouse macrophages. J Cell Sci. 1992;102(pt 4):867-880.
42. Swanson JA. Phorbol esters stimulate macropinocytosis and solute flow through macrophages. J Cell Sci. 1989;94(pt 1):135-142.
43. Damke H, Baba T, van der Bliek AM, Schmid SL. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol. 1995;131:69-80.
44. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell. 1999;10:961-974.
45. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, McGraw TE. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci USA. 1999;96:6775-6780.
46. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell. 2004;15:3542-3552.
47. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell. 1992;68:673-682.
48. Buono C, Li Y, Waldo SW, Kruth HS. Liver X receptors inhibit human monocyte-derived macrophage foam cell formation by inhibiting fluid-phase pinocytosis of LDL. J Lipid Res. 2007;48:2411-2418.
49. Pratten MK, Lloyd JB. Effects of temperature, metabolic inhibitors and some other factors on fluid-phase and adsorptive pinocytosis by rat peritoneal macrophages. Biochem J. 1979;180:567-571.
50. Davies P, Allison AC. Effects of cytochalasin B on endocytosis and exocytosis. Front Biol. 1978;46:143-160.
51. Apodaca G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic. 2001;2:149-159.
52. Fujimoto LM, Roth R, Heuser JE, Schmid SL. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic. 2000;1:161-171.
53. Goldstein JL, Brown MS. Binding and degradation of low density lipoproteins by cultured human fibroblasts: comparison of cells from a normal subject and from a patient with homozygous familial hypercholesterolemia. J Biol Chem. 1974;249:5153-5162.
54. Brown MS, Goldstein JL. Receptor-mediated control of cholesterol metabolism. Science. 1976;191:150-154.
55. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y. Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem. 1991;266:17707-17712.
56. Presley JF, Mayor S, McGraw TE, Dunn KW, Maxfield FR. Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J Biol Chem. 1997;272:13929-13936.
57. Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol. 2006;8:124-136.
58. Brown D, Paunescu TG, Breton S, Marshansky V. Regulation of the V-ATPase in kidney epithelial cells: dual role in acid-base homeostasis and vesicle trafficking. J Exp Biol. 2009;212:1762-1772.
59. Bidani A, Heming TA. Effects of bafilomycin A1 on functional capabilities of LPS-activated alveolar macrophages. J Leukoc Biol. 1995;57: 275-281.
60. Swallow CJ, Grinstein S, Rotstein OD. A vacuolar type H(+)-ATPase regulates cytoplasmic pH in murine macrophages. J Biol Chem. 1990; 265:7645-7654.
61. Tapper H, Sundler R. Cytosolic pH regulation in mouse macrophages: proton extrusion by plasma-membrane-localized H(+)-ATPase. Biochem J. 1992;281(pt 1):245-250.