The lysosomal transfer of LDL/cholesterol from macrophages into vascular smooth muscle cells induces their phenotypic alteration

Cardiovascular Research

Volumn 97, Issue 3, 2013, Pages 544-552

  Weinert, Sönke ^a   Poitz, David M ^b   Auffermann Gretzinger, Susanne ^b   Eger, Lars ^b   Herold, Joerg ^a   Medunjanin, Senad ^a   Schmeisser, Alexander ^a   Strasser, Ruth H ^b   Braun Dullaeus, Ruediger C ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Cholesterol; Low density lipoprotein (LDL); Macrophages; Smooth muscle cells

Indexed keywords

FAT DROPLET; HYBRID PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; RAB5A FP PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL COMPOSITION; CELL FUNCTION; CELL INTERACTION; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; FLUORESCENCE MICROSCOPY; FOAM CELL; GENE INDUCTION; HUMAN; HUMAN CELL; LYSOSOME; MACROPHAGE; MOLECULAR MECHANICS; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ANIMALS; AORTA, ABDOMINAL; CELL COMMUNICATION; CELLS, CULTURED; CHOLESTEROL; CHOLESTEROL, LDL; COCULTURE TECHNIQUES; HUMANS; HYDROXYMETHYLGLUTARYL COA REDUCTASES; LIPOPROTEINS, LDL; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOMES; MACROPHAGES; MICROSCOPY, FLUORESCENCE; MUSCLE, SMOOTH, VASCULAR; PHENOTYPE; RATS; RATS, WISTAR;

EID: 84874275945     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs367     Document Type: Article

References (37)

1. Doran AC, Meller N, McNamara CA. Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler Thromb Vasc Biol 2008;28:812-819.
2. Ross R. George Lyman Duff Memorial Lecture. Atherosclerosis: a problem of the biology of arterial wall cells and their interactions with blood components. Arterioscler Thromb Vasc Biol 1981;1:293-311.
3. Faggiotto A, Ross R, Harker L. Studies of hypercholesterolemia in the nonhuman primate. I. Changes that lead to fatty streak formation. Arteriosclerosis 1984;4:323-340.
4. Ruan XZ, Moorhead JF, Tao JL, Ma KL, Wheeler DC, Powis SH et al. Mechanisms of dysregulation of low-density lipoprotein receptor expression in vascular smooth muscle cells by inflammatory cytokines. Arterioscler Thromb Vasc Biol 2006;26: 1150-1155.
5. Takahashi M, Takahashi S, Suzuki C, Jia L, Morimoto H, Ise H et al. Interleukin-1beta attenuates beta-very low-density lipoprotein uptake and its receptor expression in vascular smooth muscle cells. J Mol Cell Cardiol 2005;38:637-646.
6. Matsumoto K, Hirano K, Nozaki S, Takamoto A, Nishida M, Nakagawa-Toyama Y et al. Expression of macrophage (Mphi) scavenger receptor, CD36, in cultured human aortic smooth muscle cells in association with expression of peroxisome proliferator activated receptor-gamma, which regulates gain of Mphi-like phenotype in vitro, and its implication in atherogenesis. Arterioscler Thromb Vasc Biol 2000;20: 1027-1032.
7. Lim HJ, Lee S, Lee KS, Park JH, Jang Y, Lee EJ et al. PPARgamma activation induces CD36 expression and stimulates foam cell like changes in rVSMCs. Prostaglandins Other Lipid Mediat 2006;80:165-174.
8. Bickel PE, Freeman MW. Rabbit aortic smooth muscle cells express inducible macrophage scavenger receptor messenger RNA that is absent from endothelial cells. J Clin Invest 1992;90:1450-1457.
9. Weaver AM, Lysiak JJ, Gonias SL. LDL receptor family-dependent and-independent pathways for the internalization and digestion of lipoprotein lipase-associated beta-VLDL by rat vascular smooth muscle cells. J Lipid Res 1997;38:1841-1850.
10. Wolfbauer G, Glick JM, Minor LK, Rothblat GH. Development of the smooth muscle foam cell: uptake of macrophage lipid inclusions. Proc Natl Acad Sci USA 1986;83: 7760-7764.
11. Wada Y, Sugiyama A, Yamamoto T, Naito M, Noguchi N, Yokoyama S et al. Lipid accumulation in smooth muscle cells under LDL loading is independent of LDL receptor pathway and enhanced by hypoxic conditions. Arterioscler Thromb Vasc Biol 2002; 22:1712-1719.
12. Hoff HF, Pepin JM, Morton RE. Modified low density lipoprotein isolated from atherosclerotic lesions does not cause lipid accumulation in aortic smooth muscle cells. J Lipid Res 1991;32:115-124.
13. Rong JX, Shapiro M, Trogan E, Fisher EA. Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci USA 2003;100:13531-13536.
14. Andreeva ER, Pugach IM, Orekhov AN. Subendothelial smooth muscle cells of human aorta express macrophage antigen in situ and in vitro. Atherosclerosis 1997;135:19-27.
15. Orekhov AN, Tertov VV, Mukhin DN, Koteliansky VE, Glukhova MA, Frid MG et al. Insolubilization of low density lipoprotein induces cholesterol accumulation in cultured subendothelial cells of human aorta. Atherosclerosis 1989;79:59-70.
16. Bucana C, Hoyer LC, Hobbs B, Breesman S, McDaniel M, Hanna MG Jr. Morphological evidence for the translocation of lysosomal organelles from cytotoxic macrophages into the cytoplasm of tumor target cells. Cancer Res 1976;36:4444-4458.
17. Dean MF, Cooper JA, Stahl P. Cell contact and direct transfer between co-cultured macrophages and fibroblasts. J Leukoc Biol 1988;43:539-546.
18. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. Nanotubular highways for intercellular organelle transport. Science 2004;303:1007-1010.
19. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006;224:213-232.
20. Martin K,Weiss S, Metharom P, Schmeckpeper J, Hynes B, O'Sullivan J et al. Thrombin stimulates smooth muscle cell differentiation from peripheral blood mononuclear cells via protease-activated receptor-1, RhoA, and myocardin. Circ Res 2009;105: 214-218.
21. Yang PY, Rui YC. Intercellular adhesion molecule-1 and vascular endothelial growth factor expression kinetics in macrophage-derived foam cells. Life Sci 2003;74: 471-480.
22. Manders EMM, Verbeek FJ, Aten JA. Measurement of co-localization of objects in dual-colour images. J Micros 1993;196:375-382.
23. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol 2010;30:1282-1292.
24. Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med 2002;8:1249-1256.
25. Allahverdian S, Pannu PS, Francis GA. Contribution of monocyte-derived macrophages and smooth muscle cells to arterial foam cell formation. Cardiovasc Res 2012;95:165-172.
26. Pitas RE. Expression of the acetyl low density lipoprotein receptor by rabbit fibroblasts and smooth muscle cells. Up-regulation by phorbol esters. J Biol Chem 1990; 265:12722-12727.
27. Frontini MJ, O'Neil C, Sawyez C, Chan BM, Huff MW, Pickering JG. Lipid incorporation inhibits Src-dependent assembly of fibronectin and type I collagen by vascular smooth muscle cells. Circ Res 2009;104:832-841.
28. Roda-Navarro P, Reyburn HT. Intercellular protein transfer at the NK cell immune synapse: mechanisms and physiological significance. FASEB J 2007;21:1636-1646.
29. Liu D, Bryceson YT, Meckel T, Vasiliver-Shamis G, Dustin ML, Long EO. Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 2009;31:99-109.
30. Hergenreider E, Heydt S, Treguer K, Boettger T, Horrevoets AJ, Zeiher AM et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012;14:249-256.
31. Somsel RJ, Wandinger-Ness A. Rab GTPases coordinate endocytosis. J Cell Sci 2000; 113(Pt 2):183-192.
32. Piehl M, Lehmann C, Gumpert A, Denizot JP, Segretain D, Falk MM. Internalization of large double-membrane intercellular vesicles by a clathrin-dependent endocytic process. Mol Biol Cell 2007;18:337-347.
33. Gerdes HH, Carvalho RN. Intercellular transfer mediated by tunneling nanotubes. Curr Opin Cell Biol 2008;20:470-475.
34. Garcia-Arguinzonis M, Padro T, Lugano R, Llorente-Cortes V, Badimon L. Lowdensity lipoproteins induce heat shock protein 27 dephosphorylation, oligomerization, and subcellular relocalization in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2010;30:1212-1219.
35. Vijayagopal P, Glancy DL. Macrophages stimulate cholesteryl ester accumulation in cocultured smooth muscle cells incubated with lipoprotein-proteoglycan complex. Arterioscler Thromb Vasc Biol 1996;16:1112-1121.
36. Li H, Freeman MW, Libby P. Regulation of smooth muscle cell scavenger receptor expression in vivo by atherogenic diets and in vitro by cytokines. J Clin Invest 1995; 95:122-133.
37. Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW. Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci USA 2009;106:17615-17622.