Cholesterol crystallization in human atherosclerosis is triggered in smooth muscle cells during the transition from fatty streak to fibroatheroma

Journal of Pathology

Volumn 241, Issue 5, 2017, Pages 671-682

  Ho Tin Noé, Benoît ^a   Vo, Sophie ^a   Bayles, Richard ^a   Ferrière, Stephen ^a   Ladjal, Hayette ^a   Toumi, Sondes ^a   Deschildre, Catherine ^a   Ollivier, Véronique ^a   Michel, Jean Baptiste ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

atheromatous disease; atherosclerosis; autophagy; cholesterol; cholesterol crystals; fatty streak; fibrolipidic lesion; smooth muscle cells; type I collagen

Indexed keywords

CHOLESTEROL; COLLAGEN TYPE 1; FATTY ACID; SEQUESTOSOME 1;

AORTA ATHEROSCLEROSIS; AORTIC TISSUE; APOPTOSIS; ARTICLE; ATHEROMA; AUTOPHAGY; CHOLESTEROL ESTERIFICATION; CONTROLLED STUDY; CRYSTALLIZATION; FIBROATHEROMA; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOLOGY; IN VITRO STUDY; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE CELL; AORTA; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CHEMISTRY; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; MACROPHAGE; METABOLISM; PATHOLOGY;

AORTA; ATHEROSCLEROSIS; AUTOPHAGY; CHOLESTEROL; COLLAGEN TYPE I; CRYSTALLIZATION; HUMANS; IMMUNOHISTOCHEMISTRY; LIPID METABOLISM; MACROPHAGES; MYOCYTES, SMOOTH MUSCLE; PLAQUE, ATHEROSCLEROTIC;

EID: 85014625653     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4873     Document Type: Article

References (48)

1. Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 2007; 116: 1832–1844.
2. Anitschkow N, Chalatow S. Ueber experimentelle Choleserinsteatose und ihre Bedeutung fur die Entstehung einiger pathologischer Prozesse. Zentralbl Allg Pathol Pathol Anat 1913; 24: 1-9.
3. Katz SS, Shipley GG, Small DM. Physical chemistry of the lipids of human atherosclerotic lesions. Demonstration of a lesion intermediate between fatty streaks and advanced plaques. J Clin Invest 1976; 58: 200-211.
4. Bocan TM, Guyton JR. Human aortic fibrolipid lesions. Progenitor lesions for fibrous plaques, exhibiting early formation of the cholesterol-rich core. Am J Pathol 1985; 120: 193-206.
5. Lang PD, Insull W Jr. Lipid droplets in atherosclerotic fatty streaks of human aorta. J Clin Invest 1970; 49: 1479-1488.
6. Bogren H, Larsson K. An X-ray-diffraction study of crystalline cholesterol in some pathological deposits in man. Biochim Biophys Acta 1963; 75: 65-69.
7. Stary HC, Chandler AB, Dinsmore RE, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 1995; 15: 1512-1531.
8. Abela GS. Cholesterol crystals piercing the arterial plaque and intima trigger local and systemic inflammation. J Clin Lipidol 2010; 4: 156-164.
9. Abela GS, Aziz K. Cholesterol crystals rupture biological membranes and human plaques during acute cardiovascular events – a novel insight into plaque rupture by scanning electron microscopy. Scanning 2006; 28: 1-10.
10. Abela GS, Aziz K, Vedre A, et al. Effect of cholesterol crystals on plaques and intima in arteries of patients with acute coronary and cerebrovascular syndromes. Am J Cardiol 2009; 103: 959-968.
11. Duewell P, Kono H, Rayner KJ, et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010; 464: 1357-1361.
12. Fernandez-Ortiz A, Badimon JJ, Falk E, et al. Characterization of the relative thrombogenicity of atherosclerotic plaque components: implications for consequences of plaque rupture. J Am Coll Cardiol 1994; 23: 1562-1569.
13. Janoudi A, Shamoun FE, Kalavakunta JK, et al. Cholesterol crystal induced arterial inflammation and destabilization of atherosclerotic plaque. Eur Heart J 2016; 37: 1959–1967.
14. North BE, Katz SS, Small DM. The dissolution of cholesterol monohydrate crystals in atherosclerotic plaque lipids. Atherosclerosis 1978; 30: 211-217.
15. Tangirala RK, Jerome WG, Jones NL, et al. Formation of cholesterol monohydrate crystals in macrophage-derived foam cells. J Lipid Res 1994; 35: 93-104.
16. Hawi SR, Nithipatikom K, Wohlfeil ER, et al. Raman microspectroscopy of intracellular cholesterol crystals in cultured bovine coronary artery endothelial cells. J Lipid Res 1997; 38: 1591-1597.
17. Vedre A, Pathak DR, Crimp M, et al. Physical factors that trigger cholesterol crystallization leading to plaque rupture. Atherosclerosis 2009; 203: 89-96.
18. Ho-Tin-Noe B, Le Dall J, Gomez D, et al. Early atheroma-derived agonists of peroxisome proliferator-activated receptor-gamma trigger intramedial angiogenesis in a smooth muscle cell-dependent manner. Circ Res 2011; 109: 1003-1014.
19. Ho-Tin-Noe B, Meilhac O, Rossignol P, et al. Dual effect of apolipoprotein(a) on plasmin(ogen)-induced apoptosis through modulation of cell detachment of adherent cells. Thromb Haemost 2006; 95: 142-150.
20. Hata Y, Insull W Jr. Significance of cholesterol esters as liquid crystal in human atherosclerosis. Jpn Circ J 1973; 37: 269-275.
21. Loomis CR, Shipley GG, Small DM. The phase behavior of hydrated cholesterol. J Lipid Res 1979; 20: 525-535.
22. Bittman R, Fischkoff SA. Fluorescence studies of the binding of the polyene antibiotics filipin 3, amphotericin B, nystatin, and lagosin to cholesterol. Proc Natl Acad Sci U S A 1972; 69: 3795-3799.
23. Abela GS, Shamoun F, Vedre A, et al. The effect of ethanol on cholesterol crystals during tissue preparation for scanning electron microscopy. J Am Coll Cardiol 2012; 59: 93.
24. Llorente-Cortes V, Martinez-Gonzalez J, Badimon L. Esterified cholesterol accumulation induced by aggregated LDL uptake in human vascular smooth muscle cells is reduced by HMG-CoA reductase inhibitors. Arterioscler Thromb Vasc Biol 1998; 18: 738-746.
25. Rajamaki K, Lappalainen J, Oorni K, et al. Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One 2010; 5: e11765.
26. Freigang S, Ampenberger F, Spohn G, et al. Nrf2 is essential for cholesterol crystal-induced inflammasome activation and exacerbation of atherosclerosis. Eur J Immunol 2011; 41: 2040-2051.
27. DiDonato D, Brasaemle DL. Fixation methods for the study of lipid droplets by immunofluorescence microscopy. J Histochem Cytochem 2003; 51: 773-780.
28. Stewart GT. Liquid crystals of lipid in normal and atheromatous tissue. Nature 1959; 183: 873-875.
29. Orekhov AN, Andreeva ER, Mikhailova IA, et al. Cell proliferation in normal and atherosclerotic human aorta: proliferative splash in lipid-rich lesions. Atherosclerosis 1998; 139: 41-48.
30. Bocan TM, Schifani TA, Guyton JR. Ultrastructure of the human aortic fibrolipid lesion. Formation of the atherosclerotic lipid-rich core. Am J Pathol 1986; 123: 413-424.
31. Allahverdian S, Chehroudi AC, McManus BM, et al. Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation 2014; 129: 1551-1559.
32. Nakashima Y, Fujii H, Sumiyoshi S, et al. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol 2007; 27: 1159-1165.
33. Napoli C, D'Armiento FP, Mancini FP, et al. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest 1997; 100: 2680-2690.
34. Otsuka F, Kramer MC, Woudstra P, et al. Natural progression of atherosclerosis from pathologic intimal thickening to late fibroatheroma in human coronary arteries: a pathology study. Atherosclerosis 2015; 241: 772-782.
35. 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.
36. Beranek JT. CD68 is not a macrophage-specific antigen. Ann Rheum Dis 2005; 64: 342-343; author reply 343-344.
37. Vengrenyuk Y, Nishi H, Long X, et al. Cholesterol loading reprograms the microRNA-143/145–myocardin axis to convert aortic smooth muscle cells to a dysfunctional macrophage-like phenotype. Arterioscler Thromb Vasc Biol 2015; 35: 535-546.
38. Shankman LS, Gomez D, Cherepanova OA, et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nature Med 2015; 21: 628-637.
39. Kiyak JH. Cholesterol crystals, smooth muscle cells and new data on the genesis of atherosclerosis. Pol J Pathol 1997; 48: 49-55.
40. Ouimet M, Franklin V, Mak E, et al. Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab 2011; 13: 655-667.
41. Razani B, Feng C, Coleman T, et al. Autophagy links inflammasomes to atherosclerotic progression. Cell Metab 2012; 15: 534-544.
42. Grootaert MO, da Costa Martins PA, Bitsch N, et al. Defective autophagy in vascular smooth muscle cells accelerates senescence and promotes neointima formation and atherogenesis. Autophagy 2015; 11: 2014-2032.
43. Homma S, Troxclair DA, Zieske AW, et al. Histological changes and risk factor associations in type 2 atherosclerotic lesions (fatty streaks) in young adults. Atherosclerosis 2011; 219: 184-190.
44. Feng B, Yao PM, Li Y, et al. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nature Cell Biol 2003; 5: 781-792.
45. Watson KE, Parhami F, Shin V, et al. Fibronectin and collagen I matrixes promote calcification of vascular cells in vitro, whereas collagen IV matrix is inhibitory. Arterioscler Thromb Vasc Biol 1998; 18: 1964-1971.
46. Ahmad PJ, Trcka D, Xue S, et al. Discoidin domain receptor-1 deficiency attenuates atherosclerotic calcification and smooth muscle cell-mediated mineralization. Am J Pathol 2009; 175: 2686-2696.
47. Dai XY, Zhao MM, Cai Y, et al. Phosphate-induced autophagy counteracts vascular calcification by reducing matrix vesicle release. Kidney Int 2013; 83: 1042-1051.
48. Junqueira LC, Cossermelli W, Brentani R. Differential staining of collagens type I, II and III by Sirius Red and polarization microscopy. Arch Histol Jpn 1978; 41: 267-274.