Role of extracellular vesicles in de novo mineralization: An additional novel mechanism of cardiovascular calcification

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 8, 2013, Pages 1753-1758

  New, Sophie E P ^a   Aikawa, Elena ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Atherosclerosis; Calcification; Extracellular vesicles; Inflammation; Macrophages; Rupture; Valve disease

Indexed keywords

ANNEXIN; CD63 ANTIGEN; CD9 ANTIGEN; HISTONE; HYDROXYAPATITE; LIPOCORTIN 2; LIPOCORTIN 5; PHOSPHATIDYLSERINE; PROTEINASE; TETRASPANIN;

ADAPTIVE IMMUNITY; ARTERY CALCIFICATION; ATHEROSCLEROSIS; BIOMINERALIZATION; BLOOD VESSEL CALCIFICATION; BONE MINERALIZATION; CALCIFICATION; CARDIOVASCULAR CALCIFICATION; CARDIOVASCULAR RISK; CELL MEMBRANE; CELL TRANSDIFFERENTIATION; CELL VACUOLE; CELLULAR DISTRIBUTION; CRYSTALLIZATION; DISEASE CLASSIFICATION; ENDOSOME; ENDOTHELIUM CELL; ERYTHROCYTE; EXOSOME; EXTRACELLULAR CALCIUM; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; HEART INFARCTION; HUMAN; LEUKOCYTE; LIPID COMPOSITION; LUNG CIRCULATION; MACROPHAGE; MEMBRANE MICROPARTICLE; MEMBRANE VESICLE; MOLECULAR IMAGING; MULTIVESICULAR BODY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PULMONARY HYPERTENSION; REVIEW; SMOOTH MUSCLE FIBER; THROMBOEMBOLISM; THROMBOSIS; X RAY DIFFRACTION;

ATHEROSCLEROSIS; CALCIFICATION; EXTRACELLULAR VESICLES; INFLAMMATION; MACROPHAGES; RUPTURE; VALVE DISEASE;

ANIMALS; CALCIFICATION, PHYSIOLOGIC; CALCINOSIS; CELL-DERIVED MICROPARTICLES; EXTRACELLULAR SPACE; HEART DISEASES; HUMANS; OSTEOGENESIS;

EID: 84881024473     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300128     Document Type: Review

References (56)

1. Johnson RC, Leopold JA, Loscalzo J. Vascular calcification: pathobiological mechanisms and clinical implications. Circ Res. 2006;99: 1044-1059.
2. Bobryshev YV, Killingsworth MC, Lord RS, Grabs AJ. Matrix vesicles in the fibrous cap of atherosclerotic plaque: possible contribution to plaque rupture. J Cell Mol Med. 2008;12(5B): 2073-2082.
3. Vengrenyuk Y, Carlier S, Xanthos S, Cardoso L, Ganatos P, Virmani R, Einav S, Gilchrist L, Weinbaum S. A hypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc Natl Acad Sci U S A. 2006;103: 14678-14683.
4. Vengrenyuk Y, Kaplan TJ, Cardoso L, Randolph GJ, Weinbaum S. Computational stress analysis of atherosclerotic plaques in ApoE knockout mice. Ann Biomed Eng. 2010;38: 738-747.
5. Wenk JF. Numerical modeling of stress in stenotic arteries with microcalcifications: a parameter sensitivity study. J Biomech Eng. 2011;133:014503.
6. Boström K, Watson KE, Stanford WP, Demer LL. Atherosclerotic calcification: relation to developmental osteogenesis. Am J Cardiol. 1995;75:88B-91B.
7. Steitz SA, Speer MY, Curinga G, Yang HY, Haynes P, Aebersold R, Schinke T, Karsenty G, Giachelli CM. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ Res. 2001;89: 1147-1154.
8. Towler DA, Shao JS, Cheng SL, Pingsterhaus JM, Loewy AP. Osteogenic regulation of vascular calcification. Ann N Y Acad Sci. 2006;1068: 327-333.
9. Anderson HC. Mechanisms of pathologic calcification. Rheum Dis Clin North Am. 1988;14: 303-319.
10. Zhou H, Pisitkun T, Aponte A, Yuen PS, Hoffert JD, Yasuda H, Hu X, Chawla L, Shen RF, Knepper MA, Star RA. Exosomal Fetuin-A identified by proteomics: a novel urinary biomarker for detecting acute kidney injury. Kidney Int. 2006;70: 1847-1857.
11. Delcayre A, Le Pecq JB. Exosomes as novel therapeutic nanodevices. Curr Opin Mol Ther. 2006;8: 31-38.
12. Lee Y, El Andaloussi S, Wood MJ. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet. 2012;21(R1):R125-R134.
13. Chen NX, O'Neill KD, Chen X, Moe SM. Annexin-mediated matrix vesicle calcification in vascular smooth muscle cells. J Bone Miner Res. 2008;23: 1798-1805.
14. Kapustin AN, Davies JD, Reynolds JL, McNair R, Jones GT, Sidibe A, Schurgers LJ, Skepper JN, Proudfoot D, Mayr M, Shanahan CM. Calcium regulates key components of vascular smooth muscle cell-derived matrix vesicles to enhance mineralization. Circ Res. 2011;109:e1-e12.
15. New SE, Goettsch C, Aikawa M, Marchini JF, Shibasaki M, Yabusaki K, Libby P, Shanahan CM, Croce K, Aikawa E. Macrophage-derived matrix vesicles: an alternative novel mechanism for microcalcification in atherosclerotic plaques. Circ Res. 2013;PMID:23616621.
16. Anderson HC. Electron microscopic studies of induced cartilage development and calcification. J Cell Biol. 1967;35: 81-101.
17. Bonucci E. Fine structure of early cartilage calcification. J Ultrastruct Res. 1967;20: 33-50.
18. Anderson HC. Matrix vesicles and calcification. Curr Rheumatol Rep. 2003;5: 222-226.
19. Anderson HC, Mulhall D, Garimella R. Role of extracellular membrane vesicles in the pathogenesis of various diseases, including cancer, renal diseases, atherosclerosis, and arthritis. Lab Invest. 2010;90: 1549-1557.
20. Kalra H, Simpson RJ, Ji H, et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 2012;10:e1001450.
21. van der Pol E, Böing AN, Harrison P, Sturk A, Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev. 2012;64: 676-705.
22. Chargaff E, West R. The biological significance of the thromboplastic protein of blood. J Biol Chem. 1946;166: 189-197.
23. Furie B, Furie BC. Mechanisms of thrombus formation. N Engl J Med. 2008;359: 938-949.
24. Hendrix A, Westbroek W, Bracke M, De Wever O. An ex(o)citing machinery for invasive tumor growth. Cancer Res. 2010;70: 9533-9537.
25. Amabile N, Heiss C, Real WM, Minasi P, McGlothlin D, Rame EJ, Grossman W, De Marco T, Yeghiazarians Y. Circulating endothelial microparticle levels predict hemodynamic severity of pulmonary hypertension. Am J Respir Crit Care Med. 2008;177: 1268-1275.
26. Goettsch C, Hutcheson JD, Aikawa E. MicroRNA in cardiovascular calcification: focus on targets and extracellular vesicle delivery mechanisms. Circ Res. 2013;112: 1073-1084.
27. Duer MJ, Friscić T, Proudfoot D, Reid DG, Schoppet M, Shanahan CM, Skepper JN, Wise ER. Mineral surface in calcified plaque is like that of bone: further evidence for regulated mineralization. Arterioscler Thromb Vasc Biol. 2008;28: 2030-2034.
28. Proudfoot D, Skepper JN, Hegyi L, Farzaneh-Far A, Shanahan CM, Weissberg PL. The role of apoptosis in the initiation of vascular calcification. Z Kardiol. 2001;90: 43-46.
29. Reynolds JL, Joannides AJ, Skepper JN, McNair R, Schurgers LJ, Proudfoot D, Jahnen-Dechent W, Weissberg PL, Shanahan CM. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: a potential mechanism for accelerated vascular calcification in ESRD. J Am Soc Nephrol. 2004;15: 2857-2867.
30. New SE, Aikawa E. Molecular imaging insights into early inflammatory stages of arterial and aortic valve calcification. Circ Res. 2011;108: 1381-1391.
31. Abedin M, Tintut Y, Demer LL. Vascular calcification: mechanisms and clinical ramifications. Arterioscler Thromb Vasc Biol. 2004;24: 1161-1170.
32. Tintut Y, Patel J, Parhami F, Demer LL. Tumor necrosis factor-alpha promotes in vitro calcification of vascular cells via the cAMP pathway. Circulation. 2000;102: 2636-2642.
33. Aikawa E, Nahrendorf M, Figueiredo JL, Swirski FK, Shtatland T, Kohler RH, Jaffer FA, Aikawa M, Weissleder R. Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation. 2007;116: 2841-2850.
34. Kim KM. Calcification of matrix vesicles in human aortic valve and aortic media. Fed Proc. 1976;35: 156-162.
35. Tanimura A, McGregor DH, Anderson HC. Matrix vesicles in atherosclerotic calcification. Proc Soc Exp Biol Med. 1983;172: 173-177.
36. Aikawa M, Libby P. The vulnerable atherosclerotic plaque: pathogenesis and therapeutic approach. Cardiovasc Pathol. 2004;13: 125-138.
37. Goodman WG, London G, Amann K, Block GA, Giachelli C, Hruska KA, Ketteler M, Levin A, Massy Z, McCarron DA, Raggi P, Shanahan CM, Yorioka N; Vascular Calcification Work Group. Vascular calcification in chronic kidney disease. Am J Kidney Dis. 2004;43: 572-579.
38. Aikawa E, Aikawa M, Libby P, Figueiredo JL, Rusanescu G, Iwamoto Y, Fukuda D, Kohler RH, Shi GP, Jaffer FA, Weissleder R. Arterial and aortic valve calcification abolished by elastolytic cathepsin S deficiency in chronic renal disease. Circulation. 2009;119: 1785-1794.
39. Bobryshev YV, Killingsworth MC, Huynh TG, Lord RS, Grabs AJ, Valenzuela SM. Are calcifying matrix vesicles in atherosclerotic lesions of cellular origin? Basic Res Cardiol. 2007;102: 133-143.
40. Golub EE. Role of matrix vesicles in biomineralization. Biochim Biophys Acta. 2009;1790: 1592-1598.
41. Fedde KN. Human osteosarcoma cells spontaneously release matrixvesicle- like structures with the capacity to mineralize. Bone Miner. 1992;17: 145-151.
42. Majeska RJ, Wuthier RE. Studies on matrix vesicles isolated from chick epiphyseal cartilage. Association of pyrophosphatase and ATPase activities with alkaline phosphatase. Biochim Biophys Acta. 1975;391: 51-60.
43. Balcerzak M, Malinowska A, Thouverey C, Sekrecka A, Dadlez M, Buchet R, Pikula S. Proteome analysis of matrix vesicles isolated from femurs of chicken embryo. Proteomics. 2008;8: 192-205.
44. Wuthier RE, Lipscomb GF. Matrix vesicles: structure, composition, formation and function in calcification. Front Biosci. 2012;17: 2812-2902.
45. Genge BR, Wu LN, Wuthier RE. Identification of phospholipid-dependent calcium-binding proteins as constituents of matrix vesicles. J Biol Chem. 1989;264: 10917-10921.
46. Cotmore JM, Nichols G Jr, Wuthier RE. Phospholipid-calcium phosphate complex: enhanced calcium migration in the presence of phosphate. Science. 1971;172: 1339-1341.
47. Balcerzak M, Hamade E, Zhang L, Pikula S, Azzar G, Radisson J, Bandorowicz-Pikula J, Buchet R. The roles of annexins and alkaline phosphatase in mineralization process. Acta Biochim Pol. 2003;50: 1019-1038.
48. Genge BR, Wu LN, Wuthier RE. Kinetic analysis of mineral formation during in vitro modeling of matrix vesicle mineralization: effect of annexin A5, phosphatidylserine, and type II collagen. Anal Biochem. 2007;367: 159-166.
49. Grskovic I, Kutsch A, Frie C, et al. Depletion of annexin A5, annexin A6, and collagen X causes no gross changes in matrix vesicle-mediated mineralization, but lack of collagen X affects hematopoiesis and the Th1/Th2 response. J Bone Miner Res. 2012;27: 2399-2412.
50. Neven E, De Schutter TM, De Broe ME, D'Haese PC. Cell biological and physicochemical aspects of arterial calcification. Kidney Int. 2011;79: 1166-1177.
51. Warner GP, Hubbard HL, Lloyd GC, Wuthier RE. 32Pi- and 45Ca-metabolism by matrix vesicle-enriched microsomes prepared from chicken epiphyseal cartilage by isosmotic Percoll density-gradient fractionation. Calcif Tissue Int. 1983;35: 327-338.
52. Anderson HC, Garimella R, Tague SE. The role of matrix vesicles in growth plate development and biomineralization. Front Biosci. 2005;10: 822-837.
53. Anderson HC, Sipe JB, Hessle L, Dhanyamraju R, Atti E, Camacho NP, Millan JL. Impaired calcification around matrix vesicles of growth plate and bone in alkaline phosphatase-deficient mice. J Am Pathol. 2004;164: 841-847.
54. Wu LN, Genge BR, Lloyd GC, Wuthier RE. Collagen-binding proteins in collagenase-released matrix vesicles from cartilage. Interaction between matrix vesicle proteins and different types of collagen. J Biol Chem. 1991;266: 1195-1203.
55. Khan SR, Rodriguez DE, Gower LB, Monga M. Association of Randall plaque with collagen fibers and membrane vesicles. J Urol. 2012;187: 1094-1100.
56. Nadra I, Mason JC, Philippidis P, Florey O, Smythe CD, McCarthy GM, Landis RC, Haskard DO. Proinflammatory activation of macrophages by basic calcium phosphate crystals via protein kinase C and MAP kinase pathways: a vicious cycle of inflammation and arterial calcification? Circ Res. 2005;96: 1248-1256.