Matrix vesicles: Are they anchored exosomes?

Bone

Volumn 79, Issue , 2015, Pages 29-36

  Shapiro, Irving M ^a   Landis, William J ^b   Risbud, Makarand V ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b University of Akron   (United States)

Author keywords

Chondrocyte; Exosome; Growth plate; Matrix vesicle; Mineralization; Osteoblast

Indexed keywords

CELL PROTEIN; LIPID;

BIOGENESIS; BONE MINERALIZATION; CELL COMMUNICATION; ENCHONDRAL OSSIFICATION; EXOSOME; GROWTH PLATE; HUMAN; LIPID COMPOSITION; MATRIX VESICLE; MEMBRANE MICROPARTICLE; NONHUMAN; PARTICLE SIZE; PROTEIN ANALYSIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE; ANIMAL; BONE; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; EXOSOMES; EXTRACELLULAR VESICLES; HUMANS;

EID: 84930681731     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.05.013     Document Type: Review

References (74)

1. Bonucci E. Fine structure of early cartilage calcification. J Ultrastruct Res 1967, 20:33-50.
2. Anderson H.C., Garimella R., Tague S.E. The role of matrix vesicles in growth plate development and biomineralization. Front Biosci 2005, 10:822-837.
3. Wuthier R.E., Lipscomb G.F. Matrix vesicles: structure, composition, formation and function in calcification. Front Biosci (Landmark Ed) 2011, 16:2812-2902.
4. Stratmann U., Schaarschmidt K., Wiesmann H.P., Plate U., Hohling H.J. Mineralization during matrix-vesicle-mediated mantle dentine formation in molars of albino rats: a microanalytical and ultrastructural study. Cell Tissue Res 1996, 284:223-230.
5. Landis W.J., Hodgens K.J., McKee M.D., Nanci A., Song M.J., Kiyonaga S., et al. Extracellular vesicles of calcifying turkey leg tendon characterized by immunocytochemistry and high voltage electron microscopic tomography and 3-D graphic image reconstruction. Bone Miner 1992, 17:237-241.
6. Hsu H.H., Camacho N.P., Sun F., Tawfik O., Aono H. Isolation of calcifiable vesicles from aortas of rabbits fed with high cholesterol diets. Atherosclerosis 2000, 153:337-348.
7. Deutsch D., Bab I., Mulrad A., Sela J. Purification and further characterization of isolated matrix vesicles from rat alveolar bone. Metab Bone Dis Relat Res 1981, 3:209-214.
8. Colombo M., Raposo G., Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014, 30:255-289.
9. Gebauer D., Kellermeier M., Gale J.D., Bergstrom L., Colfen H. Pre-nucleation clusters as solute precursors in crystallisation. Chem Soc Rev 2014, 43:2348-2371.
10. Anderson H.C., 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.
11. Kato T., Miyaki S., Ishitobi H., Nakamura Y., Nakasa T., Lotz M.K., et al. Exosomes from IL-1beta stimulated synovial fibroblasts induce osteoarthritic changes in articular chondrocytes. Arthritis Res Ther 2014, 16:R163.
12. Rosenthal A.K., Gohr C.M., Ninomiya J., Wakim B.T. Proteomic analysis of articular cartilage vesicles from normal and osteoarthritic cartilage. Arthritis Rheum 2011, 63:401-411.
13. Hale J.E., Wuthier R.E. The mechanism of matrix vesicle formation. Studies on the composition of chondrocyte microvilli and on the effects of microfilament-perturbing agents on cellular vesiculation. J Biol Chem 1987, 262:1916-1925.
14. Thouverey C., Malinowska A., Balcerzak M., Strzelecka-Kiliszek A., Buchet R., Dadlez M., et al. Proteomic characterization of biogenesis and functions of matrix vesicles released from mineralizing human osteoblast-like cells. J Proteomics 2011, 74:1123-1134.
15. Nollet M., Santucci-Darmanin S., Breuil V., Al-Sahlanee R., Cros C., Topi M., et al. Autophagy in osteoblasts is involved in mineralization and bone homeostasis. Autophagy 2014, 10:1965-1977.
16. Hoshi K., Ozawa H. Matrix vesicle calcification in bones of adult rats. Calcif Tissue Int 2000, 66:430-434.
17. Golub E.E., Schattschneider S.C., Berthold P., Burke A., Shapiro I.M. Induction of chondrocyte vesiculation in vitro. J Biol Chem 1983, 258:616-621.
18. Kirsch T. Determinants of pathologic mineralization. Crit Rev Eukaryot Gene Expr 2008, 18:1-9.
19. Akisaka T., Gay C.V. The plasma membrane and matrix vesicles of mouse growth plate chondrocytes during differentiation as revealed in freeze-fracture replicas. Am J Anat 1985, 173:269-286.
20. Kanabe S., Hsu H.H., Cecil R.N., Anderson H.C. Electron microscopic localization of adenosine triphosphate (ATP)-hydrolyzing activity in isolated matrix vesicles and reconstituted vesicles from calf cartilage. J Histochem Cytochem 1983, 31:462-470.
21. Borg T.K., Runyan R., Wuthier R.E. A freeze-fracture study of avian epiphyseal cartilage differentiation. Anat Rec 1981, 199:449-457.
22. Thouverey C., Strzelecka-Kiliszek A., Balcerzak M., Buchet R., Pikula S. Matrix vesicles originate from apical membrane microvilli of mineralizing osteoblast-like Saos-2 cells. J Cell Biochem 2009, 106:127-138.
23. Thyberg J., Nilsson S., Friberg U. Electron microscopic and enzyme cytochemical studies on the guinea pig metaphysis with special reference to the lysosomal system of different cell types. Cell Tissue Res 1975, 156:273-299.
24. Xiao Z., Camalier C.E., Nagashima K., Chan K.C., Lucas D.A., de la Cruz M.J., et al. Analysis of the extracellular matrix vesicle proteome in mineralizing osteoblasts. J Cell Physiol 2007, 210:325-335.
25. Yang L., Zhang Y., Cui F.Z. Two types of mineral-related matrix vesicles in the bone mineralization of zebrafish. Biomed Mater 2007, 2:21-25.
26. Wuthier R.E. Lipid composition of isolated epiphyseal cartilage cells, membranes and matrix vesicles. Biochim Biophys Acta 1975, 409:128-143.
27. Wuthier R.E. Lipids of matrix vesicles. Fed Proc 1976, 35:117-121.
28. Kirsch T., Nah H.D., Demuth D.R., Harrison G., Golub E.E., Adams S.L., et al. Annexin V-mediated calcium flux across membranes is dependent on the lipid composition: implications for cartilage mineralization. Biochemistry 1997, 36:3359-3367.
29. Laulagnier K., Motta C., Hamdi S., Roy S., Fauvelle F., Pageaux J.F., et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J 2004, 380:161-171.
30. Balcerzak M., Malinowska A., Thouverey C., Sekrecka A., Dadlez M., Buchet R., et al. Proteome analysis of matrix vesicles isolated from femurs of chicken embryo. Proteomics 2008, 8:192-205.
31. Lucero H.A., Robbins P.W. Lipid rafts-protein association and the regulation of protein activity. Arch Biochem Biophys 2004, 426:208-224.
32. Golub E.E. Biomineralization and matrix vesicles in biology and pathology. Semin Immunopathol 2011, 33:409-417.
33. Millán J.L. The role of phosphatases in the initiation of skeletal mineralization. Calcif Tissue Int. 2013, 93:299-306.
34. Maeda S., Dean D.D., Gomez R., Schwartz Z., Boyan B.D. The first stage of transforming growth factor beta1 activation is release of the large latent complex from the extracellular matrix of growth plate chondrocytes by matrix vesicle stromelysin-1 (MMP-3). Calcif Tissue Int 2002, 70:54-65.
35. Simpson R.J., Jensen S.S., Lim J.W. Proteomic profiling of exosomes: current perspectives. Proteomics 2008, 8:4083-4099.
36. Xiao Z., Conrads T.P., Beck G.R., Veenstra T.D. Analysis of the extracellular matrix and secreted vesicle proteomes by mass spectrometry. Methods Mol Biol 2008, 428:231-244.
37. Kitt K.N., Hernandez-Deviez D., Ballantyne S.D., Spiliotis E.T., Casanova J.E., Wilson J.M. Rab14 regulates apical targeting in polarized epithelial cells. Traffic 2008, 9:1218-1231.
38. Vonderheit A., Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 2005, 3:e233.
39. Simpson J.C., Griffiths G., Wessling-Resnick M., Fransen J.A., Bennett H., Jones A.T. A role for the small GTPase Rab21 in the early endocytic pathway. J Cell Sci 2004, 117:6297-6311.
40. Théry C., Regnault A., Garin J., Wolfers J., Zitvogel L., Ricciardi-Castagnoli P., et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol 1999, 147:599-610.
41. Clayton A., Turkes A., Dewitt S., Steadman R., Mason M.D., Hallett M.B. Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J 2004, 18:977-979.
42. Zhou X., Cui Y., Luan J., Zhang G., Zhang X., Han J. Label-free quantification proteomics reveals novel calcium binding proteins in matrix vesicles isolated from mineralizing Saos-2 cells. Biosci Trends 2013, 7:144-151.
43. Otsuka G., Kubo T., Imanishi J., Hirasawa Y. Expression of heat-shock-proteins in the differentiation process of chondrocytes. Nihon Geka Hokan 1996, 65:39-48.
44. Mulcahy L.A., Pink R.C., Carter D.R. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 2014, 3:24641.
45. Subra C., Grand D., Laulagnier K., Stella A., Lambeau G., Paillasse M., et al. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J Lipid Res 2010, 51:2105-2120.
46. Zhou Z. New phosphatidylserine receptors: clearance of apoptotic cells and more. Dev Cell 2007, 13:759-760.
47. Tian T., Zhu Y.L., Zhou Y.Y., Liang G.F., Wang Y.Y., Hu F.H., et al. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem 2014, 289:22258-22267.
48. Al-Nedawi K., Meehan B., Micallef J., Lhotak V., May L., Guha A., et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008, 10:619-624.
49. Andrade A.C., Nilsson O., Barnes K.M., Baron J. Wnt gene expression in the post-natal growth plate: regulation with chondrocyte differentiation. Bone 2007, 40:1361-1369.
50. Takada R., Satomi Y., Kurata T., Ueno N., Norioka S., Kondoh H., et al. Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Dev Cell 2006, 11:791-801.
51. Koles K., Budnik V. Exosomes go with the Wnt. Cell Logist 2012, 2:169-173.
52. Gross J.C., Chaudhary V., Bartscherer K., Boutros M. Active Wnt proteins are secreted on exosomes. Nat Cell Biol 2012, 14:1036-1045.
53. Ruchon A.F., Marcinkiewicz M., Ellefsen K., Basak A., Aubin J., Crine P., et al. Cellular localization of neprilysin in mouse bone tissue and putative role in hydrolysis of osteogenic peptides. J Bone Miner Res 2000, 15:1266-1274.
54. Ogawa Y., Taketomi Y., Murakami M., Tsujimoto M., Yanoshita R. Small RNA transcriptomes of two types of exosomes in human whole saliva determined by next generation sequencing. Biol Pharm Bull 2013, 36:66-75.
55. Papaioannou G., Inloes J.B., Nakamura Y., Paltrinieri E., Kobayashi T. let-7 and miR-140 microRNAs coordinately regulate skeletal development. Proc Natl Acad Sci U S A 2013, 110:E3291-E3300.
56. Nakamura Y., Inloes J.B., Katagiri T., Kobayashi T. Chondrocyte-specific microRNA-140 regulates endochondral bone development and targets Dnpep to modulate bone morphogenetic protein signaling. Mol Cell Biol 2011, 31:3019-3028.
57. Sauer G.R., Wuthier R.E. Fourier transform infrared characterization of mineral phases formed during induction of mineralization by collagenase-released matrix vesicles in vitro. J Biol Chem 1988, 263:13718-13724.
58. Mahamid J., Addadi L., Weiner S. Crystallization pathways in bone. Cells Tissues Organs 2011, 194:92-97.
59. Kirsch T., Ishikawa Y., Mwale F., Wuthier R.E. Roles of the nucleational core complex and collagens (types II and X) in calcification of growth plate cartilage matrix vesicles. J Biol Chem 1994, 269:20103-20109.
60. Kirsch T. Annexins - their role in cartilage mineralization. Front Biosci 2005, 10:576-581.
61. Wu L.N., Genge B.R., Sauer G.R., Wuthier R.E. Characterization and reconstitution of the nucleational complex responsible for mineral formation by growth plate cartilage matrix vesicles. Connect Tissue Res 1996, 35(1-4):309-315.
62. Habraken W.J., Tao J., Brylka L.J., Friedrich H., Bertinetti L., Schenk A.S., et al. Ion-association complexes unite classical and non-classical theories for the biomimetic nucleation of calcium phosphate. Nat Commun 2013, 4:1507.
63. Nudelman F., Pieterse K., George A., Bomans P.H., Friedrich H., Brylka L.J., et al. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater 2010, 9:1004-1009.
64. Gay C., Schraer H. Frozen thin-sections of rapidly forming bone: bone cell ultrastructure. Calcif Tissue Res 1975, 19:39-49.
65. Rohde M., Mayer H. Exocytotic process as a novel model for mineralization by osteoblasts in vitro and in vivo determined by electron microscopic analysis. Calcif Tissue Int 2007, 80:323-336.
66. Mahamid J., Sharir A., Gur D., Zelzer E., Addadi L., Weiner S. Bone mineralization proceeds through intracellular calcium phosphate loaded vesicles: a cryo-electron microscopy study. J Struct Biol 2011, 174:527-535.
67. Boonrungsiman S., Gentleman E., Carzaniga R., Evans N.D., McComb D.W., Porter A.E., et al. The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc Natl Acad Sci U S A 2012, 109:14170-14175.
68. Shapiro I.M., Srinivas V. Metabolic consideration of epiphyseal growth: survival responses in a taxing environment. Bone 2007, 40:561-567.
69. Dai X.Y., Zhao M.M., Cai Y., Guan Q.C., Zhao Y., Guan Y., et al. Phosphate-induced autophagy counteracts vascular calcification by reducing matrix vesicle release. Kidney Int 2013, 83:1042-1051.
70. Manjithaya R., Subramani S. Autophagy: a broad role in unconventional protein secretion?. Trends Cell Biol 2011, 21:67-73.
71. Shapiro I.M., Layfield R., Lotz M., Settembre C., Whitehouse C. Boning up on autophagy: the role of autophagy in skeletal biology. Autophagy 2014, 10:7-19.
72. Fader C.M., Colombo M.I. Multivesicular bodies and autophagy in erythrocyte maturation. Autophagy 2006, 2:122-125.
73. Amizuka N., Hasegawa T., Oda K., Luiz de Freitas P.H., Hoshi K., Li M., et al. Histology of epiphyseal cartilage calcification and endochondral ossification. Front Biosci (Elite Ed) 2012, 4:2085-2100.
74. Xiao Z., Blonder J., Zhou M., Veenstra T.D. Proteomic analysis of extracellular matrix and vesicles. J Proteomics 2009, 72:34-45.