Matrix vesicles from chondrocytes and osteoblasts: Their biogenesis, properties, functions and biomimetic models
Matrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are...
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| Published in | Biochimica et biophysica acta Vol. 1862; no. 3; pp. 532 - 546 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.03.2018
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0304-4165 0006-3002 1872-8006 1878-2434 |
| DOI | 10.1016/j.bbagen.2017.11.005 |
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| Abstract | Matrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are extracellular vesicles of approximately 100–300nm diameter harboring the biochemical machinery needed to induce mineralization.
The review comprehensively delineates our current knowledge of MV biology and highlights open questions aiming to stimulate further research. The review is constructed as a series of questions addressing issues of MVs ranging from their biogenesis and functions, to biomimetic models. It critically evaluates experimental data including their isolation and characterization methods, like lipidomics, proteomics, transmission electron microscopy, atomic force microscopy and proteoliposome models mimicking MVs.
MVs have a relatively well-defined function as initiators of mineralization. They bind to collagen and their composition reflects the composition of lipid rafts. We call attention to the as yet unclear mechanisms leading to the biogenesis of MVs, and how minerals form and when they are formed. We discuss the prospects of employing upcoming experimental models to deepen our understanding of MV-mediated mineralization and mineralization disorders such as the use of reconstituted lipid vesicles, proteoliposomes and, native sample preparations and high-resolution technologies.
MVs have been extensively investigated owing to their roles in skeletal and ectopic mineralization. MVs serve as a model system for lipid raft structures, and for the mechanisms of genesis and release of extracellular vesicles.
Matrix vesicles are extracellular vesicles that bind to collagen and can induce formation of apatitic mineral during physiological and ectopic mineralization. Lipid and protein compositions in matrix vesicles resemble those of lipid rafts. Mechanisms of the biogenesis of matrix vesicles and processes leading to mineral/apatite formation are still unclear. Proteoliposomes can serve as biomimetic models to understand matrix vesicle-mediated mineralization. [Display omitted]
•This review addresses a series of questions about matrix vesicles and biomimetic models for matrix vesicles.•Matrix vesicles are roughly spherical extracellular vesicles of 100–300nm in diameter.•Preparation of hydrated samples is necessary for preserving matrix vesicles in their native state.•Mechanisms of the biogenesis of matrix vesicles are still unclear.•Proteoliposomes can serve as a model to understand matrix vesicle-induced mineralization. |
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| AbstractList | Matrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are extracellular vesicles of approximately 100–300nm diameter harboring the biochemical machinery needed to induce mineralization.The review comprehensively delineates our current knowledge of MV biology and highlights open questions aiming to stimulate further research. The review is constructed as a series of questions addressing issues of MVs ranging from their biogenesis and functions, to biomimetic models. It critically evaluates experimental data including their isolation and characterization methods, like lipidomics, proteomics, transmission electron microscopy, atomic force microscopy and proteoliposome models mimicking MVs.MVs have a relatively well-defined function as initiators of mineralization. They bind to collagen and their composition reflects the composition of lipid rafts. We call attention to the as yet unclear mechanisms leading to the biogenesis of MVs, and how minerals form and when they are formed. We discuss the prospects of employing upcoming experimental models to deepen our understanding of MV-mediated mineralization and mineralization disorders such as the use of reconstituted lipid vesicles, proteoliposomes and, native sample preparations and high-resolution technologies.MVs have been extensively investigated owing to their roles in skeletal and ectopic mineralization. MVs serve as a model system for lipid raft structures, and for the mechanisms of genesis and release of extracellular vesicles. Matrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are extracellular vesicles of approximately 100-300nm diameter harboring the biochemical machinery needed to induce mineralization.BACKGROUNDMatrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are extracellular vesicles of approximately 100-300nm diameter harboring the biochemical machinery needed to induce mineralization.The review comprehensively delineates our current knowledge of MV biology and highlights open questions aiming to stimulate further research. The review is constructed as a series of questions addressing issues of MVs ranging from their biogenesis and functions, to biomimetic models. It critically evaluates experimental data including their isolation and characterization methods, like lipidomics, proteomics, transmission electron microscopy, atomic force microscopy and proteoliposome models mimicking MVs.SCOPE OF THE REVIEWThe review comprehensively delineates our current knowledge of MV biology and highlights open questions aiming to stimulate further research. The review is constructed as a series of questions addressing issues of MVs ranging from their biogenesis and functions, to biomimetic models. It critically evaluates experimental data including their isolation and characterization methods, like lipidomics, proteomics, transmission electron microscopy, atomic force microscopy and proteoliposome models mimicking MVs.MVs have a relatively well-defined function as initiators of mineralization. They bind to collagen and their composition reflects the composition of lipid rafts. We call attention to the as yet unclear mechanisms leading to the biogenesis of MVs, and how minerals form and when they are formed. We discuss the prospects of employing upcoming experimental models to deepen our understanding of MV-mediated mineralization and mineralization disorders such as the use of reconstituted lipid vesicles, proteoliposomes and, native sample preparations and high-resolution technologies.MAJOR CONCLUSIONSMVs have a relatively well-defined function as initiators of mineralization. They bind to collagen and their composition reflects the composition of lipid rafts. We call attention to the as yet unclear mechanisms leading to the biogenesis of MVs, and how minerals form and when they are formed. We discuss the prospects of employing upcoming experimental models to deepen our understanding of MV-mediated mineralization and mineralization disorders such as the use of reconstituted lipid vesicles, proteoliposomes and, native sample preparations and high-resolution technologies.MVs have been extensively investigated owing to their roles in skeletal and ectopic mineralization. MVs serve as a model system for lipid raft structures, and for the mechanisms of genesis and release of extracellular vesicles.GENERAL SIGNIFICANCEMVs have been extensively investigated owing to their roles in skeletal and ectopic mineralization. MVs serve as a model system for lipid raft structures, and for the mechanisms of genesis and release of extracellular vesicles. Matrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are extracellular vesicles of approximately 100-300nm diameter harboring the biochemical machinery needed to induce mineralization. The review comprehensively delineates our current knowledge of MV biology and highlights open questions aiming to stimulate further research. The review is constructed as a series of questions addressing issues of MVs ranging from their biogenesis and functions, to biomimetic models. It critically evaluates experimental data including their isolation and characterization methods, like lipidomics, proteomics, transmission electron microscopy, atomic force microscopy and proteoliposome models mimicking MVs. MVs have a relatively well-defined function as initiators of mineralization. They bind to collagen and their composition reflects the composition of lipid rafts. We call attention to the as yet unclear mechanisms leading to the biogenesis of MVs, and how minerals form and when they are formed. We discuss the prospects of employing upcoming experimental models to deepen our understanding of MV-mediated mineralization and mineralization disorders such as the use of reconstituted lipid vesicles, proteoliposomes and, native sample preparations and high-resolution technologies. MVs have been extensively investigated owing to their roles in skeletal and ectopic mineralization. MVs serve as a model system for lipid raft structures, and for the mechanisms of genesis and release of extracellular vesicles. Matrix vesicles (MVs) are released from hypertrophic chondrocytes and from mature osteoblasts, the cells responsible for endochondral and membranous ossification. Under pathological conditions, they can also be released from cells of non-skeletal tissues such as vascular smooth muscle cells. MVs are extracellular vesicles of approximately 100–300nm diameter harboring the biochemical machinery needed to induce mineralization. The review comprehensively delineates our current knowledge of MV biology and highlights open questions aiming to stimulate further research. The review is constructed as a series of questions addressing issues of MVs ranging from their biogenesis and functions, to biomimetic models. It critically evaluates experimental data including their isolation and characterization methods, like lipidomics, proteomics, transmission electron microscopy, atomic force microscopy and proteoliposome models mimicking MVs. MVs have a relatively well-defined function as initiators of mineralization. They bind to collagen and their composition reflects the composition of lipid rafts. We call attention to the as yet unclear mechanisms leading to the biogenesis of MVs, and how minerals form and when they are formed. We discuss the prospects of employing upcoming experimental models to deepen our understanding of MV-mediated mineralization and mineralization disorders such as the use of reconstituted lipid vesicles, proteoliposomes and, native sample preparations and high-resolution technologies. MVs have been extensively investigated owing to their roles in skeletal and ectopic mineralization. MVs serve as a model system for lipid raft structures, and for the mechanisms of genesis and release of extracellular vesicles. Matrix vesicles are extracellular vesicles that bind to collagen and can induce formation of apatitic mineral during physiological and ectopic mineralization. Lipid and protein compositions in matrix vesicles resemble those of lipid rafts. Mechanisms of the biogenesis of matrix vesicles and processes leading to mineral/apatite formation are still unclear. Proteoliposomes can serve as biomimetic models to understand matrix vesicle-mediated mineralization. [Display omitted] •This review addresses a series of questions about matrix vesicles and biomimetic models for matrix vesicles.•Matrix vesicles are roughly spherical extracellular vesicles of 100–300nm in diameter.•Preparation of hydrated samples is necessary for preserving matrix vesicles in their native state.•Mechanisms of the biogenesis of matrix vesicles are still unclear.•Proteoliposomes can serve as a model to understand matrix vesicle-induced mineralization. |
| Author | Simão, Ana Maria Sper Millán, José Luis Bozycki, Lukasz Buchet, Rene Magne, David Mebarek, Saida Ciancaglini, Pietro Hanein, Dorit Pikula, Joanna Bandorowicz Anderson, Karen L. Strzelecka-Kiliszek, Agnieszka Bottini, Massimo Pikula, Slawomir Volkmann, Niels Bolean, Maytê |
| AuthorAffiliation | 5 INSA Lyon, 69 622 VILLEURBANNE Cedex, France 3 Universite Lyon 1, UFR Chimie Biochimie, 69 622 VILLEURBANNE Cedex, France 4 ICBMS UMR 5246 CNRS, 69 622 VILLEURBANNE Cedex, France 6 CPE Lyon, 69 622 VILLEURBANNE Cedex, France 7 Universite de Lyon, 69 622 VILLEURBANNE Cedex, France 2 Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA 1 University of Rome Tor Vergata, Department of Experimental Medicine and Surgery, 00133 ROMA, Italy 9 Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto –USP, Departamento de Química, 14040-901 RIBEIRÃO PRETO, SP Brasil 8 Nencki Institute of Experimental Biology, Department of Biochemistry, Polish Academy of Sciences, 02-093 WARSAW, Poland |
| AuthorAffiliation_xml | – name: 1 University of Rome Tor Vergata, Department of Experimental Medicine and Surgery, 00133 ROMA, Italy – name: 2 Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA – name: 6 CPE Lyon, 69 622 VILLEURBANNE Cedex, France – name: 4 ICBMS UMR 5246 CNRS, 69 622 VILLEURBANNE Cedex, France – name: 3 Universite Lyon 1, UFR Chimie Biochimie, 69 622 VILLEURBANNE Cedex, France – name: 5 INSA Lyon, 69 622 VILLEURBANNE Cedex, France – name: 8 Nencki Institute of Experimental Biology, Department of Biochemistry, Polish Academy of Sciences, 02-093 WARSAW, Poland – name: 9 Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto –USP, Departamento de Química, 14040-901 RIBEIRÃO PRETO, SP Brasil – name: 7 Universite de Lyon, 69 622 VILLEURBANNE Cedex, France |
| Author_xml | – sequence: 1 givenname: Massimo surname: Bottini fullname: Bottini, Massimo organization: University of Rome Tor Vergata, Department of Experimental Medicine and Surgery, 00133 Roma, Italy – sequence: 2 givenname: Saida surname: Mebarek fullname: Mebarek, Saida organization: Universite Lyon 1, UFR Chimie Biochimie, 69 622 Villeurbanne Cedex, France – sequence: 3 givenname: Karen L. surname: Anderson fullname: Anderson, Karen L. organization: Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA – sequence: 4 givenname: Agnieszka surname: Strzelecka-Kiliszek fullname: Strzelecka-Kiliszek, Agnieszka organization: Nencki Institute of Experimental Biology, Department of Biochemistry, Polish Academy of Sciences, 02-093 Warsaw, Poland – sequence: 5 givenname: Lukasz surname: Bozycki fullname: Bozycki, Lukasz organization: Nencki Institute of Experimental Biology, Department of Biochemistry, Polish Academy of Sciences, 02-093 Warsaw, Poland – sequence: 6 givenname: Ana Maria Sper surname: Simão fullname: Simão, Ana Maria Sper organization: Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, Departamento de Química, 14040-901 Ribeirão Preto, SP, Brazil – sequence: 7 givenname: Maytê surname: Bolean fullname: Bolean, Maytê organization: Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, Departamento de Química, 14040-901 Ribeirão Preto, SP, Brazil – sequence: 8 givenname: Pietro surname: Ciancaglini fullname: Ciancaglini, Pietro organization: Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, Departamento de Química, 14040-901 Ribeirão Preto, SP, Brazil – sequence: 9 givenname: Joanna Bandorowicz surname: Pikula fullname: Pikula, Joanna Bandorowicz organization: Nencki Institute of Experimental Biology, Department of Biochemistry, Polish Academy of Sciences, 02-093 Warsaw, Poland – sequence: 10 givenname: Slawomir surname: Pikula fullname: Pikula, Slawomir organization: Nencki Institute of Experimental Biology, Department of Biochemistry, Polish Academy of Sciences, 02-093 Warsaw, Poland – sequence: 11 givenname: David surname: Magne fullname: Magne, David organization: Universite Lyon 1, UFR Chimie Biochimie, 69 622 Villeurbanne Cedex, France – sequence: 12 givenname: Niels surname: Volkmann fullname: Volkmann, Niels organization: Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA – sequence: 13 givenname: Dorit surname: Hanein fullname: Hanein, Dorit organization: Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA – sequence: 14 givenname: José Luis surname: Millán fullname: Millán, José Luis organization: Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA – sequence: 15 givenname: Rene surname: Buchet fullname: Buchet, Rene email: rene.buchet@univ-lyon1.fr organization: Universite Lyon 1, UFR Chimie Biochimie, 69 622 Villeurbanne Cedex, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29108957$$D View this record in MEDLINE/PubMed https://udl.hal.science/hal-02128820$$DView record in HAL |
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| SubjectTerms | Animals Apatites - metabolism Atomic force microscopy biogenesis Biomimetic Materials biomimetics bone formation Calcification, Physiologic - physiology Calcinosis - physiopathology Cellular Biology chondrocytes Chondrocytes - pathology Chondrocytes - ultrastructure collagen Collagen - metabolism Electron microscopy Extracellular Matrix - metabolism Extracellular Vesicles - physiology Humans Hypertrophy Life Sciences lipid composition Lipid raft lipids Matrix vesicles Membrane Microdomains - physiology Mineralization minerals Minerals - metabolism Models, Biological myocytes Organelle Biogenesis osteoblasts Osteoblasts - ultrastructure Proteolipids Proteoliposomes proteomics smooth muscle Specimen Handling transmission electron microscopy Vascular Calcification - physiopathology |
| Title | Matrix vesicles from chondrocytes and osteoblasts: Their biogenesis, properties, functions and biomimetic models |
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