Characterisation of matrix vesicles in skeletal and soft tissue mineralisation

Lin, Chan‐Yu; Houston, Dean; Farquharson, Colin; MacRae, Vicky

doi:10.1016/j.bone.2016.04.007

Cited by 154 publications

(142 citation statements)

References 171 publications

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“…In vertebrates these matrix vesicles are released from the osteoblasts into the extracellular space where they contact collagen. Formation of the hydroxyapatite mineral is thought to begin within these vesicles [39]. As the crystals grow the vesicles burst and the mineral formation continues in the extracellular space.…”

Section: Discussionmentioning

confidence: 99%

The skeletal proteome of the sea star Patiria miniata and evolution of biomineralization in echinoderms

Flores

Livingston

2017

BMC Evol Biol

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BackgroundProteomic studies of skeletal proteins have revealed large, complex mixtures of proteins occluded within the mineral. Many skeletal proteomes contain rapidly evolving proteins with repetitive domains, further complicating our understanding. In echinoderms, proteomic analysis of the skeletal proteomes of mineralized tissues of the sea urchin Strongylocentrotus purpuratus prominently featured spicule matrix proteins with repetitive sequences linked to a C-type lectin domain. A comparative study of the brittle star Ophiocoma wendtii skeletal proteome revealed an order of magnitude fewer proteins containing C-type lectin domains. A number of other proteins conserved in the skeletons of the two groups were identified. Here we report the complete skeletal proteome of the sea star Patiria miniata and compare it to that of the other echinoderm groups.ResultsWe have identified eighty-five proteins in the P. miniata skeletal proteome. Forty-two percent of the proteins were determined to be homologous to proteins found in the S. purpuratus skeletal proteomes. An additional 34 % were from similar functional classes as proteins in the urchin proteomes. Thirteen percent of the P. miniata proteins had homologues in the O. wendtii skeletal proteome with an additional 29% showing similarity to brittle star skeletal proteins. The P. miniata skeletal proteome did not contain any proteins with C-lectin domains or with acidic repetitive regions similar to the sea urchin or brittle star spicule matrix proteins. MSP130 proteins were also not found. We did identify a number of proteins homologous between the three groups. Some of the highly conserved proteins found in echinoderm skeletons have also been identified in vertebrate skeletons.ConclusionsThe presence of proteins conserved in the skeleton in three different echinoderm groups indicates these proteins are important in skeleton formation. That a number of these proteins are involved in skeleton formation in vertebrates suggests a common origin for some of the fundamental processes co-opted for skeleton formation in deuterostomes. The proteins we identify suggest transport of proteins and calcium via endosomes was co-opted to this function in a convergent fashion. Our data also indicate that modifications to the process of skeleton formation can occur through independent co-option of proteins following species divergence as well as through domain shuffling.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0978-z) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

The skeletal proteome of the sea star Patiria miniata and evolution of biomineralization in echinoderms

Flores

Livingston

2017

BMC Evol Biol

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“…Mineralization is initiated by the accumulation of calcium and inorganic phosphate, followed by crystal growth [2, 3]. To obtain a normal mineral deposition rate during bone remodeling, the mineralization process is controlled by several molecules that either inhibit or promote the growth of HA crystals [4, 5]. …”

Section: Introductionmentioning

confidence: 99%

Bone Alkaline Phosphatase and Tartrate-Resistant Acid Phosphatase: Potential Co-regulators of Bone Mineralization

et al. 2017

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Phosphorylated osteopontin (OPN) inhibits hydroxyapatite crystal formation and growth, and bone alkaline phosphatase (BALP) promotes extracellular mineralization via the release of inorganic phosphate from the mineralization inhibitor inorganic pyrophosphate (PPi). Tartrate-resistant acid phosphatase (TRAP), produced by osteoclasts, osteoblasts, and osteocytes, exhibits potent phosphatase activity towards OPN; however, its potential capacity as a regulator of mineralization has not previously been addressed. We compared the efficiency of BALP and TRAP towards the endogenous substrates for BALP, i.e., PPi and pyridoxal 5′-phosphate (PLP), and their impact on mineralization in vitro via dephosphorylation of bovine milk OPN. TRAP showed higher phosphatase activity towards phosphorylated OPN and PPi compared to BALP, whereas the activity of TRAP and BALP towards PLP was comparable. Bovine milk OPN could be completely dephosphorylated by TRAP, liberating all its 28 phosphates, whereas BALP dephosphorylated at most 10 phosphates. OPN, dephosphorylated by either BALP or TRAP, showed a partially or completely attenuated phosphorylation-dependent inhibitory capacity, respectively, compared to native OPN on the formation of mineralized nodules. Thus, there are phosphorylations in OPN important for inhibition of mineralization that are removed by TRAP but not by BALP. In conclusion, our data indicate that both BALP and TRAP can alleviate the inhibitory effect of OPN on mineralization, suggesting a potential role for TRAP in skeletal mineralization. Further studies are warranted to explore the possible physiological relevance of TRAP in bone mineralization.

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“…Various experiments have revealed the presence of HA crystals both inside and outside collagen fibrils in the ECM (McNally et al 2012) and also within the lumen of matrix vesicles (MVs) (Ali et al 1970;Anderson 1969;Bonucci 1970). MVs are extracellular vesicles with a diameter ranging from approximately 100 to 300 nm (Anderson 2003;Anderson et al 2010;Cui et al 2016;Golub 2009;Wuthier and Lipscomb 2011) which harbor the biochemical machinery needed to establish the appropriate inorganic pyrophosphate (PP i ) to inorganic phosphate (P i ) ratio (Ciancaglini et al 2006Harmey et al 2004;Hessle et al 2002;Johnson et al 2000;Roberts et al 2007;Yadav et al 2011;Zhou et al 2012) required to initiate the synthesis of apatitic mineral (Bechkoff et al 2008;Thouverey et al 2009;Wu et al 1997), which will subsequently be propagated onto the collagenous ECM. These vesicles are released from the hypertrophic chondrocytes and mature osteoblasts, the cells responsible for endochondral and membranous ossification.…”

Section: Mineralization Process and The Biogenesis Of Matrix Vesiclesmentioning

confidence: 99%

Biophysical aspects of biomineralization

et al. 2017

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During the process of endochondral bone formation, chondrocytes and osteoblasts mineralize their extracellular matrix (ECM) by promoting the synthesis of hydroxyapatite (HA) seed crystals in the sheltered interior of membranelimited matrix vesicles (MVs). Several lipid and proteins present in the membrane of the MVs mediate the interactions of MVs with the ECM and regulate the initial mineral deposition and posterior propagation. Among the proteins of MV membranes, ion transporters control the availability of phosphate and calcium needed for initial HA deposition. Phosphatases (orphan phosphatase 1, ectonucleotide pyrophosphatase/ phosphodiesterase 1 and tissue-nonspecific alkaline phosphatase) play a crucial role in controlling the inorganic pyrophosphate/inorganic phosphate ratio that allows MVmediated initiation of mineralization. The lipidic microenvironment can help in the nucleation process of first crystals and also plays a crucial physiological role in the function of MVassociated enzymes and transporters (type III sodiumdependent phosphate transporters, annexins and Na + /K + ATPase). The whole process is mediated and regulated by the action of several molecules and steps, which make the process complex and highly regulated. Liposomes and proteoliposomes, as models of biological membranes, facilitate the understanding of lipid-protein interactions with emphasis on the properties of physicochemical and biochemical processes. In this review, we discuss the use of proteoliposomes as multiple protein carrier systems intended to mimic the various functions of MVs during the initiation and propagation of mineral growth in the course of biomineralization. We focus on studies applying biophysical tools to characterize the biomimetic models in order to gain an understanding of the importance of lipid-protein and lipid-lipid interfaces throughout the process.Keywords Lipid microenvironment . Biomineralization . Matrix vesicles . Liposome . Proteoliposome . Hydroxyapatite Mineralization process and the biogenesis of matrix vesiclesMineralization of cartilage and bone occurs by a series of physicochemical and biochemical processes that together facilitate the deposition of calcium phosphate. The deposited calcium phosphate is subsequently converted into hydroxyapatite (HA) [Ca 10 (PO 4 ) 6 (OH) 2 ] in specific areas of the extracellular matrix (ECM). Various experiments have revealed the presence of HA crystals both inside and outside collagen fibrils in the ECM (McNally et al. 2012) and also within the

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Characterisation of matrix vesicles in skeletal and soft tissue mineralisation

Cited by 154 publications

References 171 publications

The skeletal proteome of the sea star Patiria miniata and evolution of biomineralization in echinoderms

The skeletal proteome of the sea star Patiria miniata and evolution of biomineralization in echinoderms

Bone Alkaline Phosphatase and Tartrate-Resistant Acid Phosphatase: Potential Co-regulators of Bone Mineralization

Biophysical aspects of biomineralization

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