Lipid composition modulates ATP hydrolysis and calcium phosphate mineral propagation by TNAP-harboring proteoliposomes.


Journal

Archives of biochemistry and biophysics
ISSN: 1096-0384
Titre abrégé: Arch Biochem Biophys
Pays: United States
ID NLM: 0372430

Informations de publication

Date de publication:
30 09 2020
Historique:
received: 30 04 2020
revised: 09 06 2020
accepted: 22 06 2020
pubmed: 28 7 2020
medline: 25 11 2020
entrez: 26 7 2020
Statut: ppublish

Résumé

Bone biomineralization is mediated by a special class of extracellular vesicles, named matrix vesicles (MVs), released by osteogenic cells. The MV membrane is enriched in sphingomyelin (SM), cholesterol (Chol) and tissue non-specific alkaline phosphatase (TNAP) compared with the parent cells' plasma membrane. TNAP is an ATP phosphohydrolase bound to cell and MV membranes via a glycosylphosphatidylinositol (GPI) anchor. Previous studies have shown that the lipid microenvironment influences the catalytic activity of enzymes incorporated into lipid bilayers. However, there is a lack of information about how the lipid microenvironment controls the ability of MV membrane-bound enzymes to induce mineral precipitation. Herein, we used TNAP-harboring proteoliposomes made of either pure dimyristoylphosphatidylcholine (DMPC) or DMPC mixed with either Chol, SM or both of them as MV biomimetic systems to evaluate how the composition modulates the lipid microenvironment and, in turn, TNAP incorporation into the lipid bilayer by means of calorimetry. These results were correlated with the proteoliposomes' catalytic activity and ability to induce the precipitation of amorphous calcium phosphate (ACP) in vitro. DMPC:SM proteoliposomes displayed the highest efficiency of mineral propagation, apparent affinity for ATP and substrate hydrolysis efficiency, which correlated with their highest degree of membrane organization (highest ΔH), among the tested proteoliposomes. Results obtained from turbidimetry and Fourier transformed infrared (FTIR) spectroscopy showed that the tested proteoliposomes induced ACP precipitation with the order DMPC:SM>DMPC:Chol:SM≈DMPC:Chol>DMPC which correlated with the lipid organization and the presence of SM in the proteoliposome membrane. Our study arises important insights regarding the physical properties and role of lipid organization in MV-mediated mineralization.

Identifiants

pubmed: 32710882
pii: S0003-9861(20)30491-4
doi: 10.1016/j.abb.2020.108482
pmc: PMC8390000
mid: NIHMS1732528
pii:
doi:

Substances chimiques

Calcium Phosphates 0
Liposomes 0
Proteolipids 0
Sphingomyelins 0
proteoliposomes 0
Adenosine Triphosphate 8L70Q75FXE
Cholesterol 97C5T2UQ7J
Alkaline Phosphatase EC 3.1.3.1
Dimyristoylphosphatidylcholine U86ZGC74V5

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

108482

Subventions

Organisme : NIDCR NIH HHS
ID : R01 DE012889
Pays : United States

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

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Auteurs

B Z Favarin (BZ)

Department of Chemistry, FFCLRP, University of São Paulo, Ribeirão Preto, SP, Brazil; Department of Physics, FFCLRP, University of São Paulo, Ribeirão Preto, SP, Brazil.

M Bolean (M)

Department of Chemistry, FFCLRP, University of São Paulo, Ribeirão Preto, SP, Brazil.

A P Ramos (AP)

Department of Chemistry, FFCLRP, University of São Paulo, Ribeirão Preto, SP, Brazil.

A Magrini (A)

Department of Biopathology and Imaging Diagnostics, University of Rome Tor Vergata, Rome, Italy.

N Rosato (N)

Department of Experimental Medicine, University of Rome Tor Vergata, Rome, Italy.

J L Millán (JL)

Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, USA.

M Bottini (M)

Department of Experimental Medicine, University of Rome Tor Vergata, Rome, Italy; Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, USA. Electronic address: massimo.bottini@uniroma2.it.

A J Costa-Filho (AJ)

Department of Physics, FFCLRP, University of São Paulo, Ribeirão Preto, SP, Brazil.

P Ciancaglini (P)

Department of Chemistry, FFCLRP, University of São Paulo, Ribeirão Preto, SP, Brazil. Electronic address: pietro@ffclrp.usp.br.

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