Lipid microenvironment affects the ability of proteoliposomes harboring TNAP to induce mineralization without nucleators.
Alkaline phosphatase
Biomineralization
Matrix vesicles
Nucleational core
Proteoliposome
Journal
Journal of bone and mineral metabolism
ISSN: 1435-5604
Titre abrégé: J Bone Miner Metab
Pays: Japan
ID NLM: 9436705
Informations de publication
Date de publication:
Jul 2019
Jul 2019
Historique:
received:
30
07
2018
accepted:
19
09
2018
pubmed:
17
10
2018
medline:
31
8
2019
entrez:
17
10
2018
Statut:
ppublish
Résumé
Tissue-nonspecific alkaline phosphatase (TNAP), a glycosylphosphatidylinositol-anchored ectoenzyme present on the membrane of matrix vesicles (MVs), hydrolyzes the mineralization inhibitor inorganic pyrophosphate as well as ATP to generate the inorganic phosphate needed for apatite formation. Herein, we used proteoliposomes harboring TNAP as MV biomimetics with or without nucleators of mineral formation (amorphous calcium phosphate and complexes with phosphatidylserine) to assess the role of the MVs' membrane lipid composition on TNAP activity by means of turbidity assay and FTIR analysis. We found that TNAP-proteoliposomes have the ability to induce mineralization even in the absence of mineral nucleators. We also found that the addition of cholesterol or sphingomyelin to TNAP-proteoliposomes composed of 1,2-dipalmitoyl-sn-glycero-3-phosphocholine reduced the ability of TNAP to induce biomineralization. Our results suggest that the lipid microenvironment is essential for the induction and propagation of minerals mediated by TNAP.
Identifiants
pubmed: 30324534
doi: 10.1007/s00774-018-0962-8
pii: 10.1007/s00774-018-0962-8
pmc: PMC6465158
mid: NIHMS1005940
doi:
Substances chimiques
Lipids
0
Proteolipids
0
proteoliposomes
0
Adenosine Triphosphate
8L70Q75FXE
Alkaline Phosphatase
EC 3.1.3.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
607-613Subventions
Organisme : NIDCR NIH HHS
ID : R01 DE012889
Pays : United States
Organisme : CNPq
ID : 304021/2017-2
Organisme : CNPq
ID : 167497/2017-0
Organisme : FAPESP
ID : 2016/21236-0
Références
Boskey AL (2006) Mineralization, structure and function of bone. In: Seibel MJ, Robins SP, Biezikian JP (eds) Dynamics of bone and cartilage metabolism. Academic Press, San Diego, pp 201–212
doi: 10.1016/B978-012088562-6/50013-3
Wu LN, Yoshimori T, Genge BR, Wu LN, Yoshimori T, Genge BR, Sauer GR, Kirsch T, Ishikawa Y, Wuthier RE (1993) Characterization of the nucleational core complex responsible for mineral induction by growth plate cartilage matrix vesicles. J Biol Chem 268(33):25084–25094
pubmed: 8227072
Wu LN, Genge BR, Dunkelberger DG, LeGeros RZ, Concannon B, Wuthier RE (1997) Physicochemical characterization of the nucleational core of matrix vesicles. J Biol Chem 272(7):4404–4411
doi: 10.1074/jbc.272.7.4404
pubmed: 9020163
Millán JL (2013) The role of phosphatases in the initiation of skeletal mineralization. Calcif Tissue Int 93:299–306
doi: 10.1007/s00223-012-9672-8
Bottini M, Mebarek S, Anderson KL, Strzelecka-Kiliszek A, Bozycki L, Simao AMS, Bolean M, Ciancaglini P, Pikula JB, Pikula S, Magne D, Volkmann N, Hanein D, Millan JL, Buchet R (2018) Matrix vesicles from chondrocytes and osteoblasts: Their biogenesis, properties, functions and biomimetic models. Biochim Biophys Acta Gen Subj 1862(3):532–546
Ali SY, Sajdera SW, Anderson HC (1970) Isolation and characterization of calcifying matrix vesicles from epiphyseal cartilage. Proc Natl Acad Sci USA 67:1513–1520
doi: 10.1073/pnas.67.3.1513
pubmed: 5274475
Robison R (1923) The possible significance of hexosephosphoric esters in ossification. Biochem J 17:286–293
doi: 10.1042/bj0170286
pubmed: 16743183
pmcid: 1259346
Meyer JL (1984) Can biological calcification occur in the presence of pyrophosphate? Arch Biochem Biophys 231:1–8
doi: 10.1016/0003-9861(84)90356-4
pubmed: 6326671
Rezende AA, Pizauro JM, Ciancaglini P, Leone FA (1994) Phosphodiesterase activity is a novel property of alkaline phosphatase from osseous plate. Biochem J 301(Pt 2):517–522
doi: 10.1042/bj3010517
pubmed: 8042997
pmcid: 1137111
Fleisch H, Bisaz S (1962) Mechanism of calcification: inhibitory role of pyrophosphate. Nature 195:911
doi: 10.1038/195911a0
pubmed: 13893487
Hsu HH, Camacho NP, Anderson HC (1999) Further characterization of ATP-initiated calcification by matrix vesicles isolated from rachitic rat cartilage. Membrane perturbation by detergents and deposition of calcium pyrophosphate by rachitic matrix vesicles. Biochim Biophys Acta 1416:320–332
doi: 10.1016/S0005-2736(98)00235-1
pubmed: 9889389
Ciancaglini P, Yadav MC, Simao AM, Narisawa S, Pizauro JM, Farquharson C, Hoylaerts MF, Millan JL (2010) Kinetic analysis of substrate utilization by native and TNAP-, NPP1-, or PHOSPHO1-deficient matrix vesicles. J Bone Miner Res 25(4):716–723
pubmed: 19874193
Simao AM, Yadav MC, Ciancaglini P, Millan JL (2010) Proteoliposomes as matrix vesicles' biomimetics to study the initiation of skeletal mineralization. Braz J Med Biol Res 43(3):234–241
doi: 10.1590/S0100-879X2010007500008
pubmed: 20401430
pmcid: 5298493
Yadav MC, Bottini M, Cory E, Bhattacharya K, Kuss P, Narisawa S, Sah RL, Beck L, Fadeel B, Farquharson C, Millan JL (2016) Skeletal Mineralization Deficits and Impaired Biogenesis and Function of Chondrocyte-Derived Matrix Vesicles in Phospho1(-/-) and Phospho1/Pi t1 Double-Knockout Mice. J Bone Miner Res 31(6):1275–1286
doi: 10.1002/jbmr.2790
pubmed: 26773408
pmcid: 4891278
Ciancaglini P, Simao AM, Camolezi FL, Millan JL, Pizauro JM (2006) Contribution of matrix vesicles and alkaline phosphatase to ectopic bone formation. Braz J Med Biol Res 39(5):603–610
doi: 10.1590/S0100-879X2006000500006
pubmed: 16648897
Simons K, Coskun U, Grzybek M, Lingwood D, Levental I, Kaiser HJ (2010) Lipid-protein interactions governing raft partitioning in membranes. Chem Phys Lipids 163:S10–S10
doi: 10.1016/j.chemphyslip.2010.05.032
Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50
doi: 10.1126/science.1174621
Wu LN, Genge BR, Kang MW, Arsenault AL, Wuthier RE (2002) Changes in phospholipid extractability and composition accompany mineralization of chicken growth plate cartilage matrix vesicles. J Biol Chem 277(7):5126–5133
doi: 10.1074/jbc.M107899200
pubmed: 11714705
Bolean M, Simao AMS, Barioni MB, Favarin BZ, Sebinelli HG, Veschi EA, Janku TAB, Bottini M, Hoylaerts MF, Itri R, Millan JL, Ciancaglini P (2017) Biophysical aspects of biomineralization. Biophys Rev 9(5):747–760
doi: 10.1007/s12551-017-0315-1
pubmed: 28852989
pmcid: 5662051
Balcerzak M, Radisson J, Azzar G, Farlay D, Boivin G, Pikula S, Buchet R (2007) A comparative analysis of strategies for isolation of matrix vesicles. Anal Biochem 361(2):176–182
doi: 10.1016/j.ab.2006.10.001
pubmed: 17194438
Damek-Poprawa M, Golub E, Otis L, Harrison G, Phillips C, Boesze-Battaglia K (2006) Chondrocytes utilize a cholesterol-dependent lipid translocator to externalize phosphatidylserine. Biochemistry 45(10):3325–3336
doi: 10.1021/bi0515927
pubmed: 16519527
pmcid: 4732727
Ciancaglini P, Simao AMS, Bolean M, Millan JL, Rigos CF, Yoneda JS, Colhone MC, Stabeli RG (2012) Proteoliposomes in nanobiotechnology. Biophys Rev 4(1):67–81
pubmed: 28510001
Simao AM, Yadav MC, Narisawa S, Bolean M, Pizauro JM, Hoylaerts MF, Ciancaglini P, Millan JL (2010) Proteoliposomes harboring alkaline phosphatase and nucleotide pyrophosphatase as matrix vesicle biomimetics. J Biol Chem 285(10):7598–7609
doi: 10.1074/jbc.M109.079830
pubmed: 20048161
pmcid: 2844207
Simao AM, Bolean M, Hoylaerts MF, Millan JL, Ciancaglini P (2013) Effects of pH on the production of phosphate and pyrophosphate by matrix vesicles' biomimetics. Calcif Tissue Int 93(3):222–232
doi: 10.1007/s00223-013-9745-3
pubmed: 23942722
pmcid: 3752608
Simao AMS, Bolean M, Cury TAC, Stabeli RG, Itri R, Ciancaglini P (2015) Liposomal systems as carriers for bioactive compounds. Biophys Rev 7(4):391–397
doi: 10.1007/s12551-015-0180-8
pubmed: 28510100
pmcid: 5418487
Bolean M, Simao AM, Kiffer-Moreira T, Hoylaerts MF, Millan JL, Itri R, Ciancaglini P (2015) Proteoliposomes with the ability to transport Ca(2+) into the vesicles and hydrolyze phosphosubstrates on their surface. Arch Biochem Biophys 584:79–89
doi: 10.1016/j.abb.2015.08.018
pubmed: 26325078
pmcid: 5257277
Bolean M, Borin IA, Simao AMS, Bottini M, Bagatolli LA, Hoylaerts MF, Millan JL, Ciancaglini P (2017) Topographic analysis by atomic force microscopy of proteoliposomes matrix vesicle mimetics harboring TNAP and AnxA5. Biochim Biophys Acta 1859(10):1911–1920
Itel F, Skovhus Thomsen J, Städler B (2018) Matrix vesicles-containing microreactors as support for bone-like osteoblast cells to enhance biomineralization. ACS Appl Mater Interfaces. https://doi.org/10.1021/acsami.8b10886
doi: 10.1021/acsami.8b10886
pubmed: 30113809
Bolean M, Simao AM, Favarin BZ, Millan JL, Ciancaglini P (2010) The effect of cholesterol on the reconstitution of alkaline phosphatase into liposomes. Biophys Chem 152(1–3):74–79
doi: 10.1016/j.bpc.2010.08.002
pubmed: 20810204
Bolean M, Simao AM, Favarin BZ, Millan JL, Ciancaglini P (2011) Thermodynamic properties and characterization of proteoliposomes rich in microdomains carrying alkaline phosphatase. Biophys Chem 158(2-3):111-118
doi: 10.1016/j.bpc.2011.05.019
pubmed: 21676530
pmcid: 3392897
Simao AM, Beloti MM, Cezarino RM, Rosa AL, Pizauro JM, Ciancaglini P (2007) Membrane-bound alkaline phosphatase from ectopic mineralization and rat bone marrow cell culture. Comp Biochem Physiol A Mol Integr Physiol 146(4):679–687
doi: 10.1016/j.cbpa.2006.05.008
pubmed: 16798036
Hartree EF (1972) Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal Biochem 48:422–427
doi: 10.1016/0003-2697(72)90094-2
pubmed: 4115981
Leone FA, Baranauskas JA, Furriel RP, Borin IA (2005) SigrafW: An easy-to-use program for fitting enzyme kinetic data. Biochem Mol Biol Educ 33(6):399–403
doi: 10.1002/bmb.2005.49403306399
pubmed: 21638609
Genge BR, Wu LN, Wuthier RE (2007) In vitro modeling of matrix vesicle nucleation: synergistic stimulation of mineral formation by annexin A5 and phosphatidylserine. J Biol Chem 282:26035–26045
doi: 10.1074/jbc.M701057200
pubmed: 17613532
Wuthier RE, Chin JE, Hale JE, Register TC, Hale LV, Ishikawa Y (1985) Isolation and characterization of calcium-accumulating matrix vesicles from chondrocytes of chicken epiphyseal growth plate cartilage in primary culture. J Biol Chem 260(29):15972–15979
pubmed: 3905800
Ishikawa T, Wakamura M, Kondo S (1989) Surface characterization of calcium hydroxylapatite by Fourier transform infrared spectroscopy. Langmuir 5:140–144
doi: 10.1021/la00085a025
Fowler BO, Markovic M, Tung MS (2004) Preparation and comprehensive characterization of a calcium hydroxyapatite reference material. J Res Natl Inst Stand Technol 109:553–568
doi: 10.6028/jres.109.042
pubmed: 27366634
pmcid: 4856200
Peress NS, Anderson HC, Sajdera SW (1974) The lipids of matrix vesicles from bovine fetal epiphyseal cartilage. Calcif Tissue Res 14:275–281
doi: 10.1007/BF02060301
pubmed: 4367314
Wuthier RE, Lipscomb GF (2011) Matrix vesicles: structure, composition, formation and function in calcification. Front Biosci 16:2812–2902
doi: 10.2741/3887
Favarin BZ, Andrade MAR, Bolean M, Simao AMS, Ramos AP, Hoylaerts MF, Millan JL, Ciancaglini P (2017) Effect of the presence of cholesterol in the interfacial microenvironment on the modulation of the alkaline phosphatase activity during in vitro mineralization. Colloids Surf B Biointerfaces 155:466–476
doi: 10.1016/j.colsurfb.2017.04.051
pubmed: 28472750
Lehto MT, Sharom FJ (2002) Proximity of the protein moiety of a GPI-anchored protein to the membrane surface: a FRET study. Biochemistry 41:8368–8376
doi: 10.1021/bi012038+
pubmed: 12081485
Sesana S, Re F, Bulbarelli A, Salerno D, Cazzaniga E, Masserini M (2008) Membrane features and activity of GPI-anchored enzymes: alkaline phosphatase reconstituted in model membranes. Biochemistry 47(19):5433–5440
doi: 10.1021/bi800005s
pubmed: 18416535
Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572
doi: 10.1038/42408
pubmed: 9177342
Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221–17224
doi: 10.1074/jbc.R000005200
pubmed: 10770957
Snyder B, Freire E (1980) Compositional domain structure in phosphatidylcholine-cholesterol and sphingomyelin-cholesterol bilayers. Proc Natl Acad Sci USA 77:4055–4059
doi: 10.1073/pnas.77.7.4055
pubmed: 6933455
Cheng ZH, Yasukawa A, Kandori K, Ishikawa T (1998) FTIR study of adsorption of CO
doi: 10.1021/la980339n