The roles of annexins and alkaline phosphatase in mineralization process.

• Authors: Marcin Balcerzak , Eva Hamade , Le Zhang , Slawomir Pikula , Gérard Azzar , Jacqueline Radisson , Joanna Bandorowicz-Pikula , Rene Buchet
• Languages of publication: EN

Abstracts

EN

In this review the roles of specific proteins during the first step of mineralization and nucleation are discussed. Mineralization is initiated inside the extracellular organelles-matrix vesicles (MVs). MVs, containing relatively high concentrations of Ca2+ and inorganic phosphate (Pgi), create an optimal environment to induce the formation of hydroxyapatite (HA). Special attention is given to two families of proteins present in MVs, annexins (AnxAs) and tissue-nonspecific alkaline phosphatases (TNAPs). Both families participate in the formation of HA crystals. AnxAs are Ca2+- and lipid-binding proteins, which are involved in Ca2+ homeostasis in bone cells and in extracellular MVs. AnxAs form calcium ion channels within the membrane of MVs. Although the mechanisms of ion channel formation by AnxAs are not well understood, evidence is provided that acidic pH or GTP contribute to this process. Furthermore, low molecular mass ligands, as vitamin A derivatives, can modulate the activity of MVs by interacting with AnxAs and affecting their expression. AnxAs and other anionic proteins are also involved in the crystal nucleation. The second family of proteins, TNAPs, is associated with Pi homeostasis, and can hydrolyse a variety of phosphate compounds. ATP is released in the extracellular matrix, where it can be hydrolyzed by TNAPs, ATP hydrolases and nucleoside triphosphate (NTP) pyrophosphohydrolases. However, TNAP is probably not responsible for ATP-dependent Ca2+/phosphate complex formation. It can hydrolyse pyrophosphate (PPi), a known inhibitor of HA formation and a byproduct of NTP pyrophosphohydrolases. In this respect, antagonistic activities of TNAPs and NTP pyrophosphohydrolases can regulate the mineralization process.

Keywords

EN

mineralization; hydroxyapatite; alkaline phosphatase; annexin; matrix vesicle

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2003
• Volume: 50
• Issue: 4
• Pages: 1019-1038

Dates

published

2003

received

2003-08-05

revised

2003-09-24

accepted

2003-10-7

Contributors

author

Marcin Balcerzak

• M. Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warszawa, Poland

author

Eva Hamade

• Laboratoire de Physico-Chimie Biologique, UMR CNRS 5013, Université Claude Bernard, Lyon 1, UFR de Chimie-Biochimie, F-69622 Villeurbanne, France

author

Le Zhang

• Laboratoire de Physico-Chimie Biologique, UMR CNRS 5013, Université Claude Bernard, Lyon 1, UFR de Chimie-Biochimie, F-69622 Villeurbanne, France

author

Slawomir Pikula

• M. Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warszawa, Poland

author

Gérard Azzar

• Laboratoire de Physico-Chimie Biologique, UMR CNRS 5013, Université Claude Bernard, Lyon 1, UFR de Chimie-Biochimie, F-69622 Villeurbanne, France

author

Jacqueline Radisson

• Laboratoire de Physico-Chimie Biologique, UMR CNRS 5013, Université Claude Bernard, Lyon 1, UFR de Chimie-Biochimie, F-69622 Villeurbanne, France

author

Joanna Bandorowicz-Pikula

• M. Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warszawa, Poland

author

Rene Buchet

• Laboratoire de Physico-Chimie Biologique, UMR CNRS 5013, Université Claude Bernard, Lyon 1, UFR de Chimie-Biochimie, F-69622 Villeurbanne, France

References

• Andersen MH, Berglund L, Petersen TE, Rasmussen JT. (2002) Annexin-V binds to the intracellular part of the β5 integrin receptor subunit. Biochem Biophys Res Commun.; 292: 550-7.
• Anderson HC. (1995) Molecular biology of matrix vesicles. Clin Orthopaed Relat Res.; 314: 266-80.
• Anderson HC. (2003) Matrix vesicles and calcification. Curr Rheumatol Rep.; 5: 222-6.
• Arcuri C, Giambanco I, Bianchi R, Donato R. (2002) Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience.; 109: 371-88.
• Arispe N, Rojas E, Genge BR, Wu LN, Wuthier RE. (1996) Similarity in calcium channel activity of annexin V and matrix vesicles in planar lipid bilayers. Biophys J.; 71: 1764-75.
• Avila-Sakar AJ, Kretsinger RH, Creutz CE. (2000) Membrane-bound 3D structures reveal the intrinsic flexibility of annexin VI. J Struct Biol.; 130: 54-62.
• Ayala-Sanmartin J. (2001) Cholesterol enhances phospholipid binding and aggregation of annexins by their core domain. Biochem Biophys Res Commun.; 283: 72-9.
• Ayala-Sanmartin J, Henry JP, Pradel LA. (2001) Cholesterol regulates membrane binding and aggregation by annexin 2 at submicromolar Ca2+ concentration. Biochim Biophys Acta.; 1510: 18-28.
• Balmain N. (1991) Calbindin-D9k. A vitamin-D-dependent, calcium-binding protein in mineralized tissues. Clin Orthop.; 265: 265-76.
• Balmain N. (1992) Identification of calbindin-D9k in matrix vesicles. Bone Miner.; 17: 197-201.
• Balmain N, Hotton D, Cuisinier-Gleizes P, Mathieu H. (1989) Immunoreactive calbindin-D9K localization in matrix vesicle-initiated calcification in rat epiphyseal cartilage: an immunoelectron microscope study. J Bone Miner Res.; 4: 565-75.
• Balmain N, Hotton D, Cuisinier-Gleizes P, Mathieu H. (1991) Immunoreactive calbindin-D9K in bone matrix vesicle. Histochemistry.; 95: 459-69.
• Balmain N, von Eichel B, Toury R, Belquasmi F, Hauchecorne M, Klaus G, Mehls O, Ritz E. (1995) Calbindin-D28K and -D9K and 1,25(OH)2 vitamin D3 receptor immunolocalization and mineralization induction in long-term primary cultures of rat epiphyseal chondrocytes. Bone.; 17: 37-45.
• Bandorowicz-Pikula J, Buchet R, Pikula S. (2001) Annexins as nucleotide-binding proteins: facts and speculations. BioEssays.; 23: 170-8.
• Bandorowicz-Pikula J, Kirilenko A, van Deursen R, Golczak M, Kühnel M, Lancelin JM, Pikula S, Buchet R. (2003) A putative consensus sequence for nucleotide-binding site of annexin A6. Biochemistry.; 42: 9137-46.
• Baran DT, Quail JM, Ray R, Leszyk J, Honeyman T. (2000) Annexin II is the membrane receptor that mediates the rapid actions of 1α,25-dihydroxyvitamin D3. J Cell Biochem.; 78: 34-46.
• Bartling PM, Chong KW. (1999) The involvement of phosphohydrolases in mineralization: studies on enzymatic activities extracted from red deer antler. Calcif Tissue Int.; 65: 232-6.
• Beermann ofm cap BB, Hinz HJ, Hofmann A, Huber R. (1998) Acid induced equilibrium unfolding of annexin V wild type shows two intermediate states. FEBS Lett.; 423: 265-9.
• Bellows CG, Aubin JE, Heersche JNR. (1991) Initiation and progression in mineralization of bone nodules formed in vitro: the role of alkaline phosphatase and organic phosphate. Bone Miner.; 14: 27-40.
• Berendes R, Burger A, Voges D, Demange P, Huber R. (1993) Calcium influx through annexin V ion channels into large unilamellar vesicles measured with fura-2. FEBS Lett.; 317: 131-4.
• Biggin PC, Sansom MS. (2003) Mechanosensitive channels: stress relief. Curr Biol.; 13: R183-5.
• Boskey AL. (1996) Matrix proteins and mineralization: an overview. Connect Tissue Res.; 35: 357-63.
• Bourrat C, Radisson J, Chavassieux P, Azzar G, Roux B, Meunier PJ. (2000) Activity increase after extraction of alkaline phosphatase from human osteoblastic membranes by nonionic detergents: influence of age and sex. Calcif Tissue Int.; 66: 22-8.
• Boyan BD, Schwartz Z, Swain LD, Carnes DL Jr, Zislis T. (1988) Differential expression of phenotype by resting zone and growth region costochondral chondrocytes in vitro. Bone.; 9: 185-94.
• Brachvogel B, Dikschas J, Moch H, Welzel H, von der Mark K, Hofmann C, Poschl E. (2003) Annexin A5 is not essential for skeletal development. Mol Cell Biol.; 23: 2907-13.
• Buschmann MD, Gluzband YA, Grodzinsky AJ, Hunziker EB. (1995) Mechanical compression modulates matrix biosynthesis in chondrocyte/agarose culture. J Cell Sci.; 108: 1497-508.
• Camolezi FL, Daghastanli KRP, Magalhaes PP, Pizauro JM, Ciancaglini P. (2002) Construction of an alkaline phosphatase-liposome system: a tool for mineralization study. Int J Biochem Cell Biol.; 34: 1091-101.
• Cao X, Genge BR, Wu LNY, Buzzi WR, Showman RM, Wuthier RE. (1993) Characterization, cloning and expression of the 67-kDa annexin from chicken growth plate cartilage matrix vesicles. Biochem Biophys Res Commun.; 197: 556-61.
• Caohuy H, Srivastava M, Pollard HB. (1996) Membrane fusion protein synexin (annexin VII) as a Ca2+/GTP sensor in exocytotic secretion. Proc Natl Acad Sci U S A.; 93: 10797-802.
• Dascalu A, Korenstein R, Oron Y, Nevo Z. (1996) A hyperosmotic stimulus regulates intracellular pH, calcium, and S-100 protein levels in avian chondrocytes. Biochem Biophys Res Commun.; 227: 368-73.
• Davidson RM, Lingenbrink PA, Norton LA. (1996) Continuous mechanical loading alters properties of mechanosensitive channels in G292 osteoblastic cells. Calcif Tissue Int.; 59: 500-4.
• Davidson RM, Tatakis DW, Auerbach AL. (1990) Multiple forms of mechanosensitive ion channels in osteoblast-like cells. Pflugers Arch.; 416: 646-51.
• De Diego I, Schwartz F, Siegfried H, Dauterstedt P, Heeren J, Beisiegel U, Enrich C, Grewal T. (2002) Cholesterol modulates the membrane binding and intracellular distribution of annexin 6. J Biol Chem.; 277: 32187-94.
• De Luca F, Uyeda JA, Mericq V, Mancilla EE, Yanovski JA, Barnes KM, Zile MH, Baron J. (2000) Retinoic acid is a potent regulator of growth plate chondrogenesis. Endocrinology.; 141: 346-53.
• Derfus B, Kranendonk S, Camacho N, Mandel N, Kushnaryov V, Lynch K, Ryan L. (1998) Human osteoarthritic cartilage matrix vesicles generate both calcium pyrophosphate dihydrate and apatite in vitro. Calcif Tissue Int.; 63: 258-62.
• Derfus BA, Kurtin SM, Camacho NP, Kurup I, Ryan LM. (1996) Comparison of matrix vesicles derived from normal and osteoarthritic human articular cartilage. Connect Tissue Res.; 35: 337-42.
• Donato R. (2003) Interactions of annexins with S100 proteins. In Annexins: biological implications and annexin-related pathologies. (Bandorowicz-Pikula J, ed), pp 100-13. Kluwer Academic/Plenum Publishers, New York, NY & Landes Bioscience, Georgetown, TX.
• Duncan RL, Hruska KA. (1994) Chronic, intermittent loading alters mechanosensitive channel characteristics in osteoblast-like cells. Am J Physiol.; 267: F909-16.
• Ecaot-Chevrier B, Glorieux FH, van der Rest M, Perreira G. (1983) Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture. J Cell Biol.; 96: 639-43.
• Einhorn TA, Gordon SL, Siegel SA, Hummel CF, Avitable MJ, Carty RP. (1985) Matrix vesicle enzymes in human osteoarthritis. J Orthop Res.; 3: 160-9.
• Erickson GR, Alexopoulos LG, Guilak F. (2001) Hyper-osmotic stress induces volume change and calcium transients in chondrocytes by transmembrane, phospholipid and G-protein pathways. J Biomech.; 34: 1527-35.
• Fernley HN. (1971) Mammalian alkaline phosphatase. In The Enzymes. 3rd edn. (Boyer PD, ed), pp 417-47. Academic Press, New York, London.
• Freye-Minks C, Kretsinger RH, Creutz CE. (2003) Structural and dynamic changes in human annexin VI induced by a phosphorylation-mimicking mutation, T356D. Biochemistry.; 42: 620-30.
• Garbuglia M, Verzini M, Donato R. (1998) Annexin VI binds S100A1 and S100B and blocks the ability of S100A1 and S100B to inhibit desmin and GFAP assemblies into intermediate filaments. Cell Calcium.; 24: 177-91.
• Garbuglia M, Verzini M, Hofmann A, Huber R, Donato R. (2000) S100A1 and S100B interactions with annexins. Biochim Biophys Acta.; 1498: 192-206.
• Garnero P, Delmas PD. (1996) New developments in biochemical markers for osteoporosis. Calcif Tissue Int.; 59 (Suppl 1): S2-9.
• Gelse K, Soder S, Eger W, Diemtar T, Aigner T. (2003) Osteophyte development - molecular characterization of differentiation stages. Osteoarthritis Cartilage.; 11: 141-8.
• Genge BR, Wu LNY, Adkisson IV HD, Wuthier RE. (1991) Matrix vesicle annexins exhibit proteolipid-like properties. Selective partitioning into lipophilic solvents under acidic conditions. J Biol Chem.; 266: 10678-85.
• Golczak M, Kicinska A, Bandorowicz-Pikula J, Buchet R, Szewczyk A, Pikula S. (2001a) Acidic pH-induced folding of annexin VI is a prerequisite for its insertion into lipid bilayers and formation of ion channels by the protein molecules. FASEB J.; 15: 1083-5.
• Golczak M, Kirilenko A, Bandorowicz-Pikula J, Pikula S. (2001b) Conformational states of annexin VI in solution induced by acidic pH. FEBS Lett.; 496: 49-54.
• Goossens EL, Reutelingsperger CP, Jongsma FH, Kraayenhof R, Hermens WT. (1995) Annexin V perturbs or stabilises phospholipid membranes in a calcium-dependent manner. FEBS Lett.; 359: 155-8.
• Grima DT, Kandel RA, Pepinsky B, Cruz TF. (1994) Lipocortin 2 (annexin 2) is a major substrate for constitutive tyrosine kinase activity in chondrocytes. Biochemistry.; 33: 2921-6.
• Guilak F, Zell RA, Erickson GR, Grande DA, Rubin CT, McLeod KJ, Donahue HJ. (1999) Mechanically induced calcium waves in articular chondrocytes are inhibited by gadolinium and amiloride. J Orthop Res.; 17: 421-9.
• Hamade E, Azzar G, Radisson J, Buchet R, Roux B. (2003) Chick embryo anchored alkaline phosphatase and mineralization process in vitro. Influence of Ca2+ and nature of substrates. Eur J Biochem.; 270: 2082-90.
• Harder T, Kellner R, Parton RG, Gruenberg J. (1997) Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol Biol Cell.; 8: 533-45.
• Hashimoto S, Ochs RL, Rosen F, Quach J, McCabe G, Solan J, Seegmiller JE, Terkeltaub R, Lotz M. (1998) Chondrocyte-derived apoptotic bodies and calcification of articular cartilage. Proc Natl Acad Sci U S A.; 95: 3094-9.
• Hatori M, Teixeira CC, Debolt K, Pacifici M, Shapiro IM. (1995) Adenine nucleotide metabolism by chondrocytes in vitro: role of ATP in chondrocyte maturation and matrix mineralization. J Cell Physiol.; 165: 468-74.
• Heinegard D, Oldberg A. (1989) Structure and biology of cartilage and bone matrix noncollagenous macromolecules. FASEB J.; 3: 2042-51.
• Henthorn PS, Raducha M, Edwards YH, Weiss MJ, Slaughter C, Lafferty MA, Harris H. (1987) Nucleotide and amino acid sequences of human intestinal alkaline phosphatase: close homology to placental alkaline phosphatase. Proc Natl Acad Sci U S A.; 84: 1234-8.
• Hessle H, Johnson KA, Anderson HC, Narisawa S, Sali A, Goding JW, Terkeltaub R, Millan JL. (2002) Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci U S A.; 99: 9445-9.
• Ho AM, Johnson MD, Kingsley DM. (2000) Role of the mouse ank gene in control of tissue calcification and arthritis. Science.; 289: 265-70.
• Hofmann A, Escherich A, Lewit-Bentley A, Benz J, Raguenes-Nicol C, Russo-Marie F, Gerke V, Moroder L, Huber R. (1998) Interactions of benzodiazepine derivatives with annexins. J Biol Chem.; 273: 2885-94.
• Hoshi K, Ozawa H. (2000) Matrix vesicles calcification in bones of adult rats. Calcif Tissue Int.; 66: 430-4.
• Hoyland JA, Thomas JT, Donn R, Marriott A, Ayad S, Boot-Handford RP, Grant ME, Freemont AJ. (1991) Distribution of type X collagen mRNA in normal and osteoarthritic human cartilage. Bone Miner.; 15: 151-63.
• Hsu, HHT. (1992a) Further studies on ATP-mediated Ca deposition by isolated matrix vesicles. Bone Miner.; 17: 279-83.
• Hsu HHT. (1992b) In vitro calcium deposition by rachitic rat matrix vesicles: nucleoside triphosphate supported calcium deposition. Biochim Biophys Acta.; 1116: 227-33.
• Hsu HHT, Anderson HC. (1978) Calcification of isolated matrix vesicles and reconstituted vesicles from fetal bovine cartilage. Proc Natl Acad Sci U S A.; 75: 3805-8.
• Hsu HHT, Anderson HC. (1995) A role for ATPase in the mechanisms of ATP-dependent Ca and phosphate deposition by isolated rachitic matrix vesicles. Int J Biochem Cell Biol.; 27: 1349-56.
• Hsu HHT, Anderson HC. (1996) Evidence of the presence of a specific ATPase responsible for ATP-initiated calcification by matrix vesicles isolated from cartilage and bone. J Biol Chem.; 271: 26383-8.
• Hsu HHT, Camacho NP, Anderson HC. (1999) Further characterization of ATP-initiated calcification by matrix vesicles isolated from rachitic rat cartillage. Membrane perturbation by detergents and deposition of calcium pyrophosphate by rachitic matrix vesicles. Biochim Biophys Acta.; 1416: 320-32.
• Huang R, Rosenbach M, Vaughn R, Provvedini D, Rebbe N, Hickman S, Goding J, Terkeltaub R. (1994) Expression of the murine plasma cell nucleotide pyrophosphohydrolase PC-1 is shared by human liver, bone, and cartilage cells. Regulation of PC-1 expression in osteosarcoma cells by transforming growth factor-beta. J Clin Invest.; 94: 560-7.
• Hung CT, Allen FD, Mansfield KD, Shapiro IM. (1997) Extracellular ATP modulates [Ca2+]i in retinoic acid-treated embryonic chondrocytes. Am J Physiol.; 272: C1611-7.
• Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA. (1996) Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J.; 317: 59-64.
• Isas JM, Cartailler JP, Sokolov Y, Patel DR, Langen R, Luecke H, Hall JE, Haigler HT. (2000) Annexins V and XII insert into bilayers at mildly acidic pH and form ion channels. Biochemistry.; 39: 3015-22.
• Isas JM, Patel DR, Jao C, Jayasinghe S, Cartailler JP, Haigler HT, Langen R. (2003) Global structural changes in annexin 12: The roles of phospholipid, Ca2+ and pH. J Biol Chem.; 278: 30227-34.
• Ishitsuka R. (2000) Interaction of annexins with glycosaminoglycans. Trends Glycosci Glycotechnol.; 12: 192-5.
• Ishitsuka R, Kojima K, Utsumi H, Ogawa H, Matsumoto I. (1998) Glycosaminoglycan binding properties of annexin IV, V, and VI. J Biol Chem.; 273: 9935-41.
• Jacenko O, LuValle PA, Olsen BR. (1993) Spondylometaphyseal dysplasia in mice carrying a dominant negative mutation in a matrix protein specific for cartilage-to-bone transition. Nature.; 365: 56-61.
• Johnson K, Moffa A, Chen Y, Pritzker K, Goding J, Terkeltaub R. (1999a) Matrix vesicle plasma cell membrane glycoprotein-1 regulates mineralization by murine osteoblastic MC3T3 cells. J Bone Miner Res.; 14: 883-92.
• Johnson K, Vaingankar S, Chen Y, Moffa A, Goldring MB, Sano K, Jin-Hua P, Sali A, Goding J, Terkeltaub R. (1999b) Differential mechanisms of inorganic pyrophosphate production by plasma cell membrane glycoprotein-1 and B10 in chondrocytes. Arthritis Rheum.; 42: 1986-97.
• Kam W, Clauser E, Kim YS, Kan YW, Rutter W. (1985) Cloning, sequencing, and chromosomal localization of human term placental alkaline phosphatase cDNA. Proc Natl Acad Sci U S A.; 82: 8715-9.
• Kaneko N, Ago H, Matsuda R, Inagaki E, Miyano M. (1997a) Crystal structure of annexin V with its ligand K-201 as a calcium channel activity inhibitor. J Mol Biol.; 274: 16-20.
• Kaneko N, Matsuda R, Toda M, Shimamoto K. (1997b) Inhibition of annexin V-dependent Ca2+ movement in large unilamellar vesicles by K201, a new 1,4-benzothiazepine derivative. Biochim Biophys Acta.; 1330: 1-7.
• King KB, Chubinskaya S, Reid DL, Madsen LH, Mollenhauer J. (1997) Absence of cell-surface annexin V is accompanied by defective collagen matrix binding in the Swarm rat chondrosarcoma. J Cell Biochem.; 65: 131-44.
• Kirilenko A, Golczak M, Pikula S, Bandorowicz-Pikula J. (2001) GTP-binding properties of the membrane-bound form of porcine liver annexin VI. Acta Biochim Polon.; 48: 851-65.
• Kirilenko A, Golczak M, Pikula S, Buchet R, Bandorowicz-Pikula J. (2002) GTP-induced membrane binding and ion channel activity of annexin VI: is annexin VI a GTP biosensor? Biophys J.; 82: 2737-45.
• Kirsch T, Pfaffle M. (1992) Selective binding of anchorin CII (annexin V) to type II and X collagen and to chondrocalcin (C-propeptide of type II collagen). Implications for anchoring function between matrix vesicles and matrix proteins. FEBS Lett.; 310: 143-7.
• Kirsch T, Wuthier RE. (1994) Stimulation of calcification of growth plate cartilage matrix vesicles by binding to type II and X collagens. J Biol Chem.; 269: 11462-9.
• Kirsch T, Ishikawa Y, Mwale F, Wuthier RE. (1994) Roles of the nucleational core complex and collagens (types II and X) in calcification of growth plate cartilage matrix vesicles. J Biol Chem.; 269: 20103-9.
• Kirsch T, Nah HD, Demuth DR, Harrison G, Golub EE, Adams SL, Pacifici M. (1997a) Annexin V-mediated calcium flux across membranes is dependent on the lipid composition: implications for cartilage mineralization. Biochemistry.; 36: 3359-67.
• Kirsch T, Nah HD, Shapiro IM, Pacifici M. (1997b) Regulated production of mineralization-competent matrix vesicles in hypertrophic chondrocytes. J Cell Biol.; 137: 1149-60.
• Kirsch T, Claassen H. (2000) Matrix vesicles mediate mineralization of human thyroid cartilage. Calcif Tissue Int.; 66: 292-97.
• Kirsch T, Harrison G, Golub EE, Nah HD. (2000a) The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage. J Biol Chem.; 275: 35577-83.
• Kirsch T, Swoboda B, Nah H. (2000b) Activation of annexin II and V expression, terminal differentiation, mineralization and apoptosis in human osteoarthritic cartilage. Osteoarthritis Cartilage.; 8: 294-302.
• Kohler G, Hering U, Zschornig O, Arnold K. (1997) Annexin V interaction with phosphatidylserine-containing vesicles at low and neutral pH. Biochemistry.; 36: 8189-94.
• Koprowski P, Kubalski A. (2001) Bacterial ion channels and their eukaryotic homologues. BioEssays.; 23: 1148-58.
• Kouri JB, Aguilera JM, Reyes J, Lozoya KA, Gonzalez S. (2000) Apoptotic chondrocytes from osteoarthrotic human articular cartilage and abnormal calcification of subchondral bone. J Rheumatol.; 27: 1005-19.
• Kourie JI, Wood HB. (2000) Biophysical and molecular properties of annexin-formed channels. Prog Biophys Mol Biol.; 73: 91-134.
• Li YC, Bolt MJ, Cao LP, Sitrin MD. (2001) Effects of vitamin D receptor inactivation on the expression of calbindins and calcium metabolism. Am J Physiol Endocrinol Metab.; 281: E558-64.
• Lian JB, Stein GS. (1996) Osteoblast biology. Academic Press, San Diego.
• Magnusson P, Larsson L, Magnusson M, Davie MWJ, Sharp CA. (1999) Isoforms of bone alkaline phosphatase: Characterization and origin in human trabecular and cortical bone. J Bone Miner Res.; 14: 1926-33.
• Majeska RJ, Holwerda DL, Wuthier RE. (1979) Localization of phosphatidylserine in isolated chick epiphyseal cartilage matrix vesicles with trinitrobenzenesulfonate. Calcif Tissue Int.; 27: 41-6.
• Marks SC, Popoff SN. (1988) Bone cell biology: the regulation of development, structure and function in the skeleton. Am J Anat.; 183: 1-44.
• Megli FM, Selvaggi M, De Lisi A, Quagliariello E. (1995) EPR study of annexin V-cardiolipin Ca-mediated interaction in phospholipids vesicles and isolated mitochondria. Biochim Biophys Acta.; 1236: 273-8.
• Megli FM, Mattiazzi M, Di Tullio T, Quagliariello E. (2000) Annexin V binding perturbs the cardiolipin fluidity gradient in isolated mitochondria. Can it affect mitochondrial function? Biochemistry.; 39: 5534-42.
• Millán JL. (1986) Molecular cloning and sequence analysis of human placental alkaline phosphatase. J Biol Chem.; 261: 3112-5.
• Millán JL, Manes T. (1988) Seminoma-derived Nagao isozyme is encoded by a germ-cell alkaline phosphatase gene. Proc Natl Acad Sci U S A.; 85: 3024-8.
• Mobasheri A, Carter SD, Martin-Vasallo P, Shakibaei M. (2002) Integrins and stretch activated ion channels; putative components of functional cell surface mechanoreceptors in articular chondrocytes. Cell Biol Int.; 26: 1-18.
• Mollenhauer J, Mok MT, King KB, Gupta M, Chubinskaya S, Koepp H, Cole AA. (1999) Expression of anchorin CII (cartilage annexin V) in human young, normal adult, and osteoarthritic cartilage. J Histochem Cytochem.; 47: 209-20.
• Montesuit C, Caverzasio J, Bonjour JP. (1991) Characterization of a Pi transport system in cartilage matrix vesicles: potential role in the calcification process. J Biol Chem.; 266: 17791-7.
• Mornet E, Stura E, Lia-Baldini AS, Stigbrand T, Menez A, Le Du MH. (2001) Structural evidence for a functional role of human tissue-nonspecific alkaline phosphatase in bone mineralization. J Biol Chem.; 276: 31171-8.
• Moss DW. (1992) Perspectives in alkaline phosphatase research. Clin Chem.; 38: 2486-92.
• Nakamura I, Ikegawa S, Okawa A, Okuda S, Koshizuka Y, Kawaguchi H, Nakamura K, Koyama T, Goto S, Toguchida J, Matsushita M, Ochi T, Takaoka K, Nakamura Y. (1999) Association of the human NPPS gene with ossification of the posterior longitudinal ligament of the spine (OPLL). Hum Genet.; 104: 492-7.
• Narisawa S, Fröhlander N, Millan JL. (1997) Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn.; 208: 432-46.
• Nawawi H, Samson D, Apperley J, Girgis S. (1996) Biochemical markers in patients with multiple myeloma. Clin Chim Acta.; 253: 61-77.
• Nie D, Ishikawa Y, Yoshimori T, Wuthier RE, Wu LNY. (1998) Retinoic acid treatment elevates matrix metalloproteinase-2 protein and mRNA levels in avian growth plate chondrocyte cultures. J Cell Biochem.; 68: 90-9.
• Noda M, Yoon K, Rodan GA, Koppel DE. (1987) High lateral mobility of endogenous and transfected alkaline phosphatase: a phosphatidylinositol-anchored membrane protein. J Cell Biol.; 105: 1671-7.
• Okawa A, Nakamura I, Goto S, Moriya H, Nakamura Y, Ikegawa S. (1998) Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat Genet.; 19: 271-3.
• Oling F, Santos JS, Govorukhina N, Mazeres-Dubut C, Bergsma-Schutter W, Oostergetel G, Keegstra W, Lambert O, Lewit-Bentley A, Brisson A. (2000) Structure of membrane-bound annexin A5 trimers: a hybrid cryo-EM-X-ray crystallography study. J Mol Biol.; 304: 561-73.
• Oling F, Bergsma-Schutter W, Brisson A. (2001) Trimers, dimers of trimers, and trimers of trimers are common building blocks of annexin A5 two-dimensional crystals. J Struct Biol.; 133: 55-63.
• Pfander D, Swoboda B, Kirsch T. (2001) Expression of early and late differentiation markers (proliferating cell nuclear antigen, syndecan-3, annexin VI, and alkaline phosphatase) by human osteoarthritic chondrocytes. Am J Pathol.; 159: 1777-83.
• Pizauro JM, Ciancaglini P, Leone FA. (1994) Osseous plate alkaline phosphatase is anchored by GPI. Braz J Med Biol Res.; 27: 453-6.
• Poole AR. (2001) Cartilage in health and disease. In: Arthritis and allied conditions. A textbook of rheumatology. 14th edn. Koopman WJ, ed. pp226-84. Lippincott Williams & Wilkins.
• Pullig O, Weseloh G, Ronneberger D, Kakonen S, Swoboda B. (2000) Chondrocyte differentiation in human osteoarthritis: expression of osteocalcin in normal and osteoarthritic cartilage and bone. Calcif Tissue Int.; 67: 230-40.
• Radisson J, Angrand M, Chavassieux P, Roux B, Azzar G. (1996) Differential solubilization of osteoblastic alkaline phosphatase from human primary bone cell cultures. Int J Biochem Cell Biol.; 28: 421-30.
• Raghu P, Ravinder P, Sivakumar B. (2003) A new method for purification of human plasma retinol-binding protein and transthyretin. Biotechnol Appl Biochem.; 38: 19-24.
• Rattner A, Sabido O, Le J, Vico L, Massoubre C, Frey J, Chamson A. (2000) Mineralization and alkaline phosphatase in collagen lattices populated by human osteoblasts. Calcif Tissue Int.; 66: 35-42.
• Rezende AA, Pizauro JM, Ciancaglini P, Leone FA. (1994) Phosphodiesterase activity is a novel property of alkaline phosphatase from osseous plate. Biochem J.; 301: 517-22.
• Risteli L, Risteli J. (1993) Biochemical markers of bone metabolism. Ann Med.; 25: 385-93.
• Robison R. (1924) The possible significance of hexosephosphoric esters in ossification. Biochem J.; 17: 286-93.
• Romanello M, Pani B, Bicego M, D'Andrea P. (2001) Mechanically induced ATP release from human osteoblastic cells. Biochem Biophys Res Commun.; 289: 1275-81.
• Quinn TM, Grodzinsky AJ, Buschmann MD, Kim YJ, Hunziker EB. (1998) Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. J Cell Sci.; 111: 573-83.
• Sauer GR, Genge BR, Wu LN, Donachy JE. (1994) A facilitative role for carbonic anhydrase activity in matrix vesicle mineralization. Bone Miner.; 26: 69-79.
• Schwartz Z, Boyan B. (1988) The effects of vitamin D metabolites on phospholipase A2 activity of growth zone and resting zone cartilage cells in vitro. Endocrinology.; 122: 2191-8.
• Shakibaei M, Mobasheri A. (2003) Beta1-integrins co-localize with Na, K-ATPase, epithelial sodium channels (ENaC) and voltage activated calcium channels (VACC) in mechanoreceptor complexes of mouse limb-bud chondrocytes. Histol Histopathol.; 18: 343-51.
• Skrtic D, Eanes ED. (1994) Effect of 1-hydroxyethylidene-1,1-biphosphonate on membrane-mediated calcium phosphate formation in model liposomal suspensions. Bone Miner.; 26: 219-29.
• Stechschulte DJ Jr, Morris DC, Silverton SF, Anderson HC, Vaananen HK. (1992) Presence and specific concentration of carbonic anhydrase II in matrix vesicles. Bone Miner.; 17: 187-91.
• Suzuki Y, Kubota T, Koizumi T, Satoyoshi M, Teranaka T, Kawase T, Ikeda T, Yamaguchi A, Saito S, Mikuni-Takagaki Y. (1996) Extracellular processing of bone and dentin proteins in matrix mineralization. Connect Tissue Res.; 35: 223-9.
• Swain LD, Schwartz Z, Boyan BD. (1992) Regulation of matrix vesicle phospholipid metabolism is cell maturation-dependent. Bone Miner.; 17: 192-6.
• Takagi H, Asano Y, Yamakawa N, Matsumoto I, Kimata K. (2002) Annexin 6 is a putative cell surface receptor for chondroitin sulfate chains. J Cell Sci.; 115: 3309-18.
• Taylor MG, Simkiss K, Simmons J, Wu LN, Wuthier RE. (1998) Structural studies of a phosphatidyl serine-amorphous calcium phosphate complex. Cell Mol Life Sci.; 54: 196-202.
• Tenenbaum HC. (1981) Role of organic phosphate in mineralization of bone in vitro. J Dent Res.; 60: 1586-9.
• Tenenbaum HC. (1987) Levamisole and inorganic pyrophosphate inhibit β-glycerophosphate induced mineralization of bone formed in vitro. Bone Miner.; 3: 13-26.
• Terkeltaub R, Rosenbach M, Fong F, Goding J. (1994) Causal link between nucleotide pyrophosphohydrolase overactivity and increased intracellular inorganic pyrophosphate generation demonstrated by transfection of cultured fibroblasts and osteoblasts with plasma cell membrane glycoprotein-1. Relevance to calcium pyrophosphate dihydrate deposition disease. Arthritis Rheum.; 37: 934-41.
• Valhmu WB, Wu LN, Wuthier RE. (1990) Effects of Ca/Pi ratio, Ca2+ x Pi ion product, and pH of incubation fluid on accumulation of 45Ca2+ by matrix vesicles in vitro. Bone Miner.; 8: 195-209.
• Von der Mark K, Mollenhauer J. (1997) Annexin V interactions with collagen. Cell Mol Life Sci.; 53: 539-45.
• Wang W, Kirsch T. (2002) Retinoic acid stimulates annexin-mediated growth plate chondrocyte mineralization. J Cell Biol.; 157: 1061-9.
• Wang W, Xu J, Kirsch T. (2003) Annexin-mediated Ca2+ influx regulates growth plate chondrocyte maturation and apoptosis. J Biol Chem.; 278: 3762-9.
• White AH, Watson RE, Newman B, Freemont AJ, Wallis GA. (2002) Annexin VIII is differentially expressed by chondrocytes in the mammalian growth plate during endochondral ossification and in osteoarthritic cartilage. J Bone Miner Res.; 17: 1851-8.
• Whyte MP. (1994) Hypophosphatasia and the role of alkaline phosphatase in skeletal mineralization. Endocrinol Rev.; 15: 439-61.
• Whyte MP. (2001) Hypophosphatasia. In: The metabolic and molecular bases of inherited diseases. Seriver CR, Beaudet AL, Sly WS, Valle D, Childs B, Kinzler KW, Vogelstein B, eds, pp 5313-29. McGraw-Hill, New York.
• 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: 25084-94.
• Wu LN, Genge BR, Sauer GR, Wuthier RE. (1996) Characterization and reconstitution of the nucleational complex responsible for mineral formation by growth plate cartilage matrix vesicles. Connect Tissue Res.; 35: 309-15.
• Wu LN, Genge BR, Dunkelberger DG, LeGeros RZ, Concannon B, Wuthier RE. (1997a) Physicochemical characterization of the nucleational core of matrix vesicles. J Biol Chem.; 272: 4404-11.
• Wu LN, Wuthier MG, Genge BR, Wuthier RE. (1997b) In situ levels of intracellular Ca2+ and pH in avian growth plate cartilage. Clin Orthop.; 335: 310-24.
• Wu LNY, Ishikawa Y, Nie D, Genge BR, Wuthier RE. (1997c) Retinoic acid stimulates matrix calcification and initiates type I collagen synthesis in primary cultures of avian weight-bearing growth plate chondrocytes. J Cell Biochem.; 65: 209-30.
• Wu LNY, Genge BR, Kang MW, Arsenault AL, Wuthier RE. (2002a) Changes in phospholipid extractability and composition accompany mineralization of chicken growth plate cartilage matrix vesicles. J Biol Chem.; 277: 5126-33.
• Wu LNY, Guo Y, Genge BR, Ishikawa Y, Wuthier RE. (2002b) Transport of inorganic phosphate in primary cultures of chondrocytes isolated from the tibial growth plate of normal adolescent chickens. J Cell Biochem.; 86: 475-89.
• Wu QQ, Chen Q. (2000) Mechanoregulation of chondrocyte proliferation, maturation, and hypertrophy: ion-channel dependent transduction of matrix deformation signals. Exp Cell Res.; 256: 383-91.
• Wuthier RE. (1968) Lipids of mineralizing epiphyseal tissues in the bovine fetus. J Lipid Res.; 9: 68-78.
• Wuthier RE. (1975) Lipid composition of isolated epiphyseal cartilage cells, membrane and matrix vesicles. Biochim Biophys Acta.; 409: 128-43.
• Wuthier RE, Majeska RJ, Collins GM. (1977) Biosynthesis of matrix vesicles in epiphyseal cartilage. I. In vivo incorporation of 32P orthophosphate into phospholipids of chondrocyte membrane, and matrix vesicle fractions. Calcif Tissue Res.; 23: 135-9.
• Wuthier RE, Wians FH Jr, Giancola MS, Dragic SS. (1978) In vitro biosynthesis of phospholipids by chondrocytes and matrix vesicles of epiphyseal cartilage. Biochemistry.; 17: 1431-6.
• Yellowley CE, Haut-Donahue T, Jacobs C, Donahue H. (2002) Annexin V contributes to a mechanotransduction mechanism in osteoblasts. Biophys J.; 82: 1306.