Osteoblast tissue-nonspecific alkaline phosphatase antagonizes and regulates PC-1.

Tissue-nonspecific alkaline phosphatase (TNAP) is essential for bone matrix mineralization, but the central mechanism for TNAP action remains undefined. We observed that ATP-dependent (45)Ca precipitation was decreased in calvarial osteoblast matrix vesicle (MV) fractions from TNAP-/- mice, a model of infantile hypophosphatasia. Because TNAP hydrolyzes the mineralization inhibitor inorganic pyrophosphate (PP(i)), we assessed phosphodiesterase nucleotide pyrophosphatase (PDNP/NTPPPH) activity, which hydrolyzes ATP to generate PP(i). Plasma cell membrane glycoprotein-1 (PC-1), but not the isozyme B10 (also called PDNP3) colocalized with TNAP in osteoblast MV fractions and pericellular matrix. PC-1 but not B10 increased MV fraction PP(i) and inhibited (45)Ca precipitation by MVs. TNAP directly antagonized inhibition by PC-1 of MV-mediated (45)Ca precipitation. Furthermore, the PP(i) content of MV fractions was greater in cultured TNAP-/- than TNAP+/+ calvarial osteoblasts. Paradoxically, transfection with wild-type TNAP significantly increased osteoblast MV fraction NTPPPH. Specific activity of NTPPPH also was twofold greater in MV fractions of osteoblasts from TNAP+/+ mice relative to TNAP-/- mice. Thus TNAP attenuates PC-1/NTPPPH-induced PP(i) generation that would otherwise inhibit MV-mediated mineralization. TNAP also paradoxically regulates PC-1 expression and NTPPPH activity in osteoblasts.

[1]  J. Millán,et al.  Functional Characterization of Osteoblasts and Osteoclasts from Alkaline Phosphatase Knockout Mice , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[2]  K. Sano,et al.  Genomic structure and promoter analysis of the ecto-phosphodiesterase I gene (PDNP3) expressed in glial cells. , 1999, Biochimica et biophysica acta.

[3]  R. Terkeltaub,et al.  Differential mechanisms of inorganic pyrophosphate production by plasma cell membrane glycoprotein-1 and B10 in chondrocytes. , 1999, Arthritis and rheumatism.

[4]  R. Weinstein,et al.  New Developments in the Pathogenesis and Treatment of Steroid‐Induced Osteoporosis , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[5]  Ying Chen,et al.  Matrix Vesicle Plasma Cell Membrane Glycoprotein‐1 Regulates Mineralization by Murine Osteoblastic MC3T3 Cells , 1999, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[6]  J. Gibrat,et al.  Correlations of genotype and phenotype in hypophosphatasia. , 1999, Human molecular genetics.

[7]  G. Gross,et al.  Developmental expression analysis of murine autotaxin (ATX) , 1999, Mechanisms of Development.

[8]  H. Anderson,et al.  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. , 1999, Biochimica et biophysica acta.

[9]  Yusuke Nakamura,et al.  Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine , 1998, Nature Genetics.

[10]  S. Ōmura,et al.  Intracellular retention and degradation of tissue-nonspecific alkaline phosphatase with a Gly317-->Asp substitution associated with lethal hypophosphatasia. , 1998, Biochemical and biophysical research communications.

[11]  Y. Misumi,et al.  Defective intracellular transport of tissue-nonspecific alkaline phosphatase with an Ala162-->Thr mutation associated with lethal hypophosphatasia. , 1998, Journal of biochemistry.

[12]  F. A. Leone,et al.  Inorganic pyrophosphate-phosphohydrolytic activity associated with rat osseous plate alkaline phosphatase. , 1998, Cellular and molecular biology.

[13]  R. Terkeltaub,et al.  Ecto‐phosphodiesterase/pyrophosphatase of lymphocytes and non‐lymphoid cells: structure and function of the PC‐1 family , 1998, Immunological reviews.

[14]  H. Anderson,et al.  Matrix vesicles in osteomalacic hypophosphatasia bone contain apatite-like mineral crystals. , 1997, The American journal of pathology.

[15]  A. Rosenthal,et al.  Transglutaminase activity in aging articular chondrocytes and articular cartilage vesicles. , 1997, Arthritis and rheumatism.

[16]  J. Goding,et al.  Biochemical and molecular identification of distinct forms of alkaline phosphodiesterase I expressed on the apical and basolateral plasma membrane surfaces of rat hepatocytes , 1997, Hepatology.

[17]  A. Boskey,et al.  Matrix Vesicles Promote Mineralization in a Gelatin Gel , 1997, Calcified Tissue International.

[18]  J. Millán,et al.  Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia , 1997, Developmental dynamics : an official publication of the American Association of Anatomists.

[19]  Kimimitsu Oda,et al.  Immunolocalization of tissue non-specific alkaline phosphatase in mice , 1997, Histochemistry and Cell Biology.

[20]  H. Anderson,et al.  Evidence of the Presence of a Specific ATPase Responsible for ATP-initiated Calcification by Matrix Vesicles Isolated from Cartilage and Bone* , 1996, The Journal of Biological Chemistry.

[21]  R. Terkeltaub,et al.  Expression of the nucleoside triphosphate pyrophosphohydrolase PC‐1 is induced by basic fibroblast growth factor (bFGF) and modulated by activation of the protein kinase A and C pathways in osteoblast‐like osteosarcoma cells , 1996, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[22]  D. Mccarty,et al.  Specificity of a porcine 127-kd nucleotide pyrophosphohydrolase for articular tissues. , 1996, Arthritis and rheumatism.

[23]  A. Boskey,et al.  Lipids and biomineralizations. , 1996, Progress in histochemistry and cytochemistry.

[24]  A. Boskey,et al.  Matrix proteins and mineralization: an overview. , 1996, Connective tissue research.

[25]  D. Mccarty,et al.  Understanding inorganic pyrophosphate metabolism: toward prevention of calcium pyrophosphate dihydrate crystal deposition. , 1995, Annals of the rheumatic diseases.

[26]  H. Anderson Molecular biology of matrix vesicles. , 1995, Clinical orthopaedics and related research.

[27]  M. Paulsson,et al.  Transglutaminase-catalyzed matrix cross-linking in differentiating cartilage: identification of osteonectin as a major glutaminyl substrate , 1995, The Journal of cell biology.

[28]  M. Adolphe,et al.  Transglutaminase activity in rabbit articular chondrocytes in culture. , 1995, Biochimica et biophysica acta.

[29]  P. Henthorn,et al.  Alkaline phosphatase: placental and tissue-nonspecific isoenzymes hydrolyze phosphoethanolamine, inorganic pyrophosphate, and pyridoxal 5'-phosphate. Substrate accumulation in carriers of hypophosphatasia corrects during pregnancy. , 1995, The Journal of clinical investigation.

[30]  M. Whyte Hypophosphatasia and the role of alkaline phosphatase in skeletal mineralization. , 1994, Endocrine reviews.

[31]  A. Caswell,et al.  Modulation of ecto‐nucleoside triphosphate pyrophosphatase activity of human osteoblast‐like bone cells by 1α,25‐dihydroxyvitamin D3, 24R, 25‐dihydroxyvitamin D3, parathyroid hormone, and dexamethasone , 1994, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[32]  R. Russell,et al.  Transforming growth factor β increases ecto‐nucleoside triphosphate pyrophosphatase activity of human bone‐derived cells , 1994, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[33]  M. Whyte,et al.  Evidence against a role for alkaline phosphatase in the dephosphorylation of plasma membrane proteins: Hypophosphatasia fibroblast study , 1993, Journal of cellular biochemistry.

[34]  D. Rifkin,et al.  Requirement for transglutaminase in the activation of latent transforming growth factor-beta in bovine endothelial cells , 1993, The Journal of cell biology.

[35]  D. Morris,et al.  In vitro Ca deposition by rat matrix vesicles: is the membrane association of alkaline phosphatase essential for matrix vesicle-mediated calcium deposition? , 1993, The International journal of biochemistry.

[36]  P. Henthorn,et al.  Different missense mutations at the tissue-nonspecific alkaline phosphatase gene locus in autosomal recessively inherited forms of mild and severe hypophosphatasia. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[37]  L. Bonewald,et al.  Stimulation of matrix vesicle enzyme activity in osteoblast-like cells by 1,25(OH)2D3 and transforming growth factor β (TGFβ) , 1992 .

[38]  John J. Bozzola,et al.  Electron microscopy : principles and techniques for biologists , 1992 .

[39]  D. Cole,et al.  Pseudohypophosphatasia: aberrant localization and substrate specificity of alkaline phosphatase in cultured skin fibroblasts. , 1990, American journal of human genetics.

[40]  M. Blumenberg,et al.  A rapid and simple method for introducing specific mutations into any position of DNA leaving all other positions unaltered. , 1990, Nucleic acids research.

[41]  Rachow Jw,et al.  Inorganic pyrophosphate metabolism in arthritis. , 1988 .

[42]  M. Whyte,et al.  Normal activity of nucleoside triphosphate pyrophosphatase in alkaline phosphatase-deficient fibroblasts from patients with infantile hypophosphatasia. , 1986, The Journal of clinical endocrinology and metabolism.

[43]  E. Bonucci,et al.  Biochemical and immunohistochemical evidence that in cartilage an alkaline phosphatase is a Ca2+-binding glycoprotein , 1986, The Journal of cell biology.

[44]  R. Simpson,et al.  The murine plasma cell antigen PC-1: purification and partial amino acid sequence. , 1985, Journal of immunology.

[45]  J. Meyer,et al.  Can biological calcification occur in the presence of pyrophosphate? , 1984, Archives of biochemistry and biophysics.