An asparagine at position 417 of tissue-nonspecific alkaline phosphatase is essential for its structure and function as revealed by analysis of the N417S mutation associated with severe hypophosphatasia

Molecular Genetics and Metabolism

Volumn 109, Issue 3, 2013, Pages 282-288

  Sultana, Sara ^a   Al Shawafi, Hiba A ^a   Makita, Saori ^a   Sohda, Miwa ^a   Amizuka, Norio ^b   Takagi, Ritsuo ^a   Oda, Kimimitsu ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Dimerization; Hypophosphatasia; Inborn error of metabolism; Mineralization; Tissue nonspecific alkaline phosphatase

Indexed keywords

ALKALINE PHOSPHATASE; ASPARAGINE; ASPARAGINE LINKED OLIGOSACCHARIDE; ASPARTIC ACID; DIMER; GLUTAMINE; SERINE; TISSUE NONSPECIFIC ALKALINE PHOSPHATASE; UNCLASSIFIED DRUG;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ARTICLE; CATALYSIS; CELL STRAIN COS1; CELL SURFACE; CELLULAR DISTRIBUTION; CHO CELL; DIMERIZATION; GENE EXPRESSION SYSTEM; HYPOPHOSPHATASIA; INBORN ERROR OF METABOLISM; LOSS OF FUNCTION MUTATION; MISSENSE MUTATION; NONHUMAN; POINT MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUCROSE DENSITY GRADIENT CENTRIFUGATION; TRANSIENT EXPRESSION; WILD TYPE;

EID: 84891372414     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2013.04.016     Document Type: Article

References (38)

1. M.P. Whyte, in: C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, B. Childs, K.W. Kinzler (Eds.), 8th ed., The Metabolic and Molecular Bases of Inherited Diseases, IV, McGraw-Hill, New York, 2002, pp. 5319-5329.
2. J.L. Millán, Mammalian Alkaline Phosphatases: From Biology to Applications in Medicine and Biotechnology, WILEY-VCH Verlag GmbH & Co., KGaA, Weinheim, 2006.
3. E. Mornet, Hypophosphatasia orphanet, J. Rare Dis. 2 (2007) 40.
4. M.P. Whyte, Physiological role of alkaline phosphatase explored in hypophosphatasia, Ann. N. Y. Acad. Sci. 1192 (2010) 190-200.
5. K.G. Waymire, J.D. Mahuren, J.M. Jaje, T.R. Guilarte, S.P. Coburn, G.R. MacGregor, Mice lacking tissue non-specific alkaline phosphatase die from seizures due to defective metabolism of vitamin B-6, Nat. Genet. 11 (1995) 45-51.
6. S. Narisawa, N. Fröhlander, J.L. Millán, Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia, Dev. Dyn. 208 (1997) 432-446.
7. K.N. Fedde, L. Blair, J. Silverstein, S.P. Coburn, L.M. Ryan, R.S. Weinstein, K. Waymire, S. Narisawa, J.L. Millán, G.R. MacGregor, M.P. Whyte, Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia, J. Bone Miner. Res. 14 (1999) 2015-2026.
8. R.G. Russell, S. Bisaz, A. Donath, D.B. Morgan, H. Fleisch, Inorganic pyrophosphate in plasma in normal persons and in patients with hypophosphatasia, osteogenesis imperfect, and other disorders of bone, J. Clin. Invest. 50 (1971) 961-969.
9. M. Nasu, M. Ito, Y. Ishida, N. Numa, K. Komaru, N. Nomura, K. Oda, Aberrant interchain disulfide bridge of tissue-nonspecific alkaline phosphatase with an Arg433-Cys substitution associated with severe hypophosphatasia, FEBS J. 273 (2006) 5612-5624.
10. N. Numa, Y. Ishida, M. Nasu, M. Sohda, Y. Misumi, T. Noda, K. Oda, Molecular basis of perinatal hypophosphatasia with tissue-nonspecific alkaline phosphatase bearing a conservative replacement of valine by alanine at position 406. Structural importance of the crown domain, FEBS J. 275 (2008) 2727-2737.
11. H. Shibata, M. Fukushi, A. Igarashi, Y. Misumi, Y. Ikehara, Y. Ohashi, K. Oda, Defective intracellular transport of tissue-nonspecific alkaline phosphatase with an Ala162-Thr mutation associated with lethal hypophosphatasia, J. Biochem. (Tokyo) 123 (1998) 968-977.
12. M. Fukushi-Irie, M. Ito, Y. Amaya, N. Amizuka, H. Ozawa, S. Omura, Y. Ikehara, K. Oda, Possible interference between tissue-non-specific alkaline phosphatase with an Arg54-Cys substitution and a counterpart with an Asp277-Ala substitution found in a compound heterozygote associated with severe hypophosphatasia, Biochem. J. 348 (2000) 633-642.
13. Y. Ishida, K. Komaru, M. Ito, Y. Amaya, S. Kohno, K. Oda, Tissue-nonspecific alkaline phosphatase with an Asp289-Val mutation fails to reach the cell surface and undergoes proteasome-mediated degradation, J. Biochem. (Tokyo) 134 (2003) 63-70.
14. M. Ito, N. Amizuka, H. Ozawa, K. Oda, Retention at the cis-Golgi and delayed degradation of tissue-non-specific alkaline phosphatase with an Asn153 to Asp substitution, a cause of perinatal hypophosphatasia, Biochem. J. 361 (2002) 473-480.
15. I. Brun-Heath, A.S. Lia-Baldini, S. Maillard, A. Taillandier, B. Utsch, M.E. Nunes, J.L. Serre, E. Mornet, Delayed transport of tissue-nonspecific alkaline phosphatase with missense mutations causing hypophosphatasia, Eur. J. Med. Genet. 50 (2007) 367-378.
16. G. Cai, T. Michigami, T. Yamamoto, N. Yasui, K. Satomura, M. Yamagata, M. Shima, S. Nakajima, S. Mushiake, S. Okada, K. Ozono, Analysis of localization of mutated tissue-nonspecific alkaline phosphatase proteins associated with neonatal hypophosphatasia using green fluorescent protein chimeras, J. Clin. Endocrinol. Metab. 83 (1998) 3936-3942.
17. K. Komaru, Y. Ishida, Y. Amaya, M. Goseki-Sone, H. Orimo, K. Oda, Novel aggregate formation of a frame-shift mutant protein of tissue-nonspecific alkaline phosphatase is ascribed to three cysteine residues in the C-terminal extensionm, retarded secretion and proteasomal degradation, FEBS J. 272 (2005) 1704-1717.
18. Y. Satou, H.A. Al-Ahawafi, S. Sultana, S. Makita, M. Sohda, K. Oda, Disulfide bonds are critical for tissue-nonspecific alkaline phosphatase function revealed by analysis of mutant proteins bearing a C201-Y or C489-S substitution associated with severe hypophosphatasia, Biochim. Biophys. Acta 1822 (2012) 581-588.
19. C. Segi, E. Mornet, J. Troeger, T. Voigtlaender, Perinatal hypophosphatasia: radiology, pathology and molecular biology studies in a family harboring a splicing mutation (648 + 1A) and a novelmissensemutation (N400S) in the tissue-nonspecific alkaline phosphatase (TNSALP) gene, Am. J. Med. Genet. 103 (2001) 235-240.
20. S. Makita, H.A. Al-Shawafi, S. Sultana, M. Sohda, S. Nomura, K. Oda, Adimerization defect caused by a glycine substitution at position 420 by serine in tissue-nonspecific alkaline phosphatase associated with perinatal hypophosphatasia, FEBS J. 279 (2012) 4327-4337.
21. U.K. Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227 (1970) 680-685.
22. S. Hashimoto, T. Toen, Effect of zinc in the glycine buffer on detection of alkaline phosphatase activity after polyacrylamide gel electrophoresis, Jpn. J. Electrophor. 44 (2000) 15-19, (in Japanese).
23. K. Oda, Y. Amaya, M. Fukushi-Irie, Y. Kinameri, K. Ohsuye, I. Kubota, S. Fujimura, J. Kobayashi, A general method for rapid purification of soluble versions of glycosylphosphatidylinositol-anchored proteins expressed in insect cells: an application for human tissue-nonspecific alkaline phosphatase, J. Biochem. (Tokyo) 126 (1999) 694-699.
24. E. Mornet, E. Stura, A.S. Lia-Baldini, T. Stigbrand, A. Ménez, M.H. Le Du, Structural evidence for a functional role of human tissue nonspecific alkaline phosphatase in bone mineralization, J. Biol. Chem. 276 (2001) 31171-31178.
25. M.H. Le Du, T. Stigbrand, M.J. Taussig, A. Menez, E.A. Stura, Crystal structure of alkaline phosphatase from human placenta at 1.8 A resolution. Implication for substrate specificity, J. Biol. Chem. 276 (2001) 9158-9165.
26. M.H. Le Du, J.L. Millán, Structural evidence of functional divergence in human alkaline phosphatases, J. Biol. Chem. 277 (2002) 49808-49814.
27. D. Fauvert, I. Brun-Heath, A.S. Lia-Baldini, L. Bellazi, A. Taillandier, J.L. Serre, P. de Mazancourt, E. Mornet, Mildform forms of hypophosphatasia most result from dominant negative effect of severe alleles or from compound heterozygosity for severe and moderate alleles, BMC Med. Genet. 10 (2009) 51.
28. A.S. Lia-Baldini, I. Brun-Heath, C. Carrion, B. Simon-Bouy, J.L. Serre, M.E. Numes, E. Mornet, A new mechanism of dominance in hypophosphatasia: the mutated protein can disturb the cell localization of the wild-type protein, Hum. Genet. 123 (2008) 429-432.
29. Y. Ishida, K. Komaru, K. Oda, Molecular characterization of tissue-nonspecific alkaline phosphatase with an Ala to Thr substitution at position 116 associated with dominantly inherited hypophosphatasia, Biochim. Biophys. Acta 1812 (2011) 326-332.
30. M.P. Whyte, J. Kurtzberg, W.H. McAlister, S. Mumm, M.N. Podgornik, S.P. Coburn, L.M. Ryan, C.R. Miller, G.S. Gottesman, A.K. Smith, J. Douville, B. Waters-Pick, R.D. Armstrong, P.L. Martin, Marrow cell transplantation for infantile hypophosphatasia, J. Bone Miner. Res. 18 (2003) 624-636.
31. R.A. Cahill, D. Wenkert, S.A. Perlman, A. Steele, S.P. Coburn, W.H. McAlister, S. Mumm, M.P. Whyte, Infantile hypophosphatasia: transplantation therapy trial using bone fragments and cultured osteoblasts, J. Clin. Endocrinol. Metab. 92 (2007) 2923-2930.
32. M.P. Whyte, S. Mumm, C. Deal, Adult hypophosphatasia treated with teriparatide, J. Clin. Endocrinol. Metab. 92 (2007) 1203-1208.
33. J.L. Millán, S. Narisawa, I. Lemire, T.P. Loisel, G. Boileau, P. Leonard, S. Gramatikova, R. Terkeltaub, N.P. Camacho, M.D. McKee, P. Crine, M.P. Whyte, Enzyme replacement therapy for murine hypophosphatasia, J. Bone Miner. Res. 23 (2008) 777-787.
34. M.D. McKee, Y. Nakano, D.L. Masica, J.J. Gray, I. Lemire, R. Heft, M.P. Whyte, P. Crine, J.L. Millán, Enzyme replacement therapy prevents dental defects in a model of hypophosphatasia, J. Dent. Res. 90 (4) (2011 Apr) 470-476.
35. M.C. Yadav, I. Lemire, P. Leonard, G. Boileau, L. Blond, M. Beliveau, E. Cory, R.L. Sah, M.P. Whyte, P. Crine, J.L. Millán, Dose response of bone-targeted enzyme replacement for murine hypophosphatasia, Bone 9 (2011) 250-256.
36. Y. Katsube, N. Kotobuki, M. Tadokoro, R. Kanai, T. Taketani, S. Yamaguchi, H. Ohgushi, Restoration of cellular function of mesenchymal stem cells from a hypophosphatasia patient, Gene Ther. 17 (2010) 494-502.
37. S. Yamamoto, H. Orimo, T. Matsumoto, O. Iijima, S. Narisawa, T. Maeda, J.L. Millán, T. Shimada, Prolonged survival and phenotypic correction of Akp2(-/-) hypophosphatasia mice by lentiviral gene therapy, J. Bone Miner. Res. 26 (2011) 135-142.
38. M.P. Whyte, C.R. Greenberg, N.J. Salman, M.B. Bober, W.H. McAlister, D. Wenkert, B.J. Van Sickle, J.H. Simmons, T.S. Edgar, M.L. Bauer, M.A. Hamdan, N. Bishop, R.E. Lutz, M. McGinn, S. Craig, J.N. Moore, J.W. Taylor, R.H. Cleveland, W.R. Cranley, R. Lim, T.D. Thacher, J.E. Mayhew, M. Downs, J.L. Millán, A.M. Skrinar, P. Crine, H. Landy, Enzyme-replacement therapy in life-threatening hypophosphatasia, N. Engl. J. Med. 366 (2012) 904-913.