Biochemical and thermodynamic characterization of mutated β1,4-galactosyltransferase 7 involved in the progeroid form of the Ehlers-Danlos syndrome

Biochemical Journal

Volumn 432, Issue 2, 2010, Pages 303-311

  Rahuel Clermont, Sophie ^a   Daligault, Franck ^a   Piet, Marie Helene ^a   Gulberti, Sandrine ^a   Netter, Patrick ^a   Branlant, Guy ^a   Magdalou, Jacques ^a   Lattard, Virginie ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

1,4 galactosyltransferase 7 ( 1,4 GalT7); Ehlers Danlos syndrome (EDS); Glycosaminoglycan (GAG) biosynthesis; Isothermal titration calorimetry (ITC); Substrate binding

Indexed keywords

EHLERS-DANLOS SYNDROMES; GALACTOSYLTRANSFERASE; GLYCOSAMINOGLYCANS; ISOTHERMAL TITRATION CALORIMETRY; SUBSTRATE BINDING;

BIOCHEMISTRY; BIOLOGICAL MEMBRANES; BIOSYNTHESIS; CALORIMETERS; CALORIMETRY; ESCHERICHIA COLI; GENE ENCODING; PROTEINS; TITRATION;

SUBSTRATES;

BETA1,4 GALACTOSYLTRANSFERASE 7; GALACTOSE; GALACTOSYLTRANSFERASE; GLYCOSAMINOGLYCAN; HYBRID PROTEIN; MALTOSE BINDING PROTEIN; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOHYDRATE TRANSPORT; CHO CELL; CONTROLLED STUDY; EHLERS DANLOS SYNDROME; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENE MUTATION; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROGERIA; PROTEIN EXPRESSION; THERMODYNAMICS; WILD TYPE;

ANIMALS; CHO CELLS; CLONING, MOLECULAR; CRICETINAE; CRICETULUS; EHLERS-DANLOS SYNDROME; GALACTOSYLTRANSFERASES; HUMANS; KINETICS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

ESCHERICHIA COLI;

EID: 78649568089     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100921     Document Type: Article

References (40)

1. Beighton, P., De Paepe, A., Steinmann, B., Tsipouras, P. and Wenstrup, R. J. (1998) Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK). Am. J. Med. Genet. 77, 31-37
2. Kresse, H., Rosthoj, S., Quentin, E., Hollmann, J., Glössl, J., Okada, S. and Tonnesen, T. (1987) Glycosaminoglycan-free small proteoglycan core protein is secreted by fibroblasts from a patient with a syndrome resembling progeroid. Am. J. Hum. Genet. 41, 436-453
3. Quentin, E., Gladen, A., Roden, L. and Kresse, H. (1990) A genetic defect in the biosynthesis of dermatan sulfate proteoglycan: galactosyltransferase I deficiency in fibroblasts from a patient with a progeroid syndrome. Proc. Natl. Acad. Sci. U.S.A. 87, 1342-1346
4. Faiyaz-Ul-Haque, M., Zaidi, S. H., Al-Ali, M., Al-Mureikhi, M. S., Kennedy, S., Al-Thani, G., Tsui, L. C. and Teebi, A. S. (2004) A novel missense mutation in the galactosyltransferase-I ( B4GALT7) gene in a family exhibiting facioskeletal anomalies and Ehlers-Danlos syndrome resembling the progeroid type. Am. J. Med. Genet. 128A, 39-45 (Pubitemid 38856815)
5. Gótte, M. and Kresse, H. (2005) Defective glycosaminoglycan substitution of decorin in a patient with progeroid syndrome is a direct consequence of two point mutations in the galactosyltransferase I (β4GalT-7) gene. Biochem. Genet. 43, 65-77
6. Seidler, D. G., Fayaz-Ul-Haque, M., Hansen, U., Yip, G. W., Zaidi, S. H. E., Teebi, A. S., Kiesel, L. and Gótte, M. (2006) Defective glycosylation of decorin and biglycan, altered collagen structure, and abnormal phenotype of the skin fibroblasts of an Ehlers-Danlos syndrome patient carrying the novel Arg270Cys substitution in galactosyltransferase I ((β4GalT-7). J. Mol. Med. 84, 583-594
7. Ruoslahti, E. and Yamaguchi, Y. (1991) Proteoglycans as modulators of growth factor activities. Cell 64, 867-869
8. Bandtlow, C. E. and Zimmermann, D. R. (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 80, 1267-1290
9. De Cat, B. and David, G. (2001) Developmental roles of the glypicans. Semin. Cell Dev. Biol. 12, 117-125
10. Knudson, C. B. and Knudson, W. (2001) Cartilage proteoglycans. Semin. Cell Dev. Biol. 12, 69-78
11. Rapraeger, A. C. (2001) Molecular interactions of syndecans during development. Semin. Cell Dev. Biol. 12, 107-116
12. Poole, A. R. (1986) Proteoglycans in health and disease: structures and functions. Biochem. J. 236, 1-14
13. Ruoslahti, E. (1989) Proteoglycans in cell regulation. J. Biol. Chem. 264, 13369-13372
14. Salmivirta, M., Lidholt, K. and Lindahl, U. (1996) Heparan sulfate: a piece of information. FASEB J. 10, 1270-1279
15. Taipale, J. and Keski-Oja, J. (1997) Growth factors in the extracellular matrix. FASEB J. 11, 51-59
16. Gótte, M., Spillmann, D., Yip, G. W., Versteeg, E., Echtermeyer, F. G., Van Kuppevelt, T. H. and Kiesel, L. (2008) Changes in heparan sulfate are associated with delayed wound repair, altered cell migration, adhesion and contractility in the galactosyltransferase I ((β4GalT-7) deficient form of Ehlers-Danlos syndrome. Hum. Mol. Genet. 17, 996-1009
17. Esko, J. D. and Zhang, L. (1996) Influence of core protein sequence on glycosaminoglycan assembly. Curr. Opin. Struct. Biol. 6, 663-670
18. Roden, L. (1980) The Biochemistry of Glycoproteins and Proteoglycans (Lennarz, W. G., ed), pp. 269-314, Plenum, New York
19. Almeida, R., Levery, S. B., Mandel, U., Kresse, H., Schwientek, T, Bennett, E. P. and Clausen, H. (1999) Cloning and expression of a proteoglycan UDP-galactose-(β-xylose (β1,4-galactosyltransferase I: a seventh member of the human (β4-galactosyltransferase gene family. J. Biol. Chem. 274, 26165-26171
20. Okajima, T., Fukumoto, S., Furukawa, K., Urano, T. and Furukawa, K. (1999) Molecular basis for the progeroid variant of Ehlers-Danlos syndrome: identification and characterization of two mutations in galactosyltransferase I gene. J. Biol. Chem. 274, 28841-28844
21. Furukawa, K. and Okajima, T. (2002) Galactosyltransferase I is a gene responsible for progeroid variant of Ehlers-Danlos syndrome: molecular cloning and identification of mutations. Biochim. Biophys. Acta 1573, 377-381
22. Ramakrishnan, B. and Qasba, P. K. (2010) Crystal structure of the catalytic domain of Drosophila(β1,4-galactosyltransferase-7. J. Biol. Chem. 285, 15619-15626
23. Daligault, F., Rahuel-Clermont, S., Gulberti, S., Branlant, G., Netter, P., Magdalou, J. and Lattard, V. (2009) Thermodynamic insights into the structural basis governing the donor substrate recognition by human (β1,4-galactosyltransferase 7. Biochem. J. 418, 605-614
24. Esko, J. D., Weinke, J. L., Taylor, W. H., Ekborg, G., Roden, L., Anatharamaiah, G. and Gawish, A. (1987) Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I. J. Biol. Chem. 262, 12189-12195
25. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
26. Ha, Y. W., Jeon, B. T., Moon, S. H., Toyoda, H., Toida, T., Lindhardt, R. J. and Kim, Y. S. (2005) Characterization of heparan sulfate from the unossified antler of Cervus elaphus. Carbohydr. Res. 340, 411-416
27. Turnbull, W. B. and Danaras, A. H. (2003) On the value of c: can low affinity systems be studied by isothermal titration calorimetry. J. Am. Chem. Soc. 125, 14859-14866
28. Nakamura, Y., Haines, N., Chen, J., Okajima, T., Furukawa, K., Urano, T., Stanley, P., Irvine, K. D. and Furukawa, K. (2002) Identification of a Drosophila gene encoding xylosylprotein (β4-galactosyltransferase. J. Biol. Chem. 277, 46280-46288
29. Takemae, H., Ueda, R., Okubo, R., Nakato, H., Izumi, S., Saigo, K. and Nishihara, S. (2003) Proteoglycan UDP-galactose-(β-xylose (β-1,4-galactosyltransferase I is essential for viability in Drosophila melanogaster. J. Biol. Chem. 278, 15571-15578
30. Dam, T. K. and Brewer, C. F. (2002) Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry. Chem. Rev. 102, 387-429
31. Chervenak, M. C. and Toone, E. J. (1995) Calorimetric analysis of the binding of lectins with overlapping carbohydrate-binding ligand specificities. Biochemistry 34, 5685-5695
32. Xie, H., Bolam, D. N., Nagy, T., Szabo, L., Cooper, A., Simpson, P. J., Lakey, J. H., Williamson, M. P. and Gilbert, H. J. (2001) Role of hydrogen bonding in the interaction between a xylan binding module and xylan. Biochemistry 40, 5700-5707 (Pubitemid 32440874)
33. Ramakrishnan, B., Boeggeman, E., Ramasamy, V. and Qasba, P. K. (2004) Structure and catalytic cycle of (β-1,4-galactosyltransferase. Curr. Opin. Struct. Biol. 14, 593-600
34. Hennet, T. (2002) The galactosyltransferase family. Cell. Mol. Life Sci. 59, 1081-1095
35. Amado, M., Almeida, R., Schwientek, T. and Clausen, H. (1999) Identification and characterization of large galactosyltransferase gene families: galactosyltransferases for all functions. Biochim. Biophys. Acta 1473, 35-53
36. Herman, T. and Horvitz, H. R. (1999) Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 974-979
37. Almeida, R., Amado, M., David, L., Levery, S. B., Holmes, E. H., Merkx, G., Van Kessel, A. G., Ryggaard, E., Hassan, H., Bennett, E. and Clause, H. (1997) A family of human (β4-galactosyltransferases: cloning and expression of two novel UDP-galactose-(β-N-acetylglucosamine (β1, 4-galactosyltransferases, (β4Gal-T2 and (β4Gal-T3. J. Biol. Chem. 272, 31979-31992
38. Okayama, M., Kimata, K. and Suzuki, S. (1973) The influence of p-nitrophenyl (β-D-xyloside on the synthesis of proteochondroitin sulfate by slices of embryonic chick cartilage. J. Biochem. (Tokyo) 74, 1069-1073
39. Schwartz, N. B., Galligani, L., Ho, P. L. and Dorfman, A. (1974) Stimulation of synthesis of free chondroitin sulfate chains by (β-D-xylosides in cultured cells. Proc. Natl. Acad. Sci. U.S.A. 71, 4047-4051
40. Lugemwa, F. N., Sarkar, A. K. and Esko, J. D. (1996) Unusual (β-D-xylosides that prime glycosaminoglycans in animal cells. J. Biol. Chem. 271, 19159-19165