Faulty initiation of proteoglycan synthesis causes cardiac and joint defects

American Journal of Human Genetics

Volumn 89, Issue 1, 2011, Pages 15-27

  Baasanjav, Sevjidmaa ^a,b   Al Gazali, Lihadh ^c   Hashiguchi, Taishi ^d   Mizumoto, Shuji ^d   Fischer, Bjoern ^a   Horn, Denise ^a   Seelow, Dominik ^a   Ali, Bassam R ^c   Aziz, Samir A A ^e   Langer, Ruth ^c   Saleh, Ahmed A H ^e   Becker, Christian ^f   Nürnberg, Gudrun ^f   Cantagrel, Vincent ^g   Gleeson, Joseph G ^g   Gomez, Delphine ^h   Michel, Jean Baptiste ^h   Stricker, Sigmar ⁱ   Lindner, Tom H ^b   Nürnberg, Peter ^f   Sugahara, Kazuyuki ^d   Mundlos, Stefan ^a,i   Hoffmann, Katrin ^a,i,j   more..

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^c UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

^d HOKKAIDO UNIVERSITY   (Japan)

^e Saqr Hospital   (Saudi Arabia)

^f UNIVERSITY OF COLOGNE   (Germany)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h INSERM   (France)

ⁱ MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^j MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE I; HEPARAN SULFATE; UNCLASSIFIED DRUG;

AORTA ROOT DILATATION; ARTICLE; B3GAT3 GENE; BICUSPID AORTIC VALVE; CHILD; CHROMOSOME 11; CLINICAL ARTICLE; CONGENITAL HEART MALFORMATION; ENZYME ACTIVITY; GENE; GENE MUTATION; HEART DEVELOPMENT; HEART VENTRICLE SEPTUM DEFECT; HUMAN; HUMAN CELL; JOINT DISLOCATION; LARSEN SYNDROME; MITRAL VALVE PROLAPSE; MUSCULOSKELETAL DEVELOPMENT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEOGLYCAN SYNTHESIS;

EID: 80051542339     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2011.05.021     Document Type: Article

References (45)

1. Bulik, D.A., Wei, G., Toyoda, H., Kinoshita-Toyoda, A., Waldrip, W.R., Esko, J.D.,Robbins, P.W.,andSelleck, S.B. (2000). sqv-3, -7, and -8, a set of genes affecting morphogenesis in Caenorhabditis elegans, encode enzymes required for glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. USA 97, 10838-10843.
2. Sugahara, K., Mikami, T., Uyama, T., Mizuguchi, S., Nomura, K., and Kitagawa, H. (2003). Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13, 612-620. (Pubitemid 37244117)
3. Haltiwanger, R.S., and Lowe, J.B. (2004). Role of glycosylation in development. Annu. Rev. Biochem. 73, 491-537. (Pubitemid 39050378)
4. Häcker, U., Nybakken, K., and Perrimon, N. (2005). Heparan sulphate proteoglycans: The sweet side of development. Nat. Rev. Mol. Cell Biol. 6, 530-541. (Pubitemid 40943044)
5. Berninsone, P.M. (2006). Carbohydrates and glycosylation. WormBook 18, 1-22.
6. Franks, D.M., Izumikawa, T., Kitagawa, H., Sugahara, K., and Okkema, P.G. (2006). C. elegans pharyngeal morphogenesis requires both de novo synthesis of pyrimidines and synthesis of heparan sulfate proteoglycans. Dev. Biol. 296, 409-420. (Pubitemid 44189348)
7. Bishop, J.R., Schuksz, M., and Esko, J.D. (2007). Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037. (Pubitemid 46676065)
8. Sugahara, K., and Mikami, T. (2007). Chondroitin/dermatan sulfate in the central nervous system. Curr. Opin. Struct. Biol. 17, 536-545. (Pubitemid 350019013)
9. Izumikawa, T., Kanagawa, N., Watamoto, Y., Okada, M., Saeki, M., Sakano, M., Sugahara, K., Sugihara, K., Asano, M., and Kitagawa, H. (2010). Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase- I-deficient mice. J. Biol. Chem. 285, 12190-12196.
10. Dai, J., and Rabie, A.B. (2007). VEGF: An essential mediator of both angiogenesis and endochondral ossification. J. Dent. Res. 86, 937-950.
11. Stringer, S.E. (2006). The role of heparan sulphate proteoglycans in angiogenesis. Biochem. Soc. Trans. 34, 451-453. (Pubitemid 43954009)
12. Chan, C.K., Rolle, M.W., Potter-Perigo, S., Braun, K.R., Van Biber, B.P., Laflamme, M.A., Murry, C.E., and Wight, T.N. (2010). Differentiation of cardiomyocytes from human embryonic stem cells is accompanied by changes in the extracellular matrix production of versican and hyaluronan. J. Cell. Biochem. 111, 585-596.
13. Pilia, G., Hughes-Benzie, R.M., MacKenzie, A., Baybayan, P., Chen, E.Y., Huber, R., Neri, G., Cao, A., Forabosco, A., and Schlessinger, D. (1996). Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat. Genet. 12, 241-247. (Pubitemid 26080081)
14. Capurro, M.I., Li, F., and Filmus, J. (2009). Overgrowth of a mouse model of Simpson-Golabi-Behmel syndrome is partly mediated by Indian hedgehog. EMBO Rep. 10, 901-907.
15. Sugahara, K., and Kitagawa, H. (2000). Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10, 518-527.
16. Prydz, K., and Dalen, K.T. (2000). Synthesis and sorting of proteoglycans. J. Cell Sci. 113, 193-205. (Pubitemid 30088965)
17. Guérardel, Y., Balanzino, L., Maes, E., Leroy, Y., Coddeville, B., Oriol, R., and Strecker, G. (2001). The nematode Caenorhabditis elegans synthesizes unusual O-linked glycans: Identification of glucose-substituted mucin-type O-glycans and short chondroitin-like oligosaccharides. Biochem. J. 357, 167-182. (Pubitemid 32642914)
18. Hoffmann, K., and Lindner, T.H. (2005). easyLINKAGE-Plus- Automated linkage analyses using large-scale SNP data. Bioinformatics 21, 3565-3567. (Pubitemid 41236002)
19. Lindner, T.H., and Hoffmann, K. (2005). easyLINKAGE: A PERL script for easy and automated two-/multi-point linkage analyses. Bioinformatics 21, 405-407. (Pubitemid 40246617)
20. Hoffmann, K., Dreger, C.K., Olins, A.L., Olins, D.E., Shultz, L.D., Lucke, B., Karl, H., Kaps, R., Müller, D., Vayá, A., et al. (2002). Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huët anomaly). Nat. Genet. 31, 410-414. (Pubitemid 35154452)
21. Kitagawa, H., Tone, Y., Tamura, J., Neumann, K.W., Ogawa, T., Oka, S., Kawasaki, T., and Sugahara, K. (1998). Molecular cloning and expression of glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan- protein linkage region of proteoglycans. J. Biol. Chem. 273, 6615-6618. (Pubitemid 28160318)
22. van Roij, M.H., Mizumoto, S., Yamada, S., Morgan, T., Tan- Sindhunata, M.B., Meijers-Heijboer, H., Verbeke, J.I., Markie, D., Sugahara, K., and Robertson, S.P. (2008). Spondyloepiphyseal dysplasia, Omani type: further definition of the phenotype. Am. J. Med. Genet. A 146A, 2376-2384.
23. Tone, Y., Kitagawa, H., Imiya, K., Oka, S., Kawasaki, T., and Sugahara, K. (1999). Characterization of recombinant human glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. FEBS Lett. 459, 415-420. (Pubitemid 29467379)
24. Ouzzine, M., Gulberti, S., Levoin, N., Netter, P., Magdalou, J., and Fournel-Gigleux, S. (2002). The donor substrate specificity of the human beta 1,3-glucuronosyltransferase I toward UDP-glucuronic acid is determined by two crucial histidine and arginine residues. J. Biol. Chem. 277, 25439-25445. (Pubitemid 34951857)
25. Wei, G., Bai, X., and Esko, J.D. (2004). Temperature-sensitive glycosaminoglycan biosynthesis in a Chinese hamster ovary cell mutant containing a point mutation in glucuronyltransferase I. J. Biol. Chem. 279, 5693-5698. (Pubitemid 38220598)
26. Unger, S., Lausch, E., Rossi, A., Mégarbané, A., Sillence, D., Alcausin, M., Aytes, A., Mendoza-Londono, R., Nampoothiri, S., Afroze, B., et al. (2010). Phenotypic features of carbohydrate sulfotransferase 3 (CHST3) deficiency in 24 patients: congenital dislocations and vertebral changes as principal diagnostic features. Am. J. Med. Genet. A. 152A, 2543-2549.
27. Hermanns, P., Unger, S., Rossi, A., Perez-Aytes, A., Cortina, H., Bonafé, L., Boccone, L., Setzu, V., Dutoit, M., Sangiorgi, L., et al. (2008). Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis. Am. J. Hum. Genet. 82, 1368-1374.
28. Thiele, H., Sakano, M., Kitagawa, H., Sugahara, K., Rajab, A., Höhne, W., Ritter, H., Leschik, G., Nürnberg, P., and Mundlos, S. (2004). Loss of chondroitin 6-O-sulfotransferase- 1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc. Natl. Acad. Sci. USA 101, 10155-10160. (Pubitemid 38891211)
29. Dündar, M., Müller, T., Zhang, Q., Pan, J., Steinmann, B., Vodopiutz, J., Gruber, R., Sonoda, T., Krabichler, B., Utermann, G., et al. (2009). Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome. Am. J. Hum. Genet. 85, 873-882.
30. Malfait, F., Syx, D., Vlummens, P., Symoens, S., Nampoothiri, S., Hermanns-Lê, T., Van Laer, L., and De Paepe, A. (2010). Musculocontractural Ehlers-Danlos Syndrome (former EDS type VIB) and adducted thumb clubfoot syndrome (ATCS) represent a single clinical entity caused by mutations in the dermatan-4-sulfotransferase 1 encoding CHST14 gene. Hum. Mutat. 31, 1233-1239.
31. Miyake, N., Kosho, T., Mizumoto, S., Furuichi, T., Hatamochi, A., Nagashima, Y., Arai, E., Takahashi, K., Kawamura, R., Wakui, K., et al. (2010). Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome. Hum. Mutat. 31, 966-974.
32. Pedersen, L.C., Tsuchida, K., Kitagawa, H., Sugahara, K., Darden, T.A., and Negishi, M. (2000). Heparan/chondroitin sulfate biosynthesis. Structure and mechanism of human glucuronyltransferase I. J. Biol. Chem. 275, 34580-34585.
33. Negishi, M., Dong, J., Darden, T.A., Pedersen, L.G., and Pedersen, L.C. (2003). Glucosaminylglycan biosynthesis: What we can learn from the X-ray crystal structures of glycosyltransferases GlcAT1 and EXTL2. Biochem. Biophys. Res. Commun. 303, 393-398. (Pubitemid 36349182)
34. Ouzzine, M., Antonio, L., Burchell, B., Netter, P., Fournel- Gigleux, S., and Magdalou, J. (2000). Importance of histidine residues for the function of the human liver UDP-glucuronosyltransferase UGT1A6: Evidence for the catalytic role of histidine. Mol. Pharmacol. 58, 1609-1615.
35. Gilchrist, A., Au, C.E., Hiding, J., Bell, A.W., Fernandez-Rodriguez, J., Lesimple, S., Nagaya, H., Roy, L., Gosline, S.J., Hallett, M., et al. (2006). Quantitative proteomics analysis of the secretory pathway. Cell 127, 1265-1281. (Pubitemid 44914006)
36. Kresse, H., Rosthøj, S., Quentin, E., Hollmann, J., Glössl, J., Okada, S., and Tønnesen, 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. (Pubitemid 18047474)
37. Okajima, T., Fukumoto, S., Furukawa, K., and Urano, T. (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.
38. 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. A 128A, 39-45. (Pubitemid 38856815)
39. Li, Y., Laue, K., Temtamy, S., Aglan, M., Kotan, L.D., Yigit, G., Canan, H., Pawlik, B., Nürnberg, G., Wakeling, E.L., et al. (2010). Temtamy preaxial brachydactyly syndrome is caused by loss-of-function mutations in chondroitin synthase 1, a potential target of BMP signaling. Am. J. Hum. Genet. 87, 757-767.
40. Tian, J., Ling, L., Shboul, M., Lee, H., O'Connor, B., Merriman, B., Nelson, S.F., Cool, S., Ababneh, O.H., Al-Hadidy, A., et al. (2010). Loss of CHSY1, a secreted FRINGE enzyme, causes syndromic brachydactyly in humans via increased NOTCH signaling. Am. J. Hum. Genet. 87, 768-778.
41. Saigoh, K., Izumikawa, T., Koike, T., Shimizu, J., Kitagawa, H., and Kusunoki, S. (2011). Chondroitin beta-1,4-N-acetylgalactosaminyltransferase- 1 missense mutations are associated with neuropathies. J. Hum. Genet. 56, 143-146.
42. Bruneau, B.G. (2008). The developmental genetics of congenital heart disease. Nature 451, 943-948. (Pubitemid 351301750)
43. Leong, F.T., Freeman, L.J., and Keavney, B.D. (2009). Fresh fields and pathways new: Recent genetic insights into cardiac malformation. Heart 95, 442-447.
44. Garg, V., Muth, A.N., Ransom, J.F., Schluterman, M.K., Barnes, R., King, I.N., Grossfeld, P.D., and Srivastava, D. (2005). Mutations in NOTCH1 cause aortic valve disease. Nature 437, 270-274. (Pubitemid 41294491)
45. Tone, Y., Pedersen, L.C., Yamamoto, T., Izumikawa, T., Kitagawa, H., Nishihara, J., Tamura, J., Negishi, M., and Sugahara, K. (2008). 2-o-phosphorylation of xylose and 6-o-sulfation of galactose in the protein linkage region of glycosaminoglycans influence the glucuronyltransferase-I activity involved in the linkage region synthesis. J. Biol. Chem. 283, 16801-16807.