Chondroitin sulfate synthase 1 (Chsy1) is required for bone development and digit patterning

Developmental Biology

Volumn 363, Issue 2, 2012, Pages 413-425

  Wilson, Deanna G ^a   Phamluong, Khanhky ^a   Lin, Wei Yu ^a   Barck, Kai ^a   Carano, Richard A D ^a   Diehl, Lauri ^a   Peterson, Andrew S ^a   Martin, Flavius ^a   Solloway, Mark J ^a  

^a GENENTECH INC   (United States)

Author keywords

Chondroitin sulfate; Digit patterning; Joints; Mouse embryo; Proteoglycan

Indexed keywords

CHONDROITIN SULFATE; CHONDROITIN SULFATE SYNTHASE 1; DERMATAN SULFATE; SYNTHETASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE CELL; BONE DENSITY; BONE DEVELOPMENT; BRACHYDACTYLY; CATALYSIS; CHONDRODYSPLASIA; CHSY1 GENE; CONTROLLED STUDY; DIGIT PATTERNING; EMBRYO; ENZYME ACTIVITY; GENE FUNCTION; GENE LOCUS; GENE LOSS; GENE MUTATION; GROWTH REGULATION; LIMB DEVELOPMENT; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SULFATION;

MUS;

EID: 84857108384     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.01.005     Document Type: Article

References (105)

1. Abad V., Meyers J.L., Weise M., Gafni R.I., Barnes K.M., Nilsson O., Bacher J.D., Baron J. The role of the resting zone in growth plate chondrogenesis. Endocrinology 2002, 143:1851-1857.
2. Abu-Hijleh G., Padmanabhan R. Retinoic acid-induced abnormal development of hindlimb joints in the mouse. Eur. J. Morphol. 1997, 35:327-336.
3. Archer C.W., Dowthwaite G.P., Francis-West P. Development of synovial joints. Birth Defects Res. C Embryo Today 2003, 69:144-155.
4. Baasanjav S., Al-Gazali L., Hashiguchi T., Mizumoto S., Fischer B., Horn D., Seelow D., Ali B.R., Aziz S.A., Langer R., Saleh A.A., Becker C., Nurnberg G., Cantagrel V., Gleeson J.G., Gomez D., Michel J.B., Stricker S., Lindner T.H., Nurnberg P., Sugahara K., Mundlos S., Hoffmann K. Faulty initiation of proteoglycan synthesis causes cardiac and joint defects. Am. J. Hum. Genet. 2011, 89:15-27.
5. Baldridge D., Shchelochkov O., Kelley B., Lee B. Signaling pathways in human skeletal dysplasias. Annu. Rev. Genomics Hum. Genet. 2010, 11:189-217.
6. Baur S.T., Mai J.J., Dymecki S.M. Combinatorial signaling through BMP receptor IB and GDF5: shaping of the distal mouse limb and the genetics of distal limb diversity. Development 2000, 127:605-619.
7. Bode-Lesniewska B., Dours-Zimmermann M.T., Odermatt B.F., Briner J., Heitz P.U., Zimmermann D.R. Distribution of the large aggregating proteoglycan versican in adult human tissues. J. Histochem. Cytochem. 1996, 44:303-312.
8. Brunet L.J., McMahon J.A., McMahon A.P., Harland R.M. Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 1998, 280:1455-1457.
9. Buckwalter J.A., Mankin H.J. Articular cartilage: tissue design and chondrocyte-matrix interactions. Instr. Course Lect. 1998, 47:477-486.
10. Butterfield N.C., Metzis V., McGlinn E., Bruce S.J., Wainwright B.J., Wicking C. Patched 1 is a crucial determinant of asymmetry and digit number in the vertebrate limb. Development 2009, 136:3515-3524.
11. Byrnes A.M., Racacho L., Grimsey A., Hudgins L., Kwan A.C., Sangalli M., Kidd A., Yaron Y., Lau Y.L., Nikkel S.M., Bulman D.E. Brachydactyly A-1 mutations restricted to the central region of the N-terminal active fragment of Indian Hedgehog. Eur. J. Hum. Genet. 2009, 17:1112-1120.
12. Chang S.C., Hoang B., Thomas J.T., Vukicevic S., Luyten F.P., Ryba N.J., Kozak C.A., Reddi A.H., Moos M. Cartilage-derived morphogenetic proteins. New members of the transforming growth factor-beta superfamily predominantly expressed in long bones during human embryonic development. J. Biol. Chem. 1994, 269:28227-28234.
13. Choocheep K., Hatano S., Takagi H., Watanabe H., Kimata K., Kongtawelert P. Versican facilitates chondrocyte differentiation and regulates joint morphogenesis. J. Biol. Chem. 2010, 285:21114-21125.
14. Cooke B.M., Rogerson S.J., Brown G.V., Coppel R.L. Adhesion of malaria-infected red blood cells to chondroitin sulfate A under flow conditions. Blood 1996, 88:4040-4044.
15. Cortes M., Baria A.T., Schwartz N.B. Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate. Development 2009, 136:1697-1706.
16. Dathe K., Kjaer K.W., Brehm A., Meinecke P., Nurnberg P., Neto J.C., Brunoni D., Tommerup N., Ott C.E., Klopocki E., Seemann P., Mundlos S. Duplications involving a conserved regulatory element downstream of BMP2 are associated with brachydactyly type A2. Am. J. Hum. Genet. 2009, 84:483-492.
17. Domowicz M.S., Cortes M., Henry J.G., Schwartz N.B. Aggrecan modulation of growth plate morphogenesis. Dev. Biol. 2009, 329:242-257.
18. Forlino A., Piazza R., Tiveron C., Della Torre S., Tatangelo L., Bonafe L., Gualeni B., Romano A., Pecora F., Superti-Furga A., Cetta G., Rossi A. A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse: morphological and biochemical characterization of the resulting chondrodysplasia phenotype. Hum. Mol. Genet. 2005, 14:859-871.
19. Francis-West P.H., Parish J., Lee K., Archer C.W. BMP/GDF-signalling interactions during synovial joint development. Cell Tissue Res. 1999, 296:111-119.
20. Frederick J.P., Tafari A.T., Wu S.M., Megosh L.C., Chiou S.T., Irving R.P., York J.D. A role for a lithium-inhibited Golgi nucleotidase in skeletal development and sulfation. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11605-11612.
21. Fried M., Duffy P.E. Maternal malaria and parasite adhesion. J. Mol. Med. 1998, 76:162-171.
22. Fromental-Ramain C., Warot X., Messadecq N., LeMeur M., Dolle P., Chambon P. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 1996, 122:2997-3011.
23. Gandhi N.S., Mancera R.L. The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 2008, 72:455-482.
24. Gao B., Guo J., She C., Shu A., Yang M., Tan Z., Yang X., Guo S., Feng G., He L. Mutations in IHH, encoding Indian hedgehog, cause brachydactyly type A-1. Nat. Genet. 2001, 28:386-388.
25. Gong Y., Krakow D., Marcelino J., Wilkin D., Chitayat D., Babul-Hirji R., Hudgins L., Cremers C.W., Cremers F.P., Brunner H.G., Reinker K., Rimoin D.L., Cohn D.H., Goodman F.R., Reardon W., Patton M., Francomano C.A., Warman M.L. Heterozygous mutations in the gene encoding noggin affect human joint morphogenesis. Nat. Genet. 1999, 21:302-304.
26. Gotoh M., Sato T., Akashima T., Iwasaki H., Kameyama A., Mochizuki H., Yada T., Inaba N., Zhang Y., Kikuchi N., Kwon Y.D., Togayachi A., Kudo T., Nishihara S., Watanabe H., Kimata K., Narimatsu H. Enzymatic synthesis of chondroitin with a novel chondroitin sulfate N-acetylgalactosaminyltransferase that transfers N-acetylgalactosamine to glucuronic acid in initiation and elongation of chondroitin sulfate synthesis. J. Biol. Chem. 2002, 277:38189-38196.
27. Gotoh M., Yada T., Sato T., Akashima T., Iwasaki H., Mochizuki H., Inaba N., Togayachi A., Kudo T., Watanabe H., Kimata K., Narimatsu H. Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine. J. Biol. Chem. 2002, 277:38179-38188.
28. Gritli-Linde A., Lewis P., McMahon A.P., Linde A. The whereabouts of a morphogen: direct evidence for short- and graded long-range activity of hedgehog signaling peptides. Dev. Biol. 2001, 236:364-386.
29. Gruneberg H., Lee A.J. The anatomy and development of brachypodism in the mouse. J. Embryol. Exp. Morphol. 1973, 30:119-141.
30. Gualeni B., Facchini M., De Leonardis F., Tenni R., Cetta G., Viola M., Passi A., Superti-Furga A., Forlino A., Rossi A. Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling. Matrix Biol. 2010, 29:453-460.
31. Guo X., Day T.F., Jiang X., Garrett-Beal L., Topol L., Yang Y. Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev. 2004, 18:2404-2417.
32. Hogan B.L. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 1996, 10:1580-1594.
33. Itoh S., Kanno S., Gai Z., Suemoto H., Kawakatsu M., Tanishima H., Morimoto Y., Nishioka K., Hatamura I., Yoshida M., Muragaki Y. Trps1 plays a pivotal role downstream of Gdf5 signaling in promoting chondrogenesis and apoptosis of ATDC5 cells. Genes Cells 2008, 13:355-363.
34. Izumikawa T., Kitagawa H., Mizuguchi S., Nomura K.H., Nomura K., Tamura J., Gengyo-Ando K., Mitani S., Sugahara K. Nematode chondroitin polymerizing factor showing cell-/organ-specific expression is indispensable for chondroitin synthesis and embryonic cell division. J. Biol. Chem. 2004, 279:53755-53761.
35. Izumikawa T., Uyama T., Okuura Y., Sugahara K., Kitagawa H. Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor. Biochem. J. 2007, 403:545-552.
36. Izumikawa T., Koike T., Shiozawa S., Sugahara K., Tamura J., Kitagawa H. Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization: chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members. J. Biol. Chem. 2008, 283:11396-11406.
37. Izumikawa T., Kanagawa N., Watamoto Y., Okada M., Saeki M., Sakano M., Sugahara K., Sugihara K., Asano M., Kitagawa H. Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice. J. Biol. Chem. 2010, 285:12190-12196.
38. Izumikawa T., Okuura Y., Koike T., Sakoda N., Kitagawa H. Chondroitin 4-O-sulfotransferase-1 regulates the chain length of chondroitin sulfate in co-operation with chondroitin N-acetylgalactosaminyltransferase-2. Biochem. J. 2011, 434:321-331.
39. Karsenty G., Wagner E.F. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2002, 2:389-406.
40. Kitagawa H., Uyama T., Sugahara K. Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 2001, 276:38721-38726.
41. Kitagawa H., Izumikawa T., Uyama T., Sugahara K. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J. Biol. Chem. 2003, 278:23666-23671.
42. Kluppel M., Wight T.N., Chan C., Hinek A., Wrana J.L. Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 2005, 132:3989-4003.
43. Koyama E., Ochiai T., Rountree R.B., Kingsley D.M., Enomoto-Iwamoto M., Iwamoto M., Pacifici M. Synovial joint formation during mouse limb skeletogenesis: roles of Indian hedgehog signaling. Ann. N. Y. Acad. Sci. 2007, 1116:100-112.
44. Kresse H., Rosthoj S., Quentin E., Hollmann J., Glossl J., Okada S., Tonnesen T. Glycosaminoglycan-free small proteoglycan core protein is secreted by fibroblasts from a patient with a syndrome resembling progeroid. Am. J. Hum. Genet. 1987, 41:436-453.
45. Kurima K., Warman M.L., Krishnan S., Domowicz M., Krueger R.C., Deyrup A., Schwartz N.B. A member of a family of sulfate-activating enzymes causes murine brachymorphism. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8681-8685.
46. Kusche-Gullberg M., Kjellen L. Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 2003, 13:605-611.
47. Kuss P., Villavicencio-Lorini P., Witte F., Klose J., Albrecht A.N., Seemann P., Hecht J., Mundlos S. Mutant Hoxd13 induces extra digits in a mouse model of synpolydactyly directly and by decreasing retinoic acid synthesis. J. Clin. Invest. 2009, 119:146-156.
48. Lawrence R., Lu H., Rosenberg R.D., Esko J.D., Zhang L. Disaccharide structure code for the easy representation of constituent oligosaccharides from glycosaminoglycans. Nat. Methods 2008, 5:291-292.
49. Lehmann K., Seemann P., Stricker S., Sammar M., Meyer B., Suring K., Majewski F., Tinschert S., Grzeschik K.H., Muller D., Knaus P., Nurnberg P., Mundlos S. Mutations in bone morphogenetic protein receptor 1B cause brachydactyly type A2. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12277-12282.
50. Lev R., Spicer S.S. Specific staining of sulphate groups with alcian blue at low Ph. J. Histochem. Cytochem. 1964, 12:309.
51. Li Y., Laue K., Temtamy S., Aglan M., Kotan L.D., Yigit G., Canan H., Pawlik B., Nurnberg G., Wakeling E.L., Quarrell O.W., Baessmann I., Lanktree M.B., Yilmaz M., Hegele R.A., Amr K., May K.W., Nurnberg P., Topaloglu A.K., Hammerschmidt M., Wollnik B. 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. 2010, 87:757-767.
52. Maeda I., Kohara Y., Yamamoto M., Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 2001, 11:171-176.
53. Margolis R.U., Margolis R.K. Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding. Cell Tissue Res. 1997, 290:343-348.
54. Matsumoto K., Li Y., Jakuba C., Sugiyama Y., Sayo T., Okuno M., Dealy C.N., Toole B.P., Takeda J., Yamaguchi Y., Kosher R.A. Conditional inactivation of Has2 reveals a crucial role for hyaluronan in skeletal growth, patterning, chondrocyte maturation and joint formation in the developing limb. Development 2009, 136:2825-2835.
55. McDonald J.A., Camenisch T.D. Hyaluronan: genetic insights into the complex biology of a simple polysaccharide. Glycoconj. J. 2002, 19:331-339.
56. Mizuguchi S., Uyama T., Kitagawa H., Nomura K.H., Dejima K., Gengyo-Ando K., Mitani S., Sugahara K., Nomura K. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 2003, 423:443-448.
57. Moser M., Binder O., Wu Y., Aitsebaomo J., Ren R., Bode C., Bautch V.L., Conlon F.L., Patterson C. BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol. Cell. Biol. 2003, 23:5664-5679.
58. Muenke M., Schell U. Fibroblast-growth-factor receptor mutations in human skeletal disorders. Trends Genet. 1995, 11:308-313.
59. Okajima T., Fukumoto S., Furukawa K., Urano T. Molecular basis for the progeroid variant of Ehlers-Danlos syndrome. Identification and characterization of two mutations in galactosyltransferase I gene. J. Biol. Chem. 1999, 274:28841-28844.
60. Okazaki N., Kikuno R., Ohara R., Inamoto S., Koseki H., Hiraoka S., Saga Y., Nagase T., Ohara O., Koga H. Prediction of the coding sequences of mouse homologues of KIAA gene: III. The complete nucleotide sequences of 500 mouse KIAA-homologous cDNAs identified by screening of terminal sequences of cDNA clones randomly sampled from size-fractionated libraries. DNA Res. 2003, 10:167-180.
61. Oldberg A., Antonsson P., Moses J., Fransson L.A. Amino-terminal deletions in the decorin core protein leads to the biosynthesis of proteoglycans with shorter glycosaminoglycan chains. FEBS Lett. 1996, 386:29-32.
62. Rix S., Calmont A., Scambler P.J., Beales P.L. An Ift80 mouse model of short rib polydactyly syndromes shows defects in hedgehog signalling without loss or malformation of cilia. Hum. Mol. Genet. 2011, 20:1306-1314.
63. Sakai K., Kimata K., Sato T., Gotoh M., Narimatsu H., Shinomiya K., Watanabe H. Chondroitin sulfate N-acetylgalactosaminyltransferase-1 plays a critical role in chondroitin sulfate synthesis in cartilage. J. Biol. Chem. 2007, 282:4152-4161.
64. Sato T., Gotoh M., Kiyohara K., Akashima T., Iwasaki H., Kameyama A., Mochizuki H., Yada T., Inaba N., Togayachi A., Kudo T., Asada M., Watanabe H., Imamura T., Kimata K., Narimatsu H. Differential roles of two N-acetylgalactosaminyltransferases, CSGalNAcT-1, and a novel enzyme, CSGalNAcT-2. Initiation and elongation in synthesis of chondroitin sulfate. J. Biol. Chem. 2003, 278:3063-3071.
65. Schwartz N.B., Domowicz M. Chondrodysplasias due to proteoglycan defects. Glycobiology 2002, 12:57R-68R.
66. Seemann P., Schwappacher R., Kjaer K.W., Krakow D., Lehmann K., Dawson K., Stricker S., Pohl J., Ploger F., Staub E., Nickel J., Sebald W., Knaus P., Mundlos S. Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J. Clin. Invest. 2005, 115:2373-2381.
67. Shepard J.B., Krug H.A., LaFoon B.A., Hoffman S., Capehart A.A. Versican expression during synovial joint morphogenesis. Int. J. Biol. Sci. 2007, 3:380-384.
68. Silbert J.E. Organization of glycosaminoglycan sulfation in the biosynthesis of proteochondroitin sulfate and proteodermatan sulfate. Glycoconj. J. 1996, 13:907-912.
69. Silbert J.E., Sugumaran G. Intracellular membranes in the synthesis, transport, and metabolism of proteoglycans. Biochim. Biophys. Acta 1995, 1241:371-384.
70. Silbert J.E., Sugumaran G. Biosynthesis of chondroitin/dermatan sulfate. IUBMB Life 2002, 54:177-186.
71. Snow H.E., Riccio L.M., Mjaatvedt C.H., Hoffman S., Capehart A.A. Versican expression during skeletal/joint morphogenesis and patterning of muscle and nerve in the embryonic mouse limb. Anat. Rec. 2005, 282:95-105.
72. Sohaskey M.L., Yu J., Diaz M.A., Plaas A.H., Harland R.M. JAWS coordinates chondrogenesis and synovial joint positioning. Development 2008, 135:2215-2220.
73. Solloway M.J., Dudley A.T., Bikoff E.K., Lyons K.M., Hogan B.L., Robertson E.J. Mice lacking Bmp6 function. Dev. Genet. 1998, 22:321-339.
74. Spagnoli A., O'Rear L., Chandler R.L., Granero-Molto F., Mortlock D.P., Gorska A.E., Weis J.A., Longobardi L., Chytil A., Shimer K., Moses H.L. TGF-beta signaling is essential for joint morphogenesis. J. Cell Biol. 2007, 177:1105-1117.
75. Spater D., Hill T.P., O'Sullivan R.J., Gruber M., Conner D.A., Hartmann C. Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development 2006, 133:3039-3049.
76. Spicer D. FGF9 on the move. Nat. Genet. 2009, 41:272-273.
77. Spicer A.P., Tien J.L., Joo A., Bowling R.A. Investigation of hyaluronan function in the mouse through targeted mutagenesis. Glycoconj. J. 2002, 19:341-345.
78. Sprinzak D., Lakhanpal A., Lebon L., Santat L.A., Fontes M.E., Anderson G.A., Garcia-Ojalvo J., Elowitz M.B. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 2010, 465:86-90.
79. St-Jacques B., Hammerschmidt M., McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 1999, 13:2072-2086.
80. Storm E.E., Kingsley D.M. Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 1996, 122:3969-3979.
81. Storm E.E., Kingsley D.M. GDF5 coordinates bone and joint formation during digit development. Dev. Biol. 1999, 209:11-27.
82. Storm E.E., Huynh T.V., Copeland N.G., Jenkins N.A., Kingsley D.M., Lee S.J. Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature 1994, 368:639-643.
83. Stricker S., Mundlos S. Mechanisms of digit formation: human malformation syndromes tell the story. Dev. Dyn. 2011, 240:990-1004.
84. Sugumaran G., Silbert J.E. Sulfation of chondroitin. Specificity, degree of sulfation, and detergent effects with 4-sulfating and 6-sulfating microsomal systems. J. Biol. Chem. 1988, 263:4673-4678.
85. Sugumaran G., Silbert J.E. Relationship of sulfation to ongoing chondroitin polymerization during biosynthesis of chondroitin 4-sulfate by microsomal preparations from cultured mouse mastocytoma cells. J. Biol. Chem. 1990, 265:18284-18288.
86. Thorogood P.V., Hinchliffe J.R. An analysis of the condensation process during chondrogenesis in the embryonic chick hind limb. J. Embryol. Exp. Morphol. 1975, 33:581-606.
87. Tian J., Ling L., Shboul M., Lee H., O'Connor B., Merriman B., Nelson S.F., Cool S., Ababneh O.H., Al-Hadidy A., Masri A., Hamamy H., Reversade B. Loss of CHSY1, a secreted FRINGE enzyme, causes syndromic brachydactyly in humans via increased NOTCH signaling. Am. J. Hum. Genet. 2010, 87:768-778.
88. Tickle C. Molecular basis of vertebrate limb patterning. Am. J. Med. Genet. 2002, 112:250-255.
89. Uyama T., Kitagawa H., Tanaka J., Tamura J., Ogawa T., Sugahara K. Molecular cloning and expression of a second chondroitin N-acetylgalactosaminyltransferase involved in the initiation and elongation of chondroitin/dermatan sulfate. J. Biol. Chem. 2003, 278:3072-3078.
90. Varki A. Essentials of Glycobiology 2009, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. 2nd ed.
91. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
92. Watanabe H., Yamada Y. Chondrodysplasia of gene knockout mice for aggrecan and link protein. Glycoconj. J. 2002, 19:269-273.
93. Watanabe H., Kimata K., Line S., Strong D., Gao L.Y., Kozak C.A., Yamada Y. Mouse cartilage matrix deficiency (cmd) caused by a 7 bp deletion in the aggrecan gene. Nat. Genet. 1994, 7:154-157.
94. Watanabe H., Yamada Y., Kimata K. Roles of aggrecan, a large chondroitin sulfate proteoglycan, in cartilage structure and function. J. Biochem. 1998, 124:687-693.
95. Wilkinson D.G., Nieto M.A. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol. 1993, 225:361-373.
96. Witte F., Dokas J., Neuendorf F., Mundlos S., Stricker S. Comprehensive expression analysis of all Wnt genes and their major secreted antagonists during mouse limb development and cartilage differentiation. Gene Expr. Patterns 2009, 9:215-223.
97. Wolfman N.M., Hattersley G., Cox K., Celeste A.J., Nelson R., Yamaji N., Dube J.L., DiBlasio-Smith E., Nove J., Song J.J., Wozney J.M., Rosen V. Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-beta gene family. J. Clin. Invest. 1997, 100:321-330.
98. Wotton D., Lo R.S., Swaby L.A., Massague J. Multiple modes of repression by the Smad transcriptional corepressor TGIF. J. Biol. Chem. 1999, 274:37105-37110.
99. Xu T., Bianco P., Fisher L.W., Longenecker G., Smith E., Goldstein S., Bonadio J., Boskey A., Heegaard A.M., Sommer B., Satomura K., Dominguez P., Zhao C., Kulkarni A.B., Robey P.G., Young M.F. Targeted disruption of the biglycan gene leads to an osteoporosis-like phenotype in mice. Nat. Genet. 1998, 20:78-82.
100. Yada T., Gotoh M., Sato T., Shionyu M., Go M., Kaseyama H., Iwasaki H., Kikuchi N., Kwon Y.D., Togayachi A., Kudo T., Watanabe H., Narimatsu H., Kimata K. Chondroitin sulfate synthase-2. Molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. J. Biol. Chem. 2003, 278:30235-30247.
101. Yada T., Sato T., Kaseyama H., Gotoh M., Iwasaki H., Kikuchi N., Kwon Y.D., Togayachi A., Kudo T., Watanabe H., Narimatsu H., Kimata K. Chondroitin sulfate synthase-3. Molecular cloning and characterization. J. Biol. Chem. 2003, 278:39711-39725.
102. Yanagawa S., van Leeuwen F., Wodarz A., Klingensmith J., Nusse R. The dishevelled protein is modified by wingless signaling in Drosophila. Genes Dev. 1995, 9:1087-1097.
103. Yi S.E., Daluiski A., Pederson R., Rosen V., Lyons K.M. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 2000, 127:621-630.
104. Yin M., Gentili C., Koyama E., Zasloff M., Pacifici M. Antiangiogenic treatment delays chondrocyte maturation and bone formation during limb skeletogenesis. J. Bone Miner. Res. 2002, 17:56-65.
105. Yu K., Ornitz D.M. FGF signaling regulates mesenchymal differentiation and skeletal patterning along the limb bud proximodistal axis. Development 2008, 135:483-491.