Cartilage ultrastructure in proteoglycan-deficient zebrafish mutants brings to light new candidate genes for human skeletal disorders

Journal of Pathology

Volumn 223, Issue 4, 2011, Pages 531-542

  Wiweger, Malgorzata I ^a   Avramut, Cristina M ^a   De Andrea, Carlos E ^a   Prins, Frans A ^a   Koster, Abraham J ^a   Ravelli, Raimond B G ^a   Hogendoorn, Pancras C W ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

bone; cartilage; electron microscopy; glycans; osteochondroma; skeletal dysplasia; zebrafish

Indexed keywords

BETA 1,3 GLUCURONYLTRANSFERASE 3; EXOSTOSIN 2; GLYPICAN; GLYPICAN 4; PROTEIN; PROTEOGLYCAN; SOLUTE CARRIER FAMILY 35 MEMBER B2 PROTEIN; UDP GLUCURONIC ACID DECARBOXYLASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE DISEASE; BONE DYSPLASIA; CARTILAGE; CARTILAGE CELL; CELL JUNCTION; CELL MEMBRANE; CELL STRUCTURE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; GENE MUTATION; HUMAN; HUMAN TISSUE; NONHUMAN; OSSIFICATION; PERICHONDRIUM; PHENOTYPE; PRIORITY JOURNAL; PROTEOGLYCAN SYNTHESIS; SIMPSON GOLABI BEHMEL SYNDROME; ZEBRA FISH;

ANIMALS; BONE DISEASES, DEVELOPMENTAL; CARTILAGE; CELL MEMBRANE; CHONDROCYTES; DISEASE MODELS, ANIMAL; EXTRACELLULAR MATRIX; GENETIC ASSOCIATION STUDIES; GLYCOSAMINOGLYCANS; INCLUSION BODIES; INTERCELLULAR JUNCTIONS; MICROSCOPY, ELECTRON; OSTEOGENESIS; PROTEOGLYCANS; ZEBRAFISH;

EID: 79551706241     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2824     Document Type: Article

References (35)

1. Willems SM, Wiweger M, Frans Graadt van Roggen J, et al., Running GAGs: myxoid matrix revisited. What's in it for the pathologist? Virchow Arch 2009; 456: 181-192.
2. Bovée JVMG, Hogendoorn PCW,. Multiple osteochondromas. In World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Soft Tissue and Bone, Fletcher CDM, Unni KK, Mertens F, (eds). IARC Press: Lyon, 2002; 360-362.
3. Arikawa-Hirasawa E, Wilcox WR, Le AH, et al., Dyssegmental dysplasia, Silverman-Handmaker type, is caused by functional null mutations of the perlecan gene. Nat Genet 2001; 27: 431-434. (Pubitemid 32268426)
4. Pilia G, Hughes-Benzie RM, MacKenzie A, et al., Mutations in GPC3, a glypican gene, cause the Simpson-Golabi-Behmel overgrowth syndrome. Nat Genet 1996; 12: 241-247. (Pubitemid 26080081)
5. Campos-Xavier AB, Martinet D, Bateman J, et al., Mutations in the heparan-sulfate proteoglycan glypican 6 (GPC6) impair endochondral ossification and cause recessive omodysplasia. Am J Hum Genet 2009; 84: 760-770.
6. Thiele H, Sakano M, Kitagawa H, et al., Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc Natl Acad Sci USA 2004; 101: 10155-10160. (Pubitemid 38891211)
7. Hermanns P, Unger S, Rossi A, et al., Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis. Am J Hum Genet 2008; 82: 1368-1374.
8. Schilling TF, Kimmel CB,. Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 1997; 124: 2945-2960. (Pubitemid 27370910)
9. Schilling TF, Piotrowski T, Grandel H, et al., Jaw and branchial arch mutants in zebrafish I: branchial arches. Development 1996; 123: 329-344.
10. Golling G, Amsterdam A, Sun Z, et al., Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat Genet 2002; 31: 135-140.
11. Solnica-Krezel L, Stemple DL, Mountcastle-Shah E, et al., Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development 1996; 123: 67-80. (Pubitemid 27056737)
12. Kimmel CB, Ballard WW, Kimmel SR, et al., Stages of embryonic development of the zebrafish. Dev Dyn 1995; 203: 253-310.
13. Clément A, Wiweger M, von der Hardt S, et al., Regulation of zebrafish skeletogenesis by ext2/dackel and papst1/pinscher. PLoS Genet 2008; 4: e1000136.
14. Nissen RM, Amsterdam A, Hopkins N,. A zebrafish screen for craniofacial mutants identifies wdr68 as a highly conserved gene required for endothelin-1 expression. BMC Dev Biol 2006; 6: 28.
15. Eames BF, Singer A, Smith GA, et al., UDP xylose synthase 1 is required for morphogenesis and histogenesis of the craniofacial skeleton. Dev Biol 2010; 341: 400-415.
16. Hoa N, Myers MP, Douglass TG, et al., Molecular mechanisms of paraptosis induction: implications for a non-genetically modified tumor vaccine. PLoS ONE 2009; 4: e4631.
17. de Andrea CE, Wiweger M, Prins F, et al., Primary cilia organization reflects polarity in the growth plate and implies loss of polarity and mosaicism in osteochondroma. Lab Invest 2010; 90: 1091-1101.
18. Yelick PC, Schilling TF,. Molecular dissection of craniofacial development using zebrafish. Crit Rev Oral Biol Med 2002; 13: 308-322. (Pubitemid 36041621)
19. Superti-Furga A, Unger S,. Nosology and classification of genetic skeletal disorders: 2006 revision. Am J Med Genet A 2007; 143: 1-18. (Pubitemid 46051466)
20. Hunter GK,. Role of proteoglycan in the provisional calcification of cartilage. A review and reinterpretation. Clin Orthop Relat Res 1991; 262: 256-280.
21. Carey DJ,. Biological functions of proteoglycans: use of specific inhibitors of proteoglycan synthesis. Mol Cell Biochem 1991; 104: 21-28.
22. Mitchell NS, Shepard NL,. Electron microscopic evaluation of the occurrence of matrix vesicles in cartilage. Anat Rec 1990; 227: 397-404. (Pubitemid 20222172)
23. Bassett DI, Currie PD,. The zebrafish as a model for muscular dystrophy and congenital myopathy. Hum Mol Genet 2003; 12 (2):(spec No): R265-270. (Pubitemid 37259341)
24. Telfer WR, Busta AS, Bonnemann CG, et al., Zebrafish models of collagen VI-related myopathies. Hum Mol Genet 2010; 19: 2433-2444.
25. Venkatasubramani N, Mayer AN,. A zebrafish model for the Shwachman-Diamond syndrome (SDS). Pediatr Res 2008; 63: 348-352. (Pubitemid 351450577)
26. Lee J-S, von der HS, Rusch MA, et al., Axon sorting in the optic tract requires HSPG synthesis by ext2 (dackel) and extl3 (boxer). Neuron 2004; 44: 947-960. (Pubitemid 39643091)
27. Hameetman L, Szuhai K, Yavas A, et al., The Role of EXT1 in non-hereditary osteochondroma:identification of homozygous deletions. J Natl Cancer Inst 2007; 99: 396-406. (Pubitemid 47073483)
28. Bovée JVMG,. Multiple osteochondromas. Orphanet J Rare Dis 2008; 3: 3.
29. Veugelers M, Vermeesch J, Watanabe K, et al., GPC4, the gene for human K-glypican, flanks GPC3 on Xq26: deletion of the GPC3-GPC4 gene cluster in one family with Simpson-Golabi-Behmel syndrome. Genomics 1998; 53: 1-11. (Pubitemid 28489641)
30. Veugelers M, Cat BD, Muyldermans SY, et al., Mutational analysis of the GPC3/GPC4 glypican gene cluster on Xq26 in patients with Simpson-Golabi-Behmel syndrome: identification of loss-of-function mutations in the GPC3 gene. Hum Mol Genet 2000; 9: 1321-1328. (Pubitemid 30312481)
31. Lindsay S, Ireland M, O'Brien O, et al., Large scale deletions in the GPC3 gene may account for a minority of cases of Simpson-Golabi-Behmel syndrome. J Med Genet 1997; 34: 480-483. (Pubitemid 27268126)
32. LeClair EE, Mui SR, Huang A, et al., Craniofacial skeletal defects of adult zebrafish gypican 4 (knypek) mutants. Dev Dyn 2009; 238: 2550-2563.
33. Hiraoka S, Furuichi T, Nishimura G, et al., Nucleotide-sugar transporter SLC35D1 is critical to chondroitin sulfate synthesis in cartilage and skeletal development in mouse and human. Nat Med 2007; 13: 1363-1367. (Pubitemid 350080551)
34. Rossi A, Superti-Furga A,. Mutations in the diastrophic dysplasia sulfate transporter (DTDST) gene (SLC26A2): 22 novel mutations, mutation review, associated skeletal phenotypes, and diagnostic relevance. Hum Mutat 2001; 17: 159-171. (Pubitemid 32187047)
35. Faiyaz-Ul-Haque M, Zaidi SHE, King LM, et al., Fine mapping of the X-linked split-hand/split-foot malformation (SHFM2) locus to a 5.1-Mb region on Xq26.3 and analysis of candidate genes. Clin Genet 2005; 67: 93-97.