Synovial joint formation requires local Ext1 expression and heparan sulfate production in developing mouse embryo limbs and spine

Developmental Biology

Volumn 351, Issue 1, 2011, Pages 70-81

  Mundy, Christina ^a   Yasuda, Tadashi ^a   Kinumatsu, Takashi ^a   Yamaguchi, Yu ^b   Iwamoto, Masahiro ^a   Enomoto Iwamoto, Motomi ^a   Koyama, Eiki ^a   Pacifici, Maurizio ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

Ext1; Heparan sulfate; Intervertebral joints; Limb synovial joint formation; Lubricin; Mouse skeletogenesis; Spine

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; COLLAGEN TYPE 2; COLLAGEN TYPE 2A; HEPARAN SULFATE; MATRILLIN 1; MEMBRANE PROTEIN; PROTEIN EXT1; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EMBRYO DEVELOPMENT; EPIPHYSIS; JOINT; LIMB; MESENCHYME CELL; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SPINE; TRANSGENE;

ERINACEIDAE; MUS;

EID: 79651471593     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.12.022     Document Type: Article

References (52)

1. Albrecht A.N., Schwabe G.C., Striker S., Boddrich A., Wanker E.E., Mundllos S. The synpolydactyly homolog (spdh) mutation in the mouse-a defect in patterning and growth of limb cartilage elements. Mech. Dev. 2002, 112:53-67.
2. Andersen H. Histochemical studies on the histogenesis of the knee joint and superior tibio-fibular joint in human fetuses. Acta Anat. 1961, 46:279-303.
3. Archer C.W., Dowthwaite G.P., Francis-West P. Development of synovial joints. Birth Defects Res. Pt C 2003, 69:144-155.
4. Arikawa-Hirasawa E., Watanabe H., Takami H., Hassell J.R., Yamada Y. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 1999, 23:354-358.
5. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
6. Bishop J.R., Schuksz M., Esko J.D. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 2007, 446:1030-1037.
7. 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.
8. Christ B., Huang R., Scaal M. Formation and differentiation of the avian sclerotome. Anat. Embryol. 2004, 208:333-350.
9. David G., Bai X.M., van der Schueren B., Cassiman J.-J., van der Berghe H. Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol. 1992, 119:961-975.
10. Day T.F., Guo X., Garrett-Beal L., Yang Y. Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 2005, 8:739-750.
11. Esko J.D., Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 2002, 71:435-471.
12. Hacker U., Nybakken K., Perrimon N. Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. Mol. Cell Biol. 2005, 6:530-541.
13. Holder N. An experimental investigation into the early development of the chick elbow joint. J. Embryol. Exp. Morphol. 1977, 39:115-127.
14. Hyde G., Dover S., Aszodi A., Wallis G.A., Boot-Handford R.P. Lineage tracing using matrilin-1 gene expression reveals that articular chondrocytes exist as the joint interzone forms. Dev. Biol. 2007, 304:825-833.
15. Inatani M., Irie F., Plump A.S., Tessier-Lavigne M., Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 2003, 302:1044-1046.
16. Iwamoto M., Tamamura Y., Koyama E., Komori T., Takeshita N., Williams J.A., Nakamura T., Enomoto-Iwamoto M., Pacifici M. Transcription factor ERG and joint and articular cartilage formation during mouse limb and spine skeletogenesis. Dev. Biol. 2007, 305:40-51.
17. Jay G.D., Tantravahi U., Britt D.E., Barrach H.J., Cha C.J. Homology of lubricin and superficial zone protein (SZP): products of megakaryocyte stimulating factor (MSF) gene expression by human synovial fibroblasts and articular chondrocytes localized to chromosome 1q25. J. Orthop. Res. 2001, 19:677-687.
18. Jones A.R.C., Flannery C.R. Bioregulation of lubricin expression by growth factors and cytokines. Eur. Cells Mater. 2007, 13:40-45.
19. Kahn J., Shwartz Y., Blitz E., Krief S., Sharir A., Breitel D.A., Rattenbach R., Relaix F., Maire P., Roundtree R.B., Kingsley D.M., Zelzer E. Muscle contraction is necessary to maintain joint progenitor cell fate. Dev. Cell 2009, 16:734-743.
20. Koyama E., Golden E.B., Kirsch T., Adams S.L., Chandraratna R.A.S., Michaille J.-J., Pacifici M. Retinoid signaling is required for chondrocyte maturation and endochondral bone formation during limb skeletogenesis. Dev. Biol. 1999, 208:375-391.
21. 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.
22. Koyama E., Young B., Nagayama M., Shibukawa Y., Enomoto-Iwamoto M., Iwamoto M., Maeda Y., Lanske B., Song B., Serra R., Pacifici M. Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 2007, 134:2159-2169.
23. Koyama E., Shibukawa Y., Nagayama M., Sugito H., Young B., Yuasa T., Okabe T., Ochiai T., Kamiya N., Rountree R.B., Kingsley D.M., Iwamoto M., Enomoto-Iwamoto M., Pacifici M. A distinct cohort of progenitor cells participates in synovial joint and articular cartilage formation during mouse limb skeletogenesis. Dev. Biol. 2008, 316:62-73.
24. Koziel L., Kunath M., Kelly O.G., Vortkamp A. Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev. Cell 2004, 6:801-813.
25. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
26. Lin X. Functions of heparan sulfate proteoglycans in cell signaling during development. Development 2004, 131:6009-6021.
27. Lobe C.G., Koop K.E., Kreppner W., Lomeli H., Gertsenstein M., Nagy A. Z/AP, a double receptor for Cre-mediated recombination. Dev. Biol. 1999, 208:281-292.
28. Mak K.K., Chen M.-H., Day T.F., Chuang P.-T., Yang Y. Wnt/β-catenin signaling interacts differentially with Ihh signaling in controlling endochondral bone and synovial joint formation. Development 2006, 133:3695-3707.
29. Mattipalli V.R., Huang R., Patel K., Christ B., Scaal M. Arthrotome: a specific joint forming compartment in the avian somite. Dev. Dyn. 2005, 234:48-53.
30. Merino R., Macias D., Ganan Y., Economides A.N., Wang X., Wu Q., Stahl N., Sampath T.K., Varona P., Hurle J.M. Expression and function of Gdf-5 during digit skeletogenesis in the embryonic chick leg bud. Dev. Biol. 1999, 206:33-45.
31. Mitrovic D. Development of the diathrodial joints in the rat embryo. Am. J. Anat. 1978, 151:475-485.
32. Nalin A.M., Greenlee T.K., Sandell L.J. Collagen gene expression during development of avian synovial joints: transient expression of type II and XI collagen genes in the joint capsule. Dev. Dyn. 1995, 203:352-362.
33. Namimatsu S., Ghazizadeh M., Sugisaki Y. Reversing the effects of formalin fixation with citraconic anhydride and heat: a universal antigen retrieval method. J. Histochem. Cytochem. 2005, 53:3-11.
34. Naski M.C., Colvin J.S., Coffin J.D., Ornitz D.M. Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development 1998, 125:4977-4988.
35. Ovchinnikov D.A., Deng J.M., Ogunrinu G., Behringer R.R. Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis 2000, 26:145-146.
36. Pacifici M., Koyama E., Iwamoto M. Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries. Birth Defects Res. Pt C 2005, 75:237-248.
37. Pitsillides A.A. Early effects of embryonic movement: "a shot out of the dark". J. Anat. 2006, 208:417-431.
38. Rountree R.B., Schoor M., Chen H., Marks M.E., Harley V., Mishina Y., Kingsley D.M. BMP receptor signaling is required for postnatal maintenance of articular cartilage. PLoS Biol. 2004, 2:1815-1827.
39. Serra R., Johnson M., Filvaroff E.H., LaBorde J., Sheehan D.M., Derynck R., Moses H.L. Expression of a truncated, kinase-defective TGF-β type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J. Cell Biol. 1997, 139:541-552.
40. Shibukawa Y., Young B., Wu C., Yamada S., Long F., Pacifici M., Koyama E. Temporomandibular joint formation and condyle growth require Indian hedgehog signaling. Dev. Dyn. 2007, 236:426-434.
41. Shimo T., Gentili C., Iwamoto M., Wu C., Koyama E., Pacifici M. Indian hedgehog and syndecan-3 coregulate chondrocyte proliferation and function during chick limb skeletogenesis. Dev. Dyn. 2004, 229:607-617.
42. 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.
43. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
44. 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-β signaling is essential for joint morphogenesis. J. Cell Biol. 2007, 177:1105-1117.
45. Spater D., Hill T.P., Gruber M., Hartmann C. Role of canonical Wnt-signaling in joint formation. Eur. Cells Mater. 2006, 12:71-80.
46. 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, 13:2076-2086.
47. 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.
48. Towers M., Tickle C. Growing models of vertebrate limb development. Development 2009, 136:179-190.
49. Verbout A. The development of the vertebral column. Adv. Anat. Embryol. Cell Biol. 1985, 90:1-122.
50. Viviano B.L., L.S., Pflederer C., Paine-Saunders S., Mills K., Saunders S. Altered hematopoiesis in glypican-3-deficient mice results in decreased osteoclast differentiation and a delay in endochondral ossification. Dev. Biol. 2005, 282:152-162.
51. Watterson R., Fowler I., Fowler B. The role of the neural tube and notochord in development of the axial skeleton of the chick. Am. J. Anat. 1954, 95:337-397.
52. Zhao W., Sala-Newby G.B., Dhoot G.K. Sulf1 expression pattern and its role in cartilage and joint development. Dev. Dyn. 2006, 235:3327-3335.