δ-EF1 is a negative regulator of Ihh in the developing growth plate

Journal of Cell Biology

Volumn 187, Issue 5, 2009, Pages 685-699

  Bellon, Ellen ^a   Luyten, Frank P ^a   Tylzanowski, Przemko ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EF1 DELTA; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; IHH PROTEIN, MOUSE; MESSENGER RNA; ZFHX1A PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BONE GROWTH; BONE MASS; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; GENE; GENE EXPRESSION REGULATION; GROWTH PLATE; IHH GENE; INTRON; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRABECULAR BONE; AMINO ACID SEQUENCE; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIMB; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; PHYSIOLOGY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ERINACEIDAE;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; CHONDROCYTES; EXTREMITIES; GROWTH PLATE; HEDGEHOG PROTEINS; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 74049159081     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200904034     Document Type: Article

References (73)

1. Antoine, M., and P. Kiefer. 1998. Functional characterization of transcriptional regulatory elements in the upstream region and intron 1 of the human S6 ribosomal protein gene. Biochem. J. 336:327-335.
2. Bi, W., J.M. Deng, Z. Zhang, R.R. Behringer, and B. de Crombrugghe. 1999. Sox9 is required for cartilage formation. Nat. Genet. 22:85-89. doi:10.1038/8792
3. Bitgood, M.J., and A.P. McMahon. 1995. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:126-138. doi:10.1006/dbio.1995.0010
4. Cabanillas, A.M., and D.S. Darling. 1996. Alternative splicing gives rise to two isoforms of Zfhep, a zinc finger/homeodomain protein that binds T3-response elements. DNA Cell Biol. 15:643-651. doi:10.1089/dna.1996.15. 643
5. Chen, Y., and G. Struhl. 1996. Dual roles for patched in sequestering and transducing Hedgehog. Cell. 87:553-563. doi:10.1016/S0092-8674(00)81374- 4
6. Chen, X., C.M. Macica, A. Nasiri, and A.E. Broadus. 2008. Regulation of articular chondrocyte proliferation and differentiation by indian hedgehog and parathyroid hormone-related protein in mice. Arthritis Rheum. 58:3788-3797. doi:10.1002/art.23985
7. Cohen, M.M. Jr. 2003. The hedgehog signaling network. Am. J. Med. Genet. A. 123A:5-28. doi:10.1002/ajmg.a.20495
8. Colnot, C., L. de la Fuente, S. Huang, D. Hu, C. Lu, B. St-Jacques, and J.A. Helms. 2005. Indian hedgehog synchronizes skeletal angiogenesis and perichondrial maturation with cartilage development. Development. 132:1057-1067. doi:10.1242/dev.01649
9. Comijn, J., G. Berx, P. Vermassen, K. Verschueren, L. van Grunsven, E. Bruyneel, M. Mareel, D. Huylebroeck, and F. van Roy. 2001. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell. 7:1267-1278. doi:10.1016/S1097-2765(01)00260-X
10. Davies, S.R., S. Sakano, Y. Zhu, and L.J. Sandell. 2002. Distribution of the transcription factors Sox9, AP-2, and [delta]EF1 in adult murine articular and meniscal cartilage and growth plate. J. Histochem. Cytochem. 50:1059-1065.
11. Dillner, N.B., and M.M. Sanders. 2004. Transcriptional activation by the zinc-finger homeodomain protein delta EF1 in estrogen signaling cascades. DNA Cell Biol. 23:25-34. doi:10.1089/104454904322745907
12. Dubchak, I., M. Brudno, G.G. Loots, L. Pachter, C. Mayor, E.M. Rubin, and K.A. Frazer. 2000. Active conservation of noncoding sequences revealed by three-way species comparisons. Genome Res. 10:1304-1306. doi:10.1101/gr.142200
13. Eger, A., K. Aigner, S. Sonderegger, B. Dampier, S. Oehler, M. Schreiber, G. Berx, A. Cano, H. Beug, and R. Foisner. 2005. DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene. 24:2375-2385. doi:10.1038/sj.onc.1208429
14. Franklin, A.J., T.L. Jetton, K.D. Shelton, and M.A. Magnuson. 1994. BZP, a novel serum-responsive zinc finger protein that inhibits gene transcription. Mol. Cell. Biol. 14:6773-6788.
15. Frazer, K.A., L. Pachter, A. Poliakov, E.M. Rubin, and I. Dubchak. 2004. VISTA: computational tools for comparative genomics. Nucleic Acids Res. 32:W273-W279. doi:10.1093/nar/gkh458
16. Funahashi, J., R. Sekido, K. Murai, Y. Kamachi, and H. Kondoh. 1993. Delta-crystallin enhancer binding protein delta EF1 is a zinc finger-homeodomain protein implicated in postgastrulation embryogenesis. Development. 119:433-446.
17. Genetta, T., D. Ruezinsky, and T. Kadesch. 1994. Displacement of an E-box-binding repressor by basic helix-loop-helix proteins: implications for B-cell specificity of the immunoglobulin heavy-chain enhancer. Mol. Cell. Biol. 14:6153-6163.
18. Guo, X., K.K. Mak, M.M. Taketo, and Y. Yang. 2009. The Wnt/beta-catenin pathway interacts differentially with PTHrP signaling to control chondrocyte hypertrophy and final maturation. PLoS One. 4:e6067. doi:10.1371/journal. pone.0006067
19. Hamburger, V., and H.L. Hamilton. 1992. A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 195:231-272.
20. Hammerschmidt, M., A. Brook, and A.P. McMahon. 1997. The world according to hedgehog. Trends Genet. 13:14-21. doi:10.1016/S0168-9525(96)10051-2
21. Hilton, M.J., X. Tu, and F. Long. 2007. Tamoxifen-inducible gene deletion reveals a distinct cell type associated with trabecular bone, and direct regulation of PTHrP expression and chondrocyte morphology by Ihh in growth region cartilage. Dev. Biol. 308:93-105. doi:10.1016/j.ydbio.2007.05.011
22. Himly, M., D.N. Foster, I. Bottoli, J.S. Iacovoni, and P.K. Vogt. 1998. The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology. 248:295-304. doi:10.1006/viro.1998.9290
23. Hogan, B., R. Beddington, and F.L.E. Constantini. 2004. Manipulating the mouse embryo. Cold Spring Laboratory Press. 487 pp.
24. Iwasaki, M., A.X. Le, and J.A. Helms. 1997. Expression of indian hedgehog, bone morphogenetic protein 6 and gli during skeletal morphogenesis. Mech. Dev. 69:197-202. doi:10.1016/S0925-4773(97)00145-7
25. Jethanandani, P., and R.H. Kramer. 2005. Alpha7 integrin expression is negatively regulated by deltaEF1 during skeletal myogenesis. J. Biol. Chem. 280:36037-36046. doi:10.1074/jbc.M508698200
26. Kamachi, Y., and H. Kondoh. 1993. Overlapping positive and negative regulatory elements determine lens-specific activity of the delta 1-crystallin enhancer. Mol. Cell. Biol. 13:5206-5215.
27. Karp, S.J., E. Schipani, B. St-Jacques, J. Hunzelman, H. Kronenberg, and A.P. McMahon. 2000. Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development. 127:543-548.
28. Kindblom, J.M., O. Nilsson, T. Hurme, C. Ohlsson, and L. Sävendahl. 2002. Expression and localization of Indian hedgehog (Ihh) and parathyroid hormone related protein (PTHrP) in the human growth plate during pubertal development. J. Endocrinol. 174:R1-R6. doi:10.1677/joe.0.174R001
29. Kobayashi, T., D.W. Soegiarto, Y. Yang, B. Lanske, E. Schipani, A.P. McMahon, and H.M. Kronenberg. 2005. Indian hedgehog stimulates periarticular chondrocyte differentiation to regulate growth plate length independently of PTHrP. J. Clin. Invest. 115:1734-1742. doi:10.1172/JCI24397
30. Koziel, L., M. Kunath, O.G. Kelly, and A. Vortkamp. 2004. Ext1-dependent heparan sulfate regulates the range of Ihh signaling during endochondral ossification. Dev. Cell. 6:801-813. doi:10.1016/j.devcel.2004.05.009
31. Kronenberg, H.M. 2003. Developmental regulation of the growth plate. Nature. 423:332-336. doi:10.1038/nature01657
32. Lanske, B., M. Amling, L. Neff, J. Guiducci, R. Baron, and H.M. Kronenberg. 1999. Ablation of the PTHrP gene or the PTH/PTHrP receptor gene leads to distinct abnormalities in bone development. J. Clin. Invest. 104:399-407. doi:10.1172/JCI6629
33. Lodder, E.M., A.J. Hoogeboom, J.H. Coert, and E. de Graaff. 2008. Deletion of 1 amino acid in Indian hedgehog leads to brachydactylyA1. Am. J. Med. Genet. A. 146A:2152-2154. doi:10.1002/ajmg.a.32441
34. Long, F., X.M. Zhang, S. Karp, Y. Yang, and A.P. McMahon. 2001. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development. 128:5099-5108.
35. Long, F., U.I. Chung, S. Ohba, J. McMahon, H.M. Kronenberg, and A.P. McMahon. 2004. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development. 131:1309-1318. doi:10.1242/dev.01006
36. Maeda, Y., E. Nakamura, M.T. Nguyen, L.J. Suva, F.L. Swain, M.S. Razzaque, S. Mackem, and B. Lanske. 2007. Indian Hedgehog produced by post-natal chondrocytes is essential for maintaining a growth plate and trabecular bone. Proc. Natl. Acad. Sci. USA. 104:6382-6387. doi:10.1073/pnas.0608449104
37. Mak, K.K., Y. Bi, C. Wan, P.T. Chuang, T. Clemens, M. Young, and Y. Yang. 2008. Hedgehog signaling in mature osteoblasts regulates bone formation and resorption by controlling PTHrP and RANKL expression. Dev. Cell. 14:674-688. doi:10.1016/j.devcel.2008.02.003
38. Marigo, V., R.A. Davey, Y. Zuo, J.M. Cunningham, and C.J. Tabin. 1996. Biochemical evidence that patched is the Hedgehog receptor. Nature. 384:176-179. doi:10.1038/384176a0
39. Matise, M.P., and A.L. Joyner. 1999. Gli genes in development and cancer. Oncogene. 18:7852-7859. doi:10.1038/sj.onc.1203243
40. Mullor, J.L., P. Sánchez, and A. Ruiz i Altaba. 2002. Pathways and consequences: Hedgehog signaling in human disease. Trends Cell Biol. 12:562-569. doi:10.1016/S0962-8924(02)02405-4
41. Murakami, S., and M. Noda. 2000. Expression of Indian hedgehog during fracture healing in adult rat femora. Calcif. Tissue Int. 66:272-276. doi:10.1007/PL00005843
42. Murray, D., P. Precht, R. Balakir, and W.E. Horton Jr. 2000. The transcription factor deltaEF1 is inversely expressed with type II collagen mRNA and can repress Col2a1 promoter activity in transfected chondrocytes. J. Biol. Chem. 275:3610-3618. doi:10.1074/jbc.275.5.3610
43. Nieuwenhuis, E., and C.C. Hui. 2005. Hedgehog signaling and congenital malformations. Clin. Genet. 67:193-208. doi:10.1111/j.1399-0004.2004. 00360.x
44. Nishimura, G., I. Manabe, K. Tsushima, K. Fujiu, Y. Oishi, Y. Imai, K. Maemura, M. Miyagishi, Y. Higashi, H. Kondoh, and R. Nagai. 2006. DeltaEF1 mediates TGF-beta signaling in vascular smooth muscle cell differentiation. Dev. Cell. 11:93-104. doi:10.1016/j.devcel.2006.05.011
45. Ohba, S., H. Kawaguchi, F. Kugimiya, T. Ogasawara, N. Kawamura, T. Saito, T. Ikeda, K. Fujii, T. Miyajima, A. Kuramochi, et al. 2008. Patched1 haploinsufficiency increases adult bone mass and modulates Gli3 repressor activity. Dev. Cell. 14:689-699. doi:10.1016/j.devcel.2008.03.007
46. Papin, C., L.A. van Grunsven, K. Verschueren, D. Huylebroeck, and J.C. Smith. 2002. Dynamic regulation of Brachyury expression in the amphibian embryo by XSIP1. Mech. Dev. 111:37-46. doi:10.1016/S0925-4773(01)00599-8
47. Postigo, A.A., and D.C. Dean. 1997. ZEB, a vertebrate homolog of Drosophila Zfh-1, is a negative regulator of muscle differentiation. EMBO J. 16: 3935-3943. doi:10.1093/emboj/16.13.3935
48. Provot, S., and E. Schipani. 2005. Molecular mechanisms of endochondral bone development. Biochem. Biophys. Res. Commun. 328:658-665. doi:10.1016/j.bbrc.2004.11.068
49. Provot, S., H. Kempf, L.C. Murtaugh, U.I. Chung, D.W. Kim, J. Chyung, H.M. Kronenberg, and A.B. Lassar. 2006. Nkx3.2/Bapx1 acts as a negative regulator of chondrocyte maturation. Development. 133:651-662. doi:10.1242/dev.02258
50. Reid, L.H., R.G. Gregg, O. Smithies, and B.H. Koller. 1990. Regulatory elements in the introns of the human HPRT gene are necessary for its expression in embryonic stem cells. Proc. Natl. Acad. Sci. USA. 87:4299-4303. doi:10.1073/pnas.87.11.4299
51. Remacle, J.E., H. Kraft, W. Lerchner, G. Wuytens, C. Collart, K. Verschueren, J.C. Smith, and D. Huylebroeck. 1999. New mode of DNA binding of multi-zinc finger transcription factors: deltaEF1 family members bind with two hands to two target sites. EMBO J. 18:5073-5084. doi:10.1093/emboj/18.18. 5073
52. Rodda, S.J., and A.P. McMahon. 2006. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development. 133:3231-3244. doi:10.1242/dev.02480
53. Rosen, V., J. Capparella, D. McQuaid, K. Cox, R.S. Thies, J. Song, and J. Wozney. 1993. Development of immortalized cells derived from 13DPC mouse limb buds as a system to study the effects of recombinant human bone morphogenetic protein-2 (rhBMP-2) on limb bud cell differentiation. Prog. Clin. Biol. Res. 383A:305-315.
54. Rupp, R.A., L. Snider, and H. Weintraub. 1994. Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8:1311-1323. doi:10.1101/gad.8.11.1311
55. Sekido, R., K. Murai, J. Funahashi, Y. Kamachi, A. Fujisawa-Sehara, Y. Nabeshima, and H. Kondoh. 1994. The delta-crystallin enhancer-binding protein delta EF1 is a repressor of E2-box-mediated gene activation. Mol. Cell. Biol. 14:5692-5700.
56. Sekido, R., T. Takagi, M. Okanami, H. Moribe, M. Yamamura, Y. Higashi, and H. Kondoh. 1996. Organization of the gene encoding transcriptional repressor deltaEF1 and cross-species conservation of its domains. Gene. 173:227-232. doi:10.1016/0378-1119(96)00185-0
57. Sekido, R., K. Murai, Y. Kamachi, and H. Kondoh. 1997. Two mechanisms in the action of repressor deltaEF1: binding site competition with an activator and active repression. Genes Cells. 2:771-783. doi:10.1046/j.1365-2443.1997. 1570355.x
58. Smith, A.N., M.L. Barth, T.L. McDowell, D.S. Moulin, H.N. Nuthall, M.A. Hollingsworth, and A. Harris. 1996. A regulatory element in intron 1 of the cystic fibrosis transmembrane conductance regulator gene. J. Biol. Chem. 271:9947-9954. doi:10.1074/jbc.271.17.9947
59. Smits, P., P. Dy, S. Mitra, and V. Lefebvre. 2004. Sox5 and Sox6 are needed to develop and maintain source, columnar, and hypertrophic chondrocytes in the cartilage growth plate. J. Cell Biol. 164:747-758. doi:10.1083/jcb.200312045
60. Später, D., T.P. Hill, R.J. O'sullivan, M. Gruber, D.A. Conner, and C. Hartmann. 2006. Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development. 133:3039-3049. doi:10.1242/dev.02471
61. St-Jacques, B., M. Hammerschmidt, and A.P. McMahon. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13:2072-2086. doi:10.1101/gad.13.16.2072
62. Stone, D.M., M. Hynes, M. Armanini, T.A. Swanson, Q. Gu, R.L. Johnson, M.P. Scott, D. Pennica, A. Goddard, H. Phillips, et al. 1996. The tumour-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature. 384:129-134. doi:10.1038/384129a0
63. Takagi, T., H. Moribe, H. Kondoh, and Y. Higashi. 1998. DeltaEF1, a zinc finger and homeodomain transcription factor, is required for skeleton patterning in multiple lineages. Development. 125:21-31.
64. Tavella, S., R. Biticchi, A. Schito, E. Minina, D. Di Martino, A. Pagano, A. Vortkamp, W.A. Horton, R. Cancedda, and S. Garofalo. 2004. Targeted expression of SHH affects chondrocyte differentiation, growth plate organization, and Sox9 expression. J. Bone Miner. Res. 19:1678-1688. doi:10.1359/JBMR.040706
65. Terraz, C., D. Toman, M. Delauche, P. Ronco, and J. Rossert. 2001. delta Ef1 binds to a far upstream sequence of the mouse pro-alpha 1(I) collagen gene and represses its expression in osteoblasts. J. Biol. Chem. 276:37011-37019. doi:10.1074/jbc.M104185200
66. Tickle, C. 2004. The contribution of chicken embryology to the understanding of vertebrate limb development. Mech. Dev. 121:1019-1029. doi:10.1016/j.mod.2004.05.015
67. Tylzanowski, P., K. Verschueren, D. Huylebroeck, and F.P. Luyten. 2001. Smad-interacting protein 1 is a repressor of liver/bone/kidney alkaline phosphatase transcription in bone morphogenetic protein-induced osteogenic differentiation of C2C12 cells. J. Biol. Chem. 276:40001-40007. doi:10.1074/jbc.M104112200
68. Tylzanowski, P., D. De Valck, V. Maes, J. Peeters, and F.P. Luyten. 2003. Zfhx1a and Zfhx1b mRNAs have non-overlapping expression domains during chick and mouse midgestation limb development. Gene Expr. Patterns. 3:39-42. doi:10.1016/S1567-133X(02)00092-3
69. Verschueren, K., J.E. Remacle, C. Collart, H. Kraft, B.S. Baker, P. Tylzanowski, L. Nelles, G. Wuytens, M.T. Su, R. Bodmer, et al. 1999. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J. Biol. Chem. 274:20489-20498. doi:10.1074/jbc.274.29.20489
70. Vortkamp, A., K. Lee, B. Lanske, G.V. Segre, H.M. Kronenberg, and C.J. Tabin. 1996. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 273:613-622. doi:10.1126/science.273. 5275.613
71. Watanabe, Y., K. Kawakami, Y. Hirayama, and K. Nagano. 1993. Transcription factors positively and negatively regulating the Na,K-ATPase alpha 1 subunit gene. J. Biochem. 114:849-855.
72. Williams, T.M., D. Moolten, J. Burlein, J. Romano, R. Bhaerman, A. Godillot, M. Mellon, F.J. Rauscher III, and J.A. Kant. 1991. Identification of a zinc finger protein that inhibits IL-2 gene expression. Science. 254:1791-1794. doi:10.1126/science.1840704
73. Yoshida, C.A., H. Yamamoto, T. Fujita, T. Furuichi, K. Ito, K. Inoue, K. Yamana, A. Zanma, K. Takada, Y. Ito, and T. Komori. 2004. Runx2 and Runx3 are essential for chondrocyte maturation, and Runx2 regulates limb growth through induction of Indian hedgehog. Genes Dev. 18:952-963. doi:10.1101/gad. 1174704