Multiple roles of mesenchymal β-catenin during murine limb patterning

Development

Volumn 133, Issue 7, 2006, Pages 1219-1229

  Hill, Theo P ^a   Taketo, Makoto M ^b   Birchmeier, Walter ^c   Hartmann, Christine ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b KYOTO UNIVERSITY   (Japan)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Catenin; AER; BMP; Dorsoventral axis; Emx2; Limb patterning; Lmx1b; Scapula

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; OSTEOGENIC PROTEIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTION FACTOR GREMLIN; TRANSCRIPTION FACTOR LMX1B; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR PAX1; UNCLASSIFIED DRUG; WNT PROTEIN; WNT7A PROTEIN;

AGENESIS; ARTICLE; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; FORELIMB; GENE OVEREXPRESSION; GENE TARGETING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LIMB DEVELOPMENT; MESENCHYME; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCANNING ELECTRON MICROSCOPY; SCAPULA; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ALLELES; ANIMALS; BETA CATENIN; BIOLOGICAL MARKERS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; DNA-BINDING PROTEINS; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIMB BUD; LIMB DEFORMITIES, CONGENITAL; MESODERM; MICE; MICE, MUTANT STRAINS; MSX1 TRANSCRIPTION FACTOR; SCAPULA; TRANSCRIPTION FACTORS; UP-REGULATION; WNT PROTEINS;

MURINAE;

EID: 33646130168     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02298     Document Type: Article

References (72)

1. Adamska, M., Billi, A. C., Cheek, S. and Meisler, M. H. (2005). Genetic interaction between Wnt7a and Lrp6 during patterning of dorsal and posterior structures of the mouse limb. Dev. Dyn. 233, 368-372.
2. Agarwal, P., Wylie, J. N., Galceran, J., Arkhitko, O., Li, C., Deng, C., Grosschedl, R. and Bruneau, B. G. (2003). Tbx5 is essential for forelimb bud initiation following patterning of the limb field in the mouse embryo. Development 130, 623-633.
3. Ahn, D. G., Kourakis, M. J., Rohde, L. A., Silver, L. M. and Ho, R. K. (2002). T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417, 754-758.
4. Backman, M., Machon, O., Mygland, L., van den Bout, C. J., Zhong, W., Taketo, M. M. and Krauss, S. (2005). Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev. Biol. 279, 155-168.
5. Barrow, J. R., Thomas, K. R., Boussadia-Zahui, O., Moore, R., Kemler, R., Capecchi, M. R. and McMahon, A. R. (2003). Ectodermal Wnt3/ beta-catenin signaling is required for the establishment and maintenance of the apical ectodermal ridge. Genes Dev. 17, 394-409.
6. Bennett, C. N., Ross, S. E., Longo, K. A., Bajnok, L., Hemati, N., Johnson, K. W., Harrison, S. D. and MacDougald, O. A. (2002). Regulation of Wnt signaling during adipogenesis. J. Biol. Chem. 277, 30998-31004.
7. Boulet, A. M., Moon, A. M., Arenkiel, B. R. and Capecchi, M. R. (2004). The roles of Fgf4 and Fgf8 in limb bud initiation and outgrowth. Dev. Biol. 273, 361-372.
8. Capdevila, J., Tsukui, T., Rodriquez Esteban, C., Zappavigna, V. and Izpisua Belmonte, J. C. (1999). Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mal. Cell 4, 839-849.
9. Caricasole, A., Ferraro, T., Iacovelli, L., Barletta, E., Caruso, A., Melchiorri, D., Terstappen, G. C. and Nicoletti, F (2003). Functional characterization of WNT7A signaling in PC12 cells: interaction with A FZD5 × LRP6 receptor complex and modulation by Dickkopf proteins. J. Biol. Chem. 278, 37024-37031.
10. Chen, H., Lun, Y., Ovchinnikov, D., Kokubo, H., Oberg, K. C., Pepicelli, C. V., Gan, L., Lee, B. and Johnson, R. L. (1998). Limb and kidney defects in Lmx1b mutant mice suggest an involvement of LMX1B in human nail patella syndrome. Nat Genet 19, 51-55.
11. Chiang, C., Litingitung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
12. Church, V. L. and Francis-West, P. (2002). Wnt signalling during limb development. Int. J. Dev Biol. 46, 927-936.
13. Cygan, J. A., Johnson, R. L. and McMahon, A. P. (1997). Novel regulatory interactions revealed by studies of murine limb pattern in Wnt-7a and En-1 mutants. Development 124, 5021-5032.
14. Day, T. F, Guo, X., Garrett-Beal, L. and Yang, Y. (2005). Wnt/ beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 8, 739-750.
15. Dreyer, S. D., Zhou, G., Baldini, A., Winterpacht, A., Zabel, B., Cole, W., Johnson, R. L. and Lee, B. (1998). Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome. Nat. Genet. 19, 47-50.
16. Favier, B., Rijli, F. M., Fromental-Ramain, C., Fraulob, V, Chambon, P. and Dolle, P. (1996). Functional cooperation between the non-paralogous genes Hoxa-10 and Hoxd-11 in the developing forelimb and axial skeleton. Development 122, 449-460.
17. Fromental-Ramain, C., Warot, X., Messadecq, N., LeMeur, M., Dolle, P. and Chambon, P. (1996). Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997-3011.
18. -/--like phenotype and limb deficiency in Lef1(-/ -)Tcf1(-/-) mice. Genes Dev 13, 709-717.
19. Galceran, J., Hsu, S. C. and Grosschedl, R. (2001). Rescue of a Wnt mutation by an activated form of LEF-1: regulation of maintenance but not initiation of Brachyury expression. Proc. Natl. Acad. Sci. USA 98, 8668-8673.
20. Garrity, D. M., Childs, S. and Fishman, M. C. (2002). The heartstrings mutation in zebrafish causes heart/fin Tbx5 deficiency syndrome. Development 129, 4635-4645.
21. Guha, U., Gomes, W. A., Kobayashi, T., Pestell, R. G. and Kessler J. A. (2002). In vivo evidence that BMP signaling is necessary for apoptosis in the mouse limb. Dev. Biol. 249, 108-120.
22. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M. and Taketo, M. M. (1999). Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942.
23. Hill, T. R, Spater, D., Taketo, M. M., Birchmeier, W. and Hartmann, C. (2005). Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8, 727-738.
24. Hovanes, K., Li, T. W., Munguia, J. E., Truong, T., Milovanovic, T, Lawrence Marsh, J., Holcombe, R. F. and Waterman, M. L. (2001). Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet. 28, 53-57.
25. Howe, L. R., Watanabe, O., Leonard, J. and Brown, A. M. (2003). Twist is upregulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res. 63, 1906-1913.
26. Huelsken, J., Vogel, R., Brinkmann, V., Erdmann, B., Birchmeier, C. and Birchmeier, W. (2000). Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148, 567-578.
27. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G. and Birchmeier, W. (2001). beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533-545.
28. Kawakami, Y., Capdevila, J., Buscher, D., Itoh, T, Rodriguez Esteban, C. and Izpisua Belmonte, J. C. (2001). WNT signals control FGF-dependent limb initiation and AER induction in the chick embryo. Cell 104, 891-900.
29. Kengaku, M., Capdevila, J., Rodriguez-Esteban, C., De La Pena, J., Johnson, R. L., Belmonte, J. C. and Tabin, C. J. (1998). Distinct WNT pathways regulating AER formation and dorsoventral polarity in the chick limb bud. Science 280,1274-1277.
30. Khokha, M. K., Hsu, D., Brunet, L. J., Dionne, M. S. and Harland, R. M. (2003). Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat. Genet. 34, 303-307.
31. Laufer, E., Nelson, C. E., Johnson, R. L., Morgan, B. A. and Tabin, C. (1994). Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79, 993-1003.
32. Liu, C., Nakamura, E., Knezevic, V., Hunter, S., Thompson, K. and Mackem, S. (2003). A role for the mesenchymal T-box gene Brachyury in AER formation during limb development. Development 130, 1327-1337.
33. Lobe, C. G. K. K., Kreppner, W., Lomeli, H., Gertsenstein, M. and Nagy, A. (1999). Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208, 281-292.
34. Logan, M., Martin, J. F., Nagy, A., Lobe, C., Olson, E. N. and Tabin, C. J. (2002). Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80.
35. Loomis, C. A., Harris, E., Michaud, J., Wurst, W., Hanks, M. and Joyner, A. L. (1996). The mouse Engrailed-1 gene and ventral limb patterning. Nature 382, 360-363.
36. Loomis, C. A., Kimmel, R. A., Tong, C. X., Michaud, J. and Joyner, A. L. (1998). Analysis of the genetic pathway leading to formation of ectopic apical ectodermal ridges in mouse Engrailed-1 mutant limbs. Development 125, 1137-1148.
37. Martin, G. R. (1998). The roles of FGFs in the early development of vertebrate limbs. Genes Dev. 12, 1571-1586.
38. McLeod, M. J. (1980). Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22, 299-301.
39. Mercader, N., Leonardo, E., Azpiazu, N., Serrano, A., Morata, G., Martinez, C. and Torres, M. (1999). Conserved regulation of proximodistal limb axis development by Meis1/Hth. Nature 402, 425-429.
40. Michos, O., Panman, L., Vintersten, K., Beier, K., Zeller, R. and Zuniga, A. (2004). Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131, 3401-3410.
41. Murtaugh, L. C., Chyung, J. H. and Lassar, A. B. (1999). Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13, 225-237.
42. Nelson, C. E., Morgan, B. A., Burke, A. C., Laufer, E., DiMambro, E., Murtaugh, L. C., Gonzales, E., Tessarollo, L., Parada, L. F. and Tabin, C. (1996). Analysis of Hox gene expression in the chick limb bud. Development 122, 1449-1466.
43. Ng, J. K., Kawakami, Y., Buscher, D., Raya, A., Itoh, T, Koth, C. M., Rodriguez Esteban, C., Rodriguez-Leon, J., Garrity, D. M., Fishman, M. C. et al. (2002). The limb identity gene Tbx5 promotes limb initiation by interacting with Wnt2b and Fgf10. Development 129, 5161-5170.
44. Niswander, L. (2003). Pattern formation: old models out on a limb. Nat. Rev. Genet. 4, 133-143.
45. Parr, B. A. and McMahon, A. P. (1995). Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374, 350-353.
46. Pellegrini, M., Pantano, S., Fumi, M. P., Lucchini, F. and Forabosco, A. (2001). Agenesis of the scapula in Emx2 homozygous mutants. Dev. Biol. 232, 149-156.
47. Pereira, R. C., Economides, A. N. and Canalis, E. (2000). Bone morphogenetic proteins induce gremlin, a protein that limits their activity in osteoblasts. Endocrinology 141, 4558-4563.
48. Pizette, S. and Niswander, L. (1999). BMPs negatively regulate structure and function of the limb apical ectodermal ridge. Development 126, 883-894.
49. Rallis, C., Bruneau, B. G., Del Buono, J., Seidman, C. E., Seidman, J. G., Nissim, S., Tabin, C. J. and Logan, M. P. (2003). Tbx5 is required for forelimb bud formation and continued outgrowth. Development 130, 2741-2751.
50. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
51. Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T. M. and Tabin, C. (1995). Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631-640.
52. Saunders, J. (1948). The proximo-distal sequence of the origin of the parts of the chick wing and the role of ectoderm. J. Exp. Zool. 108, 363-403.
53. Scherz, P. J., Harfe, B. D., McMahon, A. P. and Tabin, C. J. (2004). The limb bud Shh-Fgf feedback loop is terminated by expansion of former ZPA cells. Science 305, 396-399.
54. Soshnikova, N., Zechner, D., Huelsken, J., Mishina, Y., Behringer R. R., Taketo, M. M., Crenshaw, E. B., 3rd and Birchmeier, W. (2003). Genetic interaction between Wnt/beta-catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb. Genes Dev 17, 1963-1968.
55. Sun, X., Lewandoski, M., Meyers, E. N., Liu, Y. H., Maxson, R. E., Jr and Martin, G. R. (2000). Conditional inactivation of Fgf4 reveals complexity of signalling during limb bud development. Nat. Genet. 25, 83-86.
56. Sun, X., Mariani, F. V. and Martin, G. R. (2002). Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418, 501-508.
57. Takeuchi, J. K., Koshiba-Takeuchi, K., Suzuki, T., Kamimura, M., Ogura, K. and Ogura, T. (2003). Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascade. Development 130, 2729-2739.
58. te Welscher, P., Zuniga, A., Kuijper, S., Drenth, T., Goedemans, H. J., Meijlink, F. and Zeller, R. (2002). Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298, 827-830.
59. Theil, T, Aydin, S., Koch, S., Grotewold, L. and Ruther, U. (2002). Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 129, 3045-3054.
60. Theiler, K. (1989). The House Mouse - Atlas of Embryonic Development. New York, USA: Springer Verlag.
61. Tickle, C. (2003). Patterning systems - from one end of the limb to the other. Dev. Cell 4, 449-458.
62. Timmons, P. M., Wallin, J., Rigby, P. W. and Balling, R. (1994). Expression and function of Pax 1 during development of the pectoral girdle. Development 120, 2773-2785.
63. Topol, L., Jiang, X., Choi, H., Garrett-Beal, L., Carolan, P. J. and Yang, Y. (2003). Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J. Cell Biol. 162, 899-908.
64. Vogel, A., Rodriguez, C., Warnken, W. and Izpisua Belmonte, J. C. (1995). Dorsal cell fate specified by chick Lmx1 during vertebrate limb development. Nature 378, 716-720.
65. Wahba, G. M., Hostikka, S. L. and Carpenter, E. M. (2001). The paralogous Hox genes Hoxa10 and Hoxd10 interact to pattern the mouse hindlimb peripheral nervous system and skeleton. Dev. Biol. 231, 87-102.
66. Wilm, B., Dahl, E., Peters, H., Balling, R. and Imai, K. (1998). Targeted disruption of Pax1 defines its null phenotype and proves haploinsufficiency. Proc. Natl. Acad. Sci. USA 95, 8692-8697.
67. Yamaguchi, T. P., Bradley, A., McMahon, A. P. and Jones, S. (1999a). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223.
68. Yamaguchi, T. P., Takada, S., Yoshikawa, Y., Wu, N. and McMahon, A. P. (1999b). T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13, 3185-3190.
69. Yang, Y. (2003). Wnts and wing: Wnt signaling in vertebrate limb development and musculoskeletal morphogenesis. Birth Defects Res. C Embryo Today 69, 305-317.
70. Zuniga, A., Haramis, A. P., McMahon, A. P. and Zeller, R. (1999). Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 401, 598-602.
71. Zuniga, A., Quillet, R., Perrin-Schmitt, F. and Zeller, R. (2002). Mouse Twist is required for fibroblast growth factor-mediated epithelial-mesenchymal signalling and cell survival during limb morphogenesis. Mech. Dev. 114, 51-59.
72. Zuniga, A., Michos, O., Spitz, F., Haramis, A. P., Panman, L., Galli, A., Vintersten, K., Klasen, C., Mansfield, W., Kuc, S. et al. (2004). Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Genes Dev. 18, 1553-1564.