Inactivation of mouse twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development

Development

Volumn 131, Issue 2, 2004, Pages 413-424

  Zakin, Lise ^a   De Robertis, E M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bmp; Chordin; Crossveinless; Holoprosencephaly; Tgf ; Tolloid; Twisted gastrulation; Vertebral column

Indexed keywords

BINDING PROTEIN; BONE MORPHOGENETIC PROTEIN 4; METALLOPROTEINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIRTH; BRAIN DEVELOPMENT; BRANCHIAL ARCH; COMPLEX FORMATION; CONTROLLED STUDY; DEATH; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EXTRACELLULAR SPACE; EYE MALFORMATION; FEMALE; FOREBRAIN; GENE MUTATION; HEAD; HOLOPROSENCEPHALY; HOMOZYGOSITY; MALE; MOUSE; MUTANT; NONHUMAN; OSTEOPOROSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VERTEBRA MALFORMATION; XENOPUS; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; BONE AND BONES; BONE DEVELOPMENT; BONE MORPHOGENETIC PROTEINS; BRANCHIAL REGION; CHONDROGENESIS; DNA; EYE ABNORMALITIES; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOLOPROSENCEPHALY; MALE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; PREGNANCY; PROSENCEPHALON; PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 0842344611     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00946     Document Type: Article

References (79)

1. Abreu, J. G., Ketpura, N. I., Reversade, B. and de Robertis, E. M. (2002). Connective-tissue ggowth factor (CTGF) modulates cell signalling by BMP and TGF-beta. Nat. Cell Biol. 4, 599-604.
2. Abu-Issa, R., Smyth, G., Smoak, I., Yamamura, K. and Meyers, E. N. (2002). Fgf8 is required for pharyngeal arch and cardiovascular development in the mouse. Development 129, 4613-4625.
3. Acampora, D., Merlo, G. R., Paleari, L., Zerega, B., Postiglione, M. P., Mantero, S., Bober, E., Barbieri, O., Simeone, A. and Levi, G. (1999). Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126, 3795-3809.
4. Anderson, R. M., Lawrence, A. R., Stottmann, R. W., Bachiller, D. and Klingensmith, J. (2002). Chordin and noggin promote organizing centers of forebrain development in the mouse. Development 129, 4975-4987.
5. Aszodi, A., Chan, D., Hunziker, E., Bateman, J. F. and Fassler, R. (1998). Collagen II is essential for the removal of the notochord and the formation of intervertebral discs. J. Cell Biol. 143, 1399-1412.
6. Bachiller, D., Klingensmith, J., Kemp, C., Belo, J. A., Anderson, R. M., May, S. R., McMahon, J. A., McMahon, A. P., Harland, R. M., Rossant, J. et al. (2000). The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature 403, 658-661.
7. Bachiller, D., Klingensmith, J., Shneyder, N., Tran, U., Anderson, R., Rossant, J. and de Robertis, E. M. (2003). The role of Chordin/BMP signals in mammalian pharyngeal development and DiGeorge syndrome. Development 130, 3567-3578.
8. Beddington, R. S. and Robertson, E. J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.
9. Bedford, F. K., Ashworth, A., Enver, T. and Wiedemann, L. M. (1993). HEX: a novel homeobox gene expressed during haematopoiesis and conserved between mouse and human. Nucleic Acids Res. 21, 1245-1249.
10. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and de Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
11. Belo, J. A., Leyns, L., Yamada, G. and de Robertis, E. M. (1998). The prechordal midline of the chondrocranium is defective in Goosecoid-1 mouse mutants. Mech. Dev. 72, 15-25.
12. Bridges, C. (1920). The mutant crossveinless in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 6, 660-663.
13. Blitz, I. L., Cho, K. W. and Chang, C. (2003). Twisted gastrulation loss-of-function analyses support its role as a BMP inhibitor during early Xenopus embryogenesis. Development 130, 4975-4988.
14. Canalis, E., Economides, A. N. and Gazzerro, E. (2003). Bone morphogenetic proteins, their antagonists, and the skeleton. Endocrinol. Rev. 24, 218-235.
15. Chang, C., Holtzman, D. A., Chan, S., Chickering, T., Woolf, E. A., Holmgren, L. M., Bodorova, J., Gearing, D. P., Holmes, W. E. and Brivanlou, A. H. (2001). Twisted gastrulation can function as a BMP antagonist. Nature 410, 483-487.
16. Chiang, C., Litingtung, 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.
17. Coffinier, C., Ketpura, N., Tran, U., Geissert, D. and de Robertis, E. M. (2002). Mouse Crossveinless-2 is the vertebrate homolog of a Drosophila extracellular regulator of BMP signaling. Mech. Dev. 119S, S179-S184.
18. Connors, S. A., Trout, J., Ekker, M. and Mullins, M. C. (1999). The role of tolloid/mini fin in dorsoventral pattern formation of the zebrafish embryo. Development 126, 3119-3130.
19. Crossley, P. H. and Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
20. De Robertis, E. M., Larrain, J., Oelgeschläger, M. and Wessely, O. (2000). The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 1, 171-181.
21. Devlin, R. D., Du, Z., Pereira, R. C., Kimble, R. B., Economides, A. N., Jorgetti, V. and Canalis, E. (2003). Skeletal overexpression of noggin results in osteopenia and reduced bone formation. Endocrinology 144, 1972-1978.
22. Dudley, A. T., Lyons, K. M. and Robertson, E. J. (1995). A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9, 2795-2807.
23. Dunn, N. R., Winnier, G. E., Hargett, L. K., Schrick, J. J., Fogo, A. B. and Hogan, B. L. (1997). Haploinsufficient phenotypes in Bmp4 heterozygous null mice and modification by mutations in Gli3 and Alx4. Dev. Biol. 188, 235-247.
24. Eldar, A., Dorfman, R., Weiss, D., Ashe, H., Shilo, B. Z. and Barkai, N. (2002). Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 419, 304-308.
25. Erlebacher, A., Filvaroff, E. H., Gitelman, S. E. and Derynck, R. (1995). Toward a molecular understanding of skeletal development. Cell 80, 371-378.
26. Ferguson, E. L. and Anderson, K. V. (1992). Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
27. Fujiwara, T., Dehart, D. B., Sulik, K. K. and Hogan, B. L. (2002). Distinct requirements for extra-embryonic and embryonic bone morphogenetic protein 4 in the formation of the node and primitive streak and coordination of left-right asymmetry in the mouse. Development 129, 4685-4696.
28. Furuta,,Y. and Hogan, B. L. (1998). BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12, 3764-3775.
29. Furuta, Y., Piston, D. W. and Hogan, B. L. (1997). Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203-2212.
30. Garel, S., Huffman, K. J. and Rubenstein, J. L. (2003). Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants. Development 130, 1903-1914.
31. Golden, J. A., Bracilovic, A., Mc Fadden, K. A., Beesly, J. S., Rubenstein, J. L. and Grinspan, J. B. (1999). Ectopic bone morphogenetic proteins 5 and 4 in the chicken forebrain lead to cyclopia and holoprosencephaly. Proc. Natl. Acad. Sci. USA 96, 2439-2444.
32. Graf, D., Timmons, P. M., Hitchins, M., Episkopou, V., Moore, G., Ito, T., Fujiyama, A., Fisher, A. G. and Merkenschlager, M. (2001). Evolutionary conservation, developmental expression, and genomic mapping of mammalian Twisted gastrulation. Mamm. Genome 12, 554-560.
33. Graf, D., Nethisinghe, S., Palmer, D. B., Fisher, A. G. and Merkenschlager, M. (2002). The developmentally regulated expression of Twisted gastrulation reveals a role for bone morphogenetic proteins in the control of T cell development. J. Exp. Med. 196, 163-171.
34. Grüneberg, H. (1963). The Pathology of Development: A Study of Inherited Skeletal Disorders in Animals. Oxford: Blackwell Scientific.
35. Hebert, J. M., Mishina, Y. and McConnell, S. K. (2002). BMP signaling is required locally to pattern the dorsal telencephalic midline. Neuron 35, 1029-1041.
36. Hebert, J. M., Hayhurst, M., Marks, M. E., Kulessa, H., Hogan, B. L. and McConnell, S. K. (2003). BMP ligands act redundantly to pattern the dorsal telencephalic midline. Genesis 35, 214-219.
37. Henrique, D., Adam, J., Myat, A., Chitnis, A., Lewis, J. and Ish-Horowicz, D. (1995). Expression of a Delta homologue in prospective neurons in the chick. Nature 375, 787-790.
38. Hogan, B. L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
39. Ishibashi, M. and McMahon, A. P. (2002). A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo. Development 129, 4807-4819.
40. Jegalian, B. G. and de Robertis, E. M. (1992). Homeotic transformations in the mouse induced by overexpression of a Hox3.3 transgene. Cell 71, 901-910.
41. Jena, N., Martin-Seisdedos, C., McCue, P. and Croce, C. M. (1997). BMP7 null mutation in mice: developmental defects in skeleton, kidney, and eye. Exp. Cell Res. 230, 28-37.
42. Karsenty, G. (2000). Bone morphogenetic proteins and skeletal and nonskeletal development. In Skeletal Growth Factors (ed. E. Canalis), pp. 291-298. Philadelphia: Lippincott Williams and Wilkins.
43. Kingsley, D. M. (1994). The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8, 995-1008.
44. Kulessa, H. and Hogan, B. L. (2002). Generation of a loxP flanked bmp4loxP-lacZ allele marked by conditional lacZ expression. Genesis 32, 66-68.
45. Larrain, J., Bachiller, D., Lu, B., Agius, E., Piccolo, S. and de Robertis, E. M. (2000). BMP-binding modules in chordin: a model for signalling regulation in the extracellular space. Development 127, 821-830.
46. Larrain, J., Oelgeschläger, M., Ketpura, N. I., Reversade, B., Zakin, L. and de Robertis, E. M. (2001). Proteolytic cleavage of Chordin as a switch for the dual activities of Twisted gastrulation in BMP signaling. Development 128, 4439-4447.
47. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P. and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436.
48. Le Mouellic, H., Lallemand, Y. and Brulet, P. (1990). Targeted replacement of the homeobox gene Hox-3.1 by the Escherichia coli lacZ in mouse chimeric embryos. Proc. Natl. Acad. Sci. USA 87, 4712-4716.
49. Marques, G., Musacchio, M., Shimell, M. J., Wunnenberg-Stapleton, K., Cho, K. W. and O'Connor, M. B. (1997). Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91, 417-426.
50. Mason, E. D., Konrad, K. D., Webb, C. D. and Marsh, J. L. (1994). Dorsal midline fate in Drosophila embryos requires twisted gastrulation, a gene encoding a secreted protein related to human connective tissue growth factor. Genes Dev. 8, 1489-1501.
51. Mason, E. D., Williams, S., Grotendorst, G. R. and Marsh, J. L. (1997). Combinatorial signaling by Twisted Gastrulation and Decapentaplegic. Mech. Dev. 64, 61-75.
52. Massague, J. and Chen, Y. G. (2000). Controlling TGF-beta signaling. Genes Dev. 14, 627-644.
53. McMahon, J. A., Takada, S., Zimmerman, L. B., Fan, C. M., Harland, R. M. and McMahon, A. P. (1998). Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438-1452.
54. Meyers, E. N., Lewandoski, M. and Martin, G. R. (1998). An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat. Genet. 18, 136-141.
55. Ming, J. E. and Muenke, M. (2002). Multiple hits during early embryonic development: digenic diseases and holoprosencephaly. Am. J. Hum. Genet. 71, 1017-1032.
56. Miyama, K., Yamada, G., Yamamoto, T. S., Takagi, C., Miyado, K., Sakai, M., Ueno, N. and Sibuya, H. (1999). A BMP-inducible gene, dlx5, regulates osteoblast differentiation and mesoderm induction. Dev. Biol. 208, 123-133.
57. Muenke, M. and Beachy, P. A. (2000). Genetics of ventral forebrain development and holoprosencephaly. Curr. Opin. Genet. Dev. 10, 262-269.
58. Nosaka, T., Morita, S., Kitamura, H., Nakajima, H., Shibata, F., Morikawa, Y., Kataoka, Y., Ebihara, Y., Kawashima, T., Itoh, T. et al. (2003). Mammalian twisted gastrulation is essential for skeleto-lymphogenesis. Mol. Cell Biol. 23, 2969-2980.
59. Oelgeschläger, M., Larrain, J., Geissert, D. and de Robertis, E. M. (2000). The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling. Nature 405, 757-763.
60. Oelgeschläger, M., Reversade, B., Larrain, J., Little, S., Mullins, M. C. and de Robertis, E. M. (2003a) The pro-BMP activity of Twisted gastrulation is independent of BMP binding. Development 130, 4047-4056.
61. Oelgeschläger, M., Kuroda, H., Reversade, B. and de Robertis, E. M. (2003b) Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. Dev. Cell 4, 219-230.
62. Ohkubo, Y., Chiang, C. and Rubenstein, J. L. (2002). Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111, 1-17.
63. Oliver, G., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gross, P. (1995). Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121, 4045-4055.
64. Piccolo, S., Agius, E., Lu, B., Goodman, S., Dale, L. and de Robertis, E. M. (1997). Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91, 407-416.
65. Ross, J. J., Shimmi, O., Vilmos, P., Petryk, A., Kim, H., Gaudenz, K., Hermanson, S., Ekker, S. C., O'Connor, M. B. and Marsh, J. L. (2001). Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410, 479-483.
66. Rubenstein, J. L., Shimamura, K., Martinez, S. and Puelles, L. (1998). Regionalization of the prosencephalic neural plate. Annu. Rev. Neurosci. 21, 445-477.
67. Scott, I. C., Blitz, I. L., Pappano, W. N., Imamura, Y., Clark, T. G., Steiglitz, B. M., Thomas, C. L., Maas, S. A., Takahara, K., Cho, K. W. et al. (1999). Mammalian BMP-1/Tolloid-related metalloproteinases, including novel family member mammalian Tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis. Dev. Biol. 213, 283-300.
68. Scott, I. C., Blitz, I. L., Pappano, W. N., Maas, S. A., Cho, K. W. and Greenspan, D. S. (2001). Homologues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling. Nature 410, 475-478.
69. Shimmi, O. and O'Connor, M. B. (2003). Physical properties of Tld, Sog, Tsg and Dpp protein interactions are predicted to help create a sharp boundary in BMP signal during dorsal-ventral patterning of the Drosophila embryo. Development 130, 4673-4682.
70. Storm, E. E., Rubenstein, J. L. and Martin, G. R. (2003). Dosage of Fgf8 determines whether cell survival is positively regulated in the developing forebrain. Proc. Natl. Acad. Sci. USA 100, 1757-1762.
71. Stottmann, R. W., Anderson, R. M. and Klingensmith, J. (2001). The BMP antagonists Chordin and Noggin have essential but redundant roles in mouse mandibular outgrowth. Dev. Biol. 240, 457-473.
72. Sun, X., Meyers, E. N., Lewandoski, M. and Martin, G. R. (1999). Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 13, 1834-1846.
73. Theiler, K. (1988). Vertebral malformations. Adv. Anat. Embryol. Cell Biol. 112, 1-99.
74. Thomas, P. Q., Brown, A. and Beddington, R. S. (1998). Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development 125, 85-94.
75. Trumpp, A., Depew, M. J., Rubenstein, J. L., Bishop, J. M. and Martin, G. R. (1999). Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev. 13, 3136-3148.
76. Vilmos, P., Gaudenz, K., Hegedus, Z. and Marsh, J. L. (2001). The Twisted gastrulation family of proteins, together with the IGFBP and CCN families, comprise the TIC superfamily of cysteine rich secreted factors. Mol. Pathol. 54, 317-323.
77. Wieschaus, E., Nusslein-Volhard, C. and Jurgens, G. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Wilhelm Roux's Arch. Dev. Biol. 193, 296-307.
78. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
79. Zhao, M., Harris, S. E., Horn, D., Geng, Z., Nishimura, R., Mundy, G. R. and Chen, D. (2002). Bone morphogenetic protein receptor signaling is necessary for normal murine postnatal bone formation. J. Cell Biol. 157, 1049-1060.