The Tlx-2 homeobox gene is a downstream target of BMP signalling and is required for mouse mesoderm development

Development

Volumn 125, Issue 10, 1998, Pages 1877-1887

  Tang, Shao Jun ^a,b   Hoodless, Pamela A ^a   Lu, Zhan ^a   Breitman, Martin L ^c   McInnes, Roderick R ^a,b   Wrana, Jeffrey L ^a,b   Buchwald, Manuel ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c NONE

Author keywords

Bone morphogenetic protein (BMP); Gastrulation; Homeobox gene; Mesoderm; Mouse

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GROWTH FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GENE DISRUPTION; GENE INDUCTION; HOMEOBOX; LETHAL MUTANT; MESODERM; MOUSE; NONHUMAN; PRIMITIVE STREAK; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION;

ACTIVIN RECEPTORS; ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; EMBRYONIC AND FETAL DEVELOPMENT; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; MESODERM; MICE; MICE, KNOCKOUT; MUTATION; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 0031778749     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (84)

1. Acampora, D., Mazan, S., Lallemand, Y., Avantaggiato, V., Maury, M., Simeone, A. and Brulet, P. (1995). Forebrain and midbrain regions are deleted in Otx2-/-mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121, 3279-3290.
2. Ang, S. L., Jin, O., Rhinn, M., Daigle, N., Stevenson, L. and Rossant, J. (1996). A targeted mouse Otx2 mutation leads to severe detects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243-252.
3. Ang, S. L. and Rossant, J. (1994). HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78, 561-574.
4. Attisano, L. and Wrana, J. L. (1996). Signal transduction by members of the transforming growth factor-β superfamily. Cytokine and Growth Factor Reviews 7, 327-339.
5. Baker, J. C. and Harland, R. (1996). A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev. 10, 1880-1889.
6. Beddington, R. S., Rashbass, P. and Wilson, V. (1992). Brachyury - a gene affecting mouse gastrulation and early organogenesis. Development 1992 Supplement, 157-165.
7. Beddington, R. S. and Smith, J. C. (1993). Control of vertebrate gastrulation: Inducing signals and responding genes. Curr. Opin. Genet. Dev. 3, 655-661.
8. Chen, W, S., Manova, K., Weinstein, D. C., Duncan, S. A., Plump, A. S., Prezioso, V. R., Bachvarova, R. F. and Darnell, J. E. Jr. (1994). Disruption of the HNF-4 gene, expressed in visceral endoderm. leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 8, 2466-2477.
9. Chen, X., Rubock, M. J. and Whitman, M. (1996). A transcriptional partner for MAD proteins in TGF-β signalling. Nature 383, 691-696.
10. Conlon, F. L., Lyons, K. M., Takaesu, N., Barth, K. S., Kispert, A., Herrmann, B. and Robertson, E. J. (1994). A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120, 1919-1928.
11. Conlon, R. A., Reaume, A. G. and Rossant, J. (1995). Notch1 is required for the coordinate segmentation of somites. Development 121, 1533-1545.
12. Davidson, D. (1995). The function and evolution of Msx genes: pointers and paradoxes. Trends Genet. 11, 405-411.
13. de Oca Luna, M. R., Wagner, D. S. and Lozano, G. (1995). Rescue of early embryonic lethality in mdm2-dericient mice by deletion of p53. Nature 378, 203-206.
14. Dear, T. N., Colledge, W. H., Carlton, M. B., Lavenir, I., Larson, T., Smith, A. J., Warren, A. J., Evans, M. J., Sofroniew, M. V. and Rabbitts, T. H. (1995). The Hox11 gene is essential for cell survival during spleen development. Development 121, 2909-2915.
15. Dear, T. N., Sanchez-Garcia, I. and Rabbitts, T. H. (1993). The HOX11 gene encodes a DNA-binding nuclear transription factor belonging to a distinct family of homeobox gene. Proc. Natl. Acad. Sci. USA 90, 4431-4435.
16. Deng, C. X., Wynshaw-Boris, A., Shen, M. M., Daugherty, C., Ornitz, D. M. and Leder, P. (1994). Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 8, 3045-3057.
17. Dubé, I.D., Kamel-Reid, S., Yuan, C. C., Lu, M., Wu, X., Corpus, G., Raimondi, S. C., Crist, W. M., Carroll, A. J. Minowada, J. et al., (1991). A novel human homeobox gene lies at me chromosome 10 breakpoint in lymphoid neoplasias with chromosomal translocation t (10;14). Blood 78, 2996-3003.
18. Dush, M. K. and Martin, G. R. (1992). Analysis of mouse Evx genes: Evx-1 displays graded ecpression in the primitive streak. Dev. Biol. 151, 273-287.
19. Farmer, S. C., Sun, C. W., Winnier, G. E., Hogan, B. L. and Townes, T. M. (1997). The bZIP transcription factor LCR-F1 is essential for mesoderm formation in mouse development. Genes Dev. 11, 786-798.
20. Fassler, R. and Meyer, M. (1995). Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev. 9, 1896-1908.
21. Faust, C., Schumacher, A., Holdener, B. and Magnuson, T. (1995). The eed mutation disrupts anterior mesoderm production in mice. Development 121, 273-285.
22. Feldman, B., Poueymirou, W., Papaioannou, V. E., DeChiara, T. M. and Goldfarb, M. (1995). Requirement of FGF-4 for postimplantation mouse development. Science 267, 246-249.
23. Furuta, Y., Ilic, D., Kanazawa, S., Takeda, N., Yamamoto, T. and Aizawa, S. (1995). Mesodermal detect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene 11, 1989-1995.
24. Gañan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M. A. and Hurle, J. M. (1996). Role of TGFβs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122, 2349-2357.
25. George, E. L., Georges-Labouesse, E. N., Patel-King, R. S., Rayburn, H. and Hynes, R. O. (1993). Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079-1091.
26. Graff, J. M., Bansal, A. and Melton, D. A. (1996). Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell 85, 479-487.
27. Green, J. B. A. and Smith, J. C. (1990). Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391-394.
28. Haegel, H. Larue, L. Ohsugi, M. Fedorov, L. Herrenknecht, K. Kemler, R. (1995). Lack of beta-catenin affects mouse development at gastrulation. Development 121, 3529-3537.
29. Hatano, M., Aoki, T., Dezawa, M., Yusa, S., Iitsuka, Y., Koseki, H. and Taniguchi, M. (1997). A novel pathogenesis of megacolon in Ncx/Hox1 1L.1 deficient mice. J. Clin. Invest. 100, 705-801.
30. Hatano, M., Roberts, C. W., Minden, M., Crist, W. M. and Korsmeyer, S. J. (1991). Deregulation of a homeobox gene HOX11 by the t (10;14) in T cell leukemia. Science 253, 79-82.
31. Hemmati-Brivanlou, A. and Thomsen, G. H. (1995). Ventral mesodermal patterning in Xenopus embryos: Expression patterns and activities of BMP-2 and BMP-4. Dev. Genetics 17, 78-89.
32. Herrmann, B. G. (1992). Action of the Brachyury gene in mouse embryogenesis. Ciba Found. Symp. 165, 78-86.
33. Herrmann, B. G. and Kispert, A. (1994). The T genes in embryogenesis. Trends Genet. 10, 280-286.
34. nd edition. Cold Spring Harbor. New York: Cold Spring Harbor Laboratory Press.
35. Hogan, B. L. M. (1996). Bone morphogenic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
36. Holley, S.A. Neul, J. L., Attisano, L., Wrana, J. L., Sasai, Y., O'Connor, M. B., De Robertis, E. M. and Ferguson, E. L. (1996). The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86, 607-617.
37. Hoodless, P. A. and Hemmati-Brivanlou, A. (1997). Inhibitory control of neural differentiation in mammalian cells. Development, Genes and Evolution 207, 19-28.
38. Hoodless, P. A. and Wrana, J. L. (1997). The mechanism and function of signalling by the TGFβ superfamily. In Current Topics in Microbiology and Immunology, vol. 228 (ed. A. J. Pawson), pp. 235-272. New York: Springer-Verlag.
39. Hoodless, P. A, Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M. B., Attisano, L. and Wrana, J. L. (1996). MAOR1, a MAD-related protein that functions in BMP2 signalling pathways. Cell 85, 489-500.
40. Huang, H.-C., Murtaugh, L. C., Vize, P. D. and Whitman, M. (1995). Identification of a potential regulator of early transcriptional responses to mesoderm inducer in the frog embryo. EMBO J. 14, 5965-5973.
41. Illic, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., Yamamoto, T. et al. (1995). Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544.
42. Jones, S. N., Roe, A. E., Donehower, L. A. and Bradley, A. (1995). Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 378, 206-208.
43. Joyner, A. L. (1993). Gene Targeting: a Practical Approach. Oxford: IRL Press.
44. Kennedy, M.A, Gonzalez-Sarmiento, R., Kees, U. R., Lampert, F., Dear, N., Boehm, T. and Rabbitts, T. H. (1991). H0X11, a homeobox-containing T-cell oncogene on human chromosome 10q24. Proc. Natl. Acad. Sci. USA 88, 8900-8904.
45. Kim, J., Johnson, K., Chen, H.J., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by decapentaplegic. Nature 388, 304-308.
46. Kretzchmar, M., Liu, F., Hata, A., Doody, J. and Massagué, J. (1997). The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995.
47. Ladder, R., Mohun, T. J., Smith, J. C. and Snape, A. M. (1996). Xom: a Xenopus homeobox gene that mediates the early effects of BMP-4. Development 122, 2385-2394.
48. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué, J. (1996). Partnership between DPC4 and SMAD proteins in TGF-β signalling pathways. Nature 383, 832-836.
49. Le Mouellic, H., Lallemand, Y. and Brûlet, P. (1992). Homeosis in the mouse induced by a null mutation in the Hox-3.1 gene. Cell 69, 251-264.
50. Lecuit, T. and Cohen, S. M. (1997). Proximal-distal axis formation in the Drosophila leg, Nature 388, 139-145.
51. Liu, F., Hata, A., Baker, J. C., Doody, J., Carcamo, J., Harland, R. M. and Massague J. (1996). A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381, 620-623.
52. Lu, M., Gong, Z. Y., Shen, W. F. and Ho, A. C. (1991). The tcl-3 protooncogene altered by chromosomal translocation in T-cell leukemia codes for a homeobox protein. EMBO J. 10, 2905-2910.
53. Maas, R. (1997). The genetic control of early tooth development. Crit. Rev. Oral Biol. Med. 8, 4-39.
54. Macías-Silva, M., Abdollah, S., Hoodless, P. A., Pirone, R., Attisano, L. and Wrana, J. L. (1996). MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signalling. Cell 87, 1215-1224.
55. Matsuo, I., Kuratani, S., Kimura, C., Takeda, N. and Aizawa, S. (1995). Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9, 2646-2658.
56. Mead, P. E., Brivanlou, I. H., Kelley, C. M. and Zon, L. I. (1996). BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix.1. Nature 382, 357-360.
57. Mishina, Y., Suzuki, A., Ueno, N. and Behringer, R. R. (1995), Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 9, 3027-3037.
58. Onichtchouk, D., Gawantka, V., Dosch, R., Delius, H., Hirschfeld, K., Blumenstock, C. and Niehrs, C. (1996). The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling dorsalventral patterning of Xenopus mesoderm. Development 122, 2385-2394.
59. Piccolo, S., Sasai, Y., Lu, B. and De Robertis, E. M. (1996). Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of Chordin to BMP-4. Cell 86, 589-598.
60. Raju, K., Tang, S., Dube, I. D., Kamel-Reid, S., Bryce, D. M. and Breitman, M. L. (1993). Characterization and developmental expression of Tlx-1, the murine homolog of HOX11. Mech. Dev. 44, 51-64.
61. Roberts, C. W., Shutter, J. R. and Korsmeyer, S. J. (1994). Hox11 controls the genesis of the spleen. Nature 368, 747-749.
62. Satokata, T. and Maas, R. (1994). Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nature Genetics 6, 348-355.
63. Schubert, F. R., Fainsod, A., Gruebaum, Y. and Gruss, P. (1995). Expression of the novel murine homeobox gene Sax-1 in the developing nervous system. Mech. Dev. 51, 99-114.
64. Schumacher, A., Faust, C. and Magnuson T. (1996). Positional cloning of a global regulator of anterior-posterior patterning in mice. Nature 383, 250-253.
65. Shawlot, W. and Behringer, R. R. (1995). Requirement for Lim1 in head-organizer function Nature 374, 425-430.
66. Shirasawa, S., Yunker, A. M. R., Roth, K. A., Brown, G. A., Horning, S. and Korsmeyer, S. J. (1997). Enx (Hox11L1)-deficient mice develop myenteric neuronal hyperplasia and megacolon. Nature Medicine 3, 646-650.
67. Smith, J. C. (1995). Mesoderm-inducing factors and mesodermal patterning. Curt: Opin. Cell Biol. 7, 856-861.
68. St-Jacques, B. and McMahon, A. P. (1996). Early mouse development: lessons from gene targeting. Curr. Opin. Genet. Dev. 6, 439-444.
69. Stephens, L. E., Sutherland, A. E., Klimanskaya, I. V., Andrieux, A. and Meneses, J. (1995). Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9, 1883-1895.
70. Swiatek, P. J., Lindsell, C. E., del Amo, F. F., Weinmaster, G. and Gridley, T. (1994). Notch1 is essential for postimplantation development in mice. Genes Dev. 8, 707-719.
71. Tam, P. P., Williams, E. A. and Chan, W. Y. (1993). Gastrulation in the mouse embryo: ultrastructural and molecular aspects of germ layer morphogenesis. Microscopy Research and Technique 26, 301-328.
72. ten Dijke, P., Yamashita, H., Sampath, T. K., Reddi, A. H., Estevez, M., Riddle, D. L., Ichijo, H., Heldin, C. H. and Miyazono, K. (1994). Identification of type I receptors for Osteogenic Protein-1 and Bone Morphogenetic Protein-4. J. Biol. Chem. 269, 16985-16988.
73. Thomsen, G. H. (1996). Xenopus mothers against decapentaplegic is an embryonic ventralizing agent that acts downstream of the BMP2/4 receptor. Development 122, 2359-2366.
74. Varlet, I., Collignon, J. and Robertson, E. J. (1997). Nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124, 1033-1044.
75. Vidricaire, G., Jardine, K. and McBurney, M. W. (1994). Expression of the Brachyury gene during mesoderm development in differentiating embryonal carcinoma cell cultures. Development 120, 115-122.
76. Weinstein, D. C., Ruiz i Altaba, A., Chen, W. S., Hoodless, P., Prezioso, V. R., Jessell, T. M. and Darnell, J. E., Jr. (1994). The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78, 575-588.
77. Wilkinson, D. G. (1992). Whole mount in situ hybridization of vertebrate embryos. In In Situ Hybridization: a Practical Approach (ed. D. G. Wilkinson). Oxford: IRL Press.
78. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
79. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. M. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
80. Wrana, J. L. and Attisano, L. (1996). MAD-related proteins in TGFβ signalling. Trends Genet. 12, 493-496.
81. Yamaguchi, T. P., Harpal, K., Henkemeyer, M. and Rossant J. (1994), fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 8, 3032-3044.
82. Zhang, Y., Musci, T. and Derynck, R. (1997). The tumor suppressor Smad4/DPC4 as a central mediator of Smad function. Curr. Biol. 7, 270-276.
83. Zhou, X., Sasaki, H., Lowe, L., Hogan, B. L. M. and Kuehn, M. R. (1993). Nodal is a novel TGF-β-like gene expressed in the mouse node during gastrulation. Nature 361, 543-547.
84. Zimmerman, L. B., De Jesús-Escobar, J. M. and Harland, R. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606.