DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction

C.M. Jones; K.M. Lyons; P.M. Lapan; C.V. Wright; B.L. Hogan

Summary

Establishment of mesodermal tissues in the amphibian body involves a series of inductive interactions probably elicited by a variety of peptide growth factors. Results reported here suggest that mesodermal patterning involves an array of signalling molecules including DVR-4, a TGF-beta-like molecule. We show that ectopic expression of DVR-4 causes embryos to develop with an overall posterior and/or ventral character, and that DVR-4 induces ventral types of mesoderm in animal cap explants. Moreover, DVR-4 overrides the dorsalizing effects of activin. DVR-4 is therefore the first molecule reported both to induce posteroventral mesoderm and to counteract dorsalizing signals such as activin. Possible interactions between these molecules resulting in establishment of the embryonic body plan are discussed.

REFERENCES

1. Artisano L.,
2. Wrana J. L.,
3. Cheifetz S.,
4. Massague J.
(1992) Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68, 97–108
1. Asashima M.,
2. Grunz H.
(1983) Effects of inducers on inner and outer gastrula ectoderm layers of Xenopus laevis. Differentiation 23, 206–212
1. Cho K. W. Y.,
2. De Robertis E. M.
(1990) Differential activation of Xenopus homeobox genes by mesoderm-inducing growth factors and retinoic acid. Genes Dev 4, 1910–1916
1. Cho K. W. Y.,
2. Goetz J.,
3. Wright C. V. E.,
4. Fritz A.,
5. Hardwicke J.,
6. De Robertis E. M.
(1988) Differential utilization of the same reading frame in a Xenopus homeobox gene encodes two related proteins sharing the same DNA-binding specificity. EMBO J 7, 2139–2149
1. Cho K. W. Y.,
2. Morita E. A.,
3. Wright C. V. E.,
4. De Robertis E. M.
(1991) Overexpression of a homeodomain protein confers axis-forming activity to uncommitted Xenopus embryonic cells. Cell 65, 55–64
1. Christian J. L.,
2. McMahon J. A.,
3. McMahon A. P.,
4. Moon R.T.
(1991) Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to meso-derm-inducing growth factors, may play a role in ventral mesodermal patterning during embryogenesis. Development 111, 1045–1055
1. Cooke J.
(1989) Mesoderm-inducing factors and Spemann's organiser phenomenon in amphibian development. Development 107, 229–241
1. Dale L.,
2. Slack J. M. W.
(1987) Fate map of the 32-cell stage of Xenopus laevis. Development 99, 527–551
1. Dale L.,
2. Slack J. M. W.
(1987) Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100, 279–295
1. Green J. B. A.,
2. Smith J. C.
(1990) Graded changes in dose of a Xeno-pus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391–394
1. Gurdon J. B.
(1976) Injected nuclei in frog oocytes: fate, enlargement, and chromatin dispersal. J. Embryol. Exp. Morphol 36, 523–540
1. Jones C. M.,
2. Lyons K. M.,
3. Hogan B. L. M.
(1991) Involvement of Bone Morphogenetic Protein 4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531–542
1. Koster M.,
2. Plessow S.,
3. Clement J. H.,
4. Lorenz A.,
5. Tiedemann H.,
6. Knochel W.
(1991) Bone morphogenetic protein 4 (BMP-4), a member of the TGF-family, in early embryos of Xenopus laevis: analysis of mesoderm inducing activity. Mech. Dev 33, 191–200
1. Krieg P. A.,
2. Melton D. A.
(1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucl. Acids Res 12, 7057–7070
1. Krieg P. A.,
2. Melton D. A.
(1987) In vitro RNA synthesis with SP6 RNA polymerase. Meth. Enzymol 155, 397–415
1. Lyons K. M.,
2. Jones C. M.,
3. Hogan B. L. M.
(1991) The DVR gene family in embryonic development. Trends Genet 7, 408–412
1. Lyons K. M.,
2. Pelton R. W.,
3. Hogan B. L. M.
(1990) Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for Bone Morphogenetic Protein-2A (BMP-2A). Development 109, 833–844
1. Ruiz i Altaba A.,
2. Melton D. A.
(1989) Bimodal and graded expres-sion of the Xenopus homeobox gene Xhox 3 during embryonic develop-ment. Development 106, 173–183
1. Ruiz i Altaba A.,
2. Melton D. A.
(1989) Involvement of the Xenopus homeobox gene Xhox 3 in pattern formation along the anterior-posterior axis. Cell 57, 317–326
1. Ruiz i Altaba A.,
2. Melton D. A.
(1989) Interaction between peptide growth factors and homeobox genes in the establishment of antero-poste-rior polarity in embryos. Nature 341, 33–38
1. Slack J. M. W.,
2. Darlington B. G.,
3. Heath J. K.,
4. Godsave S. F.
(1987) Mesoderm induction in early Xenopus embryos by heparin-bind-ing growth factors. Nature 326, 197–200
1. Smith J. C.
(1989) Induction and early amphibian development. Current Opinion in Cell Biology 1, 1061–1070
1. Smith J. C.,
2. Price B. M. J.,
3. Green J. B. A.,
4. Weigel D.,
5. Herrmann B. G.
(1991) Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87
1. Smith W. C.,
2. Harland R. M.
(1991) Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67, 753–765
1. Sokol S.,
2. Christian J.,
3. Moon R. T.,
4. Melton D. A.
(1991) Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67, 741–752
1. St Johnston D.,
2. Nusslein-Volhard C.
(1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219
1. Wright C. V. E.,
2. Cho K. W. Y.,
3. Hardwicke J.,
4. Collins R. H.,
5. De Robertis E. M.
(1989) Interference with function of a homeobox gene in Xenopus Embryos produces malformations of the anterior spinal cord. Cell 59, 81–93

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[1] Artisano L.,
Wrana J. L.,
Cheifetz S.,
Massague J.
(1992) Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68, 97–108

[2] Artisano L.,

[3] Wrana J. L.,

[4] Cheifetz S.,

[5] Massague J.

[6] Asashima M.,
Grunz H.
(1983) Effects of inducers on inner and outer gastrula ectoderm layers of Xenopus laevis. Differentiation 23, 206–212

[7] Asashima M.,

[8] Grunz H.

[9] Cho K. W. Y.,
De Robertis E. M.
(1990) Differential activation of Xenopus homeobox genes by mesoderm-inducing growth factors and retinoic acid. Genes Dev 4, 1910–1916

[10] Cho K. W. Y.,

[11] De Robertis E. M.

[12] Cho K. W. Y.,
Goetz J.,
Wright C. V. E.,
Fritz A.,
Hardwicke J.,
De Robertis E. M.
(1988) Differential utilization of the same reading frame in a Xenopus homeobox gene encodes two related proteins sharing the same DNA-binding specificity. EMBO J 7, 2139–2149

[13] Cho K. W. Y.,

[14] Goetz J.,

[15] Wright C. V. E.,

[16] Fritz A.,

[17] Hardwicke J.,

[18] De Robertis E. M.

[19] Cho K. W. Y.,
Morita E. A.,
Wright C. V. E.,
De Robertis E. M.
(1991) Overexpression of a homeodomain protein confers axis-forming activity to uncommitted Xenopus embryonic cells. Cell 65, 55–64

[20] Cho K. W. Y.,

[21] Morita E. A.,

[22] Wright C. V. E.,

[23] De Robertis E. M.

[24] Christian J. L.,
McMahon J. A.,
McMahon A. P.,
Moon R.T.
(1991) Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to meso-derm-inducing growth factors, may play a role in ventral mesodermal patterning during embryogenesis. Development 111, 1045–1055

[25] Christian J. L.,

[26] McMahon J. A.,

[27] McMahon A. P.,

[28] Moon R.T.

[29] Cooke J.
(1989) Mesoderm-inducing factors and Spemann's organiser phenomenon in amphibian development. Development 107, 229–241

[30] Cooke J.

[31] Dale L.,
Slack J. M. W.
(1987) Fate map of the 32-cell stage of Xenopus laevis. Development 99, 527–551

[32] Dale L.,

[33] Slack J. M. W.

[34] Dale L.,
Slack J. M. W.
(1987) Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100, 279–295

[35] Dale L.,

[36] Slack J. M. W.

[37] Green J. B. A.,
Smith J. C.
(1990) Graded changes in dose of a Xeno-pus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347, 391–394

[38] Green J. B. A.,

[39] Smith J. C.

[40] Gurdon J. B.
(1976) Injected nuclei in frog oocytes: fate, enlargement, and chromatin dispersal. J. Embryol. Exp. Morphol 36, 523–540

[41] Gurdon J. B.

[42] Jones C. M.,
Lyons K. M.,
Hogan B. L. M.
(1991) Involvement of Bone Morphogenetic Protein 4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531–542

[43] Jones C. M.,

[44] Lyons K. M.,

[45] Hogan B. L. M.

[46] Koster M.,
Plessow S.,
Clement J. H.,
Lorenz A.,
Tiedemann H.,
Knochel W.
(1991) Bone morphogenetic protein 4 (BMP-4), a member of the TGF-family, in early embryos of Xenopus laevis: analysis of mesoderm inducing activity. Mech. Dev 33, 191–200

[47] Koster M.,

[48] Plessow S.,

[49] Clement J. H.,

[50] Lorenz A.,

[51] Tiedemann H.,

[52] Knochel W.

[53] Krieg P. A.,
Melton D. A.
(1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucl. Acids Res 12, 7057–7070

[54] Krieg P. A.,

[55] Melton D. A.

[56] Krieg P. A.,
Melton D. A.
(1987) In vitro RNA synthesis with SP6 RNA polymerase. Meth. Enzymol 155, 397–415

[57] Krieg P. A.,

[58] Melton D. A.

[59] Lyons K. M.,
Jones C. M.,
Hogan B. L. M.
(1991) The DVR gene family in embryonic development. Trends Genet 7, 408–412

[60] Lyons K. M.,

[61] Jones C. M.,

[62] Hogan B. L. M.

[63] Lyons K. M.,
Pelton R. W.,
Hogan B. L. M.
(1990) Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for Bone Morphogenetic Protein-2A (BMP-2A). Development 109, 833–844

[64] Lyons K. M.,

[65] Pelton R. W.,

[66] Hogan B. L. M.

[67] Ruiz i Altaba A.,
Melton D. A.
(1989) Bimodal and graded expres-sion of the Xenopus homeobox gene Xhox 3 during embryonic develop-ment. Development 106, 173–183

[68] Ruiz i Altaba A.,

[69] Melton D. A.

[70] Ruiz i Altaba A.,
Melton D. A.
(1989) Involvement of the Xenopus homeobox gene Xhox 3 in pattern formation along the anterior-posterior axis. Cell 57, 317–326

[71] Ruiz i Altaba A.,

[72] Melton D. A.

[73] Ruiz i Altaba A.,
Melton D. A.
(1989) Interaction between peptide growth factors and homeobox genes in the establishment of antero-poste-rior polarity in embryos. Nature 341, 33–38

[74] Ruiz i Altaba A.,

[75] Melton D. A.

[76] Slack J. M. W.,
Darlington B. G.,
Heath J. K.,
Godsave S. F.
(1987) Mesoderm induction in early Xenopus embryos by heparin-bind-ing growth factors. Nature 326, 197–200

[77] Slack J. M. W.,

[78] Darlington B. G.,

[79] Heath J. K.,

[80] Godsave S. F.

[81] Smith J. C.
(1989) Induction and early amphibian development. Current Opinion in Cell Biology 1, 1061–1070

[82] Smith J. C.

[83] Smith J. C.,
Price B. M. J.,
Green J. B. A.,
Weigel D.,
Herrmann B. G.
(1991) Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79–87

[84] Smith J. C.,

[85] Price B. M. J.,

[86] Green J. B. A.,

[87] Weigel D.,

[88] Herrmann B. G.

[89] Smith W. C.,
Harland R. M.
(1991) Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67, 753–765

[90] Smith W. C.,

[91] Harland R. M.

[92] Sokol S.,
Christian J.,
Moon R. T.,
Melton D. A.
(1991) Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 67, 741–752

[93] Sokol S.,

[94] Christian J.,

[95] Moon R. T.,

[96] Melton D. A.

[97] St Johnston D.,
Nusslein-Volhard C.
(1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219

[98] St Johnston D.,

[99] Nusslein-Volhard C.

[100] Wright C. V. E.,
Cho K. W. Y.,
Hardwicke J.,
Collins R. H.,
De Robertis E. M.
(1989) Interference with function of a homeobox gene in Xenopus Embryos produces malformations of the anterior spinal cord. Cell 59, 81–93

[101] Wright C. V. E.,

[102] Cho K. W. Y.,

[103] Hardwicke J.,

[104] Collins R. H.,

[105] De Robertis E. M.

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Other journals from The Company of Biologists

An interview with Swathi Arur

Jim Wells and Hanna Mikkola join our team of Editors

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Upcoming special issues

Development presents...

Main menu

User menu

Search

Summary

REFERENCES

Citation Manager Formats

Article navigation

Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

An interview with Swathi Arur

Jim Wells and Hanna Mikkola join our team of Editors

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Upcoming special issues

Development presents...