Ectoderm induces muscle-specific gene expression in Drosophila embryos

R. Baker; G. Schubiger

Summary

We have inhibited normal cell-cell interactions between mesoderm and ectoderm in wild-type Drosophila embryos, and have assayed the consequences on muscle development. Although most cells in gastrulation-arrested embryos do not differentiate, they express latent germ layer-specific genes appropriate for their position. Mesoderm cells require proximity to ectoderm to express several muscle-specific genes. We show that ventral ectoderm induces mesoderm cells to express nautilus (a MyoD homologue) and to differentiate somatic myofibers, whereas dorsal ectoderm induces mesoderm cells to express visceral and cardiac muscle-specific genes. Our findings suggest that muscle determination in Drosophila is regulated by induction between germ layers during gastrulation.

Reference

1. Azpiazu N.,
2. Frasch M.
(1993) tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev 7, 1325–1340
OpenUrl Abstract/FREE Full Text
1. Baker J.,
2. Theurkauf W. E.,
3. Schubiger G.
(1993) Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo. J. Cell Biol 122, 113–121
OpenUrl Abstract/FREE Full Text
1. Barad M.,
2. Jack T.,
3. Chadwick R.,
4. McGinnis W.
(1988) A novel, tissue-specific, Drosophila homeobox gene. EMBO J 7, 2151–2161
OpenUrl PubMed
1. Bate M.
(1990) The embryonic development of larval muscles in Drosophila. Development 110, 791–804
OpenUrl Abstract/FREE Full Text
1. Bate M.,
2. Rushton E.,
3. Currie D.
(1991) Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113, 79–89
OpenUrl Abstract
1. Bellen H. J.,
2. O'Kane C. J.,
3. Wilson C.,
4. Grossniklaus U.,
5. Kurth-Pearson R.,
6. Gehring W. J.
(1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3, 1288–1300
OpenUrl Abstract/FREE Full Text
1. Bodmer R.
(1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118, 719–729
OpenUrl Abstract
1. Broadie K.,
2. Bate M.
(1993) Muscle development is independent of innervation during Drosophila embryogenesis. Development 119, 533–543
OpenUrl Abstract
1. Corbin V.,
2. Michelson A. M.,
3. Abmayr S. M.,
4. Neel V.,
5. Alcomo E.,
6. Maniatis T.,
7. Young M. W.
(1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67, 311–323
OpenUrl CrossRef PubMed Web of Science
1. Erdelyi M.,
2. Szabad J.
(1989) Isolation and characterization of dominant female sterile mutations of Drosophilamelanogaster. I. Mutations on the third chromosome. Genetics 122, 111–127
OpenUrl Abstract/FREE Full Text
1. Fehon R. G.,
2. Dawson I. A.,
3. Artavanis-Tsakonas S.
(1994). A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120, 545–557
OpenUrl Abstract
1. Green J. B.,
2. Howes G.,
3. Symes K.,
4. Cooke J.,
5. Smith J. C.
(1990) The biological effects of XTC-MIF: quantitative comparison with Xenopus bFGF. Development 108, 173–183
OpenUrl Abstract
1. Hartenstein A. Y.,
2. Rugendorgg A.,
3. Tepass U.,
4. Hartenstein V.
(1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116, 1203–1220
OpenUrl Abstract/FREE Full Text
1. Jan L. Y.,
2. Jan Y. N.
(1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc. Natl. Acad. Sci. USA 72, 2700–2704
1. Kimelman D.,
2. Abraham J. A.,
3. Haaparanta T.,
4. Palisi T. M.,
5. Kirschner M. W.
(1988) The presence of fibroblast growth factor in the frog egg: its role as a natural mesoderm inducer. Science 242, 1053–1056
OpenUrl Abstract/FREE Full Text
1. Kosman D.,
2. Ip Y. T.,
3. Levine M.,
4. Arora K.
(1991) Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo. Science 254, 3118–3122
OpenUrl
1. Lawrence P. A.,
2. Johnston P.
(1986) The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 45, 505–513
OpenUrl CrossRef PubMed Web of Science
1. Leiss D.,
2. Hinz U.,
3. Gasch A.,
4. Mertz R.,
5. Renkawitz-Pohl R.
(1988) 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 104, 525–531
OpenUrl Abstract/FREE Full Text
1. Leptin M.,
2. Grunewald B.
(1990) Cell shape changes during gastrulation in Drosophila. Development 110, 73–84
OpenUrl Abstract
1. Lipton D. H.,
2. Jacobsen A. G.
(1973) Analysis of normal somite development. Dev. Biol 38, 73–90
1. Michelson A. M.,
2. Abmayr S. M.,
3. Bate M.,
4. Martinez-Arias A.,
5. Maniatis T.
(1990) Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Dev 4, 2086–2097
OpenUrl Abstract/FREE Full Text
1. Nicolet G.
(1970) Is the presumptive notochord responsible for somite genesis in the chick?. J. Embryol. Exp. Morphol 24, 231–262
OpenUrl
1. Paterson B. M.,
2. Walldorf U.,
3. Eldredge J.,
4. Dubendorfer A.,
5. Frasch M.,
6. Gehring W. J.
(1990) The Drosophila homologue of vertebrate myogenic-determination genes encodes a transiently expressed nuclear protein marking primary myogenic cells. Proc. Natl. Acad. Sci. USA 88, 3782–3786
OpenUrl Abstract/FREE Full Text
1. Poulson D. F.
(1945) Chromosomal control of embryogenesis in Drosophila. Am. Nat 79, 340–363
OpenUrl
1. Ray R. P.,
2. Arora K.,
3. Nusslein-Volhard C.,
4. Gelbart W. M.
(1991) The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113, 35–54
OpenUrl Abstract
1. Robinow S.,
2. White K.
(1991) Characterization and spatial distribution of the ELAV protein during Drosophilamelanogaster development. J. Neurobiol 22, 443–461
OpenUrl CrossRef PubMed Web of Science
1. Seidel F.,
2. Bock E.,
3. Krause G.
(1940) Die Organisation des Insekteneies. Naturwissenschaften 28, 433–446
OpenUrl CrossRef Web of Science
1. Shishido E.,
2. Higashijima S.,
3. Emori Y.,
4. Saigo K.
(1993) Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117, 751–761
OpenUrl Abstract
1. Staehling-Hampton K.,
2. Hoffmann F. M.,
3. Baylies M. K.,
4. Rushton E.,
5. Bate M.
(1994) dpp induces mesodermal gene expression in Drosophila. Nature 373, 783–786
OpenUrl
1. St. Johnston R. D.,
2. Gelbart W. M.
(1987) Decapentaplegic transcriptsare localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 6, 2785–2791
OpenUrl PubMed Web of Science
1. St. Johnston D.,
2. Nusslein-Volhard C.
(1992) The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219
OpenUrl CrossRef PubMed Web of Science
1. Tepass U.,
2. Hartenstein V.
(1994) Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 120, 579–590
OpenUrl Abstract
1. Thisse B.,
2. Stoetzel C.,
3. Gorostiza T. C.,
4. Perrin Schmitt F.
(1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7, 2175–2183
OpenUrl PubMed Web of Science
1. Volk T.,
2. VijayRaghaven K.
(1994) A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 120, 59–70
OpenUrl Abstract
1. Williams J. A.,
2. Bell J. B.,
3. Carroll S. B.
(1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5, 2481–2495
OpenUrl Abstract/FREE Full Text

This Issue

Download PDF

Citation Tools

Alerts

Cited by...

More in this TOC section

Show more JOURNAL ARTICLES

Other journals from The Company of Biologists

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights

[1] Azpiazu N.,
Frasch M.
(1993) tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev 7, 1325–1340
OpenUrl Abstract/FREE Full Text

[2] Azpiazu N.,

[3] Frasch M.

[4] Baker J.,
Theurkauf W. E.,
Schubiger G.
(1993) Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo. J. Cell Biol 122, 113–121
OpenUrl Abstract/FREE Full Text

[5] Baker J.,

[6] Theurkauf W. E.,

[7] Schubiger G.

[8] Barad M.,
Jack T.,
Chadwick R.,
McGinnis W.
(1988) A novel, tissue-specific, Drosophila homeobox gene. EMBO J 7, 2151–2161
OpenUrl PubMed

[9] Barad M.,

[10] Jack T.,

[11] Chadwick R.,

[12] McGinnis W.

[13] Bate M.
(1990) The embryonic development of larval muscles in Drosophila. Development 110, 791–804
OpenUrl Abstract/FREE Full Text

[14] Bate M.

[15] Bate M.,
Rushton E.,
Currie D.
(1991) Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 113, 79–89
OpenUrl Abstract

[16] Bate M.,

[17] Rushton E.,

[18] Currie D.

[19] Bellen H. J.,
O'Kane C. J.,
Wilson C.,
Grossniklaus U.,
Kurth-Pearson R.,
Gehring W. J.
(1989) P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev 3, 1288–1300
OpenUrl Abstract/FREE Full Text

[20] Bellen H. J.,

[21] O'Kane C. J.,

[22] Wilson C.,

[23] Grossniklaus U.,

[24] Kurth-Pearson R.,

[25] Gehring W. J.

[26] Bodmer R.
(1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118, 719–729
OpenUrl Abstract

[27] Bodmer R.

[28] Broadie K.,
Bate M.
(1993) Muscle development is independent of innervation during Drosophila embryogenesis. Development 119, 533–543
OpenUrl Abstract

[29] Broadie K.,

[30] Bate M.

[31] Corbin V.,
Michelson A. M.,
Abmayr S. M.,
Neel V.,
Alcomo E.,
Maniatis T.,
Young M. W.
(1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67, 311–323
OpenUrl CrossRef PubMed Web of Science

[32] Corbin V.,

[33] Michelson A. M.,

[34] Abmayr S. M.,

[35] Neel V.,

[36] Alcomo E.,

[37] Maniatis T.,

[38] Young M. W.

[39] Erdelyi M.,
Szabad J.
(1989) Isolation and characterization of dominant female sterile mutations of Drosophilamelanogaster. I. Mutations on the third chromosome. Genetics 122, 111–127
OpenUrl Abstract/FREE Full Text

[40] Erdelyi M.,

[41] Szabad J.

[42] Fehon R. G.,
Dawson I. A.,
Artavanis-Tsakonas S.
(1994). A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene. Development 120, 545–557
OpenUrl Abstract

[43] Fehon R. G.,

[44] Dawson I. A.,

[45] Artavanis-Tsakonas S.

[46] Green J. B.,
Howes G.,
Symes K.,
Cooke J.,
Smith J. C.
(1990) The biological effects of XTC-MIF: quantitative comparison with Xenopus bFGF. Development 108, 173–183
OpenUrl Abstract

[47] Green J. B.,

[48] Howes G.,

[49] Symes K.,

[50] Cooke J.,

[51] Smith J. C.

[52] Hartenstein A. Y.,
Rugendorgg A.,
Tepass U.,
Hartenstein V.
(1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116, 1203–1220
OpenUrl Abstract/FREE Full Text

[53] Hartenstein A. Y.,

[54] Rugendorgg A.,

[55] Tepass U.,

[56] Hartenstein V.

[57] Jan L. Y.,
Jan Y. N.
(1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc. Natl. Acad. Sci. USA 72, 2700–2704

[58] Jan L. Y.,

[59] Jan Y. N.

[60] Kimelman D.,
Abraham J. A.,
Haaparanta T.,
Palisi T. M.,
Kirschner M. W.
(1988) The presence of fibroblast growth factor in the frog egg: its role as a natural mesoderm inducer. Science 242, 1053–1056
OpenUrl Abstract/FREE Full Text

[61] Kimelman D.,

[62] Abraham J. A.,

[63] Haaparanta T.,

[64] Palisi T. M.,

[65] Kirschner M. W.

[66] Kosman D.,
Ip Y. T.,
Levine M.,
Arora K.
(1991) Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo. Science 254, 3118–3122
OpenUrl

[67] Kosman D.,

[68] Ip Y. T.,

[69] Levine M.,

[70] Arora K.

[71] Lawrence P. A.,
Johnston P.
(1986) The muscle pattern of a segment of Drosophila may be determined by neurons and not by contributing myoblasts. Cell 45, 505–513
OpenUrl CrossRef PubMed Web of Science

[72] Lawrence P. A.,

[73] Johnston P.

[74] Leiss D.,
Hinz U.,
Gasch A.,
Mertz R.,
Renkawitz-Pohl R.
(1988) 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 104, 525–531
OpenUrl Abstract/FREE Full Text

[75] Leiss D.,

[76] Hinz U.,

[77] Gasch A.,

[78] Mertz R.,

[79] Renkawitz-Pohl R.

[80] Leptin M.,
Grunewald B.
(1990) Cell shape changes during gastrulation in Drosophila. Development 110, 73–84
OpenUrl Abstract

[81] Leptin M.,

[82] Grunewald B.

[83] Lipton D. H.,
Jacobsen A. G.
(1973) Analysis of normal somite development. Dev. Biol 38, 73–90

[84] Lipton D. H.,

[85] Jacobsen A. G.

[86] Michelson A. M.,
Abmayr S. M.,
Bate M.,
Martinez-Arias A.,
Maniatis T.
(1990) Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Dev 4, 2086–2097
OpenUrl Abstract/FREE Full Text

[87] Michelson A. M.,

[88] Abmayr S. M.,

[89] Bate M.,

[90] Martinez-Arias A.,

[91] Maniatis T.

[92] Nicolet G.
(1970) Is the presumptive notochord responsible for somite genesis in the chick?. J. Embryol. Exp. Morphol 24, 231–262
OpenUrl

[93] Nicolet G.

[94] Paterson B. M.,
Walldorf U.,
Eldredge J.,
Dubendorfer A.,
Frasch M.,
Gehring W. J.
(1990) The Drosophila homologue of vertebrate myogenic-determination genes encodes a transiently expressed nuclear protein marking primary myogenic cells. Proc. Natl. Acad. Sci. USA 88, 3782–3786
OpenUrl Abstract/FREE Full Text

[95] Paterson B. M.,

[96] Walldorf U.,

[97] Eldredge J.,

[98] Dubendorfer A.,

[99] Frasch M.,

[100] Gehring W. J.

[101] Poulson D. F.
(1945) Chromosomal control of embryogenesis in Drosophila. Am. Nat 79, 340–363
OpenUrl

[102] Poulson D. F.

[103] Ray R. P.,
Arora K.,
Nusslein-Volhard C.,
Gelbart W. M.
(1991) The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113, 35–54
OpenUrl Abstract

[104] Ray R. P.,

[105] Arora K.,

[106] Nusslein-Volhard C.,

[107] Gelbart W. M.

[108] Robinow S.,
White K.
(1991) Characterization and spatial distribution of the ELAV protein during Drosophilamelanogaster development. J. Neurobiol 22, 443–461
OpenUrl CrossRef PubMed Web of Science

[109] Robinow S.,

[110] White K.

[111] Seidel F.,
Bock E.,
Krause G.
(1940) Die Organisation des Insekteneies. Naturwissenschaften 28, 433–446
OpenUrl CrossRef Web of Science

[112] Seidel F.,

[113] Bock E.,

[114] Krause G.

[115] Shishido E.,
Higashijima S.,
Emori Y.,
Saigo K.
(1993) Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117, 751–761
OpenUrl Abstract

[116] Shishido E.,

[117] Higashijima S.,

[118] Emori Y.,

[119] Saigo K.

[120] Staehling-Hampton K.,
Hoffmann F. M.,
Baylies M. K.,
Rushton E.,
Bate M.
(1994) dpp induces mesodermal gene expression in Drosophila. Nature 373, 783–786
OpenUrl

[121] Staehling-Hampton K.,

[122] Hoffmann F. M.,

[123] Baylies M. K.,

[124] Rushton E.,

[125] Bate M.

[126] St. Johnston R. D.,
Gelbart W. M.
(1987) Decapentaplegic transcriptsare localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J 6, 2785–2791
OpenUrl PubMed Web of Science

[127] St. Johnston R. D.,

[128] Gelbart W. M.

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

[130] St. Johnston D.,

[131] Nusslein-Volhard C.

[132] Tepass U.,
Hartenstein V.
(1994) Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 120, 579–590
OpenUrl Abstract

[133] Tepass U.,

[134] Hartenstein V.

[135] Thisse B.,
Stoetzel C.,
Gorostiza T. C.,
Perrin Schmitt F.
(1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7, 2175–2183
OpenUrl PubMed Web of Science

[136] Thisse B.,

[137] Stoetzel C.,

[138] Gorostiza T. C.,

[139] Perrin Schmitt F.

[140] Volk T.,
VijayRaghaven K.
(1994) A central role for epidermal segment border cells in the induction of muscle patterning in the Drosophila embryo. Development 120, 59–70
OpenUrl Abstract

[141] Volk T.,

[142] VijayRaghaven K.

[143] Williams J. A.,
Bell J. B.,
Carroll S. B.
(1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5, 2481–2495
OpenUrl Abstract/FREE Full Text

[144] Williams J. A.,

[145] Bell J. B.,

[146] Carroll S. B.

Main menu

User menu

Search

Development

Summary

Reference

Citation Manager Formats

Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Kathryn Virginia Anderson (1952-2020)

Zooming into 2021

Read & Publish participation extends worldwide

Upcoming special issues

Development presents...

Main menu

User menu

Search

Summary

Reference

Citation Manager Formats

Article navigation

Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Kathryn Virginia Anderson (1952-2020)

Zooming into 2021

Read & Publish participation extends worldwide

Upcoming special issues

Development presents...