The transcription factors KNIRPS and KNIRPS RELATED control cell migration and branch morphogenesis during Drosophila tracheal development

C.K. Chen; R.P. Kuhnlein; K.G. Eulenberg; S. Vincent; M. Affolter; R. Schuh

Summary

Cell migration during embryonic tracheal system development in Drosophila requires DPP and EGF signaling to generate the archetypal branching pattern. We show that two genes encoding the transcription factors KNIRPS and KNIRPS RELATED possess multiple and redundant functions during tracheal development. knirps/knirps related activity is necessary to mediate DPP signaling which is required for tracheal cell migration and formation of the dorsal and ventral branches. Ectopic knirps or knirps related expression in lateral tracheal cells respecifies their anteroposterior to a dorsoventral migration behavior, similar to that observed in the case of ectopic DPP expression. In dorsal tracheal cells knirps/knirps related activity represses the transcription factor SPALT; this repression is essential for secondary and terminal branch formation. However, in cells of the dorsal trunk, spalt expression is required for normal anteroposterior cell migration and morphogenesis. spalt expression is maintained by the EGF receptor pathway and, hence, some of the opposing activities of the EGF and DPP signaling pathways are mediated by spalt and knirps/knirps related. Furthermore, we provide evidence that the border between cells acquiring dorsal branch and dorsal trunk identity is established by the direct interaction of KNIRPS with a spalt cis-regulatory element.

REFERENCES

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OpenUrl Abstract
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OpenUrl Abstract
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OpenUrl Abstract
1. Eulenberg K. G.,
2. Schuh R.
(1997) The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis. EMBO J 16, 7156–7165
OpenUrl CrossRef PubMed Web of Science
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(1994) Drosophila melanogster: Practical uses in cell and molecular biology. Meth. Cell Biol 44, 446–488
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(1994) Redundant functions of the genes knirps and knirps-related for establishment of anterior Drosophila head structures. Proc. Nat. Acad. Sci. USA 91, 8567–8571
OpenUrl Abstract/FREE Full Text
1. Hynes R. O.,
2. Lander A. D.
(1992) Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68, 303–322
OpenUrl CrossRef PubMed Web of Science
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2. Glazer L.,
3. Shilo B. Z.
(1992) breathless, a Drosophila FGFreceptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 6, 1668–1678
OpenUrl Abstract/FREE Full Text
1. Kuhnlein R.P.,
2. Frommer G.,
3. Friedrich M.,
4. Gonzalez-Gaitan M.,
5. Weber A.,
6. Wagner-Bernholz J. F.,
7. Gehring W. J.,
8. Jäckle H.,
9. Schuh R.
(1994) spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J 13, 168–179
OpenUrl PubMed Web of Science
1. Kuhnlein R.P.,
2. Brönner G.,
3. Taubert H.,
4. Schuh R.
(1997) Regulation of Drosophila spalt gene expression. Mech. Dev 66, 107–118
OpenUrl CrossRef PubMed Web of Science
1. Kuhnlein R. P.,
2. Schuh R.
(1996) Dual function of the region specific homeotic gene spalt during Drosophila tracheal system development. Development 122, 2215–2223
OpenUrl Abstract
1. Lauffenburger D. A.,
2. Horwitz A. F.
(1996) Cell migration: A physically integrated molecular process. Cell 84, 359–369
OpenUrl CrossRef PubMed Web of Science
1. Lee T.,
2. Hacohen N.,
3. Krasnow M. A.,
4. Montel D. J.
(1996) Regulated Breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev 10, 2912–2921
OpenUrl Abstract/FREE Full Text
1. Llimargas M.,
2. Casanova J.
(1997) ventral veinless, a POU domain transcription factor, regulates different transduction pathways required for tracheal branching in Drosophila. Development 124, 3273–3281
OpenUrl Abstract
1. Montell D. J.
(1994) Moving right along: regulation of cell migration during Drosophila development. Trends Genet 10, 59–62
OpenUrl CrossRef PubMed
1. Ohshiro T.,
2. Saigo K.
(1997) Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in the Drosophila developing trachea. Development 124, 3975–3986
OpenUrl Abstract
1. Rothe M.,
2. Nauber U.,
3. Jäckle H.
(1989) Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J 8, 3087–3094
OpenUrl PubMed Web of Science
1. Rothe M.,
2. Pehl M.,
3. Taubert H.,
4. Jäckle H.
(1992) Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature 359, 156–159
OpenUrl CrossRef PubMed
1. Ruberte E.,
2. Marty T.,
3. Nellen D.,
4. Affolter M.,
5. Basler K.
(1995) An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 80, 889–897
OpenUrl CrossRef PubMed Web of Science
1. Samakovlis C.,
2. Hacohen N.,
3. Manning G.,
4. Sutherland D. C.,
5. Guillemin K.,
6. Krasnow M. A.
(1996) Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395–1407
OpenUrl Abstract
1. Schweitzer R.,
2. Shilo B.-Z.
(1997) A thousand and one roles for the Drosophila EGF receptor. Trends Genet 13, 191–196
OpenUrl CrossRef PubMed Web of Science
1. Shiga Y.,
2. Tanaka-Matakatsu M.,
3. Hayashi S.
(1996) A nuclear GFP/-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ 38, 99–106
1. Sutherland D.,
2. Samakovlis C.,
3. Krasnow M. A.
(1996) branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091–1101
OpenUrl CrossRef PubMed Web of Science
1. Thummel C. S.,
2. Pirrotta V.
(1992) New pCaSpeR P-element-vectors. Dros. Inf. Serv 71, 150–.
OpenUrl
1. Vincent S.,
2. Ruberte E.,
3. Grieder N. C.,
4. Chen C.-K.,
5. Haerry T.,
6. Schuh R.,
7. Affolter M.
(1997) DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 124, 2741–2750
OpenUrl Abstract
1. Wappner P.,
2. Gabay L.,
3. Shilo B.-Z.
(1997) Interaction between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124, 4707–4716
OpenUrl Abstract

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[1] Affolter M.,
Nellen D.,
Nussbaumer U.,
Basler K.
(1994) Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGFhomologs during Drosophila embryogenesis. Development 120, 3105–3117
OpenUrl Abstract

[2] Affolter M.,

[3] Nellen D.,

[4] Nussbaumer U.,

[5] Basler K.

[6] Brand A. H.,
Perrimon N.
(1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415
OpenUrl Abstract

[7] Brand A. H.,

[8] Perrimon N.

[9] Chiang C.,
Young K. E.,
Beachy P. A.
(1995) Control of Drosophila tracheal branching by the novel homeodomain gene unplugged, a regulatory target for genes of the bithorax complex. Development 121, 3901–3912
OpenUrl Abstract

[10] Chiang C.,

[11] Young K. E.,

[12] Beachy P. A.

[13] Eulenberg K. G.,
Schuh R.
(1997) The tracheae defective gene encodes a bZIP protein that controls tracheal cell movement during Drosophila embryogenesis. EMBO J 16, 7156–7165
OpenUrl CrossRef PubMed Web of Science

[14] Eulenberg K. G.,

[15] Schuh R.

[16] Goldstein L. S. B.,
Fryberg E. A.
(1994) Drosophila melanogster: Practical uses in cell and molecular biology. Meth. Cell Biol 44, 446–488
OpenUrl

[17] Goldstein L. S. B.,

[18] Fryberg E. A.

[19] González-Gaitán M.,
Rothe M.,
Wimmer E. A.,
Taubert H.,
Jäckle H.
(1994) Redundant functions of the genes knirps and knirps-related for establishment of anterior Drosophila head structures. Proc. Nat. Acad. Sci. USA 91, 8567–8571
OpenUrl Abstract/FREE Full Text

[20] González-Gaitán M.,

[21] Rothe M.,

[22] Wimmer E. A.,

[23] Taubert H.,

[24] Jäckle H.

[25] Hynes R. O.,
Lander A. D.
(1992) Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68, 303–322
OpenUrl CrossRef PubMed Web of Science

[26] Hynes R. O.,

[27] Lander A. D.

[28] Klämbt C.,
Glazer L.,
Shilo B. Z.
(1992) breathless, a Drosophila FGFreceptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 6, 1668–1678
OpenUrl Abstract/FREE Full Text

[29] Klämbt C.,

[30] Glazer L.,

[31] Shilo B. Z.

[32] Kuhnlein R.P.,
Frommer G.,
Friedrich M.,
Gonzalez-Gaitan M.,
Weber A.,
Wagner-Bernholz J. F.,
Gehring W. J.,
Jäckle H.,
Schuh R.
(1994) spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J 13, 168–179
OpenUrl PubMed Web of Science

[33] Kuhnlein R.P.,

[34] Frommer G.,

[35] Friedrich M.,

[36] Gonzalez-Gaitan M.,

[37] Weber A.,

[38] Wagner-Bernholz J. F.,

[39] Gehring W. J.,

[40] Jäckle H.,

[41] Schuh R.

[42] Kuhnlein R.P.,
Brönner G.,
Taubert H.,
Schuh R.
(1997) Regulation of Drosophila spalt gene expression. Mech. Dev 66, 107–118
OpenUrl CrossRef PubMed Web of Science

[43] Kuhnlein R.P.,

[44] Brönner G.,

[45] Taubert H.,

[46] Schuh R.

[47] Kuhnlein R. P.,
Schuh R.
(1996) Dual function of the region specific homeotic gene spalt during Drosophila tracheal system development. Development 122, 2215–2223
OpenUrl Abstract

[48] Kuhnlein R. P.,

[49] Schuh R.

[50] Lauffenburger D. A.,
Horwitz A. F.
(1996) Cell migration: A physically integrated molecular process. Cell 84, 359–369
OpenUrl CrossRef PubMed Web of Science

[51] Lauffenburger D. A.,

[52] Horwitz A. F.

[53] Lee T.,
Hacohen N.,
Krasnow M. A.,
Montel D. J.
(1996) Regulated Breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev 10, 2912–2921
OpenUrl Abstract/FREE Full Text

[54] Lee T.,

[55] Hacohen N.,

[56] Krasnow M. A.,

[57] Montel D. J.

[58] Llimargas M.,
Casanova J.
(1997) ventral veinless, a POU domain transcription factor, regulates different transduction pathways required for tracheal branching in Drosophila. Development 124, 3273–3281
OpenUrl Abstract

[59] Llimargas M.,

[60] Casanova J.

[61] Montell D. J.
(1994) Moving right along: regulation of cell migration during Drosophila development. Trends Genet 10, 59–62
OpenUrl CrossRef PubMed

[62] Montell D. J.

[63] Ohshiro T.,
Saigo K.
(1997) Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in the Drosophila developing trachea. Development 124, 3975–3986
OpenUrl Abstract

[64] Ohshiro T.,

[65] Saigo K.

[66] Rothe M.,
Nauber U.,
Jäckle H.
(1989) Three hormone receptor-like Drosophila genes encode an identical DNA-binding finger. EMBO J 8, 3087–3094
OpenUrl PubMed Web of Science

[67] Rothe M.,

[68] Nauber U.,

[69] Jäckle H.

[70] Rothe M.,
Pehl M.,
Taubert H.,
Jäckle H.
(1992) Loss of gene function through rapid mitotic cycles in the Drosophila embryo. Nature 359, 156–159
OpenUrl CrossRef PubMed

[71] Rothe M.,

[72] Pehl M.,

[73] Taubert H.,

[74] Jäckle H.

[75] Ruberte E.,
Marty T.,
Nellen D.,
Affolter M.,
Basler K.
(1995) An absolute requirement for both the type II and type I receptors, punt and thick veins, for dpp signaling in vivo. Cell 80, 889–897
OpenUrl CrossRef PubMed Web of Science

[76] Ruberte E.,

[77] Marty T.,

[78] Nellen D.,

[79] Affolter M.,

[80] Basler K.

[81] Samakovlis C.,
Hacohen N.,
Manning G.,
Sutherland D. C.,
Guillemin K.,
Krasnow M. A.
(1996) Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395–1407
OpenUrl Abstract

[82] Samakovlis C.,

[83] Hacohen N.,

[84] Manning G.,

[85] Sutherland D. C.,

[86] Guillemin K.,

[87] Krasnow M. A.

[88] Schweitzer R.,
Shilo B.-Z.
(1997) A thousand and one roles for the Drosophila EGF receptor. Trends Genet 13, 191–196
OpenUrl CrossRef PubMed Web of Science

[89] Schweitzer R.,

[90] Shilo B.-Z.

[91] Shiga Y.,
Tanaka-Matakatsu M.,
Hayashi S.
(1996) A nuclear GFP/-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ 38, 99–106

[92] Shiga Y.,

[93] Tanaka-Matakatsu M.,

[94] Hayashi S.

[95] Sutherland D.,
Samakovlis C.,
Krasnow M. A.
(1996) branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091–1101
OpenUrl CrossRef PubMed Web of Science

[96] Sutherland D.,

[97] Samakovlis C.,

[98] Krasnow M. A.

[99] Thummel C. S.,
Pirrotta V.
(1992) New pCaSpeR P-element-vectors. Dros. Inf. Serv 71, 150–.
OpenUrl

[100] Thummel C. S.,

[101] Pirrotta V.

[102] Vincent S.,
Ruberte E.,
Grieder N. C.,
Chen C.-K.,
Haerry T.,
Schuh R.,
Affolter M.
(1997) DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 124, 2741–2750
OpenUrl Abstract

[103] Vincent S.,

[104] Ruberte E.,

[105] Grieder N. C.,

[106] Chen C.-K.,

[107] Haerry T.,

[108] Schuh R.,

[109] Affolter M.

[110] Wappner P.,
Gabay L.,
Shilo B.-Z.
(1997) Interaction between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124, 4707–4716
OpenUrl Abstract

[111] Wappner P.,

[112] Gabay L.,

[113] Shilo B.-Z.

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