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Midgut and muscle development in Drosophila melanogaster
Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine). (Ruth Palmer)
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The fully developed and functional Drosophila midgut comprises two layers, the visceral mesoderm and the endoderm. The visceral muscle of the midgut is formed by the fusion of founder cells with fusion competent cells to form the muscle syncytia. The specification of these cells and thus the fusion and the formation of the midgut muscle is dependent on the  Receptor tyrosine kinase (RTK) Alk (Loren et al., 2003). The endoderm underlies the visceral muscle and is formed from cells that originate from the anterior and the posterior parts of the embryo. These cells use the visceral mesoderm as a substrate for their migration. Using Alk mutant animals, we have studied endoderm migration during embryonic development. While the initial migration of the endoderm is not affected in the absence of the visceral mesoderm, we observe that the later dorsal-ventral endodermal migration does not take place.

The development of the visceral muscle and its dependence on the endoderm is poorly understood.  We have analysed gürtelchen (gurt) mutant animals, originally identified in a genetic screen for mutations affecting visceral muscle formation. Gurt mutants are so named due to their belt-like phenotype of the visceral muscle (gürtelchen is German for belt). Mapping of the genomic locus identified gurt as a mutation in a previously described gene - huckebein (hkb) which is known to have an important function in endoderm development. Gurt (hkb) mutants were used to further study the interaction between the endoderm and the visceral muscle during development. The initial specification of founder cells and fusion competent myoblasts as well as fusion events are unaffected in gurt (hkb) mutants, however, the elongation and stretching of the visceral muscle does not proceed as normal. Moreover, ablation of the visceral mesoderm disrupts endoderm migration, while ablation of the endoderm results in a delayed disruption of visceral muscle formation.

Signaling between the two tissues was investigated in detail. Since Alk is a critical player in visceral muscle development, we employed Alk mutant embryos for this task. In addition to the role of Alk in specifying the founder cells and initiating the visceral muscle fusion, we have shown that Alk mediated signaling has a role in the induction of the midgut constriction process by regulating dpp expression in the developing embryonic gut.

 Finally, we wished to identify genes in the founder cells/fusion competent myoblasts that might be regulated by Alk. C3G is a gunaine nucleotide exchange factor expressed in the visceral muscle founder cells. Deletion of the Drosophila C3G locus resulted in the generation of null mutants in C3G which are viable, but display decreased longevity, fitness and are semi-lethal. Further analysis of C3G mutants indicated that C3G is essential for normal larval musculature development, in part by regulating integrin localization at muscle attachment sites.

Place, publisher, year, edition, pages
Umeå: Department of molecular biology , 2009. , 59 p.
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 1264
Keyword [en]
Drosophila, visceral mesoderm, endoderm, somatic muscles, Alk, C3G
National Category
Cell and Molecular Biology
Research subject
Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-22137ISBN: 978-91-7264-782-4 (print)OAI: oai:DiVA.org:umu-22137DiVA: diva2:212847
Distributor:
Institutionen för molekylärbiologi (Medicinska fakulteten), 901 87, Umeå
Public defence
2009-05-20, Major Groove, byggnad 6L, Institutionen för Molekylärbiologi, 13:00 (English)
Opponent
Supervisors
Available from: 2009-04-28 Created: 2009-04-24 Last updated: 2011-09-01Bibliographically approved
List of papers
1. Drosophila Anaplastic Lymphoma Kinase regulates Dpp signalling in the developing embryonic gut.
Open this publication in new window or tab >>Drosophila Anaplastic Lymphoma Kinase regulates Dpp signalling in the developing embryonic gut.
Show others...
2007 (English)In: Differentiation, ISSN 0301-4681, Vol. 75, no 5, 418-26 p.Article in journal (Refereed) Published
Abstract [en]

The Drosophila melanogaster gene Anaplastic Lymphoma Kinase (Alk) regulates a signal transduction pathway required for founder cell specification within the visceral muscle of the developing embryonic midgut. During embryonic development, the midgut visceral muscle is lined by the endodermal cell layer. In this paper, we have investigated signalling between these two tissues. Here, we show that Alk function is required for decapentaplegic (Dpp) expression and subsequent signalling via the Mad pathway in the developing gut. We propose that not only does Alk signalling regulate founder cell specification and thus fusion in the developing visceral muscle, but that Alk also regulates Dpp signalling between the visceral muscle and the endoderm. This provides an elegant mechanism with which to temporally coordinate visceral muscle fusion and later events in midgut development.

Keyword
Animals, Drosophila Proteins/genetics/*metabolism, Drosophila melanogaster/anatomy & histology/*embryology/enzymology, Embryo; Nonmammalian/*metabolism, Endoderm/cytology/metabolism, Female, Gene Expression Regulation; Developmental, Intestines/*embryology/metabolism, Mesoderm/cytology/metabolism, Protein-Tyrosine Kinases/genetics/*metabolism, Signal Transduction
Identifiers
urn:nbn:se:umu:diva-17922 (URN)10.1111/j.1432-0436.2006.00148.x (DOI)17286600 (PubMedID)
Available from: 2007-11-23 Created: 2007-11-23Bibliographically approved
2. Fusion of circular and longitudinal muscles in Drosophila is independent of the endoderm but further visceral muscle differentiation requires a close contact between mesoderm and endoderm.
Open this publication in new window or tab >>Fusion of circular and longitudinal muscles in Drosophila is independent of the endoderm but further visceral muscle differentiation requires a close contact between mesoderm and endoderm.
Show others...
2009 (English)In: Mechanisms of Development, ISSN 0925-4773, E-ISSN 1872-6356, Vol. 126, no 8-9, 721-736 p.Article in journal (Refereed) Published
Abstract [en]

In this study we describe the morphological and genetic analysis of the Drosophila mutant gürtelchen (gurt). gurt was identified by screening an EMS collection for novel mutations affecting visceral mesoderm development and was named after the distinct belt shaped visceral phenotype. Interestingly, determination of visceral cell identities and subsequent visceral myoblast fusion is not affected in mutant embryos indicating a later defect in visceral development. gurt is in fact a new huckebein (hkb) allele and as such exhibits nearly complete loss of endodermal derived structures. Targeted ablation of the endodermal primordia produces a phenotype that resembles the visceral defects observed in huckebein(gürtelchen) (hkb(gurt)) mutant embryos. It was shown previously that visceral mesoderm development requires complex interactions between visceral myoblasts and adjacent tissues. Signals from the neighbouring somatic myoblasts play an important role in cell type determination and are a prerequisite for visceral muscle fusion. Furthermore, the visceral mesoderm is known to influence endodermal migration and midgut epithelium formation. Our analyses of the visceral phenotype of hkb(gurt) mutant embryos reveal that the adjacent endoderm plays a critical role in the later stages of visceral muscle development, and is required for visceral muscle elongation and outgrowth after proper myoblast fusion.

Place, publisher, year, edition, pages
Elsevier, 2009
Keyword
Myogenesis, Visceral mesoderm, Myoblast, FCs, FCMs, gürtelchen, gurt, huckebein, hkb
National Category
Cell and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-46257 (URN)10.1016/j.mod.2009.05.001 (DOI)19463947 (PubMedID)
Available from: 2011-08-29 Created: 2011-08-29 Last updated: 2017-12-08Bibliographically approved
3. Mutational analysis of the Guanine Nucleotide Exchange Factor C3G in Drosophila melanogaster reveals a role for C3G in larval muscle development.
Open this publication in new window or tab >>Mutational analysis of the Guanine Nucleotide Exchange Factor C3G in Drosophila melanogaster reveals a role for C3G in larval muscle development.
(English)Manuscript (Other academic)
Identifiers
urn:nbn:se:umu:diva-22150 (URN)
Available from: 2009-04-24 Created: 2009-04-24 Last updated: 2010-01-14Bibliographically approved

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