Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

AbstractEvolution of morphogenesis is generally associated with changes in genetic regulation. Here we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.Impact StatementEvolutionary reduction in tissue number involves the simplification of the seaming process but not signaling during epithelial fusion.

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Two consecutive microtubule-based epithelial seaming events mediate dorsal closure in the scuttle fly Megaselia abdita

eLife ◽

10.7554/elife.33807 ◽

2018 ◽

Vol 7 ◽

Author(s):

Juan Jose Fraire-Zamora ◽

Johannes Jaeger ◽

Jérôme Solon

Keyword(s):

Drosophila Melanogaster ◽

Signaling Pathways ◽

Genetic Regulation ◽

Dorsal Closure ◽

Evolutionary Transition ◽

Morphogenetic Process ◽

Signaling Regulation ◽

Tissue System ◽

Megaselia Abdita

Evolution of morphogenesis is generally associated with changes in genetic regulation. Here, we report evidence indicating that dorsal closure, a conserved morphogenetic process in dipterans, evolved as the consequence of rearrangements in epithelial organization rather than signaling regulation. In Drosophila melanogaster, dorsal closure consists of a two-tissue system where the contraction of extraembryonic amnioserosa and a JNK/Dpp-dependent epidermal actomyosin cable result in microtubule-dependent seaming of the epidermis. We find that dorsal closure in Megaselia abdita, a three-tissue system comprising serosa, amnion and epidermis, differs in morphogenetic rearrangements despite conservation of JNK/Dpp signaling. In addition to an actomyosin cable, M. abdita dorsal closure is driven by the rupture and contraction of the serosa and the consecutive microtubule-dependent seaming of amnion and epidermis. Our study indicates that the evolutionary transition to a reduced system of dorsal closure involves simplification of the seaming process without changing the signaling pathways of closure progression.

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Faculty Opinions recommendation of Transiently reorganized microtubules are essential for zippering during dorsal closure in Drosophila melanogaster.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1033874.539803 ◽

2007 ◽

Author(s):

Elizabeth Gavis

Keyword(s):

Drosophila Melanogaster ◽

Dorsal Closure

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Targeted Expression of the Class II Phosphoinositide 3-Kinase in Drosophila melanogaster Reveals Lipid Kinase-Dependent Effects on Patterning and Interactions with Receptor Signaling Pathways

Molecular and Cellular Biology ◽

10.1128/mcb.24.2.796-808.2004 ◽

2004 ◽

Vol 24 (2) ◽

pp. 796-808 ◽

Cited By ~ 22

Author(s):

Lindsay K. MacDougall ◽

Mary Elizabeth Gagou ◽

Sally J. Leevers ◽

Ernst Hafen ◽

Michael D. Waterfield

Keyword(s):

Drosophila Melanogaster ◽

Signaling Pathways ◽

Egf Receptor ◽

Adaptor Protein ◽

Class Ii ◽

Notch Receptor ◽

Mitogen Activated Protein Kinase ◽

Class I ◽

Wing Venation ◽

Receptor Signaling

ABSTRACT Phosphoinositide 3-kinases (PI3Ks) can be divided into three distinct classes (I, II, and III) on the basis of their domain structures and the lipid signals that they generate. Functions have been assigned to the class I and class III enzymes but have not been established for the class II PI3Ks. We have obtained the first evidence for a biological function for a class II PI3K by expressing this enzyme during Drosophila melanogaster development and by using deficiencies that remove the endogenous gene. Wild-type and catalytically inactive PI3K_68D transgenes have opposite effects on the number of sensory bristles and on wing venation phenotypes induced by modified epidermal growth factor (EGF) receptor signaling. These results indicate that the endogenous PI3K_68D may act antagonistically to the EGF receptor-stimulated Ras-mitogen-activated protein kinase pathway and downstream of, or parallel to, the Notch receptor. A class II polyproline motif in PI3K_68D can bind the Drk adaptor protein in vitro, primarily via the N-terminal SH3 domain of Drk. Drk may thus be important for the localization of PI3K_68D, allowing it to modify signaling pathways downstream of cell surface receptors. The phenotypes obtained are markedly distinct from those generated by expression of the Drosophila class I PI3K, which affects growth but not pattern formation.

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Comparative approaches to the study of physiology: Drosophila as a physiological tool

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.00084.2012 ◽

2013 ◽

Vol 304 (3) ◽

pp. R177-R188 ◽

Cited By ~ 5

Author(s):

Wendi S. Neckameyer ◽

Kathryn J. Argue

Keyword(s):

Gene Expression ◽

Drosophila Melanogaster ◽

Pattern Formation ◽

Signaling Pathways ◽

Human Disease ◽

Cognitive Disorders ◽

Model System ◽

Critical Questions ◽

Developmental Signaling ◽

Shed Light

Numerous studies have detailed the extensive conservation of developmental signaling pathways between the model system, Drosophila melanogaster, and mammalian models, but researchers have also profited from the unique and highly tractable genetic tools available in this system to address critical questions in physiology. In this review, we have described contributions that Drosophila researchers have made to mathematical dynamics of pattern formation, cardiac pathologies, the way in which pain circuits are integrated to elicit responses from sensation, as well as the ways in which gene expression can modulate diverse behaviors and shed light on human cognitive disorders. The broad and diverse array of contributions from Drosophila underscore its translational relevance to modeling human disease.

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CYTOGENETIC ANALYSIS OF THE CHROMOSOMAL REGION IMMEDIATELY ADJACENT TO THE ROSY LOCUS IN DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/95.1.95 ◽

1980 ◽

Vol 95 (1) ◽

pp. 95-110 ◽

Cited By ~ 3

Author(s):

Arthur J Hilliker ◽

Stephen H Clark ◽

Arthur Chovnick ◽

William M Gelbart

Keyword(s):

Drosophila Melanogaster ◽

Polytene Chromosome ◽

Structural Information ◽

Genetic Regulation ◽

Chromosome Band ◽

Genetic Dissection ◽

Genetic Unit ◽

Complementation Groups ◽

The Relationship ◽

Chromosome Bands

ABSTRACT This report describes the genetic analysis of a region of the third chromosome of Drosophila melanogaster extending from 87D2-4 to 87E12-F1, an interval of 23 or 24 polytene chromosome bands. This region includes the rosy (ry, 3-52.0) locus, carrying the structural information for xanthine dehydrogenase (XDH). We have, in recent years, focused attention on the genetic regulation of the rosy locus and, therefore, wished to ascertain in detail the immediate genetic environmcnt of this locus. Specifically, we question if rosy is a solitary genetic unit or part of a larger complex genetic unit encompassing adjacent genes. Our data also provide opportunity to examine further the relationship between euchromatic gene distrihution and polytene chromosome structure.—The results of our genetic dissection of the rosy microregion substantiate the conclusion drawn earlier (SCHALET, KERNAGHAN and CHOVNICK 1964) that the rosy locus is the only gene in this region concerned with XDH activity and that all adjacent genetic units are functionally, as well as spatially, distinct Erom the rosy gene. Within the rosy micro-region, we observed a close correspondence between the number of complementation groups (21) and the number of polytene chromosome bands (23 or 24). Consideration of this latter observation in conjunction with those of similar studies of other chhromosomal regions supports the hypothesis that each polytene chromosome band corresponds to a single genetic unit.

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ACK Family Tyrosine Kinase Activity Is a Component of Dcdc42 Signaling during Dorsal Closure in Drosophila melanogaster

Molecular and Cellular Biology ◽

10.1128/mcb.22.11.3685-3697.2002 ◽

2002 ◽

Vol 22 (11) ◽

pp. 3685-3697 ◽

Cited By ~ 15

Author(s):

Kai Ping Sem ◽

Baharak Zahedi ◽

Ivan Tan ◽

Maria Deak ◽

Louis Lim ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Tyrosine Kinase ◽

Kinase Activity ◽

Leading Edge ◽

Small Gtpase ◽

Dominant Negative ◽

Binding Motif ◽

Dorsal Closure ◽

Tyrosine Kinase Activity ◽

Amino Terminal

ABSTRACT We have characterized Drosophila melanogaster ACK (DACK), one of two members of the ACK family of nonreceptor tyrosine kinases in Drosophila. The ACKs are likely effectors for the small GTPase Cdc42, but signaling by these proteins remains poorly defined. ACK family tyrosine kinase activity functions downstream of Drosophila Cdc42 during dorsal closure of the embryo, as overexpression of DACK can rescue the dorsal closure defects caused by dominant-negative Dcdc42. Similar to known participants in dorsal closure, DACK is enriched in the leading edge cells of the advancing epidermis, but it does not signal through activation of the Jun amino-terminal kinase cascade operating in these cells. Transcription of DACK is responsive to changes in Dcdc42 signaling specifically at the leading edge and in the amnioserosa, two tissues involved in dorsal closure. Unlike other members of the ACK family, DACK does not contain a conserved Cdc42-binding motif, and transcriptional regulation may be one route by which Dcdc42 can affect DACK function. Expression of wild-type and kinase-dead DACK transgenes in embryos, and in the developing wing and eye, reveals that ACK family tyrosine kinase activity is involved in a range of developmental events similar to that of Dcdc42.

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Discrete Functions of TRAF1 and TRAF2 in Drosophila melanogaster Mediated by c-Jun N-Terminal Kinase and NF-κB-Dependent Signaling Pathways

Molecular and Cellular Biology ◽

10.1128/mcb.23.22.7982-7991.2003 ◽

2003 ◽

Vol 23 (22) ◽

pp. 7982-7991 ◽

Cited By ~ 72

Author(s):

Guang-Ho Cha ◽

Kyoung Sang Cho ◽

Jun Hee Lee ◽

Myungjin Kim ◽

Euysoo Kim ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Signaling Pathways ◽

Nuclear Translocation ◽

Genetic Interaction ◽

Ectopic Expression ◽

Tumor Necrosis Factor Receptor ◽

Null Mutant ◽

Microbial Infection ◽

Jnk Pathway

ABSTRACT Two Drosophila tumor necrosis factor receptor-associated factors (TRAF), DTRAF1 and DTRAF2, are proposed to have similar functions with their mammalian counterparts as a signal mediator of cell surface receptors. However, their in vivo functions and related signaling pathways are not fully understood yet. Here, we show that DTRAF1 is an in vivo regulator of c-Jun N-terminal kinase (JNK) pathway in Drosophila melanogaster. Ectopic expression of DTRAF1 in the developing eye induced apoptosis, thereby causing a rough-eye phenotype. Further genetic interaction analyses revealed that the apoptosis in the eye imaginal disc and the abnormal eye morphogenesis induced by DTRAF1 are dependent on JNK and its upstream kinases, Hep and DTAK1. In support of these results, DTRAF1-null mutant showed a remarkable reduction in JNK activity with an impaired development of imaginal discs and a defective formation of photosensory neuron arrays. In contrast, DTRAF2 was demonstrated as an upstream activator of nuclear factor-κB (NF-κB). Ectopic expression of DTRAF2 induced nuclear translocation of two Drosophila NF-κBs, DIF and Relish, consequently activating the transcription of the antimicrobial peptide genes diptericin, diptericin-like protein, and drosomycin. Consistently, the null mutant of DTRAF2 showed immune deficiencies in which NF-κB nuclear translocation and antimicrobial gene transcription against microbial infection were severely impaired. Collectively, our findings demonstrate that DTRAF1 and DTRAF2 play pivotal roles in Drosophila development and innate immunity by differentially regulating the JNK- and the NF-κB-dependent signaling pathway, respectively.

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