Hemocyte-Secreted Type IV Collagen Enhances BMP Signaling to Guide Renal Tubule Morphogenesis in Drosophila

Bunt, Stephanie; Hooley, Clare; Hu, Nan; Scahill, Catherine; Weavers, Helen; Skaer, Helen

doi:10.1016/j.devcel.2010.07.019

Cited by 126 publications

(146 citation statements)

References 96 publications

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“…Restriction of BMP movement may also be important in other contexts, including several where collagen IV was already shown to regulate a shortrange Dpp signal, such as the ovarian stem cell niche and the tip of malpighian tubules (8,28). The basic collagen IV binding motif is highly conserved among the Dpp/BMP2/4 subfamily (20) and is also found in some other BMPs, including BMP3, consistent with reports that BMP3 and BMP4 can bind collagen IV (11,29).…”

Section: Discussionsupporting

confidence: 64%

Multistep molecular mechanism for Bone morphogenetic protein extracellular transport in the Drosophila embryo

Sawala

Sutcliffe

Ashe

2012

Proc. Natl. Acad. Sci. U.S.A.

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In the Drosophila embryo, formation of a bone morphogenetic protein (BMP) morphogen gradient requires transport of a heterodimer of the BMPs Decapentaplegic (Dpp) and Screw (Scw) in a protein shuttling complex. Although the core components of the shuttling complex-Short Gastrulation (Sog) and Twisted Gastrulation (Tsg)-have been identified, key aspects of this shuttling system remain mechanistically unresolved. Recently, we discovered that the extracellular matrix protein collagen IV is important for BMP gradient formation. Here, we formulate a molecular mechanism of BMP shuttling that is catalyzed by collagen IV. We show that Dpp is the only BMP ligand in Drosophila that binds collagen IV. A collagen IV binding-deficient Dpp mutant signals at longer range in vivo, indicating that collagen IV functions to immobilize free Dpp in the embryo. We also provide in vivo evidence that collagen IV functions as a scaffold to promote shuttling complex assembly in a multistep process. After binding of Dpp/ Scw and Sog to collagen IV, protein interactions are remodeled, generating an intermediate complex in which Dpp/Scw-Sog is poised for release by Tsg through specific disruption of a collagen IV-Sog interaction. Because all components are evolutionarily conserved, we propose that regulation of BMP shuttling and immobilization through extracellular matrix interactions is widely used, both during development and in tissue homeostasis, to achieve a precise extracellular BMP distribution.

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Section: Discussionsupporting

confidence: 64%

Multistep molecular mechanism for Bone morphogenetic protein extracellular transport in the Drosophila embryo

Sawala

Sutcliffe

Ashe

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Indeed, Brückner et al (2004) predicted that many phenotypes found in Pvr mutants might be indirect consequences of hemocyte dysfunction. This has certainly been borne out in independent studies of central nervous system development (Olofsson and Page, 2005;Sears et al, 2003), malpighian tubule morphogenesis (Bunt et al, 2010), and now dorsal closure. Yet, sole rescue of hemocyte function did not eliminate midline phenotypes compared with similarly staged control embryos, and a significant degree of rescue was achieved by Pvr expression in ectodermal derivatives.…”

Section: Discussionmentioning

confidence: 99%

“…Presumably, the AS has to get out of the way before converging tissues meet at the midline, but inefficient hemocyte phagocytosis might result in corpses or debris obstructing the fusing tissues. Hemocytes also secrete extracellular matrix proteins required for embryonic morphogenesis (Bunt et al, 2010;Olofsson and Page, 2005). Together, impaired hemocyte survival and migration, two characteristic phenotypes of Pvr mutants (Brückner et al, 2004;Cho et al, 2002), could contribute to both decreased removal of cell corpses and compromised integrity of tissues fusing at the midline.…”

Section: Pvr Protein Expression In the As And Ectodermmentioning

confidence: 99%

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

et al. 2015

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A leading cause of human birth defects is the incomplete fusion of tissues, often manifested in the palate, heart, or neural tube. To investigate the molecular control of tissue fusion, embryonic dorsal closure and pupal thorax closure in Drosophila are useful experimental models. We find that Pvr mutants have defects in dorsal midline closure with incomplete amnioserosa internalization and epidermal zippering, as well as cardia bifida. These defects are relatively mild in comparison to those seen with other signaling mutants such as the JNK pathway, and we demonstrate that JNK signaling is not perturbed by altering Pvr receptor tyrosine kinase activity. Rather, modulation of Pvr levels in the ectoderm has an impact on PIP3 membrane accumulation consistent with a link to PI3K signal transduction. Polarized PI3K activity influences protrusive activity from the epidermal leading edge and protrusion area changes in accord with Pvr signaling intensity, providing a possible mechanism to explain Pvr mutant phenotypes. Tissue specific rescue experiments indicate a partial requirement in epithelial tissue, but confirm the essential role of Pvr in the hemocytes for embryonic survival. Taken together, we argue that inefficient removal of the internalizing amnioserosa tissue by mutant hemocytes coupled with impaired midline zippering of mutant epithelium creates a situation in some embryos where dorsal midline closure is incomplete. Based on these observations, we suggest that efferocytosis (corpse clearance) could contribute to proper tissue closure and thus may underlie some congenital birth defects.

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“…For example, it has been shown in Xenopus that neural crest and placode cells undergo a 'chase and run' mode of migration, in which the neural crest cells chase placode cells through chemotaxis and placode cells run when they are contacted by neural crest cells (Theveneau et al, 2013). In Drosophila embryos, hemocytes and renal tubules undergo migrations that are temporally distinct, yet have been shown to guide each other's migration/ morphogenesis (Bunt et al, 2010). Interdependent cell migrations might be commonplace during development and, despite the limited temporal role of such interactions, these interactions are likely to contribute to the efficient and robust movement of cells that is required to support proper development.…”

Section: Interdependence Of Germ Cell and Cvm Cell Migrationsmentioning

confidence: 99%

“…Duchek et al, 2001;McDonald et al, 2006). However, in a few cases, it has also been found that distinct cell types can jointly influence each other's migration and/or morphogenesis (Bunt et al, 2010;Theveneau et al, 2013). Thus, directed cell migration may be regulated by a series of events that include fixed and/or moving cues.…”

Section: Introductionmentioning

confidence: 99%

The migrations of Drosophila muscle founders and primordial germ cells are interdependent

et al. 2016

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Caudal visceral mesoderm (CVM) cells migrate from posterior to anterior of the Drosophila embryo as two bilateral streams of cells to support the specification of longitudinal muscles along the midgut. To accomplish this long-distance migration, CVM cells receive input from their environment, but little is known about how this collective cell migration is regulated. In a screen we found that wunen mutants exhibit CVM cell migration defects. Wunens are lipid phosphate phosphatases known to regulate the directional migration of primordial germ cells (PGCs). PGC and CVM cell types interact while PGCs are en route to the somatic gonadal mesoderm, and previous studies have shown that CVM impacts PGC migration. In turn, we found here that CVM cells exhibit an affinity for PGCs, localizing to the position of PGCs whether mislocalized or trapped in the endoderm. In the absence of PGCs, CVM cells exhibit subtle changes, including more cohesive movement of the migrating collective, and an increased number of longitudinal muscles is found at anterior sections of the larval midgut. These data demonstrate that PGC and CVM cell migrations are interdependent and suggest that distinct migrating cell types can coordinately influence each other to promote effective cell migration during development.

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Hemocyte-Secreted Type IV Collagen Enhances BMP Signaling to Guide Renal Tubule Morphogenesis in Drosophila

Cited by 126 publications

References 96 publications

Multistep molecular mechanism for Bone morphogenetic protein extracellular transport in the Drosophila embryo

Multistep molecular mechanism for Bone morphogenetic protein extracellular transport in the Drosophila embryo

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

The migrations of Drosophila muscle founders and primordial germ cells are interdependent

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