journal article
Open Access
Aug 09, 2024
The Enigmas of Tissue Closure: Inspiration from Drosophila
Abstract
Hollow structures are essential for development and physiological activity. The construction and maintenance of hollow structures never cease throughout the lives of multicellular animals. Epithelial tissue closure is the main strategy used by living organisms to build hollow structures. The high diversity of hollow structures and the simplicity of their development in Drosophila make it an excellent model for the study of hollow structure morphogenesis. In this review, we summarize the tissue closure processes in Drosophila that give rise to or maintain hollow structures and highlight the molecular mechanisms and distinct cell biology involved in these processes.
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References
101
[1]
Chung "The formation of epithelial tubes" J. Cell Sci. (2008) 10.1242/jcs.037887
[2]
Hogan "Organogenesis: Molecular mechanisms of tubulogenesis" Nat. Rev. Genet. (2002) 10.1038/nrg840
[3]
Avagliano "Overview on neural tube defects: From development to physical characteristics" Birth Defects Res. (2019) 10.1002/bdr2.1380
[4]
Copp "Genetics and development of neural tube defects" J. Pathol. (2010) 10.1002/path.2643
[5]
Maruyama "Drosophila as a model for epithelial tube formation" Dev. Dynam. (2012) 10.1002/dvdy.22775
[6]
Andrew "Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration" Dev. Biol. (2010) 10.1016/j.ydbio.2009.09.024
[7]
Balaghi "Myosin waves and a mechanical asymmetry guide the oscillatory migration of Drosophila cardiac progenitors" Dev. Cell (2023) 10.1016/j.devcel.2023.05.005
[8]
Tran "Programmed disassembly of a microtubule-based membrane protrusion network coordinates 3D epithelial morphogenesis in Drosophila" EMBO J. (2024) 10.1038/s44318-023-00025-w
[9]
Zhang "Periodic Oscillations of Myosin-II Mechanically Proofread Cell-Cell Connections to Ensure Robust Formation of the Cardiac Vessel" Curr. Biol. (2020) 10.1016/j.cub.2020.06.041
[10]
Eltsov "Quantitative analysis of cytoskeletal reorganization during epithelial tissue sealing by large-volume electron tomography" Nat. Cell Biol. (2015) 10.1038/ncb3159
[11]
Paci "Forced into shape: Mechanical forces in Drosophila development and homeostasis" Semin. Cell Dev. Biol. (2021) 10.1016/j.semcdb.2021.05.026
[12]
Mazumdar "How one becomes many: Blastoderm cellularization in Drosophila melanogaster" Bioessays (2002) 10.1002/bies.10184
[13]
Kiehart "Cell Sheet Morphogenesis: Dorsal Closure in Drosophila melanogaster as a Model System" Annu. Rev. Cell Dev. Biol. (2017) 10.1146/annurev-cellbio-111315-125357
[14]
Saias "Decrease in Cell Volume Generates Contractile Forces Driving Dorsal Closure" Dev. Cell (2015) 10.1016/j.devcel.2015.03.016
[15]
Hayes "Drosophila dorsal closure: An orchestra of forces to zip shut the embryo" Mech. Dev. (2017) 10.1016/j.mod.2016.12.005
[16]
Jacinto "Dynamic analysis of dorsal closure in Drosophila: From genetics to cell biology" Dev. Cell (2002) 10.1016/s1534-5807(02)00208-3
[17]
Selvaggi "Force measurements of Myosin II waves at the yolk surface during Drosophila dorsal closure" Biophys. J. (2022) 10.1016/j.bpj.2021.12.038
[18]
Tah, I., Haertter, D., Crawford, J.M., Kiehart, D.P., Schmidt, C.F., and Liu, A.J. (2023). Minimal vertex model explains how the amnioserosa avoids fluidization during Drosophila dorsal closure. arXiv.
10.1101/2023.12.20.572544
[19]
Harden "Signaling pathways directing the movement and fusion of epithelial sheets: Lessons from dorsal closure in Drosophila" Differ. Res. Biol. Divers. (2002)
[20]
Panfilio "High plasticity in epithelial morphogenesis during insect dorsal closure" Biol. Open (2013) 10.1242/bio.20136072
[21]
Lv, Z., Zhang, N., Zhang, X., Grosshans, J., and Kong, D. (2022). The Lateral Epidermis Actively Counteracts Pulling by the Amnioserosa During Dorsal Closure. Front. Cell Dev. Biol., 10.
10.3389/fcell.2022.865397
[22]
Rousset, R., Carballes, F., Parassol, N., Schaub, S., Cerezo, D., and Noselli, S. (2017). Signalling crosstalk at the leading edge controls tissue closure dynamics in the Drosophila embryo. PLoS Genet., 13.
10.1371/journal.pgen.1006640
[23]
Giuliani, F., Giuliani, G., Bauer, R., and Rabouille, C. (2013). Innexin 3, a new gene required for dorsal closure in Drosophila embryo. PLoS ONE, 8.
10.1371/journal.pone.0069212
[24]
Belacortu "Drosophila as a model of wound healing and tissue regeneration in vertebrates" Dev. Dyn. (2011) 10.1002/dvdy.22753
[25]
McEwen "The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning" Development (2000) 10.1242/dev.127.16.3607
[26]
VanHook "Head involution in Drosophila: Genetic and morphogenetic connections to dorsal closure" Dev. Dyn. (2008) 10.1002/dvdy.21405
[27]
Tsai "Crawling wounded: Molecular genetic insights into wound healing from Drosophila larvae" Int. J. Dev. Biol. (2018) 10.1387/ijdb.180085mg
[28]
Nandy "Rab11 is essential for lgl mediated JNK–Dpp signaling in dorsal closure and epithelial morphogenesis in Drosophila" Dev. Biol. (2020) 10.1016/j.ydbio.2020.06.005
[29]
Garlena "The receptor tyrosine kinase Pvr promotes tissue closure by coordinating corpse removal and epidermal zippering" Development (2015)
[30]
Gheisari "Gastrulation in Drosophila melanogaster: Genetic control, cellular basis and biomechanics" Mech. Dev. (2020) 10.1016/j.mod.2020.103629
[31]
Loerke "Viscoelastic voyages—Biophysical perspectives on cell intercalation during Drosophila gastrulation" Semin. Cell Dev. Biol. (2020) 10.1016/j.semcdb.2019.11.005
[32]
Martin "The Physical Mechanisms of Drosophila Gastrulation: Mesoderm and Endoderm Invagination" Genetics (2020) 10.1534/genetics.119.301292
[33]
Rahimi "Dynamics of Spaetzle morphogen shuttling in the embryo shapes gastrulation patterning" Development (2019) 10.1242/dev.181487
[34]
Martin "Modular regulation of Rho family GTPases in development" Small GTPases (2019) 10.1080/21541248.2017.1294234
[35]
Bodmer, R., and Frasch, M. (2010). Chapter 1.2—Development and Aging of the Drosophila Heart. Heart Development and Regeneration, Academic Press.
10.1016/b978-0-12-381332-9.00002-5
[36]
Vogler "Cellular Mechanisms of Drosophila Heart Morphogenesis" J. Cardiovasc Dev. Dis. (2015)
[37]
Bileckyj, C., Blotz, B., and Cripps, R.M. (2023). Drosophila as a Model to Understand Second Heart Field Development. J. Cardiovasc Dev. Dis., 10.
10.3390/jcdd10120494
[38]
Zhang "Selective Filopodia Adhesion Ensures Robust Cell Matching in the Drosophila Heart" Dev. Cell (2018) 10.1016/j.devcel.2018.06.015
[39]
Tao "Heart development in Drosophila" Semin. Cell Dev. Biol. (2007) 10.1016/j.semcdb.2006.12.001
[40]
Ahmad "Conserved signaling mechanisms in Drosophila heart development" Dev. Dyn. (2017) 10.1002/dvdy.24530
[41]
Bishop "What is metamorphosis?" Integr. Comp. Biol. (2006) 10.1093/icb/icl004
[42]
Heyland "Signaling mechanisms underlying metamorphic transitions in animals" Integr. Comp. Biol. (2006) 10.1093/icb/icl023
[43]
Athilingam "Mechanics of epidermal morphogenesis in the Drosophila pupa" Semin. Cell Dev. Biol. (2021) 10.1016/j.semcdb.2021.06.008
[44]
Zeitlinger "Thorax closure in Drosophila: Involvement of Fos and the JNK pathway" Development (1999) 10.1242/dev.126.17.3947
[45]
Kumar "Heterophilic cell-cell adhesion of atypical cadherins Fat and Dachsous regulate epithelial cell size dynamics during Drosophila thorax morphogenesis" Mol. Biol. Cell (2020) 10.1091/mbc.e19-08-0468
[46]
Athilingam "Proximate larval epidermal cell layer generates forces for Pupal thorax closure in Drosophila" Genetics (2022) 10.1093/genetics/iyac030
[47]
Usui "Cellular basis of the dynamic behavior of the imaginal thoracic discs during Drosophila metamorphosis" Dev. Biol. (2000) 10.1006/dbio.2000.9766
[48]
Chaturvedi "Netrins: Evolutionarily Conserved Regulators of Epithelial Fusion and Closure in Development and Wound Healing" Cells Tissues Organs (2022) 10.1159/000513880
[49]
Tripathi "The wing imaginal disc" Genetics (2022) 10.1093/genetics/iyac020
[50]
Lu, J., Wang, Y., Wang, X., Wang, D., Pflugfelder, G.O., and Shen, J. (2022). The Tbx6 Transcription Factor Dorsocross Mediates Dpp Signaling to Regulate Drosophila Thorax Closure. Int. J. Mol. Sci., 23.
10.3390/ijms23094543
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Details
- Published
- Aug 09, 2024
- Vol/Issue
- 46(8)
- Pages
- 8710-8725
- License
- View
Authors
Funding
Guangdong Provincial Ordinary University Characteristic Innovation Project
Award: 2021ktscx029
Cite This Article
Xiaoying Huang, Zhongjing Su, Xiao-Jun Xie (2024). The Enigmas of Tissue Closure: Inspiration from Drosophila. Current Issues in Molecular Biology, 46(8), 8710-8725. https://doi.org/10.3390/cimb46080514
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