Condensation of the Drosophila nerve cord is oscillatory and depends on coordinated mechanical interactions

Amourda, 2017, Gene expression boundary scaling and organ size regulation in the Drosophila embryo, Dev. Growth Differ., 59, 21, 10.1111/dgd.12333 Anava, 2009, The regulative role of neurite mechanical tension in network development, Biophys. J., 96, 1661, 10.1016/j.bpj.2008.10.058 Barriga, 2018, Tissue stiffening coordinates morphogenesis by triggering collective cell migration in vivo, Nature, 554, 523, 10.1038/nature25742 Beckervordersandforth, 2008, Subtypes of glial cells in the Drosophila embryonic ventral nerve cord as related to lineage and gene expression, Mech. Dev., 125, 542, 10.1016/j.mod.2007.12.004 Bertet, 2004, Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation, Nature, 429, 667, 10.1038/nature02590 Boix-Fabrés, 2019, Automated macro approach to remove vitelline membrane autofluorescence in Drosophila embryo 4D movies, Methods Mol. Biol., 2040, 155, 10.1007/978-1-4939-9686-5_9 Bullmore, 2012, The economy of brain network organization, Nat. Rev. Neurosci., 13, 336, 10.1038/nrn3214 Bullock, 1965 Buszczak, 2007, The carnegie protein trap library: a versatile tool for Drosophila developmental studies, Genetics, 175, 1505, 10.1534/genetics.106.065961 Cajal, 1899 Campos-Ortega, 1985 Cavanaugh, 2020, RhoA mediates epithelial cell shape changes via mechanosensitive endocytosis, Dev. Cell, 52, 152, 10.1016/j.devcel.2019.12.002 Chen, 1996, grim, a novel cell death gene in Drosophila, Genes Dev., 10, 1773, 10.1101/gad.10.14.1773 Christley, 2007, Patterns of mesenchymal condensation in a multiscale, discrete stochastic model, PLoS Comput. Biol., 3, e76, 10.1371/journal.pcbi.0030076 Clément, 2017, Viscoelastic dissipation stabilizes cell shape changes during tissue morphogenesis, Curr. Biol., 27, 3132, 10.1016/j.cub.2017.09.005 Dawi, 2021, Stability bounds of a delay visco-elastic rheological model with substrate friction, J. Math. Biol., 83, 71, 10.1007/s00285-021-01699-8 DeLise, 2000, Cellular interactions and signaling in cartilage development, Osteoarthritis Cartilage, 8, 309, 10.1053/joca.1999.0306 Doubrovinski, 2017, Measurement of cortical elasticity in Drosophila melanogaster embryos using ferrofluids, Proc. Natl. Acad. Sci. USA, 114, 1051, 10.1073/pnas.1616659114 Erneux, 2009 Evans, 2010, Interdependence of macrophage migration and ventral nerve cord development in Drosophila embryos, Development, 137, 1625, 10.1242/dev.046797 Franze, 2013, The mechanical control of nervous system development, Development, 140, 3069, 10.1242/dev.079145 Franze, 2013, Mechanics in neuronal development and repair, Annu. Rev. Biomed. Eng., 15, 227, 10.1146/annurev-bioeng-071811-150045 Frenz, 1989, The mechanism of precartilage mesenchymal condensation: a major role for interaction of the cell surface with the amino-terminal heparin-binding domain of fibronectin, Dev. Biol., 136, 97, 10.1016/0012-1606(89)90133-4 Hall, 2000, All for one and one for all: condensations and the initiation of skeletal development, BioEssays, 22, 138, 10.1002/(SICI)1521-1878(200002)22:2<138::AID-BIES5>3.0.CO;2-4 Hartenstein, 2013, Initial neurogenesis in Drosophila, Wiley Interdiscip. Rev. Dev. Biol., 2, 701, 10.1002/wdev.111 Heisenberg, 2013, Forces in tissue morphogenesis and patterning, Cell, 153, 948, 10.1016/j.cell.2013.05.008 Hogan, 1999, Morphogenesis, Cell, 96, 225, 10.1016/S0092-8674(00)80562-0 Ito, 1995, Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord, Rouxs Arch. Dev. Biol., 204, 284, 10.1007/BF02179499 Jorba, 2017, Probing micromechanical properties of the extracellular matrix of soft tissues by atomic force microscopy, J. Cell. Physiol., 232, 19, 10.1002/jcp.25420 Karkali, 2020, JNK signaling in pioneer neurons directs the architectural organization of the CNS and coordinates the motor activity of the Drosophila embryo, bioRxiv, 092486 Khalilgharibi, 2019, Stress relaxation in epithelial monolayers is controlled by the actomyosin cortex, Nat. Phys., 15, 839, 10.1038/s41567-019-0516-6 Kiehart, 1986, Cytoplasmic myosin from Drosophila melanogaster, J. Cell Biol., 103, 1517, 10.1083/jcb.103.4.1517 Kilinc, 2018, The emerging role of mechanics in synapse formation and plasticity, Front. Cell. Neurosci., 12, 483, 10.3389/fncel.2018.00483 Krzic, 2012, Multiview light-sheet microscope for rapid in toto imaging, Nat. Methods, 9, 730, 10.1038/nmeth.2064 Landgraf, 1997, The origin, location, and projections of the embryonic abdominal motorneurons of Drosophila, J. Neurosci., 17, 9642, 10.1523/JNEUROSCI.17-24-09642.1997 Landgraf, 2003, Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites, Dev. Biol., 260, 207, 10.1016/S0012-1606(03)00215-X Le Novère, 2015, Quantitative and logic modelling of molecular and gene networks, Nat. Rev. Genet., 16, 146, 10.1038/nrg3885 LeGoff, 2015, Mechanical forces and growth in animal tissues, Cold Spring Harb. Perspect. Biol., 8, a019232, 10.1101/cshperspect.a019232 Li, 2017, Induction of expansion and folding in human cerebral organoids, Cell Stem Cell, 20, 385, 10.1016/j.stem.2016.11.017 Lin, 1994, Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation, Neuron, 13, 1055, 10.1016/0896-6273(94)90045-0 Lynch, 2013, Cellular mechanics of germ band retraction in Drosophila, Dev. Biol., 384, 205, 10.1016/j.ydbio.2013.10.005 Mammoto, 2010, Mechanical control of tissue and organ development, Development, 137, 1407, 10.1242/dev.024166 Martinek, 2008, Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos, J. Cell Sci., 121, 1671, 10.1242/jcs.021931 Matsubayashi, 2020, Rapid homeostatic turnover of embryonic ECM during tissue morphogenesis, Dev. Cell, 54, 33, 10.1016/j.devcel.2020.06.005 Mayer, 2010, Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows, Nature, 467, 617, 10.1038/nature09376 Meyer, 2014, Glia ECM interactions are required to shape the Drosophila nervous system, Mech. Dev., 133, 105, 10.1016/j.mod.2014.05.003 Miller, 2013, The interplay between cell signalling and mechanics in developmental processes, Nat. Rev. Genet., 14, 733, 10.1038/nrg3513 Mongera, 2018, A fluid-to-solid jamming transition underlies vertebrate body axis elongation, Nature, 561, 401, 10.1038/s41586-018-0479-2 Muñoz, 2018, Mechanical oscillations in biological tissues as a result of delayed rest-length changes, Phys. Rev. E, 98, 052409, 10.1103/PhysRevE.98.052409 Negrete, 2021, Towards a physical understanding of developmental patterning, Nat. Rev. Genet., 22, 518, 10.1038/s41576-021-00355-7 Notbohm, 2016, Cellular contraction and polarization drive collective cellular motion, Biophys. J., 110, 2729, 10.1016/j.bpj.2016.05.019 Novák, 2008, Design principles of biochemical oscillators, Nat. Rev. Mol. Cell Biol., 9, 981, 10.1038/nrm2530 Oliveira, 2014, Coordination of wing and whole-body development at developmental milestones ensures robustness against environmental and physiological perturbations, PLOS Genet., 10, e1004408, 10.1371/journal.pgen.1004408 Olofsson, 2005, Condensation of the central nervous system in embryonic Drosophila is inhibited by blocking hemocyte migration or neural activity, Dev. Biol., 279, 233, 10.1016/j.ydbio.2004.12.020 Page, 2008, Multiple roles for apoptosis facilitating condensation of the Drosophila ventral nerve cord, Genesis, 46, 61, 10.1002/dvg.20365 Pastor-Pareja, 2011, Shaping cells and organs in Drosophila by opposing roles of fat body-secreted Collagen IV and perlecan, Dev. Cell, 21, 245, 10.1016/j.devcel.2011.06.026 Patel, 1994, Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes, Methods Cell Biol., 44, 445, 10.1016/S0091-679X(08)60927-9 Petridou, 2019, Tissue rheology in embryonic organization, EMBO J., 38, e102497, 10.15252/embj.2019102497 Petrolli, 2019, Confinement-induced transition between wavelike collective cell migration modes, Phys. Rev. Lett., 122, 168101, 10.1103/PhysRevLett.122.168101 Peyret, 2019, Sustained oscillations of epithelial cell sheets, Biophys. J., 117, 464, 10.1016/j.bpj.2019.06.013 Pipa, 1973, Proliferation, movement, and regression of neurons during the postembryonic development of insects Redies, 2001, Modularity in vertebrate brain development and evolution, BioEssays, 23, 1100, 10.1002/bies.10014 Roig-Puiggros, 2020, Construction and reconstruction of brain circuits: normal and pathological axon guidance, J. Neurochem., 153, 10, 10.1111/jnc.14900 Sánchez-Soriano, 2007, Drosophila as a genetic and cellular model for studies on axonal growth, Neural Dev., 2, 9, 10.1186/1749-8104-2-9 Saunders, 2019, Open questions: how to get developmental biology into shape?, BMC Biol., 17, 17, 10.1186/s12915-019-0636-6 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schwabe, 2017, Dynamic analysis of the mesenchymal-epithelial transition of blood-brain barrier forming glia in Drosophila, Biol. Open, 6, 232 Serwane, 2017, In vivo quantification of spatially varying mechanical properties in developing tissues, Nat. Methods, 14, 181, 10.1038/nmeth.4101 Shellard, 2021, Collective durotaxis along a self-generated stiffness gradient in vivo, Nature, 600, 690, 10.1038/s41586-021-04210-x Shyer, 2017, Emergent cellular self-organization and mechanosensation initiate follicle pattern in the avian skin, Science, 357, 811, 10.1126/science.aai7868 Singh, 2012, Fibronectin and stem cell differentiation – lessons from chondrogenesis, J. Cell Sci., 125, 3703 Solon, 2009, Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure, Cell, 137, 1331, 10.1016/j.cell.2009.03.050 Spedden, 2013, Neuron biomechanics probed by atomic force microscopy, Int. J. Mol. Sci., 14, 16124, 10.3390/ijms140816124 Staddon, 2019, Mechanosensitive junction remodeling promotes robust epithelial morphogenesis, Biophys. J., 117, 1739, 10.1016/j.bpj.2019.09.027 Stark, 1997, Neural tube-ectoderm interactions are required for trigeminal placode formation, Development, 124, 4287, 10.1242/dev.124.21.4287 Stépán, 1989 Sumi, 2018, Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling, Dev. Cell, 47, 453, 10.1016/j.devcel.2018.10.025 Swanson, 2007, Quest for the basic plan of nervous system circuitry, Brain Res. Rev., 55, 356, 10.1016/j.brainresrev.2006.12.006 Technau, 2008, 628 Tessier-Lavigne, 1996, The molecular biology of axon guidance, Science, 274, 1123, 10.1126/science.274.5290.1123 Thielicke, 2018, The effects of wing twist in slow-speed flapping flight of birds: trading brute force against efficiency, Bioinspir Biomim, 13, 056015, 10.1088/1748-3190/aad5a3 Tiwari, 2021, Scaling of internal organs during Drosophila embryonic development, Biophys. J., 120, 4264, 10.1016/j.bpj.2021.05.023 Vig, 2016, On the quantification of cellular velocity fields, Biophys. J., 110, 1469, 10.1016/j.bpj.2016.02.032 Weber, 2011, Integrins and cadherins join forces to form adhesive networks, J. Cell Sci., 124, 1183, 10.1242/jcs.064618 Zhang, 2012, Signalling through mechanical inputs: a coordinated process, J. Cell Sci., 125, 3039, 10.1242/jcs.093666 Zlatic, 2009, Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis, PLoS Biol., 7, e1000135, 10.1371/journal.pbio.1000135