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Review

Cell mechanics and cell-cell recognition controls by Toll-like receptors in tissue morphogenesis and homeostasis

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Pages 233-247 | Received 15 Feb 2022, Accepted 04 May 2022, Published online: 17 May 2022

References

  • Anthoney N, Foldi I, Hidalgo A. Toll and toll-like receptor signalling in development. Dev. 2018;145(9):1–6.
  • Carvalho L, Jacinto A, Matova N. The Toll/NF-κB signaling pathway is required for epidermal wound repair in Drosophila. Proc Natl Acad Sci U S A. 2014;111(50):E5373–E5382.
  • Foldi I, Anthoney N, Harrison N, et al. Three-tier regulation of cell number plasticity by neurotrophins and Tolls in Drosophila. J Cell Biol. 2017;216(5):1421–1438.
  • Hashimoto C, Hudson KL, Anderson KV. The Toll gene of drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell. 1988;52(2):269–279.
  • Iijima N, Sato K, Kuranaga E, et al. Differential cell adhesion implemented by Drosophila Toll corrects local distortions of the anterior-posterior compartment boundary. Nat Commun. 2020;11(1). DOI:10.1038/s41467-020-20118-y
  • Lavalou J, Mao Q, Harmansa S, et al. Formation of polarized contractile interfaces by self-organized Toll-8/Cirl GPCR asymmetry. Dev Cell. 2021;56(11):1574–1588.e7.
  • Lemaitre B, Nicolas E, Michaut L, et al. The dorsoventral regulatory gene cassette spatzle/Toll/Cactus controls the potent antifungal response in Drosophila adults. Cell. 1996;86(6):973–983.
  • Leulier F, Lemaitre B. Toll-like receptors - Taking an evolutionary approach. Nat Rev Genet. 2008;9(3):165–178.
  • McIlroy G, Foldi I, Aurikko J, et al. Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nat Neurosci. 2013;16(9):1248–1256.
  • Meyer SN, Amoyel M, Bergantiños C, et al. An ancient defense system eliminates unfit cells from developing tissues during cell competition. Science(80-). 2014;346(6214). 10.1126/science.1258236
  • Paré AC, Vichas A, Fincher CT, et al. A positional Toll receptor code directs convergent extension in Drosophila. Nature. 2014;515(7528):523–527.
  • Tamada M, Shi J, Bourdot KS, et al. Toll receptors remodel epithelia by directing planar-polarized Src and PI3K activity. Dev Cell. 2021;56(11):1589–1602.e9.
  • Ward A, Hong W, Favaloro V, et al. Toll receptors instruct axon and dendrite targeting and participate in synaptic partner matching in a drosophila olfactory circuit. Neuron. 2015;85(5):1013–1028.
  • Anderson KV, Bokla L, Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the drosophila embryo: the induction of polarity by the Toll gene product. Cell. 1985a;42(3):791–798.
  • Anderson KV, Jürgens G, Nüsslein-Volhard C. Establishment of dorsal-ventral polarity in the drosophila embryo: genetic studies on the role of the Toll gene product. Cell. 1985b;42(3):779–789.
  • Belvin MP, Anderson KV. A CONSERVED SIGNALING PATHWAY: the drosophila toll-dorsal pathway. Annu Rev Cell Dev Biol. 1996;12(1):393–416.
  • Nüsslein-Volhard C. The Toll gene in drosophila pattern formation. Trends Genet. 2022;38(3):231–245.
  • Keith FJ, Gay NJ. The drosophila membrane receptor Toll can function to promote cellular adhesion. EMBO J. 1990;9(13):4299–4306.
  • Schneider DS, Hudson KL, Lin TY, et al. Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo. Genes Dev. 1991;5(5):797–807.
  • Chiang C, Beachy PA. Expression of a novel Toll-like gene spans the parasegment boundary and contributes to hedgehog function in the adult eye of Drosophila. Mech Dev. 1994;47(3):225–239.
  • Eldon E, Kooyer S, D’Evelyn D, et al. The drosophila 18 wheeler is required for morphogenesis and has striking similarities to toll. Development (Cambridge, England). 1994;120(4):885–899.
  • Kambris Z, Hoffmann JA, Imler JL, et al. Tissue and stage-specific expression of the Tolls in Drosophila embryos. Gene Expr Patterns. 2002;2(3–4):311–317.
  • Tauszig S, Jouanguy E, Hoffmann JA, et al. Toll-related receptors and the control of antimicrobial peptide expression in drosophila. Proc Natl Acad Sci U S A. 2000;97(19):10520–10525.
  • Akhouayri I, Turc C, Royet J, et al. Toll-8/tollo negatively regulates antimicrobial response in the drosophila respiratory epithelium. PLoS Pathog. 2011;7(10):e1002319.
  • Lamiable O, Arnold J, de Faria IJDS, et al. Analysis of the contribution of hemocytes and autophagy to drosophila antiviral immunity. J Virol. 2016;90(11):5415–5426.
  • Ligozygakis P, Bulet P, Reichhart JM. Critical evaluation of the role of the Toll-like receptor 18-Wheeler in the host defense of Drosophila. EMBO Rep. 2002;3(7):666–673.
  • Nakamoto M, Moy RH, Xu J, et al. Virus recognition by Toll-7 activates antiviral autophagy in drosophila. Immunity. 2012;36(4):658–667.
  • Narbonne-Reveau K, Charroux B, Royet J. Lack of an antibacterial response defect in drosophila toll-9 mutant. PLoS One. 2011;6(2):1–11.
  • Medzhitov R, Preston-Hurlburt P, Janeway CA. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. 1997;388(6640):394–397.
  • Kawai T, Akira S. Signaling to NF-κB by Toll-like receptors. Trends Mol Med. 2007;13(11):460–469.
  • Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nat Immunol. 2010;11(5):373–384.
  • Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004;4(7):499–511.
  • Sun H, Bristow BN, Qu G, et al. A heterotrimeric death domain complex in toll signaling. Proc Natl Acad Sci U S A. 2002;99(20):12871–12876.
  • Luo C, Zheng L. Independent evolution of Toll and related genes in insects and mammals. Immunogenetics. 2000;51(2):92–98.
  • Zou Z, Evans JD, Lu Z, et al. Comparative genomic analysis of the Tribolium immune system. Genome Biol. 2007;8(8):1–16.
  • Benton MA, Pechmann M, Frey N, et al. Toll genes have an ancestral role in axis elongation. Curr Biol. 2016;26(12):1609–1615.
  • Johnston LA. Competitive interactions between Cells: death, growth, and geography. Science. 2009;324(5935):1679–1682.
  • Nagata R, Igaki T. Cell competition: emerging mechanisms to eliminate neighbors. Dev Growth Differ. 2018;60(9):522–530
  • De La Cova C, Abril M, Bellosta P, et al. Drosophila myc regulates organ size by inducing cell competition. Cell. 2004. DOI:10.1016/S0092-8674(04)00214-4
  • Morata G, Ripoll P. Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev Biol. 1975;42(2):211–221.
  • Moreno E, Basler K. dMyc transforms cells into super-competitors. Cell. 2004;117(1):117–129.
  • Alpar L, Bergantiños C, Johnston LA. Spatially restricted regulation of spätzle/toll signaling during cell competition. Dev Cell. 2018;46(6):706–719.e5.
  • Germani F, Hain D, Sternlicht D, et al. The Toll pathway inhibits tissue growth and regulates cell fitness in an infection-dependent manner. Elife. 2018;7:1–10.
  • Katsukawa M, Ohsawa S, Zhang L, et al. Serpin facilitates tumor-suppressive cell competition by blocking toll-mediated yki activation in drosophila. Curr Biol. 2018;28(11):1756–1767.e6.
  • Bilder D. Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 2004;18(16):1909–1925.
  • Brumby AM, Richardson HE. scribble mutants cooperate with oncogenic ras or notch to cause neoplastic overgrowth in drosophila. EMBO J. 2003;22(21):5769–5779.
  • Lu B, Pang PT, Woo NH. The yin and yang of neurotrophin action. Nat Rev Neurosci. 2005;6(8):603–614.
  • Zhu B, Pennack JA, McQuilton P, et al. Drosophila neurotrophins reveal a common mechanism for nervous system formation. PLoS Biol. 2008;6(11):2476–2495.
  • Hepburn L, Prajsnar TK, Klapholz C, et al. A Spaetzle-like role for nerve growth factor in vertebrate immunity to staphylococcus aureus. Science(80-). 2014;346(6209):641–646.
  • Carter BD, Kaltschmidt C, Kaltschmidt B, et al. Selective activation of NF-κB by nerve growth factor through the neurotrophin receptor p75. Science(80-). 1996;272(5261):542–545.
  • Gutierrez H, Davies AM. Regulation of neural process growth, elaboration and structural plasticity by NF-κB. Trends Neurosci. 2011;34(6):316–325.
  • McLaughlin CN, Perry-Richardson JJ, Coutinho-Budd JC, et al. Dying neurons utilize innate immune signaling to prime glia for phagocytosis during development. Dev Cell. 2019;48(4):506–522.e6.
  • Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science. 2002;298(5600):1950–1954.
  • Keller R, Davidson L, Edlund A, et al. Mechanisms of convergence and extension by cell intercalation. Philosophical transactions of the royal society B: biological sciences. 2000;355(1399)897–922.
  • Shindo A. Models of convergent extension during morphogenesis. Wiley Interdiscip Rev Dev Biol. 2018;7(1):1–17.
  • Tada M, Heisenberg CP. Convergent extension: using collective cell migration and cell intercalation to shape embryos. Dev. 2012;139(21):3897–3904.
  • Bertet C, Sulak L, Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature. 2004;429(6992):667–671.
  • Irvine KD, Wieschaus E. Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development. 1994;120(4):827–841.
  • Blankenship JT, Backovic ST, Jssp S, et al. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev Cell. 2006;11(4):459–470.
  • Rauzi M, Verant P, Lecuit T, et al. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat Cell Biol. 2008;10(12):1401–1410.
  • Zallen JA, Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev Cell. 2004;6(3):343–355.
  • de M SS, Blankenship JT, Weitz O, et al. Rho-kinase directs bazooka/Par-3 planar polarity during drosophila axis elongation. Dev Cell. 2010;19(3):377–388.
  • Goodrich LV, Strutt D. Principles of planar polarity in animal development. Development. 2011;138(10):1877–1892.
  • Lawrence PA, Casal J. Planar cell polarity: two genetic systems use one mechanism to read gradients. Dev. 2018;145(23). DOI:10.1242/dev.168229
  • Seifert JRK, Mlodzik M. Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet. 2007;8(2):126–138.
  • Singh J, Mlodzik M. Planar cell polarity signaling: coordination of cellular orientation across tissues. Wiley Interdiscip Rev Dev Biol. 2012;1(4):479–499.
  • Tada M, Concha ML, Heisenberg C. Non-canonical Wnt signalling and regulation of gastrulation movements. Seminars in Cell & Developmental Biology. 2002;13(2):251–260.
  • Wallingford JB, Fraser SE, Harland RM. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev Cell. 2002;2(6):695–706.
  • Nishimura T, Honda H, Takeichi M. Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell. 2012;149(5):1084–1097.
  • Tetley RJ, Blanchard GB, Fletcher AG, et al. Unipolar distributions of junctional myosin II identify cell stripe boundaries that drive cell intercalation throughout drosophila axis extension. Elife. 2016;5(MAY2016):1–35.
  • Paré AC, Naik P, Shi J, et al. An LRR Receptor-Teneurin system directs planar polarity at compartment boundaries. Dev Cell. 2019;51(2):208–221.e6.
  • Kim S, Chung SY, Yoon J, et al. Ectopic expression of Tollo/Toll-8 antagonizes dpp signaling and induces cell sorting in the drosophila wing. Genesis. 2006. DOI:10.1002/dvg.20245
  • Dahmann C, Oates AC, Brand M. Boundary formation and maintenance in tissue development. Nat Rev Genet. 2011;12(1):43–55.
  • Crick FHC, Lawrence PA. Compartments and Polyclones in Insect Development. Science(80-). 1975;189(4200):340–347.
  • Sharrock TE, Sanson B. Cell sorting and morphogenesis in early Drosophila embryos. Semin Cell Dev Biol. 2020;107(February):147–160.
  • Umetsu D, Dahmann C. Signals and mechanics shaping compartment boundaries in drosophila. Wiley Interdiscip Rev Dev Biol. 2015;4(4):407–417.
  • Wang J, Dahmann C. Establishing compartment boundaries in Drosophila wing imaginal discs: an interplay between selector genes, signaling pathways and cell mechanics. Semin Cell Dev Biol. 2020;107:161–169.
  • Harris AK. Is cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. J Theor Biol. 1976;61(2):267–285.
  • Wayne Brodland G, Chen HH. The mechanics of cell sorting and envelopment. J Biomech. 2000;33(7):845–851.
  • Aliee M, Röper JC, Landsberg KP, et al. Physical mechanisms shaping the drosophila dorsoventral compartment boundary. Curr Biol. 2012;22(11):967–976.
  • Landsberg KP, Farhadifar R, Ranft J, et al. Increased cell bond tension governs cell sorting at the drosophila anteroposterior compartment boundary. Curr Biol. 2009;19(22):1950–1955.
  • Rudolf K, Umetsu D, Aliee M, et al. A local difference in Hedgehog signal transduction increases mechanical cell bond tension and biases cell intercalations along the Drosophila anteroposterior compartment boundary. Development. 2015;142(22):3845–3858.
  • Tsuboi A, Umetsu D, Kuranaga E, et al. Inference of cell mechanics in heterogeneous epithelial tissue based on multivariate clone shape quantification. Front Cell Dev Biol. 2017;5(AUG). DOI:10.3389/fcell.2017.00068
  • Umetsu D, Aigouy B, Aliee M, et al. Local increases in mechanical tension shape compartment boundaries by biasing cell intercalations. Curr Biol. 2014;24(15):1798–1805.
  • Steinberg MS. Reconstruction of tissues by dissociated cells. Sci. 1963. DOI:10.1126/science.141.3579.401
  • Gerttula S, Jin Y, Anderson KV. Zygotic expression and activity of the Drosophila Toll gene, a gene required maternally for embryonic dorsal-ventral pattern formation. Genetics. 1988;119(1):123–133.
  • Kornberg T. Compartments in the abdomen of Drosophila and the role of the engrailed locus. Dev Biol. 1981;86(2):363–372.
  • Madhavan MM, Madhavan K. Morphogenesis of the epidermis of adult abdomen of drosophila. J Embryol Exp Morphol. 1980;60:1–31.
  • Ninov N, Chiarelli DA, Martin-Blanco E. Extrinsic and intrinsic mechanisms directing epithelial cell sheet replacement during drosophila metamorphosis. Development. 2006;134(2):367–379.
  • Lecuit T, Lenne PF. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol. 2007;8(8):633–644.
  • Wang J, Tao Y, Reim I, et al. Expression, regulation, and requirement of the toll transmembrane protein during dorsal vessel formation in drosophila melanogaster. Mol Cell Biol. 2005;25(10):4200–4210.
  • Rose D, Zhu X, Kose H, et al. Toll, a muscle cell surface molecule, locally inhibits synaptic initiation of the RP3 motoneuron growth cone in Drosophila. Development. 1997;124(8):1561–1571.
  • Couto A, Alenius M, Dickson BJ. Molecular, anatomical, and functional organization of the drosophila olfactory system. Curr Biol. 2005;15(17):1535–1547.
  • Fishilevich E, Vosshall LB. Genetic and functional subdivision of the drosophila antennal lobe. Curr Biol. 2005;15(17):1548–1553.
  • Silbering AF, Rytz R, Grosjean Y, et al. Complementary function and integrated wiring of the evolutionarily distinct drosophila olfactory subsystems. J Neurosci. 2011;31(38):13357–13375.
  • Jefferis GSXE, Marin EC, Stocker RF, et al. Target neuron prespecification in the olfactory map of drosophila. Nature. 2001;414(6860):204–208.
  • Stocker RF, Lienhard MC, Borst A, et al. Neuronal architecture of the antennal lobe in drosophila melanogaster. Cell Tissue Res. 1990;262(1):9–34.
  • Kubota K, Keith FJ, Gay NJ. Wild type and constitutively activated forms of the drosophila Toll receptor have different patterns of N-linked glycosylation. FEBS Lett. 1995;365(1):83–86.
  • Luo C, Shen B, Manley JL, et al. Tehao functions in the Toll pathway in drosophila melanogaster: possible roles in development and innate immunity. Insect Mol Biol. 2001;10(5):457–464.
  • Sekine SU, Haraguchi S, Chao K, et al. Meigo governs dendrite targeting specificity by modulating Ephrin level and N-glycosylation. Nat Neurosci. 2013;16(6):683–691.
  • Kamemura K, Moriya H, Ukita Y, Okumura M, Miura M, Chihara T. Endoplasmic reticulum proteins Meigo and Gp93 govern dendrite targeting by regulating Toll-6 localization. Developmental Biology. 2022;484:30–39. DOI:10.1016/j.ydbio.2022.02.002
  • Umetsu D, Kuranaga E. Planar polarized contractile actomyosin networks in dynamic tissue morphogenesis. Curr Opin Genet Dev. 2017;45:90–96.
  • Pinner S, Sahai E. PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol. 2008;10(2):127–137.
  • Xue G, Hemmings BA. PKB/Akt-Dependent regulation of cell motility. JNCI J Natl Cancer Inst. 2013;105(6):393–404.
  • Nagata R, Nakamura M, Sanaki Y, et al. Cell competition is driven by autophagy. Dev Cell. 2019. DOI:10.1016/j.devcel.2019.08.018