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The Mechanisms of Embryonic Scaling

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Abstract

The phenomenon of scaling, i.e., preserving the proportions of the embryo’s spatial pattern in dependence on its overall size, is the most prominent feature of the embryonic morphogenetic fields. Up to now, attempts to understand the mechanisms of scaling have been limited to the creation and analysis of the behavior of theoretical models that, to some extent, reproduce this phenomenon in silico. Only recently, when creating such models, scientists began to use experimental data on specific genes and their products (secreted proteins), which were identified during the study of various molecular mechanisms in embryogenesis. However, no approaches for the targeted identification of genes and proteins that are directly responsible for the embryonic scaling have been described in the literature so far. Developing such approaches and putting them into practice is an important task for future research. In this work, the main current publications on the problem of embryonic scaling and possible approaches to studying the mechanisms of this phenomenon are reviewed.

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REFERENCES

  1. Almuedo-Castillo, M., Bläßle, A., Mörsdorf, D., et al., Scale-invariant patterning by size-dependent inhibition of Nodal signalling, Nat. Cell Biol., 2018, vol. 20, no. 9, pp. 1032–1042.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Angerer, L.M., Yaguchi, R., Angerer, R., and Burke, R.D., The evolution of nervous system patterning: insights from sea urchin development, Development, 2011, vol. 138, no. 17, pp. 3613–3623.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Belintsev, B.N., Dissipative structures and the problem of biological morphogenesis, Usp. Fiz. Nauk, 1983, vol. 141, no. 1, pp. 55–101.

    Article  Google Scholar 

  4. Belousov, L.V. and Bogdanovskii, S.B., Cellular mechanisms of embryonic regulations in sea urchins, Ontogenez, 1980, vol. 11, pp. 467–475.

  5. Ben-Zvi, D. and Barkai, N., Scaling of morphogen gradients by an expansion-repression integral feedback control, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 15, pp. 6924–6929. https://doi.org/10.1073/pnas.0912734107

  6. Ben-Zvi, D., Shilo, B.-Z., Fainsod, A., and Barkai, N., Scaling of the BMP morphogen activation gradient in Xenopus embryos, Nature, 2008, vol. 453, no. 7199, pp. 1205–1211.

    Article  CAS  PubMed  Google Scholar 

  7. Ben-Zvi, D., Pyrowolakis, G., Barkai, N., and Shilo, B.-Z., Expansion-repression mechanism for scaling the Dpp activation gradient in Drosophila wing imaginal discs, Curr. Biol., 2011, vol. 21, no. 16, pp. 1391–1396.

    Article  CAS  PubMed  Google Scholar 

  8. Cui, N., Hu, M., and Khalil, R.A., Biochemical and biological attributes of matrix metalloproteinases, Prog. Mol. Biol. Transl. Sci., 2017, vol. 147, pp. 1–73.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Dawes, J.H., The emergence of a coherent structure for coherent structures: localized states in nonlinear systems, Phil. Trans. A, 2010, vol. 368, no. 1924, pp. 3519–3354.

  10. Driesch, H., Der Werth der beiden ersten Furchungszellen in der Echinodermentwicklung. Experimentelle Erzeugung von Theil und Doppelbildungen, Z. Wiss. Zool., 1891, vol. 53, pp. 160–178.

    Google Scholar 

  11. DuBuc, T.Q., Stephenson, T.B., Rock, A.Q., and Martindale, M.Q., Hox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation, Nat. Com., 2018, vol. 9, no. 1, p. 2007.

    Article  CAS  Google Scholar 

  12. Eldar, A., Dorfman, R., Weiss, D., et al., Robustness of the BMP morphogen gradient in drosophila embryonic patterning, Nature, 2002, vol. 419, pp. 304–308.

    Article  CAS  PubMed  Google Scholar 

  13. Eom, D.S., Bain, E.J., Patterson, L.B., et al., Long-distance communication by specialized cellular projections during pigment pattern development and evolution, Elife, 2015, vol. 4, pp. 2686–2695.

    Article  Google Scholar 

  14. Fritzenwanker, J.H., Genikhovich, G., Kraus, Y., and Technau, U., Early development and axis specification in the sea anemone Nematostella vectensis, Dev. Biol., 2007, vol. 310, no. 2, pp. 264–279.

    Article  CAS  PubMed  Google Scholar 

  15. Genikhovich, G., Fried, P., Prünster, M.M., et al., Axis patterning by BMPs: cnidarian network reveals evolutionary constraints, Cell. Rep., 2015, vol. 10, no. 10, pp. 1646–1654.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gierer, A. and Meinhardt, H., A theory of biological pattern formation, Kybernetik, 1972, vol. 12, no. 1, pp. 30–39.

    Article  CAS  PubMed  Google Scholar 

  17. Green, J.B.A. and Sharpe, J., Positional information and reaction-diffusion: two big ideas in developmental biology combine, Development, 2015, vol. 142, no. 7, pp. 1203–1211.

    Article  CAS  PubMed  Google Scholar 

  18. Gregor, T., Tank, D.W., Wieschaus, E.F., and Bialek, W., Probing the limits to positional information, Cell, 2007, vol. 130, no. 1, pp. 153–164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Horstadius, S., The mechanisms of sea urchin development, studied by operative methods, Biol. Rev., 1939, vol. 14, no. 2, pp. 132–179.

    Article  Google Scholar 

  20. Houchmandzadeh, B., Wieschaus, E., and Leibler, S., Establishment of developmental precision and proportions in the early Drosophila embryo, Nature, 2002, vol. 415, no. 6873, pp. 798–802.

    Article  CAS  PubMed  Google Scholar 

  21. Inomata, H., Shibata, T., Haraguchi, N., and Sasai, Y., Scaling of dorsal-ventral patterning by embryo size-dependent degradation of Spemann’s organizer signals, Cell, 2013, vol. 153, no. 6, pp. 1296–1311.

    Article  CAS  PubMed  Google Scholar 

  22. Inomata, H., Scaling of pattern formations and morphogen gradients, Dev. Growth Diff., 2017, vol. 59, no. 1, pp. 41–51.

    Article  CAS  Google Scholar 

  23. Leclère, L., Bause, M., Sinigaglia, C., et al., Development of the aboral domain in Nematostella requires β-catenin and the opposing activities of Six3/6 and Frizzled5/8, Development, 2016, vol. 143, no. 10, pp. 1766–1777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lee, J.Y., Choi, H.Y., Ahn, H.J., et al., Matrix metalloproteinase-3 promotes early blood-spinal cord barrier disruption and hemorrhage and impairs long-term neurological recovery after spinal cord injury, Am. J. Pathol., 2014, vol. 184, no. 11, pp. 2985–3000.

    Article  CAS  PubMed  Google Scholar 

  25. Levin, M., Morphogenetic fields in embryogenesis, regeneration, and cancer: non-local control of complex patterning, BioSystems, 2012, vol. 109, no. 3, pp. 243–261.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Magie, C.R., Daly, M., and Martindale, M.Q., Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression, Dev. Biol., 2007, vol. 305, no. 2, pp. 483–497.

    Article  CAS  PubMed  Google Scholar 

  27. Meinhardt, H., Models of biological pattern formation: from elementary steps to the organization of embryonic axes, Curr. Topics Dev. Biol., 2008, vol. 81, no. 7, pp. 1–63.

    Article  Google Scholar 

  28. Meinhardt, H., Models for the generation and interpretation of gradients, Cold Spring Harb. Perspect. Biol., 2009, vol. 1, no. 4. a001362.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Müller, P., Rogers, K.W., Jordan, B.M., et al., Differential diffusivity of Nodal and Lefty underlies a reaction-diffusion patterning system, Science, 2012, vol. 336, no. 6082, pp. 721–724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Mathematical Biology II: Spatial Models and Biomedical Applications, Murray, J.D., Ed., New York: Springer-Verlag, 1993.

    Google Scholar 

  31. Okabe-Oho, Y., Murakami, H., Oho, S., and Sasai, M., Stable, precise, and reproducible patterning of bicoid and hunchback molecules in the early Drosophila embryo, PLoS Comput. Biol., 2009, vol. 5, no. 8. e1000486.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Porcher, A. and Dostatni, N., The bicoid morphogen system, Curr. Biol., 2010, vol. 20, no. 5, pp. R249–R254.

    Article  CAS  PubMed  Google Scholar 

  33. Putnam, N.H., Srivastava, M., Hellsten, U., et al., Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization, Science, 2007, vol. 317, no. 5834, pp. 86–94.

    Article  CAS  PubMed  Google Scholar 

  34. Rasolonjanahary, M. and Vasiev, B., Scaling of morphogenetic patterns in reaction–diffusion systems, J. Theor. Biol., 2016, vol. 404, pp. 109–119.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Satoh, K. and Kominami, T., Initial observation of potential factors involved in the specification process of oral-aboral axis in the sand dollar Scaphechinus mirabilis, Dev. Growth Differ., 2008, vol. 50, no. 8, pp. 675–687.

    Article  PubMed  Google Scholar 

  36. Schmierer, B., Tournier, A.L., Bates, P.A., and Hill, C.S., Mathematical modeling identifies Smad nucleocytoplasmic shuttling as a dynamic signal interpreting system, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, no. 18, pp. 6608–6613.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Shingleton, A.W., Frankino, W.A., Flatt, T., et al., Size and shape: the developmental regulation of static allometry in insects, BioEssays, 2007, vol. 29, no. 6, pp. 536–548.

    Article  PubMed  Google Scholar 

  38. Sick, S., Reinker, S., Timmer, J., and Schlake, T., WNT and DKK determine hair follicle spacing through a reaction–diffusion mechanism, Science, 2006, vol. 314, no. 5804, pp. 1447–1450.

    Article  CAS  PubMed  Google Scholar 

  39. Sodergren, E., Weinstock, G.M., Davidson, E.H., et al., The genome of the sea urchin Strongylocentrotus purpuratus, Science, 2006, vol. 314, no. 5801, pp. 941–952.

    Article  PubMed  Google Scholar 

  40. Teleman, A.A. and Cohen, S.M., Dpp gradient formation in the Drosophila wing imaginal disc, Cell, 2000, vol. 103, no. 6, p. 10.

    Article  Google Scholar 

  41. Turing, A., The chemical basis of morphogenesis, Phil. Trans. R. Soc. Lond. B, 1952, vol. 237, no. 641, pp. 37–72.

    Article  Google Scholar 

  42. Umulis, D.M., Analysis of dynamic morphogen scale invariance, J. R. Soc. Interface, 2009, vol. 6, no. 41, pp. 1179–1191.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Umulis, D.M. and Othmer, H.G., Mechanisms of scaling in pattern formation, Development, 2013, vol. 140, no. 24, pp. 4830–4843.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Vacquier, V.D. and Mazia, D., Twinning of sea urchin embryos by treatment with dithiothreitol. Roles of cell surface interactions and of the hyaline layer, Exp. Cell Res., 1968, vol. 52, nos. 2–3, pp. 459–468.

    Article  CAS  PubMed  Google Scholar 

  45. Warner, J.F., Guerlais, V., Amiel, A.R., et al., NvERTx: a gene expression database to compare embryogenesis and regeneration in the sea anemone Nematostella vectensis, Development, 2018, vol. 145, no. 10. dev162867.

    Article  CAS  PubMed  Google Scholar 

  46. Wartlick, O., Kicheva, A., and González-Gaitán, M., Morphogen gradient formation, Cold Spring Harb. Perspect. Biol., 2009, vol. 1, no. 3. a001255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wartlick, O., Mumcu, P., Kicheva, A., et al., Dynamics of Dpp signaling and proliferation control, Science, 2011, vol. 331, no. 6021, pp. 1154–1159.

    Article  CAS  PubMed  Google Scholar 

  48. Wolpert, L., Positional information and the spatial pattern of cellular differentiation, J. Theor. Biol., 1969, vol. 25, no. 1, pp. 1–47.

    Article  CAS  PubMed  Google Scholar 

  49. Yamaguchi, M., Yoshimoto, E., and Kondo, S., Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 12, pp. 4790–4793.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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FUNDING

This study was supported by the Russian Science Foundation (project no. 14-14-00557P).

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Correspondence to A. M. Nesterenko or A. G. Zaraisky.

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Translated by M. Batrukova

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Nesterenko, A.M., Zaraisky, A.G. The Mechanisms of Embryonic Scaling. Russ J Dev Biol 50, 95–101 (2019). https://doi.org/10.1134/S1062360419030044

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