Abstract
Cells are arranged into species-specific patterns during early embryogenesis. Such cell division patterns are important since they often reflect the distribution of localized cortical factors from eggs/fertilized eggs to specific cells as well as the emergence of organismal form. However, it has proven difficult to reveal the mechanisms that underlie the emergence of cell positioning patterns that underlie embryonic shape, likely because a systems-level approach is required that integrates cell biological, genetic, developmental, and mechanical parameters. The choice of organism to address such questions is also important. Because ascidians display the most extreme form of invariant cleavage pattern among the metazoans, we have been analyzing the cell biological mechanisms that underpin three aspects of cell division (unequal cell division (UCD), oriented cell division (OCD), and asynchronous cell cycles) which affect the overall shape of the blastula-stage ascidian embryo composed of 64 cells. In ascidians, UCD creates two small cells at the 16-cell stage that in turn undergo two further successive rounds of UCD. Starting at the 16-cell stage, the cell cycle becomes asynchronous, whereby the vegetal half divides before the animal half, thus creating 24-, 32-, 44-, and then 64-cell stages. Perturbing either UCD or the alternate cell division rhythm perturbs cell position. We propose that dynamic cell shape changes propagate throughout the embryo via cell-cell contacts to create the ascidian-specific invariant cleavage pattern.
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References
Akiyama M, Tero A, Kobayashi R (2010) A mathematical model of cleavage. J Theor Biol 264:84–94. https://doi.org/10.1016/j.jtbi.2009.12.016
Bell GP, Fletcher GC, Brain R, Thompson BJ (2015) Aurora kinases phosphorylate Lgl to induce mitotic spindle orientation in Drosophila epithelia. Curr Biol 25:61–68. https://doi.org/10.1016/j.cub.2014.10.052
Bergstralh DT, Lovegrove HE, Kujawiak I et al (2016) Pins is not required for spindle orientation in the Drosophila wing disc. Development 143:2573–2581. https://doi.org/10.1242/dev.135475
Bosveld F, Markova O, Guirao B et al (2016) Epithelial tricellular junctions act as interphase cell shape sensors to orient mitosis. Nature 530:495–498. https://doi.org/10.1038/nature16970
Bouldin CM, Kimelman D (2014) Cdc25 and the importance of G2 control: insights from developmental biology. Cell Cycle 13:2165–2171. https://doi.org/10.4161/cc.29537
Brun-Usan M, Marín-Riera M, Grande C et al (2017) A set of simple cell processes is sufficient to model spiral cleavage. Development 144:54–62. https://doi.org/10.1242/dev.140285
Cabernard C, Prehoda KE, Doe CQ (2010) A spindle-independent cleavage furrow positioning pathway. Nature 467:91–94. https://doi.org/10.1038/nature09334
Campinho P, Behrndt M, Ranft J et al (2013) Tension-oriented cell divisions limit anisotropic tissue tension in epithelial spreading during zebrafish epiboly. Nat Cell Biol 15:1405–1414. https://doi.org/10.1038/ncb2869
Carvalho CA, Moreira S, Ventura G et al (2015) Aurora A triggers Lgl cortical release during symmetric division to control planar spindle orientation. Curr Biol 25:53–60. https://doi.org/10.1016/j.cub.2014.10.053
Chabry L (1887) Contribution a l’embryologie normale et teratologique des Ascidies simples. J Anat Physiol 23:167–319
Collart C, Allen GE, Bradshaw CR et al (2013) Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341:893–896. https://doi.org/10.1126/science.1241530
Conklin EG (1905) The organization and cell-lineage of the ascidian egg. J Acad Natl Sci Phila 13:1–119
Conrad GW, Williams DC (1974) Polar lobe formation and cytokinesis in fertilized eggs of Ilyanassa obsoleta. I Ultrastructure and effects of cytochalasin B and colchicine. Dev Biol 36:363–378
Cook CE, Chenevert J, Larsson TA et al (2016) Old knowledge and new technologies allow rapid development of model organisms. Mol Biol Cell 27:882–887. https://doi.org/10.1091/mbc.E15-10-0682
Costache V, Hebras C, Pruliere G et al (2017) Kif2 localizes to a subdomain of cortical endoplasmic reticulum that drives asymmetric spindle position. Nat Commun 8:s41467–s41017. https://doi.org/10.1038/s41467-017-01048-8
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965–968. https://doi.org/10.1038/nature04336
Delsuc F, Philippe H, Tsagkogeorga G et al (2018) A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biol 16:39. https://doi.org/10.1186/s12915-018-0499-2
di Pietro F, Echard A, Morin X (2016) Regulation of mitotic spindle orientation: an integrated view. EMBO Rep 17:1106–1130. https://doi.org/10.15252/embr.201642292
Driesch H (1892) Entwicklungsmechanische Studien 1. Der Wert der erster Furchungszellen in der Echinodermentwicklung Experimentelle Erzeugung von Teil-und Doppelbildungen Z Zool 53
Driesch H (1908) The 1907 Gifford Lectures. The Science and Philosophy of the Organism. Adam & Charles Black, London
Du Q, Stukenberg PT, Macara IG (2001) A mammalian partner of inscuteable binds NuMA and regulates mitotic spindle organization. Nat Cell Biol 3:1069–1075. https://doi.org/10.1038/ncb1201-1069
Dumollard R, Hebras C, Besnardeau L, McDougall A (2013) Beta-catenin patterns the cell cycle during maternal-to-zygotic transition in urochordate embryos. Dev Biol 384:331–342. https://doi.org/10.1016/j.ydbio.2013.10.007
Dumollard R, Minc N, Salez G et al (2017) The invariant cleavage pattern displayed by ascidian embryos depends on spindle positioning along the cell’s longest axis in the apical plane and relies on asynchronous cell divisions. elife 6. https://doi.org/10.7554/eLife.19290
Duncan REL, Whiteley AH (2011) The echinoid mitotic gradient: effect of cell size on the micromere cleavage cycle. Mol Reprod Dev 78:868–878. https://doi.org/10.1002/mrd.21373
Durgan J, Kaji N, Jin D, Hall A (2011) Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J Biol Chem 286:12461–12474. https://doi.org/10.1074/jbc.M110.174235
Fielmich L-E, Schmidt R, Dickinson DJ et al (2018) Optogenetic dissection of mitotic spindle positioning in vivo. elife 7. https://doi.org/10.7554/eLife.38198
Gehring WJ (1996) The master control gene for morphogenesis and evolution of the eye. Genes Cells 1:11–15
Gönczy P (2008) Mechanisms of asymmetric cell division: flies and worms pave the way. Nat Rev Mol Cell Biol 9:355–366. https://doi.org/10.1038/nrm2388
Grill SW, Hyman AA (2005) Spindle positioning by cortical pulling forces. Dev Cell 8:461–465. https://doi.org/10.1016/j.devcel.2005.03.014
Grill SW, Gönczy P, Stelzer EH, Hyman AA (2001) Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630–633. https://doi.org/10.1038/35054572
Grill SW, Howard J, Schäffer E et al (2003) The distribution of active force generators controls mitotic spindle position. Science 301:518–521. https://doi.org/10.1126/science.1086560
Guilgur LG, Prudêncio P, Ferreira T et al (2012) Drosophila aPKC is required for mitotic spindle orientation during symmetric division of epithelial cells. Development 139:503–513. https://doi.org/10.1242/dev.071027
Hao Y, Du Q, Chen X et al (2010) Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr Biol 20:1809–1818. https://doi.org/10.1016/j.cub.2010.09.032
Hasley A, Chavez S, Danilchik M et al (2017) Vertebrate embryonic cleavage pattern determination. Adv Exp Med Biol 953:117–171. https://doi.org/10.1007/978-3-319-46095-6_4
Heisenberg C-P, Bellaïche Y (2013) Forces in tissue morphogenesis and patterning. Cell 153:948–962. https://doi.org/10.1016/j.cell.2013.05.008
Hertwig O (1884) Untersuchungen zur Morphologie und Physiologie der Zelle: Das Problem der Befruchtung und der Isotropie des Eies, eine Theorie der Vererbung. Fischer
Hirashima T, Tanaka R, Yamaguchi M, Yoshida H (2018) The ABD on the nascent polypeptide and PH domain are required for the precise Anillin localization in Drosophila syncytial blastoderm. Sci Rep 8:12910. https://doi.org/10.1038/s41598-018-31106-0
Holy J, Schatten G (1991) Differential behavior of centrosomes in unequally dividing blastomeres during fourth cleavage of sea urchin embryos. J Cell Sci 98(Pt 3):423–431
Howard J, Garzon-Coral C (2017) Physical limits on the precision of mitotic spindle positioning by microtubule pushing forces. BioEssays 39:1700122. https://doi.org/10.1002/bies.201700122
Hudson C, Kawai N, Negishi T, Yasuo H (2013) β-catenin-driven binary fate specification segregates germ layers in ascidian embryos. Curr Biol. https://doi.org/10.1016/j.cub.2013.02.005
Ishihara K, Nguyen PA, Groen AC et al (2014) Microtubule nucleation remote from centrosomes may explain how asters span large cells. Proc Natl Acad Sci USA 111:17715–17722. https://doi.org/10.1073/pnas.1418796111
Ishii R, Shimizu T (1997) Equalization of unequal first cleavage in the Tubifex egg by introduction of an additional centrosome: implications for the absence of cortical mechanisms for mitotic spindle asymmetry. Dev Biol 189:49–56. https://doi.org/10.1006/dbio.1997.8653
Januschke J, Llamazares S, Reina J, Gonzalez C (2011) Drosophila neuroblasts retain the daughter centrosome. Nat Commun 2:243. https://doi.org/10.1038/ncomms1245
Januschke J, Reina J, Llamazares S et al (2013) Centrobin controls mother-daughter centriole asymmetry in Drosophila neuroblasts. Nat Cell Biol 15:241–248. https://doi.org/10.1038/ncb2671
Kaltschmidt JA, Davidson CM, Brown NH, Brand AH (2000) Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat Cell Biol 2:7–12. https://doi.org/10.1038/71323
Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119:447–456
Kondo T, Hayashi S (2013) Mitotic cell rounding accelerates epithelial invagination. Nature 494:125–129. https://doi.org/10.1038/nature11792
Kong D, Wolf F, Großhans J (2017) Forces directing germ-band extension in Drosophila embryos. Mech Dev 144:11–22. https://doi.org/10.1016/j.mod.2016.12.001
Korotkevich E, Niwayama R, Courtois A et al (2017) The apical domain is required and sufficient for the first lineage segregation in the mouse embryo. Dev Cell 40:235–247.e7. https://doi.org/10.1016/j.devcel.2017.01.006
Kotak S, Gönczy P (2013) Mechanisms of spindle positioning: cortical force generators in the limelight. Curr Opin Cell Biol 25:741–748. https://doi.org/10.1016/j.ceb.2013.07.008
Kumano G, Nishida H (2007) Ascidian embryonic development: an emerging model system for the study of cell fate specification in chordates. Dev Dyn 236:1732–1747. https://doi.org/10.1002/dvdy.21108
Kumano G, Takatori N, Negishi T et al (2011) A maternal factor unique to ascidians silences the germline via binding to P-TEFb and RNAP II regulation. Curr Biol 21:1308–1313. https://doi.org/10.1016/j.cub.2011.06.050
Kuroda R, Endo B, Abe M, Shimizu M (2009) Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails. Nature 462:790–794. https://doi.org/10.1038/nature08597
Kuroda R, Fujikura K, Abe M et al (2016) Diaphanous gene mutation affects spiral cleavage and chirality in snails. Sci Rep 6:34809. https://doi.org/10.1038/srep34809
Lemaire P (2009) Unfolding a chordate developmental program, one cell at a time: invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians. Dev Biol 332:48–60. https://doi.org/10.1016/j.ydbio.2009.05.540
Lydersen BK, Pettijohn DE (1980) Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human/hamster hybrid cell. Cell 22:489–499
Maître J-L, Turlier H, Illukkumbura R et al (2016) Asymmetric division of contractile domains couples cell positioning and fate specification. Nature 536:344–348. https://doi.org/10.1038/nature18958
McDougall A, Chenevert J, Pruliere G et al (2015) Centrosomes and spindles in ascidian embryos and eggs. Methods Cell Biol 129:317–339. https://doi.org/10.1016/bs.mcb.2015.03.006
Merdes A, Ramyar K, Vechio JD, Cleveland DW (1996) A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell 87:447–458. https://doi.org/10.1016/S0092-8674(00)81365-3
Minc N, Piel M (2012) Predicting division plane position and orientation. Trends Cell Biol 22:193–200. https://doi.org/10.1016/j.tcb.2012.01.003
Minc N, Burgess D, Chang F (2011) Influence of cell geometry on division-plane positioning. Cell 144:414–426. https://doi.org/10.1016/j.cell.2011.01.016
Negishi T, Takada T, Kawai N, Nishida H (2007) Localized PEM mRNA and protein are involved in cleavage-plane orientation and unequal cell divisions in ascidians. Curr Biol 17:1014–1025. https://doi.org/10.1016/j.cub.2007.05.047
Negishi T, Kumano G, Nishida H (2011) Polo-like kinase 1 is required for localization of posterior end mark protein to the centrosome-attracting body and unequal cleavages in ascidian embryos. Dev Growth Differ 53:76–87. https://doi.org/10.1111/j.1440-169X.2010.01231.x
Nelson BH, Weisblat DA (1992) Cytoplasmic and cortical determinants interact to specify ectoderm and mesoderm in the leech embryo. Development 115:103–115
Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30:675–686
Nishida H (1996) Vegetal egg cytoplasm promotes gastrulation and is responsible for specification of vegetal blastomeres in embryos of the ascidian Halocynthia roretzi. Development 122:1271–1279
Nishida H (2005) Specification of embryonic axis and mosaic development in ascidians. Dev Dyn 233:1177–1193. https://doi.org/10.1002/dvdy.20469
Nishida H, Sawada K (2001) macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409:724–729. https://doi.org/10.1038/35055568
Nishikata T, Hibino T, Nishida H (1999) The centrosome-attracting body, microtubule system, and posterior egg cytoplasm are involved in positioning of cleavage planes in the ascidian embryo. Dev Biol 209:72–85. https://doi.org/10.1006/dbio.1999.9244
Olivier N, Luengo-Oroz MA, Duloquin L et al (2010) Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy. Science 329:967–971. https://doi.org/10.1126/science.1189428
Parisi E, Filosa S, De Petrocellis B, Monroy A (1978) The pattern of cell division in the early development of the sea urchin, Paracentrotus lividus. Dev Biol 65:38–49
Peng CJ, Wikramanayake AH (2013) Differential regulation of disheveled in a novel vegetal cor tical domain in sea urchin eggs and embryos: implications for the localized activation of canonical Wnt signaling. PLoS One 8:e80693. https://doi.org/10.1371/journal.pone.0080693
Peng JC-F, Wang L, Wikramanayake AH (2017) Origins of anterior-posterior polarity by localized activation of Disheveled. Mol Reprod Dev 84:443. https://doi.org/10.1002/mrd.22839
Pierre A, Sallé J, Wühr M, Minc N (2016) Generic theoretical models to predict division patterns of cleaving embryos. Dev Cell 39:667–682. https://doi.org/10.1016/j.devcel.2016.11.018
Prodon F, Yamada L, Shirae-Kurabayashi M et al (2007) Postplasmic/PEM RNAs: a class of localized maternal mRNAs with multiple roles in cell polarity and development in ascidian embryos. Dev Dyn 236:1698–1715. https://doi.org/10.1002/dvdy.21109
Prodon F, Chenevert J, Hébras C et al (2010) Dual mechanism controls asymmetric spindle position in ascidian germ cell precursors. Development 137:2011–2021. https://doi.org/10.1242/dev.047845
Prulière G, Cosson J, Chevalier S et al (2011) Atypical protein kinase C controls sea urchin cilio genesis. Mol Biol Cell 22:2042–2053. https://doi.org/10.1091/mbc.E10-10-0844
Ragkousi K, Marr K, McKinney S et al (2017) Cell-cycle-coupled oscillations in apical polarity and intercellular contact maintain order in embryonic epithelia. Curr Biol 27:1381–1386. https://doi.org/10.1016/j.cub.2017.03.064
Redemann S, Pecreaux J, Goehring NW et al (2010) Membrane invaginations reveal cortical sites that pull on mitotic spindles in one-cell C. elegans embryos. PLoS One 5:e12301. https://doi.org/10.1371/journal.pone.0012301
Ren X, Weisblat DA (2006) Asymmetrization of first cleavage by transient disassembly of one spindle pole aster in the leech Helobdella robusta. Dev Biol 292:103–115. https://doi.org/10.1016/j.ydbio.2005.12.049
Robert A (1903) Sur le développement des Troches. Thesis, Faculté des Sciences de L’Université de Paris
Saadaoui M, Machicoane M, di Pietro F et al (2014) Dlg1 controls planar spindle orientation in the neuroepithelium through direct interaction with LGN. J Cell Biol 206:707–717. https://doi.org/10.1083/jcb.201405060
Sachs J (1878) Uber die Anordnung der Zellen in jungsten Pflanzentheilen. Arb Bot Inst Wurzburg 2:46–104
Sardet C, McDougall A, Houliston E (1994) Cytoplasmic domains in eggs. Trends Cell Biol 4:166–172
Savoian MS, Rieder CL (2002) Mitosis in primary cultures of Drosophila melanogaster larval neuroblasts. J Cell Sci 115:3061–3072
Schaefer M, Shevchenko A, Shevchenko A, Knoblich JA (2000) A protein complex containing inscuteable and the Gα-binding protein Pins orients asymmetric cell divisions in Drosophila. Curr Biol 10:353–362
Schroeder TE (1980) Expressions of the prefertilization polar axis in sea urchin eggs. Dev Biol 79:428–443
Shibazaki Y, Shimizu M, Kuroda R (2004) Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo. Curr Biol 14:1462–1467. https://doi.org/10.1016/j.cub.2004.08.018
Shimizu T, Ishii R, Takahashi H (1998) Unequal cleavage in the early Tubifex embryo. Dev Growth Differ 40:257–266
Siller KH, Doe CQ (2008) Lis1/dynactin regulates metaphase spindle orientation in Drosophila neuroblasts. Dev Biol 319:1–9. https://doi.org/10.1016/j.ydbio.2008.03.018
Siller KH, Doe CQ (2009) Spindle orientation during asymmetric cell division. Nat Cell Biol 11:365–374. https://doi.org/10.1038/ncb0409-365
Siller KH, Cabernard C, Doe CQ (2006) The NuMA-related mud protein binds Pins and regulates spindle orientation in Drosophila neuroblasts. Nat Cell Biol 8:594–600. https://doi.org/10.1038/ncb1412
Sobral D, Tassy O, Lemaire P (2009) Highly divergent gene expression programs can Lead to similar chordate larval body plans. Curr Biol 19:2014–2019. https://doi.org/10.1016/j.cub.2009.10.036
Stolfi A, Lowe EK, Racioppi C et al (2014) Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians. elife 3. https://doi.org/10.7554/eLife.03728
Takatori N, Kumano G, Saiga H, Nishida H (2010) Segregation of germ layer fates by nuclear migration-dependent localization of Not mRNA. Dev Cell 19:589–598. https://doi.org/10.1016/j.devcel.2010.09.003
Tassy O, Daian F, Hudson C et al (2006) A quantitative approach to the study of cell shapes and interactions during early chordate embryogenesis. Curr Biol 16:345–358. https://doi.org/10.1016/j.cub.2005.12.044
Théry M, Jiménez-Dalmaroni A, Racine V et al (2007) Experimental and theoretical study of mitotic spindle orientation. Nature 447:493–496. https://doi.org/10.1038/nature05786
Thompson DW (1942) On growth and form, new ed. Cambridge University Press/Macmillan, Cambridge/New York
Treen N, Heist T, Wang W, Levine M (2018) Depletion of maternal cyclin B3 contributes to zygotic genome activation in the ciona embryo. Curr Biol 28:1330–1331. https://doi.org/10.1016/j.cub.2018.03.058
Turlier H, Maître J-L (2015) Mechanics of tissue compaction. Semin Cell Dev Biol 47–48:110–117. https://doi.org/10.1016/j.semcdb.2015.08.001
von Sachs J (1887) Lecture XXVII. Relations between growth and cell-division in the embryonic tissues. Lectures in plant physiology. Clarendon, Oxford, 431–459
Voronina E, Wessel GM (2006) Activator of G-protein signaling in asymmetric cell divisions of the sea urchin embryo. Dev Growth Differ 48:549–557. https://doi.org/10.1111/j.1440-169X.2006.00895.x
Weitzel HE, Illies MR, Byrum CA et al (2004) Differential stability of beta-catenin along the animal-vegetal axis of the sea urchin embryo mediated by dishevelled. Development 131:2947–2956. https://doi.org/10.1242/dev.01152
Wieschaus E, Nüsslein-Volhard C (2014) Walter Gehring (1939–2014). Curr Biol 24:R632–R634. https://doi.org/10.1016/j.cub.2014.06.039
Wieschaus E, Nüsslein-Volhard C (2016) The Heidelberg screen for pattern mutants of drosophila: a personal account. Annu Rev Cell Dev Biol 32:1–46. https://doi.org/10.1146/annurev-cellbio-113015-023138
Wilson EB (1896, 1905, 1915) The cell in development and inheritance. Macmillan, London
Winklbauer R (2015) Cell adhesion strength from cortical tension – an integration of concepts. J Cell Sci 128:3687–3693. https://doi.org/10.1242/jcs.174623
Woolner S, Papalopulu N (2012) Spindle position in symmetric cell divisions during epiboly is controlled by opposing and dynamic apicobasal forces. Dev Cell 22:775–787. https://doi.org/10.1016/j.devcel.2012.01.002
Xiong F, Ma W, Hiscock TW et al (2014) Interplay of cell shape and division orientation promotes robust morphogenesis of developing epithelia. Cell 159:415–427. https://doi.org/10.1016/j.cell.2014.09.007
Yamamoto K, Kimura A (2017) An asymmetric attraction model for the diversity and robustness of cell arrangement in nematodes. Development 144:4437–4449. https://doi.org/10.1242/dev.154609
Yu F, Morin X, Cai Y et al (2000) Analysis of partner of inscuteable, a novel player of Drosophila asymmetric divisions, reveals two distinct steps in inscuteable apical localization. Cell 100:399–409
Acknowledgments
We would like to thank Zak Swartz for thoughtful comments that improved the manuscript. We would also like to thank the funding agencies that support our work: the French government funding agency Agence National de la Recherche (ANR “MorCell”: ANR-17-CE 13-0028) and Sorbonne University for supporting the Réseau André Picard. We also thank the CRBM of Institut de la Mer de Villefranche (IMEV) that is supported by EMBRC-France, whose French state funds are managed by the ANR within the Investments of the Future program under reference ANR-10-INBS-02.
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McDougall, A., Chenevert, J., Godard, B.G., Dumollard, R. (2019). Emergence of Embryo Shape During Cleavage Divisions. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_6
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