7 research outputs found
Evolutionarily Conserved Morphogenetic Movements At The Vertebrate Head-trunk Interface Coordinate The Transport And Assembly Of Hypopharyngeal Structures
The vertebrate head-trunk interface (occipital region) has been heavily remodelled during evolution, and its development is still poorly understood. In extant jawed vertebrates, this region provides muscle precursors for the throat and tongue (hypopharyngeal/hypobranchial/hypoglossal muscle precursors, HMP) that take a stereotype path rostrally along the pharynx and are thought to reach their target sites via active migration. Yet, this projection pattern emerged in jawless vertebrates before the evolution of migratory muscle precursors. This suggests that a so far elusive, more basic transport mechanism must have existed and may still be traceable today.Here we show for the first time that all occipital tissues participate in well-conserved cell movements. These cell movements are spearheaded by the occipital lateral mesoderm and ectoderm that split into two streams. The rostrally directed stream projects along the floor of the pharynx and reaches as far rostrally as the floor of the mandibular arch and outflow tract of the heart. Notably, this stream leads and engulfs the later emerging HMP, neural crest cells and hypoglossal nerve. When we (i) attempted to redirect hypobranchial/hypoglossal muscle precursors towards various attractants, (ii) placed non-migratory muscle precursors into the occipital environment or (iii) molecularly or (iv) genetically rendered muscle precursors non-migratory, they still followed the trajectory set by the occipital lateral mesoderm and ectoderm. Thus, we have discovered evolutionarily conserved morphogenetic movements, driven by the occipital lateral mesoderm and ectoderm, that ensure cell transport and organ assembly at the head-trunk interface. © 2014 The Authors.3902231246Ainsworth, S.J., Stanley, R.L., Evans, D.J., Developmental stages of the Japanese quail (2010) J Anat, 216, pp. 3-15Alvares, L.E., Schubert, F.R., Thorpe, C., Mootoosamy, R.C., Cheng, L., Parkyn, G., Lumsden, A., Dietrich, S., Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors (2003) Dev. Cell, 5, pp. 379-390Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A., Birchmeier, C., Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud (1995) Nature, 376, pp. 768-771Blentic, A., Tandon, P., Payton, S., Walshe, J., Carney, T., Kelsh, R.N., Mason, I., Graham, A., The emergence of ectomesenchyme (2008) Dev. Dyn., 237, pp. 592-601Bothe, I., Dietrich, S., The molecular setup of the avian head mesoderm and its implication for craniofacial myogenesis (2006) Dev. Dyn., 235, pp. 2845-2860Brohmann, H., Jagla, K., Birchmeier, C., The role of Lbx1 in migration of muscle precursor cells (2000) Development, 127, pp. 437-445Cheng, L., Alvares, L.E., Ahmed, M.U., El-Hanfy, A.S., Dietrich, S., The epaxial-hypaxial subdivision of the avian somite (2004) Dev. Biol., 274, pp. 348-369Cole, N.J., Hall, T.E., Don, E.K., Berger, S., Boisvert, C.A., Neyt, C., Ericsson, R., Currie, P.D., Development and evolution of the muscles of the pelvic fin (2011) PLoS Biol., 9, pp. e1001168Couly, G.F., Coltey, P.M., Le Douarin, N.M., The triple origin of skull in higher vertebrates: a study in quail-chick chimeras (1993) Development, 117, pp. 409-429Dietrich, S., Abou-Rebyeh, F., Brohmann, H., Bladt, F., Sonnenberg-Riethmacher, E., Yamaai, T., Lumsden, A., Birchmeier, C., The role of SF/HGF and c-Met in the development of skeletal muscle (1999) Development, 126, pp. 1621-1629Dietrich, S., Schubert, F.R., Healy, C., Sharpe, P.T., Lumsden, A., Specification of the hypaxial musculature (1998) Development, 125, pp. 2235-2249Dietrich, S., Schubert, F.R., Lumsden, A., Control of dorsoventral pattern in the chick paraxial mesoderm (1997) Development, 124, pp. 3895-3908Diogo, R., Hinits, Y., Hughes, S.M., Development of mandibular, hyoid and hypobranchial muscles in the zebrafish: homologies and evolution of these muscles within bony fishes and tetrapods (2008) BMC Dev. Biol., 8, p. 24Edgeworth, F.H., The development of the head muscles in Gallus domesticus, and the morphology of the head muscles in the Sauropsida (1907) Q. J. Microsc. Sci., 52, pp. 511-556Edgeworth, F.H., (1935) The Cranial Muscles of Vertebrates, , Cambridge University Press, CambridgeEricsson, R., Knight, R., Johanson, Z., Evolution and development of the vertebrate neck (2013) J. Anat., 222, pp. 67-78Ferguson, C.A., Graham, A., Redefining the head-trunk interface for the neural crest (2004) Dev. Biol., 269, pp. 70-80Franz, T., The Splotch (Sp1H) and Splotch-delayed (Spd) alleles: differential phenotypic effects on neural crest and limb musculature (1993) Anat. Embryol. (Berl.), 187, pp. 371-377Franz, T., Kothary, R., Surani, M.A.H., Halata, Z., Grim, M., The Splotch mutation interferes with muscle development in the limbs (1993) Anat. Embryol., 187, pp. 153-160Gans, C., Northcutt, R.G., Neural crest and the origin of vertebrates: a new head (1983) Science, 220, pp. 268-274Gilbert, S.F., (2000) Developmental Biology, , Sinauer Associates Inc., Sunderland, MAGoodrich, E.S., (1958) Studies on the Structure and Development of Vertebrates, , Dover Publications Inc., New YorkGoulding, M.D., Lumsden, A., Gruss, P., Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord (1993) Development, 117, pp. 1001-1016Gross, M.K., Moran-Rivard, L., Velasquez, T., Nakatsu, M.N., Jagla, K., Goulding, M., Lbx1 is required for muscle precursor migration along a lateral pathway into the limb (2000) Development, 127, pp. 413-424Gurdon, J.B., Methods for nuclear transplantation in amphibia (1977) Methods Cell Biol., 16, pp. 125-139Hamburger, V., Hamilton, H.L., A series of normal stages in the development of the chick embryo (1951) J. Morphol., 88, pp. 49-92Han, D., Zhao, H., Parada, C., Hacia, J.G., Bringas, P., Chai, Y., A TGFbeta-Smad4-Fgf6 signaling cascade controls myogenic differentiation and myoblast fusion during tongue development (2012) Development, 139, pp. 1640-1650Harland, R.M., In situ hybridization: an improved whole-mount method for Xenopus embryos (1991) Methods Cell Biol., 36, pp. 685-695Hirano, S., Tanaka, H., Ohta, K., Norita, M., Hoshino, K., Meguro, R., Kase, M., Normal ontogenic observations on the expression of Eph receptor tyrosine kinase, Cek8, in chick embryos (1998) Anat. Embryol. (Berl.), 197, pp. 187-197Hosokawa, R., Oka, K., Yamaza, T., Iwata, J., Urata, M., Xu, X., Bringas, P., Chai, Y., TGF-beta mediated FGF10 signaling in cranial neural crest cells controls development of myogenic progenitor cells through tissue-tissue interactions during tongue morphogenesis (2010) Dev. Biol., 341, pp. 186-195Huang, R., Zhi, Q., Izpisua-Belmonte, J.C., Christ, B., Patel, K., Origin and development of the avian tongue muscles (1999) Anat. Embryol. (Berl.), 200, pp. 137-152Huang, R., Zhi, Q., Patel, K., Wilting, J., Christ, B., Contribution of single somites to the skeleton and muscles of the occipital and cervical regions in avian embryos (2000) Anat. Embryol. (Berl.), 202, pp. 375-383Kallius, E., Beitráge zur entwickelung der zunge. Teil I. Amphibien und reptilien (1901) Anat. Hefte, Abt., 1 (16), pp. 531-760Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., Schilling, T.F., Stages of embryonic development of the zebrafish (1995) Dev. Dyn., 203, pp. 253-310Kuo, B.R., Erickson, C.A., Vagal neural crest cell migratory behavior: a transition between the cranial and trunk crest (2011) Dev. Dyn., 240, pp. 2084-2100Kuratani, S., Horigome, N., Hirano, S., Developmental morphology of the head mesoderm and reevaluation of segmental theories of the vertebrate head: evidence from embryos of an agnathan vertebrate, Lampetra japonica (1999) Dev. Biol., 210, pp. 381-400Kuratani, S.C., Kirby, M.L., Migration and distribution of circumpharyngeal crest cells in the chick embryo. Formation of the circumpharyngeal ridge and E/C8+ crest cells in the vertebrate head region (1992) Anat. Rec., 234, pp. 263-280Kusakabe, R., Kuraku, S., Kuratani, S., Expression and interaction of muscle-related genes in the lamprey imply the evolutionary scenario for vertebrate skeletal muscle, in association with the acquisition of the neck and fins (2011) Dev. Biol., 350, pp. 217-227Kusakabe, R., Kuratani, S., Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey (2005) Dev. Dyn., 234, pp. 824-834Latinkic, B.V., Cooper, B., Towers, N., Sparrow, D., Kotecha, S., Mohun, T.J., Distinct enhancers regulate skeletal and cardiac muscle-specific expression programs of the cardiac alpha-actin gene in Xenopus embryos (2002) Dev. Biol., 245, pp. 57-70Lours, C., Dietrich, S., The dissociation of the Fgf-feedback loop controls the limbless state of the neck (2005) Development, 132, pp. 5553-5564Mackenzie, S., Walsh, F.S., Graham, A., Migration of hypoglossal myoblast precursors (1998) Dev. Dyn., 213, pp. 349-358Maina, F., Casagranda, F., Audero, E., Simeone, A., Comoglio, P.M., Klein, R., Ponzetto, C., Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development (1996) Cell, 87, pp. 531-542Manner, J., Seidl, W., Steding, G., Correlation between the embryonic head flexures and cardiac development. An experimental study in chick embryos (1993) Anat. Embryol. (Berl.), 188, pp. 269-285Martin, B.L., Harland, R.M., A novel role for lbx1 in Xenopus hypaxial myogenesis (2006) Development, 133, pp. 195-208Merrell, A.J., Kardon, G., Development of the diaphragm - a skeletal muscle essential for mammalian respiration (2013) FEBS J., 280, pp. 4026-4035Mootoosamy, R.C., Dietrich, S., Distinct regulatory cascades for head and trunk myogenesis (2002) Development, 129, pp. 573-583Neal, H.V., Development of the hypoglossus musculature in Petromyzon and Squalus (1897) Anat. Anz., 13, pp. 441-463Neyt, C., Jagla, K., Thisse, C., Thisse, B., Haines, L., Currie, P.D., Evolutionary origins of vertebrate appendicular muscle (2000) Nature, 408, pp. 82-86Nieuwkoop, P.D., Faber, J., (1994) Normal Table of Xenopus laevis, , Garland Publishing Inc., New York, (Daudin) (Ed.)Noden, D.M., The embryonic origins of avian cephalic and cervical muscles and associated connective tissues (1983) Am. J. Anat., 168, pp. 257-276Noden, D.M., Francis-West, P., The differentiation and morphogenesis of craniofacial muscles (2006) Dev. Dyn., 235, pp. 1194-1218Ochi, H., Westerfield, M., Lbx2 regulates formation of myofibrils (2009) BMC Dev. Biol., 9, p. 13Prunotto, C., Crepaldi, T., Forni, P.E., Ieraci, A., Kelly, R.G., Tajbakhsh, S., Buckingham, M., Ponzetto, C., Analysis of Mlc-lacZ Met mutants highlights the essential function of Met for migratory precursors of hypaxial muscles and reveals a role for Met in the development of hyoid arch-derived facial muscles (2004) Dev. Dyn., 231, pp. 582-591Qu, S., Tucker, S.C., Zhao, Q., deCrombrugghe, B., Wisdom, R., Physical and genetic interactions between Alx4 and Cart1 (1999) Development, 126, pp. 359-369Ramel, D., Wang, X., Laflamme, C., Montell, D.J., Emery, G., Rab11 regulates cell-cell communication during collective cell movements (2013) Nat Cell Biol, 15, pp. 317-324Sabo, M.C., Nath, K., Elinson, R.P., Lbx1 expression and frog limb development (2010) Dev. Genes Evol.Schäfer, K., Braun, T., Early specification of limb muscle precursor cells by the homeobox gene Lbx1h (1999) Nat. Genet., 23, pp. 213-216Schubert, F.R., Mootoosamy, R.C., Walters, E.H., Graham, A., Tumiotto, L., Munsterberg, A.E., Lumsden, A., Dietrich, S., Wnt6 marks sites of epithelial transformations in the chick embryo (2002) Mech. Dev., 114, pp. 143-148Šošic, D., Brand-Saberi, B., Schmidt, C., Christ, B., Olson, E.N., Regulation of paraxis expression and somite formation by ectoderm- and neural tube-derived signals (1997) Dev. Biol., 185, pp. 229-243Takahashi, M., Tamura, K., Buscher, D., Masuya, H., Yonei-Tamura, S., Matsumoto, K., Naitoh-Matsuo, M., Shiroishi, T., The role of Alx-4 in the establishment of anteroposterior polarity during vertebrate limb development (1998) Development, 125, pp. 4417-4425Thisse, B., Heyer, V., Lux, A., Alunni, V., Degrave, A., Seiliez, I., Kirchner, J., Thisse, C., Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening (2004) Methods Cell Biol., 77, pp. 505-519Tremblay, P., Dietrich, S., Meriskay, M., Schubert, F.R., Li, Z., Paulin, D., A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors (1998) Dev. Biol., 203, pp. 49-61Vasyutina, E., Stebler, J., Brand-Saberi, B., Schulz, S., Raz, E., Birchmeier, C., CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells (2005) Genes Dev., 19, pp. 2187-2198Wachtler, F., Jacob, M., Origin and development of the cranial skeletal muscles (1986) Bibl. Anat., 29, pp. 24-46Zhu, M., Yu, X., Ahlberg, P.E., Choo, B., Lu, J., Qiao, T., Qu, Q., Blom, H., A Silurian placoderm with osteichthyan-like marginal jaw bones (2013) Nature, 502, pp. 188-19
Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures
The vertebrate head trunk interface (occipital region) has been heavily remodelled during evolution, and its development is still poorly understood. In extant jawed vertebrates, this region provides muscle precursors for the throat and tongue (hypopharyngeal/hypobranchial/hypoglossal muscle precursors, HMP) that take a stereotype path rostrally along the pharynx and are thought to reach their target sites via active migration. Yet, this projection pattern emerged in jawless vertebrates before the evolution of migratory muscle precursors. This suggests that a so far elusive, more basic transport mechanism must have existed and may still be traceable today. Here we show for the first time that all occipital tissues participate in well-conserved cell movements. These cell movements are spearheaded by the occipital lateral mesoderm and ectoderm that split into two streams. The rostrally directed stream projects along the floor of the pharynx and reaches as far rostrally as the floor of the mandibular arch and outflow tract of the heart. Notably, this stream leads and engulfs the later emerging HMP, neural crest cells and hypoglossal nerve. When we (i) attempted to redirect hypobranchial/hypoglossal muscle precursors towards various attractants, (ii) placed non-migratory muscle precursors into the occipital environment or (iii) molecularly or (iv) genetically rendered muscle precursors non-migratory, they still followed the trajectory set by the occipital lateral mesoderm and ectoderm. Thus, we have discovered evolutionarily conserved morphogenetic movements, driven by the occipital lateral mesoderm and ectoderm, that ensure cell transport and organ assembly at the head trunk interface3902231246FUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP2006/05892-3Guy's and St. Thomas' Charitable Foundation; Biotechnology and Biological Sciences Research Council (BBSRC); European Union (EU); UoP Faculty of Scienc
Stakeholders’ expectations in utilising financial models for public-private partnership projects
International audienceThe vertebrate head-trunk interface (occipital region) has been heavily remodelled during evolution, and its development is still poorly understood. In extant jawed vertebrates, this region provides muscle precursors for the throat and tongue (hypopharyngeal/hypobranchial/hypoglossal muscle precursors, HMP) that take a stereotype path rostrally along the pharynx and are thought to reach their target sites via active migration. Yet, this projection pattern emerged in jawless vertebrates before the evolution of migratory muscle precursors. This suggests that a so far elusive, more basic transport mechanism must have existed and may still be traceable today. Here we show for the first time that all occipital tissues participate in well-conserved cell movements. These cell movements are spearheaded by the occipital lateral mesoderm and ectoderm that split into two streams. The rostrally directed stream projects along the floor of the pharynx and reaches as far rostrally as the floor of the mandibular arch and outflow tract of the heart. Notably, this stream leads and engulfs the later emerging HMP, neural crest cells and hypoglossal nerve. When we (i) attempted to redirect hypobranchial/hypoglossal muscle precursors towards various attractants, (ii) placed non-migratory muscle precursors into the occipital environment or (iii) molecularly or (iv) genetically rendered muscle precursors non-migratory, they still followed the trajectory set by the occipital lateral mesoderm and ectoderm. Thus, we have discovered evolutionarily conserved morphogenetic movements, driven by the occipital lateral mesoderm and ectoderm, that ensure cell transport and organ assembly at the head-trunk interface