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Published in: Brain Structure and Function 3/2016

01-04-2016 | Original Article

Genoarchitecture of the rostral hindbrain of a shark: basis for understanding the emergence of the cerebellum at the agnathan–gnathostome transition

Authors: Sol Pose-Méndez, Eva Candal, Sylvie Mazan, Isabel Rodríguez-Moldes

Published in: Brain Structure and Function | Issue 3/2016

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Abstract

The cerebellum is present in all extant gnathostomes or jawed vertebrates, of which cartilaginous fishes represent the most ancient radiation. Since the isthmic organizer induces the formation of the cerebellum, comparative genoarchitectonic analysis on the meso-isthmo-cerebellar region of cartilaginous fishes with respect to that of jawless vertebrates could reveal why the isthmic organizer acquires the ability to induce the formation of the cerebellum in gnathostomes. In the present work we analyzed the expression pattern of a variety of genes related to the cerebellar formation and patterning (ScOtx2, ScGbx2, ScFgf8, ScLmx1b, ScIrx1, ScIrx3, ScEn2, ScPax6 and ScLhx9) by in situ hybridization, and the distribution of Pax6 protein in the developing hindbrain of the shark Scyliorhinus canicula. The genoarchitectonic code in this species revealed high degree of conservation with respect to that of other gnathostomes. This resemblance may reveal the features of the ancestral condition of the gene network operating for specification of the rostral hindbrain patterning. Accordingly, the main subdivisions of the rostral hindbrain of S. canicula could be recognized. Our results support the existence of a rhombomere 0, identified as the ScFgf8/ScGbx2/ScEn2-positive and mainly negative ScIrx3 domain just caudal to the midbrain ScIrx1/ScOtx2/ScLmx1b-positive domain. The differential ScEn2 and Pax6 expression in the rhombomere 1 revealed anterior and posterior subdivisions. Interestingly, dissimilarities between S. canicula and lampreys (jawless vertebrates) were noted in the expression of Irx, Lhx and Pax genes, which could be part of significant gene network changes through evolution that caused the emergence of the cerebellum.
Literature
go back to reference Adachi N, Takechi M, Hirai T, Kuratani S (2012) Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head. Evol Dev 14:257–276PubMedCrossRef Adachi N, Takechi M, Hirai T, Kuratani S (2012) Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head. Evol Dev 14:257–276PubMedCrossRef
go back to reference Adams KA, Maida JM, Golden JA, Riddle RD (2000) The transcription factor Lmx1b maintains Wnt1 expression within the isthmic organizer. Development 127:1857–1867PubMed Adams KA, Maida JM, Golden JA, Riddle RD (2000) The transcription factor Lmx1b maintains Wnt1 expression within the isthmic organizer. Development 127:1857–1867PubMed
go back to reference Alonso A, Merchán P, Sandoval JE, Sánchez-Arrones L, Garcia-Cazorla A, Artuch R, Ferrán JL, Martínez-de-la-Torre M, Puelles L (2013) Development of the serotonergic cells in murine raphe nuclei and their relations with rhombomeric domains. Brain Struct Funct 218:1229–1277PubMedPubMedCentralCrossRef Alonso A, Merchán P, Sandoval JE, Sánchez-Arrones L, Garcia-Cazorla A, Artuch R, Ferrán JL, Martínez-de-la-Torre M, Puelles L (2013) Development of the serotonergic cells in murine raphe nuclei and their relations with rhombomeric domains. Brain Struct Funct 218:1229–1277PubMedPubMedCentralCrossRef
go back to reference Aroca P, Puelles L (2005) Postulated boundaries and differential fate in the developing rostral hindbrain. Brain Res Rev 49:179–190PubMedCrossRef Aroca P, Puelles L (2005) Postulated boundaries and differential fate in the developing rostral hindbrain. Brain Res Rev 49:179–190PubMedCrossRef
go back to reference Ballard WW, Mellinger J, Lechenault H (1993) A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318–336CrossRef Ballard WW, Mellinger J, Lechenault H (1993) A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318–336CrossRef
go back to reference Bellefroid EJ, Kobbe A, Gruss P, Pieler T, Gurdon JB, Papalopulu N (1998) Xiro3 encodes a Xenopus homolog of the Drosophila Iroquois genes and functions in neural specification. EMBO J 17:191–203PubMedPubMedCentralCrossRef Bellefroid EJ, Kobbe A, Gruss P, Pieler T, Gurdon JB, Papalopulu N (1998) Xiro3 encodes a Xenopus homolog of the Drosophila Iroquois genes and functions in neural specification. EMBO J 17:191–203PubMedPubMedCentralCrossRef
go back to reference Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275–2284PubMedCrossRef Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275–2284PubMedCrossRef
go back to reference Bosse A, Zülch A, Becker MB, Torres M, Gómez-Skarmeta JL, Modolell J, Gruss P (1997) Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech Dev 69:169–181PubMedCrossRef Bosse A, Zülch A, Becker MB, Torres M, Gómez-Skarmeta JL, Modolell J, Gruss P (1997) Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech Dev 69:169–181PubMedCrossRef
go back to reference Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36PubMedCrossRef Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36PubMedCrossRef
go back to reference Cheng CW, Hui C, Strähle U, Cheng SH (2001) Identification and expression of zebrafish Iroquois homeobox gene irx1. Dev Genes Evol 211:442–444PubMedCrossRef Cheng CW, Hui C, Strähle U, Cheng SH (2001) Identification and expression of zebrafish Iroquois homeobox gene irx1. Dev Genes Evol 211:442–444PubMedCrossRef
go back to reference Cheng CW, Yan CH, Choy SW, Hui MN, Hui CC, Cheng SH (2007) Zebrafish homologue irx1a is required for the differentiation of serotonergic neurons. Dev Dyn 236:2661–2667PubMedCrossRef Cheng CW, Yan CH, Choy SW, Hui MN, Hui CC, Cheng SH (2007) Zebrafish homologue irx1a is required for the differentiation of serotonergic neurons. Dev Dyn 236:2661–2667PubMedCrossRef
go back to reference Chizhikov VV, Millen KJ (2004) Control of roof plate development and signaling by Lmx1b in the caudal vertebrate CNS. J Neurosci 24:5694–56703PubMedCrossRef Chizhikov VV, Millen KJ (2004) Control of roof plate development and signaling by Lmx1b in the caudal vertebrate CNS. J Neurosci 24:5694–56703PubMedCrossRef
go back to reference Cohen DR, Cheng CW, Cheng SH, Hui CC (2000) Expression of two novel mouse Iroquois homeobox genes during neurogenesis. Mech Dev 91:317–321PubMedCrossRef Cohen DR, Cheng CW, Cheng SH, Hui CC (2000) Expression of two novel mouse Iroquois homeobox genes during neurogenesis. Mech Dev 91:317–321PubMedCrossRef
go back to reference Compagnucci C, Debiais-Thibaud M, Coolen M, Fish J, Griffin JN, Bertocchini F, Minoux M, Rijli FM, Borday-Birraux V, Casane D, Mazan S, Depew MJ (2013) Pattern and polarity in the development and evolution of the gnathostome jaw: both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Dev Biol 377:428–448PubMedCrossRef Compagnucci C, Debiais-Thibaud M, Coolen M, Fish J, Griffin JN, Bertocchini F, Minoux M, Rijli FM, Borday-Birraux V, Casane D, Mazan S, Depew MJ (2013) Pattern and polarity in the development and evolution of the gnathostome jaw: both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Dev Biol 377:428–448PubMedCrossRef
go back to reference Coolen M, Sauka-Spengler T, Nicolle D, Le-Mentec C, Lallemand Y, Da Silva C, Plouhinec JL, Robert B, Wincker P, Shi DL, Mazan S (2007) Evolution of axis specification mechanisms in jawed vertebrates: insights from a chondrichthyan. PLoS ONE 2:e374PubMedPubMedCentralCrossRef Coolen M, Sauka-Spengler T, Nicolle D, Le-Mentec C, Lallemand Y, Da Silva C, Plouhinec JL, Robert B, Wincker P, Shi DL, Mazan S (2007) Evolution of axis specification mechanisms in jawed vertebrates: insights from a chondrichthyan. PLoS ONE 2:e374PubMedPubMedCentralCrossRef
go back to reference Coolen M, Menuet A, Chassoux D, Compagnucci C, Henry S, Lévèque L, Da Silva C, Gavory F, Samain S, Wincker P, Thermes C, D’Aubenton-Carafa Y, Rodriguez-Moldes I, Naylor G, Depew M, Sourdaine P, Mazan S (2009) The dogfish Scyliorhinus canicula, a reference in jawed vertebrates. In: Behringer RR, Johnson AD, Krumlauf RE (eds) Emerging model organisms. A laboratory manual, vol 1. CSHL Press, Cold Spring Harbor, pp 431–446 Coolen M, Menuet A, Chassoux D, Compagnucci C, Henry S, Lévèque L, Da Silva C, Gavory F, Samain S, Wincker P, Thermes C, D’Aubenton-Carafa Y, Rodriguez-Moldes I, Naylor G, Depew M, Sourdaine P, Mazan S (2009) The dogfish Scyliorhinus canicula, a reference in jawed vertebrates. In: Behringer RR, Johnson AD, Krumlauf RE (eds) Emerging model organisms. A laboratory manual, vol 1. CSHL Press, Cold Spring Harbor, pp 431–446
go back to reference Ferreiro-Galve S, Candal E, Rodríguez-Moldes I (2012a) Dynamic expression of Pax6 in the shark olfactory system: evidence for the presence of Pax6 cells along the olfactory nerve pathway. J Exp Zool B (Mol Dev Evol) 318:79–90CrossRef Ferreiro-Galve S, Candal E, Rodríguez-Moldes I (2012a) Dynamic expression of Pax6 in the shark olfactory system: evidence for the presence of Pax6 cells along the olfactory nerve pathway. J Exp Zool B (Mol Dev Evol) 318:79–90CrossRef
go back to reference Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2012b) Pax6 expression during retinogenesis in sharks: comparison with markers of cell proliferation and neuronal differentiation. J Exp Zool (Mol Dev Evol) 318:91–108CrossRef Ferreiro-Galve S, Rodríguez-Moldes I, Candal E (2012b) Pax6 expression during retinogenesis in sharks: comparison with markers of cell proliferation and neuronal differentiation. J Exp Zool (Mol Dev Evol) 318:91–108CrossRef
go back to reference Germot A, Lecointre G, Plouhinec JL, Le Mentec C, Girardot F, Mazan S (2001) Structural evolution of Otx genes in craniates. Mol Biol Evol 18:1668–1678PubMedCrossRef Germot A, Lecointre G, Plouhinec JL, Le Mentec C, Girardot F, Mazan S (2001) Structural evolution of Otx genes in craniates. Mol Biol Evol 18:1668–1678PubMedCrossRef
go back to reference Glavic A, Gómez-Skarmeta JL, Mayor R (2002) The homeoprotein Xiro1 is required for midbrain–hindbrain boundary formation. Development 129:1609–1621PubMed Glavic A, Gómez-Skarmeta JL, Mayor R (2002) The homeoprotein Xiro1 is required for midbrain–hindbrain boundary formation. Development 129:1609–1621PubMed
go back to reference Gómez-Skarmeta JL, Modolell J (2002) Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev 12:403–408PubMedCrossRef Gómez-Skarmeta JL, Modolell J (2002) Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev 12:403–408PubMedCrossRef
go back to reference Green MJ, Myat AM, Emmenegger BA, Wechsler-Reya RJ, Wilson LJ, Wingate RJ (2014) Independently specified Atoh1 domains define novel developmental compartments in rhombomere 1. Development 141:389–398PubMedPubMedCentralCrossRef Green MJ, Myat AM, Emmenegger BA, Wechsler-Reya RJ, Wilson LJ, Wingate RJ (2014) Independently specified Atoh1 domains define novel developmental compartments in rhombomere 1. Development 141:389–398PubMedPubMedCentralCrossRef
go back to reference Guo C, Qiu HY, Huang Y, Chen H, Yang RQ, Chen SD, Johnson RL, Chen ZF, Ding YQ (2007) Lmx1b is essential for Fgf8 and Wnt1 expression in the isthmic organizer during tectum and cerebellum development in mice. Development 134:317–325PubMedCrossRef Guo C, Qiu HY, Huang Y, Chen H, Yang RQ, Chen SD, Johnson RL, Chen ZF, Ding YQ (2007) Lmx1b is essential for Fgf8 and Wnt1 expression in the isthmic organizer during tectum and cerebellum development in mice. Development 134:317–325PubMedCrossRef
go back to reference Haldin CE, Nijjar S, Massé K, Barnett MW, Jones EA (2003) Isolation and growth factor inducibility of the Xenopus laevis Lmx1b gene. Int J Dev Biol 47:253–262PubMed Haldin CE, Nijjar S, Massé K, Barnett MW, Jones EA (2003) Isolation and growth factor inducibility of the Xenopus laevis Lmx1b gene. Int J Dev Biol 47:253–262PubMed
go back to reference Hammond KL, Baxendale S, McCauley DW, Ingham PW, Whitfield TT (2009) Expression of patched, prdm1 and engrailed in the lamprey somite reveals conserved responses to Hedgehog signaling. Evol Dev 11:27–40PubMedCrossRef Hammond KL, Baxendale S, McCauley DW, Ingham PW, Whitfield TT (2009) Expression of patched, prdm1 and engrailed in the lamprey somite reveals conserved responses to Hedgehog signaling. Evol Dev 11:27–40PubMedCrossRef
go back to reference Hidalgo-Sánchez M, Millet S, Simeone A, Alvarado-Mallart RM (1999) Comparative analysis of Otx2, Gbx2, Pax2, Fgf8 and Wnt1 gene expressions during the formation of the chick midbrain/hindbrain domain. Mech Dev 81:175–178PubMedCrossRef Hidalgo-Sánchez M, Millet S, Simeone A, Alvarado-Mallart RM (1999) Comparative analysis of Otx2, Gbx2, Pax2, Fgf8 and Wnt1 gene expressions during the formation of the chick midbrain/hindbrain domain. Mech Dev 81:175–178PubMedCrossRef
go back to reference Hidalgo-Sánchez M, Millet S, Bloch-Gallego E, Alvarado-Mallart RM (2005a) Specification of the meso-isthmo-cerebellar region: the Otx2/Gbx2 boundary. Brain Res Rev 49:134–149PubMedCrossRef Hidalgo-Sánchez M, Millet S, Bloch-Gallego E, Alvarado-Mallart RM (2005a) Specification of the meso-isthmo-cerebellar region: the Otx2/Gbx2 boundary. Brain Res Rev 49:134–149PubMedCrossRef
go back to reference Hidalgo-Sánchez M, Martínez de la Torre M, Alvarado-Mallart RM, Puelles L (2005b) A distinct preisthmic histogenetic domain is defined by overlap of Otx2 and Pax2 gene expression in the avian caudal midbrain. J Comp Neurol 483:17–29PubMedCrossRef Hidalgo-Sánchez M, Martínez de la Torre M, Alvarado-Mallart RM, Puelles L (2005b) A distinct preisthmic histogenetic domain is defined by overlap of Otx2 and Pax2 gene expression in the avian caudal midbrain. J Comp Neurol 483:17–29PubMedCrossRef
go back to reference Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H (2003) An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 130:2365–2373PubMedCrossRef Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H (2003) An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 130:2365–2373PubMedCrossRef
go back to reference Holland LZ (2013) Evolution of new characters after whole genome duplications: insights from amphioxus. Semin Cell Dev Biol 24:101–109PubMedCrossRef Holland LZ (2013) Evolution of new characters after whole genome duplications: insights from amphioxus. Semin Cell Dev Biol 24:101–109PubMedCrossRef
go back to reference Holland LZ, Short S (2008) Gene duplication, co-option and recruitment during the origin of the vertebrate brain from the invertebrate chordate brain. Brain Behav Evol 72:91–105PubMedCrossRef Holland LZ, Short S (2008) Gene duplication, co-option and recruitment during the origin of the vertebrate brain from the invertebrate chordate brain. Brain Behav Evol 72:91–105PubMedCrossRef
go back to reference Holland LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK (2013) Evolution of bilaterian central nervous systems: a single origin? EvoDevo 4:27PubMedPubMedCentralCrossRef Holland LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK (2013) Evolution of bilaterian central nervous systems: a single origin? EvoDevo 4:27PubMedPubMedCentralCrossRef
go back to reference Ikuta T, Saiga H (2007) Dynamic change in the expression of developmental genes in the ascidian central nervous system: revisit to the tripartite model and the origin of the midbrain–hindbrain boundary region. Dev Biol 312:631–643PubMedCrossRef Ikuta T, Saiga H (2007) Dynamic change in the expression of developmental genes in the ascidian central nervous system: revisit to the tripartite model and the origin of the midbrain–hindbrain boundary region. Dev Biol 312:631–643PubMedCrossRef
go back to reference Inoue F, Parvin MS, Yamasu K (2008) Transcription of fgf8 is regulated by activating and repressive cis-elements at the midbrain–hindbrain boundary in zebrafish embryos. Dev Biol 316:471–486PubMedCrossRef Inoue F, Parvin MS, Yamasu K (2008) Transcription of fgf8 is regulated by activating and repressive cis-elements at the midbrain–hindbrain boundary in zebrafish embryos. Dev Biol 316:471–486PubMedCrossRef
go back to reference Irimia M, Piñeiro C, Maeso I, Gómez-Skarmeta JL, Casares F, García-Fernández J (2010) Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizar. EvoDevo 1:7PubMedPubMedCentralCrossRef Irimia M, Piñeiro C, Maeso I, Gómez-Skarmeta JL, Casares F, García-Fernández J (2010) Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizar. EvoDevo 1:7PubMedPubMedCentralCrossRef
go back to reference Janvier P (2008) The brain in the early fossil jawless vertebrates: evolutionary information from an empty nutshell. Brain Res Bull 75:314–318PubMedCrossRef Janvier P (2008) The brain in the early fossil jawless vertebrates: evolutionary information from an empty nutshell. Brain Res Bull 75:314–318PubMedCrossRef
go back to reference Jászai J, Reifers F, Picker A, Langenberg T, Brand M (2003) Isthmus-to-midbrain transformation in the absence of midbrain–hindbrain organizer activity. Development 130:6611–6623PubMedCrossRef Jászai J, Reifers F, Picker A, Langenberg T, Brand M (2003) Isthmus-to-midbrain transformation in the absence of midbrain–hindbrain organizer activity. Development 130:6611–6623PubMedCrossRef
go back to reference Jiménez-Guri E, Pujades C (2011) An ancient mechanism of hindbrain patterning has been conserved in vertebrate evolution. Evol Dev 13:38–46PubMedCrossRef Jiménez-Guri E, Pujades C (2011) An ancient mechanism of hindbrain patterning has been conserved in vertebrate evolution. Evol Dev 13:38–46PubMedCrossRef
go back to reference Joyner AL, Liu A, Millet S (2000) Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr Opin Cell Biol 12:736–741PubMedCrossRef Joyner AL, Liu A, Millet S (2000) Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr Opin Cell Biol 12:736–741PubMedCrossRef
go back to reference Kikuta H, Kanai M, Ito Y, Yamasu K (2003) gbx2 Homeobox gene is required for the maintenance of the isthmic region in the zebrafish embryonic brain. Dev Dyn 228:433–450PubMedCrossRef Kikuta H, Kanai M, Ito Y, Yamasu K (2003) gbx2 Homeobox gene is required for the maintenance of the isthmic region in the zebrafish embryonic brain. Dev Dyn 228:433–450PubMedCrossRef
go back to reference Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310PubMedCrossRef Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310PubMedCrossRef
go back to reference Kobayashi D, Kobayashi M, Matsumoto K, Ogura T, Nakafuku M, Shimamura K (2002) Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129:83–93PubMed Kobayashi D, Kobayashi M, Matsumoto K, Ogura T, Nakafuku M, Shimamura K (2002) Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129:83–93PubMed
go back to reference Koenig SF, Brentle S, Hamdi K, Fichtner D, Wedlich D, Gradl D (2010) En2, Pax2/5 and Tcf-4 transcription factors cooperate in patterning the Xenopus brain. Dev Biol 340:318–328PubMedCrossRef Koenig SF, Brentle S, Hamdi K, Fichtner D, Wedlich D, Gradl D (2010) En2, Pax2/5 and Tcf-4 transcription factors cooperate in patterning the Xenopus brain. Dev Biol 340:318–328PubMedCrossRef
go back to reference Kuratani S, Horigome N (2000) Developmental morphology of branchiomeric nerves in a catshark, Scylorhinus torazame, with special reference to rhombomeres, cephalic mesoderm, and distribution patterns of cephalic crest cells. Zool Sci 17:893–909CrossRef Kuratani S, Horigome N (2000) Developmental morphology of branchiomeric nerves in a catshark, Scylorhinus torazame, with special reference to rhombomeres, cephalic mesoderm, and distribution patterns of cephalic crest cells. Zool Sci 17:893–909CrossRef
go back to reference Kuratani S, Nobusada Y, Horigome N, Shigetani Y (2001) Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Philos Trans R Soc Lond B Biol Sci 356:1615–1632PubMedPubMedCentralCrossRef Kuratani S, Nobusada Y, Horigome N, Shigetani Y (2001) Embryology of the lamprey and evolution of the vertebrate jaw: insights from molecular and developmental perspectives. Philos Trans R Soc Lond B Biol Sci 356:1615–1632PubMedPubMedCentralCrossRef
go back to reference Kuratani S, Kuraku S, Murakami Y (2002) Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics. Genesis 34:175–183PubMedCrossRef Kuratani S, Kuraku S, Murakami Y (2002) Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics. Genesis 34:175–183PubMedCrossRef
go back to reference Lannoo MJ, Hawkes R (1997) A search for primitive Purkinje cells: zebrin II expression in sea lampreys (Petromyzon marinus). Neurosci Lett 237:53–55PubMedCrossRef Lannoo MJ, Hawkes R (1997) A search for primitive Purkinje cells: zebrin II expression in sea lampreys (Petromyzon marinus). Neurosci Lett 237:53–55PubMedCrossRef
go back to reference Lebel M, Agarwal P, Cheng CW, Kabir MG, Chan TY, Thanabalasingham V, Zhang X, Cohen DR, Husain M, Cheng SH, Bruneau BG, Hui CC (2003) The Iroquois homeobox gene Irx2 is not essential for normal development of the heart and midbrain–hindbrain boundary in mice. Mol Cell Biol 23:8216–8225PubMedPubMedCentralCrossRef Lebel M, Agarwal P, Cheng CW, Kabir MG, Chan TY, Thanabalasingham V, Zhang X, Cohen DR, Husain M, Cheng SH, Bruneau BG, Hui CC (2003) The Iroquois homeobox gene Irx2 is not essential for normal development of the heart and midbrain–hindbrain boundary in mice. Mol Cell Biol 23:8216–8225PubMedPubMedCentralCrossRef
go back to reference Lekven AC, Buckles GR, Kostakis N, Moon RT (2003) Wnt1 and wnt10b function redundantly at the zebrafish midbrain–hindbrain boundary. Dev Biol 254:172–187PubMedCrossRef Lekven AC, Buckles GR, Kostakis N, Moon RT (2003) Wnt1 and wnt10b function redundantly at the zebrafish midbrain–hindbrain boundary. Dev Biol 254:172–187PubMedCrossRef
go back to reference Liu A, Joyner AL (2001) EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 128:181–191PubMed Liu A, Joyner AL (2001) EN and GBX2 play essential roles downstream of FGF8 in patterning the mouse mid/hindbrain region. Development 128:181–191PubMed
go back to reference Liu A, Losos K, Joyner AL (1999) FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development 126:4827–4838PubMed Liu A, Losos K, Joyner AL (1999) FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development 126:4827–4838PubMed
go back to reference Liu ZR, Shi M, Hu ZL, Zheng MH, Du F, Zhao G, Ding YQ (2010) A refined map of early gene expression in the dorsal rhombomere 1 of mouse embryos. Brain Res Bull 82:74–82PubMedCrossRef Liu ZR, Shi M, Hu ZL, Zheng MH, Du F, Zhao G, Ding YQ (2010) A refined map of early gene expression in the dorsal rhombomere 1 of mouse embryos. Brain Res Bull 82:74–82PubMedCrossRef
go back to reference Lu J, Zhu M, Long JA, Zhao W, Senden TJ, Jia L, Quiao T (2012) The earliest known stem-tetrapod from the Lower Devonian of China. Nat Commun 3:1160PubMedCrossRef Lu J, Zhu M, Long JA, Zhao W, Senden TJ, Jia L, Quiao T (2012) The earliest known stem-tetrapod from the Lower Devonian of China. Nat Commun 3:1160PubMedCrossRef
go back to reference Marín F, Puelles L (1994) Patterning of the embryonic avian midbrain after experimental inversions: a polarizing activity from the isthmus. Dev Biol 163:19–37PubMedCrossRef Marín F, Puelles L (1994) Patterning of the embryonic avian midbrain after experimental inversions: a polarizing activity from the isthmus. Dev Biol 163:19–37PubMedCrossRef
go back to reference Marín F, Aroca P, Puelles L (2008) Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev Biol 323:230–247PubMedCrossRef Marín F, Aroca P, Puelles L (2008) Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev Biol 323:230–247PubMedCrossRef
go back to reference Martínez S (2001) The isthmic organizer and brain regionalization. Int J Dev Biol 44:367–371 Martínez S (2001) The isthmic organizer and brain regionalization. Int J Dev Biol 44:367–371
go back to reference Matsumoto K, Nishihara S, Kamimura M, Shiraishi T, Otoguro T, Uehara M, Maeda Y, Ogura K, Lumsden A, Ogura T (2004) The prepattern transcription factor Irx2, a target of the FGF8/MAP kinasecascade, is involved in cerebellum formation. Nat Neurosci 7:605–612PubMedCrossRef Matsumoto K, Nishihara S, Kamimura M, Shiraishi T, Otoguro T, Uehara M, Maeda Y, Ogura K, Lumsden A, Ogura T (2004) The prepattern transcription factor Irx2, a target of the FGF8/MAP kinasecascade, is involved in cerebellum formation. Nat Neurosci 7:605–612PubMedCrossRef
go back to reference Matsuura M, Nishihara H, Onimaru K, Kokubo N, Kuraku S, Kusakabe R, Okada N, Kuratani S, Tanaka M (2008) Identification of four Engrailed genes in the Japanese lamprey, Lethenteron japonicum. Dev Dyn 237:1581–1589PubMedCrossRef Matsuura M, Nishihara H, Onimaru K, Kokubo N, Kuraku S, Kusakabe R, Okada N, Kuratani S, Tanaka M (2008) Identification of four Engrailed genes in the Japanese lamprey, Lethenteron japonicum. Dev Dyn 237:1581–1589PubMedCrossRef
go back to reference Mazan S, Jaillard D, Baratte B, Janvier P (2000) Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics. Evol Dev 2:186–193PubMedCrossRef Mazan S, Jaillard D, Baratte B, Janvier P (2000) Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics. Evol Dev 2:186–193PubMedCrossRef
go back to reference Mishima Y, Lindgren AG, Chizhikov VV, Johnson RL, Millen KJ (2009) Overlapping function of Lmx1a and Lmx1b in anterior hindbrain roof plate formation and cerebellar growth. J Neurosci 29:11377–11384PubMedCrossRef Mishima Y, Lindgren AG, Chizhikov VV, Johnson RL, Millen KJ (2009) Overlapping function of Lmx1a and Lmx1b in anterior hindbrain roof plate formation and cerebellar growth. J Neurosci 29:11377–11384PubMedCrossRef
go back to reference Montgomery JC, Bodznick D, Yopak KE (2012) The cerebellum and cerebellum-like structures of cartilaginous fishes. Brain Behav Evol 80:152–165PubMedCrossRef Montgomery JC, Bodznick D, Yopak KE (2012) The cerebellum and cerebellum-like structures of cartilaginous fishes. Brain Behav Evol 80:152–165PubMedCrossRef
go back to reference Moreno N, Bachy I, Rétaux S, González A (2005) LIM-homeodomain genes as territory markers in the brainstem of adult and developing Xenopus laevis. J Comp Neurol 485:240–254PubMedCrossRef Moreno N, Bachy I, Rétaux S, González A (2005) LIM-homeodomain genes as territory markers in the brainstem of adult and developing Xenopus laevis. J Comp Neurol 485:240–254PubMedCrossRef
go back to reference Moreno-Bravo JA, Perez-Balaguer A, Martinez-Lopez JE, Aroca P, Puelles L, Martinez S, Puelles E (2014) Role of Shh in the development of molecularly characterized tegmental nuclei in mouse rhombomere 1. Brain Struct Funct 219:777–792. doi:10.1007/s00429-013-0534-6 PubMedCrossRef Moreno-Bravo JA, Perez-Balaguer A, Martinez-Lopez JE, Aroca P, Puelles L, Martinez S, Puelles E (2014) Role of Shh in the development of molecularly characterized tegmental nuclei in mouse rhombomere 1. Brain Struct Funct 219:777–792. doi:10.​1007/​s00429-013-0534-6 PubMedCrossRef
go back to reference Mueller T, Vernier P, Wullimann MF (2006) A phylotypic stage in vertebrate brain development: gABA cell patterns in zebrafish compared with mouse. J Comp Neurol 494:620–634PubMedCrossRef Mueller T, Vernier P, Wullimann MF (2006) A phylotypic stage in vertebrate brain development: gABA cell patterns in zebrafish compared with mouse. J Comp Neurol 494:620–634PubMedCrossRef
go back to reference Murakami Y, Watanabe A (2009) Development of the central and peripheral nervous systems in the lamprey. Dev Growth Differ 51:197–205PubMedCrossRef Murakami Y, Watanabe A (2009) Development of the central and peripheral nervous systems in the lamprey. Dev Growth Differ 51:197–205PubMedCrossRef
go back to reference Murakami Y, Ogasawara M, Sugahara F, Hirano S, Satoh N, Kuratani S (2001) Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128:3521–3531PubMed Murakami Y, Ogasawara M, Sugahara F, Hirano S, Satoh N, Kuratani S (2001) Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128:3521–3531PubMed
go back to reference Murakami Y, Uchida K, Rijli FM, Kuratani S (2005) Evolution of the brain developmental plan: insights from agnathans. Dev Biol 280:249–259PubMedCrossRef Murakami Y, Uchida K, Rijli FM, Kuratani S (2005) Evolution of the brain developmental plan: insights from agnathans. Dev Biol 280:249–259PubMedCrossRef
go back to reference Nakamura H, Sato T, Suzuki-Hirano A (2008) Isthmus organizer for mesencephalon and metencephalon. Dev Growth Differ 50(Suppl 1):S113–S118PubMedCrossRef Nakamura H, Sato T, Suzuki-Hirano A (2008) Isthmus organizer for mesencephalon and metencephalon. Dev Growth Differ 50(Suppl 1):S113–S118PubMedCrossRef
go back to reference O’Hara FP, Beck E, Barr LK, Wong LL, Kessler DS, Riddle RD (2005) Zebrafish Lmx1b.1 and Lmx1b.2 are required for maintenance of the isthmic organizer. Development 132:3163–3173PubMedPubMedCentralCrossRef O’Hara FP, Beck E, Barr LK, Wong LL, Kessler DS, Riddle RD (2005) Zebrafish Lmx1b.1 and Lmx1b.2 are required for maintenance of the isthmic organizer. Development 132:3163–3173PubMedPubMedCentralCrossRef
go back to reference Osório J, Mazan S, Rétaux S (2005) Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from LIM-homeodomain, Pax and hedgehog genes. Dev Biol 288:100–112PubMedCrossRef Osório J, Mazan S, Rétaux S (2005) Organisation of the lamprey (Lampetra fluviatilis) embryonic brain: insights from LIM-homeodomain, Pax and hedgehog genes. Dev Biol 288:100–112PubMedCrossRef
go back to reference Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ (2012) Ancient deuterostome origins of vertebrate brain signaling centres. Nature 483:289–294PubMedPubMedCentralCrossRef Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ (2012) Ancient deuterostome origins of vertebrate brain signaling centres. Nature 483:289–294PubMedPubMedCentralCrossRef
go back to reference Plouhinec JL, Leconte L, Sauka-Spengler TS, Bovolenta P, Mazan S, Saule S (2005) Comparative analysis of gnathostome Otx gene expression patterns in the developing eye: implications for the functional evolution of the multigene family. Dev Biol 278:560–575PubMedCrossRef Plouhinec JL, Leconte L, Sauka-Spengler TS, Bovolenta P, Mazan S, Saule S (2005) Comparative analysis of gnathostome Otx gene expression patterns in the developing eye: implications for the functional evolution of the multigene family. Dev Biol 278:560–575PubMedCrossRef
go back to reference Pose-Méndez S, Candal E, Adrio F, Rodríguez-Moldes I (2014) Development of the cerebellar afferent system in the shark Scyliorhinus canicula: insights into the basal organization of precerebellar nuclei in gnathostomes. J Comp Neurol 522:131–168PubMedCrossRef Pose-Méndez S, Candal E, Adrio F, Rodríguez-Moldes I (2014) Development of the cerebellar afferent system in the shark Scyliorhinus canicula: insights into the basal organization of precerebellar nuclei in gnathostomes. J Comp Neurol 522:131–168PubMedCrossRef
go back to reference Puelles L, Marín F, MartínezdelaTorre S, Martínez S (1995) The midbrain–hindbrain junction: a model system for brain regionalization through morphogenetic neuroepithelial interactions. In: Lonai P (ed) Towards analysis of vertebrate development. Harwood Publishers, Chur, pp 173–197 Puelles L, Marín F, MartínezdelaTorre S, Martínez S (1995) The midbrain–hindbrain junction: a model system for brain regionalization through morphogenetic neuroepithelial interactions. In: Lonai P (ed) Towards analysis of vertebrate development. Harwood Publishers, Chur, pp 173–197
go back to reference Rétaux S, Kano S (2010) Midline signaling and evolution of the forebrain in chordates: a focus on the lamprey Hedgehog case. Integr Comp Biol 50:98–109PubMedCrossRef Rétaux S, Kano S (2010) Midline signaling and evolution of the forebrain in chordates: a focus on the lamprey Hedgehog case. Integr Comp Biol 50:98–109PubMedCrossRef
go back to reference Rhinn M, Lun K, Amores A, Yan YL, Postlethwait JH, Brand M (2003) Cloning, expression and relationship of zebrafish gbx1 and gbx2 genes to Fgf signaling. Mech Dev 120:919–936PubMedCrossRef Rhinn M, Lun K, Amores A, Yan YL, Postlethwait JH, Brand M (2003) Cloning, expression and relationship of zebrafish gbx1 and gbx2 genes to Fgf signaling. Mech Dev 120:919–936PubMedCrossRef
go back to reference Rodríguez-Moldes I, Ferreiro-Galve S, Carrera I, Sueiro C, Candal E, Mazan S, Anadón R (2008) Development of the cerebellar body in sharks: spatiotemporal relations of Pax6-expression, cell proliferation and differentiation. Neurosci Lett 432:105–110PubMedCrossRef Rodríguez-Moldes I, Ferreiro-Galve S, Carrera I, Sueiro C, Candal E, Mazan S, Anadón R (2008) Development of the cerebellar body in sharks: spatiotemporal relations of Pax6-expression, cell proliferation and differentiation. Neurosci Lett 432:105–110PubMedCrossRef
go back to reference Rodríguez-Moldes I, Carrera I, Pose-Méndez S, Quintana-Urzainqui I, Candal E, Anadón R, Mazan S, Ferreiro-Galve S (2011) Regionalization of the shark hindbrain: a survey of an ancestral organization. Front Neuroanat 5:16PubMedPubMedCentralCrossRef Rodríguez-Moldes I, Carrera I, Pose-Méndez S, Quintana-Urzainqui I, Candal E, Anadón R, Mazan S, Ferreiro-Galve S (2011) Regionalization of the shark hindbrain: a survey of an ancestral organization. Front Neuroanat 5:16PubMedPubMedCentralCrossRef
go back to reference Rodríguez-Seguel E, Alarcón P, Gómez-Skarmeta JL (2009) The Xenopus Irx genes are essential for neural patterning and define the border between prethalamus and thalamus through mutual antagonism with the anterior repressors Fezf and Arx. Dev Biol 329:258–268PubMedCrossRef Rodríguez-Seguel E, Alarcón P, Gómez-Skarmeta JL (2009) The Xenopus Irx genes are essential for neural patterning and define the border between prethalamus and thalamus through mutual antagonism with the anterior repressors Fezf and Arx. Dev Biol 329:258–268PubMedCrossRef
go back to reference Sato T, Joyner AL (2009) The duration of Fgf8 isthmic organizer expression is key to patterning different tectal-isthmo-cerebellum structures. Development 136:3617–3626PubMedPubMedCentralCrossRef Sato T, Joyner AL (2009) The duration of Fgf8 isthmic organizer expression is key to patterning different tectal-isthmo-cerebellum structures. Development 136:3617–3626PubMedPubMedCentralCrossRef
go back to reference Sato T, Nakamura H (2004) The Fgf8 signal causes cerebellar differentiation by activating the Ras-ERK signaling pathway. Development 131:4275–4285PubMedCrossRef Sato T, Nakamura H (2004) The Fgf8 signal causes cerebellar differentiation by activating the Ras-ERK signaling pathway. Development 131:4275–4285PubMedCrossRef
go back to reference Scholpp S, Lohs C, Brand M (2003) Engrailed and Fgf8 act synergistically to maintain the boundary between diencephalon and mesencephalon. Development 130:4881–4893PubMedCrossRef Scholpp S, Lohs C, Brand M (2003) Engrailed and Fgf8 act synergistically to maintain the boundary between diencephalon and mesencephalon. Development 130:4881–4893PubMedCrossRef
go back to reference Sgaier SK, Millet S, Villanueva MP, Berenshteyn F, Song C, Joyner AL (2005) Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45:27–40PubMed Sgaier SK, Millet S, Villanueva MP, Berenshteyn F, Song C, Joyner AL (2005) Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45:27–40PubMed
go back to reference Simeone A (2000) Positioning the isthmic organizer where Otx2 and Gbx2 meet. Trends Genet 16:237–240PubMedCrossRef Simeone A (2000) Positioning the isthmic organizer where Otx2 and Gbx2 meet. Trends Genet 16:237–240PubMedCrossRef
go back to reference Sotelo C (2004) Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295–339PubMedCrossRef Sotelo C (2004) Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72:295–339PubMedCrossRef
go back to reference Steinmetz PR, Kostyuchenko RP, Fischer A, Arendt D (2011) The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol Dev 13:72–79PubMedCrossRef Steinmetz PR, Kostyuchenko RP, Fischer A, Arendt D (2011) The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol Dev 13:72–79PubMedCrossRef
go back to reference Suda Y, Kurokawa D, Takeuchi M, Kajikawa E, Kuratani S, Amemiya C, Aizawa S (2009) Evolution of Otx paralogue usages in early patterning of the vertebrate head. Dev Biol 325:282–295PubMedCrossRef Suda Y, Kurokawa D, Takeuchi M, Kajikawa E, Kuratani S, Amemiya C, Aizawa S (2009) Evolution of Otx paralogue usages in early patterning of the vertebrate head. Dev Biol 325:282–295PubMedCrossRef
go back to reference Sugahara F, Aota S, Kuraku S, Murakami Y, Takio-Ogawa Y, Hirano S, Kuratani S (2011) Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development 138:1217–1226PubMedCrossRef Sugahara F, Aota S, Kuraku S, Murakami Y, Takio-Ogawa Y, Hirano S, Kuratani S (2011) Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development 138:1217–1226PubMedCrossRef
go back to reference Sun X, Saitsu H, Shiota K, Ishibashi M (2008) Expression dynamics of the LIM-homeobox genes, Lhx1 and Lhx9, in the diencephalon during chick development. Int J Dev Biol 52:33–41PubMedCrossRef Sun X, Saitsu H, Shiota K, Ishibashi M (2008) Expression dynamics of the LIM-homeobox genes, Lhx1 and Lhx9, in the diencephalon during chick development. Int J Dev Biol 52:33–41PubMedCrossRef
go back to reference Takio Y, Kuraku S, Murakami Y, Pasqualetti M, Rijli FM, Narita Y, Kuratani S, Kusakabe R (2007) Hox gene expression patterns in Lethenteron japonicum embryos-Insights into the evolution of vertebrate Hox code. Dev Biol 308:606–620PubMedCrossRef Takio Y, Kuraku S, Murakami Y, Pasqualetti M, Rijli FM, Narita Y, Kuratani S, Kusakabe R (2007) Hox gene expression patterns in Lethenteron japonicum embryos-Insights into the evolution of vertebrate Hox code. Dev Biol 308:606–620PubMedCrossRef
go back to reference Tan JTY, Korzh V, Gong Z (1999) Expression of a zebrafish iroquois homeobox gene, Ziro3, in the midline axial structures and central nervous system. Mech Dev 87:165–168PubMedCrossRef Tan JTY, Korzh V, Gong Z (1999) Expression of a zebrafish iroquois homeobox gene, Ziro3, in the midline axial structures and central nervous system. Mech Dev 87:165–168PubMedCrossRef
go back to reference Tanaka M, Münsterberg A, Anderson WG, Prescott AR, Hazon N, Tickle C (2002) Fin development in a cartilaginous fish and the origin of vertebrate limbs. Nature 416:527–531PubMedCrossRef Tanaka M, Münsterberg A, Anderson WG, Prescott AR, Hazon N, Tickle C (2002) Fin development in a cartilaginous fish and the origin of vertebrate limbs. Nature 416:527–531PubMedCrossRef
go back to reference Tomsa JM, Langeland JA (1999) Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev Biol 207:26–37PubMedCrossRef Tomsa JM, Langeland JA (1999) Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev Biol 207:26–37PubMedCrossRef
go back to reference Urbach R (2007) A procephalic territory in Drosophila exhibiting similarities and dissimilarities compared to the vertebrate midbrain/hindbrain boundary region. Neural Dev 2:23PubMedPubMedCentralCrossRef Urbach R (2007) A procephalic territory in Drosophila exhibiting similarities and dissimilarities compared to the vertebrate midbrain/hindbrain boundary region. Neural Dev 2:23PubMedPubMedCentralCrossRef
go back to reference Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological histochemical and autoradiographic investigation. In: Brodal HOH et al (eds) Advances in anatomy, embryology and cell biology. Springer, Berlin, pp 5–21 Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological histochemical and autoradiographic investigation. In: Brodal HOH et al (eds) Advances in anatomy, embryology and cell biology. Springer, Berlin, pp 5–21
go back to reference Vaage S (1973) The histogenesis of the isthmic nuclei in chick embryos (Gallus domesticus). Z Anat Entwicklungsgesch 142:283–314PubMedCrossRef Vaage S (1973) The histogenesis of the isthmic nuclei in chick embryos (Gallus domesticus). Z Anat Entwicklungsgesch 142:283–314PubMedCrossRef
go back to reference Villar-Cerviño V, Barreiro-Iglesias A, Rodicio MC, Anadón R (2010) D-serine is distributed in neurons in the brain of the sea lamprey. J Comp Neurol 518:1688–1710PubMedCrossRef Villar-Cerviño V, Barreiro-Iglesias A, Rodicio MC, Anadón R (2010) D-serine is distributed in neurons in the brain of the sea lamprey. J Comp Neurol 518:1688–1710PubMedCrossRef
go back to reference Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31–43PubMedCrossRef Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31–43PubMedCrossRef
go back to reference Waters ST, Lewandoski M (2006) A threshold requirement for Gbx2 levels in hindbrain development. Development 133:1991–2000PubMedCrossRef Waters ST, Lewandoski M (2006) A threshold requirement for Gbx2 levels in hindbrain development. Development 133:1991–2000PubMedCrossRef
go back to reference Watson C, Paxinos G, Puelles L (2012) The mouse nervous system. Elsevier Academic Press, London Watson C, Paxinos G, Puelles L (2012) The mouse nervous system. Elsevier Academic Press, London
go back to reference Wullimann MF, Mueller T, Distel M, Babaryka A, Grothe B, Köster RW (2011) The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front Neuroanat 5:27PubMedPubMedCentralCrossRef Wullimann MF, Mueller T, Distel M, Babaryka A, Grothe B, Köster RW (2011) The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis. Front Neuroanat 5:27PubMedPubMedCentralCrossRef
go back to reference Zervas M, Millet S, Ahn S, Joyner A (2004) Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43:345–357PubMedCrossRef Zervas M, Millet S, Ahn S, Joyner A (2004) Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43:345–357PubMedCrossRef
go back to reference Zhu M, Yu X, Ahlberg PE, Choo B, Lu J, Qiao T, Qu Q, Zhao W, Jia L, Blom H, Zhu Y (2013) A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502:188–193PubMedCrossRef Zhu M, Yu X, Ahlberg PE, Choo B, Lu J, Qiao T, Qu Q, Zhao W, Jia L, Blom H, Zhu Y (2013) A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502:188–193PubMedCrossRef
Metadata
Title
Genoarchitecture of the rostral hindbrain of a shark: basis for understanding the emergence of the cerebellum at the agnathan–gnathostome transition
Authors
Sol Pose-Méndez
Eva Candal
Sylvie Mazan
Isabel Rodríguez-Moldes
Publication date
01-04-2016
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 3/2016
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-014-0973-8

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