Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features

Brain Structure and Function - Tập 221 Số 2 - Trang 815-838 - 2016
Laura Tomás‐Roca1, Rubén Corral-San-Miguel1, Pilar Aroca1, Luis Puelles1, Faustino Marı́n1
1Department of Human Anatomy and Psychobiology, School of Medicine, University of Murcia, and IMIB (Instituto Murciano de Investigación Biosanitaria), 30100, Murcia, Spain

Tóm tắt

Từ khóa


Tài liệu tham khảo

Aldes LD (1995) Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat. J Comp Neurol 353:89–108

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 218:1229–1277

Amat JA (1986) Compartimentación y dinamica neurogenética del tubo neuronal del embrion de pollo. Manifestación heterocrónica del plan estructural del neuroeje. Dissertation, University of Murcia, Spain

Ashwell KW, Hardman CD, Paxinos G (2006) Cyto- and chemoarchitecture of the sensory trigeminal nuclei of the echidna, platypus and rat. J Chem Neuroanat 31:81–107

Behringer RR, Crotty DA, Tennyson VM, Brinster RL, Palmiter RD, Wolgemuth DJ (1993) Sequences 5′ of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development 117:823–833

Bergquist H (1952) Studies on the cerebral tube in vertebrates. The neuromeres. Acta Zool 33:117–187

Borday C, Vias C, Autran S, Thoby-Brisson M, Champagnat J, Fortin G (2006) The pre-Bötzinger oscillator in the mouse embryo. J Physiol Paris 100:284–289

Boulet AM, Capecchi MR (1996) Targeted disruption of hoxc-4 causes esophageal defects and vertebral transformations. Dev Biol 177:232–249

Breier G, Dressler GR, Gruss P (1988) Primary structure and developmental expression pattern of Hox 3.1, a member of the murine Hox 3 homeobox gene cluster. EMBO J 7:1329–1336

Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522–545

Capecchi MR (1997) Hox genes and mammalian development. Cold Spring Harb Symp Quant Biol 62:273–281

Cheung CC, Hohmann JG, Clifton DK, Steiner RA (2001) Distribution of galanin messenger RNA-expressing cells in murine brain and their regulation by leptin in regions of the hypothalamus. Neuroscience 103:423–432

Clarke JD, Lumsden A (1993) Segmental repetition of neuronal phenotype sets in the chick embryo hindbrain. Development 118:151–162

Cordes SP (2001) Molecular genetics of cranial nerve development in mouse. Nat Rev Neurosci 2:611–623

Di Bonito M, Narita Y, Avallone B, Sequino L, Mancuso M, Andolfi G, Franzè AM, Puelles L, Rijli FM, Studer M (2013) Assembly of the auditory circuitry by a Hox genetic network in the mouse brainstem. PLoS Genet 9:e1003249. doi: 10.1371/journal.pgen.1003249

Díaz C, Puelles L, Marín F, Glover JC (1998) The relationship between rhombomeres and vestibular neuron populations as assessed in quail-chicken chimeras. Dev Biol 202:14–28

Duchcherer M, Baghdadwala MI, Paramonov J, Wilson RJA (2013) Localization of essential rhombomeres for respiratory rhythm generation in bullfrog tadpoles using a binary search algorithm: rhombomere 7 is essential for the gill rhythm and suppresses lung bursts before metamorphosis. Dev Neurobiol 73:888–898

Dun SL, Castellino SJ, Yang J, Chang JK, Dun NJ (2001) Cocaine- and amphetamine-regulated transcript peptide-immunoreactivity in dorsal motor nucleus of the vagus neurons of immature rats. Brain Res Dev Brain Res 131:93–102

Fantin A, Vieira JM, Plein A, Maden CH, Ruhrberg C (2013) The embryonic mouse hindbrain as a qualitative and quantitative model for studying the molecular and cellular mechanisms of angiogenesis. Nat Protoc 8:418–429

Farago AF, Awatramani RB, Dymecki SM (2006) Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50:205–218

Franklin KBJ, Paxinos G (2008) The mouse brain in stereotaxic coordinates, 3rd edn. Elsevier, Amsterdam

Fraser S, Keynes R, Lumsden A (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344:431–435

Garel S, Garcia-Dominguez M, Charnay P (2000) Control of the migratory pathway of facial branchiomotor neurones. Development 127:5297–5307

Gaufo GO, Thomas KR, Capecchi MR (2003) Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons. Development 130:5191–5201

Gaunt SJ, Krumlauf R, Duboule D (1989) Mouse homeo-genes within a subfamily, Hox-1.4, -2.6 and -5.1, display similar anteroposterior domains of expression in the embryo, but show stage- and tissue-dependent differences in their regulation. Development 107:131–141

Gaunt SJ, Coletta PL, Pravtcheva D, Sharpe PT (1990) Mouse Hox-3.4: homeobox sequence and embryonic expression patterns compared with other members of the Hox gene network. Development 109:329–339

Geisen MJ, Di Meglio T, Pasqualetti M, Ducret S, Brunet J-F, Chedotal A, Rijli F (2008) Hox paralog group 2 genes control the migration of mouse pontine neurons through Slit-Robo signaling. PLoS Biol 6(6):e142

Gerhardt H, Ruhrberg C, Abramsson A, Fujisawa H, Shima D, Betsholtz C (2004) Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev Dyn 231:503–509

Gray PA (2013) Transcription factors define the neuroanatomical organization of the medullary reticular formation. Front Neuroanat 7:7. doi: 10.3389/fnana.2013.00007

Gubert F, Zaverucha-do-Valle C, Pimentel-Coelho PM, Mendez-Otero R, Santiago MF (2009) Radial glia-like cells persist in the adult rat brain. Brain Res 1258:43–52

Guthrie S, Butcher M, Lumsden A (1991) Patterns of cell division and interkinetic nuclear migration in the chick embryo hindbrain. J Neurobiol 22:742–754

Heyman I, Faissner A, Lumsden A (1995) Cell and matrix specialisations of rhombomere boundaries. Dev Dyn 204:301–315

Hidalgo-Sánchez M, Backer S, Puelles L, Bloch-Gallego E (2012) Origin and plasticity of the subdivisions of the inferior olivary complex. Dev Biol 371:215–226

His W (1904) Die Entwickelung des menschlichen Gehirns: während der ersten Monate. S. Hirzel, Leipzig

Hökfelt T, Tsuruo Y, Ulfhake B, Cullheim S, Arvidsson U, Foster GA, Schultzberg M, Schalling M, Arborelius L, Freedman J (1989) Distribution of TRH-like immunoreactivity with special reference to coexistence with other neuroactive compounds. Ann N Y Acad Sci 553:76–105

Holstege JC, de Graaff W, Hossaini M, Cardona Cano S, Jaarsma D, van den Akker E, Deschamps J (2008) Loss of Hoxb8 alters spinal dorsal laminae and sensory responses in mice. Proc Natl Acad Sci USA 105:6338–6343

Izpisúa-Belmonte JC, Dollé P, Renucci A, Zappavigna V, Falkenstein H, Duboule D (1990) Primary structure and embryonic expression pattern of the mouse Hox-4.3 homeobox gene. Development 110:733–745

Jimenez-Guri E, Udina F, Colas J-F, Sharpe J, Padrón-Barthe L, Torres M, Pujades C (2010) Clonal analysis in mice underlines the importance of rhombomeric boundaries in cell movement restriction during hindbrain segmentation. PLoS One 5:e10112. doi: 10.1371/journal.pone.0010112

Kalia M, Fuxe K, Goldstein M (1985) Rat medulla oblongata. II. Dopaminergic, noradrenergic (A1 and A2) and adrenergic neurons, nerve fibers, and presumptive terminal processes. J Comp Neurol 233:308–332

Källén B (1953) On the Significance of the Neuromeres and Similar Structures in Vertebrate Embryos. J Embryol Exp Morphol 1:387–392

Kiecker C, Lumsden A (2005) Compartments and their boundaries in vertebrate brain development. Nat Rev Neurosci 6:553–564

Kimura H, McGeer PL, Peng J-H, McGeer EG (1984) Choline acetyltransferase-containing neurons in the rat brain. In: Björklund A, Hökfelt T, Kuhar MJ (eds) Handbook of chemical neuroanatomy, vol 3: classical transmitters and transmitter receptors in the CNS. Elsevier, Amsterdam, pp 51–67

Koylu EO, Couceyro PR, Lambert PD, Kuhar MJ (1998) Cocaine- and amphetamine-regulated transcript peptide immunohistochemical localization in the rat brain. J Comp Neurol 391:115–132

Krumlauf R (1993) Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet 9:106–112

Krumlauf R, Marshall H, Studer M, Nonchev S, Sham MH, Lumsden A (1993) Hox homeobox genes and regionalisation of the nervous system. J Neurobiol 24:1328–1340

Lim TM, Jaques KF, Stern CD, Keynes RJ (1991) An evaluation of myelomeres and segmentation of the chick embryo spinal cord. Development 113:227–238

Lumsden A (1990) The cellular basis of segmentation in the developing hindbrain. Trends Neurosci 13:329–335

Lumsden A, Keynes R (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424–428

Lumsden A, Krumlauf R (1996) Patterning the vertebrate neuraxis. Science 274:1109–1115

Mahon KA, Westphal H, Gruss P (1988) Expression of homeobox gene Hox 1.1 during mouse embryogenesis. Development 104(Suppl):187–195

Mallo M, Wellik DM, Deschamps J (2010) Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344:7–15

Manzanares M, Cordes S, Ariza-McNaughton L, Sadl V, Maruthainar K, Barsh G, Krumlauf R (1999) Conserved and distinct roles of kreisler in regulation of the paralogous Hoxa3 and Hoxb3 genes. Development 126:759–769

Marín F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714–1738

Marín F, Aroca P, Puelles L (2008) Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains. Dev Biol 323:230–247

Martínez S (2001) The isthmic organizer and brain regionalization. Int J Dev Biol 45:367–371

Martínez S, Geijo E, Sánchez-Vives MV, Puelles L, Gallego R (1992) Reduced junctional permeability at interrhombomeric boundaries. Development 116:1069–1076

Minamikawa T, Miyake T, Takamatsu T, Fujita S (1987) A new method of lectin histochemistry for the study of brain angiogenesis. Lectin angiography. Histochemistry 87:317–320

Murakami Y, Pasqualetti M, Takio Y, Hirano S, Rijli FM, Kuratani S (2004) Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain. Development 131:983–995

Neal HV (1918) Neuromeres and metameres. J Morphol 31:293–315

Nieto MA, Patel K, Wilkinson DG (1996) In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219–235

Nieuwenhuys R (1998) Morphogenesis and general structure. In: Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrates. Springer-Verlag, Berlin, pp 159–228

Nieuwenhuys R (2011) The structural, functional, and molecular organization of the brainstem. Front Neuroanat 5:33. doi: 10.3389/fnana.2011.00033

Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human central nervous system. Springer, New York

Orr H (1887) Contribution to the embryology of the lizard; With especial reference to the central nervous system and some organs of the head; together with observations on the origin of the vertebrates. J Morphol 1:311–372

Packer AI, Crotty DA, Elwell VA, Wolgemuth DJ (1998) Expression of the murine Hoxa4 gene requires both autoregulation and a conserved retinoic acid response element. Development 125:1991–1998

Pasqualetti M, Díaz C, Renaud J-S, Rijli FM, Glover JC (2007) Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo. J Neurosci 27:9670–9681

Prin F, Serpente P, Itasaki N, Gould AP (2014) Hox proteins drive cell segregation and non-autonomous apical remodelling during hindbrain segmentation. Development 141:1492–1502

Puelles L (2013) Plan of the developing vertebrate nervous system: relating embryology to the adult nervous system (prosomere model, overview of brain organization). In: Rakic P, Rubenstein J (eds) Patterning and Cell Type Specification in the Developing Cns and Pns. Elsevier, Amsterdam, pp 187–209

Puelles L, Rubenstein JL (1993) Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 16:472–479

Puelles L, Rubenstein JLR (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469–476

Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martínez S (2007) The chick brain in stereotaxic coordinates: an atlas featuring neuromeric subdivisions and mammalian homologies. Academic Press, Amsterdam

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 5:16. doi: 10.3389/fnana.2011.00016

Rubenstein JL, Martinez S, Shimamura K, Puelles L (1994) The embryonic vertebrate forebrain: the prosomeric model. Science 266:578–580

Schughart K, Utset MF, Awgulewitsch A, Ruddle FH (1988) Structure and expression of Hox-2.2, a murine homeobox-containing gene. Proc Natl Acad Sci USA 85:5582–5586

Shimeld SM, Gaunt SJ, Coletta PL, Geada AM, Sharpe PT (1993) Spatial localisation of transcripts of the Hox-C6 gene. J Anat 183:515–523

Sotelo C, Bourrat F, Triller A (1984) Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection. J Comp Neurol 222:177–199

Specht LA, Pickel VM, Joh TH, Reis DJ (1981a) Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J Comp Neurol 199:233–253

Specht LA, Pickel VM, Joh TH, Reis DJ (1981b) Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. II. Late ontogeny. J Comp Neurol 199:255–276

Stern CD, Jaques KF, Lim TM, Fraser SE, Keynes RJ (1991) Segmental lineage restrictions in the chick embryo spinal cord depend on the adjacent somites. Development 113:239–244

Studer M (2001) Initiation of facial motoneurone migration is dependent on rhombomeres 5 and 6. Development 128:3707–3716

Theiler K (1989) The house mouse: atlas of embryonic development. Springer, New York

Toth LE, Slawin KL, Pintar JE, Nguyen-Huu MC (1987) Region-specific expression of mouse homeobox genes in the embryonic mesoderm and central nervous system. Proc Natl Acad Sci USA 84:6790–6794

Tsuruo Y, Hökfelt T, Visser T (1987) Thyrotropin releasing hormone (TRH)-immunoreactive cell groups in the rat central nervous system. Exp Brain Res 68:213–217

Tümpel S, Wiedemann LM, Krumlauf R (2009) Hox genes and segmentation of the vertebrate hindbrain. Curr Top Dev Biol 88:103–137

Vaage S (1969) The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation. Ergeb Anat Entwicklungsgesch 41:3–87

Vivancos V, Chen P, Spassky N, Qian D, Dabdoub A, Kelley M, Studer M, Guthrie S (2009) Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases. Neural Dev 4:7

Vogels R, de Graaff W, Deschamps J (1990) Expression of the murine homeobox-containing gene Hox-2.3 suggests multiple time-dependent and tissue-specific roles during development. Development 110:1159–1168

Watson C (2012) Hindbrain. In: Watson C, Paxinos G, Puelles L (eds) The Mouse Nervous System. Elsevier Academic Press, Amsterdan, pp 398–423

Watson C, Paxinos G (2009) Chemoarchitectonic atlas of the mouse brain. Academic Press, London

Watson C, Kirkcaldie M, Paxinos G (2010) The Brain. An Introduction to Functional Neuroanatomy. Academic Press, London

Wickström R, Holgert H, Lagercrantz H, Hökfelt T (2000) Perinatal distribution of galanin and galanin receptor-1 mRNA in the rat hindbrain. Brain Res Dev Brain Res 123:53–65

Wilkinson DG, Krumlauf R (1990) Molecular approaches to the segmentation of the hindbrain. Trends Neurosci 13:335–339

Wingate RJ, Lumsden A (1996) Persistence of rhombomeric organisation in the postsegmental hindbrain. Development 122:2143–2152

Yan X, Lin J, Markus A, Rolfs A, Luo J (2011) Regional expression of ADAM19 during chicken embryonic development. Dev Growth Differ 53:333–346

Zákány J, Duboule D (1999) Hox genes in digit development and evolution. Cell Tissue Res 296:19–25