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

Summary

Facial branchiomotor (fbm) neurones undergo a complex migration in the segmented mouse hindbrain. They are born in the basal plate of rhombomere (r) 4, migrate caudally through r5, and then dorsally and radially in r6. To study how migrating cells adapt to their changing environment and control their pathway, we have analysed this stereotyped migration in wild-type and mutant backgrounds. We show that during their migration, fbm neurones regulate the expression of genes encoding the cell membrane proteins TAG-1, Ret and cadherin 8. Specific combinations of these markers are associated with each migratory phase in r4, r5 and r6. In Krox20 and kreisler mutant mouse embryos, both of which lack r5, fbm neurones migrate dorsally into the anteriorly positioned r6 and adopt an r6-specific expression pattern. In embryos deficient for Ebf1, a gene normally expressed in fbm neurones, part of the fbm neurones migrate dorsally within r5. Accordingly, fbm neurones prematurely express a combination of markers characteristic of an r6 location. These data suggest that fbm neurones adapt to their changing environment by switching on and off specific genes, and that Ebf1 is involved in the control of these responses. In addition, they establish a close correlation between the expression pattern of fbm neurones and their migratory behaviour, suggesting that modifications in gene expression participate in the selection of the local migratory pathway.

REFERENCES

    1. Ackerman S. L.,
    2. Kozak L. P.,
    3. Przyborski S. A.,
    4. Rund L. A.,
    5. Boyer B. B.,
    6. Knowles B. B.
    (1997) The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386, 838–842
    OpenUrlCrossRefPubMed
    1. Alcantara S.,
    2. Ruiz M.,
    3. De Castro F.,
    4. Soriano E.,
    5. Sotelo C.
    (2000) Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development 127, 1359–1372
    OpenUrlAbstract
    1. Altman J.,
    2. Bayer S. A.
    (1982) Development of the cranial nerve ganglia and related nuclei in the rat. Adv Anat. Embryol. Cell Biol 74, 1–90
    OpenUrlPubMed
    1. Ashwell K. W.,
    2. Watson C. R.
    (1983) The development of facial motoneurones in the mouse—neuronal death and the innervation of the facial muscles. J. Embryol. Exp. Morphol 77, 117–141
    OpenUrlPubMedWeb of Science
    1. Auclair F.,
    2. Valdes N.,
    3. Marchand R.
    (1996) Rhombomere-specific origin of branchial and visceral motoneurons of the facial nerve in the rat embryo. J. Comp. Neurol 369, 451–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Bell E.,
    2. Wingate R. J.,
    3. Lumsden A.
    (1999) Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284, 2168–2171
    OpenUrlAbstract/FREE Full Text
    1. Bloch-Gallego E.,
    2. Ezan F.,
    3. Tessier-Lavigne M.,
    4. Sotelo C.
    (1999) Floorplate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J. Neurosci 19, 4407–4420
    OpenUrlAbstract/FREE Full Text
    1. Brose K.,
    2. Tessier-Lavigne M.
    (2000) Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol 10, 95–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Castellani V.,
    2. Chedotal A.,
    3. Schachner M.,
    4. Faivre-Sarrailh C.,
    5. Rougon G.
    (2000) Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27, 237–249
    OpenUrlCrossRefPubMedWeb of Science
    1. Cordes S. P.,
    2. Barsh G. S.
    (1994) The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025–1034
    OpenUrlCrossRefPubMedWeb of Science
    1. Dodd J.,
    2. Morton S. B.,
    3. Karagogeos D.,
    4. Yamamoto M.,
    5. Jessell T. M.
    (1988) Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron 1, 105–116
    OpenUrlCrossRefPubMedWeb of Science
    1. Durbec P.,
    2. Marcos-Gutierrez C. V.,
    3. Kilkenny C.,
    4. Grigoriou M.,
    5. Wartiowaara K.,
    6. Suvanto P.,
    7. Smith D.,
    8. Ponder B.,
    9. Costantini F.,
    10. Saarma M.,
    11. et al.
    (1996) GDNF signalling through the Ret receptor tyrosine kinase. Nature 381, 789–793
    OpenUrlCrossRefPubMed
    1. Durbec P. L.,
    2. Larsson-Blomberg L. B.,
    3. Schuchardt A.,
    4. Costantini F.,
    5. Pachnis V.
    (1996) Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 122, 349–358
    OpenUrlAbstract
    1. Ericson J.,
    2. Thor S.,
    3. Edlund T.,
    4. Jessell T. M.,
    5. Yamada T.
    (1992) Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555–1560
    OpenUrlAbstract/FREE Full Text
    1. Frohman M. A.,
    2. Martin G. R.,
    3. Cordes S. P.,
    4. Halamek L. P.,
    5. Barsh G. S.
    (1993) Altered rhombomere-specific gene expression and hyoid bone differentiation in the mouse segmentation mutant, kreisler (kr). Development 117, 925–936
    OpenUrlAbstract
    1. Furley A. J.,
    2. Morton S. B.,
    3. Manalo D.,
    4. Karagogeos D.,
    5. Dodd J.,
    6. Jessell T. M.
    (1990) The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell 61, 157–170
    OpenUrlCrossRefPubMedWeb of Science
    1. Garel S.,
    2. Marin F.,
    3. Mattei M. G.,
    4. Vesque C.,
    5. Vincent A.,
    6. Charnay P.
    (1997) Family of Ebf/Olf-1-related genes potentially involved in neuronal differentiation and regional specification in the central nervous system. Dev. Dyn 210, 191–205
    OpenUrlCrossRefPubMedWeb of Science
    1. Garel S.,
    2. Marin F.,
    3. Grosschedl R.,
    4. Charnay P.
    (1999) Ebf1 controls early cell differentiation in the embryonic striatum. Development 126, 5285–5294
    OpenUrlAbstract
    1. Gilardi-Hebenstreit P.,
    2. Nieto M. A.,
    3. Frain M.,
    4. Mattei M. G.,
    5. Chestier A.,
    6. Wilkinson D. G.,
    7. Charnay P.
    (1992) An Eph-related receptor protein tyrosine kinase gene segmentally expressed in the developing mouse hindbrain. Oncogene 7, 2499–2506
    OpenUrlPubMedWeb of Science
    1. Goddard J. M.,
    2. Rossel M.,
    3. Manley N. R.,
    4. Capecchi M. R.
    (1996) Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122, 3217–3228
    OpenUrlAbstract
    1. Hagman J.,
    2. Travis A.,
    3. Grosschedl R.
    (1991) A novel lineage-specific nuclear factor regulates mb-1 gene transcription at the early stages of B cell differentiation. EMBO J 10, 3409–3417
    OpenUrlPubMedWeb of Science
    1. Hagman J.,
    2. Belanger C.,
    3. Travis A.,
    4. Turck C. W.,
    5. Grosschedl R.
    (1993) Cloning and functional characterization of early B-cell factor, a regulator of lymphocyte-specific gene expression. Genes Dev 7, 760–773
    OpenUrlAbstract/FREE Full Text
    1. Helmbacher F.,
    2. Pujades C.,
    3. Desmarquet C.,
    4. Frain M.,
    5. Rijli F.,
    6. Chambon P.,
    7. Charnay P.
    (1998) Hoxa-1 and Krox-20 synergize to control the development of rhombomere 3. Development 125, 4739–4748
    OpenUrlAbstract
    1. Korematsu K.,
    2. Redies C.
    (1997) Restricted expression of cadherin-8 in segmental and functional subdivisions of the embryonic mouse brain. Dev. Dyn 208, 178–189
    OpenUrlCrossRefPubMedWeb of Science
    1. Kuhn T. B.,
    2. Stoeckli E. T.,
    3. Condrau M. A.,
    4. Rathjen F. G.,
    5. Sonderegger P.
    (1991) Neurite outgrowth on immobilized axonin-1 is mediated by a heterophilic interaction with L1(G4). J. Cell Biol 115, 1113–1126
    OpenUrlAbstract/FREE Full Text
    1. Lin H.,
    2. Grosschedl R.
    (1995) Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263–267
    OpenUrlCrossRefPubMed
    1. Lumsden A.,
    2. Keynes R.
    (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424–428
    OpenUrlCrossRefPubMed
    1. Lumsden A.
    (1990) The cellular basis of segmentation in the developing hindbrain. Trends Neurosci 13, 329–335
    OpenUrlCrossRefPubMedWeb of Science
    1. Manzanares M.,
    2. Trainor P. A.,
    3. Nonchev S.,
    4. Ariza-McNaughton L.,
    5. Brodie J.,
    6. Gould A.,
    7. Marshall H.,
    8. Morrison A.,
    9. Kwan C. T.,
    10. Sham M. H.,
    11. et al.
    (1999) The role of kreisler in segmentation during hindbrain development. Dev. Biol 211, 220–237
    OpenUrlCrossRefPubMed
    1. Marcus R. C.,
    2. Blazeski R.,
    3. Godement P.,
    4. Mason C. A.
    (1995) Retinal axon divergence in the optic chiasm: uncrossed axons diverge from crossed axons within a midline glial specialization. J. Neurosci 15, 3716–3729
    OpenUrlAbstract
    1. Marin F.,
    2. Puelles L.
    (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur. J. Neurosci 7, 1714–1738
    OpenUrlCrossRefPubMedWeb of Science
    1. Mathis L.,
    2. Sieur J.,
    3. Voiculescu O.,
    4. Charnay P.,
    5. Nicolas J.
    (1999) Successive patterns of clonal cell dispersion in relation to neuromeric subdivision in the mouse neuroepithelium. Development 126, 4095–4106
    OpenUrlAbstract
    1. McKay I. J.,
    2. Muchamore I.,
    3. Krumlauf R.,
    4. Maden M.,
    5. Lumsden A.,
    6. Lewis J.
    (1994) The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres. Development 120, 2199–2211
    OpenUrlAbstract
    1. McKay I. J.,
    2. Lewis J.,
    3. Lumsden A.
    (1997) Organization and development of facial motor neurons in the kreisler mutant mouse. Eur. J. Neurosci 9, 1499–1506
    OpenUrlCrossRefPubMedWeb of Science
    1. Murphy P.,
    2. Davidson D. R.,
    3. Hill R. E.
    (1989) Segment-specific expression of a homoeobox-containing gene in the mouse hindbrain. Nature 341, 156–159
    OpenUrlCrossRefPubMed
    1. Nardelli J.,
    2. Thiesson D.,
    3. Fujiwara Y.,
    4. Tsai F. Y.,
    5. Orkin S. H.
    (1999) Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev. Biol 210, 305–321
    OpenUrlCrossRefPubMedWeb of Science
    1. Natarajan D.,
    2. Grigoriou M.,
    3. Marcos-Gutierrez C. V.,
    4. Atkins C.,
    5. Pachnis V.
    (1999) Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture. Development 126, 157–168
    OpenUrlAbstract
    1. Pachnis V.,
    2. Mankoo B.,
    3. Costantini F.
    (1993) Expression of the c-ret proto-oncogene during mouse embryogenesis. Development 119, 1005–1017
    OpenUrlAbstract
    1. Pata I.,
    2. Studer M.,
    3. van D. J.,
    4. Briscoe J.,
    5. Kuuse S.,
    6. Engel J. D.,
    7. Grosveld F.,
    8. Karis A.
    (1999) The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development 126, 5523–5531
    OpenUrlAbstract
    1. Pattyn A.,
    2. Morin X.,
    3. Cremer H.,
    4. Goridis C.,
    5. Brunet J. F.
    (1997) Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124, 4065–4075
    OpenUrlAbstract
    1. Pattyn A.,
    2. Hirsch M.,
    3. Goridis C.,
    4. Brunet J. F.
    (2000) Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127, 1349–1358
    OpenUrlAbstract
    1. Redies C.,
    2. Takeichi M.
    (1996) Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev. Biol 180, 413–423
    OpenUrlCrossRefPubMedWeb of Science
    1. Robinson V.,
    2. Smith A.,
    3. Flenniken A. M.,
    4. Wilkinson D. G.
    (1997) Roles of Eph receptors and ephrins in neural crest pathfinding. Cell Tiss. Res 290, 265–274
    OpenUrlCrossRefPubMedWeb of Science
    1. Sandell J. H.,
    2. Masland R. H.
    (1988) Photoconversion of some fluorescent markers to a diaminobenzidine product. J. Histochem. Cytochem 36, 555–559
    OpenUrlAbstract/FREE Full Text
    1. Schneider-Maunoury S.,
    2. Topilko P.,
    3. Seitandou T.,
    4. Levi G.,
    5. Cohen-Tannoudji M.,
    6. Pournin S.,
    7. Babinet C.,
    8. Charnay P.
    (1993) Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75, 1199–1214
    OpenUrlCrossRefPubMedWeb of Science
    1. Schneider-Maunoury S.,
    2. Seitanidou T.,
    3. Charnay P.,
    4. Lumsden A.
    (1997) Segmental and neuronal architecture of the hindbrain of Krox-20 mouse mutants. Development 124, 1215–1226
    OpenUrlAbstract
    1. Schneider-Maunoury S.,
    2. Gilardi-Hebenstreit P.,
    3. Charnay P.
    (1998) How to build a vertebrate hindbrain. Lessons from genetics. C. R. Acad. Sci. Iii 321, 819–834
    OpenUrlPubMed
    1. Seitanidou T.,
    2. Schneider-Maunoury S.,
    3. Desmarquet C.,
    4. Wilkinson D. G.,
    5. Charnay P.
    (1997) Krox-20 is a key regulator of rhombomere-specific gene expression in the developing hindbrain. Mech. Dev 65, 31–42
    OpenUrlCrossRefPubMedWeb of Science
    1. Serafini T.,
    2. Colamarino S. A.,
    3. Leonardo E. D.,
    4. Wang H.,
    5. Beddington R.,
    6. Skarnes W. C.,
    7. Tessier-Lavigne M.
    (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001–1014
    OpenUrlCrossRefPubMedWeb of Science
    1. Studer M.,
    2. Lumsden A.,
    3. Ariza-McNaughton L.,
    4. Bradley A.,
    5. Krumlauf R.
    (1996) Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630–634
    OpenUrlCrossRefPubMed
    1. Swiatek P. J.,
    2. Gridley T.
    (1993) Perinatal lethality and defects in hindbrain development in mice homozygous for a targeted mutation of the zinc finger gene Krox20. Genes Dev 7, 2071–2084
    OpenUrlAbstract/FREE Full Text
    1. Szekely G.,
    2. Matesz C.
    (1993) The efferent system of cranial nerve nuclei: a comparative neuromorphological study. Adv. Anat. Embryol. Cell Biol 128, 1–92
    OpenUrlPubMed
    1. Tang M. J.,
    2. Worley D.,
    3. Sanicola M.,
    4. Dressler G. R.
    (1998) The RET-glial cell-derived neurotrophic factor (GDNF) pathway stimulates migration and chemoattraction of epithelial cells. J. Cell Biol 142, 1337–1345
    OpenUrlAbstract/FREE Full Text
    1. Tanihara H.,
    2. Sano K.,
    3. Heimark R. L.,
    4. St John T.,
    5. Suzuki S.
    (1994) Cloning of five human cadherins clarifies characteristic features of cadherin extracellular domain and provides further evidence for two structurally different types of cadherin. Cell Adhes. Commun 2, 15–26
    OpenUrlPubMedWeb of Science
    1. Trupp M.,
    2. Arenas E.,
    3. Fainzilber M.,
    4. Nilsson A. S.,
    5. Sieber B. A.,
    6. Grigoriou M.,
    7. Kilkenny C.,
    8. Salazar-Grueso E.,
    9. Pachnis V.,
    10. Arumae U.
    (1996) Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature 381, 785–789
    OpenUrlCrossRefPubMed
    1. Wang M. M.,
    2. Reed R. R.
    (1993) Molecular cloning of the olfactory neuronal transcription factor Olf-1 by genetic selection in yeast. Nature 364, 121–126
    OpenUrlCrossRefPubMed
    1. Wang S. S.,
    2. Tsai R. Y.,
    3. Reed R. R.
    (1997) The characterization of the Olf-1/EBF-like HLH transcription factor family: implications in olfactory gene regulation and neuronal development. J. Neurosci 17, 4149–4158
    OpenUrlAbstract/FREE Full Text
    1. Wilkinson D. G.,
    2. Bhatt S.,
    3. Chavrier P.,
    4. Bravo R.,
    5. Charnay P.
    (1989) Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse. Nature 337, 461–464
    OpenUrlCrossRefPubMed
    1. Wingate R. J.,
    2. Lumsden A.
    (1996) Persistence of rhombomeric organisation in the postsegmental hindbrain. Development 122, 2143–2152
    OpenUrlAbstract
    1. Yee K. T.,
    2. Simon H. H.,
    3. Tessier L. M.,
    4. O'Leary D. M.
    (1999) Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24, 607–622
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Control of the migratory pathway of facial branchiomotor neurones
S. Garel, M. Garcia-Dominguez, P. Charnay
Development 2000 127: 5297-5307;
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