An early role for Wnt signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity

PLoS Biology

Volumn 4, Issue 8, 2006, Pages 1438-1452

  Nordström, Ulrika ^a   Maier, Esther ^a   Jessell, Thomas M ^b   Edlund, Thomas ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; RETINOIC ACID; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR; WNT PROTEIN; AVIAN PROTEIN; HOMEODOMAIN PROTEIN; T BOX TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM; DNA FINGERPRINTING; DORSAL ROOT; EXPLANT; GASTRULA; GENE EXPRESSION; GENETIC TRAIT; HOX GENE; MOTONEURON; NEURAL STEM CELL; NEURAL TUBE; NEUROECTODERM; SPINAL CORD; VENTRAL ROOT; ANIMAL; CHICK EMBRYO; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HOMEOBOX; METABOLISM; PRENATAL DEVELOPMENT; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; STEM CELL;

VERTEBRATA;

ANIMALS; AVIAN PROTEINS; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; MOTOR NEURONS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELLS; T-BOX DOMAIN PROTEINS; TRETINOIN; WNT PROTEINS;

EID: 33747353254     PISSN: 15457885     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0040252     Document Type: Article

References (94)

1. Guthrie S (2004) Neuronal development: Putting motor neurons in their place. Curr Biol 14: R166-168.
2. Jessell TM (2000) Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nat Rev Genet 1: 20-29.
3. Lumsden A, Krumlauf R (1996) Patterning the vertebrate neuraxis. Science 274: 1109-1115.
4. Briscoe J, Ericson J (1999) The specification of neuronal identity by graded Sonic Hedgehog signaling. Semin Cell Dev Biol 10: 353-362.
5. Helms AW, Johnson JE (2003) Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol 13: 42-49.
6. Bel-Vialar S, Itasaki N, Krumlauf R (2002) Initiating Hox gene expression: In the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129: 5103-5115.
7. Dasen JS, Liu JP, Jessell TM (2003) Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425: 926-933.
8. Liu JP, Laufer E, Jessell TM (2001) Assigning the positional identity of spinal motor neurons. Rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32: 997-1012.
9. Sockanathan S, Perlmann T, Jessell TM (2003) Retinoid receptor signaling in post-mitotic motor neurons regulates rostrocaudal positional identity and axonal projection pattern. Neuron 40: 97-111.
10. Sharma K, Sheng HZ, Lettieri K, Li H, Karavanov A, et al. (1998) LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95: 817-828.
11. Guidato S, Prin F, Guthrie S (2003) Somatic motoneurone specification in the hindbrain: The influence of somite-derived signals, retinoic acid, and Hoxa3. Development 130: 2981-2996.
12. Briscoe J, Ericson J (2001) Specification of neuronal fates in the ventral neural tube. Curr Opin Neurobiol 11: 43-49.
13. Carpenter EM (2002) Hox genes and spinal cord development. Dev Neurosci 24: 24-34.
14. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, et al. (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40: 65-79.
15. Trainor PA, Krumlauf R (2001) Hox genes, neural crest cells, and branchial arch patterning. Curr Opin Cell Biol 13: 698-705.
16. Shah V, Drill E, Lance-Jones C (2004) Ectopic expression of Hoxd10 in thoracic spinal segments induces motoneurons with a lumbosacral molecular profile and axon projections to the limb. Dev Dyn 231: 43-56.
17. Bell E, Wingate RJ, Lumsden A (1999) Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284: 2168-2171.
18. Jungbluth S, Bell E, Lumsden A (1999) Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development 126: 2751-2758.
19. McClintock JM, Kheirbek MA, Prince VE (2002) Knockdown of duplicated zebrafish hoxb1 genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. Development 129: 2339-2354.
20. Briscoe J, Wilkinson DG (2004) Establishing neuronal circuitry: Hox genes make the connection. Genes Dev 18: 1643-1648.
21. Dasen JS, Tice BC, Brenner-Morton S, Jessell TM (2005) A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123: 477-491.
22. Ehrman LA, Yutzey KE (2001) Anterior expression of the caudal homolog cCdx-B activates a posterior genetic program in avian embryos. Dev Dyn 221: 412-421.
23. Charite J, de Graaff W, Consten D, Reijnen MJ, Korving J, et al. (1998) Transducing positional information to the Hox genes: Critical interaction of cdx gene products with position-sensitive regulatory elements. Development 125: 4349-4358.
24. Isaacs HV, Pownall ME, Slack JM (1998) Regulation of Hox gene expression and posterior development by the Xenopus caudal homolog Xcad3. Embo J 17: 3413-3427.
25. van den Akker E, Forlani S, Chawengsaksophak K, de Graaff W, Beck F, et al. (2002) Cdx1 and Cdx2 have overlapping functions in anteroposterior patterning and posterior axis elongation. Development 129: 2181-2193.
26. Marom K, Shapira E, Fainsod A (1997) The chicken caudal genes establish an anterior-posterior gradient by partially overlapping temporal and spatial patterns of expression. Mech Dev 64: 41-52.
27. Deschamps J, van den Akker E, Forlani S, De Graaff W, Oosterveen T, et al. (1999) Initiation, establishment, and maintenance of Hox gene expression patterns in the mouse. Int J Dev Biol 43: 635-650.
28. Shimizu T, Bae YK, Muraoka O, Hibi M (2005) Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev Biol 279: 125-141.
29. Niederreither K, Subbarayan V, Dolle P, Chambon P (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21: 444-448.
30. Dupe V, Lumsden A (2001) Hindbrain patterning involves graded responses to retinoic acid signaling. Development 128: 2199-2208.
31. Muhr J, Graziano E, Wilson S, Jessell TM, Edlund T (1999) Convergent inductive signals specify midbrain, hindbrain, and spinal cord identity in gastrula stage chick embryos. Neuron 23: 689-702.
32. Nordstrom U, Jessell TM, Edlund T (2002) Progressive induction of caudal neural character by graded Wnt signaling. Nat Neurosci 5: 525-532.
33. Nieto MA, Bradley LC, Wilkinson DG (1991) Conserved segmental expression of Krox-20 in the vertebrate hindbrain and its relationship to lineage restriction. Development Suppl 2: 59-62.
34. Ahn DG, Ruvinsky I, Oates AC, Silver LM, Ho RK (2000) tbx20, a new vertebrate T-box gene expressed in the cranial motor neurons and developing cardiovascular structures in zebrafish. Mech Dev 95: 253-258.
35. Iio A, Koide M, Hidaka K, Morisaki T (2001) Expression pattern of novel chick T-box gene, tbx20. Dev Genes Evol 211: 559-562.
36. Kraus F, Haenig B, Kispert A (2001) Cloning and expression analysis of the mouse T-box gene tbx20. Mech Dev 100: 87-91.
37. Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R (1998) A role for SOX1 in neural determination. Development 125: 1967-1978.
38. Uchikawa M, Kamachi Y, Kondoh H (1999) Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: Their expression during embryonic organogenesis of the chicken. Mech Dev 84: 103-120.
39. Uwanogho D, Rex M, Cartwright EJ, Pearl G, Healy C, et al. (1995) Embryonic expression of the chicken Sox2, Sox3, and Sox11 genes suggests an interactive role in neuronal development. Mech Dev 49: 23-36.
40. Rex M, Orme A, Uwanogho D, Tointon K, Wigmore PM, et al. (1997) Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn 209: 323-332.
41. Hidalgo-Sanchez M, Simeone A, Alvarado-Mallart RM (1999) Fgf8 and Gbx2 induction concomitant with Otx2 repression is correlated with midbrain-hindbrain fate of caudal prosencephalon. Development 126: 3191-3203.
42. Millet S, Campbell K, Epstein DJ, Losos K, Harris E, et al. (1999) A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature 401: 161-164.
43. Porter JA, von Kessler DP, Ekker SC, Young KE, Lee JJ, et al. (1995) The product of hedgehog autoproteolytic cleavage active in local and long-range signaling. Nature 374: 363-366.
44. Roelink H, Porter JA, Chiang C, Tanabe Y, Chang DT, et al. (1995) Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81: 445-455.
45. Yamaguchi TP (2001) Heads or tails: Wnts and anterior-posterior patterning. Curr Biol 11: R713-724.
46. Karabagli H, Karabagli P, Ladher RK, Schoenwolf GC (2002) Comparison of the expression patterns of several fibroblast growth factors during chick gastrulation and neurulation. Anat Embryol (Berl) 205: 365-370.
47. Chapman SC, Brown R, Lees L, Schoenwolf GC, Lumsden A (2004) Expression analysis of chick Wnt and frizzled genes and selected inhibitors in early chick patterning. Dev Dyn 229: 668-676.
48. McGrew LL, Hoppler S, Moon RT (1997) Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mech Dev 69: 105-114.
49. Wilson S, Rydstrom A, Trimborn T, Willert K, Nusse R, et al. (2001) The status of Wnt signaling regulates neural and epidermal fates in the chick embryo. Nature 411: 325-330.
50. Hsieh JC, Rattner A, Smallwood PM, Nathans J (1999) Biochemical characterization of Wnt-frizzled interactions using a soluble, biologically active vertebrate Wnt protein. Proc Natl Acad Sci U S A 96: 3546-3551.
51. Mohammadi M, McMahon G, Sun L, Tang C, Hirth P, et al. (1997) Structures of the tyrosine kinase domain of fibroblast growth factor receptor in complex with inhibitors. Science 276: 955-960.
52. Moreno TA, Kintner C (2004) Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev Cell 6: 205-218.
53. Ericson J, Muhr J, Placzek M, Lints T, Jessell TM, et al. (1995) Sonic hedgehog induces the differentiation of ventral forebrain neurons: A common signal for ventral patterning within the neural tube. Cell 81: 747-756.
54. Gunhaga L, Jessell TM, Edlund T (2000) Sonic hedgehog signaling at gastrula stages specifies ventral telencephalic cells in the chick embryo. Development 127: 3283-3293.
55. Candia AF, Wright CV (1996) Differential localization of Mox-1 and Mox-2 proteins indicates distinct roles during development. Int J Dev Biol 40: 1179-1184.
56. Kispert A, Ortner H, Cooke J, Herrmann BG (1995) The chick Brachyury gene: Developmental expression pattern and response to axial induction by localized activin. Dev Biol 168: 406-415.
57. Swindell EC, Thaller C, Sockanathan S, Petkovich M, Jessell TM, et al. (1999) Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev Biol 216: 282-296.
58. Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dolle P (2000) Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127: 75-85.
59. Berggren K, McCaffery P, Drager U, Forehand CJ (1999) Differential distribution of retinoic acid synthesis in the chicken embryo as determined by immunolocalization of the retinoic acid synthetic enzyme, RALDH-2. Dev Biol 210: 288-304.
60. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, et al. (1999) Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361-365.
61. Heisenberg CP, Houart C, Take-Uchi M, Rauch GJ, Young N, et al. (2001) A mutation in the Gsk3-binding domain of zebrafish Masterblind/Axin1 leads to a fate transformation of telencephalon and eyes to diencephalon. Genes Dev 15: 1427-1434.
62. Fekany-Lee K, Gonzalez E, Miller-Bertoglio V, Solnica-Krezel L (2000) The homeobox gene bozozok promotes anterior neuroectoderm formation in zebrafish through negative regulation of BMP2/4 and Wnt pathways. Development 127: 2333-2345.
63. Erter CE, Wilm TP, Basler N, Wright CV, Solnica-Krezel L (2001) Wnt8 is required in lateral mesendodermal precursors for neural posteriorization in vivo. Development 128: 3571-3583.
64. Domingos PM, Itasaki N, Jones CM, Mercurio S, Sargent MC, et al. (2001) The Wnt/beta-catenin pathway posteriorizes neural tissue in Xenopus by an indirect mechanism requiring FGF signaling. Dev Biol 239: 148-160.
65. Fredieu JR, Cui Y, Maier D, Danilchik MV, Christian JL (1997) Xwnt-8 and lithium can act upon either dorsal mesodermal or neurectodermal cells to cause a loss of forebrain in Xenopus embryos. Dev Biol 186: 100-114.
66. Kiecker C, Niehrs C (2001) A morphogen gradient of Wnt/beta-catenin signaling regulates anteroposterior neural patterning in Xenopus. Development 128: 4189-4201.
67. Kudoh T, Wilson SW, Dawid IB (2002) Distinct roles for Fgf, Wnt, and retinoic acid in posteriorizing the neural ectoderm. Development 129: 4335-4346.
68. Popperl H, Schmidt C, Wilson V, Hume CR, Dodd J, et al. (1997) Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm. Development 124: 2997-3005.
69. Takada S, Stark KL, Shea MJ, Vassileva G, McMahon JA, et al. (1994) Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev 8: 174-189.
70. Pilon N, Oh K, Sylvestre JR, Bouchard N, Savory J, et al. (2006) Cdx4 is a direct target of the canonical Wnt pathway. Dev Biol 289: 55-63.
71. Lickert H, Domon C, Huls G, Wehrle C, Duluc I, et al. (2000) Wnt/beta-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine. Development 127: 3805-3813.
72. Prinos P, Joseph S, Oh K, Meyer BI, Gruss P, et al. (2001) Multiple pathways governing Cdx1 expression during murine development. Dev Biol 239: 257-269.
73. Ikeya M, Takada S (2001) Wnt-3a is required for somite specification along the anteroposterior axis of the mouse embryo and for regulation of Cdx1 expression. Mech Dev 103: 27-33.
74. Taylor JK, Levy T, Suh ER, Traber PG (1997) Activation of enhancer elements by the homeobox gene Cdx2 is cell- line specific. Nucleic Acids Res 25: 2293-2300.
75. Subramanian V, Meyer BI, Gruss P (1995) Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell 83: 641-653.
76. Kolm PJ, Apekin V, Sive H (1997) Xenopus hindbrain patterning requires retinoid signaling. Dev Biol 192: 1-16.
77. Grandel H, Lun K, Rauch GJ, Rhinn M, Piotrowski T, et al. (2002) Retinoic acid signaling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 129: 2851-2865.
78. Diez del Corral R, Storey KG (2004) Opposing FGF and retinoid pathways: A signaling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26: 857-869.
79. Crossley PH, Martin GR (1995) The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121: 439-451.
80. Hume CR, Dodd J (1993) Cwnt-8C: A novel Wnt gene with a potential role in primitive streak formation and hindbrain organization. Development 119: 1147-1160.
81. Swindell EC, Eichele G (1999) Retinoid metabolizing enzymes in development. Biofactors 10: 85-89.
82. Lekven AC, Thorpe CJ, Waxman JS, Moon RT (2001) Zebrafish wnt8 encodes two wnt8 proteins on a bicistronic transcript and is required for mesoderm and neurectoderm patterning. Dev Cell 1: 103-114.
83. Muhr J, Jessell TM, Edlund T (1997) Assignment of early caudal identity to neural plate cells by a signal from caudal paraxial mesoderm. Neuron 19: 487-502.
84. Ensini M, Tsuchida TN, Belting HG, Jessell TM (1998) The control of rostrocaudal pattern in the developing spinal cord: Specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 125: 969-982.
85. Begemann G, Schilling TF, Rauch GJ, Geisler R, Ingham PW (2001) The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128: 3081-3094.
86. Yoshikawa Y, Fujimori T, McMahon AP, Takada S (1997) Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev Biol 183: 234-242.
87. Delfino-Machin M, Lunn JS, Breitkreuz DN, Akai J, Storey KG (2005) Specification and maintenance of the spinal cord stem zone. Development 132: 4273-4283.
88. Novitch BG, Wichterle H, Jessell TM, Sockanathan S (2003) A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40: 81-95.
89. Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, et al. (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90: 169-180.
90. Lohnes D (2003) The Cdx1 homeodomain protein: An integrator of posterior signaling in the mouse. Bioessays 25: 971-980.
91. Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morph 88: 49-92.
92. Shibamoto S, Higano K, Takada R, Ito F, Takeichi M, et al. (1998) Cytoskeletal reorganization by soluble Wnt-3a protein signaling. Genes Cells 3: 659-670.
93. Schaeren-Wiemers N, Gerfin-Moser A (1993) A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: In situ hybridization using digoxigenin-labeled cRNA probes. Histochemistry 100: 431-440.
94. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, et al. (1994) Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79: 957-970.