Opposing FGF and retinoid pathways: A signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis

BioEssays

Volumn 26, Issue 8, 2004, Pages 857-869

  Del Corral, Ruth Diez ^a   Storey, Kate G ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; RETINOIC ACID; RETINOID;

ANIMAL TISSUE; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE; GENE ASSIGNMENT; GENE SWITCHING; HOX GENE; MESODERM; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN DOMAIN; REVIEW; VERTEBRATE;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; EMBRYO; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; MESODERM; MODELS, BIOLOGICAL; RETINOIDS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SPINAL CORD;

VERTEBRATA;

EID: 4344583103     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20080     Document Type: Review

References (105)

1. Storey KG. 2002. Vertebrate Neurogenesis. In: Tickle C, editor. Molecular Basis of Patterning in Vertebrate Development, Frontiers in Molecular Biology. Oxford: Oxford University Press, p 90-113.
2. Pera EM, Ikeda A, Eivers E, De Robertis EM. 2003. Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev 17:3023-3028.
3. Sheng G, dos Reis M, Stern CD. 2003. Churchill, a zinc finger transcriptional activator, regulates the transition between gastrulation and neurulation. Cell 115:603-613.
4. Wilson SI, Edlund T. 2001. Neural induction: toward a unifying mechanism. Nat Neurosci 4 Suppl:1161-1168.
5. Wilson SW, Houart C. 2004. Early steps in the development of the forebrain. Dev Cell 6:167-181.
6. Selleck MA, Bronner-Fraser M. 1995. Origins of the avian neural crest: the role of neural plate-epidermal interactions. Development 121: 525-538.
7. Brown JM, Storey KG. 2000. A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal cell fates. Current Biology 10:869-872.
8. Jessell TM. 2000. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20-29.
9. Itasaki N, Sharpe J, Morrison A, Krumlauf R. 1996. Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron 16:487-500.
10. Gould A, Itasaki N, Krumlauf R. 1998. Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21:39-51.
11. 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.
12. 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.
13. Omelchenko N, Lance-Jones C. 2003. Programming neural Hoxd10: in vivo evidence that early node-associated signals predominate over paraxial mesoderm signals at posterior spinal levels. Dev Biol 261:99-115.
14. Ang SL, Rossant J. 1993. Anterior mesendoderm induces mouse Engrailed genes in explant cultures. Development 118:139-149.
15. Ang SL, Conlon RA, Jin O, Rossant J. 1994. Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120:2979-2989.
16. Bang AG, Papalopulu N, Kintner C, Goulding MD. 1997. Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. Development 124:2075-2085.
17. 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.
18. Woo K, Fraser SE. 1997. Specification of the zebrafish nervous system by nonaxial signals. Science 277:254-257.
19. Koshida S, Shinya M, Mizuno T, Kuroiwa A, Takeda H. 1998. Initial anteroposterior pattern of the zebrafish central nervous system is determined by differential competence of the epiblast. Development 125:1957-1966.
20. 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.
21. Cox WG, Hemmati-Brivanlou A. 1995. Caudalization of neural fate by tissue recombination and bFGF. Development 121:4349-4358.
22. Lamb TM, Harland RM. 1995. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development 121:3627-3636.
23. Storey KG, Goriely A, Sargent CM, Brown JM, Burns HD, et al. 1998. Early posterior neural tissue is induced by FGF in the chick embryo. Development 125:473-484.
24. McGrew LL, Lai CJ, Moon RT. 1995. Specification of the anteroposterior neural axis through synergistic interaction of the Wnt signaling cascade with noggin and follistatin. Developmental Biology 172:337-342.
25. Nordstrom U, Jessell TM, Edlund T. 2002. Progressive induction of caudal neural character by graded Wnt signaling. Nat Neurosci 5:525-532.
26. Sharpe CR. 1991. Retinoic acid can mimic endogenous signals involved in transformation of the Xenopus nervous system. Neuron 7: 239-247.
27. Blumberg B, Bolado J, Jr., Moreno TA, Kintner C, Evans RM, et al. 1997. An essential role for retinoid signaling in anteroposterior neural patterning. Development 124:373-379.
28. Thisse B, Wright CV, Thisse C. 2000. Activin- and Nodal-related factors control antero-posterior patterning of the zebrafish embryo. Nature 403: 425-428.
29. 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.
30. Momoi A, Yoda H, Steinbeisser H, Fagotto F, Kondoh H, et al. 2003. Analysis of Wnt8 for neural posteriorizing factor by identifying Frizzled 8c and Frizzled 9 as functional receptors for Wnt8. Mech Dev 120:477-489.
31. Oosterveen T, Niederreither K, Dolle P, Chambon P, Meijlink F, et al. 2003. Retinoids regulate the anterior expression boundaries of 5′ Hoxb genes in posterior hindbrain. Embo J 22:262-269.
32. 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.
33. Mathis L, Kulesa PM, Fraser SE. 2001. FGF receptor signalling is required to maintain neural progenitors during Hensen's node progression, Nat Cell Biol 3:559-566.
34. Mathis L, Nicolas JF. 2000. Different clonal dispersion in the rostral and caudal mouse central nervous system. Development 127:1277-1290.
35. Spann P, Ginsburg M, Rangini Z, Fainsod A, Eyal Giladi H, et al. 1994. The spatial and temporal dynamics of Sax1 (CHox3) homeobox gene expression in the chick's spinal cord. Development 120:1817-1828.
36. Henrique D, Tyler D, Kintner C, Heath JK, Lewis JH, et al. 1997. cash4, a novel achaete-scute homolog induced by Hensen's node during generation of the posterior nervous system. Genes Dev 11:603-615.
37. Bertrand N, Medevielle F, Pituello F. 2000. FGF signalling controls the timing of Pax6 activation in the neural tube. Development 127:4837-4843.
38. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, et al. 2003. Opposing FGF and Retinoid pathways control ventral neural patterning, neuronal differentiation and segmentation during body axis extension. Neuron 40:65-79.
39. Diez del Corral R, Breitkreuz DN, Storey KG. 2002. Onset of neuronal differentiation is regulated by paraxial mesoderm and requires attenuation of FGF signalling. Development 129:1681-1691.
40. Sechrist J, Bronner Fraser M. 1991. Birth and differentiation of reticular neurons in the chick hindbrain: ontogeny of the first neuronal population. Neuron 7:947-963.
41. Pituello F, Medevielle F, Foulquier F, Duprat AM. 1999. Activation of Pax6 depends on somitogenesis in the chick embryo cervical spinal cord. Development 126:587-596.
42. Lewis J. 1996. Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol 6:3-10.
43. Bertrand N, Castro DS, Guillemot F. 2002. Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517-530.
44. Scardigli R, Schuurmans C, Gradwohl G, Guillemot F. 2001. Cross-regulation between Neurogenin2 and pathways specifying neuronal identity in the spinal cord. Neuron 31:203-217.
45. Scardigli R, Baumer N, Gruss P, Guillemot F, Le Roux I. 2003. Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development 130:3269-3281.
46. Pierani A. Brenner-Morton S, Chiang C, Jessell TM. 1999. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97:903-915.
47. 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.
48. Maden M, Sonneveld E, van der Saag PT, Gale E. 1998. The distribution of endogenous retinoic acid in the chick embryo: implications for developmental mechanisms. Development 125:4133-4144.
49. 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.
50. Wilson L, Gale E, Maden M. 2003. The role of retinoic acid in the morphogenesis of the neural tube. J Anat 203:357-368.
51. Gale E, Zile M, Maden M, 1999. Hindbrain respecification in the retinoid-deficient quail. Mech Dev 89:43-54.
52. Mic FA, Haselbeck RJ, Cuenca AE, Duester G. 2002. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 129: 2271-2282.
53. Niederreither K, Vermot J, Fraulob V, Chambon P, Dolle P. 2002. Retinaldehyde dehydrogenase 2 (RALDH2)-independent patterns of retinoic acid synthesis in the mouse embryo. Proc Natl Acad Sci USA 99:16111-16116.
54. Sockanathan S, Jessell TM. 1998. Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94:503-514.
55. Sockanathan S, Perlmann T, Jessell TM. 2003. Retinoid receptor signaling in postmitotic motor neurons regulates rostrocaudal positional identity and axonal projection pattern. Neuron 40:97-111.
56. Lee SMK, Danielian PS, Fritzsch B, McMahon AP. 1997. Evidence that FGF8 signalling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development 124:959-969.
57. Qian X, Davis AA, Goderie SK, Temple S. 1997. FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 18:81-93.
58. Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, et al. 2001. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30:65-78.
59. Ying QL, Stavridis M, Griffiths D, Li M, Smith A. 2003. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21:183-186.
60. Bain G, Ray WJ, Yao M, Gottlieb DI. 1994. From embryonal carcinoma cells to neurons: the P19 pathway. Bioessays 16:343-348.
61. Papalopulu N, Kintner C. 1996. A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development 122:3409-3418.
62. Renoncourt Y, Carroll P, Filippi P, Arce V, Alonso S. 1998. Neurons derived in vitro from ES cells express homeoproteins characteristic of motoneurons and interneurons. Mech Dev 79:185-197.
63. Wichterle H, Lieberam I, Porter JA, Jessell TM. 2002. Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385-397.
64. Dubrulle J, Pourquie O. 2004. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427:419-422.
65. Abu-Abed S, Dolle P, Metzger D, Wood C, MacLean G, et al. 2003. Developing with lethal RA levels: genetic ablation of Rarg can restore the viability of mice lacking Cyp26a1. Development 130:1449-1459.
66. Dubrulle J, McGrew MJ, Pourquie O. 2001. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106:219-232.
67. Sawada A, Shinya M, Jiang YJ, Kawakami A, Kuroiwa A, et al. 2001. Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 128:4873-4880.
68. Moreno TA, Kintner C. 2004. Regulation of Segmental Patterning by Retinoic Acid Signaling during Xenopus Somitogenesis. Dev Cell 6: 205-218.
69. Maerz WJ, Baselga J, Reuter VE, Mellado B, Myers ML, et al. 1998. FGF4 dissociates anti-tumorigenic from differentiation signals of retinoic acid in human embryonal carcinomas. Oncogene 17:761-767.
70. Pertovaara L, Tienari J, Vainikka S, Partanen J, Saksela O, et al. 1993. Modulation of fibroblast growth factor receptor expression and signalling during retinoic acid-induced differentiation of Tera-2 teratocarcinoma cells. Biochem Biophys Res Commun 191:149-156.
71. Liaudet-Coopman ED, Wellstein A. 1996. Regulation of gene expression of a binding protein for fibroblast growth factors by retinoic acid. J Biol Chem 271:21303-21308.
72. Brondani V, Klimkait T, Egly JM, Hamy F. 2002. Promoter of FGF8 reveals a unique regulation by unliganded RARalpha. J Mol Biol 319: 715-728.
73. Antonyak MA, McNeill CJ, Wakshlag JJ, Boehm JE, Cerione RA. 2003. Activation of the Ras-ERK pathway inhibits retinoic acid-induced stimulation of tissue transglutaminase expression in NIH3T3 cells. J Biol Chem 278:15859-15866.
74. Mercader N, Leonardo E, Piedra ME, Martinez AC, Ros MA, et al. 2000. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127:3961-3970.
75. Irving C, Mason I. 2000. Signalling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 127:177-186.
76. Vasiliauskas D, Stern CD. 2001. Patterning the embryonic axis, fgf signaling and how vertebrate embryos measure time. Cell 106:133-136.
77. 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.
78. Dasen JS, Liu JP, Jessell TM. 2003. Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425:926-933.
79. Kmita M, Duboule D. 2003. Organizing axes in time and space; 25 years of colinear tinkering. Science 301:331-333.
80. Pownall ME, Isaacs HV, Slack JM. 1998. Two phases of Hox gene regulation during early Xenopus development. Curr Biol 8:673-676.
81. Zakany J, Kmita M, Alarcon P, De la Pompa JL, Duboule D. 2001. Localised and transient transcription of Hox genes suggests a link between patterning and the segmentation clock. Cell 106:207-217.
82. Pourquie O. 2003. The segmentation clock: converting embryonic time into spatial pattern. Science 301:328-330.
83. Weston AD, Blumberg B, Underhill TM. 2003. Active repression by unliganded retinoid receptors in development: less is sometimes more. J Cell Biol 161:223-228.
84. McMahon JA, Takada S, Zimmerman LB, Fan CM, Harland RM, et al. 1998. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev 12: 1438-1452.
85. Liem KF, Jessell TM, Briscoe J. 2000. Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127:4855-4866.
86. Patten I, Placzek M. 2002. Opponent activities of Shh and BMP signaling during floor plate induction in vivo. Curr Biol 12:47-52.
87. Gabay L, Lowell S, Rubin LL, Anderson DJ. 2003. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40:485-499.
88. Briscoe J, Pierani A, Jessell TM, Ericson J. 2000. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435-445.
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. Brewster R, Mullor JL, Ruiz i Altaba A. 2000. Gli2 functions in FGF signaling during antero-posterior patterning. Development 127:4395-4405.
91. Sela-Donenfeld D, Kalcheim C. 2000. Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Development 127:4845-4854.
92. Burstyn-Cohen T, Kalcheim C. 2002. Association between the cell cycle and neural crest delamination through specific regulation of G1/S transition. Dev Cell 3:383-395.
93. Stafford D, Prince VE. 2002. Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development, Curr Biol 12: 1215-1220.
94. Davis GK, Patel NH. 2002. Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu Rev Entomol 47:669-699.
95. Stollewerk A, Schoppmeier M, Damen WG. 2003. Involvement of Notch and Delta genes in spider segmentation. Nature 423:863-865.
96. Garcia Martinez V, Alvarez IS, Schoenwolf GC. 1993. Locations of the ectodermal and nonectodermal subdivisions of the epiblast at stages 3 and 4 of avian gastrulation and neurulation. J Exp Zool 267:431-446.
97. Psychoyos D, Stern CD. 1996. Fates and migratory routes of primitive streak cells in the chick embryo. Development 122:1523-1534.
98. Kimmel CB, Warga RM, Schilling TF. 1990. Origin and organization of the zebrafish fate map. Development 108:581-594.
99. 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.
100. Chapman SC, Schubert FR, Schoenwolf GC, Lumsden A. 2002. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev Biol 245:187-199.
101. Blentic A, Gale E, Maden M. 2003. Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Dev Dyn 227:114-127.
102. Sagerstrom CG, Grinbalt Y, Sive H. 1996. Anteroposterior patterning in the zebrafish. Danio rerio: an explant assay reveals inductive and suppressive cell interactions. Development 122:1873-1883.
103. Storey KG, Selleck MA, Stern CD. 1995. Neural induction and regionalisation by different subpopulations of cells in Hensen's node. Development. 121:417-428.
104. Beddington RSP. 1994. Induction of a second neural axis by the mouse node. Development 120:613-620.
105. Bang AG, Papalopulu N, Goulding MD, Kintner C. 1999. Expression of Pax-3 in the lateral neural plate is dependent on a Wnt-mediated signal from posterior nonaxial mesoderm. Dev Biol 212:366-380.