Lrrn1 is required for formation of the midbrain-hindbrain boundary and organiser through regulation of affinity differences between midbrain and hindbrain cells in chick

Developmental Biology

Volumn 352, Issue 2, 2011, Pages 341-352

  Tossell, Kyoko ^a,d   Andreae, Laura C ^b   Cudmore, Chloe ^a   Lang, Emily ^a   Muthukrishnan, Uma ^a   Lumsden, Andrew ^b   Gilthorpe, Jonathan D ^c   Irving, Carol ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UMEÅ UNIVERSITY   (Sweden)

^d UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Boundary; Capricious; Lrrn1; Midbrain hindbrain boundary organiser; Tartan

Indexed keywords

FIBROBLAST GROWTH FACTOR 8; GLYCOSYLTRANSFERASE; LEUCINE RICH REPEAT NEURONAL 1 PROTEIN; LUNATIC FRINGE PROTEIN; NOTCH RECEPTOR; PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN DEVELOPMENT; CELL COMPARTMENTALIZATION; CELL FATE; CHICK; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; EMBRYO; ENZYME REGULATION; GENE FUNCTION; GENE SEGREGATION; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; RHOMBENCEPHALON; SIGNAL TRANSDUCTION;

EID: 79953028498     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.02.002     Document Type: Article

References (61)

1. Adams K.A., Maida J.M., Golden J.A., Riddle R.D. The transcription factor Lmx1b maintains Wnt1 expression within the isthmic organizer. Development 2000, 127:1857-1867.
2. Andreae L.C., Peukert D., Lumsden A., Gilthorpe J.D. Analysis of Lrrn1 expression and its relationship to neuromeric boundaries during chick neural development. Neural Dev. 2007, 2:22.
3. Bottcher R.T., Pollet N., Delius H., Niehrs C. The transmembrane protein XFLRT3 forms a complex with FGF receptors and promotes FGF signalling. Nat. Cell Biol. 2004, 6:38-44.
4. Broccoli V., Boncinelli E., Wurst W. The caudal limit of Otx2 expression positions the isthmic organizer. Nature 1999, 401:164-168.
5. Campbell R.E., Tour O., Palmer A.E., Steinbach P., Baird G.S., Zacharias D.A., Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl Acad. Sci. 2002, 99:7877-7882.
6. Canning C.A., Lee L., Irving C., Mason I., Jones C.M. Sustained interactive Wnt and FGF signaling is required to maintain isthmic identity. Dev. Biol. 2007, 305:276-286.
7. Cheng Y.C., Amoyel M., Qiu X., Jiang Y.J., Xu Q., Wilkinson D.G. Notch activation regulates the segregation and differentiation of rhombomere boundary cells in the zebrafish hindbrain. Dev. Cell 2004, 6:539-550.
8. Chi C.L., Martinez S., Wurst W., Martin G.R. The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 2003, 130:2633-2644.
9. Christiansen J.H., Coles E.G., Robinson V., Pasini A., Wilkinson D.G. Screening from a subtracted embryonic chick hindbrain cDNA library: identification of genes expressed during hindbrain, midbrain and cranial neural crest development. Mech. Dev. 2001, 102:119-133.
10. Cooke J., Moens C., Roth L., Durbin L., Shiomi K., Brennan C., Kimmel C., Wilson S., Holder N. Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 2001, 128:571-580.
11. Crossley P.H., Martinez S., Martin G.R. Midbrain development induced by FGF8 in the chick embryo. Nature 1996, 380:66-68.
12. Garcia-Calero E., Garda A.L., Marin F., Puelles L. Expression of Lrrn1 marks the prospective site of the zona limitans thalami in the early embryonic chicken diencephalon. Gene Expr. Patterns 2006, 6:879-885.
13. Guo C., Qiu H.Y., Huang Y., Chen H., Yang R.Q., Chen S.D., Johnson R.L., Chen Z.F., Ding Y.Q. Lmx1b is essential for Fgf8 and Wnt1 expression in the isthmic organizer during tectum and cerebellum development in mice. Development 2007, 134:317-325.
14. Guthrie S., Lumsden A. Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 1991, 112:221-229.
15. Haines B.P., Gupta R., Jones C.M., Summerbell D., Rigby P.W. The NLRR gene family and mouse development: modified differential display PCR identifies NLRR-1 as a gene expressed in early somitic myoblasts. Dev. Biol. 2005, 281:145-159.
16. Haines B.P., Wheldon L.M., Summerbell D., Heath J.K., Rigby P.W. Regulated expression of FLRT genes implies a functional role in the regulation of FGF signalling during mouse development. Dev. Biol. 2006, 297:14-25.
17. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 1992, 195:231-272.
18. Hidalgo-Sanchez M., Millet S., Simeone A., Alvarado-Mallart R.M. Comparative analysis of Otx2, Gbx2, Pax2, Fgf8 and Wnt1 gene expressions during the formation of the chick midbrain/hindbrain domain. Mech. Dev. 1999, 81:175-178.
19. Irving C., Flenniken A., Alldus G., Wilkinson D.G. Cell-cell interactions and segmentation in the developing vertebrate hindbrain. Biochem. Soc. Symp. 1996, 62:85-95.
20. Irving C., Malhas A., Guthrie S., Mason I. Establishing the trochlear motor axon trajectory: role of the isthmic organiser and Fgf8. Development 2002, 129:5389-5398.
21. Irving C., Mason I. Signalling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 2000, 127:177-186.
22. Jungbluth S., Larsen C., Wizenmann A., Lumsden A. Cell mixing between the embryonic midbrain and hindbrain. Curr. Biol. 2001, 11:204-207.
23. Karaulanov E.E., Bottcher R.T., Niehrs C. A role for fibronectin-leucine-rich transmembrane cell-surface proteins in homotypic cell adhesion. EMBO Rep. 2006, 7:283-290.
24. Katahira T., Sato T., Sugiyama S., Okafuji T., Araki I., Funahashi J., Nakamura H. Interaction between Otx2 and Gbx2 defines the organizing center for the optic tectum. Mech. Dev. 2000, 91:43-52.
25. Langenberg T., Brand M. Lineage restriction maintains a stable organizer cell population at the zebrafish midbrain-hindbrain boundary. Development 2005, 132:3209-3216.
26. Lumsden A., Krumlauf R. Patterning the vertebrate neuraxis. Science 1996, 274:1109-1115.
27. Mao Y., Kerr M., Freeman M. Modulation of Drosophila retinal epithelial integrity by the adhesion proteins capricious and tartan. PLoS ONE 2008, 3:e1827.
28. Marin F., Puelles L. Patterning of the embryonic avian midbrain after experimental inversions: a polarizing activity from the isthmus. Dev. Biol. 1994, 163:19-37.
29. Martinez S., Crossley P.H., Cobos I., Rubenstein J.L., Martin G.R. FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development 1999, 126:1189-1200.
30. Martinez S., Marin F., Nieto M.A., Puelles L. Induction of ectopic engrailed expression and fate change in avian rhombomeres: intersegmental boundaries as barriers. Mech. Dev. 1995, 51:289-303.
31. Matsunaga E., Katahira T., Nakamura H. Role of Lmx1b and Wnt1 in mesencephalon and metencephalon development. Development 2002, 129:5269-5277.
32. McMahon A.P., Bradley A. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 1990, 62:1073-1085.
33. Mellitzer G., Xu Q., Wilkinson D.G. Eph receptors and ephrins restrict cell intermingling and communication. Nature 1999, 400:77-81.
34. Milan M., Cohen S.M. A re-evaluation of the contributions of Apterous and Notch to the dorsoventral lineage restriction boundary in the Drosophila wing. Development 2003, 130:553-562.
35. Milan M., Perez L., Cohen S.M. Boundary formation in the Drosophila wing: functional dissection of Capricious and Tartan. Dev. Dyn. 2005, 233:804-810.
36. Milan M., Weihe U., Perez L., Cohen S.M. The LRR proteins capricious and Tartan mediate cell interactions during DV boundary formation in the Drosophila wing. Cell 2001, 106:785-794.
37. Millet S., Bloch-Gallego E., Simeone A., Alvarado-Mallart R.M. The caudal limit of Otx2 gene expression as a marker of the midbrain/hindbrain boundary: a study using in situ hybridisation and chick/quail homotopic grafts. Development 1996, 122:3785-3797.
38. Millet S., Campbell K., Epstein D.J., Losos K., Harris E., Joyner A.L. A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature 1999, 401:161-164.
39. Mosyak L., Wood A., Dwyer B., Buddha M., Johnson M., Aulabaugh A., Zhong X., Presman E., Benard S., Kelleher K., et al. The structure of the Lingo-1 ectodomain, a module implicated in central nervous system repair inhibition. J. Biol. Chem. 2006, 281:36378-36390.
40. Nittenberg R., Patel K., Joshi Y., Krumlauf R., Wilkinson D.G., Brickell P.M., Tickle C., Clarke J.D. Cell movements, neuronal organisation and gene expression in hindbrains lacking morphological boundaries. Development 1997, 124:2297-2306.
41. O'Hara F.P., Beck E., Barr L.K., Wong L.L., Kessler D.S., Riddle R.D. Zebrafish Lmx1b.1 and Lmx1b.2 are required for maintenance of the isthmic organizer. Development 2005, 132:3163-3173.
42. Pan Y., Lin M.H., Tian X., Cheng H.T., Gridley T., Shen J., Kopan R. Gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev. Cell 2004, 7:731-743.
43. Reifers F., Bohli H., Walsh E.C., Crossley P.H., Stainier D.Y., Brand M. Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 1998, 125:2381-2395.
44. Sakurai K.T., Kojima T., Aigaki T., Hayashi S. Differential control of cell affinity required for progression and refinement of cell boundary during Drosophila leg segmentation. Dev. Biol. 2007, 309:126-136.
45. Shamim H., Mahmood R., Logan C., Doherty P., Lumsden A., Mason I. Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Development 1999, 126:945-959.
46. Shamim H., Mason I. Expression of Fgf4 during early development of the chick embryo. Mech. Dev. 1999, 85:189-192.
47. Shinza-Kameda M., Takasu E., Sakurai K., Hayashi S., Nose A. Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, capricious. Neuron 2006, 49:205-213.
48. Shishido E., Takeichi M., Nose A. Drosophila synapse formation: regulation by transmembrane protein with Leu-rich repeats, CAPRICIOUS. Science 1998, 280:2118-2121.
49. Taguchi A., Wanaka A., Mori T., Matsumoto K., Imai Y., Tagaki T., Tohyama M. Molecular cloning of novel leucine-rich repeat proteins and their expression in the developing mouse nervous system. Brain Res. Mol. Brain Res. 1996, 35:31-40.
50. Taniguchi H., Tohyama M., Takagi T. Cloning and expression of a novel gene for a protein with leucine-rich repeats in the developing mouse nervous system. Brain Res. Mol. Brain Res. 1996, 36:45-52.
51. Tossell, K., Kiecker, C., Wizenmann, A., Lang, E., Irving, C., submitted for publication. Notch signalling regulates formation of the boundary at the midbrain-hindbrain interface.
52. Trokovic R., Jukkola T., Saarimaki J., Peltopuro P., Naserke T., Weisenhorn D.M., Trokovic N., Wurst W., Partanen J. Fgfr1-dependent boundary cells between developing mid- and hindbrain. Dev. Biol. 2005, 278:428-439.
53. Wassarman K.M., Lewandoski M., Campbell K., Joyner A.L., Rubenstein J.L., Martinez S., Martin G.R. Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development 1997, 124:2923-2934.
54. Wizenmann A., Lumsden A. Segregation of rhombomeres by differential chemoaffinity. Mol. Cell. Neurosci. 1997, 9:448-459.
55. Wu J.Y., Rao Y. Fringe: defining borders by regulating the notch pathway. Curr. Opin. Neurobiol. 1999, 9:537-543.
56. Wurst W., Bally-Cuif L. Neural plate patterning: upstream and downstream of the isthmic organizer. Nat. Rev. Neurosci. 2001, 2:99-108.
57. Xu Q., Mellitzer G., Robinson V., Wilkinson D.G. In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 1999, 399:267-271.
58. Yaneza M., Gilthorpe J.D., Lumsden A., Tucker A.S. No evidence for ventrally migrating neural tube cells from the mid- and hindbrain. Dev. Dyn. 2002, 223:163-167.
59. Ye W., Bouchard M., Stone D., Liu X., Vella F., Lee J., Nakamura H., Ang S.L., Busslinger M., Rosenthal A. Distinct regulators control the expression of the mid-hindbrain organizer signal FGF8. Nat. Neurosci. 2001, 4:1175-1181.
60. Yuan S., Schoenwolf G.C. The spatial and temporal pattern of C-Lmx1 expression in the neuroectoderm during chick neurulation. Mech. Dev. 1999, 88:243-247.
61. Zervas M., Millet S., Ahn S., Joyner A.L. Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 2004, 43:345-357.