Hox proteins drive cell segregation and non-autonomous apical remodelling during hindbrain segmentation

Development (Cambridge)

Volumn 141, Issue 7, 2014, Pages 1492-1502

  Prin, Fabrice ^a   Serpente, Patricia ^a   Itasaki, Nobue ^a,b   Gould, Alex P ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Apical polarity; Cell affinities; Cell segregation; Cell sorting; Cell tension; Chick; Hindbrain; Hox; Mouse; Rhombomeres; Segmentation

Indexed keywords

CELL SURFACE PROTEIN; EPHRIN; HOX PROTEIN; HOX4 PROTEIN; RETINOIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CELL ADHESION; CELL ENLARGEMENT; CELL SELECTION; CHICK; ELECTROPORATION; HOX GENE; LOSS OF FUNCTION MUTATION; MOSAICISM; MOUSE; NEUROEPITHELIUM; NEUROMERE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RHOMBENCEPHALON;

APICAL POLARITY; CELL AFFINITIES; CELL SEGREGATION; CELL SORTING; CELL TENSION; CHICK; HINDBRAIN; HOX; MOUSE; RHOMBOMERES; SEGMENTATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CELL MOVEMENT; CHICK EMBRYO; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; MEMBRANE PROTEINS; MICE; RHOMBENCEPHALON; TRANSCRIPTION FACTORS;

EID: 84896278943     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.098954     Document Type: Article

References (107)

1. Alexander, T., Nolte, C. and Krumlauf, R. (2009). Hox genes and segmentation of the hindbrain and axial skeleton. Annu. Rev. Cell Dev. Biol. 25, 431-456.
2. Araujo, M. and Nieto, M. A. (1997). The expression of chick EphA7 during segmentation of the central and peripheral nervous system. Mech. Dev. 68, 173-177.
3. Barrow, J. R., Stadler, H. S. and Capecchi, M. R. (2000). Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development 127, 933-944.
4. Batlle, E. and Wilkinson, D. G. (2012). Molecular mechanisms of cell segregation and boundary formation in development and tumorigenesis. Cold Spring Harb. Perspect. Biol. 4, a008227.
5. Becker, N., Seitanidou, T., Murphy, P., Mattéi, M. G., Topilko, P., Nieto, M. A., Wilkinson, D. G., Charnay, P. and Gilardi-Hebenstreit, P. (1994). Several receptor tyrosine kinase genes of the Eph family are segmentally expressed in the developing hindbrain. Mech. Dev. 47, 3-17.
6. Behringer, R. R., Crotty, D. A., Tennyson, V. M., Brinster, R. L., Palmiter, R. D. and Wolgemuth, D. J. (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.
7. Bergemann, A. D., Cheng, H. J., Brambilla, R., Klein, R. and Flanagan, J. G. (1995). ELF-2, a new member of the Eph ligand family, is segmentally expressed in mouse embryos in the region of the hindbrain and newly forming somites. Mol. Cell. Biol. 15, 4921-4929.
8. Birgbauer, E. and Fraser, S. E. (1994). Violation of cell lineage restriction compartments in the chick hindbrain. Development 120, 1347-1356.
9. Blumberg, B., Bolado, J., Jr, Moreno, T. A., Kintner, C., Evans, R. M. and Papalopulu, N. (1997). An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
10. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R. and Capecchi, M. R. (1993). Loss of Hox-A1 (Hox-1. 6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075.
11. Conlon, R. A. and Rossant, J. (1992). Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116, 357-368.
12. Cooke, J., Moens, C., Roth, L., Durbin, L., Shiomi, K., Brennan, C., Kimmel, C., Wilson, S. and Holder, N. (2001). Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 128, 571-580.
13. Cooke, J. E., Kemp, H. A. and Moens, C. B. (2005). EphA4 is required for cell adhesion and rhombomere-boundary formation in the zebrafish. Curr. Biol. 15, 536-542.
14. Cordes, S. P. and Barsh, G. S. (1994). The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79, 1025-1034.
15. Curt, J. R., de Navas, L. F. and Sánchez-Herrero, E. (2013). Differential activity of Drosophila Hox genes induces myosin expression and can maintain compartment boundaries. PLoS ONE 8, e57159.
16. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
17. Dasen, J. S. and Jessell, T. M. (2009). Hox networks and the origins of motor neuron diversity. Curr. Top. Dev. Biol. 88, 169-200.
18. Dasen, J. S., Tice, B. C., Brenner-Morton, S. and Jessell, T. M. (2005). A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123, 477-491.
19. Davenne, M., Maconochie, M. K., Neun, R., Pattyn, A., Chambon, P., Krumlauf, R. and Rijli, F. M. (1999). Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22, 677-691.
20. Dupé, V. and Lumsden, A. (2001). Hindbrain patterning involves graded responses to retinoic acid signalling. Development 128, 2199-2208.
21. Estrada, B. and Sánchez-Herrero, E. (2001). The Hox gene Abdominal-B antagonizes appendage development in the genital disc of Drosophila. Development 128, 331-339.
22. Filas, B. A., Oltean, A., Majidi, S., Bayly, P. V., Beebe, D. C. and Taber, L. A. (2012). Regional differences in actomyosin contraction shape the primary vesicles in the embryonic chicken brain. Phys. Biol. 9, 066007.
23. Flenniken, A. M., Gale, N. W., Yancopoulos, G. D. and Wilkinson, D. G. (1996). Distinct and overlapping expression patterns of ligands for Eph-related receptor tyrosine kinases during mouse embryogenesis. Dev. Biol. 179, 382-401.
24. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
25. Fraser, S., Keynes, R. and Lumsden, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344, 431-435.
26. Frohman, M. A., Martin, G. R., Cordes, S. P., Halamek, L. P. and Barsh, G. S. (1993). Altered rhombomere-specific gene expression and hyoid bone differentiation in the mouse segmentation mutant, kreisler (kr). Development 117, 925-936.
27. Gale, N. W., Flenniken, A., Compton, D. C., Jenkins, N., Copeland, N. G., Gilbert, D. J., Davis, S., Wilkinson, D. G. and Yancopoulos, G. D. (1996). Elk-L3, a novel transmembrane ligand for the Eph family of receptor tyrosine kinases, expressed in embryonic floor plate, roof plate and hindbrain segments. Oncogene 13, 1343-1352.
28. Gandille, P., Narbonne-Reveau, K., Boissonneau, E., Randsholt, N., Busson, D. and Pret, A. M. (2010). Mutations in the polycomb group gene polyhomeotic lead to epithelial instability in both the ovary and wing imaginal disc in Drosophila. PLoS ONE 5, e13946.
29. Garcia-Bellido, A. (1968). Cell affinities in antennal homoeotic mutants of Drosophila melanogaster. Genetics 59, 487-499.
30. Garcia-Bellido, A., Ripoll, P. and Morata, G. (1973). Developmental compartmentalisation of the wing disk of Drosophila. Nat. New Biol. 245, 251-253.
31. Gavalas, A., Davenne, M., Lumsden, A., Chambon, P. and Rijli, F. M. (1997). Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124, 3693-3702.
32. Giudicelli, F., Taillebourg, E., Charnay, P. and Gilardi-Hebenstreit, P. (2001). Krox-20 patterns the hindbrain through both cell-autonomous and non cell-autonomous mechanisms. Genes Dev. 15, 567-580.
33. Giudicelli, F., Gilardi-Hebenstreit, P., Mechta-Grigoriou, F., Poquet, C. and Charnay, P. (2003). Novel activities of Mafb underlie its dual role in hindbrain segmentation and regional specification. Dev. Biol. 253, 150-162.
34. González-Reyes, A., Urquia, N., Gehring, W. J., Struhl, G. and Morata, G. (1990). Are cross-regulatory interactions between homoeotic genes functionally significant? Nature 344, 78-80.
35. Gould, A., Morrison, A., Sproat, G., White, R. A. and Krumlauf, R. (1997). Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev. 11, 900-913.
36. Gould, A., Itasaki, N. and Krumlauf, R. (1998). Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21, 39-51.
37. Gouti, M., Briscoe, J. and Gavalas, A. (2011). Anterior Hox genes interact with components of the neural crest specification network to induce neural crest fates. Stem Cells 29, 858-870.
38. Guidato, S., Prin, F. and Guthrie, S. (2003). Somatic motoneurone specification in the hindbrain: the influence of somite-derived signals, retinoic acid and Hoxa3. Development 130, 2981-2996.
39. Guthrie, S. and Lumsden, A. (1991). Formation and regeneration of rhombomere boundaries in the developing chick hindbrain. Development 112, 221-229.
40. Guthrie, S., Butcher, M. and Lumsden, A. (1991). Patterns of cell division and interkinetic nuclear migration in the chick embryo hindbrain. J. Neurobiol. 22, 742-754.
41. Guthrie, S., Prince, V. and Lumsden, A. (1993). Selective dispersal of avian rhombomere cells in orthotopic and heterotopic grafts. Development 118, 527-538.
42. Haines, B. P. and Rigby, P. W. (2007). Developmentally regulated expression of the LRRTM gene family during mid-gestation mouse embryogenesis. Gene Expr. Patterns 7, 23-29.
43. Hamburger, V. and Hamilton, H. L. (1992). A series of normal stages in the development of the chick embryo. 1951. Dev. Dyn. 195, 231-272.
44. Helmbacher, F., Pujades, C., Desmarquet, C., Frain, M., Rijli, F. M., Chambon, P. and Charnay, P. (1998). Hoxa1 and Krox-20 synergize to control the development of rhombomere 3. Development 125, 4739-4748.
45. Heyman, I., Faissner, A. and Lumsden, A. (1995). Cell and matrix specialisations of rhombomere boundaries. Dev. Dyn. 204, 301-315.
46. Iimura, T. and Pourquié, O. (2006). Collinear activation of Hoxb genes during gastrulation is linked to mesoderm cell ingression. Nature 442, 568-571.
47. Irving, C., Nieto, M. A., DasGupta, R., Charnay, P. and Wilkinson, D. G. (1996). Progressive spatial restriction of Sek-1 and Krox-20 gene expression during hindbrain segmentation. Dev. Biol. 173, 26-38.
48. Itasaki, N., Sharpe, J., Morrison, A. and Krumlauf, R. (1996). Reprogramming Hox expression in the vertebrate hindbrain: influence of paraxial mesoderm and rhombomere transposition. Neuron 16, 487-500.
49. Itasaki, N., Bel-Vialar, S. and Krumlauf, R. (1999). 'Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1, E203-E207.
50. Jimenez-Guri, E., Udina, F., Colas, J. F., Sharpe, J., Padrón-Barthe, L., Torres, M. and Pujades, C. (2010). Clonal analysis in mice underlines the importance of rhombomeric boundaries in cell movement restriction during hindbrain segmentation. PLoS ONE 5, e10112.
51. Kayam, G., Kohl, A., Magen, Z., Peretz, Y., Weisinger, K., Bar, A., Novikov, O., Brodski, C. and Sela-Donenfeld, D. (2013). A novel role for Pax6 in the segmental organization of the hindbrain. Development 140, 2190-2202.
52. Landsberg, K. P., Farhadifar, R., Ranft, J., Umetsu, D., Widmann, T. J., Bittig, T., Said, A., Jülicher, F. and Dahmann, C. (2009). Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr. Biol. 19, 1950-1955.
53. Lecuit, T. and Lenne, P. F. (2007). Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633-644.
54. Leonard, L., Horton, C., Maden, M. and Pizzey, J. A. (1995). Anteriorization of CRABP-I expression by retinoic acid in the developing mouse central nervous system and its relationship to teratogenesis. Dev. Biol. 168, 514-528.
55. Lewis, E. B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276, 565-570.
56. Lumsden, A. (1990). The cellular basis of segmentation in the developing hindbrain. Trends Neurosci. 13, 329-335.
57. Lumsden, A. and Keynes, R. (1989). Segmental patterns of neuronal development in the chick hindbrain. Nature 337, 424-428.
58. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-1115.
59. Maden, M., Horton, C., Graham, A., Leonard, L., Pizzey, J., Siegenthaler, G., Lumsden, A. and Eriksson, U. (1992). Domains of cellular retinoic acid-binding protein I (CRABP I) expression in the hindbrain and neural crest of the mouse embryo. Mech. Dev. 37, 13-23.
60. Mahmood, R., Kiefer, P., Guthrie, S., Dickson, C. and Mason, I. (1995). Multiple roles for FGF-3 during cranial neural development in the chicken. Development 121, 1399-1410.
61. Manzanares, M., Trainor, P. A., Nonchev, S., Ariza-McNaughton, L., Brodie, J., Gould, A., Marshall, H., Morrison, A., Kwan, C. T., Sham, M. H. et al. (1999). The role of kreisler in segmentation during hindbrain development. Dev. Biol. 211, 220-237.
62. Marín, F. and Charnay, P. (2000). Hindbrain patterning: FGFs regulate Krox20 and mafB/kr expression in the otic/preotic region. Development 127, 4925-4935.
63. Martinez-Arias, A. and Lawrence, P. A. (1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639-642.
64. McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
65. McKay, I. J., Muchamore, I., Krumlauf, R., Maden, M., Lumsden, A. and Lewis, J. (1994). The kreisler mouse: a hindbrain segmentation mutant that lacks two rhombomeres. Development 120, 2199-2211.
66. McLarren, K. W., Litsiou, A. and Streit, A. (2003). DLX5 positions the neural crest and preplacode region at the border of the neural plate. Dev. Biol. 259, 34-47.
67. Megason, S. G. and McMahon, A. P. (2002). A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087-2098.
68. Mellitzer, G., Xu, Q. and Wilkinson, D. G. (1999). Eph receptors and ephrins restrict cell intermingling and communication. Nature 400, 77-81.
69. Mirenda, V., Jarmin, S. J., David, R., Dyson, J., Scott, D., Gu, Y., Lechler, R. I., Okkenhaug, K. and Marelli-Berg, F. M. (2007). Physiologic and aberrant regulation of memory T-cell trafficking by the costimulatory molecule CD28. Blood 109, 2968-2977.
70. Moens, C. B., Yan, Y. L., Appel, B., Force, A. G. and Kimmel, C. B. (1996). valentino: a zebrafish gene required for normal hindbrain segmentation. Development 122, 3981-3990.
71. Momose, T., Tonegawa, A., Takeuchi, J., Ogawa, H., Umesono, K. and Yasuda, K. (1999). Efficient targeting of gene expression in chick embryos by microelectroporation. Dev. Growth Differ. 41, 335-344.
72. Morata, G. and Garcia-Bellido, A. (1976). Developmental analysis of some mutants of the bithorax system of Drosophila. Rouxs Arch. Dev. Biol. 179, 125-143.
73. Morata, G. and Lawrence, P. A. (1975). Control of compartment development by the engrailed gene in Drosophila. Nature 255, 614-617.
74. Morrison, A., Ariza-McNaughton, L., Gould, A., Featherstone, M. and Krumlauf, R. (1997). HOXD4 and regulation of the group 4 paralog genes. Development 124, 3135-3146.
75. Nieto, M. A., Gilardi-Hebenstreit, P., Charnay, P. and Wilkinson, D. G. (1992). A receptor protein tyrosine kinase implicated in the segmental patterning of the hindbrain and mesoderm. Development 116, 1137-1150.
76. Ninomiya, H., David, R., Damm, E. W., Fagotto, F., Niessen, C. M. and Winklbauer, R. (2012). Cadherin-dependent differential cell adhesion in Xenopus causes cell sorting in vitro but not in the embryo. J. Cell Sci. 125, 1877-1883.
77. Nittenberg, R., Patel, K., Joshi, Y., Krumlauf, R., Wilkinson, D. G., Brickell, P. M., Tickle, C. and Clarke, J. D. (1997). Cell movements, neuronal organisation and gene expression in hindbrains lacking morphological boundaries. Development 124, 2297-2306.
78. Pattyn, A., Morin, X., Cremer, H., Goridis, C. and Brunet, J. F. (1997). Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124, 4065-4075.
79. Pöpperl, H., Bienz, M., Studer, M., Chan, S. K., Aparicio, S., Brenner, S., Mann, R. S. and Krumlauf, R. (1995). Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81, 1031-1042.
80. Prin, F., Ng, K. E., Thaker, U., Drescher, U. and Guthrie, S. (2005). Ephrin-As play a rhombomere-specific role in trigeminal motor axon projections in the chick embryo. Dev. Biol. 279, 402-419.
81. Rossel, M. and Capecchi, M. R. (1999). Mice mutant for both Hoxa1 and Hoxb1 show extensive remodeling of the hindbrain and defects in craniofacial development. Development 126, 5027-5040.
82. Sadl, V. S., Sing, A., Mar, L., Jin, F. and Cordes, S. P. (2003). Analysis of hindbrain patterning defects caused by the kreisler(enu) mutation reveals multiple roles of Kreisler in hindbrain segmentation. Dev. Dyn. 227, 134-142.
83. Schneider-Maunoury, S., Seitanidou, T., Charnay, P. and Lumsden, A. (1997). Segmental and neuronal architecture of the hindbrain of Krox-20 mouse mutants. Development 124, 1215-1226.
84. Sela-Donenfeld, D., Kayam, G. and Wilkinson, D. G. (2009). Boundary cells regulate a switch in the expression of FGF3 in hindbrain rhombomeres. BMC Dev. Biol. 9, 16.
85. Serpente, P., Tümpel, S., Ghyselinck, N. B., Niederreither, K., Wiedemann, L. M., Dollé, P., Chambon, P., Krumlauf, R. and Gould, A. P. (2005). Direct crossregulation between retinoic acid receptor beta and Hox genes during hindbrain segmentation. Development 132, 503-513.
86. Steinberg, M. S. (1963). Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141, 401-408.
87. Steinberg, M. S. (1970). Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J. Exp. Zool. 173, 395-433.
88. Steinberg, M. S. (2007). Differential adhesion in morphogenesis: a modern view. Curr. Opin. Genet. Dev. 17, 281-286.
89. Stoner, C. M. and Gudas, L. J. (1989). Mouse cellular retinoic acid binding protein: cloning, complementary DNA sequence, and messenger RNA expression during the retinoic acid-induced differentiation of F9 wild type and RA-3-10 mutant teratocarcinoma cells. Cancer Res. 49, 1497-1504.
90. Struhl, G. (1981). A gene product required for correct initiation of segmental determination in Drosophila. Nature 293, 36-41.
91. Studer, M., Gavalas, A., Marshall, H., Ariza-McNaughton, L., Rijli, F. M., Chambon, P. and Krumlauf, R. (1998). Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development 125, 1025-1036.
92. Takahashi, M. and Osumi, N. (2011). Pax6 regulates boundary-cell specification in the rat hindbrain. Mech. Dev. 128, 289-302.
93. Theil, T., Frain, M., Gilardi-Hebenstreit, P., Flenniken, A., Charnay, P. and Wilkinson, D. G. (1998). Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. Development 125, 443-452.
94. Theil, T., Ariza-McNaughton, L., Manzanares, M., Brodie, J., Krumlauf, R. and Wilkinson, D. G. (2002). Requirement for downregulation of kreisler during late patterning of the hindbrain. Development 129, 1477-1485.
95. Townes, P. L. and Holtfreter, J. (1955). Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128, 53-120.
96. Tschopp, P. and Duboule, D. (2011). A genetic approach to the transcriptional regulation of Hox gene clusters. Annu. Rev. Genet. 45, 145-166.
97. Tümpel, S., Wiedemann, L. M. and Krumlauf, R. (2009). Hox genes and segmentation of the vertebrate hindbrain. Curr. Top. Dev. Biol. 88, 103-137.
98. 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.
99. Vincent, J. P. and O'Farrell, P. H. (1992). The state of engrailed expression is not clonally transmitted during early Drosophila development. Cell 68, 923-931.
100. Voiculescu, O., Taillebourg, E., Pujades, C., Kress, C., Buart, S., Charnay, P. and Schneider-Maunoury, S. (2001). Hindbrain patterning: Krox20 couples segmentation and specification of regional identity. Development 128, 4967-4978.
101. Weisinger, K., Kohl, A., Kayam, G., Monsonego-Ornan, E. and Sela-Donenfeld, D. (2012). Expression of hindbrain boundary markers is regulated by FGF3. Biol. Open 1, 67-74.
102. Wilkinson, D. G., Bhatt, S., Chavrier, P., Bravo, R. and Charnay, P. (1989). Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse. Nature 337, 461-464.
103. Wizenmann, A. and Lumsden, A. (1997). Segregation of rhombomeres by differential chemoaffinity. Mol. Cell. Neurosci. 9, 448-459.
104. Wood, H., Pall, G. and Morriss-Kay, G. (1994). Exposure to retinoic acid before or after the onset of somitogenesis reveals separate effects on rhombomeric segmentation and 3′ HoxB gene expression domains. Development 120, 2279-2285.
105. Xu, Q., Alldus, G., Holder, N. and Wilkinson, D. G. (1995). Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121, 4005-4016.
106. Xu, Q., Mellitzer, G., Robinson, V. and Wilkinson, D. G. (1999). In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399, 267-271.
107. Zhu, D., Jarmin, S., Ribeiro, A., Prin, F., Xie, S. Q., Sullivan, K., Briscoe, J., Gould, A. P., Marelli-Berg, F. M. and Gu, Y. (2010). Applying an adaptive watershed to the tissue cell quantification during T-cell migration and embryonic development. Methods Mol. Biol. 616, 207-228.