Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development

Development

Volumn 125, Issue 11, 1998, Pages 2063-2074

  Grigoriou, Maria ^a   Tucker, Abigail S ^b   Sharpe, Paul T ^b   Pachnis, Vassilis ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b GUY S HOSPITAL   (United Kingdom)

Author keywords

Branchial arches; Epithelial mesenchymal interactions; Fgf8; Lhx6; Lhx7; LIM homeodomain; Medial ganglionic eminence; Tooth development

Indexed keywords

HOMEODOMAIN PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRANCHIAL ARCH; CELL COMMUNICATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM; EXPLANT; FOREBRAIN; GENE CONTROL; GENE EXPRESSION; IN SITU HYBRIDIZATION; MANDIBLE; MAXILLA; MESENCHYME; MORPHOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TELENCEPHALON; TOOTH DEVELOPMENT;

AMINO ACID SEQUENCE; ANIMALS; BRANCHIAL REGION; DNA, COMPLEMENTARY; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTORS; GANGLIA; GENE EXPRESSION REGULATION; GENE LIBRARY; GENES, HOMEOBOX; HEAD; HOMEODOMAIN PROTEINS; MANDIBLE; MAXILLA; MICE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROSENCEPHALON; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TISSUE DISTRIBUTION; TOOTH;

EID: 0031860254     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Åberg, T., Wozney, J. and Thesleff, I. (1997). Expression patterns of BMPs in the developing mouse tooth suggests roles in morphogenesis and cell differentiation. Dev Dyn. 210, 383-396.
2. Agulnick, A. D., Taira, M., Breen, J. J., Tanaka, T., Dawid, I. B. and Westphal, H. (1996). Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins. Nature 384, 270-2.
3. Arber, S. and Caroni, P. (1996). Specificity of single LIM motifs in targeting and LIM/LIM interactions in situ. Genes Dev. 10, 289-300.
4. Bayer, S. A. (1984). Neurogenesis in the rat neostriatum. Int. J. Dev. Neurosci. 2, 163-175.
5. Bitgood, M.J. and McMahon, A.P. (1995). Hedgehog and BMP genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172, 126-138.
6. Blair, S. S., B rower, D. L., Thomas, J. B. and Zavortink, M. (1994). The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120, 1805-15.
7. Bourgouin, C., Lundgren, S. E. and Thomas, J. B. (1992). Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9, 549-61.
8. Bulfone, A., Kim, H. J., Puelles, L., Porteus, M. H., Grippo, J. F. and Rubenstein, J. L. (1993a). The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos Mech. Dev. 40, 129-40.
9. Bulfone, A., Puelles, L., Porteus, M. H., Frohman, M. A., Martin, G. R. and Rubenstein, J. L. (1993b). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1 ), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13, 3155-72.
10. Burglin, T. R. (1994). A comprehensive classification of homeobox genes. In Guidebook to the Homeobox Cenex (ed. D. Duboule), pp. 28-64. Sambrook and Tooze publications.
11. Chapman, G. and Rathjen, P. D. (1995). Sequence and evolutionary conservation of the murine Gbx-2 homeobox gene. FEBS Len. 364, 289-292.
12. Chen, G. C., Zheng, L. and Chan, C. S. (1996). The LIM domain-containing Dbml GTPase-activating protein is required for normal cellular morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 1376-1390.
13. Cohen, B., McGuffin, M. E., Pfeifle, C., Segal, D. and Cohen, S. M. (1992). apterous, a gene required for imaginai disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev. 6, 715-729.
14. Conn, M. J., Izpisua-Belmonte, J. C., Abud, H., Heath, J. K. and Tickle, C. (1995). Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80, 739-746.
15. Crossley, P. H. and Martin, G. R. (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.
16. Crossley, P. H., Martinez, S. and Martin, G. R. (1996a). Midbrain development induced by FGF8 in the chick embryo. Nature 380, 66-68.
17. Crossley, P. H., Minowada, G., MacArthur, C. A. and Martin, G. R. (1996b). Roles for FGF8 in the induction, initiation, and maintenance of chick limb development. Cell 84, 127-136.
18. Dawid, I. B., Toyama, R. and Taira, M. (1995). LIM domain proteins. C. R. Acad. Sci III 318, 295-306.
19. Deacon, T. W., Pakzaban, P. and Isacson, O. ( 1994). The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: neural transplantation and developmental evidence. Brain Res. 668, 211-219.
20. Dolle, P., Price, M. and Duboule, D. (1992). Expression of the murine Dlx1 homeobox gene during facial, ocular and limb development. Differentiation 49, 93-99.
21. Feuerstein, R., Wang, X., Song, D., Cooke, N. E. and Liebhaber, S. A. (1994). The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc. Natl. Acad. Sci. USA 91, 10655-10659.
22. Freyd, G., Kim, S. K. and Horvitz, H. R. ( 1990). Novel cysteine-rich motif and homeodomain in the product of the Caenorhabditis elegans cell lineage gene lin-11. Nature 344, 876-879.
23. Fukiishi, Y. and Morris-Kay, G. M. (1992). Migration of cranial neural crest cells to the pharyngeal arches and heart in rat embryos. Cell. Tissue Res. 268, 1-8.
24. Heikinheimo, M., Lawshe, A., Shackleford, G.M., Wilson, D.B., and MacArthur, C. (1994). Fgf8 expression in the post-gastrulation mouse suggests roles in the development of the face, limbs, and central nervous system. Mech. Dev. 48, 129-138.
25. Imai, H., Osumi Yamashita, N., Ninomiya, Y. and Eto, K. (1996). Contribution of early-emigrating midbrain crest cells to the dental mesenchyme of mandibular molar teeth in rat embryos. Dev. Biol. 176, 151-165.
26. Iseki, S., Araga, A., Ohuchi, H., Nohno, T., Yoshioka, H., Hayashi, F. and Noji, S. (1996). Sonic hedgehog is expressed in epithelial cells during development of whisker, hair and tooth. Biochem. Biophys. Res. Commun. 218, 688-693.
27. Jowett, A. K., Vainio, S., Ferguson, M. W., Sharpe, P. T. and Thesleff, I. (1993). Epithelial-mesenchymal interactions are required for msx 1 and msx 2 gene expression in the developing murine molar tooth. Development 117, 461-470.
28. Jurata, L. W., Kenny, D. A. and Gill, G. N. (1996). Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc. Natl. Acad. Sci. USA 93, 11693-11698.
29. Karlsson, O., Thor, S., Norberg, T., Ohlsson, H. and Edlund, T. (1990). Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo- and a Cys-His domain. Nature 344. 879-882.
30. Kikuchi, Y., H.Segawa, Tokumoto, M., Tsubokawa, T., Hotta, Y., Uyemura, K. and Okamoto, H. (1997). Ocular and cerebellar defects in Zebrafish induced by overexpression of the LIM domains of the Islet-3 LIM/homeodomain protein. Neuron 18, 369-382.
31. Kratochwil, K., Dull, M., Farinas, I., Galceran, J. and Grosschedl, R. (1996). Lef 1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev. 10. 1382-1394.
32. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78. 191-201.
33. Lammers, G. J., Gribnau, A. A. M. and Donkelaar, H. J. T. (1980). Neurogenesis in the basal forebrain in the Chinese hamster (Cricetulus griseus). Anat. Embryol. 158, 193-211.
34. Lumsden, A. G. S. (1988). Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103. 155-169.
35. Lumsden, A. and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109-15.
36. Lundgren, S. E., Callahan, C. A., Thor, S. and Thomas, J. B. (1995). Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121, 1769-73.
37. MacKenzie, A., Leeming, G. L., Jowett, A. K., Ferguson, M. W. and Sharpe, P. T. (1991). The homeobox gene Hox 7. 1 has specific regional and temporal expression patterns during early murine craniofacial embryogenesis, especially tooth development in vivo and in vitro. Development 111, 269-85.
38. MacKenzie, A., Ferguson, M. W. and Sharpe, P. T. (1992). Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. Development 115, 403-20.
39. Mahmood, R., Bresnick, J., Hornbruch, A., Mahony, C., Morton, N., Colquhoun, K., Martin, P., Lumsden, A., Dickson, C. and Mason, I (1995). A role for FGF-8 in the initiation and maintenance of vertebrate limb bud outgrowth. Curr. Biol. 5, 797-806.
40. Marchand, R., Lajoie, L. and Blanchet, C. (1986), Histogenesis at the level of the basal forebrain. Neuroscience 17, 581-607.
41. Neubuser, A. Peters, H., Balling, R., and Martin, G.R. (1997). Antagonistic Interactions between FGF and BMP signaling pathways: A mechanism for positioning the sites of tooth development. Cell 90, 247-255.
42. Noden, D. (1983). The role of the neural crest in patterning of avian cranial skeletal, connective and muscle tissues. Dev. Biol. 96, 144-165.
43. Ohuchi, H., Nakagawa, T., Yamamoto, A., Araga, A., Ohata, T., Ishimaru, Y., Yoshioka, H., Kuwana, T., Nohno, T., Yamasaki, M., Itoh, N. and Noji, S. (1997). The mesenchymal factor, FGF10, initiates and maintains the outgrowth of the chick limb bud through interaction with FGF8, an apical ectodermal factor. Development 124, 2235-2244.
44. Olsson, M., Campbell, K., Wictorin, K. and Bjorklund, A. (1995). Projection neurons in fetal striatal transplants are predominantly derived from the lateral ganglionic eminence. Neuroscience 69. 1169-1182.
45. Osumi Yamashita, N., Ninomiya, Y., Doi, H. and Eto, K. (1994). The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Dev. Biol. 164, 409-419.
46. Peters, H., Neubüser, A. and Balling, R. (1998). Pax genes and oncogenesis: Pax9 meets tooth development. Eur. J. Oral. Sci. 106, 38-43.
47. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T. and Jessell, T. M. (1996). Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
48. Porteus, M. H., Bulfone, A., Liu, J. K., Puelles, L., Lo, L. C. and Rubenstein, J. L. (1994). DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neurosci. 14, 6370-6383.
49. Richman, J. M. and Tickle, C. (1989). Epithelia are interchangeable between facial primordia of chick embryos and morphogenesis is controlled by the mesenchyme. Dev. Biol. 136, 201-210.
50. Richman, J. M. and Tickle, C. (1992). Epithelial-mesenchymal interactions in the outgrowth of limb buds and facial primordia in chick embryos. Dev. Biol. 154, 299-308.
51. Riddle, R. D., Ensini, M., Nelson, C., Tsuchida, T., Jessell, T, M. and Tabin, C. (1995). Induction of the LIM homeobox gene Lmxl by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83, 631-640.
52. Robinson, G. W. and Mahon, K. A. (1994). Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech. Dev. 48, 199-215.
53. Sanchez Garcia, I. and Rabbitts, T. H. (1993). Redox regulation of in vitro DNA-binding activity by the homeodomain of the Isl-1 protein. J. Mol. Biol. 231, 945-949.
54. Satokata, I. and Maas, R. (1994). Msxl deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6, 348-356.
55. Saxen, L. (1966). The effect of tetracyclin on osteogenesis in vitro, J. Exp. Zool. 162, 269-294.
56. Schaeren-Wiemers, N. and 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-labelled cRNA probes. Histochemistry- 100, 431-440.
57. Schmeichel, K. L. and Beckerle, M. C. ( 1994). The LIM domain is a modular protein-binding interface. Cell 79, 211-219.
58. Serbedzija, G. N., Bronner Fraser, M. and Fraser, S. E. (1992). Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116, 297-307.
59. Sheng, H. Z., Moriyama, K., Yamashita, T., Li, H., Potter, S. S., Mahon, K. A., Westphal, H. (1997). Multistep control of pituitary organogenesis. Science 278, 1809-1812.
60. Shimamura, K. and Rubenstein, J. L. R. (1997). Inductive interactions direct arly regionalization of the mouse forebrain. Development 124, 2709-2718.
61. Taira, M., Otani, H., Jamrich, M. and Dawid, I. B. (1994). Expression of the LIM class homeobox gene Xlim-1 in pronephros and CNS cell lineages of Xenopus embryos is affected by retinoic acid and exogastrulation. Development 120, 1525-1536.
62. Taira, M., Evrard, J. L., Steinmetz, A. and Dawid, I. B. (1995). Classification of LIM proteins. Trends Genet. 11, 431-2.
63. Tanabe, Y. and Jessell, T. M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
64. Thesleff, I. and Nieminen, P. (1996). Tooth morphogenesis and cell differentiation. Curr. Opin. Cell Biol. 8, 844-850.
65. Thomas, B. L., Thicker, A. S., Ferguson, C., Qiu, M., Hardcastle, Z., Rubenstein, J. L. R. and Sharpe, P. T. (1997) The role of Dlx-1 and Dlx2 in patterning of the murine dentition. Development 124, 4811-4818.
66. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
67. Tickle, C. (1995). Vertebrate limb development. Curr. Opin. Genet. Dev, 5 (4), 478-484.
68. Trowel, O. A. (1959). The culture of mature organs in a synthetic medium. Exp. Cell Res. 16, 118-147.
69. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-790.
70. Vainio, S., Karavanova, I., Jowett, A. and Thesleff, I (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
71. van Genderen, C., Okamura, R. M., Farinas, I., Quo, R. G., Parslow, T. G., Bruhn, L. and Grosschedl, R. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1 -deficient mice. Genes Dev. 8, 2691-2703.
72. Vogel, A., Rodriguez, C., Warnken, W. and Izpisua Belmonte, J. C. (1995). Dorsal cell fate specified by chick. Lmx1 during vertebrate limb development. Nature 378, 716-720.
73. Way J.C., Chalfie C. M. (1988). mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons in C. elegans. Cell 54, 5-16.
74. Wilkinson, D. G. (1992). Whole mount in situ hybridization of vertebrate embryos. In In Situ hybridization: A Practical Approach, (ed. D. G. Wilkinson), pp. 75-83. Oxford : IRL Press.
75. Xue, D., Tu, Y. and Chalfie, M. (1993). Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 261, 1324-1328.