Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation

Development

Volumn 130, Issue 3, 2003, Pages 495-505

  Mukhopadhyay, Muhua ^a   Teufel, Andreas ^a   Yamashita, Tsuyoshi ^a,d   Agulnick, Alan D ^a,e   Chen, Lan ^a   Downs, Karen M ^b   Schindler, Alice ^a   Grinberg, Alexander ^a   Huang, Sing Ping ^a   Dorward, David ^c   Westphal, Heiner ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d ASAHIKAWA MEDICAL COLLEGE   (Japan)

^e Georgia Biobusiness Center   (United States)

Author keywords

Anterior posterior axis; Ldb1; Mouse; Otx2; Wnt inhibitor(s)

Indexed keywords

BINDING PROTEIN; HOMEODOMAIN PROTEIN; LIM DOMAIN BINDING PROTEIN 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT PROTEIN;

AMNION; ANIMAL TISSUE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO AXIS; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; FETUS MEMBRANE; GASTRULATION; GENE DELETION; GENE EXPRESSION; HEAD; HEART; MESODERM; MOUSE; MOUSE MUTANT; NONHUMAN; PHENOTYPE; PLEIOTROPY; PRIMORDIAL GERM CELL; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RHOMBENCEPHALON; YOLK SAC;

ANIMALS; BASE SEQUENCE; BODY PATTERNING; DNA; DNA-BINDING PROTEINS; FEMALE; FETAL HEART; GASTRULA; GENE TARGETING; MALE; MESODERM; MICE; MICE, KNOCKOUT; OOCYTES; PHENOTYPE; PREGNANCY; PROTO-ONCOGENE PROTEINS; RNA, MESSENGER; WNT PROTEINS; ZEBRAFISH PROTEINS;

ANIMALIA; MAMMALIA;

EID: 0037327126     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00225     Document Type: Review

References (84)

1. -/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121, 3279-3290.
2. Acampora, D., Avantaggiato, V., Tuorto, F., Briata, P., Corte, G. and Simeone, A. (1998). Visceral endoderm-restricted translation of Otx1 mediates recovery of Otx2 requirements for specification of anterior neural plate and normal gastrulation. Development 125, 5091-5104.
3. 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, 270-272.
4. Andree, B., Duprez, D., Vorbusch, B., Arnold, H. H. and Brand, T. (1998). BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech. Dev. 70, 119-131.
5. Ang, S. L., Conlon, R. A., Jin, O. and Rossant, J. (1994). Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120, 2979-2989.
6. Ang, S. L. and Rossant, J. (1994). HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78, 561-574.
7. Ang, S. L., Jin, O., Rhinn, M., Daigle, N., Stevenson, L. and Rossant, J. (1996). A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243-252.
8. Bach, I., Carriere, C., Ostendorff, H. P., Andersen, B. and Rosenfeld, M. G. (1997). A family of LIM domain-associated cofactors confer transcriptional synergism between LIM and Otx homeodomain proteins. Genes Dev. 11, 1370-1380.
9. Bach, L. (2000). The LIM domain: regulation by association. Mech. Dev. 91, 5-17.
10. Beddington, R. S. P. (1994). Induction of a second neural axis by the mouse node. Development 120, 613-620.
11. Beddington, R. S. P. and Robertson, E. J. (1998). Anterior patterning in mouse. Trends Genet. 14, 277-284.
12. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and De Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
13. Belo, J. A., Bachiller, D., Agius, E., Kemp, C., Borges, A. C., Marques, S., Piccolo, S. and DeRobertis, E. M. (2000). Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development. Genesis 26, 265-270.
14. Bielinska, M., Narita, N. and Wilson, D. B. (1999). Distinct roles for visceral endoderm during embryonic mouse development. Int. J. Dev. Biol. 43, 183-205.
15. Borello, U., Coletta, M., Tajbakhsh, S., Leyns, L., De Robertis, E. M., Buckingham, M. and Cossu, G. (1999). Transplacental delivery of the Wnt antagonist Frzb1 inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos. Development 126, 4247-4255.
16. Bouillet, P., Oulad-Abdelghani, M., Ward, S. J., Bronner, S., Chambon, P. and Dolle, P. (1996). A new mouse member of the Wnt gene family, mWnt-8, is expressed during early embryogenesis and is ectopically induced by retinoic acid. Mech. Development 58, 141-152.
17. Breen, J. J., Agulnick, A. D., Westphal, H. and Dawid, I. B. (1998). Interactions between LIM domains and the LIM domain-binding protein Ldb1. J. Biol. Chem. 273, 4712-4717.
18. Cassata, G., Rohrig, S., Kuhn, F., Hauri, H. P., Baumeister, R. and Burglin, T. R. (2000). The Caenorhabditis elegans Ldb/NLI/Clim orthologue Ldb-1 is required for neuronal function. Dev. Biol. 226, 45-56.
19. Chesley, P. (1935). Development of the short-tailed mutant in the house mouse. J. Exp. Zool. 70, 429-453.
20. Chiquoine, A. D. (1954). The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat. Rec. 118, 135-146.
21. Cross, J. C., Werb, Z. and Fisher, S. J. (1994). Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508-1518.
22. Dawid, I. B., Breen, J. J. and Toyama, R. (1998). LIM domains: multiple roles as adapters and functional modifiers in protein interactions. Trends Genet. 14, 156-162.
23. de Souza, F. S. J. and Niehrs, C. (2000). Anterior endoderm and head induction in early vertebrate embryos. Cell Tissue Res. 300, 207-217.
24. Dufort, D., Schwartz, L., Harpal, K. and Rossant, J. (1998). The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125, 3015-3025.
25. Foley, A. C. and Stern, C. D. (2001). Evolution of vertebrate forebrain development: how many different mechanisms? J. Anat. 199, 35-52.
26. Garcia-Martinez, V. and Schoenwolf, G. C. (1993). Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol. 159, 706-719.
27. German, M. S., Wang, J., Chadwick, R. B. and Rutter, W. J. (1992). Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex. Genes Dev. 6, 2165-2176.
28. Glinka, A., Wu, W., Delius, H., Monaghan, P. A., Blumenstock, C. and Niehrs, C. (1998). Dickkopf1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362.
29. Gluecksohn-Schoenheimer, S. (1949). The effect of a lethal mutation responsible for duplications and twinning in mouse embryos. J. Exp. Zool. 110, 47-76.
30. Gurtner, G. C., Davis, V., Li, H., McCoy, M. J., Sharpe, A. and Cybulsky, M. I. (1995). Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 9, 1-14.
31. Herrmann, B. G. (1992). Action of the Brachyury gene in mouse embryogenesis. Ciba Found. Symp. 165, 78-86.
32. Hoang, B. H., Thomas, J. T., Abdul-Karim, F. W., Correia, K. M., Conlon, R. A., Luyten, F. P. and Ballock, R. T. (1998). Expression pattern of two Frizzled-related genes, Frzb-1 and Sfrp-1, during mouse embryogenesis suggests a role for modulating action of Wnt family members. Dev. Dyn. 212, 364-372.
33. Hobert, O. and Westphal, H. (2000). Functions of LIM-homeobox genes. Trends Genet. 16, 75-83.
34. 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.
35. Jurata, L. W. and Gill, G. N. (1997). Functional analysis of the nuclear LIM domain interactor NLI. Mol. Cell. Biol. 17, 5688-5698.
36. Jurata, L. W. and Gill, N. (1998). Structure and function of LIM domains. Curr. Top. Microbiol. Immunol. 228, 75-113.
37. Kinder, S. J., Tsang, T. E., Ang, S. L., Behringer, R. R. and Tam, P. P. (2001). Defects of the body plan of mutant embryos lacking Lim1, Otx2 or Hnf3beta activity. Int. J. Dev. Biol. 45, 347-355.
38. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P. and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436.
39. Lawson, K. A. and Hage, W. J. (1994). Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found. Symp. 182, 68-84.
40. Lints, T. J., Parsons, L. M., Hartley, L., Lyons, I. and Harvey, R. P. (1993). Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119, 419-431.
41. Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R. and Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nature Genet. 22, 361-365.
42. Leimeister, C., Bach, A. and Gessler, M. (1998). Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family. Mech. Dev. 75, 29-42.
43. Leyns, L., Bouwmeester, T., Kim, S. H., Piccolo, S. and De Robertis, E. M. (1997). Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88, 747-756.
44. Marvin, M. J., Di Rocco, G., Gardiner, A., Bush, S. M. and Lassar, A. B. (2001). Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev. 15, 316-327.
45. Matsuo, I., Kuratani, S., Kimura, C., Takeda, N. and Aizawa, S. (1995). Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9, 2646-2658.
46. McMahon, A. P. and Moon, R. T. (1989). Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58, 1075-1084.
47. Meyer, A. and Schartl, M. (1999). Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell. Biol. 11, 699-704.
48. Molkentin, J. D., Lin, Q., Duncan, S. A. and Olson, E. N. (1997). Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes. Dev. 11, 1061-1072.
49. Morcillo, P., Rosen, C. and Dorsett, D. (1996). Genes regulating the remote wing margin enhancer in the Drosophila cut locus. Genetics 144, 1143-1154.
50. Morcillo, P., Rosen, C., Baylies, M. K. and Dorsett, D. (1997). Chip, a widely expressed chromosomal protein required for segmentation and activity of a remote wing margin enhancer in Drosophila. Genes Dev. 11, 2729-2740.
51. Mukhopadhyay, M., Shtrom, S., Rodriguez-Esteban, C., Chen, L., Tsukui, T., Gomer, L., Dorward, D. W., Glinka, A., Grinberg, A., Huang, S. P., Niehrs, C., Belmonte, J. C. and Westphal, H. (2001). Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell 1, 423-434.
52. Nakano, T., Murata, T., Matsuo, I. and Aizawa, S. (2000). OTX2 directly interacts with LIM1 and HNF-3beta. Biochem. Biophys. Res. Commun. 267, 64-70.
53. Niehrs, C. (1999). Head in the Wnt. Trends in Genet. 15, 314-319.
54. Oliver, G., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gruss, P, (1995). Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121, 4045-4055.
55. Perry, W. L. 3rd, Vasicek, T. J., Lee, J. J., Rossi, J. M., Zeng, L., Zhang, T., Tilghman, S. M. and Costantini, F. (1995). Phenotypic and molecular analysis of a transgenic insertional allele of the mouse Fused locus. Genetics 141, 321-332.
56. Pöpperl, H., Schmidt, C., Wilson, V., Hume, C. R., Dodd, J., Krumlauf, R. and Beddington, R. S. (1997). Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis andcauses a truncation of the anterior neuroectoderm. Development 124, 2997-3005.
57. Rhinn, M., Dierich, A., Shawlot, W., Behringer, R. R., Le Meur, M. and Ang, S. L. (1998). Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development 125, 845-856.
58. Robards, A. W. and Wilson, A. J., eds (1993). Basic biological preparation techniques for SEM. In Procedures in Electron Microscopy, pp. 11.4.1-11.4.17. Chichester: John Wiley & Sons.
59. Saga, Y., Hata, N., Kobayashi, S., Magnuson, T., Seldin, M. F. and Taketo, M. M. (1996). MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development 122, 2769-2778.
60. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J. and Inoue, T. (1999). MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126, 3437-3447.
61. Sanchez-Garcia, I. and Rabbitts, T. H. (1994). The LIM domain: a new structural motif found in zinc-finger-like proteins. Trends Genet. 10, 315-320.
62. Schneider, V. A. and Mercola, M. (2001). Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes. Dev. 15, 304-315.
63. Schultheiss, T. M., Burch, J. B. and Lassar, A. B. (1997). A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes and Dev. 11, 451-462.
64. Shawlot, W. and Behringer, R. R. (1995). Requirement for Lim1 in head-organizer function. Nature 374, 425-430.
65. Shawlot, W., Wakamiya, M., Kwan, K. M., Kania, A., Jessell, T. M. and Behringer, R. R. (1999). Lim1 is required in both primitive streak-derived tissues and visceral endoderm for head formation in the mouse. Development 126, 4925-4932.
66. Simeone, A., Acampora, D., Mallamaci, A., Stornaiuolo, A., D'Apice, M. R., Nigro, V. and Boncinelli, E. (1993). A vertebrate gene related to orthodenticle contains a homeodomain of the Bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12, 2735-2747.
67. Taira, M., Otani, H., Saint-Jeannet, J. P. and Dawid, I. B. (1994). Role of the LIM class homeodomain protein Xlim-1 in neural and muscle induction by the Spemann organizer in Xenopus. Nature 372, 677-679.
68. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
69. Tam, P. P. and Zhou, S. X. (1996). The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124-132.
70. Tam, P. P. and Steiner, K. A. (1999). Anterior patterning by synergistic activity of the early gastrula organizer and the anterior germ layer tissues of the mouse embryo. Development 126, 5171-5179.
71. Thomas, P. and Beddington, R. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6, 1487-1496.
72. Torigoi, E., Bennani-Baiti, I. M., Rosen, C., Gonzalez, K., Morcillo, P., Ptashne, M. and Dorsett, D. (2000). Chip interacts with diverse homeodomain proteins and potentiates bicoid activity in vivo. Proc. Natl. Acad. Sci. USA 97, 2686-2691.
73. Tsang, T. E., Shawlot, W., Kinder, S. J., Kobayashi, A., Kwan, K. M., Schughart, K., Kania, A., Jessell, T. M., Behringer, R. R. and Tam, P. P. (2000). Lim1 activity is required for intermediate mesoderm differentiation in the mouse embryo. Dev. Biol. 223, 77-90.
74. Tsang, T. E., Khoo, P. L., Jamieson, R. V., Zhou, S. X., Ang, S. L., Behringer, R. and Tam, P. P. (2001). The allocation and differentiation of mouse primordial germ cells. Int. J. Dev. Biol. 45, 549-555.
75. Varlet, I., Collignon, J. and Robertson, E. J. (1997). Nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124, 1033-1044.
76. Visvader, J. E., Mao, X., Fujiwara, Y., Halm, K. and Orkin, S. H. (1997). The LIM-domain binding protein Ldb1 and its partner LMO2 act as negative regulators of erythroid differentiation. Proc. Natl. Acad. Sci. USA 94, 13707-13712.
77. Wadman, I. A., Osada, H., Grutz, G., Agulnick, A. D., Westphal, H., Forster, A. and Rabbits, T. H. (1997). The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J. 16, 3145-3157.
78. Wang, S., Krinks, M., Lin, K., Luyten, F. P. and Moos, M. (1997). Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88, 757-766.
79. Weinstein, D. C., Ruizi Altaba, A., Chen, W. S., Hoodless, P., Prezioso, V. R., Jessell, T. M. and Darnell, J. E., Jr (1994). The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78, 575-588.
80. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
81. Ying, Y., Liu, X. M., Marble, A., Lawson, K. A. and Zhao, G. Q. (2000). Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 14, 1053-1063.
82. Yamaguchi, T. P. (2001). Heads or tails: Wnts and anterior-posterior patterning. Curr. Biol. 11, R713-R724.
83. Yamashita, T., Agulnick, A. D., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Westphal, H. (1998). Genomic structure and chromosomal localization of the mouse LIM domain-binding protein 1 gene, Ldb1. Genomics 48, 87-92.
84. Zeng, L., Fagotto, F., Zhang, T., Hsu, W., Vasicek, T. J., Perry, W. L. 3rd, Lee, J. J., Tilghman, S. M., Gumbiner, B. M. and Costantini, F. (1997). The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90, 181-192.