Node and midline defects are associated with left-right development in Delta1 mutant embryos

Development

Volumn 130, Issue 1, 2003, Pages 3-13

  Przemeck, Gerhard K H ^a   Heinzmann, Ulrich ^a   Beckers, Johannes ^a   de Angelis, Martin Hrabé ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Floorplate; Gastrulation; Left right asymmetry; Midline; Mouse; Node formation; Notch signalling; Notochord

Indexed keywords

DELTA1 PROTEIN; NOTCH RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; CELL DIFFERENTIATION; CONGENITAL HEART DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; EMBRYO; EMBRYO AXIS; EMBRYO CELL; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; EXPERIMENTAL MODEL; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; GENETIC ANALYSIS; GENETIC CONSERVATION; MORPHOGENESIS; MOUSE; MUTANT; NONHUMAN; ORGANOGENESIS; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE; WILD TYPE;

ABNORMALITIES, MULTIPLE; ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; EMBRYONIC AND FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART DEFECTS, CONGENITAL; HOMOZYGOTE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; NOTOCHORD; ORGANIZERS, EMBRYONIC; RANDOM ALLOCATION; RECEPTOR, NOTCH1; RECEPTOR, NOTCH2; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 0037232490     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00176     Document Type: Review

References (90)

1. Ang, S. L., Wierda, A., Wong, D., Stevens, K. A., Cascio, S., Rossant, J. and Zaret, K. S. (1993). The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119, 1301-1315.
2. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabé de Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature 400, 877-881.
3. Appel, B., Fritz, A., Westerfield, M., Grunwald, D. J., Eisen, J. S. and Riley, B. B. (1999). Delta-mediated specification of midline cell fates in zebrafish embryos. Curr. Biol. 9, 247-256.
4. Artavanis-Tsakonas, S., Matsuno, K. and Fortini, M. E. (1995). Notch signaling. Science 268, 225-232.
5. Artavanis-Tsakonas, S., Rand, M. D. and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776.
6. Beckers, J., Clark, A., Wünsch, K., Hrabé de Angelis, M. and Gossler, A. (1999). Expression of the mouse Delta1 gene during organogenesis and fetal development. Mech. Dev. 84, 165-168.
7. Beddington, R. S. and Robertson, E. J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.
8. Bettenhausen, B., Hrabé de Angelis, M., Simon, D., Guenet, J. L. and Gossler, A. (1995). Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 121, 2407-2418.
9. Bisgrove, B. W., Essner, J. J. and Yost, H. J. (1999). Regulation of midline development by antagonism of lefty and nodal signaling. Development 126, 3253-3262.
10. Bisgrove, B. W., Essner, J. J. and Yost, H. J. (2000). Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. Development 127, 3567-3579.
11. Bisgrove, B. W. and Yost, H. J. (2001). Classification of left-right patterning defects in zebrafish, mice, and humans. Am. J. Med. Genet. 101, 315-323.
12. Blum, M., Steinbeisser, H., Campione, M. and Schweickert, A. (1999). Vertebrate left-right asymmetry: old studies and new insights. Cell. Mol. Biol. 45, 505-516.
13. Boettger, T., Wittler, L. and Kessel, M. (1999). FGF8 functions in the specification of the right body side of the chick. Curr. Biol. 9, 277-280.
14. Campione, M., Steinbeisser, H., Schweickert, A., Deissler, K., van Bebber, F., Lowe, L. A., Nowotschin, S., Viebahn, C., Haffter, P., Kuehn, M. R. et al. (1999). The homeobox gene Pitx2: mediator of asymmetric left-right signaling in vertebrate heart and gut looping. Development 126, 1225-1234.
15. Capdevila, J., Vogan, K. J., Tabin, C. J. and Izpisua Belmonte, J. C. (2000). Mechanisms of left-right determination in vertebrates. Cell 101, 9-21.
16. Cohen, B., Bashirullah, A., Dagnino, L., Campbell, C., Fisher, W. W., Leow, C. C., Whiting, E., Ryan, D., Zinyk, D., Boulianne, G. et al. (1997). Fringe boundaries coincide with Notch-dependent patterning centres in mammals and alter Notch-dependent development in Drosophila. Nat. Genet. 16, 283-288.
17. Conlon, F. L., Lyons, K. M., Takaesu, N., Barth, K. S., Kispert, A., Herrmann, B. and Robertson, E. J. (1994). A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120, 1919-1928.
18. Danos, M. C. and Yost, H. J. (1995). Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development 121, 1467-1474.
19. Danos, M. C. and Yost, H. J. (1996). Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177, 96-103.
20. Davidson, B. P., Kinder, S. J., Steiner, K., Schoenwolf, G. C. and Tam, P. P. (1999). Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. Dev. Biol. 211, 11-26.
21. De Bellard, M. E., Ching, W., Gossler, A. and Bronner-Fraser, M. (2002). Disruption of segmental neural crest migration and Ephrin expression in Delta-1 null mice. Dev. Biol. 249, 121-130.
22. de la Pompa, J. L., Wakeham, A., Correia, K. M., Samper, E., Brown, S., Aguilera, R. J., Nakano, T., Honjo, T., Mak, T. W., Rossant, J. et al. (1997). Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124, 1139-1148.
23. Del Amo, F. F., Smith, D. E., Swiatek, P. J., Gendron-Maguire, M., Greenspan, R. J., McMahon, A. P. and Gridley, T. (1992). Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 115, 737-744.
24. Doherty, D., Feger, G., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1996). Delta is a ventral to dorsal signal complementary to Serrate, another Notch ligand, in Drosophila wing formation. Genes Dev. 10, 421-434.
25. 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.
26. Dunwoodie, S. L., Henrique, D., Harrison, S. M. and Beddington, R. S. (1997). Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development 124, 3065-3076.
27. Essner, J. J., Vogan, K. J., Wagner, M. K., Tabin, C. J., Yost, H. J. and Brueckner, M. (2002). Conserved function for embryonic nodal cilia. Nature 418, 37-38.
28. Faisst, A. M., Alvarez-Bolado, G., Treichel, D. and Gruss, P. (2002). Rotatin is a novel gene required for axial rotation and left-right specification in mouse embryos. Mech. Dev. 113, 15-28.
29. Firulli, A. B., McFadden, D. G., Lin, Q., Srivastava, D. and Olson, E. N. (1998). Heart and extra-embryonic mesodermal defects in mouse embryos lacking the bHLH transcription factor Hand1. Nat. Genet. 18, 266-270.
30. Frisen, J. and Lendahl, U. (2001). Oh no, Notch again! BioEssays 23, 3-7.
31. Fujinaga, M. (1997). Development of sidedness of asymmetric body structures in vertebrates. Int. J. Dev. Biol. 41, 153-186.
32. Gage, P. J., Suh, H. and Camper, S. A. (1999). Dosage requirement of Pitx2 for development of multiple organs. Development 126, 4643-4651.
33. Garcia-Castro, M. J., Vielmetter, E. and Bronner-Fraser, M. (2000). N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. Science 288, 1047-1051.
34. Hamada, H., Meno, C., Watanabe, D. and Saijoh, Y. (2002). Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 3, 103-113.
35. Hermann, G. J., Leung, B. and Priess, J. R. (2000). Left-right asymmetry in C. elegans intestine organogenesis involves a LIN-12/Notch signaling pathway. Development 127, 3429-3440.
36. Herrmann, B. G. (1991). Expression pattern of the Brachyury gene in whole-mount TWis/TWis mutant embryos. Development 113, 913-917.
37. Hrabé de Angelis, M., McIntyre, J., 2nd and Gossler, A. (1997). Maintenance of somite borders in mice requires the Delta homologue DII1. Nature 386, 717-721.
38. Hutter, H. and Schnabel, R. (1995). Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: a multistep process involving a series of inductive events. Development 121, 3417-3424.
39. Ibanez-Tallon, I., Gorokhova, S. and Heintz, N. (2002). Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum. Mol. Genet. 11, 715-721.
40. Ip, T. Y. and Gridley, T. (2002). Cell movements during gastrulation: Snail dependent and independent pathways. Curr. Opin. Genet. Dev. 12, 423-429.
41. Irvine, K. D. and Rauskolb, C. (2001). Boundaries in development: formation and function. Annu. Rev. Cell Dev. Biol. 17, 189-214.
42. Izraeli, S., Lowe, L. A., Bertness, V. L., Good, D. J., Dorward, D. W., Kirsch, I. R. and Kuehn, M. R. (1999). The SIL gene is required for mouse embryonic axial development and left- right specification. Nature 399, 691-694.
43. Jiang, Y. J., Aerne, B. L., Smithers, L., Haddon, C., Ish-Horowicz, D. and Lewis, J. (2000). Notch signalling and the synchronization of the somite segmentation clock. Nature 408, 475-479.
44. Johnston, S. H., Rauskolb, C., Wilson, R., Prabhakaran, B., Irvine, K. D. and Vogt, T. F. (1997). A family of mammalian Fringe genes implicated in boundary determination and the Notch pathway. Development 124, 2245-2254.
45. Kiernan, A. E., Ahituv, N., Fuchs, H., Balling, R., Avraham, K. B., Steel, K. P. and Hrabé de Angelis, M. (2001). The Notch ligand Jagged1 is required for inner ear sensory development. Proc. Natl. Acad. Sci. USA 98, 3873-3878.
46. Kinder, S. J., Tsang, T. E., Wakamiya, M., Sasaki, H., Behringer, R. R., Nagy, A. and Tam, P. P. (2001). The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm. Development 128, 3623-3634.
47. King, T., Beddington, R. S. and Brown, N. A. (1998). The role of the brachyury gene in heart development and left-right specification in the mouse. Mech. Dev. 79, 29-37.
48. Klessinger, S. and Christ, B. (1996). Axial structures control laterality in the distribution pattern of endothelial cells. Anat. Embryo]. 193, 319-330.
49. Kusumi, K., Sun, E. S., Kerrebrock, A. W., Bronson, R. T., Chi, D. C., Bulotsky, M. S., Spencer, J. B., Birren, B. W., Frankel, W. N. and Lander, E. S. (1998). The mouse pudgy mutation disrupts Delta homologue Dll3 and initiation of early somite boundaries. Nat. Genet. 19, 274-278.
50. Larsson, C., Lardelli, M., White, I. and Lendahl, U. (1994). The human NOTCH1, 2, and 3 genes are located at chromosome positions 9q34, 1p13-p11, and 19p13.2-p13.1 in regions of neoplasia-associated translocation. Genomics 24, 253-258.
51. Latimer, A. J., Dong, X., Markov, Y. and Appel, B. (2002). Delta-Notch signaling induces hypochord development in zebrafish. Development 129, 2555-2563.
52. Levin, M., Johnson, R. L., Stern, C. D., Kuehn, M. and Tabin, C. (1995). A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82, 803-814.
53. Levin, M., Roberts, D. J., Holmes, L. B. and Tabin, C. (1996). Laterality defects in conjoined twins. Nature 384, 321.
54. Lewis, J. (1998). Notch signalling and the control of cell fate choices in vertebrates. Semin. Cell Dev. Biol. 9, 583-589.
55. Lin, C. R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, F., Izpisua-Belmonte, J. C. and Rosenfeld, M. G. (1999). Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401, 279-282.
56. Lohr, J. L., Danos, M. C., Groth, T. W. and Yost, H. J. (1998). Maintenance of asymmetric nodal expression in Xenopus laevis. Dev. Genet. 23, 194-202.
57. Lohr, J. L., Danos, M. C. and Yost, H. J. (1997). Left-right asymmetry of a nodal-related gene is regulated by dorsoanterior midline structures during Xenopus development. Development 124, 1465-1472.
58. Lowe, L. A., Yamada, S. and Kuehn, M. R. (2001). Genetic dissection of nodal function in patterning the mouse embryo. Development 128, 1831-1843.
59. Lu, M. F., Pressman, C., Dyer, R., Johnson, R. L. and Martin, J. F. (1999). Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401, 276-278.
60. Melloy, P. G., Ewart, J. L., Cohen, M. F., Desmond, M. E., Kuehn, M. R. and Lo, C. W. (1998). No turning, a mouse mutation causing left-right and axial patterning defects. Dev. Biol. 193, 77-89.
61. Meno, C., Ito, Y., Saijoh, Y., Matsuda, Y., Tashiro, K., Kuhara, S. and Hamada, H. (1997). Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos. Genes Cells 2, 513-524.
62. Meno, C., Shimono, A., Saijoh, Y., Yashiro, K., Mochida, K., Ohishi, S., Noji, S., Kondoh, H. and Hamada, H. (1998). lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94, 287-297.
63. Meno, C., Gritsman, K., Ohishi, S., Ohfuji, Y., Heckscher, E., Mochida, K., Shimono, A., Kondoh, H., Talbot, W. S., Robertson, E. J. et al. (1999). Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol. Cell 4, 287-298.
64. Mercola, M. and Levin, M. (2001). Left-right asymmetry determination in vertebrates. Annu. Rev. Cell Dev. Biol. 17, 779-805.
65. Meyers, E. N. and Martin, G. R. (1999). Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science 285, 403-406.
66. Micchelli, C. A. and Blair, S. S. (1999). Dorsoventral lineage restriction in wing imaginal discs requires Notch. Nature 401, 473-476.
67. Mitsiadis, T. A., Henrique, D., Thesleff, I. and Lendahl, U. (1997). Mouse Serrate-1 (Jagged-1): expression in the developing tooth is regulated by epithelial-mesenchymal interactions and fibroblast growth factor-4. Development 124, 1473-1483.
68. Morrison, A., Hodgetts, C., Gossler, A., Hrabé de Angelis, M. and Lewis, J. (1999). Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech. Dev. 84, 169-172.
69. Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M. and Hirokawa, N. (1998). Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95, 829-837.
70. Nonaka, S., Shiratori, H., Saijoh, Y. and Hamada, H. (2002). Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418, 96-99.
71. Oka, C., Nakano, T., Wakeham, A., de la Pompa, J. L., Mori, C., Okazaki, S., Kawaichi, M., Shiota, K., Mak, T. W. and Honjo, T. (1995). Disruption of the mouse RBP-J kappa gene results in early embryonic lethality. Development 121, 3291-3301.
72. Okada, Y., Nonaka, S., Tanaka, Y., Saijoh, Y., Hamada, H. and Hirokawa, N. (1999). Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol. Cell 4, 459-468.
73. Rauskolb, C., Correia, T. and Irvine, K. D. (1999). Fringe-dependent separation of dorsal and ventral cells in the Drosophila wing. Nature 401, 476-480.
74. Riley, P., Anson-Cartwright, L. and Cross, J. C. (1998). The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nat. Genet. 18, 271-275.
75. Ryan, A. K., Blumberg, B., Rodriguez-Esteban, C., Yonei-Tamura, S., Tamura, K., Tsukui, T., de la Pena, J., Sabbagh, W., Greenwald, J., Choe, S. et al. (1998). Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 394, 545-551.
76. Schneider, H. and Brueckner, M. (2000). Of mice and men: dissecting the genetic pathway that controls left-right asymmetry in mice and humans. Am. J. Med. Genet. 97, 258-270.
77. Shiratori, H., Sakuma, R., Watanabe, M., Hashiguchi, H., Mochida, K., Sakai, Y., Nishino, J., Saijoh, Y., Whitman, M. and Hamada, H. (2001). Two-step regulation of left-right asymmetric expression of Pitx2: initiation by nodal signaling and maintenance by Nkx2. Mol. Cell 7, 137-149.
78. Spoörle, R. and Schughart, K. (1998). Paradox segmentation along inter- and intrasomitic borderlines is followed by dysmorphology of the axial skeleton in the open brain (opb) mouse mutant. Dev. Genet. 22, 359-373.
79. Spurr, A. R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26, 31-43.
80. Srivastava, D., Cserjesi, P. and Olson, E. N. (1995). A subclass of bHLH proteins required for cardiac morphogenesis. Science 270, 1995-1999.
81. Sulik, K., Dehart, D. B., Iangaki, T., Carson, J. L., Vrablic, T, Gesteland, K. and Schoenwolf, G. C. (1994). Morphogenesis of the murine node and notochordal plate. Dev. Dyn. 201, 260-278.
82. Tam, P. P. and Beddington, R. S. (1987). The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99, 109-126.
83. Tam, P. P. and Behringer, R. R. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech. Dev. 68, 3-25.
84. Thomas, T., Yamagishi, H., Overbeek, P. A., Olson, E. N. and Srivastava, D. (1998). The bHLH factors, dHAND and eHAND, specify pulmonary and systemic cardiac ventricles independent of left-right sidedness. Dev. Biol. 196, 228-236.
85. -/- mutant mice unveil a convergence of the shh and retinoic acid pathways in the control of Lefty-1. Proc. Natl. Acad. Sci. USA 96, 11376-11381.
86. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
87. Williams, R., Lendahl, U. and Lardelli, M. (1995). Complementary and combinatorial patterns of Notch gene family expression during early mouse development. Mech. Dev. 53, 357-368.
88. Wood, W. B. (1997). Left-right asymmetry in animal development. Annu. Rev. Cell Dev. Biol. 13, 53-82.
89. Wurst, W. and Gossler, A. (2000). Gene trap strategies in ES cells. In Gene Targeting: A Practical Approach (ed. A. L. Joyner), pp. 207-254. New York: Oxford University Press.
90. Zhou, X., Sasaki, H., Lowe, L., Hogan, B. L. and Kuehn, M. R. (1993). Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 361, 543-547.