The splanchnic mesodermal plate directs spleen and pancreatic laterality, and is regulated by Bapx1/Nkx3.2

Development

Volumn 131, Issue 19, 2004, Pages 4665-4675

  Hecksher Sørensen, Jacob ^a,b   Watson, Robert P ^a   Lettice, Laura A ^a   Serup, Palle ^b   Eley, Lorraine ^c   De Angelis, Carlo ^a   Ahlgren, Ulf ^a,d   Hill, Robert E ^a  

^a WESTERN GENERAL HOSPITAL   (United Kingdom)

^b HAGEDORN RESEARCH INSTITUTE   (Denmark)

^c INSTITUTE OF HUMAN GENETICS   (United Kingdom)

^d UMEÅ UNIVERSITY   (Sweden)

Author keywords

Bapx1; Fgf regulation; LR asymmetry; Mouse; Pancreas; SMP; Spleen

Indexed keywords

FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 9; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR BAPX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASPLENIA; AUTONOMIC NERVOUS SYSTEM; COLUMNAR EPITHELIUM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO AXIS; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STRUCTURES; ENDODERM; GENE EXPRESSION; GENE MUTATION; GENETIC REGULATION; HEMIMELIA; MESENCHYME; MESODERM; MOUSE; MUTAGENICITY; NONHUMAN; PANCREAS MALFORMATION; PATHOGENESIS; PRIORITY JOURNAL; STOMACH;

ABNORMALITIES, MULTIPLE; ANIMALS; BODY PATTERNING; CELL DIVISION; EPITHELIUM; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; MESODERM; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MODELS, BIOLOGICAL; MORPHOGENESIS; PANCREAS; SIGNAL TRANSDUCTION; SPLEEN; STOMACH; TRANSCRIPTION FACTORS; VERTEBRATES;

ANIMALIA;

EID: 7244224986     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01364     Document Type: Article

References (59)

1. Ahlgren, U., Pfaff, S. L., Jessell, T. M., Edlund, T. and Edlund, H. (1997). Independent requirement for ISL1 in formation of pancreatic mesenchyme and islet cells. Nature 385, 257-260.
2. Akazawa, H., Komuro, I., Sugitani, Y., Yazaki, Y., Nagai, R. and Noda, T. (2000). Targeted disruption of the homeobox transcription factor Bapx1 results in lethal skeletal dysplasia with asplenia and gastroduodenal malformation. Genes Cells 5, 499-513.
3. Aylsworth, A. S. (2001). Clinical aspects of defects in the determination of laterality. Am. J. Med. Genet. 101, 345-355.
4. Azpiazu, N. and Frasch, M. (1993). Tinman and bagpipe: two homeo box genes that determine, cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 7, 1325-1340.
5. Bellusci, S., Grindley, J., Emoto, H., Itoh, N. and Hogan, B. L. (1997). Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124, 4867-4878.
6. Bhushan, A., Itoh, N., Kato, S., Thiery, J. P., Czernichow, P., Bellusci, S. and Scharfmann, R. (2001). Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128, 5109-5117.
7. Bisgrove, B. W., Morelli, S. H. and Yost, H. J. (2003). Genetics of human laterality disorders: insights from vertebrate model systems. Annu. Rev. Genomics Hum. Genet. 4, 1-32.
8. Boorman, C. J. and Shimeld, S. M. (2002). The evolution of left-right asymmetry in chordates. BioEssays 24, 1004-1011.
9. Bowers, P. N., Brueckner, M. and Yost, H. J. (1996). Laterality disturbances. Prog. Ped. Cardiol. 6, 53-62.
10. Burn, J. (1991). Disturbance of morphological laterality in humans. Ciba Found. Symp. 162, 282-296.
11. Capdevila, I. and Belmonte, J. C. (2000). Knowing left from right: the molecular basis of laterality defects. Mol. Med. Today 6, 112-118.
12. 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.
13. Colvin, J. S., Feldman, B., Nadeau, J. H., Goldfarb, M. and Ornitz, D. M. (1999). Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev. Dyn. 216, 72-88.
14. Dear, T. N., Colledge, W. H., Carlton, M. B., Lavenir, I., Larson, T., Smith, A. J., Warren, A. J., Evans, M. J., Sofroniew, M. V. and Rabbitts, T. H. (1995). The Hox11 gene is essential for cell survival during spleen development. Development 121, 2909-2915.
15. Debich, D. E., Devine, W. A. and Anderson, R. H. (1990). Polysplenia with normally structured hearts. Am. J. Cardiol. 65, 1274-1275.
16. Gage, P. J., Suh, H. and Camper, S. A. (1999). Dosage requirement of Pitx2 for development of multiple organs. Development 126, 4643-4651.
17. Green, M. C. (1967). A defect of the splanchnic mesoderm caused by the mutant gene dominant hemimelia in the mouse. Dev. Biol. 15, 62-89.
18. Hamada, H., Meno, C., Watanabe, D. and Saijoh, Y. (2002). Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 3, 103-113.
19. Hecksher-Sorensen, J. and Sharpe, J. (2001). 3D confocal reconstruction of gene expression in mouse. Mech. Dev. 100, 59-63.
20. Herbrand, H., Pabst, O., Hill, R. and Arnold, H.-H. (2002). Transcription factors Nkx3.1 and Nkx3.2 (Bapx1) play and overlapping role in sclerotomal development of the mouse. Mech. Dev. 117, 217-224.
21. Herzer, U., Crocoll, A., Barton, D., Howells, N. and Englert, C. (1999). The Wilms tumor suppressor gene wt1 is required for development of the spleen. Curr. Biol. 9, 837-840.
22. Horne-Badovinac, S., Rebagliati, M. and Stainier, D. Y. R. (2003). A cellular framework for gut-looping morphogenesis in Zebrafish. Science 302, 662-665.
23. Ivemark, B. I. (1955). Implications of agenesis of the spleen on the pathogenesis of conotruncus anomalies in childhood; an analysis of the heart malformations in the splenic agenesis syndrome, with fourteen new cases. Acta Paediatr. 44, 7-110.
24. Jacinto, A. and Baum, B. (2003). Actin in development. Mech. Dev. 120, 1337-1349.
25. Kanzler, B. and Dear, T. N. (2001). Hox11 acts cell autonomously in spleen development and its absence results in altered cell fate of mesenchymal spleen precursors. Dev. Biol. 234, 231-243.
26. Kitamura, K., Miura, H., Miyagawa-Tomita, S., Yanazawa, M., Katoh-Fukui, Y., Suzuki, R., Ohuchi, H., Suehiro, A., Motegi, Y., Nakahara, Y. et al. (1999). Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126, 5749-5758.
27. Lettice, L. A., Purdie, L. A., Carlson, G. J., Kilanowski, F., Dorin, J. and Hill, R. E. (1999). The mouse bagpipe gene controls development of axial skeleton, skull, and spleen. Proc. Natl. Acad. Sci. USA 96, 9695-9700.
28. Lettice, L., Hecksher-Sorensen, J. and Hill, R. (2001). The role of Bapx1 (Nkx3. 2) in the development and evolution of the axial skeleton. J. Anat. 199, 181-187.
29. 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.
30. Liu, C., Liu, W., Lu, M. F., Brown, N. A. and Martin, J. F. (2001). Regulation of left-right asymmetry by thresholds of Pitx2c activity. Development 128, 2039-2048.
31. Logan, M., Pagan-Westphal, S. M., Smith, D. M., Paganessi, L. and Tabin, C. J. (1998). The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell 94, 307-317.
32. Lu, J., Richardson, J. A. and Olsen, E. N. (1998). Capsulin: a novel bHLH transcription factor expressed in epicardial progenitors and mesenchyme of visceral organs. Mech. Dev. 73, 23-32.
33. 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.
34. Lu, J., Chang, P., Richardson, J. A., Gan, L., Weiler, H. and Olson, E. N. (2000). The basic helix-loop-helix transcription factor capsulin controls spleen organogenesis. Proc. Natl. Acad Sci. USA 97, 9525-9530.
35. Morgan, D., Turnpenny, L., Goodship, J., Dai, W., Majumder, K., Matthews, L., Gardner, A., Schuster, G., Vien, L., Harrison, W. et al. (1998). Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nat. Genet. 20, 149-156.
36. Mundlos, S., Pelletier, J., Darveau, A., Bachmann, M., Winterpacht, A. and Zabel, B. (1993). Nuclear localisation of the protein encoded by the Wilms' tumor gene WT1 in embryonic and adult tissues. Development 119, 1329-1341.
37. 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.
38. 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.
39. Patterson, K. D., Drysdale, T. A. and Krieg, P. A. (2000). Embryonic origins of spleen asymmetry. Development 127 167-175.
40. Peters, K., Ornitz, D., Werner, S. and Williams, L. (1993). Unique expression pattern of the FGF receptor 3 gene during mouse organogenesis. Dev. Biol. 155, 423-430.
41. Piedra, M. E., Icardo, J. M., Albajar, M., Rodriguez-Rey, J. C. and Ros, M. A. (1998). Pitx2 participates in the late phase of the pathway controlling left-right asymmetry. Cell 94, 319-324.
42. Quinlan, R., Martin, P. and Graham, A. (2004). The role of actin cables in directing the morphogenesis of the pharyngeal pouches. Development 131, 593-599.
43. Roberts, C. W., Shutter, J. R. and Korsmeyer, S. J. (1994). Hox11 controls the genesis of the spleen. Nature 368, 747-749.
44. Rodriguez Esteban, C., Capdevila, J., Economides, A. N., Pascual, J., Ortiz, A. and Izpisua Belmonte, J. C. (1999). The novel Cer-like protein Caronte mediates the establishment of embryonic left-right asymmetry. Nature 401, 243-251.
45. Schneider, A., Mijalski, T., Schlange, T., Daig W., Overbeek, P., Arnold, H. H. and Brand, T. (1999). The homeobox gene NKX3.2 is a target of left-right signalling and is expressed on opposite sides in chick and mouse embryos. Curr. Biol. 9, 911-914.
46. Semina, E. V., Reiter, R., Leysens, N. J., Alward, W. L., Small, K. W., Datson, N. A., Siegel-Bartelt, J., Bieke-Nelson, D., Bitoun, P., Zabel, B. U. et al. (1996). Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat. Genet. 14, 392-399.
47. Seo, J. W., Brown, N. A., Ho, S. Y. and Anderson, R. H. (1992). Abnormal laterality and congenital cardiac anomalies. Relations of visceral and cardiac morphologies in the iv/iv mouse. Circulation 86, 642-650.
48. Sharpe, J., Ahlgren, U., Perry, P., Hill, B., Ross, A., Hecksher-Sorensen, J., Baldock, R. and Davidson, D. (2002). Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296, 541-545.
49. 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.
50. Smith, L. S. (1982). Introduction to Fish Physiology. Neptune, NJ: T. F. H. Publications.
51. Thiel, G. A. and Downey, H. (1921). The development of the mammalian spleen with special reference to its hematopoietic activity. Am. J. Anat. 28, 279-333.
52. Tissier-Seta, J. P., Mucchielli, M. L., Mark, M., Mattei, M. G., Goridis, C. and Brunet, J. F. (1995). Barx1, a new mouse homeodomain transcription factor expressed in cranio-facial ectomesenchyme and the stomach. Mech. Dev. 51, 3-15.
53. Tribioli, C. and Lufkin, T. (1999). The murine Bapx1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development 126, 5699-5711.
54. Tribioli, C., Frasch, M. and Lufkin, T. (1997). Bapx1: an evolutionary conserved homologue of the Drosophila bagpipe homeobox gene is expressed in splanchnic mesoderm and the embryonic skeleton. Mech. Dev. 65, 145-162.
55. Wallace, K. N. and Pack, M. (2003). Unique and conserved aspects of gut development in zebrafish. Dev. Biol. 255, 12-29.
56. Watanabe, D., Saijoh, Y., Nonaka, S., Sasaki, G., Ikawa, Y., Yokoyama, T. and Hamada, H. (2003). The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 130, 1725-1734.
57. Weaver, M., Dunn, N. R. and Hogan, B. L. M. (2000). Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127, 2695-2704.
58. Wilkinson, D. (ed.) (1992). Whole mount in situ hybridisation of vertebrate embryos. In In Situ Hybridisation: a Practical Approach, pp. 75-83. Oxford, UK: IRL Press.
59. Yokoyama, T., Copeland, N. G., Jenkins, N. A., Montgomery, C. A., Elder, F. F. and Overbeek, P. A. (1993). Reversal of left-right asymmetry: a situs inversus mutation. Science 260, 679-682.