Disintegration of the medial epithelial seam: Is cell death important in palatogenesis?

Development Growth and Differentiation

Volumn 53, Issue 2, 2011, Pages 259-268

  Iseki, Sachiko ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Apoptosis; Cell death; Medial edge epithelium; Medial edge seam disintegration; Palatogenesis

Indexed keywords

RECOMBINANT TRANSFORMING GROWTH FACTOR BETA3; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

CELL DEATH; CELL FATE; CELL MIGRATION; CLEFT PALATE; CRANIOFACIAL MORPHOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM; HUMAN; MEDIAL EPITHELIAL SEAM; MORPHOGENESIS; NONHUMAN; NOSE SEPTUM; PALATE; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL DEATH; EPITHELIAL CELLS; HUMANS; PALATE;

EID: 79951843121     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2010.01245.x     Document Type: Review

References (68)

1. Ahmed, S., Liu, C. C. & Nawshad, A. 2007. Mechanisms of palatal epithelial seam disintegration by transforming growth factor (TGF) b3. Dev. Biol. 309, 193-207.
2. Bahi, N., Zhang, J., Llovera, M., Ballester, M., Comella, J. X. & Sanchis, D. 2006. Switch from caspase-dependent to caspase-independent death during heart development: essential role of endonuclease G in ischemia-induced DNA processing of differentiated cardiomyocytes. J. Biol. Chem. 281, 22943-22952.
3. Byrne, C., Tainsky, M. & Fuchs, E. 1994. Programming gene expression in developing epidermis. Development 120, 2369-2383.
4. Carette, M. J. & Ferguson, M. W. 1992. The fate of medial edge epithelial cells during palatal fusion in vitro: an analysis by DiI labelling and confocal microscopy. Development 114, 379-388.
5. Cecconi, F., Alvarez-Bolado, G., Meyer, B. I., Roth, K. A. & Gruss, P. 1998. Apaf1 (CED-4 Homolog) regulates programmed cell death in mammalian development. Cell 94, 727-737.
6. Choi, K. Y., Kim, H. J., Cho, B. C., Kim, I. S., Kim, H. J. & Ryoo, H. M. 2009. A TGF-beta-induced gene, betaig-h3, is crucial for the apoptotic disappearance of the medial edge epithelium in palate fusion. J. Cell. Biochem. 107, 818-825.
7. Chautan, M., Chazal, G., Cecconi, F., Gruss, P. & Golstein, P. 1999. Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr. Biol. 9, 967-970.
8. Chipuk, J. E. & Green, D. R. 2005. Do inducers of apoptosis trigger caspase-independent cell death? Nat. Rev. Mol. Cell Biol. 6, 268-275.
9. Cuervo, R. & Covarrubias, L. 2004. Death is the major fate of medial edge epithelial cells and the cause of basal lamina degradation during palatogenesis. Development 9, 967-970.
10. Cuervo, R., Valencia, C., Chandraratna, R. A. & Covarrubias, L. 2002. Programmed cell death is required for palate shelf fusion and is regulated by retinoic acid. Dev. Biol. 245, 145-156.
11. Cui, X. M., Shiomi, N., Chan, J., Saito, T., Yamamoto, T., Ito, Y., Bringas, P., Chai, Y. & Shuler, C. F. 2005. Over expression of Smad2 in Tgf-b3-null mutant mice rescue cleft palate. Dev. Biol. 278, 192-202.
12. Dassule, H. R., Lewis, P., Bei, M., Maas, R. & McMahon, A. P. 2000. Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785.
13. DeAngelis, V. & Nalbandian, J. 1968. Ultrastructure of mouse and rat palatal processes prior to and during secondary palate formation. Arch. Oral Biol. 13, 601-608.
14. Dixon, J., Jones, N. C., Sandell, L. L., Jayasinghe, S. M., Crane, J., Rey, J. P., Dixon, M. J. & Trainor, P. A. 2006. Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc. Natl. Acad. Sci. USA 103, 13403-13408.
15. Dudas, M., Kim, J., Li, W. Y., Nagy, A., Larsson, J., Karlsson, S., Chai, Y. & Kaartinen, V. 2006. Epithelial and ectomesenchymal role of the type I TGF-beta receptor ALK5 during facial morphogenesis and palatal fusion. Dev. Biol. 296, 298-314.
16. Dudas, M., Li, W.-Y., Kim, J., Tang, A. & Kaartinenm, V. 2007. Palatal fusion - Where do the midline cells go? A review on cleft palate, a major human birth defect Acta Histochem. 109, 1-14.
17. Farbman, A. I. 1968. Electron microscope study of palate fusion in mouse embryos. Dev. Biol. 18, 93-116.
18. Ferguson, M. W. 1988. Palate development. Development 103(Suppl.), 41-61.
19. Fitchett, J. E. & Hay, E. D. 1989. Medial edge epithelium transforms to mesenchyme after embryonic palatal shelves fuse. Dev. Biol. 131, 455-474.
20. Fitzpatrick, D. R., Denhez, F., Kondaiah, P. & Akhurst, R. J. 1990. Differential expression of TGF beta isoforms in murine palatogenesis. Development 109, 585-595.
21. Goudy, S., Law, A., Sanchez, G., Baldwin, H. S. & Brown, C. 2010. Tbx1 is necessary for palatal elongation and elevation. Mech. Dev. 127, 292-300.
22. Griffith, C. M. & Hay, E. D. 1992. Epithelial-mesenchymal transformation during palatal fusion: carboxyfluorescein traces cells at light and electron microscopic levels. Development 116, 1087-1099.
23. Gritli-Linde, A. 2007. Molecular control of secondary palate development. Dev. Biol. 301, 309-326.
24. Gurley, J. M., Wamsley, M. S. & Sandell, L. J. 2004. Alterations in apoptosis and epithelial-mesenchymal transformation in an in vitro cleft palate model. Plast. Reconstr. Surg. 113, 907-914.
25. Hayward, A. F. 1969. Ultrastructural changes in the epithelium during fusion of the palatal processes in rats. Arch. Oral Biol. 14, 661-678.
26. Heldin, C. H., Miyazono, K. & ten Dijke, P. 1997. TGF-beta signaling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
27. Honarpour, N., Du, C., Richardson, J. A., Hammer, R. E., Wang, X. & Herz, J. 2000. Adult Apaf-1-deficient mice exhibit male infertility. Dev. Biol. 218, 248-258.
28. Ito, Y., Yeo, J. Y., Chytil, A., Han, J., Bringas Jr, P., Nakajima, A., Shuler, C. F., Moses, H. L. & Chai, Y. 2003. Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 130, 5269-5280.
29. Jiang, X., Iseki, S., Maxso, R.E., Sucov, H.M. & Morriss-Kay, G.M. 2002. Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241, 106-116.
30. Jin, J.-Z. & Ding, J. 2006. Analysis of cell migration, transdifferentiation and apoptosis during mouse secondary palate fusion. Development 133, 3341-3347.
31. Kaartinen, V., Cui, X. M., Heisterkamp, N., Groffen, J. & Shuler, C. F. 1997. Transforming growth factor-b3 regulates transdifferentiation of medial edge epithelium during palatal fusion and associated degradation of the basement membrane. Dev. Dyn. 209, 255-260.
32. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N. & Groffen, J. 1995. Abnormal lung development and cleft palate in mice lacking TGF-b3 indicates defects of epithelial- mesenchymal interaction. Nat. Genet. 11, 415-421.
33. Kim, J.-E., Kim, S.-J., Jeong, H.-W., Lee, B.-H., Choi, J.-Y., Park, R.-W., Park, J.Y. & Kim, I.-S. 2003. RGD peptides released from big-h3, a TGF-β-induced cell-adhesive molecule, mediate apoptosis. Oncogene 22, 2045-2053.
34. Kroemer, G. & Martin, S. J. 2005. Caspase-independent cell death. Nat. Med. 11, 725-730.
35. Kuida, K., Haydar, T. F., Kuan, C. Y., Gu, Y., Taya, C., Karasuyama, H., Su, M. S., Rakic, P. & Flavell, R. A. 1998. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325-337.
36. Kuida, K., Zheng, T. S., Na, S., Kuan, C., Yang, D., Karasuyama, H., Rakic, P. & Flavell, R. A. 1996. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384, 368-372.
37. Massagué, J. 1998. TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
38. Martínez-Álvarez, C., Tudela, C., Pérez-Miguelsanz, J., O'Kane, S., Puerta, J. & Ferguson, M. W. 2000. Medial edge epithelial cell fate during palatal fusion. Dev. Biol. 220, 343-357.
39. Naiche, L. A., Harrelson, Z., Kelly, R. G. & Papaioannou, V. E. 2005. T-box genes in vertebrate development. Annu. Rev. Genet. 39, 219-239.
40. Nawshad, A. 2008. Palatal seam disintegration: to die or not to die? that is no longer the question. Dev. Dyn. 237, 2643-2656.
41. Nogai, H., Rosowski, M., Grün, J., Rietz, A., Debus, N., Schmidt, G., Lauster, C., Janitz, M., Vortkamp, A. & Lauster, R. 2008. Follistatin antagonizes transforming growth factor-beta3-induced epithelial-mesenchymal transition in vitro: implications for murine palatal development supported by microarray analysis. Differentiation 76, 404-416.
42. Pelton, R. W., Hogan, B. L., Miller, D. A. & Moses, H. L. 1990. Differential expression of genes encoding TGFs beta 1, beta 2, and beta 3 during murine palate formation. Dev. Biol. 141, 456-460.
43. Proetzel, G., Pawlowski, S. A., Wiles, M. V., Yin, M., Boivin, G. P., Howles, P. N., Ding, J., Ferguson, M. W. & Doetschman, T. 1995. Transforming growth factor-beta 3 is required for secondary palate fusion. Nat. Genet. 11, 409-414.
44. Schutte, B. C. & Murray, J. C. 1999a. The many faces and factors of orofacial clefts. Hum. Mol. Genet. 8, 1853-1859.
45. Shapiro, B. L. & Sweney, L. 1969. Electron microscopic and histochemical examination of oral epithelial-mesenchymal interaction (programmed cell death). J. Dent. Res. 48, 652-660.
46. Shuler, C. F., Guo, Y., Majumder, A. & Luo, R. Y. 1991. Molecular and morphologic changes during the epithelial-mesenchymal transformation of palatal shelf medial edge epithelium in vitro. Int. J. Dev. Biol. 35, 463-472.
47. Shuler, C. F., Halpern, D. E., Guo, Y. & Sank, A. C. 1992. Medial edge epithelium fate traced by cell lineage analysis during epithelial-mesenchymal transformation in vivo. Dev. Biol. 154, 318-330.
48. Smiley, G.R. 1970. Fine structure of mouse embroyonic palatal epithelium prior to and after midline fusion. Arch. Oral Biol. 15, 287-294.
49. Smiley, G.R. & Koch, W.E. 1975. A comparison of secondary palate development with different in vitro techniques. Anat. Rec. 181, 711-723.
50. Soriano, P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
51. Takahara, S., Takigawa, T. & Shiota, K. 2004. Programmed cell death is not a necessary prerequisite for fusion of the fetal mouse palate. Int. J. Dev. Biol. 48, 39-46.
52. Takigawa, T. & Shiota, K. 2004. Terminal differentiation of palatal medial edge epithelial cells in vitro is not necessarily dependent on palatal shelf contact and midline epithelial seam formation. Int. J. Dev. Biol. 48, 307-317.
53. Taya, Y., O'Kane, S. & Ferguson, M. W. J. 1999. Pathogenesis of cleft palate in TGF-b3 knockout mice. Development 126, 3869-3879.
54. Trelstad, R.l., Hayashi, A., Hayashi, K. & Donahoe, P. K. 1982. The epithelial-mesenchymal interface of the male rate Mullerian duct: loss of basement membrane integrity and ductal regression. Dev. Biol. 92, 27-40.
55. Tudela, C., Formoso, M. A., Martínez, T., Pérez, R., Aparicio, M., Maestro, C., Del Río, A., Martínez, A., Ferguson, M. & Martínez-Alvarez, C. 2002. TGF-beta3 is required for the adhesion and intercalation of medial edge epithelial cells during palate fusion. Int. J. Dev. Biol. 46, 333-336.
56. Vandenabeele, P., Vanden Berghe, T. & Festjens, N. 2006. Caspase inhibitors promote alternative cell death pathways. Sci. STKE. 358, pe44.
57. Vasioukhin, V., Bauer, C., Degenstein, L., Wise, B. & Fuchs, E. 2001. Hyperproliferation and defects in epithelial polarity upon conditional ablation of α-Catenin in skin. Cell 104, 605-617.
58. Vaziri Sani, F., Kaartinen, V., El Shahawy, M., Linde, A. & Gritli-Linde, A. 2005. Fate-mapping of the epithelial seam during palatal fusion rules out epithelial -mesenchymal transformation. Dev. Biol. 285, 490-495.
59. Waterman, R. E. & Meller, S. M. 1974. Alterations in the epithelial surface of human palatal shelves prior to and during fusion: a scanning electron microscopic study. Anat. Rec. 180, 111-135.
60. Woo, M., Hakem, R., Soengas, M. S., Duncan, G. S., Shahinian, A., Kägi, D., Hakem, A., McCurrach, M., Khoo, W., Kaufman, S. A., Senaldi, G., Howard, T., Lowe, S. W. & Mak, T. W. 1998. Essential contribution of caspase 3/CPP32 to apoptosis and its associated nuclear changes. Genes Dev. 12, 806-819.
61. Xiong, W., He, F., Morikawa, Y., Yu, X., Zhang, Z., Lan, Y., Jiang, R., Cserjesi, P. & Chen, Y. 2009. Hand2 is required in the epithelium for palatogenesis in mice. Dev. Biol. 330, 131-141.
62. Xu, X., Han, J., Ito, Y., Bringas, Jr, P., Urata, M. M. & Chai, Y. 2006. Cell autonomous requirement for Tgfbr2 in the disappearance of medial edge epithelium during palatal fusion. Dev. Biol. 297, 238-248.
63. Yamamoto, T., Cui, X. M. & Shuler, C. F. 2003. Role of ERK1/2 signaling during EGF-induced inhibition of palatal fusion. Dev. Biol. 260, 512-521.
64. Yang, X., Kilgallen, S., Andreeva, V., Spicer, D. B., Pinz, I. & Friesel, R. 2010. Conditional expression of Spry1 in neural crest causes craniofacial and cardiac defects. BMC Dev. Biol. 10, 48.
65. Yoshida, H., Kong, Y. Y., Yoshida, R., Elia, A. J., Hakem, A., Hakem, R., Penninger, J. M. & Mak, T. W. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739-750.
66. Yoshida, T., Vivatbutsiri, P., Morriss-Kay, G., Saga, Y. & Iseki, S. 2008. Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 125, 797-808.
67. Zirzow, S., Lüdtke, T. H., Brons, J. F., Petry, M., Christoffels, V. M. & Kispert, A. 2009. Expression and requirement of T-box transcription factors Tbx2 and Tbx3 during secondary palate development in the mouse. Dev. Biol. 336, 145-155.
68. Zoupa, M., Seppala, M., Mitsiadis, T. & Cobourne, M. T. 2006. Tbx1 is expressed at multiple sites of epithelial-mesenchymal interaction during early development of the facial complex. Int. J. Dev. Biol. 50, 504-510.