Apoptosis in amphibian development

Jean-Marie Exbrayat, Elara N. Moudilou, Lucie Abrouk, Claire Brun

Université de Lyon, UMRS 449, Biologie générale, Université catholique de Lyon, Reproduction et développement comparé, Ecole Pratique des Hautes Etudes, 25 rue du Plat, F-692088, Lyon Cedex 02, France.

DOI: 10.4236/abb.2012.326087                

Abstract

Amphibians and more particularly X. laevis are models often used for studying apoptosis during embryonic development. Using several methods, searchers determined the localization of programmed cell deaths (PCD). Several experimental methods also have been used to understand the regulatory mechanisms of apoptosis, throughout development, contributing to elucidate the general action of several genes and proteins. Apoptosis occurs very early, with a first program under control of maternal genes expressed before MBT, in order to eliminate damaged cells before gastrulation, and a second program at the onset of gastrulation. PCD is also observed during neurulation. Then, apoptotic cells are observed in amphibian organogenesis and metamorphosis. Results of these researches showed both importance of PCD for embryonic development, and the complexity of its regulation. Results obtained can be useful to understand others aspects of the importance of apoptosis, particularly pathological aspects.

Keywords

PCD; Apoptosis; Development; Metamorphosis; Amphibian; Xenopus

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Estabel, J. Konig, N., Shiokawa, K., Exbrayat, J.M. (2005) Apoptosis in Xenopus genus. In: Scovassi, I. Ed., Apoptosis. Research Signpost, Trivandrum, 147-156.
[2]	Nieuwkoop and Faber (1967) Normal table of Xenopus laevis (Daudin), North Holland, Amsterdam.
[3]	Schreiber, A.M., Cai, L., Brown, D.D. (2004) Remodeling of the intestine during metamorphosis of Xenopus laevis. Proceedings of National Academy of Sciences U.S.A., 8, 3720-3725.
[4]	Nakajima, K., Fujimoto, K., Yaoita, Y. (2005) Programmed cell death during amphibian metamorphosis. Seminar in Cell and Developmental Biology, 16, 271-280.
[5]	Glucksman, A. (1951) Cell deaths in normal vertebrate ontogeny. Biological Review, 26, 59-86.
[6]	Imoh, H. (1986) Cell death during normal gastrulation in the newt, Cynops pyrrhogaster. Cell Differentiation, 19, 35-42.
[7]	Sanders, E.K., Torkkeli, P.H., French, A.S. (1997) Patterns of cell death during gastrulation in chick and mouse embryos. Anatomy Embryology, 195, 147-154.
[8]	Hensey, C., Gautier, J. (1998) Programmed cell death during Xenopus development: a spatio-temporal analysis. Developmental Biology, 203, 36-48.
[9]	Cole, L.K., Ross, L.S. (2001) Apoptosis in the developing zebrafish embryo. Developmental Biology, 240, 123-142.
[10]	Kerr, J.F.R., Harmon, B., Searle, J. (1972) Apoptosis: basic biological phenomenon with wide-range implications in tissue kinetics. British Journal of Cancer, 26, 239-257.
[11]	Hensey, C., Gautier, J. (1997) A developmental timer that regulates apoptosis at the onset of gastrulation. Mechanism of Development, 69, 183-195.
[12]	Hensey, C., Gautier, J. (1999) Developmental regulation of induced and programmed cell death in Xenopus embryos. Annals of New York Academy of Sciences, 887, 105-119.
[13]	Greenwood, J., Gautier, J. (2005) From oogenesis through gastrulation: developmental regulation of apoptosis. Seminars in Cell and Developmental Biology, 16, 215-224.
[14]	Stack, J.H., Newport, J.W. (1997) Developmentally regulated activation of apoptosis early in Xenopus gastrulation results in cyclin A degradation during interphase of the cell cycle. Development, 124, 3185-3195.
[15]	Sible, J.C., Anderson, .JA., Lewellyn, A.L., Maller, J.L. (1997) Zygotic transcription is required to block a maternal program of apoptosis in Xenopus embryos. Developmental Biology, 189, 335-346.
[16]	Maller, J.L., Gross, S.D., Schwab, M.S., Finkielstein, C.V., Taieb, F.E., Qian Y.W. (2001) Cell cycle transitions in early Xenopus development. Novartis Foundation Symposia, 237, 58-73.
[17]	Shiokawa, K., Kai, M., Higo, T., Kaito, C., Yokoska, J., Yasuhiko, Y., Kajita, E., Nagano, M., Yamada, Y., Shibata, M., Muto, T., Shinga, J., Hara, H., Takayama, E., Fukamachi, H., Yaoita, Y., Igarashi, K. (2000) Maternal program of apoptosis activated shortly after midblastula transition by overexpression of S-adenosylmethionine decarboxylase in Xenopus early embryos. Comparative Biochemistry Physiology, B Biochemistry and Molecular Biology, 126, 149-155.
[18]	Kaito, C., Kai, M., Higo, T., Takayama, E., Fukamachi, H., Sekimizu, K., Shiokawa, K. (2001) Activation of the maternally preset program of apoptosis by microinjection of 5-aza-2'-deoxycytidine and 5-methyl-2'-deoxycytidine-5'-triphosphate in Xenopus laevis embryos. Development, Growth, Differentiation, 43, 383-390.
[19]	Takayama, E., Higo, T., Kai, M., Fukasawa, M., Nakajima, K., Hara, H., Tadakuma, T., Igarashi K., Yaoita, Y., Shiokawa, K. (2004) Involvement of caspase-9 in execution of the maternal program of apoptosis in Xenopus late blastulae overexpressed with S-adenosylmethionine decarboxylase. Biochemical and Biophysical Research Communications, 24, 325, 1367-1375.
[20]	Carter, A.D., Sible, J.C. (2003) Loss of XChk1 function triggers apoptosis after the midblastula transition in Xenopus laevis embryos. Mechanism of Development, 120, 315-323.
[21]	Kai, M., Kaito, C., Fukamachi, H., Higo, T., Takayama, E., Hara, H., Ohya, Y., Igarashi, K., Shiokawa, K. (2003) Overexpression of S-adenosylmethionine decarboxylase (SAMDC) in Xenopus embryos activates maternal program of apoptosis as a “fail-safe” mechanism of early embryogenesis. Cell Research, 13, 147-158.
[22]	Wroble, B.N., Sible, J.C. (2005) Chk2/Cds1 protein kinase blocks apoptosis during early development of Xenopus laevis. Developmental Dynamics, 233, 1359-1365.
[23]	Ruzov, A., Shorning, B., Mortusewicz, O., Dunican, D.S., Leonhard T, H., Meehan, R.R. (2009) MBD4 and MLH1 are required for apoptotic induction in xDNMT1-depleted embryos. Development, 136, 2277-2286.
[24]	De Marco, N., Campanella, C., Carotenuto, R. (2011) In X. laevis embryos high levels of the anti-apoptotic factor p27BBP/eIF6 are stage-dependently found in BrdU and TUNEL-reactive territories. Zygote, 19, 157-163.
[25]	Schuff, M., Siegel, D., Bardine, N., Oswald, F., Donow, C., Knichel, W. (2009) FoxO genes are dispensable during gastrulation but required for late embryogenesis in Xenopus laevis. Developmental Biology, 15, 259-273.
[26]	Trindade, M., Messenger, N., Papin, C., Grimmer, D., Fairclough, L., Tada, M., Smith, J.C. (2003) Regulation of apoptosis in the Xenopus embryo by Bix3. Development, 130, 4611-4622.
[27]	Ikegami, R., Hunter, P., Yager, T.D. (1999) Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo. Developmental Biology, 15, 409-433.
[28]	Endo, T., Kusakabe, M., Sunadome, K., Yamamoto, T., Nishida, E. (2011) The kinase SGK1 in the endoderm and mesoderm promotes ectodermal survival by down-regulating components of the death-inducing signaling complex. Science of Signalisation, 18, 156.
[29]	Wallingford, J.B., Seufert, D.W., Virta, V.C., Vize, P.D. (1997) p53 activity is essential for normal development in Xenopus. Current Biology, 7, 747-757.
[30]	Malikova, M.A., Van Stry, M., Symes, K. (2007) Apoptosis regulates notochord development in Xenopus. Developmental Biology, 311, 434-448.
[31]	Andreazzoli, M., Gestri, G., Angeloni, D., Menna, E., Barsacchi, G. (1999) Role of Xrx1 in Xenopus eye and anterior brain development. Development, 126, 2451-2460.
[32]	Yeo, W., Gautier, J. (2003) A role for programmed cell death during early neurogenesis in Xenopus. Developmental Biology, 260, 31-45.
[33]	Kim, G.H., Park, E., Han, J.K. (2005) The assembly of POSH-JNK regulates Xenopus anterior neural development. Developmental Biology, 286, 256-269.
[34]	Sugimoto, K., Okabayashi, K., Sedohara, A., Hayata, T., Asashima, M. (2007) The role of XBtg2 in Xenopus neural development. Developmental Neurosciences, 29, 468-479.
[35]	Tribulo, C., Aybar, M., Sanchez, S.S., Mayor, R. (2004) A balance between the anti-apoptotic activity of Slug and the apoptotic activity of msx1 is required for the proper development of the neural crest. Developmental Biology, 275, 325-342.
[36]	Carl, T.F., Dufton, C., Hanken, J., Klymkowsky, M.W. (1999) Inhibition of neural crest migration in Xenopus using antisense slug RNA. Developmental Biology, 213, 101-115.
[37]	Aybar, M.J., Nieto, A., Mayor, R. (2003) Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest. Development, 30, 483-494.
[38]	La Bonne, C., Bronner-Fraser, M. (2000) Snail-related transcriptional repressors are required in Xenopus for both the induction of the neural crest and its subsequent migration. Developmental Biology, 221, 195-205.
[39]	Mayor, R., Guerrero, N., Young, R.M., Gomez-Skarmeta, J.L., Cuellar, C. (2000) A novel function for the Xslug gene: control of dorsal mesendoderm development by repressing BMP-4. Mechanism of Development, 97, 47-56.
[40]	Schneider, M., Schambony, A., Wedlich, D. (2010) Prohibitin1 acts as a neural crest specifier in Xenopus development by repressing the transcription factor E2F1. Development, 137, 4073-4081.
[41]	De Marco, N., Iannone, L., Carotenuto, R., Biffo, S., Vitale, A., Campanella, C. (2010) p27(BBP)/eIF6 acts as an anti-apoptotic factor upstream of Bcl-2 during Xenopus laevis development. Cell Death Differentiation, 17, 360-372.
[42]	Hutson, L.D., Bothwell, M. (2001) Expression and function of Xenopus laevis p75(NTR) suggest evolution of developmental regulatory mechanisms. Journal of Neurobiology, 49, 79-98.
[43]	Estabel, J. (2004).Apoptoses physiologiques et apoptoses expérimentalement induites au cours du développement de Xenopus laevis, Ph.D. Thesis, EPHE, Lyon.
[44]	Poitras, L., Bisson, N., Islam, N., Moss, T. (2003) A tissue restricted role for the Xenopus Jun N-terminal kinase MLK2 in cement gland and pronephric tubule differentiation. Developmental Biology, 254, 200-214.
[45]	Weber, R. (1964); Ultrastructural changes in regressing tail muscles of Xenopus laevis at metamorphosis Journal of Cell Biology, 22, 481-487.
[46]	Kerr, J.F.R., Harmon, B., Searle, J. (1974) An electron-microscope study of cell deletion in the Anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated tail muscle fibres. Journal of Cell Science, 14, 571-585.
[47]	Tata, J.R. (1996) Metamorphosis: an exquisite model for hormonal regulation of post-embryonic development. Biochemical Society Symposia, 62, 123-136.
[48]	Shi, Y.B., Ihizuya-Oka, A. (2001) Thyroid-hormone regulation of apoptotic tissue remodeling implications from molecular analysis of amphibian metamorphosis. Progress in Nucleic Acid Research and Molecular Biology, 65, 53-100.
[49]	Bertrand, S. Laudet, V. (2001) La métamorphose des amphibiens: un modèle prometteur pour étudier les protéases de la matrice. Médecine/Sciences, 17, 1195-1200.
[50]	Dodd, M.H.I., Dodd, J.M. (1976) Physiology of the Amphibia. In: Loft, B. Ed., Academic Press, New York.
[51]	Su, Y., Damjanowski, S, Shi, Y., Shi, Y.B. (1999) Molecular and cellular basis of tissue remodeling during amphibian metamorphosis. Histology Histopathology, 14, 175-183.
[52]	Ishizuya-Oka, A., Hasebe, T., Shi, Y.B. (2010). Apoptosis in amphibian organs during metamorphosis. Apoptosis, 15, 350-364.
[53]	Tata, J.R. (2006) Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Molecular and Cellular Endocrinology, 26, 246, 10-20.
[54]	Kanamori, A., Brown, D.D. (1996) The analysis of complex developmental programmes: amphibian metamorphosis. Genes Cells. 1, 429-435.
[55]	Du Pasquier, D., Rinheval, V., Sinzelle, L., Chesneau, A., Ballagny, C., Sachs, L.M., Demeneix, B., Mazabraud, A.(2006). Developmental cell death during Xenopus metamorphosis involves BID cleavage and caspase2 and 8 activation. Developmental Dynamics, 235, 2083-2094.
[56]	Estabel, J., Mercer, A., Koenig, N., Exbrayat, J.-M. (2003) Programmed cell death in Xenopus laenis metamorphosis development prior to, and during, metamorphosis. Life Science, 73, 3298-3306.
[57]	Marsh-Armstrong, N., Cai, L., Brown, D.D. (2004) Thyroid hormone controls the development of connections between the spinal cord and limbs during Xenopus laevis metamorphosis. Proceedings of National Academy of Sciences U S A., 101, 165-170.
[58]	Hughes, A.F. (1961) Cell degeneration in the larval ventral horn of Xenopus laevis. Journal of Embryology and Experimental Morphology, 9, 269-284.
[59]	Prestige, M.C. (1965) Cell turnover in the spinal ganglia of Xenopus laevis tadpoles. Journal of Embryology and Experimental Morphology, 13, 63-72.
[60]	Hourdry, J., Beaumont, A. (1985) Les métamorphoses des amphibiens. Masson, Paris.
[61]	Jenkins, S., Straznicky, C. (1986) Naturally occurring and induced ganglion cell death. A retinal whole-mount autoradiographic study in Xenopus. Anatomical Embryology, 174, 59-66.
[62]	Gaze, R.M., Grant, P. (1992) Spatio-temporal patterns of retinal ganglion cell death during Xenopus development. Journal of Comparative Neurology, 315, 264-274.
[63]	Udin, S.B., Grant, S. (1999). Plasticity in the tectum of Xenopus laevis: binocular maps. Program in Neurobiology, 59, 81-106.
[64]	Oppenheim, R.W. (1991) Cell death during development of the nervous system. Annual Review of Neurosciences, 14, 453-501.
[65]	Robert, A., Clarke, J.D.W. (1982) The neuronatomy of an Amphibian embryo spinal cord. Philosophical Transactions of Royal Society of London, B, 296, 195-212.
[66]	Lamborghini, J.E. (1987) Disappearance of Rohon-Beard neurons from the spinal cord of Xenopus laevis. Journal of Comparative Neurology, 264, 47-55.
[67]	Coen, L., Du Pasquier, D., Le Mevel, S., Brown, S., Tata, J., Mazabraud, A., Demeneix, B.A. (2001) Xenopus Bcl-X(L) selectively protects Rohon-Beard neurons from metamorphic degeneration. Proceedings of National Academy of Sciences USA, 98, 7869-7874.
[68]	Cruz-Reyes, J., Tata, J.R. (1995) Cloning, characterization and expression of two Bcl-2 like cell survival genes. Gene, 158, 171-179.
[69]	Nakajima, K., Yaoita, Y. (2003) Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Development Dynamics, 227, 246-255.
[70]	Nishikawa, A., Hayashi, H. (1995) Spatial, temporal and hormonal regulation of programmed muscles cell death during metamorphosis of the frog Xenopus laevis. Differentiation, 59, 207-214.
[71]	Sachs, L.M., Abdallah, B., Hassan, A. Levi, G., Read, J.C., Demeneix, B.A. (1997) Apoptosis in Xenopus tadpole tail muscles involves Bax-dependent pathways. FASEB Journal, 11, 801-808
[72]	Das, B., Schreider, A.M., Huag, H., Brown, D.D.(2002) Multiple thyroid hormone-induced muscle growth and death programs during metamorphosis in Xenopus laevis. Proceedings of National Academy of Sciences USA, 99, 12230-12235.
[73]	Rowe, I., Le Blay, K., Du Pasquier, D., Palmier, K., Levi, G., Demeneix, B., Coen, L. (2005) Apoptosis of tail muscle during amphibian metamorphosis involves a caspase 9-dependent mechanism. Developmental Dynamics, 233, 76-87.
[74]	Shi, Y.B., Ishizuya-Oka, A. (1996) Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Current Topics in Developmental Biology, 32, 205-235.
[75]	Ishizuya-Oka, A., Ueda, S. (1996) Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell and Tissue Research, 286, 467-476.
[76]	Atkinson, B.G., Helbing, C., Chen, Y.Q. (1994) Perspectives in comparative endocrinology. In: Davy, D.G., Tobe, S.S., Peter, R.G. Eds. National Research Council of Canada, Ottawa, 416.
[77]	Shi, Y.B., Ishizuya-Oka, A. (1997) Autoactivation of Xenopus Thyroid Hormone Receptor beta Genes Correlates with Larval Epithelial Apoptosis and Adult Cell Proliferation. Journal of Biomedical Science, 4, 9-18.
[78]	Shi, Y.B., Ishizuya-Oka, A. (2001) Thyroid hormone regulation of apoptotic tissue remodeling: implications from molecular analysis of amphibian metamorphosis. Progress in Nucleic Acid Research and Molecular Biology, 65, 53-100.
[79]	Ishizuya-Oka, A., Ueda, S., Inokuchi, T., Amano, T., Damjanovski, S., Stolow, M., Shi, YB. (2001) Thyroid hormone-induced expression of sonic hedgehog correlates with adult epithelial development during remodeling of the Xenopus stomach and intestine. Differentiation, 69, 27-37.
[80]	Kaltenbach, J.C., Fry, A.E., Colpitts, K.M., Faszewski, .EE. (2012) Apoptosis in the digestive tract of herbivorous Rana pipiens larvae and carnivorous Ceratophrys ornata larvae: an immunohistochemical study. Journal of Morphology, 273, 103-108.
[81]	Hasebe, T., Kajita, M., Fujimoto, K., Yaoita, Y., Ishizuya-Oka, A.(2007) Expression profiles of the duplicated matrix metalloproteinase-9 genes suggest their different roles in apoptosis of larval intestinal epithelial cells during Xenopus laevis metamorphosis. Developmental Dynamics, 236, 2338-2345.
[82]	Ishizuya-Oka, A., Shi, Y.B. (2005) Molecular mechanisms for thyroid hormone-induced remodeling in the amphibian digestive tract: a model for studying organ regeneration. Development Growth Differentiation, 47, 601-607.
[83]	Schreiber, A.M., Brown, D.D. (2003) Tadpole skin dies autonomously in response to thyroid hormone at metamorphosis. Proceedings of National Academy of Sciences U S A., 100, 1769-1774.
[84]	Tamori, Y., Wakahara, M. (2000) Conversion of red blood cells (RBCs) from the larval to the adult type during metamorphosis in Xenopus: specific removal of mature larval-type RBCs by apoptosis. International Journal of Developmental Biology, 44, 373-380.
[85]	Yaoita, Y., Shi, Y.B., Brown, D.D. (1990) Xenopus laevis alpha and beta thyroid hormone receptors. Proceedings of the National Academy of Sciences of the USA, 87, 7090–7094.
[86]	Shi, Y.B., Ishizuya-Oka, A. (1996) Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Current Topics in Developmental Biology, 32, 205-235.
[87]	Shi, Y.B., Li, Q., Damjanovski, S., Aano, T., Ishizuya-Oka, A. (1998) Regulation of apoptosis during development: input from the extracellular matrix (review). International Journal of Molecular Medicine, 2, 273-282.
[88]	Shi, Y.B., Sachs, L.M., Jones, P., Li, Q., Ishizuya-Oka, A. (1998) Thyroid hormone regulation of Xenopus laevis metamorphosis: functions of thyroid hormone receptors and roles of extracellular matrix remodeling. Wound Repair Regeneration, 6, 314-322.
[89]	Berry, D.L., Schwartzman, R.A., Brown, D.D. (1998) The expression pattern of thyroid hormone response genes in the tadpole tail identifies multiple resorption programs. Developmental Biology, 203, 12-23.
[90]	Ishizuya-Oka, A., Shi, Y.B. (2005) Molecular mechanisms for thyroid hormone-induced remodeling in the amphibian digestive tract: a model for studying organ regeneration. Development Growth Differentiation, 47, 601-607.
[91]	Ishizuya-Oka, A., Shi, Y.B. (2008) Thyroid hormone regulation of stem cell development during intestinal remodeling. Molecular Cellular Endocrinology, 288, 71-78.
[92]	Hasebe, T., Hartman, R., Matsuda, H. Shi, Y.B. (2006) Spatial and temporal expression profiles suggest the in-volvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis. Cell and Tissue Research, 324, 105-116.
[93]	Hasebe, T., Kajita, M., Iwabuchi, M., Ohsumi, K., Ishizuya-Oka, A. (2011) Thyroid hormone-regulated expression of nuclear lamins correlates with dedifferentiation of intestinal epithelial cells during Xenopus laevis metamorphosis. Developmental Genes and Evolution, 221, 199-208.
[94]	Hasebe T, Kajita M, Shi YB, Ishizuya-Oka A (2008) Thyroid hormone-up-regulated hedgehog interacting protein is involved in larval-to-adult intestinal remodeling by regulating sonic hedgehog signaling pathway in Xenopus laevis. Developmental Dynamics, 237, 3006-3015.
[95]	Wang, G.J., Schmued, L.C., Andrews, A.M., Scallet, A.C., Slikker, W., Binienda, Z. (2000) Systemic administration of domic acid-induced spinal cord lesions in neonatal rats. Journal of Spinal Cord Medicine, 23, 31-39.
[96]	Estabel, J., Exbrayat, J.M. (2002) Localisation des récepteurs AMPA/kainate dans les organes périphériques chez Xenopus laevis par immunohistochimie. Revue Francaise d’Histotechnologie, 15, 9-14.
[97]	Mouterfi, N., Moudilou, E., Estabel, J., Konig, N., Benyamin, Y., Exbrayat, J.M. (2006) Effets d’un traitement pharmacologique par un antagoniste des récepteurs ionotropes du glutamate sur l’apoptose et l’expression des calpaines chez des têtards. Revue Francaise d’Histotechnologie, 19, 113-117.
[98]	Mouterfi, N., Moudilou, E.N., Exbrayat J.M., Brun, C. (2007) Glutamate induced calpains-like expression in Xenopus laevis development. 14th European Congress of Herpetology., September 2007, Porto (Portugal), Abstracts, 25.
[99]	Moudilou, E.N., Mouterfi, N., Exbrayat, J.M., Brun, C. (2010) Calpains expression during Xenopus laevis development. Tissue and Cell, 42, 275–281.
[100]	Rowe, I., Coen, L., Le Blay, K., Le Mevel, S., Demeneix, B.A. (2002) Autonomous regulation of muscle fibre fate during metamorphosis in Xenopus tropicalis. Developmental Dynamics, 224, 381-390.
[101]	Del Pino, E.M., Medina, A. (1998) Neural development in the marsupial frog Gastrotheca riobambae. International Journal of Developmental Biology, 42, 723-731.
[102]	Haydar, T.H., Kuan, C.I., Flavell, R.A., Rakic, P. (1999) The role of cell death in regulating the size and shape of the mammalian forebrain. Cerebral Cortex, 9, 621-626.