Skip to main content
SpringerLink
Log in

Apoptosis in amphibian organs during metamorphosis

  • Unusual Model Systems for Cell Death Research
  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

During amphibian metamorphosis, the larval tissues/organs rapidly degenerate to adapt from the aquatic to the terrestrial life. At the cellular level, a large quantity of apoptosis occurs in a spatiotemporally-regulated fashion in different organs to ensure timely removal of larval organs/tissues and the development of adult ones for the survival of the individuals. Thus, amphibian metamorphosis provides us a good opportunity to understand the mechanisms regulating apoptosis. To investigate this process at the molecular level, a number of thyroid hormone (TH) response genes have been isolated from several organs of Xenopus laevis tadpoles and their expression and functional analyses are now in progress using modern molecular and genetic technologies. In this review, we will first summarize when and where apoptosis occurs in typical larva-specific and larval-to-adult remodeling amphibian organs to highlight that the timing of apoptosis is different in different tissues/organs, even though all are induced by the same circulating TH. Next, to discuss how TH spatiotemporally regulates the apoptosis, we will focus on apoptosis of the X. laevis small intestine, one of the best characterized remodeling organs. Functional studies of TH response genes using transgenic frogs and culture techniques have shown that apoptosis of larval epithelial cells can be induced by TH either cell-autonomously or indirectly through interactions with extracellular matrix (ECM) components of the underlying basal lamina. Here, we propose that multiple intra- and extracellular apoptotic pathways are coordinately controlled by TH to ensure massive but well-organized apoptosis, which is essential for the proper progression of amphibian metamorphosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Shi Y-B (1999) Amphibian metamorphosis: from morphology to molecular biology. Wiley, New York

    Google Scholar 

  2. Tata JR (1993) Gene expression during metamorphosis: an ideal model for post-embryonic development. Bioessays 15:239–248

    Article  PubMed  CAS  Google Scholar 

  3. Yoshizato K (1989) Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Int Rev Cytol 119:97–149

    Article  PubMed  CAS  Google Scholar 

  4. Wyllie AH, Kerr JF, Currie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251–306

    Article  PubMed  CAS  Google Scholar 

  5. Kerr JF, 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 muscle fibers. J Cell Sci 14:571–585

    PubMed  CAS  Google Scholar 

  6. Decker RS (1976) Influence of thyroid hormones on neuronal death and differentiation in larval Rana pipiens. Dev Biol 49:101–118

    Article  PubMed  CAS  Google Scholar 

  7. Ishizuya-Oka A, Shimozawa A (1992) Programmed cell death and heterolysis of larval epithelial cells by macrophage-like cells in the anuran small intestine in vivo and in vitro. J Morphol 213:185–195

    Article  PubMed  CAS  Google Scholar 

  8. Dodd MHI, Dodd JM (1976) The biology of metamorphosis. In: Lofts B (ed) Physiology of amphibia. Academic Press, New York, pp 467–599

    Google Scholar 

  9. Kikuyama S, Kawamura K, Tanaka S, Yamamoto K (1993) Aspects of amphibian metamorphosis: hormonal control. Int Rev Cytol 145:105–148

    Article  PubMed  CAS  Google Scholar 

  10. Tata JR (1966) Requirement for RNA and protein synthesis for induced regression of the tadpole tail in organ culture. Dev Biol 13:77–94

    Article  PubMed  CAS  Google Scholar 

  11. Derby A, Jeffrey JJ, Eisen AZ (1979) The induction of collagenase and acid phosphatase by thyroxine in resorbing tadpole gills in vitro. J Exp Zool 207:391–398

    Article  CAS  Google Scholar 

  12. Kinoshita T, Sasaki F, Watanabe K (1986) Regional specificity of anuran larval skin during metamorphosis: dermal specificity in development and histolysis of recombined skin grafts. Cell Tissue Res 245:297–304

    Article  PubMed  CAS  Google Scholar 

  13. Niki K, Namiki H, Kikuyama S, Yoshizato K (1982) Epidermal tissue requirement for tadpole tail regression induced by thyroid hormone. Dev Biol 94:116–120

    Article  PubMed  CAS  Google Scholar 

  14. Yoshizato K (2007) Molecular mechanism and evolutional significance of epithelial-mesenchymal interactions in the body- and tail-dependent metamorphic transformation of anuran larval skin. Int Rev Cytol 260:213–260

    Article  PubMed  CAS  Google Scholar 

  15. Shi Y-B, Brown DD (1993) The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J Biol Chem 268:20312–20317

    PubMed  CAS  Google Scholar 

  16. Wang Z, Brown DD (1993) Thyroid hormone-induced gene expression program for amphibian tail resorption. J Biol Chem 268:16270–16278

    PubMed  CAS  Google Scholar 

  17. Buchholz DR, Heimeier RA, Das B, Washington T, Shi Y-B (2007) Pairing morphology with gene expression in thyroid hormone-induced intestinal remodeling and identification of a core set of TH-induced genes across tadpole tissues. Dev Biol 303:576–590

    Article  PubMed  CAS  Google Scholar 

  18. Das B, Cai L, Carter MG, Piao YL, Sharov AA, Ko MS, Brown DD (2006) Gene expression changes at metamorphosis induced by thyroid hormone in Xenopus laevis tadpoles. Dev Biol 291:342–355

    Article  PubMed  CAS  Google Scholar 

  19. Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). Garland, New York

    Google Scholar 

  20. Taylor AC, Kollros JJ (1946) Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7–23

    Article  Google Scholar 

  21. Rossi A (1958) Tavole cronologiche dello sviluppo embrionale e larvale del Bufo bufo (L.). Monit Zool Ital 66:133–149

    Google Scholar 

  22. Berry DL, Schwartzman RA, Brown DD (1998) The expression pattern of thyroid hormone response genes in the tadpole tail identifies multiple resorption programs. Dev Biol 203:12–23

    Article  PubMed  CAS  Google Scholar 

  23. Davis BP, Jeffrey JJ, Eisen AZ, Derby A (1975) The induction of collagenase by thyroxine in resorbing tadpole tailfin in vitro. Dev Biol 44:217–222

    Article  PubMed  CAS  Google Scholar 

  24. Estabel J, Mercer A, Konig N, Exbrayat JM (2003) Programmed cell death in Xenopus laevis spinal cord, tail and other tissues, prior to, and during, metamorphosis. Life Sci 73:3297–3306

    Article  PubMed  CAS  Google Scholar 

  25. Little GH, Flores A (1996) Programmed cell death in the anuran tadpole tail requires expression of a cell surface glycoprotein. Comp Biochem Physiol B Biochem Mol Biol 113:289–293

    Article  PubMed  CAS  Google Scholar 

  26. Mathew S, Fu L, Fiorentino M, Matsuda H, Das B, Shi Y-B (2009) Differential regulation of cell type-specific apoptosis by stromelysin-3: a potential mechanism via the cleavage of the laminin receptor during tail resorption in Xenopus laevis. J Biol Chem 284:18545–18556

    Article  PubMed  CAS  Google Scholar 

  27. Nakajima K, Fujimoto K, Yaoita Y (2005) Programmed cell death during amphibian metamorphosis. Semin Cell Dev Biol 16:271–280

    Article  PubMed  CAS  Google Scholar 

  28. Nakajima K, Yaoita Y (2003) Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Dev Dyn 227:246–255

    Article  PubMed  CAS  Google Scholar 

  29. Nishikawa A, Hayashi H (1995) Spatial, temporal and hormonal regulation of programmed muscle cell death during metamorphosis of the frog Xenopus laevis. Differentiation 59:207–214

    Article  PubMed  CAS  Google Scholar 

  30. 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. Dev Dyn 233:76–87

    Article  PubMed  CAS  Google Scholar 

  31. Sachs LM, Abdallah B, Hassan A, Levi G, De Luze A, Reed JC, Demeneix BA (1997) Apoptosis in Xenopus tadpole tail muscles involves Bax-dependent pathways. FASEB J 11:801–808

    PubMed  CAS  Google Scholar 

  32. Kinoshita T, Sasaki F, Watanabe K (1985) Autolysis and heterolysis of the epidermal cells in anuran tadpole tail regression. J Morphol 185:269–275

    Article  Google Scholar 

  33. Niki K, Yoshizato K (1986) An epidermal factor which induces thyroid hormone-dependent regression of mesenchymal tissues of the tadpole tail. Dev Biol 118:306–308

    Article  PubMed  CAS  Google Scholar 

  34. Atkinson BG (1975) Biochemical and histological changes in the respiratory system of Rana catesbeiana larvae during normal and induced metamorphosis. Dev Biol 45:151–165

    Article  PubMed  CAS  Google Scholar 

  35. Cooper EL (1967) Lympho-myeloid organs of Amphibia. I. Appearance during larval and adult stages of Rana catesbeiana. J Morphol 122:381–397

    Article  PubMed  CAS  Google Scholar 

  36. Minnich B, Bartel H, Lametschwandtner A (2002) How a highly complex three-dimensional network of blood vessels regresses: the gill blood vascular system of tadpoles of Xenopus during metamorphosis. A SEM study on microvascular corrosion casts. Microvasc Res 64:425–437

    Article  PubMed  Google Scholar 

  37. Gilbert LI, Frieden E (1981) Metamorphosis, a problem in developmental biology. Plenum Press, New York

    Google Scholar 

  38. Coen L, Le Blay K, Rowe I, Demeneix BA (2007) Caspase-9 regulates apoptosis/proliferation balance during metamorphic brain remodeling in Xenopus. Proc Natl Acad Sci USA 104:8502–8507

    Article  PubMed  CAS  Google Scholar 

  39. Denver RJ (1998) The molecular basis of thyroid hormone-dependent central nervous system remodeling during amphibian metamorphosis. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 119:219–228

    Article  PubMed  CAS  Google Scholar 

  40. Kollros JJ, Thiesse ML (1985) Growth and death of cells of the mesencephalic fifth nucleus in Xenopus laevis larvae. J Comp Neurol 233:481–489

    Article  PubMed  CAS  Google Scholar 

  41. Kollros JJ (1984) Growth and death of cells of the mesencephalic fifth nucleus in Rana pipiens larvae. J Comp Neurol 224:386–394

    Article  PubMed  CAS  Google Scholar 

  42. 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. Dev Growth Differ 47:601–607

    Article  PubMed  CAS  Google Scholar 

  43. Shi Y-B, Ishizuya-Oka A (1996) Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Curr Top Dev Biol 32:205–235

    Article  PubMed  CAS  Google Scholar 

  44. Shi Y-B, Li Q, Damjanovski S, Amano T, Ishizuya-Oka A (1998) Regulation of apoptosis during development: input from the extracellular matrix (Review). Int J Mol Med 2:273–282

    PubMed  CAS  Google Scholar 

  45. Ishizuya-Oka A, Ueda S (1996) Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res 286:467–476

    Article  PubMed  CAS  Google Scholar 

  46. Pearl EJ, Bilogan CK, Mukhi S, Brown DD, Horb ME (2009) Xenopus pancreas development. Dev Dyn 238:1271–1286

    Article  PubMed  CAS  Google Scholar 

  47. Mukhi S, Mao J, Brown DD (2008) Remodeling the exocrine pancreas at metamorphosis in Xenopus laevis. Proc Natl Acad Sci USA 105:8962–8967

    Article  PubMed  Google Scholar 

  48. Kaung HC (1983) Changes of pancreatic beta cell population during larval development of Rana pipiens. Gen Comp Endocrinol 49:50–56

    Article  PubMed  CAS  Google Scholar 

  49. Farrar ES, Hulsebus JJ (1988) Morphometry of pancreatic beta cell populations during larval growth and metamorphosis of Rana catesbeiana. Gen Comp Endocrinol 69:65–70

    Article  PubMed  CAS  Google Scholar 

  50. Accordi F, Chimenti C (2001) Programmed cell death in the pancreas of Bufo bufo during metamorphosis. J Anat 199:419–427

    Article  PubMed  CAS  Google Scholar 

  51. Rollins-Smith LA (1998) Metamorphosis and the amphibian immune system. Immunol Rev 166:221–230

    Article  PubMed  CAS  Google Scholar 

  52. Manning MJ, Horton JD (1969) Histogenesis of lymphoid organs in larvae of the South African clawed toad, Xenopus laevis (Daudin). J Embryol Exp Morphol 22:265–277

    PubMed  CAS  Google Scholar 

  53. Grant P, Clothier RH, Johnson RO, Ruben LN (1998) In situ lymphocyte apoptosis in larval Xenopus laevis, the South African clawed toad. Dev Comp Immunol 22:449–455

    Article  PubMed  CAS  Google Scholar 

  54. Dorn AR, Broyles RH (1982) Erythrocyte differentiation during the metamorphic hemoglobin switch of Rana catesbeiana. Proc Natl Acad Sci USA 79:5592–5596

    Article  PubMed  CAS  Google Scholar 

  55. Hasebe T, Kawamura K, Kikuyama S (1996) Genomic DNA fragmentation in red blood cells of the bullfrog during metamorphosis. Dev Growth Differ 38:605–615

    Article  CAS  Google Scholar 

  56. Hasebe T, Oshima H, Kawamura K, Kikuyama S (1999) Rapid and selective removal of larval erythrocytes from systemic circulation during metamorphosis of the bullfrog, Rana catesbeiana. Dev Growth Differ 41:639–643

    Article  PubMed  CAS  Google Scholar 

  57. 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. Int J Dev Biol 44:373–380

    PubMed  CAS  Google Scholar 

  58. Mello MLS, Maria SS, Schildknecht PHPA, Grazziotin NA (2000) DNA fragmentation in programmed cell death in nucleate erythrocytes: a cytochemical analysis. Acta Histochem Cytochem 33:355–359

    Article  Google Scholar 

  59. Balls M, Bownes M (1985) Metamorphosis. Oxford University Press, New York

    Google Scholar 

  60. Kawasaki H, Iwamuro S (2008) Potential roles of histones in host defense as antimicrobial agents. Infect Disord Drug Targets 8:195–205

    PubMed  CAS  Google Scholar 

  61. Kawai A, Ikeya J, Kinoshita T, Yoshizato K (1994) A three-step mechanism of action of thyroid hormone and mesenchyme in metamorphic changes in anuran larval skin. Dev Biol 166:477–488

    Article  PubMed  CAS  Google Scholar 

  62. Suzuki K, Machiyama F, Nishino S, Watanabe Y, Kashiwagi K, Kashiwagi A, Yoshizato K (2009) Molecular features of thyroid hormone-regulated skin remodeling in Xenopus laevis during metamorphosis. Dev Growth Differ 51:411–427

    PubMed  CAS  Google Scholar 

  63. Izutsu Y, Yoshizato K (1993) Metamorphosis-dependent recognition of larval skin as non-self by inbred adult frogs (Xenopus laevis). J Exp Zool 266:163–167

    Article  PubMed  CAS  Google Scholar 

  64. Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205–219

    Article  PubMed  CAS  Google Scholar 

  65. Degterev A, Boyce M, Yuan J (2003) A decade of caspases. Oncogene 22:8543–8567

    Article  PubMed  CAS  Google Scholar 

  66. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281:1312–1316

    Article  PubMed  CAS  Google Scholar 

  67. Green DR, Kroemer G (2004) The pathophysiology of mitochondrial cell death. Science 305:626–629

    Article  PubMed  CAS  Google Scholar 

  68. Spierings D, McStay G, Saleh M, Bender C, Chipuk J, Maurer U, Green DR (2005) Connected to death: the (unexpurgated) mitochondrial pathway of apoptosis. Science 310:66–67

    Article  PubMed  CAS  Google Scholar 

  69. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656

    Article  PubMed  CAS  Google Scholar 

  70. Becker KB, Stephens KC, Davey JC, Schneider MJ, Galton VA (1997) The type 2 and type 3 iodothyronine deiodinases play important roles in coordinating development in Rana catesbeiana tadpoles. Endocrinology 138:2989–2997

    Article  PubMed  CAS  Google Scholar 

  71. Gereben B, Zavacki AM, Ribich S, Kim BW, Huang SA, Simonides WS, Zeold A, Bianco AC (2008) Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev 29:898–938

    Article  PubMed  CAS  Google Scholar 

  72. Morvan Dubois G, Sebillot A, Kuiper GG, Verhoelst CH, Darras VM, Visser TJ, Demeneix BA (2006) Deiodinase activity is present in Xenopus laevis during early embryogenesis. Endocrinology 147:4941–4949

    Article  PubMed  CAS  Google Scholar 

  73. St Germain DL, Schwartzman RA, Croteau W, Kanamori A, Wang Z, Brown DD, Galton VA (1994) A thyroid hormone-regulated gene in Xenopus laevis encodes a type III iodothyronine 5-deiodinase. Proc Natl Acad Sci USA 91:7767–7771

    Article  PubMed  CAS  Google Scholar 

  74. Cai L, Brown DD (2004) Expression of type II iodothyronine deiodinase marks the time that a tissue responds to thyroid hormone-induced metamorphosis in Xenopus laevis. Dev Biol 266:87–95

    Article  PubMed  CAS  Google Scholar 

  75. Huang H, Marsh-Armstrong N, Brown DD (1999) Metamorphosis is inhibited in transgenic Xenopus laevis tadpoles that overexpress type III deiodinase. Proc Natl Acad Sci USA 96:962–967

    Article  PubMed  CAS  Google Scholar 

  76. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM (1995) The nuclear receptor superfamily: the second decade. Cell 83:835–839

    Article  PubMed  CAS  Google Scholar 

  77. Buchholz DR, Tomita A, Fu L, Paul BD, Shi Y-B (2004) Transgenic analysis reveals that thyroid hormone receptor is sufficient to mediate the thyroid hormone signal in frog metamorphosis. Mol Cell Biol 24:9026–9037

    Article  PubMed  CAS  Google Scholar 

  78. Buchholz DR, Hsia SC, Fu L, Shi Y-B (2003) A dominant-negative thyroid hormone receptor blocks amphibian metamorphosis by retaining corepressors at target genes. Mol Cell Biol 23:6750–6758

    Article  PubMed  CAS  Google Scholar 

  79. Schreiber AM, Brown DD (2003) Tadpole skin dies autonomously in response to thyroid hormone at metamorphosis. Proc Natl Acad Sci USA 100:1769–1774

    Article  PubMed  CAS  Google Scholar 

  80. Schreiber AM, Das B, Huang H, Marsh-Armstrong N, Brown DD (2001) Diverse developmental programs of Xenopus laevis metamorphosis are inhibited by a dominant negative thyroid hormone receptor. Proc Natl Acad Sci USA 98:10739–10744

    Article  PubMed  CAS  Google Scholar 

  81. Yaoita Y, Shi Y-B, Brown DD (1990) Xenopus laevis α and β thyroid hormone receptors. Proc Natl Acad Sci USA 87:7090–7094

    Article  PubMed  CAS  Google Scholar 

  82. Yaoita Y, Brown DD (1990) A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis. Genes Dev 4:1917–1924

    Article  PubMed  CAS  Google Scholar 

  83. Berry DL, Rose CS, Remo BF, Brown DD (1998) The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs. Dev Biol 203:24–35

    Article  PubMed  CAS  Google Scholar 

  84. Kawahara A, Baker BS, Tata JR (1991) Developmental and regional expression of thyroid hormone receptor genes during Xenopus metamorphosis. Development 112:933–943

    PubMed  CAS  Google Scholar 

  85. Kanamori A, Brown DD (1992) The regulation of thyroid hormone receptor β genes by thyroid hormone in Xenopus laevis. J Biol Chem 267:739–745

    PubMed  CAS  Google Scholar 

  86. Furlow JD, Yang HY, Hsu M, Lim W, Ermio DJ, Chiellini G, Scanlan TS (2004) Induction of larval tissue resorption in Xenopus laevis tadpoles by the thyroid hormone receptor agonist GC-1. J Biol Chem 279:26555–26562

    Article  PubMed  CAS  Google Scholar 

  87. Amano T, Yoshizato K (1998) Isolation of genes involved in intestinal remodeling during anuran metamorphosis. Wound Repair Regen 6:302–313

    Article  PubMed  CAS  Google Scholar 

  88. Buckbinder L, Brown DD (1992) Thyroid hormone-induced gene expression changes in the developing frog limb. J Biol Chem 267:25786–25791

    PubMed  CAS  Google Scholar 

  89. Denver RJ, Pavgi S, Shi Y-B (1997) Thyroid hormone-dependent gene expression program for Xenopus neural development. J Biol Chem 272:8179–8188

    Article  PubMed  CAS  Google Scholar 

  90. Helbing CC, Werry K, Crump D, Domanski D, Veldhoen N, Bailey CM (2003) Expression profiles of novel thyroid hormone-responsive genes and proteins in the tail of Xenopus laevis tadpoles undergoing precocious metamorphosis. Mol Endocrinol 17:1395–1409

    Article  PubMed  CAS  Google Scholar 

  91. Sachs LM, Le Mevel S, Demeneix BA (2004) Implication of bax in Xenopus laevis tail regression at metamorphosis. Dev Dyn 231:671–682

    Article  PubMed  CAS  Google Scholar 

  92. Cruz-Reyes J, Tata JR (1995) Cloning, characterization and expression of two Xenopus bcl-2-like cell-survival genes. Gene 158:171–179

    Article  PubMed  CAS  Google Scholar 

  93. Coen L, du Pasquier D, Le Mevel S, Brown S, Tata J, Mazabraud A, Demeneix BA (2001) Xenopus Bcl-X(L) selectively protects Rohon-Beard neurons from metamorphic degeneration. Proc Natl Acad Sci USA 98:7869–7874

    Article  PubMed  CAS  Google Scholar 

  94. Du Pasquier D, Rincheval V, Sinzelle L, Chesneau A, Ballagny C, Sachs LM, Demeneix B, Mazabraud A (2006) Developmental cell death during Xenopus metamorphosis involves BID cleavage and caspase 2 and 8 activation. Dev Dyn 235:2083–2094

    Article  PubMed  CAS  Google Scholar 

  95. Wang K, Yin XM, Chao DT, Milliman CL, Korsmeyer SJ (1996) BID: a novel BH3 domain-only death agonist. Genes Dev 10:2859–2869

    Article  PubMed  CAS  Google Scholar 

  96. van Loo G, Saelens X, van Gurp M, MacFarlane M, Martin SJ, Vandenabeele P (2002) The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ 9:1031–1042

    Article  PubMed  CAS  Google Scholar 

  97. Montesanti A, Deignan K, Hensey C (2007) Cloning and characterization of Xenopus laevis Smac/DIABLO. Gene 392:187–195

    Article  PubMed  CAS  Google Scholar 

  98. Nakajima K, Takahashi A, Yaoita Y (2000) Structure, expression, and function of the Xenopus laevis caspase family. J Biol Chem 275:10484–10491

    Article  PubMed  CAS  Google Scholar 

  99. Yaoita Y, Nakajima K (1997) Induction of apoptosis and CPP32 expression by thyroid hormone in a myoblastic cell line derived from tadpole tail. J Biol Chem 272:5122–5127

    Article  PubMed  CAS  Google Scholar 

  100. Esposti MD (2002) The roles of Bid. Apoptosis 7:433–440

    Article  PubMed  CAS  Google Scholar 

  101. Wagner MJ, Gogela-Spehar M, Skirrow RC, Johnston RN, Riabowol K, Helbing CC (2001) Expression of novel ING variants is regulated by thyroid hormone in the Xenopus laevis tadpole. J Biol Chem 276:47013–47020

    Article  PubMed  CAS  Google Scholar 

  102. Greenwood J, Gautier J (2007) XLX is an IAP family member regulated by phosphorylation during meiosis. Cell Death Differ 14:559–567

    Article  PubMed  CAS  Google Scholar 

  103. Tsuchiya Y, Murai S, Yamashita S (2005) Apoptosis-inhibiting activities of BIR family proteins in Xenopus egg extracts. FEBS J 272:2237–2250

    Article  PubMed  CAS  Google Scholar 

  104. Hutson LD, Bothwell M (2001) Expression and function of Xenopus laevis p75(NTR) suggest evolution of developmental regulatory mechanisms. J Neurobiol 49:79–98

    Article  PubMed  CAS  Google Scholar 

  105. Mangurian C, Johnson RO, McMahan R, Clothier RH, Ruben LN (1998) Expression of a Fas-like proapoptotic molecule on the lymphocytes of Xenopus laevis. Immunol Lett 64:31–38

    Article  PubMed  CAS  Google Scholar 

  106. Mawaribuchi S, Tamura K, Okano S, Takayama S, Yaoita Y, Shiba T, Takamatsu N, Ito M (2008) Tumor necrosis factor-α attenuates thyroid hormone-induced apoptosis in vascular endothelial cell line XLgoo established from Xenopus tadpole tails. Endocrinology 149:3379–3389

    Article  PubMed  CAS  Google Scholar 

  107. Tamura K, Noyama T, Ishizawa YH, Takamatsu N, Shiba T, Ito M (2004) Xenopus death receptor-M1 and -M2, new members of the tumor necrosis factor receptor superfamily, trigger apoptotic signaling by differential mechanisms. J Biol Chem 279:7629–7635

    Article  PubMed  CAS  Google Scholar 

  108. Domanski D, Helbing CC (2007) Analysis of the Rana catesbeiana tadpole tail fin proteome and phosphoproteome during T3-induced apoptosis: identification of a novel type I keratin. BMC Dev Biol 7:94

    Article  PubMed  CAS  Google Scholar 

  109. Skirrow RC, Helbing CC (2007) Decreased cyclin-dependent kinase activity promotes thyroid hormone-dependent tail regression in Rana catesbeiana. Cell Tissue Res 328:281–289

    Article  PubMed  CAS  Google Scholar 

  110. Ji L, Domanski D, Skirrow RC, Helbing CC (2007) Genistein prevents thyroid hormone-dependent tail regression of Rana catesbeiana tadpoles by targeting protein kinase C and thyroid hormone receptor α. Dev Dyn 236:777–790

    Article  PubMed  CAS  Google Scholar 

  111. Skirrow RC, Veldhoen N, Domanski D, Helbing CC (2008) Roscovitine inhibits thyroid hormone-induced tail regression of the frog tadpole and reveals a role for cyclin C/Cdk8 in the establishment of the metamorphic gene expression program. Dev Dyn 237:3787–3797

    Article  PubMed  CAS  Google Scholar 

  112. Marshall JA, Dixon KE (1978) Cell proliferation in the intestinal epithelium of Xenopus laevis tadpoles. J Exp Zool 203:31–40

    Article  Google Scholar 

  113. Ishizuya-Oka A, Shimozawa A (1987) Ultrastructural changes in the intestinal connective tissue of Xenopus laevis during metamorphosis. J Morphol 193:13–22

    Article  PubMed  CAS  Google Scholar 

  114. Su Y, Shi Y, Stolow MA, Shi Y-B (1997) Thyroid hormone induces apoptosis in primary cell cultures of tadpole intestine: cell type specificity and effects of extracellular matrix. J Cell Biol 139:1533–1543

    Article  PubMed  CAS  Google Scholar 

  115. Halestrap AP (2009) Mitochondria and reperfusion injury of the heart—a holey death but not beyond salvation. J Bioenerg Biomembr 41:113–121

    Article  PubMed  CAS  Google Scholar 

  116. Su Y, Shi Y, Shi Y-B (1997) Cyclosporin A but not FK506 inhibits thyroid hormone-induced apoptosis in tadpole intestinal epithelium. FASEB J 11:559–565

    PubMed  CAS  Google Scholar 

  117. Hanada H, Katsu K, Kanno T, Sato EF, Kashiwagi A, Sasaki J, Inoue M, Utsumi K (2003) Cyclosporin A inhibits thyroid hormone-induced shortening of the tadpole tail through membrane permeability transition. Comp Biochem Physiol B Biochem Mol Biol 135:473–483

    Article  PubMed  CAS  Google Scholar 

  118. Shi Y-B, Ishizuya-Oka A (1997) Autoactivation of Xenopus thyroid hormone receptor b genes correlates with larval epithelial apoptosis and adult cell proliferation. J Biomed Sci 4:9–18

    Article  PubMed  CAS  Google Scholar 

  119. Patterton D, Hayes WP, Shi Y-B (1995) Transcriptional activation of the matrix metalloproteinase gene stromelysin-3 coincides with thyroid hormone-induced cell death during frog metamorphosis. Dev Biol 167:252–262

    Article  PubMed  CAS  Google Scholar 

  120. Stolow MA, Bauzon DD, Li J, Sedgwick T, Liang VC, Sang QA, Shi Y-B (1996) Identification and characterization of a novel collagenase in Xenopus laevis: possible roles during frog development. Mol Biol Cell 7:1471–1483

    PubMed  CAS  Google Scholar 

  121. Hasebe T, Hartman R, Matsuda H, Shi Y-B (2006) Spatial and temporal expression profiles suggest the involvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis. Cell Tissue Res 324:105–116

    Article  PubMed  CAS  Google Scholar 

  122. Shi Y-B, Ishizuya-Oka A (2001) Thyroid hormone regulation of apoptotic tissue remodeling: implications from molecular analysis of amphibian metamorphosis. Prog Nucleic Acid Res Mol Biol 65:53–100

    Article  PubMed  CAS  Google Scholar 

  123. Fu L, Tomita A, Wang H, Buchholz DR, Shi Y-B (2006) Transcriptional regulation of the Xenopus laevis Stromelysin-3 gene by thyroid hormone is mediated by a DNA element in the first intron. J Biol Chem 281:16870–16878

    Article  PubMed  CAS  Google Scholar 

  124. Basset P, Bellocq JP, Wolf C, Stoll I, Hutin P, Limacher JM, Podhajcer OL, Chenard MP, Rio MC, Chambon P (1990) A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas. Nature 348:699–704

    Article  PubMed  CAS  Google Scholar 

  125. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2:161–174

    Article  PubMed  CAS  Google Scholar 

  126. Lefebvre O, Wolf C, Limacher JM, Hutin P, Wendling C, LeMeur M, Basset P, Rio MC (1992) The breast cancer-associated stromelysin-3 gene is expressed during mouse mammary gland apoptosis. J Cell Biol 119:997–1002

    Article  PubMed  CAS  Google Scholar 

  127. Pei D, Weiss SJ (1995) Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 375:244–247

    Article  PubMed  CAS  Google Scholar 

  128. Ishizuya-Oka A, Li Q, Amano T, Damjanovski S, Ueda S, Shi Y-B (2000) Requirement for matrix metalloproteinase stromelysin-3 in cell migration and apoptosis during tissue remodeling in Xenopus laevis. J Cell Biol 150:1177–1188

    Article  PubMed  CAS  Google Scholar 

  129. Fu L, Hasebe T, Ishizuya-Oka A, Shi Y-B (2007) Roles of matrix metalloproteinases and ECM remodeling during thyroid hormone-dependent intestinal metamorphosis in Xenopus laevis. Organogenesis 3:14–19

    Article  PubMed  Google Scholar 

  130. Fu L, Ishizuya-Oka A, Buchholz DR, Amano T, Matsuda H, Shi Y-B (2005) A causative role of stromelysin-3 in extracellular matrix remodeling and epithelial apoptosis during intestinal metamorphosis in Xenopus laevis. J Biol Chem 280:27856–27865

    Article  PubMed  CAS  Google Scholar 

  131. Amano T, Fu L, Marshak A, Kwak O, Shi Y-B (2005) Spatio-temporal regulation and cleavage by matrix metalloproteinase stromelysin-3 implicate a role for laminin receptor in intestinal remodeling during Xenopus laevis metamorphosis. Dev Dyn 234:190–200

    Article  PubMed  CAS  Google Scholar 

  132. Amano T, Kwak O, Fu L, Marshak A, Shi Y-B (2005) The matrix metalloproteinase stromelysin-3 cleaves laminin receptor at two distinct sites between the transmembrane domain and laminin binding sequence within the extracellular domain. Cell Res 15:150–159

    Article  PubMed  CAS  Google Scholar 

  133. Fiorentino M, Fu L, Shi Y-B (2009) Mutational analysis of the cleavage of the cancer-associated laminin receptor by stromelysin-3 reveals the contribution of flanking sequences to site recognition and cleavage efficiency. Int J Mol Med 23:389–397

    PubMed  CAS  Google Scholar 

  134. Fujimoto K, Nakajima K, Yaoita Y (2006) One of the duplicated matrix metalloproteinase-9 genes is expressed in regressing tail during anuran metamorphosis. Dev Growth Differ 48:223–241

    Article  PubMed  CAS  Google Scholar 

  135. 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. Dev Dyn 236:2338–2345

    Article  PubMed  CAS  Google Scholar 

  136. Morodomi T, Ogata Y, Sasaguri Y, Morimatsu M, Nagase H (1992) Purification and characterization of matrix metalloproteinase 9 from U937 monocytic leukaemia and HT1080 fibrosarcoma cells. Biochem J 285:603–611

    PubMed  CAS  Google Scholar 

  137. Du Pasquier L, Flajnik MF (1990) Expression of MHC class II antigens during Xenopus development. Dev Immunol 1:85–95

    Article  PubMed  CAS  Google Scholar 

  138. Flajnik MF, Hsu E, Kaufman JF, Du Pasquier D (1987) Changes in the immune system during metamorphosis of Xenopus. Immunol Today 8:58–64

    Article  Google Scholar 

  139. Marshall JA, Dixon KE (1978) Cell specialization in the epithelium of the small intestine of feeding Xenopus laevis tadpoles. J Anat 126:133–144

    PubMed  CAS  Google Scholar 

  140. McAvoy JW, Dixon KE (1978) Cell specialization in the small intestinal epithelium of adult Xenopus laevis: structural aspects. J Anat 125:155–169

    PubMed  CAS  Google Scholar 

  141. Mukaigasa K, Hanasaki A, Maeno M, Fujii H, Hayashida SI, Itoh M, Kobayashi M, Tochinai S, Hatta M, Iwabuchi K, Taira M, Onoe K, Izutsu Y (2009) The keratin-related Ouroboros proteins function as immune antigens mediating tail regression in Xenopus metamorphosis. Proc Natl Acad Sci USA (in press)

  142. Tata JR (1994) Hormonal regulation of programmed cell death during amphibian metamorphosis. Biochem Cell Biol 72:581–588

    Article  PubMed  CAS  Google Scholar 

  143. Ikuzawa M, Shimizu K, Yasumasu S, Iuchi I, Shi Y-B, Ishizuya-Oka A (2006) Thyroid hormone-induced expression of a bZip-containing transcription factor activates epithelial cell proliferation during Xenopus larval-to-adult intestinal remodeling. Dev Genes Evol 216:109–118

    Article  PubMed  CAS  Google Scholar 

  144. Ishizuya-Oka A, Hasebe T, Buchholz DR, Kajita M, Fu L, Shi Y-B (2009) Origin of the adult intestinal stem cells induced by thyroid hormone in Xenopus laevis. FASEB J 23:2568–2575

    Article  PubMed  CAS  Google Scholar 

  145. Amano T, Noro N, Kawabata H, Kobayashi Y, Yoshizato K (1998) Metamorphosis-associated and region-specific expression of calbindin gene in the posterior intestinal epithelium of Xenopus laevis larva. Dev Growth Differ 40:177–188

    Article  PubMed  CAS  Google Scholar 

  146. Schreiber AM, Cai L, Brown DD (2005) Remodeling of the intestine during metamorphosis of Xenopus laevis. Proc Natl Acad Sci USA 102:3720–3725

    Article  PubMed  CAS  Google Scholar 

  147. Hodin RA, Meng S, Chamberlain SM (1994) Thyroid hormone responsiveness is developmentally regulated in the rat small intestine: a possible role for the α-2 receptor variant. Endocrinology 135:564–568

    Article  PubMed  CAS  Google Scholar 

  148. Kress E, Rezza A, Nadjar J, Samarut J, Plateroti M (2008) The thyroid hormone receptor-α (TRα) gene encoding TRα1 controls deoxyribonucleic acid damage-induced tissue repair. Mol Endocrinol 22:47–55

    Article  PubMed  CAS  Google Scholar 

  149. Ishizuya-Oka A, Shi Y-B (2008) Thyroid hormone regulation of stem cell development during intestinal remodeling. Mol Cell Endocrinol 288:71–78

    Article  PubMed  CAS  Google Scholar 

  150. Plateroti M, Kress E, Mori JI, Samarut J (2006) Thyroid hormone receptor α1 directly controls transcription of the β-catenin gene in intestinal epithelial cells. Mol Cell Biol 26:3204–3214

    Article  PubMed  CAS  Google Scholar 

  151. Qi JS, Yuan Y, Desai-Yajnik V, Samuels HH (1999) Regulation of the mdm2 oncogene by thyroid hormone receptor. Mol Cell Biol 19:864–872

    PubMed  CAS  Google Scholar 

  152. Rankin SA, Hasebe T, Zorn AM, Buchholz DR (2009) Improved cre reporter transgenic Xenopus. Dev Dyn 238:2401–2408

    Article  PubMed  Google Scholar 

  153. Leloup J, Buscaglia M (1977) Triiodothyronine, hormone of amphibian metamorphosis. C R Hebd Seances Acad Sci 284:2261–2263

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the JSPS Grants-in-Aid for Scientific Research (C) (Grant number 20570060 to A. I.-O.) and in part by the Intramural Research Program of NICHD, NIH.

Author information

Authors and Affiliations

  1. Department of Biology, Nippon Medical School, Kawasaki, Kanagawa, 211-0063, Japan

    Atsuko Ishizuya-Oka & Takashi Hasebe

  2. Laboratory of Gene Regulation and Development, National Institute for Child Health and Human Development, NIH, Bethesda, MD, 20892-5431, USA

    Yun-Bo Shi

Authors
  1. Atsuko Ishizuya-Oka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Hasebe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yun-Bo Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Atsuko Ishizuya-Oka or Yun-Bo Shi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishizuya-Oka, A., Hasebe, T. & Shi, YB. Apoptosis in amphibian organs during metamorphosis. Apoptosis 15, 350–364 (2010). https://doi.org/10.1007/s10495-009-0422-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-009-0422-y

Keywords

Search

Navigation