Tail regression induced by elevated retinoic acid signaling in amphioxus larvae occurs by tissue remodeling, not cell death

Evolution and Development

Volumn 13, Issue 5, 2011, Pages 427-435

  Koop, Demian ^a   Holland, Linda Z ^a   Setiamarga, Davin ^a   Schubert, Michael ^b   Hollanda, Nicholas D ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; RETINOIC ACID;

APOPTOSIS; CYPRINID; CYTOLOGY; CYTOPLASM; LARVA; ORGANIC ACID; PROTEIN; REGRESSION ANALYSIS; SIGNALING; VITAMIN;

ANAL CANAL; ANIMAL; APOPTOSIS; ARTICLE; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INVERTEBRATE CHORDATA; LARVA; METABOLISM; PHYLOGENY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TAIL; ULTRASTRUCTURE;

ANAL CANAL; ANIMALS; APOPTOSIS; CHORDATA, NONVERTEBRATE; CYTOSKELETAL PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION; LARVA; PHYLOGENY; SIGNAL TRANSDUCTION; TAIL; TRETINOIN;

BRANCHIOSTOMA; BRANCHIOSTOMA LANCEOLATUM; CHORDATA; DANIO RERIO; INVERTEBRATA; MAMMALIA;

EID: 80055026700     PISSN: 1520541X     EISSN: 1525142X     Source Type: Journal    
DOI: 10.1111/j.1525-142X.2011.00501.x     Document Type: Article

References (57)

1. Abascal, F., Zardoya, R., and Posada, D. 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104-2105.
2. Bahe, S., Stierhof, Y. D., Wilkinson, C. J., Leiss, F., and Nigg, E. A. 2005. Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J. Cell Biol. 171: 27-33.
3. Balmer, J. E., and Blomhoff, R. 2005. A robust characterization of retinoic acid response elements based on a comparison of sites in three species. J. Steroid Biochem. Mol. Biol. 96: 347-354.
4. Bayascas, J. R., Yuste, V. J., Benito, E., Garcia-Fern'andez, J., and Comella, J. X. 2002. Isolation of AmphiCASP-3/7, an ancestral caspase from amphioxus (Branchiostoma floridae); evolutionary considerations for vertebrate caspases. Cell Death Differ. 9: 1078-1089.
5. Burge, C., and Karlin, S. 1997. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268: 78-94.
6. Campo-Paysaa, F., Marlétaz, F., Laudet, V., and Schubert, M. 2008. Retinoic acid signaling in development: tissue-specific functions and evolutionary origins. Genesis 46: 640-656.
7. Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17: 540-552.
8. Chan, B. W., et al. 2001. Maternal diabetes increases the risk of caudal regression caused by retinoic acid. Diabetes 51: 2811-2816.
9. Collins, M. D. 1999. Teratology of retinoids. Ann. Rev. Pharmacol. Toxicol. 39: 399-430.
10. Dalf́ o, D., Albalat, R., Molotkov, A., Deuster, G., and Gonz'alez-Duarte, R. 2002. Retinoic acid synthesis in the prevertebrate amphioxus involves retinal oxidation. Dev. Genes Evol. 212: 388-393.
11. De Luca, L. M. 1991. Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J. 5: 2924-2933.
12. De Luca, L. M., and Ross, S. A. 1996. Retinoic acid response elements as positive and negative regulators of the expression of the homeobox b-1 gene. Nutr. Rev. 54: 61-63.
13. Duestername, G. 2008. Retinoic acid synthesis and signaling during early organogenesis. Cell 134: 921-931.
14. Emoto, Y., Wada, H., Okamoto, H., Kudo, A., and Imai, Y. 2005. Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev. Biol. 278: 415-427.
15. Escriva, H., Holland, N. D., Groenmeyer, H., Laudet, V., and Holland, L. Z. 2002. The retinoic acid signaling pathway regulates anterior/posterior patterning in the nerve cord and pharynx of amphioxus, a chordate lacking neural crest. Development 129: 2905-2916.
16. Evans, T. 2005. Regulation of hematopoiesis by retinoid signaling. Exp. Hematol. 33: 1055-1061.
17. Fawcett, D. W., and Porter, K. R. 1954. A study of the fine structure of ciliated epithelia. J. Morphol. 94: 221-282.
18. Firat, D., Kuntsal, L., and Sirin, Y. 2005. Protective effects of prenatal administration of folic acid on retinoic acid-induced cellular damages of Meckel's cartilages in rats. Tohoku J. Exp. Med. 205: 27-36.
19. Flood, P. R. 1975. Ciliary rootlet-fibres as tail fin-rays in larval amphioxus (Branchiostoma lanceolatum, Pallas). J. Ultrastruct. Res. 51: 218-225.
20. Fukami, M., et al. 2010. Anorectal and urinary anomalies and aberrant retinoic acid metabolism in cytochrome P450 oxidoreductase deficiency. Mol. Genet. Metab. 100: 269-73.
21. Holland, L. Z., and Holland, N. D. 1996. Expression of AmphiHox-1 and AmphiPax-1 in amphioxus embryos treated with retinoic acid: insights into evolution and patterning of the chordate nerve cord and pharynx. Development 122: 1829-1838.
22. Holland,N.D., Paris,M., andKoop,D. 2009. The club-shaped gland of amphioxus: export of secretion to the pharynx in pre-metamorphic larvae and apoptosis during metamorphosis. Acta Zool. Stockh. 90: 372-379.
23. Honein, M. Z., Paulozzi, L. J., and Erikson, J. D. 2001. Continued occurrence of AccutaneR _ -exposed pregnancies. Teratology 64: 399-430.
24. Jiang, Z., et al. 2008. Exdpf is a key regulator of exocrine pancreas development controlled by retinoic acid and ptf1a in zebrafish. PLoS Biol. 6: e293.
25. Karperien,M., et al. 1999. Identification of a retinoic acid-inducible element in themurine PTH/PTHrP (parathyroid hormone/parathyroid hormone-related peptide) receptor gene. Mol. Endocrinol. 13: 1183-1196.
26. Katoh, K., Kuma, K., Toh, H., and Miyata, T. 2005. MAFFT version 5: improvement inaccuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511-518.
27. Katoh, K., and Toh, H. 2008. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFTbased framework. BMC Bioinformatics 9: 212.
28. Kelley, M.W., Turner, J. K., andReh, T. A. 1994.Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120: 2091-2102.
29. Koop, D., et al. 2010. Retinoic acid signaling targets Hox genes during the amphioxus gastrula stage: insights into early anteriorposterior patterning of the chordate body plan. Dev. Biol. 338: 98-106.
30. Mainguy, G., In der Rieden, P. M., Berezikov, E., Woltering, J. M., Plasterk, R. H., and Durston, A. H. 2003. A position-dependent organization of retinoid response elements is conserved in the vertebrate Hox clusters. Trends Genet. 19: 476-479.
31. Marlétaz,F., Holland, L. Z.,Laudet,V., and Schubert,M. 2006.Retinoic acid signaling and the evolution of chordates. Int. J. Biol. Sci. 2: 38-47.
32. Maŕi{dotless}-Beffa, M., and Murciano,C. 2010. Dermoskeleton morphogenesis in zebrafish fins. Dev. Dyn. 239: 2779-2794.
33. Martin, B. L., and Kimelman, D. 2010. Brachyury establishes the embryonic mesodermal progenitor niche. Genes Dev. 24: 2778-2783.
34. Nakata, M., et al. 2009. Induction of Wnt5a-expressing mesenchymal cells adjacent to the cloacal plate is an essential process for its proximodistal elongation and subsequent anorectal development. Pediatr. Res. 66: 149-154.
35. Padmanabhan, R. 1998. Retinoic acid-induced caudal regression syndrome in the mouse fetus. Reprod. Toxicol. 12: 139-151.
36. Perlmann, T., Rangarajan, P. N., Umesono, K., and Evans, R.M. 1993. Determinants for selective RAR and TR recognition of direct repeat HREs. Genes Dev. 7: 1411-1422.
37. Pitera, J. E., Smith, W., Woolf, A. S., and Milla, P. J. 2001. Embryonic gut anomalies in a mouse model of retinoic acid-induced caudal regression syndrome-delayed gut looping, rudimentary caecum, and anorectal anomalies. Am. J. Pathol. 159: 2321-2329.
38. Putnam, N. H., et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064-1071.
39. Ramalho-Santos,M., Melton,D. A., and McMahon, A. P. 2000. Hedgehog signals regulatemultiple aspects of gastrointestinal development. Development. 127: 2763-2772.
40. Sasaki, Y., Iwai, N., Tsuda, T., and Kimura, O. 2004. Sonic hedgehog and bone morphogenetic protein 4 expression in the hindgut region ofmurine embryos with anorectal malformations. J. Pediatr. Surg. 39: 170-173.
41. Schubert, M., Holland,N.D.,Escriva,H., Holland, L. Z., and Laudet,V. 2004. Retinoic acid influences anteroposterior positioning of epidermal sensory neurons and their gene expression in a developing chordate (amphioxus). Proc. Natl. Acad. Sci. U.S.A. 101: 10320-10325.
42. Schubert, M., Holland, N. D., Laudet, V., and Holland, L. Z. 2006. A retinoic acid-Hox hierarchy controls both anterior/posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus. Dev. Biol. 296: 190-202.
43. Schubert, M., Yu, J. K., Holland, N. D., Escriva, H., Laudet, V., and Holland, L. Z. 2005. Retinoic acid signaling acts via Hox1 to establish the posterior limit of the pharynx in the chordate amphioxus. Development 132: 61-73.
44. Sessions, R. P., Lloyd, R. A, Sulik, K. K., and Mesrobian, H. G. J. 1993. Imperforate anus induced by etretinate in mice. Teratology 47: 435A.
45. Sive, H. L., Draper, B. W., Harland, R. M., and Weintraub, H. 1990. Identification of a retinoic acid-sensitive period during primary axis formation in Xenopus laevis. Genes Dev. 4: 932-942.
46. Stamatakis, A., Hoover, P., andRougemont, J. 2008.ARapid Bootstrap Algorithm for the RAxML Web-Servers. Syst. Biol. 75: 758-771.
47. Suzuki, K., Economides, A., Yanagita, M., Graf, D., and Yamada, G. 2009. New horizons at the caudal embryos: coordinated urogenital/reproductive organ formation by growth factor signaling. Curr. Opin. Gen. Dev. 19: 491-496.
48. Theodosiou, M., Laudet, V., and Schubert, M. 2010. From carrot to clinic: an overview of the retinoic acid signaling pathway. Cell. Mol. Life Sci. 67: 1423-1445.
49. Varani, J., Gibbs, D. F., Inman, D. R., Shah, B., Fligiel, S. E. G., and Voorhees, J. J. 1991. Inhibition of epithelial cell adhesion by retinoic acid. Am. J. Pathol. 138: 887-895.
50. Wada, H., Escriva, H., Zhang, S., and Laudet, V. 2006. Conserved RARE localization in amphioxus Hox clusters and implications for Hox code evolution in the vertebrate neural crest. Dev. Dyn. 235: 1522-1531.
51. Yang, J., et al. 2005. The ciliary rootlet maintains long-term stability of sensory cilia. Mol. Cell. Biol. 25: 4129-4137.
52. Yang, J., and Li, T. S. 2006. Focus on molecules: Rootletin. Exp. Eye Res. 83: 1-2.
53. Yang, J., Liu,X.Q.,Yue,G. H.,Adamian, M., Bulgakov,O., and Li, T. S. 2002. Rootletin, a novel coiled-coil protein, is a structural component of the ciliary rootlet. J. Cell Biol. 159: 431-440.
54. Yelon, D., and Stainier, D. Y. R. 2002. Pattern formation: swimming in retinoic acid. Curr. Biol. 12: R707-R709.
55. Yu, J. K. 2010. The evolutionary origin of the vertebrate neural crest and its developmental gene regulatory network-insights from amphioxus. Zoology 113: 1-9.
56. Yu, J. K., and Holland, L. Z. 2004. Cephalochordate (amphioxus) embryos: procurement, culture, basic methods. Meth. Cell Biol. 74: 195-215.
57. Yu, J. K., et al. 2007. Axial patterning in cephalochordates and the evolution of the organizer. Nature 445: 613-617.