Development Genes and Evolution

, Volume 215, Issue 1, pp 32–40 | Cite as

Anatomical and molecular reinvestigation of lamprey endostyle development provides new insight into thyroid gland evolution

Original Article

Abstract

The thyroid gland of vertebrates is considered to be homologous to the endostyle of non-vertebrate chordates (cephalochordates, urochordates), a key character for understanding the origin and evolution of the chordate body plan. In lampreys, the larval endostyle transforms into an adult thyroid gland during metamorphosis, reflecting evolutionary changes that occurred in the vertebrate lineage. Focussing on thyroid-like cells in the endostyle, we here relate morphologically visible steps of lamprey (Lampetra fluviatilis) endostyle differentiation to embryonic stages and determine the onset of thyroid-like function. Analysing lamprey endostyle development using semi-thin histological sections, immunohistochemical detection of thyroid hormone, and the molecular marker thyroid transcription factor1 (Ttf1) refines our current view of the homology between endostyle and thyroid gland. In contrast to earlier literature, we find that a duct always persists to connect the endostyle lumen to the pharynx, a structure that resembles the thyroglossal duct in thyroid development and could further support the homology between endostyle and thyroid. Before the onset of thyroid-like function, Ttf1 expression becomes restricted to the ventral part of the endostyle, on the one hand showing that dorsal thyroid-like cells produce thyroid hormone in the absence of Ttf1, and on the other suggesting that Ttf1 was initially involved in specifying ventral fates in the endostyle.

Keywords

Endostyle Thyroid Nkx2.1 T4 Cyclostomes 

Notes

Acknowledgements

We thank Julia von Gartzen (Köln) for excellent technical assistance, Ansgar Büschges and coworkers (Köln) for supply with adult lampreys, Arne Nolte (Köln) for invaluable help with lamprey fishing and all our colleagues in Köln and Berlin for helpful comments and support. We are further grateful to Sylvie Mazan and Tatjana Sauka-Spengler (Paris) for helpful hints regarding lamprey in situ hybridisation protocols, John Chandler for critically reading the manuscript and Albrecht Fischer (Mainz) for encouraging this work.

References

  1. Barrington E, Sage M (1972) The endostyle and thyroid. In: Hardisty M, Potter I (eds) The biology of lampreys, vol 2. Academic Press, London, pp 105–134Google Scholar
  2. Dohrn A (1886) Studien zur Urgestalt des Wirbeltierkörpers, 8. Studie: Thyreoidea bei Petromyzon, Amphioxus und Tunicaten. Mitt Zool Stn Neapel 6:49–92Google Scholar
  3. Elsalini OA, von Gartzen J, Cramer M, Rohr KR (2003) Zebrafish hhex, nk2.1a and pax2.1 regulate thyroid growth and differentiation downstream of Nodal-dependent transcription factors. Dev Biol 263:67–80PubMedGoogle Scholar
  4. Fujita H (1972) Electron microscopic autoradiography on the iodine metabolism of the thyroid gland in phylogenetic aspect. Acta Histochim Cytochim 5:205–207Google Scholar
  5. Fujita H, Honma Y (1966) Electron microscopical studies on the thyroid of a cyclostome, Lampetra japonica, during its upstream migration. Z Zellforsch Mikrosk Anat 73:559–575PubMedGoogle Scholar
  6. Fujita H, Honma Y (1969) Iodine metabolism of the endostyle of larval lampreys, Ammocoetes of Lampetra japonica. Electron microscopic autoradiography of 125-I. Z Zellforsch Mikrosk Anat 98:525–537PubMedGoogle Scholar
  7. Fujita H, Sawano F (1979) Fine structural localization of endogeneous peroxidase in the endostyle of ascidians, Ciona intestinalis. A part of phylogenetic studies of the thyroid gland. Arch Histol Jpn 42:319–326PubMedGoogle Scholar
  8. Gorbman A, Bern HA (1962) Textbook of comparative endocrinology. Wiley, New YorkGoogle Scholar
  9. Hardisty M, Baker B (1982) Endocrinoloy of lampreys. In: Hardisty M, Potter I (eds) Biology of lampreys, vol 4B. Academic Press, London, pp 1–115Google Scholar
  10. Kieckebusch H-H (1928) Beiträge zur Kenntnis des Baues und der Entwicklung der Schilddrüse bei den Neunaugenlarven (Lampetra fluviatilis L. und Lampetra planeri BL.). Z Morphol Oekol Tiere Abt A 11:17–360Google Scholar
  11. Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ (1996) The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10:60–69PubMedGoogle Scholar
  12. Lazzaro D, Price M, de Felice M, Di Lauro R (1991) The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093–1104PubMedGoogle Scholar
  13. Mansouri A, Chowdhury K, Gruss P (1998) Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet 19:87–90PubMedGoogle Scholar
  14. Martinez Barbera JP, Clements M, Thomas P, Rodriguez T, Meloy D, Kioussis D, Beddington RS (2000) The homeobox gene Hex is required in definitive endodermal tissues for normal forebrain, liver and thyroid formation. Development 127:2433–2445PubMedGoogle Scholar
  15. Mascia A, De Felice M, Lipardi C, Gentile R, Cali G, Zannini M, Di Lauro R, Nitsch L (1997) Transfection of TTF-1 gene induces thyroglobulin gene expression in undifferentiated FRT cells. Biochim Biophys Acta 1354:171–181PubMedGoogle Scholar
  16. McCauley DW, Bronner-Fraser M (2002) Conservation of Pax gene expression in ectodermal placodes of the lamprey. Gene 287:129–139PubMedGoogle Scholar
  17. Müller W (1873) Über die Hypobranchialrinne der Tunicaten und deren Vorhandensein bei Amphioxus und den Cyclostomen. Jena Z Med 7:327–332Google Scholar
  18. Ogasawara M (2000) Overlapping expression of amphioxus homologs of the thyroid transcription factor-1 gene and thyroid peroxidase gene in the endostyle: insight into evolution of the thyroid gland. Dev Genes Evol 210:231–242PubMedGoogle Scholar
  19. Ogasawara M, Di Lauro R, Satoh N (1999) Ascidian homologs of mammalian thyroid transcription factor-1 gene are expressed in the endostyle. Zool Sci 16:559–565Google Scholar
  20. Ogasawara M, Shigetani Y, Suzuki S, Kuratani S, Satoh N (2001) Expression of thyroid transcription factor-1 (TTF-1) gene in the ventral forebrain and endostyle of the agnathan vertebrate, Lampetra japonica. Genesis 30:51–58PubMedGoogle Scholar
  21. Piavis G (1971) Embryology. In: Hardisty M, Potter I (eds) The biology of lampreys, vol 1. Academic Press, London, pp 361–399Google Scholar
  22. Raine JC, Leatherland JF (2000) Morphological and functional development of the thyroid tissue in rainbow trout (Oncorhynchus mykiss) embryos. Cell Tissue Res 301:235–244PubMedGoogle Scholar
  23. Raine JC, Takemura A, Leatherland JF (2001) Assessment of thyroid function in adult medaka (Oryzias latipes) and juvenile rainbow trout (Oncorhynchus mykiss) using immunostaining methods. J Exp Zool 290:366–378PubMedGoogle Scholar
  24. Reese A (1902) Structure and development of the thyroid gland in Petromyzon. Proc Acad Nat Sci Philadelphia 54:85–112Google Scholar
  25. Rohr KB, Concha ML (2000) Expression of nk2.1a during early development of the thyroid gland in zebrafish. Mech Dev 95:267–270PubMedGoogle Scholar
  26. Suzuki S, Kondo Y (1973) Thyroidal morphogenesis and biosynthesis of thyroglobulin before and after metamorphasis in the lamprey, Lampetra reissneri. Gen Comp Endocrinol 21:451–460PubMedGoogle Scholar
  27. Tahara Y (1988) Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool Sci 5:109–118Google Scholar
  28. Venkatesh TV, Holland ND, Holland LZ, Su MT, Bodmer R (1999) Sequence and developmental expression of amphioxus AmphiNk2–1: insights into the evolutionary origin of the vertebrate thyroid gland and forebrain. Dev Genes Evol 209:254–259PubMedGoogle Scholar
  29. Wendl T, Lun K, Mione M, Favor J, Brand M, Wilson SW, Rohr KB (2002) pax2.1 is required for the development of thyroid follicles in zebrafish. Development 129:3751–3760PubMedGoogle Scholar
  30. Wright GM, Youson JH (1976) Transformation of the endostyle of the anadromous sea lamprey, Petromyzon marinus L., during metamorphosis. I. Light microscopy and autoradiography with 125I1. Gen Comp Endocrinol 30:243–257PubMedGoogle Scholar
  31. Wright GM, Filosa MF, Youson JH (1978a) Immunocytochemical localization of thyroglobulin in the endostyle of the anadromous sea lamprey, Petromyzon marinus L. Am J Anat 152:263–268PubMedGoogle Scholar
  32. Wright GM, Filosa MF, Youson JH (1978b) Light and electron microscopic immunocytochemical localization of thyroglobulin in the thyroid gland of the anadromous sea lamprey, Petromyzon marinus L., during its upstream migration. Cell Tissue Res 187:473–478PubMedGoogle Scholar
  33. Wright GM, Filosa MF, Youson JH (1980) Immunocytochemical localization of thyroglobulin in the transforming endostyle of anadromous sea lampreys, Petromyzon marinus L., during metamorphosis. Gen Comp Endocrinol 42:187–194PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Bernhard Kluge
    • 1
  • Nathalie Renault
    • 2
  • Klaus B. Rohr
    • 1
  1. 1.Institute for Developmental BiologyUniversity of CologneCologneGermany
  2. 2.Charité University HospitalHumboldt UniversityBerlinGermany

Personalised recommendations