Skip to main content
Log in

Development of Xenopus laevis skin glands producing 5-hydroxytryptamine and caerulein

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The granular glands in Xenopus laevis skin are known to contain large quantities of biogenic amines and bioactive peptides which closely resemble mammalian brain-gut peptides. We studied the development of glands producing 5-hydroxytryptamine (5-HT) and caerulein using immunohistochemistry, HPLC-fluorometric systems and RIA. The immunoreactivities of 5-HT and caerulein were first detected in the spherical gland rudiments in the stratum spongiosum at St. 58 (Nieuwkoop and Faber stage), or at the beginning of metamorphosis. Both immunoreactivities appeared in the same rudiment at the same time. Some of the gland rudiments have a small lumen filled with both immunoreactive materials at St. 58–59. During the rest of the metamorphic period, the glands grow in size, accumulating immunoreactive materials in the lumen. The concentrations of 5-HT and caerulein in the skin of tadpoles were below 1 ng per mg wet tissue at St. 58–59, increased as metamorphosis proceeded and reached 63 and 134 ng per mg wet tissue at St. 66, or at the end of metamorphosis, respectively. The amphibian granular glands where large quantities of biogenic amines and hormone-like peptides are rapidly synthesized may provide a useful model for the study of the development of amine- and peptide-producing cells including neurons and paraneurons.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anastasi A, Erspamer V, Endeam R (1968) Isolation and amino acid sequence of caerulein, the active decapeptide of the skin of Hyla caerulea. Arch Biochem Biophys 125:57–68

    Google Scholar 

  • Anastasi A, Bertaccini G, Cei JM, De Caro G, Erspamer V, Impicciatore M, Roseghini M (1970) Presence of caerulein in extracts of the skin of Leptodactylus pentadactylus labryinthicus and Xenopus laevis. Br J Pharmacol 38:221–228

    Google Scholar 

  • Andreu D, Ashauer H, Kreil G, Merrifield RB (1985) Solidphase synthesis of PYL and isolation of its natural counterpart, PGLa (PYLa-(4–24)) from skin secretion of Xenopus laevis. Eur J Biochem 149:531–535

    Google Scholar 

  • Araki K, Tachibana S, Uchiyama T, Nakajima T, Yasuhara T (1973) Isolation and structure of a new active peptide “Xenopsin” on the smooth muscle, especially on a strip of fundus from rat stomach, from the skin of Xenopus laevis. Chem Pharmacol Bull 21:281–284

    Google Scholar 

  • Bennett GW, Ball M, Clothier RH, Marsden CA (1981) Location and release of TRH and 5-HT from amphibian skin. Cell Biol Int Rep 5:151–158

    Google Scholar 

  • Bovbjerg AM (1963) Development of the glands of the dermal plicae in Rana pipiens. J Morphol 113:231–243

    Google Scholar 

  • Carraway R, Ruane SE, Feurle GE, Taylor S (1982) Amphibian neurotensin (NT) is not Xenopsin (XP): Dual presence of NT-like and XP-like peptides in various amphibia. Endocrinology 110:1094–1101

    Google Scholar 

  • Delfino G, Brizzi R, Calloni C (1985) Dermo-epithelial interactions during the development of cutaneous gland anlagen in amphibia: A light and electron microscope study on several species with some cytochemical findings. Z Mikrosk Anat Forsch, Leipzig 99:225–253

    Google Scholar 

  • Delfino G, Brizzi R, Calloni C (1982) Development of cutaneous glands in Salamandrina terdigitata (Lacepede, 1788) (amphibia: Urodela); Findings by light and electron microscopy. Z Mikrosk Anat Forsch, Leipzig 96:948–971

    Google Scholar 

  • Dimaline R (1983) Is caerulein amphibian CCK? Peptides 4:457–462

    Google Scholar 

  • Dockray GJ, Hopkins CR (1975) Caerulein secretion by dermal glands in Xenopus laevis. J Cell Biol 64:724–733

    Google Scholar 

  • Dodd MHI, Dodd JM (1976) The biology of metamorphosis. In: Lofts BA (ed) Physiology of the Amphibia. Academic Press, New York, pp 467–599

    Google Scholar 

  • Erspamer V (1983) Amphibian skin peptides in mammals-looking ahead. Trends Neuro Sci 6:200–201

    Google Scholar 

  • Flucher BE, Lenglachner-Bachinger C, Pohlhammer K, Adam H, Mollay C (1986) Skin peptides in Xenopus laevis: Morphological requirements for precursor processing in developing and regeneration granular skin gland. J Cell Biol 103:2299–2309

    Google Scholar 

  • Fujita T (1983) Messenger substances of neurons and paraneurons: The chemical nature and the routes and ranges of their transport to targets. Biomed Res 4:239–256

    Google Scholar 

  • Hoffmann W, Bach TC, Seliger H, Kreil G (1983) Biosynthesis of caerulein in the skin of Xenopus laevis: partial sequences of precursors as deduced from cDNA clones. EMBO J 2:111–114

    Google Scholar 

  • Hökfelt T, Millhorn D, Seroogy K, Tsuruo Y, Ceccatelli S, Lindh B, Meister B, Melander T, Schalling M, Bartfai T, Terenius L (1987) Coexistence of peptides with classical neurotransmitters. Experientia 43:768–780

    PubMed  Google Scholar 

  • Iguchi K, Yanaihara C, Kubota M, Iwanaga T, Fujita T, Matsuo Y, Miyoshi A, Yanaihara N (1983) Porcine cholecystokinin-33 amino-terminal specific radioimmunoassay developed with synthetic porcine cholecystokinin-33 amino-terminal heptacosapeptide. Biomed Res 4 [Suppl] 189–196

    Google Scholar 

  • Inselvini M (1975) First appearance of caerulein during the development of Xenopus laevis. Gen Pharmacol 6:215–217

    Google Scholar 

  • King J, Millar RP (1981) TRH, GH-RIH and LH-RH in Metamorphosing Xenopus laevis. Gen Comp Endocrinol 44:20–27

    Google Scholar 

  • Kollros J, Kaltenbach JC (1952) Metamorphosis of larval skin in Rana pipiens. Physiol Zool 25:163–170

    Google Scholar 

  • McGarry MP, Vanable JW Jr (1969) The role of thyroxine in the formation of the gland rudiments in the skin of Xenopus laevis. Dev Biol 20:426–434

    Google Scholar 

  • Nieuwkoop PD, Faber J (1956) Normal table of Xenopus laevis (Daudin). North-Holland Publ. Co, Amsterdam

    Google Scholar 

  • Pearse AGE (1976) Peptides in brain and intestine. Nature 262:92–94

    Google Scholar 

  • Richter K, Kawashima E, Egger R, Kreil G (1984) Biosynthesis of thyrotropin releasing hormone in the skin of Xenopus laevis: partial sequence of the precursor deduced from cloned cDNA. EMBO J 3:617–621

    Google Scholar 

  • Solcia E, Usellini L, Buffa R, Rindi G, Villani L, Zampatti C, Silini E (1987) Endocrine cells producing regulatory peptides. Experientia 43:839–850

    Google Scholar 

  • Sternberger LA, Jardy PH Jr, Cuculis JJ, Meyers HG (1970) Unlabeled antibody-enzyme method of immunocytochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in the identification of spirochtes. J Histochem Cytochem 18:315–333

    Google Scholar 

  • Vacca LL, Rosario SL, Zimmerman EA, Tomashefsky P, Po-Ying NG, Hsu KG (1975) Application of immunoperoxidase technique to localize horseradish peroxidase-tracer in the central nervous system. J Histochem Cytochem 23:208–215

    Google Scholar 

  • Vanable WJ Jr (1964) Granular gland development during Xenopus laevis metamorphosis. Dev Biol 10:331–357

    Google Scholar 

  • Verma K (1965) Regional differences in skin gland differentiation in Rana pipiens. J Morphol 117:73–86

    Google Scholar 

  • Wakabayashi T, Kato H, Tachibana S (1984) An unusual repetitive structure of caerulein mRNA from the skin of Xenopus laevis. Gene 31:295–299

    Google Scholar 

  • Wakabayashi T, Kato H, Tachibana S (1985) Complete nucleotide sequence of mRNA for caerulein precursor from Xenopus skin: the mRNA contains an unusual repetitive structure. Nucleic Acids Res 13:1817–1828

    Google Scholar 

  • Yoshie S, Iwanaga T, Fujita T (1985) Coexistence of bombesin and 5-hydroxytryptamine in the cutaneous gland of the frog, Bombiana orientalis. Cell Tissue Res 239:25–29

    Google Scholar 

  • Zasloff M (1987) Magainins, a class of antimicrobial peptides from Xenopus skin: Isolation, characterization of two active form, and partial cDNA sequence of a precursor. Proc Natl Acad Sci USA 84:5449–5453

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seki, T., Kikuyama, S. & Yanaihara, N. Development of Xenopus laevis skin glands producing 5-hydroxytryptamine and caerulein. Cell Tissue Res. 258, 483–489 (1989). https://doi.org/10.1007/BF00218860

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00218860

Key words

Navigation