Abstract
The biosynthesis of the peptides caerulein and PGLa in granular skin glands of Xenopus laevis proceeds through a pathway that involves discrete morphological rearrangements of the entire secretory compartment. Immunocytochemical localization of these peptides during gland development indicates that biosynthetic precursors are synthesized in intact secretory cells, whereas posttranslational processing requires morphological reorganization to a vacuolated stage. The bulk of the processed secretory material is then stored in vacuolae- derived storage granules. In the mature gland, storage granules are still formed at a low level. However, in this case processing takes place in a distinct cytoplasmic structure, the multicored body, which we suggest to be functionally equivalent to vacuolae. When granular glands regenerate after having lost all their storage granules upon strong stimuli, another morphological pathway is used. 2 wk after gland depletion, secretory cells become arranged in a monolayer that covers the luminal surface of the gland. Storage granules are formed continuously within these intact secretory cells. Here, precursor processing does not require a vacuolated stage as in newly generated glands but occurs in multicored bodies. Most storage granules seem to be formed in the third week of regeneration. The high biosynthetic activity is also reflected by the high activity of the putative processing enzyme dipeptidyl aminopeptidase during this period of regeneration.
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- Anastasi A., Bertaccini G., Cei J. M., De Caro G., Erspamer V., Impicciatore M., Roseghini M. Presence of caerulein in extracts of the skin of Leptodactylus pentadactylus labyrinthicus and of Xenopus laevis. Br J Pharmacol. 1970 Jan;38(1):221–228. doi: 10.1111/j.1476-5381.1970.tb10351.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anastasi A., Erspamer V., Endean R. Isolation and amino acid sequence of caerulein, the active decapeptide of the skin of hyla caerulea. Arch Biochem Biophys. 1968 Apr;125(1):57–68. doi: 10.1016/0003-9861(68)90638-3. [DOI] [PubMed] [Google Scholar]
- Andreu D., Aschauer H., Kreil G., Merrifield R. B. Solid-phase synthesis of PYLa and isolation of its natural counterpart, PGLa [PYLa-(4-24)] from skin secretion of Xenopus laevis. Eur J Biochem. 1985 Jun 18;149(3):531–535. doi: 10.1111/j.1432-1033.1985.tb08957.x. [DOI] [PubMed] [Google Scholar]
- Araki K., Tachibana S., Uchiyama M., Nakajima T., Yasuhara T. Isolation and structure of a new active peptide "Xenopsin" on the smooth muscle, especially on a strip of fundus from a rat stomach, from the skin of Xenopus laevis. Chem Pharm Bull (Tokyo) 1973 Dec;21(12):2801–2804. doi: 10.1248/cpb.21.2801. [DOI] [PubMed] [Google Scholar]
- Bennett G. W., Balls M., Clothier R. H., Marsden C. A., Robinson G., Wemyss-Holden G. D. Location and release of TRH and 5-HT from amphibian skin. Cell Biol Int Rep. 1981 Feb;5(2):151–158. doi: 10.1016/0309-1651(81)90023-0. [DOI] [PubMed] [Google Scholar]
- Bertaccini G. Active polypeptides of nonmammalian origin. Pharmacol Rev. 1976 Jun;28(2):127–177. [PubMed] [Google Scholar]
- Dockray G. J., Hopkins C. R. Caerulein secretion by dermal glands in Xenopus laevis. J Cell Biol. 1975 Mar;64(3):724–733. doi: 10.1083/jcb.64.3.724. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Erspamer V. Biogenic amines and active polypeptides of the amphibian skin. Annu Rev Pharmacol. 1971;11:327–350. doi: 10.1146/annurev.pa.11.040171.001551. [DOI] [PubMed] [Google Scholar]
- Feurle G. E., Carraway R. E., Rix E., Knauf W. Evidence for the presence of xenopsin-related peptide(s) in the gastric mucosa of mammals. J Clin Invest. 1985 Jul;76(1):156–162. doi: 10.1172/JCI111940. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoffmann W., Bach T. C., Seliger H., Kreil G. Biosynthesis of caerulein in the skin of Xenopus laevis: partial sequences of precursors as deduced from cDNA clones. EMBO J. 1983;2(1):111–114. doi: 10.1002/j.1460-2075.1983.tb01390.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoffmann W., Richter K., Kreil G. A novel peptide designated PYLa and its precursor as predicted from cloned mRNA of Xenopus laevis skin. EMBO J. 1983;2(5):711–714. doi: 10.1002/j.1460-2075.1983.tb01489.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hopkins C. R. The fine structure of the cutaneous poison glands in Xenopus laevis. J Physiol. 1971 Dec;219(2):9P–10P. [PubMed] [Google Scholar]
- Julius D., Blair L., Brake A., Sprague G., Thorner J. Yeast alpha factor is processed from a larger precursor polypeptide: the essential role of a membrane-bound dipeptidyl aminopeptidase. Cell. 1983 Mar;32(3):839–852. doi: 10.1016/0092-8674(83)90070-3. [DOI] [PubMed] [Google Scholar]
- Kreil G., Haiml L., Suchanek G. Stepwise cleavage of the pro part of promelittin by dipeptidylpeptidase IV. Evidence for a new type of precursor--product conversion. Eur J Biochem. 1980 Oct;111(1):49–58. doi: 10.1111/j.1432-1033.1980.tb06073.x. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Orci L., Halban P., Amherdt M., Ravazzola M., Vassalli J. D., Perrelet A. Nonconverted, amino acid analog-modified proinsulin stays in a Golgi-derived clathrin-coated membrane compartment. J Cell Biol. 1984 Dec;99(6):2187–2192. doi: 10.1083/jcb.99.6.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orci L., Ravazzola M., Amherdt M., Madsen O., Vassalli J. D., Perrelet A. Direct identification of prohormone conversion site in insulin-secreting cells. Cell. 1985 Sep;42(2):671–681. doi: 10.1016/0092-8674(85)90124-2. [DOI] [PubMed] [Google Scholar]
- Reading M. A digestion technique for the reduction of background staining in the immunoperoxidase method. J Clin Pathol. 1977 Jan;30(1):88–90. doi: 10.1136/jcp.30.1.88. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sigel M. B., Sinha Y. N., VanderLaan W. P. Production of antibodies by inoculation into lymph nodes. Methods Enzymol. 1983;93:3–12. doi: 10.1016/s0076-6879(83)93031-8. [DOI] [PubMed] [Google Scholar]
- Small J. V., Fürst D. O., De Mey J. Localization of filamin in smooth muscle. J Cell Biol. 1986 Jan;102(1):210–220. doi: 10.1083/jcb.102.1.210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sternberger L. A., Hardy P. H., Jr, Cuculis J. J., Meyer H. G. The unlabeled antibody enzyme method of immunohistochemistry: preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem. 1970 May;18(5):315–333. doi: 10.1177/18.5.315. [DOI] [PubMed] [Google Scholar]
- Tatemoto K., Mutt V. Isolation of two novel candidate hormones using a chemical method for finding naturally occurring polypeptides. Nature. 1980 Jun 5;285(5764):417–418. doi: 10.1038/285417a0. [DOI] [PubMed] [Google Scholar]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- VANABLE J. W., Jr GRANULAR GLAND DEVELOPMENT DURING XENOPUS LAEVIS METAMORPHOSIS. Dev Biol. 1964 Dec;10:331–357. doi: 10.1016/0012-1606(64)90049-1. [DOI] [PubMed] [Google Scholar]