Serous cutaneous glands in the South American horned frog Ceratophrys ornata (Leptodactylformes, Chthonobatrachia, Ceratophrydae): Ultrastructural expression of poison biosynthesis and maturation

Journal of Morphology

Volumn 268, Issue 8, 2007, Pages 690-700

  Arifulova, Irina ^a   Delfino, Giovanni ^b   Dujsebayeva, Tatjana ^c   Fedotovskikh, Galina ^d   Nosi, Daniele ^b   Terreni, Alessandro ^e  

^a AL FARABI KAZAKH NATIONAL UNIVERSITY   (Kazakhstan)

^b UNIVERSITY OF FLORENCE   (Italy)

^c Ministry of Education and Science of the Republic of Kazakhstan   (Kazakhstan)

^d Kazakhstan   (Kazakhstan)

^e CAREGGI UNIVERSITY HOSPITAL   (Italy)

Author keywords

Anura; Ceratophrydae; Cutaneous glands; Ultrastructure

Indexed keywords

AMPHIBIAN VENOM;

ANIMAL; ARTICLE; BIOSYNTHESIS; CLASSIFICATION; EXOCRINE GLAND; FROGS AND TOADS; HISTOLOGY; METABOLISM; PHYSIOLOGY; SECRETORY VESICLE; SKIN; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AMPHIBIAN VENOMS; ANIMALS; ANURA; EXOCRINE GLANDS; MICROSCOPY, ELECTRON, TRANSMISSION; SECRETORY VESICLES; SKIN;

ANURA; CERATOPHRYS ORNATA; HEMIPHRACTUS;

EID: 34547746418     PISSN: 03622525     EISSN: 10974687     Source Type: Journal    
DOI: 10.1002/jmor.10541     Document Type: Article

References (48)

1. Alvarez BB, Delfino G, Nosi D, Terreni A. 2005. Ultrastructure of poison glands of South American frogs: A comparison between Physalaemus albonotatus and Leptodactylus chaquensis (Anura: Leptodactylidae). J Morphol 263:247-258.
2. Angel R, Delfino G, Parra GJ. 2003. Ultrastructural patterns of secretory activity in poison cutaneous glands of larval and juvenile Dendrobates auratus (Amphibia, Anura). Toxicon 41:29-39.
3. Balboni F, Bernabei PA, Barberio C, Sanna A, Rossi Ferrini P, Delfino G. 1992. Cutaneous venom of Bombina variegata pachypus Amphibia, Anura): Effects on the growth of the human HL 60 cell line. Cell Biol Int Rep 16:329-338.
4. Barberio C, Delfino G, Mastromei G. 1987. A low molecular weight protein with antimicrobial activity in the cutaneous "venom" of the yellow-belied toad (Bombina variegata pachypus). Toxicon 25:899-909.
5. Barra D, Simmaco M. 1995. Amphibian skin: A promising resource for antimicrobial peptides. Trends Biotechnol 13:205-209.
6. Bertossi F. 1937. Sulle ghiandole granulose cutanee di Bombinator igneus Laur. Monitore Zool Ital 48:341-344.
7. Cei JM. 1980. Amphibians of Argentina. Monit Zool Ital NS, Monografia 2: p XII + 609.
8. Cei JM, Erspamer V, Roseghini M. 1967. Taxonomic and evolutionary significance of biogenic amines and polypeptides occurring in amphibian skin. I. Neotropical leptodactylid frogs. Syst Zool 16:328-342.
9. Daly JW. 1998. Thirty years of discovering arthropod alkaloids in amphibian skin. J Nat Prod 61:162-172.
10. Daly JW, Myers CW, Whittaker N. 1987. Further classification of skin alkaloids from Neotropical poison frogs (Dendrobatidae), with a general survey of toxic/noxious substances in the Amphibia. Toxicon 25:1023-1095.
11. Delfino G. 1976. Structural and ultrastructural aspects of the cutaneous granular glands in Bombina variegata (L.) (Amphibia Anura Discoglossudae). Monitore Zool Ital NS 10:421-448.
12. Delfino G. 1977. Il differenziamento delle ghiandole granulose cutanee in larve di Bombina variegata pachypus (Bonaparte) (Anfibio, Anuro, Discoglosside). Ricerca al microscopio ottico e al microscopio elettronico. Archo Ital Anat Embriol 82:337-352.
13. Delfino G. 1980. L'attività rigeneratrice del tratto intercalare nelle ghiandole granulose cutanee dell'Ululone Bombina variegata pachypus (Bonaparte) (Anfibio, Anuro, Discoglosside); studio sperimentale al microscopio elettronico. Archo Ital Anat Embriol 85:283-310.
14. Delfino G. 1991. Ultrastructural aspects of venom secretion in anuran cutaneous glands. In: TU AT, editor. Handbook of Natural Toxins, Vol. 5: Reptile venoms and toxins. New York: Marcel Dekker. pp 777-802.
15. Delfino G, Melis G. 1998. Serous cutaneous glands in the natterjack Bufo calamita (Anura, Bufonidae): The fundamental role of aggregation processes during poison maturation. Zoology 101:53-66.
16. Delfino G, Brizzi R, Borrelli G. 1988. Cutaneous glands in anurans: Differentiation of the secretory syncytium in serous Anlagen. Zool Jahrbüch (Anat) 117:255-275.
17. Delfino G, Brizzi R, Calloni C. 1990. A morpho-functional characterization of the serous cutaneous glands in Bombina orientalis (Anura: Discoglossidae). Zool Anz 225:295-310.
18. Delfino G, Brizzi R, De Santis R, Melosi M. 1992. Serous cutaneous glands of the western spade-foot Pelobates cultripes (Amphibia: Anura): An ultrastructural study on adults and juveniles. Archo Ital Anat Embriol 97:109-120.
19. Delfino G, Brizzi R, Jantra S, Streitberger M. 1993. Cutaneous venom glands in the Tyrrhenian painted frog Discoglossus sardus (Tschudi), ontogenetic evolution of the biosynthesis apparatus. Acta Biol Benrodis 5:129-139.
20. Delfino G, Brizzi R, Calloni C. 1994. Serous cutaneous glands in the tree-frog Hyla arborea (L.): Origin, ontogenetic evolution, and possible functional implications of the secretory granule substructure. Acta Zool (Stockholm) 75:27-36.
21. Delfino G, Brizzi R, Jantra S, Feri L. 1995a. Post-Golgian maturative processes during the biosynthesis of poison secretion in cutaneous glands of the European common toad Bufo bufo. J Nat Tox 4:97-113.
22. Delfino G, Brizzi R, Feri L. 1995b. Chemical skin defence in Bufo bufo: An ultrastructural study during ontogenesis. Zool Anz 234:101-111.
23. Delfino G, Brizzi R, Alvarez BB, Kracke-Berndorff R. 1998a. Serous cutaneous glands in Phyllomedusa hypochondrialis (Anura, Hylidae): Secretory patterns during ontogenesis. Tissue Cell 30:30-40.
24. Delfino G, Brizzi R, Kracke-Berndorff R, Alvarez BB. 1998b. Serous cutaneous gland dimorphism in the skin of Melanophryniscus stelzeneri (Anura: Bufonidae). J Morphol 237:19-32.
25. Delfino G, Alvarez BB, Brizzi R, Cespedez JA. 1998c. Serous cutaneous glands of Argentine Phyllomedusa Wagler 1830 (Anura Hylidae): secretory polymorphism and adaptive plasticity. Trop Zool 11:333-351.
26. Delfino G, Brizzi R, Alvarez BB, Taddei L. 1999. Secretory polymorphism and serous cutaneous gland heterogeneity in Bufo granulosus (Amphibia, Anura). Toxicon 37:1281-1296.
27. Delfino G, Nosi D, Brizzi R, Alvarez BB. 2001a. Serous cutaneous glands in the paludiculine frog Physalaemus biligonigerus (Anura, Leptodactylidae): Patterns of cytodifferentiation and secretory activity in prematomorphic specimens. Acta zool (Stockholm) 82:149-158.
28. Delfino G, Nosi D, Giachi F. 2001b. Secretory granule-cytoplasm relationships in serous glands of anurans: Ultrastructural evidence and possible functional role. Toxicon 39:1161-1171.
29. Delfino G, Brizzi R, Nosi D, Terreni A. 2002. Serous cutaneous glands in new world hylid frogs: An ultrastructural study on skin poisons confirms phylogenetic relationships between Osteopilus septentrionalis and Phrynohyas venulosa. J Morphol 253:176-186.
30. Faraggiana R. 1937. Sulla presenza di due tipi di ghiandole granulose nella pelle di Bombinator pachypus Fitz. Monitore Zool Ital 48:13-16.
31. Faszewski EE, Kaltenbach JC. 1995. Histology and lectin-binding patterns in the skin of the terrestrial horned frog Ceratophrys ornata. Cell Tissue Res 281:169-177.
32. Flucher BE, Lenglachner-Bachinger C, Pohlhammer K, Adams H, Mollay C. 1986. Skin peptides in Xenopus laevis: Morphological requirements for precursor processing in developing and regenerating granular skin glands. J Cell Biol 103:2299-2309.
33. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, De Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BI, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC. 2006. The amphibian tree of life. Bull Am Mus Nat Hist 297:1-370.
34. Glaumann H. 1989. Crinophagy as a means for degrading excess secretory proteins in rat liver. Revis Biol Celular 20:97-110. Gosner KL. 1960. A simplified table for staging anuran embryos and larvae with notes of identification. Herpetologica 16:183-190.
35. Glauert AM. 1975. Fixation, dehydration and embedding of biological samples. In: Glauert AM, editor. Practical Methods in Electron Microscopy. Amsterdam: Elsevier North-Holland Biomedical Press.
36. Hayat MA. 1981. Principles and techniques of electron microscopy. Biological applications. London: Edward Arnold.
37. Luft JH. 1961. Improvement in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409-414.
38. ie. 345 p.
39. Meyer K, Linde H. 1971. Collection of toad venoms and chemistry of the toad venom steroids. In: Bücherl W, Buckley EF, editors. Venomous animals and their venoms, Vol. 2. New York: Academic Press. pp 521-556.
40. Neuwirth M, Daly JW, Myers CW, Tice LW 1979. Morphology of the granular secretory glands in skin of poison-dart frogs (Dendrobatidae). Tissue Cell 11:755-771.
41. Nosi D, Terreni A, Alvarez BB, Delfino G. 2002. Serous gland polymorphism in the skin of Phyllomedusa hypochondrialis azurea (Anura, Hylidae): Response by different gland types to norepinephrine stimulation. Zoomorphology 121:139-148.
42. Sanna A, Bernabei PA, Brunelli T, Rossi Ferrini P, Delfino G. 1993. The cutaneous venom of Bombina orientalis: Cyrotoxic effects on the human HL 60 cell line and a comparison with Bombina variegata. J Nat Tox 2:161-173.
43. Schimtz G, Müller G. 1991. Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J Lip Res 22:1539-1570.
44. Terreni A, Nosi D, Delfino G. 2002. Cutaneous serous glands in South-American anurans, an ultrastructural comparison between hylid and pseudid species. Ital J Zool 69:115-123.
45. Terreni A, Nosi D, Greven H, Delfino G. 2003. Development of serous cutaneous glands in Scinax nasica (Anura, Hylidae): Patterns of poison biosynthesis and maturation in comparison with larval glands in specimens of other families. Tissue Cell 35:274-287.
46. Toledo RC, Jared C. 1995. Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol A 111:1-29.
47. Zasloff M. 1987. Magainins, a class of antimicrobial peptides from Xenopus skin: Isolation, characterization of two active forms and partial cDNA sequence of a precursor. Proc Natl Acad.Sci USA 84:5499-5453.
48. Zasloff M, Martin B, Chen H-C. 1988. Antimicrobial activity of synthetic magainin peptides and several analogues. Proc Natl Acad Sci USA 85:910-913.