Serous Glands in the Skin of the Tungara Frog, Engystomops pustulosus (Cope, 1864) (Anura, Leptodactylidae): Degenerated Secretory Units are Selectively Removed by Macrophages

Irina Arifulova, Giovanni Delfino, Tatjana Dujsebayeva, Galina Fedotovskikh, Filippo Giachi

Abstract


The cutaneous apparatus of Engystomops pustulosus (Cope, 1864) (the Tungara frog) includes serous glands that show impressive patterns of degeneration in their syncytial secretory units, and thus represent suitable organ models to investigate the role of macrophages in renewal processes of multicellular structures. The present case report exploits this chance and highlights that: (a) degenerating glands pertain to the Ia line of the polymorphic serous gland assortment in Tungara skin; (b) resident macrophages migrate from spongy dermis and remove syncytium debris; (c) secretory syncytium collapse results from impairment of the equilibrium between serous product manufacturing/storage and merocrine release into the dermal environment; (d) Intercalated tract (or gland neck) and myoepithelium (included its ortho-sympathetic nerve supply), are neither involved in degeneration nor affected by macrophage response. According to present evidence and current literature, it is concluded that the scavenger activity of macrophages prepares secretory unit renewal, performed by stem cells from the neck. In addition, gland functional rehabilitation may rely on effectiveness of the preexisting neuromuscular apparatus to achieve secretory bulk release onto the cutaneous surface.

Keywords


Tungara frog; dermal macrophages; serous glands; ultrastructure

Full Text:

PDF

References


Arifulova I., Delfino G., Dujsebayeva T., Fedotovskikh G., Nosi D., and Terreni A. (2007), «Serous cutaneous glands in the South American horned frog Ceratophrys ornata (Leptodactylformes, Chthonobatrachia, Ceratophrydae): Ultrastructural expression of poison biosynthesis and maturation», J. Morphol., 268, 690 – 700.

Balboni F., Bernabei P. A., Barberio C., Sanna A., Rossi Ferrini P. G., and 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.

Bani G. (1976), «Cellule mioepiteliali accluse alle ghiandole cutanee di alcuni Anfibi», Archo Ital. Anat. Embriol., 81, 133 – 184.

Barberio C., Delfino G., and Mastromei G. (1987), «A low molecular weight protein with antimicrobial activity in the cutaneous ‘venom’ of the yellow-bellied toad (Bombina variegata pachypus)», Toxicon, 25, 899 – 909.

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.

Delfino G. (1991), «Ultrastructural aspects of venom secretion in anuran cutaneous glands», in: A. T. Tu (ed.), Handbook of Natural Toxins. Vol. 5. Reptile and Amphibian Venoms, Marcel Dekker Inc., New York, pp. 777 – 801.

Delfino G., Amerini S. and Mugelli A. (1982), «In vitro studies on the ‘venom’ emission from the skin of Bombina variegata pachypus (Bonaparte) (Amphibia Anura Discoglossidae)», Cell Biol. Int. Rep., 6, 843 – 850.

Delfino G., Brizzi R., Alvarez B. B., and Kracke-Berndorff R. (1998), «Serous cutaneous glands in Phyllomedusa hypochondrialis (Anura, Hylidae): secretory patterns during ontogenesis», Tissue Cell, 30, 30 – 40.

Delfino G., Brizzi R., Alvarez B. B., and Gentili M. (1999), «Granular cutaneous glands in the frog Physalaemus biligonigerus (Anura, Leptodactylidae): a comparison between ordinary serous and «inguinal» glands», Tissue Cell, 31, 576 – 586.

Delfino G., Brizzi R., and Borrelli G. (1988), «Cutaneous glands in Anurans: Differentiation of the secretory syncytium in serous anlagen», Zool. Jb. Anat., 117, 255 – 275.

Delfino G., Brizzi R., and Calloni C. (1990), «A morpho-functional characterization of the serous cutaneous glands in Bombina orientalis (Anura: Discoglossidae)», Zool. Anz., 225, 295 – 310.

Delfino G., Brizzi R., De Santis R., and 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.

Delfino G., Brizzi R., and Melis G. (1996), «Merocrine secretion from serous cutaneous glands in Rana esculenta complex and Rana iberica», Alytes, 13, 179 – 192.

Delfino G., Brizzi R., Nosi D., and 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.

Delfino G., Drewes R. C., Magherini C., Malentacchi C., Nosi D. and Terreni A. (2006), «Serous cutaneous glands of the Pacific tree-frog Hyla regilla (Anura, Hylidae): Patterns of secretory release induced by nor-epinephrine», Tissue Cell, 38, 65 – 77.

Delfino G., Giachi F., Malentacchi C., and Nosi D. (2015), «Ultrastructural evidence of serous gland polymorphism in the skin of the tungara frog Engystomops pustulosus (Anura Leptodactylidae)», The Anat. Rec., 298, 1659 – 1667.

Delfino G., Giachi F., Nosi D., and Malentacchi C. (2010), «Serous cutaneous glands in Phyllobates bicolor (Anura: Dendrobatidae): an ontogenetic, ultrastructural study on secretory product biosynthesis and maturation», Copeia, 2010, 27 – 37.

Delfino G., Giachi F., and Nosi D. (2014), «Poison storage and maturation in serous cutaneous glands of anurans: an integrative ultrastructural outlook», in: H. Lambert (ed.), Frogs: Genetic Diversity, Neural Development and Ecological Implication, Nova Publishers, New York, pp. 1 – 71.

Delfino G., Nosi D., and Giachi F. (2001), «Secretory granule- cytoplasm relationships in serous glands of anurans: ultrastructural evidence and possible functional role», Toxicon, 39, 1161 – 1171.

Faraggiana R. (1938), «Ricerche istologiche sulle ghiandole cutanee granulose degli Anfibi Anuri. I. Bufo vulgaris e Bufo viridis», Archo Ital. Anat. Embriol., 39, 327 – 376.

Faraggiana R. (1939), «Ricerche istologiche sulle ghiandole cutanee granulose degli Anfibi Anuri. II. Rana esculenta, Rana agilis e Bombinator pachypus», Archo Ital. Anat. Embriol., 41, 390 – 410.

Glaumann H. (1989), «Crinophagy as a means for degrading excess secretory proteins in rat liver», Rev. sobre Biol. Celular, 20, 97 – 110.

Karnovsky M. J. (1965), «A formaldehyde-glularaldehyde fixative of high osomolarity for use in electron microscopy», J. Cell Biol., 27, 137A.

Mastromei G., Barberio C., Pistolesi S., and Delfino G. (1991), «A bactericidal protein in Bombina variegata pachypus skin venom», Toxicon, 29, 321 – 328.

Melzer S., Clerens S., and Bishop P. J. (2013), «Skin gland morphology and secretory peptides in naturalized Litoria species in New Zealand», J. Herpetol., 47, 565 – 574.

Nosi D., Delfino G., and Quercioli F. (2013), «Serous cutaneous glands in anurans: Fourier transform analysis of the repeating secretory granule substructure», Naturwissenschaften, 100, 209 – 218.

Nosi D., Terreni A., Alvarez B. B., and Delfino G. (2002), «Serous cutaneous gland polymorphism in the skin of Phyllomedusa hypochondrialis azurea (Anura, Hylidae). Response by different gland types to norepinephrine stimulation», Zoomorphology, 121, 139 – 148.

Popescu L. M., Gherghiceanu M., Mandache E., and Cretoiu D. (2006), «Caveolae in smooth muscles: nanocontacts», J. Cell. Mol. Med., 10, 960 – 990.

Quagliata S., Malentacchi C., Giachi F., and Delfino G. (2008b), «Chemical skin defence in the Eastern fire-bellied toad Bombina orientalis: an ultrastructural approach to the mechanism of poison gland rehabilitation after discharge», Acta Herpetol., 3, 139 – 153.

Quagliata S., Pacini S., Punzi T., Malentacchi C., Ruggiero M., and Delfino G. (2008a), «Bombesin promotes vasculogenesis and angiogenesis in chick chorio-allantoic membrane: a morphometric, structural and ultrastructural study», J. Morphol., 269, 72 – 83.

Sanna A., Bernabei P. A., Rossi Ferrini P., Brunelli T., and Delfino G. (1993), «The cutaneous venom of Bombina orientalis: cytotoxic effects on the human HL 60 cell line and a comparison with Bombina variegata», J. Nat. Toxins, 2, 161 – 173.

Sevinc M., Nosi D., Brizzi R., Terreni A., Malentacchi C., and Delfino G. (2005), «Ultrastructural study on host-guest relationships between anuran serous cutaneous glands and nematodes», Caryologia, 58, 112 – 131.

Sopel M. (2010), «The myoepithelial cell: its role in normal mammary glands and breast cancer», Folia Morphol., 69, 1 – 14.




DOI: https://doi.org/10.30906/1026-2296-2021-28-5-281-290

Refbacks

  • There are currently no refbacks.


You can subscribe to the print or electronic version of the journal on the site of EastView Company. If you have any questions, please write to the email sales@ivis.ru