The aim of this study was to characterize the nature and regional distribution of the glycoconjugates secreted by epidermal mucous cells in Eisenia foetida (Annelida). Specimens were divided into six regions from anterior to posterior. The histochemistry was carried out by using standard histochemical methods. Histochemical staining properties of glycoconjugates in epidermal mucous cells were determined regionally. The epidermis of all regions contained strong to stronger PAS (+) cells in various degrees. The epidermis of the first, fourth, fifth, and sixth regions had strong to stronger AB pH 2.5 (+) cells. On the contrary, all regions contained weak to moderate AB pH 0.5 and AB pH 1.0 (+) cells. Most of mucous cells in epidermis of the first region contained both PAS (+) and AB (+) mucosubstances. All regions included weaker to weak AF (+) cells. All regions featured KOH/PAS (+) cells, with a slight reduction in reaction intensity in the epidermis of the last three regions. In this context, the different staining patterns observed in epidermal mucous cells hinted at their functional roles with respect to production of mucus with different physical properties. This study provided comprehensive information about the regional distribution patterns of the glycoconjugates and an opportunity to compare their distributional patterns in other annelids. 1. Introduction Histological, histochemical, and ultrastructural studies have unveiled the existence of a variable and complex structure of the epidermis in annelids [1–3]. The epidermis of the annelids consists of a monolayered epithelium, which contains glandular, supporting, ciliated, and sensory cells. The epidermis is covered by a cuticle composed of collagen fibers embedded in a matrix [4]. The glandular cells in the surface epithelia secrete mucus that is rich in glycans, glycoproteins, and sialic acid residues [5–7]. In the annelids, this mucous secretion also plays a fundamental role in the formation of the ground substance of tubes, protection from dehydration, absorption of metabolites, and protection against parasites [4]. The glycoconjugates, which are essential components of the glycocalyx of many cell types, take part in many functions, including osmoregulation, cell to cell recognition, binding of hormones, protection of cells from phagocytosis and dehydration, differentiation, defense, and ion transport [8]. In some epithelial cells, which morphologically and functionally polarize in relation to different behaviours in ion transport [9], it is likely that a functional specialization of the
References
[1]
H. E. Potswald, “A fine structural analysis of the epidermis and cuticle of the Oligochaete Aeolosoma bengalense Stephenson,” Journal of Morphology, vol. 135, no. 2, pp. 185–212, 1971.
[2]
J. A. Aguirre, J. Aijon, and J. L. Lopez-Campos, “Histochemical analysis on the normal skin of Allolobophora chlorotica Sav. (Annelida, Oligochaeta),” Archives de Biologie, vol. 92, no. 2, pp. 237–245, 1981.
[3]
U. Welsch, V. Storch, and K. S. Richards, “Annelida—epidermal cells,” in Biology of the Integument, Vol. 1. Invertebrates, H. J. Bereiter, A. G. Matoltsy, and K. S. Richards, Eds., chapter 17, pp. 269–296, Springer, Berlin, Germany, 1984.
[4]
V. Storch, “Integument,” in Microfauna Marina, W. Westheide and C. O. Hermans, Eds., vol. 4 of The Ultrastructure of Polychaeta, pp. 13–36, Gustav Fischer, Stuttgart, Germany, 1988.
[5]
N. S. Gorgees and L. J. Rashan, “Histomorphological and histochemical studies on the epidermis of the lumbricid worm, Dendrobaena atheca cernosvitov,” Zeitschrift für Mikroskopisch-Anatomische Forschung, vol. 96, no. 6, pp. 1078–1088, 1982.
[6]
M. Mastrodonato, E. Lepore, M. Gherardi, S. Zizza, M. Sciscioli, and D. Ferri, “Histochemical and ultrastructural analysis of the epidermal gland cells of Branchiomma luctuosum (Polychaeta, Sabellidae),” Invertebrate Biology, vol. 124, no. 4, pp. 303–309, 2005.
[7]
H. B. F. Amaral, S. H. Mateus, L. C. Ferreira et al., “Localization and characterization of sulfated glycosaminoglycans in the body of the earthworm Eisenia andrei (Oligochaeta, Annelida),” Acta Histochemica, vol. 113, no. 4, pp. 442–452, 2011.
[8]
A. Licata, A. Mauceri, L. Ainis et al., “Lectin histochemistry of epidermal glandular cells in the earthworm Lumbricus terrestris (Annelida Oligochaeta),” European Journal of Histochemistry, vol. 46, no. 2, pp. 173–178, 2002.
[9]
S. S. Spicer, D. A. Baron, A. Sato, and B. A. Shulte, “Variability of cell surface glycoconjugates—relation to differences in cell function,” Journal of Histochemistry and Cytochemistry, vol. 29, no. 9, pp. 994–1002, 1981.
[10]
M. Pisam and P. Ripoche, “Redistribution of surface macromolecules in dissociated epithelial cells,” Journal of Cell Biology, vol. 71, no. 3, pp. 907–920, 1976.
[11]
T. Fujimoto and K. Ogawa, “Cell membrane polarity in dissociated frog urinary bladder epithelial cells,” Journal of Histochemistry and Cytochemistry, vol. 31, no. 1, pp. 131–138, 1983.
[12]
K. S. Richards, “Epidermis and cuticle,” in Physiology of Annelids, P. J. Mill, Ed., pp. 33–61, Academic Press, London, UK, 1978.
[13]
A.-R. Im, Y. Park, J.-S. Sim et al., “Glycosaminoglycans from earthworms (Eisenia andrei),” Glycoconjugate Journal, vol. 27, no. 2, pp. 249–257, 2010.
[14]
W. J. Curry, I. Fairweather, C. F. Johnston, D. W. Halton, and K. D. Buchanan, “Immunocytochemical demonstration of vertebrate neuropeptides in the earthworm Lumbricus terrestris (Annelida, Oligochaeta),” Cell and Tissue Research, vol. 257, no. 3, pp. 577–586, 1989.
[15]
A. Licata, A. Mauceri, M. B. Ricca, P. Lo Cascio, S. Martella, and A. Amato, “Immunohistochemical localization of calcium-binding proteins (CaBPs) in the epidermis of the earthworm Lumbricus terrestris (Annelida, Oligochaeta),” Acta Histochemica, vol. 102, no. 2, pp. 159–166, 2000.
[16]
A. Licata, L. Ainis, S. Martella et al., “Immunohistochemical localization of nNOS in the skin and nerve fibers of the earthworm Lumbricus terrestris L. (Annelida oligochaeta),” Acta Histochemica, vol. 104, no. 3, pp. 289–295, 2002.
[17]
K. S. Richards, “The histochemistry of the large granular, orthochromatic, mucous cells of some lumbricids,” Annales d'Histochimie, vol. 18, no. 4, pp. 289–300, 1973.
[18]
K. S. Richards, “The histochemistry of the metachromatic mucous cells of some lumbricids,” Annales d'Histochimie, vol. 19, no. 3, pp. 187–197, 1974.
[19]
K. S. Richards, “The histochemistry of the small granular, proteinaceous cell (albumen cells) of the epidermis of some lumbricids. (Annelida: Oligochaeta),” Annales d'Histochimie, vol. 19, no. 4, pp. 239–251, 1974.
[20]
K. S. Richards, “The histochemistry of the mucous cells of the epidermis of some lumbricillid enchytraeids (Annelida, Oligochaeta),” Cellular and Molecular Biology, vol. 22, no. 2, pp. 219–225, 1977.
[21]
K. S. Richards, “Structure and function in the oligochaete epidermis (Annelida),” in Comparative Biology of Skin, R. I. C. Spearman, Ed., vol. 39 of Symposia of Zoological Society of London, pp. 171–193, 1977.
[22]
C. Suzutani, “Light microscopic and electron microscopical observations on the clitellar epithelium of Tubifex,” Journal of the Faculty of Science Hokkaido University Series VI Zoology, vol. 21, no. 1, pp. 1–11, 1977.
[23]
V. D. Dall Pai, I. R. Santos Costa, A. C. Campos Pacheco, C. E. Alves, and N. Macha, “Histochemical study of mucopolysaccharides in epidermal mucous cells and subjacent granular cells of Glossoscolex uruguayensis L. (Righi, 1978),” Folia Histochemica et Cytochemica, vol. 19, no. 2, pp. 107–114, 1981.
[24]
V. K. Garg, S. Chand, A. Chhillar, and A. Yadav, “Growth and reproduction of Eisenia foetida in various animal wastes during vermicomposting,” Applied Ecology and Environmental Research, vol. 3, no. 2, pp. 51–59, 2005.
[25]
F. Monroy, M. Aira, J. Domínguez, and A. Velando, “Seasonal population dynamics of Eisenia fetida (Savigny, 1826) (Oligochaeta, Lumbricidae) in the field,” Comptes Rendus-Biologies, vol. 329, no. 11, pp. 912–915, 2006.
[26]
G. M. Morris, “Secretory cells in the clitellar epithelium of Eisenia foetida (Annelida, Oligochaeta): a histochemical and ultrastructural study,” Journal of Morphology, vol. 185, no. 1, pp. 89–100, 1985.
[27]
H. Herlant-Meewis, “Evolution des caractéres sexuels au cours de la croissance et de la reproduction chez Eisenia foetida,” Annales de la Société Royale Zoologique de Belgique, vol. 89, pp. 281–336, 1959.
[28]
L. S. Smith, “Digestive functions in teleost fishes,” in Fish Nutrition, J. E. Halver, Ed., pp. 331–421, Academic Press, San Diego, Calif, USA, 1989.
[29]
A. A. Obuoforibo, “Mucosubstances in Brunner's glands of the mouse,” Journal of Anatomy, vol. 119, no. 2, pp. 287–294, 1975.
[30]
G. Zimmer, G. Reuter, and R. Schauer, “Use of influenza C virus for detection of 9-O-acetylated sialic acids on immobilized glycoconjugates by esterase activity,” European Journal of Biochemistry, vol. 204, no. 1, pp. 209–215, 1992.
[31]
M. Mastrodonato, M. Gherardi, G. Todisco, M. Sciscioli, and E. Lepore, “The epidermis of Timarete filigera (Polychaeta, Cirratulidae): Histochemical and ultrastructural analysis of the gland cells,” Tissue and Cell, vol. 38, no. 5, pp. 279–284, 2006.
[32]
H. M. Murray, D. Gallardi, Y. S. Gidge, and G. L. Sheppard, “Histology and mucous histochemistry of the integument and body wall of a marine polychaete worm, Ophryotrocha n. sp. (Annelida: Dorvilleidae) associated with Steelhead Trout Cage Sites on the South Coast of Newfoundland,” Journal of Marine Biology, vol. 2012, Article ID 202515, 7 pages, 2012.
[33]
A. Tsukise and K. Yamada, “The histochemistry of complex carbohydrates in the scrotum of the boar,” Histochemistry, vol. 72, no. 4, pp. 511–521, 1981.
[34]
A. K. Mittal, O. Fujimori, H. Ueda, and K. Yamada, “Carbohydrates in the epidermal mucous cells of a fresh-water fish Mastacembelus pancalus (Mastacembelidae, Pisces) as studied by electron-microscopic cytochemical methods,” Cell and Tissue Research, vol. 280, no. 3, pp. 531–539, 1995.
[35]
J. F. A. McManus, “Histological and histochemical uses of periodic acid,” Stain Technology, vol. 23, pp. 99–108, 1948.
[36]
R. W. Mowry, “Alcian blue techniques for the histochemical study of acidic carbohydrates,” Journal of Histochemistry and Cytochemistry, vol. 4, pp. 407–408, 1956.
[37]
R. LEV and S. S. SPICER, “Specific staining of sulphate groups with alcian blue at low pH,” Journal of Histochemistry and Cytochemistry, vol. 12, article 309, 1964.
[38]
G. Gomori, “Gomori’s aldehyde fuchsin stain,” in Cellular Pathology Technique, C. F. A. Culling, R. T. Allison, and W. T. Barr, Eds., pp. 214–255, Butterworths, London, UK, 1985.
[39]
S. S. Spicer and D. R. Mayer, “Aldehyde fuchsin/alcian blue,” in Cellular Pathology Technique, C. F. A. Culling, R. T. Allison, and W. T. Barr, Eds., pp. 214–255, Butterworths, London, UK, 1985.
[40]
C. F. Culling, P. E. Reid, and W. L. Dunn, “The effect of saponification upon certain histochemical reactions of the epithelial mucins of the gastrointestinal tract,” Journal of Histochemistry and Cytochemistry, vol. 19, no. 11, pp. 654–662, 1971.
