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Mucin in epithelial cells in oesophagus and stomach of black tetra, Gymnocorymbus ternetzi (Characidae, Teleostei)

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Abstract

Histochemical properties of the mucus cells in oesophagus and stomach in a teleost, black tetra (Gymnocorymbus ternetzi), are described and compared. These cells were sac-shaped, very numerous, and embraced by ordinary epithelial cells with highly variable shape, throughout the entire length of oesophagus. The stomach luminal epithelial cells were filled with mucin apically, whereas the gastric gland cells lacked mucin. When treated with alcian blue (pH 2.5) before periodic acid–Schiff, the oesophagus mucin displayed a colour between blue and magenta, whereas it was strongly magenta in stomach. After high iron diamine followed by alcian blue (pH 2.5), the oesophagus mucin displayed a clean blue colour, whereas the stomach mucin was uncoloured. The present results for the lectin affinities in mucus cells in oesophagus of black tetra were similar to those of stomach and together suggest that these mucins contain significant amounts of N-acetylglucosamines, galactose-N-acetylgalactosamines sequences, and probably some sialic acid in terminal positions attached to the N-acetylglucosamine, but the mucin seems nearly or entirely to lack glucose and mannose. In addition, all its N-acetylgalactosamines in oesophagus, unlike in stomach, seem to be attached to galactose, as these amines were not coloured by DBA in oesophagus, but intensely coloured by PNA. Together the present results suggest that the oesophagus mucin in black tetra contains both neutral and carboxylated glycoproteins, but lacks sulphated glycoproteins, whereas the stomach mucin contains neutral glycoproteins only. The present results for black tetra suggest that the large amounts of oesophageal mucus and its increased toughness caused by anions may largely compensate for the lack of salivary glands. The stomach mucin lacks anions, a feature which may enhance the flow of the mucus and therefore also its ability to clean and protect the stomach wall against the gastric juice.

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References

  • Arellano JM, Storch V, Sarasquete C (2001) A histological and histochemical study of the oesophagus and oesogaster of the Senegal sole, Solea senegalensis. Eur J Histochem 45:279–294

    Article  CAS  PubMed  Google Scholar 

  • Banan Khojasteh SM, Sheikhzadeh F, Mohammadnejad D, Azami A (2009) Histological, histochemical and ultrastructural study of the intestine of rainbow trout (Oncorhynchus mykiss). World Appl Sci J 6:1525–1531

    CAS  Google Scholar 

  • Bhavanandon VP, Katlic AW (1979) The interaction of wheat germ agglutinin with sialoglycoproteins. The role of sialic acid. J Biol Chem 254:4000–4008

    Google Scholar 

  • Bone Q, Moore R (2008) Biology of fishes, 3rd edn. Taylor and Francis Group, Abingdon

    Google Scholar 

  • Cao XJ, Wang WM (2009) Histology and mucin histochemistry of the digestive tract of yellow catfish, Pelteobagrus fulvidraco. Anat Histol Embryol 38:254–261. doi:10.1111/j.1439-0264.2009.00932.x

    Article  CAS  PubMed  Google Scholar 

  • Cao XJ, Wang WM, Song F (2011) Anatomical and histological characteristics of the intestine of the topmouth culter (Culter alburnus). Anat Histol Embryol 40:292–298. doi:10.1111/j.1439-0264.2011.01069.x

    Article  CAS  PubMed  Google Scholar 

  • Carrassón M, Grau A, Dopazo LR, Crespo S (2006) A histological, histochemical and ultrastructural study of the digestive tract of Dentex dentex (Pisces, Sparidae). Histol Histopathol 21:579–593

    PubMed  Google Scholar 

  • Culling DFA (1974) Handbook of histopathological and histochemical techniques. Butterworth, London

    Google Scholar 

  • Desantis S, Acone F, Zizza S, Deflorio M, Fernández JLP, Sarasquete C, De Metrio G (2009) Glycohistochemical study of the toadfish Halobatrachus didactylus (Schneider, 1801) stomach. Sientia Marina 73:515–525. doi:10.3989/scimar.2009.73n3515

    Article  CAS  Google Scholar 

  • Díaz AO, García AM, Devincenti CV, Goldemberg AL (2003) Morphological and histochemical characterization of the mucosa of the digestive tract in Engraulis anchoita (Hubbs and Marini, 1935). Anat Histol Embryol 32:341–346. doi:10.1111/j.1439-0264.2003.00490.x

    Article  PubMed  Google Scholar 

  • Díaz AO, Escalante AH, García AM, Goldemberg AL (2006) Histology and histochemistry of the pharyngeal cavity and oesophagus of the silverside Odontesthes bonariensis (Cuvier and Valenciennes). Anat Histol Embryol 35:42–46. doi:10.1111/j.1439-0264.2005.00654.x

    Article  PubMed  Google Scholar 

  • Díaz AO, García AM, Goldemberg AL (2008a) Glycoconjugates in the mucosa of the digestive tract of Cynoscion guatucupa: a histochemical study. Acta Histochem 110:76–85. doi:10.1016/j.acthis.2007.08.002

    Article  PubMed  Google Scholar 

  • Díaz AO, García AM, Figueroa DE, Goldemberg AL (2008b) The mucosa of the digestive tract in Micropogonias furnieri: a light and electron microscope approach. Anat Histol Embryol 37:251–256. doi:10.1111/j.1439-0264.2007.00837.x

    Article  PubMed  Google Scholar 

  • Domeneghini C, Straini RP, Veggetti A (1998) Gut glycoconjugates in Sparus aurata L. (Pisces, Teleostei). A comparative histochemical study in larval and adult ages. Histol Histopathol 13:359–372

    CAS  PubMed  Google Scholar 

  • Domeneghini C, Arrighi S, Radaelli G, Bosi G, Mascarello F (1999) Morphological and histochemial peculiarities of the gut in the white sturgeon, Acipenser transmontanus. Eur J Histochem 43:135–145

    CAS  PubMed  Google Scholar 

  • Evans DH, Claiborne JB, Currie S (eds) (2013) The physiology of fishes. Taylor and Francis, Boca Raton

    Google Scholar 

  • Faccioli CK, Chedid RA, Amaral ACD, Franceschini Vicentini IB, Vicentini CA (2014) Morphology and histochemistry of the digestive tract in carnivorous freshwater Hemisorubim platyrhynchos (Siluriformes: Pimelodidae). Micron 64:10–19. doi:10.1016/j.micron.2014.03.011

    Article  CAS  PubMed  Google Scholar 

  • Fiertak A, Kilarski WM (2002) Glycoconjugates of the intestinal goblet cells of four cyrpinids. Cell Mol Life Sci 59:1724–1733. doi:10.1007/PL00012500

    Article  CAS  PubMed  Google Scholar 

  • Gad A, Sylvén B (1969) On the nature of the high iron diamine method for sulfomucins. J Histochem Cytochem 17:156–160

    Article  CAS  PubMed  Google Scholar 

  • Garrido MVO, Torres MIN, Equisoain MAA (1993) Histological, histochemical and ultrastructural analysis of he gastric mucosa in Oncorhynchus mykiss. Aquaculture 115:121–132

    Article  Google Scholar 

  • Germano RD, Stabille SR, Mari RD, Pereira JNB, Faglioni JRS, Neto MHD (2014) Morphological characteristics of the Pterodoras granulosus digestive tube (Valenciennes, 1821) (Osteichthyes, Doradidae). Acta Zool 95:166–175. doi:10.1111/azo.12016

    Article  Google Scholar 

  • Graham RC, Karnowsky MJ (1966) The early stages of absorption of injected peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. Adv Carbohydr Chem Biochem 35:127–131

    Google Scholar 

  • Grimstone AV, Skaer RJ (1972) A guidebook to microscopical methods. Cambridge University Press, London

    Google Scholar 

  • Grossell M, Farrell AP, Brauner CJ (eds) (2011) Fish physiology: The multifunctional gut of fish. Elsevier, London

    Google Scholar 

  • Helfman GS, Collette BB, Facey DE, Bowen BW (2009) The diversity of fishes: biology, evolution, and ecology, 2nd edn. Wiley-Blackwell, Chichester

    Google Scholar 

  • Hernandez MPG, Lozano MT, Elbal MT, Agulleiro B (2001) Development of the digestive tract of sea bass (Dicentrarchus labrax L). Light and electron microscopic studies. Anat Embryol 204:39–57

    Article  Google Scholar 

  • Hernandez DR, Gianselli MP, Domitrovic HA (2009) Morphology, histology and histochemistry of the digestive system of South American Catfish (Rhamdia quelen). Int J Morphol 27:105–111

    Article  Google Scholar 

  • Jaroszewska M, Dabrowski K, Wilczynska B, Kakarekok T (2008) Struture of the gut of the racer goby Neogobius gymnotrachelus (Kessler, 1857). J Fish Biol 72:1773–1786. doi:10.1111/j.1095-8649.2008.01870.x

    Article  Google Scholar 

  • Kullander SO (1999) Fish species – how and why. Rev Fish Biol Fish 9:325–352. doi:10.1023/A:1008959313491

    Article  Google Scholar 

  • Kunz YW (2004) Developmental biology of teleost fishes. Fish and fisheries series. Springer, Dordrecht

    Book  Google Scholar 

  • Leathem AJC, Atkins NJ (1983) Lectin binding to paraffin section techniques. In: Bullock GK, Petrusz P (eds) Techniques in immunocytochemistry. Academic Press, London

    Google Scholar 

  • Leknes IL (1980) Ultrastructure of atrial endocardium and myocardium in three species of Gadidae (Teleostei). Cell Tissue Res 210:1–10

    CAS  PubMed  Google Scholar 

  • Leknes IL (2011) Histochemical studies on mucin-rich cells in digestive tract of Buenos Aires tetra (Characidae: Teleostei). Acta Histochem 113:353–357. doi:10.1016/j.acthis.2010.01.010

    Article  CAS  PubMed  Google Scholar 

  • Lovell T (ed) (1998) Nutrition and feeding of fish, 2nd edn. Kluwer Academic Publishers, Norwell

    Google Scholar 

  • Lund Y, Mejdell CM, Röcklinsberg H, Anthony R, Håstein T (2007) Expanding the moral circle: farmedfish as objects of moral concern. Dis Aquat Organisms 75:109–118. doi:10.3354/dao075109

    Article  Google Scholar 

  • Mittal AK, Ueda T, Fujimori O, Yamada K (1994) Histochemical analysis of glycoproteins in the unicellular glands in the epidermis of an Indian freshwater fish Mastacembelus pancalus (Hamilton). Histochem J 26:666–677

    Article  CAS  PubMed  Google Scholar 

  • Nakamura O, Watanabe T, Kamiya H, Muramoto K (2001) Galectin containing cells in the skin and mucosal tissues in Japanese conger eel, Conger myriaster: an immunohistochemical study. Dev Comp Immunol 25:431–437. doi:10.1016/S0145-305X(01)00012-X

    Article  CAS  PubMed  Google Scholar 

  • Nelson JS (2006) Fishes of the world. Wiley, Hoboken

    Google Scholar 

  • Ostaszewska T (2005) Developmental changes of digestive system structures in pike-perch (Sander lucio perca L.). Electron J Ichthyol 2:65–78

    Google Scholar 

  • Pearse AGE (1985) Histochemistry–theoretical and applied, 4th edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Pedini V, Scocco P, Radaelli G, Fagioli O, Ceccarelli P (2001) Carbohydrate histochemistry of the alimentary canal of the shi drum, Umbrina cirrosa L. Anat Histol Embryol 30:345–349. doi:10.1046/j.1439-0264.2001.00345.x

    Article  CAS  PubMed  Google Scholar 

  • Ramphal R, Pyle M (1983) Evidence for mucins and sialic acid as receptors for Pseudomonas aeruginosa in lower respiratory tract. Infect Immun 41:339–344

    PubMed Central  CAS  PubMed  Google Scholar 

  • Redondo MJ, Alvarez-Pellitero P (2010) Carbohydrate patterns in the digestive tract of Sparus aurata L. and Psetta maxima (L.) (Teleostei) parasitized by Enteromyxum leei and E. scopththalmi (Myxozoa). Parasitol Int 59:445–453. doi:10.1016/j.parint.2010.06.005

    Article  CAS  PubMed  Google Scholar 

  • Reite OB (1996) The mast cell nature of granule cells in the digestive tract of the pike, Esox lucius: similarity to mammalian mucosal mast cells and globule leucocytes. Fish Shellfish Immunol 6:363–369

    Article  Google Scholar 

  • Santos CM, Duarte S, Souza TGL, Ribeiro TP, Sales A, Araujo FG (2007) Histology and histochemical characterization of the digestive tract of Pimelodus maculates (Pimelodidae; Siluriformes) in Funil reservoir, Rio de Janeiro, Brazil. Iheringia Série Zoo 97:411–417

    Article  Google Scholar 

  • Sarasquete C, Gisbert E, Ribeiro L, Vieira L, Dinis MT (2001) Glycoconjuates in epidermal, branchial and digestive mucous cells and gastric glands of gilthead sea bream, Sparus aurata, Senegal sole, Solea senegalensis and Siberian sturgeon, Acipenser baeri development. Eur J Histochem 45:267–278

    Article  CAS  PubMed  Google Scholar 

  • Sato H, Ohwada S, Hoshino T (1991) Lectin histochemistry on esophageal mucosa of pigs. Tohoku J Agric Res 42:1–8

    Article  Google Scholar 

  • Scillitani G, Liquori GE, Mastrodonato M, Ferri D (2008) Histochemical and immunohistochemical characterization of exocrine cells in the foregut of the red-eared slider turtle, Trachemys scripta (Emydidae). Archives Histol Cytol 71:279–290

    Article  CAS  Google Scholar 

  • Sibbing FA, Uribe R (1985) Regional specialization in the oro-pharyngeal wall and food processing in carp (Cyrpinus carpio L). Neth J Zool 35:377–422

    Article  Google Scholar 

  • Spicer SS (1965) Diamine methods for differentiating mucosubstances histochemically. J Histochem Cytochem 13:211–234

    Article  CAS  PubMed  Google Scholar 

  • Takiue S, Akiyoshi H (2013) Light and scanning electron microscope examination of the digestive tract in Peppered moray eel, Gymnothorax pictus (Elopomorpha). Anat Rec 296:443–451. doi:10.1002/ar.22652

    Article  Google Scholar 

  • Tibbetts IR (1997) The distribution and function of mucous cells and their secretions in the alimentary tract of Arramphus sclerolepis krefftii. J Fish Biol 50:809–820

    Google Scholar 

  • Wolczuk K, Nowakowska J, Plachocki D, Kakareko T (2014) Histological, histochemical and ultrastructural analysis reveals functional division of the oesophagogasteric segment i freshwater tubenose goby Proterorhinus semilunaris Heckel, 1837. Zoomorphol. doi:10.1007/s00435-014-0250-7

    Google Scholar 

  • Wootton RJ, Smith C (2015) Reproductive biology of teleost fishes. Wiley-Blackwell, Chichester

    Google Scholar 

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Correspondence to Ingvar Leiv Leknes.

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Communicated by A. Schmidt-Rhaesa.

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Leknes, I.L. Mucin in epithelial cells in oesophagus and stomach of black tetra, Gymnocorymbus ternetzi (Characidae, Teleostei). Zoomorphology 134, 269–277 (2015). https://doi.org/10.1007/s00435-015-0256-9

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