Morphological and Histochemical Investigations of Esophagogastric Tract of a Lizard, Laudakia stellio (Agamidae, Linnaeus 1758)

Abstract

Histological structures of esophagus and stomach tissue samples of Lacerta stellio have been studied, and glycosaminoglycan (GAG) distribution has been histochemically determined. Histologically, esophagus and stomach of L. stellio are composed of four layers: mucosa, submucosa, muscularis mucosae and serosa. Mucosa of esophagus is covered by simple columnar ciliated epithelium with many mucous secreting goblet cells and contains branched tubular glands.

Stomach of L. stellio is composed of fundus (oral and aboral) and pylorus regions. Mucosa is covered by columnar epithelium. Fundic glands are branched tubular glands while pyloric glands are usually simple tubular glands. In both regions of the stomach, glands are subdivided into three areas as base, neck and isthmus. Both in the esophagus and stomach, muscular layer is in the form of smooth muscle having inner circular and outer longitudinal layers.

According to the results obtained by Alcian Blue (pH 5.8)/Periodic Acid Schiff staining, stomach is similar to esophagus in that neutral mucins and hyaluronic acid (HA) are dominant in isthmus and neck regions of gland tissue of stomach. In the base of the stomach, only neutral mucins have been observed. HA has been observed to be dominant in all other regions of both stomach and esophagus, along with some but not much sulphated GAGs.

References

  1. 1.

    Ahmed, Y. A., El-Hafez, A. A. E., Zayed, A. E. (2009) Histological and histochemical studies on the esophagus, stomach and small intestines of Varanus niloticus. J. Vet. Anat. 2, 35–48.

    Article  Google Scholar 

  2. 2.

    Allen, A., Flemström, G. (2005) Gastroduodenal mucus bicarbonate barrier: protection against acid and pepsin. Am. J. Physiol. Cell Physiol. 288, C1–C19.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. 3.

    Arellano, J. M., Storch, V., Sarasquete, C. (2002) Ultrastructural study on the intestine of Senegal sole, Solea senegalensis. J. Appl. Ichthyol. 18, 154–158.

    Article  Google Scholar 

  4. 4.

    Aughey, E., Frye, L. F. (2001) Comparative Veterinary Histology. Manson Publishing Ltd., pp. 105–107.

    Book  Google Scholar 

  5. 5.

    Bancroft, J. D., Cook, H. C. (1994) Manual of Histological Techniques and Their Diagnostic Application. Churchill Livingstone. London, p. 457.

    Google Scholar 

  6. 6.

    Bansil, R., Turner, B. S. (2006) Mucin structure, aggregation, physiological functions and biomedical applications. Current Opinion in Colloid & Interface Science 11, 164–170.

    CAS  Article  Google Scholar 

  7. 7.

    Domeneghini, C., Ponnelli, R. S., 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  PubMed Central  Google Scholar 

  8. 8.

    Domeneghini, C., Arrighi, S., Radaelli, G., Bosi, G., Veggetti, A. (2005) Histochemical analysis of glycoconjugate secretion in the alimentary canal Anguilla anguilla L. Acta Histochem. 106, 477–487.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. 9.

    Ezeasor, D. N. (1984) Light and electron microscopic studies on the esophageal epithelium of the Rainbow Trout, Salmo gairdneri. Anat. Anz. 155, 71–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Ferri, D., Liquori, G. E. (1994) Immunohistochemical investigations on the pyloric glands of the ruin lizard (Podarcis sicula campestris de Betta). Acta Histochem. 96, 96–103.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 11.

    Ferri, D., Liquori, G. E., Natale, L., Santarelli, G., Scillitani, G. (2001) Mucin histochemistry of the digestive tract of the red-legged frog Rana aurora aurora. Acta Histochem. 103, 225–237.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

    Ferri, D., Liquori, G. E. (1992) Characterization of secretory cell glycoconjugates in the alimentary tract of the ruin lizard (Podarcis sicula campestris de Betta) by means of lectin histochemistry. Acta Histochem. 93, 341–349.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Gabe, M., Saint-Girons, H. (1972) Contribution al’histologie de l’estomac des lepidossauriens (Reptilis). Zool. Jb. 89, 572–599.

    Google Scholar 

  14. 14.

    Gandhi, N. S., Mancera, R. L. (2008) The structure of glycosaminoglycans and their interaction with proteins. Chem. Biol. Drug Des. 72, 455–482.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Geyikoglu, F., Temelli, A., Ozkaral, A. (2002) Muscle fiber types of the tunica muscularis externa at the upper part of the sparrow (Passer domesticus) esophagus. Turk. J. Zool. 26, 217–221.

    Google Scholar 

  16. 16.

    Goldstein, C. D., Jankiewicz, J. J., Desmond, M. E. (1986) Identification of glycosaminoglycans in the chondrocranium of the chick embryo before and at the onset of chondrogenesis. J. Embryol. Exp. Morphol. 93, 29–49.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Humbert, W. R., Kirsch, R., Meister, M. F. (1984) Scanning electron microscopic study of the oesophageal mucous layer in the eel, Anguilla anguilla L. J. Fish Biol. 25, 117–122.

    Article  Google Scholar 

  18. 18.

    Imai, M., Shibata, T., Izumi, T. (1992) Histological and histochemical investigations on Japanese lizard esophagus. Okajimas Folia Anat. Jpn. 69, 25–34.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Imai, M., Shibata, T., Moriguchi, K. (1991) Pepsinogen granules in the esophageal epithelium of the rock snake. Okajimas Folia Anat. Jpn. 68, 231–234.

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Imai, M., Shibata, T., Moriguchi, K., Hayama, H. (1991) Glands distributed in the lamina propria mucosae of the oesophagus in the gecko and Japanese lizard. Okajimas Folia Anat. Jpn. 68, 289–293.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Ingelfinger, F. J. (1958) Esophageal motility. Physiol. Rev. 38, 533–584.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    Liquori, G. E., Mastrodonato, M., Zizza, S., Ferri, D. (2007) Glycoconjugate histochemistry of the digestive tract of Triturus carnifex (Amphibia, Caudata). J. Mol. Hist. 38, 191–199.

    CAS  Article  Google Scholar 

  23. 23.

    Loumbourdis, N. S. (2003) Mucosubstance histochemistry in the esophagus of the lizard Agama stellio stellio. Amphibia-Reptilia 24, 224–229.

    Article  Google Scholar 

  24. 24.

    Lupa, H. (1977) Histology of the digestive tract. In: Gans, C., Parsons, T. S. (ed.). Biology of the Reptilia. Academic Press, London, pp. 225–302.

    Google Scholar 

  25. 25.

    Morrison, C. M., Wright, J. R. (1999) A study of the histology of the digestive tract of the Nile tilapia. J. Fish Biol. 54, 597–606.

    Article  Google Scholar 

  26. 26.

    Oinuma, T., Kawano, J. I., Suganuma T. (1991) Glycoconjugate histochemistry of Xenopus laevis fundic gland with special reference to mucouse neck cells during development. Anat. Rec. 230, 502–512.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Pedini, V., Dall’Aglio, C., Parillo, F., Scocco, P. (2004) A lectin histochemical study of the oesophagus of shi drum. J. Fish Biol. 64, 625–631.

    Article  Google Scholar 

  29. 29.

    Prabhakar, V., Capila, I., Sasisekharan, R. (2009) Glycosaminoglycan characterization methodologies: probing biomolecular interactions. Meth. Mol. Biol. 534, 331–340.

    CAS  Google Scholar 

  30. 30.

    Russell, A. L. (1999) Glycosaminoglycan (GAG) deficiency in protective barrier as an underlying, primary cause of ulcerative colitis, Crohn’s disease, interstitial cystitis and possibly Reiter’s syndrome. Medical Hypothesis 52, 297–301.

    CAS  Article  Google Scholar 

  31. 31.

    Sancar-Bas, S., Kaptan, E., Sengezer-Inceli, M., Sezen, A., Us, H. (2009) Glycoconjugate histochemistry in the Fundic stomach and small intestine of the frog (Rana ridibunda). IUFS J. Biol. 68, 93–104.

    Google Scholar 

  32. 32.

    Sartori, S. S. R., Nogueira, K. O. P. C., Rocha, A. S. R., Neves, C. A. (2010) Morphology of the stomach of the tropical house gecko Hemidactylus mabouia (Squamata: Gekkonidae). Acta Zoologica, 1–8.

    Google Scholar 

  33. 33.

    Scott, J. E. (1996) Alcian blue. Now you see it, now you don’t. Eur. J. Oral Sci. 104, 2–9.

    CAS  Article  Google Scholar 

  34. 34.

    Selvan, P. S., Ushakumary, S., Ramesh, G. (2008) Studies on the histochemistry of the proventriculus and gizzard of post-hatch guinea fowl (Numida meleagris). Inter. J. Poultry Scien. 7, 1112–1116.

    Article  CAS  Google Scholar 

  35. 35.

    Sheahan, D. G., Jervis, H. R. (1976) Comparative histochemistry of gastrointestinal mucosubstances. Am. J. Anat. 146, 103–131.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. 36.

    Smith, L. S. (1989) Digestive functions in teleost fish. In: J. E. Halvert (ed.), Fish Nutrition Academic Press, San Diego, pp. 331–421.

    Google Scholar 

  37. 37.

    Starck, J. M., Beese, K. (2002) Structural flexibility of the small intestine and liver of garter snakes in response to feding and fasting. J. Exp. Biol. 205, 1377–1388.

    PubMed  PubMed Central  Google Scholar 

  38. 38.

    Suganuma, T., Katsuyama, T., Tsukahara, M., Tatematsu, M., Sakakura, Y., Murata, F. (1981) Comparative histochemical study of alimentary tracts with special reference to the mucous neck cell of the stomach. Am. J. Anat. 161, 219–238.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  39. 39.

    Suprasert, A., Fujioka, T., Yamad, K. (1987) The histochemistry of glycoconjugates in the colonic epithelium of the chicken. Histochemistry 86, 491–497.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. 40.

    Suzuki, S., Mizutani, A., Koike, Y., Kato, M., Yoshida, K., Kimata, K. (1991) Glycosaminoglycan chains of proteoglycans: approaches to the study of their structure and function. Pure Appl. Chem. 63, 545–554.

    CAS  Article  Google Scholar 

  41. 41.

    Taylor, P. M., Tyler, M. J. (1986) Pepsin in the toad Bufo marinus. Comp. Biochem. Physiol. 84, 669–672.

    CAS  Article  Google Scholar 

  42. 42.

    Tuckett, F., Morris-Kay, G. (1988) Alcian blue staining of glycosaminoglycans in embrionic material: Effect of different fixatives. Histochem. J. 20, 174–182.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  43. 43.

    Uriona, T. J., Farmer, C. G., Dazely, J., Clayton, F., Moore, J. (2005) Structure and function of the esophagus of the American alligator (Alligator mississippiensis). J. Exp. Biol. 208, 3047–3053.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. 44.

    Ünal, G., Çetinkaya, O., Kankaya, E., Elp, M. (2001) Histological study of the organogenesis of the digestive system and swim bladder of the Chalcalburnus tarichi Palas, 1811 (Cyprinidae). Turk. J. Zool. 25, 217–228.

    Google Scholar 

  45. 45.

    Yamabayashi, S. (1987) Periodic acid-Sciff-Alcian blue: A method for the differential staining of glycoproteins. Histochem. J. 19, 565–571.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. 46.

    Yoshida, M. (2001) A light microscope study of the distribution of muscle in the frog esophagus and stomach. J. Smooth Muscle Res. 37, 95–104.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yücel Başımoğlu Koca.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Cite this article

Başımoğlu Koca, Y., Gürcü, B. Morphological and Histochemical Investigations of Esophagogastric Tract of a Lizard, Laudakia stellio (Agamidae, Linnaeus 1758). BIOLOGIA FUTURA 62, 376–387 (2011). https://doi.org/10.1556/ABiol.62.2011.4.4

Download citation

Keywords

  • Histology
  • histochemistry
  • esophagus
  • stomach
  • L. stellio