Distribution and relative frequency of immunohistochemically detected endocrine cells in the stomach of New Zealand White rabbit (Oryctolagus cuniculus)

Document Type: Full paper (Original article)

Authors

1 Department of Biology, Faculty of Science and Art, Süleyman Demirel University, 32260, Isparta, Turkey

2 Department of Biology, Faculty of Science and Art, Mehmet Akif Ersoy University, 15100, Burdur, Turkey

Abstract

Background: Gastrointestinal (GI) endocrine cells produce many GI hormones that perform various physiological functions of the digestive system. Aims: We aimed to investigate the presence and distribution of immunoreactive (IR) endocrine cells to glucagon, somatostatin, cholecystokinin-8 (CCK-8), serotonin, secretin and histamine in the stomach of adult male New Zealand White rabbit (Oryctolagus cuniculus). Methods: For immunohistochemical staining, peroxidase anti-peroxidase (PAP) method was applied to stomach samples. Results: Glucagon-IR cells of closed- and open type were found throughout all the stomach parts examined. Somatostatin-IR cells of closed- and open type in the cardiac and oxyntic glands were localized to deep portions of foveola gastrica. CCK-8 IR cells that were not observed in the cardia and fundus were mostly localized to the glands and lamina epithelialis in the pyloric part near the duodenum. Oval-shaped open and closed type serotonin-IR cells were mostly dispersed throughout the fundic and pyloric glands. Secretin-IR cells were rare in the pyloric and cardiac region although they were not observed in the fundic glands. Histamine-IR cells were rarely found in the cardia, fundus and pylorus. Conclusion: Our findings show that glucagon, histamine, somatostatin, secretin and serotonin might be produced by all the stomach regions while pyloric region had only CCK-8 IR. These distribution patterns also provide further evidence of species-specific differences, which might be important from the evolutionary aspect of the digestive tract in relation to evolutional niches and nutrient resources.

Keywords


Adnyane, IK; Zuki, AB; Noordin, MM and Agungpriyono, S (2011). Immunohistochemical study of endocrine cells in the gastrointestinal tract of the Barking deer, Muntiacus muntjac. Anat. Histol. Embryol., 40: 365-374.

Agungpriyono, S; Macdonald, A; Leus, KY; Kitamura, N; Adnyane, IK; Goodall, GP; Hondo, E and Yamada, J (2000). Immunohistochemical study on the distribution of endocrine cells in the gastrointestinal tract of the babirusa, Babyrousa babyrussa (Suidae). Anat. Histol. Embryol., 29: 173-178.

Agungpriyono, S; Yamada, J; Kitamura, N; Yamamoto, Y; Said, N; Sigit, K and Yamasita, T (1994). Immuno-cytochemical study of the distribution of endocrine cells in the gastrointestinal tract of the lesser mouse deer (Tragulus javanicus). Acta Anat., 15: 232-238.

Arena, PC; Richardson, KC and Yamada, J (1990). An immunohistochemical study of endocrine cells of the alimentary tract of the king’s skink (Egernia kingii). J. Anat., 170: 73-85.

Baltazar, ET; Kitamura, N; Hondo, E; Yamada, J; Mala, CP and Simborio, LT (1998). Immunohistochemical study of endocrine cells in the gastrointestinal tract of the Philippine carabao (Bubalus bubalis). Anat. Histol. Embryol., 27: 407-411.

Bell, FR (1979). The relevance of the new knowledge of gastrointestinal hormones to veterinary science. Vet. Sci. Commun., 2: 305-314.

Beyaz, F; Liman, N; Ergün, E; Ergün, L and Özbek, M (2017). Intestinal macrophages in Peyer’s patches, sacculus rotundus and appendix of Angora rabbit. Cell. Tissue. Res., 370: 285-295.

Budipitojo, T; Fibrianto, YH and Mulyani, GT (2016). Gut endocrine cells in the stomach of Sunda Porcupines (Hystrix javanica). Asian J. Anim. Sci., 10: 268-272.

Castaldo, L and Lucini, C (1991). An immunohistochemical study on the endocrine cells in the gastrointestinal tract of domestic duck. Eur. J. Basic. Appl. Histochem., 35: 131-143.

Dall’aglio, C; Scocco, P; Ceccakelli, P and Pedini, V (1998). Neuroendocrine cells in the gastrointestinal tract of wild boar. Anat. Histol. Embryol., 27: 381-385.

D’Este, L; Buffa, R and Renda, T (1994). Phylogenetic aspects of the occurrence and distribution of secretogranin II immunoreactivity in lower vertebrate gut. Arch. Histol. Cytol., 57: 235-252.

Fan, L and Iseki, S (1999). Immunohistochemical localization of vascular endothelial growth factor in the globule leukocyte/mucosal mast cell of the rat respiratory and digestive tracts. Histochem. Cell. Biol., 111: 13-21.

Firmiano, EMS; Cardoso, NN; Sales, A; Santos, MAJ; Mendes, ALS and Nascimento, AA (2017). Immuno-histochemical study of the six types of endocrine cells in the enteropancreatic system of the lizard Tropidurus torquatus (Squamata:Tropiduridae). Eur. Zool. J., 84: 266-276.

Hakanson, R; Böttcher, G; Ekblad, E; Panula, P; Simonsson, M; Dohlsten, M; Halberg, T and Sundler, F (1986). Histamine in endocrine cells in the stomach. Histochemistry. 86: 5-17.

Kitamura, N; Yamada, J; Watanabe, T and Yamashita, T (1990). An immunohistochemical study on the distribution of endocrine cells in the gastrointestinal tract of the musk shrew, Suncus murinus, Histol. Histopathol., 5: 83-88.

Krause, J; Yamada, J and Cutts, JH (1985). Quantitative distribution of enteroendocrine cells in the gastrointestinal tract of the adult opossum, Didelphis virginiana. J. Anat., 140: 591-605.

Ku, SK; Lee, HS and Lee, JH (2003). An immuno-histochemical study of the gastrointestinal endocrine cells in the C57BL/6 mice. Anat. Histol. Embryol., 32: 21-28.

Ku, SK; Lee, HS and Lee, JH (2004). An immuno-histochemical study of the gastroin-testinal endocrine cells in the BALB/c mouse. Anat. Histol. Embryol., 33: 42-48.

Ku, SK; Lee, HS and Lee, JH (2006). The regional distribution and relative frequency of gastrointestinal endocrine cells in the nude mice, Balb/c-nu/nu: an immunohistochemical study. Anat. Histol. Embryol., 35: 104-110.

Ku, SK; Lee, HS; Lee, JH and Park, KD (2001). An immunohistochemical study on the endocrine cells in the alimentary tract of the red-eared slider (Trachemys scripta elegans). Anat. Histol. Embryol., 30: 33-39.

Ku, SK; Lee, JH; Lee, HS and Park, KD (2002). The regional distribution and relative frequency of gastrointestinal endocrine cells in SHK-1 hairless mice: an immunohistochemical study. Anat. Histol. Embryol., 31: 78-84.

Lee, HS; Choi, SH and Ku, SK (2010). Regional distribution and relative frequency of gastrointestinal endocrine cells in the ddN mice: an immunohistochemical study. Anat. Histol. Embryol., 39: 521-528.

Lee, HS; Hashimoto, Y; Kon, Y and Sugimura, M (1991). An immunohistochemical study of the gastro-entero-pancreatic endocrine cells in the alimentary tract of the Korean tree squirrel, Sciurus vulgaris corea. Jpn. J. Vet. Res., 39: 117-131.

Lee, HS and Ku, SK (2004). An immunohistochemical study of endocrine cells in the alimentary tract of the grass lizard, Takydromus wolteri Fischer (Laceridae). Acta Histochem., 106: 171-178.

Lee, HS; Ku, SK and Lee, JH (1998). Localization of endocrine cells in the gastrointestinal tract of the Manchurian chipmunk, Tamias sibiricus barberi. Korean J. Biol. Sci., 2: 395-401.

Lee, JE; Lee, HS; Choi, SH and Ku, SK (2014). The regional distribution and frequency of endocrine cells in the Korean golden frog, Rana plancyi chosenica: an immuno-histochemical study. Anim. Cells Syst., 18: 250-258.

Lee, JH; Lee, HS; Ku, SK; Park, KD and Kim, KS (2000). Immunohistochemical study of the gastrointestinal endocrine cells in the Mongolian gerbils, Meriones unguiculatus. Korean J. Vet. Sci., 40: 653-660.

Mimoda, T; Kitamura, N; Hondo, E and Yamada, J (1998). Immunohistochemical colocalization of serotonin, substance P and met-enkephalin-Arg6-Gly7-Leu8 in the endocrine cells of the ruminant duodenum. Anat. Histol. Embryol., 27: 65-69.

Nisa, C; Kitamura, N; Sasaki, M; Agungpriyono, S; Choliq, C; Budipitojo, T; Yamada, J and Sigit, K (2005). Immunohistochemical study on the distribution and relative frequency of endocrine cells in the stomach of the Malayan Pangolin, Manis javanica. Anat. Histol. Embryol., 34: 373-378.

Özbek, M; Ergün, E; Beyaz, F; Ergün, L; Özgenç, Ö and Erhan, F (2018). Prenatal development and histochemical characteristics of gastrointestinal mucins in sheep fetuses. Microsc. Res. Tech., 81: 630-648.

Öztop, M; Cinar, K and Turk, S (2018). Immunolocalization of natriuretic peptides and their receptors in goat (Capra
hircus
) heart. Biotech Histochem. 93(6):389-404.

Santos, CM; Nascimento, AA; Peracchi, AL; Sales, A; Mikalauskas, JS and Gouveia, SF (2008). Immuno-cytochemical study of gastrintestinal endocrine cells in insectivorous bats (Mammalia: Chiroptera). Braz. J. Biol., 68: 663-669.

Solcia, E; Capella, C; Vassallo, G and Buffa, R (1975). Endocrine cells of the gastric mucosa. Int. Rev. Cytol., 42: 223-286.

Tahara, A; Nishibori, M; Ohtsuka, A; Sawada, K; Sakiyama, J and Saeki, K (2000). Immunohistochemical localization of histamine N-methyltransferase in guinea pig tissues. J. Histochem. Cytochem., 48: 943-954.

Timurkaan, S; Karan, M and Aydın, A (2005). Immuno-histochemical study of the distribution of serotonin in the gastrointestinal tract of the porcupines (Hystrix cristata). Rev. Vet. Med., 156: 533-536.

Timurkaan, S; Timurkaan, N; Ozkan, T and Girgin, M (2009). Immunohistochemical distribution of somatostatin, glucagon and gastrin in the gastric fundus of the Citellus (Spermophilus xanthoprymnus). J. Anim. Vet. Adv., 8: 2210-2214.

Vieira-Lopes, DA; Pinheiro, NL; Sales, A; Ventura, A; Araújo, FG; Gomes, ID and Nascimento, AA (2013). Immunohistochemical study of the digestive tract of Oligosarcus hepsetus. World J. Gastroenterol., 19: 1919-1929.

Yamada, J; Tauchi, M; Rerkamnuaychoke, W; Endo, H; Chungsamarnyart, N; Kimura, J; Kurohmaru, M; Hondo, E; Kitamura, N; Nishida, T and Hayashi, Y (1999). Immunohistochemical survey of the gut endocrine cells in the common tree shrew (Tupaia belangeri). J. Vet. Med. Sci., 61: 761-767.

Yaman, M; Tarakçi, G; Bayrakdar, B; Atalar, A and Dabak, O (2007). Immunohistochemical study of gastrointestinal endocrine cells in the Porcupine (Hystrix cristata). Rev. Med. Vet., 158: 196-200.