Abstract
In order to replace the diffusive loss of water to the surrounding environment, seawater (SW)-acclimated euryhaline fishes have gastrointestinal tracts with higher ion/water flux in concert with greater permeability, and contrast that to freshwater (FW)-acclimated fish. To understand the cellular basis for these differences, we examined cell proliferation and apoptosis in the anterior intestine of mudskipper transferred from one-third SW to FW or to SW for 1 and 7 days, and those kept out of water for 1 day. The intestinal apoptosis (indicated by DNA laddering) increased during seawater acclimation. TUNEL staining detected numerous apoptotic cells over the epithelium of SW-acclimated fish. Cell proliferation ([3H]thymidine incorporation) in the FW fish was greater than those in SW 7 days after transfer. Labeling with a Proliferating cell nuclear antigen (PCNA) antibody indicated that proliferating cells were greater in number and randomly distributed in the epithelium of FW fish, whereas in SW fish they were almost entirely in the troughs of the intestinal folds. There were no changes in cell turnover in fish kept out of water. During acclimation to different salinities, modification of the cell turnover and abundance may play an important role in regulating the permeability (and transport capacity) of the gastrointestinal tract of fish.
Similar content being viewed by others
Abbreviations
- FW:
-
Freshwater
- PCNA:
-
Proliferating cell nuclear antigen
- SW:
-
Seawater
References
Aoki M, Kaneko T, Katoh F, Hasegawa S, Tsutsui N, Aida K (2003) Intestinal water absorption through aquaporin 1 expressed in the apical membrane of mucosal epithelial cells in seawater-adapted Japanese eel. J Exp Biol 206:3495–3505
Baserga R (1991) Growth regulation of the PCNA gene. J Cell Sci 98:433–436
Bentley PJ (2002) Endocrines and Osmoregulation. In: Zoophysiology, vol 39. Springer, Berlin Heidelberg New York
Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. III. Evidence from columnar, enteroendocrine, and mucous cells in the adult mouse. Am J Anat 160:77–91
Bravo R, Macdonald-Bravo H (1987) Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. J Cell Biol 105:1549–1554
Brunk U, Schellens J, Westermark B (1977) Influence of epidermal growth factor (EGF) on ruffling activity, pinocytosis and proliferation of cultivated human glia cells. Exp Cell Res 103:295–302
Cheng H, Leblond CP (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat 141:503–519
Cutler CP, Brezillon S, Bekir S, Sanders IL, Hazon N, Cramb G (2000) Expression of a duplicate Na, K-ATPase beta(1)-isoform in the European eel (Anguilla anguilla). Am J Physiol Regul Integr Comp Physiol 279:222–229
Cutler CP, Cramb G (2001) Molecular physiology of osmoregulation in eels and other teleosts: the role of transporter isoforms and gene duplication. Comp Biochem Physiol A 130:551–564
Frankfurt O, Rosen ST (2004) Mechanisms of glucocorticoid-induced apoptosis in hematologic malignancies: updates. Curr Opin Oncol 16:553–563
Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493–501
Gordon MS, Ng WW, Yip AY (1978) Aspects of the physiology of terrestrial life in amphibious fishes. III. The Chinese mudskipper Periophthalmus cantonensis. J Exp Biol 72:57–75
Hirano T (1986) The spectrum of prolactin action in teleosts. Prog Clin Biol Res 205:53–74
Hirano T (1991) Endocrine control of osmoregulation in migratory fishes. In: Mauchline J, Nemoto T (eds) Marine Biology. Hakusen-sha, Tokyo, pp 3–14
Hirano T, Mayer-Gostan N (1976) Eel esophagus as an osmoregulatory organ. Proc Nat Acad Sci USA 73:1348–1350
Ishizuya-Oka A, Shimozawa A (1991) Induction of metamorphosis by thyroid hormone in anuran small intestine cultured organotypically in vitro. In Vitro Cell Dev Biol 27:853–857
Ishizuya-Oka A, Ueda S (1996) Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res 286:467–476
Iwata K, Kajimura M, Sakamoto T (2000) Functional ureogenesis in the gobiid fish, Mugilogobius abei. J Exp Biol 203:3703–3715
Karnaky KJ Jr (1998) Osmotic and ionic regulation. In: Evans DH (ed) The physiology of fishes, 2nd edn. CRC Press, New York, pp 157–176
Kirsch R, Meister MF (1982) Progressive processing of ingested water in the gut of seawater teleosts. J Exp Biol 98:67–81
Lee CG, Ip YK (1987) Environmental effect on plasma thyroxin (T4), 3,5,3’-triido-L-thyronine (T3), prolactin and cyclic adenosine 3’,5’-monophosphate (cAMP) content in the mudskippers Periophthalmus chrysospilos and Boleophthalmus boddaerti. Comp Biochem Physiol 87:1009–1014
Loretz CA (1995) Electrophysiology of ion transport in teleost intestinal cells. In: Wood CM, Shuttleworth TJ (eds) Cellular and molecular approaches to fish ionic regulation. Academic Press, San Diego,NY, pp 25–56
Mackay WC, Janick R (1979) Changes in the eel intestine during seawater adaptation. Comp Biochem Physiol 62:757–761
Manzon LA (2002) The role of prolactin in fish osmoregulation: a review. Gen Comp Endocrinol 125:291–310
Marshall WS, Singer TD (2002) Cystic fibrosis transmembrane conductance regulator in teleost fish. Biochim Biophys Acta 1566:16–27
McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794
Morley M, Chadwick A, El Tounsy EM (1981) The effect of prolactin on water absorption by the intestine of the trout (Salmo gairdneri). Gen Comp Endocrinol 44:64–68
Nishikawa A, Yoshizato K (1986) Hormonal regulation of growth and life span of bullfrog tadpole tail epidermal cells cultured in vitro. J Exp Zool 237:221–230
Oide M (1967) Effects of inhibitors on transport of water and ion in isolated intestine and Na+-K+ ATPase in intestinal mucosa of the eel. Annot Zool Jpn 40:130–135
Oide H, Utida S (1967) Changes in water and ion transport in isolated intestines of the eel during salt adaptation and migration. Mar Biol 1:102–106
Oide H, Utida S (1968) Changes in intestinal absorption and renal excretion of water during adaptation to seawater in the Japanese eel. Mar Biol 1:172–177
Reichardt HM (2004) Immunomodulatory activities of glucocorticoids: insights from transgenesis and gene targeting. Curr Pharm 10:2797–2805
Sakamoto T, Yasunaga H, Yokota S, Ando M (2002) Differential display of skin mRNAs regulated under varying environmental conditions in a mudskipper. J Comp Physiol B 172:447–453
Sakamoto T, Amano M, Hyodo S, Moriyama S, Takahashi A, Kawauchi H, Ando M (2005a) Expression of prolactin-releasing peptide and prolactin in the euryhaline mudskippers (Periophthalmus modestus): prolactin-releasing peptide as a primary regulator of prolactin. J Mol Endocrinol 34:825–834
Sakamoto T, Oda A, Narita K, Takahashi H, Oda T, Fujiwara J, Godo W (2005b) Prolactin: fishy tales of its primary regulator and function. Ann NY Acad Sci 1040:184–188
Santos-Ruiz L, Santamaria JA, Ruiz-Sanchez J, Becerra J (2002) Cell proliferation during blastema formation in the regenerating teleost fin. Dev Dyn 223:262–272
Schettino T, Lionetto MG (2003) Cl- absorption in European eel intestine and its regulation. J Exp Zoolog A 300:63–68
Smith HW (1930) The absorption and excretion of water and salts by marine teleosts. Am J Physiol 93:480–505
Sturm A, Bury N, Dengreville L, Fagart J, Flouriot G, Rafestin-Oblin ME, Prunet P (2005) 11-deoxycorticosterone is a potent agonist of the rainbow trout (Oncorhynchus mykiss) mineralocorticoid receptor. Endocrinology 146:47–55
Suzuki Y, Itakura M, Kashiwagi M, Nakamura N, Matsuki T, Sakuta H, Naito N, Takano K, Fujita T, Hirose S (1999) Identification by differential display of a hypertonicity-inducible inward rectifier potassium channel highly expressed in chloride cells. J Biol Chem 274:11376–11382
Takahashi H, Sakamoto T, Hyodo S, Shepherd BS, Kaneko T, Grau EG (2005) Expression of glucocorticoid receptor in the intestine of a euryhaline teleost, the Mozambique tilapia (Oreochromis mossambicus): effect of seawater exposure and cortisol treatment. DOI 10.1016/j.lfs.2005.09.050.tr.
Tanuma S, Siokawa D, Tanimoto Y, Ikekita M, Sakagami H, Takeda M, Fukuda S, Kochi M (1993) Benzylideneascorbate induces apoptosis in L929 tumor cells. Biochem Biophys Res Commun 194:29–35
Tata JR (1993) Gene expression during metamorphosis: an ideal model for post-embryonic development. Bioessays 15:239–248
Veillette PA, White RJ, Specker JL (1993) Changes in intestinal fluid transport in Atlantic salmon (Salmo salar L) during parr-smolt transformation. Fish Physiol Biochem 12:193–202
Weyts FA, Flik G, Rombout JH, Verburg-van Kemenade BM (1998) Cortisol induces apoptosis in activated B cells, not in other lymphoid cells of the common carp, Cyprinus carpio L. Dev Comp Immunol 22:551–562
Yamamoto M, Hirano T (1978) Morphological changes in the esophageal epithelium of the eel, Anguilla japonica, during adaptation to seawater. Cell Tissue Res 192:25–38
Acknowledgments
We thank Drs. Masaaki Ando and Akira Kawahara for valuable discussions and guidance. We also thank Drs. Stephen D. McCormick and Michelle Y. Monette for critical reading the manuscript. This work was supported in part by grants-in-aid for scientific research from the Ministry of Education and the Fisheries Agency of Japan. The experimental work was carried out in accordance with Guidelines for Animal Experimentation of Okayama University complied with the current lows of Japan.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume
Rights and permissions
About this article
Cite this article
Takahashi, H., Sakamoto, T. & Narita, K. Cell proliferation and apoptosis in the anterior intestine of an amphibious, euryhaline mudskipper (Periophthalmus modestus) . J Comp Physiol B 176, 463–468 (2006). https://doi.org/10.1007/s00360-006-0067-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-006-0067-x