Aquaporin 8 mRNA expression after intestinal resection in rat

Yu Koyama, Hitoshi Kameyama, Jun Sakata, Takashi Kobayashi, Masahiro Minagawa, Shin-ichi Kosugi, Tadashi Yamamoto, Kohei Akazawa, Toshifumi Wakai

Department of Medical Informatics, Niigata University Graduate School of Medical & Dental Sciences, Niigata, Japan.
Department of Renal Pathology, Institute of Nephrology, Niigata University Graduate School of Medical & Dental Sciences, Niigata, Japan.
Division of Digestive & General Surgery, Niigata University Graduate School of Medical & Dental Sciences, Niigata, Japan.

DOI: 10.4236/ojgas.2014.42011                

Abstract

Backgrounds: Aquaporins (AQPs), the mammalian water channels, have been localized in various organs, including the gastrointestinal (GI) tract. We examined AQPs expression in rat models of massive intestineal resection to determine the functions of AQPs in the GI tract. Methods: Female Sprague-Dawley rats (n = 15) underwent 90% resection of the small intestine, and Female Wistar-Kyoto rats (n = 10), received subtotal colectomy, and were sacrificed following the operations. RNase protection assay and quantitative reverse transcription-polymerase chain reaction (RT-PCR) were performed to measure the AQPs mRNA expression in the GI tract. Immunohistochemistry was performed to confirm AQP8 protein expression. Results: AQP8 mRNA expression (mean ± standard error), was enhanced in the jejunum of the short bowel rats at days 7 and 14 (37.6% ± 1.4% and 18.5% ± 2.4%, respectively, p < 0.01). Enhancement of AQP8 mRNA was also observed in the remnant rectum of the subtotal colectomized rats at both days 21 and 42 (116.1% ± 4.5% and 143.3% ± 7.4%, respectively, p < 0.01). Immunohistochemistry demonstrated enhanced AQP8 expression in the remnant rectum of the subtotal colectomized rats. No intensive change was observed with other AQPs in both models. Conclusions: Our results suggest a compensatory role of AQP8 in the maintenance of intestinal fluid balance.

Keywords

Aquaporin 8; Short Bowel; Subtotal Colectomy; RNase Protection Assay; QuantitativeRT-PCR

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	King, L.S. and Agre, P. (1996) Pathophysiology of the aquaporin water channels. Annual Review of Physiology, 58, 619-648. http://dx.doi.org/10.1146/annurev.ph.58.030196.003155
[2]	Preston, G.M., Carroll, T.P., Guggino, W.B. and Agre, P. (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science, 256, 385-387. http://dx.doi.org/10.1126/science.256.5055.385
[3]	Fushimi, K., Uchida, S., Hara, Y., Hirata, Y., Marumo, F. and Sasaki, S. (1993) Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature, 361, 549-552. http://dx.doi.org/10.1038/361549a0
[4]	Ishibashi, K., Sasaki, S., Fushimi, K., Uchida, S., Kuwahara, M., Saito, H., Furukawa, T., Nakajima, K., Yamaguchi, Y., Gojobori, T. and Marumo, F. (1994) Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proceedings of the National Academy of Sciences USA, 91, 6269-6273.
[5]	Jung, J.S., Bhat, R.V., Preston, G.M., Guggino, W.B., Baraban, J.M. and Agre, P. (1994) Molecular characterization of an aquaporin cDNA from brain: Candidate osmoreceptor and regulator of water balance. Proceedings of the National Academy of Sciences USA, 91, 13052-13056.
[6]	Raina, S., Preston, G.M., Guggino, W.B. and Agre, P. (1995) Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues. Journal of Biological Chemistry, 270, 1908-1912. http://dx.doi.org/10.1074/jbc.270.4.1908
[7]	Ma, T., Yang, B., Kuo, W.L. and Verkman, A.S. (1996) cDNA cloning and gene structure of a novel water channel expressed exclusively in human kidney: Evidence for a gene cluster of aquaporins at chromosome locus 12q13. Genomicus, 35, 543-550. http://dx.doi.org/10.1006/geno.1996.0396
[8]	Ishibashi, K., Kuwahara, M., Gu, Y., Kageyama, Y., Tohsaka, A., Suzuki, F., Marumo, F. and Sasaki, S. (1997) Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. Journal of Biological Chemistry, 272, 20782-20786. http://dx.doi.org/10.1074/jbc.272.33.20782
[9]	Koyama, Y., Yamamoto, T., Kondo, D., Funaki, H., Yaoita, E., Kawasaki, K., Sato, N., Hatakeyama, K. and Kihara, I. (1997) Molecular cloning of a new aquaporin from rat pancreas and liver. Journal of Biological Chemistry, 272, 30329-30333. http://dx.doi.org/10.1074/jbc.272.48.30329
[10]	Ishibashi, K., Kuwahara, M., Gu, Y., Tanaka, Y., Marumo, F. and Sasaki, S. (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochemical and Biophysical Research Communications, 244, 268-274. http://dx.doi.org/10.1006/bbrc.1998.8252
[11]	Hatakeyama, S., Yoshida, Y., Tani, T., Koyama, Y., Nihei, K., Ohshiro, K., Kamiie, J.I., Yaoita, E., Suda, T., Hatakeyama, K. and Yamamoto, T. (2001) Cloning of a new aquaporin (aqp10) abundantly expressed in duodenum and jejunum. Biochemical and Biophysical Research Communications, 287, 814-819. http://dx.doi.org/10.1006/bbrc.2001.5661
[12]	Koyama, Y., Yamamoto, T., Tani, T., Nihei, K., Kondo, D., Funaki, H., Yaoita, E., Kawasaki, K., Sato, N., Hatakeyama, K. and Kihara, I. (1999) Expression and localization of aquaporins in rat gastrointestinal tract. American Journal of Physiology, 276, C621-C627.
[13]	Tani, T., Koyama, Y., Nihei, K., Hatakeyama, S., Ohshiro, K., Yoshida, Y., Yaoita, E., Sakai, Y., Hatakeyama, K. and Yamamoto, T. (2001) Immunolocalization of aquaporin-8 in rat digestive organs and testis. Archives of Histology and Cytololgy, 64, 159-168. http://dx.doi.org/10.1679/aohc.64.159
[14]	Berry, V., Francis, P., Kaushal, S., Moore, A. and Bhattacharya, S. (2000) Missense mutations in MIP underlie autosomal dominant ‘polymorphic’ and lamellar cataracts linked to 12q. Nauret Genetics, 25, 15-17. http://dx.doi.org/10.1038/75538
[15]	King, L.S., Choi, M., Fernandez, P.C., Cartron, J.P. and Agre, P. (2001) Defective urinary-concentrating ability due to a complete deficiency of aquaporin-1. New England Journal of Medicine, 345, 175-179. http://dx.doi.org/10.1056/NEJM200107193450304
[16]	King, L.S., Nielsen, S., Agre, P. and Brown, R.H. (2002) Decreased pulmonary vascular permeability in aquaporin-1-null humans. Proceedings of the National Academy of Sciences USA, 99, 1059-1063.
[17]	Deen, P.M., Verdijk, M.A., Knoers, N.V., Wieringa, B., Monnens, L.A., van Os, C.H. and van Oost, B.A. (1994) Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science, 264, 92-95. http://dx.doi.org/10.1126/science.8140421
[18]	Ma, T., Yang, B., Gillespie, A., Carlson, E.J., Epstein, C.J. and Verkman, A.S. (1997) Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. Journal of Clinical Investigation, 100, 957-962. http://dx.doi.org/10.1172/JCI231
[19]	Ma, T., Song, Y., Yang, B., Gillespie, A., Carlson, E.J., Epstein, C.J. and Verkman, A.S. (2000) Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels. Proceedings of the National Academy of Sciences USA, 97, 4386-4391.
[20]	Steinfeld, S., Cogan, E., King, L.S., Agre, P., Kiss, R. and Delporte, C. (2001) Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjögren’s syndrome patients. Laboratory Investigation, 81, 143-148. http://dx.doi.org/10.1038/labinvest.3780221
[21]	Verkman, A.S., Yang, B., Song, Y., Manley, G.T. and Ma, T. (2000) Role of water channels in fluid transport studied by phenotype analysis of aquaporin knockout mice. Experimental Physiology, 85, 233S-241S. http://dx.doi.org/10.1111/j.1469-445X.2000.tb00028.x
[22]	Silberstein, C., Kierbel, A., Amodeo, G., Zotta, E., Bigi, F., Berkowski, D. and Ibarra, C. (1999) Functional characterization and localization of AQP3 in the human colon. Brazilian Journal of Medical and Biological Research, 32, 1303-1313. http://dx.doi.org/10.1590/S0100-879X1999001000018
[23]	Purdy, M.J., Cima, R.R., Doble, M.A., Klein, M.A., Zinner, M.J. and Soybel, D.I. (1999) Selective decrease in levels of mRNA encoding a water channel (AQP3) in ileal mucosa after ileostomy in the rat. Journal of Gastrointestinal Surgery, 3, 54-60. http://dx.doi.org/10.1016/S1091-255X(99)80009-2