Intestinal Aquaporins

Abstract

Aquaporins (AQPs) are integral, hydrophobic, and transmembrane proteins that facilitate passive transport of water depending on the osmotic pressure on both sides of the cell membrane. Of these channel proteins, those that are permeable only to water are called 'classical aquaporins', those that allow the passage of small molecules such as glycerol in addition to water are called 'aquaglyceroporins', and those with different structures and cellular distributions are called 'super aquaporins'. Aquaporins have a great role in the gastrointestinal tract as well as in the whole organism. Transepithelial transport of fluid in the intestine occurs spontaneously, either by paracellular or cellular routes, or both. The paracellular pathway is mediated by tight junctions in the intestinal epithelium and their passage is regulated based on the size and load of substances, while the cellular pathway is passive diffusion mediated by aquaporins and co-transporters. Among them, aquaporins are the major cellular pathway for bidirectional fluid transport in the gut. Aquaporins have important roles in the gut. Based on these roles, information, and research on whether aquaporins can be regulated by drugs and dietary supplements to increase intestinal health and improve their functions is increasing day by day. In this review, the functions of aquaporins in the intestinal tract, their situations in intestinal diseases, and the drugs and dietary supplements used for the treatment of these diseases are discussed together with current studies.

Keywords

• aquaporins
• gut health
• intestinal system

References

1. Aihara, E., Engevik, K. A., Montrose, M. H. (2017). Trefoil factor peptides and gastrointestinal function. Annual Review of Physiology, 79, 357. https://doi.org/10.1146/annurev-physiol-021115-105447
2. Aihara, E., Engevik, K. A., Montrose, M. H. (2017). Trefoil factor peptides and gastrointestinal function. Annual Review of Physiology, 79, 357. https://doi.org/10.1146/annurev-physiol-021115-105447
3. Ansar, T., Tahir, M., Lone, K. P., Munir, B. (2013). Immunolocalization of aquaporin-10 in tuberculous human ileum. Journal of the College of Physicians and Surgeons Pakistan, 23(6), 392–396. ID: emr-142561
4. Ansar, T., Tahir, M., Lone, K. P., Munir, B. (2013). Immunolocalization of aquaporin-10 in tuberculous human ileum. Journal of the College of Physicians and Surgeons Pakistan, 23(6), 392–396. ID: emr-142561
5. Brown, D. (2017). The discovery of water channels (aquaporins). Annals of Nutrition and Metabolism, 70(Suppl. 1), 37–42. https://doi.org/10.1159/000463061 Cao, M., Yang, M., Ou, Z., Li, D., Geng, L., Chen, P., … Gong, S. (2014). Involvement of aquaporins in a mouse model of Rotavirusdiarrhoea. Springer, 29(4), 211–217. https://doi.org/10.1007/s12250-014-3469-z
6. Brown, D. (2017). The discovery of water channels (aquaporins). Annals of Nutrition and Metabolism, 70(Suppl. 1), 37–42. https://doi.org/10.1159/000463061 Cao, M., Yang, M., Ou, Z., Li, D., Geng, L., Chen, P., … Gong, S. (2014). Involvement of aquaporins in a mouse model of Rotavirusdiarrhoea. Springer, 29(4), 211–217. https://doi.org/10.1007/s12250-014-3469-z
7. Chao, G., Zhang, S. (2018). Aquaporins 1, 3 and 8 expression and cytokines in irritable bowel syndrome rats’ colon via cAMP-PKA pathway. International Journal of Clinical and Experimental Pathology, 11(8), 4117. PMID: 31949803
8. Chao, G., Zhang, S. (2018). Aquaporins 1, 3 and 8 expression and cytokines in irritable bowel syndrome rats’ colon via cAMP-PKA pathway. International Journal of Clinical and Experimental Pathology, 11(8), 4117. PMID: 31949803

9. Chen, C., Chen, R. P., Lin, H. H., Zhang, W. Y., Huang, X. L., Huang, Z. M. (2016). Tolvaptan regulates aquaporin-2 and faecal water in cirrhotic rats with ascites. World Journal of Gastroenterology, 22(12), 3363–3371. https://doi.org/10.3748/wjg.v22.I12.3363
10. Chen, C., Chen, R. P., Lin, H. H., Zhang, W. Y., Huang, X. L., Huang, Z. M. (2016). Tolvaptan regulates aquaporin-2 and faecal water in cirrhotic rats with ascites. World Journal of Gastroenterology, 22(12), 3363–3371. https://doi.org/10.3748/wjg.v22.I12.3363
11. Deng, Y., Li, M., Mei, L., Cong, L., … Y. L.-B. (2018). Manipulation of intestinal dysbiosis by a bacterial mixture ameliorates loperamide-induced constipation in rats. Wageningen Academic Publishers, 9(3), 453–464. https://doi.org/10.3920/bm2017.0062
12. Deng, Y., Li, M., Mei, L., Cong, L., … Y. L.-B. (2018). Manipulation of intestinal dysbiosis by a bacterial mixture ameliorates loperamide-induced constipation in rats. Wageningen Academic Publishers, 9(3), 453–464. https://doi.org/10.3920/bm2017.0062
13. Dong, N., Xue, C., Zhang, L., Zhang, T., Wang, C., Bi, C., Shan, A. (2020). Oleanolic acid enhances tight junctions and ameliorates inflammation in Salmonella typhimurium -induced diarrhoea in mice via the TLR4/NF-κB and MAPK pathway. Food & Function, 11(1), 1122–1132. https://doi.org/10.1039/c9fo01718f
14. Dong, N., Xue, C., Zhang, L., Zhang, T., Wang, C., Bi, C., Shan, A. (2020). Oleanolic acid enhances tight junctions and ameliorates inflammation in Salmonella typhimurium -induced diarrhoea in mice via the TLR4/NF-κB and MAPK pathway. Food & Function, 11(1), 1122–1132. https://doi.org/10.1039/c9fo01718f
15. Engevik, A. C., Kaji, I., Engevik, M. A., Meyer, A. R., Weis, V. G., Goldstein, A., … Goldenring, J. R. (2018). Loss of MYO5B Leads to Reductions in Na+ Absorption with Maintenance of CFTR-Dependent Cl– Secretion in Enterocytes. Gastroenterology, 155(6), 1883-1897.e10. https://doi.org/10.1053/j.gastro.2018.08.025
16. Engevik, A. C., Kaji, I., Engevik, M. A., Meyer, A. R., Weis, V. G., Goldstein, A., … Goldenring, J. R. (2018). Loss of MYO5B Leads to Reductions in Na+ Absorption with Maintenance of CFTR-Dependent Cl– Secretion in Enterocytes. Gastroenterology, 155(6), 1883-1897.e10. https://doi.org/10.1053/j.gastro.2018.08.025
17. Fan, W., Ren, H., Cao, Y., Wang, Y., Huo, G. (2017). Low dietary protein and high carbohydrate infant formula affects the microbial ecology of the large intestine in neonatal rats. Canadian Journal of Microbiology, 63(12), 951–960. https://doi.org/10.1139/cjm-2017-0242
18. Fan, W., Ren, H., Cao, Y., Wang, Y., Huo, G. (2017). Low dietary protein and high carbohydrate infant formula affects the microbial ecology of the large intestine in neonatal rats. Canadian Journal of Microbiology, 63(12), 951–960. https://doi.org/10.1139/cjm-2017-0242
19. Fischbarg, J. (2010). Fluid transport across leaky epithelia: Central role of the tight junction and supporting role of aquaporins. Physiological Reviews, 90(4), 1271–1290. https://doi.org/10.1152/physrev.00025.2009
20. Fischbarg, J. (2010). Fluid transport across leaky epithelia: Central role of the tight junction and supporting role of aquaporins. Physiological Reviews, 90(4), 1271–1290. https://doi.org/10.1152/physrev.00025.2009
21. Gan, J. H., Huang, Y. F., Peng, D. Y., Yu, N. J., Chen, W. D., Luo, J. P., Han, L. (2019). Therapeutic effect and mechanism of three kinds of Dendrobium on constipation in rats with spleen Yin deficiency. ZhongguoZhong Yao ZaZhi = ZhongguoZhongyaoZazhi = China Journal of Chinese MateriaMedica, 44(12), 2600–2606. https://doi.org/10.19540/j.cnki.cjcmm.20190128.002
22. Gan, J. H., Huang, Y. F., Peng, D. Y., Yu, N. J., Chen, W. D., Luo, J. P., Han, L. (2019). Therapeutic effect and mechanism of three kinds of Dendrobium on constipation in rats with spleen Yin deficiency. ZhongguoZhong Yao ZaZhi = ZhongguoZhongyaoZazhi = China Journal of Chinese MateriaMedica, 44(12), 2600–2606. https://doi.org/10.19540/j.cnki.cjcmm.20190128.002
23. Gu, L., Li, N., Gong, J., Li, Q., Zhu, W.,Li, J. (2011). Berberine ameliorates intestinal epithelial tight-junction damage and down-regulates myosin light chain kinase pathways in a mouse model of endotoxinemia. The Journal of Infectious Diseases, 203(11), 1602–1612. https://doi.org/10.1093/infdis/jir147
24. Gu, L., Li, N., Gong, J., Li, Q., Zhu, W.,Li, J. (2011). Berberine ameliorates intestinal epithelial tight-junction damage and down-regulates myosin light chain kinase pathways in a mouse model of endotoxinemia. The Journal of Infectious Diseases, 203(11), 1602–1612. https://doi.org/10.1093/infdis/jir147
25. He, L., Huang, N., Li, H., Tian, J., Zhou, X., … T. L.(2017). AMPK/α-ketoglutarate axis regulates intestinal water and ion homeostasis in young pigs. Journal of Agricultural and Food Chemistry, 65(11), 2287–2298. https://doi.org/10.1021/acs.jafc.7b00324
26. He, L., Huang, N., Li, H., Tian, J., Zhou, X., … T. L.(2017). AMPK/α-ketoglutarate axis regulates intestinal water and ion homeostasis in young pigs. Journal of Agricultural and Food Chemistry, 65(11), 2287–2298. https://doi.org/10.1021/acs.jafc.7b00324
27. Hong, Y., Liew, S. C., Thean, L. F., Tang, C. L., Cheah, P. Y. (2018). Human colorectal cancer initiation is bidirectional, and cell growth, metabolic genes and transporter genes are early drivers of tumorigenesis. Cancer Letters, 431, 213–218. https://doi.org/10.1016/j.canlet.2018.06.005
28. Hong, Y., Liew, S. C., Thean, L. F., Tang, C. L., Cheah, P. Y. (2018). Human colorectal cancer initiation is bidirectional, and cell growth, metabolic genes and transporter genes are early drivers of tumorigenesis. Cancer Letters, 431, 213–218. https://doi.org/10.1016/j.canlet.2018.06.005
29. Huang, H., Liao, D., Liang, L., Song, L., Zhao, W. (2015). Genistein inhibits Rotavirus replication and upregulates AQP4 expression in Rotavirus-infected Caco-2 cells. Archives of Virology, 160(6), 1421–1433. https://doi.org/10.1007/S00705-015-2404
30. Huang, H., Liao, D., Liang, L., Song, L., Zhao, W. (2015). Genistein inhibits Rotavirus replication and upregulates AQP4 expression in Rotavirus-infected Caco-2 cells. Archives of Virology, 160(6), 1421–1433. https://doi.org/10.1007/S00705-015-2404
31. Huang, Y. H., Zhou, X. Y., Wang, H. M., Xu, H., Chen, J., Lv, N. H. (2013). Aquaporin 5 promotes the proliferation and migration of human gastric carcinoma cells. Tumour Biology 2013 34:3, 34(3), 1743–1751. https://doi.org/10.1007/s13277-013-0712-4
32. Huang, Y. H., Zhou, X. Y., Wang, H. M., Xu, H., Chen, J., Lv, N. H. (2013). Aquaporin 5 promotes the proliferation and migration of human gastric carcinoma cells. Tumour Biology 2013 34:3, 34(3), 1743–1751. https://doi.org/10.1007/s13277-013-0712-4
33. Hui, L., Zang, K., Wang, M., Shang, F., Zhang, G. (2018). Coculture with Clostridium difficile promotes apoptosis of human intestinal microvascular endothelial cells. Journal of International Medical Research, 46(11), 4631–4739. https://doi.org/10.1177/0300060518799267
34. Hui, L., Zang, K., Wang, M., Shang, F., Zhang, G. (2018). Coculture with Clostridium difficile promotes apoptosis of human intestinal microvascular endothelial cells. Journal of International Medical Research, 46(11), 4631–4739. https://doi.org/10.1177/0300060518799267
35. Ikarashi, N., Baba, K., Ushiki, T., Kon, R., Mimura, A., Toda, T., … Sugiyama, K. (2011). The laxative effect of bisacodyl is attributable to decreased aquaporin-3 expression in the colon induced by increased PGE 2 secretion from macrophages. American Journal of Physiology - Gastrointestinal and Liver Physiology, 301(5). https://doi.org/10.1152/ajpgi.00286.2011
36. Ikarashi, N., Baba, K., Ushiki, T., Kon, R., Mimura, A., Toda, T., … Sugiyama, K. (2011). The laxative effect of bisacodyl is attributable to decreased aquaporin-3 expression in the colon induced by increased PGE 2 secretion from macrophages. American Journal of Physiology - Gastrointestinal and Liver Physiology, 301(5). https://doi.org/10.1152/ajpgi.00286.2011
37. Ikarashi, N., Kon, R., Sugiyama, K. (2016). Aquaporins in the colon as a new therapeutic target in diarrhoea and constipation. International Journal of Molecular Sciences 2016, Vol. 17, Page 1172, 17(7), 1172. https://doi.org/10.3390/ijms17071172
38. Ikarashi, N., Kon, R., Sugiyama, K. (2016). Aquaporins in the colon as a new therapeutic target in diarrhoea and constipation. International Journal of Molecular Sciences 2016, Vol. 17, Page 1172, 17(7), 1172. https://doi.org/10.3390/ijms17071172
39. Ikarashi, N., Mimura, A., Kon, R., Iizasa, T., Omodaka, M., Nagoya, C., … Sugiyama, K. (2012). The concomitant use of an osmotic laxative, magnesium sulphate, and a stimulant laxative, bisacodyl, does not enhance the laxative effect. European Journal of Pharmaceutical Sciences, 45(1–2), 73–78. https://doi.org/10.1016/j.ejps.2011.10.024
40. Ikarashi, N., Mimura, A., Kon, R., Iizasa, T., Omodaka, M., Nagoya, C., … Sugiyama, K. (2012). The concomitant use of an osmotic laxative, magnesium sulphate, and a stimulant laxative, bisacodyl, does not enhance the laxative effect. European Journal of Pharmaceutical Sciences, 45(1–2), 73–78. https://doi.org/10.1016/j.ejps.2011.10.024
41. Jiang, L., Li, J., Liu, X., Burnstock, G., Xiang, Z. (2014). Expression of aquaporin-4 water channels in the digestive tract of the guinea pig. Journal of Molecular Histology, 45(2), 229–241. https://doi.org/10.1007/s10735-013-9545-0
42. Jiang, L., Li, J., Liu, X., Burnstock, G., Xiang, Z. (2014). Expression of aquaporin-4 water channels in the digestive tract of the guinea pig. Journal of Molecular Histology, 45(2), 229–241. https://doi.org/10.1007/s10735-013-9545-0
43. Jin, S. Y., Liu, Y. L., Xu, L. N., Jiang, Y., Wang, Y., Yang, B. X., … Ma, T. H. (2006). Cloning and characterization of porcine aquaporin 1 water channel expressed extensively in gastrointestinal system. World Journal of Gastroenterology: WJG, 12(7), 1092. https://doi.org/10.3748/wjg.v12.I7.1092
44. Jin, S. Y., Liu, Y. L., Xu, L. N., Jiang, Y., Wang, Y., Yang, B. X., … Ma, T. H. (2006). Cloning and characterization of porcine aquaporin 1 water channel expressed extensively in gastrointestinal system. World Journal of Gastroenterology: WJG, 12(7), 1092. https://doi.org/10.3748/wjg.v12.I7.1092
45. Kassa, E. G., Zlotkin-Rivkin, E., Friedman, G., Ramachandran, R. P., Melamed-Book, N., Weiss, A. M., … Aroeti, B. (2019). EnteropathogenicEscherichia coli remodels host endosomes to promote endocytic turnover and breakdown of surface polarity. Public Library of Science Pathogens, 15(6). https://doi.org/10.1371/journal.ppat.1007851
46. Kassa, E. G., Zlotkin-Rivkin, E., Friedman, G., Ramachandran, R. P., Melamed-Book, N., Weiss, A. M., … Aroeti, B. (2019). EnteropathogenicEscherichia coli remodels host endosomes to promote endocytic turnover and breakdown of surface polarity. Public Library of Science Pathogens, 15(6). https://doi.org/10.1371/journal.ppat.1007851
47. Kourghi, M., Pei, J. v., de Ieso, M. L., Nourmohammadi, S., Chow, P. H., Yool, A. J. (2018). Fundamental structural and functional properties of Aquaporin ion channels found across the kingdoms of life. Clinical and Experimental Pharmacology and Physiology, 45(4), 401–409. https://doi.org/10.1111/1440-1681.12900
48. Kourghi, M., Pei, J. v., de Ieso, M. L., Nourmohammadi, S., Chow, P. H., Yool, A. J. (2018). Fundamental structural and functional properties of Aquaporin ion channels found across the kingdoms of life. Clinical and Experimental Pharmacology and Physiology, 45(4), 401–409. https://doi.org/10.1111/1440-1681.12900
49. Krone, J. E. C., Agyekum, A. K., terBorgh, M., Hamonic, K., Penner, G. B., Columbus, D. A. (2019). Characterization of urea transport mechanisms in the intestinal tract of growing pigs. American Journal of Physiology - Gastrointestinal and Liver Physiology, 317(6), G839–G844. https://doi.org/10.1152/ajpgi.00220.2019
50. Krone, J. E. C., Agyekum, A. K., terBorgh, M., Hamonic, K., Penner, G. B., Columbus, D. A. (2019). Characterization of urea transport mechanisms in the intestinal tract of growing pigs. American Journal of Physiology - Gastrointestinal and Liver Physiology, 317(6), G839–G844. https://doi.org/10.1152/ajpgi.00220.2019
51. Laforenza, U. (2012). Water channel proteins in the gastrointestinal tract. Molecular Aspects of Medicine, 33(5–6), 642–650. https://doi.org/10.1016/j.mam.2012.03.001
52. Laforenza, U. (2012). Water channel proteins in the gastrointestinal tract. Molecular Aspects of Medicine, 33(5–6), 642–650. https://doi.org/10.1016/j.mam.2012.03.001
53. Laforenza, U., Gastaldi, G., Grazioli, M., Cova, E., Tritto, S., Faelli, A., … Ventura, U. (2005). Expression and immunolocalization of aquaporin‐7 in rat gastrointestinal tract. Wiley Online Library, 97(8), 605–613. https://doi.org/10.1042/bc20040090
54. Laforenza, U., Gastaldi, G., Grazioli, M., Cova, E., Tritto, S., Faelli, A., … Ventura, U. (2005). Expression and immunolocalization of aquaporin‐7 in rat gastrointestinal tract. Wiley Online Library, 97(8), 605–613. https://doi.org/10.1042/bc20040090
55. Laforenza, U., Gastaldi, G., Polimeni, M., Tritto, S., Tosco, M., Ventura, U., … Yasui, M. (2009). Aquaporin-6 is expressed along the rat gastrointestinal tract and upregulated by feeding in the small intestine. BMC Physiology, 9(1), 1–12. https://doi.org/10.1186/1472-6793-9-18
56. Laforenza, U., Gastaldi, G., Polimeni, M., Tritto, S., Tosco, M., Ventura, U., … Yasui, M. (2009). Aquaporin-6 is expressed along the rat gastrointestinal tract and upregulated by feeding in the small intestine. BMC Physiology, 9(1), 1–12. https://doi.org/10.1186/1472-6793-9-18
57. Li, C., Wang, W. (2017). Molecular biology of aquaporins. In B. Yang (Ed.), Aquaporins, Advances in Experimental Medicine and Biology (Vol. 969, pp. 1–34). Beijing, China: © Springer Science+Business Media B.V. https://doi.org/10.1007/978-94-024-1057-0_1
58. Li, C., Wang, W. (2017). Molecular biology of aquaporins. In B. Yang (Ed.), Aquaporins, Advances in Experimental Medicine and Biology (Vol. 969, pp. 1–34). Beijing, China: © Springer Science+Business Media B.V. https://doi.org/10.1007/978-94-024-1057-0_1
59. Lundgren, O., Peregrin, A. T., Persson, K., Kordasti, S., Uhnoo, I., Svensson, L. (2000). Role of the enteric nervous system in the fluid and electrolyte secretion of Rotavirusdiarrhoea. Science, 287(5452), 491–495. https://doi.org/10.1126/science.287.5452.491
60. Lundgren, O., Peregrin, A. T., Persson, K., Kordasti, S., Uhnoo, I., Svensson, L. (2000). Role of the enteric nervous system in the fluid and electrolyte secretion of Rotavirusdiarrhoea. Science, 287(5452), 491–495. https://doi.org/10.1126/science.287.5452.491
61. Lv, H., Li, Y., Xue, C., Dong, N., Bi, C., Shan, A. (2022). Aquaporin: targets for dietary nutrients to regulate intestinal health. Journal of Animal Physiology and Animal Nutrition, 106(1), 167–180. https://doi.org/10.1111/jpn.13539
62. Lv, H., Li, Y., Xue, C., Dong, N., Bi, C., Shan, A. (2022). Aquaporin: targets for dietary nutrients to regulate intestinal health. Journal of Animal Physiology and Animal Nutrition, 106(1), 167–180. https://doi.org/10.1111/jpn.13539
63. Magouliotis, D. E., Tasiopoulou, V. S., Baloyiannis, I., Mamaloudis, I., Tzovaras, G. (2020). Transcriptomic analysis of the aquaporin gene family and associated interactors in rectal cancer. MicroRNA, 9(2), 153–166. https://doi.org/10.2174/2211536608666190917153332
64. Magouliotis, D. E., Tasiopoulou, V. S., Baloyiannis, I., Mamaloudis, I., Tzovaras, G. (2020). Transcriptomic analysis of the aquaporin gene family and associated interactors in rectal cancer. MicroRNA, 9(2), 153–166. https://doi.org/10.2174/2211536608666190917153332
65. Marchbank, T., Playford, R. J. (2018). Trefoil factor family peptides enhance cell migration by increasing cellular osmotic permeability and aquaporin 3 levels. The Federation of American Societies for Experimental Biology (FASEB) Journal, 32(2), 1017–1024. https://doi.org/10.1096/fj.201700799r
66. Marchbank, T., Playford, R. J. (2018). Trefoil factor family peptides enhance cell migration by increasing cellular osmotic permeability and aquaporin 3 levels. The Federation of American Societies for Experimental Biology (FASEB) Journal, 32(2), 1017–1024. https://doi.org/10.1096/fj.201700799r
67. Mobasheri, A., Marples, D. (2004). Expression of the AQP-1 water channel in normal human tissues: A semiquantitative study using tissue microarray technology. American Journal of Physiology - Cell Physiology, 286(3 55-3). https://doi.org/10.1152/ajpcell.00408.2003
68. Mobasheri, A., Marples, D. (2004). Expression of the AQP-1 water channel in normal human tissues: A semiquantitative study using tissue microarray technology. American Journal of Physiology - Cell Physiology, 286(3 55-3). https://doi.org/10.1152/ajpcell.00408.2003
69. Moon, C., Soria, J. C., Jang, S. J., Lee, J., Hoque, M. O., Sibony, M., … Mao, L. (2003). Involvement of aquaporins in colorectal carcinogenesis. Oncogene 2003 22:43, 22(43), 6699–6703. https://doi.org/10.1038/sj.onc.1206762
70. Moon, C., Soria, J. C., Jang, S. J., Lee, J., Hoque, M. O., Sibony, M., … Mao, L. (2003). Involvement of aquaporins in colorectal carcinogenesis. Oncogene 2003 22:43, 22(43), 6699–6703. https://doi.org/10.1038/sj.onc.1206762
71. Moosavi, M. S., Elham, Y. (2020). Aquaporins1, 3 and 5 in different tumors, their expression, prognosis value and role as new therapeutic targets. Pathology and Oncology Research, 26(2), 615–625. https://doi.org/10.1007/S12253-019-00646-9
72. Moosavi, M. S., Elham, Y. (2020). Aquaporins1, 3 and 5 in different tumors, their expression, prognosis value and role as new therapeutic targets. Pathology and Oncology Research, 26(2), 615–625. https://doi.org/10.1007/S12253-019-00646-9
73. Okada, S., Misaka, T., Matsumoto, I., Watanabe, H., Abe, K. (2003). Aquaporin-9 is expressed in a mucus-secreting goblet cell subset in the small intestine. The Federation of European Biochemical Societies (FEBS) Letters, 540(1–3), 157–162. https://doi.org/10.1016/s0014-5793(03)00256-4
74. Okada, S., Misaka, T., Matsumoto, I., Watanabe, H., Abe, K. (2003). Aquaporin-9 is expressed in a mucus-secreting goblet cell subset in the small intestine. The Federation of European Biochemical Societies (FEBS) Letters, 540(1–3), 157–162. https://doi.org/10.1016/s0014-5793(03)00256-4
75. Parvin, M. N., Kurabuchi, S., Murdiastuti, K., Yao, C., Kosugi-Tanaka, C., Akamatsu, T., … Hosoi, K. (2005). Subcellular redistribution of AQP5 by vasoactive intestinal polypeptide in the Brunner’s gland of the rat duodenum. American Journal of Physiology - Gastrointestinal and Liver Physiology, 288(6 51-6), 1283–1291. https://doi.org/10.1152/ajpgi.00030.2004
76. Parvin, M. N., Kurabuchi, S., Murdiastuti, K., Yao, C., Kosugi-Tanaka, C., Akamatsu, T., … Hosoi, K. (2005). Subcellular redistribution of AQP5 by vasoactive intestinal polypeptide in the Brunner’s gland of the rat duodenum. American Journal of Physiology - Gastrointestinal and Liver Physiology, 288(6 51-6), 1283–1291. https://doi.org/10.1152/ajpgi.00030.2004
77. Ricanek, P., Lunde, L. K., Frye, S. A., Støen, M., Nygård, S., Morth, J. P., … Tønjum, T. (2015). Reduced expression of aquaporins in human intestinal mucosa in early-stage inflammatory bowel disease. Clinical and Experimental Gastroenterology, 8, 49. https://doi.org/10.2147/ceg.s70119
78. Ricanek, P., Lunde, L. K., Frye, S. A., Støen, M., Nygård, S., Morth, J. P., … Tønjum, T. (2015). Reduced expression of aquaporins in human intestinal mucosa in early-stage inflammatory bowel disease. Clinical and Experimental Gastroenterology, 8, 49. https://doi.org/10.2147/ceg.s70119
79. Shan, T., Cui, X., Li, W., Lin, W., Li, Y. (2014). AQP5: A novel biomarker that predicts poor clinical outcome in colorectal cancer. Oncology Reports, 32(4), 1564–1570. https://doi.org/10.3892/or.2014.3377
80. Shan, T., Cui, X., Li, W., Lin, W., Li, Y. (2014). AQP5: A novel biomarker that predicts poor clinical outcome in colorectal cancer. Oncology Reports, 32(4), 1564–1570. https://doi.org/10.3892/or.2014.3377
81. Sun, L.-L., Jiang, H.-B., Liu, B.-Y., Li, W.-D., Du, A.-L., Luo, X.-Q., Li, X.-Q. (2018). Effects of rhein on intestinal transmission, colonic electromyography, and expression of aquaporin-3 by colonic epithelium cells in constipated mice. International Journal of Clinical and Experimental Pathology, 11(2), 614. PMID: 31938147
82. Sun, L.-L., Jiang, H.-B., Liu, B.-Y., Li, W.-D., Du, A.-L., Luo, X.-Q., Li, X.-Q. (2018). Effects of rhein on intestinal transmission, colonic electromyography, and expression of aquaporin-3 by colonic epithelium cells in constipated mice. International Journal of Clinical and Experimental Pathology, 11(2), 614. PMID: 31938147
83. Thiagarajah, J. R., Chang, J., Goettel, J. A., Verkman, A. S., Lencer, W. I. (2017). Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia. Proceedings of the National Academy of Sciences of the United States of America, 114(3), 568–573. https://doi.org/10.1073/pnas.1612921114
84. Thiagarajah, J. R., Chang, J., Goettel, J. A., Verkman, A. S., Lencer, W. I. (2017). Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia. Proceedings of the National Academy of Sciences of the United States of America, 114(3), 568–573. https://doi.org/10.1073/pnas.1612921114
85. Thiagarajah, J. R., Zhao, D., Verkman, A. S. (2007). Impaired enterocyte proliferation in aquaporin-3 deficiency in mouse models of colitis. Gut, 56(11), 1529–1535. https://doi.org/10.1136/gut.2006.104620
86. Thiagarajah, J. R., Zhao, D., Verkman, A. S. (2007). Impaired enterocyte proliferation in aquaporin-3 deficiency in mouse models of colitis. Gut, 56(11), 1529–1535. https://doi.org/10.1136/gut.2006.104620
87. Wang, K. S., Ma, T., Filiz, F., Verkman, A. S., Bastidas, J. A. (2000). Colon water transport in transgenic mice lacking aquaporin-4 water channels. American Journal of Physiology - Gastrointestinal and Liver Physiology, 279(2 42-2). https://doi.org/10.1152/ajpgi.2000.279.2.g463
88. Wang, K. S., Ma, T., Filiz, F., Verkman, A. S., Bastidas, J. A. (2000). Colon water transport in transgenic mice lacking aquaporin-4 water channels. American Journal of Physiology - Gastrointestinal and Liver Physiology, 279(2 42-2). https://doi.org/10.1152/ajpgi.2000.279.2.g463
89. Willaert, W., Mareel, M., van de Putte, D., van Nieuwenhove, Y., Pattyn, P., Ceelen, W. (2014). Lymphatic spread, nodal count, and the extent of lymphadenectomy in cancer of the colon. Cancer Treatment Reviews, 40(3), 405–413. https://doi.org/10.1016/j.ctrv.2013.09.013
90. Willaert, W., Mareel, M., van de Putte, D., van Nieuwenhove, Y., Pattyn, P., Ceelen, W. (2014). Lymphatic spread, nodal count, and the extent of lymphadenectomy in cancer of the colon. Cancer Treatment Reviews, 40(3), 405–413. https://doi.org/10.1016/j.ctrv.2013.09.013
91. Wu, T., Li, K., Yi, D., Wang, L., Zhao, D., Lv, Y., … Wu, G. (2018). Dietary supplementation with trihexanoin enhances intestinal function of weaned piglets. International Journal of Molecular Sciences 2018, Vol. 19, Page 3277, 19(10), 3277. https://doi.org/10.3390/ijms19103277
92. Wu, T., Li, K., Yi, D., Wang, L., Zhao, D., Lv, Y., … Wu, G. (2018). Dietary supplementation with trihexanoin enhances intestinal function of weaned piglets. International Journal of Molecular Sciences 2018, Vol. 19, Page 3277, 19(10), 3277. https://doi.org/10.3390/ijms19103277
93. Xiang, T., Ge, S., Wen, J., Xie, J., Yang, L., Wu, X., Cheng, N. (2018). The possible association between AQP9 in the intestinal epithelium and acute liver injury-induced intestinal epithelium damage. Molecular Medicine Reports, 18(6), 4987–4993. https://doi.org/10.3892/mmr.2018.9542
94. Xiang, T., Ge, S., Wen, J., Xie, J., Yang, L., Wu, X., Cheng, N. (2018). The possible association between AQP9 in the intestinal epithelium and acute liver injury-induced intestinal epithelium damage. Molecular Medicine Reports, 18(6), 4987–4993. https://doi.org/10.3892/mmr.2018.9542
95. Yde, J., Keely, S., Wu, Q., Borg, J. F., Lajczak, N., O’Dwyer, A., … Moeller, H. B. (2016). Characterization of AQPs in mouse, rat, and human colon and their selective regulation by bile acids. Frontiers in Nutrition, 3. https://doi.org/10.3389/fnut.2016.00046/full
96. Yde, J., Keely, S., Wu, Q., Borg, J. F., Lajczak, N., O’Dwyer, A., … Moeller, H. B. (2016). Characterization of AQPs in mouse, rat, and human colon and their selective regulation by bile acids. Frontiers in Nutrition, 3. https://doi.org/10.3389/fnut.2016.00046/full
97. Yi, D., Li, B., Hou, Y., Wang, L., Zhao, D., Chen, H., … Wu, G. (2018). Dietary supplementation with an amino acid blend enhances intestinal function in piglets. Amino Acids, 50(8), 1089–1100. https://doi.org/10.1007/S00726-018-2586-7
98. Yi, D., Li, B., Hou, Y., Wang, L., Zhao, D., Chen, H., … Wu, G. (2018). Dietary supplementation with an amino acid blend enhances intestinal function in piglets. Amino Acids, 50(8), 1089–1100. https://doi.org/10.1007/S00726-018-2586-7
99. Yin, J., Liang, Y., Wang, D., Yan, Z., Yin, H., Wu, D., Su, Q. (2018). Naringenin induces laxative effects by upregulating the expression levels of c-Kit and SCF, as well as those of aquaporin 3 in mice with loperamide-induced constipation. International Journal of Molecular Medicine, 41(2), 649–658. https://doi.org/10.3892/ijmm.2017.3301
100. Yin, J., Liang, Y., Wang, D., Yan, Z., Yin, H., Wu, D., Su, Q. (2018). Naringenin induces laxative effects by upregulating the expression levels of c-Kit and SCF, as well as those of aquaporin 3 in mice with loperamide-induced constipation. International Journal of Molecular Medicine, 41(2), 649–658. https://doi.org/10.3892/ijmm.2017.3301
101. Zahn, A., Moehle, C., Langmann, T., Ehehalt, R., Autschbach, F., Stremmel, W., Schmitz, G. (2007). Aquaporin-8 expression is reduced in ileum and induced in colon of patients with ulcerative colitis. World Journal of Gastroenterology: WJG, 13(11), 1687. https://doi.org/10.3748/wjg.v13.I11.1687
102. Zahn, A., Moehle, C., Langmann, T., Ehehalt, R., Autschbach, F., Stremmel, W., Schmitz, G. (2007). Aquaporin-8 expression is reduced in ileum and induced in colon of patients with ulcerative colitis. World Journal of Gastroenterology: WJG, 13(11), 1687. https://doi.org/10.3748/wjg.v13.I11.1687
103. Zhang, D., Zhang, K., Su, W., Zhao, Y., Ma, X., Qian, G., … Ma, H. (2017). Aquaporin-3 is down-regulated in jejunum villi epithelial cells during enterotoxigenicEscherichia coli-induced diarrhoea in mice. Microbial Pathogenesis, 107, 430–435 https://doi.org/10.1016/j.micpath.2017.04.031
104. Zhang, D., Zhang, K., Su, W., Zhao, Y., Ma, X., Qian, G., … Ma, H. (2017). Aquaporin-3 is down-regulated in jejunum villi epithelial cells during enterotoxigenicEscherichia coli-induced diarrhoea in mice. Microbial Pathogenesis, 107, 430–435 https://doi.org/10.1016/j.micpath.2017.04.031
105. Zhang, J., Li, S., Deng, F., Baikeli, B., Yu, W., Liu, G. (2019). Distribution of aquaporins and sodium transporters in the gastrointestinal tract of a desert hare, Lepus yarkandensis. Scientific Reports 2019 9:1, 9(1), 1–14. https://doi.org/10.1038/s41598-019-53291-2
106. Zhang, J., Li, S., Deng, F., Baikeli, B., Yu, W., Liu, G. (2019). Distribution of aquaporins and sodium transporters in the gastrointestinal tract of a desert hare, Lepus yarkandensis. Scientific Reports 2019 9:1, 9(1), 1–14. https://doi.org/10.1038/s41598-019-53291-2
107. Zhang, W., Zhu, B., Xu, J., Liu, Y., Qiu, E., Li, Z., … Zhi, F. (2018). Bacteroidesfragilis protects against antibiotic associateddiarrhoea in rats by modulating intestinal defences. Frontiers in Immunology, 9(MAY). https://doi.org/10.3389/fimmu.2018.01040/full
108. Zhang, W., Zhu, B., Xu, J., Liu, Y., Qiu, E., Li, Z., … Zhi, F. (2018). Bacteroidesfragilis protects against antibiotic associateddiarrhoea in rats by modulating intestinal defences. Frontiers in Immunology, 9(MAY). https://doi.org/10.3389/fimmu.2018.01040/full
109. Zhang, Y., Wang, X., Sha, S., Liang, S., Zhao, L., Liu, L., … Wu, K. (2012). Berberine increases the expression of NHE3 and AQP4 in sennosideA-induced diarrhoea model. Fitoterapia, 83(6), 1014–1022. https://doi.org/10.1016/j.fitote.2012.05.015
110. Zhang, Y., Wang, X., Sha, S., Liang, S., Zhao, L., Liu, L., … Wu, K. (2012). Berberine increases the expression of NHE3 and AQP4 in sennosideA-induced diarrhoea model. Fitoterapia, 83(6), 1014–1022. https://doi.org/10.1016/j.fitote.2012.05.015
111. Zhao, G., Li, J., Wang, J., Shen, X., Sun, J. (2014). Aquaporin 3 and 8 are down-regulated in TNBS-induced rat colitis. Biochemical and Biophysical Research Communications, 443(1), 161–166. https://doi.org/10.1016/j.bbrc.2013.11.067
112. Zhao, G., Li, J., Wang, J., Shen, X., Sun, J. (2014). Aquaporin 3 and 8 are down-regulated in TNBS-induced rat colitis. Biochemical and Biophysical Research Communications, 443(1), 161–166. https://doi.org/10.1016/j.bbrc.2013.11.067
113. Zhao, G. X., Dong, P. P., Peng, R., Li, J., Zhang, D. Y., Wang, J. Y., … Sun, J. Y. (2016). Expression, localization, and possible functions of aquaporins 3 and 8 in rat digestive system. Biotechnic&Histochemistry 91(4), 269–276. https://doi.org/10.3109/10520295.2016.1144079
114. Zhao, G. X., Dong, P. P., Peng, R., Li, J., Zhang, D. Y., Wang, J. Y., … Sun, J. Y. (2016). Expression, localization, and possible functions of aquaporins 3 and 8 in rat digestive system. Biotechnic&Histochemistry 91(4), 269–276. https://doi.org/10.3109/10520295.2016.1144079
115. Zhu, S., Ran, J., Yang, B., Mei, Z. (2017). Aquaporinsin digestive system. In B. Yang (Ed.), Aquaporins, Advances in Experimental Medicine and Biology (Vol. 969, pp. 123–130). Beijing, China: © Springer Science+Business Media B.V.
116. Zhu, S., Ran, J., Yang, B., Mei, Z. (2017). Aquaporinsin digestive system. In B. Yang (Ed.), Aquaporins, Advances in Experimental Medicine and Biology (Vol. 969, pp. 123–130). Beijing, China: © Springer Science+Business Media B.V.
117. Zhu, Y., Wang, Y., Teng, W., Shan, Y., Yi, S., Zhu, S., Li, Y. (2019). Role of aquaporin-3 in intestinal injury induced by sepsis. Biological and Pharmaceutical Bulletin, 42(10), 1641–1650. https://doi.org/10.1248/bpb.b19-00073
118. Zhu, Y., Wang, Y., Teng, W., Shan, Y., Yi, S., Zhu, S., Li, Y. (2019). Role of aquaporin-3 in intestinal injury induced by sepsis. Biological and Pharmaceutical Bulletin, 42(10), 1641–1650. https://doi.org/10.1248/bpb.b19-00073
119. Zhuang, S., Zhong, J., Zhou, Q., Zhong, Y., Liu, P., Liu, Z. (2019). Rhein protects against barrier disruption and inhibits inflammation in intestinal epithelial cells. International Immunopharmacology, 71, 321–327. https://doi.org/10.1016/j.intimp.2019.03.030
120. Zhuang, S., Zhong, J., Zhou, Q., Zhong, Y., Liu, P., Liu, Z. (2019). Rhein protects against barrier disruption and inhibits inflammation in intestinal epithelial cells. International Immunopharmacology, 71, 321–327. https://doi.org/10.1016/j.intimp.2019.03.030