Abstract
Expression of the aquaporin-4 (AQP4) water channel was systematically studied in the digestive tract of the guinea pig using Western blot and immunofluorescence techniques. The results showed that AQP4 was expressed widely in different segments of the guinea pig digestive tract. AQP4-immunoreactivity was confined to parietal cells in the stomach, and absorptive and glandular epithelial cells of small and large intestine. AQP4 protein was also expressed by enteric glial cells of submucosal and myenteric ganglia and primary nerve trunks. AQP4 was expressed by both type I and type II enteric gliocytes, but not by type III or type IV enteric gliocytes, indicating that enteric gliocytes have a heterogeneous distribution in the gut wall. In addition, different patterns of AQP4 expression in the enteric nervous system of human, guinea pig, rat and mouse colon mucosa were identified: in rat and mouse AQP4 was localised to a small subpopulation of neurons; in the guinea pig AQP4 was localised to enteric glial cells; and in the human colon mucosa, AQP4 was also detected mainly in the glial cells. It has been speculated that AQP4 may be involved in water transport in the gastrointestinal tract. Its role in enteric neurons and glia is unknown, but, by analogy with the brain, AQP4 may be involved in the formation and resolution of edema.
Similar content being viewed by others
References
Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels–from atomic structure to clinical medicine. J Physiol 542:3–16
Amiry-Moghaddam M, Ottersen OP (2003) The molecular basis of water transport in the brain. Nat Rev Neurosci 4:991–1001
Barrett KE (2008) New ways of thinking about (and teaching about) intestinal epithelial function. Adv Physiol Educ 32:25–34
Field M (2003) Intestinal ion transport and the pathophysiology of diarrhea. J Clin Investig 111:931–943
Fischbarg J (2010) Fluid transport across leaky epithelia: central role of the tight junction and supporting role of aquaporins. Physiol Rev 90:1271–1290
Frigeri A, Gropper MA, Turck CW, Verkman AS (1995) Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc Natl Acad Sci USA 92(10):4328–4331
Fujita A, Horio Y, Nielsen S, Nagelhus EA, Hata F, Ottersen OP, Kurachi Y (1999) High-resolution immunogold cytochemistry indicates that AQP4 is concentrated along the basal membrane of parietal cell in rat stomach. FEBS Lett 459:305–309
Gao H, He C, Fang X, Hou X, Feng X, Yang H, Zhao X, Ma T (2006) Localization of aquaporin-1 water channel in glial cells of the human peripheral nervous system. Glia 53(7):783–787
Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta 1788:1213–1228
Gulbransen BD, Sharkey KA (2012) Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 9:625–632
Hanani M, Reichenbach A (1994) Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 278:153–160
Huang Y, Tola VB, Fang P, Soybel DI, Van Hoek AN (2003) Partitioning of aquaporin-4 water channel mRNA and protein in gastric glands. Dig Dis Sci 48:2027–2036
Ishibashi K (2006) Aquaporin superfamily with unusual npa boxes: S-aquaporins (superfamily, sip-like and subcellular-aquaporins). Cell Mol Biol (Noisy-le-grand) 52:20–27
Isokpehi RD, Rajnarayanan RV, Jeffries CD, Oyeleye TO, Cohly HH (2009) Integrative sequence and tissue expression profiling of chicken and mammalian aquaporins. BMC Genomics 10(Suppl 2):S7
Jessen KR, Mirsky R (1983) Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3:2206–2218
King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5:687–698
Koyama Y, Yamamoto T, Tani T, Nihei K, Kondo D, Funaki H, Yaoita E, Kawasaki K, Sato N, Hatakeyama K, Kihara I (1999) Expression and localization of aquaporins in rat gastrointestinal tract. Am J Physiol 276(3 Pt 1):C621–C627
Laforenza U (2012) Water channel proteins in the gastrointestinal tract. Mol Aspects Med 33(5–6):642–650
Laforenza U, Cova E, Gastaldi G, Tritto S, Grazioli M, LaRusso NF, Splinter PL, D’Adamo P, Tosco M, Ventura U (2005) Aquaporin-8 is involved in water transport in isolated superficial colonocytes from rat proximal colon. J Nutr 135(10):2329–2336
Ma T, Verkman AS (1999) Aquaporin water channels in gastrointestinal physiology. J Physiol 517(Pt 2):317–326
Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, Chan P, Verkman AS (2000) Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6:159–163
Manley GT, Binder DK, Papadopoulos MC, Verkman AS (2004) New insights into water transport and edema in the central nervous system from phenotype analysis of aquaporin-4 null mice. Neuroscience 129:983–991
Misaka T, Abe K, Iwabuchi K, Kusakabe Y, Ichinose M, Miki K, Emori Y, Arai S (1996) A water channel closely related to rat brain aquaporin 4 is expressed in acid- and pepsinogen-secretory cells of human stomach. FEBS Lett 381(3):208–212
Nicchia GP, Nico B, Camassa LM, Mola MG, Loh N, Dermietzel R, Spray DC, Svelto M, Frigeri A (2004) The role of aquaporin-4 in the blood-brain barrier development and integrity: studies in animal and cell culture models. Neuroscience 129:935–945
Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171–180
Papadopoulos MC, Krishna S, Verkman AS (2002) Aquaporin water channels and brain edema. Mt Sinai J Med 69:242–248
Papadopoulos MC, Manley GT, Krishna S, Verkman AS (2004) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 18:1291–1293
Rojek A, Praetorius J, Frokiaer J, Nielsen S, Fenton RA (2008) A current view of the mammalian aquaglyceroporins. Annu Rev Physiol 70:301–327
Rosenthal R, Milatz S, Krug SM, Oelrich B, Schulzke JD, Amasheh S, Gunzel D, Fromm M (2010) Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci 123:1913–1921
Ruhl A (2005) Glial cells in the gut. Neurogastroenterol Motil 17:777–790
Thi MM, Spray DC, Hanani M (2008) Aquaporin-4 water channels in enteric neurons. J Neurosci Res 86:448–456
Verkman AS (2006) Roles of aquaporins in kidney revealed by transgenic mice. Semin Nephrol 26:200–208
Verkman AS (2009) Aquaporins: translating bench research to human disease. J Exp Biol 212:1707–1715
Yoshimura K, Sugiura K, Ohmori Y, Aste N, Saito N (2011) Immunolocalization of aquaporin-4 in the brain, kidney, skeletal muscle, and gastro-intestinal tract of chicken. Cell Tissue Res 344:51–61
Acknowledgments
The authors thank Dr. Gillian E. Knight for her excellent editorial assistance. This work was supported by 973 Program (2011CB504401 to Z. Xiang) and the National Natural Science Foundation of PR China (30970918 to Z. Xiang).
Author information
Authors and Affiliations
Corresponding author
Additional information
Ling Jiang, Jian Li and Xiaofeng Liu contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jiang, L., Li, J., Liu, X. et al. Expression of aquaporin-4 water channels in the digestive tract of the guinea pig. J Mol Hist 45, 229–241 (2014). https://doi.org/10.1007/s10735-013-9545-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10735-013-9545-0