ORIGINAL PAPER
Cellular localization and putative role of aquaporin-2 Ser-261 in the bovine kidney
,
 
,
 
 
 
More details
Hide details
1
West Pomeranian University of Technology in Szczecin, Faculty of Biotechnology and Animal Husbandry, Department of Physiology, Cytobiology and Proteomics, Klemensa Janickiego 29, 71-270 Szczecin, Polan
 
2
Pomeranian Medical University, Department of Histology and Developmental Biology, Żołnierska 48, 71-210 Szczecin, Poland
 
 
Publication date: 2019-02-28
 
 
Corresponding author
K. Michałek   

West Pomeranian University of Technology in Szczecin, Faculty of Biotechnology and Animal Husbandry, Department of Physiology, Cytobiology and Proteomics, Klemensa Janickiego 29, 71-270 Szczecin, Poland
 
 
J. Anim. Feed Sci. 2019;28(1):15-21
 
KEYWORDS
TOPICS
ABSTRACT
Aquaporin-2 (AQP2) is a small, transmembrane protein, active in the principal cells of the renal collecting duct system. Phosphorylation and dephosphorylation of this protein regulate its redistribution in the cell, thereby influencing renal water reabsorption. The aims of the study were to identify and analyse the location of AQP2 phosphorylated at position 261, and to determine its potential role in renal water balance regulation, because data on AQP2 in cattle are scarce, and the mechanisms regulating its expression and cellular localization remain unclear. The analyses were carried out on kidneys collected from eight Polish Holstein-Friesian Black-and-White male calves, aged 5–7 months. It was found, using immunohistochemistry and commercially available phosphospecific antibodies, that in cattle AQP2 Ser-261 is located exclusively in the apical plasma membrane of the principal cells of the collecting duct. This atypical location of AQP2 Ser-261 allows to conclude that it may play a significant role in the process of renal water retention. The results of our previous studies on the regulation of renal total AQP2 excretion with urine in calves, as well as the bioinformatic analysis of available data presented in this study, seem to support this assumption. In addition, bioinformatic tools predicted mitogen activated protein kinases (MAPK) as a possible vasopressin-independent factor involved in AQP2 Ser-261 phosphorylation and accumulation in the apical plasma membrane.
 
REFERENCES (33)
1.
Brown D., 2008. Aquaporins and vasopressin signaling in the kidney health and diseases: introduction. Semin. Nephrol. 28, 215–216, https://doi.org/10.1016/j.semn....
 
2.
Brown D., Hasler U., Nunes P., Bouley R., Lu H.A.J., 2008. Phosphorylation events and the modulation of aquaporin 2 cell surface expression. Curr. Opin. Nephrol. Hypertens. 17, 491–498, https://doi.org/10.1097/MNH.0b....
 
3.
Christensen B.M., Zelenina M., Aperia A., Nielsen S., 2000. Localization and regulation of PKA-phosphorylated AQP2 in response to V(2)-receptor agonist/antagonist treatment. Am. J. Physiol. Renal Physiol. 278, F29–F42, https://doi.org/10.1152/ajpren....
 
4.
Eto K., Noda Y., Horikawa S., Uchida S., Sasaki S., 2010. Phosphorylation of aquaporin-2 regulates its water permeability. J. Biol. Chem. 285, 40777–40784, https://doi.org/10.1074/jbc.M1....
 
5.
Fenton R.A., Moeller H.B., Hoffert J.D., Yu M.-J., Nielsen S., Knepper M.A., 2008. Acute regulation of aquaporin-2 phosphorylation at Ser-264 by vasopressin. Proc. Natl. Acad. Sci. USA 105, 3134–3139, https://doi.org/10.1073/pnas.0....
 
6.
Fushimi K., Sasaki S., Marumo F., 1997. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of aquaporin-2 water channel. J. Biol. Chem. 271, 14800–14804, https://doi.org/10.1074/jbc.27....
 
7.
Guevara T., Sancho M., Pérez-Payá E., Orzáez M., 2014. Role of CDK5/cyclin complexes in ischemia-induced death and survival of renal tubular cells. Cell Cycle 13, 1671–1626, https://doi.org/10.4161/cc.286....
 
8.
Hasler U., Nunes P., Bouley R., Lu H.A.J., Matsuzaki T., Brown D., 2008. Acute hypertonicity alters aquaporin-2 trafficking and induces a MAPK-dependent accumulation at the plasma membrane of renal epithelial cells. J. Biol. Chem. 283, 26643–26661, https://doi.org/10.1074/jbc.M8....
 
9.
Hoffert J.D., Fenton R.A., Moeller H.B., Simons B., Tchapyjnikov D., McDill B.W., Yu M.-J., Pisitkun T., Chen F., Knepper M.A., 2008. Vasopressin-stimulated increase in phosphorylation at Ser269 potentiates plasma membrane retention of aquaporin-2. J. Biol. Chem. 283, 24617–24627, https://doi.org/10.1074/jbc.M8....
 
10.
Hoffert J.D., Nielsen J., Yu M.-J., Pisitkun T., Schleicher S.M., Nielsen S., 2007. Dynamics of aquaporin-2 serine-261 phosphorylation in response to short-term vasopressin treatment in collecting duct. Am. J. Physiol. Renal Physiol. 292, F691–F700, https://doi.org/10.1152/ajpren....
 
11.
Hoffert J.D., Pisitkun T., Wang G., Shen R.-F., Knepper M.A., 2006. Quantitative phosphoproteomics of vasopressin-sensitive renal cells: Regulation of aquaporin-2 phosphorylation at two sites. Proc. Natl. Acad. Sci. USA 103, 7159–7164, https://doi.org/10.1073/pnas.0....
 
12.
Holmes R.P., 2012. The role of renal water channels in health and disease. Mol. Aspects Med. 33, 547–552, https://doi.org/10.1016/j.mam.....
 
13.
Kamsteeg E.J., Heijnen I., van Os C.H., Deen P.M.T., 2000. The subcellular localization of an aquaporin-2 tetramer depends on the stoichiometry of phosphorylated and nonphosphorylated monomers. J. Cell Biol. 151, 919–930, https://doi.org/10.1083/jcb.15....
 
14.
Kiely B., Feldman G., Ryan M.P., 2003. Modulation of renal epithelial barrier function by mitogen-activated protein kinases (MAPKs): Mechanism of cyclosporine A-induced increase in transepithelial resistance. Kidney Int. 63, 908–916, https://doi.org/10.1046/j.1523....
 
15.
Kitchen P., Day R.E., Salman M.M., Conner M.T., Bill R.M., Conner A.C., 2015. Beyond water homeostasis: Diverse functional roles of mammalian aquaporins. Biochim. Biophys. Acta 1850, 2410–2421, https://doi.org/10.1016/j.bbag....
 
16.
Kortenoeven M.L.A., Fenton R.A., 2014. Renal aquaporins and water balance disorders. Biochim. Biophys. Acta 1840, 1533–1549, https://doi.org/10.1016/j.bbag....
 
17.
Kwon T.-H., Frøkiær J., Nielsen S., 2013. Regulation of aquaporin-2 in the kidney: A molecular mechanism of body-water homeostasis. Kidney Res. Clin. Pract. 32, 96–102, https://doi.org/10.1016/j.krcp....
 
18.
Li Y.-H., Eto K., Horikawa S., Uchida S., Sasaki S., Li X.-J., Noda Y., 2009. Aquaporin-2 regulates cell volume recovery via tropomyosin. Int. J. Biochem. Cell Biol. 41, 2466–2476, https://doi.org/10.1016/j.bioc....
 
19.
Michalek K., 2016. Aquaglyceroporin in the kidney: Present state of knowledge and prospects. J. Physiol. Pharmacol. 67, 185–193.
 
20.
Michałek K., Dratwa-Chałupnik A., Ciechanowicz A.K., Malinowski E., 2014a. Aquaporin 2: Identification and analysis of expression in calves’ urine during their first month of life. Can. J. Anim. Sci. 94, 653–659, https://doi.org/10.4141/cjas-2....
 
21.
Michałek K., Laszczyńska M., Ciechanowicz A.K., Herosimczyk A., Rotter I., Oganowska M., Lepczyński A., Dratwa-Chałupnik A., 2014b. Immunohistochemical identification of aquaporin 2 in the kidneys of young beef cattle. Biotech. Histochem. 89, 342–347, https://doi.org/10.3109/105202....
 
22.
Moeller H.B., Fenton R.A., 2012. Cell biology of vasopressin-regulated aquaporin-2 trafficking. Pflugers. Arch. 464, 133–144, https://doi.org/10.1007/s00424....
 
23.
Moeller H.B., Knepper M.A., Fenton R.A., 2009. Serine 269 phosphorylated aquaporin-2 is targeted to the apical membrane of collecting duct principal cells. Kidney Int. 75, 295–303, https://doi.org/10.1038/ki.200....
 
24.
Moeller H.B., Olesen E.T.B., Fenton R.A., 2011. Regulation of the water channel aquapori-2 by psttranslation modification. Am. J. Physiol. Renal Physiol. 300, F1062–F1073, https://doi.org/10.1152/ajpren....
 
25.
Nejsum L.N., Zelenina M., Aperia A., Frøkiær J., Nielsen S., 2005. Bidirectional regulation of AQP2 trafficking and recycling: involvement of AQP2-S256 phosphorylation. Am. J. Physiol. Renal Physiol. 288, F930–F938, https://doi.org/10.1152/ajpren....
 
26.
Nishimoto G., Zelenina M., Li D., Yasui M., Aperia A., Nielsen S., Nairn A.C., 1999. Arginine vasopressin stimulates phosphorylation of aquaporin-2 in rat renal tissue. Am. J. Physiol. 276, F254–F259, https://doi.org/10.1152/ajpren....
 
27.
Rieg T., Tang T., Murray F., Schroth J., Insel P.A., Fenton R.A., Hammond H.K., Vallon V., 2010. Adenylate cyclase 6 determines cAMP formation and aquaporin-2 phosphorylation and trafficking in inner medulla. J. Am. Soc. Nephrol. 21, 2059–2068, https://doi.org/10.1681/ASN.20....
 
28.
Takata K., Matsuzaki T., Tajika Y., Ablimit A., Hasegawa T., 2008. Localization and trafficking of aquaporin 2 in the kidney. Histochem. Cell. Biol. 130, 197–209, https://doi.org/10.1007/s00418....
 
29.
Tamma G., Lasorsa D., Trimpert Ch. et al., 2014. A protein kinase A-independent pathway controlling Aquaporin 2 trafficking as a possible cause for the syndrome of inappropriate antidiuresis associated with polycystic kidney disease 1 haploinsufficiency. J. Am. Soc. Nephrol. 25, 2241–2253, https://doi.org/10.1681/ASN.20....
 
30.
Tamma G., Robben J.H., Trimpert Ch., Boone M., Deen P.M.T., 2011. Regulation of AQP2 localization by S256 and S261 phosphorylation and ubiquitination. Am J Physiol. Cell Physiol. 300, C636–C646, https://doi.org/10.1152/ajpcel....
 
31.
van Balkom B.W.M., Savelkoul P.J.M., Markovich D., Hofman E., Nielsen S., van der Sluijs P., Deen P.M.T., 2002. The role of putative phosphorylation sites in the targeting and shuttling of the aquaporin-2 water channel. J. Biol. Chem. 277, 41473–41479, https://doi.org/10.1074/jbc.M2....
 
32.
Wilson J.L.L., Miranda C.A., Knepper M.A., 2013. Vasopressin and the regulation of aquaporin-2. Clin. Exp. Nephrol. 17, 751–764, https://doi.org/10.1007/s10157....
 
33.
Yui N., Sasaki S., Uchida S., 2017. Aquaporin-2 Ser-261 phosphorylation is regulated in combination with Ser-256 and Ser-269 phosphorylation. Biochem. Biophys. Res. Commun. 482, 524–529, https://doi.org/10.1016/j.bbrc....
 
ISSN:1230-1388
Journals System - logo
Scroll to top