DOI QR코드

DOI QR Code

Characterization and expression profiles of aquaporins (AQPs) 1a and 3a in mud loach Misgurnus mizolepis after experimental challenges

  • Lee, Sang Yoon (Department of Marine Bio-Materials and Aquaculture, Pukyong National University) ;
  • Nam, Yoon Kwon (Department of Marine Bio-Materials and Aquaculture, Pukyong National University) ;
  • Kim, Yi Kyung (Department of Marine Biotechnology, Gangneung-Wonju National University)
  • Received : 2017.05.15
  • Accepted : 2017.09.02
  • Published : 2017.09.30

Abstract

Two distinct cDNAs encoding aquaporins (mmAQPs 1a and 3a) were isolated and characterized from mud loach Misgurnus mizolepis. The identified mud loach AQP cDNAs encode for polypeptides of 260 and 302 amino acids. Topology predictions confirmed six putative membrane-spanning domains connected by five loops and the N- and C-terminal domains being cytoplasmic. The mud loach AQPs 1a and 3a showed broad distribution in multiple tissues including immune-responsive tissues as well as osmoregulatory tissues. Hence, the diversity of AQP distribution and expression possibly indicated its differential functions in the regulation of fluid movement in response to environmental stimuli. The transcription of mmAQP genes was differentially modulated by immune challenges. In particular, the mmAQP3a expression level in the liver was more responsive to immune challenges than that of mmAQP1a. Taken together, fish stimulation or infection resulted in significant modulation of mud loach AQP genes, suggesting potential functional roles of these proteins in piscine pathophysiological process.

Keywords

References

  1. An KW, Kim NN, Choi CY. Cloning and expression of aquaporin 1 and arginine vasotocin receptor mRNA from the black porgy, Acanthopagrus schlegli: effect of freshwater acclimation. Fish Physiol Biochem. 2008;34:185-94. https://doi.org/10.1007/s10695-007-9175-0
  2. Aoki M, Kaneko T, Katoh F, Hasegawa S, Tsutsui N, Aida K. Intestinal water absorption through aquaporin 1 expressed in the apical membrane of mucosal epithelial cells in seawater-adapted Japanese eel. J Exp Biol. 2003;206:3495-505. https://doi.org/10.1242/jeb.00579
  3. Boj M, Chauvigne F, Zapater C, Cerda J. Gonadotropin-activated androgendependent and independent pathways regulate aquaporin expression during teleost (Sparus aurata) spermatogenesis. PLoS One. 2015;10:e0142512. https://doi.org/10.1371/journal.pone.0142512
  4. Borgnia M, Nielsen S, Engel A, Agre P. Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem. 1999;68:425-58. https://doi.org/10.1146/annurev.biochem.68.1.425
  5. Cheng W, Chen JC. Effects of pH, temperature and salinity on immune parameters of the freshwater prawn Macrobrachium rosenbergii. Fish Shellfish Immunol. 2000;10:387-91. https://doi.org/10.1006/fsim.2000.0264
  6. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson TD. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res. 2003;31:3497-500. https://doi.org/10.1093/nar/gkg500
  7. Cho YS, Kim BS, Kim DS, Nam YK. Modulation of warm-temperature-acclimationassociated 65-kDa protein genes (Wap65-1 and Wap65-2) in mud loach (Misgurnus mizolepis, Cypriniformes) liver in response to different stimulatory treatments. Fish Shellfish Immunol. 2012;32:662-9. https://doi.org/10.1016/j.fsi.2012.01.009
  8. Choi YJ, Shin HS, Cho SH, Yamamoto Y, Ueda H, Lee J, Choi CY. Expression of aquaporin-3 and -8 mRNAs in the parr and smolt stages of sockeye salmon, Oncorhynchus nerka: effects of cortisol treatment and seawater acclimation. Comp Biochem Physiol A Mol Integr Physiol. 2013;165:228-36. https://doi.org/10.1016/j.cbpa.2013.03.013
  9. Cutler CP, Cramb G. Water transport and aquaporin expression in fish. In: Molecular Biology and Physiology of Water and Solute Transport. Springer US; 2000. p. 433-441.
  10. Deane EE, Luk JC, Woo NY. Aquaporin 1a expression in gill, intestine, and kidney of the euryhaline silver sea bream. Front Physiol. 2011;21:2.
  11. Deane EE, Woo NY. Tissue distribution, effects of salinity acclimation, and ontogeny of aquaporin 3 in the marine teleost, silver sea bream (Sparus sarba). Mar Biotechnol (NY). 2006;8:663-71. https://doi.org/10.1007/s10126-006-6001-0
  12. Fiol DF, Kultz D. Osmotic stress sensing and signaling in fishes. FEBS J. 2007;274:5790-8. https://doi.org/10.1111/j.1742-4658.2007.06099.x
  13. Gasteiger E GA, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. In: Walker JM, editor. The Proteomics Protocols Handbook. Humana Press; 2005. p. 571-607.
  14. Giffard-Mena I, Boulo V, Aujoulat F, Fowden H, Castille R, Charmantier G, Cramb G. Aquaporins molecular characterization in the sea-bass (Dicentrarchus labrax): the effect of salinity on AQP1 and AQP3 expression. Comp Biochem Physiol A. 2007;148:430-44. https://doi.org/10.1016/j.cbpa.2007.06.002
  15. Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta. 2009;1788:1213-28. https://doi.org/10.1016/j.bbamem.2009.03.009
  16. Grosell M. The role of the gastrointestinal tract in salt and water balance. In: Grosell M, Farrell AP, Brauner CJ, editors. The multifunctional gut of fish. San Diego: Academic; 2011. p. 136-64.
  17. Henry RP, Gehnrich S, Weihrauch D, Towle DW. Salinity-mediated carbonic anhydrase induction in the gills of the euryhaline green crab, Carcinus maenas. Comp Biochem Physiol A Mol Integr Physiol. 2003;136:243-58. https://doi.org/10.1016/S1095-6433(03)00113-2
  18. Ishibashi K, Kondo S, Hara S, Morishita Y. The evolutionary aspects of aquaporin family. Am J Phys. 2011;300:R566-76.
  19. Kim YK, Lee SY, Kim BS, Kim DS, Nam YK. Isolation and mRNA expression analysis of aquaporin isoforms in marine medaka Oryzias dancena, a euryhaline teleost. Comp Biochem Physiol A Mol Integr Physiol. 2014;171:1-8. https://doi.org/10.1016/j.cbpa.2014.01.012
  20. Kim YK, Watanabe S, Kaneko T, Huh MD, Park SI. Expression of aquaporins 3, 8 and 10 in the intestines of freshwater- and seawater-acclimated Japanese eels Anguilla japonica. Fish Sci. 2010;76:695-702.
  21. King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol. 2004;5:687-98. https://doi.org/10.1038/nrm1469
  22. Kozono D, Ding X, Iwasaki I, Meng X, Kamagata Y, Agre P, Kitagawa Y. Functional expression and characterization of an archaeal aquaporin AqpM from Methanothermobacter marburgenesis. J Biol Chem. 2003;278:10649-56. https://doi.org/10.1074/jbc.M212418200
  23. Kramer-Zucker AG, Wiessner S, Jensen AM, Drummond IA. Organization of the pronephric filtration apparatus in zebrafish requires Nephrin, Podocin and the FERM domain protein mosaic eyes. Dev Biol. 2005;285:316-29. https://doi.org/10.1016/j.ydbio.2005.06.038
  24. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567-80. https://doi.org/10.1006/jmbi.2000.4315
  25. Kubista M, Andrade JM, Bengtsson M, Forootan A, Jonak J, Lind K, Sindelka R, Sjoback R, Sjogreen B, Strombom L, Stahlberg A, Zoric N. The real-time polymerase chain reaction. Mol Asp Med. 2006;27:95-125. https://doi.org/10.1016/j.mam.2005.12.007
  26. Kwon SR, Nam YK, Kim SK, Kim DS, Kim KH. Generation of Edwardsiella tarda ghosts by bacteriophage PhiX174 lysis gene E. Aquaculture. 2005;250:16-21. https://doi.org/10.1016/j.aquaculture.2005.02.052
  27. Lee SY, Kim DS, Nam YK. Altered expression of mud loach (Misgurnus mizolepis; Cypriniformes) hepcidin mRNA during experimental challenge with nonpathogenic or pathogenic bacterial species. J Fish Pathol. 2011;24:279-87. https://doi.org/10.7847/jfp.2011.24.3.279
  28. Lehmann GL, Carreras FI, Soria LR, Gradilone SA, Marinelli RA. LPS induces the TNF-${\alpha}$- mediated downregulation of rat liver aquaporin-8: role in sepsis-associated cholestasis. Am J Physiol Gastrointest Liver Physiol. 2008;294:G567-75. https://doi.org/10.1152/ajpgi.00232.2007
  29. Madsen SS, Bujak J, Tipsmark CK. Aquaporin expression in the Japanese medaka (Oryzias latipes) in freshwater and seawater: challenging the paradigm of intestinal water transport? J Exp Biol. 2014;217:3108-21. https://doi.org/10.1242/jeb.105098
  30. Mobasheri A, Marples D. Expression of the AQP-1 water channel in normal human tissues: a semiquantitative study using tissue microarray technology. Am J Phys. 2004;286:C529-37. https://doi.org/10.1152/ajpcell.00408.2003
  31. Moshtaghi A, Rahi ML, Nguyen VT, Mather PB, Hurwood DA. A transcriptomic scan for potential candidate genes involved in osmoregulation in an obligate freshwater palaemonid prawn (Macrobrachium australiense). Peer J. 2016;4:e2520. https://doi.org/10.7717/peerj.2520
  32. Nam YK, Cho YS, Lee SY, Kim BS, Kim DS. Molecular characterization of hepcidin gene from mud loach (Misgurnus mizolepis; Cypriniformes). Fish Shellfish Immunol. 2011;31:1251-8. https://doi.org/10.1016/j.fsi.2011.09.007
  33. Nielsen S, Kwon TH, Christensen BM, Promeneur D, Frokiaer J, Marples D. Physiology and pathophysiology of renal aquaporins. J Am Soc Nephrol. 1999;10:647-63.
  34. Paulsen SM, Lunde H, Engstad RE, Robertsen B. In vivo effects of ${\beta}$-glucan and LPS on regulation of lysozyme activity and mRNA expression in Atlantic salmon (Salmo Salar L.). Fish Shellfish Immunol. 2003;14:39-54. https://doi.org/10.1006/fsim.2002.0416
  35. Plumb JA. Edwardsiella Septicaemias. In: Woo PTK, Bruno DW, editors. Fish diseases and disorders, volume 3: viral, bacterial, and fungal infections, vol. 3. Oxon: CAB International; 1999. p. 479-521.
  36. Preston GM, Jung JS, Guggino WB, Agre P. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem. 1993;268:17-20.
  37. Rodriguez A, Catalan V, Gomez-Ambrosi J, Garcia-Navarro S, Rotellar F, Valenti V, Silva C, Gil MJ, Salvador J, Burrell MA, Calamita G, Malagon MM, Fruhbeck G. Insulin-and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade. J Clin Endocrinol Metab. 2011;96:E586-97. https://doi.org/10.1210/jc.2010-1408
  38. Rombout JH, Abelli L, Picchietti S, Scapigliati G, Kiron V. Teleost intestinal immunology. Fish Shellfish Immunol. 2011;31:616-26. https://doi.org/10.1016/j.fsi.2010.09.001
  39. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101-8. https://doi.org/10.1038/nprot.2008.73
  40. Thompson JD, Higgins DG, Gibson TJ. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673-80. https://doi.org/10.1093/nar/22.22.4673
  41. Tingaud-Sequeira A, Calusinska M, Finn RN, Chauvigne F, Lozano J, Cerda J. The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evol Biol. 2010;10:38. https://doi.org/10.1186/1471-2148-10-38
  42. Tyagi MG, Tangevelu P. A possible role of aquaporin water channels in blood cell migration in spleen; interaction with cluster of differentiation molecules. J Exp Sci. 2010;1:41-2.
  43. Verkman AS. Aquaporins in clinical medicine. Annu Rev Med. 2012;63:303-16. https://doi.org/10.1146/annurev-med-043010-193843
  44. Watanabe S, Hirano T, Grau EG, Kaneko T. Osmosensitivity of prolactin cells is enhanced by the water channel aquaporin-3 in a euryhaline Mozambique tilapia (Oreochromis mossambicus). Am J Phys. 2009;296:R446-53.
  45. Watanabe S, Kaneko T, Aida K. Aquaporin-3 expressed in the basolateral membrane of gill chloride cells in Mozambique tilapia Oreochromis mossambicus adapted to freshwater and seawater. J Exp Biol. 2005;208:2673-82. https://doi.org/10.1242/jeb.01684
  46. Wheeler DL, Church DM, Federhen S, Lash AE, Madden TL, Pontius JU, Schuler GD, Schriml LM, Sequeira E, Tatusova TA, Wagner L. Database resources of the National Center for Biotechnology. Nucleic Acids Res. 2003;31:28-33. https://doi.org/10.1093/nar/gkg033
  47. Wolf JC, Wolfe MJ. A brief overview of nonneoplastic hepatic toxicity in fish. Toxico Pathol. 2005;33:75-85. https://doi.org/10.1080/01926230590890187
  48. Zhu C, Chen Z, Jiang Z. Expression, distribution and role of aquaporin water channels in human and animal stomach and intestines. Int J Mol Sci. 2016;17:1399. https://doi.org/10.3390/ijms17091399
  49. Zhu N, Feng X, He C, Gao H, Yang L, Ma Q, Guo L, Qiao Y, Yang H, Ma T. Defective macrophage function in aquaporin-3 deficiency. FASEB J. 2011;25:4233-9. https://doi.org/10.1096/fj.11-182808

Cited by

  1. Differential Expression and Localization of Branchial AQP1 and AQP3 in Japanese Medaka ( Oryzias latipes ) vol.8, pp.5, 2017, https://doi.org/10.3390/cells8050422
  2. Participation of Na+/K+-ATPase and aquaporins in the uptake of water during moult processes in the shrimp Palaemon argentinus (Nobili, 1901) vol.189, pp.5, 2017, https://doi.org/10.1007/s00360-019-01232-w
  3. Regulation mechanism of aquaporin 9 gene on inflammatory response and cardiac function in rats with myocardial infarction through extracellular signal-regulated kinase1/2 pathway vol.34, pp.12, 2019, https://doi.org/10.1007/s00380-019-01452-8