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Research Articles

Deciphering the role of aquaporin 1 in the adaptation of the stinging catfish Heteropneustes fossilis to environmental hypertonicity by molecular dynamics simulation studies

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Pages 2075-2089 | Received 06 Jan 2021, Accepted 05 Jan 2022, Published online: 18 Jan 2022

References

  • Ahmmed, M. K., Ahmmed, F., Kabir, K. A., Faisal, M., Ahmed, S. I., & Ahsan, M. N. (2017). Biochemical impacts of salinity on the catfish, Heteropneustes fossilis (Bloch, 1794), and possibility of their farming at low saline water. Aquaculture Research, 48(8), 4251–4261. https://doi.org/10.1111/are.13246
  • Allen, W. J., Lemkul, J. A., & Bevan, D. R. (2009). GridMAT-MD: A grid-based membrane analysis tool for use with molecular dynamics. Journal of Computational Chemistry, 30(12), 1952–1958.
  • An, K. W., Kim, N. N., & Choi, C. Y. (2008). Cloning and expression of aquaporin 1 and arginine vasotocin receptor mRNA from the black porgy, Acanthopagrus schlegeli: effect of freshwater acclimation. Fish Physiology and Biochemistry, 34(2), 185–194.
  • Aoki, M., Kaneko, T., Katoh, F., Hasegawa, S., Tsutsui, N., & Aida, K. (2003). Intestinal water absorption through aquaporin 1 expressed in the apical membrane of mucosal epithelial cells in seawater-adapted Japanese eel. The Journal of Experimental Biology, 206(Pt 19), 3495–3505. https://doi.org/10.1242/jeb.00579
  • Aroca, R., Amodeo, G., Fernández-Illescas, S., Herman, E. M., Chaumont, F., & Chrispeels, M. J. (2005). The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiology, 137(1), 341–353.
  • Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1-3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
  • Binesh, A. R., & Kamali, R. (2015). Molecular dynamics insights into human aquaporin 2 water channel. Biophysical Chemistry, 207, 107–113. https://doi.org/10.1016/j.bpc.2015.10.002
  • Chaube, R., Chauvigné, F., Tingaud-Sequeira, A., Joy, K. P., Acharjee, A., Singh, V., & Cerdá, J. (2011). Molecular and functional characterization of catfish (Heteropneustes fossilis) aquaporin-1b: changes in expression during ovarian development and hormone-induced follicular maturation. General and Comparative Endocrinology, 170(1), 162–171.
  • Chen, L. M., Zhao, J., Musa-Aziz, R., Pelletier, M. F., Drummond, I. A., & Boron, W. F. (2010). Cloning and characterization of a zebrafish homologue of human AQP1: A bifunctional water and gas channel. The American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 299, 1163–1174.
  • Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research, 16(22), 10881–10890. https://doi.org/10.1093/nar/16.22.10881
  • Cutler, C. P., & Cramb, G. (2000). Water transport and aquaporin expression in fish. In Hohmann, S. and Nielsen, S. (Eds.), Molecular biology and physiology of water and solute transport (pp. 431–441). Kluwer Academic Press.
  • Das, M., Banerjee, B., Choudhury, M. G., & Saha, N. (2013). Environmental hypertonicity causes induction of gluconeogenesis in the air-breathing singhi catfish, Heteropneustes fossilis. PLoS One, 8(12), e85535. https://doi.org/10.1371/journal.pone.0085535
  • de Groot, B. L., & Grubmüller, H. (2001). Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science (New York, N.Y.), 294(5550), 2353–2357. https://doi.org/10.1126/science.1066115
  • de Groot, B. L., Engel, A., & Grubmuller, H. (2001). A refined structure of human aquaporin 1. FEBS Letters, 504(3), 206–211.
  • Deane, E. E., Luk, J. C., & Woo, N. Y. (2011). Aquaporin 1a expression in gill, intestine, and kidney of the euryhaline silver sea bream. Frontiers in Physiology, 2, 39. https://doi.org/10.3389/fphys.2011.00039
  • Domański, J., Stansfeld, P. J., Sansom, M. S. P., & Beckstein, O. (2010). Lipidbook: A public repository for force field parameters used in membrane simulations. The Journal of Membrane Biology, 236(3), 255–258.
  • Dong, C., Chen, L., Feng, J., Xu, J., Mahboob, S., Al-Ghanim, K., Li, X., & Xu, P. (2016). Genome wide identification, phylogeny, and expression of Aquaporin genes in common carp (Cyprinus carpio). PLoS One, 11(12), e0166160. https://doi.org/10.1371/journal.pone.0166160
  • Giffard-Mena, I., Boulo, V., Aujoulat, F., Fowden, H., Castille, R., Charmantier, G., & Cramb, G. (2007). Aquaporin molecular characterization in the sea-bass (Dicentrarchus labrax): The effect of salinity on AQP1 and AQP3 expression. Comparative Biochemistry & Physiology, 148A, 430–444.
  • Goswami, N., Hussain, I., & Borah, P. (2018). Molecular dynamics approach to probe the antigenicity of PagN – an outer membrane protein of Salmonella Typhi. Journal of Biomolecular Structure & Dynamics, 36(8), 2131–2146.
  • Hadidi, H., Kamali, R., & Binesh, A. (2020). Dynamics and energetics of water transport through aquaporin mutants causing nephrogenic diabetes insipidus (NDI): A molecular dynamics study. Journal of Biomolecular Structure and Dynamics, 1–12. https://doi.org/10.1080/07391102.2020.1824813
  • Hashido, M., Ikeguchi, M., & Kidera, A. (2005). Comparative simulations of aquaporin family: AQP1, AQPZ, AQP0 and GlpF. FEBS Letters, 579(25), 5549–5552. https://doi.org/10.1016/j.febslet.2005.09.018
  • Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447.
  • Heyda, J., Hrobárik, T., & Jungwirth, P. (2009). Ion-specific interactions between halides and basic amino acids in water. The Journal of Physical Chemistry. A, 113(10), 1969–1975. https://doi.org/10.1021/jp807993f
  • http://www.mdtutorials.com/gmx/membrane_protein/Files/water_deletor.pl.
  • https://server.poissonboltzmann.org/.
  • Hub, J. S., & de Groot, B. L. (2008). Mechanism of selectivity in aquaporins and aquaglyceroporins. Proceedings of the National Academy of Sciences of the United States of America, 105(4), 1198–1203. https://doi.org/10.1073/pnas.0707662104
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD – visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
  • Kandt, C., Ash, W. L., & Tieleman, D. P. (2007). Setting up and running molecular dynamics simulations of membrane proteins. Methods (San Diego, Calif.), 41(4), 475–488. https://doi.org/10.1016/j.ymeth.2006.08.006
  • Kim, Y. K., Lee, S. Y., Kim, B. S., Kim, D. S., & Kim, Y. K. N. (2014). Isolation and mRNA expression analysis of aquaporin isoforms in marine medaka Oryzias dancena, a euryhaline teleost. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 171, 1–8.
  • Kim, Y. K., Watanabe, S., Kaneko, T., Huh, M. D., & Park, S. I. (2010). Expression of aquaporins 3, 8 and 10 in the intestines of freshwater and seawater-acclimated Japanese eels Anguilla japonica. Fisheries Science, 76(4), 695–702. https://doi.org/10.1007/s12562-010-0259-x
  • Kirscht, A., Sonntag, Y., Kjellbom, P., & Johanson, U. (2018). A structural preview of aquaporin 8 via homology modeling of seven vertebrate isoforms. BMC Structural Biology, 18(2), 1–15.
  • Kubista, M., Andrade, J. M., Bengtsson, M., Forootan, A., Jonák, J., Lind, K., Sindelka, R., Sjöback, R., Sjögreen, B., Strömbom, L., Ståhlberg, A., & Zoric, N. (2006). The real-time polymerase chain reaction. Molecular Aspects of Medicine, 27(2-3), 95–125. https://doi.org/10.1016/j.mam.2005.12.007
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
  • Law, R. J., & Sansom, M. S. P. (2004). Homology modeling and molecular dynamics simulations: comparative studies of human aquaporin-1. European Biophysics Journal, 33(6), 477–489. https://doi.org/10.1007/s00249-004-0398-z
  • Lee, S. Y., Nam, Y. K., & Kim, Y. K. (2017). Characterization and expression profiles of aquaporins (AQPs) 1a and 3a in mud loach Misgurnus mizolepis after experimental challenges. Fisheries and Aquatic Science, 20(23), 1–9.
  • Lindahl, E., Hess, B., & van der Spoel, D. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7(8), 306–317. https://doi.org/10.1007/s008940100045
  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif.), 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262
  • Ma, Q., Liu, X., Li, A., Liu, S., & Zhuang, Z. (2020). Effects of osmotic stress on the expression profiling of aquaporin genes in the roughskin sculpin (Trachidermus fasciatus). Acta Oceanologica Sinica, 39, 19–25.
  • Maroli, N., Jayakrishnan, A., Manoharan, R. R., Kolandaivel, P., & Krishna, K. (2019). Combined Inhibitory Effects of Citrinin, Ochratoxin-A, and T-2 Toxin on Aquaporin-2. The Journal of Physical Chemistry. B, 123(27), 5755–5768. https://doi.org/10.1021/acs.jpcb.9b03829
  • Martinez, A.-S., Cutler, C. P., Wilson, G. D., Phillips, C., Hazon, N., & Cramb, G. (2005). Cloning and expression of three aquaporin homologues from the European eel (Anguilla anguilla): Effects of seawater acclimation and cortisol treatment on renal expression. Biology of the Cell, 97(8), 615–627. https://doi.org/10.1042/BC20040111
  • Murata, K., Mitsuoka, K., Hirai, T., Walz, T., Agre, P., Heymann, J. B., Engel, A., & Fujiyoshi, Y. (2000). Structural determinants of water permeation through aquaporin-1. Nature, 407(6804), 599–605. https://doi.org/10.1038/35036519
  • Piggot, T. J., Piñeiro, Á., & Khalid, S. (2017). Correction to molecular dynamics simulations of phosphatidylcholine membranes: A comparative force field study. Journal of Chemical Theory and Computation, 13(4), 1862–1865.
  • Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/10.1093/bioinformatics/btt055
  • Ren, G., Reddy, V. S., Cheng, A., Melnyk, P., & Mitra, A. K. (2001). Visualization of a water-selective pore by electron crystallography in vitreous ice. Proceedings of the National Academy of Sciences of the United States of America, 98(4), 1398–1403.
  • Rio, D. C., Ares, M., Jr, Hannon, G. J., & Nilsen, T. W. (2010). Purification of RNA using TRIzol (TRI reagent). Cold Spring Harbor Protocols, 2010(6), pdb.prot5439. https://doi.org/10.1101/pdb.prot5439
  • Rubenstein, D. A., Yin, W., & Frame, M. D. (2015). Intraocular fluid flow. In Biomedical engineering, biofluid mechanics (2nd ed., pp. 355–373), Academic Press. https://doi.org/10.1016/B978-0-12-800944-4.00010-X
  • Ruiz Carrillo, D., To Yiu Ying, J., Darwis, D., Soon, C. H., Cornvik, T., Torres, J., & Lescar, J. (2014). Crystallization and preliminary crystallographic analysis of human aquaporin 1 at a resolution of 3.28 Å. Acta Crystallographica F: Structural Biology Communications, 70(Pt 12), 1657–1663. https://doi.org/10.1107/S2053230X14024558
  • Schmid, N., Eichenberger, A. P., Choutko, A., Riniker, S., Winger, M., Mark, A. E., & van Gunsteren, W. F. (2011). Definition and testing of the GROMOS force-field versions 54A7 and 54B7. European Biophysics Journal : EBJ, 40(7), 843–856. [Database] https://doi.org/10.1007/s00249-011-0700-9
  • Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols, 3(6), 1101–1108. https://doi.org/10.1038/nprot.2008.73
  • Smart, O. S., Goodfellow, J. M., & Wallace, B. A. (1993). The pore dimensions of Gramicidin A. Biophysical Journal, 65(6), 2455–2460.
  • Sui, H., Han, B. G., Lee, J. K., Walian, P., & Jap, B. K. (2001). Structural basis of water-specific transport through the AQP1 water channel. Nature, 414(6866), 872–878. https://doi.org/10.1038/414872a
  • Takata, K., Matsuzaki, T., & Tajika, Y. (2004). Aquaporins: Water channel proteins of the cell membrane. Progress in Histochemistry and Cytochemistry, 39(1), 1–83. https://doi.org/10.1016/j.proghi.2004.03.001
  • Tipsmark, C. K., Sorensen, K. J., & Madsen, S. S. (2010). Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. The Journal of Experimental Biology, 213(3), 368–379. https://doi.org/10.1242/jeb.034785
  • Umenishi, F., & Schrier, R. W. (2002). Identification and Characterization of a Novel Hypertonicity-Responsive Element in the Human Aquaporin-1 Gene. Biochemical and Biophysical Research Communications, 292(3), 771–775.
  • Umenishi, F., & Schrier, R. W. (2003). Hypertonicity-induced aquaporin-1 (AQP1) expression is mediated by the activation of MAPK pathways and hypertonicity-responsive element in the AQP1 gene. Journal of Biological Chemistry, 278(18), 15765–15770. https://doi.org/10.1074/jbc.M209980200
  • van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718.
  • Verkman, A. S., & Mitra, A. K. (2000). Structure and function of aquaporin water channels. American Journal of Physiology. Renal Physiology, 278(1), F13–F28. https://doi.org/10.1152/ajprenal.2000.278.1.F13
  • Watanabe, S., Hirano, T., Grau, E. G., & Kaneko, T. (2009). Osmosensitivity of prolactin cells is enhanced by the water channel aquaporin 3 in a euryhaline Mozambique tilapia (Oreochromis mozambicus). American Journal of Physiology, 296, 446–453.
  • Wistow, G., Pisano, M., & Chepelinsky, A. (1991). Tandem sequence repeats in transmembrane channel proteins. Trends in Biochemical Sciences, 16(5), 170–171.
  • Zhang, Y. J. (2015). Y. I-TASSER server: NEW development for protein structure and function predictions. Nucleic Acids Research, 43, 174–181.

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