Aquaporins: A Multidisciplinary Perspective on the Water Channel Proteins

Aquaporins are unique water channel proteins located at cell membranes that possess high water permeability and high solute rejection. Their primary function is to maintain the osmotic balance of the cells via regulating the water transport. However, their discovery had also provided the scientists to understand the pathophysiology of some diseases. In fact, aquaporins are shown to be strongly related to cancer by taking part in several tumor-related processes such as cell migration, cell proliferation and cell adhesion. Other than their functions in human body, recently, aquaporins have started to be used in engineering biomimetic membranes, for different applications such as desalination. This review investigates the properties and functions of the aquaporins in a multidisciplinary point of view and demonstrates the recent developments in aquaporin-based research.

Kaynakça

[1] Macey, R.L. and R.E.L. Farmer, Inhibition of water and solute permeability in human red cells. Biochimica et Biophysica Acta (BBA) - Biomembranes 1970; 211(1): 104-106.

[2] Benga, G., et al., Water Permeability in Human-Erythrocytes - Identification of Membrane-Proteins Involved in Water Transport. European Journal of Cell Biology 1986; 41(2): 252-262.

[3] Denker, B.M., et al., Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. Journal of Biological Chemistry 1988; 263(30): 15634-42.

[4] Preston, G.M., et al., Appearance of Water Channels in Xenopus Oocytes Expressing Red Cell CHIP28 Protein. Science 1992; 256(5055): 385-387.

[5] Agre, P., et al., Aquaporin CHIP: the archetypal molecular water channel. American Journal of Physiology-Renal Physiology 1993; 265(4): F463-F476.

[6] Agre, P., Aquaporin Water Channels (Nobel Lecture). Angewandte Chemie International Edition, 2004; 43(33): 4278-4290.

[7] Verkman, A.S., M.O. Anderson, and M.C. Papadopoulos, Aquaporins: important but elusive drug targets. Nature Reviews Drug Discovery 2014; 13(4): 259-277.

[8] Tesse, A., et al., Aquaporins as Targets of Dietary Bioactive Phytocompounds. Frontiers in Molecular Biosciences 2018; 5(30): 1-13.

[9] Almasalmeh, A., et al., Structural determinants of the hydrogen peroxide permeability of aquaporins. The FEBS Journal 2014; 281(3): 647-656.

[10] Verkman, A.S. and A.K. Mitra, Structure and function of aquaporin water channels. American Journal of Physiology-Renal Physiology 2000; 278(1): F13-F28.

[11] King, L.S., D. Kozono, and P. Agre, From structure to disease: The evolving tale of aquaporin biology. Nature Reviews Molecular Cell Biology 2004; 5(9): 687-698.

[12] Sui, H., et al., Structural basis of water-specific transport through the AQP1 water channel. Nature 2001; 414(6866): 872-878.

[13] Murata, K., et al., Structural determinants of water permeation through aquaporin-1. Nature 2000; 407(6804): 599-605.

[14] Papadopoulos, M.C. and S. Saadoun, Key roles of aquaporins in tumor biology. Biochimica et Biophysica Acta (BBA) - Biomembranes 2015; 1848(10, Part B): 2576-2583.

[15] Pelagalli, A., et al., Aquaporins in Health and Disease: An Overview Focusing on the Gut of Different Species. International Journal of Molecular Sciences 2016; 17(8): 1213.

[16] Kitchen, P., et al., Beyond water homeostasis: Diverse functional roles of mammalian aquaporins. Biochimica et Biophysica Acta (BBA) - General Subjects 2015; 1850(12): 2410-2421.

[17] Noda, Y., et al., Aquaporins in kidney pathophysiology. Nature Reviews Nephrology 2010; 6(3): 168-178.

[18] Hsu, K., et al., Adaptable interaction between aquaporin-1 and band 3 reveals a potential role of water channel in blood CO(2) transport. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 2017; 31(10): 4256-4264.

[19] Ma, T., et al., Defective Secretion of Saliva in Transgenic Mice Lacking Aquaporin-5 Water Channels. Journal of Biological Chemistry 1999; 274(29): 20071-20074.8

[20] Huisjes, R., et al., Squeezing for Life - Properties of Red Blood Cell Deformability. Frontiers in physiology 2018; 9: 656-656.

[21] Loitto, V.-M., et al., Neutrophil leukocyte motility requires directed water influx. Journal of Leukocyte Biology 2002; 71(2): 212-222.

[22] Saadoun, S., et al., Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. Journal of Cell Science 2005; 118(24): 5691-5698.

[23] Auguste, K.I., et al., Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. The FASEB Journal 2007; 21(1): 108-116.

[24] Ruiz-Ederra, J. and A.S. Verkman, Aquaporin-1-facilitated keratocyte migration in cell culture and in vivo corneal wound healing models. Experimental Eye Research 2009; 89(2): 159-165.

[25] Bisi, S., et al., Membrane and actin dynamics interplay at lamellipodia leading edge. Current Opinion in Cell Biology 2013; 25(5): 565-573.

[26] Papadopoulos, M.C., S. Saadoun, and A.S. Verkman, Aquaporins and cell migration. Pflügers Archiv - European Journal of Physiology 2008; 456(4): 693-700.

[27] Stroka, Kimberly M., et al., Water Permeation Drives Tumor Cell Migration in Confined Microenvironments. Cell 2014; 157(3): 611-623.

[28] Zhang, H. and A.S. Verkman, Evidence against Involvement of Aquaporin-4 in Cell–Cell Adhesion. Journal of Molecular Biology 2008; 382(5): 1136-1143.

[29] Kasa, P., et al., Aquaporins in female specific cancers. Gene 2019; 700: 60-64.

[30] Verkman, A.S., M. Hara-Chikuma, and M.C. Papadopoulos, Aquaporins—new players in cancer biology. Journal of Molecular Medicine 2008; 86(5): 523-529.

[31] Hu, J. and A.S. Verkman, Increased migration and metastatic potential of tumor cells expressing aquaporin water channels. The FASEB Journal 2006; 20(11): 1892-1894.

[32] Maltaneri, R.E., et al., Aquaporin-1 plays a key role in erythropoietin-induced endothelial cell migration. Biochimica et biophysica acta. Molecular cell research 2020; 1867(1): 118569.

[33] Direito, I., et al., Differential expression of aquaporin-3 and aquaporin-5 in pancreatic ductal adenocarcinoma. Journal of Surgical Oncology 2017; 115(8): 980-996.

[34] Zou, W., et al., AQP1 and AQP3 Expression are Associated With Severe Symptoms and Poor-prognosis of the Pancreatic Ductal Adenocarcinoma. Applied Immunohistochemistry & Molecular Morphology 2019; 27(1): 40-47.

[35] Huang, X., L. Huang, and M. Shao, Aquaporin 3 facilitates tumor growth in pancreatic cancer by modulating mTOR signaling. Biochemical and Biophysical Research Communications 2017; 486(4): 1097-1102.

[36] Wei, M., et al., Decreased expression of aquaporin 1 correlates with clinicopathological features of patients with cervical cancer. OncoTargets and therapy 2019; 12: 2843-2851.

[37] Bründl, J., et al., Expression, localisation and potential significance of aquaporins in benign and malignant human prostate tissue. BMC urology 2018; 18(1): 75-75.

[38] Rossi, L., et al., Urinary Excretion of Kidney Aquaporins as Possible Diagnostic Biomarker of Diabetic Nephropathy. Journal of diabetes research 2017; 2017: 4360357-4360357.

[39] Huber, V.J., M. Tsujita, and T. Nakada, Aquaporins in drug discovery and pharmacotherapy. Molecular Aspects of Medicine 2012; 33(5): 691-703.

[40] Calamita, G., J. Perret, and C. Delporte, Aquaglyceroporins: Drug Targets for Metabolic Diseases? Frontiers in physiology 2018; 9: 851-851.

[41] Nicchia, G.P., et al., Inhibition of aquaporin-1 dependent angiogenesis impairs tumour growth in a mouse model of melanoma. Journal of Molecular Medicine 2013; 91(5): 613-623.

[42] Shu, C., et al., Inhibitory effect of AQP1 silencing on adhesion and angiogenesis in ectopic endometrial cells of mice with endometriosis through activating the Wnt signaling pathway. Cell Cycle 2019; 18(17): 2026-2039.

[43] de Almeida, A., et al., The mechanism of aquaporin inhibition by gold compounds elucidated by biophysical and computational methods. Chemical Communications 2017; 53(27): 3830-3833.

[44] Spinello, A., et al., The inhibition of glycerol permeation through aquaglyceroporin-3 induced by mercury(II): A molecular dynamics study. Journal of Inorganic Biochemistry 2016; 160: 78-84.

[45] Sonntag, Y., et al., Identification and characterization of potent and selective aquaporin-3 and aquaporin-7 inhibitors. The Journal of biological chemistry 2019; 294(18): 7377-7387.

[46] Yadav, D.K., et al., Computational Modeling on Aquaporin-3 as Skin Cancer Target: A Virtual Screening Study. Frontiers in chemistry 2020; 8: 250-250.

[47] Ben, Y., et al., Upregulation of AQP3 and AQP5 induced by dexamethasone and ambroxol in A549 cells. Respiratory physiology & neurobiology 2008; 161(2): 111-118.

[48] Chang, Y.-L., et al., Dexamethasone attenuates methacholine-mediated aquaporin 5 downregulation in human nasal epithelial cells via suppression of NF-κB activation. International Forum of Allergy & Rhinology 2018; 8(1): 64-71.

[49] Rump, K., et al., DNA methylation of a NF-κB binding site in the aquaporin 5 promoter impacts on mortality in sepsis. Scientific Reports 2019; 9(1): 18511.

[50] da Silva, I.V., et al., Revisiting the metabolic syndrome: the emerging role of aquaglyceroporins. Cellular and Molecular Life Sciences 2018; 75(11): 1973-1988.

[51] Madeira, A., T.F. Moura, and G. Soveral, Aquaglyceroporins: implications in adipose biology and obesity. Cellular and Molecular Life Sciences 2015; 72(4): 759-771.

[52] Baldini, F., et al., Aquaporin-9 is involved in the lipid-lowering activity of the nutraceutical silybin on hepatocytes through modulation of autophagy and lipid droplets composition. Biochimica et biophysica acta. Molecular and cell biology of lipids 2020; 1865(3): 158586.

[53] Tradtrantip, L., et al., Aquaporin-Targeted Therapeutics: State-of-the-Field, in Aquaporins, B. Yang, Editor. 2017, Springer Netherlands: Dordrecht. 239-250.

[54] Barboiu, M., Artificial water channels – incipient innovative developments. Chemical Communications 2016; 52(33): 5657-5665.

[55] Kumar, M., et al., Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z. Proceedings of the National Academy of Sciences 2007; 104(52): 20719-20724.

[56] Shen, Y.-x., et al., Biomimetic membranes: A review. Journal of Membrane Science 2014; 454: 359-381.

[57] Farinas, J. and A.S. Verkman, Cell volume and plasma membrane osmotic water permeability in epithelial cell layers measured by interferometry. Biophysical Journal 1996; 71(6): 3511-3522.

[58] Jakowiecki, J., et al., Aquaporin-graphene interface: relevance to point-of-care device for renal cell carcinoma and desalination. Interface focus 2018; 8(3): 20170066-20170066.

[59] Li, X., et al., Nature gives the best solution for desalination: Aquaporin-based hollow fiber composite membrane with superior performance. Journal of Membrane Science 2015; 494: 68-77.

[60] Tang, C.Y., et al., Desalination by biomimetic aquaporin membranes: Review of status and prospects. Desalination 2013; 308: 34-40.

[61] Li, X., et al., Preparation of supported lipid membranes for aquaporin Z incorporation. Colloids and Surfaces B: Biointerfaces 2012; 94: 333-340.

[62] Wang, M., et al., Layer-by-Layer Assembly of Aquaporin Z-Incorporated Biomimetic Membranes for Water Purification. Environmental Science & Technology 2015; 49(6): 3761-3768.

[63] Werber, J., C. Osuji, and M. Elimelech, Materials for Next-Generation Desalination and Water Purification Membranes. Nature Reviews Materials 2016; 1: 16018.

[64] Masuda, K., et al., Fabrication and Conductive Properties of Multilayered Ultrathin Films Designed by Layer-byLayer Assembly of Water-Soluble Fullerenes. Langmuir 2010; 26(16): 13472-13478.

[65] Madsen, H., et al., Use of biomimetic forward osmosis membrane for trace organics removal. Journal of Membrane Science 2015; 476: 469-474.

[66] Luo, W., et al., Biomimetic aquaporin membranes for osmotic membrane bioreactors: Membrane performance and contaminant removal. Bioresource Technology 2018; 249: 62-68.

[67] Uduman, N., et al., Marine microalgae flocculation and focused beam reflectance measurement. Chemical Engineering Journal 2010; 162: 935-940.

[68] Munshi, F., et al., Dewatering using an AquaporinBased Polyethersulfone Forward Osmosis Membrane. Separation and Purification Technology 2018; 204: 154-161.

[69] Li, Y., et al., Fabrication of aquaporin-based biomimetic membrane for seawater desalination. Desalination 2019; 467: 103-112.

[70] Li, Z., et al., Aquaporin based biomimetic membrane in forward osmosis: Chemical cleaning resistance and practical operation. Desalination 2017; 420: 208-215.

Kaynak Göster