DOI: https://doi.org/10.25305/unj.156586

Cerebrospinal fluid flow. Part 2. Aquaporins and their role in CNS water homeostasis

Ievgenii I. Slynko, Alexey S. Nekhlopochin, Tatyana A. Malysheva

Abstract


The capabilities of the central nervous system to receive, integrate and process the incoming information, as well as to ensure an adequate timely response, are directly determined by the ability to maintain the electrochemical gradient of ions, a certain concentration of organic molecules and the transport of water through the plasma membrane of nerve cells. This dynamic disequilibrium is a key mechanism in the generation and transmission of information in neuronal intercellular communication, in the activation of extracellular signaling molecules, and in the metabolic support of the neural tissue.

It is obvious that maintaining stable homeostasis in the central nervous system is strictly regulated by the mechanisms of ion transport, organic and inorganic molecules, and water. Astrocytes provided with proteins of ionic and aqueous transmembrane channels communicate with neurons and cells lining the cavities filled with fluid. So astroglia is the basic element in achieving such homeostatic regulation of the CNS.

Astroglial-mediated homeostasis is highly dynamic, and it has been proven that the disruption of surface expression and the polarization of transport proteins in astroglial cells underlies various pathological conditions.

The discovery and further investigation of functional characteristics of specialized water channels — aquaporins was one of the milestones in the study of the mechanisms for maintaining water homeostasis of CNS. The present review deals with base ideas concerning the role of aquaporins in the processes of water transport, such as regulating cell volume, controlling the size of extracellular space, production and drainage of cerebrospinal fluid. Certain pathological conditions caused by a violation of water homeostasis and the drainage system of the central nervous system are considered.


Keywords


cerebrospinal fluid; water homeostasis; aquaporins; water channels

References


1. Badaut J, Fukuda AM, Jullienne A, Petry KG. Aquaporin and brain diseases. Biochim. Biophys. Acta - Gen. Subj. 2014 May;1840(5):1554-65. [CrossRef] [PubMed]

2. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S. Aquaporin water channels--from atomic structure to clinical medicine. J. Physiol. 2002 Jul 1;542(Pt 1):3-16. [CrossRef] [PubMed]

3. Verkman AS, Anderson MO, Papadopoulos MC. Aquaporins: important but elusive drug targets. Nat. Rev. Drug Discov. 2014 Apr;13(4):259-77. [CrossRef] [PubMed]

4. Tait MJ, Saadoun S, Bell BA, Papadopoulos MC. Water movements in the brain: role of aquaporins. Trends Neurosci. 2008 Jan;31(1):37-43. [CrossRef] [PubMed]

5. MacAulay N, Zeuthen T. Water transport between CNS compartments: contributions of aquaporins and cotransporters. Neuroscience 2010 Jul 28;168(4):941-56. [CrossRef] [PubMed]

6. Bering EA. Water Exchange of Central Nervous System and Cerebrospinal Fluid. J. Neurosurg. 1952 May;9(3):275-87. [CrossRef] [PubMed]

7. Bateman GA. Extending the hydrodynamic hypothesis in chronic hydrocephalus. Neurosurg. Rev. 2005 Oct 12;28(4):333-4. [CrossRef] [PubMed]

8. Sidel VW, Solomon AK. Entrance of water into human red cells under an osmotic pressure gradient. J. Gen. Physiol. 1957 Nov 20;41(2):243-57. [CrossRef] [PubMed]

9. Denker BM, Smith BL, Kuhajda FP, Agre P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 1988 Oct 25;263(30):15634-42. [PubMed]

10. Agre P, Saboori AM, Asimos A, Smith BL. Purification and partial characterization of the Mr 30,000 integral membrane protein associated with the erythrocyte Rh(D) antigen. J. Biol. Chem. 1987 Dec 25;262(36):17497-503. [PubMed]

11. Preston GM, Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: member of an ancient channel family. Proc. Natl. Acad. Sci. U. S. A. 1991 Dec 15;88(24):11110-4. [CrossRef] [PubMed]

12. van Hoek AN, Hom ML, Luthjens LH, de Jong MD, Dempster JA, van Os CH. Functional unit of 30 kDa for proximal tubule water channels as revealed by radiation inactivation. J. Biol. Chem. 1991 Sep 5;266(25):16633-5. [PubMed]

13. Gorin MB, Yancey SB, Cline J, Revel JP, Horwitz J. The major intrinsic protein (MIP) of the bovine lens fiber membrane: characterization and structure based on cDNA cloning. Cell 1984 Nov;39(1):49-59. [CrossRef] [PubMed]

14. Agre P, Sasaki S, Chrispeels MJ. Aquaporins: a family of water channel proteins. Am. J. Physiol. Physiol. 1993 Sep;265(3):F461-F461. [CrossRef] [PubMed]

15. Agre P. Molecular physiology of water transport: aquaporin nomenclature workshop. Mammalian aquaporins. Biol. cell 1997 Aug;89(5-6):255-7. [CrossRef] [PubMed]

16. Heymann JB, Agre P, Engel A. Progress on the Structure and Function of Aquaporin 1. J. Struct. Biol. 1998;121(2):191-206. [CrossRef] [PubMed]

17. Abascal F, Irisarri I, Zardoya R. Diversity and evolution of membrane intrinsic proteins. Biochim. Biophys. Acta - Gen. Subj. 2014 May;1840(5):1468-81. [CrossRef] [PubMed]

18. Finn RN, Cerdà J. Evolution and Functional Diversity of Aquaporins. Biol. Bull. 2015 Aug;229(1):6-23. [CrossRef] [PubMed]

19. Day RE, Kitchen P, Owen DS, Bland C, Marshall L, Conner AC, Bill RM, Conner MT. Human aquaporins: Regulators of transcellular water flow. Biochim. Biophys. Acta - Gen. Subj. 2014 May;1840(5):1492-506. [CrossRef] [PubMed]

20. Ishibashi K, Tanaka Y, Morishita Y. The role of mammalian superaquaporins inside the cell. Biochim. Biophys. Acta - Gen. Subj. 2014 May;1840(5):1507-12. [CrossRef] [PubMed]

21. Xu M, Xiao M, Li S, Yang B. Aquaporins in Nervous System. Adv. Exp. Med. Biol. 2017;969:81-103. [CrossRef] [PubMed]

22. Verkman AS, Mitra AK. Structure and function of aquaporin water channels. Am. J. Physiol. Physiol. 2000 Jan;278(1):F13-28. [CrossRef] [PubMed]

23. Kimelberg HK. Water homeostasis in the brain: Basic concepts. Neuroscience 2004 Jan;129(4):851-60. [CrossRef] [PubMed]

24. Maugeri R, Schiera G, Di Liegro C, Fricano A, Iacopino D, Di Liegro I. Aquaporins and Brain Tumors. Int. J. Mol. Sci. 2016 Jun 29;17(7):1029. [CrossRef] [PubMed]

25. De Ieso ML, Yool AJ. Mechanisms of Aquaporin-Facilitated Cancer Invasion and Metastasis. Front. Chem. 2018;6:135. [CrossRef] [PubMed]

26. Zabad RK, Stewart R, Healey KM. Pattern Recognition of the Multiple Sclerosis Syndrome. Brain Sci. 2017 Oct 24;7(10) [CrossRef] [PubMed]

27. Bernitsas E. Pathophysiology and Imaging Diagnosis of Demyelinating Disorders. Brain Sci. 2018 Mar 14;8(3) [CrossRef] [PubMed]

28. Verkhratsky A, Nedergaard M. Physiology of Astroglia. Physiol. Rev. 2018;98(1):239-389. [CrossRef] [PubMed]

29. Oshio K, Watanabe H, Song Y, Verkman AS, Manley GT. Reduced cerebrospinal fluid production and intracranial pressure in mice lacking choroid plexus water channel Aquaporin-1. FASEB J. 2005 Jan;19(1):76-8. [CrossRef] [PubMed]

30. Shields SD, Mazario J, Skinner K, Basbaum AI. Anatomical and functional analysis of aquaporin 1, a water channel in primary afferent neurons. Pain 2007 Sep;131(1):8-20. [CrossRef] [PubMed]

31. Fukuda AM, Pop V, Spagnoli D, Ashwal S, Obenaus A, Badaut J. Delayed increase of astrocytic aquaporin 4 after juvenile traumatic brain injury: Possible role in edema resolution? Neuroscience 2012 Oct 11;222:366-78. [CrossRef] [PubMed]

32. Yang W, Tan Z, Dong D, Ding Y, Meng H, Zhao Y, Xin X, Bi W. Association of aquaporin-1 with tumor migration, invasion and vasculogenic mimicry in glioblastoma multiforme. Mol. Med. Rep. 2017 Dec 12;17(2):3206-11. [CrossRef] [PubMed]

33. El Hindy N, Rump K, Lambertz N, Zhu Y, Frey UH, Bankfalvi A, Siffert W, Sure U, Peters J, Adamzik M, Sandalcioglu IE. The functional Aquaporin 1 -783G/C-polymorphism is associated with survival in patients with glioblastoma multiforme. J. Surg. Oncol. 2013 Dec;108(7):492-8. [CrossRef] [PubMed]

34. Johnson MD, O’Connell M. Na-K-2Cl cotransporter and aquaporin 1 in arachnoid granulations, meningiomas, and meningiomas invading dura. Hum. Pathol. 2013 Jun;44(6):1118-24. [CrossRef] [PubMed]

35. Stroka KM, Jiang H, Chen S-H, Tong Z, Wirtz D, Sun SX, Konstantopoulos K. Water Permeation Drives Tumor Cell Migration in Confined Microenvironments. Cell 2014 Apr 24;157(3):611-23. [CrossRef] [PubMed]

36. Papadopoulos MC, Saadoun S. Key roles of aquaporins in tumor biology. Biochim. Biophys. Acta - Biomembr. 2015 Oct;1848(10):2576-83. [CrossRef] [PubMed]

37. Hoshi A, Tsunoda A, Tada M, Nishizawa M, Ugawa Y, Kakita A. Expression of Aquaporin 1 and Aquaporin 4 in the Temporal Neocortex of Patients with Parkinson’s Disease. Brain Pathol. 2017 Mar;27(2):160-8. [CrossRef] [PubMed]

38. Nesic O, Lee J, Unabia GC, Johnson K, Ye Z, Vergara L, Hulsebosch CE, Perez-Polo JR. Aquaporin 1 - a novel player in spinal cord injury. J. Neurochem. 2008 May;105(3):628-40. [CrossRef] [PubMed]

39. Noell S, Fallier-Becker P, Mack AF, Hoffmeister M, Beschorner R, Ritz R. Water Channels Aquaporin 4 and -1 Expression in Subependymoma Depends on the Localization of the Tumors. PLoS One 2015 Jun 26;10(6):e0131367. [CrossRef] [PubMed]

40. El Hindy N, Bankfalvi A, Herring A, Adamzik M, Lambertz N, Zhu Y, Siffert W, Sure U, Sandalcioglu IE. Correlation of aquaporin-1 water channel protein expression with tumor angiogenesis in human astrocytoma. Anticancer Res. 2013 Feb;33(2):609-13. [PubMed]

41. Kim JH, Lee YW, Park KA, Lee WT, Lee JE. Agmatine Attenuates Brain Edema through Reducing the Expression of Aquaporin-1 after Cerebral Ischemia. J. Cereb. Blood Flow Metab. 2010 May 23;30(5):943-9. [CrossRef] [PubMed]

42. Oshio K, Watanabe H, Yan D, Verkman AS, Manley GT. Impaired pain sensation in mice lacking Aquaporin-1 water channels. Biochem. Biophys. Res. Commun. 2006 Mar 24;341(4):1022-8. [CrossRef] [PubMed]

43. Ma T, Frigeri A, Hasegawa H, Verkman AS. Cloning of a water channel homolog expressed in brain meningeal cells and kidney collecting duct that functions as a stilbene-sensitive glycerol transporter. J. Biol. Chem. 1994 Aug 26;269(34):21845-9. [PubMed]

44. Yang M, Gao F, Liu H, Yu WH, He GQ, Zhuo F, Qiu GP, Sun SQ. Immunolocalization of Aquaporins in Rat Brain. Anat. Histol. Embryol. 2011 Aug;40(4):299-306. [CrossRef] [PubMed]

45. Li X, Lei T, Xia T, Chen X, Feng S, Chen H, Chen Z, Peng Y, Yang Z. Molecular characterization, chromosomal and expression patterns of three aquaglyceroporins (AQP3, 7, 9) from pig. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2008 Mar;149(3):468-76. [CrossRef] [PubMed]

46. Yang M, Gao F, Liu H, Yu WH, Sun SQ. Temporal changes in expression of aquaporin3, -4, -5 and -8 in rat brains after permanent focal cerebral ischemia. Brain Res. 2009 Sep 22;1290:121-32. [CrossRef] [PubMed]

47. Oklinski MK, Skowronski MT, Skowronska A, Rützler M, Nørgaard K, Nieland JD, Kwon TH, Nielsen S. Aquaporins in the Spinal Cord. Int. J. Mol. Sci. 2016 Dec 7;17(12):2050. [CrossRef] [PubMed]

48. Nicchia GP, Pisani F, Simone L, Cibelli A, Mola MG, Dal Monte M, Frigeri A, Bagnoli P, Svelto M. Glio-vascular modifications caused by Aquaporin-4 deletion in the mouse retina. Exp. Eye Res. 2016 May;146:259-68. [CrossRef] [PubMed]

49. Wu X, Zhang J-T, Li D, Zhou J, Yang J, Zheng H-L, Chen J-G, Wang F. Aquaporin-4 deficiency facilitates fear memory extinction in the hippocampus through excessive activation of extrasynaptic GluN2B-containing NMDA receptors. Neuropharmacology 2017 Jan;112(Pt A):124-34. [CrossRef] [PubMed]

50. Papadopoulos MC, Verkman AS. Aquaporin water channels in the nervous system. Nat. Rev. Neurosci. 2013 Apr 13;14(4):265-77. [CrossRef] [PubMed]

51. Hsu MS, Seldin M, Lee DJ, Seifert G, Steinhäuser C, Binder DK. Laminar-specific and developmental expression of aquaporin-4 in the mouse hippocampus. Neuroscience 2011 Mar 31;178:21-32. [CrossRef] [PubMed]

52. Hubbard JA, Hsu MS, Seldin MM, Binder DK. Expression of the Astrocyte Water Channel Aquaporin-4 in the Mouse Brain. ASN Neuro 2015 Oct 15;7(5):175909141560548. [CrossRef] [PubMed]

53. Lan Y-L, Zhao J, Ma T, Li S. The Potential Roles of Aquaporin 4 in Alzheimer’s Disease. Mol. Neurobiol. 2016 Oct 3;53(8):5300-9. [CrossRef] [PubMed]

54. Kress BT, Iliff JJ, Xia M, Wang M, Wei HS, Zeppenfeld D, Xie L, Kang H, Xu Q, Liew JA, Plog BA, Ding F, Deane R, Nedergaard M. Impairment of paravascular clearance pathways in the aging brain. Ann. Neurol. 2014 Dec;76(6):845-61. [CrossRef] [PubMed]

55. Smith AJ, Jin B-J, Ratelade J, Verkman AS. Aggregation state determines the localization and function of M1– and M23–aquaporin-4 in astrocytes. J. Cell Biol. 2014 Feb 17;204(4):559-73. [CrossRef] [PubMed]

56. Stokum JA, Gerzanich V, Simard JM. Molecular pathophysiology of cerebral edema. J. Cereb. Blood Flow Metab. 2016 Mar 16;36(3):513-38. [CrossRef] [PubMed]

57. Hirt L, Fukuda AM, Ambadipudi K, Rashid F, Binder D, Verkman A, Ashwal S, Obenaus A, Badaut J. Improved long-term outcome after transient cerebral ischemia in aquaporin-4 knockout mice. J. Cereb. Blood Flow Metab. 2017 Jan 20;37(1):277-90. [CrossRef] [PubMed]

58. Du K-X, Dong Y, Zhang Y, Hou L-W, Fan D-X, Luo Y, Zhang X-L, Jia T-M, Lou J-Y. Effects of dexamethasone on aquaporin-4 expression in brain tissue of rat with bacterial meningitis. Int. J. Clin. Exp. Pathol. 2015;8(3):3090-6. [PubMed]

59. Tang G, Yang G-Y. Aquaporin-4: A Potential Therapeutic Target for Cerebral Edema. Int. J. Mol. Sci. 2016 Sep 29;17(10):1413. [CrossRef] [PubMed]

60. Jurynczyk M, Geraldes R, Probert F, Woodhall MR, Waters P, Tackley G, DeLuca G, Chandratre S, Leite MI, Vincent A, Palace J. Distinct brain imaging characteristics of autoantibody-mediated CNS conditions and multiple sclerosis. Brain 2017 Mar 1;140(3):617-27. [CrossRef] [PubMed]

61. Yao X, Uchida K, Papadopoulos MC, Zador Z, Manley GT, Verkman AS. Mildly Reduced Brain Swelling and Improved Neurological Outcome in Aquaporin-4 Knockout Mice following Controlled Cortical Impact Brain Injury. J. Neurotrauma 2015 Oct 1;32(19):1458-64. [CrossRef] [PubMed]

62. Hubbard JA, Szu JI, Binder DK. The role of aquaporin-4 in synaptic plasticity, memory and disease. Brain Res. Bull. 2018 Jan;136:118-29. [CrossRef] [PubMed]

63. Ikeshima-Kataoka H. Neuroimmunological Implications of AQP4 in Astrocytes. Int. J. Mol. Sci. 2016 Aug 10;17(8):1306. [CrossRef] [PubMed]

64. Ximenes-da-Silva A. Metal Ion Toxins and Brain Aquaporin-4 Expression: An Overview. Front. Neurosci. 2016;10:233. [CrossRef] [PubMed]

65. Iuso A, Kriћaj D. TRPV4-AQP4 interactions ‘turbocharge’ astroglial sensitivity to small osmotic gradients. Channels 2016 May 3;10(3):172-4. [CrossRef] [PubMed]

66. Geng X, Yang B. Transport Characteristics of Aquaporins. Adv. Exp. Med. Biol. 2017;969:51-62. [CrossRef] [PubMed]

67. Wu Q, Zhang Y-J, Gao J-Y, Li X-M, Kong H, Zhang Y-P, Xiao M, Shields CB, Hu G. Aquaporin-4 Mitigates Retrograde Degeneration of Rubrospinal Neurons by Facilitating Edema Clearance and Glial Scar Formation After Spinal Cord Injury in Mice. Mol. Neurobiol. 2014 Jun 4;49(3):1327-37. [CrossRef] [PubMed]

68. Juenemann M, Braun T, Doenges S, Nedelmann M, Mueller C, Bachmann G, Singh P, Blaes F, Gerriets T, Tschernatsch M. Aquaporin-4 autoantibodies increase vasogenic edema formation and infarct size in a rat stroke model. BMC Immunol. 2015 May 20;16:30. [CrossRef] [PubMed]

69. Chen J-Q, Zhang C-C, Jiang S-N, Lu H, Wang W. Effects of Aquaporin 4 Knockdown on Brain Edema of the Uninjured Side After Traumatic Brain Injury in Rats. Med. Sci. Monit. 2016 Dec 8;22:4809-19. [CrossRef] [PubMed]

70. Engelhardt B, Liebner S. Novel insights into the development and maintenance of the blood–brain barrier. Cell Tissue Res. 2014 Mar 4;355(3):687-99. [CrossRef] [PubMed]

71. DeStefano JG, Jamieson JJ, Linville RM, Searson PC. Benchmarking in vitro tissue-engineered blood–brain barrier models. Fluids Barriers CNS 2018 Dec 4;15(1):32. [CrossRef] [PubMed]

72. Jeong S. Molecular and Cellular Basis of Neurodegeneration in Alzheimer’s Disease. Mol. Cells 2017 Sep 30;40(9):613-20. [CrossRef] [PubMed]

73. Xia M, Yang L, Sun G, Qi S, Li B. Mechanism of depression as a risk factor in the development of Alzheimer’s disease: the function of AQP4 and the glymphatic system. Psychopharmacology (Berl). 2017 Feb 12;234(3):365-79. [CrossRef] [PubMed]

74. Plog BA, Nedergaard M. The Glymphatic System in Central Nervous System Health and Disease: Past, Present, and Future. Annu. Rev. Pathol. Mech. Dis. 2018 Jan 24;13(1):379-94. [CrossRef] [PubMed]

75. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M. A Paravascular Pathway Facilitates CSF Flow Through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid. Sci. Transl. Med. 2012 Aug 15;4(147):147ra111-147ra111. [CrossRef] [PubMed]

76. Bucchieri F, Farina F, Zummo G, Cappello F. Lymphatic vessels of the dura mater: a new discovery? J. Anat. 2015 Nov;227(5):702-3. [CrossRef] [PubMed]

77. Morris AWJ, Sharp MM, Albargothy NJ, Fernandes R, Hawkes CA, Verma A, Weller RO, Carare RO. Vascular basement membranes as pathways for the passage of fluid into and out of the brain. Acta Neuropathol. 2016 May 14;131(5):725-36. [CrossRef] [PubMed]

78. Jessen NA, Munk ASF, Lundgaard I, Nedergaard M. The Glymphatic System: A Beginner’s Guide. Neurochem. Res. 2015 Dec 7;40(12):2583-99. [CrossRef] [PubMed]

79. Peng W, Achariyar TM, Li B, Liao Y, Mestre H, Hitomi E, Regan S, Kasper T, Peng S, Ding F, Benveniste H, Nedergaard M, Deane R. Suppression of glymphatic fluid transport in a mouse model of Alzheimer’s disease. Neurobiol. Dis. 2016 Sep;93:215-25. [CrossRef] [PubMed]

80. Nwaobi SE, Cuddapah VA, Patterson KC, Randolph AC, Olsen ML. The role of glial-specific Kir4.1 in normal and pathological states of the CNS. Acta Neuropathol. 2016 Jul 9;132(1):1-21. [CrossRef] [PubMed]

81. Nagelhus EA, Mathiisen TM, Ottersen OP. Aquaporin-4 in the central nervous system: Cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 2004 Jan;129(4):905-13. [CrossRef] [PubMed]

82. Nagelhus EA, Horio Y, Inanobe A, Fujita A, Haug FM, Nielsen S, Kurachi Y, Ottersen OP. Immunogold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia 1999 Mar;26(1):47-54. [CrossRef] [PubMed]

83. Zhang H, Verkman AS. Aquaporin-4 independent Kir4.1 K+ channel function in brain glial cells. Mol. Cell. Neurosci. 2008 Jan;37(1):1-10. [CrossRef] [PubMed]

84. Haj-Yasein NN, Bugge CE, Jensen V, Østby I, Ottersen OP, Hvalby Ø, Nagelhus EA. Deletion of aquaporin-4 increases extracellular K+ concentration during synaptic stimulation in mouse hippocampus. Brain Struct. Funct. 2015 Jul 18;220(4):2469-74. [CrossRef] [PubMed]

85. Syková E, Chvátal A. Glial cells and volume transmission in the CNS. Neurochem. Int. 2000 Apr;36(4-5):397-409. [CrossRef] [PubMed]

86. Mola MG, Sparaneo A, Gargano CD, Spray DC, Svelto M, Frigeri A, Scemes E, Nicchia GP. The speed of swelling kinetics modulates cell volume regulation and calcium signaling in astrocytes: A different point of view on the role of aquaporins. Glia 2016 Jan;64(1):139-54. [CrossRef] [PubMed]

87. Thrane AS, Rappold PM, Fujita T, Torres A, Bekar LK, Takano T, Peng W, Wang F, Rangroo Thrane V, Enger R, Haj-Yasein NN, Skare O, Holen T, Klungland A, Ottersen OP, Nedergaard M, Nagelhus EA. Critical role of aquaporin-4 (AQP4) in astrocytic Ca2+ signaling events elicited by cerebral edema. Proc. Natl. Acad. Sci. 2011 Jan 11;108(2):846-51. [CrossRef] [PubMed]

88. Jo AO, Ryskamp DA, Phuong TTT, Verkman AS, Yarishkin O, MacAulay N, Kri aj D. TRPV4 and AQP4 Channels Synergistically Regulate Cell Volume and Calcium Homeostasis in Retinal Muller Glia. J. Neurosci. 2015 Sep 30;35(39):13525-37. [CrossRef] [PubMed]

89. Filippidis AS, Carozza RB, Rekate HL. Aquaporins in Brain Edema and Neuropathological Conditions. Int. J. Mol. Sci. 2016 Dec 28;18(1) [CrossRef] [PubMed]

90. Allen NJ. Astrocyte Regulation of Synaptic Behavior. Annu. Rev. Cell Dev. Biol. 2014 Oct 11;30(1):439-63. [CrossRef] [PubMed]

91. Enger R, Dukefoss DB, Tang W, Pettersen KH, Bjørnstad DM, Helm PJ, Jensen V, Sprengel R, Vervaeke K, Ottersen OP, Nagelhus EA. Deletion of Aquaporin-4 Curtails Extracellular Glutamate Elevation in Cortical Spreading Depression in Awake Mice. Cereb. Cortex 2017 Jan 1;27(1):24-33. [CrossRef] [PubMed]

92. Szu JI, Binder DK. The Role of Astrocytic Aquaporin-4 in Synaptic Plasticity and Learning and Memory. Front. Integr. Neurosci. 2016 Feb 24;10:8. [CrossRef] [PubMed]

93. Lan Y-L, Wang X, Lou J-C, Ma X-C, Zhang B. The potential roles of aquaporin 4 in malignant gliomas. Oncotarget 2017 May 9;8(19):32345-55. [CrossRef] [PubMed]

94. Michalski D, Pitsch R, Pillai DR, Mages B, Aleithe S, Grosche J, Martens H, Schlachetzki F, Härtig W. Delayed histochemical alterations within the neurovascular unit due to transient focal cerebral ischemia and experimental treatment with neurotrophic factors. PLoS One 2017;12(4):e0174996. [CrossRef] [PubMed]

95. Zhang C, Chen J, Lu H. Expression of aquaporin-4 and pathological characteristics of brain injury in a rat model of traumatic brain injury. Mol. Med. Rep. 2015 Nov;12(5):7351-7. [CrossRef] [PubMed]

96. Clйment T, Rodriguez-Grande B, Badaut J. Aquaporins in brain edema. J. Neurosci. Res. 2018 Nov 15; [CrossRef] [PubMed]

97. Hirt L, Ternon B, Price M, Mastour N, Brunet J-F, Badaut J. Protective role of early aquaporin 4 induction against postischemic edema formation. J. Cereb. Blood Flow Metab. 2009 Feb 5;29(2):423-33. [CrossRef] [PubMed]

98. Hsu Y, Tran M, Linninger AA. Dynamic regulation of aquaporin-4 water channels in neurological disorders. Croat. Med. J. 2015 Oct;56(5):401-21. [CrossRef] [PubMed]

99. Vella J, Zammit C, Di Giovanni G, Muscat R, Valentino M. The central role of aquaporins in the pathophysiology of ischemic stroke. Front. Cell. Neurosci. 2015;9:108. [CrossRef] [PubMed]

100. Stokum JA, Kurland DB, Gerzanich V, Simard JM. Mechanisms of Astrocyte-Mediated Cerebral Edema. Neurochem. Res. 2015 Feb 5;40(2):317-28. [CrossRef] [PubMed]

101. Fukuda AM, Adami A, Pop V, Bellone JA, Coats JS, Hartman RE, Ashwal S, Obenaus A, Badaut J. Posttraumatic Reduction of Edema with Aquaporin-4 RNA Interference Improves Acute and Chronic Functional Recovery. J. Cereb. Blood Flow Metab. 2013 Oct 31;33(10):1621-32. [CrossRef] [PubMed]

102. Patterson SL, Goglin SE. Neuromyelitis Optica. Rheum. Dis. Clin. North Am. 2017 Nov;43(4):579-91. [CrossRef] [PubMed]

103. Long Y, Liang J, Zhong R, Wu L, Qiu W, Lin S, Gao C, Chen X, Zheng X, Yang N, Gao M, Wang Z. Aquaporin-4 antibody in neuromyelitis optica: re-testing study in a large population from China. Int. J. Neurosci. 2017 Sep 2;127(9):790-9. [CrossRef] [PubMed]

104. Phuan P-W, Ratelade J, Rossi A, Tradtrantip L, Verkman AS. Complement-dependent Cytotoxicity in Neuromyelitis Optica Requires Aquaporin-4 Protein Assembly in Orthogonal Arrays. J. Biol. Chem. 2012 Apr 20;287(17):13829-39. [CrossRef] [PubMed]

105. Akaishi T, Nakashima I. Efficiency of antibody therapy in demyelinating diseases. Int. Immunol. 2017 Jul 1;29(7):327-35. [CrossRef] [PubMed]

106. Tradtrantip L, Asavapanumas N, Verkman AS. Therapeutic Cleavage of Anti-Aquaporin-4 Autoantibody in Neuromyelitis Optica by an IgG-Selective Proteinase. Mol. Pharmacol. 2013 Jun 1;83(6):1268-75. [CrossRef] [PubMed]

107. Tradtrantip L, Jin B-J, Yao X, Anderson MO, Verkman AS. Aquaporin-Targeted Therapeutics: State-of-the-Field. Adv. Exp. Med. Biol. 2017;969:239-50. [CrossRef] [PubMed]

108. Xiong W, Ran J, Jiang R, Guo P, Shi X, Li H, Lv X, Li J, Chen D. miRNA-320a inhibits glioma cell invasion and migration by directly targeting aquaporin 4. Oncol. Rep. 2018 Feb 20;39(4):1939-47. [CrossRef] [PubMed]

109. Zhang H, Verkman AS. Evidence against Involvement of Aquaporin-4 in Cell–Cell Adhesion. J. Mol. Biol. 2008 Oct 24;382(5):1136-43. [CrossRef] [PubMed]

110. Xu Z, Xiao N, Chen Y, Huang H, Marshall C, Gao J, Cai Z, Wu T, Hu G, Xiao M. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol. Neurodegener. 2015 Dec 2;10(1):58. [CrossRef] [PubMed]

111. Yang C, Huang X, Huang X, Mai H, Li J, Jiang T, Wang X, Lü T. Aquaporin-4 and Alzheimer’s Disease. J. Alzheimer’s Dis. 2016 May 10;52(2):391-402. [CrossRef] [PubMed]

112. Smith AJ, Verkman AS. The “glymphatic” mechanism for solute clearance in Alzheimer’s disease: game changer or unproven speculation? FASEB J. 2018 Feb;32(2):543-51. [CrossRef] [PubMed]

113. Verkman AS, Smith AJ, Phuan P, Tradtrantip L, Anderson MO. The aquaporin-4 water channel as a potential drug target in neurological disorders. Expert Opin. Ther. Targets 2017 Dec 2;21(12):1161-70. [CrossRef] [PubMed]

114. Zelenina M. Regulation of brain aquaporins. Neurochem. Int. 2010 Nov;57(4):468-88. [CrossRef] [PubMed]

115. Pirici I, Balsanu T, Bogdan C, Margaritescu C, Divan T, Vitalie V, Mogoanta L, Pirici D, Carare R, Muresanu D. Inhibition of Aquaporin-4 Improves the Outcome of Ischaemic Stroke and Modulates Brain Paravascular Drainage Pathways. Int. J. Mol. Sci. 2017 Dec 23;19(1):46. [CrossRef] [PubMed]

116. Previch L, Ma L, Wright J, Singh S, Geng X, Ding Y. Progress in AQP Research and New Developments in Therapeutic Approaches to Ischemic and Hemorrhagic Stroke. Int. J. Mol. Sci. 2016 Jul 18;17(7):1146. [CrossRef] [PubMed]

117. Chai RC, Jiang JH, Wong AYK, Jiang F, Gao K, Vatcher G, Hoi Yu AC. AQP5 is differentially regulated in astrocytes during metabolic and traumatic injuries. Glia 2013 Oct;61(10):1748-65. [CrossRef] [PubMed]

118. Yamamoto N, Yoneda K, Asai K, Sobue K, Tada T, Fujita Y, Katsuya H, Fujita M, Aihara N, Mase M, Yamada K, Miura Y, Kato T. Alterations in the expression of the AQP family in cultured rat astrocytes during hypoxia and reoxygenation. Brain Res. Mol. Brain Res. 2001 May 20;90(1):26-38. [CrossRef] [PubMed]

119. Lambertz N, Hindy N El, Adler C, Rump K, Adamzik M, Keyvani K, Bankfalvi A, Siffert W, Erol Sandalcioglu I, Bachmann HS. Expression of aquaporin 5 and the AQP5 polymorphism A(-1364)C in association with peritumoral brain edema in meningioma patients. J. Neurooncol. 2013 Apr 8;112(2):297-305. [CrossRef] [PubMed]

120. Nagase H, Agren J, Saito A, Liu K, Agre P, Hazama A, Yasui M. Molecular cloning and characterization of mouse aquaporin 6. Biochem. Biophys. Res. Commun. 2007 Jan 5;352(1):12-6. [CrossRef] [PubMed]

121. Sakai H, Sato K, Kai Y, Shoji T, Hasegawa S, Nishizaki M, Sagara A, Yamashita A, Narita M. Distribution of aquaporin genes and selection of individual reference genes for quantitative real-time RT-PCR analysis in multiple tissues of the mouse. Can. J. Physiol. Pharmacol. 2014 Sep;92(9):789-96. [CrossRef] [PubMed]

122. Ishibashi K, Kuwahara M, Gu Y, Kageyama Y, Tohsaka A, Suzuki F, Marumo F, Sasaki S. Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J. Biol. Chem. 1997 Aug 15;272(33):20782-6. [PubMed]

123. Brown PD, Davies SL, Speake T, Millar ID. Molecular mechanisms of cerebrospinal fluid production. Neuroscience 2004;129(4):957-70. [CrossRef] [PubMed]

124. Patyal P, Alvarez-Leefmans F. Expression of NKCC1 and Aquaporins 4, 7 and 9 in Mouse Choroid Plexus and Ependymal Cells. The FASEB Journal. 2016;30(1_supplement):lb621-lb621. https://www.fasebj.org/doi/abs/10.1096/fasebj.30.1_supplement.lb621

125. Koyama N, Ishibashi K, Kuwahara M, Inase N, Ichioka M, Sasaki S, Marumo F. Cloning and Functional Expression of Human Aquaporin8 cDNA and Analysis of Its Gene. Genomics 1998 Nov 15;54(1):169-72. [CrossRef] [PubMed]

126. Oshio K, Binder D., Yang B, Schecter S, Verkman A., Manley G. Expression of aquaporin water channels in mouse spinal cord. Neuroscience 2004 Jan;127(3):685-93. [CrossRef] [PubMed]

127. Zhu S, Wang K, Gan S, Xu J, Xu S, Sun S. Expression of aquaporin8 in human astrocytomas: Correlation with pathologic grade. Biochem. Biophys. Res. Commun. 2013 Oct 11;440(1):168-72. [CrossRef] [PubMed]

128. Yang B, Song Y, Zhao D, Verkman AS. Phenotype analysis of aquaporin-8 null mice. Am. J. Physiol. Physiol. 2005 May;288(5):C1161-70. [CrossRef] [PubMed]

129. Dong R, Tao S, Liu Z, Zheng W, Yu D. Down-regulation of AQP8 suppresses glioma cells growth and invasion/migration via cell cycle pathway. Int J Clin Exp Patho 2016;9(2):1240-8. https://pdfs.semanticscholar.org/6ecc/330d49f2464ea04c274b613607476f1afc73.pdf

130. Arciénega II, Brunet JF, Bloch J, Badaut J. Cell locations for AQP1, AQP4 and 9 in the non-human primate brain. Neuroscience 2010 Jun 2;167(4):1103-14. [CrossRef] [PubMed]

131. Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M, Frøkiaer J, Nielsen S. Immunolocalization of AQP9 in Liver, Epididymis, Testis, Spleen, and Brain. Biochem. Biophys. Res. Commun. 2000 Oct 5;276(3):1118-28. [CrossRef] [PubMed]

132. Jelen S, Parm Ulhøi B, Larsen A, Frøkiær J, Nielsen S, Rützler M. AQP9 Expression in Glioblastoma Multiforme Tumors Is Limited to a Small Population of Astrocytic Cells and CD15+/CalB+ Leukocytes. PLoS One 2013 Sep 25;8(9):e75764. [CrossRef] [PubMed] [PubMed Central]

133. Badaut J, Brunet J-F, Guérin C, Regli L, Pellerin L. Alteration of glucose metabolism in cultured astrocytes after AQP9-small interference RNA application. Brain Res. 2012 Sep 14;1473:19-24. [CrossRef] [PubMed]

134. Fossdal G, Vik-Mo EO, Sandberg C, Varghese M, Kaarbø M, Telmo E, Langmoen IA, Murrell W. Aqp 9 and brain tumour stem cells. ScientificWorldJournal. 2012;2012:915176. [CrossRef] [PubMed] [PubMed Central]

135. Tchekneva EE, Khuchua Z, Davis LS, Kadkina V, Dunn SR, Bachman S, Ishibashi K, Rinchik EM, Harris RC, Dikov MM, Breyer MD. Single amino acid substitution in aquaporin 11 causes renal failure. J. Am. Soc. Nephrol. 2008 Oct;19(10):1955-64. [CrossRef] [PubMed] [PubMed Central]

136. Ishibashi K. Aquaporin subfamily with unusual NPA boxes. Biochim. Biophys. Acta - Biomembr. 2006 Aug;1758(8):989-93. [CrossRef] [PubMed]


GOST Style Citations






Copyright (c) 2019 Ievgenii I. Slynko, Alexey S. Nekhlopochin, Tatyana A. Malysheva

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.