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

Volumn 64, Issue 1, 2016, Pages 139-154

  Mola, Maria Grazia ^a   Sparaneo, Angelo ^b   Gargano, Concetta Domenica ^a   Spray, David C ^c   Svelto, Maria ^a   Frigeri, Antonio ^a,c   Scemes, Eliana ^c   Nicchia, Grazia Paola ^a,c  

^a UNIVERSITY OF BARI   (Italy)

^b CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

AQP1; AQP4; Cell swelling; Hypotonic stimulus; RVD

Indexed keywords

AQUAPORIN 1; AQUAPORIN 4; CALCIUM; GADOLINIUM; HYPOTONIC SOLUTION; MANNITOL; RUTHENIUM RED; VANILLOID RECEPTOR 4; AQP1 PROTEIN, HUMAN; AQP4 PROTEIN, HUMAN; AQP4 PROTEIN, MOUSE; TRPV4 PROTEIN, MOUSE; TRPV4 PROTEIN, RAT; VANILLOID RECEPTOR; WATER;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FUNCTION; CELL KINETICS; CELL LINE; CELL MEMBRANE; CELL STIMULATION; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EXTRACELLULAR CALCIUM; EXTRACELLULAR SPACE; MOUSE; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REGULATORY VOLUME DECREASE; WATER PERMEABILITY; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL SIZE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; KINETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; RAT;

ANIMALS; AQUAPORIN 1; AQUAPORIN 4; ASTROCYTES; CALCIUM; CALCIUM SIGNALING; CELL MEMBRANE; CELL SIZE; CELLS, CULTURED; EXTRACELLULAR SPACE; HUMANS; KINETICS; MICE, KNOCKOUT; RATS; TRPV CATION CHANNELS; WATER;

EID: 84954395952     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22921     Document Type: Article

References (69)

1. Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S. 2002. Aquaporin water channels-From atomic structure to clinical medicine. J Physiol 542:3-16.
2. Altamirano J, Brodwick MS, Alvarez-Leefmans FJ. 1998. Regulatory volume decrease and intracellular calcium in murine neuroblastoma cells studied with fluorescent probes. J Gen Physiol 112:145-160.
3. Amiry-Moghaddam M, Ottersen OP. 2003. The molecular basis of water transport in the brain. Nat Rev Neurosci 4:991-1001. (Review).
4. Amiry-Moghaddam M, Xue R, Haug FM, Neely JD, Bhardwaj A, Agre P, Adams ME, Froehner SC, Mori S, Ottersen OP. 2004. Alpha-syntrophin deletion removes the perivascular but not endothelial pool of aquaporin-4 at the blood-brain barrier and delays the development of brain edema in an experimental model of acute hyponatremia. FASEB J 18:542-544.
5. Basco D, Blaauw B, Pisani F, Sparaneo A, Nicchia GP, Mola MG, Reggiani C, Svelto M, Frigeri A. 2013. AQP4-dependent water transport plays a functional role in exercise-induced skeletal muscle adaptations. PLoS One 8:e58712. doi: 10.1371/journal.pone.0058712. Erratum in: PLoS One 8(6). doi:10.1371/annotation/86fc2632-913c-490d-8b9b-e925b38baec5.
6. Benfenati V, Caprini M, Dovizio M, Mylonakou MN, Ferroni S, Ottersen OP, Amiry-Moghaddam M. 2011. An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc Natl Acad Sci USA 108:2563-2568.
7. Binder DK, Oshio K, Ma T, Verkman AS, Manley GT. 2004. Increased seizure threshold in mice lacking aquaporin-4 water channels. Neuroreport 15:259-262.
8. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT. 2006. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53:631-636.
9. Chi C, Trinkaus-Randall V. 2013. New insights in wound response and repair of epithelium. J Cell Physiol 228:925-929.
10. Connors NC, Adams ME, Froehner SC, Kofuji P. 2004. The potassium channel Kir4.1 associates with the dystrophin-glycoprotein complex via alpha-syntrophin in glia. J Biol Chem 2279:28387-28392.
11. De Bellis M, Pisani F, Mola MG, Basco D, Catalano F, Nicchia GP, Svelto M, Frigeri A. 2014. A novel human aquaporin-4 splice variant exhibits a dominant-negative activity: A new mechanism to regulate water permeability. Mol Biol Cell 25:470-480. doi: 10.1091/mbc.E13-06-0331.
12. Farinas J, Simanek V, Verkman AS. 1995. Cell volume measured by total internal reflection microfluorimetry: Application to water and solute transport in cells transfected with water channel homologs. Biophys J 68:1613-1620.
13. Fischer R, Schliess F, Haussinger D. 1997. Characterization of the hypo-osmolarity-induced calcium response in cultured rat astrocytes. Glia 20:51-58.
14. Foskett JK, Wong MM, Sue AQG, Robertson MA. 1994. Isosmotic modulation of cell volume and intracellular ion activities during stimulation of single exocrine cells. J Exp Zool 268:104-110.
15. Frigeri A, Nicchia GP, Nico B, Quondamatteo F, Herken R, Roncali L, Svelto M. 2001. Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J 15:90-98.
16. Galizia L, Pizzoni A, Fernandez J, Rivarola V, Capurro C, Ford P. 2012. Functional interaction between AQP2 and TRPV4 in renal cells. J Cell Biochem 113:580-589.
17. Grinstein S, Smith JD. 1990. Calcium-independent cell volume regulation in human lymphocytes. Inhibition by charybdotoxin. J Gen Physiol 95:97-120.
18. Grynkiewicz G, Poenie M, Tsien RY. 1985. A new generation of calcium indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
19. Gunthorpe MJ, Benham CD, Randall A, Davis JB. 2002. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol Sci 23:183-191.
20. Haj-Yasein NN, Jensen V, Ostby I, Omholt SW, Voipio J, Kaila K, Ottersen OP, Hvalby O, Nagelhus EA. 2012. Aquaporin-4 regulates extracellular space volume dynamics during high-frequency synaptic stimulation: A gene deletion study in mouse hippocampus. Glia 60:867-874. doi: 10.1002/glia.22319.
21. Hammami S, Willumsen NJ, Olsen HL, Morera FJ, Latorre R, Klaerke DA. 2009. Cell volume and membrane stretch independently control K+ channel activity. J Physiol 587:2225-2231. doi: 10.1113/jphysiol.2008.163550.
22. Hoffmann EK, Dunham PB. 1995. Membrane mechanisms and intracellular signalling in cell volume regulation. (Kwang JW, Ed.), Int Rev Cytol 161:172-262.
23. Hoffmann EK, Lambert IH, Pedersen SF. 2009. Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193-277.
24. Kimelberg HK. 1992. Astrocytic edema in CNS trauma. J Neurotrauma 9:S71-S81.
25. Kimelberg HK, Rutledge E, Goderie S, Charniga C. 1995. Astrocytic swelling due to hypotonic or high K+ medium causes inhibition of glutamate and aspartate uptake and increases their release. J Cereb Blood Flow Metab 15:409-416.
26. Kitaura H, Tsujita M, Huber VJ, Kakita A, Shibuki K, Sakimura K, Kwee IL, Nakada T. 2009. Activity-dependent glial swelling is impaired in aquaporin-4 knockout mice. Neurosci Res 64:208-212.
27. Kuipers AJ, Middelbeek J, van Leeuwen FN. 2012. Mechanoregulation of cytoskeletal dynamics by TRP channels. Eur J Cell Biol 91:834-846.
28. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D. 1998. Functional significance of cell volume regulatory mechanisms. Physiol Rev 78:247-306.
29. Li YK, Wang F, Wang W, Luo Y, Wu PF, Xiao JL, Hu ZL, Jin Y, Hu G, Chen JG. 2012. Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: Involvement of downregulation of glutamate transporter-1 expression. Neuropsychopharmacology 37:1867-1878.
30. Liu X, Bandyopadhyay BC, Nakamoto T, Singh B, Liedtke W, Melvin JE, Ambudkar I. 2006. A role for AQP5 in activation of TRPV4 by hypotonicity: Concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 281:15485-15495.
31. Macknight AD, Gordon LG, Purves RD. 1994. Problems in the understanding of cell volume regulation. J Exp Zool 268:80-89. Review.
32. Manley GT, Binder DK, Papadopoulos MC, Verkman AS. 2004. New insights into water transport and edema in the central nervous system from phenotype analysis of aquaporin-4 null mice. Neuroscience 129:983-991. (Review).
33. McCarty NA, O'Neil RG. 1992. Calcium signaling in cell volume regulation. Physiol Rev 72:1037-1061.
34. McNally BA, Prakriya M. 2012. Permeation, selectivity and gating in store-operated CRAC channels. J Physiol 590:4179-4191.
35. Moe SE, Sorbo JG, Sogaard R, Zeuthen T, Petter Ottersen O, Holen T, 2008. New isoforms of rat Aquaporin-4. Genomics 91:367-377.
36. Mola MG, Nicchia GP, Svelto M, Spray DC, Frigeri A. 2009. Automated cell-based assay for screening of aquaporin inhibitors. Anal Chem 81:8219-8229.
37. Mongin AA, Kimelberg HK. 2005. Astrocytic swelling in neuropathology, in Neuroglia (KettenmannH. and RansomB. R., eds), pp. 550-562. Oxford University Press, Oxford, New York.
38. Morales-Mulia S, Vaca L, Hernandez-Cruz A, Pasantes-Morales H. 1998. Osmotic swelling-induced changes in cytosolic calcium do not affect regulatory volume decrease in rat cultured suspended cerebellar astrocytes. J Neurochem 71:2330-2338.
39. Nagelhus EA, Mathiisen TM, Ottersen OP. 2004. Aquaporin-4 in the central nervous system: Cellular and subcellular distribution and coexpression with KIR4.1. Neuroscience 129:905-913.
40. Nicchia GP, Frigeri A, Liuzzi GM, Santacroce MP, Nico B, Procino G, Quondamatteo F, Herken R, Roncali L, Svelto M. 2000. Aquaporin-4-containing astrocytes sustain a temperature- and mercury-insensitive swelling in vitro. Glia 31:29-38.
41. Nicchia GP, Frigeri A, Liuzzi GM, Svelto M. 2003. Inhibition of aquaporin-4 expression in astrocytes by RNAi determines alteration in cell morphology, growth, and water transport and induces changes in ischemia-related genes. FASEB J 17:1508-1510.
42. Nicchia GP, Rossi A, Mola MG, Procino G, Frigeri A, Svelto M. 2008. Actin cytoskeleton remodeling governs aquaporin-4 localization in astrocytes. Glia 56:1755-1766.
43. Nicchia GP, Srinivas M, Li W, Brosnan CF, Frigeri A, Spray DC. 2005. New possible roles for aquaporin-4 in astrocytes: Cell cytoskeleton and functional relationship with connexin43. FASEB J 19:1674-1676.
44. Nicchia GP, Stigliano C, Sparaneo A, Rossi A, Frigeri A, Svelto M. 2013. Inhibition of aquaporin-1 dependent angiogenesis impairs tumour growth in a mouse model of melanoma. J Mol Med (Berl) 91:613-623.
45. O'Connor ER, Kimelberg HK. 1993. Role of calcium in astrocyte volume regulation and in the release of ions and amino acids. J Neurosci 13:2638-2650.
46. Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S, 2001. Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol 532 (Part 1):3-16.
47. Padmawar P, Yao X, Bloch O, Manley GT, Verkman AS. 2005. K+ waves in brain cortex visualized using a long-wavelength K+-sensing fluorescent indicator. Nat Methods 2:825-827.
48. Pangrsic T, Potokar M, Haydon PG, Zorec R, Kreft M. 2006. Astrocyte swelling leads to membrane unfolding, not membrane insertion. J Neurochem 99:514-523.
49. Papadopoulos MC, Verkman AS. 2013. Aquaporin water channels in the nervous system. Nat Rev Neurosci 14:265-277.
50. Pasantes-Morales H, Morales Mulia S. 2000. Influence of calcium on regulatory volume decrease: Role of potassium channels. Nephron 86:414-427.
51. Pettit EJ, Fay FS. 1998. Cytosolic free calcium and the cytoskeleton in the control of leukocyte chemotaxis. Physiol Rev 78:949-967.
52. Potokar M, Stenovec M, Jorgačevski J, Holen T, Kreft M, Ottersen OP, Zorec R. 2013. Regulation of AQP4 surface expression via vesicle mobility in astrocytes. Glia 61:917-928. doi: 10.1002/glia.22485.
53. Risher WC, Andrew RD, Kirov SA. 2009. Real-time passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 57:207-221. doi: 10.1002/glia.20747.
54. Russell JM. 2000. Sodium-potassium-chloride cotransport. Physiol Rev 80:211-276. (Review).
55. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS. 2005. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691-5698.
56. Sanchez-Olea R, Morales Mulia M, Moran J, Pasantes-Morales H. 1995. Inhibition by dihydropyridines of regulatory volume decrease and osmolyte fluxes in cultured astrocytes is unrelated to extracellular calcium. Neurosci Lett 193:165-168.
57. Sánchez JC, Danks TA, Wilkins RJ. 2003. Mechanisms involved in the increase in intracellular calcium following hypotonic shock in bovine articular chondrocytes. Gen Physiol Biophys 22:487-500.
58. SCEMES E. (2008). Modulation of astrocyte P2Y1 receptors by the carboxyl terminal domain of the gap junction protein Cx43. Glia 56: 145-153.
59. Shigetomi E, Bushong EA, Haustein MD, Tong X, Jackson-Weaver O, Kracun S, Xu J, Sofroniew MV, Ellisman MH, Khakh BS. 2013. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J Gen Physiol 141:633-647.
60. Skucas VA, Mathews IB, Yang J, Cheng Q, Treister A, Duffy AM, Verkman AS, Hempstead BL, Wood MA, Binder DK, Scharfman HE. 2011. Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J Neurosci 31:6392-6397.
61. Solenov E, Watanabe H, Manley GT, Verkman AS. 2004. Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286:C426-C432.
62. Strohschein S, Hüttmann K, Gabriel S, Binder DK, Heinemann U, Steinhäuser C. 2011. Impact of aquaporin-4 channels on K+ buffering and gap junction coupling in the hippocampus. Glia 59:973-980. doi: 10.1002/glia.21169.
63. Verkman AS. 2000. Water permeability measurement in living cells and complex tissues. J Membr Biol 173:73-87.
64. Verkman AS. 2002. Physiological importance of aquaporin water channels. Ann Med 34:192-200.
65. Verkman AS. 2012. Aquaporins in clinical medicine. Annu Rev Med 63:303-316.
66. 2+ signalling: An unexpected complexity. Nat Rev Neurosci 15:327-335.
67. Walz W. 1987. Swelling and potassium uptake in cultured astrocytes. Can J Physiol Pharmacol 65:1051-1057.
68. Yang XC, Sachs F. 1989. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 243:1068-1071.
69. Zhang H, Verkman AS. 2008. Aquaporin-4 independent Kir4.1 K+ channel function in brain glial cells. Mol Cell Neurosci 37:1-10.