Maintenance and regulation of extracellular volume and the ion environment in Drosophila larval nerves

GLIA

Volumn 59, Issue 9, 2011, Pages 1312-1321

  Leiserson, William M ^a   Keshishian, Haig ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Blood brain barrier; Blood nerve barrier; Extracellular fluid; Osmoregulation

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AQUAPORIN; CHLORIDE CHANNEL; GAP JUNCTION PROTEIN; ION; POTASSIUM CHANNEL; POTASSIUM CHLORIDE COTRANSPORTER; PROTEIN SERINE THREONINE KINASE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ABDOMEN; ARTICLE; BLOOD BRAIN BARRIER; BLOOD NERVE BARRIER; CELL FUNCTION; CEREBROSPINAL FLUID DRAINAGE; CHEMICAL ENVIRONMENT; DROSOPHILA; ENDOTHELIUM CELL; EXTRACELLULAR SPACE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; IN VIVO STUDY; LARVA; MAMMAL; MICROVASCULATURE; MORPHOLOGY; NERVE; NERVE FIBER; NERVOUS SYSTEM; NONHUMAN; PERINEURIUM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BLOOD-BRAIN BARRIER; DROSOPHILA; EXTRACELLULAR SPACE; HUMANS; LARVA; NERVE TISSUE; PHENOTYPE; WATER-ELECTROLYTE IMBALANCE;

EID: 79959969818     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21132     Document Type: Article

References (128)

1. Alvarez-Leefmans FJ, Leon-Olea M, Mendoza-Sotelo J, Alvarez FJ, Anton B, Garduno R. 2001. Immunolocalization of the Na(+)-K(+)-2Cl(-) cotransporter in peripheral nervous tissue of vertebrates. Neuroscience 104: 569-582.
2. Anzini P, Neuberg DH, Schachner M, Nelles E, Willecke K, Zielasek J, Toyka KV, Suter U, Martini R. 1997. Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin 32. J Neurosci 17: 4545-4551.
3. Arnold W, Nadol JBJr, Weidauer H. 1981. Ultrastructural histopathology in a case of human ototoxicity due to loop diuretics. Acta Otolaryngol 91: 399-414.
4. Auld V. 1996. The role of glia in the development of the insect nervous system. In: Jessen KR, Richardson WD, editors. Glial cell development: Basic principles and clinical relevance. Oxford: Bios Scientific Publishers Ltd. pp 229-250.
5. Auld VJ, Fetter RD, Broadie K, Goodman CS. 1995. Gliotactin, a novel transmembrane protein on peripheral glia, is required to form the blood-nerve barrier in Drosophila. Cell 81: 757-767.
6. Bainton RJ, Tsai LT, Schwabe T, DeSalvo M, Gaul U, Heberlein U. 2005. Moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123: 145-156.
7. Banerjee S, Pillai AM, Paik R, Li J, Bhat MA. 2006a. Axonal ensheathment and septate junction formation in the peripheral nervous system of Drosophila. J Neurosci 26: 3319-3329.
8. Banerjee S, Sousa AD, Bhat MA. 2006b. Organization and function of septate junctions: An evolutionary perspective. Cell Biochem Biophys 46: 65-77.
9. Baumgartner S, Littleton JT, Broadie K, Bhat MA, Harbecke R, Lengyel JA, Chiquet-Ehrismann R, Prokop A, Bellen HJ. 1996. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell 87: 1059-1068.
10. Begg M, Cruickshank WJ. 1963. A partial analysis of Drosophila larval haemolymph. Proc Royal Soc Edinbergh Ser B: Containing Papers of a Biological Character 68: 215-236.
11. Behr M, Riedel D, Schuh R. 2003. The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila. Dev Cell 5: 611-620.
12. Berthold C-H, Rydmark M. 1995. Morphology of normal peripheral axons. In: Waxman SG, Kocsis JD, Stys PK, editors. The axon: Structure, function, and pathophysiology. New York: Oxford University Press. pp 13-48.
13. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, St Martin M, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ. 2001. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30: 369-383.
14. Bishop GH, Briggs AP, Ronzoni E. 1925. Body fluids of the honey bee larva. II. Chemical constituents of the blood, and their osmotic effects. J Biol Chem 66: 77-88.
15. Boettger T, Hubner CA, Maier H, Rust MB, Beck FX, Jentsch TJ. 2002. Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4. Nature 416: 874-878.
16. Boettger T, Rust MB, Maier H, Seidenbecher T, Schweizer M, Keating DJ, Faulhaber J, Ehmke H, Pfeffer C, Scheel O, et al. 2003. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. Embo J 22: 5422-5434.
17. Bone GJ. 1944. Le rapport de sodium/potassium dans le liquide coelomique des insectes. Annales de la Société Royale Zoologique de Belgique 75: 123.
18. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B. 2001. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30: 385-397.
19. Brecher L. 1929. The inorganic properties of chrysalis blood (Sphynx pinastri, Pieris brassicae): Changes in the content of inorganic properties in pupation (Pieris brassicae). Biochemische Zeitschrift 211: 40-64.
20. Budnik V, Zhong Y, Wu CF. 1990. Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J Neurosci 10: 3754-3768.
21. Byun N, Delpire E. 2007. Axonal and periaxonal swelling precede peripheral neurodegeneration in KCC3 knockout mice. Neurobiol Dis 28: 39-51.
22. Campos-Ortega JA, Hartenstein V. 1997. The embryonic development of Drosophila melanogaster. New York: Springer. xvii, 405p.
23. Carlson SD, Juang JL, Hilgers SL, Garment MB. 2000. Blood barriers of the insect. Annu Rev Entomol 45: 151-174.
24. Chen H, Sun D. 2005. The role of Na-K-Cl co-transporter in cerebral ischemia. Neurol Res 27: 280-286.
25. Coles JA, Dietmer JW. 2005. Glial cell regulation of extracellular potassium. In: Kettenmann H, Ransom BR, editors. Neuroglia. Oxford: Oxford University Press. pp 334-345.
26. Coles JA, Orkand RK, Yamate CL, Tsacopoulos M. 1986. Free concentrations of Na, K, and Cl in the retina of the honeybee drone: Stimulus-induced redistribution and homeostasis. Ann N Y Acad Sci 481: 303-317.
27. Croghan PC, Lockwood APM. 1960. The composition of the haemolymph of the larva of Drosophila melanogaster. J Exp Biol 37: 339-343.
28. Crouch JJ, Sakaguchi N, Lytle C, Schulte BA. 1997. Immunohistochemical localization of the Na-K-Cl co-transporter (NKCC1) in the gerbil inner ear. J Histochem Cytochem 45: 773-778.
29. Davson H, Welch K, Segal MB. 1987. Physiology and pathophysiology of the cerebrospinal fluid. New York: Churchill Livingstone. 1013p.
30. Delpire E, Lu J, England R, Dull C, Thorne T. 1999. Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl co-transporter. Nat Genet 22: 192-195.
31. Dietzel I, Heinemann U, Hofmeier G, Lux HD. 1980. Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res 40: 432-439.
32. Dietzel I, Heinemann U, Hofmeier G, Lux HD. 1982. Stimulus-induced changes in extracellular Na+ and Cl- concentration in relation to changes in the size of the extracellular space. Exp Brain Res 46: 73-84.
33. Dixon MJ, Gazzard J, Chaudhry SS, Sampson N, Schulte BA, Steel KP. 1999. Mutation of the Na-K-Cl co-transporter gene Slc12a2 results in deafness in mice. Hum Mol Genet 8: 1579-1584.
34. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD. 2007. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27: 11354-11365.
35. Dowd BF, Forbush B. 2003. PASK (proline-alanine-rich STE20-related kinase), a regulatory kinase of the Na-K-Cl cotransporter (NKCC1). J Biol Chem 278: 27347-27353.
36. Drilhon A. 1934. The organic fluids of moths. Comptes Rendus Des Seances De La Societe De Biologie Et De Ses Filiales 115: 1194-1195.
37. Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ. 2005. NKCC1 transporter facilitates seizures in the developing brain. Nat Med 11: 1205-1213.
38. Edenfeld G, Volohonsky G, Krukkert K, Naffin E, Lammel U, Grimm A, Engelen D, Reuveny A, Volk T, Klambt C. 2006. The splicing factor crooked neck associates with the RNA-binding protein HOW to control glial cell maturation in Drosophila. Neuron 52: 969-980.
39. Edwards JS, Swales LS, Bate M. 1993. The differentiation between neuroglia and connective tissue sheath in insect ganglia revisited: The neural lamella and perineurial sheath cells are absent in a mesodermless mutant of Drosophila. J Comp Neurol 333: 301-308.
40. Faivre-Sarrailh C, Banerjee S, Li J, Hortsch M, Laval M, Bhat MA. 2004. Drosophila contactin, a homolog of vertebrate contactin, is required for septate junction organization and paracellular barrier function. Development 131: 4931-4942.
41. Flagella M, Clarke LL, Miller ML, Erway LC, Giannella RA, Andringa A, Gawenis LR, Kramer J, Duffy JJ, Doetschman T, et al. 1999. Mice lacking the basolateral Na-K-2Cl cotransporter have impaired epithelial chloride secretion and are profoundly deaf. J Biol Chem 274: 26946-26955.
42. Frankenhaeuser B, Hodgkin AL. 1956. The after-effects of impulses in the giant nerve fibres of Loligo. J Physiol 131: 341-376.
43. Fredieu JR, Mahowald AP. 1989. Glial interactions with neurons during Drosophila embryogenesis. Development 106: 739-748.
44. Gagnon KB, England R, Delpire E. 2006. Characterization of SPAK and OSR1, regulatory kinases of the Na-K-2Cl cotransporter. Mol Cell Biol 26: 689-698.
45. Gagnon KB, England R, Delpire E. 2007. A single binding motif is required for SPAK activation of the Na-K-2Cl cotransporter. Cell Physiol Biochem 20: 131-142.
46. Ganetzky B, Wu CF. 1983. Neurogenetic analysis of potassium currents in Drosophila: Synergistic effects on neuromuscular transmission in double mutants. J Neurogenet 1: 17-28.
47. Genova JL, Fehon RG. 2003. Neuroglian, Gliotactin, and the Na+/K+ ATPase are essential for septate junction function in Drosophila. J Cell Biol 161: 979-989.
48. Han DD, Stein D, Stevens LM. 2000. Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. Development 127: 573-583.
49. Haugland FN, Wu CF. 1990. A voltage-clamp analysis of gene-dosage effects of the Shaker locus on larval muscle potassium currents in Drosophila. J Neurosci 10: 1357-1371.
50. Hoyle G. 1952. High blood potassium in insects in relation to nerve conduction. Nature 169: 281-282.
51. Hubner CA, Rust MB. 2006. Physiology of cation-chloride cotransporters. Adv Mol Cell Biol 38: 241-277.
52. Hummel T, Attix S, Gunning D, Zipursky SL. 2002. Temporal control of glial cell migration in the Drosophila eye requires gilgamesh, hedgehog, and eye specification genes. Neuron 33: 193-203.
53. Juang JL, Carlson SD. 1994. Analog of vertebrate anionic sites in blood-brain interface of larval Drosophila. Cell Tissue Res 277: 87-95.
54. Kahle KT, Ring AM, Lifton RP. 2008. Molecular physiology of the WNK kinases. Annu Rev Physiol 70: 329-355.
55. Kamasawa N, Sik A, Morita M, Yasumura T, Davidson KG, Nagy JI, Rash JE. 2005. Connexin-47 and connexin-32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops and Schmidt-Lanterman incisures: Implications for ionic homeostasis and potassium siphoning. Neuroscience 136: 65-86.
56. Kikuchi T, Adams JC, Miyabe Y, So E, Kobayashi T. 2000. Potassium ion recycling pathway via gap junction systems in the mammalian cochlea and its interruption in hereditary nonsyndromic deafness. Med Electron Microsc 33: 51-56.
57. Klambt C. 2009. Modes and regulation of glial migration in vertebrates and invertebrates. Nat Rev Neurosci 10: 769-779.
58. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA. 2000. Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. J Neurosci 20: 5733-5740.
59. Kofuji P, Newman EA. 2004. Potassium buffering in the central nervous system. Neuroscience 129: 1045-1056.
60. Kriventseva EV, Rahman N, Espinosa O, Zdobnov EM. 2008. OrthoDB: The hierarchical catalog of eukaryotic orthologs. Nucleic Acids Res 36(Database issue): D271-D275.
61. Lamb RS, Ward RE, Schweizer L, Fehon RG. 1998. Drosophila coracle, a member of the protein 4.1 superfamily, has essential structural functions in the septate junctions and developmental functions in embryonic and adult epithelial cells. Mol Biol Cell 9: 3505-3519.
62. Lane NJ. 1991. Morphology of glial blood-brain barriers. Ann N Y Acad Sci 633: 348-362.
63. Lee T, Luo L. 2001. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci 24: 251-254.
64. Leiserson WM, Forbush B, Keshishian H. 2011. Regulation of extracellular volume of the nervous system through an evolutionarily conserved molecular mechanism. Glia 59: 320-332.
65. Leiserson WM, Harkins EW, Keshishian H. 2000. Fray a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron 28: 793-806.
66. Llimargas M, Strigini M, Katidou M, Karagogeos D, Casanova J. 2004. Lachesin is a component of a septate junction-based mechanism that controls tube size and epithelial integrity in the Drosophila tracheal system. Development 131: 181-190.
67. Lord BA, DiBona DR. 1976. Role of the septate junction in the regulation of paracellular transepithelial flow. J Cell Biol 71: 967-972.
68. MacVicar BA, Feighan D, Brown A, Ransom B. 2002. Intrinsic optical signals in the rat optic nerve: Role for K(+) uptake via NKCC1 and swelling of astrocytes. Glia 37: 114-123.
69. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL. 2003. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
70. Menichella DM, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. 2003. Connexins are critical for normal myelination in the CNS. J Neurosci 23: 5963-5973.
71. Menichella DM, Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. 2006. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci 26: 10984-10991.
72. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P. 2001. Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 21: 5429-5438.
73. Newman EA, Frambach DA, Odette LL. 1984. Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225: 1174-1175.
74. Noirot-Timothee C, Noirot C. 1980. Septate and scalariform junctions in arthropods. Int Rev Cytol 63: 97-140.
75. O'Donnell ME, Tran L, Lam TI, Liu XB, Anderson SE. 2004. Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J Cereb Blood Flow Metab 24: 1046-1056.
76. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Bussow H, Schilling K, Steinhauser C, et al. 2003. Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J Neurosci 23: 4549-4559.
77. Oh S, Ri Y, Bennett MV, Trexler EB, Verselis VK, Bargiello TA. 1997. Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron 19: 927-938.
78. Orkand RK. 1986. Glial-interstitial fluid exchange. Ann N Y Acad Sci 481: 269-272.
79. Orkand RK, Nicholls JG, Kuffler SW. 1966. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29: 788-806.
80. Osterwalder T, Yoon KS, White BH, Keshishian H. 2001. A conditional tissue-specific transgene expression system using inducible GAL4. Proc Natl Acad Sci USA 98: 12596-12601.
81. Parker RJ, Auld VJ. 2006. Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17: 66-77.
82. Paul SM, Ternet M, Salvaterra PM, Beitel GJ. 2003. The Na+/K+ ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130: 4963-4974.
83. Piechotta K, Garbarini N, England R, Delpire E. 2003. Characterization of the interaction of the stress kinase SPAK with the Na+-K+-2Cl- cotransporter in the nervous system: Evidence for a scaffolding role of the kinase. J Biol Chem 278: 52848-52856.
84. Plotkin MD, Kaplan MR, Peterson LN, Gullans SR, Hebert SC, Delpire E. 1997a. Expression of the Na(+)-K(+)-2Cl- cotransporter BSC2 in the nervous system. Am J Physiol 272(1 Pt 1): C173-C183.
85. Plotkin MD, Snyder EY, Hebert SC, Delpire E. 1997b. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: A possible mechanism underlying GABA's excitatory role in immature brain. J Neurobiol 33: 781-795.
86. Ransom BR, Yamate CL, Connors BW. 1985. Activity-dependent shrinkage of extracellular space in rat optic nerve: A developmental study. J Neurosci 5: 532-535.
87. Richardson C, Alessi DR. 2008. The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J Cell Sci 121 (Part 20): 3293-3304.
88. Roman G, Endo K, Zong L, Davis RL. 2001. P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc Natl Acad Sci USA 98: 12602-12607.
89. Ruiz-Canada C, Budnik V. 2006. Introduction on the use of the Drosophila embryonic/larval neuromuscular junction as a model system to study synapse development and function, and a brief summary of pathfinding and target recognition. Int Rev Neurobiol 75: 1-31.
90. Santi PA, Lakhani BN. 1983. The effect of bumetanide on the stria vascularis: A stereological analysis of cell volume density. Hear Res 12: 151-165.
91. Scherer SS, Xu YT, Nelles E, Fischbeck K, Willecke K, Bone LJ. 1998. Connexin32-null mice develop demyelinating peripheral neuropathy. Glia 24: 8-20.
92. Schmid A, Chiba A, Doe CQ. 1999. Clonal analysis of Drosophila embryonic neuroblasts: Neural cell types, axon projections and muscle targets. Development 126: 4653-4689.
93. Schmidt H, Rickert C, Bossing T, Vef O, Urban J, Technau GM. 1997. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol 189: 186-204.
94. Schulte J, Tepass U, Auld VJ. 2003. Gliotactin, a novel marker of tricellular junctions, is necessary for septate junction development in Drosophila. J Cell Biol 161: 991-1000.
95. Schwabe T, Bainton RJ, Fetter RD, Heberlein U, Gaul U. 2005. GPCR signaling is required for blood-brain barrier formation in drosophila. Cell 123: 133-144.
96. Sepp KJ, Schulte J, Auld VJ. 2000. The developmental dynamics of peripheral glia in Drosophila melanogaster. Glia, in press.
97. Silies M, Edenfeld G, Engelen D, Stork T, Klambt C. 2007. Development of the peripheral glial cells in Drosophila. Neuron Glia Biol 3: 35-43.
98. Somjen GG. 2002. Ion regulation in the brain: Implications for pathophysiology. Neuroscientist 8: 254-267.
99. Stewart BA, Atwood HL, Renger JJ, Wang J, Wu CF. 1994. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J Comp Physiol A 175: 179-191.
100. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klambt C. 2008. Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28: 587-597.
101. Strigini M, Cantera R, Morin X, Bastiani MJ, Bate M, Karagogeos D. 2006. The IgLON protein Lachesin is required for the blood-brain barrier in Drosophila. Mol Cell Neurosci 32(1-2): 91-101.
102. Struhl G, Basler K. 1993. Organizing activity of wingless protein in Drosophila. Cell 72: 527-540.
103. Su G, Kintner DB, Flagella M, Shull GE, Sun D. 2002a. Astrocytes from Na+-K+-Cl- cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am J Physiol Cell Physiol 282: C1147-C1160.
104. Su G, Kintner DB, Sun D. 2002b. Contribution of Na+-K+-Cl- cotransporter to high-[K+]o- induced swelling and EAA release in astrocytes. Am J Physiol Cell Physiol 282: C1136-C1146.
105. Sun YT, Lin TS, Tzeng SF, Delpire E, Shen MR. 2010. Deficiency of electroneutral K+-Cl- cotransporter 3 causes a disruption in impulse propagation along peripheral nerves. Glia 58: 1544-1552.
106. Sutherland D, Samakovlis C, Krasnow MA. 1996. Branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87: 1091-1101.
107. Svoboda J, Sykova E. 1991. Extracellular space volume changes in the rat spinal cord produced by nerve stimulation and peripheral injury. Brain Res 560: 216-224.
108. Tatsumi K, Tsuji S, Miwa H, Morisaku T, Nuriya M, Orihara M, Kaneko K, Okano H, Yasui M. 2009. Drosophila big brain does not act as a water channel, but mediates cell adhesion. FEBS Lett 583: 2077-2082.
109. Tepass U, Hartenstein V. 1994. The development of cellular junctions in the Drosophila embryo. Dev Biol 161: 563-596.
110. Tepass U, Tanentzapf G, Ward R, Fehon R. 2001. Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet 35: 747-784.
111. Tobias JM. 1948. The high potassium and low sodium in the body fluid and tissues of a phytophagous insect, the silkworm Bombyx mori and the change before pupation. J Cell Physiol 31: 143-148.
112. Treherne JE, Schofield PK. 1981. Mechanisms of ionic homeostasis in the central nervous system of an insect. J Exp Biol 95: 61-73.
113. Vetter DE, Mann JR, Wangemann P, Liu J, McLaughlin KJ, Lesage F, Marcus DC, Lazdunski M, Heinemann SF, Barhanin J. 1996. Inner ear defects induced by null mutation of the isk gene. Neuron 17: 1251-1264.
114. Vitari AC, Thastrup J, Rafiqi FH, Deak M, Morrice NA, Karlsson HK, Alessi DR. 2006. Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 397: 223-231.
115. von Hilchen CM, Beckeruordersandforth RM, Rickert C, Technau GM, Altenhein B. 2008. Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech Dev 125: 337-352.
116. Walz W. 2000. Role of astrocytes in the clearance of excess extracellular potassium. Neurochem Int 36: 291-300.
117. Walz W, Hinks EC. 1985. Carrier-mediated KCl accumulation accompanied by water movements is involved in the control of physiological K+ levels by astrocytes. Brain Res 343: 44-51.
118. Walz W, Hinks EC. 1986. A transmembrane sodium cycle in astrocytes. Brain Res 368: 226-232.
119. Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzaki H, Ogawa T, Mori N, Fukuda A, Sato K. 2002. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res Dev Brain Res 139: 59-66.
120. Wang H, Yan Y, Kintner DB, Lytle C, Sun D. 2003. GABA-mediated trophic effect on oligodendrocytes requires Na-K-2Cl cotransport activity. J Neurophysiol 90: 1257-1265.
121. Wangemann P. 2002. K+ cycling and the endocochlear potential. Hear Res 165: 1-9.
122. Wood RL. 1959. Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J Biophys Biochem Cytol 6: 343-352.
123. Wu VM, Schulte J, Hirschi A, Tepass U, Beitel GJ. 2004. Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control. J Cell Biol 164: 313-323.
124. Wu VM, Yu MH, Paik R, Banerjee S, Liang Z, Paul SM, Bhat MA, Beitel GJ. 2007. Drosophila varicose, a member of a new subgroup of basolateral MAGUKs, is required for septate junctions and tracheal morphogenesis. Development 134: 999-1009.
125. Xu T, Rubin GM. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
126. Yan Y, Dempsey RJ, Sun D. 2001. Na+-K+-Cl- cotransporter in rat focal cerebral ischemia. J Cereb Blood Flow Metab 21: 711-721.
127. Zdebik AA, Wangemann P, Jentsch TJ. 2009. Potassium ion movement in the inner ear: Insights from genetic disease and mouse models. Physiology (Bethesda) 24: 307-316.
128. Zhao HB, Kikuchi T, Ngezahayo A, White TW. 2006. Gap junctions and cochlear homeostasis. J Membr Biol 209: 177-186.