Chloride cotransporters as a molecular mechanism underlying spreading depolarization-induced dendritic beading

Journal of Neuroscience

Volumn 35, Issue 35, 2015, Pages 12172-12187

  Steffensen, Annette B ^a   Sword, Jeremy ^b   Croom, Deborah ^b   Kirov, Sergei A ^b   MacAulay, Nanna ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cl cotransporters; Cotransporters; Dendritic beading; Neuronal swelling; Spreading depression; Two photon microscopy

Indexed keywords

CHLORIDE COTRANSPORTER; ENHANCED GREEN FLUORESCENT PROTEIN; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; 4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; ADENOSINE TRIPHOSPHATE; CHEMOKINE RECEPTOR; CHLORATE; CHLORIC ACID; COTRANSPORTER; CX3CR1 PROTEIN, HUMAN; FUROSEMIDE; FUSED HETEROCYCLIC RINGS; LATRUNCULIN A; LOOP DIURETIC AGENT; OUABAIN; THIAZOLIDINE DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CHLORIDE TRANSPORT; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL CA1 REGION; IMAGE ANALYSIS; LASER MICROSCOPY; MALE; MICROGLIA; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SPREADING DEPOLARIZATION; TRANSMISSION ELECTRON MICROSCOPY; TWO PHOTON LASER SCANNING MICROSCOPY; ANIMAL; CYTOLOGY; DENDRITE; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; PYRAMIDAL NERVE CELL; SPREADING CORTICAL DEPRESSION; TRANSGENIC MOUSE;

4,4'-DIISOTHIOCYANOSTILBENE-2,2'-DISULFONIC ACID; ADENOSINE TRIPHOSPHATE; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CA1 REGION, HIPPOCAMPAL; CHLORATES; CORTICAL SPREADING DEPRESSION; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; FUROSEMIDE; IN VITRO TECHNIQUES; MALE; MICE; MICE, TRANSGENIC; OUABAIN; PYRAMIDAL CELLS; RECEPTORS, CHEMOKINE; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SYMPORTERS; THIAZOLIDINES;

EID: 84940936345     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0400-15.2015     Document Type: Article

References (93)

1. Aiba I, Carlson AP, Sheline CT, Shuttleworth CW (2012) Synaptic release and extracellular actions of Zn2+ limit propagation of spreading depression and related events in vitro and in vivo. J Neurophysiol 107:1032–1041.Medline
2. Aitken PG, Borgdorff AJ, Juta AJA, Kiehart DP, Somjen GG, Wadman WJ (1998) Volume changes induced by osmotic stress in freshly isolated rat hippocampal neurons. Pflugers Arch 436:991–998.Medline
3. Alper SL (2009) Molecular physiology and genetics of Na+-independent SLC4 anion exchangers. J Exp Biol 212:1672–1683.CrossRefMedline
4. Anderson TR, Andrew RD (2002) Spreading depression: imaging and blockade in the rat neocortical brain slice. J Neurophysiol 88:2713–2725.CrossRefMedline
5. Anderson TR, Jarvis CR, Biedermann AJ, Molnar C, Andrew RD (2005) Blocking the anoxic depolarization protects without functional compromise following simulated stroke in cortical brain slices. J Neurophysiol 93:963–979.Medline
6. Andrew RD, Labron MW, Boehnke SE, Carnduff L, Kirov SA (2007) Physiological evidence that pyramidal neurons lack functional water channels. Cereb Cortex 17:787–802.Medline
7. Atkinson SJ, Hosford MA, Molitoris BA (2004) Mechanism of actin polymerization in cellular ATP depletion. J Biol Chem 279:5194–5199.CrossRefMedline
8. Ayata C, Shin HK, Salomone S, Ozdemir-Gursoy Y, Boas DA, Dunn AK, Moskowitz MA (2004) Pronounced hypoperfusion during spreading depression in mouse cortex. J Cereb Blood Flow Metab 24:1172–1182.Medline
9. Balestrino M, Young J, Aitken P (1999) Block of (Na+, K+) ATPase with ouabain induces spreading depression-like depolarization in hippocampal slices. Brain Res 838:37–44. CrossRefMedline
10. Bird MM (1984) The effects of taxol on embryonic chick tectum maintained in culture: an electron microscope study. J Ultrastruct Res 89:123–135. CrossRefMedline
11. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61:820–838.CrossRefMedline
12. Broër S, Broër A, Schneider HP, Stegen C, Halestrap AP, Deitmer JW (1999) Characterization of the high-affinity monocarboxylate transporterMCT2 in Xenopus laevis oocytes. Biochem J 341:529–535. CrossRefMedline
13. Canals S, Makarova I, López-Aguado L, Largo C, Ibarz JM, Herreras O (2005) Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression. J Neurophysiol 94:943–951.CrossRefMedline
14. Chang JC, Shook LL, Biag J, Nguyen EN, Toga AW, Charles AC, Brennan KC (2010) Biphasic direct current shift, haemoglobin desaturation and neurovascular uncoupling in cortical spreading depression. Brain 133:996–1012.CrossRefMedline
15. Chen S, Mohajerani MH, Xie Y, Murphy TH (2012) Optogenetic analysis of neuronal excitability during global ischemia reveals selective deficits in sensory processing following reperfusion in mouse cortex. J Neurosci 32:13510–13519.CrossRefMedline
16. Clement EA, Richard A, Thwaites M, Ailon J, Peters S, Dickson CT (2008) Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 3:e2004.CrossRefMedline
17. Davies ML, Kirov SA, Andrew RD (2007) Whole isolated neocortical and hippocampal preparations and their use in imaging studies. J Neurosci Methods 166:203–216.CrossRefMedline
18. DeFazio RA, Keros S, Quick MW, Hablitz JJ (2000) Potassium-coupled chloride cotransport controls intracellular chloride in rat neocortical pyramidal neurons. J Neurosci 20:8069–8076.Medline
19. Del Prete E, Lutz TA, Scharrer E (2004) Inhibition of glucose oxidation by a-cyano-4-hydroxycinnamic acid stimulates feeding in rats. Physiol Behav 80:489–498.CrossRefMedline
20. Dietz RM, Weiss JH, Shuttleworth CW (2008) Zn2+ influx is critical for some forms of spreading depression in brain slices. J Neurosci 28:8014–8024.CrossRefMedline
21. do Carmo RJ, Martins-Ferreira H (1984) Spreading depression of Leao probed with ion-selective microelectrodes in isolated chick retina. An Acad Bras Cienc 56:401–421.Medline
22. Douglas HA, Callaway JK, Sword J, Kirov SA, Andrew RD (2011) Potent inhibition of anoxic depolarization by the sodium channel blocker dibucaine. J Neurophysiol 105:1482–1494.CrossRefMedline
23. Dreier JP (2011) The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 17:439–447.CrossRefMedline
24. Dreier JP, Reiffurth C (2015) The stroke-migraine depolarization continuum. Neuron 86:902–922.CrossRefMedline
25. Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ (2006) Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 129:3224–3237.CrossRefMedline
26. Dreier JP, Isele T, Reiffurth C, Offenhauser N, Kirov SA, Dahlem MA, Herreras O (2013) Is spreading depolarization characterized by an abrupt, massive release of gibbs free energy from the human brain cortex? Neuroscientist 19:25–42.CrossRefMedline
27. Dunn AK, Bolay H, Moskowitz MA, Boas DA (2001) Dynamic imaging of cerebral blood flow using laser speckle. J Cereb Blood Flow Metab 21:195–201.Medline
28. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41–51.CrossRefMedline
29. Gisselsson LL, Matus A, Wieloch T (2005) Actin redistribution underlies the sparing effect of mild hypothermia on dendritic spine morphology after in vitro ischemia. J Cereb Blood Flow Metab 25:1346–1355.CrossRefMedline
30. Hadjikhani N, Sanchez Del Rio M, Wu O, Schwartz D, Bakker D, Fischl B, Kwong KK, Cutrer FM, Rosen BR, Tootell RB, Sorensen AG, Moskowitz MA (2001) Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc Natl Acad Sci U S A 98:4687–4692.CrossRefMedline
31. Halestrap AP (2013) The SLC16 gene family—structure, role and regulation in health and disease. Mol Aspects Med 34:337–349.CrossRefMedline
32. Hansen AJ, Zeuthen T (1981) Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. Acta Physiol Scand 113:437–445.CrossRefMedline
33. Hartings JA, Bullock MR, Okonkwo DO, Murray LS, Murray GD, Fabricius M, Maas AI, Woitzik J, Sakowitz O, Mathern B, Roozenbeek B, Lingsma H, Dreier JP, Puccio AM, Shutter LA, Pahl C, Strong AJ (2011a) Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet Neurol 10:1058–1064.CrossRefMedline
34. Hartings JA, Watanabe T, Bullock MR, Okonkwo DO, Fabricius M, Woitzik J, Dreier JP, Puccio A, Shutter LA, Pahl C, Strong AJ (2011b) Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain 134:1529–1540.CrossRefMedline
35. Hasbani MJ, Hyrc KL, Faddis BT, Romano C, Goldberg MP (1998) Distinct roles for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp Neurol 154:241–258.CrossRefMedline
36. Hasbani MJ, Schlief ML, Fisher DA, Goldberg MP (2001) Dendritic spines lost during glutamate receptor activation reemerge at original sites of synaptic contact. J Neurosci 21:2393–2403.Medline
37. Hines DJ, Hines RM, Mulligan SJ, Macvicar BA (2009) Microglia processes block the spread of damage in the brain and require functional chloride channels. Glia 57:1610–1618.CrossRefMedline
38. Hoskison MM, Shuttleworth CW (2006) Microtubule disruption, not calpain-dependent loss of MAP2, contributes to enduring NMDAinduced dendritic dysfunction in acute hippocampal slices. Exp Neurol 202:302–312.CrossRefMedline
39. Hoskison MM, Yanagawa Y, Obata K, Shuttleworth CW (2007) Calciumdependent NMDA-induced dendritic injury and MAP2 loss in acute hippocampal slices. Neuroscience 145:66–79.CrossRefMedline
40. Iyirhiaro GO, Brust TB, Rashidian J, Galehdar Z, Osman A, Phillips M, Slack RS, Macvicar BA, Park DS (2008) Delayed combinatorial treatment with flavopiridol and minocycline provides longer term protection for neuronal soma but not dendrites following global ischemia. J Neurochem 105:703–713.CrossRefMedline
41. Jensen FE, Harris KM (1989) Preservation of neuronal ultrastructure in hippocampal slices using rapid microwave-enhanced fixation. J Neurosci Methods 29:217–230.CrossRefMedline
42. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106–4114.CrossRefMedline
43. Kakazu Y, Akaike N, Komiyama S, Nabekura J (1999) Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19:2843–2851.Medline
44. Kirov SA, Sorra KE, Harris KM (1999) Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876–2886.Medline
45. Kirov SA, Petrak LJ, Fiala JC, Harris KM (2004) Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience 127:69–80.CrossRefMedline
46. Kopito RR, Lee BS, Simmons DM, Lindsey AE, Morgans CW, Schneider K (1989) Regulation of intracellular pH by a neuronal homolog of the erythrocyte anion exchanger. Cell 59:927–937.CrossRefMedline
47. Korpi ER, Lüddens H (1997) Furosemide interactions with brain GABAA receptors. Br J Pharmacol 120:741–748.CrossRefMedline
48. Kraig RP, Nicholson C (1978) Extracellular ionic variations during spreading depression. Neuroscience 3:1045–1059.CrossRefMedline
49. LaManna JC, Rosenthal M (1975) Effect of ouabain and phenobarbital on oxidative metabolic activity associated with spreading cortical depression in cats. Brain Res 88:145–149.CrossRefMedline
50. Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ (2011) Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J Cereb Blood Flow Metab 31:17–35.CrossRefMedline
51. Leao AAP (1944) Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophysiol 7:391–396.
52. Li P, Murphy TH (2008) Two-photon imaging during prolonged middle cerebral artery occlusion in mice reveals recovery of dendritic structure after reperfusion. J Neurosci 28:11970–11979.CrossRefMedline
53. MacAulay N, Zeuthen T (2010) Water transport between CNS compartments: contributions of aquaporins and cotransporters. Neuroscience 168:941–956.CrossRefMedline
54. MacAulay N, Hamann S, Zeuthen T (2004) Water transport in the brain: role of cotransporters. Neuroscience 129:1029–1042. CrossRef
55. Masuda T, Croom D, Hida H, Kirov SA (2011) Capillary blood flow around microglial somata determines dynamics of microglial processes in ischemic conditions. Glia 59:1744–1753.CrossRefMedline
56. Mazel T, Richter F, Vargová L, Syková E (2002) Changes in extracellular space volume and geometry induced by cortical spreading depression in immature and adult rats. Physiol Res 51:S85–S93.Medline
57. Menna G, Tong CK, Chesler M (2000) Extracellular pH changes and accompanying cation shifts during ouabain-induced spreading depression. J Neurophysiol 83:1338–1345. Medline
58. Mies G, Paschen W (1984) Regional changes of blood flow, glucose, and ATP content determined on brain sections during a single passage of spreading depression in rat brain cortex. Exp Neurol 84:249–258. CrossRefMedline
59. Mohajerani MH, McVea DA, Fingas M, Murphy TH (2010) Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J Neurosci 30:3745–3751. CrossRefMedline
60. Müller M (2000) Effects of chloride transport inhibition and chloride substitution on neuron function and on hypoxic spreading-depression-like depolarization in rat hippocampal slices. Neuroscience 97:33–45. CrossRefMedline
61. Müller M, Somjen GG (1999) Intrinsic optical signals in rat hippocampal slices during hypoxia-induced spreading depression-like depolarization. J Neurophysiol 82:1818–1831. Medline
62. Müller M, Somjen GG (2000) Na+ and K+ concentrations, extra-and intracellular voltages, and the effect of TTX in hypoxic rat hippocampal slices. J Neurophysiol 83:735–745.
63. Murphy TH, Li P, Betts K, Liu R (2008) Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J Neurosci 28:1756–1772. CrossRefMedline
64. Mutch WAC, Hansen AJ (1984) Extracellular pH changes during spreading depression and cerebral ischemia: mechanisms of brain pH regulation. J Cereb Blood Flow Metab 4:17–27. CrossRefMedline
65. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314–1318. CrossRefMedline
66. Oliveira-Ferreira AI, Milakara D, Alam M, Jorks D, Major S, Hartings JA, Lückl J, Martus P, Graf R, Dohmen C, Bohner G, Woitzik J, Dreier JP (2010) Experimental and preliminary clinical evidence of an ischemic zone with prolonged negative DC shifts surrounded by a normally perfused tissue belt with persistent electrocorticographic depression. J Cereb Blood Flow Metab 30:1504–1519. CrossRefMedline
67. Pagliardini S, Gosgnach S, Dickson CT (2013) Spontaneous sleep-like brain state alternations and breathing characteristics in urethane anesthetized mice. PLoS One 8:e70411. CrossRefMedline
68. Papadopoulos MC, Verkman AS (2013) Aquaporin water channels in the nervous system. Nat Rev Neurosci 14:265–277. CrossRefMedline
69. Pasantes-Morales H, Maar TE, Morán J (1993) Cell volume regulation in cultured cerebellar granule neurons. J Neurosci Res 34:219–224. CrossRefMedline
70. Payne JA (1997) Functional characterization of the neuronal-specific K-Cl cotransporter: implications for [K+]o regulation. Am J Physiol Cell Physiol 273:C1516–C1525.
71. Payne JA, Stevenson TJ, Donaldson LF (1996) Molecular characterization of a putative K-Cl cotransporter in rat brain A neuronal-specific isoform. J Biol Chem 271:16245–16252. CrossRefMedline
72. Pérez-Pinzón MA, Tao L, Nicholson C (1995) Extracellular potassium, volume fraction, and tortuosity in rat hippocampal CA1, CA3, and cortical slices during ischemia. J Neurophysiol 74:565–573. Medline
73. Pierre K, Magistretti PJ, Pellerin L (2002) MCT2 is a major neuronal monocarboxylate transporter in the adult mouse brain. J Cereb Blood Flow Metab 22:586–595. Medline
74. Plotkin MD, Kaplan MR, Peterson LN, Gullans SR, Hebert SC, Delpire E (1997) Expression of the Na+-K+-2Cl+ cotransporter BSC2 in the nervous system. Am J Physiol Cell Physiol 41:C173.
75. 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. CrossRefMedline
76. Risher WC, Ard D, Yuan J, Kirov SA (2010) Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci 30:9859–9868. CrossRefMedline
77. Risher WC, Croom D, Kirov SA (2012) Persistent astroglial swelling accompanies rapid reversible dendritic injury during stroke-induced spreading depolarizations. Glia 60:1709–1720. CrossRefMedline
78. Rungta RL, Choi HB, Tyson JR, Malik A, Dissing-Olesen L, Lin PJ, Cain SM, Cullis PR, Snutch TP, MacVicar BA (2015) The cellular mechanisms of neuronal swelling underlying cytotoxic edema. Cell 161:610–621. CrossRefMedline
79. Schliwa M, Euteneuer U, Bulinski JC, Izant JG (1981) Calcium lability of cytoplasmic microtubules and its modulation by microtubule-associated proteins. Proc Natl Acad Sci U S A 78:1037–1041. CrossRefMedline
80. Sigler A, Goroshkov A, Murphy TH (2008) Hardware and methodology for targeting single brain arterioles for photothrombotic stroke on an upright microscope. J Neurosci Methods 170:35–44. CrossRefMedline
81. Somjen GG (2001) Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 81:1065–1096. Medline
82. Somjen GG (2004) Ions in the brain: normal function, seizures, and stroke. New York: Oxford UP.
83. Spector I, Shochet NR, Kashman Y, Groweiss A (1983) Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219:493–495. CrossRefMedline
84. Sword J, Masuda T, Croom D, Kirov SA (2013) Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging. Brain 136:1446–1461. CrossRefMedline
85. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, Kasischke KA, Nedergaard M (2007) Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 10:754–762. CrossRefMedline
86. Windmüller O, Lindauer U, Foddis M, Einhäupl KM, Dirnagl U, Heinemann U, Dreier JP (2005) Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain 128:2042–2051. CrossRefMedline
87. Yamamoto K, Morimoto K, Yanagihara T (1986) Cerebral ischemia in the gerbil: transmission electron microscopic and immunoelectron microscopic investigation. Brain Res 384:1–10. CrossRefMedline
88. Yamamoto K, Hayakawa T, Mogami H, Akai F, Yanagihara T (1990) Ultrastructural investigation of the CA1 region of the hippocampus after transient cerebral ischemia in gerbils. Acta Neuropathol 80:487–492. CrossRefMedline
89. Yang O, Cuccia D, Choi B (2011) Real-time blood flow visualization using the graphics processing unit. J Biomed Optics 16:016009. CrossRef
90. Zeuthen T (1994) Cotransport of K+, Cl- and H2O by membrane proteins from choroid plexus epithelium of Necturus maculosus. J Physiol 478:203–219. CrossRefMedline
91. Zeuthen T, MacAulay N (2012) Cotransport of water by Na+-K+-2Cl+ cotransporters expressed in Xenopus oocytes: NKCC1 versus NKCC2. J Physiol 590:1139–1154. CrossRefMedline
92. Zeuthen T, Hamann S, La Cour M (1996) Cotransport of H+, lactate and H2O by membrane proteins in retinal pigment epithelium of bullfrog. J Physiol 497:3–17. CrossRef
93. Zhou N, Gordon GR, Feighan D, MacVicar BA (2010) Transient swelling, acidification, and mitochondrial depolarization occurs in neurons but not astrocytes during spreading depression. Cereb Cortex 20:2614–2624. CrossRefMedline