Spinal cord injury causes a wide-spread, persistent loss of Kir4.1 and glutamate transporter 1: Benefit of 17β-oestradiol treatment

Brain

Volumn 133, Issue 4, 2010, Pages 1013-1025

  Olsen, Michelle L ^a   Campbell, Susan C ^a   McFerrin, Michael B ^a   Floyd, Candace L ^a,b   Sontheimer, Harald ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Astrocyte glutamate transporter; Inward rectifier potassium channel; Oestrogen; Potassium buffering; Spinal cord injury

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; GLIAL FIBRILLARY ACIDIC PROTEIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL KIR4.1; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL LOSS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; NEUROPROTECTION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD INJURY; TRANSLATION REGULATION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ESTRADIOL; EXCITATORY AMINO ACID TRANSPORTER 2; MALE; NERVE CRUSH; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; THORACIC VERTEBRAE; TREATMENT OUTCOME;

EID: 77950821270     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq049     Document Type: Article

References (38)

1. Bordey A, Sontheimer H. Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 1998; 32: 286-303.
2. Butt AM, Kalsi A. Inwardly rectifying potassium channels (Kir) in central nervous system glia: a special role for Kir4.1 in glial functions. J Cell Mol Med 2006; 10: 33-44.
3. Chaovipoch P, Jelks KA, Gerhold LM, West EJ, Chongthammakun S, Floyd CL. 17beta-estradiol is protective in SC injury in post-and pre-menopausal rats. J Neurotrauma 2006; 23: 830-852
4. Dhandapani KM, Brann DW. Role of astrocytes in estrogen-mediated neuroprotection. Exp Gerontol 2007; 42: 70-75
5. Dibaj P, Kaiser M, Hirrlinger J, Kirchhoff F, Neusch C. Kir4.1 channels regulate swelling of astroglial processes in experimental SC edema. J Neurochem 2007; 103: 2620-2628
6. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD. 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 2007; 27: 11354-11365
7. Dusart I, Schwab ME. Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat SC. Eur J Neurosci 1994; 6: 712-724
8. Farkas I, Varju P, Liposits Z. Estrogen modulates potassium currents and expression of the Kv4.2 subunit in GT1-7 cells. Neurochem Int 2007; 50: 619-627
9. Farooque M, Suo Z, Arnold PM, Wulser MJ, Chou CT, Vancura RW, et al. Gender-related differences in recovery of locomotor function after SC injury in mice. Spinal Cord 2006; 44: 182-187
10. Hinterkeuser S, Schrö der W, Hager G, Seifert G, Blümcke I, Elger CE, et al. Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Europ J Neurosci 2000; 12: 2087-2096
11. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, et al. TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 2007; 130: 535-547
12. Kachadroka S, Hall AM, Niedzielko TL, Chongthammakun S, Floyd CL. Effect of endogenous androgens on 17b-estradiol-mediated protection after spinal cord injury in male rats. J Neurotrauma 2010; 27: 1-16.
13. Kaiser M, Maletzki I, Hulsmann S, Holtmann B, Schulz-Schaeffer W, Kirchhoff F, et al. Progressive loss of a glial potassium channel (KCNJ10) in the SC of the SOD1 (G93A) transgenic mouse model of amyotrophic lateral sclerosis. J Neurochem 2006; 99: 900-912
14. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA. Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. J Neurosci 2000; 20: 5733-5740
15. Kucheryavykh YV, Kucheryavykh LY, Nichols CG, Maldonado HM, Baksi K, Reichenbach A, et al. Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 2007; 55: 274-281
16. Lee IH, Lindqvist E, Kiehn O, Widenfalk J, Olson L. Glial and neuronal connexin expression patterns in the rat SC during development and following injury. J Comp Neurol 2005; 489: 1-10.
17. Liang Z, Valla J, Sefidvash-Hockley S, Rogers J, Li R. Effects of estrogen treatment on glutamate uptake in cultured human astrocytes derived from cortex of Alzheimer's disease patients. J Neurochem 2002; 80: 807-814
18. MacFarlane SN, Sontheimer H. Electrophysiological changes that accompany reactive gliosis in vitro. J Neurosci 1997; 17: 7316-7329
19. Martinez L, de Lacalle S. Astrocytic reaction to a lesion, under hormonal deprivation. Neurosci Lett 2007; 415: 190-193
20. Neusch C, Papadopoulos N, Muller M, Maletzki I, Winter SM, Hirrlinger J, et al. Lack of the Kir4.1 channel subunit abolishes K+ buffering properties of astrocytes in the ventral respiratory group: impact on extracellular K+ regulation. J Neurophysiol 2006; 95: 1843-1852
21. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P. Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 2001; 21: 5429-5438
22. Olsen ML, Campbell SL, Sontheimer H. Differential distribution of kir4.1 in SC astrocytes suggests regional differences in k+ homeostasis. J Neurophysiol 2007; 98: 786-793
23. Olsen ML, Higashimori H, Campbell SL, Hablitz JJ, Sontheimer H. Functional expression of K(ir)4.1 channels in SC astrocytes. Glia 2006; 53: 516-528
24. Olsen ML, Sontheimer H. Mislocalization of Kir channels in malignant glia. Glia 2004; 46: 63-73.
25. Olsen ML, Sontheimer H. Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. J Neurochem 2008; 107: 589-601.
26. Pannicke T, Uckermann O, Iandiev I, Biedermann B, Wiedemann P, Perlman I, et al. Altered membrane physiology in Muller glial cells after transient ischemia of the rat retina. Glia 2005; 50: 1-11.
27. Pawlak J, Brito V, Kuppers E, Beyer C. Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Brain Res Mol Brain Res 2005; 138: 1-7.
28. Pekny M, Pekna M. Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol 2004; 204: 428-437
29. Platania P, Laureanti F, Bellomo M, Giuffrida R, Giuffrida-Stella AM, Catania MV, et al. Differential expression of estrogen receptors alpha and beta in the SC during postnatal development: localization in glial cells. Neuroendocrinology 2003; 77: 334-340
30. Platania P, Seminara G, Aronica E, Troost D, Vincenza CM, Angela SM. 17beta-estradiol rescues spinal motoneurons from AMPA-induced toxicity: a role for glial cells. Neurobiol Dis 2005; 20: 461-470
31. Profyris C, Cheema SS, Zang D, Azari MF, Boyle K, Petratos S. Degenerative and regenerative mechanisms governing SC injury. Neurobiol Dis 2004; 15: 415-436
32. Ransom CB, Sontheimer H. Biophysical and pharmacological characterization of inwardly rectifying K+ currents in rat spinal cord astrocytes. J Neurophysiol 1995; 72: 333-346
33. Ritz M, Hausmann O. Effect of 17beta-estradiol on functional outcome, release of cytokines, astrocyte reactivity and inflammatory spreading after spinal cord injury in male rats. Brain Res 2008; 1203: 177-188
34. Rolls A, Shechter R, Schwartz M. The bright side of the glial scar in CNS repair. Nat Rev Neurosci 2009; 10: 235-241
35. Sato K, Matsuki N, Ohno Y, Nakazawa K. Estrogens inhibit l-glutamate uptake activity of astrocytes via membrane estrogen receptor alpha. J Neurochem 2003; 86: 1498-1505
36. Sribnick EA, Matzelle DD, Ray SK, Banik NL. Estrogen treatment of SC injury attenuates calpain activation and apoptosis. J Neurosci Res 2006; 84: 1064-1075
37. Sribnick EA, Wingrave JM, Matzelle DD, Wilford GG, Ray SK, Banik NL. Estrogen attenuated markers of inflammation and decreased lesion volume in acute SC injury in rats. J Neurosci Res 2005; 82: 283-293
38. Vera-Portocarrero LP, Mills CD, Ye Z, Fullwood SD, McAdoo DJ, Hulsebosch CE, et al. Rapid changes in expression of glutamate transporters after SC injury. Brain Res 2002; 927: 104-110