GABAergic disinhibition and impaired KCC2 cotransporter activity underlie tumor-associated epilepsy

GLIA

Volumn 63, Issue 1, 2015, Pages 23-36

  Campbell, Susan L ^a   Robel, Stefanie ^a   Cuddapah, Vishnu A ^a   Robert, Stephanie ^a   Buckingham, Susan C ^a   Kahle, Kristopher T ^b,c   Sontheimer, Harald ^a  

^a University of Alabama at Birmingham   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

GABA; Glioma; KCC2; Peritumoral epilepsy

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 1; POTASSIUM CHLORIDE COTRANSPORTER 2; 4 AMINOBUTYRIC ACID A RECEPTOR; COTRANSPORTER; POTASSIUM-CHLORIDE SYMPORTERS;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL BODY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAM; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; FEMALE; GABAERGIC TRANSMISSION; GENE EXPRESSION; GLIOMA; GLIOMA CELL; HIPPOCAMPAL NEURONAL CULTURE; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL NETWORK; NEUROPATHIC PAIN; NONHUMAN; PERFORATED PATCH CLAMP; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; SPASTICITY; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; TEMPORAL LOBE EPILEPSY; WESTERN BLOTTING; WHOLE CELL PATCH CLAMP; ANIMAL; BRAIN TUMOR; COMPLICATION; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; BRAIN NEOPLASMS; EPILEPSY; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLIOMA; INTERNEURONS; MALE; MICE; NEURONS; RECEPTORS, GABA-A; SYMPORTERS; SYNAPTIC TRANSMISSION;

EID: 84911990081     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22730     Document Type: Article

References (50)

1. Andrioli A, Alonso-Nanclares L, Arellano JI, DeFelipe J. 2007. Quantitative analysis of parvalbumin-immunoreactive cells in the human epileptic hippocampus. Neuroscience 149:131-143.
2. Barmashenko G, Hefft S, Aertsen A, Kirschstein T, Kohling R. 2011. Positive shifts of the GABAA receptor reversal potential due to altered chloride homeostasis is widespread after status epilepticus. Epilepsia 52:1570-1578.
3. Ben-Ari Y. 2002. Excitatory actions of gaba during development: The nature of the nurture. Nat Rev Neurosci 3:728-739.
4. Ben-Ari Y, Gairsa JL, Tyzio R, Khazipov R. 2007. GABA: A pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87:1215-1284.
5. Ben-Ari Y, Khalilov I, Kahle KT, Cherubini E. 2012. The GABA excitatory/inhibitory shift in brain maturation and neurological disorders. Neuroscientist 18:467-486.
6. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S, Ogunrinu T, Sontheimer H. 2011. Glutamate release by primary brain tumors induces epileptic activity. Nat Med 17:1269-1274.
7. Campbell SL, Buckingham SC, Sontheimer H. 2012. Human glioma cells induce hyperexcitability in cortical networks. Epilepsia 53:1360-1370.
8. Chang EF, Potts MB, Keles GE, Lamborn KR, Chang SM, Barbaro NM, Berger MS. 2008. Seizure characteristics and control following resection in 332 patients with low-grade gliomas. J Neurosurg 108:227-235.
9. Cherubini E, Gaiarsa JL, Ben-Ari Y. 1991. Gaba: An excitatory inhibitor in early postnatal life. Trends Neurosci 14:515-519.
10. Chung WJ, Lyons SA, Nelson GM, Hamza H, Gladson CL, Gillespie GY, Sontheimer H. 2005. Inhibition of cystine uptake disrupts the growth of primary brain tumors. J Neurosci 25:7101-7110.
11. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R. 2002. On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421.
12. Conti L, Palma E, Roseti C, Lauro C, Cipriani R, de GM, Aronica E, Limatola C. 2011. Anomalous levels of Cl- transporters cause a decrease of GABAergic inhibition in human peritumoral epileptic cortex. Epilepsia 52:1635-1644.
13. Danbolt NC. 2001. Glutamate uptake. Prog Neurobiol 65:1-105.
14. de Groot M, Reijneveld JC, Aronica E, Heimans JJ. 2012. Epilepsy in patients with a brain tumour: Focal epilepsy requires focused treatment. Brain 135:1002-1016.
15. de Groot J, Sontheimer H. 2010. Glutamate and the biology of gliomas. Glia 59:1181-1189.
16. Deisz RA. 2002. Cellular mechanisms of pharmacoresistance in slices from epilepsy surgery. Novartis Found Symp 243:186-199.
17. Drexel M, Preidt AP, Kirchmair E, Sperk G. 2011. Parvalbumin interneurons and calretinin fibers arising from the thalamic nucleus reuniens degenerate in the subiculum after kainic acid-induced seizures. Neuroscience 189:316-329.
18. Giannini C, Sarkaria JN, Saito A, Uhm JH, Galanis E, Carlson BL, Schroeder MA, James CD. 2005. Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme. Neuro Oncol 7:164-176.
19. Gilbert CD. 1993. Circuitry, architecture, and functional dynamics of visual cortex. Cereb Cortex 3:373-386.
20. Gramatzki D, Herrmann C, Happold C, Becker KA, Gulbins E, Weller M, Tabatabai G. 2013. Glioma cell death induced by irradiation or alkylating agent chemotherapy is independent of the intrinsic ceramide pathway. PLoS One 8:1-16.
21. Haas BR, Cuddapah VA, Watkins S, Rohn KJ, Dy TE, Sontheimer H. 2011. With-No-Lysine kinase 3 (WNK3) stimulates glioma invasion by regulating cell volume. Am J Physiol Cell Physiol 301:C1150-C1160.
22. Hauser WA, Annegers JF, Kurland LT. 1993. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935-1984. Epilepsia 34:453-468.
23. Hildebrand J, Lecaille C, Perennes J, Delattre JY. 2005. Epileptic seizures during follow-up of patients treated for primary brain tumors. Neurology 65:212-215.
24. Isokawa M. 1996. Decrement of GABAA receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J Neurophysiol 75:1901-1908.
25. Kahle KT, Rinehart J, Lifton RP. 2010. Phosphoregulation of the Na-K-2Cl and K-Cl cotransporters by the WNK kinases. Biochim Biophys Acta 1802:1150-1158.
26. Kahle KT, Staley KJ, Nahed BV, Gamba G, Hebert SC, Lifton RP, Mount DB. 2008. Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 4:490-503.
27. Knopp A, Frahm C, Fidzinski P, Witte OW, Behr J. 2008. Loss of GABAergic neurons in the subiculum and its functional implications in temporal lobe epilepsy. Brain 131:1516-1527.
28. Kohling R, Vreugdenhil M, Bracci E, Jefferys JG. 2000. Ictal epileptiform activity is facilitated by hippocampal GABAA receptor-mediated oscillations. J Neurosci 20:6820-6829.
29. Lee H, Chen CX, Liu YJ, Aizenman E, Kandler K. 2005. KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur J Neurosci 21:2593-2599.
30. Marcus HJ, Carpenter KL, Price SJ, Hutchinson PJ. 2010. In vivo assessment of high-grade glioma biochemistry using microdialysis: A study of energy-related molecules, growth factors and cytokines. J Neurooncol 97:11-23.
31. National Cancer Institute. 2005. REMBRANDT home page. Available at: http://rembrandt.nci.nih.gov. Accessed on October 14, 2013.
32. Omuro A, DeAngelis LM. 2013. Glioblastoma and other malignant gliomas: A clinical review. JAMA 310:1842-1850.
33. 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.
34. Porter KR, McCarthy BJ, Freels S, Kim Y, Davis FG. 2010. Prevalence estimates for primary brain tumors in the United States by age, gender, behavior, and histology. Neuro Oncol 12:520-527.
35. Ratte S, Lacaille JC. 2006. Selective degeneration and synaptic reorganization of hippocampal interneurons in a chronic model of temporal lobe epilepsy. Adv Neurol 97:69-76.
36. Ritz MF, Hausmann ON. 2008. Effect of 17beta-estradiol on functional outcome, release of cytokines, astrocyte reactivity and inflammatory spreading after spinal cord injury in male rats. Brain Res 1203:177-188.
37. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
38. Savaskan NE, Heckel A, Hahnen E, Engelhorn T, Doerfler A, Ganslandt O, Nimsky C, Buchfelder M, Eyupoglu IY. 2008. Small interfering RNA-mediated xCT silencing in gliomas inhibits neurodegeneration and alleviates brain edema. Nat Med 14:629-632.
39. Scharfman HE. 2007. The neurobiology of epilepsy. Curr Neurol Neurosci Rep 7:348-354.
40. Schwaller B, Tetko IV, Tandon P, Silveira DC, Vreugdenhil M, Henzi T, Potier MC, Celio MR, Villa AE. 2004. Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol Cell Neurosci 25:650-663.
41. Smits A, Jin Z, Elsir T, Pedder H, Nister M, Alafuzoff I, Dimberg A, Edqvist P, Ponten F, Aronica E, Birnir B. 2012. GABA-A channel subunit expression in human glioma correlates with tumor histology and clinical. PLoS One 7:1-10.
42. Staley K, Smith R. 2001. A new form of feedback at the GABA(A) receptor. Nat Neurosci 4:674-676.
43. Takano T, Lin JH, Arcuino G, Gao Q, Yang J, Nedergaard M. 2001. Glutamate release promotes growth of malignant gliomas. Nat Med 7:1010-1015.
44. Van Brederode JF, Mulligan KA, Hendrickson AE. 1990. Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298:1-22.
45. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. 2002. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12:395-410.
46. Ye ZC, Rothstein JD, Sontheimer H. 1999. Compromised glutamate transport in human glioma cells: Reduction-mislocalization of sodium-dependent glutamate transporters and enhanced activity of cystine-glutamate exchange. J Neurosci 19:10767-10777.
47. Ye ZC, Sontheimer H. 1999. Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59:4383-4391.
48. Yuen TI, Morokoff AP, Bjorksten A, D'Abaco G, Paradiso L, Finch S, Wong D, Reid CA, Powell KL, Drummond KJ, Rosenthal MA, Kaye AH, O'Brien TJ. 2012. Glutamate is associated with a higher risk of seizures in patients with gliomas. Neurology 79:883-889.
49. Zalutsky MR. 2005. Current status of therapy of solid tumors: Brain tumor therapy. J Nucl Med 46:49.
50. Zhu L, Polley N, Mathews GC, Delpire E. 2008. NKCC1 and KCC2 prevent hyperexcitability in the mouse hippocampus. Epilepsy Res 79:201-212.