Cortical GABAergic excitation contributes to epileptic activities around human glioma

Science Translational Medicine

Volumn 6, Issue 244, 2014, Pages

  Pallud, Johan ^a,b,c,d   Le Van Quyen, Michel ^a,b   Bielle, Franck ^a,e   Pellegrino, Christophe ^f,g   Varlet, Pascale ^c,d   Labussiere, Marianne ^a,b   Cresto, Noémie ^a,b   Dieme, Marie Joseph ^e   Baulac, Michel ^a,b,e   Duyckaerts, Charles ^a,e   Kourdougli, Nazim ^f,g   Chazal, Geneviève ^f,g   Devaux, Bertrand ^c,d   Rivera, Claudio ^f,g,h   Miles, Richard ^a,b   Capelle, Laurent ^a,e   Huberfeld, Gilles ^a,b,e,i  

^a SORBONNE UNIVERSITÉ   (France)

^b INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^c CENTRE HOSPITALIER SAINTE ANNE   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^f Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^g AIX MARSEILLE UNIVERSITY   (France)

^h UNIVERSITY OF HELSINKI   (Finland)

ⁱ INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR; CHLORIDE; GLUTAMIC ACID; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; GLUTAMIC ACID DERIVATIVE;

4 AMINOBUTYRIC ACID RELEASE; ADULT; ARTICLE; BRAIN SLICE; CANCER INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; EPILEPSY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; GABAERGIC TRANSMISSION; GLIOMA; HIGH FREQUENCY OSCILLATION; HUMAN; HUMAN TISSUE; INTERNEURON; NEOCORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; ACTION POTENTIAL; BRAIN TUMOR; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

ACTION POTENTIALS; BRAIN NEOPLASMS; CHLORIDES; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GLIOMA; GLUTAMATES; HUMANS; INTERNEURONS; NEOCORTEX;

EID: 84904498200     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3008065     Document Type: Article

References (60)

1. M.S. van Breemen, E. B. Wilms, C. J. Vecht, Epilepsy in patients with brain tumours: Epidemiology, mechanisms, and management. Lancet Neurol. 6, 421-430 (2007).
2. J. Pallud, L. Capelle, G. Huberfeld, Tumoral epileptogenicity: How does it happen? Epilepsia 54, 30-34 (2013).
3. J. F. Hirsch, J. Buisson-Ferey, M. Sachs, J. C. Hirsch, J. Scherrer, Electrocorticogram and unitary activites with expanding lesions in man. Electroencephalogr. Clin. Neurophysiol. 21, 417-428 (1966).
4. M. S. Berger, S. Ghatan, M. M. Haglund, J. Dobbins, G. A. Ojemann, Low-grade gliomas associated with intractable epilepsy: Seizure outcome utilizing electrocorticography during tumor resection. J. Neurosurg. 79, 62-69 (1993).
5. M. M. Haglund, M. S. Berger, D. D. Kunkel, J. E. Franck, S. Ghatan, G. A. Ojemann, Changes in γ-aminobutyric acid and somatostatin in epileptic cortex associated with low-grade gliomas. J. Neurosurg. 77, 209-216 (1992).
6. J. Pallud, P. Varlet, B. Devaux, S. Geha, M. Badoual, C. Deroulers, P. Page, E. Dezamis, C. Daumas-Duport, F. X. Roux, Diffuse low-grade oligodendrogliomas extend beyond MRI-defined abnormalities. Neurology 74, 1724-1731 (2010).
7. J. Pallud, Diffuse low-grade gliomas: What does "complete resection" mean? in Tumors of the central nervous system: Gliomas, glioblastomas. Part 2. (Springer Netherlands, Dordrecht, 2011), pp. 153-161.
8. S. C. Buckingham, S. L. Campbell, B. R. Haas, V. Montana, S. Robel, T. Ogunrinu, H. Sontheimer, Glutamate release by primary brain tumors induces epileptic activity. Nat. Med. 17, 1269-1274 (2011).
9. A. Bordey, H. Sontheimer, Electrophysiological properties of human astrocytic tumor cells in situ: Enigma of spiking glial cells. J. Neurophysiol. 79, 2782-2793 (1998).
10. + buffering to cell differentiation. J. Neurochem. 107, 589-601 (2008).
11. Z. C. Ye, J. D. Rothstein, H. Sontheimer, 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 (1999).
12. J. de Groot, H. Sontheimer, Glutamate and the biology of gliomas. Glia 59, 1181-1189 (2011).
13. T. Takano, J. H. Lin, G. Arcuino, Q. Gao, J. Yang, M. Nedergaard, Glutamate release promotes growth of malignant gliomas. Nat. Med. 7, 1010-1015 (2001).
14. A. Hamberger, B. Nyström, S. Larsson, H. Silfvenius, C. Nordborg, Amino acids in the neuronal microenvironment of focal human epileptic lesions. Epilepsy Res. 9, 32-43 (1991).
15. S. A. Lyons, W. J. Chung, A. K. Weaver, T. Ogunrinu, H. Sontheimer, Autocrine glutamate signaling promotes glioma cell invasion. Cancer Res. 67, 9463-9471 (2007).
16. H. J. Marcus, K. L. Carpenter, S. J. Price, P. J. Hutchinson, 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 (2010).
17. M. Roslin, R. Henriksson, P. Bergström, U. Ungerstedt, A. T. Bergenheim, Baseline levels of glucose metabolites, glutamate and glycerol in malignant glioma assessed by stereotactic microdialysis. J. Neurooncol. 61, 151-160 (2003).
18. H. K. Wolf, D. Roos, I. Blümcke, T. Pietsch, O. D. Wiestler, Perilesional neurochemical changes in focal epilepsies. Acta Neuropathol. 91, 376-384 (1996).
19. P. Marco, R. G. Sola, S. Ramón y Cajal, J. DeFelipe, Loss of inhibitory synapses on the soma and axon initial segment of pyramidal cells in human epileptic peritumoural neocortex: Implications for epilepsy. Brain Res. Bull. 44, 47-66 (1997).
20. B. Schaller, S. J. Rüegg, Brain tumor and seizures: Pathophysiology and its implications for treatment revisited. Epilepsia 44, 1223-1232 (2003).
21. I. Cohen, V. Navarro, S. Clemenceau, M. Baulac, R. Miles, On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298, 1418-1421 (2002).
22. G. Huberfeld, L. Wittner, S. Clemenceau, M. Baulac, K. Kaila, R. Miles, C. Rivera, Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J. Neurosci. 27, 9866-9873 (2007).
23. R. Köhling, A. Lücke, H. Straub, E. J. Speckmann, I. Tuxhorn, P. Wolf, H. Pannek, F. Oppel, Spontaneous sharp waves in human neocortical slices excised from epileptic patients. Brain 121 (Pt. 6), 1073-1087 (1998).
24. G. Huberfeld, L. Menendez de la Prida, J. Pallud, I. Cohen, M. Le Van Quyen, C. Adam, S. Clemenceau, M. Baulac, R. Miles, Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy. Nat. Neurosci. 14, 627-634 (2011).
25. R. Miles, P. Blaesse, G. Huberfeld, L. Wittner, K. Kaila, in Chloride Homeostasis and GABA Signaling in Temporal Lobe Epilepsy, J. L. Noebels, M. Avoli, M. A. Rogawski, R. W. Olsen, A. V. Delgado-Escueta, Eds. [National Center for Biotechnology Information (US), Bethesda (MD), ed. 4, 2012].
26. C. W. Habela, N. J. Ernest, A. F. Swindall, H. Sontheimer, Chloride accumulation drives volume dynamics underlying cell proliferation and migration. J. Neurophysiol. 101, 750-757 (2009).
27. C. W. Habela, M. L. Olsen, H. Sontheimer, ClC3 is a critical regulator of the cell cycle in normal and malignant glial cells. J. Neurosci. 28, 9205-9217 (2008).
28. A receptors on human glioma cells. Eur. J. Neurosci. 10, 231-238 (1998).
29. S. Z. Young, A. Bordey, GABA's control of stem and cancer cell proliferation in adult neural and peripheral niches. Physiology (Bethesda) 24, 171-185 (2009).
30. N. J. Ernest, H. Sontheimer, Extracellular glutamine is a critical modulator for regulatory volume increase in human glioma cells. Brain Res. 1144, 231-238 (2007).
31. B. R. Haas, H. Sontheimer, Inhibition of the Sodium-Potassium-Chloride Cotransporter Isoform-1 reduces glioma invasion. Cancer Res. 70, 5597-5606 (2010).
32. - transporters cause a decrease of GABAergic inhibition in human peritumoral epileptic cortex. Epilepsia 52, 1635-1644 (2011).
33. D. N. Louis, H. Ohgaki, O.D. Wiestler, W. K. Cavenee (Eds.), World Health Organization Classification of Tumours of the Central Nervous System (IARC press, 2007).
34. A. Bragin, I. Mody, C. L. Wilson, J. Engel Jr., Local generation of fast ripples in epileptic brain. J. Neurosci. 22, 2012-2021 (2002).
35. L. Menendez de la Prida, R. Benavides-Piccione, R. Sola, M. A. Pozo, Electrophysiological properties of interneurons from intraoperative spiking areas of epileptic human temporal neocortex. Neuroreport 13, 1421-1425 (2002).
36. V. I. Dzhala, D. M. Talos, D. A. Sdrulla, A. C. Brumback, G. C. Mathews, T. A. Benke, E. Delpire, F. E. Jensen, K. J. Staley, NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11, 1205-1213 (2005).
37. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255 (1999).
38. N. J. Ernest, A. K. Weaver, L. B. Van Duyn, H. W. Sontheimer, Relative contribution of chloride channels and transporters to regulatory volume decrease in human glioma cells. Am. J. Physiol. Cell Physiol. 288, C1451-C1460 (2005).
39. J. Engel Jr., A. Bragin, R. Staba, I. Mody, High-frequency oscillations: What is normal and what is not? Epilepsia 50, 598-604 (2009).
40. G. Foffani, Y. G. Uzcategui, B. Gal, L. Menendez de la Prida, Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 55, 930-941 (2007).
41. M. M. Zaatreh, K. S. Firlik, D. D. Spencer, S. S. Spencer, Temporal lobe tumoral epilepsy: Characteristics and predictors of surgical outcome. Neurology 61, 636-641 (2003).
42. R. Soffietti, B. G. Baumert, L. Bello, A. von Deimling, H. Duffau, M. Frénay, W. Grisold, R. Grant, F. Graus, K. Hoang-Xuan, M. Klein, B. Melin, J. Rees, T. Siegal, A. Smits, R. Stupp, W. Wick, European Federation of Neurological Societies, Guidelines on management of low-grade gliomas: Report of an EFNS-EANO Task Force. Eur. J. Neurol. 17, 1124-1133 (2010).
43. A. Pace, A. Vidiri, E. Galiè, M. Carosi, S. Telera, A. M. Cianciulli, P. Canalini, D. Giannarelli, B. Jandolo, C. M. Carapella, Temozolomide chemotherapy for progressive low-grade glioma: Clinical benefits and radiological response. Ann. Oncol. 14, 1722-1726 (2003).
44. J. H. Sherman, K. Moldovan, H. K. Yeoh, R. M. Starke, N. Pouratian, M. E. Shaffrey, D. Schiff, Impact of temozolomide chemotherapy on seizure frequency in patients with low-grade gliomas. J. Neurosurg. 114, 1617-1621 (2011).
45. A. Rosati, A. Tomassini, B. Pollo, C. Ambrosi, A. Schwarz, A. Padovani, B. Bonetti, Epilepsy in cerebral glioma: Timing of appearance and histological correlations. J. Neurooncol. 93, 395-400 (2009).
46. -- cotransporter, in epilepsy-associated malformations of cortical development. Neuroscience 145, 185-196 (2007).
47. J. S. Kim, W. B. Kim, Y. B. Kim, Y. Lee, Y. S. Kim, F. Y. Shen, S. W. Lee, D. Park, H. J. Choi, J. Hur, J. J. Park, H. C. Han, C. S. Colwell, Y. W. Cho, Y. I. Kim, Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat. J. Neurosci. 31, 13312-13322 (2011).
48. S. C. Buckingham, S. Robel, Glutamate and tumor-associated epilepsy: Glial cell dysfunction in the peritumoral environment. Neurochem. Int. 63, 696-701 (2013).
49. Q. Yan, H. L. Yu, J. T. Li, Study on the expression of BDNF in human gliomas. Sichuan Da Xue Xue Bao Yi Xue Ban 40, 415-417 (2009). Downloaded from stm.sciencemag.org on July 19, 2014
50. A. Chiaretti, L. Aloe, A. Antonelli, A. Ruggiero, M. Piastra, R. Riccardi, G. Tamburrini, C. Di Rocco, Neurotrophic factor expression in childhood low-grade astrocytomas and ependymomas. Childs Nerv. Syst. 20, 412-419 (2004).
51. C. Rivera, J. Voipio, J. Thomas-Crusells, H. Li, Z. Emri, S. Sipilä, J. A. Payne, L. Minichiello, M. Saarma, K. Kaila, Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24, 4683-4691 (2004).
52. - in and out of cells: Implications for control of cell volume and neuronal excitability. Proc. Natl. Acad. Sci. U.S.A. 102, 16783-16788 (2005).
53. J. Macas, M. C. Ku, C. Nern, Y. Xu, H. Bühler, M. Remke, M. Synowitz, K. Franz, V. Seifert, K.H. Plate, H. Kettenmann, R. Glass, S. Momma, Generation of neuronal progenitor cells in response to tumors in the human brain. Stem Cells 32, 244-257 (2014).
54. K. Lote, A. E. Stenwig, K. Skullerud, H. Hirschberg, Prevalence and prognostic significance of epilepsy in patients with gliomas. Eur. J. Cancer 34, 98-102 (1998).
55. J. Pallud, E. Audureau, M. Blonski, N. Sanai, L. Bauchet, D. Fontaine, E. Mandonnet, E. Dezamis, D. Psimaras, J. Guyotat, P. Peruzzi, P. Page, B. Gal, E. Párraga, M. H. Baron, M. Vlaicu, R. Guillevin, B. Devaux, H. Duffau, L. Taillandier, L. Capelle, G. Huberfeld, Epileptic seizures in diffuse low-grade gliomas in adults. Brain 137, 449-462 (2014).
56. V. Dzhala, G. Valeeva, J. Glykys, R. Khazipov, K. Staley, Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain. J. Neurosci. 32, 4017-4031 (2012).
57. A. Beaumont, M. Clarke, I. R. Whittle, The effects of malignant glioma on the EEG and seizure thresholds: An experimental study. Acta Neurochir. 138, 370-381 (1996).
58. S. E. Connor, R. Gunny, T. Hampton, R. O'gorman, Magnetic resonance image registration and subtraction in the assessment of minor changes in low grade glioma volume. Eur. Radiol. 14, 2061-2066 (2004).
59. M. A. Hammoud, B. L. Ligon, R. elSouki, W. M. Shi, D. F. Schomer, R. Sawaya, Use of intraoperative ultrasound for localizing tumors and determining the extent of resection: A comparative study with magnetic resonance imaging. J. Neurosurg. 84, 737-741 (1996).
60. R. J. Staba, C. L. Wilson, A. Bragin, I. Fried, J. Engel Jr., Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol. 88, 1743-1752 (2002).