Gabaergic alterations in neocortex of patients with pharmacoresistant temporal lobe epilepsy can explain the comorbidity of anxiety and depression: The potential impact of clinical factors

Frontiers in Cellular Neuroscience

Volumn 8, Issue JAN, 2015, Pages

  Rocha, Luisa ^a   Alonso Vanegas, Mario ^b   Martínez Juarez, Iris E ^b   Orozco Suárez, Sandra ^c   Escalante Santiago, David ^c   Feria Romero, Iris AngéLica ^c   Zavala Tecuapetla, Cecilia ^a,b   Cisneros Franco, José Miguel ^b   Buentello García, Ricardo Masao ^b   Cienfuegos, JesúS ^b  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^c National Medical Center   (Mexico)

Author keywords

Anxiety; Depression; G protein; GABA receptors; Temporal lobe epilepsy; Temporal neocortex

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN;

ADOLESCENT; ADULT; ANXIETY; ARTICLE; AUTOPSY; AUTORADIOGRAPHY; CLINICAL ARTICLE; COMORBIDITY; CONTROLLED STUDY; DEPRESSION; HUMAN; NEOCORTEX; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TEMPORAL LOBE EPILEPSY;

EID: 84938053518     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00442     Document Type: Article

References (61)

1. Aston, C., Jiang, L., and Sokolov, B. P. (2005). Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol. Psychiatry 10, 309-322. doi:10.1038/sj.mp.4001565
2. Avissar, S., and Schreiber, G. (1992). The involvement ofguanine nucleotide binding proteins in the pathogenesis and treatment of affective disorders. Biol. Psychiatry 31, 435459. doi:10.1016/0006-3223(92)90257-Z
3. Avoli, M., Louvel, J., Drapeau, C., Pumain, R., and Kurcewicz, I. (1995). GABAA-mediated inhibition and in vitro epileptogenesis in the human neocortex. J. Neurophysiol. 73,468-484.
4. Babb, T. L., Pretorius, J. K., Kupfer, W. R., and Crandall, P. H. (1989). Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J. Neurosci. 9, 2562-2574.
5. Beauregard, M., Leroux, J. M., Bergman, S., Arzoumanian, Y., Beaudoin, G., Bour-gouin, P., et al. (1988). The functional neuroanatomy of major depression: an fMRI study using an emotional activation paradigm. Neuroreport 9, 3253-3258. doi:10.1097/00001756-199810050-00022
6. Briellmann, R. S., Hopwood, M. J., and Jackson, G. D. (2007). Major depression in temporal lobe epilepsy with hippocampal sclerosis: clinical and imaging correlates. J. Neurol. Neurosurg. Psychiatr. 78, 1226-1230.doi:10.1136/jnnp.2006. 104521
7. Chagnac-Amitai, Y., and Connors, B. W. (1989). Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61, 747-758.
8. Chandra, D., Halonen, L. M., Linden, A. M., Procaccini, C., Hellsten, K., Homanics, G. E., et al. (2010). Prototypic GABA(A) receptor agonist muscimol acts preferentially through forebrain high-affinity binding sites. Neuropsychopharmacology 35, 999-1007. doi:10.1038/npp.2009.203
9. Croarkin, P. E., Levinson, A. J., and Daskalakis, Z. J. (2011). Evidence for GABAer-gic inhibitory deficits in major depressive disorder. Neurosci. Biobehav. Rev. 35, 818-825. doi:10.1016/j.neubiorev.2010.10.002
10. Drevets, W. C., Price, J. L., and Furey, M. L. (2008). Brain structural and functional abnormalities in mood disorders: implications for neurocircuitrymodels ofdepression. BrainStruct. Funct. 213, 93-118. doi:10.1007/s00429-008-0189-x
11. During, M. J., and Spencer, D. D. (1993). Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341, 1607-1610. doi:10.1016/0140-6736(93)90754-5
12. Earnheart, J. C., Schweizerm, C., Crestani, F., Iwasato, T., Itohara, S., Mohler, H., et al. (2007). GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxietyand depression states. J. Neurosci. 27, 3845-3854. doi:10.1523/JNEUROSCI.3609-06.2007
13. Enna, S. J., and Bowery, N. G. (2004). GABAB receptor alterations as indicators of physiological and pharmacological function. Biochem. Pharmacol. 68, 1541-1548. doi:10.1016/j.bcp.2004.06.037
14. First, M. B., Spitzer, R. L., Gibbon, M., and Williams, J. B. W. (1999). Entrevista Clinica Estructurada Para los Trastornos del eje I del DSM-IV. Version Clinica (SCID-I). Barcelona: Masson.
15. Frølund B., Ebert B., Kristiansen U., Liljefors T., and Krogsgaard-Larsen P. (2002). GABA(A) receptor ligands and their therapeutic potentials. Curr. Top. Med. Chem. 2, 817-832. doi:10.2174/1568026023393525
16. Gómez-Arias, B., Crail-Melendez, D., Lopez-Zapata, R., and Martinez-Juarez, I. E. (2012). Severity of anxiety and depression are related to a higher perception of adverse effects of antiepileptic drugs. Seizure 21, 588-594. doi:10.1016/j.seizure.2012.06.003
17. Goncalves, E. B., and Cendes, F. (2011). Depression in patients with refractory temporal lobe epilepsy. Arq. Neuropsiquiatr. 69, 775-777. doi:10.1590/S0004-282X2011000600010
18. Gonzalez-Maeso, J., Rodriguez-Puertas, R., Gabilondo A. M., and Meana, J. J. (2000). Characterization of receptor-mediated [35S]GTPgammaS binding to cortical membranes from postmortem human brain. Eur. J. Pharmacol. 390, 25-36. doi:10.1016/S0014-2999(99)00827-4
19. Grabowska-Grzyb, A., Jedrzejczak, J., Naganska, E., and Fiszer, U. (2006). Risk factors for depression in patients with epilepsy. Epilepsy Behav. 8, 411-417. doi:10.1016/j.yebeh.2005.12.005
20. Gravielle, M. C., Faris, R., Russek, S. J., and Farb, D. H. (2005). GABA induces activity dependent delayed-onset uncoupling of GABA/benzodiazepine site interactions in neocortical neurons. J. Biol. Chem. 280, 20954-20960. doi:10.1074/jbc. M500131200
21. Herrero, M. J., Blanch, J., Peri, J. M., De Pablo, J., Pintor, L., and Bulbena, A. (2003). A validation studyof the hospital anxietyand depression scale (HADS) in a Spanish population. Gen. Hosp. Psychiatry 25,277-283. doi:10.1016/S0163-8343(03)00043-4
22. Hines, R. M., Davies, P. A., Moss, S. J., and Maguire, J. (2012). Functional regulation of GABAA receptors in nervous system pathologies. Curr. Opin. Neurobiol. 22, 552-558. doi:10.1016/j.conb.2011.10.007
23. Kanner, A. M. (2011). Depression and epilepsy: a bidirectional relation? Epilepsia 52(Suppl. 1), 21-27. doi:10.1111/j.1528-1167.2010.02907.x
24. Kendrick, K. M., Keverne, E. B., Chapman, C., and Baldwin, B. A. (1988). Microdial-ysis measurement of oxytocin, aspartate, gamma-aminobutyric acid and gluta-mate release from the olfactorybulb of the sheep during vagino cervical stimulation. Brain Res. 442, 171-174. doi:10.1016/0006-8993(88)91447-3
25. Koepp, M. J., Hammers, A., Labbe, C., Woermann, F. G., Brooks, D. J., and Duncan, J. S. (2000). 11C-flumazenil PET in patients with refractory temporal lobe epilepsy and normal MRI. Neurology 54, 332-339. doi:10.1212/WNL.54.2.332
26. Kohl, M. M., and Paulsen, O. (2010). The roles of GABAB receptors in cortical network activity. Adv. Pharmacol. 58, 205-229. doi:10.1016/S1054-3589(10) 58009-8
27. Kondziella, D., Alvestad, S., Vaaler, A., and Sonnewald, U. (2007). Which clinical and experimental data link temporal lobe epilepsy with depression? J. Neurochem. 103, 2136-2152. doi:10.1111/j.1471-4159.2007.04926.x
28. la Fougere, C., Rominger, A., Forster, S., Geisler, J., and Bartenstein, P. (2009). PET and SPECT in epilepsy: a critical review. Epilepsy Behav. 15, 50-55. doi:10.1016/j.yebeh.2009.02.025
29. Lavoie, A. M., and Twyman, R. E. (1996). Direct evidence for diazepam modulation of GABAA receptor microscopic affinity. Neuropharmacology 35, 1383-1392. doi:10.1016/S0028-3908(96)00077-9
30. Lowe, S. L., Francis, P. T., Procter, A. W., Palmer, A. M., Davison, A. N., and Bowen, D. M. (1988). Gamma-aminobutyric acid concentration in brain tissue attwo stages of Alzheimer's disease. Brain 111(Pt 4), 785-799. doi:10.1093/brain/111.4.785
31. Lowry, O. H., Rosenbrough, N. J., Farr, R. J., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-273.
32. Luna-Munguia, H., Orozco-Suarez, S., and Rocha, L. (2011). Effects of high fre-quencyelectrical stimulation and R-verapamil on seizure susceptibilityand glu-tamate and GABArelease in amodel ofphenytoin-resistant seizures. Neurophar-macology 61, 807-814. doi:10.1016/j.neuropharm.2011.05.027
33. Maguire, J., and Mody, I. (2008). GABA(A)R plasticityduring pregnancy: relevance to postpartum depression. Neuron 59, 207-213. doi:10.1016/j.neuron.2008.06.019
34. Martin, S.B., Waniewski, R.A., Battaglioli, G., and Martin, D. L. (2003). Post-mortem degradation of brain glutamate decarboxylase. Neurochem. Int. 42, 549-554. doi:10.1016/S0197-0186(02)00189-4
35. Mathern, G. W., Babb, T. L., Pretorius, J. K., and Leite, J. P. (1995). Reactive synap-togenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J. Neurosci. 15, 3990-4004.
36. Merali, Z., Du, L., Hrdina, P., Palkovits, M., Faludi, G., Poulter, M. O., et al. (2004). Dysregulation in the suicide brain: mRNA expression of corticotropin-releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region. J. Neurosci. 24, 1478-1485. doi:10.1523/JNEUROSCI.4734-03.2004
37. Motohashi, N. (1992). GABA receptor alterations after chronic lithium administration. Comparison with carbamazepine and sodium valproate. Prog. Neuropsychopharmacol. Biol. Psychiatry16, 571-579. doi:10.1016/0278-5846(92) 90062-J
38. Mula, M., and Sander, J. W. (2007). Negative effects ofantiepileptic drugs on mood in patients with epilepsy. DrugSaf. 30,555-567. doi:10.2165/00002018-200730070-00001
39. Nikolaus, S., Antke, C., Beu, M., and Muller, H. W. (2010). Cortical GABA, striatal dopamine and midbrain serotonin as the key players in compulsive and anxiety disorders-results from in vivo imaging studies. Rev. Neurosci. 21, 119-139. doi:10.1515/REVNEURO.2010.21.2.119
40. Nyitrai, G., Kekesi, K. A., and Juhasz, G. (2006). Extracellular level ofGABAand Glu: in vivo microdialysis-HPLC measurements. Curr. Top. Med. Chem. 6, 935-940. doi:10.2174/156802606777323674
41. Olsen, R. W. (1981). GABA-benzodiazepine-barbiturate receptor interactions. J. Neurochem. 37, 1-13. doi:10.1111/j.1471-4159.1981.tb05284.x
42. Ongur, D., and Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10, 206-219.
43. Ongur, D., An, X., and Price, J. L. (1998). Prefrontal cortical projections to the hypo-thalamus in macaque monkeys. J. Comp. Neurol. 401, 480-505. doi:10.1002/(SICI)1096-9861(19981130)401:4<480::AID-CNE4>3.3.CO;2-6
44. Ongur, D., Ferry, A. T., and Price, J. L. (2003). Architectonic subdivision of the human orbital and medial prefrontal cortex. J. Comp. Neurol. 460, 425-449. doi:10.1002/cne.10609
45. Pacey, L. K., Tharmalingam, S., and Hampson, D. R. (2011). Subchronic administration and combination metabotropic glutamate and GABAB receptor drug therapy in fragile X syndrome. J. Pharmacol. Exp. Ther. 338, 897-905. doi:10.1124/jpet.111.183327
46. Pacheco, M. A., Stockmeier, C., Meltzer, H. Y., Overholser, J. C., Dilley, G. E., and Jope, R. S. (1996). Alterations in phosphoinositide signaling and G-protein levels in depressed suicide brain. Brain Res. 723, 37-45. doi:10.1016/0006-8993(96)00207-7
47. Partiot, A., Grafman, J., Sadato, N., Wachs, J., and Hallett, M. (1995). Brain activation during the generation of non-emotional and emotional plans. Neuroreport 6, 1397-1400. doi:10.1097/00001756-199507100-00009
48. Peng, W. F., Ding, J., Li, X., Mao, L. Y., and Wang, X. (2014). Clinical risk factors for depressive symptoms in patients with epilepsy. Acta Neurol. Scand. 129, 343-349. doi:10.1111/ane.12191
49. Pericic, D., Strac, D. S., Jembrek, M. J., and Vlainic, J. (2007). Allosteric uncoupling and up-regulation of benzodiazepine and GABA recognition sites following chronic diazepam treatment of HEK 293 cells stably transfected with alpha1beta2gamma2S subunits of GABA (A) receptors. Naunyn Schmiedebergs Arch. Pharmacol. 375, 177-187. doi:10.1007/s00210-007-0152-z
50. Princivalle, A. P., Duncan, J. S., Thom, M., and Bowery, N. G. (2002). Studies of GABA(B) receptors labelled with [(3)H]-CGP62349 in hippocampus resected from patients with temporal lobe epilepsy. Br. J. Pharmacol. 136, 1099-1106. doi:10.1038/sj.bjp.0704812
51. Rocha, L., Alonso-Vanegas, M., Orozco-Suarez, S., Alcantara-Gonzalez, D., Cruzblanca, H., and Castro, E. (2014). Do certain signal transduction mechanisms explain the comorbidityofepilepsyand mood disorders? EpilepsyBehav. 38, 25-31. doi:10.1016/j.yebeh.2014.01.001
52. Saleem, K. S., Price, J. L., and Hashikawa, T. (2007). Cytoarchitectonic and chemoar-chitectonic subdivisions of the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 500, 973-1006. doi:10.1002/cne.21141
53. San-Juan, D., Tapia, C. A., Gonzalez-Aragon, M. F., Martinez Mayorga, A., Staba, R. J., and Alonso-Vanegas, M. (2011). The prognostic role of electrocorticogra-phyin tailored temporal lobe surgery. Seizure 20, 564-569. doi:10.1016/j.seizure.2011.04.006
54. Sheline, Y. I., Barch, D. M., Price, J. L., Rundle, M. M., Vaishnavi, S. N., Snyder, A. Z., et al. (2009). The default mode network and self-referential processes in depression. Proc. Natl. Acad. Sci. U.S.A. 106, 1942-1947. doi:10.1073/pnas.0812686106
55. Sperk, G., Drexel, M., and Pirker, S. (2009). Neuronal plasticity in animal models and the epileptic human hippocampus. Epilepsia 50(Suppl 12), 29-31. doi:10.1111/j.1528-1167.2009.02365.x
56. Suzuki Y., Mimaki T., Arai, H., Okada, S., and Kuriyama, K. (1991). Effectofgamma-vinyl gamma-aminobutyric acid on the gamma-aminobutyric acid receptor-coupled chloride ion channel in vesicles from the brain of the rat. Neurophar-macology 30, 423-427. doi:10.1016/0028-3908(91)90002-S
57. Taniyama, K., Niwa, M., Kataoka, Y., and Yamashita, K. (1992). Activation ofprotein kinase C suppresses the gamma-aminobutyric acidB receptor-mediated inhibition of the vesicular release of noradrenaline and acetylcholine. J. Neurochem. 58, 1239-1245. doi:10.1111/j.1471-4159.1992.tb11334.x
58. Teichgraber, L. A., Lehmann, T. N., Meencke, H. J., Weiss, T., Nitsch, R., and Deisz, R. A. (2009). Impaired function of GABA(B) receptors in tissues from pharma-coresistant epilepsy patients. Epilepsia 50, 1697-1716. doi:10.1111/j.1528-1167.2009.02094.x
59. Uhlhaas, P. J., and Singer, W. (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11, 100-113. doi:10.1038/nrn2774
60. Vithlani, M., Hines, R. M., Zhong, P., Terunuma, M., Hines, D. J., Revilla-Sanchez, R., et al. (2013). The abilityofBDNF to modifyneurogenesis and depressive-like behaviors is dependent upon phosphorylation of tyrosine residues 365/367 in the GABA(A)-receptor y2 subunit. J. Neurosci. 33, 15567-15577. doi:10.1523/ JNEUROSCI.1845-13.2013
61. Whitehouse, P. J., Lynch, D., and Kuhar, M. J. (1984). Effects of postmortem delay and temperature on neurotransmitter receptor binding in a rat model of the human autopsy process. J. Neurochem. 43, 553-559. doi:10.1111/j.1471-4159.1984.tb00934.x