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BioMed Research International
Volume 2013 (2013), Article ID 960126, 11 pages
http://dx.doi.org/10.1155/2013/960126
Clinical Study

Microtubule-Associated Proteins in Mesial Temporal Lobe Epilepsy with and without Psychiatric Comorbidities and Their Relation with Granular Cell Layer Dispersion

1Ribeirao Preto Medical School, Department of Neurosciences and Behavior, University of Sao Paulo (USP), Avenida Bandeirantes 3900, 14049-900 Ribeirao Preto, SP, Brazil
2Center for Interdisciplinary Research on Applied Neurosciences (NAPNA), USP, Avenida Bandeirantes 3900, 14049-900 Ribeirao Preto, SP, Brazil
3National Institute of Science and Technology in Translational Medicine (INCT-TM/CNPq), Avenida Bandeirantes 3900, 14049-900 Ribeirao Preto, SP, Brazil
4Ribeirao Preto Medical School, Department of Surgery, USP, Avenida Bandeirantes 3900, 14049-900 Ribeirao Preto, SP, Brazil

Received 30 April 2013; Revised 19 July 2013; Accepted 24 July 2013

Academic Editor: Johan Pallud

Copyright © 2013 Ludmyla Kandratavicius et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. W. Mathern, T. L. Babb, J. K. Pretorius, and J. P. Leite, “Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata,” Journal of Neuroscience, vol. 15, no. 5, pp. 3990–4004, 1995. View at Scopus
  2. T. L. Babb, W. R. Kupfer, J. K. Pretorius, P. H. Crandall, and M. F. Levesque, “Synaptic reorganization by mossy fibers in human epileptic fascia dentata,” Neuroscience, vol. 42, no. 2, pp. 351–363, 1991. View at Publisher · View at Google Scholar · View at Scopus
  3. T. L. Babb, W. J. Brown, J. Pretorius, C. Davenport, J. P. Lieb, and P. H. Crandall, “Temporal lobe volumetric cell densities in temporal lobe epilepsy,” Epilepsia, vol. 25, no. 6, pp. 729–740, 1984. View at Scopus
  4. M. Isokawa, “Remodeling dendritic spines of dentate granule cells in temporal lobe epilepsy patients and the rat pilocarpine model,” Epilepsia, vol. 41, supplement 6, pp. S14–S17, 2000. View at Scopus
  5. M. E. Scheibel, P. H. Crandall, and A. B. Scheibel, “The hippocampal-dentate complex in temporal lobe epilepsy. A Golgi study,” Epilepsia, vol. 15, no. 1, pp. 55–80, 1974. View at Scopus
  6. C. R. Houser, “Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy,” Brain Research, vol. 535, no. 2, pp. 195–204, 1990. View at Publisher · View at Google Scholar · View at Scopus
  7. A. V. Silva, J.-C. Houzel, I. Croaro et al., “Granular cell dispersion and bilamination: two distinct histopathological patterns in epileptic hippocampi?” Epileptic Disorders, vol. 9, no. 4, pp. 438–442, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Kandratavicius, P. Rosa-Neto, M. R. Monteiro et al., “Distinct increased metabotropic glutamate receptor type 5 (mGluR5) in temporal lobe epilepsy with and without hippocampal sclerosis,” Hippocampus, 2013. View at Publisher · View at Google Scholar
  9. L. Kandratavicius, C. Lopes-Aguiar, L. S. Bueno-Junior, R. N. Romcy-Pereira, J. E. Hallak, and J. P. Leite, “Psychiatric comorbidities in temporal lobe epilepsy: possible relationships between psychotic disorders and involvement of limbic circuits,” Revista Brasileira de Psiquiatria, vol. 34, pp. 454–466, 2012.
  10. L. Kandratavicius, R. N. Ruggiero, J. E. Hallak, N. Garcia-Cairasco, and J. P. Leite, “Pathophysiology of mood disorders in temporal lobe epilepsy,” Revista Brasileira de Psiquiatria, vol. 34, pp. S233–S259, 2012.
  11. L. Kandratavicius, J. E. Hallak, L. T. Young, J. A. Assirati Jr., C. G. Carlotti Jr., and J. P. Leite, “Differential aberrant sprouting in temporal lobe epilepsy with psychiatric co-morbidities,” Psychiatry Research, vol. 195, no. 3, pp. 144–150, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Pollard, M. khrestchatisky, J. Moreau, Y. Ben-Ari, and A. Represa, “Correlation between reactive sprouting and microtubule protein expression in epileptic hippocampus,” Neuroscience, vol. 61, no. 4, pp. 773–788, 1994. View at Publisher · View at Google Scholar · View at Scopus
  13. X. X. Yan, Y. Cai, J. Shelton et al., “Chronic temporal lobe epilepsy is associated with enhanced Alzheimer-like neuropathology in 3xTg-AD mice,” PLoS ONE, vol. 7, Article ID e48782, 2012.
  14. F.-F. Tian, C. Zeng, Y.-F. Ma et al., “Potential roles of Cdk5/p35 and tau protein in hippocampal mossy fiber sprouting in the PTZ kindling model,” Clinical Laboratory, vol. 56, no. 3-4, pp. 127–136, 2010. View at Scopus
  15. R. P. Tucker, “The roles of microtubule-associated proteins in brain morphogenesis: a review,” Brain Research Reviews, vol. 15, no. 2, pp. 101–120, 1990. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Dehmelt and S. Halpain, “The MAP2/Tau family of microtubule-associated proteins,” Genome Biology, vol. 6, no. 1, article 204, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Rosoklija, G. Toomayan, S. P. Ellis et al., “Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings,” Archives of General Psychiatry, vol. 57, no. 4, pp. 349–356, 2000. View at Scopus
  18. D. Cotter, S. Wilson, E. Roberts, R. Kerwin, and I. P. Everall, “Increased dendritic MAP2 expression in the hippocampus in schizophrenia,” Schizophrenia Research, vol. 41, no. 2, pp. 313–323, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Cotter, R. Kerwin, B. Doshi, C. S. Martin, and I. P. Everall, “Alterations in hippocampal non-phosphorylated MAP2 protein expression in schizophrenia,” Brain Research, vol. 765, no. 2, pp. 238–246, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. S. E. Arnold, “Cellular and molecular neuropathology of the parahippocampal region in schizophrenia,” Annals of the New York Academy of Sciences, vol. 911, pp. 275–292, 2000. View at Scopus
  21. S. E. Arnold, V. M.-Y. Lee, R. E. Gur, and J. Q. Trojanowski, “Abnormal expression of two microtubule-associated proteins (MAP2 and MAP5) in specific subfields of the hippocampal formation in schizophrenia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 23, pp. 10850–10854, 1991. View at Scopus
  22. P. Gudmundsson, I. Skoog, M. Waern et al., “The relationship between cerebrospinal fluid biomarkers and depression in elderly women,” The American Journal of Geriatric Psychiatry, vol. 15, no. 10, pp. 832–838, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. A. J. Law, C. S. Weickert, T. M. Hyde, J. E. Kleinman, and P. J. Harrison, “Reduced spinophilin but not microtubule-associated protein 2 expression in the hippocampal formation in schizophrenia and mood disorders: molecular evidence for a pathology of dendritic spines,” The American Journal of Psychiatry, vol. 161, no. 10, pp. 1848–1855, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Blumcke, W. Zuschratter, J. C. Schewe et al., “Cellular pathology of hilar neurons in Ammon's horn sclerosis,” Journal of Comparative Neurology, vol. 414, pp. 437–453, 1999.
  25. C. L. Dalmagro, T. R. Velasco, M. M. Bianchin et al., “Psychiatric comorbidity in refractory focal epilepsy: a study of 490 patients,” Epilepsy and Behavior, vol. 25, pp. 593–597, 2012.
  26. A. Gaitatzis, M. R. Trimble, and J. W. Sander, “The psychiatric comorbidity of epilepsy,” Acta Neurologica Scandinavica, vol. 110, no. 4, pp. 207–220, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. A. T. Berg, “Identification of pharmacoresistant epilepsy,” Neurologic Clinics, vol. 27, no. 4, pp. 1003–1013, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Engel Jr., “Current concepts: surgery for seizures,” The New England Journal of Medicine, vol. 334, no. 10, pp. 647–652, 1996. View at Scopus
  29. P. Sachdev, “Schizophrenia-like psychosis and epilepsy: the status of the association,” The American Journal of Psychiatry, vol. 155, no. 3, pp. 325–336, 1998. View at Scopus
  30. A. W. Beard and E. Slater, “The schizophrenic-like psychoses of epilepsy,” Proceedings of the Royal Society of Medicine, vol. 55, pp. 311–316, 1962. View at Scopus
  31. G. F. Anhê, A. S. Torrão, T. C. A. Nogueira et al., “ERK3 associates with MAP2 and is involved in glucose-induced insulin secretion,” Molecular and Cellular Endocrinology, vol. 251, no. 1-2, pp. 33–41, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. D. M. O. Ramirez, S. Andersson, and D. W. Russell, “Neuronal expression and subcellular localization of cholesterol 24-hydroxylase in the mouse brain,” Journal of Comparative Neurology, vol. 507, no. 5, pp. 1676–1693, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. U. K. Jinwal, J. Koren III, S. I. Borysov et al., “The Hsp90 cochaperone, FKBP51, increases tau stability and polymerizes microtubules,” Journal of Neuroscience, vol. 30, no. 2, pp. 591–599, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. Hou, Q. Li, L. He et al., “Microtubule association of the neuronal p35 activator of Cdk5,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 18666–18670, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Lorente de No, “Studies on the structure of the cerebral cortex II. Continuation of study of the ammonic system,” Journal Für Psychologie Und Neurologie, vol. 46, pp. 113–177, 1934.
  36. M. Abercrombie, “Estimation of nuclear population from microtome sections,” Anatomical Record, vol. 94, pp. 239–247, 1946.
  37. G. W. Mathern, P. D. Adelson, L. D. Cahan, and J. P. Leite, “Hippocampal neuron damage in human epilepsy: meyer's hypothesis revisited,” Progress in Brain Research, vol. 135, pp. 237–251, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. G. W. Mathern, J. K. Pretorius, D. Mendoza et al., “Hippocampal N-methyl-D-aspartate receptor subunit mRNA levels in temporal lobe epilepsy patients,” Annals of Neurology, vol. 46, pp. 343–358, 1999.
  39. G. W. Mathern, D. Mendoza, A. Lozada et al., “Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy,” Neurology, vol. 52, no. 3, pp. 453–472, 1999. View at Scopus
  40. G. W. Mathern, J. K. Pretorius, H. I. Kornblum et al., “Human hippocampal AMPA and NMDA mRNA levels in temporal lobe epilepsy patients,” Brain, vol. 120, no. 11, pp. 1937–1959, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. G. W. Mathern, T. L. Babb, B. G. Vickrey, M. Melendez, and J. K. Pretorius, “The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy,” Brain, vol. 118, no. 1, pp. 105–118, 1995. View at Scopus
  42. J. E. Peixoto-Santos, O. Y. Galvis-Alonso, T. R. Velasco et al., “Increased metallothionein I/II expression in patients with temporal lobe epilepsy,” Plos ONE, vol. 7, Article ID e44709, 2012.
  43. M. Thom, “Hippocampal sclerosis: progress since sommer,” Brain Pathology, vol. 19, no. 4, pp. 565–572, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Lurton, L. Sundstrom, C. Brana, B. Bloch, and A. Rougier, “Possible mechanisms inducing granule cell dispersion in humans with temporal lobe epilepsy,” Epilepsy Research, vol. 26, no. 2, pp. 351–361, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Crespel, P. Coubes, M.-C. Rousset et al., “Immature-like astrocytes are associated with dentate granule cell migration in human temporal lobe epilepsy,” Neuroscience Letters, vol. 330, no. 1, pp. 114–118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. N. Heck, J. Garwood, J.-P. Loeffler, Y. Larmet, and A. Faissner, “Differential upregulation of extracellular matrix molecules associated with the appearance of granule cell dispersion and mossy fiber sprouting during epileptogenesis in a murine model of temporal lobe epilepsy,” Neuroscience, vol. 129, no. 2, pp. 309–324, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. T. M. Freiman, J. Eismann-Schweimler, and M. Frotscher, “Granule cell dispersion in temporal lobe epilepsy is associated with changes in dendritic orientation and spine distribution,” Experimental Neurology, vol. 229, no. 2, pp. 332–338, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. B. L. Murphy and S. C. Danzer, “Somatic translocation: a novel mechanism of granule cell dendritic dysmorphogenesis and dispersion,” Journal of Neuroscience, vol. 31, no. 8, pp. 2959–2964, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. D. Hsu, “The dentate gyrus as a filter or gate: a look back and a look ahead,” Progress in Brain Research, vol. 163, pp. 601–613, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. I. Blümcke, I. Kistner, H. Clusmann et al., “Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies,” Acta Neuropathologica, vol. 117, no. 5, pp. 535–544, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Pauli, M. Hildebrandt, J. Romstöck, H. Stefan, and I. Blümcke, “Deficient memory acquisition in temporal lobe epilepsy is predicted by hippocampal granule cell loss,” Neurology, vol. 67, no. 8, pp. 1383–1389, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. T. D. Perera, J. D. Coplan, S. H. Lisanby et al., “Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates,” Journal of Neuroscience, vol. 27, no. 18, pp. 4894–4901, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Kodama, T. Fujioka, and R. S. Duman, “Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat,” Biological Psychiatry, vol. 56, no. 8, pp. 570–580, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. T. D. Perera, A. J. Dwork, K. A. Keegan et al., “Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult Nonhuman primates,” PLoS ONE, vol. 6, no. 4, Article ID e17600, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Moncrieff and J. Leo, “A systematic review of the effects of antipsychotic drugs on brain volume,” Psychological Medicine, vol. 40, no. 9, pp. 1409–1422, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. J. P. Leite, T. L. Babb, J. K. Pretorius, P. A. Kuhlman, K. M. Yeoman, and G. W. Mathern, “Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats,” Epilepsy Research, vol. 26, no. 1, pp. 219–231, 1996. View at Publisher · View at Google Scholar · View at Scopus
  57. A. H. Ratzliff, V. Santhakumar, A. Howard, and I. Soltesz, “Mossy cells in epilepsy: rigor mortis or vigor mortis?” Trends in Neurosciences, vol. 25, no. 3, pp. 140–144, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Yang, G. Wang, H. Wang, Z. Liu, and X. Wang, “Cytoskeletal alterations in rat hippocampus following chronic unpredictable mild stress and re-exposure to acute and chronic unpredictable mild stress,” Behavioural Brain Research, vol. 205, no. 2, pp. 518–524, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. H.-J. Yang, Y.-F. Li, H.-T. Zhang et al., “Up-regulation of microtubule-associated protein 4 and drebrin A mRNA expression by antidepressants in rat hippocampus following chronic stress,” Neuroscience Letters, vol. 351, no. 3, pp. 206–208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. V. Fournet, G. de Lavilleon, A. Schweitzer, B. Giros, A. Andrieux, and M. P. Martres, “Both chronic treatments by epothilone D and fluoxetine increase the short-term memory and differentially alter the mood status of STOP/MAP6 KO mice,” Journal of Neurochemistry, vol. 123, pp. 982–996, 2012.
  61. P. Schönknecht, A. Hempel, A. Hunt et al., “Cerebrospinal fluid tau protein levels in schizophrenia,” European Archives of Psychiatry and Clinical Neuroscience, vol. 253, no. 2, pp. 100–102, 2003. View at Scopus
  62. S. H. Fatemi, J. A. Earle, and T. McMenomy, “Reduction in Reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression,” Molecular Psychiatry, vol. 5, no. 6, pp. 654–663, 2000. View at Scopus
  63. S. L. Eastwood, P. W. J. Burnet, and P. J. Harrison, “Altered synaptophysin expression as a marker of synaptic pathology in schizophrenia,” Neuroscience, vol. 66, no. 2, pp. 309–319, 1995. View at Publisher · View at Google Scholar · View at Scopus
  64. J. S. Chambers, D. Thomas, L. Saland, R. L. Neve, and N. I. Perrone-Bizzozero, “Growth-associated protein 43 (GAP-43) and synaptophysin alterations in the dentate gyrus of patients with schizophrenia,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 29, no. 2, pp. 283–290, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. S. L. Eastwood and P. J. Harrison, “Decreased expression of vesicular glutamate transporter 1 and complexin II mRNAs in schizophrenia: further evidence for a synaptic pathology affecting glutamate neurons,” Schizophrenia Research, vol. 73, no. 2-3, pp. 159–172, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. E. A. Proper, A. B. Oestreicher, G. H. Jansen et al., “Immunohistochemical characterization of mossy fibre sprouting in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy,” Brain, vol. 123, pp. 19–30, 2000. View at Scopus
  67. W. F. Gattaz, K. D. Valente, N. R. B. Raposo, S. Vincentiis, and L. L. Talib, “Increased PLA2 activity in the hippocampus of patients with temporal lobe epilepsy and psychosis,” Journal of Psychiatric Research, vol. 45, no. 12, pp. 1617–1620, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Mershin, E. Pavlopoulos, O. Fitch, B. C. Braden, D. V. Nanopoulos, and E. M. C. Skoulakis, “Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons,” Learning and Memory, vol. 11, no. 3, pp. 277–287, 2004. View at Publisher · View at Google Scholar · View at Scopus
  69. L. Pennanen, D. P. Wolfer, R. M. Nitsch, and J. Götz, “Impaired spatial reference memory and increased exploratory behavior in P301L tau transgenic mice,” Genes, Brain and Behavior, vol. 5, no. 5, pp. 369–379, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Priel, J. A. Tuszynski, and N. J. Woolf, “Neural cytoskeleton capabilities for learning and memory,” Journal of Biological Physics, vol. 36, no. 1, pp. 3–21, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. E. C. Lauterbach, “Psychotropic drug effects on gene transcriptomics relevant to Parkinson's disease,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 38, pp. 107–115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  72. E. C. Lauterbach, “Psychotropic drug effects on gene transcriptomics relevant to Alzheimer disease,” Alzheimer Disease and Associated Disorders, vol. 26, no. 1, pp. 1–7, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. R. Gittins and P. J. Harrison, “Neuronal density, size and shape in the human anterior cingulate cortex: a comparison of Nissl and NeuN staining,” Brain Research Bulletin, vol. 63, no. 2, pp. 155–160, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. A. D. Stan, S. Ghose, X.-M. Gao et al., “Human postmortem tissue: what quality markers matter?” Brain Research, vol. 1123, no. 1, pp. 1–11, 2006. View at Publisher · View at Google Scholar · View at Scopus