Alterations of the microvascular network in the sclerotic hippocampus of patients with temporal lobe epilepsy

Epilepsy and Behavior

Volumn 38, Issue , 2014, Pages 48-52

  Alonso Nanclares, Lidia ^a,b,c   DeFelipe, Javier ^a,b,c  

^a INSTITUTO CAJAL   (Spain)

^b TECHNICAL UNIVERSITY OF MADRID   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Angiogenesis; Blood vessels; Blood brain barrier; Electron microscopy; Vascular pathology

Indexed keywords

ANGIOGENESIS; BLOOD BRAIN BARRIER; BLOOD VESSEL; DISEASE ASSOCIATION; HIPPOCAMPAL SCLEROSIS; HISTOPATHOLOGY; HUMAN; MICROVASCULATURE; REVIEW; TEMPORAL LOBE EPILEPSY; HIPPOCAMPUS; PATHOLOGY;

EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; HUMANS; MICROVESSELS;

EID: 84910646863     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2013.12.009     Document Type: Review

References (58)

1. Meldrum B.S., Bruton C.J. Epilepsy. Greenfield's Neuropathology 1992, 1246-1283. Arnold, London. 5th ed. J. Adams, L.W. Duchen (Eds.).
2. Honavar M., Meldrum B.S. Epilepsy. Greenfield's Neuropathology 1997, 931-971. Arnold, London. 6th ed. D.I. Graham, P.L. Lantos (Eds.).
3. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res 1990, 535:195-204.
4. de Lanerolle N.C., Kim J.H., Robbins R.J., Spencer D.D. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 1989, 495:387-395.
5. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989, 26:321-330.
6. Babb T.L., Kupfer W.R., Pretorius J.K., Crandall P.H., Levesque M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 1991, 42:351-363.
7. Babb T.L., Ying Z., Mikuni N., Nishiyama K., Drazba J., Bingaman W., et al. Brain plasticity and cellular mechanisms of epileptogenesis in human and experimental cortical dysplasia. Epilepsia 2000, 41(Suppl. 6):S76-S81.
8. Sloviter R.S. Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1991, 1:41-66.
9. Muñoz A., Arellano J.I., DeFelipe J. GABABR1 receptor protein expression in human mesial temporal cortex: changes in temporal lobe epilepsy. J Comp Neurol 2002, 449:166-179.
10. Muñoz A., Mendez P., DeFelipe J., Alvarez-Leefmans F.J. Cation-chloride cotransporters and GABA-ergic innervation in the human epileptic hippocampus. Epilepsia 2007, 48:663-673.
11. Wittner L., Eross L., Szabo Z., Toth S., Czirjak S., Halasz P., et al. Synaptic reorganization of calbindin-positive neurons in the human hippocampal CA1 region in temporal lobe epilepsy. Neuroscience 2002, 115:961-978.
12. Arellano J.I., Ballesteros-Yanez I., DeFelipe J., Munoz A., Sola R.G. Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain 2004, 127:45-64.
13. Sommer W. Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch Psychiatr Nervenkr 1880, 308:631-675.
14. Bratz E. Ammonshorn befunde bei Epileptikern. Arch Psychiatr Nervenkr 1899, 31:820-835.
15. Eid T., Brines M.L., Cerami A., Spencer D.D., Kim J.H., Schweitzer J.S., et al. Increased expression of erythropoietin receptor on blood vessels in the human epileptogenic hippocampus with sclerosis. J Neuropathol Exp Neurol 2004, 63:73-83.
16. Eid T., Lee T.S., Thomas M.J., Miry-Moghaddam M., Bjornsen L.P., Spencer D.D., et al. Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci U S A 2005, 102:1193-1198.
17. Seiffert E., Dreier J.P., Ivens S., Bechmann I., Tomkins O., Heinemann U., et al. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 2004, 24:7829-7836.
18. Pavlovsky L., Seiffert E., Heinemann U., Korn A., Golan H., Friedman A. Persistent BBB disruption may underlie alpha interferon-induced seizures. J Neurol 2005, 252:42-46.
19. Tomkins O., Shelef I., Kaizerman I., Misk A., Afawi Z., Eliushin A., et al. Blood-brain barrier disruption in post-traumatic epilepsy. J Neurol Neurosurg Psychiatry 2008, 79:774-777.
20. Van Vliet E.A., da Costa S., Redeker S., van Schaik R., Aronica E., Gorter J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007, 130:521-534.
21. Uva L., Librizzi L., Marchi N., Noe F., Bongiovanni R., Vezzani A., et al. Acute induction of epileptiform discharges by pilocarpine in the in vitro isolated guinea-pig brain requires enhancement of blood-brain barrier permeability. Neuroscience 2008, 151:303-312.
22. Oby E., Janigro D. The blood-brain barrier and epilepsy. Epilepsia 2006, 47:1761-1774.
23. Ravizza T., Noe F., Zardoni D., Vaghi V., Sifringer M., Vezzani A. Interleukin converting enzyme inhibition impairs kindling epileptogenesis in rats by blocking astrocytic IL-1beta production. Neurobiol Dis 2008, 31:327-333.
24. Lo E.H., Dalkara T., Moskowitz M.A. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003, 4:399-415.
25. Rigau V., Morin M., Rousset M.C., de BF, Lebrun A., Coubes P., et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007, 130:1942-1956.
26. Morin-Brureau M., Lebrun A., Rousset M.C., Fagni L., Bockaert J., de Bock F., et al. Epileptiform activity induces vascular remodeling and zonula occludens 1 downregulation in organotypic hippocampal cultures: role of VEGF signaling pathways. J Neurosci 2011, 31:10677-10688.
27. Morin-Brureau M., Rigau V., Lerner-Natoli M. Why and how to target angiogenesis in focal epilepsies. Epilepsia 2012, 53(Suppl. 6):64-68.
28. Pitkanen A., Lukasiuk K. Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epilepsy Behav 2009, 14(Suppl. 1):16-25.
29. Hunsberger J.G., Bennett A.H., Selvanayagam E., Duman R.S., Newton S.S. Gene profiling the response to kainic acid induced seizures. Mol Brain Res 2005, 141:95-112.
30. Kastanauskaite A., Alonso-Nanclares L., Blazquez-Llorca L., Pastor J., Sola R.G., DeFelipe J. Alterations of the microvascular network in sclerotic hippocampi from patients with epilepsy. J Neuropathol Exp Neurol 2009, 68:939-950.
31. Lerner-Natoli M., de Bock F., Bockaert J., Rondouin G. NADPH diaphorase-positive cells in the brain after status epilepticus. Neuroreport 1994, 5:2633-2637.
32. Brown W.R., Thore C.R. Review: cerebral microvascular pathology in ageing and neurodegeneration. Neuropathol Appl Neurobiol 2011, 37:56-74.
33. Bell M.A., Scarrow W.G. Staining for microvascular alkaline phosphatase in thick celloidin sections of nervous tissue: morphometric and pathological applications. Microvasc Res 1984, 27:189-203.
34. Bell M.A., Ball M.J. Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 1985, 335:139-143.
35. Brown W.R., Moody D.M., Thore C.R., Challa V.R., Anstrom J.A. Vascular dementia in leukoaraiosis may be a consequence of capillary loss not only in the lesions, but in normal-appearing white matter and cortex as well. J Neurol Sci 2007, 257:62-66.
36. Thore C.R., Anstrom J.A., Moody D.M., Challa V.R., Marion M.C., Brown W.R. Morphometric analysis of arteriolar tortuosity in human cerebral white matter of preterm, young, and aged subjects. J Neuropathol Exp Neurol 2007, 66:337-345.
37. Erakovic V., Zupan G., Varljen J., Laginja J., Simonic A. Altered activities of rat brain metabolic enzymes in electroconvulsive shock-induced seizures. Epilepsia 2001, 42:181-189.
38. Whyte M.P., Mahuren J.D., Fedde K.N., Cole F.S., McCabe E.R., Coburn S.P. Perinatal hypophosphatasia: tissue levels of vitamin B6 are unremarkable despite markedly increased circulating concentrations of pyridoxal-5'-phosphate. Evidence for an ectoenzyme role for tissue-nonspecific alkaline phosphatase. J Clin Invest 1988, 81:1234-1239.
39. Waymire K.G., Mahuren J.D., Jaje J.M., Guilarte T.R., Coburn S.P., MacGregor G.R. Mice lacking tissue non-specific alkaline phosphatase die from seizures due to defective metabolism of vitamin B-6. Nat Genet 1995, 11:45-51.
40. Narisawa S., Froehlander N., Millan J.L. Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn 1997, 208:432-446.
41. Narisawa S., Wennberg C., Luis Millan J. Abnormal vitamin B 6 metabolism in alkaline phosphatase knock-out mice causes multiple abnormalities, but not the impaired bone mineralization. J Pathol 2001, 193:125-133.
42. Nunes M.L., Mugnol F., Bica I., Fiori R.M. Pyridoxine-dependent seizures associated with hypophosphatasia in a newborn. J Child Neurol 2002, 17:222-224.
43. Calhau C., Hipolito-Reis C., Azevedo I. Alkaline phosphatase and exchange surfaces. Clin Biochem 1999, 32:153-154.
44. Fonta C., Negyessy L., Renaud L., Barone P. Areal and subcellular localization of the ubiquitous alkaline phosphatase in the primate cerebral cortex: evidence for a role in neurotransmission. Cereb Cortex 2004, 14:595-609.
45. Avoli M. Is epilepsy a disorder of inhibition or excitation?. Prog Clin Biol Res 1983, 124:23-37.
46. Prince D.A., Jacobs K.M., Salin P.A., Hoffman S., Parada I. Chronic focal neocortical epileptogenesis: does disinhibition play a role?. Can J Physiol Pharmacol 1997, 75:500-507.
47. DeFelipe J. Chandelier cells and epilepsy. Brain 1999, 122(Pt 10):1807-1822.
48. Cullen K.M., Kocsi Z., Stone J. Microvascular pathology in the aging human brain: evidence that senile plaques are sites of microhaemorrhages. Neurobiol Aging 2006, 27:1786-1796.
49. del Zoppo G.J., Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 2003, 23:879-894.
50. Sanes J.R., Engvall E., Butkowski R., Hunter D.D. Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J Cell Biol 1990, 111:1685-1699.
51. Hamann G.F., Schrock H., Burggraf D., Wunderlich N., Liebetrau M., Kuschinsky W. Microvascular Basal lamina damage after embolic stroke in the rat: relationship to cerebral blood flow. J Cereb Blood Flow Metab 2003, 23:1293-1297.
52. Caffo M., Germanò A., Caruso G., Meli F., Galatioto S., Sciacca M.P., et al. An immunohistochemical study of extracellular matrix proteins laminin, fibronectin and type IV collagen in paediatric glioblastoma multiforme. Acta Neurochir 2004, 146:1113-1118.
53. Uspenskaia O., Liebetrau M., Herms J., Danek A., Hamann G.F. Aging is associated with increased collagen type IV accumulation in the basal lamina of human cerebral microvessels. BMC Neurosci 2004, 5:37.
54. Buttner A., Kroehling C., Mall G., Penning R., Weis S. Alterations of the vascular basal lamina in the cerebral cortex in drug abuse: a combined morphometric and immunohistochemical investigation. Drug Alcohol Depend 2005, 79:63-70.
55. Andrioli A., Alonso-Nanclares L., Arellano J.I., DeFelipe J. Quantitative analysis of parvalbumin-immunoreactive cells in the human epileptic hippocampus. Neuroscience 2007, 149:131-143.
56. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 2004, 5:347-360.
57. Drake C.T., Iadecola C. The role of neuronal signaling in controlling cerebral blood flow. Brain Lang 2007, 102:141-152.
58. Iadecola C., Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci 2007, 10:1369-1376.