Correlation between clinical and histologic findings in the human neonatal hippocampus after perinatal asphyxia

Journal of Neuropathology and Experimental Neurology

Volumn 73, Issue 4, 2014, Pages 324-334

  Schiering, Irene A M ^a   De Haan, Timo R ^a   Niermeijer, Jikke Mien F ^a   Koelman, Johannes H ^b   Majoie, Charles B L M ^b   Reneman, Liesbeth ^b   Aronica, Eleonora ^b,c,d  

^a EMMA CHILDREN S HOSPITAL   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Asphyxia; Astrocytes; Epilepsy; Glutamate; Hippocampus; Inflammation; Neonate

Indexed keywords

AQUAPORIN 4; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3D; INTERLEUKIN 1BETA; METABOTROPIC RECEPTOR;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN DAMAGE; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; FEMALE; GLIA CELL; HIPPOCAMPUS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOHISTOCHEMISTRY; INFANTILE SPASM; MALE; NEWBORN; PERINATAL ASPHYXIA; PRIORITY JOURNAL;

AQUAPORIN 4; ASPHYXIA NEONATORUM; CASPASE 3; COHORT STUDIES; COMPLEMENT C1Q; ELECTROENCEPHALOGRAPHY; FEMALE; HIPPOCAMPUS; HLA-DR ANTIGENS; HUMANS; INFANT, NEWBORN; INTENSIVE CARE UNITS; INTERLEUKIN-1BETA; MAGNETIC RESONANCE IMAGING; MALE; NEUROGLIA; NEURONS; RECEPTORS, METABOTROPIC GLUTAMATE; SEIZURES;

EID: 84897415906     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0000000000000056     Document Type: Article

References (59)

1. Ferriero DM. Neonatal brain injury. N Engl J Med 2004;351:1985-95
2. Lawn JE, Kerber K, Enweronu-Laryea C, et al. 3.6 million neonatal deathsYwhat is progressing and what is not? Semin Perinatol 2010;34: 371-86
3. Glass HC, Hong KJ, Rogers EE, et al. Risk factors for epilepsy in children with neonatal encephalopathy. Pediatr Res 2011;70:535-40
4. Perez A, Ritter S, Brotschi B, et al. Long-Term neurodevelopmental outcome with hypoxic-ischemic encephalopathy. J Pediatr 2013;163:454-59
5. Glass HC, Glidden D, Jeremy RJ, et al. Clinical neonatal seizures are independently associated with outcome in infants at risk for hypoxicischemic brain injury. J Pediatr 2009;155:318-23
6. Holmes GL. The long-Term effects of neonatal seizures. Clin Perinatol 2009;36:901-14, vii-viii
7. Johnston MV, Trescher WH, Ishida A, et al. Neurobiology of hypoxicischemic injury in the developing brain. Pediatr Res 2001;49:735-41
8. Ferrari DC, Nesic O, Perez-Polo Jr. Perspectives on neonatal hypoxia/ ischemia-induced edema formation. Neurochem Res 2010;35:1957-65
9. Kleman NW, Sun D, Cengiz P. Mechanisms underlying neonatal hypoxia ischemia. Open Drug Discovery J 2010;2:129-37
10. Pin JP, Acher F. The metabotropic glutamate receptors: Structure, activation mechanism and pharmacology. Curr Drug Targets CNS Neurol Disord 2002;1:297-317
11. Mukherjee S, Manahan-Vaughan D. Role of metabotropic glutamate receptors in persistent forms of hippocampal plasticity and learning. Neuropharmacology 2013;66:65-81
12. Jantzie LL, Talos DM, Selip DB, et al. Developmental regulation of group I metabotropic glutamate receptors in the premature brain and their protective role in a rodent model of periventricular leukomalacia. Neuron Glia Biol 2010;6:277-88
13. Meng S, Qiao M, Lin L, et al. Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur J Neurosci 2004;19:2261-69
14. Badaut J, Ashwal S, Tone B, et al. Temporal and regional evolution of aquaporin-4 expression and magnetic resonance imaging in a rat pup model of neonatal stroke. Pediatr Res 2007;62:248-54
15. Ferrari DC, Nesic OB, Perez-Polo Jr. Oxygen resuscitation does not ameliorate neonatal hypoxia/ischemia-induced cerebral edema. J Neurosci Res 2010;88:2056-65
16. Hagberg H, Gilland E, Bona E, et al. Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxiaischemia in neonatal rats. Pediatr Res 1996;40:603-9
17. Hedtjarn M, Mallard C, Hagberg H. Inflammatory gene profiling in the developing mouse brain after hypoxia-ischemia. J Cereb Blood Flow Metab 2004;24:1333-51
18. Aronica E, Ravizza T, Zurolo E, et al. Astrocyte immune responses in epilepsy. Glia 2012;60:1258-68
19. Vezzani A, Aronica E, Mazarati A, et al. Epilepsy and brain inflammation. Exp Neurol 2013;244:11-21
20. Squier W, Cowan FM. The value of autopsy in determining the cause of failure to respond to resuscitation at birth. Semin Neonatol 2004;9: 331-45
21. Alderliesten T, Nikkels PG, Benders MJ, et al. Antemortem cranial MRI compared with postmortem histopathologic examination of the brain in term infants with neonatal encephalopathy following perinatal asphyxia. Arch Dis Child Fetal Neonatal Ed 2013;98:F304-9
22. Aronica E, Gorter JA, Jansen GH, et al. Expression and cell distribution of group I and group II metabotropic glutamate receptor subtypes in taylor-Type focal cortical dysplasia. Epilepsia 2003;44:785-95
23. Aronica E, Gorter JA, Redeker S, et al. Distribution, characterization and clinical significance of microglia in glioneuronal tumours from patients with chronic intractable epilepsy. Neuropathol Appl Neurobiol 2005;31: 280-91
24. Ravizza T, Boer K, Redeker S, et al. The IL-1 beta system in epilepsyassociated malformations of cortical development. Neurobiol Dis 2006; 24:128-43
25. Iyer A, Zurolo E, Spliet WGM, et al. Evaluation of the innate and adaptive immunity in type I and type II focal cortical dysplasias. Epilepsia 2010;51:1763-73
26. Toering ST, Boer K, de Groot M, et al. Expression patterns of synaptic vesicle protein 2A in focal cortical dysplasia and TSC-cortical tubers. Epilepsia 2009;50:1409-18
27. Iwasaki Y, Mimuro M, Yoshida M, et al. Enhanced aquaporin-4 immunoreactivity in sporadic Creutzfeldt-Jakob disease. Neuropathology 2007; 27:314-23
28. Aoki K, Uchihara T, Tsuchiya K, et al. Enhanced expression of aquaporin 4 in human brain with infarction. Acta Neuropathol 2003;106:121-24
29. Gomori E, Pal J, Abraham H, et al. Fetal development of membrane water channel proteins aquaporin-1 and aquaporin-4 in the human brain. Int J Dev Neurosci 2006;24:295-305
30. Talos DM, Follett PL, Folkerth RD, et al. Developmental regulation of alpha-Amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 2006;497:61-77
31. Yang P, Zhang J, Zhao L, et al. Developmental distribution pattern of metabotropic glutamate receptor 5 in prenatal human hippocampus. Neurosci Bull 2012;28:704-14
32. Cooper JM, Vargha-Khadem F, Gadian DG, et al. The effect of hippocampal damage in children on recalling the past and imagining new experiences. Neuropsychologia 2011;49:1843-50
33. Fleiss B, Coleman HA, Castillo-Melendez M, et al. Effects of birth asphyxia on neonatal hippocampal structure and function in the spiny mouse. Int J Dev Neurosci 2011;29:757-66
34. Rees S, Harding R, Walker D. The biological basis of injury and neuroprotection in the fetal and neonatal brain. Int J Dev Neurosci 2011; 29:551-63
35. Burtrum D, Silverstein FS. Hypoxic-ischemic brain injury stimulates glial fibrillary acidic protein mRNA and protein expression in neonatal rats. Exp Neurol 1994;126:112-18
36. Fellin T, Haydon PG. Do astrocytes contribute to excitation underlying seizures? Trends Mol Med 2005;11:530-33
37. Steinhauser C, Boison D. Epilepsy: Crucial role for astrocytes. Glia 2012; 60:1191
38. Aronica E, Gorter J. Gene expression profile in temporal lobe epilepsy. Neuroscientist 2007;13:1-9
39. Vezzani A, Auvin S, Ravizza T, et al. Glia-neuronal interactions in ictogenesis and epileptogenesis: Role of inflammatory mediators. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV, eds. Jasper's Basic Mechanisms of the Epilepsies, 4th ed. Bethesda, MD: National Center for Biotechnology Information, 2012
40. Holers VM. The complement system as a therapeutic target in autoimmunity. Clin Immunol 2003;107:140-51
41. Bonifati DM, Kishore U. Role of complement in neurodegeneration and neuroinflammation. Mol Immunol 2007;44:999-1010
42. Rus H, Cudrici C, David S, et al. The complement system in central nervous system diseases. Autoimmunity 2006;39:395-402
43. Cowell RM, Plane JM, Silverstein FS. Complement activation contributes to hypoxic-ischemic brain injury in neonatal rats. J Neurosci 2003; 23:9459-68
44. Aronica E, Boer K, van Vliet EA, et al. Complement activation in experimental and human temporal lobe epilepsy. Neurobiol Dis 2007;26: 497-511
45. van Laerhoven H, de Haan TR, Offringa M, et al. Prognostic tests in term neonates with hypoxic-ischemic encephalopathy: A systematic review. Pediatrics 2013;131:88-98
46. Nagelhus EA, Ottersen OP. Physiological roles of aquaporin-4 in brain. Physiol Rev 2013;93:1543-62
47. Tourdias T, Mori N, Dragonu I, et al. Differential aquaporin 4 expression during edema build-up and resolution phases of brain inflammation. J Neuroinflammation 2011;8:143
48. Illarionova NB, Gunnarson E, Li Y, et al. Functional and molecular interactions between aquaporins and Na,K-ATPase. Neuroscience 2010; 168:915-25
49. Binder DK, Nagelhus EA, Ottersen OP. Aquaporin-4 and epilepsy. Glia 2012;60:1203-14
50. van Vliet EA, da Costa Araújo S, Redeker S, et al. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007; 130:521-34
51. Rigau V, Morin M, Rousset MC, et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007; 130:1942-56
52. Seiffert E, Dreier JP, Ivens S, et al. Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 2004; 24:7829-36
53. Heinemann U, Kaufer D, Friedman A. Blood-brain barrier dysfunction, TGFbeta signaling, and astrocyte dysfunction in epilepsy. Glia 2012;60:1251-57
54. D'Antoni S, Berretta A, Bonaccorso CM, et al. Metabotropic glutamate receptors in glial cells. Neurochem Res 2008;33:2436-43
55. Durand D, Carniglia L, Caruso C, et al. mGlu3 receptor and astrocytes: Partners in neuroprotection. Neuropharmacology 2013;66:1-11
56. Aronica E, Gorter JA, Ijlst-Keizers H, et al. Expression and functional role of mGluR3 and mGluR5 in human astrocytes and glioma cells: Opposite regulation of glutamate transporter proteins. Eur J Neurosc 2003;17:2106-18
57. Catania MV, D'Antoni S, Bonaccorso CM, et al. Group I metabotropic glutamate receptors: A role in neurodevelopmental disorders? Mol Neurobiol 2007;35:298-307
58. Gegelashvili G, Dehnes Y, Danbolt NC, et al. The high-Affinity glutamate transporters GLT1, GLAST, and EAAT4 are regulated via different signalling mechanisms. Neurochem Int 2000;37:163-70
59. Ngomba RT, Santolini I, Salt TE, et al. Metabotropic glutamate receptors in the thalamocortical network: Strategic targets for the treatment of absence epilepsy. Epilepsia 2011;52:1211-22