Secretions from placenta, after hypoxia/reoxygenation, can damage developing neurones of brain under experimental conditions

Experimental Neurology

Volumn 261, Issue , 2014, Pages 386-395

  Curtis, Daniel J ^a   Sood, Aman ^a   Phillips, Tom J ^a   Nishiguchi, Akihiro ^b   Leinster, Veron ^a   Coyle, Christopher ^a   Lacharme Lora, Lizeth ^a   Beaumont, Oliver ^a   Kemp, Helena ^c   Goodall, Roberta ^c   Cornes, Leila ^c   Giugliano, Michele ^d   Barone, Rocco A ^d   Matsusaki, Michiya ^b   Akashi, Mitsuru ^b   Tanaka, Hiroyoshi Y ^e   Kano, Mitsunobu ^e   McGarvey, Jennifer ^a   Halemani, Nagaraj D ^a   Simon, Katja ^f   Keehan, Robert ^a   Ind, William ^a   Masters, Tracey ^c   Grant, Simon ^c   Athwal, Sharan ^c   Collett, Gavin ^g   Tannetta, Dionne ^g   Sargent, Ian L ^g   Scull Brown, Emma ^a   Liu, Xun ^a   Aquilina, Kristian ^h   Cohen, Nicki ^a   Lane, Jon D ^a   Thoresen, Marianne ^a   Hanley, Jon ^a   Randall, Andrew ^a   Case, C Patrick ^a   more..

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

^c SOUTHMEAD HOSPITAL   (United Kingdom)

^d UNIVERSITY OF ANTWERP   (Belgium)

^e UNIVERSITY OF TOKYO   (Japan)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h FRENCHAY HOSPITAL   (United Kingdom)

Author keywords

Cerebral cortex; Dendrite; Development; Hypoxia; Neurodevelopmental disorder; Neurone; Parvalbumin; Placenta; Reoxygenation; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM; GLUTAMATE RECEPTOR; GLUTAMIC ACID; PARVALBUMIN; REACTIVE OXYGEN METABOLITE; CALCIUM ION; FREE RADICAL; CULTURE MEDIUM; GLIAL FIBRILLARY ACIDIC PROTEIN; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL DENSITY; CONTROLLED STUDY; CYTOTROPHOBLAST; DENDRITIC SPINE; EMBRYO; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; MALE; MITOCHONDRION; NEWBORN; NONHUMAN; PLACENTA; PRIORITY JOURNAL; RAT; REOXYGENATION; SYNAPSE; THALAMUS RETICULAR NUCLEUS; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CELL ASSAY; CELL MATURATION; CELL SIZE; CELLULAR DISTRIBUTION; CELLULAR SECRETION; CHEMICAL COMPOSITION; DENDRITIC CELL; EMBRYO CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; NERVE CELL LESION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ADVERSE EFFECTS; ANIMAL; ANIMAL EMBRYO; ANOXIA; BRAIN; CELL CULTURE; CELL HYPOXIA; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; DENDRITE; DOSE RESPONSE; DRUG EFFECTS; FETUS; GROWTH, DEVELOPMENT AND AGING; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; TISSUE CULTURE TECHNIQUE; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; BRAIN; CELL HYPOXIA; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA, CONDITIONED; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; FEMALE; FETUS; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; MEMBRANE POTENTIALS; NEURONS; OXYGEN; PLACENTA; PREGNANCY; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; TISSUE CULTURE TECHNIQUES;

EID: 84905457846     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.05.003     Document Type: Article

References (57)

1. Abekawa T., Ito K., Nakato Y., Koyama T. Developmental GABAergic deficit enhances methamphetamine-induced apoptosis. Psychopharmacology (Berl) 2011, 215:413-427.
2. Aquilina K., Chakkarapani E., Love S., Thoresen M. Neonatal rat model of intraventricular haemorrhage and post-haemorrhagic ventricular dilatation with long-term survival into adulthood. Neuropathol. Appl. Neurobiol. 2011, 37:156-165.
3. Baburamani A.A., Ek C.J., Walker D.W., Castillo-Melendez M. Vulnerability of the developing brain to hypoxic-ischemic damage: contribution of the cerebral vasculature to injury and repair?. Front. Physiol. 2012, 3:424.
4. Barker D.J. The developmental origins of adult disease. J. Am. Coll. Nutr. 2004, 23:588S-595S.
5. Beas-Zárate C., Perez-Vega M.I., Gonzalez-Burgos I. Neonatal exposure to monosodium L-glutamate induces cell death and cytoarchitectural impairments in hippocampal CA1 pyramidal neurons of adult rats. Brain Res. 2002, 952:275-281.
6. Bhabra G., Sood A., Fisher B., Cartwright L., Saunders M., Evans W.H., Surprenant A., Lopez-Castejon G., Mann S., Davis S.A., Hails L.A., Ingham E., Verkade P., Lane J., Heesom K., Newson R., Case C.P. Nanoparticles can cause DNA damage across a cellular barrier. Nat. Nanotechnol. 2009, 4:876-883.
7. Bonnin A., Goeden N., Chen K., Wilson M.L., King J., Shih J.C., Blakely R.D., Deneris E.S., Levitt P. A transient placental source of serotonin for the fetal forebrain. Nature 2011, 472:347-350.
8. Bosco C., Diaz E. Placental hypoxia and foetal development versus alcohol exposure in pregnancy. Alcohol Alcohol. 2012, 47:109-117.
9. Cetin I., de Santis M.S., Taricco E., Radaelli T., Teng C., Ronzoni S., Spada E., Milani S., Pardi G. Maternal and fetal amino acid concentrations in normal pregnancies and in pregnancies with gestational diabetes mellitus. Am. J. Obstet. Gynecol. 2005, 192:610-617.
10. Chen X., Threlkeld S.W., Cummings E.E., Juan I., Makeyev O., Besio W.G., Gaitanis J., Banks W.A., Sadowska G.B., Stonestreet B.S. Ischemia-reperfusion impairs blood-brain barrier function and alters tight junction protein expression in the ovine fetus. Neuroscience 2012, 226:89-100.
11. Chicha L., Smith T., Guzman R. Stem cells for brain repair in neonatal hypoxia-ischemia. Childs Nerv. Syst. 2014, 30:37-46.
12. Class Q.A., Abel K.M., Khashan A.S., Rickert M.E., Dalman C., Larsson H., Hultman C.M., Långström N., Lichtenstein P., D'Onofrio B.M. Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychol. Med. 2013, 17:1-14.
13. Coyle J.T. NMDA receptor and schizophrenia: a brief history. Schizophr. Bull. 2012, 38:920-926.
14. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
15. Engidawork E., Chen Y., Dell'Anna E., Goiny M., Lubec G., Ungerstedt U., Andersson K., Herrera-Marschitz M. Effect of perinatal asphyxia on systemic and intracerebral pH and glycolysis metabolism in the rat. Exp. Neurol. 1997, 145:390-396.
16. Fanos V., Antonucci R., Barberini L., Noto A., Atzori L. Clinical application of metabolomics in neonatology. J. Matern. Fetal Neonatal Med. 2012, 25(Suppl. 1):104-109.
17. Fatemi S.H., Folsom T.D. The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr. Bull. 2009, 35:528-548.
18. Fryer S.L., McGee C.L., Matt G.E., Riley E.P., Mattson S.N. Evaluation of psychopathological conditions in children with heavy prenatal alcohol exposure. Pediatrics 2007, 119:e733-e741.
19. Gerstein M., Huleihel M., Mane R., Stilman M., Kashtuzki I., Hallak M., Golan H. Remodeling of hippocampal GABAergic system in adult offspring after maternal hypoxia and magnesium sulfate load: immunohistochemical study. Exp. Neurol. 2005, 196:18-29.
20. Gorman J.M., Docherty J.P. A hypothesized role for dendritic remodeling in the etiology of mood and anxiety disorders. J. Neuropsychiatry Clin. Neurosci. 2010, 22:256-264.
21. Gray E., Ginty M., Kemp K., Scolding N., Wilkins A. Peroxisome proliferator-activatedreceptor-α agonists protect cortical neurons from inflammatory mediators and improve peroxisomal function. Eur. J. Neurosci. 2011, 33:1421-1432.
22. Hsiao E.Y., Patterson P.H. Placental regulation of maternal-fetal interactions and brain development. Dev. Neurobiol. 2012, 72:1317-1326.
23. Hung T.H., Charnock-Jones D.S., Skepper J.N., Burton G.J. Secretion of tumor necrosis factor-alpha from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation invitro: a potential mediator of the inflammatory response in preeclampsia. Am. J. Pathol. 2004, 164:1049-1061.
24. Jia N., Yang K., Sun Q., Cai Q., Li H., Cheng D., Fan X., Zhu Z. Prenatal stress causes dendritic atrophy of pyramidal neurons in hippocampal CA3 region by glutamate in offspring rats. Dev. Neurobiol. 2010, 70:114-125.
25. Karl P.I., Kwun R., Slonim A., Fisher S.E. Ethanol elevates fetal serum glutamate levels in the rat. Alcohol. Clin. Exp. Res. 1995, 19:177-181.
26. Li H.P., Chen X., Li M.Q. Gestational diabetes induces chronic hypoxia stress and excessive inflammatory response in murine placenta. Int. J. Clin. Exp. Pathol. 2013, 6:650-659.
27. 1 and A(2A) receptors in rat brain from mothers and neonates. Neuroscience 2011, 199:133-142.
28. Malarkey E.B., Parpura V. Mechanisms of glutamate release from astrocytes. Neurochem. Int. 2008, 52:142-154.
29. McKay R. Developmental biology: remarkable role for the placenta. Nature 2011, 472:298-299.
30. Metzger F. Molecular and cellular control of dendrite maturation during brain development. Curr. Mol. Pharmacol. 2010, 3:1-11.
31. Mikaelsson M.A., Constância M., Dent C.L., Wilkinson L.S., Humby T. Placental programming of anxiety in adulthood revealed by Igf2-null models. Nat. Commun. 2013, 4:2311.
32. Moores R.R., Vaughn P.R., Battaglia F.C., Fennessey P.V., Wilkening R.B., Meschia G. Glutamate metabolism in fetus and placenta of late-gestation sheep. Am. J. Physiol. 1994, 267:R89-R96.
33. Morrison G., Fraser D.D., Cepinskas G. Mechanisms and consequences of acquired brain injury during development. Pathophysiology 2012, 2013(20):49-57.
34. Nakamura Y., Wood C.L., Patton A.P., Jaafari N., Henley J.M., Mellor J.R., Hanley J.G. PICK1 inhibition of the Arp2/3 complex controls dendritic spine size and synaptic plasticity. EMBO J. 2011, 30:719-730.
35. Nishiguchi A., Yoshida H., Matsusaki M., Akashi M. Rapid construction of three-dimensional multilayered tissues with endothelial tube networks by the cell-accumulation technique. Adv. Mater. 2011, 23:3506-3510.
36. Noorlander C.W., de Graan P.N., Nikkels P.G., Schrama L.H., Visser G.H. Distribution of glutamate transporters in the human placenta. Placenta 2004, 25:489-495.
37. Olvera-Cortés E., López-Vázquez M.A., Beas-Zárate C., González-Burgos I. Neonatal exposure to monosodium glutamate disrupts place learning ability in adult rats. Pharmacol. Biochem. Behav. 2005, 82:247-251.
38. Potter S., DeMarse T. A new approach to neural cell culture for long-term studies. J. Neurosci. Methods 2001, 110:17-24.
39. Rapoport J.L., Giedd J.N., Gogtay N. Neurodevelopmental model of schizophrenia: update 2012. Mol. Psychiatry 2012, 17:1228-1238.
40. Rees S., Harding R., Walker D. The biological basis of injury and neuroprotection in the fetal and neonatal brain. Int. J. Dev. Neurosci. 2011, 29:551-563.
41. Samudio-Ruiz S.L., Allan A.M., Sheema S., Caldwell K.K. Hippocampal N-methyl-D-aspartate receptor subunit expression profiles in a mouse model of prenatal alcohol exposure. Alcohol. Clin. Exp. Res. 2010, 34:342-353.
42. Sandman C.A., Wadhwa P.D., Dunkel-Schetter C., Chicz-DeMet A., Belman J., Porto M., Murata Y., Garite T.J., Crinella F.M. Psychobiological influences of stress and HPA regulation on the human fetus and infant birth outcomes. Ann. N. Y. Acad. Sci. 1994, 739:198-210.
43. Solbach S., Celio M.R. Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat. Embryol. 1991, 184:103-124.
44. Sood A., et al. Signalling of DNA damage and cytokines across cell barriers exposed to nanoparticles depends on barrier thickness. Nat. Nanotechnol. 2011, 6:824-833.
45. Stanek J. Hypoxic patterns of placental injury: a review. Arch. Pathol. Lab. Med. 2013, 137:706-720.
46. Stolp H., Neuhaus A., Sundramoorthi R., Molnár Z. The long and the short of it: gene and environment interactions during early cortical development and consequences for long-term neurological disease. Front. Psychiatry 2012, 3:50.
47. Takai H., Katayama K., Yasoshima A., Uetsuka K., Nakayama H., Doi K. NMDA-induced apoptosis in the developing rat brain. Exp. Toxicol. Pathol. 2003, 55:33-37.
48. Takasaki Y. Studies on brain lesions after administration of monosodium L-glutamate to mice. II. Absence of brain damage following administration of monosodium L-glutamate in the diet. Toxicology 1978, 9:307-318.
49. Tanemura K., Igarashi K., Matsugami T.R., Aisaki K., Kitajima S., Kanno J. J. Toxicol. Sci. 2009, 34(Suppl. 2):SP279-SP286.
50. Tannetta D.S., Sargent I.L., Linton E.A., Redman C.W. Vitamins C and E inhibit apoptosis of cultured human term placenta trophoblast. Placenta 2008, 29:680-690.
51. Tucker A.M., Aquilina K., Chakkarapani E., Hobbs C.E., Thoresen M. Development of amplitude-integrated electroencephalography and interburst interval in the rat. Pediatr. Res. 2009, 65:62-66.
52. Van Lieshout R.J., Voruganti L.P. Diabetes mellitus during pregnancy and increased risk of schizophrenia in offspring: a review of the evidence and putative mechanisms. J. Psychiatry Neurosci. 2008, 33:395-404.
53. Van Pelt J., Wolters P., Corner M., Rutten W., Ramarkers G. Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE Trans. Biomed. Eng. 2004, 51:2051-2062.
54. Wallace G.H., Arellano J.M., Gruner T.M. Non-syndromic cleft lip and palate: could stress be a causal factor?. Women Birth 2011, 24:40-46.
55. Yu T.X., Zhao Y., Shi W.C., Ma R.D., Yu L.J. Effects of maternal oral administration of monosodium glutamate at a late stage of pregnancy on developing mouse fetal brain. Brain Res. 1997, 747:195-206.
56. Yu L., Zhang Y., Ma R., Bao L., Fang J., Yu T. Potent protection of ferulic acid against excitotoxic effects of maternal intragastric administration of monosodium glutamate at a late stage of pregnancy on developing mouse fetal brain. Eur. Neuropsychopharmacol. 2006, 16:170-177.
57. Zhang Y., Zou S., Zhang X., Zhang Y. Correlation of domestic violence during pregnancy with plasma amino-acid neurotransmitter, cortisol levels and catechol-o-methyltransferase Val(158)Met polymorphism in neonates. Asia Pac Psychiatry 2013, 5:2-10.