Maternal dietary loads of alpha-tocopherol increase synapse density and glial synaptic coverage in the hippocampus of adult offspring

European Journal of Histochemistry

Volumn 58, Issue 2, 2014, Pages 120-126

  Salucci, S ^a   Ambrogini, P ^a   Lattanzi, D ^a   Betti, M ^a   Gobbi, P ^a   Galati, C ^a   Galli, F ^b   Cuppini, R ^a   Minelli, Andrea ^a  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Axo spinous synapses; CA1 stratum radiatum; Electron microscopy; Glia synapse relationship; Morphometry; Tripartite synapses; Vitamin E

Indexed keywords

EID: 84899727422     PISSN: 1121760X     EISSN: None     Source Type: Journal    
DOI: 10.4081/ejh.2014.2355     Document Type: Article

References (77)

1. Azzi A. Molecular mechanisms of α-tocopherol action. Free Radic Biol Med 2007;43:16-21.
2. Azzi A, Gysin R, Kempná P, Munteanu A, Negis Y, Villacorta L, et al. Vitamin E mediates cell signaling and regulation of gene expression. Ann NY Acad Sci 2004;1031: 86-95.
3. Rimbach G, Fisher A, Stoecklin E, Barella L. Modulation of hepatic gene expression by alpha tocopherol in cultured cells and in vivo. Ann NY Acad Sci 2004;1031:102-108.
4. Galli F, Azzi, A. Present trends in vitamin E research. Biofactors 2010;36:33-42.
5. Brigelius-Flohe R, Kelly FJ, Salonen JT, Neuzil J, Zingg JM, Azzi A. The European perspective on Vitamin E: current knowledge and future research. Am J Clin Nutr 2002;76:703-716.
6. Betti M, Minelli A, Canonico B, Castaldo P, Magi S, Aisa MC, et al. Antiproliferative effects of tocopherols (vitamin E) on murine glioma C6 cells: homologue-specific control of PKC/ERK and cyclin signaling. Free Radic Biol Med 2006;41:464-72.
7. Varga Z, Kosaras E, Komodi E, Katko M, Karpati I, Balla J, et al. Effects of tocopherols and 2,2'-carboxyethyl hydroxychromans on phorbol-ester-stimulated neutrophils. J Nutr Biochem 2008;19:320-7.
8. Betti M, Ambrogini P, Minelli A, Floridi A, Lattanzi D, Ciuffoli S, et al. Maternal dietary loads of α-tocopherol depress protein kinase C signaling and synaptic plasticity in rat postnatal developing hippocampus and promote permanent deficits in adult offspring. J Nutr Biochem 2011;22: 60-70.
9. Ferri P, Cecchini T, Ambrogini P, Betti M, Cuppini R, Del Grande P, et al. α-tocopherol affects neuronal plasticity in adult rat dentate gyrus: the possible role of PKCα. J Neurobiol 2006;66:793-810.
10. Eriksson UJ, Borg LA. Diabetes and embryonic malformations: role of substrateinduced free-oxygen radical production for dysmorphogenesis in cultured rat embryos. Diabetes 1993;42:411-9.
11. Mikhail MS, Anyaegbunam A, Garfinkel D, Palan PR, Basu J, Romney SL. Preeclampsia and antioxidant nutrients: decreased plasma levels of reduced ascorbic acid,α-tocopherol and beta-carotene in women with preeclampsia. Am J Obst Gynecol 1994;171:150-7.
12. Von Mandach U, Huch R, Huch A. Maternal and cord serum vitamin E levels in normal and abnormal pregnancy. Int J Vitam Nutr 1993;63:26-32.
13. Gupta S, Aziz N, Sekhon L, Agarwal R, Mansour G, Li J. Lipid peroxidation and antioxidant status in preeclampsia: a systematic review. Obst Gynecol Surv 2009;64:750-9.
14. Gallo C, Renzi P, Loizzo A, Piacente S, Festa M, Caputo M, et al. Potential therapeutic effects of vitamin E and C on placental oxidative stress induced by nicotine: an in vitro evidence. Open Biochem 2010;4:77-82
15. Rumbold AR, Crowther CA. Vitamin E supplementation in pregnancy. Cochrane database Syst Rev 2005;18:CD004069.
16. Poston L, Briley AL, Seed PT, Kelly FJ, Shennan AH. Vitamins in Pre-eclampsia (VIP) Trial Consortium Vitamin C and Vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomized placebo-controlled trial. Lancet 2006;367: 1145-54.
17. Polyzos NP, Mauri D, Tsappi M, Tzioras S, Kamposioras K, Cortinovis I. Combined Vitamin C and E supplementation during pregnancy for pre-eclampsia prevention: a systematic review. Obst Gynecol Surv 2007;62:202-6.
18. Rumbold AR, Duley L, Crowther CA, Hasiam RR. Antioxidants for preventing pre-eclampsia. Cochrane Database Syst Rev 2008;23:CD004227.
19. Kano M, Hashimoto K, Chen C, Abeliovich A, Alba A, Kurihara H, et al. Impaired synapse elimination during cerebellar development in PKCα mutant mice. Cell 1995;83:1223-31.
20. Hama H, Hara H, Yamaguchi K, Miyawaki A. PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 2004;41:405-15.
21. Kapfhammer JP. Cellular and molecular control of dendritic growth and development of cerebellar Purkinje cells. Prog Histochem Cytochem 2004;39:131-82.
22. Shahak H, Slotkin TA, Yanai J. Alterations in PKCgamma in the mouse hippocampus after prenatal exposure to heroin: a link from cell signaling to behavioral outcome. Brain Res Dev Brain Res 2003;140:117-25.
23. Xu SZ, Bullock L, Shan CJ, Cornelius K, Rajanna B. PKC isoforms were reduced by lead in the developing rat brain. Int J Dev Neurosci 2005;23:53-64.
24. Paulraj R, Behari J. Protein kinase C activity in the developing rat brain cells exposed to 2.45 GHz radiation. Electromagn Biol Med 2006;25:61-70.
25. Yanai J, Brick-Turin Y, Dotan S, Langford R, Pinkas A, Slotkin TA. A mechanism-based complementary screening approach for the amelioration and reversal of neurobehavioral teratogenicity. Neurotoxicol Teratol 2010;32:109-13.
26. Ambrogini P, Ciuffoli S, Lattanzi D, Minelli A, Bucherelli C, Baldi E, et al. Maternal dietary loads of α-tocopherol differentially influence fear conditioning and spatial learning in adult offspring. Physiol Beha 2011;104:809-15.
27. DeFelipe J, Conti F, Van Eyck SL, Manzoni T. Demonstration of glutamate-positive axon terminals forming asymmetric synapses in cat neocortex. Brain Res 1988;455:162-5.
28. Jarrard LE. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 1993;60:9-26.
29. Mizuno K, Giese KP. Hippocampusdependent memory formation: do memory type-specific mechanisms exist? J Pharmacol Sci 2005;98:191-7.
30. Minelli A, Castaldo P, Gobbi P, Salucci S, Magi S, Amoroso S. Cellular and subcellular localization of Na+-Ca2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium 2007;41:221-34.
31. Gobbi P, Castaldo P, Minelli A, Salucci S, Magi S, Corcione E, et al. Mitochondrial localization of Na+/Ca2+ exchangers NCX1-3 in neurons and astrocytes of adult rat brain in situ. Pharmacol Res 2007;56: 556-65.
32. Peters A, Palay SL, Webster HdeF. The fine structure of the nervous system. Neurons and their supporting cells, 3th ed. New York: Oxford University Press, 1991.
33. Yoneyama M, Kawada K, Gotoh Y, Shiba T, Ogita K. Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells. Neurochem Int 2010;56:740-6.
34. Tsatmali M, Walcott EC, Makarenkova H, Crossin KL. Reactive oxygen species modulate the differentiation of neurons in clonal cortical cultures. Mol Cell Neurosci 2006;33:345-57.
35. Coyoy A, Olguin-Albuerne M, Martinez- Briseno P, Moran J. Role of reactive oxygen species and NADPH-oxidase in the development of rat cerebellum. Neurochem Int 2013;62:998-1011.
36. Munno DW, Syed NI. Synaptogenesis in the CNS: an odyssey from wiring together to firing together. J Physiol 2003;552:1-11.
37. Hua JY, Smith SJ. Neural activity and the dynamics of central nervous system development. Nat Neurosci 2004;7:327-32.
38. Chklovskii DB, Mel BW, Svoboda K. Cortical rewiring and information storage. Nature 2004;431:782-8.
39. De Roo M, Klauser P, Garcia PM, Poglia L, Muller D. Spine dynamics and synapse remodeling during LTP and memory processes. Prog Brain Res 2008;169:199-207.
40. Harris KM, Jensen FE, Tsao B. Threedimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 1992;12:2685-705.
41. Eastwood SL, Weickert CS, Webster MJ, Herman MM, Kleinman JE, Harrison PJ. Synaptophysin protein and mRNA expression in the human hippocampal formation from birth to old age. Hippocampus 2006;16:645-54.
42. Pokorny J, Yamamoto T. Postnatal ontogenesis of hippocampal CA1 area in rats. II. Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull 1981;7:121-30.
43. Garner CC, Waites CL, Ziv NE. Synapse development: still looking for the forest, still lost in the trees. Cell Tissue Res 2006;326:249-62.
44. Chen C, Kano M, Abeliovich A, Chen L, Bao S, Kim JJ, et al. Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKCα mutant mice. Cell 1995;83:1233-42.
45. Paus T, Keshavan M, Giedd JN. Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 2008;9: 947-57.
46. Pikkarainen M, Rönkkö S, Savander V, Insausti R, Pitkänen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol 1999;403: 229-60.
47. McEwen BS. The ever-changing brain: cellular and molecular mechanisms for the effects of stressful experiences. Dev Neurobiol 2012;72:878-90.
48. Davidson RJ, McEwen BS. Social influences on neuroplasticity: stress and interventions to promote well-being. Nat Neurosci 2012;15:689-95.
49. Harris KM, Stevens JK. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 1989;9:2982-97.
50. Perea G, Navarrete M, Araque A. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 2009;32:421-31.
51. Mauch DH, Nägler K, Schumacher S, Göritz C, Müller EC, Otto A, et al. CNS synaptogenesis promoted by glia-derived cholesterol. Science 2001;294:1354-7.
52. Allen NJ, Barres B. Signaling between glia and neurons: focus on synaptic plasticity. Curr Opin Neurobiol 2005;15:542-8.
53. Pfrieger FW. Role of glial cells in the formation and maintenance of synapses. Brain Res Rev 2010;63:39-46.
54. Eroglu C, Barres B. Regulation of synaptic connectivity by glia. Nature 2010;468:223-54.
55. Boehler MD, Wheeler BC, Brewer GJ. Added astroglia promote greater synapse density and higher activity in neuronal networks. Neuron Glia Biol 2007;3:127-40.
56. Nishida H, Okabe S. Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 2007;27:331-40.
57. Perea G, Araque A. Glia modulates synaptic transmission. Brain Res Rev 2010;63:93-102.
58. Schipke CG, Kettenmann H. Astrocyte responses to neuronal activity. Glia 2004; 47:226-32.
59. Perea G, Araque A. Properties of synaptically- evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 2005;25:2192-203.
60. Volterra A, Steinhauser C. Glial modulation of synaptic transmission in the hippocampus. Glia 2004;47:249-57.
61. Kozlov AS, Angulo MC, Audinat E, Charpak S. Target cell-specific modulation of neuronal activity by astrocytes. Proc Natl Acad Sci USA 2006;103:10058-63.
62. Parpura V, Zorec R. Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 2010;63:83-92.
63. Diamond JS. Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development. J Neurosci 2005;25:2906-16.
64. Tsingounis AV, Wadiche JI. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 2007;8:935-47.
65. Gordon GR, Baimoukhametova DV, Hewitt SA, Rajapaksha WR, Fisher TE, Bains JS. Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 2005;8:1078-86.
66. Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, et al. Astrocytic purinergic signaling coordinated synaptic networks. Science 2005;310:113-6.
67. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, et al. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 2006;125:775-84.
68. Henneberger C, Papouin T, Oliet SH, Rusakov DA. Long-term potentiation depends on release of D-serine from astrocytes. Nature 2010;463:232-6.
69. Katagiri H, Tanaka K, Manabe T. Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 2001;14:547-53.
70. Filosa A, Paixao S, Honsek SD, Carmona MA, Becker L, Feddersen B, et al. Neuronglia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat Neurosci 2009;12:1285-92.
71. Tanaka M, Shih PY, Gomi H, Yoshida T, Nakai J, Ando R, et al. Astrocytic Ca2+ signals are required for the functional integrity of tripartite synapses. Molecular Brain 2013;6:6-18.
72. Verkhratsky A, Orkland RK, Kettenmann H. Glial calcium: homeostasis and signaling function. Physiol Rev 1998;78:99-141.
73. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, Taves SR, et al. What is the role of astrocyte calcium in neurophysiology? Neuron 2008;59:932-46.
74. Omrani A, Melone M, Bellesi M, Safiulina V, Aida T, Tanaka K, et al. Up-regulation of GLT-1 severely impairs LTD at mossy fibre- CA3 synapses. J Physiol 2009;587:4575-88.
75. Hruska M, Dalva MB. Ephrin regulation of synapse formation, function and plasticity. Mol Cell Neurosci 2012;50:35-44.
76. Carmona MA, Murai KK, Wang L, Roberts AJ, Pasquale EB. Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proc Natl Acad Sci USA 2009;106:12524-9.
77. Boskovic R, Gargaun L, Oren D, Djulus J, Koen G. Pregnancy outcome following high doses of vitamin E supplementation. Reprod Toxicol 2005;20:85-8.