Hippocampal neurogenesis and memory in adolescence following intrauterine growth restriction.
brain-derived neurotrophic factor
dendrites
dentate gyrus
fetal growth restriction
hippocampus
pattern separation
spatial memory
Journal
Hippocampus
ISSN: 1098-1063
Titre abrégé: Hippocampus
Pays: United States
ID NLM: 9108167
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
22
07
2020
revised:
18
10
2020
accepted:
15
11
2020
pubmed:
16
12
2020
medline:
25
2
2022
entrez:
15
12
2020
Statut:
ppublish
Résumé
Intrauterine growth restriction (IUGR) is associated with hippocampal alterations that can increase the risk of short-term memory impairments later in life. Despite the role of hippocampal neurogenesis in learning and memory, research into the long-lasting impact of IUGR on these processes is limited. We aimed to determine the effects of IUGR on neuronal proliferation, differentiation and morphology, and on memory function at adolescent equivalent age. At embryonic day (E) 18 (term ∼E22), placental insufficiency was induced in pregnant Wistar rats via bilateral uterine vessel ligation to generate IUGR offspring (n = 10); control offspring (n = 11) were generated via sham surgery. From postnatal day (P) 36-44, spontaneous location recognition (SLR), novel object location and recognition (NOL, NOR), and open field tests were performed. Brains were collected at P45 to assess neurogenesis (immunohistochemistry), dendritic morphology (Golgi staining), and brain-derived neurotrophic factor expression (BDNF; Western blot analysis). In IUGR versus control rats there was no difference in object preference in the NOL or NOR, the similar and dissimilar condition of the SLR task, or in locomotion and anxiety-like behavior in the open field. There was a significant increase in the linear density of immature neurons (DCX+) in the subgranular zone (SGZ) of the dentate gyrus (DG), but no difference in the linear density of proliferating cells (Ki67+) in the SGZ, nor in areal density of mature neurons (NeuN+) or microglia (Iba-1+) in the DG in IUGR rats compared to controls. Dendritic morphology of dentate granule cells did not differ between groups. Protein expression of the BDNF precursor (pro-BDNF), but not mature BDNF, was increased in the hippocampus of IUGR compared with control rats. These findings highlight that while the long-lasting prenatal hypoxic environment may impact brain development, it may not impact hippocampal-dependent learning and memory in adolescence.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
321-334Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Aimone, J. B., Deng, W., & Gage, F. H. (2011). Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron, 70(4), 589-596. https://doi.org/10.1016/j.neuron.2011.05.010
Akers, K. G., Martinez-Canabal, A., Restivo, L., Yiu, A. P., De Cristofaro, A., Hsiang, H.-L. L., … Shoji, H. (2014). Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science, 344(6184), 598-602.
Altman, J., & Das, G. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. Journal of Comparative Neurology, 124(3), 319-335.
Antunes, M., & Biala, G. (2012). The novel object recognition memory: Neurobiology, test procedure, and its modifications. Cognitive Process, 13(2), 93-110. https://doi.org/10.1007/s10339-011-0430-z
Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joels, M. (2009). Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiology of Learning and Memory, 92(3), 292-300. https://doi.org/10.1016/j.nlm.2009.03.004
Barker, G. R. I., & Warburton, E. C. (2011). Evaluating the neural basis of temporal order memory for visual stimuli in the rat. European Journal of Neuroscience, 33(4), 705-716.
Bekinschtein, P., Kent, B. A., Oomen, C. A., Clemenson, G. D., Gage, F. H., Saksida, L. M., & Bussey, T. J. (2013). BDNF in the dentate gyrus is required for consolidation of "pattern-separated" memories. Cell Reports, 5(3), 759-768. https://doi.org/10.1016/j.celrep.2013.09.027
Bekinschtein, P., Kent, B. A., Oomen, C. A., Clemenson, G. D., Gage, F. H., Saksida, L. M., & Bussey, T. J. (2014). Brain-derived neurotrophic factor interacts with adult-born immature cells in the dentate gyrus during consolidation of overlapping memories. Hippocampus, 24(8), 905-911. https://doi.org/10.1002/hipo.22304
Borodinova, A., & Salozhin, S. (2017). Differences in the biological functions of BDNF and proBDNF in the central nervous system. Neuroscience and Behavioral Physiology, 47(3), 251-265.
Brown, J. P., Couillard-Després, S., Cooper-Kuhn, C. M., Winkler, J., Aigner, L., & Kuhn, H. G. (2003). Transient expression of doublecortin during adult neurogenesis. Journal of Comparative Neurology, 467(1), 1-10.
Buhusi, M., Etheredge, C., Granholm, A.-C., & Buhusi, C. V. (2017). Increased hippocampal ProBDNF contributes to memory impairments in aged mice. Frontiers in Aging Neuroscience, 9, 284.
Camprubi Camprubi, M., Balada Caballe, R., Ortega Cano, J. A., Ortega de la Torre, M. L., Duran Fernandez-Feijoo, C., Girabent-Farres, M., … Alcantara, S. (2017). Learning and memory disabilities in IUGR babies: Functional and molecular analysis in a rat model. Brain and Behavior: A Cognitive Neuroscience Perspective, 7(3), e00631. https://doi.org/10.1002/brb3.631
Chen, J., Li, C.-R., Yang, H., Liu, J., Zhang, T., Jiao, S.-S., … Xu, Z.-Q. (2016). proBDNF attenuates hippocampal neurogenesis and induces learning and memory deficits in aged mice. Neurotoxicity Research, 29(1), 47-53.
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., … Bussey, T. J. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 325, 2010-2213. https://doi.org/10.1126/science.1173215
Colle, E., Schiff, D., Andrew, G., Bauer, C. B., & Fitzhardinge, P. (1976). Insulin responses during catch-up growth of infants who were small for gestational age. Pediatrics, 57(3), 363-371.
Couillard-Despres, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., … Aigner, L. (2005). Doublecortin expression levels in adult brain reflect neurogenesis. European Journal of Neuroscience, 21(1), 1-14. https://doi.org/10.1111/j.1460-9568.2004.03813.x
Delcour, M., Olivier, P., Chambon, C., Pansiot, J., Russier, M., Liberge, M., … Coq, J. O. (2012). Neuroanatomical, sensorimotor and cognitive deficits in adult rats with white matter injury following prenatal ischemia. Brain Pathology, 22(1), 1-16. https://doi.org/10.1111/j.1750-3639.2011.00504.x
Delcour, M., Russier, M., Amin, M., Baud, O., Paban, V., Barbe, M. F., & Coq, J. O. (2012). Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behavioural Brain Research, 232(1), 233-244. https://doi.org/10.1016/j.bbr.2012.03.029
Deng, W., Aimone, J. B., & Gage, F. H. (2010). New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nature Reviews Neuroscience, 11(5), 339-350. https://doi.org/10.1038/nrn2822
Dieni, S., & Rees, S. (2003). Dendritic morphology is altered in hippocampal neurons following prenatal compromise. Developmental Neurobiology, 55(1), 41-52. https://doi.org/10.1002/neu.10194
Dieni, S., & Rees, S. (2005). BDNF and TrkB protein expression is altered in the fetal hippocampus but not cerebellum after chronic prenatal compromise. Experimental Neurology, 192(2), 265-273. https://doi.org/10.1016/j.expneurol.2004.06.003
Dougherty, K. D., Dreyfus, C. F., & Black, I. B. (2000). Brain-derived neurotrophic factor in astrocytes, oligodendrocytes, and microglia/macrophages after spinal cord injury. Neurobiology of Disease, 7(6 Pt B), 574-585. https://doi.org/10.1006/nbdi.2000.0318
Ennaceur, A., & Delacour, J. (1988). A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural Brain Research, 31(1), 47-59.
Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., & Gage, F. H. (1998). Neurogenesis in the adult human hippocampus. Nature Medicine, 4(11), 1313-1317. https://doi.org/10.1038/3305
Figueras, F., & Gardosi, J. (2011). Intrauterine growth restriction: New concepts in antenatal surveillance, diagnosis, and management. American Journal of Obstetrics and Gynecology, 204(4), 288-300. https://doi.org/10.1016/j.ajog.2010.08.055
Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B., Vinet, M.-C., … Kahn, A. (1999). Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron, 23(2), 247-256.
Fung, C., Ke, X., Brown, A. S., Yu, X., McKnight, R. A., & Lane, R. H. (2012). Uteroplacental insufficiency alters rat hippocampal cellular phenotype in conjunction with ErbB receptor expression. Pediatric Research, 72(1), 2-9. https://doi.org/10.1038/pr.2012.32
Furuta, M., Ninomiya-Baba, M., Chiba, S., Funabashi, T., Akema, T., & Kunugi, H. (2015). Exposure to social defeat stress in adolescence improves the working memory and anxiety-like behavior of adult female rats with intrauterine growth restriction, independently of hippocampal neurogenesis. Hormones Behavior, 70, 30-37.
Gao, X., Smith, G. M., & Chen, J. (2009). Impaired dendritic development and synaptic formation of postnatal-born dentate gyrus granular neurons in the absence of brain-derived neurotrophic factor signaling. Experimental Neurology, 215(1), 178-190. https://doi.org/10.1016/j.expneurol.2008.10.009
Geva, R., Eshel, R., Leitner, Y., Fattal-Valevski, A., & Harel, S. (2006). Memory functions of children born with asymmetric intrauterine growth restriction. Brain Research, 1117(1), 186-194. doi:https://doi.org/10.1016/j.brainres.2006.08.004
Geva, R., Eshel, R., Leitner, Y., Valevski, A. F., & Harel, S. (2006). Neuropsychological outcome of children with intrauterine growth restriction: A 9-year prospective study. Pediatrics, 118(1), 91-100. https://doi.org/10.1542/10.1542/peds.2005-2343
Gilchrist, C., Cumberland, A., Walker, D., & Tolcos, M. (2018). Intrauterine growth restriction and development of the hippocampus: Implications for learning and memory in children and adolescents. The Lancet Child & Adolescent Health, 2(10), 755-764. https://doi.org/10.1016/s2352-4642(18)30245-1
Gleeson, J. G., Lin, P. T., Flanagan, L. A., & Walsh, C. A. (1999). Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23(2), 257-271.
Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nature Neuroscience, 2(3), 260-265. https://doi.org/10.1038/6365
Greenberg, M. E., Xu, B., Lu, B., & Hempstead, B. L. (2009). New insights in the biology of BDNF synthesis and release: Implications in CNS function. Journal of Neuroscience, 29(41), 12764-12767.
Guo, J., Ji, Y., Ding, Y., Jiang, W., Sun, Y., Lu, B., & Nagappan, G. (2016). BDNF pro-peptide regulates dendritic spines via caspase-3. Cell Death & Disease, 7(6), e2264-e2264.
Hammond, R. S., Tull, L. E., & Stackman, R. W. (2004). On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiology of Learning and Memory, 82(1), 26-34. https://doi.org/10.1016/j.nlm.2004.03.005
Hill, R. A., & van den Buuse, M. (2011). Sex-dependent and region-specific changes in TrkB signaling in BDNF heterozygous mice. Brain Research, 1384, 51-60. https://doi.org/10.1016/j.brainres.2011.01.060
Jin, K., Minami, M., Lan, J. Q., Mao, X. O., Batteur, S., Simon, R. P., & Greenberg, D. A. (2001). Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proceedings of the National Academy of Sciences, 98(8), 4710-4715.
Jin, K., Sun, Y., Xie, L., Peel, A., Mao, X. O., Batteur, S., & Greenberg, D. A. (2003). Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Molecular and Cellular Neuroscience, 24(1), 171-189.
Jonasson, Z. (2005). Meta-analysis of sex differences in rodent models of learning and memory: A review of behavioral and biological data. Neuroscience Biobehavioral Reviews, 28(8), 811-825.
Kent, B. A., Beynon, A. L., Hornsby, A. K., Bekinschtein, P., Bussey, T. J., Davies, J. S., & Saksida, L. M. (2015). The orexigenic hormone acyl-ghrelin increases adult hippocampal neurogenesis and enhances pattern separation. Psychoneuroendocrinology, 51, 431-439. https://doi.org/10.1016/j.psyneuen.2014.10.015
Klempin, F., Kronenberg, G., Cheung, G., Kettenmann, H., & Kempermann, G. (2011). Properties of doublecortin-(DCX)-expressing cells in the piriform cortex compared to the neurogenic dentate gyrus of adult mice. PLoS One, 6(10), e25760. https://doi.org/10.1371/journal.pone.0025760
Kok, J. H., Lya den Ouden, A., Verloove-Vanhorick, S. P., & Brand, R. (1998). Outcome of very preterm small for gestational age infants: The first nine years of life. BJOG: An International Journal of Obstetrics & Gynaecology, 105(2), 162-168. https://doi.org/10.1111/j.1471-0528.1998.tb10046.x
Lauritz, B., Siebel, A. L., Guille, V., Jefferies, A. J., & Wlodek, M. E. (2012). Growth restriction alters adult spatial memory and sensorimotor gating in a sex-specific manner. Journal of Developmental Origins of Health and Disease, 3(1), 59-68. https://doi.org/10.1017/S2040174411000729
Lee, R., Kermani, P., Teng, K. K., & Hempstead, B. L. (2001). Regulation of cell survival by secreted proneurotrophins. Science, 294(5548), 1945-1948.
Leitner, Y., Fattal-Valevski, A., Geva, R., Eshel, R., Toledano-Alhadef, H., Rotstein, M., … Harel, S. (2007). Neurodevelopmental outcome of children with intrauterine growth retardation: A longitudinal, 10-year prospective study. Journal of Child Neurology, 22(5), 580-587. https://doi.org/10.1177/0883073807302605
Leitner, Y., Heldman, D., Harel, S., & Pick, C. G. (2005). Deficits in spatial orientation of children with intrauterine growth retardation. Brain Research Bulletin, 67(1-2), 13-18. https://doi.org/10.1016/j.brainresbull.2005.04.017
Leuner, B., Mendolia-Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E., & Shors, T. J. (2004). Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. Journal of Neuroscience, 24(34), 7477-7481. https://doi.org/10.1523/JNEUROSCI.0204-04.2004
Lodygensky, G. A., Seghier, M. L., Warfield, S. K., Tolsa, C. B., Sizonenko, S., Lazeyras, F., & Hüppi, P. S. (2008). Intrauterine growth restriction affects the preterm infant's hippocampus. Pediatric Research, 63(4), 438-443. https://doi.org/10.1203/PDR.0b013e318165c005
Lu, B., Pang, P. T., & Woo, N. H. (2005). The yin and yang of neurotrophin action. Nature Reviews Neuroscience, 6(8), 603-614.
Mandruzzato, G., Antsaklis, A., Botet, F., Chervenak, F. A., Figueras, F., Grunebaum, A., … Wapm. (2008). Intrauterine restriction (IUGR). J Perinatal Medicine, 36(4), 277-281. doi:https://doi.org/10.1515/JPM.2008.050
McDougall, A. R. A., Wiradjaja, V., Azhan, A., Li, A., Hale, N., Wlodek, M. E., … Tolcos, M. (2017). Intrauterine growth restriction alters the postnatal development of the rat cerebellum. Developmental Neuroscience., 39, 215-227. https://doi.org/10.1159/000470902
Mizui, T., Ishikawa, Y., Kumanogoh, H., Lume, M., Matsumoto, T., Hara, T., … Itami, C. (2015). BDNF pro-peptide actions facilitate hippocampal LTD and are altered by the common BDNF polymorphism Val66Met. Proceedings of the National Academy of Sciences, 112(23), E3067-E3074.
Padilla, N., Falcon, C., Sanz-Cortes, M., Figueras, F., Bargallo, N., Crispi, F., … Gratacos, E. (2011). Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: A magnetic resonance imaging study. Brain Research, 1382, 98-108. https://doi.org/10.1016/j.brainres.2011.01.032
Paxinos, G., & Watson, C. (2006). The rat brain in stereotaxic coordinates: Hard cover edition, Amsterdam, The Netherlands: Elsevier.
Pokorný, J., & Trojan, S. (1986). The development of hippocampal structure and how it is influenced by hypoxia. Acta Universitatis Carolinae. Medica. Monographia, 113, 1-79.
Rees, S., Bocking, A. D., & Harding, R. (1988). Structure of the fetal sheep brain in experimental growth retardation. Journal of Developmental Physiology, 10(3), 211-225.
Reichardt, L. F. (2006). Neurotrophin-regulated signalling pathways. Philosophical Transactions of the Royal Society B: Biological Sciences, 361(1473), 1545-1564.
Scholzen, T., & Gerdes, J. (2000). The Ki-67 protein: From the known and the unknown. Journal of Cellular Physiology, 182(3), 311-322.
Seibenhener, M. L., & Wooten, M. C. (2015). Use of the open field maze to measure locomotor and anxiety-like behavior in mice. Journal of Visualized Experiments, 96, e52434. https://doi.org/10.3791/52434
Suffren, S., Angulo, D., Ding, Y., Reyes, P., Marin, J., Hernandez, J. T., … Lodygensky, G. A. (2017). Long-term attention deficits combined with subcortical and cortical structural central nervous system alterations in young adults born small for gestational age. Early Human Development, 110, 44-49.
Teng, H. K., Teng, K. K., Lee, R., Wright, S., Tevar, S., Almeida, R. D., … Lee, F. S. (2005). ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. Journal of Neuroscience, 25(22), 5455-5463.
Tolcos, M., Bateman, E., O'Dowd, R., Markwick, R., Vrijsen, K., Rehn, A., & Rees, S. (2011). Intrauterine growth restriction affects the maturation of myelin. Experimental Neurology, 232(1), 53-65. https://doi.org/10.1016/j.expneurol.2011.08.002
Tolcos, M., Markwick, R., O'Dowd, R., Martin, V., Turnley, A., & Rees, S. (2015). Intrauterine growth restriction: Effects on neural precursor cell proliferation and angiogenesis in the Foetal subventricular zone. Developmental Neuroscience, 37(4-5), 453-463. https://doi.org/10.1159/000371344
von Beckerath, A. K., Kollmann, M., Rotky-Fast, C., Karpf, E., Lang, U., & Klaritsch, P. (2013). Perinatal complications and long-term neurodevelopmental outcome of infants with intrauterine growth restriction. American Journal of Obstetrics and Gynecology, 208(2), 130 e131-130 e136. https://doi.org/10.1016/j.ajog.2012.11.014
von Bohlen Und Halbach, O. (2007). Immunohistological markers for staging neurogenesis in adult hippocampus. Cell and Tissue Research, 329(3), 409-420. https://doi.org/10.1007/s00441-007-0432-4
Voyer, D., Voyer, S., & Bryden, M. P. (1995). Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables. Psychological Bulletin, 117(2), 250-270.
Wigglesworth, J. S. (1974). Fetal growth retardation. Animal model: Uterine vessel ligation in the pregnant rat. The American Journal of Pathology, 77(2), 347-350.
Wilson, R. C., Vacek, T., Lanier, D. L., & Dewsbury, D. A. (1976). Open-field behavior in muroid rodents. Behavioral Biology, 17(4), 495-506.
Workman, A. D., Charvet, C. J., Clancy, B., Darlington, R. B., & Finlay, B. L. (2013). Modeling transformations of neurodevelopmental sequences across mammalian species. Journal of Neuroscience, 33(17), 7368-7383. https://doi.org/10.1523/JNEUROSCI.5746-12.2013
Xu, Z. Q., Sun, Y., Li, H. Y., Lim, Y., Zhong, J. H., & Zhou, X. F. (2011). Endogenous proBDNF is a negative regulator of migration of cerebellar granule cells in neonatal mice. European Journal of Neuroscience, 33(8), 1376-1384.
Yagi, S., Chow, C., Lieblich, S. E., & Galea, L. A. (2016). Sex and strategy use matters for pattern separation, adult neurogenesis, and immediate early gene expression in the hippocampus. Hippocampus, 26(1), 87-101.
Yanney, M., & Marlow, N. (2004). Paediatric consequences of fetal growth restriction. Seminars in Fetal and Neonatal Medicine, 9(5), 411-418. https://doi.org/10.1016/j.siny.2004.03.005
Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., … Schwartz, M. (2006). Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nature Neuroscience, 9(2), 268-275. https://doi.org/10.1038/nn1629