Developmental and Functional Brain Impairment in Offspring from Preeclampsia-Like Rats
详细信息    查看全文
  • 作者:Xueyuan Liu ; Wenlong Zhao ; Haiyan Liu ; Yaoyue Kang ; Chen Ye…
  • 关键词:Preeclampsia ; like ; l ; NAME ; Water maze ; Adult hippocampal neurogenesis ; Gliogenesis
  • 刊名:Molecular Neurobiology
  • 出版年:2016
  • 出版时间:March 2016
  • 年:2016
  • 卷:53
  • 期:2
  • 页码:1009-1019
  • 全文大小:8,963 KB
  • 参考文献:1.Griffith MI, Mann JR, McDermott S (2011) The risk of intellectual disability in children born to mothers with preeclampsia or eclampsia with partial mediation by low birth weight. Hypertens Pregnancy Off J Int Soc Study Hypertens Pregnancy 30(1):108–115. doi:10.​3109/​10641955.​2010.​507837 CrossRef
    2.Gilbert WM, Danielsen B (2003) Pregnancy outcomes associated with intrauterine growth restriction. Am J Obstet Gynecol 188(6):1596–1599, discussion 1599–1601CrossRef PubMed
    3.Barker DJ (2006) Adult consequences of fetal growth restriction. Clin Obstet Gynecol 49(2):270–283CrossRef PubMed
    4.Buhimschi I, Yallampalli C, Chwalisz K, Garfield RE (1995) Pre-eclampsia-like conditions produced by nitric oxide inhibition: effects of l -arginine, d -arginine and steroid hormones. Human Reprod (Oxf Engl) 10(10):2723–2730
    5.Fantel AG, Nekahi N, Shepard TH, Cornel LM, Unis AS, Lemire RJ (1997) The teratogenicity of N(omega)-nitro-l -ariginine methyl ester (l -NAME), a nitric oxide synthase inhibitor, in rats. Reprod Toxicol (Elmsford, NY) 11(5):709–717CrossRef
    6.Diaz V, Lebras-Isabet MN, Denjean A (2005) Effect of Nomega-nitro-l -arginine methyl ester-induced intrauterine growth restriction on postnatal lung growth in rats. Pediatr Res 58(3):557–561. doi:10.​1203/​01.​pdr.​0000179398.​62365.​43 CrossRef PubMed
    7.Palmsten K, Buka SL, Michels KB (2010) Maternal pregnancy-related hypertension and risk for hypertension in offspring later in life. Obstet Gynecol 116(4):858–864. doi:10.​1097/​AOG.​0b013e3181f3a1f9​ PubMedCentral CrossRef PubMed
    8.Karumanchi SA, Maynard SE, Stillman IE, Epstein FH, Sukhatme VP (2005) Preeclampsia: a renal perspective. Kidney Int 67(6):2101–2113. doi:10.​1111/​j.​1523-1755.​2005.​00316.​x CrossRef PubMed
    9.Woodworth MB, Custo Greig L, Kriegstein AR, Macklis JD (2012) SnapShot: cortical development. Cell 151(4):918–918 e911. doi:10.​1016/​j.​cell.​2012.​10.​004 CrossRef PubMed
    10.Pescosolido MF, Yang U, Sabbagh M, Morrow EM (2012) Lighting a path: genetic studies pinpoint neurodevelopmental mechanisms in autism and related disorders. Dialogues Clin Neurosci 14(3):239–252PubMedCentral PubMed
    11.Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg R (2010) Pre-eclampsia. Lancet 376(9741):631–644. doi:10.​1016/​s0140-6736(10)60279-6 CrossRef PubMed
    12.Whitehouse AJ, Robinson M, Newnham JP, Pennell CE (2012) Do hypertensive diseases of pregnancy disrupt neurocognitive development in offspring? Paediatr Perinat Epidemiol 26(2):101–108. doi:10.​1111/​j.​1365-3016.​2011.​01257.​x CrossRef PubMed
    13.Wu CS, Sun Y, Vestergaard M, Christensen J, Ness RB, Haggerty CL, Olsen J (2008) Preeclampsia and risk for epilepsy in offspring. Pediatrics 122(5):1072–1078. doi:10.​1542/​peds.​ 2007-3666 CrossRef PubMed
    14.Vorhees CV, Williams MT (2006) Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc 1(2):848–858. doi:10.​1038/​nprot.​2006.​116 PubMedCentral CrossRef PubMed
    15.Lopez-Atalaya JP, Ciccarelli A, Viosca J, Valor LM, Jimenez-Minchan M, Canals S, Giustetto M, Barco A (2011) CBP is required for environmental enrichment-induced neurogenesis and cognitive enhancement. EMBO J 30(20):4287–4298. doi:10.​1038/​emboj.​2011.​299 PubMedCentral CrossRef PubMed
    16.Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY (2012) Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484(7394):376–380. doi:10.​1038/​nature10959 PubMedCentral CrossRef PubMed
    17.Stangl D, Thuret S (2009) Impact of diet on adult hippocampal neurogenesis. Genes Nutr 4(4):271–282. doi:10.​1007/​s12263-009-0134-5 PubMedCentral CrossRef PubMed
    18.Ramel SE, Georgieff MK (2014) Preterm nutrition and the brain. World Rev Nutr Diet 110:190–200. doi:10.​1159/​000358467 CrossRef PubMed
    19.Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484. doi:10.​1016/​j.​cell.​2006.​01.​016 CrossRef PubMed
    20.Hansen-Pupp I, Hellstrom-Westas L, Cilio CM, Andersson S, Fellman V, Ley D (2007) Inflammation at birth and the insulin-like growth factor system in very preterm infants. Acta Paediatr (Oslo, Norway 1992) 96(6):830–836. doi:10.​1111/​j.​1651-2227.​2007.​00276.​x CrossRef
    21.Kajantie E, Eriksson JG, Osmond C, Thornburg K, Barker DJ (2009) Pre-eclampsia is associated with increased risk of stroke in the adult offspring: the Helsinki birth cohort study. Stroke J Cereb Circ 40(4):1176–1180. doi:10.​1161/​strokeaha.​108.​538025 CrossRef
    22.Paulis L, Becker ST, Lucht K, Schwengel K, Slavic S, Kaschina E, Thone-Reineke C, Dahlof B, Baulmann J, Unger T, Steckelings UM (2012) Direct angiotensin II type 2 receptor stimulation in Nomega-nitro-l -arginine-methyl ester-induced hypertension: the effect on pulse wave velocity and aortic remodeling. Hypertension 59(2):485–492. doi:10.​1161/​hypertensionaha.​111.​185496 CrossRef PubMed
    23.Freeman MR, Rowitch DH (2013) Evolving concepts of gliogenesis: a look way back and ahead to the next 25 years. Neuron 80(3):613–623. doi:10.​1016/​j.​neuron.​2013.​10.​034 CrossRef PubMed
    24.Martinez-Orgado J, Gonzalez R, Alonso MJ, Salaices M (2004) Impairment of fetal endothelium-dependent relaxation in a rat model of preeclampsia by chronic nitric oxide synthase inhibition. J Soc Gynecol Investig 11(2):82–88. doi:10.​1016/​j.​jsgi.​2003.​08.​003 CrossRef PubMed
    25.Gereltsetseg G, Matsuzaki T, Iwasa T, Kinouchi R, Nakazawa H, Yamamoto S, Kuwahara A, Yasui T, Irahara M (2012) Delay in the onset of puberty of intrauterine growth retarded female rats cannot be rescued with hypernutrition after birth. Endocr J 59(11):963–972CrossRef PubMed
    26.Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250. doi:10.​1146/​annurev.​neuro.​28.​051804.​101459 CrossRef PubMed
    27.Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem (Cold Spring Harb NY) 16(2):147–154. doi:10.​1101/​lm.​1172609 CrossRef
    28.Campbell S, Macqueen G (2004) The role of the hippocampus in the pathophysiology of major depression. J Psychiatr Neurosci JPN 29(6):417–426
    29.Rickmann M, Amaral DG, Cowan WM (1987) Organization of radial glial cells during the development of the rat dentate gyrus. J Comp Neurol 264(4):449–479. doi:10.​1002/​cne.​902640403 CrossRef PubMed
    30.Merkle FT, Tramontin AD, Garcia-Verdugo JM, Alvarez-Buylla A (2004) Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A 101(50):17528–17532. doi:10.​1073/​pnas.​0407893101 PubMedCentral CrossRef PubMed
    31.Li X, Barkho BZ, Luo Y, Smrt RD, Santistevan NJ, Liu C, Kuwabara T, Gage FH, Zhao X (2008) Epigenetic regulation of the stem cell mitogen FGF-2 by Mbd1 in adult neural stem/progenitor cells. J Biol Chem 283(41):27644–27652. doi:10.​1074/​jbc.​M804899200 PubMedCentral CrossRef PubMed
    32.Waterhouse EG, An JJ, Orefice LL, Baydyuk M, Liao GY, Zheng K, Lu B, Xu B (2012) BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. J Neurosci Off J Soc Neurosci 32(41):14318–14330. doi:10.​1523/​jneurosci.​ 0709-12.​2012 CrossRef
    33.Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000) Basic fibroblast growth factor (FGF2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci Off J Soc Neurosci 20(13):5012–5023
    34.Stevens HE, Jiang GY, Schwartz ML, Vaccarino FM (2012) Learning and memory depend on fibroblast growth factor receptor 2 functioning in hippocampus. Biol Psychiatry 71(12):1090–1098. doi:10.​1016/​j.​biopsych.​2012.​03.​013 PubMedCentral CrossRef PubMed
    35.Mudo G, Bonomo A, Di Liberto V, Frinchi M, Fuxe K, Belluardo N (2009) The FGF-2/FGFRs neurotrophic system promotes neurogenesis in the adult brain. J Neural Transm (Vienna Austria 1996) 116(8):995–1005. doi:10.​1007/​s00702-009-0207-z CrossRef
    36.Wang D, Song X, Wang Y, Li X, Jia S, Wang Z (2014) Gene expression profile analysis in epilepsy by using the partial least squares method. TheScientificWorldJOURNAL 2014:731091. doi:10.​1155/​2014/​731091 PubMedCentral PubMed
    37.Paradiso B, Marconi P, Zucchini S, Berto E, Binaschi A, Bozac A, Buzzi A, Mazzuferi M, Magri E, Navarro Mora G, Rodi D, Su T, Volpi I, Zanetti L, Marzola A, Manservigi R, Fabene PF, Simonato M (2009) Localized delivery of fibroblast growth factor-2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model. Proc Natl Acad Sci U S A 106(17):7191–7196. doi:10.​1073/​pnas.​0810710106 PubMedCentral CrossRef PubMed
    38.Beaumont TL, Yao B, Shah A, Kapatos G, Loeb JA (2012) Layer-specific CREB target gene induction in human neocortical epilepsy. J Neurosci Off J Soc Neurosci 32(41):14389–14401. doi:10.​1523/​jneurosci.​ 3408-12.​2012 CrossRef
    39.Covic M, Karaca E, Lie DC (2010) Epigenetic regulation of neurogenesis in the adult hippocampus. Heredity 105(1):122–134. doi:10.​1038/​hdy.​2010.​27 CrossRef PubMed
    40.Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Sci (New York, NY) 323(5917):1074–1077. doi:10.​1126/​science.​1166859 CrossRef
  • 作者单位:Xueyuan Liu (1) (2)
    Wenlong Zhao (3) (8)
    Haiyan Liu (1)
    Yaoyue Kang (4)
    Chen Ye (5)
    Weirong Gu (1) (2)
    Rong Hu (1)
    Xiaotian Li (1) (2) (6) (7)

    1. Obstetrics and Gynecology Hospital of Fudan University, 200011, Shanghai, China
    2. Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai, 200011, China
    3. University of Chinese Academy of Sciences, Shanghai, 200031, China
    8. Institute of Neuroscience, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai, 200031, China
    4. Division of Infectious Disease, Huashan Hospital, Fudan University, Shanghai, China
    5. Shanghai Changzheng Hospital, Second Military Medical University, Shanghai, China
    6. Institute of Biomedical Sciences, Fudan University, Shanghai, 200011, China
    7. Shanghai Key Laboratory of Birth Defects, Shanghai, 200011, China
  • 刊物主题:Neurosciences; Neurobiology; Cell Biology; Neurology;
  • 出版者:Springer US
  • ISSN:1559-1182
文摘
Preeclampsia is associated with developmental delay in infants and with an increased risk of various diseases in adulthood, including hypertension and epilepsy. It has been reported that several organs show developmental retardation and functional deficiency in offspring of preeclamptic rats. However, the developmental and functional changes in brains of the offspring of preeclamptic rats remain unknown. Here, we established a preeclampsia-like rat model induced using Nω-nitro-l-arginine methyl ester (l-NAME) to analyze the developmental and functional changes in brains of the offspring. Body and brain weights were decreased in the l-NAME group at postnatal day 0 (P0). However, there were no significant differences between the l-NAME and control groups in brain and body weights at P56. Upon further analysis, we detected a deficiency in neurogenesis, but not in apoptosis, which contributed to the smaller brains of the offspring in the l-NAME group at P0. Additionally, we observed an increase in gliogenesis to compensate for the brain weights of the offspring at P56. Although the weight and laminar structure of the brains were essentially normal at P56, spatial learning and memory were severely impaired. We also found that adult hippocampal neurogenesis was disrupted in the offspring from preeclampsia-like rats, which may explain the cognitive deficiency. Moreover, qRT-PCR revealed a reduced expression of neurogenesis-related genes in the offspring. Overall, we have described the deleterious effects of preeclampsia on the brains of offspring, providing clues to the cellular and molecular mechanisms involved in this pathogenesis, which may aid in the development of therapeutic approaches. Keywords Preeclampsia-like l-NAME Water maze Adult hippocampal neurogenesis Gliogenesis

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700