Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 18, 2015 - Issue 8
316
Views
17
CrossRef citations to date
0
Altmetric
Original research paper

Fetal and neonatal iron deficiency but not copper deficiency increases vascular complexity in the developing rat brain

, , , , &

References

  • McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr 2009;12(4):444–54. doi: 10.1017/S1368980008002401
  • Fretham SJ, Carlson ES, Georgieff MK. The role of iron in learning and memory. Adv Nutr 2011;2(2):112–21. doi: 10.3945/an.110.000190
  • Lozoff B, Georgieff MK. Iron deficiency and brain development. Semin Pediatr Neurol 2006;13(3):158–65. doi: 10.1016/j.spen.2006.08.004
  • Johnson WT. Copper and brain function. In: Lieberman HR, Kanarek RB, Prasad C, (eds.) Nutritional neuroscience. Boca Raton: Taylor and Francis Group; 2005. p. 289–305.
  • Uriu-Adams JY, Scherr RE, Lanoue L, Keen CL. Influence of copper on early development: prenatal and postnatal considerations. Biofactors 2010;36(2):136–52.
  • Bastian TW, Lassi KC, Anderson GW, Prohaska JR. Maternal iron supplementation attenuates the impact of perinatal copper deficiency but does not eliminate hypotriiodothyroninemia nor impaired sensorimotor development. J Nutr Biochem 2011;22(11):1084–90. doi: 10.1016/j.jnutbio.2010.09.007
  • LaManna JC, Chavez JC, Pichiule P. Structural and functional adaptation to hypoxia in the rat brain. J Exp Biol 2004;207(Pt 18):3163–9. doi: 10.1242/jeb.00976
  • LaManna JC, Vendel LM, Farrell RM. Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 1992;72(6):2238–43.
  • Ogunshola OO, Stewart WB, Mihalcik V, Solli T, Madri JA, Ment LR. Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res Dev Brain Res 2000;119(1):139–53. doi: 10.1016/S0165-3806(99)00125-X
  • Marti HH, Risau W. Systemic hypoxia changes the organ-specific distribution of vascular endothelial growth factor and its receptors. Proc Natl Acad Sci USA 1998;95(26):15809–14. doi: 10.1073/pnas.95.26.15809
  • Pichiule P, LaManna JC. Angiopoietin-2 and rat brain capillary remodeling during adaptation and deadaptation to prolonged mild hypoxia. J Appl Physiol 2002;93(3):1131–9. doi: 10.1152/japplphysiol.00318.2002
  • Miller JT, Bartley JH, Wimborne HJ, Walker AL, Hess DC, Hill WD, et al. The neuroblast and angioblast chemotaxic factor SDF-1 (CXCL12) expression is briefly up regulated by reactive astrocytes in brain following neonatal hypoxic-ischemic injury. BMC Neurosci 2005;6:63. doi: 10.1186/1471-2202-6-63
  • Baburamani AA, Ek CJ, Walker DW, 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. doi: 10.3389/fphys.2012.00424
  • Dore-Duffy P, LaManna JC. Physiologic angiodynamics in the brain. Antioxid Redox Signal 2007;9(9):1363–71. doi: 10.1089/ars.2007.1713
  • Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004;10(8):858–64. doi: 10.1038/nm1075
  • Toblli JE, Cao G, Oliveri L, Angerosa M. Effects of iron deficiency anemia and its treatment with iron polymaltose complex in pregnant rats, their fetuses and placentas: oxidative stress markers and pregnancy outcome. Placenta 2012;33(2):81–7. doi: 10.1016/j.placenta.2011.11.017
  • Carlson ES, Stead JD, Neal CR, Petryk A, Georgieff MK. Perinatal iron deficiency results in altered developmental expression of genes mediating energy metabolism and neuronal morphogenesis in hippocampus. Hippocampus 2007;17(8):679–91. doi: 10.1002/hipo.20307
  • Tran PV, Fretham SJ, Wobken J, Miller BS, Georgieff MK. Gestational–neonatal iron deficiency suppresses and iron treatment reactivates IGF signaling in developing rat hippocampus. Am J Physiol Endocrinol Metab 2012;302(3):E316–24. doi: 10.1152/ajpendo.00369.2011
  • Matak P, Zumerle S, Mastrogiannaki M, El Balkhi S, Delga S, Mathieu JR, et al. Copper deficiency leads to anemia, duodenal hypoxia, upregulation of HIF-2alpha and altered expression of iron absorption genes in mice. PLOS One 2013;8(3):e59538. doi: 10.1371/journal.pone.0059538
  • Feng W, Ye F, Xue W, Zhou Z, Kang YJ. Copper regulation of hypoxia-inducible factor-1 activity. Mol Pharmacol 2009;75(1):174–82. doi: 10.1124/mol.108.051516
  • Pyatskowit JW, Prohaska JR. Iron injection restores brain iron and hemoglobin deficits in perinatal copper-deficient rats. J Nutr 2008;138(10):1880–6.
  • Bastian TW, Anderson JA, Fretham SJ, Prohaska JR, Georgieff MK, Anderson GW. Fetal and neonatal iron deficiency reduces thyroid hormone-responsive gene mRNA levels in the neonatal rat hippocampus and cerebral cortex. Endocrinology 2012;153(11):5668–80. doi: 10.1210/en.2012-1067
  • Bastian TW, Prohaska JR, Georgieff MK, Anderson GW. Perinatal iron and copper deficiencies alter neonatal rat circulating and brain thyroid hormone concentrations. Endocrinology 2010;151(8):4055–65. doi: 10.1210/en.2010-0252
  • Bastian TW, Prohaska JR, Georgieff MK, Anderson GW. Fetal and neonatal iron deficiency exacerbates mild thyroid hormone insufficiency effects on male thyroid hormone levels and brain thyroid hormone-responsive gene expression. Endocrinology 2014;155(3):1157–67. doi: 10.1210/en.2013-1571
  • Prohaska JR. Changes in tissue growth, concentrations of copper, iron, cytochrome oxidase and superoxide dismutase subsequent to dietary or genetic copper deficiency in mice. J Nutr 1983;113(10):2048–58.
  • Gerhart DZ, LeVasseur RJ, Broderius MA, Drewes LR. Glucose transporter localization in brain using light and electron immunocytochemistry. J Neurosci Res 1989;22(4):464–72. doi: 10.1002/jnr.490220413
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012;9(7):671–5. doi: 10.1038/nmeth.2089
  • Harb R, Whiteus C, Freitas C, Grutzendler J. In vivo imaging of cerebral microvascular plasticity from birth to death. J Cereb Blood Flow Metab 2013;33(1):146–56. doi: 10.1038/jcbfm.2012.152
  • Murugesan N, Demarest TG, Madri JA, Pachter JS. Brain regional angiogenic potential at the neurovascular unit during normal aging. Neurobiol Aging 2012;33(5):1004.e1–16. doi: 10.1016/j.neurobiolaging.2011.09.022
  • Yamamoto K, de Waard V, Fearns C, Loskutoff DJ. Tissue distribution and regulation of murine von Willebrand factor gene expression in vivo. Blood 1998;92(8):2791–801.
  • Vannucci SJ, Maher F, Simpson IA. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 1997;21(1):2–21. doi: 10.1002/(SICI)1098-1136(199709)21:1<2::AID-GLIA2>3.0.CO;2-C
  • Sharp FR, Bernaudin M. HIF1 and oxygen sensing in the brain. Nat Rev Neurosci 2004;5(6):437–48. doi: 10.1038/nrn1408
  • Stoltzfus R. Defining iron-deficiency anemia in public health terms: a time for reflection. J Nutr 2001;131(2S-2):565S–7S.
  • Carlson ES, Tkac I, Magid R, O'Connor MB, Andrews NC, Schallert T, et al. Iron is essential for neuron development and memory function in mouse hippocampus. J Nutr 2009;139(4):672–9. doi: 10.3945/jn.108.096354
  • Carlson ES, Fretham SJ, Unger E, O'Connor M, Petryk A, Schallert T, et al. Hippocampus specific iron deficiency alters competition and cooperation between developing memory systems. J Neurodev Disord 2010;2(3):133–43. doi: 10.1007/s11689-010-9049-0
  • Fretham SJ, Carlson ES, Georgieff MK. Neuronal-specific iron deficiency dysregulates mammalian target of rapamycin signaling during hippocampal development in nonanemic genetic mouse models. J Nutr 2013;143(3):260–6. doi: 10.3945/jn.112.168617
  • Tuor UI, Kurpita G, Simone C. Correlation of local changes in cerebral blood flow, capillary density, and cytochrome oxidase during development. J Comp Neurol 1994;342(3):439–48. doi: 10.1002/cne.903420310
  • Hawkins BT, Davis TP. The blood–brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005;57(2):173–85. doi: 10.1124/pr.57.2.4
  • Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 2002;125(Pt 11):2549–57. doi: 10.1093/brain/awf257
  • Ben-Shachar D, Yehuda S, Finberg JP, Spanier I, Youdim MB. Selective alteration in blood–brain barrier and insulin transport in iron-deficient rats. J Neurochem 1988;50(5):1434–7. doi: 10.1111/j.1471-4159.1988.tb03027.x
  • Garcia SJ, Gellein K, Syversen T, Aschner M. Iron deficient and manganese supplemented diets alter metals and transporters in the developing rat brain. Toxicol Sci 2007;95(1):205–14. doi: 10.1093/toxsci/kfl139
  • Monnot AD, Behl M, Ho S, Zheng W. Regulation of brain copper homeostasis by the brain barrier systems: effects of Fe-overload and Fe-deficiency. Toxicol Appl Pharmacol 2011;256(3):249–57. doi: 10.1016/j.taap.2011.02.003
  • Zatta P, Frank A. Copper deficiency and neurological disorders in man and animals. Brain Res Rev 2007;54(1):19–33. doi: 10.1016/j.brainresrev.2006.10.001
  • Ward NL, Lamanna JC. The neurovascular unit and its growth factors: coordinated response in the vascular and nervous systems. Neurol Res 2004;26(8):870–83. doi: 10.1179/016164104X3798
  • Brunette KE, Tran PV, Wobken JD, Carlson ES, Georgieff MK. Gestational and neonatal iron deficiency alters apical dendrite structure of CA1 pyramidal neurons in adult rat hippocampus. Dev Neurosci 2010;32(3):238–48. doi: 10.1159/000314341

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.