Neonatal Iron Deficiency Results in Irreversible Changes in Dopamine Function in Rats
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Iron deficiency in human infants and in young animal models produces changes in neural functioning that may be related to monoamine metabolism. This study employed both behavioral and biochemical approaches in a design using cross-fostering to examine alterations in dopamine (DA) function when iron deficiency occurs during the neonatal period. We measured brain Fe, dopamine transporters (DAT) and dopamine receptor density in rats made iron deficient, or not, from postnatal day (PND) 4 to PND 14 or 21. Some pups were then weaned to an iron-deficient diet and others to the control diet to examine the reversibility of these effects. Behaviors related to dopamine function were measured. Dopamine D(2) receptor (D(2)R), D(1)R and iron concentrations were approximately 70, 80 and 30% of control values, respectively, in the nucleus accumbens and striatum in iron-deficient rats at PND 14. The DAT density was also reduced to 50% of control density in the nucleus accumbens but was unchanged in the striatum. By PND 21, there was also a significant 50% lowering of DAT, D(1)R and D(2)R densities in the prefrontal cortex (PFC). Iron repletion at PND 21-49 normalized D(1)R, D(2)R, and DAT levels in the nucleus accumbens, PFC and ventral midbrain but not in the striatum. In summary, neonatal iron deficiency is associated with changes in DA biology that vary with duration of iron deficiency, and are not completely normalized despite replenishment of iron status. Changes in DA-related behaviors that were persistent after postweaning iron repletion suggest the existence of a critical neonatal developmental period that is expressed by alterations in DA functioning.
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Deviations from normal iron levels have been indicated in the pathogenesis of aging, neurodegenerative disease, cancer, and infection.
“Deviations from normal iron levels have been indicated in the pathogenesis of aging, neurodegenerative disease, cancer, and infection (18, 23, 156, 180, 299, 334).”
From Intracellular iron transport and storage: from molecular mechanisms to health implications (2008) · cites this paper as [18]
Iron deficiency may have deleterious effects on neurotransmission, myelination, and dopamine receptor and transporter functions.
“Iron deficiency may have deleterious effects on neurotransmission, myelination, and dopamine receptor and transporter functions (18).”
From Intracellular iron transport and storage: from molecular mechanisms to health implications (2008) · cites this paper as [18]
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Reeves, P. G., Nielsen, F. H., & Fahey, G. C., Jr. (1993) · Journal of Nutrition · doi:10.1093/jn/123.11.1939 · Cited by 8,730 · see citing works
Applied statistics for the behavioral sciences
Hinkle, D. E., Wiersma, W., & Jurs, S. G. (1979) · Cited by 2,119 · see citing works
Iron Deficiency in Infancy and Childhood
Desforges, J. F., & Oski, F. A. (1993) · New England Journal of Medicine · doi:10.1056/nejm199307153290308 · Cited by 798 · see citing works
Reversal of developmental delays in iron-deficient anaemic infants treated with iron
Idjradinata, P. S., & Pollitt, E. (1993) · The Lancet · doi:10.1016/0140-6736(93)92477-b · Cited by 489 · see citing works
Roncagliolo, M., Marcelo Garrido, S., Walter, T., Peirano, P. D., & Lozoff, B. (1998) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/68.3.683 · Cited by 371 · see citing works
Tarazi, F. I., & Baldessarini, R. J. (2000) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(99)00108-2 · Cited by 327 · see citing works
Effect of Iron Therapy on Behavior Performance in Nonanemic, Iron-Deficient Infants
Oski, F. A., Honig, A. S., Helu, B. M., & Howanitz, P. J. (1983) · PEDIATRICS · doi:10.1542/peds.71.6.877 · Cited by 308 · see citing works
Iron Deficiency and Cognitive Function
Pollitt, E. (1993) · Annual Review of Nutrition · doi:10.1146/annurev.nu.13.070193.002513 · Cited by 288 · see citing works
Iron Deficiency Alters Dopamine Transporter Functioning in Rat Striatum
Erikson, K. M., Jones, B. C., & Beard, J. L. (2000) · Journal of Nutrition · doi:10.1093/jn/130.11.2831 · Cited by 273 · see citing works
Self-citationBehavior of Infants with Iron-Deficiency Anemia
Lozoff, B., Klein, N. K., Nelson, E. C., McClish, D. K., Manuel, M., & Chacon, M. E. (1998) · Child Development · doi:10.1111/j.1467-8624.1998.tb06130.x · Cited by 263 · see citing works
Putative biological mechanisms of the effect of iron deficiency on brain biochemistry and behavior
Youdim, M. B. H., Ben‐Shachar, D., & Yehuda, S. (1989) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/50.3.607 · Cited by 238 · see citing works
Erikson, K. M., Piñero, D. J., Connor, J. R., & Beard, J. L. (1997) · Journal of Nutrition · doi:10.1093/jn/127.10.2030 · Cited by 237 · see citing works
Self-citationIn Vivo Dopamine Metabolism Is Altered in Iron-Deficient Anemic Rats
Nelson, C., Erikson, K. M., Piñero, D. J., & Beard, J. L. (1997) · Journal of Nutrition · doi:10.1093/jn/127.12.2282 · Cited by 204 · see citing works
Self-citationIron, Transferrin, and Ferritin in the Rat Brain During Development and Aging
Roskams, A. J., & Connor, J. R. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63020709.x · Cited by 173 · see citing works
Variations in Dietary Iron Alter Brain Iron Metabolism in Developing Rats
Piñero, D. J., Li, N., Connor, J. R., & Beard, J. L. (2000) · Journal of Nutrition · doi:10.1093/jn/130.2.254 · Cited by 163 · see citing works
Self-citationEffect of prenatal iron deficiency on myelination in rat pups.
Yu, G. S., Steinkirchner, T. M., Rao, G. A., & Larkin, E. C. (1986) · PubMed Central · Cited by 156 · see citing works
Nutritional iron and dopamine binding sites in the rat brain
Ashkenazi, R., Ben‐Shachar, D., & Youdim, M. B. H. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90509-3 · Cited by 149 · see citing works
Neurobehavioral analysis of developmental iron deficiency in rats
Beard, J. L., Erikson, K. M., & Jones, B. C. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00092-x · Cited by 147 · see citing works
Self-citationLeslie, C. A., Robertson, M. W., Cutler, A. J., & Bennett, J. P. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90195-o · Cited by 126 · see citing works
Importance of Fetal and Neonatal Iron: Adequacy for Normal Development of Central Nervous System
Larkin, E. C., & Rao, G. A. (1990) · Springer eBooks · doi:10.1007/978-1-4471-1766-7_5 · Cited by 115 · see citing works
Behavioral implications of dopaminergic neurons in the mesolimbic system.
Sd, I., & Koob, G. F. (1977) · PubMed · Cited by 96 · see citing works
Behavioral aspects of iron deficiency.
Lozoff, B., & Brittenham, G. (1986) · PubMed · Cited by 90 · see citing works
Variations in Dietary Iron Alter Behavior in Developing Rats
Piñero, D. J., Jones, B. C., & Beard, J. L. (2001) · Journal of Nutrition · doi:10.1093/jn/131.2.311 · Cited by 89 · see citing works
Self-citationBrain Iron, Transferrin and Ferritin Concentrations Are Altered in Developing Iron-Deficient Rats
Chen, Q., Connor, J. R., & Beard, J. L. (1995) · Journal of Nutrition · doi:10.1093/jn/125.6.1529 · Cited by 88 · see citing works
Self-citationYoudim, M. B. H., Yehuda, S., & Ben-Uriah, Y. (1981) · European Journal of Pharmacology · doi:10.1016/0014-2999(81)90048-0 · Cited by 88 · see citing works
Impact of iron deficiency on cognition in infancy and childhood.
Walter, T. (1993) · PubMed · Cited by 80 · see citing works
Ontogeny of dopamine D1 receptors in rat forebrain: a quantitative autoradiographic study
Murrin, L. C., & Zeng, W. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90178-2 · Cited by 70 · see citing works
Severe or marginal iron deficiency affects spontaneous physical activity in rats
Hunt, J., Zito, C. A., Erjavec, J., & Johnson, L. (1994) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/59.2.413 · Cited by 69 · see citing works
Brain iron and dopamine receptor function.
Youdim, M. B. H., Ben‐Shachar, D., Ashkenazi, R., & Yehuda, S. (1983) · PubMed · Cited by 67 · see citing works
Iron Deficiency in Infancy and Childhood
Borgna‐Pignatti, C., & Marsella, M. (2008) · Pediatric Annals · doi:10.3928/00904481-20080501-09 · Cited by 63 · see citing works
Impact of maternal iron deficiency on quality and quantity of milk ingested by neonatal rats
O’Connor, D. L., Picciano, M. F., & Sherman, A. R. (1988) · British Journal Of Nutrition · doi:10.1079/bjn19880120 · Cited by 34 · see citing works
Iron deficiency alters H- and L-ferritin expression in rat brain.
Han, J., Day, J. R., Thomson, K. A., Connor, J. R., & Beard, J. L. (2000) · PubMed · Cited by 30 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Biomarkers of Nutrition for Development—Folate Review
Bailey, L. B., Stover, P. J., McNulty, H., Fenech, M. F., Gregory, J. F., Mills, J. L., Pfeiffer, C. M., Fazili, Z., Zhang, M., Ueland, P. M., et al. (2015) · Journal of Nutrition · doi:10.3945/jn.114.206599 · Cited by 1,170 · see citing works
Intracellular iron transport and storage: from molecular mechanisms to health implications
Mackenzie, E. L., Iwasaki, K., & Tsuji, Y. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2007.1893 · Cited by 526 · see citing works
McCann, J. C., & Ames, B. N. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.4.931 · Cited by 501 · see citing works
Iron Deficiency and Child Development
Lozoff, B. (2007) · Food and Nutrition Bulletin · doi:10.1177/15648265070284s409 · Cited by 450 · see citing works
Altered dopaminergic profile in the putamen and substantia nigra in restless leg syndrome
Connor, J. R., Wang, X.-S., Allen, R. P., Beard, J. L., Wiesinger, J. A., Felt, B. T., & Earley, C. J. (2009) · Brain · doi:10.1093/brain/awp125 · Cited by 355 · see citing works
Self-citationBiomarkers of Nutrition for Development (BOND)—Iron Review
Lynch, S. R., Pfeiffer, C. M., Georgieff, M., Brittenham, G. M., Fairweather‐Tait, S. J., Hurrell, R. F., McArdle, H. J., & Raiten, D. J. (2018) · Journal of Nutrition · doi:10.1093/jn/nxx036 · Cited by 363 · see citing works
High‐field magnetic resonance imaging of brain iron: birth of a biomarker?
Schenck, J. F., & Zimmerman, E. A. (2004) · NMR in Biomedicine · doi:10.1002/nbm.922 · Cited by 330 · see citing works
Why Iron Deficiency Is Important in Infant Development
Beard, J. L. (2008) · The Journal of Nutrition · doi:10.1093/jn/138.12.2534 · Cited by 316 · see citing works
Self-citationRole of micronutrients in the periconceptional period
Cetin, I., Berti, C., & Calabrese, S. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp025 · Cited by 320 · see citing works
Iron and mechanisms of emotional behavior
Kim, J., & Wessling‐Resnick, M. (2014) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2014.07.003 · Cited by 314 · see citing works
Long-term brain and behavioral consequences of early iron deficiency
Georgieff, M. (2011) · Nutrition Reviews · doi:10.1111/j.1753-4887.2011.00432.x · Cited by 303 · see citing works
Lukowski, A. F., Koss, M., Burden, M. J., Jonides, J., Nelson, C. A., Kaciroti, N., Jiménez, E., & Lozoff, B. (2010) · Nutritional Neuroscience · doi:10.1179/147683010x12611460763689 · Cited by 303 · see citing works
Nold, J. L., & Georgieff, M. (2004) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2004.01.003 · Cited by 299 · see citing works
Early Iron Deficiency Has Brain and Behavior Effects Consistent with Dopaminergic Dysfunction1–3
Lozoff, B. (2011) · Journal of Nutrition · doi:10.3945/jn.110.131169 · Cited by 260 · see citing works
Perinatal Iron Deficiency Alters the Neurochemical Profile of the Developing Rat Hippocampus
Rao, R., Tkáč, I., Townsend, E. L., Rolf Gruetter, A., & Georgieff, M. (2003) · Journal of Nutrition · doi:10.1093/jn/133.10.3215 · Cited by 252 · see citing works
Brain iron metabolism and its perturbation in neurological diseases
Crichton, R. R., Dexter, D. T., & Ward, R. J. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0470-z · Cited by 246 · see citing works
The Metabolism of Neuronal Iron and Its Pathogenic Role in Neurological Disease: Review
Moos, T., & Morgan, E. H. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1306.002 · Cited by 234 · see citing works
The Benefits and Risks of Iron Supplementation in Pregnancy and Childhood
Georgieff, M., Krebs, N. F., & Cusick, S. E. (2019) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-082018-124213 · Cited by 215 · see citing works
Pre- and postweaning iron deficiency alters myelination in Sprague-Dawley rats
Beard, J. L., Wiesinger, J. A., & Connor, J. R. (2003) · Developmental Neuroscience · doi:10.1159/000073507 · Cited by 200 · see citing works
Self-citationIron Homeostasis in the Neonate
Collard, K. J. (2009) · PEDIATRICS · doi:10.1542/peds.2008-1047 · Cited by 182 · see citing works
Brain Iron Metabolism Dysfunction in Parkinson’s Disease
Jiang, H. F., Wang, J., Rogers, J. T., & Xie, J. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-9879-1 · Cited by 184 · see citing works
Serum Iron Levels and the Risk of Parkinson Disease: A Mendelian Randomization Study
Pichler, I., Del Greco M., F., Gögele, M., Lill, C. M., Bertram, L., Do, C. B., Eriksson, N., Foroud, T., Myers, R. H., PD GWAS Consortium, et al. (2013) · PLoS Medicine · doi:10.1371/journal.pmed.1001462 · Cited by 173 · see citing works
“Low peripheral iron levels may reduce the functioning of neuronal enzymes or receptors, since iron is a crucial cofactor of tyrosine hydroxylase [49], plays a role in the synthesis of monoamine neurotransmitters, and is involved in dopaminergic neurodevelopment [50].”
BackgroundRecent Evidence from Human and Animal Studies Regarding Iron Status and Infant Development
Beard, J. (2007) · Journal of Nutrition · doi:10.1093/jn/137.2.524s · Cited by 164 · see citing works
Self-citationIron in neuronal function and dysfunction
Salvador, G. A. (2010) · BioFactors · doi:10.1002/biof.80 · Cited by 154 · see citing works
Parkinson's disease: Alterations in iron and redox biology as a key to unlock therapeutic strategies
Ma, L., Azad, M. G., Dharmasivam, M., Richardson, V., Quinn, R. J., Feng, Y., Pountney, D. L., Tonissen, K. F., Mellick, G. D., Yanatori, I., et al. (2021) · Redox Biology · doi:10.1016/j.redox.2021.101896 · Cited by 148 · see citing works
Iron deficiency: Differential effects on monoamine transporters
Burhans, M. S., Dailey, C., Beard, Z., Wiesinger, J. A., Murray‐Kolb, L. E., Jones, B. C., & Beard, J. L. (2005) · Nutritional Neuroscience · doi:10.1080/10284150500047070 · Cited by 143 · see citing works
Self-citationIron, the substantia nigra and related neurological disorders
Snyder, A. M., & Connor, J. R. (2008) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.08.005 · Cited by 137 · see citing works
Care of the Infant of the Diabetic Mother
Hay, W. W. (2011) · Current Diabetes Reports · doi:10.1007/s11892-011-0243-6 · Cited by 136 · see citing works
Iron‐deficiency anemia in infancy and poorer cognitive inhibitory control at age 10 years
Algarín, C. R., Nelson, C. A., Peirano, P. D., Westerlund, A., Reyes, S., & Lozoff, B. (2013) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.12118 · Cited by 132 · see citing works
Tran, P. V., Fretham, S. J. B., Carlson, E. S., & Georgieff, M. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e31819d90a1 · Cited by 128 · see citing works
Neurotoxicants, Micronutrients, and Social Environments
Hubbs‐Tait, L., Nation, J. R., Krebs, N. F., & Bellinger, D. C. (2005) · Gothic.net · doi:10.1111/j.1529-1006.2005.00024.x · Cited by 125 · see citing works
New Evidence of Iron and Zinc Interplay at the Enterocyte and Neural Tissues
Kordas, K., & Stoltzfus, R. J. (2004) · Journal of Nutrition · doi:10.1093/jn/134.6.1295 · Cited by 110 · see citing works
Dietary Factors in the Etiology of Parkinson’s Disease
Ağım, Z. S., & Cannon, J. R. (2015) · BioMed Research International · doi:10.1155/2015/672838 · Cited by 107 · see citing works
Iron Status and Neurobehavioral Development of Premature Infants
Armony-Sivan, R., Eidelman, A. I., Lanir, A., Sredni, D., & Yehuda, S. (2004) · Journal of Perinatology · doi:10.1038/sj.jp.7211178 · Cited by 105 · see citing works
Tran, P. V., Carlson, E. S., Fretham, S. J. B., & Georgieff, M. (2008) · Journal of Nutrition · doi:10.3945/jn.108.091553 · Cited by 101 · see citing works
Iron Metabolism and Brain Development in Premature Infants
Wang, Y., Wu, Y., Li, T., Wang, X., & Zhu, C. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00463 · Cited by 98 · see citing works
Early Iron Deficiency Alters Sensorimotor Development and Brain Monoamines in Rats1
Unger, E. L., Paul, T., Murray-Kolb, L. E., Felt, B., Jones, B. C., & Beard, J. L. (2007) · The Journal of Nutrition · doi:10.1093/jn/137.1.118 · Cited by 97 · see citing works
Self-citationBehavioral consequences of developmental iron deficiency in infant rhesus monkeys
Golub, M. S., Hogrefe, C. E., Germann, S. L., Capitanio, J. P., & Lozoff, B. (2005) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2005.10.005 · Cited by 90 · see citing works
The effect of childhood malnutrition on externalizing behavior
Liu, J., & Raine, A. (2006) · Current Opinion in Pediatrics · doi:10.1097/01.mop.0000245360.13949.91 · Cited by 90 · see citing works
Fetal iron deficiency induces chromatin remodeling at the Bdnf locus in adult rat hippocampus
Tran, P. V., Kennedy, B. C., Lien, Y., Simmons, R. A., & Georgieff, M. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00429.2014 · Cited by 89 · see citing works
Anemia or low hemoglobin levels preceding Parkinson disease: A case-control study
Savica, R., Grossardt, B. R., Carlin, J. M., Icen, M., Bower, J. H., Ahlskog, J. E., Maraganore, D. M., Steensma, D. P., & Rocca, W. A. (2009) · Neurology · doi:10.1212/wnl.0b013e3181bd80c1 · Cited by 87 · see citing works
Tran, P. V., Kennedy, B. C., Pisansky, M. T., Won, K., Gewirtz, J. C., Simmons, R. A., & Georgieff, M. (2016) · Journal of Nutrition · doi:10.3945/jn.115.227561 · Cited by 83 · see citing works
Unger, E. L., Hurst, A., Georgieff, M., Schallert, T., Rao, R., Connor, J. R., Kaciroti, N., Lozoff, B., & Felt, B. T. (2012) · Journal of Nutrition · doi:10.3945/jn.112.162198 · Cited by 83 · see citing works
Impairment of emotional behavior and spatial learning in adult Wistar rats by ferrous sulfate
Maâroufi, K., Ammari, M., Jeljeli, M., Roy, V., Sakly, M., & Abdelmelek, H. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.10.019 · Cited by 82 · see citing works
Schmidt, A., Waldow, K. J., Grove, W. M., Salinas, J. A., & Georgieff, M. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.3.475 · Cited by 80 · see citing works
Trace metal regulation of neuronal apoptosis: From genes to behavior
Levenson, C. W. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.010 · Cited by 77 · see citing works
Effect of perinatal iron deficiency on myelination and associated behaviors in rat pups
WU, L. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.003 · Cited by 77 · see citing works
Iron Deficiency: Beyond Anemia
Yadav, D. K., & Chandra, J. (2010) · The Indian Journal of Pediatrics · doi:10.1007/s12098-010-0129-7 · Cited by 76 · see citing works
Iron and ageing: an introduction to iron regulatory mechanisms
Levenson, C. W., & Tassabehji, N. M. (2004) · Ageing Research Reviews · doi:10.1016/j.arr.2004.03.001 · Cited by 74 · see citing works
Unger, E. L., Wiesinger, J. A., Hao, L., & Beard, J. L. (2008) · Journal of Nutrition · doi:10.3945/jn.108.095224 · Cited by 73 · see citing works
Self-citationCeruloplasmin in neurodegenerative diseases
Texel, S. J., Xu, X., & Harris, Z. L. (2008) · Biochemical Society Transactions · doi:10.1042/bst0361277 · Cited by 73 · see citing works
Early Postnatal Iron Repletion Overcomes Lasting Effects of Gestational Iron Deficiency in Rats1
Beard, J. L., Unger, E. L., Bianco, L. E., Paul, T., Rundle, S. E., & Jones, B. C. (2007) · Journal of Nutrition · doi:10.1093/jn/137.5.1176 · Cited by 71 · see citing works
Self-citationRole of dietary iron restriction in a mouse model of Parkinson's disease
Levenson, C. W., Cutler, R. G., Ladenheim, B., Cadet, J. L., Hare, J., & Mattson, M. P. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.08.014 · Cited by 64 · see citing works
Hephaestin and Ceruloplasmin Play Distinct but Interrelated Roles in Iron Homeostasis in Mouse Brain
Jiang, R., Hua, C., Wan, Y., Jiang, B., Hu, H., Zheng, J., Fuqua, B. K., Dunaief, J. L., Anderson, G. J., David, S., et al. (2015) · Journal of Nutrition · doi:10.3945/jn.114.207316 · Cited by 60 · see citing works
Iron deficiency with or without anemia impairs prepulse inhibition of the startle reflex
Pisansky, M. T., Wickham, R. J., Su, J., Fretham, S. J. B., Yuan, L., Sun, M., Gewirtz, J. C., & Georgieff, M. (2013) · Hippocampus · doi:10.1002/hipo.22151 · Cited by 59 · see citing works
Polańska, K., Hanke, W., Król, A. I., Gromadzińska, J., Kuraś, R., Janasik, B., Wąsowicz, W., Mirabella, F., Chiarotti, F., & Calamandrei, G. (2017) · Environmental Research · doi:10.1016/j.envres.2017.06.037 · Cited by 56 · see citing works
Abnormal Motor Function Persists Following Recovery from Perinatal Copper Deficiency in Rats
Penland, J. G., & Prohaska, J. R. (2004) · Journal of Nutrition · doi:10.1093/jn/134.8.1984 · Cited by 55 · see citing works
How do established developmental risk-factors for schizophrenia change the way the brain develops?
Eyles, D. W. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01273-2 · Cited by 55 · see citing works
Choudhury, V., Amin, S. B., Agarwal, A., Lm, S., Soni, A., & Saluja, S. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.113084 · Cited by 54 · see citing works
Effects of nanoparticle zinc oxide on emotional behavior and trace elements homeostasis in rat brain
Amara, S., Slama, I. B., Omri, K., Ghoul, J. M. E., Mir, L. E., Rhouma, K. B., Abdelmelek, H., & Sakly, M. (2013) · Toxicology and Industrial Health · doi:10.1177/0748233713491802 · Cited by 53 · see citing works
Carlson, E. S., Fretham, S. J. B., Unger, E. L., O’Connor, M. B., Petryk, A., Schallert, T. J., Rao, R., Tkáč, I., & Georgieff, M. (2010) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-010-9049-0 · Cited by 50 · see citing works
Deng, Q.-Y., Zhou, X., Chen, J., Pan, M.-Q., Gao, H., Zhou, J., Wang, D.-M., Chen, Q., Zhang, X.-M., Wang, Q., et al. (2017) · Brain Research · doi:10.1016/j.brainres.2016.11.007 · Cited by 48 · see citing works
Iron as a model nutrient for understanding the nutritional origins of neuropsychiatric disease
Barks, A. K., Hall, A. M., Tran, P. V., & Georgieff, M. (2018) · Pediatric Research · doi:10.1038/s41390-018-0204-8 · Cited by 47 · see citing works
Bourque, S. L., Iqbal, U. H., Reynolds, J. N., Adams, M. A., & Nakatsu, K. (2008) · Journal of Nutrition · doi:10.1093/jn/138.5.931 · Cited by 49 · see citing works
Iron Deprivation during Fetal Development Changes the Behavior of Juvenile Rhesus Monkeys2
Golub, M. S., Hogrefe, C. E., & Germann, S. L. (2007) · Journal of Nutrition · doi:10.1093/jn/137.4.979 · Cited by 48 · see citing works
Li, Y., Kim, J., Buckett, P. D., Bhlke, M., Maher, T. J., & Wessling‐Resnick, M. (2011) · Journal of Nutrition · doi:10.3945/jn.111.145946 · Cited by 47 · see citing works
Quantitative Genetic Analysis of Ventral Midbrain and Liver Iron in BXD Recombinant Inbred Mice
Jones, B. C., Reed, C. L., HITZEMANN, R. J., Wiesinger, J. A., Mccarthy, K., Buwen, J. P., & Beard, J. L. (2003) · Nutritional Neuroscience · doi:10.1080/10284150310001624192 · Cited by 46 · see citing works
Self-citationCorrection: Serum Iron Levels and the Risk of Parkinson Disease: A Mendelian Randomization Study
Pichler, I., Fabiola Del Greco, M., Gögele, M., Lill, C. M., Bertram, L., Do, C. B., Eriksson, N., Foroud, T., Myers, R. H., Nalls, M. A., et al. (2013) · PLoS Medicine · doi:10.1371/annotation/c4d81646-0c0e-4a3e-9425-b220bae2d8b6 · Cited by 46 · see citing works
Dysregulated iron metabolism in the choroid plexus in fragile X-associated tremor/ataxia syndrome
Ariza, J., Steward, C., Rueckert, F., Widdison, M., Coffman, R. E., Afjei, A., Noctor, S. C., Hagerman, R. J., Hagerman, P. J., & Martínez-Cerdeño, V. (2014) · Brain Research · doi:10.1016/j.brainres.2014.11.058 · Cited by 44 · see citing works
Manganese efflux in Parkinsonism: Insights from newly characterized SLC30A10 mutations
DeWitt, M. R., Chen, P., & Aschner, M. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.01.058 · Cited by 43 · see citing works
Associations between Blood Zinc Concentrations and Sleep Quality in Childhood: A Cohort Study
Ji, X., & Liu, J. (2015) · Nutrients · doi:10.3390/nu7075247 · Cited by 43 · see citing works
Калашников, В. В., Zajcev, A. M., Атрощенко, М. М., Miroshnikov, S. A., Frolov, A. N., Zavyalov, O. A., Калинкова, Л. В., & Калашникова, Т. В. (2018) · Environmental Science and Pollution Research · doi:10.1007/s11356-018-2334-2 · Cited by 42 · see citing works
Reichel, C. M., Wacan, J. J., Farley, C. M., Stanley, B. J., Crawford, C. A., & McDougall, S. A. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.02.002 · Cited by 42 · see citing works
Age-dependent effects of gestational and lactational iron deficiency on anxiety behavior in rats
Eseh, R., & Zimmerberg, B. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.019 · Cited by 39 · see citing works
Iron accumulation and dysregulation in the putamen in fragile X‐associated tremor/ataxia syndrome
Ariza, J., Rogers, H., Hartvigsen, A., Snell, M., Dill, M., Judd, D., Hagerman, P. J., & Martínez‐Cerdeño, V. (2017) · Movement Disorders · doi:10.1002/mds.26902 · Cited by 38 · see citing works
Wiesinger, J. A., Buwen, J. P., Cifelli, C. J., Unger, E. L., Jones, B. C., & Beard, J. L. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04175.x · Cited by 38 · see citing works
Self-citationGeorgieff, M., Tran, P. V., & Carlson, E. S. (2018) · Development and Psychopathology · doi:10.1017/s0954579418000500 · Cited by 37 · see citing works
Degremont, A., Jain, R., Philippou, E., & Latunde-Dada, G. O. (2020) · Nutrition Reviews · doi:10.1093/nutrit/nuaa065 · Cited by 36 · see citing works
Working memory impairment and recovery in iron deficient children
Otero, G., Pliego-Rivero, F. B., Porcayo, R., & Alcántara, G. G. M. (2008) · Clinical Neurophysiology · doi:10.1016/j.clinph.2008.04.015 · Cited by 35 · see citing works
Akathisia and Restless Legs Syndrome
Ferré, S., Guitart, X., Quiroz, C., Rea, W. P., García-Malo, C., Garcı́a-Borreguero, D., Allen, R. P., & Earley, C. J. (2021) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2021.02.012 · Cited by 34 · see citing works
Fetal iron deficiency alters the proteome of adult rat hippocampal synaptosomes
Tran, P. V., Dakoji, S., Reise, K., Storey, K. K., & Georgieff, M. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00292.2013 · Cited by 33 · see citing works
Patton, S. M., Coe, C. L., Lubach, G. R., & Connor, J. R. (2012) · Developmental Neuroscience · doi:10.1159/000341919 · Cited by 33 · see citing works
Xu, E., Chen, M., Zheng, J., Maimaitiming, Z., Zhong, T., & Chen, H. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.07.134 · Cited by 32 · see citing works
Burhans, M. S., Dailey, C., Wiesinger, J. A., Murray‐Kolb, L. E., Jones, B. C., & Beard, J. L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.02.014 · Cited by 31 · see citing works
Self-citationChanging iron content of the mouse brain during development
Holmes‐Hampton, G. P., Chakrabarti, M., Cockrell, A. L., McCormick, S. P., Abbott, L. C., Lindahl, L. S., & Lindahl, P. A. (2012) · Metallomics · doi:10.1039/c2mt20086d · Cited by 31 · see citing works
Han, M., Chang, J., & Kim, J. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13717 · Cited by 31 · see citing works
Iron supplementation brings up a lacking P300 in iron deficient children
Otero, G., Pliego-Rivero, F. B., Contreras, G., Ricardo, J., & Fernández, T. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.05.008 · Cited by 29 · see citing works
Effect of Mineral and Bone Metabolism on Restless Legs Syndrome in Hemodialysis Patients
Neves, P. D. M. D. M., Graciolli, F. G., Oliveira, I. B., Bridi, R. A., Moysés, R. M. A., & Elias, R. M. (2017) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.6396 · Cited by 28 · see citing works
Harvey, L., & Boksa, P. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.09.009 · Cited by 27 · see citing works
Methylphenidate improves cognitive deficits produced by infantile iron deficiency in rats
Mohamed, W. M. Y., Unger, E. L., Kambhampati, S., & Jones, B. C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.07.025 · Cited by 24 · see citing works
Self-citationBrain iron metabolism and its perturbation in neurological diseases
Crichton, R. R., Dexter, D. T., & Ward, R. J. (2011) · Monatshefte für Chemie - Chemical Monthly · doi:10.1007/s00706-011-0472-z · Cited by 23 · see citing works
Brain iron metabolism and its perturbation in neurological diseases
Crichton, R. R., Dexter, D. T., & Ward, R. J. (2012) · Springer eBooks · doi:10.1007/978-3-7091-1001-0_1 · Cited by 22 · see citing works
Wainwright, P. E., Lomanowska, A. M., McCutcheon, D., Park, E. J., Clandinin, M. T., & Ramanujam, K. S. (2007) · Nutritional Neuroscience · doi:10.1080/10284150701284035 · Cited by 22 · see citing works
An Overview of Iron in Term Breast-Fed Infants
Qasem, W. A., & Friel, J. K. (2015) · Clinical Medicine Insights Pediatrics · doi:10.4137/cmped.s26572 · Cited by 22 · see citing works
Long-Term Brain and Behavioral Consequences of Early-Life Iron Deficiency
Kennedy, B. C., Wallin, D. J., Tran, P. V., & Georgieff, M. (2016) · Springer eBooks · doi:10.1007/978-3-319-22023-9_15 · Cited by 21 · see citing works
Dietary iron absorption during early postnatal life
Helman, S. L., Anderson, G. J., & Frazer, D. M. (2019) · BioMetals · doi:10.1007/s10534-019-00181-9 · Cited by 21 · see citing works
Perinatal iron deficiency as an early risk factor for schizophrenia
Maxwell, A. M., & Rao, R. (2021) · Nutritional Neuroscience · doi:10.1080/1028415x.2021.1943996 · Cited by 20 · see citing works
Iron Injection Restores Brain Iron and Hemoglobin Deficits in Perinatal Copper-Deficient Rats
Pyatskowit, J. W., & Prohaska, J. R. (2008) · Journal of Nutrition · doi:10.1093/jn/138.10.1880 · Cited by 20 · see citing works
McEchron, M. D., Alexander, D. N., Gilmartin, M. R., & Paronish, M. D. (2007) · Developmental Neuroscience · doi:10.1159/000110502 · Cited by 19 · see citing works
A review of the auditory-gut-brain axis
Graham, A. S., Ben‐Azu, B., Tremblay, M., Torre, P., Senekal, M., Laughton, B., van der Kouwe, A. J. W., Jankiewicz, M., Kaba, M., & Holmes, M. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1183694 · Cited by 28 · see citing works
- Authors
- Beard, J., Erikson, K. M., & Jones, B. C.
- Affiliations
- Wake Forest University (US)
- Wake Forest University Health Sciences (US)
- Pennsylvania State University (US)
- Corresponding author
- Beard, John
- Venue
- The Journal of Nutrition
- Publisher
- Elsevier BV
- Published
- 2003-04
- Volume
- 133
- Issue
- 4
- Pages
- 1174-1179
- ISSN
- 0022-3166 (ISSN-L)
- OpenAlex
- W1933823002
- Cited by
- 172
- References
- 32
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 9 · 2023: 4 · 2022: 1 · 2021: 7 · 2020: 3 · 2019: 8 · 2018: 8 · 2017: 7 · 2016: 9 · 2015: 8 · 2014: 6 · 2013: 13 · 2012: 7
- FWCI
- 4.13
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- neonatal iron deficiency, dopaminergic activity, dopamine transporter, dopamine D2 receptor, dopamine D1 receptor, iron repletion, nucleus accumbens, striatum, prefrontal cortex, ventral midbrain, cross-fostering, iron-deficient diet, monoamine metabolism, critical developmental periods
- MeSH terms
- Iron Deficiencies, Animals, Animals, Newborn, Behavior, Animal, Dopamine, Female, Ligands, Male, Membrane Glycoproteins, Nerve Tissue Proteins, Protein Binding, Rats, Sprague-Dawley, Receptors, Dopamine D1, Receptors, Dopamine D2, Membrane Transport Proteins, Dopamine Plasma Membrane Transport Proteins, Rats
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