Gestational and lactational iron deficiency alters the developing striatal metabolome and associated behaviors in young rats

Journal of Nutrition

Volumn 137, Issue 4, 2007, Pages 1043-1049

  Ward, Kay L ^a   Tkac, Ivan ^a,b   Jing, Yuezhou ^c   Felt, Barbara ^c   Beard, John ^d   Connor, James ^e   Schallert, Timothy ^f   Georgieff, Michael K ^a,b   Rao, Raghavendra ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^f UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; GLYCEROPHOSPHORYLCHOLINE; INOSITOL; N ACETYLASPARTIC ACID; PHOSPHORYLCHOLINE;

ANEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BODY WEIGHT; BRAIN WEIGHT; CHIN; CONTROLLED STUDY; CORPUS STRIATUM; ENERGY METABOLISM; FEMALE; FORELIMB; GESTATION PERIOD; GLIA CELL; HEMATOCRIT; IRON DEFICIENCY; LACTATION; MALE; METABOLITE; METABOLOMICS; MYELINATION; NEUROTRANSMISSION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERINATAL PERIOD; RAT; VIBRISSA;

RATTUS;

EID: 34247102590     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/137.4.1043     Document Type: Article

References (59)

1. World Health Organization.. Iron deficiency anemia: assessment, prevention and control: a guide for program managers. Geneva: World Health Organization; 2001. Available from: http://whqlibdoc.who.int/hq/2001/WHO_NHD_01. 3.pdf
2. Georgieff MK, Mills MM, Gordon K, Wobken JD. Reduced neonatal liver iron concentrations after uteroplacental insufficiency. J Pediatr. 1995;127:308-11.
3. Petry CD, Eaton MA, Wobken JD, Mills MM, Johnson DE, Georgieff MK. Iron deficiency of liver, heart, and brain in newborn infants of diabetic mothers. J Pediatr. 1992;121:109-14.
4. Walter T, De Andrac I, Chadud P, Perales CG. Iron deficiency anemia: adverse effects on infant psychomotor development. Pediatrics. 1989;84:7-17.
5. Pollitt E, Hathirat P, Kotchabhakdi NJ, Missell L, Valyasevi A. Iron deficiency and educational achievement in Thailand. Am J Clin Nutr. 1989;50:687-96.
6. Lozoff B, Jimenez E, Wolf AW. Long-term developmental outcome of infants with iron deficiency. N Engl J Med. 1991;325:687-94.
7. Grantham-McGregor S, Ani C. A review of studies on the effect of iron deficiency on cognitive development in children. J Nutr. 2001;131:649S-66S.
8. Lozoff B, Jimenez E, Hagen J, Mollen E, Wolf AW. Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics. 2000;105:E51.
9. Youdim MB, Yehuda S. The neurochemical basis of cognitive deficits induced by brain iron deficiency: involvement of dopamine-opiate system. Cell Mol Biol. 2000;46:491-500.
10. Lozoff B, Brittenham G, Viteri FE, Urrutia JJ. Behavioral abnormalities in infants with iron deficiency anemia. In: Pollitt E, Leibel RL, editors. Iron deficiency: brain biochemistry and behavior. New York: Raven Press; 1982. p. 183-193.
11. Lozoff B, Wolf AW, Jimenez E. Iron-deficiency anemia and infant development: effects of extended oral iron therapy. J Pediatr. 1996;129:382-9.
12. Beard JL, Felt B, Schallert T, Burhans M, Connor JR, Georgieff MK. Moderate iron deficiency in infancy: biology and behavior in young rats. Behav Brain Res. 2006;170:224-32.
13. Felt BT, Beard JL, Schallert T, Shao J, Aldridge JW, Connor JR, Georgieff M, Lozoff B. Persistent neurochemical and behavioral abnormalities in adulthood despite early iron supplementation for perinatal iron deficiency anemia in rats. Behav Brain Res. 2006;171:261-70.
14. Connor JR, Menzies SL. Altered cellular distribution of iron in the central nervous system of myelin deficient rats. Neuroscience. 1990;34:265-71.
15. deUngria M, Rao R, Wobken JD, Luciana M, Nelson CA, Georgieff MK. Perinatal iron deficiency decreases cytochrome c oxidase (CytOx) activity in selected regions of neonatal rat brain. Pediatr Res. 2000;48:169-76.
16. Rao R, Tkac I, Townsend EL, Gruetter R, Georgieff MK. Perinatal iron deficiency alters the neurochemical profile of the developing rat hippocampus. J Nutr. 2003;133:3215-21.
17. Raman L, Tkac I, Ennis K, Georgieff MK, Gruetter R, Rao R. In vivo effects of chronic hypoxia on the neurochemical profile of the developing rat hippocampus. Dev Brain Res. 2005;156:202-9.
18. Schallert T, Petrie BF, Whishaw IQ. Neonatal dopamine depletion: spared and unspared sensorimotor and attentional disorders and effects of further depletion in adulthood. Psychobiology. 1989;17:386-96.
19. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology. 2000;39:777-87.
20. Felt BT, Lozoff B. Brain iron and behavior of rats are not normalized by treatment of iron deficiency anemia during early development. J Nutr. 1996;126:693-701.
21. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med. 1993;29:804-11.
22. Tkac I, Starcuk Z, Choi IY, Gruetter R. In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med. 1999;41:649-56.
23. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993;30:672-9.
24. Rao R, de Ungria M, Sullivan D, Wu P, Wobken JD, Nelson CA. Perinatal brain iron deficiency increases the vulnerability of rat hippocampus to hypoxic ischemic insult. J Nutr. 1999;129:199-206.
25. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42:121-30.
26. Hua Y, Schallert T, Keep RF, Wu J, Hoff JT, Xi G. Behavioral tests after intracerebral hemorrhage in the rat. Stroke. 2002;33:2478-84.
27. Woodlee MT, Asseo-Garcia AM, Zhao X, Liu SJ, Jones TA, Schallert T. Testing forelimb placing "across the midline" reveals distinct, lesion-dependent patterns of recovery in rats. Exp Neurol. 2005;191:310-7.
28. Aldridge JW, Berridge KC. Coding of serial order by neostriatal neurons: a ''natural action'' approach to movement sequence. J Neurosci. 1998;18:2777-87.
29. Schallert T, Upchurch M, Lobaugh N, Farrar SB, Spirduso WW, Gilliam P, Vaughn D, Wilcox RE. Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav. 1982;16:455-62.
30. Dallman PR. Biochemical basis for the manifestations of iron deficiency. Annu Rev Nutr. 1986;6:13-40.
31. Erecinska M, Silver IA. ATP and brain function. J Cereb Blood Flow Metab. 1989;9:2-19.
32. Plaschke K, Yun SW, Martin E, Hoyer S, Bardenheuer HJ. Interrelation between cerebral energy metabolism and behaviour in a rat model of permanent brain vessel occlusion. Brain Res. 1999;830:320-9.
33. Tarnopolsky MA, Beal MF. Potential for creatine and other therapies targeting cellular energy dysfunction in neurological disorders. Ann Neurol. 2001;49:561-74.
34. Wallimann T, Dolder M, Schlattner U, Eder M, Hornemann T, O'Gorman E, Ruck A, Brdiczka D. Some new aspects of creatine kinase (CK): compartmentation, structure, function and regulation for cellular and mitochondrial bioenergetics and physiology. Biofactors. 1998;8:229-34.
35. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab. 2001;21:1133-45.
36. 13C NMR studies of compartmentalized cerebral carbohydrate metabolism. Neurochem Int. 2002;41:143-54.
37. Takahashi M, Billups B, Rossi D, Sarantis M, Hamann M, Attwell D. The role of glutamate transporters in glutamate homeostasis in the brain. J Exp Biol. 1997;200:401-9.
38. Lovinger DM, Partridge JG, Tang KC. Plastic control of striatal glutamatergic transmission by ensemble actions of several neurotransmitters and targets for drugs of abuse. Ann N Y Acad Sci. 2003;1003:226-40.
39. Ill AM, Mitchell TR, Neely EB, Connor JR. Metabolic analysis of mouse brains that have compromised iron storage. Metab Brain Dis. 2006;21:77-87.
40. Bluml S, Seymour KJ, Ross BD. Developmental changes in choline- and ethanolamine-containing compounds measured with proton-decoupled (31) P MRS in in vivo human brain. Magn Reson Med. 1999;42:643-54.
41. Brand A, Richter-Landsberg C, Leibfritz D. Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci. 1993;15:289-98.
42. Burri R, Steffen C, Herschkowitz N. N-acetyl-L-aspartate is a major source of acetyl groups for lipid synthesis during rat brain development. Dev Neurosci. 1991;13:403-11.
43. Catani M, Mecocci P, Tarducci R, Howard R, Pelliccioli GP, Mariani E, Metastasio A, Benedetti C, Senin U, Cherubini A. Proton magnetic resonance spectroscopy reveals similar white matter biochemical changes in patients with chronic hypertension and early Alzheimer's disease. J Am Geriatr Soc. 2002;50:1707-10.
44. Chakraborty G, Mekala P, Yahya D, Wu G, Ledeen RW. Intraneuronal N-acetylaspartate supplies acetyl groups for myelin lipid synthesis: evidence for myelin-associated aspartoacylase. J Neurochem. 2001;78:736-45.
45. Fisher SK, Novak JE, Agranoff BW. Inositol and higher inositol phosphates in neural tissues: homeostasis, metabolism and functional significance. J Neurochem. 2002;82:736-54.
46. Shonk TK, Moats RA, Gifford P, Michaelis T, Mandigo JC, Izumi J, Ross BD. Probable Alzheimer disease: diagnosis with proton MR spectroscopy. Radiology. 1995;195:65-72.
47. Yu GS, Steinkirchner TM, Rao GA, Larkin EC. Effect of prenatal iron deficiency on myelination in rat pups. Am J Pathol. 1986;125:620-4.
48. Connor JR, Benkovic SA. Iron regulation in the brain: histochemical, biochemical, and molecular considerations. Ann Neurol. 1992;32:Suppl:S51-61.
49. Ortiz E, Pasquini JM, Thompson K, Felt B, Butkus G, Beard J, Connor JR. Effect of manipulation of iron storage, transport, or availability on myelin composition and brain iron content in three different animal models. J Neurosci Res. 2004;77:681-9.
50. Roncagliolo M, Garrido M, Walter T, Peirano P, Lozoff B. Evidence of altered central nervous system development in infants with iron deficiency anemia at 6 mo: delayed maturation of auditory brainstem responses. Am J Clin Nutr. 1998;68:683-90.
51. DeRegnier RA, Nelson CA, Thomas KM, Wewerka S, Georgieff MK. Neurophysiologic evaluation of auditory recognition memory in healthy newborn infants and infants of diabetic mothers. J Pediatr. 2000;137:777-84.
52. Morris CM, Candy JM, Oakley AE, Bloxham CA, Edwardson JA. Histochemical distribution of non-haem iron in the human brain. Acta Anat (Basel). 1992;144:235-57.
53. Exposito I, Del Arco A, Segovia G, Mora F. Endogenous dopamine increases extracellular concentrations of glutamate and GABA in striatum of the freely moving rat: involvement of D1 and D2 dopamine receptors. Neurochem Res. 1999;24:849-56.
54. Lin JY, Dubey R, Funk GD, Lipski J. Receptor subtype-specific modulation by dopamine of glutamatergic responses in striatal medium spiny neurons. Brain Res. 2003;959:251-62.
55. Lisman JE, Grace AA. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron. 2005;46:703-13.
56. O'Donnell P. Dopamine gating of forebrain neural ensembles. Eur J Neurosci. 2003;17:429-35.
57. Sesack SR, Carr DB, Omelchenko N, Pinto A. Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann N Y Acad Sci. 2003;1003:36-52.
58. West AR, Floresco SB, Charara A, Rosenkranz JA, Grace AA. Electrophysiological interactions between striatal glutamatergic and dopaminergic systems. Ann N Y Acad Sci. 2003;1003:53-74.
59. Jorgenson LA, Sun M, O'Connor M, Georgieff MK. Fetal iron deficiency disrupts the maturation of synaptic function and efficacy in area CA1 of the developing rat hippocampus. Hippocampus. 2005;15:1094-102.