Prevalent iron metabolism gene variants associated with increased brain ferritin iron in healthy older men.

Prevalent gene variants involved in iron metabolism [hemochromatosis (HFE) H63D and transferrin C2 (TfC2)] have been associated with higher risk and earlier age at onset of Alzheimer's disease (AD), especially in men. Brain iron increases with age, is higher in men, and is abnormally elevated in several neurodegenerative diseases, including AD and Parkinson's disease, where it has been reported to contribute to younger age at onset in men. The effects of the common genetic variants (HFE H63D and/or TfC2) on brain iron were studied across eight brain regions (caudate, putamen, globus pallidus, thalamus, hippocampus, white matter of frontal lobe, genu, and splenium of corpus callosum) in 66 healthy adults (35 men, 31 women) aged 55 to 76. The iron content of ferritin molecules (ferritin iron) in the brain was measured with MRI utilizing the Field Dependent Relaxation Rate Increase (FDRI) method. 47% of the sample carried neither genetic variant (IRON-) and 53% carried one and/or the other (IRON+). IRON+ men had significantly higher FDRI compared to IRON- men (p=0.013). This genotype effect was not observed in women who, as expected, had lower FDRI than men. This is the first published evidence that these highly prevalent genetic variants in iron metabolism genes can influence brain iron levels in men. Clinical phenomena such as differential gender-associated risks of developing neurodegenerative diseases and age at onset may be associated with interactions between iron genes and brain iron accumulation. Clarifying mechanisms of brain iron accumulation may help identify novel interventions for age-related neurodegenerative diseases.

[1]  W H Oldendorf,et al.  Field dependent transverse relaxation rate increase may be a specific measure of tissue iron stores , 1993, Magnetic resonance in medicine.

[2]  C. Ross,et al.  Single Particle Characterization of Iron-induced Pore-forming α-Synuclein Oligomers* , 2008, Journal of Biological Chemistry.

[3]  Ashley I. Bush,et al.  Therapeutics for Alzheimer’s disease based on the metal hypothesis , 2008, Neurotherapeutics.

[4]  J. Connor,et al.  Increased incidence of the Hfe mutation in amyotrophic lateral sclerosis and related cellular consequences , 2004, Journal of the Neurological Sciences.

[5]  R B D'Agostino,et al.  Aspirin intake and the use of serum ferritin as a measure of iron status. , 2001, The American journal of clinical nutrition.

[6]  C. Batich,et al.  In situ characterization and mapping of iron compounds in Alzheimer's disease tissue. , 2005, Journal of Alzheimer's disease : JAD.

[7]  B. Todorich,et al.  Oligodendrocytes and myelination: The role of iron , 2009, Glia.

[8]  Neena Singh,et al.  Abnormal Brain Iron Homeostasis in Human and Animal Prion Disorders , 2009, PLoS pathogens.

[9]  A. Hofman,et al.  Mutations in the hemochromatosis gene (HFE), Parkinson's disease and parkinsonism , 2003, Neuroscience Letters.

[10]  Bastiaan R Bloem,et al.  Gender differences in Parkinson’s disease , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[11]  O. Combarros,et al.  Interaction of the H63D Mutation in the Hemochromatosis Gene with the Apolipoprotein E Epsilon 4 Allele Modulates Age at Onset of Alzheimer’s Disease , 2003, Dementia and Geriatric Cognitive Disorders.

[12]  H. Kraemer,et al.  How can we learn about developmental processes from cross-sectional studies, or can we? , 2000, The American journal of psychiatry.

[13]  P Z Marmarelis,et al.  MRI evaluation of brain iron in earlier- and later-onset Parkinson's disease and normal subjects. , 1999, Magnetic resonance imaging.

[14]  D. Commenges,et al.  Analysis of the effect of aluminum in drinking water and transferrin C2 allele on Alzheimer's disease , 2006, European journal of neurology.

[15]  J. Connor,et al.  Iron, brain ageing and neurodegenerative disorders , 2004, Nature Reviews Neuroscience.

[16]  D. Kell Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases , 2008, BMC Medical Genomics.

[17]  Jim Mintz,et al.  Human brain myelination and amyloid beta deposition in Alzheimer’s disease , 2007, Alzheimer's & Dementia.

[18]  J. Frackowiak,et al.  Formation of amyloid-β oligomers in brain vascular smooth muscle cells transiently exposed to iron-induced oxidative stress , 2009, Acta Neuropathologica.

[19]  G. Bartzokis Alzheimer's disease as homeostatic responses to age-related myelin breakdown , 2011, Neurobiology of Aging.

[20]  Rodney A. Brooks,et al.  Magnetic resonance imaging of brain iron in health and disease , 1995, Journal of the Neurological Sciences.

[21]  M. Ynsa,et al.  A novel approach to the identification and quantitative elemental analysis of amyloid deposits--insights into the pathology of Alzheimer's disease. , 2009, Biochemical and biophysical research communications.

[22]  S. Mandel,et al.  Cell signaling pathways and iron chelation in the neurorestorative activity of green tea polyphenols: special reference to epigallocatechin gallate (EGCG). , 2008, Journal of Alzheimer's disease : JAD.

[23]  G. Bartzokis,et al.  In vivo evaluation of brain iron in Alzheimer disease using magnetic resonance imaging. , 2000, Archives of general psychiatry.

[24]  M. Muckenthaler,et al.  Iron toxicity in diseases of aging: Alzheimer's disease, Parkinson's disease and atherosclerosis. , 2009, Journal of Alzheimer's disease : JAD.

[25]  J. Connor,et al.  Iron status and neural functioning. , 2003, Annual review of nutrition.

[26]  C. Frampton,et al.  The significance of haemochromatosis gene mutations in the general population: implications for screening , 1998 .

[27]  E. Broussolle,et al.  Clinical report of three patients with hereditary hemochromatosis and movement disorders , 2000, Movement disorders : official journal of the Movement Disorder Society.

[28]  J A Frank,et al.  Hepatic hemosiderosis in non‐human primates: Quantification of liver iron using different field strengths , 1997, Magnetic resonance in medicine.

[29]  K. Heilman,et al.  Relative Frequencies of Alzheimer Disease, Lewy Body, Vascular and Frontotemporal Dementia, and Hippocampal Sclerosis in the State of Florida Brain Bank , 2002, Alzheimer disease and associated disorders.

[30]  R. Floyd,et al.  The Role of Metal Ions in Oxidative Processes and Aging , 1993, Toxicology and industrial health.

[31]  J. Wesson Ashford,et al.  ApoE genotype accounts for the vast majority of AD risk and AD pathology , 2004, Neurobiology of Aging.

[32]  R A Brooks,et al.  The quantitative Relation Between T1‐Weighted and T2‐Weighted MRI of Normal gray Matter and iron concentration , 1995, Journal of magnetic resonance imaging : JMRI.

[33]  Qing X Yang,et al.  MRI and histological analysis of beta‐amyloid plaques in both human Alzheimer's disease and APP/PS1 transgenic mice , 2009, Journal of magnetic resonance imaging : JMRI.

[34]  G. Perry,et al.  Three-dimensional tomographic imaging and characterization of iron compounds within Alzheimer's plaque core material. , 2008, Journal of Alzheimer's disease : JAD.

[35]  G. Bartzokis,et al.  MR evaluation of age-related increase of brain iron in young adult and older normal males. , 1997, Magnetic resonance imaging.

[36]  G. Orphanides,et al.  Induction of iron homeostasis genes during estrogen-induced uterine growth and differentiation , 2006, Molecular and Cellular Endocrinology.

[37]  B. Hallgren,et al.  THE EFFECT OF AGE ON THE NON‐HAEMIN IRON IN THE HUMAN BRAIN , 1958, Journal of neurochemistry.

[38]  S. Mandel,et al.  Targeting multiple Alzheimer's disease etiologies with multimodal neuroprotective and neurorestorative iron chelators , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[39]  David Katz,et al.  The relation between brain iron and NMR relaxation times: An in vitro study , 1996, Magnetic resonance in medicine.

[40]  P. Zandi,et al.  Incidence of AD may decline in the early 90s for men, later for women , 2002, Neurology.

[41]  George Perry,et al.  Increased iron and free radical generation in preclinical Alzheimer disease and mild cognitive impairment. , 2010, Journal of Alzheimer's disease : JAD.

[42]  R. Maccioni,et al.  Mild cognitive impairment and Alzheimer patients display different levels of redox-active CSF iron. , 2008, Journal of Alzheimer's disease : JAD.

[43]  J. Joshi,et al.  Ferritin: The role of aluminum in ferritin function , 1991, Neurobiology of Aging.

[44]  C. Morris,et al.  Histochemical distribution of non-haem iron in the human brain. , 1992, Acta anatomica.

[45]  廣瀬 渉 Age-associated increases in heme oxygenase-1 and ferritin immunoreactivity in the autopsied brain , 2003 .

[46]  Jim Mintz,et al.  Brain ferritin iron may influence age- and gender-related risks of neurodegeneration , 2007, Neurobiology of Aging.

[47]  G. Bartzokis,et al.  In vivo MR evaluation of age-related increases in brain iron. , 1994, AJNR. American journal of neuroradiology.

[48]  R. Hider,et al.  Iron chelation as a potential therapy for neurodegenerative disease. , 2008, Biochemical Society transactions.

[49]  L. Grummer-Strawn,et al.  Prevalence of C282Y and H63D mutations in the hemochromatosis (HFE) gene in the United States. , 2001, JAMA.

[50]  Jim Mintz,et al.  Brain ferritin iron as a risk factor for age at onset in neurodegenerative diseases , 2005, Alzheimer's & Dementia.

[51]  A. Warren,et al.  Are hereditary hemochromatosis mutations involved in Alzheimer disease? , 2000, American journal of medical genetics.

[52]  A. Thomson,et al.  Iron and the translation of the amyloid precursor protein (APP) and ferritin mRNAs: riboregulation against neural oxidative damage in Alzheimer's disease. , 2008, Biochemical Society transactions.

[53]  J. Bulte,et al.  T1 and T2 of ferritin solutions: Effect of loading factor , 1996, Magnetic resonance in medicine.

[54]  T. Montine,et al.  Association of HFE mutations with neurodegeneration and oxidative stress in Alzheimer's disease and correlation with APOE , 2003, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[55]  D. Geschwind,et al.  Altered iron metabolism is part of the choroid plexus response to peripheral inflammation. , 2009, Endocrinology.

[56]  G. Bartzokis,et al.  Increased basal ganglia iron levels in Huntington disease. , 1999, Archives of neurology.

[57]  M Worwood,et al.  Iron genes, iron load and risk of Alzheimer’s disease , 2006, Journal of Medical Genetics.

[58]  A. Hofman,et al.  HFE variants, APOE and Alzheimer's disease: Findings from the population-based Rotterdam Study , 2009, Neurobiology of Aging.

[59]  P D Griffiths,et al.  Iron in the basal ganglia in Parkinson's disease. An in vitro study using extended X-ray absorption fine structure and cryo-electron microscopy. , 1999, Brain : a journal of neurology.

[60]  N. Martin,et al.  Relative importance of female‐specific and non‐female‐specific effects on variation in iron stores between women , 2003, British journal of haematology.

[61]  M. Youdim Brain iron deficiency and excess; cognitive impairment and neurodegenration with involvement of striatum and hippocampus , 2008, Neurotoxicity Research.

[62]  Xudong Huang,et al.  Amyloid precursor protein and alpha synuclein translation, implications for iron and inflammation in neurodegenerative diseases. , 2009, Biochimica et biophysica acta.

[63]  W. Freeman,et al.  A CSF biomarker panel for identification of patients with amyotrophic lateral sclerosis , 2009, Neurology.

[64]  J. Connor,et al.  HFE mutations and Alzheimer's disease. , 2006, Journal of Alzheimer's disease : JAD.

[65]  Lorene M Nelson,et al.  Incidence of Parkinson's disease: variation by age, gender, and race/ethnicity. , 2003, American journal of epidemiology.