Characterization of biometal profiles in neurological disorders
Abstract
Many neurodegenerative and neuropsychiatric disorders have been reported to coincide with the dysregulation of metal ions in the body and central nervous system. However, in most cases, it is not the imbalance of a single divalent metal ion but a plethora of metal ions reported to be altered. Given that different divalent metal ions are often able to bind to a protein in a competitive manner, although with different affinities, and that they might use similar transporters for uptake and regulation, it is likely that the imbalance of one metal ion will downstream affect the homeostasis of other metal ions. Thus, based on this assumption, we hypothesize that the dysregulation of a specific metal ion will lead to a characteristic biometal profile. Similar profiles might therefore be detected in various neurological disorders. Moreover, if such shared biometal profiles exist across different neurological disorders, it is possible that shared behavioural impairments in these disorders result from the imbalance in metal ion homeostasis. Thus, here, we evaluate the reported excess or deficiency of metal ions in various neurological disorders and aim to integrate reported alterations in metal ions to generate a characteristic biometal profile for the disorder. Based on this, we try to predict which alterations in biometals will be caused by the overload or deficiency of one particular metal ion. Moreover, investigating the behavioural phenotypes of rodent models suffering from alterations in biometals, we assess whether a shared behavioural phenotype exists for disorders with similar biometal profiles. Our results show that observed behavioural aspects of some neurological disorders are reflected in their specific biometal profile and mirrored by mouse models suffering from similar biometal deregulations.
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Metal ion imbalance in the brain is among the primary triggers in the etiology of Alzheimer's disease.
“Metal ion imbalance in the brain is among the primary triggers in the etiology of AD and hence it is appropriate to tackle this said illness with a chelation therapy technique employing metal ions (Pfaender et al., 2014).”
From An update on the novel and approved drugs for Alzheimer disease (2022) · cites this paper as Pfaender et al., 2014
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Fasae, K. D., Abolaji, A. O., Faloye, T. R., Odunsi, A., Oyetayo, B. O., Enya, J. I., Rotimi, J. A., Akinyemi, R., Whitworth, A. J., & Aschner, M. (2021) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2021.126779 · Cited by 160 · see citing works
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“Like NC, PrLD-containing proteins are intrinsic to SGs and can multimerize into Zn2+-dependent LLPS processes of aggregate-prone neurodegenerative disease markers TIA-1, TDP-43, FUS/TLS, Tau, amyloid-β, synucleins, and SOD1 (Caragounis et al., 2010; Garnier et al., 2017; Pfaender and Grabrucker, 2014; Rayman et al., 2…”
BackgroundMicronutrients and Brain Development
Mattei, D., & Pietrobelli, A. (2019) · Current Nutrition Reports · doi:10.1007/s13668-019-0268-z · Cited by 112 · see citing works
Zinc in Gut-Brain Interaction in Autism and Neurological Disorders
Vela, G., Stark, P., Socha, M. T., Sauer, A. K., Hagmeyer, S., & Grabrucker, A. M. (2015) · Neural Plasticity · doi:10.1155/2015/972791 · Cited by 101 · see citing works
Behavioral impairments in animal models for zinc deficiency
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“For example, low serum zinc levels have been reported in Autism Spectrum Disorders (ASD), Attention deficit hyperactivity disorder (ADHD), Mood Disorders, such as depression, Schizophrenia (SCZ), and Spinocerebellar ataxia type 2 (Pfaender and Grabrucker, 2014).”
BackgroundSauer, A. K., Pfaender, S., Hagmeyer, S., Tarana, L., Mattes, A.-K., Briel, F., Küry, S., Boeckers, T. M., & Grabrucker, A. M. (2017) · BioMetals · doi:10.1007/s10534-017-0033-y · Cited by 97 · see citing works
“Intriguingly, among individuals with Autism Spectrum Disorders (ASD), the incidence rate of Zn deficiency has been reported to be significantly higher compared to age matched healthy control subjects (Pfaender and Grabrucker 2014).”
Sauer, A. K., & Grabrucker, A. M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01295 · Cited by 85 · see citing works
“Clinical studies have reported a reduction of blood zinc concentration in depressed patients (McLoughlin and Hodge, 1990; Maes et al., 1997; Siwek et al., 2013; Swardfager et al., 2013; Pfaender and Grabrucker, 2014) A recent meta-analysis found that depression in subjects was associated with significantly lower perip…”
Stem Cell Transplantation Therapy and Neurological Disorders: Current Status and Future Perspectives
Rahman, M. M., Islam, M. R., Islam, M. T., Harun-Or-Rashid, M., Islam, M., Abdullah, S., Uddin, M. B., Das, S., Rahaman, M. S., Ahmed, M., et al. (2022) · Biology · doi:10.3390/biology11010147 · Cited by 63 · see citing works
“Increased iron levels are correlated with patients’ longevity [142,143].”
BackgroundGender Dependent Evaluation of Autism like Behavior in Mice Exposed to Prenatal Zinc Deficiency
Grabrucker, S., Boeckers, T. M., & Grabrucker, A. M. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00037 · Cited by 76 · see citing works
“Nowadays, many studies on human patients report zinc deficiency to occur frequently associated with neuropsychiatric disorders such as ASD, Attention deficit hyperactivity disorder (ADHD), Mood Disorders such as Depression, and Schizophrenia (Pfaender and Grabrucker, 2014).”
Zinc binding to RNA recognition motif of TDP-43 induces the formation of amyloid-like aggregates
Garnier, C., Devred, F., Byrne, D., Puppo, R., Roman, A. Y., Malesinski, S., Golovin, A. V., Lebrun, R., Ninkina, N. N., & Tsvetkov, P. O. (2017) · Scientific Reports · doi:10.1038/s41598-017-07215-7 · Cited by 76 · see citing works
Socha, K., Klimiuk, K., Naliwajko, S. K., Soroczyńska, J., Puścion‐Jakubik, A., Markiewicz‐Żukowska, R., & Kochanowicz, J. (2021) · Nutrients · doi:10.3390/nu13020287 · Cited by 72 · see citing works
“In AD, abnormal homeostasis of trace elements has been regarded as a contributing factor [19].”
BackgroundGao, F., Zhao, J., Liu, P., Ji, D., Zhang, L., Zhang, M., Li, Y., & Xiao, Y. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.09.098 · Cited by 71 · see citing works
Pfaender, S., Sauer, A. K., Hagmeyer, S., Mangus, K., Linta, L., Liebau, S., Bockmann, J., Huguet, G., Bourgeron, T., Boeckers, T. M., et al. (2017) · Scientific Reports · doi:10.1038/srep45190 · Cited by 68 · see citing works
“It was also shown that a low Zn level may lead to Cu toxicity 28 , which can cause neurological deficits in children.”
InfluentialZinc as a therapy in a rat model of autism prenatally induced by valproic acid
Cezar, L. C., Kirsten, T. B., da Fonseca, C. C. N., Lima, A. P., Bernardi, M. M., & Felício, L. F. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.02.008 · Cited by 69 · see citing works
“ciated with neuropsychiatric disorders (Gao et al., 2011; Pfaender and Grabrucker, 2014; Takeda et al., 2007; Whittle et al., 2009).”
MethodSharma, A., Pachauri, V., & Flora, S. J. S. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01247 · Cited by 67 · see citing works
“biometals might be playing a crucial role in the pathogenesis of AD (Zhang, 2005; Mandel et al., 2007; Henry et al., 2010; DeToma et al., 2012; Kotler et al., 2014; Pfaender and Grabrucker, 2014).”
BackgroundDesign and synthesis of donepezil analogues as dual AChE and BACE-1 inhibitors
Gabr, M. T., & Abdel‐Raziq, M. S. (2018) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2018.06.031 · Cited by 65 · see citing works
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Recent progress in polymer-based optical chemosensors for Cu2+ and Hg2+ Ions: A comprehensive review
Choudhury, N., Saha, B., & De, P. (2020) · European Polymer Journal · doi:10.1016/j.eurpolymj.2020.110233 · Cited by 55 · see citing works
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Recent Advances in Targeting Transition Metals (Copper, Iron, and Zinc) in Alzheimer’s Disease
Singh, R., Panghal, A., Jadhav, K., Thakur, A., Verma, R. K., Singh, C., Goyal, M., Kumar, J., & Namdeo, A. G. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04256-8 · Cited by 47 · see citing works
“The consequence of interactions between the metal ions and the crucial proteins APP and its derivatives, Aβ and tau, metal imbalances in the brain are seen in AD [4, 36] (Fig.”
Across the spectrum: integrating multidimensional metal analytics for in situ metallomic imaging
Stewart, T. J. (2018) · Metallomics · doi:10.1039/c8mt00235e · Cited by 46 · see citing works
Zinc Binding to S100B Affords Regulation of Trace Metal Homeostasis and Excitotoxicity in the Brain
Hagmeyer, S., Cristóvão, J. S., Mulvihill, J. J., Boeckers, T. M., Gomes, C. M., & Grabrucker, A. M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00456 · Cited by 44 · see citing works
“…and neuropsychological disorders such as mood disorders, autism spectrum disorders (ASD), Alzheimer’s disease (AD), Parkinson’s disease (PD), Huntington’s disease (HD), multiple sclerosis (MS), TBI and amyotrophic lateral sclerosis (ALS) (Pfaender and Grabrucker, 2014; Prakash et al., 2015).”
Hagmeyer, S., Sauer, A. K., & Grabrucker, A. M. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00011 · Cited by 43 · see citing works
“Shank3 and Zinc Transporters Aside from GI problems, zinc deficiency was shown to be highly prevalent in individuals with PMDS (Grabrucker et al., 2014; Pfaender and Grabrucker, 2014; Pfaender et al., 2017) and ASD (Yasuda et al.”
Lan, J., Zeng, R., Jiang, X., Hou, J., Liu, Y., Hu, Z.-H., Li, H., Li, Y., Xie, S., Ding, Y., et al. (2019) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2019.103413 · Cited by 41 · see citing works
Sauer, A. K., Malijauskaite, S., Meleady, P., Boeckers, T. M., McGourty, K., & Grabrucker, A. M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04052-w · Cited by 41 · see citing works
“This commonality proposes Zn depletion as a possible common cause for ASD-specific microbiota alterations observed in PZD-mice and human ASD patients that frequently suffer from Zn deficiency early in development [38].”
BackgroundZinc and vitamin A deficiency in a cohort of children with autism spectrum disorder
Sweetman, D., O'Donnell, S. M., Lalor, A., Grant, T., & Greaney, H. (2019) · Child Care Health and Development · doi:10.1111/cch.12655 · Cited by 40 · see citing works
Zinc transporters protein level in postmortem brain of depressed subjects and suicide victims
Rafało-Ulińska, A., Piotrowska, J., Kryczyk‐Poprawa, A., Opoka, W., Sowa-Kućma, M., Misztak, P., Rajkowska, G., Stockmeier, C. A., Datka, W., Nowak, G., et al. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.09.008 · Cited by 39 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript variety of health problems (Pfaender and Grabrucker, 2014; Pochwat et al., 2015).”
BackgroundGrabrucker, S., Haderspeck, J., Sauer, A. K., Kittelberger, N., Asoglu, H., Abaei, A., Rasche, V., Schön, M., Boeckers, T. M., & Grabrucker, A. M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00450 · Cited by 39 · see citing works
“Zinc deficiency is implicated in several neurological disorders (Pfaender and Grabrucker, 2014).”
Leal, S., Cristóvão, J. S., Biesemeier, A., Cardoso, I., & Gomes, C. (2015) · Metallomics · doi:10.1039/c4mt00278d · Cited by 35 · see citing works
Highly cytotoxic DNA-interacting copper( ii ) coordination compounds
Brissos, R. F., Torrents, E., Mello-Andrade, F., Pires, W. C., Silveira-Lacerda, E. D. P., Caballero, A. B., Caubet, A., Massera, C., Roubeau, O., Teat, S. J., et al. (2014) · Metallomics · doi:10.1039/c4mt00152d · Cited by 38 · see citing works
Choudhury, N., & De, P. (2021) · Journal of Macromolecular Science Part A · doi:10.1080/10601325.2021.1960172 · Cited by 38 · see citing works
“most lethal ones as dysregulation of their concentration may have detrimental effects on normal biological processes.([5,6])”
BackgroundMitra, J., Guerrero, E. N., Hegde, P. M., Wang, H., Boldogh, I. R., Rao, K. S. J., MITRA, S. P., & Hegde, M. L. (2014) · Biomolecules · doi:10.3390/biom4030678 · Cited by 37 · see citing works
“Although numerous hypotheses have been proposed for the involvement of metals in various neurological dysfunctions (reviewed in [7,174]), conclusive evidence still remains vague, presumably due to the complex and dynamic nature of metal levels and toxicity.”
BackgroundEffects of Trace Metal Profiles Characteristic for Autism on Synapses in Cultured Neurons
Hagmeyer, S., Mangus, K., Boeckers, T. M., & Grabrucker, A. M. (2015) · Neural Plasticity · doi:10.1155/2015/985083 · Cited by 39 · see citing works
“The authors declare that there is no conflict of interests regarding the publication of this paper.”
BackgroundMethodInfluentialDysregulated Iron Homeostasis as Common Disease Etiology and Promising Therapeutic Target
Holbein, B. E., & Lehmann, C. (2023) · Antioxidants · doi:10.3390/antiox12030671 · Cited by 37 · see citing works
“Many neurological conditions have been shown to coincide with altered bodily distribution of various transition series biometals, especially in the case of iron [89].”
BackgroundDalès, J.-P., & Desplat‐Jégo, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239105 · Cited by 36 · see citing works
“Due to these interactions, the increase or the loss of one metal can lead to the establishment of a completely new metal profile affecting many others [168].”
BackgroundCiubotariu, D., Ghiciuc, C. M., & Lupușoru, C. E. (2015) · Substance Abuse Treatment Prevention and Policy · doi:10.1186/s13011-015-0025-2 · Cited by 33 · see citing works
“Moreover, decreased zinc has a certain influence on other mechanisms involved in the addiction downward spiral, as it is associated with depression-like symptoms and anxiety in both humans and animal models [26, 27], which are known to induce drug-taking behaviour [108].”
BackgroundHeavy Metals and Neurological Disorders: From Exposure to Preventive Interventions
Rehman, Q., Rehman, K., & Akash, M. S. H. (2021) · Emerging Contaminants and Associated Treatment Technologies · doi:10.1007/978-3-030-66376-6_4 · Cited by 39 · see citing works
Baecker, T., Mangus, K., Pfaender, S., Chhabra, R., Boeckers, T. M., & Grabrucker, A. M. (2014) · BioMetals · doi:10.1007/s10534-014-9764-1 · Cited by 32 · see citing works
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Prenatal Zinc Deficient Mice as a Model for Autism Spectrum Disorders
Sauer, A. K., Hagmeyer, S., & Grabrucker, A. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116082 · Cited by 33 · see citing works
Zhang, P., Georgiou, C. A., & Brusić, V. (2016) · Briefings in Bioinformatics · doi:10.1093/bib/bbw131 · Cited by 30 · see citing works
“Furthermore, Mg and Zn deficiency and lower levels of Ca, Fe, Mn and Se and increased level of Cu and other toxic metals have been observed, and these differences have been more pronounced in autistic children then in controls [121,126,128-130].”
BackgroundBłażewicz, A., Liao, K.-Y., Liao, H.-H., Niziński, P., Komsta, Ł., Momčilović, B., Jabłońska‐Czapla, M., Michalski, R., Prystupa, A., Sak, J. J., et al. (2017) · BioMed Research International · doi:10.1155/2017/3178784 · Cited by 29 · see citing works
Drug-like chelating agents: a potential lead for Alzheimer's disease
Huang, W., Wei, W., & Shen, Z. (2014) · RSC Advances · doi:10.1039/c4ra09193k · Cited by 29 · see citing works
The Role of Trace Metals in Alzheimer’s Disease
Benedictis, C. A. D., Vilella, A., & Grabrucker, A. M. (2019) · Codon Publications eBooks · doi:10.15586/alzheimersdisease.2019.ch6 · Cited by 31 · see citing works
“Due to these interactions, the loss of, or increase in, one trace metal can lead to the establishment of a completely new biometal profile affecting many other trace metals of a system (9).”
BackgroundConcentrations of Essential Trace Metals in the Brain of Animal Species—A Comparative Study
Benedictis, C. A. D., Raab, A., Ducie, E., Howley, S., Feldmann, J., & Grabrucker, A. M. (2020) · Brain Sciences · doi:10.3390/brainsci10070460 · Cited by 26 · see citing works
“Zinc is one of the most abundant trace metals in the brain, playing a pivotal role in neuronal activities, synaptic plasticity, and in the regulation of post-synaptic proteins [57,58].”
BackgroundMetals toxicity and its correlation with the gene expression in Alzheimer's disease
Yadav, J., Verma, A., Ahmad, M. K., Garg, R. K., Shiuli, Mahdi, A. A., & Srivastava, S. (2021) · Molecular Biology Reports · doi:10.1007/s11033-021-06386-x · Cited by 26 · see citing works
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Dreaming of a New World Where Alzheimer’s Is a Treatable Disorder
Catania, M., Giaccone, G., Salmona, M., Tagliavini, F., & Fede, G. D. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00317 · Cited by 24 · see citing works
“…of acetylcholine (ACh), mitochondrial dysfunction, oxidative stress, inflammation and dyshomeostasis of biometals might be actively involved in AD (Querfurth and LaFerla, 2010; Pfaender and Grabrucker, 2014; Stancu et al., 2014; Selkoe and Hardy, 2016; Wilkins and Swerdlow, 2016; Hardy, 2017).”
BackgroundWang, Z., Xie, S., Li, X., Wu, J., Wang, X., & Kong, L. (2015) · RSC Advances · doi:10.1039/c5ra13594j · Cited by 23 · see citing works
Golasik, M., Jawień, W., Przybyłowicz, A., Szyfter, W., Herman, M., Golusiński, W., Florek, E., & Piekoszewski, W. (2015) · Metallomics · doi:10.1039/c4mt00285g · Cited by 23 · see citing works
The enteric nervous system deficits in autism spectrum disorder
Wang, X., Tang, R., Wei, Z., Zhan, Y., Lu, J., & Li, Z. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1101071 · Cited by 22 · see citing works
“However, the prevalence of zinc deficiency has been found to be significantly higher among individuals with ASD compared to age-matched healthy controls (Grabrucker, 2013; Pfaender and Grabrucker, 2014).”
BackgroundRice: a potential vehicle for micronutrient fortification
Junaid-ur-Rahman, S., Chughtai, M. F. J., Khaliq, A., Liaqat, A., Pasha, I., Ahsan, S., Tanweer, S., Saeed, K., Siddiqa, A., Mehmood, T., et al. (2022) · Clinical Phytoscience · doi:10.1186/s40816-022-00342-3 · Cited by 20 · see citing works
“5 Selenium Keshan disease, Keshin‐Beck disease and myxedema‐ tous cretinism [91] (Westermark, 2021)”
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“com pathological changes in the neuronal balance of metal ions such as zinc, calcium, iron and copper [3–5] in these diseases.”
BackgroundN-cadherin-mediated cell adhesion is regulated by extracellular Zn2+
Heiliger, E., Osmanagic, A., Haase, H., Golenhofen, N., Grabrucker, A. M., Weth, A., & Baumgärtner, W. (2015) · Metallomics · doi:10.1039/c4mt00300d · Cited by 19 · see citing works
Effects of High Levels of Copper on the Depression-Related Memory Disorders
Liu, X., Lin, C., Wang, S., Yu, X., Jia, Y., & Chen, J. (2022) · The Journals of Gerontology Series A · doi:10.1093/gerona/glac222 · Cited by 18 · see citing works
Unravelling neurological disorders through metallomics-based approaches
de Jesus, J. R., & Arruda, M. A. Z. (2020) · Metallomics · doi:10.1039/d0mt00234h · Cited by 18 · see citing works
de Jesus, J. R., Galazzi, R. M., Júnior, C. A. L., & Arruda, M. A. Z. (2022) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2022.126964 · Cited by 16 · see citing works
Prevalence of low dietary zinc intake in women and pregnant women in Ireland
Benedictis, C. A. D., Trame, S., Rink, L., & Grabrucker, A. M. (2022) · Irish Journal of Medical Science (1971 -) · doi:10.1007/s11845-022-03181-w · Cited by 18 · see citing works
Zinc Binds to RRM2 Peptide of TDP-43
Golovin, A. V., Devred, F., Yatoui, D., Roman, A. Y., Zalevsky, A. O., Puppo, R., Lebrun, R., Guerlesquin, F., & Tsvetkov, P. O. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239080 · Cited by 16 · see citing works
Daini, E., Hagmeyer, S., Benedictis, C. A. D., Cristóvão, J. S., Bodria, M., Ross, A. M., Raab, A., Boeckers, T. M., Feldmann, J., Gomes, C. M., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01694-z · Cited by 18 · see citing works
Sauer, A. K., Hagmeyer, S., & Grabrucker, A. M. (2016) · InTech eBooks · doi:10.5772/63203 · Cited by 16 · see citing works
Human Serum Albumin-Inspired Glycopeptide-Based Multifunctional Inhibitor of Amyloid-β Toxicity
Roy, R., Pradhan, K., Khan, J., Das, G., Mukherjee, N., Das, D., & Ghosh, S. (2020) · ACS Omega · doi:10.1021/acsomega.0c01028 · Cited by 14 · see citing works
Metalloneurochemistry and the Pierian Spring: ‘Shallow Draughts Intoxicate the Brain’
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Putative contributions of the sex chromosome proteins SOX3 and SRY to neurodevelopmental disorders
Tahira, A. C., Barbosa, A. R., Feltrin, A. S., Gastaldi, V. D., de Toledo, V. H. C., de Carvalho Pereira, J. G., Lisboa, B. C. G., de Souza Reis, V. N., dos Santos, A. C. F., Maschietto, M., et al. (2019) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32704 · Cited by 11 · see citing works
“Low serum zinc levels were also observed in neuropsychiatric disorders (Pfaender & Grabrucker, 2014), including ASD (Grabrucker, 2014).”
BackgroundAmbeskovic, M., Laplante, D. P., Kenney, T., Elgbeili, G., Beaumier, P., Azat, N., Simcock, G. P., Kildea, S. V., King, S., & Metz, G. A. S. (2022) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2022.127036 · Cited by 11 · see citing works
Liu, Y., Zhou, Q., Zhao, Y., Wang, Y., Wang, Y., Wang, J., Xu, J., & Xue, C. (2015) · Biological Trace Element Research · doi:10.1007/s12011-015-0517-y · Cited by 11 · see citing works
“Biometals such as zinc, iron, copper, vanadium, and calcium play key roles in diverse physiological processes for living organisms, including humans, but can be toxic in excess [3].”
Targeting Metal Homeostasis as a Therapeutic Strategy for Alzheimer’s Disease
Department of Biomedical, M. A. N. S., Vilella, A., Daini, E., Department of Biomedical, M. A. N. S., De Benedictis, C. A., Cellular Neurobiology and Neuro-Nanotechnology Lab, D. O. B. S., Grabrucker, A. M., Cellular Neurobiology and Neuro-Nanotechnology Lab, D. O. B. S., Bernal Institute, U. O. L., & Health Research Institute (HRI), U. O. L. (2020) · Alzheimer’s Disease: Drug Discovery · doi:10.36255/exonpublications.alzheimersdisease.2020.ch5 · Cited by 12 · see citing works
Elemental Metabolomics: Modulation of Egg Metallome with Flavonoids, an Exploratory Study
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“Biometals are considered the trace metals that play a role in the normal body function [1].”
BackgroundExtracerebral Dysfunction in Animal Models of Autism Spectrum Disorder
Hill‐Yardin, E. L., McKeown, S. J., Novarino, G., & Grabrucker, A. M. (2017) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-319-52498-6_9 · Cited by 8 · see citing works
Protective effects of neocuproine copper chelator against oxidative damage in NSC34 cells
Nunes, E. A., Manieri, T. M., Matias, A. C., Bertuchi, F. R., da Silva, D. A., Lago, L., Sato, R. H., & Cerchiaro, G. (2018) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2018.06.019 · Cited by 7 · see citing works
Total Reflection X-ray Fluorescence Analysis of Plasma Elements in Autistic Children from India
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“Genetic factors might be largely responsible for the occurrence of ASD that alone or in a combination with specific environmental factors trigger the development of ASD [1].”
BackgroundNutrition, Neurotransmitters, and Behavior
Kumar, S., Mishra, T., Prajapati, A., & Sethi, P. (2022) · Nutritional neurosciences · doi:10.1007/978-981-19-5021-6_5 · Cited by 6 · see citing works
Sustainable remediation of paint factory wastewater using electrocoagulation
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Neurochemistry of lead and manganese
Austin, R. N., Freeman, J. L., & Guilarte, T. R. (2016) · Metallomics · doi:10.1039/c6mt90017h · Cited by 6 · see citing works
Ebner, B. A., Erdahl, S. A., Lundgreen, C. S., Vassilaki, M. E., Kremers, W. K., Knopman, D. S., Petersen, R. C., Berry, D. J., Lewallen, D. G., Jannetto, P. J., et al. (2025) · Acta Neuropathologica · doi:10.1007/s00401-025-02856-9 · Cited by 6 · see citing works
Mazhar, W., Farooq, S., Iqbal, A., Ansari, S. H., Choudhary, M. I., Rahman, A., & Musharraf, S. G. (2017) · RSC Advances · doi:10.1039/c6ra28514g · Cited by 5 · see citing works
How Single Site Mutations Can Help Understanding Structure Formation of Amyloid β1−40
Schwarze, B., & Huster, D. (2023) · Macromolecular Bioscience · doi:10.1002/mabi.202200489 · Cited by 5 · see citing works
Investigation of the Genotoxicological Profile of Aqueous Betula pendula Extracts
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Ciubotariu, D., Lupușoru, R. V., Luca, E., Mititelu-Tarțău, L., & Lupușoru, C. E. (2017) · Biological Trace Element Research · doi:10.1007/s12011-017-0995-1 · Cited by 4 · see citing works
Grabrucker, S., & Grabrucker, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804562-6.00009-9 · Cited by 3 · see citing works
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The history of metals in autism spectrum disorders
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Molecular Mechanisms and Aspects on the Role of Neuropeptide Y as a Zn2+ and Cu2+ Chelator
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Metals and amyloid gain-of-toxic mechanisms in neurodegenerative diseases
Cristóvão, J. S., Moreira, G. G., Grabrucker, A. M., & Gomes, C. M. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819132-3.00009-9 · Cited by 3 · see citing works
How does “Protein Corona” Affect the In vivo Efficiency of Polymeric Nanoparticles? State of Art
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ZINC IMBALANCE AND THE OPPORTUNITY OF ZINC SUPPLEMENTATION IN ALCOHOLICS AND DRUG USERS
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“The body obtains its essential biometals from food sources and water (Kawahara et al., 2023; Pfaender & Grabrucker, 2014).”
A Bright Spiropyran-Based Zinc Sensor for Live-Cell Imaging
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The role of trace elements in Alzheimer's disease
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- Authors
- Pfaender, S., & Grabrucker, A. M.
- Affiliations
- Universität Ulm (DE)
- Corresponding author
- Grabrucker, Andreas M.
- Venue
- Metallomics
- Publisher
- Oxford University Press (OUP)
- Published
- 2014
- Volume
- 6
- Issue
- 5
- Pages
- 960-977
- ISSN
- 1756-5901 (ISSN-L)
- 1756-591X
- OpenAlex
- W2018891401
- Cited by
- 117
- References
- 169
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 14 · 2021: 7 · 2020: 14 · 2019: 10 · 2018: 13 · 2017: 14 · 2016: 11 · 2015: 9 · 2014: 6
- FWCI
- 1.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Metallomics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alzheimer's Association (NIRG-12-235441, L.SBN.0083)
- Royal Society
- Royal Society of Chemistry
- Universität Ulm (“Baustein 3.2”)
- International Graduate School in Molecular Medicine Ulm
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
- Life Sciences › Neuroscience › Neurology › Neurological diseases and metabolism
- Keywords
- metal homeostasis, neurological disorders, neurodegenerative diseases, neuropsychiatric disorders, metal transporters, behavioral phenotypes, rodent models, metal deficiency
- MeSH terms
- Humans, Metals, Nervous System Diseases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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