Cholesterol in brain disease: Sometimes determinant and frequently implicated

Martín, Mauricio G; Pfrieger, Frank; Dotti, Carlos G

doi:10.15252/embr.201439225

Cited by 310Cholesterol and Lipid MetabolismAlzheimer's disease research and treatmentsLysosomal Storage Disorders Research

Cholesterol in brain disease: Sometimes determinant and frequently implicated

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Martín, Mauricio G, Pfrieger, Frank, Dotti, Carlos G·2014·The EMBO Reports

DOI 10.15252/embr.201439225PMC PMC4253844

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Abstract

Cholesterol is essential for neuronal physiology, both during development and in the adult life: as a major component of cell membranes and precursor of steroid hormones, it contributes to the regulation of ion permeability, cell shape, cell-cell interaction, and transmembrane signaling. Consistently, hereditary diseases with mutations in cholesterol-related genes result in impaired brain function during early life. In addition, defects in brain cholesterol metabolism may contribute to neurological syndromes, such as Alzheimer's disease (AD), Huntington's disease (HD), and Parkinson's disease (PD), and even to the cognitive deficits typical of the old age. In these cases, brain cholesterol defects may be secondary to disease-causing elements and contribute to the functional deficits by altering synaptic functions. In the first part of this review, we will describe hereditary and non-hereditary causes of cholesterol dyshomeostasis and the relationship to brain diseases. In the second part, we will focus on the mechanisms by which perturbation of cholesterol metabolism can affect synaptic function.

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The beneficial effects of statins in Mecp2-deficient mice presumably reflect mechanisms of action other than inhibition of cholesterol synthesis, given that brain cholesterol synthesis is already moderately suppressed in these mice.
“As statins were designed to act primarily by inhibiting cholesterol synthesis, their beneficial effects in the Mecp2-deficient mouse presumably reflect other mechanisms of action given that brain cholesterol synthesis is already moderately suppressed in these mice (Orth and Bellosta, 2012; Martin et al., 2014).”
From Suppression of brain cholesterol synthesis in male Mecp2-deficient mice is age dependent and not accompanied by a concurrent change in the rate of fatty acid synthesis (2017) · cites this paper as Martin et al., 2014
The ‘Cholesterol in brain disease: hereditary causes’ section (page unavailable) reports decreased brain sterol synthesis in adult Mecp2-mutant mice and improved behavior and lifespan after fluvastatin treatment. The ‘Therapeutic approaches to cholesterol-related brain diseases’ section (page unavailable) describes other possible beneficial actions of statins. The paper does not conclude that those other actions explain fluvastatin’s benefits in the Mecp2-deficient mice. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Diet-derived cholesterol cannot cross the BBB and cannot compensate the low cholesterol level in the brain of SLOS patients with neurologic symptoms.
“Nevertheless, diet-derived cholesterol cannot cross the BBB and cannot compensate the low cholesterol level in the brain [3,24].”
From Loss of Mevalonate/Cholesterol Homeostasis in the Brain: A Focus on Autism Spectrum Disorder and Rett Syndrome (2019) · cites this paper as [24]
The most severe DHCR7 mutations cause fetal or newborn death, while less severe variants cause developmental defects in specific organs such as facial and cranial malformations, hypospadia or complete gonadal absence.
“The most severe mutations of this gene cause fetal or newborn death, while less severe variants cause developmental defects in specific organs such as facial and cranial malformations, hypospadia or complete gonadal absence [24].”
From Loss of Mevalonate/Cholesterol Homeostasis in the Brain: A Focus on Autism Spectrum Disorder and Rett Syndrome (2019) · cites this paper as [24]
Cholesterol has been implied in the production and clearance of beta amyloid.
“Cholesterol has been implied in the production and clearance of beta amyloid [24].”
From Loss of Mevalonate/Cholesterol Homeostasis in the Brain: A Focus on Autism Spectrum Disorder and Rett Syndrome (2019) · cites this paper as [24]
Disruption of cholesterol homeostasis perturbs cell-autonomous and non-cell-autonomous functions, including inhibition of crucial signaling pathways and cellular crosstalk.
“Disruption of cholesterol homeostasis has also been shown to perturb cell-autonomous and non-cell-autonomous functions, including inhibition of crucial signaling pathways and cellular crosstalk (Bjorkhem and Meaney, 2004; Martin et al., 2014).”
From Sterol dysregulation in Smith–Lemli–Opitz syndrome causes astrocyte immune reactivity through microglia crosstalk (2022) · cites this paper as Martin et al., 2014

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Upregulation of BACE1 and β-Amyloid Protein Mediated by Chronic Cerebral Hypoperfusion Contributes to Cognitive Impairment and Pathogenesis of Alzheimer’s Disease
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TREM2 regulates microglial cholesterol metabolism upon chronic phagocytic challenge
Nugent, A. A., Lin, K., van Lengerich, B., Lianoglou, S., Przybyla, L., Davis, S. S., Llapashtica, C., Wang, J., Kim, D. J., Xia, D., et al. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.007 · Cited by 745 · see citing works
There's Something Wrong with my MAM; the ER–Mitochondria Axis and Neurodegenerative Diseases
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A Historical Review of Brain Drug Delivery
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Li, R.-Y., Qin, Q., Yang, H.-C., Wang, Y.-Y., Mi, Y.-X., Yin, Y.-S., Wang, M., Yu, C.-J., & Tang, Y. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00542-y · Cited by 204 · see citing works
Mitochondrial cholesterol: Metabolism and impact on redox biology and disease
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Brain cell type-specific cholesterol metabolism and implications for learning and memory
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Epigallocatechin-3-Gallate (EGCG): New Therapeutic Perspectives for Neuroprotection, Aging, and Neuroinflammation for the Modern Age
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Analytical methods for cholesterol quantification
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Intracellular Cholesterol Trafficking and Impact in Neurodegeneration
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Local cholesterol metabolism orchestrates remyelination
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Lead (Pb) and neurodevelopment: A review on exposure and biomarkers of effect (BDNF, HDL) and susceptibility
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Fetal Alcohol Spectrum Disorders: An Overview from the Glia Perspective
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Synaptic tau: A pathological or physiological phenomenon?
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Cholesterol‐loaded nanoparticles ameliorate synaptic and cognitive function in Huntington's disease mice
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Cholesterol 24-Hydroxylation by CYP46A1: Benefits of Modulation for Brain Diseases
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Plasma Lipids as Biomarkers for Alzheimer's Disease: A Systematic Review
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Restoring brain cholesterol turnover improves autophagy and has therapeutic potential in mouse models of spinocerebellar ataxia
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24S‐hydroxycholesterol: Cellular effects and variations in brain diseases
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ABCA1‐Mediated Cholesterol Efflux Capacity to Cerebrospinal Fluid Is Reduced in Patients With Mild Cognitive Impairment and Alzheimer's Disease
Yassine, H. N., Feng, Q., Chiang, J., Petrosspour, L. M., Fonteh, A. N., Chui, H. C., & Harrington, M. G. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.115.002886 · Cited by 80 · see citing works
Can Cholesterol Metabolism Modulation Affect Brain Function and Behavior?
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A systematic review and meta-analysis of serum cholesterol and triglyceride levels in patients with Parkinson’s disease
Fu, X., Wang, Y., He, X., Li, H., Liu, H., & Zhang, X. (2020) · Lipids in Health and Disease · doi:10.1186/s12944-020-01284-w · Cited by 74 · see citing works
27-Hydroxycholesterol Induces Aberrant Morphology and Synaptic Dysfunction in Hippocampal Neurons
Merino‐Serrais, P., Loera‐Valencia, R., Rodriguez‐Rodriguez, P., Parrado‐Fernández, C., Ismail, M. A. M., Maioli, S., Matute, E., Jimenez-Mateos, E. M., Björkhem, I., DeFelipe, J., et al. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy274 · Cited by 71 · see citing works
Loss of parkin promotes lipid rafts-dependent endocytosis through accumulating caveolin-1: implications for Parkinson’s disease
Cha, S., Choi, Y. R., Heo, C. H., Kang, S., Joe, E.-H., Jou, I., Kim, H.-M., & Park, S. M. (2015) · Molecular Neurodegeneration · doi:10.1186/s13024-015-0060-5 · Cited by 66 · see citing works
Overnutrition Determines LPS Regulation of Mycotoxin Induced Neurotoxicity in Neurodegenerative Diseases
Martins, I. J. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161226190 · Cited by 67 · see citing works
Aging Triggers a Repressive Chromatin State at Bdnf Promoters in Hippocampal Neurons
Palomer, E., Martín‐Segura, A., Baliyan, S., Ahmed, T., Balschun, D., Venero, C., Martín, M. G., & Dotti, C. G. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.08.028 · Cited by 66 · see citing works
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Impaired cholesterol metabolism, neurons, and neuropsychiatric disorders
Cheon, S. Y. (2023) · Experimental Neurobiology · doi:10.5607/en23010 · Cited by 67 · see citing works
Peroxisomal dysfunction in neurodegenerative diseases
Jo, D. S., & Cho, D. (2019) · Archives of Pharmacal Research · doi:10.1007/s12272-019-01131-2 · Cited by 64 · see citing works
Oxysterol levels and metabolism in the course of neuroinflammation: insights from in vitro and in vivo models
Mutemberezi, V., Buisseret, B., Masquelier, J., Guillemot‐Legris, O., Alhouayek, M., & Muccioli, G. G. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1114-8 · Cited by 62 · see citing works
The axonal endoplasmic reticulum: One organelle—many functions in development, maintenance, and plasticity
Luarte, A., Cornejo, V., Bertin, F., Gallardo, J., & Couve, A. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22560 · Cited by 53 · see citing works
Biallelic pathogenic variants in the lanosterol synthase gene LSS involved in the cholesterol biosynthesis cause alopecia with intellectual disability, a rare recessive neuroectodermal syndrome
Besnard, T., Sloboda, N., Goldenberg, A., Küry, S., Cogné, B., Bréhéret, F., Trochu, E., Conrad, S., Vincent, M., Deb, W., et al. (2019) · Genetics in Medicine · doi:10.1038/s41436-019-0445-x · Cited by 61 · see citing works
ApoE4 reduction: An emerging and promising therapeutic strategy for Alzheimer's disease
Li, Y., Macyczko, J. R., Liu, C.-C., & Bu, G. (2022) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2022.03.011 · Cited by 61 · see citing works
Role of mitochondrial raft-like microdomains in the regulation of cell apoptosis
Garofalo, T., Manganelli, V., Grasso, M., Mattei, V., Ferri, A., Misasi, R., & Sorice, M. (2015) · APOPTOSIS · doi:10.1007/s10495-015-1100-x · Cited by 61 · see citing works
Targeting cellular cholesterol for anticancer therapy
Gu, L., Saha, S. T., Thomas, J., & Kaur, M. (2019) · FEBS Journal · doi:10.1111/febs.15018 · Cited by 63 · see citing works
Cholesterol – A putative endogenous contributor towards Parkinson's disease
Paul, R. K., Choudhury, A., & Borah, A. (2015) · Neurochemistry International · doi:10.1016/j.neuint.2015.07.025 · Cited by 61 · see citing works
TDP-43 mediates SREBF2-regulated gene expression required for oligodendrocyte myelination
Ho, W. Y., Chang, J., Lim, K., Cazenave‐Gassiot, A., Nguyen, A. T., Foo, J. C., Muralidharan, S., Viera-Ortiz, A., Ong, S. J. M., Hor, J. H., et al. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.201910213 · Cited by 60 · see citing works
Allosteric modulation of the adenosine A2A receptor by cholesterol
Huang, S. K., Almurad, O., Pejana, R. J., Morrison, Z. A., Pandey, A. N., Picard, L.-P., Nitz, M., Sljoka, A., & Prosser, R. S. (2021) · eLife · doi:10.7554/elife.73901 · Cited by 60 · see citing works
Post-translational control of the long and winding road to cholesterol.
Sharpe, L. J., Coates, H., & Brown, A. J. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.010723 · Cited by 46 · see citing works
Lead exposure induces Alzheimers's disease (AD)-like pathology and disturbes cholesterol metabolism in the young rat brain.
Zhou, C.-C., Gao, Z.-Y., Wang, J., Wu, M.-Q., Hu, S., Chen, F., Liu, J.-X., Pan, H., & Yan, C.-H. (2018) · Toxicology Letters · doi:10.1016/j.toxlet.2018.06.1065 · Cited by 53 · see citing works
The role of DHCR24 in the pathogenesis of AD: re-cognition of the relationship between cholesterol and AD pathogenesis
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“…reports, low cholesterol levels have also been noted in the hippocampus of aging human brains and in hippocampal synapses of aging mice (Desai, Paronis, Martin, Desai, & Bergman, 2010; Martín et al. 2014; Svennerholm, Bostr€om, Helander, & Jungbjer, 1991; Thelen, Falkai, Bayer, & L€utjohann, 2006).”
Background
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Authors: Martín, M. G., Pfrieger, F., & Dotti, C. G.
Affiliations: Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
Centre National de la Recherche Scientifique (FR)
Consejo Superior de Investigaciones Científicas (ES)
Corresponding author: Martín, Mauricio G
Pfrieger, Frank
Dotti, Carlos G
ORCID: Martín, Mauricio G
Pfrieger, Frank
Dotti, Carlos G
Venue: The EMBO Reports
Publisher: Springer Science and Business Media LLC
Published: 2014-09-15
Volume: 15
Issue: 10
Pages: 1036-1052
ISSN: 1469-221X (ISSN-L)
1469-3178
DOI: 10.15252/embr.201439225
PMC: PMC4253844
OpenAlex: W2027703774
Cited by: 304
References: 235
Citations by year: 2026: 18 · 2025: 28 · 2024: 31 · 2023: 42 · 2022: 40 · 2021: 27 · 2020: 30 · 2019: 24 · 2018: 25 · 2017: 12 · 2016: 16 · 2015: 10
FWCI: 2.35
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: EMBO Reports (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
Lirias (submittedVersion)
CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
Topics: Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Physiology › Lysosomal Storage Disorders Research
Keywords: brain cholesterol, cholesterol metabolism, Alzheimer's disease, Huntington's disease, Parkinson's disease, cognitive impairment, synaptic function, ion permeability, transmembrane signaling
MeSH terms: Alzheimer Disease, Cell Membrane, Cholesterol, Humans, Huntington Disease, Mutation, Neurons, Parkinson Disease, Gonadal Steroid Hormones, Lipid Metabolism

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Cholesterol in brain disease: Sometimes determinant and frequently implicated

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