Moderate differences in common feeding diets change lipid composition in the hippocampal dentate gyrus and affect spatial cognitive flexibility in male rats

Maliković, Jovana; Vuyyuru, Harish; Koefeler, Harald; Šmidák, Roman; Höger, Harald; Kalaba, Predrag; Hussein, A. M.; Lübec, Gert; Korz, Volker

doi:10.1016/j.neuint.2019.04.017

Cited by 6 publications

(8 citation statements)

References 31 publications

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“…In the present study regarding the hypothalamus we found differences in only one ceramide (Cer 17:2) and the level was reduced in OMI as compared to OMU. Thus, levels of ceramides and sphingomyelins are less affected and cannot serve as biomarkers of cognitive decline in the hypothalamus in contrast to the hippocampus, where both lipid species predicted spatial cognition and cognitive flexibility (Huston et al, 2016;Maliković et al, 2019b).…”

Section: Discussionmentioning

confidence: 99%

“…So far, the lipid neurochemical basis has not been fully provided in studies related to cognition and memory. Mostly, the work is focusing on individual lipids although the introduction and development of mass spectrometric techniques with the aim to generate brain lipidomes has allowed deeper insight into lipid composition and mechanisms in several species and a series of brain subregions and subareas (Köfeler et al, 2010;Oliveira et al, 2016;Smidak et al, 2017b;Lerner et al, 2019;Maliković et al, 2019b).…”

Section: Introductionmentioning

confidence: 99%

“…In previous studies we focused on differences in hippocampal lipid profiles in good and bad learners (Maliković et al, 2019a) as well as steroid and thyroid hormone levels between young male rats, comparable in terms of spatial memory performance to OMU and OMI male rats selected from a large cohort by a spatial memory paradigm, the hole-board (Maliković et al, 2019b). These hormones are generally related to spatial learning and memory by modulating hippocampal plasticity (McGaugh et al, 1975;Bohus and de Kloet, 1981;Joëls and de Kloet, 1991;Joëls, 2018) and the release and production are widely regulated by the hypothalamus.…”

Section: Introductionmentioning

confidence: 99%

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Differences in Hypothalamic Lipid Profiles of Young and Aged Male Rats With Impaired and Unimpaired Spatial Cognitive Abilities and Memory

Wackerlig

Köfeler

Korz

et al. 2020

Front. Aging Neurosci.

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Lipids play a major role for several brain functions, including cognition and memory. There is a series of work on individual lipids showing involvement in memory mechanisms, a concise lipidome was not reported so far. Moreover, there is no evidence for age-related memory decline and there is only work on brain of young vs. aging animals. Aging animals, however, are not a homogeneous group with respect to memory impairments, thus animals with impaired and unimpaired memory can be discriminated. Following recent studies of hippocampal lipid profiles and hypothalamus controlled hormone profiles, the aim of this study was to compare hypothalamic, lipidomic changes in male Sprague-Dawley rats between young (YM), old impaired (OMI) and old unimpaired (OMU) males. Grouping criterions for aged rats were evaluated by testing them in a spatial memory task, the hole-board. YMs were also tested. Subsequently brains were removed, dissected and hypothalami were kept at −80 • C until sample preparation and analysis on liquid chromatography / mass spectrometry (LC-MS). Significant differences in the amounts of a series of lipids from several classes could be detected between young and aged and between OMI and OMU. A large number of lipids were increased in OMI and a smaller number in OMU as compared to young rats. Differences of lipid ratios (log2 of ratio) between OMI and OMU consisted of glycerophosphocholines (

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Differences in Hypothalamic Lipid Profiles of Young and Aged Male Rats With Impaired and Unimpaired Spatial Cognitive Abilities and Memory

Wackerlig

Köfeler

Korz

et al. 2020

Front. Aging Neurosci.

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“…Recently, studies have demonstrated substantial impact of diet and nutritional interventions on the brain lipid composition ( 20 , 21 ). Maliković et al ( 20 ) demonstrated that energy reduced diet during adulthood can modulate the brain lipid levels, which resulted in impaired reversal learning. In another study, feeding rats with cereal modified brain cholesterol, vitamin E, and fatty acid distributions ( 22 ).…”

Section: Introductionmentioning

confidence: 99%

Early Life to Adult Brain Lipidome Dynamic: A Temporospatial Study Investigating Dietary Polar Lipid Supplementation Efficacy

et al. 2022

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The lipid composition of the brain is well regulated during development, and the specific temporospatial distribution of various lipid species is essential for the development of optimal neural functions. Dietary lipids are the main source of brain lipids and thus contribute to the brain lipidome. Human milk is the only source of a dietary lipids for exclusively breastfed infant. Notably, it contains milk fat globule membrane (MFGM) enriched in polar lipids (PL). While early life is a key for early brain development, the interplay between dietary intake of polar lipids and spatial dynamics of lipid distribution during brain development is poorly understood. Here, we carried out an exploratory study to assess the early postnatal temporal profiling of brain lipidome between postnatal day (PND) 7 and PND 50 using matrix-assisted laser desorption ionization as a mass spectrometry imaging (MALDI-MSI) in an in vivo preclinical model. We also assessed the effect of chronic supplementation with PL extracted from alpha-lactalbumin-enriched whey protein concentrate (WPC) containing 10% lipids, including major lipid classes found in the brain (37% phospholipids and 15% sphingomyelin). MALDI-MSI of the spatial and temporal accretion of lipid species during brain development showed that the brain lipidome is changing heterogeneously along time during brain development. In addition, increases in 400+ PL supplement-dependent lipids were observed. PL supplementation had significant spatial and temporal effect on specific fatty esters, glycerophosphocholines, glycerophosphoethanolamines, and phosphosphingolipids. Interestingly, the average levels of these lipids per brain area tended to be constant in various brain structures across the age groups, paralleling the general brain growth. In contrast, other lipids, such as cytidine diphosphate diacylglycerol, diacylglycerophosphates, phosphocholines, specific ether-phosphoethanolamines, phosphosphingolipids, glycerophosphoinositols, and glycerophosphoserines showed clear age-dependent changes uncoupled from the general brain growth. These results suggest that the dietary PL supplementation may preferentially provide the building blocks for the general brain growth during development. Our findings add to the understanding of brain-nutrient relations, their temporospatial dynamics, and potential impact on neurodevelopment.

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“…Kim and colleagues (Kim et al 2017) found dysregulated metabolism of phosphatidylcholines and ceramides in the plasma of Alzheimer's disease patients and tandem mass spectrometry (MS/MS) lipidomics are the method of choice to detect subtle changes of the lipidome in brain disease and upon pharmacological or dietary intervention (Hanson et al 2019). Recently, we found that a number of lipids classes, namely glycerophosphocholines, glycerophosphoethanolamines, hexosyceramides, and sphingomyelins, were downregulated in the hippocampus of young male rats showing an impairment of spatial cognitive flexibility (Malikovic et al 2019). However, there is evidence that lipid processes in the frontal cortex are also involved the formation and consolidation of spatial reference memories (Moreira et al 2012;Zamzow et al 2019), probably based on the connections to the hippocampus.…”

Section: Introductionmentioning

confidence: 99%

Molecular species of oxidized phospholipids in brain differentiate between learning- and memory impaired and unimpaired aged rats

et al. 2022

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Loss of cognitive function is a typical consequence of aging in humans and rodents. The extent of decline in spatial memory performance of rats, assessed by a hole-board test, reaches from unimpaired and comparable to young individuals to severely memory impaired. Recently, proteomics identified peroxiredoxin 6, an enzyme important for detoxification of oxidized phospholipids, as one of several synaptosomal proteins discriminating between aged impaired and aged unimpaired rats. In this study, we investigated several components of the epilipidome (modifications of phospholipids) of the prefrontal cortex of young, aged memory impaired (AI) and aged unimpaired (AU) rats. We observed an age-related increase in phospholipid hydroperoxides and products of phospholipid peroxidation, including reactive aldehydophospholipids. This increase went in hand with cortical lipofuscin autofluorescence. The memory impairment, however, was paralleled by additional specific changes in the aged rat brain epilipidome. There was a profound increase in phosphocholine hydroxides, and a significant decrease in phosphocholine-esterified azelaic acid. As phospholipid-esterified fatty acid hydroxides, and especially those deriving from arachidonic acid are both markers and effectors of inflammation, the findings suggest that in addition to age-related reactive oxygen species (ROS) accumulation, age-related impairment of spatial memory performance has an additional and distinct (neuro-) inflammatory component.

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Moderate differences in common feeding diets change lipid composition in the hippocampal dentate gyrus and affect spatial cognitive flexibility in male rats

Cited by 6 publications

References 31 publications

Differences in Hypothalamic Lipid Profiles of Young and Aged Male Rats With Impaired and Unimpaired Spatial Cognitive Abilities and Memory

Differences in Hypothalamic Lipid Profiles of Young and Aged Male Rats With Impaired and Unimpaired Spatial Cognitive Abilities and Memory

Early Life to Adult Brain Lipidome Dynamic: A Temporospatial Study Investigating Dietary Polar Lipid Supplementation Efficacy

Molecular species of oxidized phospholipids in brain differentiate between learning- and memory impaired and unimpaired aged rats

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