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Targeted Suppression of Lipoprotein Receptor LSR in Astrocytes Leads to Olfactory and Memory Deficits in Mice

El Hajj, Aseel, Herzine, Ameziane, Calcagno, Gaetano, Désor, Frédéric, Djelti, Fathia, Bombail, Vincent, Denis, Isabelle, Oster, Thierry, Malaplate, Catherine, Vigier, Maxime, Kaminski, Sandra, Pauron, Lynn, Corbier, Catherine, Yen, Frances T., Lanhers, Marie-Claire, Claudepierre, Thomas·2022·International Journal of Molecular Sciences
DOI 10.3390/ijms23042049PMC PMC8878779
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Abstract

Perturbations of cholesterol metabolism have been linked to neurodegenerative diseases. Glia–neuron crosstalk is essential to achieve a tight regulation of brain cholesterol trafficking. Adequate cholesterol supply from glia via apolipoprotein E-containing lipoproteins ensures neuronal development and function. The lipolysis-stimulated lipoprotein receptor (LSR), plays an important role in brain cholesterol homeostasis. Aged heterozygote Lsr+/− mice show altered brain cholesterol distribution and increased susceptibility to amyloid stress. Since LSR expression is higher in astroglia as compared to neurons, we sought to determine if astroglial LSR deficiency could lead to cognitive defects similar to those of Alzheimer’s disease (AD). Cre recombinase was activated in adult Glast-CreERT/lsrfl/fl mice by tamoxifen to induce astroglial Lsr deletion. Behavioral phenotyping of young and old astroglial Lsr KO animals revealed hyperactivity during the nocturnal period, deficits in olfactory function affecting social memory and causing possible apathy, as well as visual memory and short-term working memory problems, and deficits similar to those reported in neurodegenerative diseases, such as AD. Furthermore, GFAP staining revealed astroglial activation in the olfactory bulb. Therefore, astroglial LSR is important for working, spatial, and social memory related to sensory input, and represents a novel pathway for the study of brain aging and neurodegeneration.

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Figure 1 Modification of gene expression in astroglial Lsr cKO mice. (A) Verification of Lsr gene excision in astroglial cells using RT-qPCR. Box plot presentation of fold expression of total Lsr and different Lsr subunits α, α’, and β in 13-month-old cKO mice (n = 5) with respect to WT mice (n = 5) in the hippocampus (a) and olfactory bulb (b). (B) Box plot presentation of fold expression of cholesterol-related gene expression in 13-month-old cKO mice (n = 5) with respect to WT mice (n = 5) in the hippocampus (a) and olfactory bulb (b). Abbreviations: abca1, ATP-binding cassette transporter 1; hmgcr, HMG CoA reductase; srebp1, sterol regulatory element-binding transcription factor 1; cyp46a1, cytochrome P450 family 46 subfamily A member 1. Statistical significance between WT and cKO mice is shown as: * p ≤ 0.05, ** p ≤ 0.01.
Figure 1 Modification of gene expression in astroglial Lsr cKO mice. (A) Verification of Lsr gene excision in astroglial cells using RT-qPCR. Box plot presentation of fold expression of total Lsr and different Lsr subunits α, α’, and β in 13-month-old cKO mice (n = 5) with respect to WT mice (n = 5) in the hippocampus (a) and olfactory bulb (b). (B) Box plot presentation of fold expression of cholesterol-related gene expression in 13-month-old cKO mice (n = 5) with respect to WT mice (n = 5) in the hippocampus (a) and olfactory bulb (b). Abbreviations: abca1, ATP-binding cassette transporter 1; hmgcr, HMG CoA reductase; srebp1, sterol regulatory element-binding transcription factor 1; cyp46a1, cytochrome P450 family 46 subfamily A member 1. Statistical significance between WT and cKO mice is shown as: * p ≤ 0.05, ** p ≤ 0.01.CC BY · PubMed Central
Figure 2 Activity assessment of astroglial Lsr cKO mice. (A) Home cage activity in WT (n = 18) and cKO (n = 16) mice. (a) Hourly measurements of walking time expressed as % over a 24 h period. (b) Sum of walking time in hours (h) during dark cycle, light cycle, and the sum of both cycles (whole period). (B) Open field test for WT (n = 20) and cKO (n =18) mice. (a) Time ratio spent in center (Z3) over that of periphery (Z1). (b) Distance ratio traveled in center (Z3) over that of periphery (Z1). (c) Time spent in Z3 for 3-month-old mice. (d) Distance traveled in Z3 for 3-month-old mice. (e) Time spent in Z3 for 8-month-old mice. (f) Distance traveled in Z3 for 8-month-old mice. (g) Time spent in Z1 for 8-month-old mice. (h) Distance traveled in Z1 for older 8-month-old mice. Statistical significance between WT vs. cKO mice is shown as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001; comparison of age (3 months and 8 months) is indicated as: # p ≤ 0.05, ### p ≤ 0.001.
Figure 2 Activity assessment of astroglial Lsr cKO mice. (A) Home cage activity in WT (n = 18) and cKO (n = 16) mice. (a) Hourly measurements of walking time expressed as % over a 24 h period. (b) Sum of walking time in hours (h) during dark cycle, light cycle, and the sum of both cycles (whole period). (B) Open field test for WT (n = 20) and cKO (n =18) mice. (a) Time ratio spent in center (Z3) over that of periphery (Z1). (b) Distance ratio traveled in center (Z3) over that of periphery (Z1). (c) Time spent in Z3 for 3-month-old mice. (d) Distance traveled in Z3 for 3-month-old mice. (e) Time spent in Z3 for 8-month-old mice. (f) Distance traveled in Z3 for 8-month-old mice. (g) Time spent in Z1 for 8-month-old mice. (h) Distance traveled in Z1 for older 8-month-old mice. Statistical significance between WT vs. cKO mice is shown as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001; comparison of age (3 months and 8 months) is indicated as: # p ≤ 0.05, ### p ≤ 0.001.CC BY · PubMed Central
Figure 3 Olfactory assessment in cKO mice. (A) Buried cookie test results for WT (n = 20) and cKO (n = 18) mice. (a) Time taken to take and eat the visible cookie in habituation phase. (b) Time taken to find buried cookie. (B) Habituation/cross-habituation test results for WT (n = 10) and cKO (n = 10) mice. This test consists of a 5 min habituation step to the tea ball (no odor), then three 1 min habituation sessions to mineral oil, followed by three 2 min habituation sessions to rose oil, and by three 2 min habituation sessions to female urine. The test then ended with a 2 min odor discrimination step to female urine containing 1% lemon oil (U + L). Statistical significance when comparing a single point between cKO vs. WT mice is represented as: * p ≤ 0.05, ** p ≤ 0.01. Statistical significance when comparing different sessions for same genotype are indicated as: # p ≤ 0.05, ### p ≤ 0.001.
Figure 3 Olfactory assessment in cKO mice. (A) Buried cookie test results for WT (n = 20) and cKO (n = 18) mice. (a) Time taken to take and eat the visible cookie in habituation phase. (b) Time taken to find buried cookie. (B) Habituation/cross-habituation test results for WT (n = 10) and cKO (n = 10) mice. This test consists of a 5 min habituation step to the tea ball (no odor), then three 1 min habituation sessions to mineral oil, followed by three 2 min habituation sessions to rose oil, and by three 2 min habituation sessions to female urine. The test then ended with a 2 min odor discrimination step to female urine containing 1% lemon oil (U + L). Statistical significance when comparing a single point between cKO vs. WT mice is represented as: * p ≤ 0.05, ** p ≤ 0.01. Statistical significance when comparing different sessions for same genotype are indicated as: # p ≤ 0.05, ### p ≤ 0.001.CC BY · PubMed Central
Figure 4 Vision and visual memory assessment of WT (n = 20) and cKO (n = 18) mice using object recognition test. (a) Session 1 (S1): exploration time for the same set of objects at position A and position B. (b) Total exploration time in S1 at 4.5 and 9 months of age. (c) Session 2 (S2): exploration time of an old object used in S1 and a novel object, which were positioned randomly in the apparatus. (d) Total exploration time in S2, in seconds, at 4.5 and 9 months of age. Statistical significance is shown as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001. ## p ≤ 0.01.
Figure 4 Vision and visual memory assessment of WT (n = 20) and cKO (n = 18) mice using object recognition test. (a) Session 1 (S1): exploration time for the same set of objects at position A and position B. (b) Total exploration time in S1 at 4.5 and 9 months of age. (c) Session 2 (S2): exploration time of an old object used in S1 and a novel object, which were positioned randomly in the apparatus. (d) Total exploration time in S2, in seconds, at 4.5 and 9 months of age. Statistical significance is shown as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001. ## p ≤ 0.01.CC BY · PubMed Central
Figure 5 Sociability and social novelty assessment of WT (n = 20) and cKO (n = 18) mice. 5- (a,b) and 10- (c,d) month-old mice. (a,c) Session 1 (S1): exploration time (s) of stranger 1 vs. empty cup. (b,e) Session 2: exploration time (s) of stranger 1 used in S1 and a novel stranger. (e) Total exploration time in S1, in seconds, at 5 and 10 months of age. (f) Total exploration time (s) in S2 at 5 and 10 months of age. Statistical significance between cKO and WT mice at a certain time point is represented as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001. Statistical significance with age in cKO and WT mice is represented as: # p ≤ 0.05, ### p ≤ 0.001.
Figure 5 Sociability and social novelty assessment of WT (n = 20) and cKO (n = 18) mice. 5- (a,b) and 10- (c,d) month-old mice. (a,c) Session 1 (S1): exploration time (s) of stranger 1 vs. empty cup. (b,e) Session 2: exploration time (s) of stranger 1 used in S1 and a novel stranger. (e) Total exploration time in S1, in seconds, at 5 and 10 months of age. (f) Total exploration time (s) in S2 at 5 and 10 months of age. Statistical significance between cKO and WT mice at a certain time point is represented as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001. Statistical significance with age in cKO and WT mice is represented as: # p ≤ 0.05, ### p ≤ 0.001.CC BY · PubMed Central
Figure 6 Short- and long-term memory assessment. (A) Y-maze for WT (n = 20) and cKO (n = 18) mice. (a) Alternation (%) at the ages of 4 and 9 months. (b) Total number of entries at the ages of 4 and 9 months. (B) Barnes maze for WT (n = 15) and cKO (n = 15) mice. (c) The time taken to find the escape chamber, measured 3 times per day for 5 consecutive days. On day 8, one single test session was performed to assess long-term memory. (d) Time taken to leave departure zone (Z1), measured 3 times per day for 5 consecutive days. Statistical significance between cKO and WT mice at different time points is represented as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001. Statistical significance with time in cKO or WT mice is represented as: ### p ≤ 0.001.
Figure 6 Short- and long-term memory assessment. (A) Y-maze for WT (n = 20) and cKO (n = 18) mice. (a) Alternation (%) at the ages of 4 and 9 months. (b) Total number of entries at the ages of 4 and 9 months. (B) Barnes maze for WT (n = 15) and cKO (n = 15) mice. (c) The time taken to find the escape chamber, measured 3 times per day for 5 consecutive days. On day 8, one single test session was performed to assess long-term memory. (d) Time taken to leave departure zone (Z1), measured 3 times per day for 5 consecutive days. Statistical significance between cKO and WT mice at different time points is represented as: * p ≤ 0.05, ** p ≤ 0.01, *** p ≤ 0.001. Statistical significance with time in cKO or WT mice is represented as: ### p ≤ 0.001.CC BY · PubMed Central
Figure 7 Astrocyte activation in astroglial Lsr in WT (n = 5) and cKO (n = 5) mice. (A) Sagittal brain section corresponding to the regions of interest. (B) Number of GFAP+ cells in different brain structures. Sagittal brain sections were stained with glial fibrillary acidic protein (GFAP). The measurements of the number of GFAP+ cells were the result of three sagittal sections analyzed per animal; the mean of all values represents one mouse. (C) Representative images from WT and cKO mice with GFAP staining (green) on sagittal sections counterstained with DAPI (nuclear blue staining). Scale bar 100 μm. Each value represents the mean ± SEM (** p < 0.01). Abbreviations: OB, olfactory bulb; Cx, cortex; Hp, hippocampus; DG, dentate gyrus; CA, cornu ammonis; SLM, stratum lacunosum-moleculare.
Figure 7 Astrocyte activation in astroglial Lsr in WT (n = 5) and cKO (n = 5) mice. (A) Sagittal brain section corresponding to the regions of interest. (B) Number of GFAP+ cells in different brain structures. Sagittal brain sections were stained with glial fibrillary acidic protein (GFAP). The measurements of the number of GFAP+ cells were the result of three sagittal sections analyzed per animal; the mean of all values represents one mouse. (C) Representative images from WT and cKO mice with GFAP staining (green) on sagittal sections counterstained with DAPI (nuclear blue staining). Scale bar 100 μm. Each value represents the mean ± SEM (** p < 0.01). Abbreviations: OB, olfactory bulb; Cx, cortex; Hp, hippocampus; DG, dentate gyrus; CA, cornu ammonis; SLM, stratum lacunosum-moleculare.CC BY · PubMed Central

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Authors
El Hajj, A., Herzine, A., Calcagno, G., Désor, F., Djelti, F., Bombail, V., Denis, I., Oster, T., Malaplate, C., Vigier, M., Kaminski, S., Pauron, L., Corbier, C., Yen, F. T., Lanhers, M.-C., & Claudepierre, T.
Affiliations
  • UR AFPA Laboratory, Qualivie Team, University of Lorraine, 54505 Vandoeuvre-lès-Nancy, France
  • UR 7300, Stress Immunity Pathogens Laboratory, Faculty of Medicine, University of Lorraine, 54500 Vandœuvre-lès-Nancy, France
  • UMR 914, Physiology of Nutrition and Feeding Behaviour, INRAE-Agroparistech-Université Paris-Saclay, 78352 Jouy-en-Josas, France
ORCID
Venue
International Journal of Molecular Sciences
Publisher
MDPI AG
Published
2022-02-12
Volume
23
Issue
4
Pages
2049
ISSN
1422-0067
DOI
10.3390/ijms23042049
PMC
PMC8878779
Cited by
9
References
7
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
  • Region Lorraine (N/A)
  • FEDER (N/A)
  • Fondation Alzheimer (N/A)
  • LUE Impact Biomolecules (N/A)
  • Ministry of Higher Education Research and Innovation (N/A)
  • Inserm (N/A)

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