An amyloid β42-dependent deficit in anandamide mobilization is associated with cognitive dysfunction in Alzheimer's disease
The endocannabinoids and their attending cannabinoid (CB)1 receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analy...
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| Published in | Neurobiology of aging Vol. 33; no. 8; pp. 1522 - 1532 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.08.2012
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0197-4580 1558-1497 1558-1497 |
| DOI | 10.1016/j.neurobiolaging.2011.03.012 |
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| Abstract | The endocannabinoids and their attending cannabinoid (CB)1 receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of postmortem brain samples from 38 Alzheimer's disease (AD) patients and 17 control subjects, matched for age and postmortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl-sn-glycero-phosphoethanolamine-N-arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl-sn-glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (1) anandamide content in midfrontal cortex and scores of the Kendrick's Digit Copy test (p = 0.004, r = 0.81; n = 10), which measures speed of information processing; and (2) anandamide content in temporal cortex and scores of the Boston Naming test (p = 0.027, r = 0.52; n = 18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, amyloid β-protein (Aβ)42, while showing no association with Aβ40 levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ42 in Swedish mutant form of amyloid precursor protein (APPSWE)/Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ42-dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD. |
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| AbstractList | The endocannabinoids and their attending cannabinoid (CB)1 receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of postmortem brain samples from 38 Alzheimer's disease (AD) patients and 17 control subjects, matched for age and postmortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl-sn-glycero-phosphoethanolamine-N-arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl-sn-glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (1) anandamide content in midfrontal cortex and scores of the Kendrick's Digit Copy test (p = 0.004, r = 0.81; n = 10), which measures speed of information processing; and (2) anandamide content in temporal cortex and scores of the Boston Naming test (p = 0.027, r = 0.52; n = 18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, amyloid β-protein (Aβ)42, while showing no association with Aβ40 levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ42 in Swedish mutant form of amyloid precursor protein (APPSWE)/Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ42-dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD. The endocannabinoids and their attending cannabinoid (CB)(1) receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of postmortem brain samples from 38 Alzheimer's disease (AD) patients and 17 control subjects, matched for age and postmortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl-sn-glycero-phosphoethanolamine-N-arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl-sn-glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (1) anandamide content in midfrontal cortex and scores of the Kendrick's Digit Copy test (p = 0.004, r = 0.81; n = 10), which measures speed of information processing; and (2) anandamide content in temporal cortex and scores of the Boston Naming test (p = 0.027, r = 0.52; n = 18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, amyloid β-protein (Aβ)(42), while showing no association with Aβ(40) levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ(42) in Swedish mutant form of amyloid precursor protein (APP(SWE))/Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ(42)-dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD.The endocannabinoids and their attending cannabinoid (CB)(1) receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of postmortem brain samples from 38 Alzheimer's disease (AD) patients and 17 control subjects, matched for age and postmortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl-sn-glycero-phosphoethanolamine-N-arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl-sn-glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (1) anandamide content in midfrontal cortex and scores of the Kendrick's Digit Copy test (p = 0.004, r = 0.81; n = 10), which measures speed of information processing; and (2) anandamide content in temporal cortex and scores of the Boston Naming test (p = 0.027, r = 0.52; n = 18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, amyloid β-protein (Aβ)(42), while showing no association with Aβ(40) levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ(42) in Swedish mutant form of amyloid precursor protein (APP(SWE))/Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ(42)-dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD. Abstract The endocannabinoids and their attending cannabinoid (CB)1 receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of postmortem brain samples from 38 Alzheimer's disease (AD) patients and 17 control subjects, matched for age and postmortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl- sn -glycero-phosphoethanolamine- N -arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl- sn -glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (1) anandamide content in midfrontal cortex and scores of the Kendrick's Digit Copy test ( p = 0.004, r = 0.81; n = 10), which measures speed of information processing; and (2) anandamide content in temporal cortex and scores of the Boston Naming test ( p = 0.027, r = 0.52; n = 18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, amyloid β-protein (Aβ)42 , while showing no association with Aβ40 levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ42 in Swedish mutant form of amyloid precursor protein (APPSWE )/Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ42 -dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD. The endocannabinoids and their attending CB 1 cannabinoid receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of post mortem brain samples from 38 Alzheimer’s disease (AD) patients and 17 control subjects, matched for age and post mortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl- sn -glycero-phosphoethanolamine- N -arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl- sn -glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (a) anandamide content in midfrontal cortex and scores of the Kendrick’s digit copying test ( P =0.004, r=0.81; n =10), which measures speed of information processing; and (b) anandamide content in temporal cortex and scores of the Boston naming test ( P =0.027, r=0.52; n =18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, Aβ 42 , while showing no association with Aβ 40 levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ 42 in APP SWE /Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ 42 -dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD. The endocannabinoids and their attending cannabinoid (CB)(1) receptors have been implicated in the control of cognition, but their possible roles in dementias are still unclear. In the present study, we used liquid chromatography/mass spectrometry to conduct an endocannabinoid-targeted lipidomic analysis of postmortem brain samples from 38 Alzheimer's disease (AD) patients and 17 control subjects, matched for age and postmortem interval. The analysis revealed that midfrontal and temporal cortex tissue from AD patients contains, relative to control subjects, significantly lower levels of the endocannabinoid anandamide and its precursor 1-stearoyl, 2-docosahexaenoyl-sn-glycero-phosphoethanolamine-N-arachidonoyl (NArPE). No such difference was observed with the endocannabinoid 2-arachidonoyl-sn-glycerol or 15 additional lipid species. In AD patients, but not in control subjects, statistically detectable positive correlations were found between (1) anandamide content in midfrontal cortex and scores of the Kendrick's Digit Copy test (p = 0.004, r = 0.81; n = 10), which measures speed of information processing; and (2) anandamide content in temporal cortex and scores of the Boston Naming test (p = 0.027, r = 0.52; n = 18), which assesses language facility. Furthermore, anandamide and NArPE levels in midfrontal cortex of the study subjects inversely correlated with levels of the neurotoxic amyloid peptide, amyloid β-protein (Aβ)(42), while showing no association with Aβ(40) levels, amyloid plaque load or tau protein phosphorylation. Finally, high endogenous levels of Aβ(42) in Swedish mutant form of amyloid precursor protein (APP(SWE))/Neuro-2a cells directly reduced anandamide and NArPE concentrations in cells lysates. The results suggest that an Aβ(42)-dependent impairment in brain anandamide mobilization contributes to cognitive dysfunction in AD. |
| Author | Astarita, Giuseppe Cotman, Carl W. Cribbs, David H. Piomelli, Daniele Jung, Kwang-Mook Vasilevko, Vitaly Head, Elizabeth Yasar, Sevil |
| AuthorAffiliation | a Department of Pharmacology, University of California, Irvine, Irvine, CA, USA, 92697 d Division of Geriatric Medicine and Gerontology, Johns Hopkins University School of Medicine, Baltimore, MD, USA, 21224 b Department of Biological Chemistry, University of California, Irvine, Irvine, CA, USA, 92697 e Unit of Drug Discovery and Development, Italian Institute of Technology, Genova, Italy c Institute for Memory Impairments and Neurological Disorders, University of California, Irvine, Irvine, CA, USA, 92697 |
| AuthorAffiliation_xml | – name: c Institute for Memory Impairments and Neurological Disorders, University of California, Irvine, Irvine, CA, USA, 92697 – name: a Department of Pharmacology, University of California, Irvine, Irvine, CA, USA, 92697 – name: b Department of Biological Chemistry, University of California, Irvine, Irvine, CA, USA, 92697 – name: d Division of Geriatric Medicine and Gerontology, Johns Hopkins University School of Medicine, Baltimore, MD, USA, 21224 – name: e Unit of Drug Discovery and Development, Italian Institute of Technology, Genova, Italy |
| Author_xml | – sequence: 1 givenname: Kwang-Mook surname: Jung fullname: Jung, Kwang-Mook organization: Department of Pharmacology, University of California, Irvine, Irvine, CA, USA – sequence: 2 givenname: Giuseppe surname: Astarita fullname: Astarita, Giuseppe organization: Department of Pharmacology, University of California, Irvine, Irvine, CA, USA – sequence: 3 givenname: Sevil surname: Yasar fullname: Yasar, Sevil organization: Division of Geriatric Medicine and Gerontology, Johns Hopkins University School of Medicine, Baltimore, MD, USA – sequence: 4 givenname: Vitaly surname: Vasilevko fullname: Vasilevko, Vitaly organization: Institute for Memory Impairments and Neurological Disorders, University of California, Irvine, Irvine, CA, USA – sequence: 5 givenname: David H. surname: Cribbs fullname: Cribbs, David H. organization: Institute for Memory Impairments and Neurological Disorders, University of California, Irvine, Irvine, CA, USA – sequence: 6 givenname: Elizabeth surname: Head fullname: Head, Elizabeth organization: Institute for Memory Impairments and Neurological Disorders, University of California, Irvine, Irvine, CA, USA – sequence: 7 givenname: Carl W. surname: Cotman fullname: Cotman, Carl W. organization: Institute for Memory Impairments and Neurological Disorders, University of California, Irvine, Irvine, CA, USA – sequence: 8 givenname: Daniele surname: Piomelli fullname: Piomelli, Daniele email: piomelli@uci.edu organization: Department of Pharmacology, University of California, Irvine, Irvine, CA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21546126$$D View this record in MEDLINE/PubMed |
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| Copyright | 2012 Elsevier Inc. Elsevier Inc. Copyright © 2012 Elsevier Inc. All rights reserved. 2011 Elsevier Inc. All rights reserved. 2011 |
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| Keywords | Endocannabinoid Amyloid β42 Human brain Lipidomics Alzheimer's disease Cognitive dysfunction Anandamide Amyloid β 42 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 ObjectType-Undefined-3 Present address: Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY, USA Department of Molecular and Cellular Biochemistry, University of Kentucky, Lexington, KY, USA, 40506. K.-M.J. and G.A. contributed equally to this work. |
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| Snippet | The endocannabinoids and their attending cannabinoid (CB)1 receptors have been implicated in the control of cognition, but their possible roles in dementias... Abstract The endocannabinoids and their attending cannabinoid (CB)1 receptors have been implicated in the control of cognition, but their possible roles in... The endocannabinoids and their attending cannabinoid (CB)(1) receptors have been implicated in the control of cognition, but their possible roles in dementias... The endocannabinoids and their attending CB 1 cannabinoid receptors have been implicated in the control of cognition, but their possible roles in dementias are... |
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| SubjectTerms | Aged Alzheimer Disease - metabolism Alzheimer's disease Amyloid beta-Peptides - metabolism Amyloid β42 Anandamide Arachidonic Acids - metabolism Cadaver Cerebral Cortex - metabolism Cognition Disorders - metabolism Cognitive dysfunction Endocannabinoid Endocannabinoids Female Human brain Humans Internal Medicine Lipid Metabolism Lipidomics Male Neurology Peptide Fragments - metabolism Polyunsaturated Alkamides - metabolism Tissue Distribution |
| Title | An amyloid β42-dependent deficit in anandamide mobilization is associated with cognitive dysfunction in Alzheimer's disease |
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