Progressive white matter atrophy with altered lipid profiles is partially reversed by short-term abstinence in an experimental model of alcohol-related neurodegeneration
Chronic ethanol exposure causes white matter (WM) atrophy and degeneration with major impairments in the structural integrity of myelin. Since myelin is composed of oligodendrocyte lipid-rich membranes, understanding the consequences and reversibility of alcohol-related oligodendrocyte dysfunction i...
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| description | Chronic ethanol exposure causes white matter (WM) atrophy and degeneration with major impairments in the structural integrity of myelin. Since myelin is composed of oligodendrocyte lipid-rich membranes, understanding the consequences and reversibility of alcohol-related oligodendrocyte dysfunction in relation to myelin structure could provide new insights into the pathogenesis of WM degeneration and potential strategies for treatment. Adult male Long Evans rats were pair-fed with isocaloric liquid diets containing 0% or 26% ethanol (caloric) for 3 or 8 weeks. During the last 2 weeks of feeding, the ethanol groups were binged with 2 g/kg of ethanol by intraperitoneal (i.p.) injection on Mondays, Wednesdays, and Fridays; controls were treated with i.p. saline. For recovery effects, at the 6-week time point, ethanol exposures were tapered over 2 days, and then discontinued, rendering the rats ethanol-free for 12 days. Anterior corpus callosum WM lipid ion profiles were analyzed using matrix-assisted laser desorption ionization-imaging mass spectrometry (MALDI-IMS) and correlated with histopathology. Ethanol exposures caused progressive atrophy and reductions in myelin staining intensity within the corpus callosum, whereas short-term recovery partially reversed those effects. MALDI-IMS demonstrated striking ethanol-associated alterations in WM lipid profiles characterized by reduced levels of phosphatidylinositols, phosphatidylserines, phosphatidylethanolamines, and sulfatides, and partial “normalization” of lipid expression with recovery. Ethanol exposure duration and recovery responses were further distinguished by heatmap hierarchical dendrogram and PCA plots. In conclusion, chronic+binge ethanol exposures caused progressive, partially reversible WM atrophy with myelin loss associated with reduced expression of WM phospholipids and sulfatides. The extent of WM lipid abnormalities suggests that ethanol broadly impairs molecular and biochemical functions regulating myelin synthesis, degradation, and maintenance in oligodendrocytes.
•Chronic ethanol exposure broadly alters cerebral white matter myelin lipid profiles.•Ethanol reduces white matter expression of sulfatides and various phospholipids.•Short-term recovery partly reverses ethanol's effects on myelin lipid profiles. |
| doi_str_mv | 10.1016/j.alcohol.2017.05.008 |
| format | Article |
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•Chronic ethanol exposure broadly alters cerebral white matter myelin lipid profiles.•Ethanol reduces white matter expression of sulfatides and various phospholipids.•Short-term recovery partly reverses ethanol's effects on myelin lipid profiles.</description><identifier>ISSN: 0741-8329</identifier><identifier>EISSN: 1873-6823</identifier><identifier>DOI: 10.1016/j.alcohol.2017.05.008</identifier><identifier>PMID: 29084630</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Abstinence ; Alcohol Abstinence - trends ; Alcohol recovery ; Alcohol use ; Alcoholic beverages ; Alcoholism ; Alcoholism - metabolism ; Alcoholism - pathology ; Alcohols ; Animal cognition ; Animals ; Atrophy ; Brain research ; Chronic+binge alcohol ; Cognitive ability ; Corpus callosum ; Dementia ; Disease Models, Animal ; Drug abuse ; Ethanol ; Ethanol - administration & dosage ; Ethanol - toxicity ; Exposure ; Histopathology ; Imaging mass spectrometry ; Insulin resistance ; Ionization ; Lipid Metabolism - physiology ; Lipids ; MALDI ; Male ; Mass spectrometry ; Mass spectroscopy ; Membranes ; Myelin ; Neurodegeneration ; Neurodegenerative Diseases - chemically induced ; Neurodegenerative Diseases - metabolism ; Neurodegenerative Diseases - pathology ; Neurosciences ; Nicotine ; Oligodendrocytes ; Pathogenesis ; Pathology ; Phospholipids ; Rats ; Rats, Long-Evans ; Recovery (Medical) ; Rodents ; Scientific imaging ; Signal transduction ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods ; Substantia alba ; Time Factors ; White Matter - drug effects ; White Matter - metabolism ; White Matter - pathology</subject><ispartof>Alcohol (Fayetteville, N.Y.), 2017-12, Vol.65, p.51-62</ispartof><rights>2017 Elsevier Inc.</rights><rights>Copyright © 2017 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c495t-a2abcbdf5d67fac65706a0f261b003abd08c7536da280c15dcf8ad678b59cfb23</citedby><cites>FETCH-LOGICAL-c495t-a2abcbdf5d67fac65706a0f261b003abd08c7536da280c15dcf8ad678b59cfb23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S074183291730229X$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29084630$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yalcin, Emine B.</creatorcontrib><creatorcontrib>McLean, Tory</creatorcontrib><creatorcontrib>Tong, Ming</creatorcontrib><creatorcontrib>de la Monte, Suzanne M.</creatorcontrib><title>Progressive white matter atrophy with altered lipid profiles is partially reversed by short-term abstinence in an experimental model of alcohol-related neurodegeneration</title><title>Alcohol (Fayetteville, N.Y.)</title><addtitle>Alcohol</addtitle><description>Chronic ethanol exposure causes white matter (WM) atrophy and degeneration with major impairments in the structural integrity of myelin. Since myelin is composed of oligodendrocyte lipid-rich membranes, understanding the consequences and reversibility of alcohol-related oligodendrocyte dysfunction in relation to myelin structure could provide new insights into the pathogenesis of WM degeneration and potential strategies for treatment. Adult male Long Evans rats were pair-fed with isocaloric liquid diets containing 0% or 26% ethanol (caloric) for 3 or 8 weeks. During the last 2 weeks of feeding, the ethanol groups were binged with 2 g/kg of ethanol by intraperitoneal (i.p.) injection on Mondays, Wednesdays, and Fridays; controls were treated with i.p. saline. For recovery effects, at the 6-week time point, ethanol exposures were tapered over 2 days, and then discontinued, rendering the rats ethanol-free for 12 days. Anterior corpus callosum WM lipid ion profiles were analyzed using matrix-assisted laser desorption ionization-imaging mass spectrometry (MALDI-IMS) and correlated with histopathology. Ethanol exposures caused progressive atrophy and reductions in myelin staining intensity within the corpus callosum, whereas short-term recovery partially reversed those effects. MALDI-IMS demonstrated striking ethanol-associated alterations in WM lipid profiles characterized by reduced levels of phosphatidylinositols, phosphatidylserines, phosphatidylethanolamines, and sulfatides, and partial “normalization” of lipid expression with recovery. Ethanol exposure duration and recovery responses were further distinguished by heatmap hierarchical dendrogram and PCA plots. In conclusion, chronic+binge ethanol exposures caused progressive, partially reversible WM atrophy with myelin loss associated with reduced expression of WM phospholipids and sulfatides. The extent of WM lipid abnormalities suggests that ethanol broadly impairs molecular and biochemical functions regulating myelin synthesis, degradation, and maintenance in oligodendrocytes.
•Chronic ethanol exposure broadly alters cerebral white matter myelin lipid profiles.•Ethanol reduces white matter expression of sulfatides and various phospholipids.•Short-term recovery partly reverses ethanol's effects on myelin lipid profiles.</description><subject>Abstinence</subject><subject>Alcohol Abstinence - trends</subject><subject>Alcohol recovery</subject><subject>Alcohol use</subject><subject>Alcoholic beverages</subject><subject>Alcoholism</subject><subject>Alcoholism - metabolism</subject><subject>Alcoholism - pathology</subject><subject>Alcohols</subject><subject>Animal cognition</subject><subject>Animals</subject><subject>Atrophy</subject><subject>Brain research</subject><subject>Chronic+binge alcohol</subject><subject>Cognitive ability</subject><subject>Corpus callosum</subject><subject>Dementia</subject><subject>Disease Models, Animal</subject><subject>Drug abuse</subject><subject>Ethanol</subject><subject>Ethanol - administration & dosage</subject><subject>Ethanol - toxicity</subject><subject>Exposure</subject><subject>Histopathology</subject><subject>Imaging mass spectrometry</subject><subject>Insulin resistance</subject><subject>Ionization</subject><subject>Lipid Metabolism - physiology</subject><subject>Lipids</subject><subject>MALDI</subject><subject>Male</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Membranes</subject><subject>Myelin</subject><subject>Neurodegeneration</subject><subject>Neurodegenerative Diseases - chemically induced</subject><subject>Neurodegenerative Diseases - metabolism</subject><subject>Neurodegenerative Diseases - pathology</subject><subject>Neurosciences</subject><subject>Nicotine</subject><subject>Oligodendrocytes</subject><subject>Pathogenesis</subject><subject>Pathology</subject><subject>Phospholipids</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><subject>Recovery (Medical)</subject><subject>Rodents</subject><subject>Scientific imaging</subject><subject>Signal transduction</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - 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trends</topic><topic>Alcohol recovery</topic><topic>Alcohol use</topic><topic>Alcoholic beverages</topic><topic>Alcoholism</topic><topic>Alcoholism - metabolism</topic><topic>Alcoholism - pathology</topic><topic>Alcohols</topic><topic>Animal cognition</topic><topic>Animals</topic><topic>Atrophy</topic><topic>Brain research</topic><topic>Chronic+binge alcohol</topic><topic>Cognitive ability</topic><topic>Corpus callosum</topic><topic>Dementia</topic><topic>Disease Models, Animal</topic><topic>Drug abuse</topic><topic>Ethanol</topic><topic>Ethanol - administration & dosage</topic><topic>Ethanol - toxicity</topic><topic>Exposure</topic><topic>Histopathology</topic><topic>Imaging mass spectrometry</topic><topic>Insulin resistance</topic><topic>Ionization</topic><topic>Lipid Metabolism - physiology</topic><topic>Lipids</topic><topic>MALDI</topic><topic>Male</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Membranes</topic><topic>Myelin</topic><topic>Neurodegeneration</topic><topic>Neurodegenerative Diseases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Alcohol (Fayetteville, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yalcin, Emine B.</au><au>McLean, Tory</au><au>Tong, Ming</au><au>de la Monte, Suzanne M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Progressive white matter atrophy with altered lipid profiles is partially reversed by short-term abstinence in an experimental model of alcohol-related neurodegeneration</atitle><jtitle>Alcohol (Fayetteville, N.Y.)</jtitle><addtitle>Alcohol</addtitle><date>2017-12-01</date><risdate>2017</risdate><volume>65</volume><spage>51</spage><epage>62</epage><pages>51-62</pages><issn>0741-8329</issn><eissn>1873-6823</eissn><abstract>Chronic ethanol exposure causes white matter (WM) atrophy and degeneration with major impairments in the structural integrity of myelin. Since myelin is composed of oligodendrocyte lipid-rich membranes, understanding the consequences and reversibility of alcohol-related oligodendrocyte dysfunction in relation to myelin structure could provide new insights into the pathogenesis of WM degeneration and potential strategies for treatment. Adult male Long Evans rats were pair-fed with isocaloric liquid diets containing 0% or 26% ethanol (caloric) for 3 or 8 weeks. During the last 2 weeks of feeding, the ethanol groups were binged with 2 g/kg of ethanol by intraperitoneal (i.p.) injection on Mondays, Wednesdays, and Fridays; controls were treated with i.p. saline. For recovery effects, at the 6-week time point, ethanol exposures were tapered over 2 days, and then discontinued, rendering the rats ethanol-free for 12 days. Anterior corpus callosum WM lipid ion profiles were analyzed using matrix-assisted laser desorption ionization-imaging mass spectrometry (MALDI-IMS) and correlated with histopathology. Ethanol exposures caused progressive atrophy and reductions in myelin staining intensity within the corpus callosum, whereas short-term recovery partially reversed those effects. MALDI-IMS demonstrated striking ethanol-associated alterations in WM lipid profiles characterized by reduced levels of phosphatidylinositols, phosphatidylserines, phosphatidylethanolamines, and sulfatides, and partial “normalization” of lipid expression with recovery. Ethanol exposure duration and recovery responses were further distinguished by heatmap hierarchical dendrogram and PCA plots. In conclusion, chronic+binge ethanol exposures caused progressive, partially reversible WM atrophy with myelin loss associated with reduced expression of WM phospholipids and sulfatides. The extent of WM lipid abnormalities suggests that ethanol broadly impairs molecular and biochemical functions regulating myelin synthesis, degradation, and maintenance in oligodendrocytes.
•Chronic ethanol exposure broadly alters cerebral white matter myelin lipid profiles.•Ethanol reduces white matter expression of sulfatides and various phospholipids.•Short-term recovery partly reverses ethanol's effects on myelin lipid profiles.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>29084630</pmid><doi>10.1016/j.alcohol.2017.05.008</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Alcohol (Fayetteville, N.Y.), 2017-12, Vol.65, p.51-62 |
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| source | MEDLINE; Elsevier ScienceDirect Journals Complete |
| subjects | Abstinence Alcohol Abstinence - trends Alcohol recovery Alcohol use Alcoholic beverages Alcoholism Alcoholism - metabolism Alcoholism - pathology Alcohols Animal cognition Animals Atrophy Brain research Chronic+binge alcohol Cognitive ability Corpus callosum Dementia Disease Models, Animal Drug abuse Ethanol Ethanol - administration & dosage Ethanol - toxicity Exposure Histopathology Imaging mass spectrometry Insulin resistance Ionization Lipid Metabolism - physiology Lipids MALDI Male Mass spectrometry Mass spectroscopy Membranes Myelin Neurodegeneration Neurodegenerative Diseases - chemically induced Neurodegenerative Diseases - metabolism Neurodegenerative Diseases - pathology Neurosciences Nicotine Oligodendrocytes Pathogenesis Pathology Phospholipids Rats Rats, Long-Evans Recovery (Medical) Rodents Scientific imaging Signal transduction Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization - methods Substantia alba Time Factors White Matter - drug effects White Matter - metabolism White Matter - pathology |
| title | Progressive white matter atrophy with altered lipid profiles is partially reversed by short-term abstinence in an experimental model of alcohol-related neurodegeneration |
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