Maternal Repetitive Hypoxia Prior to Mating Confers Epigenetic Resilience to Memory Impairment in Male Progeny
We showed previously in a mouse model of vascular cognitive impairment and dementia involving chronic cerebral hypoperfusion (CCH) that repetitive hypoxic conditioning (RHC) of both parents results in the epigenetic, intergenerational transmission of resilience to recognition memory loss in adult pr...
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| Veröffentlicht in: | Behavioral neuroscience 2023-06, Vol.137 (3), p.178-183 |
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| creator | Broyles, Emrey E. Corell, David H. Gidday, Jeffrey M. |
| description | We showed previously in a mouse model of vascular cognitive impairment and dementia involving chronic cerebral hypoperfusion (CCH) that repetitive hypoxic conditioning (RHC) of both parents results in the epigenetic, intergenerational transmission of resilience to recognition memory loss in adult progeny, as assessed by the novel object recognition test. The present study was undertaken in the same model to determine whether RHC treatment of one or both parents is required to confer dementia resilience intergenerationally. We found inherited resilience to 3 months of CCH in males is maternally mediated (p = .006). Statistically, we observed a strong trend for the paternal germline to contribute as well (p = .052). We also found that, in contrast to what is widely observed in males, females display intact recognition memory (p = .001) after 3 months of CCH, revealing a heretofore unidentified sexual dimorphism with respect to cognitive impact during disease progression. Overall, results of our study strongly implicate epigenetic changes in maternal germ cells, induced by our repetitive systemic hypoxic stimulus, contributing to a modified differentiation program capable of establishing a dementia-resilient phenotype in adult male first-generation progeny. |
| doi_str_mv | 10.1037/bne0000554 |
| format | Article |
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The present study was undertaken in the same model to determine whether RHC treatment of one or both parents is required to confer dementia resilience intergenerationally. We found inherited resilience to 3 months of CCH in males is maternally mediated (p = .006). Statistically, we observed a strong trend for the paternal germline to contribute as well (p = .052). We also found that, in contrast to what is widely observed in males, females display intact recognition memory (p = .001) after 3 months of CCH, revealing a heretofore unidentified sexual dimorphism with respect to cognitive impact during disease progression. Overall, results of our study strongly implicate epigenetic changes in maternal germ cells, induced by our repetitive systemic hypoxic stimulus, contributing to a modified differentiation program capable of establishing a dementia-resilient phenotype in adult male first-generation progeny.</description><identifier>ISSN: 0735-7044</identifier><identifier>ISSN: 1939-0084</identifier><identifier>EISSN: 1939-0084</identifier><identifier>DOI: 10.1037/bne0000554</identifier><identifier>PMID: 36862475</identifier><language>eng</language><publisher>United States: American Psychological Association</publisher><subject>Animal ; Animals ; Anoxia ; Brain Ischemia ; Cognitive ability ; Cognitive Dysfunction - genetics ; Dementia ; Dementia disorders ; Disease Models, Animal ; Disease transmission ; Epigenesis, Genetic ; Epigenetics ; Female ; Germ cells ; Hypoxia ; Male ; Males ; Memory ; Memory Disorders ; Memory Disorders - genetics ; Mice ; Offspring ; Pattern recognition ; Phenotypes ; Recognition (Learning) ; Resilience (Psychological) ; Sexual dimorphism ; Transgenerational Patterns ; Vascular dementia</subject><ispartof>Behavioral neuroscience, 2023-06, Vol.137 (3), p.178-183</ispartof><rights>2023 American Psychological Association</rights><rights>2023, American Psychological Association</rights><rights>Copyright American Psychological Association Jun 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a472t-16c95b678f49faf75f81668811c54fac09dcaf0d040dfb36c77ba6b432dd622e3</citedby><orcidid>0000-0002-4641-0465</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36862475$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Schoenbaum, Geoffrey</contributor><creatorcontrib>Broyles, Emrey E.</creatorcontrib><creatorcontrib>Corell, David H.</creatorcontrib><creatorcontrib>Gidday, Jeffrey M.</creatorcontrib><title>Maternal Repetitive Hypoxia Prior to Mating Confers Epigenetic Resilience to Memory Impairment in Male Progeny</title><title>Behavioral neuroscience</title><addtitle>Behav Neurosci</addtitle><description>We showed previously in a mouse model of vascular cognitive impairment and dementia involving chronic cerebral hypoperfusion (CCH) that repetitive hypoxic conditioning (RHC) of both parents results in the epigenetic, intergenerational transmission of resilience to recognition memory loss in adult progeny, as assessed by the novel object recognition test. The present study was undertaken in the same model to determine whether RHC treatment of one or both parents is required to confer dementia resilience intergenerationally. We found inherited resilience to 3 months of CCH in males is maternally mediated (p = .006). Statistically, we observed a strong trend for the paternal germline to contribute as well (p = .052). We also found that, in contrast to what is widely observed in males, females display intact recognition memory (p = .001) after 3 months of CCH, revealing a heretofore unidentified sexual dimorphism with respect to cognitive impact during disease progression. Overall, results of our study strongly implicate epigenetic changes in maternal germ cells, induced by our repetitive systemic hypoxic stimulus, contributing to a modified differentiation program capable of establishing a dementia-resilient phenotype in adult male first-generation progeny.</description><subject>Animal</subject><subject>Animals</subject><subject>Anoxia</subject><subject>Brain Ischemia</subject><subject>Cognitive ability</subject><subject>Cognitive Dysfunction - genetics</subject><subject>Dementia</subject><subject>Dementia disorders</subject><subject>Disease Models, Animal</subject><subject>Disease transmission</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>Female</subject><subject>Germ cells</subject><subject>Hypoxia</subject><subject>Male</subject><subject>Males</subject><subject>Memory</subject><subject>Memory Disorders</subject><subject>Memory Disorders - genetics</subject><subject>Mice</subject><subject>Offspring</subject><subject>Pattern recognition</subject><subject>Phenotypes</subject><subject>Recognition (Learning)</subject><subject>Resilience (Psychological)</subject><subject>Sexual dimorphism</subject><subject>Transgenerational Patterns</subject><subject>Vascular dementia</subject><issn>0735-7044</issn><issn>1939-0084</issn><issn>1939-0084</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc1u1DAUhS0EokNhwwOgSGwQYsBO_JcVQqNCKxWBEKwtx7keXCV2sJOKvD13mFJ-Fnjjhb_76R4fQh4z-pLRRr3qIlA8QvA7ZMPapt1SqvldsqGqEVtFOT8hD0q5QoZTLu6Tk0ZqWXMlNiS-tzPkaIfqE0wwhzlcQ3W-Tul7sNXHHFKu5lQhFOK-2qXoIZfqbAp7iEg7nCphCBAd_ORgTHmtLsbJhjxCnKsQcXgAVCUcWR-Se94OBR7d3Kfky9uzz7vz7eWHdxe7N5dby1U9b5l0reik0p633nolvGZSas2YE9xbR9veWU97zNP7rpFOqc7Kjjd138u6huaUvD56p6UboXe4SraDmXIYbV5NssH8_RLDV7NP14ZRXetWaDQ8uzHk9G2BMpsxFAfDYCOkpZha4Uo1U5Ij-vQf9Cothz9FSjNOBVXq_xS6mpppTZF6fqRcTqVk8Lc7M2oObZvfbSP85M-Ut-ivehF4cQTsZM1UVmczljZAcUvOmPwgMwyljWFKNz8AWcC1mA</recordid><startdate>20230601</startdate><enddate>20230601</enddate><creator>Broyles, Emrey E.</creator><creator>Corell, David H.</creator><creator>Gidday, Jeffrey M.</creator><general>American Psychological Association</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7RZ</scope><scope>PSYQQ</scope><scope>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4641-0465</orcidid></search><sort><creationdate>20230601</creationdate><title>Maternal Repetitive Hypoxia Prior to Mating Confers Epigenetic Resilience to Memory Impairment in Male Progeny</title><author>Broyles, Emrey E. ; Corell, David H. ; Gidday, Jeffrey M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a472t-16c95b678f49faf75f81668811c54fac09dcaf0d040dfb36c77ba6b432dd622e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animal</topic><topic>Animals</topic><topic>Anoxia</topic><topic>Brain Ischemia</topic><topic>Cognitive ability</topic><topic>Cognitive Dysfunction - genetics</topic><topic>Dementia</topic><topic>Dementia disorders</topic><topic>Disease Models, Animal</topic><topic>Disease transmission</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetics</topic><topic>Female</topic><topic>Germ cells</topic><topic>Hypoxia</topic><topic>Male</topic><topic>Males</topic><topic>Memory</topic><topic>Memory Disorders</topic><topic>Memory Disorders - genetics</topic><topic>Mice</topic><topic>Offspring</topic><topic>Pattern recognition</topic><topic>Phenotypes</topic><topic>Recognition (Learning)</topic><topic>Resilience (Psychological)</topic><topic>Sexual dimorphism</topic><topic>Transgenerational Patterns</topic><topic>Vascular dementia</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Broyles, Emrey E.</creatorcontrib><creatorcontrib>Corell, David H.</creatorcontrib><creatorcontrib>Gidday, Jeffrey M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>APA PsycArticles®</collection><collection>ProQuest One Psychology</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Behavioral neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Broyles, Emrey E.</au><au>Corell, David H.</au><au>Gidday, Jeffrey M.</au><au>Schoenbaum, Geoffrey</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Maternal Repetitive Hypoxia Prior to Mating Confers Epigenetic Resilience to Memory Impairment in Male Progeny</atitle><jtitle>Behavioral neuroscience</jtitle><addtitle>Behav Neurosci</addtitle><date>2023-06-01</date><risdate>2023</risdate><volume>137</volume><issue>3</issue><spage>178</spage><epage>183</epage><pages>178-183</pages><issn>0735-7044</issn><issn>1939-0084</issn><eissn>1939-0084</eissn><abstract>We showed previously in a mouse model of vascular cognitive impairment and dementia involving chronic cerebral hypoperfusion (CCH) that repetitive hypoxic conditioning (RHC) of both parents results in the epigenetic, intergenerational transmission of resilience to recognition memory loss in adult progeny, as assessed by the novel object recognition test. The present study was undertaken in the same model to determine whether RHC treatment of one or both parents is required to confer dementia resilience intergenerationally. We found inherited resilience to 3 months of CCH in males is maternally mediated (p = .006). Statistically, we observed a strong trend for the paternal germline to contribute as well (p = .052). We also found that, in contrast to what is widely observed in males, females display intact recognition memory (p = .001) after 3 months of CCH, revealing a heretofore unidentified sexual dimorphism with respect to cognitive impact during disease progression. Overall, results of our study strongly implicate epigenetic changes in maternal germ cells, induced by our repetitive systemic hypoxic stimulus, contributing to a modified differentiation program capable of establishing a dementia-resilient phenotype in adult male first-generation progeny.</abstract><cop>United States</cop><pub>American Psychological Association</pub><pmid>36862475</pmid><doi>10.1037/bne0000554</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-4641-0465</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animal Animals Anoxia Brain Ischemia Cognitive ability Cognitive Dysfunction - genetics Dementia Dementia disorders Disease Models, Animal Disease transmission Epigenesis, Genetic Epigenetics Female Germ cells Hypoxia Male Males Memory Memory Disorders Memory Disorders - genetics Mice Offspring Pattern recognition Phenotypes Recognition (Learning) Resilience (Psychological) Sexual dimorphism Transgenerational Patterns Vascular dementia |
| title | Maternal Repetitive Hypoxia Prior to Mating Confers Epigenetic Resilience to Memory Impairment in Male Progeny |
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