Regulation of Mitochondrial Genome Inheritance by Autophagy and Ubiquitin-Proteasome System : Implications for Health, Fitness, and Fertility
Mitochondria, the energy-generating organelles, play a role in numerous cellular functions including adenosine triphosphate (ATP) production, cellular homeostasis, and apoptosis. Maternal inheritance of mitochondria and mitochondrial DNA (mtDNA) is universally observed in humans and most animals. In...
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description | Mitochondria, the energy-generating organelles, play a role in numerous cellular functions including adenosine triphosphate (ATP) production, cellular homeostasis, and apoptosis. Maternal inheritance of mitochondria and mitochondrial DNA (mtDNA) is universally observed in humans and most animals. In general, high levels of mitochondrial heteroplasmy might contribute to a detrimental effect on fitness and disease resistance. Therefore, a disposal of the sperm-derived mitochondria inside fertilized oocytes assures normal preimplantation embryo development. Here we summarize the current research and knowledge concerning the role of autophagic pathway and ubiquitin-proteasome-dependent proteolysis in sperm mitophagy in mammals, including humans. Current data indicate that sperm mitophagy inside the fertilized oocyte could occur along multiple degradation routes converging on autophagic clearance of paternal mitochondria. The influence of assisted reproductive therapies (ART) such as intracytoplasmic sperm injection (ICSI), mitochondrial replacement (MR), and assisted fertilization of oocytes from patients of advanced reproductive age on mitochondrial function, inheritance, and fitness and for the development and health of ART babies will be of particular interest to clinical audiences. Altogether, the study of sperm mitophagy after fertilization has implications in the timing of evolution and developmental and reproductive biology and in human health, fitness, and management of mitochondrial disease. |
doi_str_mv | 10.1155/2014/981867 |
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Maternal inheritance of mitochondria and mitochondrial DNA (mtDNA) is universally observed in humans and most animals. In general, high levels of mitochondrial heteroplasmy might contribute to a detrimental effect on fitness and disease resistance. Therefore, a disposal of the sperm-derived mitochondria inside fertilized oocytes assures normal preimplantation embryo development. Here we summarize the current research and knowledge concerning the role of autophagic pathway and ubiquitin-proteasome-dependent proteolysis in sperm mitophagy in mammals, including humans. Current data indicate that sperm mitophagy inside the fertilized oocyte could occur along multiple degradation routes converging on autophagic clearance of paternal mitochondria. The influence of assisted reproductive therapies (ART) such as intracytoplasmic sperm injection (ICSI), mitochondrial replacement (MR), and assisted fertilization of oocytes from patients of advanced reproductive age on mitochondrial function, inheritance, and fitness and for the development and health of ART babies will be of particular interest to clinical audiences. Altogether, the study of sperm mitophagy after fertilization has implications in the timing of evolution and developmental and reproductive biology and in human health, fitness, and management of mitochondrial disease.</description><identifier>ISSN: 2314-6133</identifier><identifier>EISSN: 2314-6141</identifier><identifier>DOI: 10.1155/2014/981867</identifier><identifier>PMID: 25028670</identifier><language>eng</language><publisher>Cairo, Egypt: Hindawi Puplishing Corporation</publisher><subject>Analysis ; Animals ; Apoptosis ; Autophagy ; Autophagy (Cytology) ; Autophagy - physiology ; Biomedical research ; Cell cycle ; Colleges & universities ; Deoxyribonucleic acid ; DNA ; Embryos ; Female ; Fertility ; Fertility - physiology ; Genes ; Genetic regulation ; Genome, Mitochondrial - physiology ; Genomes ; Humans ; Infertility ; Influence ; Male ; Mammals ; Mitochondria ; Mitochondrial Degradation - physiology ; Mitochondrial DNA ; Oocytes - metabolism ; Phosphorylation ; Proteasome Endopeptidase Complex - physiology ; Proteins ; Proteolysis ; Review ; Sperm ; Sperm Maturation - physiology ; Spermatogenesis ; Spermatozoa - metabolism ; Ubiquitin - metabolism ; Womens health</subject><ispartof>BioMed research international, 2014-01, Vol.2014 (2014), p.1-16</ispartof><rights>Copyright © 2014 Won-Hee Song et al.</rights><rights>COPYRIGHT 2014 John Wiley & Sons, Inc.</rights><rights>Copyright © 2014 Won-Hee Song et al. Won-Hee Song et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</rights><rights>Copyright © 2014 Won-Hee Song et al. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c527t-9d3653deeba679f4939ca592f166ed75ab6a1ebaecd75050e8b51bd752f66b33</citedby><cites>FETCH-LOGICAL-c527t-9d3653deeba679f4939ca592f166ed75ab6a1ebaecd75050e8b51bd752f66b33</cites><orcidid>0000-0003-2978-2774 ; 0000-0002-9231-2823</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4083708/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4083708/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25028670$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Krijgsveld, Jeroen</contributor><creatorcontrib>Song, Won-Hee</creatorcontrib><creatorcontrib>Ballard, John William Oman</creatorcontrib><creatorcontrib>Yi, Young-Joo</creatorcontrib><creatorcontrib>Sutovsky, Peter</creatorcontrib><title>Regulation of Mitochondrial Genome Inheritance by Autophagy and Ubiquitin-Proteasome System : Implications for Health, Fitness, and Fertility</title><title>BioMed research international</title><addtitle>Biomed Res Int</addtitle><description>Mitochondria, the energy-generating organelles, play a role in numerous cellular functions including adenosine triphosphate (ATP) production, cellular homeostasis, and apoptosis. Maternal inheritance of mitochondria and mitochondrial DNA (mtDNA) is universally observed in humans and most animals. In general, high levels of mitochondrial heteroplasmy might contribute to a detrimental effect on fitness and disease resistance. Therefore, a disposal of the sperm-derived mitochondria inside fertilized oocytes assures normal preimplantation embryo development. Here we summarize the current research and knowledge concerning the role of autophagic pathway and ubiquitin-proteasome-dependent proteolysis in sperm mitophagy in mammals, including humans. Current data indicate that sperm mitophagy inside the fertilized oocyte could occur along multiple degradation routes converging on autophagic clearance of paternal mitochondria. The influence of assisted reproductive therapies (ART) such as intracytoplasmic sperm injection (ICSI), mitochondrial replacement (MR), and assisted fertilization of oocytes from patients of advanced reproductive age on mitochondrial function, inheritance, and fitness and for the development and health of ART babies will be of particular interest to clinical audiences. Altogether, the study of sperm mitophagy after fertilization has implications in the timing of evolution and developmental and reproductive biology and in human health, fitness, and management of mitochondrial disease.</description><subject>Analysis</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Autophagy</subject><subject>Autophagy (Cytology)</subject><subject>Autophagy - physiology</subject><subject>Biomedical research</subject><subject>Cell cycle</subject><subject>Colleges & universities</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Embryos</subject><subject>Female</subject><subject>Fertility</subject><subject>Fertility - physiology</subject><subject>Genes</subject><subject>Genetic regulation</subject><subject>Genome, Mitochondrial - physiology</subject><subject>Genomes</subject><subject>Humans</subject><subject>Infertility</subject><subject>Influence</subject><subject>Male</subject><subject>Mammals</subject><subject>Mitochondria</subject><subject>Mitochondrial Degradation - physiology</subject><subject>Mitochondrial DNA</subject><subject>Oocytes - metabolism</subject><subject>Phosphorylation</subject><subject>Proteasome Endopeptidase Complex - physiology</subject><subject>Proteins</subject><subject>Proteolysis</subject><subject>Review</subject><subject>Sperm</subject><subject>Sperm Maturation - physiology</subject><subject>Spermatogenesis</subject><subject>Spermatozoa - metabolism</subject><subject>Ubiquitin - metabolism</subject><subject>Womens health</subject><issn>2314-6133</issn><issn>2314-6141</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>RHX</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFkk1v1DAQhiMEotXSE2eQJS4IGuqP2Ek4IK0qtl2pCATlbDnJZOMqsbe2A8qP4D_jNGX5uGDJ8ljzzDszmkmSpwS_IYTzM4pJdlYWpBD5g-SYMpKlgmTk4cFm7Cg58f4Gx1MQgUvxODmiHNMYgY-TH59hN_YqaGuQbdEHHWzdWdM4rXp0AcYOgLamA6eDMjWgakLrMdh9p3YTUqZBXyt9O-qgTfrJ2QDKzxFfJh9gQG_Rdtj3ur6T96i1Dl2C6kN3ijY6GPD-9E5jAy7oXofpSfKoVb2Hk_t3lVxv3l-fX6ZXHy-25-urtOY0D2nZMMFZA1ApkZdtVrKyVrykLRECmpyrSigSnVDHD-YYioqTKtq0FaJibJW8W2T3YzVAU4MJTvVy7_Sg3CSt0vJvj9Gd3NlvMsMFy-NdJS_vBZy9HcEHOWhfQ98rA3b0kghCBMtwNud68Q96Y0dnYncyzo8WnLEi_03tVA9Sm9bGvPUsKtcZzTHllJNIvV6o2lnvHbSHkgmW8zrIeR3ksg6Rfv5nlwf21_Aj8GoBOm0a9V3_R-3ZAkNEoFUHONbFMsF-AgTDx4k</recordid><startdate>20140101</startdate><enddate>20140101</enddate><creator>Song, Won-Hee</creator><creator>Ballard, John William Oman</creator><creator>Yi, Young-Joo</creator><creator>Sutovsky, Peter</creator><general>Hindawi Puplishing Corporation</general><general>Hindawi Publishing Corporation</general><general>John Wiley & Sons, Inc</general><general>Hindawi Limited</general><scope>ADJCN</scope><scope>AHFXO</scope><scope>RHU</scope><scope>RHW</scope><scope>RHX</scope><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>3V.</scope><scope>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>CWDGH</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2978-2774</orcidid><orcidid>https://orcid.org/0000-0002-9231-2823</orcidid></search><sort><creationdate>20140101</creationdate><title>Regulation of Mitochondrial Genome Inheritance by Autophagy and Ubiquitin-Proteasome System : Implications for Health, Fitness, and Fertility</title><author>Song, Won-Hee ; Ballard, John William Oman ; Yi, Young-Joo ; Sutovsky, Peter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c527t-9d3653deeba679f4939ca592f166ed75ab6a1ebaecd75050e8b51bd752f66b33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Autophagy</topic><topic>Autophagy (Cytology)</topic><topic>Autophagy - 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Maternal inheritance of mitochondria and mitochondrial DNA (mtDNA) is universally observed in humans and most animals. In general, high levels of mitochondrial heteroplasmy might contribute to a detrimental effect on fitness and disease resistance. Therefore, a disposal of the sperm-derived mitochondria inside fertilized oocytes assures normal preimplantation embryo development. Here we summarize the current research and knowledge concerning the role of autophagic pathway and ubiquitin-proteasome-dependent proteolysis in sperm mitophagy in mammals, including humans. Current data indicate that sperm mitophagy inside the fertilized oocyte could occur along multiple degradation routes converging on autophagic clearance of paternal mitochondria. The influence of assisted reproductive therapies (ART) such as intracytoplasmic sperm injection (ICSI), mitochondrial replacement (MR), and assisted fertilization of oocytes from patients of advanced reproductive age on mitochondrial function, inheritance, and fitness and for the development and health of ART babies will be of particular interest to clinical audiences. Altogether, the study of sperm mitophagy after fertilization has implications in the timing of evolution and developmental and reproductive biology and in human health, fitness, and management of mitochondrial disease.</abstract><cop>Cairo, Egypt</cop><pub>Hindawi Puplishing Corporation</pub><pmid>25028670</pmid><doi>10.1155/2014/981867</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0003-2978-2774</orcidid><orcidid>https://orcid.org/0000-0002-9231-2823</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animals Apoptosis Autophagy Autophagy (Cytology) Autophagy - physiology Biomedical research Cell cycle Colleges & universities Deoxyribonucleic acid DNA Embryos Female Fertility Fertility - physiology Genes Genetic regulation Genome, Mitochondrial - physiology Genomes Humans Infertility Influence Male Mammals Mitochondria Mitochondrial Degradation - physiology Mitochondrial DNA Oocytes - metabolism Phosphorylation Proteasome Endopeptidase Complex - physiology Proteins Proteolysis Review Sperm Sperm Maturation - physiology Spermatogenesis Spermatozoa - metabolism Ubiquitin - metabolism Womens health |
title | Regulation of Mitochondrial Genome Inheritance by Autophagy and Ubiquitin-Proteasome System : Implications for Health, Fitness, and Fertility |
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