Peroxisomal Multifunctional Protein 2 Is Essential for Lipid Homeostasis in Sertoli Cells and Male Fertility in Mice
Inactivation of peroxisomal β-oxidation in mice, by knocking out multifunctional protein-2 (MFP-2; also called d-bifunctional enzyme), causes male infertility. In the testis, extensive accumulations of neutral lipids were observed in Sertoli cells, beginning in prepubertal mice and evolving in compl...
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| Veröffentlicht in: | Endocrinology (Philadelphia) 2006-05, Vol.147 (5), p.2228-2236 |
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| creator | Huyghe, Steven Schmalbruch, Henning De Gendt, Karel Verhoeven, Guido Guillou, Florian Van Veldhoven, Paul P Baes, Myriam |
| description | Inactivation of peroxisomal β-oxidation in mice, by knocking out multifunctional protein-2 (MFP-2; also called d-bifunctional enzyme), causes male infertility. In the testis, extensive accumulations of neutral lipids were observed in Sertoli cells, beginning in prepubertal mice and evolving in complete testicular atrophy by the age of 4 months. Spermatogenesis was already severely affected at the age of 5 wk, and pre- and postmeiotic germ cells gradually disappeared from the tubuli seminiferi. Based on cytochemical stainings and biochemical analyses, the lipid droplets consisted of cholesteryl esters and neutral glycerolipids. Furthermore, peroxisomal β-oxidation substrates, such as very-long-chain fatty acids and pristanic acid, accumulated in the testis, whereas the concentration of docosapentaenoic acid, a polyunsaturated fatty acid and peroxisomal β-oxidation product, was reduced. The testicular defects were also present in double MFP-2/peroxisome proliferator-activated receptor-α knockout mice, ruling out the possibility that they were mediated through the activation of this nuclear receptor. Immunoreactivity for peroxisomal proteins, including MFP-2, was detected in Sertoli cells as well as in germ cells and Leydig cells. The pivotal role of peroxisomal metabolism in Sertoli cells was also demonstrated by generating mice with a Sertoli cell-selective elimination of peroxisomes through cell type-specific inactivation of the peroxin 5 gene. These mice also developed lipid inclusions and were infertile, and their testes fully degenerated by the age of 4 months. In conclusion, the present data demonstrate that peroxisomal β-oxidation is essential for lipid homeostasis in the testis and for male fertility. |
| doi_str_mv | 10.1210/en.2005-1571 |
| format | Article |
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In the testis, extensive accumulations of neutral lipids were observed in Sertoli cells, beginning in prepubertal mice and evolving in complete testicular atrophy by the age of 4 months. Spermatogenesis was already severely affected at the age of 5 wk, and pre- and postmeiotic germ cells gradually disappeared from the tubuli seminiferi. Based on cytochemical stainings and biochemical analyses, the lipid droplets consisted of cholesteryl esters and neutral glycerolipids. Furthermore, peroxisomal β-oxidation substrates, such as very-long-chain fatty acids and pristanic acid, accumulated in the testis, whereas the concentration of docosapentaenoic acid, a polyunsaturated fatty acid and peroxisomal β-oxidation product, was reduced. The testicular defects were also present in double MFP-2/peroxisome proliferator-activated receptor-α knockout mice, ruling out the possibility that they were mediated through the activation of this nuclear receptor. Immunoreactivity for peroxisomal proteins, including MFP-2, was detected in Sertoli cells as well as in germ cells and Leydig cells. The pivotal role of peroxisomal metabolism in Sertoli cells was also demonstrated by generating mice with a Sertoli cell-selective elimination of peroxisomes through cell type-specific inactivation of the peroxin 5 gene. These mice also developed lipid inclusions and were infertile, and their testes fully degenerated by the age of 4 months. In conclusion, the present data demonstrate that peroxisomal β-oxidation is essential for lipid homeostasis in the testis and for male fertility.</description><identifier>ISSN: 0013-7227</identifier><identifier>EISSN: 1945-7170</identifier><identifier>DOI: 10.1210/en.2005-1571</identifier><identifier>PMID: 16484321</identifier><identifier>CODEN: ENDOAO</identifier><language>eng</language><publisher>Bethesda, MD: Endocrine Society</publisher><subject>17-Hydroxysteroid Dehydrogenases - metabolism ; Age ; Animals ; Atrophy ; Biological and medical sciences ; Cell activation ; Cholesterol Esters - chemistry ; Deactivation ; Endocrinology and metabolism ; Enoyl-CoA Hydratase - metabolism ; Esters ; Fatty acids ; Fatty Acids - metabolism ; Fatty Acids - pharmacology ; Fatty Acids, Unsaturated - metabolism ; Fertility ; Fundamental and applied biological sciences. Psychology ; Germ cells ; Heterozygote ; Homeostasis ; Homozygote ; Human health and pathology ; Immunohistochemistry ; Immunoreactivity ; Inactivation ; Inclusions ; Infertility ; Infertility, Male ; Leydig Cells ; Life Sciences ; Lipid Metabolism ; Lipids ; Lipids - chemistry ; Male ; Males ; Mice ; Mice, Knockout ; Mice, Transgenic ; Multienzyme Complexes - metabolism ; Multifunctional protein-2 ; Oxidation ; Oxygen - metabolism ; Peroxin ; Peroxisomal Multifunctional Protein-2 ; Peroxisome proliferator-activated receptors ; Peroxisomes - metabolism ; Polyunsaturated fatty acids ; PPAR alpha - genetics ; Proteins ; Rats ; Receptors ; Reverse Transcriptase Polymerase Chain Reaction ; RNA - metabolism ; Seminiferous Tubules - metabolism ; Sertoli cells ; Sertoli Cells - metabolism ; Spermatogenesis ; Testes ; Testis - metabolism ; Vertebrates: endocrinology</subject><ispartof>Endocrinology (Philadelphia), 2006-05, Vol.147 (5), p.2228-2236</ispartof><rights>Copyright © 2006 by The Endocrine Society 2006</rights><rights>2006 INIST-CNRS</rights><rights>Copyright © 2006 by The Endocrine Society</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c561t-7f1c90046f89f5babd232d51a9dc242bb10af5b1d526b824ab892694a4ac55d93</citedby><cites>FETCH-LOGICAL-c561t-7f1c90046f89f5babd232d51a9dc242bb10af5b1d526b824ab892694a4ac55d93</cites><orcidid>0000-0002-7325-5317</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=17712233$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16484321$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02657089$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Huyghe, Steven</creatorcontrib><creatorcontrib>Schmalbruch, Henning</creatorcontrib><creatorcontrib>De Gendt, Karel</creatorcontrib><creatorcontrib>Verhoeven, Guido</creatorcontrib><creatorcontrib>Guillou, Florian</creatorcontrib><creatorcontrib>Van Veldhoven, Paul P</creatorcontrib><creatorcontrib>Baes, Myriam</creatorcontrib><title>Peroxisomal Multifunctional Protein 2 Is Essential for Lipid Homeostasis in Sertoli Cells and Male Fertility in Mice</title><title>Endocrinology (Philadelphia)</title><addtitle>Endocrinology</addtitle><description>Inactivation of peroxisomal β-oxidation in mice, by knocking out multifunctional protein-2 (MFP-2; also called d-bifunctional enzyme), causes male infertility. In the testis, extensive accumulations of neutral lipids were observed in Sertoli cells, beginning in prepubertal mice and evolving in complete testicular atrophy by the age of 4 months. Spermatogenesis was already severely affected at the age of 5 wk, and pre- and postmeiotic germ cells gradually disappeared from the tubuli seminiferi. Based on cytochemical stainings and biochemical analyses, the lipid droplets consisted of cholesteryl esters and neutral glycerolipids. Furthermore, peroxisomal β-oxidation substrates, such as very-long-chain fatty acids and pristanic acid, accumulated in the testis, whereas the concentration of docosapentaenoic acid, a polyunsaturated fatty acid and peroxisomal β-oxidation product, was reduced. The testicular defects were also present in double MFP-2/peroxisome proliferator-activated receptor-α knockout mice, ruling out the possibility that they were mediated through the activation of this nuclear receptor. Immunoreactivity for peroxisomal proteins, including MFP-2, was detected in Sertoli cells as well as in germ cells and Leydig cells. The pivotal role of peroxisomal metabolism in Sertoli cells was also demonstrated by generating mice with a Sertoli cell-selective elimination of peroxisomes through cell type-specific inactivation of the peroxin 5 gene. These mice also developed lipid inclusions and were infertile, and their testes fully degenerated by the age of 4 months. In conclusion, the present data demonstrate that peroxisomal β-oxidation is essential for lipid homeostasis in the testis and for male fertility.</description><subject>17-Hydroxysteroid Dehydrogenases - metabolism</subject><subject>Age</subject><subject>Animals</subject><subject>Atrophy</subject><subject>Biological and medical sciences</subject><subject>Cell activation</subject><subject>Cholesterol Esters - chemistry</subject><subject>Deactivation</subject><subject>Endocrinology and metabolism</subject><subject>Enoyl-CoA Hydratase - metabolism</subject><subject>Esters</subject><subject>Fatty acids</subject><subject>Fatty Acids - metabolism</subject><subject>Fatty Acids - pharmacology</subject><subject>Fatty Acids, Unsaturated - metabolism</subject><subject>Fertility</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Germ cells</subject><subject>Heterozygote</subject><subject>Homeostasis</subject><subject>Homozygote</subject><subject>Human health and pathology</subject><subject>Immunohistochemistry</subject><subject>Immunoreactivity</subject><subject>Inactivation</subject><subject>Inclusions</subject><subject>Infertility</subject><subject>Infertility, Male</subject><subject>Leydig Cells</subject><subject>Life Sciences</subject><subject>Lipid Metabolism</subject><subject>Lipids</subject><subject>Lipids - chemistry</subject><subject>Male</subject><subject>Males</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>Multienzyme Complexes - metabolism</subject><subject>Multifunctional protein-2</subject><subject>Oxidation</subject><subject>Oxygen - metabolism</subject><subject>Peroxin</subject><subject>Peroxisomal Multifunctional Protein-2</subject><subject>Peroxisome proliferator-activated receptors</subject><subject>Peroxisomes - metabolism</subject><subject>Polyunsaturated fatty acids</subject><subject>PPAR alpha - genetics</subject><subject>Proteins</subject><subject>Rats</subject><subject>Receptors</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>RNA - metabolism</subject><subject>Seminiferous Tubules - metabolism</subject><subject>Sertoli cells</subject><subject>Sertoli Cells - metabolism</subject><subject>Spermatogenesis</subject><subject>Testes</subject><subject>Testis - metabolism</subject><subject>Vertebrates: endocrinology</subject><issn>0013-7227</issn><issn>1945-7170</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10VGL1DAQB_Aiird3-uazBMQTwZ5JmrTN47HcuQe7eKA-hzRNMUearJlUvG9vSosLok8hw4-ZTP5F8YrgK0IJ_mj8FcWYl4Q35EmxIYLxsiENflpsMCZV2VDanBXnAA_5yhirnhdnpGYtqyjZFOnexPDLQhiVQ4fJJTtMXicbfL7fx5CM9YiiO0A3AMYnm8tDiGhvj7ZHuzCaAEmBBZTdFxNTcBZtjXOAlO_RQTmDbnPZOpseZ3Ow2rwong3KgXm5nhfFt9ubr9tduf_86W57vS81r0kqm4FogTGrh1YMvFNdTyvac6JErymjXUewynXSc1p3LWWqawWtBVNMac57UV0U75e-35WTx2hHFR9lUFburvdyrmFa8wa34ifJ9nKxxxh-TAaSHC3ovIjyJkwg66athWB1hm_-gg9hivm7QFakwjmF3DCrD4vSMQBEM_yZT7Ccc5PGyzk3OeeW-eu16dSNpj_hNagM3q5AgVZuiMprCyfXNITSqsru3eLCdPzfyHIdWS3S-D7oaL05RgNw2uafD_0N3Zu7sA</recordid><startdate>20060501</startdate><enddate>20060501</enddate><creator>Huyghe, Steven</creator><creator>Schmalbruch, Henning</creator><creator>De Gendt, Karel</creator><creator>Verhoeven, Guido</creator><creator>Guillou, Florian</creator><creator>Van Veldhoven, Paul P</creator><creator>Baes, Myriam</creator><general>Endocrine Society</general><general>Oxford University Press</general><scope>IQODW</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>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-7325-5317</orcidid></search><sort><creationdate>20060501</creationdate><title>Peroxisomal Multifunctional Protein 2 Is Essential for Lipid Homeostasis in Sertoli Cells and Male Fertility in Mice</title><author>Huyghe, Steven ; Schmalbruch, Henning ; De Gendt, Karel ; Verhoeven, Guido ; Guillou, Florian ; Van Veldhoven, Paul P ; Baes, Myriam</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c561t-7f1c90046f89f5babd232d51a9dc242bb10af5b1d526b824ab892694a4ac55d93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>17-Hydroxysteroid Dehydrogenases - metabolism</topic><topic>Age</topic><topic>Animals</topic><topic>Atrophy</topic><topic>Biological and medical sciences</topic><topic>Cell activation</topic><topic>Cholesterol Esters - chemistry</topic><topic>Deactivation</topic><topic>Endocrinology and metabolism</topic><topic>Enoyl-CoA Hydratase - metabolism</topic><topic>Esters</topic><topic>Fatty acids</topic><topic>Fatty Acids - metabolism</topic><topic>Fatty Acids - pharmacology</topic><topic>Fatty Acids, Unsaturated - metabolism</topic><topic>Fertility</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Germ cells</topic><topic>Heterozygote</topic><topic>Homeostasis</topic><topic>Homozygote</topic><topic>Human health and pathology</topic><topic>Immunohistochemistry</topic><topic>Immunoreactivity</topic><topic>Inactivation</topic><topic>Inclusions</topic><topic>Infertility</topic><topic>Infertility, Male</topic><topic>Leydig Cells</topic><topic>Life Sciences</topic><topic>Lipid Metabolism</topic><topic>Lipids</topic><topic>Lipids - chemistry</topic><topic>Male</topic><topic>Males</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Mice, Transgenic</topic><topic>Multienzyme Complexes - metabolism</topic><topic>Multifunctional protein-2</topic><topic>Oxidation</topic><topic>Oxygen - metabolism</topic><topic>Peroxin</topic><topic>Peroxisomal Multifunctional Protein-2</topic><topic>Peroxisome proliferator-activated receptors</topic><topic>Peroxisomes - metabolism</topic><topic>Polyunsaturated fatty acids</topic><topic>PPAR alpha - genetics</topic><topic>Proteins</topic><topic>Rats</topic><topic>Receptors</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>RNA - metabolism</topic><topic>Seminiferous Tubules - metabolism</topic><topic>Sertoli cells</topic><topic>Sertoli Cells - metabolism</topic><topic>Spermatogenesis</topic><topic>Testes</topic><topic>Testis - metabolism</topic><topic>Vertebrates: endocrinology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Huyghe, Steven</creatorcontrib><creatorcontrib>Schmalbruch, Henning</creatorcontrib><creatorcontrib>De Gendt, Karel</creatorcontrib><creatorcontrib>Verhoeven, Guido</creatorcontrib><creatorcontrib>Guillou, Florian</creatorcontrib><creatorcontrib>Van Veldhoven, Paul P</creatorcontrib><creatorcontrib>Baes, Myriam</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Endocrinology (Philadelphia)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Huyghe, Steven</au><au>Schmalbruch, Henning</au><au>De Gendt, Karel</au><au>Verhoeven, Guido</au><au>Guillou, Florian</au><au>Van Veldhoven, Paul P</au><au>Baes, Myriam</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Peroxisomal Multifunctional Protein 2 Is Essential for Lipid Homeostasis in Sertoli Cells and Male Fertility in Mice</atitle><jtitle>Endocrinology (Philadelphia)</jtitle><addtitle>Endocrinology</addtitle><date>2006-05-01</date><risdate>2006</risdate><volume>147</volume><issue>5</issue><spage>2228</spage><epage>2236</epage><pages>2228-2236</pages><issn>0013-7227</issn><eissn>1945-7170</eissn><coden>ENDOAO</coden><abstract>Inactivation of peroxisomal β-oxidation in mice, by knocking out multifunctional protein-2 (MFP-2; also called d-bifunctional enzyme), causes male infertility. In the testis, extensive accumulations of neutral lipids were observed in Sertoli cells, beginning in prepubertal mice and evolving in complete testicular atrophy by the age of 4 months. Spermatogenesis was already severely affected at the age of 5 wk, and pre- and postmeiotic germ cells gradually disappeared from the tubuli seminiferi. Based on cytochemical stainings and biochemical analyses, the lipid droplets consisted of cholesteryl esters and neutral glycerolipids. Furthermore, peroxisomal β-oxidation substrates, such as very-long-chain fatty acids and pristanic acid, accumulated in the testis, whereas the concentration of docosapentaenoic acid, a polyunsaturated fatty acid and peroxisomal β-oxidation product, was reduced. The testicular defects were also present in double MFP-2/peroxisome proliferator-activated receptor-α knockout mice, ruling out the possibility that they were mediated through the activation of this nuclear receptor. Immunoreactivity for peroxisomal proteins, including MFP-2, was detected in Sertoli cells as well as in germ cells and Leydig cells. The pivotal role of peroxisomal metabolism in Sertoli cells was also demonstrated by generating mice with a Sertoli cell-selective elimination of peroxisomes through cell type-specific inactivation of the peroxin 5 gene. These mice also developed lipid inclusions and were infertile, and their testes fully degenerated by the age of 4 months. In conclusion, the present data demonstrate that peroxisomal β-oxidation is essential for lipid homeostasis in the testis and for male fertility.</abstract><cop>Bethesda, MD</cop><pub>Endocrine Society</pub><pmid>16484321</pmid><doi>10.1210/en.2005-1571</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-7325-5317</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 17-Hydroxysteroid Dehydrogenases - metabolism Age Animals Atrophy Biological and medical sciences Cell activation Cholesterol Esters - chemistry Deactivation Endocrinology and metabolism Enoyl-CoA Hydratase - metabolism Esters Fatty acids Fatty Acids - metabolism Fatty Acids - pharmacology Fatty Acids, Unsaturated - metabolism Fertility Fundamental and applied biological sciences. Psychology Germ cells Heterozygote Homeostasis Homozygote Human health and pathology Immunohistochemistry Immunoreactivity Inactivation Inclusions Infertility Infertility, Male Leydig Cells Life Sciences Lipid Metabolism Lipids Lipids - chemistry Male Males Mice Mice, Knockout Mice, Transgenic Multienzyme Complexes - metabolism Multifunctional protein-2 Oxidation Oxygen - metabolism Peroxin Peroxisomal Multifunctional Protein-2 Peroxisome proliferator-activated receptors Peroxisomes - metabolism Polyunsaturated fatty acids PPAR alpha - genetics Proteins Rats Receptors Reverse Transcriptase Polymerase Chain Reaction RNA - metabolism Seminiferous Tubules - metabolism Sertoli cells Sertoli Cells - metabolism Spermatogenesis Testes Testis - metabolism Vertebrates: endocrinology |
| title | Peroxisomal Multifunctional Protein 2 Is Essential for Lipid Homeostasis in Sertoli Cells and Male Fertility in Mice |
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