Loss of the Nuclear Receptor Corepressor SLIRP Compromises Male Fertility
Nuclear receptors (NRs) and their coregulators play fundamental roles in initiating and directing gene expression influencing mammalian reproduction, development and metabolism. SRA stem Loop Interacting RNA-binding Protein (SLIRP) is a Steroid receptor RNA Activator (SRA) RNA-binding protein that i...
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| Vydáno v: | PloS one Ročník 8; číslo 8; s. e70700 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
Public Library of Science
15.08.2013
Public Library of Science (PLoS) |
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| ISSN: | 1932-6203, 1932-6203 |
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| Abstract | Nuclear receptors (NRs) and their coregulators play fundamental roles in initiating and directing gene expression influencing mammalian reproduction, development and metabolism. SRA stem Loop Interacting RNA-binding Protein (SLIRP) is a Steroid receptor RNA Activator (SRA) RNA-binding protein that is a potent repressor of NR activity. SLIRP is present in complexes associated with NR target genes in the nucleus; however, it is also abundant in mitochondria where it affects mitochondrial mRNA transcription and energy turnover. In further characterisation studies, we observed SLIRP protein in the testis where its localization pattern changes from mitochondrial in diploid cells to peri-acrosomal and the tail in mature sperm. To investigate the in vivo effects of SLIRP, we generated a SLIRP knockout (KO) mouse. This animal is viable, but sub-fertile. Specifically, when homozygous KO males are crossed with wild type (WT) females the resultant average litter size is reduced by approximately one third compared with those produced by WT males and females. Further, SLIRP KO mice produced significantly fewer progressively motile sperm than WT animals. Electron microscopy identified disruption of the mid-piece/annulus junction in homozygous KO sperm and altered mitochondrial morphology. In sum, our data implicates SLIRP in regulating male fertility, wherein its loss results in asthenozoospermia associated with compromised sperm structure and mitochondrial morphology. |
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| AbstractList | Nuclear receptors (NRs) and their coregulators play fundamental roles in initiating and directing gene expression influencing mammalian reproduction, development and metabolism. SRA stem Loop Interacting RNA-binding Protein (SLIRP) is a Steroid receptor RNA Activator (SRA) RNA-binding protein that is a potent repressor of NR activity. SLIRP is present in complexes associated with NR target genes in the nucleus; however, it is also abundant in mitochondria where it affects mitochondrial mRNA transcription and energy turnover. In further characterisation studies, we observed SLIRP protein in the testis where its localization pattern changes from mitochondrial in diploid cells to peri-acrosomal and the tail in mature sperm. To investigate the in vivo effects of SLIRP, we generated a SLIRP knockout (KO) mouse. This animal is viable, but sub-fertile. Specifically, when homozygous KO males are crossed with wild type (WT) females the resultant average litter size is reduced by approximately one third compared with those produced by WT males and females. Further, SLIRP KO mice produced significantly fewer progressively motile sperm than WT animals. Electron microscopy identified disruption of the mid-piece/annulus junction in homozygous KO sperm and altered mitochondrial morphology. In sum, our data implicates SLIRP in regulating male fertility, wherein its loss results in asthenozoospermia associated with compromised sperm structure and mitochondrial morphology. Nuclear receptors (NRs) and their coregulators play fundamental roles in initiating and directing gene expression influencing mammalian reproduction, development and metabolism. SRA stem Loop Interacting RNA-binding Protein (SLIRP) is a Steroid receptor RNA Activator (SRA) RNA-binding protein that is a potent repressor of NR activity. SLIRP is present in complexes associated with NR target genes in the nucleus; however, it is also abundant in mitochondria where it affects mitochondrial mRNA transcription and energy turnover. In further characterisation studies, we observed SLIRP protein in the testis where its localization pattern changes from mitochondrial in diploid cells to peri-acrosomal and the tail in mature sperm. To investigate the in vivo effects of SLIRP, we generated a SLIRP knockout (KO) mouse. This animal is viable, but sub-fertile. Specifically, when homozygous KO males are crossed with wild type (WT) females the resultant average litter size is reduced by approximately one third compared with those produced by WT males and females. Further, SLIRP KO mice produced significantly fewer progressively motile sperm than WT animals. Electron microscopy identified disruption of the mid-piece/annulus junction in homozygous KO sperm and altered mitochondrial morphology. In sum, our data implicates SLIRP in regulating male fertility, wherein its loss results in asthenozoospermia associated with compromised sperm structure and mitochondrial morphology.Nuclear receptors (NRs) and their coregulators play fundamental roles in initiating and directing gene expression influencing mammalian reproduction, development and metabolism. SRA stem Loop Interacting RNA-binding Protein (SLIRP) is a Steroid receptor RNA Activator (SRA) RNA-binding protein that is a potent repressor of NR activity. SLIRP is present in complexes associated with NR target genes in the nucleus; however, it is also abundant in mitochondria where it affects mitochondrial mRNA transcription and energy turnover. In further characterisation studies, we observed SLIRP protein in the testis where its localization pattern changes from mitochondrial in diploid cells to peri-acrosomal and the tail in mature sperm. To investigate the in vivo effects of SLIRP, we generated a SLIRP knockout (KO) mouse. This animal is viable, but sub-fertile. Specifically, when homozygous KO males are crossed with wild type (WT) females the resultant average litter size is reduced by approximately one third compared with those produced by WT males and females. Further, SLIRP KO mice produced significantly fewer progressively motile sperm than WT animals. Electron microscopy identified disruption of the mid-piece/annulus junction in homozygous KO sperm and altered mitochondrial morphology. In sum, our data implicates SLIRP in regulating male fertility, wherein its loss results in asthenozoospermia associated with compromised sperm structure and mitochondrial morphology. |
| Audience | Academic |
| Author | DeBoer, Kathleen Colley, Shane M. Phillips, Michael R. de Kretser, David M. Smith, Stephanie O'Bryan, Moira K. Merriner, D. Jo Leedman, Peter J. Genevieve, Ben Searles, Richelle Firman, Renee C. Wintle, Larissa Stuckey, Bronwyn G. A. Russell, Victoria Bentel, Jacqueline M. Simmons, Leigh W. |
| AuthorAffiliation | 8 School of Medicine and Pharmacology, University of Western Australia, Crawley, Australia 2 Research Centre, Royal Perth Hospital, Perth, Australia Baylor College of Medicine, United States of America 3 Centre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, Australia 5 Keogh Institute for Medical Research, Sir Charles Gairdner Hospital, Nedlands, Australia 1 Laboratory for Cancer Medicine, The University of Western Australia Centre for Medical Research, Western Australian Institute for Medical Research, Perth, Australia 7 School of Pathology and Laboratory Medicine, University of Western Australia, Crawley, Australia 6 Anatomical Pathology, PathWest Laboratory Medicine, Royal Perth Hospital, Perth, Australia 4 Male Infertility and Germ Cell Biology Laboratory, Department of Anatomy and Developmental Biology, Monash University, Clayton, Australia |
| AuthorAffiliation_xml | – name: 5 Keogh Institute for Medical Research, Sir Charles Gairdner Hospital, Nedlands, Australia – name: Baylor College of Medicine, United States of America – name: 3 Centre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, Australia – name: 4 Male Infertility and Germ Cell Biology Laboratory, Department of Anatomy and Developmental Biology, Monash University, Clayton, Australia – name: 6 Anatomical Pathology, PathWest Laboratory Medicine, Royal Perth Hospital, Perth, Australia – name: 8 School of Medicine and Pharmacology, University of Western Australia, Crawley, Australia – name: 7 School of Pathology and Laboratory Medicine, University of Western Australia, Crawley, Australia – name: 1 Laboratory for Cancer Medicine, The University of Western Australia Centre for Medical Research, Western Australian Institute for Medical Research, Perth, Australia – name: 2 Research Centre, Royal Perth Hospital, Perth, Australia |
| Author_xml | – sequence: 1 givenname: Shane M. surname: Colley fullname: Colley, Shane M. – sequence: 2 givenname: Larissa surname: Wintle fullname: Wintle, Larissa – sequence: 3 givenname: Richelle surname: Searles fullname: Searles, Richelle – sequence: 4 givenname: Victoria surname: Russell fullname: Russell, Victoria – sequence: 5 givenname: Renee C. surname: Firman fullname: Firman, Renee C. – sequence: 6 givenname: Stephanie surname: Smith fullname: Smith, Stephanie – sequence: 7 givenname: Kathleen surname: DeBoer fullname: DeBoer, Kathleen – sequence: 8 givenname: D. Jo surname: Merriner fullname: Merriner, D. Jo – sequence: 9 givenname: Ben surname: Genevieve fullname: Genevieve, Ben – sequence: 10 givenname: Jacqueline M. surname: Bentel fullname: Bentel, Jacqueline M. – sequence: 11 givenname: Bronwyn G. A. surname: Stuckey fullname: Stuckey, Bronwyn G. A. – sequence: 12 givenname: Michael R. surname: Phillips fullname: Phillips, Michael R. – sequence: 13 givenname: Leigh W. surname: Simmons fullname: Simmons, Leigh W. – sequence: 14 givenname: David M. surname: de Kretser fullname: de Kretser, David M. – sequence: 15 givenname: Moira K. surname: O'Bryan fullname: O'Bryan, Moira K. – sequence: 16 givenname: Peter J. surname: Leedman fullname: Leedman, Peter J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23976951$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_animal_2023_101012 crossref_primary_10_1093_biolre_ioac069 crossref_primary_10_1111_andr_300 crossref_primary_10_1038_celldisc_2017_30 crossref_primary_10_1093_hmg_ddu468 crossref_primary_10_1007_s00439_020_02159_x crossref_primary_10_1016_j_febslet_2015_11_007 crossref_primary_10_1016_j_cub_2014_09_047 crossref_primary_10_1038_s41598_019_55057_2 crossref_primary_10_1093_humupd_dmaf023 crossref_primary_10_1155_2020_9060356 crossref_primary_10_1371_journal_pgen_1005423 crossref_primary_10_1136_jmedgenet_2021_108137 crossref_primary_10_1093_hmg_ddae020 crossref_primary_10_1096_fj_202402135R crossref_primary_10_1111_andr_12100 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: The authors have declared that no competing interests exist. MO and PL are joint senior authors on this work. Conceived and designed the experiments: SC DdK MO PL. Performed the experiments: SC LW RS VR RF SS KdB DJM BG JB. Analyzed the data: SC LW RS DJM BS MP LS DdK MO PL. Contributed reagents/materials/analysis tools: RF LS BG BS LS DdK MO PL. Wrote the paper: SC JB BS DdK MO PL. |
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| Title | Loss of the Nuclear Receptor Corepressor SLIRP Compromises Male Fertility |
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