The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes.
Sperm activation is a fascinating example of cell differentiation, in which immotile spermatids undergo a rapid and dramatic transition to become mature, motile sperm. Because the sperm nucleus is transcriptionally silent, this transition does not involve transcriptional changes. Although Caenorhabd...
Saved in:
| Main Authors: | , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2018-06-01
|
| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.2005069&type=printable |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850230698343923712 |
|---|---|
| author | Yanmei Zhao Chieh-Hsiang Tan Amber Krauchunas Andrea Scharf Nicholas Dietrich Kurt Warnhoff Zhiheng Yuan Marina Druzhinina Sam Guoping Gu Long Miao Andrew Singson Ronald E Ellis Kerry Kornfeld |
| author_facet | Yanmei Zhao Chieh-Hsiang Tan Amber Krauchunas Andrea Scharf Nicholas Dietrich Kurt Warnhoff Zhiheng Yuan Marina Druzhinina Sam Guoping Gu Long Miao Andrew Singson Ronald E Ellis Kerry Kornfeld |
| author_sort | Yanmei Zhao |
| collection | DOAJ |
| description | Sperm activation is a fascinating example of cell differentiation, in which immotile spermatids undergo a rapid and dramatic transition to become mature, motile sperm. Because the sperm nucleus is transcriptionally silent, this transition does not involve transcriptional changes. Although Caenorhabditis elegans is a leading model for studies of sperm activation, the mechanisms by which signaling pathways induce this transformation remain poorly characterized. Here we show that a conserved transmembrane zinc transporter, ZIPT-7.1, regulates the induction of sperm activation in Caenorhabditis nematodes. The zipt-7.1 mutant hermaphrodites cannot self-fertilize, and males reproduce poorly, because mutant spermatids are defective in responding to activating signals. The zipt-7.1 gene is expressed in the germ line and functions in germ cells to promote sperm activation. When expressed in mammalian cells, ZIPT-7.1 mediates zinc transport with high specificity and is predominantly located on internal membranes. Finally, genetic epistasis places zipt-7.1 at the end of the spe-8 sperm activation pathway, and ZIPT-7.1 binds SPE-4, a presenilin that regulates sperm activation. Based on these results, we propose a new model for sperm activation. In spermatids, inactive ZIPT-7.1 is localized to the membranous organelles, which contain higher levels of zinc than the cytoplasm. When sperm activation is triggered, ZIPT-7.1 activity increases, releasing zinc from internal stores. The resulting increase in cytoplasmic zinc promotes the phenotypic changes characteristic of activation. Thus, zinc signaling is a key step in the signal transduction process that mediates sperm activation, and we have identified a zinc transporter that is central to this activation process. |
| format | Article |
| id | doaj-art-95ef2d03bedb46e392edb80c63246d45 |
| institution | OA Journals |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2018-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-95ef2d03bedb46e392edb80c63246d452025-08-20T02:03:47ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852018-06-01166e200506910.1371/journal.pbio.2005069The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes.Yanmei ZhaoChieh-Hsiang TanAmber KrauchunasAndrea ScharfNicholas DietrichKurt WarnhoffZhiheng YuanMarina DruzhininaSam Guoping GuLong MiaoAndrew SingsonRonald E EllisKerry KornfeldSperm activation is a fascinating example of cell differentiation, in which immotile spermatids undergo a rapid and dramatic transition to become mature, motile sperm. Because the sperm nucleus is transcriptionally silent, this transition does not involve transcriptional changes. Although Caenorhabditis elegans is a leading model for studies of sperm activation, the mechanisms by which signaling pathways induce this transformation remain poorly characterized. Here we show that a conserved transmembrane zinc transporter, ZIPT-7.1, regulates the induction of sperm activation in Caenorhabditis nematodes. The zipt-7.1 mutant hermaphrodites cannot self-fertilize, and males reproduce poorly, because mutant spermatids are defective in responding to activating signals. The zipt-7.1 gene is expressed in the germ line and functions in germ cells to promote sperm activation. When expressed in mammalian cells, ZIPT-7.1 mediates zinc transport with high specificity and is predominantly located on internal membranes. Finally, genetic epistasis places zipt-7.1 at the end of the spe-8 sperm activation pathway, and ZIPT-7.1 binds SPE-4, a presenilin that regulates sperm activation. Based on these results, we propose a new model for sperm activation. In spermatids, inactive ZIPT-7.1 is localized to the membranous organelles, which contain higher levels of zinc than the cytoplasm. When sperm activation is triggered, ZIPT-7.1 activity increases, releasing zinc from internal stores. The resulting increase in cytoplasmic zinc promotes the phenotypic changes characteristic of activation. Thus, zinc signaling is a key step in the signal transduction process that mediates sperm activation, and we have identified a zinc transporter that is central to this activation process.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.2005069&type=printable |
| spellingShingle | Yanmei Zhao Chieh-Hsiang Tan Amber Krauchunas Andrea Scharf Nicholas Dietrich Kurt Warnhoff Zhiheng Yuan Marina Druzhinina Sam Guoping Gu Long Miao Andrew Singson Ronald E Ellis Kerry Kornfeld The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. PLoS Biology |
| title | The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. |
| title_full | The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. |
| title_fullStr | The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. |
| title_full_unstemmed | The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. |
| title_short | The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. |
| title_sort | zinc transporter zipt 7 1 regulates sperm activation in nematodes |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.2005069&type=printable |
| work_keys_str_mv | AT yanmeizhao thezinctransporterzipt71regulatesspermactivationinnematodes AT chiehhsiangtan thezinctransporterzipt71regulatesspermactivationinnematodes AT amberkrauchunas thezinctransporterzipt71regulatesspermactivationinnematodes AT andreascharf thezinctransporterzipt71regulatesspermactivationinnematodes AT nicholasdietrich thezinctransporterzipt71regulatesspermactivationinnematodes AT kurtwarnhoff thezinctransporterzipt71regulatesspermactivationinnematodes AT zhihengyuan thezinctransporterzipt71regulatesspermactivationinnematodes AT marinadruzhinina thezinctransporterzipt71regulatesspermactivationinnematodes AT samguopinggu thezinctransporterzipt71regulatesspermactivationinnematodes AT longmiao thezinctransporterzipt71regulatesspermactivationinnematodes AT andrewsingson thezinctransporterzipt71regulatesspermactivationinnematodes AT ronaldeellis thezinctransporterzipt71regulatesspermactivationinnematodes AT kerrykornfeld thezinctransporterzipt71regulatesspermactivationinnematodes AT yanmeizhao zinctransporterzipt71regulatesspermactivationinnematodes AT chiehhsiangtan zinctransporterzipt71regulatesspermactivationinnematodes AT amberkrauchunas zinctransporterzipt71regulatesspermactivationinnematodes AT andreascharf zinctransporterzipt71regulatesspermactivationinnematodes AT nicholasdietrich zinctransporterzipt71regulatesspermactivationinnematodes AT kurtwarnhoff zinctransporterzipt71regulatesspermactivationinnematodes AT zhihengyuan zinctransporterzipt71regulatesspermactivationinnematodes AT marinadruzhinina zinctransporterzipt71regulatesspermactivationinnematodes AT samguopinggu zinctransporterzipt71regulatesspermactivationinnematodes AT longmiao zinctransporterzipt71regulatesspermactivationinnematodes AT andrewsingson zinctransporterzipt71regulatesspermactivationinnematodes AT ronaldeellis zinctransporterzipt71regulatesspermactivationinnematodes AT kerrykornfeld zinctransporterzipt71regulatesspermactivationinnematodes |