Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins
Summary: Meiotic gene expression in budding yeast is tightly controlled by RNA-binding proteins (RBPs), with the meiosis-specific RBP Rim4 playing a key role in sequestering mid-late meiotic transcripts to prevent premature translation. However, the mechanisms governing assembly and disassembly of t...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-09-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S221112472301063X |
| _version_ | 1827834835383615488 |
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| author | Rudian Zhang Wenzhi Feng Suhong Qian Shunjin Li Fei Wang |
| author_facet | Rudian Zhang Wenzhi Feng Suhong Qian Shunjin Li Fei Wang |
| author_sort | Rudian Zhang |
| collection | DOAJ |
| description | Summary: Meiotic gene expression in budding yeast is tightly controlled by RNA-binding proteins (RBPs), with the meiosis-specific RBP Rim4 playing a key role in sequestering mid-late meiotic transcripts to prevent premature translation. However, the mechanisms governing assembly and disassembly of the Rim4-mRNA complex, critical for Rim4’s function and stability, remain poorly understood. In this study, we unveil regulation of the Rim4 ribonucleoprotein (RNP) complex by the yeast 14-3-3 proteins Bmh1 and Bmh2. These proteins form a Rim4-Bmh1-Bmh2 heterotrimeric complex that expels mRNAs from Rim4 binding. We identify four Bmh1/2 binding sites (BBSs) on Rim4, with two residing within the RNA recognition motifs (RRMs). Phosphorylation and dephosphorylation of serine/threonine (S/T) residues at these BBSs by PKA kinase and Cdc14 phosphatase activities primarily control formation of Rim4-Bmh1/2, regulating Rim4’s subcellular distribution, function, and stability. These findings shed light on the intricate post-transcriptional regulatory mechanisms governing meiotic gene expression. |
| first_indexed | 2024-03-12T05:58:46Z |
| format | Article |
| id | doaj.art-918e9061117a4878a80712baa1c230f9 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-12T05:58:46Z |
| publishDate | 2023-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-918e9061117a4878a80712baa1c230f92023-09-03T04:23:49ZengElsevierCell Reports2211-12472023-09-01429113052Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteinsRudian Zhang0Wenzhi Feng1Suhong Qian2Shunjin Li3Fei Wang4Department of Cell Biology, UT Southwestern Medical Center, Dallas, TX 75390, USADepartment of Cell Biology, UT Southwestern Medical Center, Dallas, TX 75390, USADepartment of Cell Biology, UT Southwestern Medical Center, Dallas, TX 75390, USADepartment of Cell Biology, UT Southwestern Medical Center, Dallas, TX 75390, USADepartment of Cell Biology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Corresponding authorSummary: Meiotic gene expression in budding yeast is tightly controlled by RNA-binding proteins (RBPs), with the meiosis-specific RBP Rim4 playing a key role in sequestering mid-late meiotic transcripts to prevent premature translation. However, the mechanisms governing assembly and disassembly of the Rim4-mRNA complex, critical for Rim4’s function and stability, remain poorly understood. In this study, we unveil regulation of the Rim4 ribonucleoprotein (RNP) complex by the yeast 14-3-3 proteins Bmh1 and Bmh2. These proteins form a Rim4-Bmh1-Bmh2 heterotrimeric complex that expels mRNAs from Rim4 binding. We identify four Bmh1/2 binding sites (BBSs) on Rim4, with two residing within the RNA recognition motifs (RRMs). Phosphorylation and dephosphorylation of serine/threonine (S/T) residues at these BBSs by PKA kinase and Cdc14 phosphatase activities primarily control formation of Rim4-Bmh1/2, regulating Rim4’s subcellular distribution, function, and stability. These findings shed light on the intricate post-transcriptional regulatory mechanisms governing meiotic gene expression.http://www.sciencedirect.com/science/article/pii/S221112472301063XCP: Cell biology |
| spellingShingle | Rudian Zhang Wenzhi Feng Suhong Qian Shunjin Li Fei Wang Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins Cell Reports CP: Cell biology |
| title | Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins |
| title_full | Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins |
| title_fullStr | Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins |
| title_full_unstemmed | Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins |
| title_short | Regulation of Rim4 distribution, function, and stability during meiosis by PKA, Cdc14, and 14-3-3 proteins |
| title_sort | regulation of rim4 distribution function and stability during meiosis by pka cdc14 and 14 3 3 proteins |
| topic | CP: Cell biology |
| url | http://www.sciencedirect.com/science/article/pii/S221112472301063X |
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