Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes
Summary: TRPM7 (transient receptor potential cation channel subfamily M member 7) is a chanzyme with channel and kinase domains essential for embryo development. Using gamete-specific Trpm7-null lines, we report that TRPM7-mediated Mg2+ influx is indispensable for reaching the blastocyst stage. TRPM...
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| Format: | Article |
| Language: | English |
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Elsevier
2023-10-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723012445 |
| _version_ | 1797660326712311808 |
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| author | Neha Gupta Cristina Soriano-Úbeda Paula Stein Virginia Savy Brian N. Papas Goli Ardestani Ingrid Carvacho Dominique Alfandari Carmen J. Williams Rafael A. Fissore |
| author_facet | Neha Gupta Cristina Soriano-Úbeda Paula Stein Virginia Savy Brian N. Papas Goli Ardestani Ingrid Carvacho Dominique Alfandari Carmen J. Williams Rafael A. Fissore |
| author_sort | Neha Gupta |
| collection | DOAJ |
| description | Summary: TRPM7 (transient receptor potential cation channel subfamily M member 7) is a chanzyme with channel and kinase domains essential for embryo development. Using gamete-specific Trpm7-null lines, we report that TRPM7-mediated Mg2+ influx is indispensable for reaching the blastocyst stage. TRPM7 is expressed dynamically from gametes to blastocysts; displays stage-specific localization on the plasma membrane, cytoplasm, and nucleus; and undergoes cleavage that produces C-terminal kinase fragments. TRPM7 underpins Mg2+ homeostasis, and excess Mg2+ but not Zn2+ or Ca2+ overcomes the arrest of Trpm7-null embryos; expressing Trpm7 mRNA restores development, but mutant versions fail or are partially rescued. Transcriptomic analyses of Trpm7-null embryos reveal an abundance of oxidative stress-pathway genes, confirmed by mitochondrial dysfunction, and a reduction in transcription factor networks essential for proliferation; Mg2+ supplementation corrects these defects. Hence, TRPM7 underpins Mg2+ homeostasis in preimplantation embryos, prevents oxidative stress, and promotes gene expression patterns necessary for developmental progression and cell-lineage specification. |
| first_indexed | 2024-03-11T18:29:10Z |
| format | Article |
| id | doaj.art-a5b04c756beb49d29a15840e6514831d |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-03-11T18:29:10Z |
| publishDate | 2023-10-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-a5b04c756beb49d29a15840e6514831d2023-10-13T13:53:25ZengElsevierCell Reports2211-12472023-10-014210113232Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametesNeha Gupta0Cristina Soriano-Úbeda1Paula Stein2Virginia Savy3Brian N. Papas4Goli Ardestani5Ingrid Carvacho6Dominique Alfandari7Carmen J. Williams8Rafael A. Fissore9Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, MA 01003, USADepartment of Veterinary and Animal Sciences, University of Massachusetts, Amherst, MA 01003, USA; Department of Veterinary Medicine, Surgery, and Anatomy, Veterinary School, University of León, León, SpainReproductive & Developmental Biology Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC, USAReproductive & Developmental Biology Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC, USAIntegrative Bioinformatics Support Group, Biostatistics and Computational Biology Branch, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC, USADepartment of Veterinary and Animal Sciences, University of Massachusetts, Amherst, MA 01003, USA; Clinical Research Embryologist, Boston IVF, Waltham, MA, USAFaculty of Medicine, Universidad Católica del Maule, Talca, ChileDepartment of Veterinary and Animal Sciences, University of Massachusetts, Amherst, MA 01003, USAReproductive & Developmental Biology Laboratory, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC, USADepartment of Veterinary and Animal Sciences, University of Massachusetts, Amherst, MA 01003, USA; Corresponding authorSummary: TRPM7 (transient receptor potential cation channel subfamily M member 7) is a chanzyme with channel and kinase domains essential for embryo development. Using gamete-specific Trpm7-null lines, we report that TRPM7-mediated Mg2+ influx is indispensable for reaching the blastocyst stage. TRPM7 is expressed dynamically from gametes to blastocysts; displays stage-specific localization on the plasma membrane, cytoplasm, and nucleus; and undergoes cleavage that produces C-terminal kinase fragments. TRPM7 underpins Mg2+ homeostasis, and excess Mg2+ but not Zn2+ or Ca2+ overcomes the arrest of Trpm7-null embryos; expressing Trpm7 mRNA restores development, but mutant versions fail or are partially rescued. Transcriptomic analyses of Trpm7-null embryos reveal an abundance of oxidative stress-pathway genes, confirmed by mitochondrial dysfunction, and a reduction in transcription factor networks essential for proliferation; Mg2+ supplementation corrects these defects. Hence, TRPM7 underpins Mg2+ homeostasis in preimplantation embryos, prevents oxidative stress, and promotes gene expression patterns necessary for developmental progression and cell-lineage specification.http://www.sciencedirect.com/science/article/pii/S2211124723012445CP: Developmental biologyCP: Cell biology |
| spellingShingle | Neha Gupta Cristina Soriano-Úbeda Paula Stein Virginia Savy Brian N. Papas Goli Ardestani Ingrid Carvacho Dominique Alfandari Carmen J. Williams Rafael A. Fissore Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes Cell Reports CP: Developmental biology CP: Cell biology |
| title | Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes |
| title_full | Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes |
| title_fullStr | Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes |
| title_full_unstemmed | Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes |
| title_short | Essential role of Mg2+ in mouse preimplantation embryo development revealed by TRPM7 chanzyme-deficient gametes |
| title_sort | essential role of mg2 in mouse preimplantation embryo development revealed by trpm7 chanzyme deficient gametes |
| topic | CP: Developmental biology CP: Cell biology |
| url | http://www.sciencedirect.com/science/article/pii/S2211124723012445 |
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