Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production
Although many recombinant proteins have been produced in seeds at high yields without adverse effects on the plant, endoplasmic reticulum (ER) stress and aberrant localization of endogenous or recombinant proteins have also been reported. The production of murine interleukin-10 (mIL-10) in Arabidops...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-06-01
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| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.00777/full |
| _version_ | 1818925514746757120 |
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| author | Elsa Arcalis Verena Ibl Julia Hilscher Thomas Rademacher Linda Avesani Francesca Morandini Luisa Bortesi Mario Pezzotti Alessandro Vitale Dietmar Pum Thomas De Meyer Thomas De Meyer Ann Depicker Ann Depicker Eva Stoger |
| author_facet | Elsa Arcalis Verena Ibl Julia Hilscher Thomas Rademacher Linda Avesani Francesca Morandini Luisa Bortesi Mario Pezzotti Alessandro Vitale Dietmar Pum Thomas De Meyer Thomas De Meyer Ann Depicker Ann Depicker Eva Stoger |
| author_sort | Elsa Arcalis |
| collection | DOAJ |
| description | Although many recombinant proteins have been produced in seeds at high yields without adverse effects on the plant, endoplasmic reticulum (ER) stress and aberrant localization of endogenous or recombinant proteins have also been reported. The production of murine interleukin-10 (mIL-10) in Arabidopsis thaliana seeds resulted in the de novo formation of ER-derived structures containing a large fraction of the recombinant protein in an insoluble form. These bodies containing mIL-10 were morphologically similar to Russell bodies found in mammalian cells. We confirmed that the compartment containing mIL-10 was enclosed by ER membranes, and 3D electron microscopy revealed that these structures have a spheroidal shape. Another feature shared with Russell bodies is the continued viability of the cells that generate these organelles. To investigate similarities in the formation of Russell-like bodies and the plant-specific protein bodies formed by prolamins in cereal seeds, we crossed plants containing ectopic ER-derived prolamin protein bodies with a line accumulating mIL-10 in Russell-like bodies. This resulted in seeds containing only one population of protein bodies in which mIL-10 inclusions formed a central core surrounded by the prolamin-containing matrix, suggesting that both types of protein aggregates are together removed from the secretory pathway by a common mechanism. We propose that, like mammalian cells, plant cells are able to form Russell-like bodies as a self-protection mechanism, when they are overloaded with a partially transport-incompetent protein, and we discuss the resulting challenges for recombinant protein production. |
| first_indexed | 2024-12-20T02:42:26Z |
| format | Article |
| id | doaj.art-3c9eeec500f84ef2839a2afb931a703f |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-20T02:42:26Z |
| publishDate | 2019-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-3c9eeec500f84ef2839a2afb931a703f2022-12-21T19:56:17ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-06-011010.3389/fpls.2019.00777457449Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein ProductionElsa Arcalis0Verena Ibl1Julia Hilscher2Thomas Rademacher3Linda Avesani4Francesca Morandini5Luisa Bortesi6Mario Pezzotti7Alessandro Vitale8Dietmar Pum9Thomas De Meyer10Thomas De Meyer11Ann Depicker12Ann Depicker13Eva Stoger14Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, AustriaDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, AustriaDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, AustriaFraunhofer Institute for Molecular Biology and Applied Ecology IME, Aachen, GermanyDepartment of Biotechnology, University of Verona, Verona, ItalyDepartment of Biotechnology, University of Verona, Verona, ItalyDepartment of Biotechnology, University of Verona, Verona, ItalyDepartment of Biotechnology, University of Verona, Verona, ItalyInstitute of Agricultural Biology and Biotechnology, CNR, Milan, ItalyDepartment of Nanobiotechnology, University of Natural Resources and Life Sciences, Vienna, AustriaDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, BelgiumVIB Center for Plant Systems Biology, Ghent, BelgiumDepartment of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, AustriaAlthough many recombinant proteins have been produced in seeds at high yields without adverse effects on the plant, endoplasmic reticulum (ER) stress and aberrant localization of endogenous or recombinant proteins have also been reported. The production of murine interleukin-10 (mIL-10) in Arabidopsis thaliana seeds resulted in the de novo formation of ER-derived structures containing a large fraction of the recombinant protein in an insoluble form. These bodies containing mIL-10 were morphologically similar to Russell bodies found in mammalian cells. We confirmed that the compartment containing mIL-10 was enclosed by ER membranes, and 3D electron microscopy revealed that these structures have a spheroidal shape. Another feature shared with Russell bodies is the continued viability of the cells that generate these organelles. To investigate similarities in the formation of Russell-like bodies and the plant-specific protein bodies formed by prolamins in cereal seeds, we crossed plants containing ectopic ER-derived prolamin protein bodies with a line accumulating mIL-10 in Russell-like bodies. This resulted in seeds containing only one population of protein bodies in which mIL-10 inclusions formed a central core surrounded by the prolamin-containing matrix, suggesting that both types of protein aggregates are together removed from the secretory pathway by a common mechanism. We propose that, like mammalian cells, plant cells are able to form Russell-like bodies as a self-protection mechanism, when they are overloaded with a partially transport-incompetent protein, and we discuss the resulting challenges for recombinant protein production.https://www.frontiersin.org/article/10.3389/fpls.2019.00777/fullmolecular farmingrecombinant proteinprotein bodieselectron tomographysubcellular targeting |
| spellingShingle | Elsa Arcalis Verena Ibl Julia Hilscher Thomas Rademacher Linda Avesani Francesca Morandini Luisa Bortesi Mario Pezzotti Alessandro Vitale Dietmar Pum Thomas De Meyer Thomas De Meyer Ann Depicker Ann Depicker Eva Stoger Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production Frontiers in Plant Science molecular farming recombinant protein protein bodies electron tomography subcellular targeting |
| title | Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production |
| title_full | Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production |
| title_fullStr | Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production |
| title_full_unstemmed | Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production |
| title_short | Russell-Like Bodies in Plant Seeds Share Common Features With Prolamin Bodies and Occur Upon Recombinant Protein Production |
| title_sort | russell like bodies in plant seeds share common features with prolamin bodies and occur upon recombinant protein production |
| topic | molecular farming recombinant protein protein bodies electron tomography subcellular targeting |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.00777/full |
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