The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks
Golgins are a family of Golgi-localized long coiled-coil proteins. The major golgin function is thought to be the tethering of vesicles, membranes, and cytoskeletal elements to the Golgi. We previously showed that knockdown of one of the longest golgins, Giantin, altered the glycosylation patterns o...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-08-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fcell.2019.00160/full |
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| author | Ayano Satoh Mitsuko Hayashi-Nishino Takuto Shakuno Junko Masuda Mayuko Koreishi Runa Murakami Yoshimasa Nakamura Toshiyuki Nakamura Naomi Abe-Kanoh Naomi Abe-Kanoh Yasuko Honjo Joerg Malsam Sidney Yu Kunihiko Nishino |
| author_facet | Ayano Satoh Mitsuko Hayashi-Nishino Takuto Shakuno Junko Masuda Mayuko Koreishi Runa Murakami Yoshimasa Nakamura Toshiyuki Nakamura Naomi Abe-Kanoh Naomi Abe-Kanoh Yasuko Honjo Joerg Malsam Sidney Yu Kunihiko Nishino |
| author_sort | Ayano Satoh |
| collection | DOAJ |
| description | Golgins are a family of Golgi-localized long coiled-coil proteins. The major golgin function is thought to be the tethering of vesicles, membranes, and cytoskeletal elements to the Golgi. We previously showed that knockdown of one of the longest golgins, Giantin, altered the glycosylation patterns of cell surfaces and the kinetics of cargo transport, suggesting that Giantin maintains correct glycosylation through slowing down transport within the Golgi. Giantin knockdown also altered the sizes and numbers of mini Golgi stacks generated by microtubule de-polymerization, suggesting that it maintains the independence of individual Golgi stacks. Therefore, it is presumed that Golgi stacks lose their independence following Giantin knockdown, allowing easier and possibly increased transport among stacks and abnormal glycosylation. To gain structural insights into the independence of Golgi stacks, we herein performed electron tomography and 3D modeling of Golgi stacks in Giantin knockdown cells. Compared with control cells, Giantin-knockdown cells had fewer and smaller fenestrae within each cisterna. This was supported by data showing that the diffusion rate of Golgi membrane proteins is faster in Giantin-knockdown Golgi, indicating that Giantin knockdown structurally and functionally increases connectivity among Golgi cisternae and stacks. This increased connectivity suggests that contrary to the cis-golgin tether model, Giantin instead inhibits the tether and fusion of nearby Golgi cisternae and stacks, resulting in transport difficulties between stacks that may enable the correct glycosylation of proteins and lipids passing through the Golgi. |
| first_indexed | 2024-12-22T11:05:40Z |
| format | Article |
| id | doaj.art-9f868208c8924e6f85c59f72e33b0813 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-22T11:05:40Z |
| publishDate | 2019-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-9f868208c8924e6f85c59f72e33b08132022-12-21T18:28:20ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2019-08-01710.3389/fcell.2019.00160460665The Golgin Protein Giantin Regulates Interconnections Between Golgi StacksAyano Satoh0Mitsuko Hayashi-Nishino1Takuto Shakuno2Junko Masuda3Mayuko Koreishi4Runa Murakami5Yoshimasa Nakamura6Toshiyuki Nakamura7Naomi Abe-Kanoh8Naomi Abe-Kanoh9Yasuko Honjo10Joerg Malsam11Sidney Yu12Kunihiko Nishino13Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama, JapanInstitute of Scientific and Industrial Research, Osaka University, Osaka, JapanGraduate School of Natural Science and Technology, Okayama University, Okayama, JapanGraduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama, JapanGraduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama, JapanGraduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, Okayama, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanGraduate School of Environmental and Life Science, Okayama University, Okayama, JapanDepartment of Public Health and Applied Nutrition, Institute of Biomedical Sciences, Graduate School Tokushima University, Tokushima, JapanResearch Institute for Radiation Biology and Medicine, Hiroshima University, Hiroshima, JapanCenter for Biochemistry (BZH), Heidelberg University, Heidelberg, GermanySchool of Biomedical Sciences, The Chinese University of Hong Kong, Hong Kong, Hong KongInstitute of Scientific and Industrial Research, Osaka University, Osaka, JapanGolgins are a family of Golgi-localized long coiled-coil proteins. The major golgin function is thought to be the tethering of vesicles, membranes, and cytoskeletal elements to the Golgi. We previously showed that knockdown of one of the longest golgins, Giantin, altered the glycosylation patterns of cell surfaces and the kinetics of cargo transport, suggesting that Giantin maintains correct glycosylation through slowing down transport within the Golgi. Giantin knockdown also altered the sizes and numbers of mini Golgi stacks generated by microtubule de-polymerization, suggesting that it maintains the independence of individual Golgi stacks. Therefore, it is presumed that Golgi stacks lose their independence following Giantin knockdown, allowing easier and possibly increased transport among stacks and abnormal glycosylation. To gain structural insights into the independence of Golgi stacks, we herein performed electron tomography and 3D modeling of Golgi stacks in Giantin knockdown cells. Compared with control cells, Giantin-knockdown cells had fewer and smaller fenestrae within each cisterna. This was supported by data showing that the diffusion rate of Golgi membrane proteins is faster in Giantin-knockdown Golgi, indicating that Giantin knockdown structurally and functionally increases connectivity among Golgi cisternae and stacks. This increased connectivity suggests that contrary to the cis-golgin tether model, Giantin instead inhibits the tether and fusion of nearby Golgi cisternae and stacks, resulting in transport difficulties between stacks that may enable the correct glycosylation of proteins and lipids passing through the Golgi.https://www.frontiersin.org/article/10.3389/fcell.2019.00160/fullGolgigolginsglycosylationendoplasmic reticulumelectron tomography |
| spellingShingle | Ayano Satoh Mitsuko Hayashi-Nishino Takuto Shakuno Junko Masuda Mayuko Koreishi Runa Murakami Yoshimasa Nakamura Toshiyuki Nakamura Naomi Abe-Kanoh Naomi Abe-Kanoh Yasuko Honjo Joerg Malsam Sidney Yu Kunihiko Nishino The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks Frontiers in Cell and Developmental Biology Golgi golgins glycosylation endoplasmic reticulum electron tomography |
| title | The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks |
| title_full | The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks |
| title_fullStr | The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks |
| title_full_unstemmed | The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks |
| title_short | The Golgin Protein Giantin Regulates Interconnections Between Golgi Stacks |
| title_sort | golgin protein giantin regulates interconnections between golgi stacks |
| topic | Golgi golgins glycosylation endoplasmic reticulum electron tomography |
| url | https://www.frontiersin.org/article/10.3389/fcell.2019.00160/full |
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