Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics
The plasma membrane (PM) serves multiple functions to support cell activities with its heterogeneous molecular distribution. Fatty acids (FAs) are hydrophobic components of the PM whose saturation and length determine the membrane’s physical properties. The FA distribution contributes to the PM’s la...
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-12-01
|
| Series: | Cells |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2073-4409/12/1/10 |
| _version_ | 1797626139854766080 |
|---|---|
| author | Chi Zhang Kenji Kikushima Mizuki Endo Tomoaki Kahyo Makoto Horikawa Takaomi Matsudaira Tatsuya Tanaka Yusuke Takanashi Tomohito Sato Yutaka Takahashi Lili Xu Naoki Takayama Ariful Islam Md. Al Mamun Takeaki Ozawa Mitsutoshi Setou |
| author_facet | Chi Zhang Kenji Kikushima Mizuki Endo Tomoaki Kahyo Makoto Horikawa Takaomi Matsudaira Tatsuya Tanaka Yusuke Takanashi Tomohito Sato Yutaka Takahashi Lili Xu Naoki Takayama Ariful Islam Md. Al Mamun Takeaki Ozawa Mitsutoshi Setou |
| author_sort | Chi Zhang |
| collection | DOAJ |
| description | The plasma membrane (PM) serves multiple functions to support cell activities with its heterogeneous molecular distribution. Fatty acids (FAs) are hydrophobic components of the PM whose saturation and length determine the membrane’s physical properties. The FA distribution contributes to the PM’s lateral heterogeneity. However, the distribution of PM FAs is poorly understood. Here, we proposed the FA cluster hypothesis, which suggested that FAs on the PM exist as clusters. By the optogenetic tool translocating the endoplasmic reticulum (ER), we were able to manipulate the distribution of PM FAs. We used time-of-flight combined secondary ion mass spectrometry (TOF-SIMS) to image PM FAs and discovered that PM FAs were presented and distributed as clusters and are also manipulated as clusters. We also found the existence of multi-FA clusters formed by the colocalization of more than one FA. Our optogenetic tool also decreased the clustering degree of FA clusters and the formation probability of multi-FA clusters. This research opens up new avenues and perspectives to study PM heterogeneity from an FA perspective. This research also suggests a possible treatment for diseases caused by PM lipid aggregation and furnished a convenient tool for therapeutic development. |
| first_indexed | 2024-03-11T10:06:15Z |
| format | Article |
| id | doaj.art-c51a95ecac054aa38c21ce91fdbc4d5c |
| institution | Directory Open Access Journal |
| issn | 2073-4409 |
| language | English |
| last_indexed | 2024-03-11T10:06:15Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Cells |
| spelling | doaj.art-c51a95ecac054aa38c21ce91fdbc4d5c2023-11-16T15:04:50ZengMDPI AGCells2073-44092022-12-011211010.3390/cells12010010Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined OptogeneticsChi Zhang0Kenji Kikushima1Mizuki Endo2Tomoaki Kahyo3Makoto Horikawa4Takaomi Matsudaira5Tatsuya Tanaka6Yusuke Takanashi7Tomohito Sato8Yutaka Takahashi9Lili Xu10Naoki Takayama11Ariful Islam12Md. Al Mamun13Takeaki Ozawa14Mitsutoshi Setou15Department of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Chemistry, School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanFoundation for Promotion of Material Science and Technology of Japan, 1-18-6 Kitami, Setagaya-ku, Tokyo 157-0067, JapanFoundation for Promotion of Material Science and Technology of Japan, 1-18-6 Kitami, Setagaya-ku, Tokyo 157-0067, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanDepartment of Chemistry, School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, JapanDepartment of Cellular and Molecular Anatomy, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu, Shizuoka 431-3192, JapanThe plasma membrane (PM) serves multiple functions to support cell activities with its heterogeneous molecular distribution. Fatty acids (FAs) are hydrophobic components of the PM whose saturation and length determine the membrane’s physical properties. The FA distribution contributes to the PM’s lateral heterogeneity. However, the distribution of PM FAs is poorly understood. Here, we proposed the FA cluster hypothesis, which suggested that FAs on the PM exist as clusters. By the optogenetic tool translocating the endoplasmic reticulum (ER), we were able to manipulate the distribution of PM FAs. We used time-of-flight combined secondary ion mass spectrometry (TOF-SIMS) to image PM FAs and discovered that PM FAs were presented and distributed as clusters and are also manipulated as clusters. We also found the existence of multi-FA clusters formed by the colocalization of more than one FA. Our optogenetic tool also decreased the clustering degree of FA clusters and the formation probability of multi-FA clusters. This research opens up new avenues and perspectives to study PM heterogeneity from an FA perspective. This research also suggests a possible treatment for diseases caused by PM lipid aggregation and furnished a convenient tool for therapeutic development.https://www.mdpi.com/2073-4409/12/1/10plasma membrane fatty acidsTOF-SIMSoptogeneticsmembrane heterogeneityfatty acid imaging |
| spellingShingle | Chi Zhang Kenji Kikushima Mizuki Endo Tomoaki Kahyo Makoto Horikawa Takaomi Matsudaira Tatsuya Tanaka Yusuke Takanashi Tomohito Sato Yutaka Takahashi Lili Xu Naoki Takayama Ariful Islam Md. Al Mamun Takeaki Ozawa Mitsutoshi Setou Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics Cells plasma membrane fatty acids TOF-SIMS optogenetics membrane heterogeneity fatty acid imaging |
| title | Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics |
| title_full | Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics |
| title_fullStr | Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics |
| title_full_unstemmed | Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics |
| title_short | Imaging and Manipulation of Plasma Membrane Fatty Acid Clusters Using TOF-SIMS Combined Optogenetics |
| title_sort | imaging and manipulation of plasma membrane fatty acid clusters using tof sims combined optogenetics |
| topic | plasma membrane fatty acids TOF-SIMS optogenetics membrane heterogeneity fatty acid imaging |
| url | https://www.mdpi.com/2073-4409/12/1/10 |
| work_keys_str_mv | AT chizhang imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT kenjikikushima imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT mizukiendo imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT tomoakikahyo imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT makotohorikawa imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT takaomimatsudaira imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT tatsuyatanaka imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT yusuketakanashi imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT tomohitosato imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT yutakatakahashi imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT lilixu imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT naokitakayama imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT arifulislam imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT mdalmamun imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT takeakiozawa imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics AT mitsutoshisetou imagingandmanipulationofplasmamembranefattyacidclustersusingtofsimscombinedoptogenetics |