TY - JOUR
T1 - Phagocytosis is mediated by two-dimensional assemblies of the F-BAR protein GAS7
AU - Hanawa-Suetsugu, Kyoko
AU - Itoh, Yuzuru
AU - Ab Fatah, Maisarah
AU - Nishimura, Tamako
AU - Takemura, Kazuhiro
AU - Takeshita, Kohei
AU - Kubota, Satoru
AU - Miyazaki, Naoyuki
AU - Wan Mohamad Noor, Wan Nurul Izzati
AU - Inaba, Takehiko
AU - Nguyen, Nhung Thi Hong
AU - Hamada-Nakahara, Sayaka
AU - Oono-Yakura, Kayoko
AU - Tachikawa, Masashi
AU - Iwasaki, Kenji
AU - Kohda, Daisuke
AU - Yamamoto, Masaki
AU - Kitao, Akio
AU - Shimada, Atsushi
AU - Suetsugu, Shiro
N1 - Funding Information:
We thank Prof. Oliver Daumke (Max-Delbrück-Centrum for Molecular Medicine) for critical reading of the manuscript. We thank Prof. Toshio Kitamura (The University of Tokyo) for the PLAT-A cells, Prof. Masahito Ikawa (Osaka University) and Prof. Taro Kawai (Nara Institute of Science and Technology) for the CRISPR/Cas9 system, Dr. Yohei Katoh and Prof. Kazuhisa Nakayama (Kyoto University) for the nanobody to GFP, Dr. Takahiro Fujiwara, Dr. Rinshi S. Kasai (Kyoto University) and Dr. Kenichi G.N. Suzuki (Gifu University) for advice on STORM and PALM, Dr. Kouta Mayanagi (Kyushu University), Dr. Hideki Shigematsu (RIKEN SPring-8 Center) and Ryo Ugawa (Laboratory for Technical Support, Medical Institute of Bioregulation, Kyushu University) for their support and advice on electron microscopy and Dr. Arthur Melo, Ayumi Takemoto, Kuniko Ohtake, Kosaku Kamihara, Ayana Wada, Katsuya Inamine, Yuki Kawasaki, Seiichiro Hayashi and all of the members of the laboratories for technical assistance and helpful discussions, and the staff members of the beamlines, Dr. Kunio Hirata (RIKEN SPring-8 Center), Dr. Naoki Sakai (RIKEN SPring-8 Center), Dr. Seiki Baba (Japan Synchrotron Radiation Research Institute) and Dr. Takashi Kumasaka (Japan Synchrotron Radiation Research Institute) and others, for assistance with our data collection. Synchrotron radiation experiments were performed at the Photon Factory with the approval of the Photon Factory Program Advisory Committee (Proposal Nos. 2011G092 and 2012G691) and at SPring-8 beamlines BL32XU, BL38B1 and BL44XU. This work was supported by grants from the Funding Program for Next Generation World-Leading Researchers (NEXT program LS031), JSPS (KAKENHI 26291037, JP15H0164, JP15H05902, JP17H03674, JP17H06006), JST CREST (JPMJCR1863), Osaka Cancer Research Foundation, the Naito Foundation, the Sumitomo Foundation, the Mitsubishi Foundation, the Sagawa Foundation for Promotion of Cancer Research and the NAIST Interdisciplinary Frontier Research Project to S.S., JSPS (KAKENHI 24687014, 25121726, JP17K07309) to A.S., JSPS (KAKENHI JP16K07351) to K.H.-S., JSPS (KAKENHI 23121507) to Y.I., JSPS (KAKENHI JP15H04357, JP17KT0026), MEXT ‘Priority Issue on Post-K Computer’ (Building Innovative Drug Discovery Infrastructure through Functional Control of Biomolecular Systems) to A.K. and Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from Japan Agency for Medical Research and Development (AMED), under Grant Numbers JP19am0101070 and JP19am0101072. The computations were partly performed using the supercomputers at the RCCS, The National Institute of Natural Science, ISSP and The University of Tokyo. This research also used the computational resources of the K computer, provided by the RIKEN Advanced Institute for Computational Science through the HPCI System Research project (Project ID: hp180201). This work was partly performed in the Cooperative Research Project Program of the Medical Institute of Bioregulation, Kyushu University.
Publisher Copyright:
© 2019, The Author(s).
PY - 2019/12/1
Y1 - 2019/12/1
N2 - Phagocytosis is a cellular process for internalization of micron-sized large particles including pathogens. The Bin-Amphiphysin-Rvs167 (BAR) domain proteins, including the FCH-BAR (F-BAR) domain proteins, impose specific morphologies on lipid membranes. Most BAR domain proteins are thought to form membrane invaginations or protrusions by assembling into helical submicron-diameter filaments, such as on clathrin-coated pits, caveolae, and filopodia. However, the mechanism by which BAR domain proteins assemble into micron-scale phagocytic cups was unclear. Here, we show that the two-dimensional sheet-like assembly of Growth Arrest-Specific 7 (GAS7) plays a critical role in phagocytic cup formation in macrophages. GAS7 has the F-BAR domain that possesses unique hydrophilic loops for two-dimensional sheet formation on flat membranes. Super-resolution microscopy reveals the similar assemblies of GAS7 on phagocytic cups and liposomes. The mutations of the loops abolishes both the membrane localization of GAS7 and phagocytosis. Thus, the sheet-like assembly of GAS7 plays a significant role in phagocytosis.
AB - Phagocytosis is a cellular process for internalization of micron-sized large particles including pathogens. The Bin-Amphiphysin-Rvs167 (BAR) domain proteins, including the FCH-BAR (F-BAR) domain proteins, impose specific morphologies on lipid membranes. Most BAR domain proteins are thought to form membrane invaginations or protrusions by assembling into helical submicron-diameter filaments, such as on clathrin-coated pits, caveolae, and filopodia. However, the mechanism by which BAR domain proteins assemble into micron-scale phagocytic cups was unclear. Here, we show that the two-dimensional sheet-like assembly of Growth Arrest-Specific 7 (GAS7) plays a critical role in phagocytic cup formation in macrophages. GAS7 has the F-BAR domain that possesses unique hydrophilic loops for two-dimensional sheet formation on flat membranes. Super-resolution microscopy reveals the similar assemblies of GAS7 on phagocytic cups and liposomes. The mutations of the loops abolishes both the membrane localization of GAS7 and phagocytosis. Thus, the sheet-like assembly of GAS7 plays a significant role in phagocytosis.
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U2 - 10.1038/s41467-019-12738-w
DO - 10.1038/s41467-019-12738-w
M3 - Article
C2 - 31628328
AN - SCOPUS:85073511723
VL - 10
JO - Nature Communications
JF - Nature Communications
SN - 2041-1723
IS - 1
M1 - 4763
ER -