Opposing roles for SNAP23 in secretion in exocrine and endocrine pancreatic cells
The membrane fusion of secretory granules with plasma membranes is crucial for the exocytosis of hormones and enzymes. Secretion disorders can cause various diseases such as diabetes or pancreatitis. Synaptosomal-associated protein 23 (SNAP23), a soluble N-ethyl-maleimide sensitive fusion protein at...
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| Published in | The Journal of cell biology Vol. 215; no. 1; pp. 121 - 138 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
10.10.2016
The Rockefeller University Press |
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| Abstract | The membrane fusion of secretory granules with plasma membranes is crucial for the exocytosis of hormones and enzymes. Secretion disorders can cause various diseases such as diabetes or pancreatitis. Synaptosomal-associated protein 23 (SNAP23), a soluble N-ethyl-maleimide sensitive fusion protein attachment protein receptor (SNARE) molecule, is essential for secretory granule fusion in several cell lines. However, the in vivo functions of SNAP23 in endocrine and exocrine tissues remain unclear. In this study, we show opposing roles for SNAP23 in secretion in pancreatic exocrine and endocrine cells. The loss of SNAP23 in the exocrine and endocrine pancreas resulted in decreased and increased fusion of granules to the plasma membrane after stimulation, respectively. Furthermore, we identified a low molecular weight compound, MF286, that binds specifically to SNAP23 and promotes insulin secretion in mice. Our results demonstrate opposing roles for SNAP23 in the secretion mechanisms of the endocrine and exocrine pancreas and reveal that the SNAP23-binding compound MF286 may be a promising drug for diabetes treatment. |
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| AbstractList | The membrane fusion of secretory granules with plasma membranes is crucial for the exocytosis of hormones and enzymes. Secretion disorders can cause various diseases such as diabetes or pancreatitis. Synaptosomal-associated protein 23 (SNAP23), a soluble N-ethyl-maleimide sensitive fusion protein attachment protein receptor (SNARE) molecule, is essential for secretory granule fusion in several cell lines. However, the in vivo functions of SNAP23 in endocrine and exocrine tissues remain unclear. In this study, we show opposing roles for SNAP23 in secretion in pancreatic exocrine and endocrine cells. The loss of SNAP23 in the exocrine and endocrine pancreas resulted in decreased and increased fusion of granules to the plasma membrane after stimulation, respectively. Furthermore, we identified a low molecular weight compound, MF286, that binds specifically to SNAP23 and promotes insulin secretion in mice. Our results demonstrate opposing roles for SNAP23 in the secretion mechanisms of the endocrine and exocrine pancreas and reveal that the SNAP23-binding compound MF286 may be a promising drug for diabetes treatment. Kunii et al. reveal that the SNARE protein SNAP23 plays distinct roles in the secretion of amylase in exocrine cells and of insulin in endocrine cells the pancreas and show that MF286, a novel inhibitor of SNAP23, may be a new drug candidate for diabetes. The membrane fusion of secretory granules with plasma membranes is crucial for the exocytosis of hormones and enzymes. Secretion disorders can cause various diseases such as diabetes or pancreatitis. Synaptosomal-associated protein 23 (SNAP23), a soluble N -ethyl-maleimide sensitive fusion protein attachment protein receptor (SNARE) molecule, is essential for secretory granule fusion in several cell lines. However, the in vivo functions of SNAP23 in endocrine and exocrine tissues remain unclear. In this study, we show opposing roles for SNAP23 in secretion in pancreatic exocrine and endocrine cells. The loss of SNAP23 in the exocrine and endocrine pancreas resulted in decreased and increased fusion of granules to the plasma membrane after stimulation, respectively. Furthermore, we identified a low molecular weight compound, MF286, that binds specifically to SNAP23 and promotes insulin secretion in mice. Our results demonstrate opposing roles for SNAP23 in the secretion mechanisms of the endocrine and exocrine pancreas and reveal that the SNAP23-binding compound MF286 may be a promising drug for diabetes treatment. |
| Author | Aoyagi, Kyota Ohmuraya, Masaki Kim, Yoon-Jeong Harada, Reiko Kobayashi, Masaki Ohara-Imaizumi, Mica Kawakami, Ryosuke Yoshimura, Shin-Ichiro Ohno, Mitsuyo Nemoto, Tomomi Shimizu, Takeshi Lin, Bangzhong Kitamura, Tadahiro Sato, Ken Kondoh, Yasumitsu Simizu, Siro Osada, Hiroyuki Nagamatsu, Shinya Kasai, Haruo Kunii, Masataka Nunomura, Kazuto Harada, Akihiro Sato, Takashi Takahashi, Noriko |
| AuthorAffiliation | 1 Laboratory of Molecular Traffic, Department of Molecular and Cellular Biology, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan 7 Chemical Biology Research Group, RIKEN Center for Sustainable Resource Science, Saitama 351-0198, Japan 4 Laboratory of Structural Physiology, Graduate School of Medicine, Center for Disease Biology and Integrative Medicine, The University of Tokyo, Tokyo 113-0033, Japan 8 Department of Applied Chemistry, Faculty of Science and Technology, Keio University, Kanagawa 223-8522, Japan 3 Department of Biochemistry, Kyorin University School of Medicine, Tokyo 181-8611, Japan 6 Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Hokkaido 001-0020, Japan 2 Department of Cell Biology, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan 11 Department of Judo Therapy, Takarazuka University of Medical and Health Care, Hyogo 666-0152, Japan 5 Metabolic Signal R |
| AuthorAffiliation_xml | – name: 2 Department of Cell Biology, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan – name: 6 Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Hokkaido 001-0020, Japan – name: 5 Metabolic Signal Research Center, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan – name: 7 Chemical Biology Research Group, RIKEN Center for Sustainable Resource Science, Saitama 351-0198, Japan – name: 10 Institute of Resource Development and Analysis, Kumamoto University, Kumamoto 860-0811, Japan – name: 11 Department of Judo Therapy, Takarazuka University of Medical and Health Care, Hyogo 666-0152, Japan – name: 9 Drug Discovery Team, Office for University-Industry Collaboration Planning and Promotion, Osaka University, Osaka 565-0871, Japan – name: 4 Laboratory of Structural Physiology, Graduate School of Medicine, Center for Disease Biology and Integrative Medicine, The University of Tokyo, Tokyo 113-0033, Japan – name: 1 Laboratory of Molecular Traffic, Department of Molecular and Cellular Biology, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan – name: 8 Department of Applied Chemistry, Faculty of Science and Technology, Keio University, Kanagawa 223-8522, Japan – name: 3 Department of Biochemistry, Kyorin University School of Medicine, Tokyo 181-8611, Japan |
| Author_xml | – sequence: 1 givenname: Masataka orcidid: 0000-0001-7222-7456 surname: Kunii fullname: Kunii, Masataka organization: Laboratory of Molecular Traffic, Department of Molecular and Cellular Biology, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan Department of Cell Biology, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan – sequence: 2 givenname: Mica surname: Ohara-Imaizumi fullname: Ohara-Imaizumi, Mica organization: Department of Biochemistry, Kyorin University School of Medicine, Tokyo 181-8611, Japan – sequence: 3 givenname: Noriko surname: Takahashi fullname: Takahashi, Noriko organization: Laboratory of Structural Physiology, Graduate School of Medicine, Center for Disease Biology and Integrative Medicine, The University of Tokyo, Tokyo 113-0033, Japan – sequence: 4 givenname: Masaki surname: Kobayashi fullname: Kobayashi, Masaki organization: Metabolic Signal Research Center, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan – sequence: 5 givenname: Ryosuke surname: Kawakami fullname: Kawakami, Ryosuke organization: Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Hokkaido 001-0020, Japan – sequence: 6 givenname: Yasumitsu surname: Kondoh fullname: Kondoh, Yasumitsu organization: Chemical Biology Research Group, RIKEN Center for Sustainable Resource Science, Saitama 351-0198, Japan – sequence: 7 givenname: Takeshi surname: Shimizu fullname: Shimizu, Takeshi organization: Chemical Biology Research Group, RIKEN Center for Sustainable Resource Science, Saitama 351-0198, Japan – sequence: 8 givenname: Siro surname: Simizu fullname: Simizu, Siro organization: Department of Applied Chemistry, Faculty of Science and Technology, Keio University, Kanagawa 223-8522, Japan – sequence: 9 givenname: Bangzhong surname: Lin fullname: Lin, Bangzhong organization: Drug Discovery Team, Office for University-Industry Collaboration Planning and Promotion, Osaka University, Osaka 565-0871, Japan – sequence: 10 givenname: Kazuto surname: Nunomura fullname: Nunomura, Kazuto organization: Drug Discovery Team, Office for University-Industry Collaboration Planning and Promotion, Osaka University, Osaka 565-0871, Japan – sequence: 11 givenname: Kyota surname: Aoyagi fullname: Aoyagi, Kyota organization: Department of Biochemistry, Kyorin University School of Medicine, Tokyo 181-8611, Japan – sequence: 12 givenname: Mitsuyo surname: Ohno fullname: Ohno, Mitsuyo organization: Laboratory of Structural Physiology, Graduate School of Medicine, Center for Disease Biology and Integrative Medicine, The University of Tokyo, Tokyo 113-0033, Japan – sequence: 13 givenname: Masaki surname: Ohmuraya fullname: Ohmuraya, Masaki organization: Institute of Resource Development and Analysis, Kumamoto University, Kumamoto 860-0811, Japan – sequence: 14 givenname: Takashi surname: Sato fullname: Sato, Takashi organization: Laboratory of Molecular Traffic, Department of Molecular and Cellular Biology, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan – sequence: 15 givenname: Shin-Ichiro orcidid: 0000-0003-3632-0674 surname: Yoshimura fullname: Yoshimura, Shin-Ichiro organization: Department of Cell Biology, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan – sequence: 16 givenname: Ken surname: Sato fullname: Sato, Ken organization: Laboratory of Molecular Traffic, Department of Molecular and Cellular Biology, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan – sequence: 17 givenname: Reiko surname: Harada fullname: Harada, Reiko organization: Department of Cell Biology, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan Department of Judo Therapy, Takarazuka University of Medical and Health Care, Hyogo 666-0152, Japan – sequence: 18 givenname: Yoon-Jeong surname: Kim fullname: Kim, Yoon-Jeong organization: Drug Discovery Team, Office for University-Industry Collaboration Planning and Promotion, Osaka University, Osaka 565-0871, Japan – sequence: 19 givenname: Hiroyuki surname: Osada fullname: Osada, Hiroyuki organization: Chemical Biology Research Group, RIKEN Center for Sustainable Resource Science, Saitama 351-0198, Japan – sequence: 20 givenname: Tomomi surname: Nemoto fullname: Nemoto, Tomomi organization: Laboratory of Molecular and Cellular Biophysics, Research Institute for Electronic Science, Hokkaido University, Hokkaido 001-0020, Japan – sequence: 21 givenname: Haruo orcidid: 0000-0003-2327-9027 surname: Kasai fullname: Kasai, Haruo organization: Laboratory of Structural Physiology, Graduate School of Medicine, Center for Disease Biology and Integrative Medicine, The University of Tokyo, Tokyo 113-0033, Japan – sequence: 22 givenname: Tadahiro surname: Kitamura fullname: Kitamura, Tadahiro organization: Metabolic Signal Research Center, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan – sequence: 23 givenname: Shinya surname: Nagamatsu fullname: Nagamatsu, Shinya organization: Department of Biochemistry, Kyorin University School of Medicine, Tokyo 181-8611, Japan – sequence: 24 givenname: Akihiro orcidid: 0000-0002-2484-9784 surname: Harada fullname: Harada, Akihiro email: aharada@acb.med.osaka-u.ac.jp organization: Laboratory of Molecular Traffic, Department of Molecular and Cellular Biology, Institute for Molecular and Cellular Regulation, Gunma University, Gunma 371-8512, Japan Department of Cell Biology, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan aharada@acb.med.osaka-u.ac.jp |
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| Snippet | The membrane fusion of secretory granules with plasma membranes is crucial for the exocytosis of hormones and enzymes. Secretion disorders can cause various... Kunii et al. reveal that the SNARE protein SNAP23 plays distinct roles in the secretion of amylase in exocrine cells and of insulin in endocrine cells the... |
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| SubjectTerms | Acinar Cells - metabolism Acinar Cells - ultrastructure Amylases - metabolism Animals Cell Fusion Cells Cellular biology Enzymes Exocytosis Glucose Transporter Type 4 - metabolism Insulin - metabolism Insulin Secretion Islets of Langerhans - cytology Membranes Mice, Knockout Microscopy, Fluorescence, Multiphoton Models, Biological Molecular weight Pancreas, Exocrine - cytology Parotid Gland - cytology Protein Transport Proteins Qb-SNARE Proteins - deficiency Qb-SNARE Proteins - metabolism Qc-SNARE Proteins - deficiency Qc-SNARE Proteins - metabolism Secretory Vesicles - metabolism SNARE Proteins - metabolism Synaptosomal-Associated Protein 25 - metabolism |
| Title | Opposing roles for SNAP23 in secretion in exocrine and endocrine pancreatic cells |
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