Regulation of mucosal immune system by polarized sorting in epithelial cells

• Project Area: Intracellular logistics: interdisciplinary approaches to pathophysiology of membrane traffic
• Project/Area Number: 20113003
• Research Category: Grant-in-Aid for Scientific Research on Innovative Areas (Research in a proposed research area)
• Allocation Type: Single-year Grants
• Review Section: Biological Sciences
• Research Institution: The Institute of Physical and Chemical Research
• Principal Investigator: OHNO Hiroshi 独立行政法人理化学研究所, 免疫系構築研究チーム, チームリーダー (50233226)
• Co-Investigator(Kenkyū-buntansha): KIMURA Shunsuke 北海道大学, 医学研究科, 助教 (40444525)
• Project Period (FY): 2008 – 2012
• Project Status: Completed (Fiscal Year 2012)
• Budget Amount: ¥173,550,000 (Direct Cost: ¥133,500,000、Indirect Cost: ¥40,050,000); Fiscal Year 2012: ¥31,980,000 (Direct Cost: ¥24,600,000、Indirect Cost: ¥7,380,000); Fiscal Year 2011: ¥31,980,000 (Direct Cost: ¥24,600,000、Indirect Cost: ¥7,380,000); Fiscal Year 2010: ¥31,980,000 (Direct Cost: ¥24,600,000、Indirect Cost: ¥7,380,000); Fiscal Year 2009: ¥31,980,000 (Direct Cost: ¥24,600,000、Indirect Cost: ¥7,380,000); Fiscal Year 2008: ¥45,630,000 (Direct Cost: ¥35,100,000、Indirect Cost: ¥10,530,000)
• Keywords: 細胞内ロジスティクス / 上皮細胞極性輸送 / AP-1B / GP2 / M-Sec / 粘膜免疫系 / 上皮細胞間Tリンパ球 / 経口ワクチン / M細胞 / トランスサイトーシス

Research Abstract

We have studied the regulation of mucosal immune system by polarized sorting in epithelial cells using AP-1B, M-cell-specific GP2 and M-Sec as molecular targets. AP-1B was revealed to connect cellular polarity and proliferation. We have also shown that AP-1B KO mice suffer from spontaneous colitis because of mis-sorting of cytokine receptors. GP2 has been shown to serve as a bacterial uptake receptor on M cells important for subsequent specific mucosal immune responses. We were also able to show that M-Sec is an important regulator for the formation of tunneling nanotubes connecting remote cells.

Research Products

• [Journal Article] AP-1B-mediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice. (2013)
  • Author(s): Hase, K., Nakatsu, F., Ohmae, M., Sugihara, K., Shioda, N., Takahashi, D., Obata, Y., Furusawa, Y., Fujimura, Y., Yamashita, T., Fukuda, S., Okamoto, H., Asano, M., Yonemura, S., Ohno, H.
  • Journal Title: Gastroenterol. Volume: (in press)
  • Peer Reviewed
• [Journal Article] Critical role of the IgM Fc receptor in IgM homeostasis, B-cell survival, and humoral immune responses. (2012)
  • Author(s): Ouchida, R., Mori, H., Hase, K., Takatsu, H., Kurosaki, T., Tokuhisa, T., Ohno, H., Wang, J. Y.
  • Journal Title: Proc Natl Acad Sci U S A. Volume: 109
  • Peer Reviewed
• [Journal Article] Altered Ig levels and antibody responses in mice deficient for the Fc receptor for IgM (Fc□R). (2012)
  • Author(s): Honjo, K., Kubagawa, Y., Jones, D. M., Dizon, B., Zhu, Z., Ohno, H., Izui, S., Kearney, J. F., Kubagawa, H.
  • Journal Title: Proc Natl Acad Sci U S A. Volume: 109 Pages: 15882-15887
  • Peer Reviewed
• [Journal Article] AP1B plays an important role in intestinal tumorigenesis with the truncating mutation of an APC gene. (2012)
  • Author(s): Mimura, M., Masuda, A., Nishiumi, S., Kawakami, K., Fujishima, Y., Yoshie, T., Mizuno, S., Miki, I., Ohno, H., Hase, K., Minamoto, T., Azuma, T., Yoshida, M.
  • Journal Title: Int. J. Cancer Volume: 130 Pages: 1011-1020
  • Peer Reviewed
• [Journal Article] Epithelial cell-intrinsic notch signaling plays an essential role in the maintenance of gut immune homeostasis (2012)
  • Author(s): Obata Y., et al
  • Journal Title: J.Immunol. Volume: 188 Issue: 5 Pages: 2427-2436
  • DOI: 10.4049/jimmunol.1101128
  • Peer Reviewed
• [Journal Article] The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells (2012)
  • Author(s): Kanaya, T., Hase, K., Takahashi, D., Fukuda, S., Hoshino, K., Sasaki, I., Hemmi, H., Knoop, K. A., Kumar, N., Sato, M., Katsuno, T., Yokosuka, O., Toyooka, K., Nakai, K., Sakamoto, A., Kitahara, Y., Jinnohara, T., McSorley, S. J., Kaisho, T., Williams, I. R., and Ohno, H.
  • Journal Title: Nat Immunol Volume: 13 Issue: 8 Pages: 729-736
  • DOI: 10.1038/ni.2352
  • Peer Reviewed
• [Journal Article] Critical role of the IgM Fc receptor in IgM homeostasis, B cell survival and humoral immune responses (2012)
  • Author(s): Ouchida, R., Mori, H., Hase, K., Takatsu, H., Kurosaki, T., Tokuhisa, T., Ohno, H., Wang. J. -Y.
  • Journal Title: Proc. Natl. Acad. Sci. USA Volume: 109 Issue: 40 Pages: 2699-2706
  • DOI: 10.1073/pnas.1210706109
  • Peer Reviewed
• [Journal Article] The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice. (2011)
  • Author(s): Takahashi, D., Hase, K., Kimura, S., Nakatsu, F., Ohmae, M., Mandai, Y., Sato, T., Date, Y., Ebisawa, M., Kato, T., Obata, Y., Fukuda, S., Kawamura, Y., Dohi, T., Katsuno, T., Tokosuka, O., Waguri, S., Ohno, H.
  • Journal Title: Gatroenterol. Volume: 141 Pages: 621-632
  • Peer Reviewed
• [Journal Article] The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice (2011)
  • Author(s): Takahashi, D., et al
  • Journal Title: Gastroenterology Volume: 14 Issue: 2 Pages: 621-632
  • DOI: 10.1053/j.gastro.2011.04.056
  • Peer Reviewed
• [Journal Article] AP1B plays an important role in intestinal tumorigenesis with the truncating mutation of an APC gene (2011)
  • Author(s): Mimura, M., et al
  • Journal Title: Int.J.Cancer Volume: 130 Issue: 5 Pages: 1011-1020
  • DOI: 10.1002/ijc.26131
  • Peer Reviewed
• [Journal Article] Bifidobacteria can protect from enteropathogenic infection through production of acetate. (2011)
  • Author(s): Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., Tobe, T., Clarke, J. M., Topping, D. L., Suzuki, T., Taylor, T. D., Itoh, K., Kikuchi, J., Morita, H., Hattori, M., Ohno, H.
  • Journal Title: Nature 469 Pages: 543-547
  • Peer Reviewed
• [Journal Article] Dynamic Omics Approach Identifies Nutrition-Mediated Microbial Interactions (2011)
  • Author(s): Nakanishi, Y., et al.
  • Journal Title: J.Proteome Res. Volume: 10 Pages: 824-836
  • Peer Reviewed
• [Journal Article] Bifidobacteria can protect from enteropathogenic infection through production of acetate (2011)
  • Author(s): Fukuda, S., et al.
  • Journal Title: Nature Volume: 4692 Pages: 543-547
  • Peer Reviewed
• [Journal Article] Identification of TOSO/FAIM3 as an Fc receptor for IgM (2011)
  • Author(s): Shima H., et al.
  • Journal Title: Int.Immunol. Volume: 22 Pages: 149-156
  • Peer Reviewed
• [Journal Article] Identification of TOSO/FAIM3 as an Fc receptor for IgM. (2010)
  • Author(s): Shima, H., Takatsu, H., Fukuda, S., Ohmae, M., Hase, K., Kubagawa, H., Wang, J.-Y., Ohno, H.
  • Journal Title: Int. Immunol. Volume: 22 Pages: 149-156
  • NAID: 10027391592
  • Peer Reviewed
• [Journal Article] M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. (2009)
  • Author(s): Hase, K., Kimura, S., Takatsu, H., Ohmae, M., Kawano, S., Kitamura, H., Ito, M., Watarai, H., Hazelet, C. C., Yeaman, C., Ohno, H.
  • Journal Title: Nature Cell Biol. Volume: 11 Pages: 1427-1432
  • Peer Reviewed
• [Journal Article] Uptake through Glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response. (2009)
  • Author(s): Hase, K., Kawano, K., Nochi, T., Pontes, G. S., Fukuda, S., Ebisawa, M., Kadokura, K., Tobe, T., Fujimura, Y., Kawano, S., Nakato, G., Kimura, S., Murakami, T., Iimura, M., Hamura, K., Fukuoka, S. I., Lowe, A. W., Waguri, S., Itoh, K, Kiyono, H., Ohno, H.
  • Journal Title: Nature Volume: 462 Pages: 226-230
  • Peer Reviewed
• [Journal Article] Uptake through Glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response (2009)
  • Author(s): Hase, K., Kawano, K., Nochi, T., Pontes, G. S., Fukuda, S., Ebisawa, M., Kadokura, K., Tobe, T., Fujimura, Y., Kawano, S., Nakato, G., Kimura, S., Murakami, T., Iimura, M., Hamura, K., Fukuoka, S. I., Lowe, A. W., Waguri, S., Itoh, K, Kiyono, H., Ohno, H.
  • Journal Title: Nature 462 Pages: 226-230
  • Peer Reviewed
• [Journal Article] M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex (2009)
  • Author(s): Hase, K., Kimura, S., Takatsu, H., Ohmae, M., Kawano, S., Kitamura, H., Ito, M., Watarai, H., Hazelet, C. C., Yeaman, C., Ohno, H.
  • Journal Title: Nature Cell Biol 11 Pages: 1427-1432
  • Peer Reviewed
• [Journal Article] Uptake via Glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response (2009)
  • Author(s): Hase, K.et al.
  • Journal Title: Nature 462 Pages: 226-230
  • Peer Reviewed
• [Journal Article] M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex (2009)
  • Author(s): Hase, K.et al.
  • Journal Title: Nat.Cell Biol. 11 Pages: 1427-1432
  • Peer Reviewed
• [Journal Article] New approach for M-cell-specific molecules screening by comprehensive transcriptome analysis (2009)
  • Author(s): Nakato, G.et al.
  • Journal Title: DNA Res. 16 Pages: 227-235
  • Peer Reviewed
• [Journal Article] Rats harboring S284L Chrna4 mutation show attenuation of synaptic and extrasynaptic GABAergic transmission and exhibit the nocturnal frontal lobe epilepsy phenotype. (2008)
  • Author(s): Zhu, G., Okada, M., Yoshida, S., Ieno, S., Mori, F., Takahara, T., Saito, RR., Miura, Y., Kishi, A., Tomiyama, M., Sato, A., Kojima, T., Fukuma, G., Wakabayashi, K., Hase, K., Ohno, H., Kijima, H., Takano, Y., Mitsudome, A., Kaneko, S., Hirose, S
  • Journal Title: J.Neurosci. 28 Pages: 12465-12476
  • Peer Reviewed
• [Journal Article] Aberrant trafficking of the high-affinity choline transporter in AP-3-deficient mice. (2008)
  • Author(s): Misawa, H., Fujigaya, H., Nishimura, T., Moriwaki, Y., Okuda, T., Kawashima, K., Nakata, K., Ruggiero, A. M., Blakely, R. D., Nakatsu, F., Ohno, H.
  • Journal Title: Eur.J.Neurosci. 27 Pages: 3109-3117
  • Peer Reviewed
• [Journal Article] AP1B plays an important role in intestinal tumorigenesis with the truncating mutation of an APC gene.
  • Author(s): Mimura, M., Masuda, A., Nishiumi, S., Kawakami, K., Fujishima, Y., Yoshie, T., Mizuno, S., Miki, I., Ohno, H., Hase, K., Minamoto, T., Azuma, T., Yoshida, M.
  • Journal Title: Int. J. Cancer in press
  • Peer Reviewed
• [Presentation] Understanding the host-gut microbiota interaction with multi-omics approach (2012)
  • Author(s): Ohno,H
  • Organizer: 第85回日本生化学会大会
  • Place of Presentation: Fukuoka, Japan
  • Year and Date: 2012-12-14
  • Invited
• [Presentation] The role of M cells in intestinal immunity. (2012)
  • Author(s): Ohno, H.
  • Organizer: International Endotoxin & Innate Immunity Society Meeting 2012, Homeostatic Inflammation Symposium, Japan Endotoxin and Innate Immunity Society 2012.
  • Place of Presentation: Tokyo, Japan
  • Year and Date: 2012-10-26
• [Presentation] The role of M cells in intestinal immunity (2012)
  • Author(s): Ohno, H
  • Organizer: International Endotoxin ＆ Innate Immunity Society Meeting 2012, Homeostatic Inflammation Symposium, Japan Endotoxin and Innate Immunity Society 2012
  • Place of Presentation: Tokyo, Japan
  • Year and Date: 2012-10-23
  • Invited
• [Presentation] Function and differentiation of M cells, a unique subset of intestinal epithelial cells specialized for mucosal antigen-uptake. (2012)
  • Author(s): Ohno, H.
  • Organizer: The 12th International Symposium on Dendritic Cells.
  • Place of Presentation: Daegu, Korea
  • Year and Date: 2012-10-11
• [Presentation] Function and differentiation of M cells, a unique subset of intestinal epithelial cells specialized for mucosal antigen-uptake (2012)
  • Author(s): Ohno, H
  • Organizer: The 12th International Symposium on Dendritic Cells
  • Place of Presentation: Daegu, Korea
  • Year and Date: 2012-10-07
  • Invited
• [Presentation] Antigen delivery to the gut immune system through epithelium: M cells vs FAE? (2012)
  • Author(s): Ohno, H.
  • Organizer: Gordon Research Conference, Lysosomes & Endocytosis Andover
  • Place of Presentation: NH, USA
  • Year and Date: 2012-06-21
• [Presentation] Antigen delivery to the gut immune system through epithelium: M cells vs FAE? (2012)
  • Author(s): Ohno, H
  • Organizer: Gordon Research Conference, Lysosomes & Endocytosis
  • Place of Presentation: Andoverm NH, USA
  • Year and Date: 2012-06-17
  • Invited
• [Presentation] M cells, a unique subset of intestinal epithelial cells specialized for mucosal antigen-uptake. (2012)
  • Author(s): Ohno, H.
  • Organizer: The 2012 Spring Conference of the Korean Association of Immunologists.
  • Place of Presentation: Seoul, Korea
  • Year and Date: 2012-04-13
• [Presentation] M cells, a unique subset of intestinal epithelial cells specialized for mucosal antigen-uptake (2012)
  • Author(s): Ohno, H
  • Organizer: The 2012 Spring Conference of the Korean Association of Immunologists
  • Place of Presentation: Seoul, Korea
  • Year and Date: 2012-04-12
  • Invited
• [Presentation] Function and differentiation of M cells, a unique subset of intestinal epithelial cells important for mucosal immunity. (2011)
  • Author(s): Ohno, H.
  • Organizer: ComBio2011, Plenary Lecture,
  • Place of Presentation: Cairns, Australia
  • Year and Date: 2011-09-28
• [Presentation] Function and differentiation of M cells, a unique subset of intestinal epithelial cells important for mucosal immunity (2011)
  • Author(s): Ohno, H.
  • Organizer: ComBio2011
  • Place of Presentation: Cains, australia(招待講演)
  • Year and Date: 2011-09-28
• [Presentation] The role of M-Sec in tunneling nanotube formation (2011)
  • Author(s): Ohno, H.
  • Organizer: EMBO Meeting 2011
  • Place of Presentation: Vienna, Austria(招待講演)
  • Year and Date: 2011-09-11
• [Presentation] The role of M-Sec in tunneling nanotube formation. (2011)
  • Author(s): Ohno, H., Hase, K., Kimura, S., Fukai, S.
  • Organizer: EMBO Meeting 2011 Workshop 'Role of nanotubes in intercellular signaling'
  • Place of Presentation: Vienna, Austria
  • Year and Date: 2011-09-10
• [Presentation] M Cells and Antigen Delivery to DCs in the Gut. (2011)
  • Author(s): Hase, K., Kawano, K., Ebisawa, M., Ohno, H.
  • Organizer: Keystone Symposia 'Dendritic Cells and the Initiation of Adaptive Immunity (J7)'
  • Place of Presentation: Santa Fe, NM, USA
  • Year and Date: 2011-02-16
• [Presentation] M cells and Antigen Delivery to DCs in the Gut (2011)
  • Author(s): Ohno H.
  • Organizer: Keystone Syposia
  • Place of Presentation: Santa Fe, NM, USA
  • Year and Date: 2011-02-16
• [Presentation] M-Sec : a promoter of tunneling nanotube formation (2010)
  • Author(s): Ohno, H.
  • Organizer: Biochemistry and Molecular Biology 2010
  • Place of Presentation: Kobe, Japan
  • Year and Date: 2010-12-09
• [Presentation] 食物アレルギーと腸管免疫・経口免疫寛容 (2010)
  • Author(s): 大野博司
  • Organizer: 第60回日本アレルギー学会秋季学術大会
  • Place of Presentation: 東京
  • Year and Date: 2010-11-27
• [Presentation] GP2-dependent antigen transcytosis by M cells intiates antigen-specific mucosal immune response. (2010)
  • Author(s): Hase, K., Nochi, T., Pontes, G. S., Fukuda, S., Ebisawa, M., Kadokura, K., Kiyono, H., Ohno, H.
  • Organizer: 14th International Congress of Immunology (ICI 2010)
  • Place of Presentation: 神戸
  • Year and Date: 2010-08-26
• [Presentation] Identification of TOSO/FAIM3 as an Fc receptor for IgM. (2010)
  • Author(s): Shima, H., Takatsu, H., Fukuda, S., Ohmae, M., Hase, K., Kubagawa, H., Wang, J.-Y., Ohno, H.
  • Organizer: 14th International Congress of Immunology (ICI 2010)
  • Place of Presentation: 神戸
  • Year and Date: 2010-08-25
• [Presentation] Glycoprotein 2 : An Antigen-Uptake Receptor on Intestinal Epithelial M Cells for Mucosal Immunity (2010)
  • Author(s): Ohno, H.
  • Organizer: Traffc Symposium
  • Place of Presentation: Kyoto, Japan
  • Year and Date: 2010-06-04
• [Presentation] Bacterial recognition and uptake by M cells (2010)
  • Author(s): Ohno, H.
  • Organizer: The 63rd Annual Meeting of the Japan Society for Cell Biology
  • Place of Presentation: Osaka, Japan
  • Year and Date: 2010-05-21
• [Presentation] Identification of RNA aptamers targeting mouse GP2 proteins by SELEX (2009)
  • Author(s): Hanazawa, M.
  • Organizer: 第32回日本分子生物学会年会
  • Place of Presentation: 横浜
  • Year and Date: 2009-12-11
• [Presentation] CCR6^<hi> CD11c^+ B cells promote M-cell differentiation in Peyer's patch. (2009)
  • Author(s): Ebisawa, M., Hase, K., Takahashi, D., Kitamura, H., Williams, I. R., Ohno, H.
  • Organizer: 第32回日本分子生物学会年会ワークショップ
  • Place of Presentation: 横浜
  • Year and Date: 2009-12-09
• [Presentation] Multiple Omics Identified Microbial Metabolites to Protect Host from Enterohemorrhagi Escherichia coli O157:H7 Lethal Infection (2009)
  • Author(s): Fukuda, S.
  • Organizer: 第32回日本分子生物学会年会
  • Place of Presentation: 横浜
  • Year and Date: 2009-12-09
• [Presentation] CCR6^<hi> CD11c^+ B cells promote M-cell differentiation in Peyer's patch (2009)
  • Author(s): Ebisawa, M.
  • Organizer: 第32回日本分子生物学会年会
  • Place of Presentation: 横浜
  • Year and Date: 2009-12-09
• [Presentation] Identification of microRNAs in LPS-stimulated macrophage-like cells (2009)
  • Author(s): Shimura, N.
  • Organizer: 第32回日本分子生物学会年会
  • Place of Presentation: 横浜
  • Year and Date: 2009-12-09
• [Presentation] GP2-dependent antigen transcytosis by M cells initiates antigen-specific mucosal immune response (2009)
  • Author(s): 長谷耕二
  • Organizer: 第39回日本免疫学会総会学術集会
  • Place of Presentation: 大阪
  • Year and Date: 2009-12-04
• [Presentation] GP2-dependent antigen transcytosis by M cells initiates antigen-specific mucosal immune response. (2009)
  • Author(s): Hase, K., Nochi, T., Pontes, G. S., Fukuda, S., Ebisawa, M., Kadokura, K., Kiyono, H., Ohno, H.
  • Organizer: 第39回日本免疫学会総会学術集会シンポジウム
  • Place of Presentation: 大阪
  • Year and Date: 2009-12-02
• [Presentation] Functional analysis of CCL9 in the intestinal immune system (2009)
  • Author(s): Yamazaki, R.
  • Organizer: 第39回日本免疫学会総会学術集会
  • Place of Presentation: 大阪
  • Year and Date: 2009-12-02
• [Presentation] Spatial and temporal specific expression patterns of RANK and RANKL in developing peripheral lymphoid organs (2009)
  • Author(s): Sugiyama, M.
  • Organizer: 第39回日本免疫学会総会学術集会
  • Place of Presentation: 大阪
  • Year and Date: 2009-12-02
• [Presentation] M-Sec による細胞間ナノチューブ形成促進の分子機構 (2009)
  • Author(s): 長谷耕二、高津宏之、木村俊介、大野博司
  • Organizer: 第61回日本細胞生物学会大会ワークショップ
  • Place of Presentation: 名古屋
  • Year and Date: 2009-06-03
• [Presentation] M-Secによる細胞間ナノチューブ形成促進の分子機構 (2009)
  • Author(s): 長谷耕二
  • Organizer: 第61回日本細胞生物学会大会
  • Place of Presentation: 名古屋
  • Year and Date: 2009-06-03
• [Presentation] Functional analysis of CCL9 in the intestinal immune system (2009)
  • Author(s): Yamazaki, R.
  • Organizer: 第61回日本細胞生物学会大会
  • Place of Presentation: 名古屋
  • Year and Date: 2009-06-02
• [Presentation] Study on the process of antigen transcytosis by M cells (2009)
  • Author(s): Kimura, S
  • Organizer: 第61回日本細胞生物学会大会
  • Place of Presentation: 名古屋
  • Year and Date: 2009-06-02
• [Presentation] Cell polarity regulates proliferation of intestinal epithelial cells. (2008)
  • Author(s): Hase, K., Nakatsu, F., Ohno, H.
  • Organizer: 第31回日本分子生物学会年会・第81回日本生化学会大会合同大会
  • Place of Presentation: 神戸
  • Year and Date: 2008-12-11
• [Book] 臨床粘膜免疫学 (2010)
  • Author(s): 大野博司
  • Publisher: シナジー
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