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Enhancement of sensitivity to anti-cancer immunity in NRF2-addiected cancers

Research Project

Project/Area Number 16K15228
Research Category

Grant-in-Aid for Challenging Exploratory Research

Allocation TypeMulti-year Fund
Research Field Pathological medical chemistry
Research InstitutionTohoku University

Principal Investigator

Motohashi Hozumi  東北大学, 加齢医学研究所, 教授 (00282351)

Project Period (FY) 2016-04-01 – 2017-03-31
Project Status Completed (Fiscal Year 2016)
Budget Amount *help
¥3,640,000 (Direct Cost: ¥2,800,000、Indirect Cost: ¥840,000)
Fiscal Year 2016: ¥3,640,000 (Direct Cost: ¥2,800,000、Indirect Cost: ¥840,000)
Keywords転写因子 / がん / がん遺伝子 / 酸化ストレス応答 / KEAP1 / NRF2 / がん細胞 / がん微小環境 / 乳がん / ストレス
Outline of Final Research Achievements

NRF2 is a master transcriptional activator playing a critical role in the defense mechanism against oxidative insults. NRF2 activates genes encoding cytoprotective enzymes and antioxidant proteins in response to electrophiles and reactive oxygen species (ROS), conferring resistance against xenobiotic and oxidative stress. While NRF2 activation is beneficial to our health, NRF2 is responsible for the malignant progression of various human cancers. To develop a new anti-cancer therapy for NRF2-addicted malignant cancers, we examined molecular mechanisms how NRF2 activation influences on the cancer evasion from the anti-cancer immunity. We found that NRF2 in cancer cells reduces expression of MHC class I and other genes involved in the antigen presentation, suggesting that NRF2 promotes the cancer evasion from the anti-cancer immunity.

Report

(2 results)
  • 2016 Annual Research Report   Final Research Report ( PDF )
  • Research Products

    (48 results)

All 2017 2016

All Journal Article (11 results) (of which Int'l Joint Research: 4 results,  Peer Reviewed: 11 results,  Open Access: 9 results,  Acknowledgement Compliant: 3 results) Presentation (37 results) (of which Int'l Joint Research: 9 results,  Invited: 17 results)

  • [Journal Article] Glucocorticoid receptor signaling represses the antioxidant response by inhibiting histone acetylation mediated by the transcriptional activatpr NRF22017

    • Author(s)
      Alam MM, Okazaki K, Nguyen LTT, Ota N, Kitamura H, Murakami S, Shima H, Igarashi K, Sekine H, Motohashi H
    • Journal Title

      J Biol Chem

      Volume: 印刷中 Issue: 18 Pages: 7519-7530

    • DOI

      10.1074/jbc.m116.773960

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Nrf2 suppresses macrophage inflammatory response by blocking proinflammatory cytokine transcription.2016

    • Author(s)
      Kobayashi EH, Suzuki T, Funayama R, Nagashima T, Hayashi M, Sekine H, Tanaka N, Moriguchi T, Motohashi H, Nakayama K, Yamamoto M.
    • Journal Title

      Nat Commun

      Volume: 7 Issue: 1 Pages: 11624-11624

    • DOI

      10.1038/ncomms11624

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research / Acknowledgement Compliant
  • [Journal Article] p62/Sqstm1 promotes malignancy of HCV-positive hepatocellular carcinoma through Nrf2-dependent metabolic reprogramming2016

    • Author(s)
      Saito T, Ichimura Y, Taguchi K, Suzuki T, Mizushima T, Takagi K, Hirose Y, Nagahashi M, Iso T, Fukutomi T, Ohishi M, Endo K, Uemura T, Nishito Y, Okuda S, Obata M, Kouno T, Imamura R, Tada Y, Obata R, Yasuda D, Takahashi K, Fujimura T, Pi J, Lee MS, Ueno T, Ohe T, Mashino T, Wakai T, Kojima H, Okabe T, Nagano T et al.
    • Journal Title

      Nature Commun

      Volume: 7 Issue: 1 Pages: 12030-12030

    • DOI

      10.1038/ncomms12030

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] CD271 regulates the proliferation and motility of hypopharyngeal cancer cells2016

    • Author(s)
      Mochizuki M, Tamai K, Imai T, Sugawara S, Ogama N, Nakamura M, Matsuura K, Yamaguchi K, Satoh K, Sato I, Motohashi H, Sugamura K, Tanaka N
    • Journal Title

      Sci Rep

      Volume: 6 Issue: 1 Pages: 30707-30707

    • DOI

      10.1038/srep30707

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] The structural origin of metabolic quantitative diversity2016

    • Author(s)
      Koshiba S, Motoike I, Kojima K, Hasegawa T, Shirota M, Saito T, Saigusa D, Danjoh I, Katsuoka F, Ogishima S, ... Yamamoto M.
    • Journal Title

      Sci Rep

      Volume: 6 Issue: 1 Pages: 31463-31463

    • DOI

      10.1038/srep31463

    • URL

      https://pure.teikyo.jp/en/publications/f23f66dd-859e-4088-8e53-de40d99cc561

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Establishment of protocols for global metabolomics by LC-MS for biomarker discovery2016

    • Author(s)
      Saigusa D, Okamura Y, Motoike IN, Katoh Y, Kurosawa Y, Saijyo R, Koshiba S, Yasuda J, Motohashi H, Sugawara J, Tanabe O, Kinoshita K, Yamamoto M
    • Journal Title

      PLoS One

      Volume: 11 Issue: 8 Pages: e0160555-e0160555

    • DOI

      10.1371/journal.pone.0160555

    • URL

      https://pure.teikyo.jp/en/publications/789e31b9-dbb0-4124-986b-c259a28c9328

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] Protein polysulfidation-dependent persulfide dioxygenase activity of ethylmalonic encephalopathy protein 12016

    • Author(s)
      Jung M, Kasamatsu S, Matsunaga T, Akashi S, Ono K, Nishimura A, Morita M, Abdul Hamid H, Fujii S, Kitamura H, Sawa T, Ida T, Motohashi H, Akaike T.
    • Journal Title

      Biochem Biophys Res Commun

      Volume: 480 Issue: 2 Pages: 180-186

    • DOI

      10.1016/j.bbrc.2016.10.022

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research / Acknowledgement Compliant
  • [Journal Article] Redox signaling regulated by electrophiles and reactive sulfur species2016

    • Author(s)
      Nishida M, Kumagai Y, Ihara H, Fujii S, Motohashi H, Akaike T.
    • Journal Title

      Journal of Clinical Biochemistry and Nutrition

      Volume: 58 Issue: 2 Pages: 91-98

    • DOI

      10.3164/jcbn.15-111

    • NAID

      130005132519

    • ISSN
      0912-0009, 1880-5086
    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access / Acknowledgement Compliant
  • [Journal Article] Redox signaling regulated by an electrophilic cyclic nucleotide and reactive cysteine persulfides2016

    • Author(s)
      Fujii S, Sawa T, Nishida M, Ihara H, Ida T, Motohashi H, Akaike T.
    • Journal Title

      Arch Biochem Biophys.

      Volume: 595 Pages: 140-146

    • DOI

      10.1016/j.abb.2015.11.008

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed / Open Access
  • [Journal Article] 酸化ストレス応答転写因子NRF2の転写制御機構2016

    • Author(s)
      関根弘樹、本橋ほづみ
    • Journal Title

      実験医学

      Volume: 34 Pages: 2517-2524

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed
  • [Journal Article] Recent advances in elucidating KEAP1-NRF2 functions in hematopoietic/immune cells and leukemic cells2016

    • Author(s)
      Murakami S, Motohashi H
    • Journal Title

      Rinsho Ketsueki

      Volume: 57 Pages: 1860-1868

    • NAID

      130005420735

    • Related Report
      2016 Annual Research Report
    • Peer Reviewed
  • [Presentation] 8-ニトロcGMPとタンパク質poly-S-グアニル化による親電子シグナルの可逆制御2017

    • Author(s)
      赤司壮一郎、笠松真吾、ジョン ミンギョン、松永哲郎、井田智章、藤井重元、澤 智裕、熊谷嘉人、本橋ほづみ、赤池孝章
    • Organizer
      第90回日本細菌学会総会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2017-03-19
    • Related Report
      2016 Annual Research Report
  • [Presentation] アルコールデヒドロゲナーゼ5タンパク質ポリスフリド化の酵素活性制御機能2017

    • Author(s)
      Chazia Glulamo Abdula、笠松真吾、西村明、Md. Morshedul Alam、井田智章、松永哲郎、藤井重元、居原 秀、本橋ほづみ、赤池孝章
    • Organizer
      第90回日本細菌学会総会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2017-03-19
    • Related Report
      2016 Annual Research Report
  • [Presentation] 細菌のイオウ呼吸はすべての生物種に保存されている:哺乳類における新しいエネルギー代謝経路・イオウ呼吸の発見2017

    • Author(s)
      赤池孝章、井田智章、松永哲郎、守田匡伸、笠松真吾、西村 明、藤井重元、居原 秀、ジョン ミンギョン、 赤司壮一郎、澤 智裕、本橋ほづみ
    • Organizer
      第90回日本細菌学会総会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2017-03-19
    • Related Report
      2016 Annual Research Report
  • [Presentation] 有機水銀定量曝露による細胞内システインパースルフィドの分解消耗と親電子シグナルの破綻2017

    • Author(s)
      井田智章、笠松真吾、居原秀、ヒシャム アブドル ハミル、チャジア グラモ アブドドゥラ、津々木博康、澤智裕、熊谷嘉人、本橋ほづみ、西田基宏、赤池孝章
    • Organizer
      第16回分子予防環境医学研究会
    • Place of Presentation
      熊本市国際交流会館(熊本)
    • Year and Date
      2017-02-03
    • Related Report
      2016 Annual Research Report
  • [Presentation] KEAP1-NRF2 system in stress responss and cancer malignancy2017

    • Author(s)
      本橋ほづみ
    • Organizer
      Kumamoto University Advence Research Project A & Program for Advancing Strategic International Networks to Accelerate the Circulation of Talented Researchers, International Symposium
    • Place of Presentation
      Kumamoto University, Kumamoto
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] KEAP1-NRF2 system in anti-oxidant response and regulation of cell proliferation and senescence2017

    • Author(s)
      本橋ほづみ
    • Organizer
      International Symposium “Redox Signaling in host defense and oxidative stress” 第90回日本細菌学会総会
    • Place of Presentation
      仙台国際センター(仙台)
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] Systemic activation of NRF2 alleviates chronic inflammation in a mouse model of lethal autoimmune diseases2016

    • Author(s)
      鈴木琢磨、村上昌平、張替秀郎、本橋ほづみ
    • Organizer
      第45回日本免疫学会学術集会
    • Place of Presentation
      沖縄コンベンションセンター(沖縄)
    • Year and Date
      2016-12-05
    • Related Report
      2016 Annual Research Report
  • [Presentation] KEAP1-NRF2 system as a cysteine-based redox sensor-effector for our defense mechanism2016

    • Author(s)
      本橋ほづみ
    • Organizer
      Lecture series
    • Place of Presentation
      The Jagiellonian University, Krakow, Polamd
    • Year and Date
      2016-11-21
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] NRF2の活性化がもたらす自己免疫疾患の慢性炎症改善作用2016

    • Author(s)
      鈴木琢磨、村上昌平、山本雅之、張替秀郎、本橋ほづみ
    • Organizer
      第89回日本生化学会大会合同大会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2016-09-25
    • Related Report
      2016 Annual Research Report
  • [Presentation] がん細胞におけるNRF2依存性転写活性化機構のゲノムワイドな解析2016

    • Author(s)
      岡崎慶斗、関根弘樹、勝岡史城、植野和子、長﨑正朗、山本雅之、本橋ほづみ
    • Organizer
      第89回日本生化学会大会合同大会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2016-09-25
    • Related Report
      2016 Annual Research Report
  • [Presentation] 転写因子NRF1のOGT-HCF-1複合体を介した分解制御機構2016

    • Author(s)
      関根弘樹、加藤幸一郎、福田愛菜、鈴木教郎、辻田忠志、岡崎慶斗、Md. Morshedul Alam、小林聡、山本雅之、本橋ほづみ
    • Organizer
      第89回日本生化学会大会合同大会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2016-09-25
    • Related Report
      2016 Annual Research Report
  • [Presentation] 2-ヒドロキシグルタル酸の精子形成・胎児発生における生理的役割の検討2016

    • Author(s)
      百々美奈、北村大志、太田奈緒、三枝大輔、勝岡史城、千葉初音、岡江寛明、有馬隆博、小関健由、本橋ほづみ
    • Organizer
      第89回日本生化学会大会合同大会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2016-09-25
    • Related Report
      2016 Annual Research Report
  • [Presentation] KEAP1の体細胞変異がもたらす腫瘍形成能促進機構の解明2016

    • Author(s)
      北村大志、小野寺好明、鈴木貴、本橋ほづみ
    • Organizer
      第89回日本生化学会大会合同大会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2016-09-25
    • Related Report
      2016 Annual Research Report
  • [Presentation] 造血幹細胞におけるKEAP1-NRF2制御系の機能解析2016

    • Author(s)
      村上昌平、山本雅之、本橋ほづみ
    • Organizer
      第89回日本生化学会大会合同大会
    • Place of Presentation
      仙台国際センター(仙台)
    • Year and Date
      2016-09-25
    • Related Report
      2016 Annual Research Report
  • [Presentation] 精巣における2-ヒドロキシグルタル酸の産生機構と生理的作用の検討2016

    • Author(s)
      百々美奈、北村大志、太田奈緒、三枝大輔、小関健由、本橋ほづみ
    • Organizer
      日本生化学会東北支部会 第82会例会
    • Place of Presentation
      弘前大学医学部 基礎大講堂(弘前)
    • Year and Date
      2016-05-21
    • Related Report
      2016 Annual Research Report
  • [Presentation] KEAP1の体細胞変異はRASシグナルと協調して腫瘍形成能を促進させる2016

    • Author(s)
      北村大志、本橋ほづみ
    • Organizer
      日本生化学会東北支部会 第82会例会
    • Place of Presentation
      弘前大学医学部 基礎大講堂(弘前)
    • Year and Date
      2016-05-21
    • Related Report
      2016 Annual Research Report
  • [Presentation] 致死的自己免疫疾患に対してNRF2の恒常的活性化がもたらす抗炎症作用の解析2016

    • Author(s)
      鈴木琢磨、村上昌平、山本雅之、張替秀郎、本橋ほづみ
    • Organizer
      日本生化学会東北支部会 第82会例会
    • Place of Presentation
      弘前大学医学部 基礎大講堂(弘前)
    • Year and Date
      2016-05-21
    • Related Report
      2016 Annual Research Report
  • [Presentation] Translation-coupled protein polysulfation, a unique biosynthesis pathway of cysteine persulfide2016

    • Author(s)
      Ida T, Ihara H, Wei F, Tomizawa K, Kasamatsu S, Matsunaga T, Kumagai Y, Sawa T, Motohashi H, Akaike T
    • Organizer
      The 9th International Conference of the Biology, Chemistry and Theapeutic applications of nitric oxide
    • Place of Presentation
      Sendai International Center (Sendai)
    • Year and Date
      2016-05-20
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Regulatory mechanisms of alcohol dehydrogenase 5 activity via protein polysulfuration2016

    • Author(s)
      Kasamatsu S, Md. Morshedul Alam, Ida T, Matsunaga T, Fujii S, Ihara H, Motohashi H, Akaike T
    • Organizer
      The 9th International Conference of the Biology, Chemistry and Theapeutic applications of nitric oxide
    • Place of Presentation
      Sendai International Center (Sendai)
    • Year and Date
      2016-05-20
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Regulation of reactive sulfuer species by ethylmalonic encephalopathy protein 1, persulfide dioxygenase2016

    • Author(s)
      Jung S, Matsuaga T, Kitamura H, Ono K, Ida T, Fujii S, Sawa T, Motohashi H, Akaike T
    • Organizer
      The 9th International Conference of the Biology, Chemistry and Theapeutic applications of nitric oxide
    • Place of Presentation
      Sendai International Center (Sendai)
    • Year and Date
      2016-05-20
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Regulation of mitochondrial energy metabolism by cysteine persulfide produced by mitochondrial cysteinyl-tRNA synthass2016

    • Author(s)
      Sato F, Okutomi M Matsunaga T, Kasamatsu S, Kaneki M, Ida T, Morita M, Tomizawa K, Fujii S, Motohashi H, Akaiake T
    • Organizer
      The 9th International Conference of the Biology, Chemistry and Theapeutic applications of nitric oxide
    • Place of Presentation
      Sendai International Center (Sendai)
    • Year and Date
      2016-05-20
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research
  • [Presentation] Regulation of mitochondria biogenesis by cysteine persulfide produced by cysteinyl-tRNA synthetase2016

    • Author(s)
      Nishimura A, Matsunaga T, Ida T, Kasamatsu S, Morita M, Fanyan W, Tomizawa K, Fujii S, Motohashi H, Akaike T
    • Organizer
      The 9th International Conference of the Biology, Chemistry and Theapeutic applications of nitric oxide
    • Place of Presentation
      Sendai International Center (Sendai)
    • Year and Date
      2016-05-20
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research
  • [Presentation] NRF2活性化による強大音曝露に伴う酸化ストレスからの内耳保護効果(1) -Nrf2-/-マウス解析-2016

    • Author(s)
      本蔵陽平、水足邦雄、塩谷彰浩、川瀬哲明、香取幸夫、本橋ほづみ
    • Organizer
      第117回日本耳鼻咽喉科学会通常総会・学術講演会
    • Place of Presentation
      名古屋国際会議場(名古屋)
    • Year and Date
      2016-05-18
    • Related Report
      2016 Annual Research Report
  • [Presentation] NRF2依存性環境ストレス応答:内耳酸化ストレス障害の軽減に対するNRF2の貢献2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第49回日本毒性学会学術年会 シンポジウム
    • Place of Presentation
      ウインクあいち(愛知県産業労働センター)(名古屋)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] がんの悪性化と酸化ストレス応答機構2016

    • Author(s)
      本橋ほづみ
    • Organizer
      安田女子大学・薬学部・薬学科 10周年記念学術講演会
    • Place of Presentation
      安田女子大学(広島)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] KEAP1-NRF2制御系による酸化ストレス応答と細胞老化制御2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第69回日本酸化ストレス学会学術集会 教育講演
    • Place of Presentation
      仙台国際センター(仙台)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] Purification and analysis of endogenous NRF2 complex in the presence and absence of active PI3K-AKT signaling2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第89回日本生化学会大会 シンポジウム「細胞のロバストネスを規定するタンパク質複合体のダイナミクス」
    • Place of Presentation
      仙台国際センター(仙台)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] Enhancement mechanisms of NRF2-dependent transcriptional activation in cancer cells がん細胞におけるNRF2依存的転写活性の増強メカニズム2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第75回日本癌学会学術総会
    • Place of Presentation
      パシフィコ横浜(横浜)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] 造血細胞の分化・増殖における酸化ストレス応答機構の役割2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第78回日本血液学会学術集会 教育講演
    • Place of Presentation
      パシフィコ横浜(横浜)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] NRF2の活性制御による加齢疾患の予防と治療の可能性2016

    • Author(s)
      本橋ほづみ
    • Organizer
      スマート・エイジングカレッジin東京
    • Place of Presentation
      東京丸の内・東北大学東京分室(東京)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] KEAP1-NRF2制御系による酸化ストレス応答とその破綻2016

    • Author(s)
      本橋ほづみ
    • Organizer
      Marianna Research Council (MRC)
    • Place of Presentation
      聖マリアンナ医科大学(川崎)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] Nrf2活性化によるNrf2依存性がんの治療戦略2016

    • Author(s)
      本橋ほづみ
    • Organizer
      日本放射線影響学会 第59回大会
    • Place of Presentation
      JMSアステールプラザ(広島)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] NRF2による酸化ストレス応答と細胞老化制御2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第11回臨床ストレス応答学会大会 シンポジウム
    • Place of Presentation
      山口大学医学部(宇部)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] Antioxidant response and cell senescence regulation by KEAP1-NRF2 system2016

    • Author(s)
      本橋ほづみ
    • Organizer
      “Frontiers in aging research toward healthy longevity”
    • Place of Presentation
      丸の内MY PLAZAホール(東京)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] KEAP1-NRF2 system in stress response and cancer malignancy2016

    • Author(s)
      本橋ほづみ
    • Organizer
      III International Scienctific Conference: Oxygen 2016
    • Place of Presentation
      The Jagiellonian University, Krakow, Poland
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] 酸化ストレス応答機構KEAP1-NRF2経路による細胞老化制御2016

    • Author(s)
      本橋ほづみ
    • Organizer
      第39回日本分子生物学会年会 シンポジウム「エピゲノム制御:疾患発症における意義」
    • Place of Presentation
      パシフィコ横浜(横浜)
    • Related Report
      2016 Annual Research Report
    • Invited
  • [Presentation] NRF2 and ROS metabolism. Educational session2016

    • Author(s)
      本橋ほづみ
    • Organizer
      Educational session. ESMO Asia 2016
    • Place of Presentation
      Suntec Signapore Convention & Exhibition Centre, Singapore
    • Related Report
      2016 Annual Research Report
    • Int'l Joint Research / Invited

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Published: 2016-04-21   Modified: 2018-03-22  

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