Molecular and Cellular Glycoproteomics Research Group

Research Project

Post-translational protein modification (glycosylation, amino acid isomerization, etc.) has a pivotal role in the functional regulation of proteins via the modifications of their three-dimensional structures, subcellular localization, and interactions with other functional molecules. To better understand the biological roles of such modifications, it is important to elucidate how physiological and pathological changes will alter the synthetic machinery/mechanism, and consequently, what sites of what proteins will be modified with which structural compartments, at each level of proteins, cells, tissues, and organisms. To confront these important matters, this research group aims to develop multi-omics technologies, including glycoproteomics, glycomics, glyco-transcriptomics, and glyco-metabolomics, etc. These multi-omics data will be available in the public databases that we and our colleagues developed, which will contribute to the glycoscience community.

Many diseases such as cancer trigger changes in cell glycomes, known as "disease-related glycosylation alteration." We have previously developed various disease-biomarkers and molecular-targeted drugs by targeting this disease-related glycosylation alteration. On the other hand, the biological significance of the phenomena is yet not well understood. Our goal is reaching to a comprehensive understanding of the physiological and pathological "function of glycans" in tumors, virus infections, aging as well as immunities, reproductions, and other cell functions by using multi-omics approaches.

Results

• Miyashita, SI; Ogura, T; Matsuura, SI; Fukuda, E.
  Quantitative Evaluation of Iron-Containing Proteins Bound to Mesoporous Silica Microspheres by Inductively Coupled Plasma Mass Spectrometry and Confocal Laser Raman Microscopy.
  MOLECULES. 2025 Mar 11;30(6):1252. doi:10.3390/molecules30061252
• Takada, N; Ishikawa, M; Sato, K; Kunikata, H; Ninomiya, T; Hanyuda, A; Fukuda, E; Yamaguchi, K; Ono, C; Kirihara, T; Shintani, C; Tsusu, C; Osanai, A; Goshima, N; Izumi, Y; Zorumski, CF; Nakazawa, T.
  Proteome-Wide Analysis of Autoantibodies in Open-Angle Glaucoma in Japanese Population: A Pilot Study.
  BIOMEDICINES. 2025 Mar 14;13(3):718. doi:10.3390/biomedicines13030718
• Boottanun, P; Fuseya, S; Kuno, A.
  Toward spatial glycomics and glycoproteomics: Innovations and applications.
  BBA ADV. 2025 Feb. doi:10.1016/j.bbadva.2025.100146
• Sato, T; Sugiyama, D; Koseki, J; Kojima, Y; Hattori, S; Sone, K; Nishinakamura, H; Ishikawa, T; Ishikawa, Y; Kato, T; Kiyoi, H; Nishikawa, H.
  Sustained inhibition of CSF1R signaling augments antitumor immunity through inhibiting tumor-associated macrophages.
  JCI INSIGHT. 2025 JAN 9. doi:10.1172/jci.insight.178146
• Shimazaki, H; Uojima, H; Yamasaki, K; Obayashi, T;Fuseya, S; Sato, T; Mizokami, M; Kuno, A.
  M2BPgs-HCC: An Automated Multilectin Bead Array Indicating Aberrant Glycosylation Signatures Toward Hepatitis C Virus-Associated Hepatocellular Carcinoma Prognosis.
  MOLECULES. 2024 Nov 28;29(23):5640. doi:10.3390/molecules29235640
• Nagai-Okatani, C; Tomioka, A; Tominaga, D; Sakaue, H; Kuno, A; Kaji, H.
  Inter-tissue glycan heterogeneity: site-specific glycoform analysis of mouse tissue N-glycoproteomes using MS1-based glycopeptide detection method assisted by lectin microarray.
  ANALYTICAL AND BIOANALYTICAL CHEMISTRY. 2024 Dec 16. doi:10.1007/s00216-024-05686-y
• Okamura, Y; Gochi, K; Ishikawa, T; Hayashi, T; Fuseya, S; Suzuki, R; Kanai, M; Inoue, Y; Murakami, Y; Sadaki, S; Jeon, H; Hayama, M; Ishii, H; Tsunakawa, Y; Ochi, H; Sato, S; Hamada, M; Abe, C; Morita, H; Okada, R; Shiba, D; Muratani, M; Shinohara, M; Akiyama, T; Kudo, T; Takahashi, S.
  Impact of microgravity and lunar gravity on murine skeletal and immune systems during space travel.
  SCI REP. 2024 Nov 20;14(1):28774. doi:10.1038/s41598-024-79315-0
• Yamaguchi, Y; Ishii, K; Koizumi, S; Sakaue, H; Maruno, T; Fukuhara, M; Shibuya, R; Tsunaka, Y; Matsushita, A; Bandoh, K; Torisu, T; Murata-Kishimoto, C; Tomioka, A; Mizukado, S; Kaji, H; Kashiwakura, Y; Ohmori, T; Kuno, A; Uchiyama, S.
  Mucin-Type O-Glycosylation in Viral Protein 2 Indirectly Affects the Transduction Efficiency of Recombinant Adeno-Associated Virus Serotype 6.
  MOLECULAR THERAPY. Vol 32 No 4S1, 688-689. 22 APR 2024. doi:
• Sakaue, H; Kuno, A.
  isoAsp-Quest: Workflow development for isoAsp identification using database searches.
  J BIOCHEM. 2024 Oct 23:mvae071. doi: 10.1093/jb/mvae071
• Shimazaki, H; Fuseya, S; Ono, A; Ootani, H; Mizukado, S; Obayashi, T; Tanaka, N; Kajiyama, K; Ashitomi, M; Yamauchi, K; Yasuda, S; Miyabe, T; Nakamura, K; Segawa, O; Kuno, A; Sawakami, K.
  Benchtop glyco-analyzer: from development of biomarker to potential use in clinical setting.
  CLINICAL CHEMISTRY. 2024 Oct 1. doi: 10.1093/clinchem/hvae106.381
• Hayashi, Y; Tajiri, K; Ozawa, T; Angata, K; Sato, T; Togayachi, A; Nagashima, I; Shimizu, H; Murayama, A; Muraishi, N; Narimatsu, H; Yasuda, I.
  Impact of preS1 Evaluation in the Management of Chronic Hepatitis B Virus Infection.
  MEDICINA (Kaunas). 2024 Aug 16;60(8):1334. doi: 10.3390/medicina60081334
• Nagai-Okatani, C; Tominaga, D; Tomioka, A; Sakaue, H; Goda, N; Ko, S; Kuno, A; Kaji, H.
  GRable version 1.0: A software tool for site-specific glycoform analysis with improved MS1-based glycopeptide detection with parallel clustering and confidence evaluation with MS2 information.
  MOL CELL PROTEOMICS. 2024 Aug 22:100833. doi: 10.1016/j.mcpro.2024.100833
• Xu, Z; Zhang, H; Tian, J; Ku, X; Wei, R; Hou, J; Zhang, C; Yang, F; Zou, X; Li, Y; Kaji, H; Tao, SC; Kuno, A; Yan, W; Da, LT; Zhang, Y.
  O-glycosylation of SARS-CoV-2 spike protein by host O-glycosyltransferase strengthens its trimeric structure.
  ACTA BIOCHIM BIOPHYS SIN (Shanghai). 2024 Jul 26. doi: 10.3724/abbs.2024127
• Fuseya, S; Ono, A; Ootani, H; Mizukado, S; Obayashi, T; Tanaka, N; Shimazaki, H; Kajiyama, K; Ashitomi, M; Yasuda, S; Miyabe, T; Nakamura, K; Segawa, O; Sawakami, K; Kuno, A.
  Rapid Glyco-Qualitative Assessment of Recombinant Proteins Using a Fully Automated System.
  J VIS EXP. 2024 Jun 28;(208). doi: 10.3791/66571
• Hayashi, T; Sadaki, S; Tsuji, R; Okada, R; Fuseya, S; Kanai, M; Nakamura, A; Okamura, Y; Muratani, M; Wenchao, G; Sugasawa, T; Mizuno, S; Warabi, E; Kudo, T; Takahashi, S; Fujita, R.
  Dual-specificity phosphatases 13 and 27 as key switches in muscle stem cell transition from proliferation to differentiation.
  STEM CELLS. 2024 Jul 8:sxae045. doi: 10.1093/stmcls/sxae045
• Yamaguchi, Y; Ishii, K; Koizumi, S; Sakaue, H; Maruno, T; Fukuhara, M; Shibuya, R; Tsunaka, Y; Matsushita, A; Bandoh, K; Torisu, T; Murata-Kishimoto, C; Tomioka, A; Mizukado, S; Kaji, H; Kashiwakura, Y; Ohmori, T; Kuno, A;; Uchiyama, S.
  Glycosylation of recombinant adeno-associated virus serotype 6.
  MOL THER METHODS CLIN DEV. 2024 Apr 25;32(2):101256. doi: 10.1016/j.omtm.2024.101256
• Hiono, T; Sakaue, H; Tomioka, A; Kaji, H; Sasaki, M; Orba, Y; Sawa, H; Kuno, A.
  Combinatorial Approach with Mass Spectrometry and Lectin Microarray Dissected Site-Specific Glycostem and Glycoleaf Features of the Virion-Derived Spike Protein of Ancestral and γ Variant SARS-CoV-2 Strains.
  J PROTEOME RES. 2024 Mar 27. doi: 10.1021/acs.jproteome.3c00874
• Miyashita, S; Ogura, T; Matsuura, S; Fukuda, E.
  Particle Size Measurement and Detection of Bound Proteins of Non-Porous/Mesoporous Silica Microspheres by Single-Particle Inductively Coupled Plasma Mass Spectrometry.
  MOLECULES. 2024 Feb 6. 29(5):1086. doi: 10.3390/molecules29051086
• Phuyathip, W; Putthisen, S; Panawan O, Ma-In P; Teeravirote, K; Sintusen, P; Udomkitkosol, S; Detarya, M; Luang. S; Mahalapbutr, P; Sato, T; Kuno, A; Chuangchaiya, S; Silsirivanit, A.
  Role of Wisteria floribunda agglutinin binding glycans in carcinogenesis and metastasis of cholangiocarcinoma.
  HISTOCHEM CELL BIOL. 2024 Feb 23. doi: 10.1007/s00418-024-02270-4
• Matsuda, A; Boottanun, P; Koizumi, S; Nagai, M; Kuno, A.
  Differential Glycoform Analysis of MUC1 Derived from Biological Specimens Using an Antibody-Overlay Lectin Microarray.
  METHODS MOL BIOL. 2024;2763:223-236. doi: 10.1007/978-1-0716-3670-1_19
• Niibori-Nambu, A; Yamasaki, Y; Kobayashi, D; Angata, K; Kuno, A; Panawan, O; Silsilivanit, A; Narimatsu, H; Araki, N.
  Chondroitin sulfate modification of CSPG4 regulates the maintenance and differentiation of glioma initiating cells via integrin-associated signaling.
  J BIOL CHEM. 2024 Feb 1:105706. doi: 10.1016/j.jbc.2024.105706
• Shimazaki, H; Nakamura, K; Ono, A; Segawa, O; Sawakami, K; Koizuka, M; Hirayama, M; Hori, K; Tajima, H; Kuno, A.
  Auto-Lectin Dotcoding by Two Octopuses: Rapid Analysis of Fluorescence-Labeled Glycoproteins by an 8-channel Fully-Automatic Bead Array Scanner with a Rolling-Circle Detector.
  ANAL CHEM. 2023 Aug 3. doi: 10.1021/acs.analchem.3c01395
• Boottanun, P; Nagai-Okatani, C; Nagai, M; Ungkulpasvich, U; Yamane, S; Yamada, M; Kuno, A.
  An improved evanescent fluorescence scanner suitable for high-resolution glycome mapping of formalin-fixed paraffin-embedded tissue sections.
  ANALYTICAL AND BIOANALYTICAL CHEMISTRY. 2023 JUL 3. doi: 10.1007/s00216-023-04824-2
• Tanaka, S; Sakaue, H, Koiwai, T; Okuda, N; Okuyama, K; Horioka, Y; Hiramatsu, Y; Kawashima, M; Ishiguro, N; Sato, T.
  Near-infrared radiation causes sebaceous gland enlargement along with an ROS-dependent augmentation of epidermal growth factor receptor expression in hamsters.
  EXPERIMENTAL DERMATOLOGY. 2023 JUL 4. doi: 10.1111/exd.14878
• Fuseya, S; Izumi, H; Hamano, A; Murakami, Y; Suzuki, R; Koiwai, R; Hayashi, T; Kuno, A, Takahashi, S; Kudo, T.
  Reduction in disialyl-T antigen levels in mice deficient for both St6galnac3 and St6galnac4 results in blood filling of lymph nodes.
  SCI REP. 2023 Jun 29;13(1):10582. doi: 10.1038/s41598-023-37363-y
• Matsuda, KM; Kotani, H; Yamaguchi, K; Okumura, T; Fukuda, E; Kono, M; Hisamoto, T; Kawanabe, R; Norimatsu, Y; Kuzumi, A; Fukayama, M; Fukasawa, T; Ebata, S; Yoshizaki-Ogawa, A; Okamura, T; Shoda, H; Fujio, K; Goshima, N; Sato, S; Yoshizaki, A.
  Significance of anti-transcobalamin receptor antibodies in cutaneous arteritis revealed by proteome-wide autoantibody screening.
  J AUTOIMMUN. 2023 Jan 30;135:102995. doi: 10.1016/j.jaut.2023.102995
• Itakura, Y; Hasegawa, Y; Kikkawa, Y; Murakami, Y; Sugiura, K; Nagai-Okatani, C; Sasaki, N; Umemura, M; Takahashi, Y; Kimura, T; Kuno, A; Ishiwata, T; Toyoda, M.
  Spatiotemporal changes of tissue glycans depending on localization in cardiac aging.
  REGEN THER. 2023 Jan 7;22:68-78. doi: 10.1016/j.reth.2022.12.009
• Zou, X; Lu, J; Deng, Y; Liu, Q; Yan, X; Cui, Y; Xiao, X; Fang, M; Yang, F; Sawaki, H; Sato, T; Tan, B; Lu, X; Feng, B; Kuno, A; Narimatsu, H; Gao, C; Zhang, Y.
  ST6GAL1 inhibits metastasis of hepatocellular carcinoma via modulating sialylation of MCAM on cell surface.
  ONCOGENE. 2022 Dec 17. doi: 10.1038/s41388-022-02571-9
• Tasaki, M; Tateno, H; Sato, T; Narimatsu, H; Saito, K; Nakagawa, Y; Aoki, T; Kamimura, M; Ushiki, T; Takahashi, K; Tomita, Y.
  Hyporesponsiveness against donors ABO antigens of renal grafts after ABO-incompatible kidney transplantation.
  CLIN EXP NEPHROL. 2022 Oct 8. doi: 10.1007/s10157-022-02280-3
• Hiono, T; Kuno, A.
  Glycan Profiling of Viral Glycoproteins with the Lectin Microarray.
  METHODS MOL BIOL. 2022;2556:59-68. doi: 10.1007/978-1-0716-2635-1_6
• Matsuda, KM; Yoshizaki, A; Yamaguchi, K; Fukuda, E; Okumura, T; Ogawa, K; Ono, C; Norimatsu, Y; Kotani, H; Hisamoto, T; Kawanabe, R; Kuzumi, A; Fukasawa, T; Ebata, S; Miyagawa, T; Yoshizaki-Ogawa, A; Goshima, N; Sato, S.
  Autoantibody Landscape Revealed by Wet Protein Array: Sum of Autoantibody Levels Reflects Disease Status.
  FRONT IMMUNOL. 2022 May 4;13:893086. doi: 10.3389/fimmu.2022.893086
• Kuroda, T; Hattori, Y; Kagami, A; Fukuda, E; Tamura, G.
  Genetic modification in the body to make friends with cancer cells?! Dreaming of cancer treatment in 100 years.
  CANCER SCIENCE. 113 1517-1517; FEB
• Fujimoto, M; Arai, E; Nishiyama, N; Maeshima, A; Fujimoto, H; Kitamura, H; Kuno, A; Yoshida, T; Kanai, Y.
  Lectin staining analysis of protein glycosylation in urothelial carcinomas.
  CANCER SCIENCE. 113 378-378; FEB
• Kitazume, Y; Arai, E; Matsuda, A; Kakuda, S; Ohara, K; Maeshima, A; Kuno, A; Yoshida, T; Kanai, Y.
  Alteration of protein glycosylation in renal carcinogenesis.
  CANCER SCIENCE. 113 1284-1284; FEB
• Nagata, Y; Kageyama, S; Ishikawa, T; Kokura, S; Okayama, T; Abe, T; Murakami, M; Otsuka, K; Ariyoshi, T; Kojima, T; Taniguchi, K; Kobayashi, S; Shimada, H; Yajima, S; Suzuki, T; Hirano, S; Tsuchikawa, T; Shichinohe, T; Ueda, S; Kanetaka, K; Yoneda, A; Wada, H; Doki, Y; Yamaue, H; Katsuda, M; Ohi, M; Yasuda, H; Kondo, K; Kataoka, M; Kodera, Y; Koike, M; Shiraishi, T; Miyahara, Y; Goshima,N;Fukuda, E; Yamaguchi, K; Sato, E; Ikeda, H; Yamada, T; Osako, M; Hirai, K; Miyamoto, H; Watanabe, T; Shiku, H.
  Prognostic significance of NY-ESO-1 antigen and PIGR expression in esophageal tumors of CHP-NY-ESO-1-vaccinated patients as adjuvant therapy.
  CANCER IMMUNOL IMMUNOTHER. 2022 Apr 16. doi: 10.1007/s00262-022-03194-5
• Tasaki, M; Tateno, H; Sato, T; Tomioka, A; Kaji, H; Narimatsu, H; Saito, K; Nakagawa, Y; Aoki, T; Kamimura, M; Ushiki, T; Okada, M; Miwa, Y; Hotta, K; Yoshida, Y; Takahashi, K; Tomita, Y.
  A Novel Method of CD31-Combined ABO Carbohydrate Antigen Microarray Predicts Acute Antibody-Mediated Rejection in ABO-Incompatible Kidney Transplantation.
  TRANSPL INT. 2022 Mar 23;35:10248. doi: 10.3389/ti.2022.10248
• Suzuki, R; Nakamura, Y; Koiwai, R; Fuseya, S; Murakami, Y; Hagiwara, K; Sato, T; Takahashi, S; Kudo, T.
  Global Loss of Core 1-Derived O-Glycans in Mice Leads to High Mortality Due to Acute Kidney Failure and Gastric Ulcers.
  INT J MOL SCI. 2022 Jan 24;23(3):1273. doi: 10.3390/ijms23031273
• Sogabe, M; Kojima, S; Kaya, T; Tomioka, A; Kaji, H; Sato, T; Chiba, Y; Shimizu, A; Tanaka, N; Suzuki, N; Hayashi, I; Mikami, M; Togayachi, A; Narimatsu, H.
  Sensitive New Assay System for Serum Wisteria floribunda Agglutinin-Reactive Ceruloplasmin That Distinguishes Ovarian Clear Cell Carcinoma from Endometrioma.
  ANALYTICAL CHEMISTRY; doi:10.1021/acs.analchem.1c04302
• Nagai-Okatani, C; Zou, X; Matsuda, A; Itakura, Y; Toyoda, M; Zhang, Y; Kuno, A.
  Tissue Glycome Mapping: Lectin Microarray-Based Differential Glycomic Analysis of Formalin-Fixed Paraffin-Embedded Tissue Sections.
  METHODS MOL BIOL. 2022;2460:161-180. doi: 10.1007/978-1-0716-2148-6_10
• Angata, K; Wagatsuma, T; Togayachi, A; Sato, T; Sogabe, M; Tajiri, K; Ozawa, T; Nagashima, I; Shimizu, H; Iijima, S; Korenaga, M; Kuno, A; Kaji, H; Mizokami, M; Narimatsu, H.
  O-glycosylated HBsAg peptide can induce specific antibody neutralizing HBV infection.
  BIOCHIM BIOPHYS ACTA GEN SUBJ. 2021 Sep 25:130020. doi: 10.1016/j.bbagen.2021.130020
• Funakoshi, Y; Ohji, G; Yakushijin, K; Ebisawa, K; Arakawa, Y; Saegusa, J; Matsumoto, H; Imanishi, T; Fukuda, E; Matsutani, T; Mori, Y; Iwata, K; Minami, H.
  Massive surge of mRNA expression of clonal B-cell receptor in patients with COVID-19.
  HELIYON. 2021 Aug;7(8):e07748. doi: 10.1016/j.heliyon.2021.e07748. Epub 2021 Aug 10
• Noro, E; Matsuda,A; Kyoutou,T; Sato, T; Tomioka,A; Nagai,M; Sogabe,M; Tsuruno,C; Takahama,Y; Kuno, A; Tanaka,Y; Kaji, H; Narimatsu, H.
  N-glycan structures of Wisteria floribunda agglutinin-positive Mac2 binding protein in the serum of patients with liver fibrosis.
  GLYCOBIOLOGY. 2021 Jun 29:cwab060. doi: 10.1093/glycob/cwab060
• Sakata-Matsuzawa, M; Denda-Nagai, K; Fujihira, H; Noji, M; Ishii-Schrade, KB; Matsuda, A; Kuno, A; Okazaki, M; Nakai, K; Horimoto, Y; Saito, M; Irimura, T
  Glycans unique to the relapse-prone subset within triple-negative breast cancer as revealed by lectin array-based analysis of surgical specimens
  PLoS One. 2021 May 11;16(5):e0250747. doi: 10.1371/journal.pone.0250747. eCollection