Annual Report 2020
Division of Genetics
Hiroyuki Mano, Masahito Kawazu, Shinji Kohsaka, Toshihide Ueno, Satoshi Inoue, (Masutani group) Mitsuko Masutani, Shoji Imamichi, Yuka Sasaki, (Yamamoto group) Yusuke Yamamoto, (Shiotani group) Bunsyo Shiotani, (Masuda group) Mari Masuda
Introduction
By sequencing the genome of cancer specimens, not only will the essential cause of carcinogenesis be clarified, but significant progress will be made in elucidating the tumor diversity and the progression mechanism of cancer. By combining this information and functional assays, we strive for the total cure of cancer patients.
The Team and What We Do
Masutani group: This research group collaborates with the Department of Radiation Oncology, NCC Hospital, the Division of Boron Neutron Capture Therapy of the Exploratory Oncology Research & Clinical Trial Center (NCC-EPOC), and other research institutes and studies radiation oncology focusing on BNCT and cancer chemotherapy targeting poly(ADP-ribosylation) and DNA damage response pathways.
Yamamoto group: The Yamamoto Group focused on non-coding RNAs, the cancer microenvironment, and extracellular vesicles to elucidate the mechanisms of cancer development and metastasis, as well as tissue stem cell maintenance and developing diagnostic markers and nucleic acid drugs for cancer.
Shiotani group: This group focuses on disorders in the DNA replication process to elucidate the mechanisms of genomic instability and cancer development through DNA replication stress resistance responses, and is developing new therapeutic strategies based on these findings.
Masuda Group: This group has been focusing on cancer-specific signaling pathways in various types of cancer (e.g., Wnt signaling in colorectal cancer) and identifying therapeutic targets and biomarkers using our in-house reverse-phase protein array (RPPA) platform and other omics technologies.
Research activities
1) To assess the pathogenicity of variants of unknown significance (VUSs) within BRCA2, we developed a method, the MANO-B method, for high-throughput functional evaluation utilizing BRCA2-deficient cells and poly(ADP-ribose) polymerase (PARP) inhibitors. We classified the functional impact of 186 BRCA2 VUSs with our computational pipeline, resulting in the classification of 37 variants as abnormal/likely abnormal. We further described a simplified, on-demand annotation system that could be used as a companion diagnostic for PARP inhibitors in patients with unknown BRCA2 VUSs.
2) We conducted comprehensive molecular profiling of desmoid tumors (DTs) to discover novel oncogenic mutations and prognostic biomarkers, and we found that CTNNB1 mutations and a chr6 copy number loss are likely the causative mutations underlying the tumorigenesis of DTs.
3) Through collaboration with the Department of Radiation Oncology at the NCC Hospital and industry, we conducted preclinical research as well as basic and translational studies of the accelerator-based BNCT system introduced in the NCC and research on boron carrier drugs. We also investigated the biological significance of factors involved in cellular responses to boron neutron capture reaction and gamma-irradiation. (Masutani group)
4) We studied poly(ADP-ribose) metabolism involved in radiation responses to develop novel anti-cancer therapeutic agents. (Masutani group)
5) We have elucidated the secretion mechanism of cancer-specific exosomes, and demonstrated that suppressing cancer exosomes can inhibit cancer metastasis, which could be a novel therapeutic strategy. We also identified exosomal proteins and miRNAs that are abundant in the blood of cancer patients, and developed novel liquid biopsy markers. (Yamamoto group)
6) We searched for novel therapeutic compounds for cancer cells with specific genetic mutations and rare cancers. For this purpose, drug screening was conducted and several candidate compounds were selected. Furthermore, we elucidated the molecular mechanisms of the anti-tumor effects of these drugs on cancer cells. (Yamamoto group)
7) We performed single-cell RNA-seq for searching specific genes and cells involved in the progression of lung cancer and breast cancer. In breast cancer, we elucidated the molecular mechanism of the transition of ductal carcinoma in situ to invasive breast carcinoma. In lung cancer, we explored the effects of smoking on each cell type at the single cell level. (Yamamoto group)
8) Using the KrasG12V lung adenocarcinoma model, we showed that an ATR kinase-dependent DNA replication stress resistance system avoids the delay in DNA replication fork progression and promotes transformation by acquiring genomic instability. (Shiotani Group)
9) Lung carcinoma cells with abnormalities in SMARCA4, a SWI/SNF chromatin remodeling complex factor, show strong sensitivity to ATR inhibitors due to the DNA replication fork instability induced by severe DNA replication stress. The same results were obtained with three different ATR inhibitors, suggesting that SMARCA4 deficiency could be an effective predictor of ATR inhibitor efficacy. (Shiotani Group)
10) The TNIK inhibitor, NCB-0846, appears to reprogram cell lineage by changing the expression patterns of transcription factors, thereby converting osteosarcoma cells into adipose-like cells. (Masuda Group)
11) In malignant pleural mesothelioma cells sensitive to an FGFR inhibitor, FGF2 is highly expressed and binds to the FGF receptor expressed by the cells, leading to activation of autocrine signaling. We anticipate FGF2 is, therefore, a companion marker for the FGFR inhibitor. (Masuda Group)
12) In collaboration with NCC-EPOC, we identified a molecule associated with advanced pancreatic cancer-induced cachexia using RPPA analysis of liver metastasis tissue samples. (Masuda Group)
Education
Four trainees from The University of Tokyo, one from Kyushu University, two from Juntendo University, one from Jikei University School of Medicine, and a young project researcher.
Three trainees from Nagasaki University (research exchange), a young project researcher, and two adjunct scientists. (Masutani group)
Three trainees from Jikei University School of Medicine, one from Keio University, and two from Waseda University (Yamamoto group)
One trainee from each of the following (three in total): Hoshi Pharmaceutical University, Kitasato University, and Tokyo College of Biotechnology (Shiotani Group)
Two trainees from Keio University and three trainees from Gakushuin University (Masuda Group)
The Future
Clinical genomics is now being implemented in clinical practice and sequencing technologies including whole genome sequencing, long read sequencing, and single cell analysis are advancing remarkably. We aim to contribute to the development and further improvement of clinical medicine through research and development of sequencing and screening technologies, and identification of useful biomarkers.
List of papers published in 2020
Journal
1. Hirozane T, Masuda M, Sugano T, Sekita T, Goto N, Aoyama T, Sakagami T, Uno Y, Moriyama H, Sawa M, Asano N, Nakamura M, Matsumoto M, Nakayama R, Kondo T, Kawai A, Kobayashi E, Yamada T. Direct conversion of osteosarcoma to adipocytes by targeting TNIK. JCI Insight, 6:2021
2. Sugano T, Masuda M, Takeshita F, Motoi N, Hirozane T, Goto N, Kashimoto S, Uno Y, Moriyama H, Sawa M, Nagakawa Y, Tsuchida A, Seike M, Gemma A, Yamada T. Pharmacological blockage of transforming growth factor-β signalling by a Traf2- and Nck-interacting kinase inhibitor, NCB-0846. Br J Cancer, 124:228-236, 2021
3. Zhou Y, Yamamoto Y, Takeshita F, Yamamoto T, Xiao Z, Ochiya T. Delivery of miR-424-5p via Extracellular Vesicles Promotes the Apoptosis of MDA-MB-231 TNBC Cells in the Tumor Microenvironment. Int J Mol Sci, 22:2021
4. Yoshida K, Yamamoto Y, Ochiya T. miRNA signaling networks in cancer stem cells. Regen Ther, 17:1-7, 2021
5. Nakayama J, Han Y, Kuroiwa Y, Azuma K, Yamamoto Y, Semba K. The In Vivo Selection Method in Breast Cancer Metastasis. Int J Mol Sci, 22:2021
6. Watase C, Shiino S, Shimoi T, Noguchi E, Kaneda T, Yamamoto Y, Yonemori K, Takayama S, Suto A. Breast Cancer Brain Metastasis-Overview of Disease State, Treatment Options and Future Perspectives. Cancers (Basel), 13:2021
7. Yoshida K, Yokoi A, Yamamoto Y, Kajiyama H. ChrXq27.3 miRNA cluster functions in cancer development. J Exp Clin Cancer Res, 40:112, 2021
8. Nakamura IT, Ikegami M, Hasegawa N, Hayashi T, Ueno T, Kawazu M, Yagishita S, Goto Y, Shinno Y, Kojima Y, Takamochi K, Takahashi F, Takahashi K, Mano H, Kohsaka S. Development of an optimal protocol for molecular profiling of tumor cells in pleural effusions at single-cell level. Cancer Sci, 112:2006-2019, 2021
9. Kohsaka S, Hirata M, Ikegami M, Ueno T, Kojima S, Sakai T, Ito K, Naka N, Ogura K, Kawai A, Iwata S, Okuma T, Yonemoto T, Kobayashi H, Suehara Y, Hiraga H, Kawamoto T, Motoi T, Oda Y, Matsubara D, Matsuda K, Nishida Y, Mano H. Comprehensive molecular and clinicopathological profiling of desmoid tumours. Eur J Cancer, 145:109-120, 2021
10. Hirose T, Ikegami M, Endo M, Matsumoto Y, Nakashima Y, Mano H, Kohsaka S. Extensive functional evaluation of exon 20 insertion mutations of EGFR. Lung Cancer, 152:135-142, 2021
11. Hayashi T, Kohsaka S, Takamochi K, Kishikawa S, Ikarashi D, Sano K, Hara K, Onagi H, Suehara Y, Takahashi F, Saito T, Nakatsura T, Kitano S, Suzuki K, Yao T. Histological characteristics of lung adenocarcinoma with uncommon actionable alterations: special emphasis on MET exon 14 skipping alterations. Histopathology, 78:987-999, 2021
12. Naito Y, Aburatani H, Amano T, Baba E, Furukawa T, Hayashida T, Hiyama E, Ikeda S, Kanai M, Kato M, Kinoshita I, Kiyota N, Kohno T, Kohsaka S, Komine K, Matsumura I, Miura Y, Nakamura Y, Natsume A, Nishio K, Oda K, Oda N, Okita N, Oseto K, Sunami K, Takahashi H, Takeda M, Tashiro S, Toyooka S, Ueno H, Yachida S, Yoshino T, Tsuchihara K. Clinical practice guidance for next-generation sequencing in cancer diagnosis and treatment (edition 2.1). Int J Clin Oncol, 26:233-283, 2021
13. Suehara Y, Kohsaka S, Hayashi T, Akaike K, Kurisaki-Arakawa A, Sato S, Kobayashi E, Mizuno S, Ueno T, Morii T, Okuma T, Kurihara T, Hasegawa N, Sano K, Sasa K, Okubo T, Kim Y, Mano H, Saito T. Identification of a Novel MAN1A1-ROS1 Fusion Gene Through mRNA-based Screening for Tyrosine Kinase Gene Aberrations in a Patient with Leiomyosarcoma. Clin Orthop Relat Res, 479:838-852, 2021
14. Kishikawa S, Hayashi T, Saito T, Takamochi K, Kohsaka S, Sano K, Sasahara N, Sasa K, Kurihara T, Hara K, Suehara Y, Takahashi F, Suzuki K, Yao T. Diffuse expression of MUC6 defines a distinct clinicopathological subset of pulmonary invasive mucinous adenocarcinoma. Mod Pathol, 34:786-797, 2021
15. Tsuyama S, Kohsaka S, Hayashi T, Suehara Y, Hashimoto T, Kajiyama Y, Tsurumaru M, Ueno T, Mano H, Yao T, Saito T. Comprehensive clinicopathological and molecular analysis of primary malignant melanoma of the oesophagus. Histopathology, 78:240-251, 2021
16. Uchihara T, Miyake K, Yonemura A, Komohara Y, Itoyama R, Koiwa M, Yasuda T, Arima K, Harada K, Eto K, Hayashi H, Iwatsuki M, Iwagami S, Baba Y, Yoshida N, Yashiro M, Masuda M, Ajani JA, Tan P, Baba H, Ishimoto T. Extracellular Vesicles from Cancer-Associated Fibroblasts Containing Annexin A6 Induces FAK-YAP Activation by Stabilizing β1 Integrin, Enhancing Drug Resistance. Cancer Res, 80:3222-3235, 2020
17. Sekita T, Yamada T, Kobayashi E, Yoshida A, Hirozane T, Kawai A, Uno Y, Moriyama H, Sawa M, Nagakawa Y, Tsuchida A, Matsumoto M, Nakamura M, Nakayama R, Masuda M. Feasibility of Targeting Traf2-and-Nck-Interacting Kinase in Synovial Sarcoma. Cancers (Basel), 12:2020
18. Miyanaga A, Masuda M, Motoi N, Tsuta K, Nakamura Y, Nishijima N, Watanabe SI, Asamura H, Tsuchida A, Seike M, Gemma A, Yamada T. Whole-exome and RNA sequencing of pulmonary carcinoid reveals chromosomal rearrangements associated with recurrence. Lung Cancer, 145:85-94, 2020
19. Sugano T, Yoshida M, Masuda M, Ono M, Tamura K, Kinoshita T, Tsuda H, Honda K, Gemma A, Yamada T. Prognostic impact of ACTN4 gene copy number alteration in hormone receptor-positive, HER2-negative, node-negative invasive breast carcinoma. Br J Cancer, 122:1811-1817, 2020
20. Liew LC, Gailhouste L, Tan GC, Yamamoto Y, Takeshita F, Nakagama H, Ochiya T. MicroRNA-124a inhibits endoderm lineage commitment by targeting Sox17 and Gata6 in mouse embryonic stem cells. Stem Cells, 38:504-515, 2020
21. Chikuda J, Otsuka K, Shimomura I, Ito K, Miyazaki H, Takahashi RU, Nagasaki M, Mukudai Y, Ochiya T, Shimane T, Shirota T, Yamamoto Y. CD44s Induces miR-629-3p Expression in Association with Cisplatin Resistance in Head and Neck Cancer Cells. Cancers (Basel), 12:2020
22. Tadokoro H, Hirayama A, Kudo R, Hasebe M, Yoshioka Y, Matsuzaki J, Yamamoto Y, Sugimoto M, Soga T, Ochiya T. Adenosine leakage from perforin-burst extracellular vesicles inhibits perforin secretion by cytotoxic T-lymphocytes. PLoS One, 15:e0231430, 2020
23. Yoshihara M, Kajiyama H, Yokoi A, Sugiyama M, Koya Y, Yamakita Y, Liu W, Nakamura K, Moriyama Y, Yasui H, Suzuki S, Yamamoto Y, Ricciardelli C, Nawa A, Shibata K, Kikkawa F. Ovarian cancer-associated mesothelial cells induce acquired platinum-resistance in peritoneal metastasis via the FN1/Akt signaling pathway. Int J Cancer, 146:2268-2280, 2020
24. Urabe F, Kosaka N, Sawa Y, Yamamoto Y, Ito K, Yamamoto T, Kimura T, Egawa S, Ochiya T. miR-26a regulates extracellular vesicle secretion from prostate cancer cells via targeting SHC4, PFDN4, and CHORDC1. Sci Adv, 6:eaay3051, 2020
25. Kumazaki M, Shimomura I, Kiyono T, Ochiya T, Yamamoto Y. Cell-type specific tumorigenesis with Ras oncogenes in human lung epithelial cells. Biochem Biophys Res Commun, 525:483-490, 2020
26. Duleba M, Yamamoto Y, Neupane R, Rao W, Xie J, Qi Y, Liew AA, Niroula S, Zhang Y, Mahalingam R, Wang S, Goller K, Ajani JA, Vincent M, Ho KY, Hou JK, Hyams JS, Sylvester FA, Crum CP, McKeon F, Xian W. Cloning of ground-state intestinal stem cells from endoscopic biopsy samples. Nat Protoc, 15:1612-1627, 2020
27. Prieto-Vila M, Shimomura I, Kogure A, Usuba W, Takahashi RU, Ochiya T, Yamamoto Y. Quercetin Inhibits Lef1 and Resensitizes Docetaxel-Resistant Breast Cancer Cells. Molecules, 25:2020
28. Kogure A, Naito Y, Yamamoto Y, Yashiro M, Kiyono T, Yanagihara K, Hirakawa K, Ochiya T. Cancer cells with high-metastatic potential promote a glycolytic shift in activated fibroblasts. PLoS One, 15:e0234613, 2020
29. Sanchez Calle A, Yamamoto T, Kawamura Y, Hironaka-Mitsuhashi A, Ono M, Tsuda H, Shimomura A, Tamura K, Takeshita F, Ochiya T, Yamamoto Y. Long non-coding NR2F1-AS1 is associated with tumor recurrence in estrogen receptor-positive breast cancers. Mol Oncol, 14:2271-2287, 2020
30. Urabe F, Kosaka N, Sawa Y, Ito K, Kimura T, Egawa S, Ochiya T, Yamamoto Y. The miR-1908/SRM regulatory axis contributes to extracellular vesicle secretion in prostate cancer. Cancer Sci, 111:3258-3267, 2020
31. Yoshida K, Yokoi A, Kato T, Ochiya T, Yamamoto Y. The clinical impact of intra- and extracellular miRNAs in ovarian cancer. Cancer Sci, 111:3435-3444, 2020
32. Ichikawa A, Fujita Y, Hosaka Y, Kadota T, Ito A, Yagishita S, Watanabe N, Fujimoto S, Kawamoto H, Saito N, Yoshida M, Hashimoto M, Minagawa S, Hara H, Motoi N, Yamamoto Y, Ochiya T, Araya J, Kuwano K. Chaperone-mediated autophagy receptor modulates tumor growth and chemoresistance in non-small cell lung cancer. Cancer Sci, 111:4154-4165, 2020
33. Ukai S, Honma R, Sakamoto N, Yamamoto Y, Pham QT, Harada K, Takashima T, Taniyama D, Asai R, Fukada K, Naka K, Tanabe K, Ohdan H, Yasui W. Molecular biological analysis of 5-FU-resistant gastric cancer organoids; KHDRBS3 contributes to the attainment of features of cancer stem cell. Oncogene, 39:7265-7278, 2020
34. Otsuka K, Yamamoto Y, Ochiya T. Uncovering temperature-dependent extracellular vesicle secretion in breast cancer. J Extracell Vesicles, 10:e12049, 2020
35. Kurashima K, Kashiwagi H, Shimomura I, Suzuki A, Takeshita F, Mazevet M, Harata M, Yamashita T, Yamamoto Y, Kohno T, Shiotani B. SMARCA4 deficiency-associated heterochromatin induces intrinsic DNA replication stress and susceptibility to ATR inhibition in lung adenocarcinoma. NAR Cancer, 2:zcaa005, 2020
36. Hayashi T, Odintsov I, Smith RS, Ishizawa K, Liu AJW, Delasos L, Kurzatkowski C, Tai H, Gladstone E, Vojnic M, Kohsaka S, Suzawa K, Liu Z, Kunte S, Mattar MS, Khodos I, Davare MA, Drilon A, Cheng E, Stanchina E, Ladanyi M, Somwar R. RET inhibition in novel patient-derived models of RET-fusion positive lung adenocarcinoma reveals a role for MYC upregulation. Dis Model Mech, 14:2020
37. Kobayashi H, Shin M, Makise N, Shinozaki-Ushiku A, Ikegami M, Taniguchi Y, Shinoda Y, Kohsaka S, Ushiku T, Oda K, Miyagawa K, Aburatani H, Mano H, Tanaka S. Genetic Testing Distinguishes Multiple Chondroid Chordomas with Neuraxial Bone Metastases from Multicentric Tumors. Case Rep Genet, 2020:8877722, 2020
38. Kurihara T, Suehara Y, Akaike K, Hayashi T, Kohsaka S, Ueno T, Hasegawa N, Takagi T, Sasa K, Okubo T, Kim Y, Mano H, Yao T, Kaneko K, Saito T. Nanostring-based screening for tyrosine kinase fusions in inflammatory myofibroblastic tumors. Sci Rep, 10:18724, 2020
39. Hirata E, Ishibashi K, Kohsaka S, Shinjo K, Kojima S, Kondo Y, Mano H, Yano S, Kiyokawa E, Sahai E. The Brain Microenvironment Induces DNMT1 Suppression and Indolence of Metastatic Cancer Cells. iScience, 23:101480, 2020
40. Hayashi T, Kohsaka S, Takamochi K, Hara K, Kishikawa S, Sano K, Takahashi F, Suehara Y, Saito T, Takahashi K, Suzuki K, Yao T. Clinicopathological characteristics of lung adenocarcinoma with compound EGFR mutations. Hum Pathol, 103:42-51, 2020
41. Shinozaki-Ushiku A, Kohsaka S, Kage H, Oda K, Miyagawa K, Nakajima J, Aburatani H, Mano H, Ushiku T. Genomic profiling of multiple primary cancers including synchronous lung adenocarcinoma and bilateral malignant mesotheliomas: Identification of a novel BAP1 germline variant. Pathol Int, 70:775-780, 2020
42. Suehara Y, Kohsaka S, Yamaguchi S, Hayashi T, Kurihara T, Sano K, Sasa K, Akaike K, Ueno T, Kojima S, Ikegami M, Mizuno S, Okubo T, Kim Y, Kaneko K, Saito T, Kato S, Mano H. Assessment of Predictive Biomarkers of the Response to Pazopanib Based on an Integrative Analysis of High-grade Soft-tissue Sarcomas: Analysis of a Tumor Sample from a Responder and Patients with Other Soft-tissue Sarcomas. Clin Orthop Relat Res, 478:2461-2476, 2020
43. Ikegami M, Kohsaka S, Ueno T, Momozawa Y, Inoue S, Tamura K, Shimomura A, Hosoya N, Kobayashi H, Tanaka S, Mano H. High-throughput functional evaluation of BRCA2 variants of unknown significance. Nat Commun, 11:2573, 2020
44. Hayashi T, Takamochi K, Kohsaka S, Kishikawa S, Suehara Y, Takahashi F, Suzuki K, Saito T, Yao T. Transformation from EGFR/PTEN co-mutated lung adenocarcinoma to small cell carcinoma in lymph node metastasis. Pathol Int, 70:295-299, 2020
45. Inoue S, Yoshida E, Fukui Y, Ueno T, Kawazu M, Takeyama R, Ikemura M, Osuga Y, Terao Y, Hirota Y, Mano H. KRAS mutations in uterine endometrium are associated with gravidity and parity. Cell Death Dis, 11:347, 2020
46. Akahane K, Yasuda T, Tsuzuki S, Hayakawa F, Kiyokawa N, Somazu S, Watanabe A, Kagami K, Abe M, Harama D, Goi K, Kawazu M, Kojima S, Imamura T, Goto H, Iwamoto S, Minegishi M, Abe M, Hojo H, Inaba T, Mano H, Sugita K, Inukai T. High prevalence of MEF2D fusion in human B-cell precursor acute lymphoblastic leukemia cell lines. Hematol Oncol, 38:614-617, 2020
47. Kawazoe A, Kuboki Y, Shinozaki E, Hara H, Nishina T, Komatsu Y, Yuki S, Wakabayashi M, Nomura S, Sato A, Kuwata T, Kawazu M, Mano H, Togashi Y, Nishikawa H, Yoshino T. Multicenter Phase I/II Trial of Napabucasin and Pembrolizumab in Patients with Metastatic Colorectal Cancer (EPOC1503/SCOOP Trial). Clin Cancer Res, 26:5887-5894, 2020
48. Kumagai S, Togashi Y, Sakai C, Kawazoe A, Kawazu M, Ueno T, Sato E, Kuwata T, Kinoshita T, Yamamoto M, Nomura S, Tsukamoto T, Mano H, Shitara K, Nishikawa H. An Oncogenic Alteration Creates a Microenvironment that Promotes Tumor Progression by Conferring a Metabolic Advantage to Regulatory T Cells. Immunity, 53:187-203.e8, 2020
49. Kumagai S, Togashi Y, Kamada T, Sugiyama E, Nishinakamura H, Takeuchi Y, Vitaly K, Itahashi K, Maeda Y, Matsui S, Shibahara T, Yamashita Y, Irie T, Tsuge A, Fukuoka S, Kawazoe A, Udagawa H, Kirita K, Aokage K, Ishii G, Kuwata T, Nakama K, Kawazu M, Ueno T, Yamazaki N, Goto K, Tsuboi M, Mano H, Doi T, Shitara K, Nishikawa H. The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies. Nat Immunol, 21:1346-1358, 2020
50. Tateishi K, Miyake Y, Kawazu M, Sasaki N, Nakamura T, Sasame J, Yoshii Y, Ueno T, Miyake A, Watanabe J, Matsushita Y, Shiba N, Udaka N, Ohki K, Fink AL, Tummala SS, Natsumeda M, Ikegaya N, Nishi M, Ohtake M, Miyazaki R, Suenaga J, Murata H, Aoki I, Miller JJ, Fujii Y, Ryo A, Yamanaka S, Mano H, Cahill DP, Wakimoto H, Chi AS, Batchelor TT, Nagane M, Ichimura K, Yamamoto T. A Hyperactive RelA/p65-Hexokinase 2 Signaling Axis Drives Primary Central Nervous System Lymphoma. Cancer Res, 80:5330-5343, 2020
51. Tsuzuki S, Yasuda T, Kojima S, Kawazu M, Akahane K, Inukai T, Imaizumi M, Morishita T, Miyamura K, Ueno T, Karnan S, Ota A, Hyodo T, Konishi H, Sanada M, Nagai H, Horibe K, Tomita A, Suzuki K, Muramatsu H, Takahashi Y, Miyazaki Y, Matsumura I, Kiyoi H, Hosokawa Y, Mano H, Hayakawa F. Targeting MEF2D-fusion Oncogenic Transcriptional Circuitries in B-cell Precursor Acute Lymphoblastic Leukemia. Blood Cancer Discov, 1:82-95, 2020
52. Sonoda Y, Sasaki Y, Gunji A, Shirai H, Araki T, Imamichi S, Onodera T, Ryd?n AM, Watanabe M, Itami J, Honda T, Ashizawa K, Nakao K, Masutani M. Reduced Tumorigenicity of Mouse ES Cells and the Augmented Anti-Tumor Therapeutic Effects under Parg Deficiency. Cancers (Basel), 12:2020
53. Nozaki T, Nakamoto K, Myat AB, Sasaki Y, Imamichi S, Onodera T, Masutani M. Effects of 3-aminobenzamide on cell cycle arrest after gamma-irradiation. J Trans Sci, 6:1-6, 2020