研究内容
癌組織の形態情報ならびに分子発現情報と臨床情報をリンクした多次元的な解析を行うことで、各臓器がんに特徴的な病態に関わる分子機構、がん間質相互作用に代表される様な複雑な生体内での細胞・分子ネットワークの解明を目指しています。
具体的には、1)個々の臓器癌の特徴的な病理像(多段階発癌、浸潤・転移)の詳細な臨床病理解析、2)それら癌組織の網羅的遺伝子・タンパク発現解析と、in situ発現解析、3)Tissueマイクロアレイ、デジタルスライド、蛍光定量デジタルスライド技術の応用による形態分子情報の定量解析、4)高度免疫不全マウス同所移植によるin vivo機能解析モデルの確立と応用を行い、癌の新規診断マーカーあるいは治療標的の候補分子を効率よく同定、解析しています。中でも、難治癌の代表である肝癌・膵癌・肺癌・卵巣癌等を主な対象とし、これまでに、早期肝細胞癌診断マーカー(HSP70, CAP2)・早期肺腺癌診断マーカー(MRP3)の開発、膵癌神経浸潤モデルの確立と制御分子(CD74, SNCG)の同定、EMTの分子病理研究、肝細胞癌・基底細胞癌で過剰発現するWnt・Hh標的分子(GPR49/LGR5)の同定などを行ってきました。
代表的な研究の一つとして、肝細胞癌の多段階発癌モデルをご紹介します。
肝細胞癌の多段階発癌モデル

HCC, hepatocellular carcinoma, 肝細胞癌;
CLD, chronic liver disease, 慢性肝疾患; RN, regenerative nodule, 再生結節;
DN, dysplastic nodule, 異型結節; N/N, nodule-in-nodule, 結節内結節
肝細胞癌の大半は、慢性障害肝(ウイルス性肝炎、アルコール性・非アルコール性肝障害等)を背景として発生します。癌になる前の段階(異型結節)や既存の構造を置き換えるように増生する癌(早期肝細胞癌)から結節内結節(早期肝細胞癌から進行肝細胞癌に移行つつある状態)を経て進行肝細胞癌となっていくことが知られています。こうしたモデルを多段階発癌モデルといいます。肝臓は癌の領域が比較的わかりやすいため、癌の評価が他臓器よりも容易です。こうした特徴を活かし、次のような研究を行っています。
(Jpn J Clin Oncol 40(9):891-896, 2010より一部改変して転載)

多段階発現モデルを用いると様々なことが分かってきます。写真左は結節内結節の肝細胞癌の顕微鏡写真で、非癌部・早期肝細胞癌・進行肝細胞癌が含まれています(それぞれ組織像が異なっています)。各段階の組織を採取して網羅的遺伝子解析を行いました。
例えば、非癌部と癌部(特に早期肝細胞癌)を比較したところ、HSP70・CAP2・Bmi-1等の遺伝子が癌部で高く発現していることがわかりました。研究を進めたところ、これらの遺伝子に対応した分子が癌を診断するのに役立つことが分かったため、診断マーカーや悪性度診断に応用されています.
また、早期肝細胞癌と進行肝細胞癌の部分を比較したところ、p53やCK19等の遺伝子が進行肝細胞癌で高く発現することがあることがわかりました。このような遺伝子の発現が癌の悪性度(浸潤性が強い、転移しやすい、再発しやすい等)にどのように関わっているのか、そのメカニズムを現在研究中です。
(Jpn J Clin Oncol 40(9):891-896, 2010より一部改変して転載)

進行癌、早期癌、背景肝におけるH&E像および同部における各種マーカーの免疫染色所見です。慢性障害肝→早期肝細胞癌→進行肝細胞癌と見ていくと、免疫染色の染色結果が異なることが見て取れます。HSP70やCAP-2は早期肝細胞癌の段階から段階的に発現の増加が認められますが、Bmi-1は早期肝細胞癌の段階で特に発現が高い傾向があります。一方、p53やCK19については多段階発癌過程の後期に発現異常を認めることが多いです。
(Jpn J Clin Oncol 40(9):891-896, 2010より一部改変して転載)
研究成果
2021年
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尾島英知、田中伸哉 (編集)
病理と臨床39巻9号2021年 9月発行 文光堂
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【病理医が知っておくべき法令や指針】『経験談 証拠保全を受けた病理解剖症例の経験』 病理と臨床39巻9号 Page911-913(2021.09)
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2020年
Inter-muscle differences in modulation of motor evoked potentials and posterior root-muscle reflexes evoked from lower-limb muscles during agonist and antagonist muscle contractions.Saito A, Nakagawa K, Masugi Y, Nakazawa K
Experimental brain research 2020年11月
First Successful Delivery after Uterus Transplantation in MHC-Defined Cynomolgus Macaques.
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Journal of clinical medicine 9 ( 11 ) 2020年11月
Surgery for colloid carcinoma of the pancreas with portal vein tumor thrombus: a case report.
Udagawa D, Shimazu M, Sakuragawa T, Maruyama S, Uchi Y, Miura E, Masugi Y, Sakamoto M
Surgical case reports 6 ( 1 ) 252 2020年10月
Experimental techniques for the development of a uterus transplantation model in cynomolgus macaques.Kisu I, Banno K, Obara H, Kato Y, Yamada Y, Matsubara K, Matoba Y, Adachi M, Emoto K, Masugi Y, Saiki Y, Ishigaki H, Itagaki I, Kawamoto I, Iwatani C, Nakagawa T, Murase M, Tsuchiya H, Nakagawa K, Shiina T, Aoki D
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Telomerase reverse transcriptase (TERT) promoter mutation correlated with intratumoral heterogeneity in hepatocellular carcinoma
Kwa W.T., Effendi K., Yamazaki K., Kubota N., Hatano M., Ueno A., Masugi Y., Sakamoto M.
Pathology International 70 ( 9 ) 624 - 632 2020年09月
O-Glycan-Altered Extracellular Vesicles: A Specific Serum Marker Elevated in Pancreatic Cancer.
Yokose T, Kabe Y, Matsuda A, Kitago M, Matsuda S, Hirai M, Nakagawa T, Masugi Y, Hishiki T, Nakamura Y, Shinoda M, Yagi H, Abe Y, Oshima G, Hori S, Nakano Y, Honda K, Kashiro A, Morizane C, Nara S, Kikuchi S, Shibahara T, Itonaga M, Ono M, Minegishi N, Koshiba S, Yamamoto M, Kuno A, Handa H, Sakamoto M, Suematsu M, Kitagawa Y
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Scientific reports 10 ( 1 ) 13910 2020年08月
Urgent distal pancreatectomy for intraperitoneal hemorrhage due to the spontaneous rupture of a pancreatic metastatic tumor from synovial sarcoma: a case report.
Yokose T, Kitago M, Oshima G, Abe K, Masugi Y, Miura E, Shinoda M, Yagi H, Abe Y, Hori S, Matsusaka Y, Endo Y, Toyama K, Okuda S, Kitagawa Y
BMC surgery 20 ( 1 ) 175 2020年08月
Insulin-Like Growth Factor-1 Receptor Expression and Disease Recurrence and Survival in Patients with Resected Pancreatic Ductal Adenocarcinoma.
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Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 29 ( 8 ) 1586 - 1595 2020年08月
A case of pancreatic hamartoma with characteristic radiological findings: radiological-pathological correlation
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Combination of KRAS and SMAD4 mutations in formalin-fixed paraffin-embedded tissues as a biomarker for pancreatic cancer
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Cancer Science 111 ( 6 ) 2174 - 2182 2020年06月
Usefulness of 18 F-fluorodeoxyglucose positron emission tomography/computed tomography for predicting the prognosis and treatment response of neoadjuvant therapy for pancreatic ductal adenocarcinoma
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Cancer Medicine (Cancer Medicine) 9 ( 12 ) 4059 - 4068 2020年06月
Upregulation of cyclase-associated actin cytoskeleton regulatory protein 2 in epithelial ovarian cancer correlates with aggressive histologic types and worse outcomes
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Japanese Journal of Clinical Oncology 50 ( 6 ) 643 - 652 2020年05月
Association of autophagy status with amount of Fusobacterium nucleatum in colorectal cancer
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Journal of Pathology 250 ( 4 ) 397 - 408 2020年04月
Clinicopathological features of hepatocellular carcinoma with fatty change: Tumors with macrovesicular steatosis have better prognosis and aberrant expression patterns of perilipin and adipophilin
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Discovery of Pancreatic Ductal Adenocarcinoma-Related Aberrant Glycosylations: A Multilateral Approach of Lectin Microarray-Based Tissue Glycomic Profiling With Public Transcriptomic Datasets
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Serum Krebs von den Lungen-6 level in the disease progression and treatment of Mycobacterium avium complex lung disease
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Respirology (Respirology) 26 ( 1 ) 112 - 119 2020年
A case of intrahepatic cholangiocellular carcinoma due to thorotrast deposition, well-controlled by radiofrequency ablation therapy
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Acta Hepatologica Japonica 61 ( 5 ) 262 - 269 2020年
Blocking VCAM-1 inhibits pancreatic tumour progression and cancer-associated thrombosis/thromboembolism
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Gut (Gut) 2020年
Decreased αGlcNAc glycosylation in biliary tract cancer progression from BilIN to invasive adenocarcinoma
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CANCER SCIENCE 2020年10月
Diffuse MIST1 expression and decreased αGlcNAc glycosylation on MUC6 are distinct hallmark for gastric neoplasms exhibiting oxyntic gland differentiation
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HISTOPATHOLOGY 77 ( 3 ) 413 2020年09月
Association of glomerular DNA damage and DNA methylation with one-year eGFR decline in IgA nephropathy
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Scientific Reports (Scientific Reports) 10 ( 1 ) 2020年12月
Evaluation of Gleason Grade Group 5 in a Contemporary Prostate Cancer Grading System and Literature Review
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Clinical Genitourinary Cancer 19 ( 1 ) 69 - 75.e5 2020年
The Newly Described Filigree Pattern Is an Expansion of the Micropapillary Adenocarcinoma Concept Rather Than a Proposed New Subtype
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Role of CC chemokine receptor 9 in the progression of murine and human non-alcoholic steatohepatitis
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Imiquimod-induced dermatitis impairs thymic tolerance of autoreactive CD4+ T cells to desmoglein 3
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IL-6 and G-CSF production resulting from lung cancer in an HIV patient
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Three distinct stroma types in human pancreatic cancer identified by image analysis of fibroblast subpopulations and collagen
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Incidentally detected microcystic serous cystadenoma of the pancreas with splenic invasion: a case report and literature review
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Pre-hepatectomy type IV collagen 7S predicts post-hepatectomy liver failure and recoveryIshii M., Itano O., Shinoda M., Kitago M., Abe Y., Hibi T., Yagi H., Takeuchi A., Tsujikawa H., Abe T., Kitagawa Y.
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Effectiveness of color correction on the quantitative analysis of histopathological
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Steatotic and nonsteatotic scirrhous hepatocellular carcinomas reveal distinct
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Establishment of Patient-Derived Organoids and Drug Screening for Biliary
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Monoclonal antibody therapies in multiple myeloma: a challenge to develop
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Combined Genetic and Chromosomal Characterization of Wilms Tumors Identifies
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Characterization of spatial distribution of tumor-infiltrating CD8 + T
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Pathogenesis of multiple pancreatic cancers involves multicentric carcinogenesis
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Activation of ERK Is Associated with Hepatocellular Carcinoma with Aggressive
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Clinical and Endoscopic Characteristics of Pyogenic Granuloma in the Small
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Long-Term Outcome and Rejection After Allogeneic Uterus Transplantation
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Efficacy and safety of preoperative 5-fluorouracil, cisplatin, and mitomycin
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Macrophage migration inhibitory factor-CD74 interaction regulates the expression
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Calcium intake and risk of colorectal cancer according to tumor-infiltrating
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Smoking and risk of colorectal cancer sub-classified by tumor-infiltrating
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Non-invasive liver fibrosis assessment correlates with collagen and elastic
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αGlcNAc and its catalyst α4GnT are diagnostic and prognostic markers in
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Analysis of A4gnt Knockout Mice Reveals an Essential Role for Gastric Sulfomucins
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Maternal undernutrition aggravates renal tubular necrosis and interstitial
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Acute Interstitial Nephritis With Karyomegalic Epithelial Cells After Nivolumab
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A grading system that predicts the risk of dialysis induction in IgA nephropathy
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N., Hirano K., Matsushima M., Yokoo T., Horikoshi S., Suzuki Y., Yasuda
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Prediction of extraprostatic extension by MRI tumor contact length: difference
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T., Kosaka T., Mizuno R., Kikuchi E., Oya M., Jinzaki M.Prostate Cancer
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Predicting spread through air spaces (STAS) preoperatively: Can imaging
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Journal of Thoracic Disease 11 ( Suppl 15 ) S1938 - S1941 2019年
Contiguous Metastasis of Pulmonary Adenocarcinoma to Meningioma
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Journal of Neurological Surgery, Part A: Central European Neurosurgery
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Plasmacytoid dendritic cells protect against immune-mediated acute liver
injury via IL-35
Koda Y., Nakamoto N., Chu P., Ugamura A., Mikami Y., Teratani T., Tsujikawa
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Diffuse and canalicular patterns of glypican-3 expression reflect malignancy
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FDG-PET/CTの集積で診断され術中の局所診断に苦慮した非機能性膵神経内分泌腫瘍(PNET)の1切除例 病変の術中検出限界、ピットフォールについて
竹村 裕介, 北郷 実, 板野 理, 篠田 昌宏, 八木 洋, 阿部 雄太, 大島 剛, 堀 周太郎, 藤田 優裕, 益田 悠貴, 久保田 直人,
辻川 華子, 川井田 みほ, 北川 雄光膵臓 (日本膵臓学会) 34 ( 1 ) 22 - 29 2019年02月
Clinical value of 3D SPECT/CT imaging for assessing jaw bone invasion in
oral cancer patients
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Shiba H., Jinzaki M., Kawana H., Nakagawa T
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Living donor liver re-transplantation for recurrent hepatoblastoma in the
liver graft following complete eradication of peritoneal metastases under
indocyanine green fluorescence imaging
Takahashi N., Yamada Y., Hoshino K., Kawaida M., Mori T., Abe K., Fujimura
T., Matsubara K., Hibi T., Shinoda M., Obara H., Isshiki K., Shima H.,
Shimada H., Kameyama K., Fuchimoto Y., Kitagawa Y., Kuroda T
Cancers 11 ( 5 ) 2019年05月
Successful resection of pancreatic metastasis from oesophageal squamous
cell carcinoma: a case report and review of the literature
Koizumi W., Kitago M., Shinoda M., Yagi H., Abe Y., Oshima G., Hori S.,
Inomata K., Kawakubo H., Kawaida M., Kitagawa Y.
BMC Cancer 19 ( 1 ) 2019年04月
Hysteroscopic Photodynamic Diagnosis Using 5-Aminolevulinic Acid: A High-Sensitivity
Diagnostic Method for Uterine Endometrial Malignant Diseases
Matoba Y., Banno K., Kisu I., Kobayashi Y., Tsuji K., Nagai S., Yamagami
W., Nakamura M., Tominaga E., Kawaida M., Aoki D.
Journal of Minimally Invasive Gynecology 2019年
Colon perforation due to antigenemia-negative cytomegalovirus gastroenteritis
after liver transplantation: A case report and review of literatureYokose
T., Obara H., Shinoda M., Nakano Y., Kitago M., Yagi H., Abe Y., Yamada
Y., Matsubara K., Oshima G., Hori S., Ibuki S., Higashi H., Masuda Y.,
Hayashi M., Mori T., Kawaida M., Fujimura T., Hoshino K., Kameyama K.,
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World Journal of Gastroenterology 25 ( 15 ) 1899 - 1906 2019年
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Accuracy of non-invasive scoring systems for diagnosing non-alcoholic steatohepatitis-related
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Itoh Y., Seko Y., Shima T., Nakajima T., Mizuno K., Kawamura Y., Akuta
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Hepatology Research 48 ( 13 ) 1099 - 1107 2018年12月
Evaluation of pancreatic fibrosis with acoustic radiation force impulse
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Fujita Y., Kitago M., Abe T., Itano O., Shinoda M., Abe Y., Yagi H., Hibi
T., Ishii M., Nakano Y., Okuma K., Hashimoto M., Takeuchi A., Masugi Y.,
Jinzaki M., Sakamoto M., Kitagawa Y.
Pancreas 47 ( 10 ) 1277 - 1282 2018年11月
CD26 is a potential therapeutic target by humanized monoclonal antibody
for the treatment of multiple myeloma
Nishida H., Hayashi M., Morimoto C., Sakamoto M., Yamada T.
Blood Cancer Journal 8 ( 11 ) 2018年11月
Immunohistochemical visualization of the signature of activated Hedgehog
signaling pathway in cutaneous epithelial tumors
Tanese K., Emoto K., Kubota N., Fukuma M., Sakamoto M
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Landscape of immune microenvironment in hepatocellular carcinoma and its
additional impact on histological and molecular classification
Kurebayashi Y., Ojima H., Tsujikawa H., Kubota N., Maehara J., Abe Y.,
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Hepatology 68 ( 3 ) 1025 - 1041 2018年09月
cHCC-CCA: Consensus terminology for primary liver carcinomas with both
hepatocytic and cholangiocytic differentation
Brunt E., Aishima S., Clavien P., Fowler K., Goodman Z., Gores G., Gouw
A., Kagen A., Klimstra D., Komuta M., Kondo F., Miksad R., Nakano M., Nakanuma
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Hepatology 68 ( 1 ) 113 - 126 2018年07月
Bone-Targeted Agents in Multiple Myeloma
Hiroko Nishida
Hematology Reports. 2018; 10 (12-16).
Novel method for DNA methylation analysis using high-performance liquid
chromatography and its clinical application
Yotani T., Yamada Y., Arai E., Tian Y., Gotoh M., Komiyama M., Fujimoto
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Cancer Science 109 ( 5 ) 1690 - 1700 2018年05月
Concurrent presentation of an intraductal tubulopapillary neoplasm and
intraductal papillary mucinous neoplasm in the branch duct of the pancreas,
with a superior mesenteric artery aneurysm: A case reportInomata K., Kitago
M., Obara H., Fujii-Nishimura Y., Shinoda M., Yagi H., Abe Y., Hibi T.,
Matsubara K., Oshima G., Sekimoto Y., Inoue M., Itano O., Sakamoto M.,
Kitagawa Y.
World Journal of Surgical Oncology 16 ( 1 ) 2018年04月
Mesenchymal–epithelial transition of pancreatic cancer cells at perineural
invasion sites is induced by Schwann cells
Fujii-Nishimura Y., Yamazaki K., Masugi Y., Douguchi J., Kurebayashi Y.,
Kubota N., Ojima H., Kitago M., Shinoda M., Hashiguchi A., Sakamoto M
Pathology International 68 ( 4 ) 214 - 223 2018年04月
Impact of resection and ablation for single hypovascular hepatocellular
carcinoma ≤2 cm analysed with propensity score weighting
Takayasu K., Arii S., Sakamoto M., Matsuyama Y., Kudo M., Kaneko S., Nakashima
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The challenges and promises of quanifying liver fibrosis and steatosis
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Hatano M., Abe T., Hashiguchi A., Sakamoto M.Acta Hepatologica Japonica
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Induction of differentiation of intrahepatic cholangiocarcinoma cells to
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Scientific Reports 8 ( 1 ) 2018年12月
Epigenome mapping of human normal purified hepatocytes: Personal epigenome
variation and genome-epigenome correlation
Arai E., Miura F., Totoki Y., Yamashita S., Tian Y., Gotoh M., Ojima H.,
Nakagawa H., Takahashi Y., Nakamura H., Hama N., Kato M., Kimura H., Suzuki
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PI3K-mTOR pathway identified as a potential therapeutic target in biliary
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Japanese Journal of Clinical Oncology 48 ( 4 ) 396 - 399 2018年04月
The Japanese Society of Pathology Guidelines on the handling of pathological
tissue samples for genomic research: Standard operating procedures based
on empirical analyses
Kanai Y., Nishihara H., Miyagi Y., Tsuruyama T., Taguchi K., Katoh H.,
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The potentiality of laparoscopic partial liver excisional biopsy using
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A curative treatment strategy using tumor debulking surgery combined with
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Preoperative diagnosis of clear cell sarcoma of the kidney by detection
of BCOR internal tandem duplication in circulating tumor DNA
Ueno-Yokohata H., Okita H., Nakasato K., Hishiki T., Shirai R., Tsujimoto
S., Osumi T., Yoshimura S., Yamada Y., Shioda Y., Kiyotani C., Terashima
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Outcome of renal tumors registered in Japan Wilms Tumor Study-2 (JWiTS-2):
A report from the Japan Children's Cancer Group (JCCG)
Koshinaga T., Takimoto T., Oue T., Okita H., Tanaka Y., Nozaki M., Tsuchiya
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Pediatric Blood and Cancer 65 ( 7 ) e27056 2018年04月
Tumour CD274 (PD-L1) expression and T cells in colorectal cancer
Masugi, Y., Nishihara, R., Yang, J., Mima, K., da Silva, A., Shi, Y., Inamura,
K., Cao, Y., Song, M., Nowak, J. A., Liao, X., Nosho, K., Chan, A. T.,
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Aspirin Use and Colorectal Cancer Survival According to Tumor CD274 (Programmed
Cell Death 1 Ligand 1) Expression Status
Hamada, T., Cao, Y., Qian, Z. R., Masugi, Y., Nowak, J. A., Yang, J., Song,
M., Mima, K., Kosumi, K., Liu, L., Shi, Y., da Silva, A., Gu, M., Li, W.,
Keum, N., Zhang, X., Wu, K., Meyerhardt, J. A., Giovannucci, E. L., Giannakis,
M., Rodig, S. J., Freeman, G. J., Nevo, D., Wang, M., Chan, A. T., Fuchs,
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Indication for resection and possibility of observation for intraductal
papillary mucinous neoplasm with high-risk stigmata.
Abe K, Kitago M, Masugi Y, Iwasaki E, Yagi H, Abe Y, Hasegawa Y, Fukuhara
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Peritoneal dissemination of pancreatic cancer caused by endoscopic ultrasound-guided
fine needle aspiration: A case report and literature review.
Kojima H, Kitago M, Iwasaki E, Masugi Y, Matsusaka Y, Yagi H, Abe Y, Hasegawa
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The Amount of Bifidobacterium Genus in Colorectal Carcinoma Tissue in Relation
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Kosumi K., Hamada T., Koh H., Borowsky J., Bullman S., Twombly T., Nevo
D., Masugi Y., Liu L., da Silva A., Chen Y., Du C., Gu M., Li C., Li W.,
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Evaluation of pancreatic fibrosis with acoustic radiation force impulse
imaging and automated quantification of pancreatic tissue components
Fujita Y., Kitago M., Abe T., Itano O., Shinoda M., Abe Y., Yagi H., Hibi
T., Ishii M., Nakano Y., Okuma K., Hashimoto M., Takeuchi A., Masugi Y.,
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Fusobacterium nucleatum in Colorectal Cancer Relates to Immune Response
Differentially by Tumor Microsatellite Instability Status
Hamada T., Zhang X., Mima K., Bullman S., Sukawa Y., Nowak J., Kosumi K.,
Masugi Y., Twombly T., Cao Y., Song M., Liu L., da Silva A., Shi Y., Gu
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Vitamin D status after colorectal cancer diagnosis and patient survival
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Hamada T., Liu L., Nowak J., Mima K., Cao Y., Ng K., Twombly T., Song M.,
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Liver Fibrosis Markers Improve Prediction of Outcome in Non-Acetaminophen-Associated
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Characterization of the Neuroendocrine Tumor Immune MicroenvironmentDa
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Continuity of transcriptomes among colorectal cancer subtypes based on
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Quantitative assessment of liver fibrosis reveals a nonlinear association
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Masugi Y, Abe T, Tsujikawa H, Effendi K, Hashiguchi A, Abe M, Imai Y, Hino
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