Identification of the novel deletion-type PML-RARA mutation associated with the retinoic acid resistance in acute promyelocytic leukemia
All-trans retinoic acid (ATRA) and arsenic trioxide (ATO) are essential for acute promyelocytic leukemia (APL) treatment. It has been reported that mutations in PML-RARA confer resistance to ATRA and ATO, and are associated with poor prognosis. Although most PML-RARA mutations were point mutations,...
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Published in | PloS one Vol. 13; no. 10; p. e0204850 |
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Abstract | All-trans retinoic acid (ATRA) and arsenic trioxide (ATO) are essential for acute promyelocytic leukemia (APL) treatment. It has been reported that mutations in PML-RARA confer resistance to ATRA and ATO, and are associated with poor prognosis. Although most PML-RARA mutations were point mutations, we identified a novel seven amino acid deletion mutation (p.K227_T233del) in the RARA region of PML-RARA in a refractory APL patient. Here, we analyzed the evolution of the mutated clone and demonstrated the resistance of the mutated clone to retinoic acid (RA). Mutation analysis of PML-RARA was performed using samples from a chemotherapy- and ATRA-resistant APL patient, and the frequencies of mutated PML-RARA transcript were analyzed by targeted deep sequencing. To clarify the biological significance of the identified PML-RARA mutations, we analyzed the ATRA-induced differentiation and PML nuclear body formation in mutant PML-RARA-transduced HL-60 cells. At molecular relapse, the p.K227_T233del deletion and the p.R217S point-mutation in the RARA region of PML-RARA were identified, and their frequencies increased after re-induction therapy with another type of retinoiec acid (RA), tamibarotene. In deletion PML-RARA-transduced cells, the CD11b expression levels and NBT reducing ability were significantly decreased compared with control cells and the formation of PML nuclear bodies was rarely observed after RA treatment. These results indicate that this deletion mutation was closely associated with the disease progression during RA treatment. |
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AbstractList | All-trans retinoic acid (ATRA) and arsenic trioxide (ATO) are essential for acute promyelocytic leukemia (APL) treatment. It has been reported that mutations in PML-RARA confer resistance to ATRA and ATO, and are associated with poor prognosis. Although most PML-RARA mutations were point mutations, we identified a novel seven amino acid deletion mutation (p.K227_T233del) in the RARA region of PML-RARA in a refractory APL patient. Here, we analyzed the evolution of the mutated clone and demonstrated the resistance of the mutated clone to retinoic acid (RA). Mutation analysis of PML-RARA was performed using samples from a chemotherapy- and ATRA-resistant APL patient, and the frequencies of mutated PML-RARA transcript were analyzed by targeted deep sequencing. To clarify the biological significance of the identified PML-RARA mutations, we analyzed the ATRA-induced differentiation and PML nuclear body formation in mutant PML-RARA-transduced HL-60 cells. At molecular relapse, the p.K227_T233del deletion and the p.R217S point-mutation in the RARA region of PML-RARA were identified, and their frequencies increased after re-induction therapy with another type of retinoiec acid (RA), tamibarotene. In deletion PML-RARA-transduced cells, the CD11b expression levels and NBT reducing ability were significantly decreased compared with control cells and the formation of PML nuclear bodies was rarely observed after RA treatment. These results indicate that this deletion mutation was closely associated with the disease progression during RA treatment. All- trans retinoic acid (ATRA) and arsenic trioxide (ATO) are essential for acute promyelocytic leukemia (APL) treatment. It has been reported that mutations in PML-RARA confer resistance to ATRA and ATO, and are associated with poor prognosis. Although most PML-RARA mutations were point mutations, we identified a novel seven amino acid deletion mutation (p.K227_T233del) in the RARA region of PML-RARA in a refractory APL patient. Here, we analyzed the evolution of the mutated clone and demonstrated the resistance of the mutated clone to retinoic acid (RA). Mutation analysis of PML-RARA was performed using samples from a chemotherapy- and ATRA-resistant APL patient, and the frequencies of mutated PML-RARA transcript were analyzed by targeted deep sequencing. To clarify the biological significance of the identified PML-RARA mutations, we analyzed the ATRA-induced differentiation and PML nuclear body formation in mutant PML-RARA -transduced HL-60 cells. At molecular relapse, the p.K227_T233del deletion and the p.R217S point-mutation in the RARA region of PML-RARA were identified, and their frequencies increased after re-induction therapy with another type of retinoiec acid (RA), tamibarotene. In deletion PML-RARA -transduced cells, the CD11b expression levels and NBT reducing ability were significantly decreased compared with control cells and the formation of PML nuclear bodies was rarely observed after RA treatment. These results indicate that this deletion mutation was closely associated with the disease progression during RA treatment. |
Audience | Academic |
Author | Ishikawa, Yuichi Hirano, Daiki Hattori, Hikaru Miyao, Kotaro Yamaguchi, Yohei Kiyoi, Hitoshi Akashi, Akimi Ushijima, Yoko Kawashima, Naomi Matsushita, Tadashi Adachi, Yoshiya Harada, Yasuhiko Terakura, Seitaro Nishida, Tetsuya |
AuthorAffiliation | 1 Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan 2 Department of Medical Technique, Nagoya University Hospital, Nagoya, Japan European Institute of Oncology, ITALY 3 Department of Transfusion Medicine, Nagoya University Hospital, Nagoya, Japan |
AuthorAffiliation_xml | – name: 3 Department of Transfusion Medicine, Nagoya University Hospital, Nagoya, Japan – name: 1 Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – name: 2 Department of Medical Technique, Nagoya University Hospital, Nagoya, Japan – name: European Institute of Oncology, ITALY |
Author_xml | – sequence: 1 givenname: Hikaru surname: Hattori fullname: Hattori, Hikaru organization: Department of Medical Technique, Nagoya University Hospital, Nagoya, Japan – sequence: 2 givenname: Yuichi orcidid: 0000-0001-6024-6617 surname: Ishikawa fullname: Ishikawa, Yuichi organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 3 givenname: Naomi surname: Kawashima fullname: Kawashima, Naomi organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 4 givenname: Akimi surname: Akashi fullname: Akashi, Akimi organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 5 givenname: Yohei surname: Yamaguchi fullname: Yamaguchi, Yohei organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 6 givenname: Yasuhiko surname: Harada fullname: Harada, Yasuhiko organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 7 givenname: Daiki surname: Hirano fullname: Hirano, Daiki organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 8 givenname: Yoshiya surname: Adachi fullname: Adachi, Yoshiya organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 9 givenname: Kotaro surname: Miyao fullname: Miyao, Kotaro organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 10 givenname: Yoko surname: Ushijima fullname: Ushijima, Yoko organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 11 givenname: Seitaro surname: Terakura fullname: Terakura, Seitaro organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 12 givenname: Tetsuya surname: Nishida fullname: Nishida, Tetsuya organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan – sequence: 13 givenname: Tadashi surname: Matsushita fullname: Matsushita, Tadashi organization: Department of Transfusion Medicine, Nagoya University Hospital, Nagoya, Japan – sequence: 14 givenname: Hitoshi surname: Kiyoi fullname: Kiyoi, Hitoshi organization: Department of Hematology and Oncology, Nagoya University Graduate School of Medicine, Nagoya, Japan |
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CitedBy_id | crossref_primary_10_1016_j_ctarc_2020_100284 crossref_primary_10_1016_j_rpor_2019_12_026 crossref_primary_10_3390_cancers13205055 crossref_primary_10_3390_ijms20143559 crossref_primary_10_3390_cancers15143535 crossref_primary_10_18632_aging_203166 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: We have the following interests: Hitoshi Kiyoi received research funding, which is unrelated to this study, from Chugai Pharmaceutical Co. Ltd., Bristol-Myers Squibb, Kyowa Hakko Kirin Co. Ltd., Zenyaku Kogyo Co. Ltd., FUJIFILM Corporation, Nippon Boehringer Ingelheim Co. Ltd., Astellas Pharma Inc. and Celgene Corporation, consulting fees from Astellas Pharma Inc. and Daiichi Sankyo Co. Ltd., and honoraria from Bristol-Myers Squibb and Pfizer Japan Inc. The other authors have declared that no competing interests exist. This does not alter our adherence to PLOS ONE policies on sharing data and materials. |
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Snippet | All-trans retinoic acid (ATRA) and arsenic trioxide (ATO) are essential for acute promyelocytic leukemia (APL) treatment. It has been reported that mutations... All- trans retinoic acid (ATRA) and arsenic trioxide (ATO) are essential for acute promyelocytic leukemia (APL) treatment. It has been reported that mutations... |
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SubjectTerms | Acid resistance Acids Acute myelocytic leukemia Acute promyeloid leukemia Amino acids Analysis Arsenic Arsenic trioxide Biology and Life Sciences Blood CD11b antigen CD11b Antigen - genetics Cell Line, Tumor Chemotherapy Clonal deletion Development and progression Disease Progression Down-Regulation Drug resistance Drug Resistance, Neoplasm Drug therapy Female Gene deletion Gene Expression Regulation, Neoplastic - drug effects Gene mutation Genetic aspects Hematology HL-60 Cells Humans Induction therapy Leukemia Leukemia, Promyelocytic, Acute - drug therapy Leukemia, Promyelocytic, Acute - genetics Lymphocyte receptors Medical prognosis Medical research Medical treatment Medicine Medicine and Health Sciences Mutation Oncogene Proteins, Fusion - genetics Oncology Patient outcomes Patients Physiological aspects Point Mutation Prognosis Promyeloid leukemia Research and Analysis Methods Retinoic acid Risk factors Sequence Deletion Transcription Tretinoin Tretinoin - pharmacology University graduates |
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Title | Identification of the novel deletion-type PML-RARA mutation associated with the retinoic acid resistance in acute promyelocytic leukemia |
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