Somatic Mutations and Clonal Hematopoiesis in Aplastic Anemia

Although aplastic anemia is responsive to immunosuppressive therapy, small subpopulations of hematopoietic cells with clonal gene mutations may exist, and different sets of mutations show distinct clinical behavior and response to therapy. Acquired aplastic anemia is caused by immune-mediated destru...

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Published inThe New England journal of medicine Vol. 373; no. 1; pp. 35 - 47
Main Authors Yoshizato, Tetsuichi, Dumitriu, Bogdan, Hosokawa, Kohei, Makishima, Hideki, Yoshida, Kenichi, Townsley, Danielle, Sato-Otsubo, Aiko, Sato, Yusuke, Liu, Delong, Suzuki, Hiromichi, Wu, Colin O, Shiraishi, Yuichi, Clemente, Michael J, Kataoka, Keisuke, Shiozawa, Yusuke, Okuno, Yusuke, Chiba, Kenichi, Tanaka, Hiroko, Nagata, Yasunobu, Katagiri, Takamasa, Kon, Ayana, Sanada, Masashi, Scheinberg, Phillip, Miyano, Satoru, Maciejewski, Jaroslaw P, Nakao, Shinji, Young, Neal S, Ogawa, Seishi
Format Journal Article
LanguageEnglish
Published United States Massachusetts Medical Society 02.07.2015
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Online AccessGet full text
ISSN0028-4793
1533-4406
1533-4406
DOI10.1056/NEJMoa1414799

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Abstract Although aplastic anemia is responsive to immunosuppressive therapy, small subpopulations of hematopoietic cells with clonal gene mutations may exist, and different sets of mutations show distinct clinical behavior and response to therapy. Acquired aplastic anemia is caused by immune-mediated destruction of hematopoietic stem and progenitor cells. 1 CD34+ cells and early progenitors are uniformly reduced in aplastic anemia. 2 Bone marrow transplantation is curative, and patients may also have a response to immunosuppressive therapy. 3 , 4 With improved survival, the late development of myelodysplastic syndromes, acute myeloid leukemia (AML), or both has been noted in about 15% of patients and termed “clonal evolution.” 5 Although “clonal evolution” historically has been used to describe the development of cancer in patients with an immune disease, this term is a misnomer, since there is evidence of clonal hematopoiesis associated . . .
AbstractList Although aplastic anemia is responsive to immunosuppressive therapy, small subpopulations of hematopoietic cells with clonal gene mutations may exist, and different sets of mutations show distinct clinical behavior and response to therapy. Acquired aplastic anemia is caused by immune-mediated destruction of hematopoietic stem and progenitor cells. 1 CD34+ cells and early progenitors are uniformly reduced in aplastic anemia. 2 Bone marrow transplantation is curative, and patients may also have a response to immunosuppressive therapy. 3 , 4 With improved survival, the late development of myelodysplastic syndromes, acute myeloid leukemia (AML), or both has been noted in about 15% of patients and termed “clonal evolution.” 5 Although “clonal evolution” historically has been used to describe the development of cancer in patients with an immune disease, this term is a misnomer, since there is evidence of clonal hematopoiesis associated . . .
In patients with acquired aplastic anemia, destruction of hematopoietic cells by the immune system leads to pancytopenia. Patients have a response to immunosuppressive therapy, but myelodysplastic syndromes and acute myeloid leukemia develop in about 15% of the patients, usually many months to years after the diagnosis of aplastic anemia. We performed next-generation sequencing and array-based karyotyping using 668 blood samples obtained from 439 patients with aplastic anemia. We analyzed serial samples obtained from 82 patients. Somatic mutations in myeloid cancer candidate genes were present in one third of the patients, in a limited number of genes and at low initial variant allele frequency. Clonal hematopoiesis was detected in 47% of the patients, most frequently as acquired mutations. The prevalence of the mutations increased with age, and mutations had an age-related signature. DNMT3A-mutated and ASXL1-mutated clones tended to increase in size over time; the size of BCOR- and BCORL1-mutated and PIGA-mutated clones decreased or remained stable. Mutations in PIGA and BCOR and BCORL1 correlated with a better response to immunosuppressive therapy and longer and a higher rate of overall and progression-free survival; mutations in a subgroup of genes that included DNMT3A and ASXL1 were associated with worse outcomes. However, clonal dynamics were highly variable and might not necessarily have predicted the response to therapy and long-term survival among individual patients. Clonal hematopoiesis was prevalent in aplastic anemia. Some mutations were related to clinical outcomes. A highly biased set of mutations is evidence of Darwinian selection in the failed bone marrow environment. The pattern of somatic clones in individual patients over time was variable and frequently unpredictable. (Funded by Grant-in-Aid for Scientific Research and others.).
BACKGROUNDIn patients with acquired aplastic anemia, destruction of hematopoietic cells by the immune system leads to pancytopenia. Patients have a response to immunosuppressive therapy, but myelodysplastic syndromes and acute myeloid leukemia develop in about 15% of the patients, usually many months to years after the diagnosis of aplastic anemia.METHODSWe performed next-generation sequencing and array-based karyotyping using 668 blood samples obtained from 439 patients with aplastic anemia. We analyzed serial samples obtained from 82 patients.RESULTSSomatic mutations in myeloid cancer candidate genes were present in one third of the patients, in a limited number of genes and at low initial variant allele frequency. Clonal hematopoiesis was detected in 47% of the patients, most frequently as acquired mutations. The prevalence of the mutations increased with age, and mutations had an age-related signature. DNMT3A-mutated and ASXL1-mutated clones tended to increase in size over time; the size of BCOR- and BCORL1-mutated and PIGA-mutated clones decreased or remained stable. Mutations in PIGA and BCOR and BCORL1 correlated with a better response to immunosuppressive therapy and longer and a higher rate of overall and progression-free survival; mutations in a subgroup of genes that included DNMT3A and ASXL1 were associated with worse outcomes. However, clonal dynamics were highly variable and might not necessarily have predicted the response to therapy and long-term survival among individual patients.CONCLUSIONSClonal hematopoiesis was prevalent in aplastic anemia. Some mutations were related to clinical outcomes. A highly biased set of mutations is evidence of Darwinian selection in the failed bone marrow environment. The pattern of somatic clones in individual patients over time was variable and frequently unpredictable. (Funded by Grant-in-Aid for Scientific Research and others.).
Author Hosokawa, Kohei
Shiraishi, Yuichi
Chiba, Kenichi
Wu, Colin O
Sanada, Masashi
Ogawa, Seishi
Scheinberg, Phillip
Makishima, Hideki
Yoshizato, Tetsuichi
Katagiri, Takamasa
Tanaka, Hiroko
Miyano, Satoru
Sato-Otsubo, Aiko
Okuno, Yusuke
Maciejewski, Jaroslaw P
Liu, Delong
Clemente, Michael J
Kataoka, Keisuke
Nagata, Yasunobu
Sato, Yusuke
Shiozawa, Yusuke
Young, Neal S
Nakao, Shinji
Yoshida, Kenichi
Townsley, Danielle
Dumitriu, Bogdan
Kon, Ayana
Suzuki, Hiromichi
AuthorAffiliation 1 Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho, Kyoto-shi Sakyo-ku, Kyoto, 606-8501, Japan
2 Hematology Branch, National Heart, Lung and Blood Institute, Bethesda, United States
6 Laboratory of DNA Information Analysis, Human Genome Center, University of Tokyo, Japan
4 Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland, United States
5 Office of Biostatistics Research, National Heart, Lung and Blood Institute, Bethesda, United Sates
7 Department of Pediatrics, Graduate School of Medicine, Nagoya University, Japan
3 Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan
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– name: 2 Hematology Branch, National Heart, Lung and Blood Institute, Bethesda, United States
– name: 6 Laboratory of DNA Information Analysis, Human Genome Center, University of Tokyo, Japan
– name: 7 Department of Pediatrics, Graduate School of Medicine, Nagoya University, Japan
– name: 4 Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland, United States
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  fullname: Yoshizato, Tetsuichi
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
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  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
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  givenname: Kohei
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  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 4
  givenname: Hideki
  surname: Makishima
  fullname: Makishima, Hideki
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 5
  givenname: Kenichi
  surname: Yoshida
  fullname: Yoshida, Kenichi
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 6
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  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 7
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  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 8
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  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 9
  givenname: Delong
  surname: Liu
  fullname: Liu, Delong
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
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  surname: Suzuki
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  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
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  givenname: Colin O
  surname: Wu
  fullname: Wu, Colin O
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 12
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  surname: Shiraishi
  fullname: Shiraishi, Yuichi
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 13
  givenname: Michael J
  surname: Clemente
  fullname: Clemente, Michael J
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 14
  givenname: Keisuke
  surname: Kataoka
  fullname: Kataoka, Keisuke
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 15
  givenname: Yusuke
  surname: Shiozawa
  fullname: Shiozawa, Yusuke
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 16
  givenname: Yusuke
  surname: Okuno
  fullname: Okuno, Yusuke
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 17
  givenname: Kenichi
  surname: Chiba
  fullname: Chiba, Kenichi
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 18
  givenname: Hiroko
  surname: Tanaka
  fullname: Tanaka, Hiroko
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 19
  givenname: Yasunobu
  surname: Nagata
  fullname: Nagata, Yasunobu
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 20
  givenname: Takamasa
  surname: Katagiri
  fullname: Katagiri, Takamasa
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 21
  givenname: Ayana
  surname: Kon
  fullname: Kon, Ayana
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 22
  givenname: Masashi
  surname: Sanada
  fullname: Sanada, Masashi
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 23
  givenname: Phillip
  surname: Scheinberg
  fullname: Scheinberg, Phillip
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 24
  givenname: Satoru
  surname: Miyano
  fullname: Miyano, Satoru
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 25
  givenname: Jaroslaw P
  surname: Maciejewski
  fullname: Maciejewski, Jaroslaw P
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 26
  givenname: Shinji
  surname: Nakao
  fullname: Nakao, Shinji
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 27
  givenname: Neal S
  surname: Young
  fullname: Young, Neal S
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
– sequence: 28
  givenname: Seishi
  surname: Ogawa
  fullname: Ogawa, Seishi
  organization: From the Department of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto (T.Y., K.Y., A.S.-O., Y. Sato, H.S., K.K., Y. Shiozawa, Y.N., A.K., M.S., S.O.), Department of Cellular Transplantation Biology, Division of Cancer Medicine, Graduate School of Medical Sciences, Kanazawa University, Kanazawa (K.H., T.K., S.N.), Laboratory of DNA Information Analysis, Human Genome Center, Institute of Medical Science, University of Tokyo, Tokyo (Y. Shiraishi, K.C., H.T., S.M.), and the Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya (Y.O.) — all in Japan; the Hematology Branch (B.D., K.H., D.T., D.L., P.S., N.S.Y.) and Office of Biostatistics Research (C.O.W.), National Heart, Lung, and Blood Institute, Bethesda, MD; and the Department of Translational Hematology and Oncology Research, Taussig Cancer Institute, Cleveland Clinic, Cleveland (H.M., M.J.C., J.P.M.)
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26132940$$D View this record in MEDLINE/PubMed
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N.S.Y., and S.O. designed the study. B.D., K.H., T.K., M.C. and H.M. gathered the data. Experiments and data analysis were performed by T.Y., B.D., K.H., H.M., K.Y., A.S., D.L., C.W., K.K., Y. Sato, H.S., Y.N., Y. Shiozawa, T.K., A.K., M.C., M.S., J.M. S.N. and N.S.Y.. Specimens were provided by K.H., H.M., T.K. and M.C.. Bioinfomatical calculations were done by T.Y., D.L., C.W., A.S., Y. Sato, H.S., K.C., Y.O., H.T., Y. Shiozawa, Y. Shiraishi and S.M.. T.Y., P.S., B.D., N.S.Y., and S.O. wrote the first daft and revised the manuscript. N.S.Y. and S.O. are responsible for all the data and analyses and decided to publish the paper.
Shared first or last author
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Snippet Although aplastic anemia is responsive to immunosuppressive therapy, small subpopulations of hematopoietic cells with clonal gene mutations may exist, and...
In patients with acquired aplastic anemia, destruction of hematopoietic cells by the immune system leads to pancytopenia. Patients have a response to...
BackgroundIn patients with acquired aplastic anemia, destruction of hematopoietic cells by the immune system leads to pancytopenia. Patients have a response to...
BACKGROUNDIn patients with acquired aplastic anemia, destruction of hematopoietic cells by the immune system leads to pancytopenia. Patients have a response to...
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StartPage 35
SubjectTerms Acute myeloid leukemia
Age
Age Factors
Aged
Anemia
Anemia, Aplastic - blood
Anemia, Aplastic - genetics
Anemia, Aplastic - mortality
Aplastic anemia
Bone marrow
Cancer
Clone Cells
Erythrocytes
Female
Gene frequency
Hematopoiesis - genetics
Humans
Immune system
Immunosuppressive agents
Karyotyping
Leukemia, Myeloid, Acute - genetics
Male
Middle Aged
Mutation
Myelodysplastic syndrome
Myelodysplastic Syndromes - genetics
Myeloid leukemia
Pancytopenia
Polymorphism, Single Nucleotide
Risk Factors
Sequence Analysis, DNA
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