Exome sequencing identifies somatic mutations of DDX3X in natural killer/T-cell lymphoma
Zhu Chen, Sai-Juan Chen, Wei-Li Zhao and colleagues identify recurrent loss-of-function mutations in the RNA helicase gene DDX3X in 20% of subjects with natural killer/T-cell lymphoma (NKTCL) in their study. The results suggest that DDX3X acts as a tumor suppressor and that its inactivation leads to...
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| Published in | Nature genetics Vol. 47; no. 9; pp. 1061 - 1066 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.09.2015
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1061-4036 1546-1718 1546-1718 |
| DOI | 10.1038/ng.3358 |
Cover
| Abstract | Zhu Chen, Sai-Juan Chen, Wei-Li Zhao and colleagues identify recurrent loss-of-function mutations in the RNA helicase gene
DDX3X
in 20% of subjects with natural killer/T-cell lymphoma (NKTCL) in their study. The results suggest that
DDX3X
acts as a tumor suppressor and that its inactivation leads to poor clinical outcome.
Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56
+
and cytoCD3
+
lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations
1
. The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene
DDX3X
(21/105 subjects, 20.0%), tumor suppressors (
TP53
and
MGA
), JAK-STAT-pathway molecules (
STAT3
and
STAT5B
) and epigenetic modifiers (
MLL2
,
ARID1A
,
EP300
and
ASXL3
). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-κB and MAPK pathways. Clinically, patients with
DDX3X
mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL. |
|---|---|
| AbstractList | Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56(+) and cytoCD3(+) lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations. The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene DDX3X (21/105 subjects, 20.0%), tumor suppressors (TP53 and MGA), JAK-STAT-pathway molecules (STAT3 and STAT5B) and epigenetic modifiers (MLL2, ARID1A, EP300 and ASXL3). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-κB and MAPK pathways. Clinically, patients with DDX3X mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL.Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56(+) and cytoCD3(+) lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations. The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene DDX3X (21/105 subjects, 20.0%), tumor suppressors (TP53 and MGA), JAK-STAT-pathway molecules (STAT3 and STAT5B) and epigenetic modifiers (MLL2, ARID1A, EP300 and ASXL3). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-κB and MAPK pathways. Clinically, patients with DDX3X mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL. Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56(+) and cytoCD3(+) lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations. The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene DDX3X (21/105 subjects, 20.0%), tumor suppressors (TP53 and MGA), JAK-STAT-pathway molecules (STAT3 and STAT5B) and epigenetic modifiers (MLL2, ARID1A, EP300 and ASXL3). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-κB and MAPK pathways. Clinically, patients with DDX3X mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL. Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56^sup +^ and cytoCD3^sup +^ lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations1. The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene DDX3X (21/105 subjects, 20.0%), tumor suppressors (TP53 and MGA), JAK-STAT-pathway molecules (STAT3 and STAT5B) and epigenetic modifiers (MLL2, ARID1A, EP300 and ASXL3). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-?B and MAPK pathways. Clinically, patients with DDX3X mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL. Zhu Chen, Sai-Juan Chen, Wei-Li Zhao and colleagues identify recurrent loss-of-function mutations in the RNA helicase gene DDX3X in 20% of subjects with natural killer/T-cell lymphoma (NKTCL) in their study. The results suggest that DDX3X acts as a tumor suppressor and that its inactivation leads to poor clinical outcome. Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56 + and cytoCD3 + lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations 1 . The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene DDX3X (21/105 subjects, 20.0%), tumor suppressors ( TP53 and MGA ), JAK-STAT-pathway molecules ( STAT3 and STAT5B ) and epigenetic modifiers ( MLL2 , ARID1A , EP300 and ASXL3 ). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-κB and MAPK pathways. Clinically, patients with DDX3X mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL. Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of [CD56.sup.+] and cyto[CD3.sup.+] lymphocytes with aggressive clinical course, which is prevalent in Asian and South American populations (1). The molecular pathogenesis of NKTCL has largely remained elusive. We identified somatic gene mutations in 25 people with NKTCL by whole-exome sequencing and confirmed them in an extended validation group of 80 people by targeted sequencing. Recurrent mutations were most frequently located in the RNA helicase gene DDX3X (21/105 subjects, 20.0%), tumor suppressors (TP53 and MGA), JAK-STAT-pathway molecules (STAT3 and STAT5B) and epigenetic modifiers (MLL2, ARID1A, EP300 and ASXL3). As compared to wild-type protein, DDX3X mutants exhibited decreased RNA-unwinding activity, loss of suppressive effects on cell-cycle progression in NK cells and transcriptional activation of NF-κB and MAPK pathways. Clinically, patients with DDX3X mutations presented a poor prognosis. Our work thus contributes to the understanding of the disease mechanism of NKTCL. |
| Audience | Academic |
| Author | Yang, Lin-Hua Shi, Ju-Mei Wang, Li Pan, Chun-Ming Yan, Zi-Xun Chen, Fang-Yuan Zhang, Zi-Guan Xu, Lan Shen, Yang Ding, Hao Xue, Wen Dong, Ying Zhao, Wei-Li Hu, Yuan Wang, Zhao Chen, Sai-Juan Xie, Yin-Yin Sun, Zi-Min Zhang, Feng Peng, Zhi-Gang Yan, Jin-Song Meng, Guoyu Zhao, Xia Jiang, Lu Gu, Zhao-Hui Chen, Zhu Huang, Jin-Yan Cai, Chang-Ping Hu, Jian-Da Wang, Jian-Min Wang, Jin-Fen Hou, Jian Lu, Jing Zhou, Jian-Feng Li, Yang Liu, Yuan-Hua Shi, Jing-Yi Zheng, Zhong |
| Author_xml | – sequence: 1 givenname: Lu surname: Jiang fullname: Jiang, Lu organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 2 givenname: Zhao-Hui surname: Gu fullname: Gu, Zhao-Hui organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 3 givenname: Zi-Xun surname: Yan fullname: Yan, Zi-Xun organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 4 givenname: Xia surname: Zhao fullname: Zhao, Xia organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 5 givenname: Yin-Yin surname: Xie fullname: Xie, Yin-Yin organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 6 givenname: Zi-Guan surname: Zhang fullname: Zhang, Zi-Guan organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 7 givenname: Chun-Ming surname: Pan fullname: Pan, Chun-Ming organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 8 givenname: Yuan surname: Hu fullname: Hu, Yuan organization: Department of Otorhinolaryngology, Rui Jin Hospital, SJTU School of Medicine – sequence: 9 givenname: Chang-Ping surname: Cai fullname: Cai, Chang-Ping organization: Department of Otorhinolaryngology, Rui Jin Hospital, SJTU School of Medicine – sequence: 10 givenname: Ying surname: Dong fullname: Dong, Ying organization: Department of Oncology, Second Affiliated Hospital of Zhejiang University School of Medicine – sequence: 11 givenname: Jin-Yan surname: Huang fullname: Huang, Jin-Yan organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 12 givenname: Li surname: Wang fullname: Wang, Li organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 13 givenname: Yang surname: Shen fullname: Shen, Yang organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 14 givenname: Guoyu surname: Meng fullname: Meng, Guoyu organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 15 givenname: Jian-Feng surname: Zhou fullname: Zhou, Jian-Feng organization: Department of Hematology, Tongji Medical College, Huazhong University of Science and Technology, Tongji Hospital – sequence: 16 givenname: Jian-Da surname: Hu fullname: Hu, Jian-Da organization: Fujian Institute of Hematology, Fujian Medical University Union Hospital – sequence: 17 givenname: Jin-Fen surname: Wang fullname: Wang, Jin-Fen organization: Department of Pathology, Shanxi Oncology Hospital – sequence: 18 givenname: Yuan-Hua surname: Liu fullname: Liu, Yuan-Hua organization: Department of Oncology, Jiangsu Cancer Hospital – sequence: 19 givenname: Lin-Hua surname: Yang fullname: Yang, Lin-Hua organization: Department of Hematology, Second Affiliated Hospital of Shanxi Medical University – sequence: 20 givenname: Feng surname: Zhang fullname: Zhang, Feng organization: Department of Hematology, Anhui Oncology Hospital, Bengbu Medical College – sequence: 21 givenname: Jian-Min surname: Wang fullname: Wang, Jian-Min organization: Department of Hematology, Changhai Hospital, Second Military Medical University – sequence: 22 givenname: Zhao surname: Wang fullname: Wang, Zhao organization: Department of Hematology, Beijing Friendship Hospital, Capital Medical University – sequence: 23 givenname: Zhi-Gang surname: Peng fullname: Peng, Zhi-Gang organization: Department of Hematology, First Affiliated Hospital of Guangxi Medical University – sequence: 24 givenname: Fang-Yuan surname: Chen fullname: Chen, Fang-Yuan organization: Department of Hematology, Renji Hospital, SJTU School of Medicine – sequence: 25 givenname: Zi-Min surname: Sun fullname: Sun, Zi-Min organization: Department of Hematology, Anhui Provincial Hospital – sequence: 26 givenname: Hao surname: Ding fullname: Ding, Hao organization: Department of Radiation Oncology, Eye and ENT Hospital of Fudan University – sequence: 27 givenname: Ju-Mei surname: Shi fullname: Shi, Ju-Mei organization: Department of Hematology, Shanghai Tenth People's Hospital, Tongji University School of Medicine – sequence: 28 givenname: Jian surname: Hou fullname: Hou, Jian organization: Department of Hematology, Changzheng Hospital, Second Military Medical University – sequence: 29 givenname: Jin-Song surname: Yan fullname: Yan, Jin-Song organization: Department of Hematology, Second Hospital of Dalian Medical University – sequence: 30 givenname: Jing-Yi surname: Shi fullname: Shi, Jing-Yi organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 31 givenname: Lan surname: Xu fullname: Xu, Lan organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 32 givenname: Yang surname: Li fullname: Li, Yang organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 33 givenname: Jing surname: Lu fullname: Lu, Jing organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 34 givenname: Zhong surname: Zheng fullname: Zheng, Zhong organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 35 givenname: Wen surname: Xue fullname: Xue, Wen organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine – sequence: 36 givenname: Wei-Li surname: Zhao fullname: Zhao, Wei-Li email: zhao.weili@yahoo.com organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine, Pôle de Recherches Sino-Français en Science du Vivant et Génomique, Laboratory of Molecular Pathology – sequence: 37 givenname: Zhu surname: Chen fullname: Chen, Zhu email: zchen@stn.sh.cn organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine, Pôle de Recherches Sino-Français en Science du Vivant et Génomique, Laboratory of Molecular Pathology – sequence: 38 givenname: Sai-Juan surname: Chen fullname: Chen, Sai-Juan email: sjchen@stn.sh.cn organization: State Key Laboratory of Medical Genomics, Shanghai Institute of Hematology, Rui Jin Hospital, Shanghai Jiao Tong University (SJTU) School of Medicine and Collaborative Innovation Center of Systems Biomedicine, Pôle de Recherches Sino-Français en Science du Vivant et Génomique, Laboratory of Molecular Pathology |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26192917$$D View this record in MEDLINE/PubMed |
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| Snippet | Zhu Chen, Sai-Juan Chen, Wei-Li Zhao and colleagues identify recurrent loss-of-function mutations in the RNA helicase gene
DDX3X
in 20% of subjects with... Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56(+) and cytoCD3(+) lymphocytes with aggressive clinical course, which is prevalent... Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of [CD56.sup.+] and cyto[CD3.sup.+] lymphocytes with aggressive clinical course, which is... Natural killer/T-cell lymphoma (NKTCL) is a malignant proliferation of CD56^sup +^ and cytoCD3^sup +^ lymphocytes with aggressive clinical course, which is... |
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| SubjectTerms | 631/208/514/1948 631/208/68 631/208/737 631/67/1990/291/1621/1916 Adult Aged Aged, 80 and over Agriculture Amino Acid Sequence Animal Genetics and Genomics Bioinformatics Biomedicine Cancer Research Cell Cycle DEAD-box RNA Helicases - genetics Diagnosis DNA Mutational Analysis Epigenetics Exome Exome sequencing Female Gene expression Gene Function Gene mutations Genomes Health aspects Human Genetics Humans Identification and classification Kaplan-Meier Estimate Kinases letter Lymphocytes Lymphoma Lymphoma, T-Cell - genetics Lymphoma, T-Cell - mortality Lymphoma, T-Cell - pathology Male Medical prognosis Medical research Middle Aged Molecular Sequence Data Multivariate analysis Mutation Pathogenesis Prognosis Risk factors Signal Transduction Studies T cell lymphoma Uniparental Disomy - genetics Young Adult |
| Title | Exome sequencing identifies somatic mutations of DDX3X in natural killer/T-cell lymphoma |
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