Targetable kinase gene fusions in high-risk B-ALL: a study from the Children's Oncology Group
Philadelphia chromosome-like (Ph-like) acute lymphoblastic leukemia (ALL) is a high-risk subtype characterized by genomic alterations that activate cytokine receptor and kinase signaling. We examined the frequency and spectrum of targetable genetic lesions in a retrospective cohort of 1389 consecuti...
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| Veröffentlicht in: | Blood Jg. 129; H. 25; S. 3352 |
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| Hauptverfasser: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
| Veröffentlicht: |
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22.06.2017
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| ISSN: | 1528-0020, 1528-0020 |
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| Abstract | Philadelphia chromosome-like (Ph-like) acute lymphoblastic leukemia (ALL) is a high-risk subtype characterized by genomic alterations that activate cytokine receptor and kinase signaling. We examined the frequency and spectrum of targetable genetic lesions in a retrospective cohort of 1389 consecutively diagnosed patients with childhood B-lineage ALL with high-risk clinical features and/or elevated minimal residual disease at the end of remission induction therapy. The Ph-like gene expression profile was identified in 341 of 1389 patients, 57 of whom were excluded from additional analyses because of the presence of
-
(n = 46) or
-
(n = 11). Among the remaining 284 patients (20.4%), overexpression and rearrangement of
(
-
or
-
) were identified in 124 (43.7%), with concomitant genomic alterations activating the JAK-STAT pathway (
,
,
) identified in 63 patients (50.8% of those with
rearrangement). Among the remaining patients, using reverse transcriptase polymerase chain reaction or transcriptome sequencing, we identified targetable ABL-class fusions (
,
,
, and
) in 14.1%,
rearrangements or
fusions in 8.8%, alterations activating other JAK-STAT signaling genes (
,
,
) in 6.3% or other kinases (
,
,
) in 4.6%, and mutations involving the Ras pathway (
,
,
,
) in 6% of those with Ph-like ALL. We identified 8 new rearrangement partners for 4 kinase genes previously reported to be rearranged in Ph-like ALL. The current findings provide support for the precision-medicine testing and treatment approach for Ph-like ALL implemented in Children's Oncology Group ALL trials. |
|---|---|
| AbstractList | Philadelphia chromosome-like (Ph-like) acute lymphoblastic leukemia (ALL) is a high-risk subtype characterized by genomic alterations that activate cytokine receptor and kinase signaling. We examined the frequency and spectrum of targetable genetic lesions in a retrospective cohort of 1389 consecutively diagnosed patients with childhood B-lineage ALL with high-risk clinical features and/or elevated minimal residual disease at the end of remission induction therapy. The Ph-like gene expression profile was identified in 341 of 1389 patients, 57 of whom were excluded from additional analyses because of the presence of
-
(n = 46) or
-
(n = 11). Among the remaining 284 patients (20.4%), overexpression and rearrangement of
(
-
or
-
) were identified in 124 (43.7%), with concomitant genomic alterations activating the JAK-STAT pathway (
,
,
) identified in 63 patients (50.8% of those with
rearrangement). Among the remaining patients, using reverse transcriptase polymerase chain reaction or transcriptome sequencing, we identified targetable ABL-class fusions (
,
,
, and
) in 14.1%,
rearrangements or
fusions in 8.8%, alterations activating other JAK-STAT signaling genes (
,
,
) in 6.3% or other kinases (
,
,
) in 4.6%, and mutations involving the Ras pathway (
,
,
,
) in 6% of those with Ph-like ALL. We identified 8 new rearrangement partners for 4 kinase genes previously reported to be rearranged in Ph-like ALL. The current findings provide support for the precision-medicine testing and treatment approach for Ph-like ALL implemented in Children's Oncology Group ALL trials. Philadelphia chromosome-like (Ph-like) acute lymphoblastic leukemia (ALL) is a high-risk subtype characterized by genomic alterations that activate cytokine receptor and kinase signaling. We examined the frequency and spectrum of targetable genetic lesions in a retrospective cohort of 1389 consecutively diagnosed patients with childhood B-lineage ALL with high-risk clinical features and/or elevated minimal residual disease at the end of remission induction therapy. The Ph-like gene expression profile was identified in 341 of 1389 patients, 57 of whom were excluded from additional analyses because of the presence of BCR-ABL1 (n = 46) or ETV6-RUNX1 (n = 11). Among the remaining 284 patients (20.4%), overexpression and rearrangement of CRLF2 (IGH-CRLF2 or P2RY8-CRLF2) were identified in 124 (43.7%), with concomitant genomic alterations activating the JAK-STAT pathway (JAK1, JAK2, IL7R) identified in 63 patients (50.8% of those with CRLF2 rearrangement). Among the remaining patients, using reverse transcriptase polymerase chain reaction or transcriptome sequencing, we identified targetable ABL-class fusions (ABL1, ABL2, CSF1R, and PDGFRB) in 14.1%, EPOR rearrangements or JAK2 fusions in 8.8%, alterations activating other JAK-STAT signaling genes (IL7R, SH2B3, JAK1) in 6.3% or other kinases (FLT3, NTRK3, LYN) in 4.6%, and mutations involving the Ras pathway (KRAS, NRAS, NF1, PTPN11) in 6% of those with Ph-like ALL. We identified 8 new rearrangement partners for 4 kinase genes previously reported to be rearranged in Ph-like ALL. The current findings provide support for the precision-medicine testing and treatment approach for Ph-like ALL implemented in Children's Oncology Group ALL trials.Philadelphia chromosome-like (Ph-like) acute lymphoblastic leukemia (ALL) is a high-risk subtype characterized by genomic alterations that activate cytokine receptor and kinase signaling. We examined the frequency and spectrum of targetable genetic lesions in a retrospective cohort of 1389 consecutively diagnosed patients with childhood B-lineage ALL with high-risk clinical features and/or elevated minimal residual disease at the end of remission induction therapy. The Ph-like gene expression profile was identified in 341 of 1389 patients, 57 of whom were excluded from additional analyses because of the presence of BCR-ABL1 (n = 46) or ETV6-RUNX1 (n = 11). Among the remaining 284 patients (20.4%), overexpression and rearrangement of CRLF2 (IGH-CRLF2 or P2RY8-CRLF2) were identified in 124 (43.7%), with concomitant genomic alterations activating the JAK-STAT pathway (JAK1, JAK2, IL7R) identified in 63 patients (50.8% of those with CRLF2 rearrangement). Among the remaining patients, using reverse transcriptase polymerase chain reaction or transcriptome sequencing, we identified targetable ABL-class fusions (ABL1, ABL2, CSF1R, and PDGFRB) in 14.1%, EPOR rearrangements or JAK2 fusions in 8.8%, alterations activating other JAK-STAT signaling genes (IL7R, SH2B3, JAK1) in 6.3% or other kinases (FLT3, NTRK3, LYN) in 4.6%, and mutations involving the Ras pathway (KRAS, NRAS, NF1, PTPN11) in 6% of those with Ph-like ALL. We identified 8 new rearrangement partners for 4 kinase genes previously reported to be rearranged in Ph-like ALL. The current findings provide support for the precision-medicine testing and treatment approach for Ph-like ALL implemented in Children's Oncology Group ALL trials. |
| Author | Roberts, Kathryn G Jenkins, Heather Stonerock, Eileen Devidas, Meenakshi Shao, Ying Dai, Yunfeng Salzer, Wanda L Heerema, Nyla A Willman, Cheryl L Gastier-Foster, Julie M Easton, John Burke, Michael J Zhang, Jinghui Angiolillo, Anne L Tran, Thai Hoa Nguyen, Jonathan V Zweidler-McKay, Patrick A Reshmi, Shalini C Carroll, William L Harvey, Richard C Smith, Amy Valentine, Marc Liu, Yu Gu, Zhaohui Payne-Turner, Debbie Chen, I-Ming Raetz, Elizabeth A Rabin, Karen R Li, Yongjin Wood, Brent L Loh, Mignon L Hunger, Stephen P Carroll, 3rd, Andrew J Borowitz, Michael J Mullighan, Charles G |
| Author_xml | – sequence: 1 givenname: Shalini C surname: Reshmi fullname: Reshmi, Shalini C organization: Department of Pathology, The Ohio State University College of Medicine, Columbus, OH – sequence: 2 givenname: Richard C orcidid: 0000-0002-4904-9767 surname: Harvey fullname: Harvey, Richard C organization: University of New Mexico Cancer Center, Albuquerque, NM – sequence: 3 givenname: Kathryn G surname: Roberts fullname: Roberts, Kathryn G organization: Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 4 givenname: Eileen surname: Stonerock fullname: Stonerock, Eileen organization: Institute for Genomic Medicine, Nationwide Children's Hospital, Columbus, OH – sequence: 5 givenname: Amy surname: Smith fullname: Smith, Amy organization: Comprehensive Cancer Center, The Ohio State University College of Medicine, Columbus, OH – sequence: 6 givenname: Heather surname: Jenkins fullname: Jenkins, Heather organization: Institute for Genomic Medicine, Nationwide Children's Hospital, Columbus, OH – sequence: 7 givenname: I-Ming surname: Chen fullname: Chen, I-Ming organization: University of New Mexico Cancer Center, Albuquerque, NM – sequence: 8 givenname: Marc surname: Valentine fullname: Valentine, Marc organization: Department of Cytogenetics and – sequence: 9 givenname: Yu surname: Liu fullname: Liu, Yu organization: Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 10 givenname: Yongjin surname: Li fullname: Li, Yongjin organization: Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 11 givenname: Ying surname: Shao fullname: Shao, Ying organization: Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 12 givenname: John surname: Easton fullname: Easton, John organization: Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 13 givenname: Debbie surname: Payne-Turner fullname: Payne-Turner, Debbie organization: Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 14 givenname: Zhaohui surname: Gu fullname: Gu, Zhaohui organization: Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 15 givenname: Thai Hoa surname: Tran fullname: Tran, Thai Hoa organization: Department of Pediatrics, UCSF Benioff Children's Hospital and Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA – sequence: 16 givenname: Jonathan V surname: Nguyen fullname: Nguyen, Jonathan V organization: Department of Pediatrics, UCSF Benioff Children's Hospital and Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA – sequence: 17 givenname: Meenakshi surname: Devidas fullname: Devidas, Meenakshi organization: Department of Biostatistics, University of Florida, Gainesville, FL – sequence: 18 givenname: Yunfeng surname: Dai fullname: Dai, Yunfeng organization: Department of Biostatistics, University of Florida, Gainesville, FL – sequence: 19 givenname: Nyla A surname: Heerema fullname: Heerema, Nyla A organization: Department of Pathology, The Ohio State University College of Medicine, Columbus, OH – sequence: 20 givenname: Andrew J surname: Carroll, 3rd fullname: Carroll, 3rd, Andrew J organization: Department of Genetics, University of Alabama at Birmingham, Birmingham, AL – sequence: 21 givenname: Elizabeth A surname: Raetz fullname: Raetz, Elizabeth A organization: Department of Pediatrics, University of Utah, Salt Lake City, UT – sequence: 22 givenname: Michael J surname: Borowitz fullname: Borowitz, Michael J organization: Department of Pathology, Johns Hopkins University, Baltimore, MD – sequence: 23 givenname: Brent L surname: Wood fullname: Wood, Brent L organization: Seattle Children's Hospital, Seattle, WA – sequence: 24 givenname: Anne L surname: Angiolillo fullname: Angiolillo, Anne L organization: Children's National Medical Center, Washington, DC – sequence: 25 givenname: Michael J surname: Burke fullname: Burke, Michael J organization: Department of Pediatrics, Medical College of Wisconsin, Milwaukee, WI – sequence: 26 givenname: Wanda L surname: Salzer fullname: Salzer, Wanda L organization: US Army Medical Research and Materiel Command, Fort Detrick, MD – sequence: 27 givenname: Patrick A surname: Zweidler-McKay fullname: Zweidler-McKay, Patrick A organization: Department of Pediatrics, MD Anderson Cancer Center, Houston, TX – sequence: 28 givenname: Karen R surname: Rabin fullname: Rabin, Karen R organization: Department of Pediatrics, Baylor College of Medicine, Houston, TX – sequence: 29 givenname: William L surname: Carroll fullname: Carroll, William L organization: Perlmutter Cancer Center, NYU Langone Medical Center, New York, NY – sequence: 30 givenname: Jinghui surname: Zhang fullname: Zhang, Jinghui organization: Department of Computational Biology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 31 givenname: Mignon L surname: Loh fullname: Loh, Mignon L organization: Department of Pediatrics, UCSF Benioff Children's Hospital and Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA – sequence: 32 givenname: Charles G surname: Mullighan fullname: Mullighan, Charles G organization: Department of Pathology, St. Jude Children's Research Hospital, Memphis, TN – sequence: 33 givenname: Cheryl L surname: Willman fullname: Willman, Cheryl L organization: University of New Mexico Cancer Center, Albuquerque, NM – sequence: 34 givenname: Julie M surname: Gastier-Foster fullname: Gastier-Foster, Julie M organization: Department of Pediatrics, The Ohio State University College of Medicine, Columbus, OH; and – sequence: 35 givenname: Stephen P surname: Hunger fullname: Hunger, Stephen P organization: Department of Pediatrics, Children's Hospital of Philadelphia and Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28408464$$D View this record in MEDLINE/PubMed |
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| DOI | 10.1182/blood-2016-12-758979 |
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| DeliveryMethod | no_fulltext_linktorsrc |
| Discipline | Medicine Chemistry Biology Anatomy & Physiology |
| EISSN | 1528-0020 |
| ExternalDocumentID | 28408464 |
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| References | 28642359 - Blood. 2017 Jun 22;129(25):3280-3282 |
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| SubjectTerms | Child Female Fusion Proteins, bcr-abl - genetics Gene Expression Regulation, Leukemic Gene Fusion Humans Interleukin-7 Receptor alpha Subunit - genetics Janus Kinase 2 - genetics Male Mutation Philadelphia Chromosome Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - genetics Protein Kinases - genetics Receptors, Cytokine - genetics Retrospective Studies Transcriptome |
| Title | Targetable kinase gene fusions in high-risk B-ALL: a study from the Children's Oncology Group |
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