Ex vivo drug response profiling detects recurrent sensitivity patterns in drug-resistant acute lymphoblastic leukemia
Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker discovery. We provide proof of concept data by profiling 60 drugs on 68 acute lymphoblastic leukemia (ALL) samples mostly from resistant dis...
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| Published in | Blood Vol. 129; no. 11; pp. e26 - e37 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
16.03.2017
American Society of Hematology |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0006-4971 1528-0020 |
| DOI | 10.1182/blood-2016-09-738070 |
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| Abstract | Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker discovery. We provide proof of concept data by profiling 60 drugs on 68 acute lymphoblastic leukemia (ALL) samples mostly from resistant disease in cocultures of bone marrow stromal cells. Patient-derived xenografts retained the original pattern of mutations found in the matched patient material. Stromal coculture did not prevent leukemia cell cycle activity, but a specific sensitivity profile to cell cycle–related drugs identified samples with higher cell proliferation both in vitro and in vivo as leukemia xenografts. In patients with refractory relapses, individual patterns of marked drug resistance and exceptional responses to new agents of immediate clinical relevance were detected. The BCL2-inhibitor venetoclax was highly active below 10 nM in B-cell precursor ALL (BCP-ALL) subsets, including MLL-AF4 and TCF3-HLF ALL, and in some T-cell ALLs (T-ALLs), predicting in vivo activity as a single agent and in combination with dexamethasone and vincristine. Unexpected sensitivity to dasatinib with half maximal inhibitory concentration values below 20 nM was detected in 2 independent T-ALL cohorts, which correlated with similar cytotoxic activity of the SRC inhibitor KX2-391 and inhibition of SRC phosphorylation. A patient with refractory T-ALL was treated with dasatinib on the basis of drug profiling information and achieved a 5-month remission. Thus, drug profiling captures disease-relevant features and unexpected sensitivity to relevant drugs, which warrants further exploration of this functional assay in the context of clinical trials to develop drug repurposing strategies for patients with urgent medical needs.
•Ex vivo drug profiling captures disease-relevant features and relevant sensitivity to therapeutic agents in ALL.•A subset of drug-resistant T-ALL without mutations in ABL1 is highly responsive to dasatinib, which provides a rationale for drug repurposing. |
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| AbstractList | Ex vivo drug profiling captures disease-relevant features and relevant sensitivity to therapeutic agents in ALL. A subset of drug-resistant T-ALL without mutations in ABL1 is highly responsive to dasatinib, which provides a rationale for drug repurposing. Ex vivo drug profiling captures disease-relevant features and relevant sensitivity to therapeutic agents in ALL. A subset of drug-resistant T-ALL without mutations in ABL1 is highly responsive to dasatinib, which provides a rationale for drug repurposing. Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker discovery. We provide proof of concept data by profiling 60 drugs on 68 acute lymphoblastic leukemia (ALL) samples mostly from resistant disease in cocultures of bone marrow stromal cells. Patient-derived xenografts retained the original pattern of mutations found in the matched patient material. Stromal coculture did not prevent leukemia cell cycle activity, but a specific sensitivity profile to cell cycle–related drugs identified samples with higher cell proliferation both in vitro and in vivo as leukemia xenografts. In patients with refractory relapses, individual patterns of marked drug resistance and exceptional responses to new agents of immediate clinical relevance were detected. The BCL2-inhibitor venetoclax was highly active below 10 nM in B-cell precursor ALL (BCP-ALL) subsets, including MLL -AF4 and TCF3-HLF ALL, and in some T-cell ALLs (T-ALLs), predicting in vivo activity as a single agent and in combination with dexamethasone and vincristine. Unexpected sensitivity to dasatinib with half maximal inhibitory concentration values below 20 nM was detected in 2 independent T-ALL cohorts, which correlated with similar cytotoxic activity of the SRC inhibitor KX2-391 and inhibition of SRC phosphorylation. A patient with refractory T-ALL was treated with dasatinib on the basis of drug profiling information and achieved a 5-month remission. Thus, drug profiling captures disease-relevant features and unexpected sensitivity to relevant drugs, which warrants further exploration of this functional assay in the context of clinical trials to develop drug repurposing strategies for patients with urgent medical needs. Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker discovery. We provide proof of concept data by profiling 60 drugs on 68 acute lymphoblastic leukemia (ALL) samples mostly from resistant disease in cocultures of bone marrow stromal cells. Patient-derived xenografts retained the original pattern of mutations found in the matched patient material. Stromal coculture did not prevent leukemia cell cycle activity, but a specific sensitivity profile to cell cycle-related drugs identified samples with higher cell proliferation both in vitro and in vivo as leukemia xenografts. In patients with refractory relapses, individual patterns of marked drug resistance and exceptional responses to new agents of immediate clinical relevance were detected. The BCL2-inhibitor venetoclax was highly active below 10 nM in B-cell precursor ALL (BCP-ALL) subsets, including MLL-AF4 and TCF3-HLF ALL, and in some T-cell ALLs (T-ALLs), predicting in vivo activity as a single agent and in combination with dexamethasone and vincristine. Unexpected sensitivity to dasatinib with half maximal inhibitory concentration values below 20 nM was detected in 2 independent T-ALL cohorts, which correlated with similar cytotoxic activity of the SRC inhibitor KX2-391 and inhibition of SRC phosphorylation. A patient with refractory T-ALL was treated with dasatinib on the basis of drug profiling information and achieved a 5-month remission. Thus, drug profiling captures disease-relevant features and unexpected sensitivity to relevant drugs, which warrants further exploration of this functional assay in the context of clinical trials to develop drug repurposing strategies for patients with urgent medical needs. Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker discovery. We provide proof of concept data by profiling 60 drugs on 68 acute lymphoblastic leukemia (ALL) samples mostly from resistant disease in cocultures of bone marrow stromal cells. Patient-derived xenografts retained the original pattern of mutations found in the matched patient material. Stromal coculture did not prevent leukemia cell cycle activity, but a specific sensitivity profile to cell cycle-related drugs identified samples with higher cell proliferation both in vitro and in vivo as leukemia xenografts. In patients with refractory relapses, individual patterns of marked drug resistance and exceptional responses to new agents of immediate clinical relevance were detected. The BCL2-inhibitor venetoclax was highly active below 10 nM in B-cell precursor ALL (BCP-ALL) subsets, including and ALL, and in some T-cell ALLs (T-ALLs), predicting in vivo activity as a single agent and in combination with dexamethasone and vincristine. Unexpected sensitivity to dasatinib with half maximal inhibitory concentration values below 20 nM was detected in 2 independent T-ALL cohorts, which correlated with similar cytotoxic activity of the SRC inhibitor KX2-391 and inhibition of SRC phosphorylation. A patient with refractory T-ALL was treated with dasatinib on the basis of drug profiling information and achieved a 5-month remission. Thus, drug profiling captures disease-relevant features and unexpected sensitivity to relevant drugs, which warrants further exploration of this functional assay in the context of clinical trials to develop drug repurposing strategies for patients with urgent medical needs. Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker discovery. We provide proof of concept data by profiling 60 drugs on 68 acute lymphoblastic leukemia (ALL) samples mostly from resistant disease in cocultures of bone marrow stromal cells. Patient-derived xenografts retained the original pattern of mutations found in the matched patient material. Stromal coculture did not prevent leukemia cell cycle activity, but a specific sensitivity profile to cell cycle–related drugs identified samples with higher cell proliferation both in vitro and in vivo as leukemia xenografts. In patients with refractory relapses, individual patterns of marked drug resistance and exceptional responses to new agents of immediate clinical relevance were detected. The BCL2-inhibitor venetoclax was highly active below 10 nM in B-cell precursor ALL (BCP-ALL) subsets, including MLL-AF4 and TCF3-HLF ALL, and in some T-cell ALLs (T-ALLs), predicting in vivo activity as a single agent and in combination with dexamethasone and vincristine. Unexpected sensitivity to dasatinib with half maximal inhibitory concentration values below 20 nM was detected in 2 independent T-ALL cohorts, which correlated with similar cytotoxic activity of the SRC inhibitor KX2-391 and inhibition of SRC phosphorylation. A patient with refractory T-ALL was treated with dasatinib on the basis of drug profiling information and achieved a 5-month remission. Thus, drug profiling captures disease-relevant features and unexpected sensitivity to relevant drugs, which warrants further exploration of this functional assay in the context of clinical trials to develop drug repurposing strategies for patients with urgent medical needs. •Ex vivo drug profiling captures disease-relevant features and relevant sensitivity to therapeutic agents in ALL.•A subset of drug-resistant T-ALL without mutations in ABL1 is highly responsive to dasatinib, which provides a rationale for drug repurposing. |
| Author | Voegeli, Pamela Delorenzi, Mauro Muckenthaler, Martina U. Von Stackelberg, Arend Stanulla, Martin Jenni, Silvia Higi, Salome Cario, Gunnar Brown, Timothy J. Bandapalli, Obul R. Collins, Robert H. Chang, Bill H. Frismantas, Viktoras Dunn, Samuel H. Marovca, Blerim Pail, Orrin Meisel, Roland Eckert, Cornelia Diaz-Flores, Ernesto Tchinda, Joelle Bornhauser, Beat C. Loh, Mignon L. Saha, Vaskar Irving, Julie A. Bourquin, Jean-Pierre Horvath, Peter Kunz, Joachim Eugster, Sabrina Kulozik, Andreas E. Dobay, Maria Pamela Schrappe, Martin Radimerski, Thomas Balasubramanian, Gnana P. Uhrig, Sebastian Richter-Pechanska, Paulina Rinaldi, Anna Tyner, Jeffrey W. |
| Author_xml | – sequence: 1 givenname: Viktoras surname: Frismantas fullname: Frismantas, Viktoras organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 2 givenname: Maria Pamela surname: Dobay fullname: Dobay, Maria Pamela organization: Swiss Institute of Bioinformatics, Lausanne, Switzerland – sequence: 3 givenname: Anna surname: Rinaldi fullname: Rinaldi, Anna organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 4 givenname: Joelle surname: Tchinda fullname: Tchinda, Joelle organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 5 givenname: Samuel H. surname: Dunn fullname: Dunn, Samuel H. organization: School of Medicine, The University of Texas Southwestern Medical Center, Dallas, TX – sequence: 6 givenname: Joachim surname: Kunz fullname: Kunz, Joachim organization: Department of Pediatric Oncology, Hematology and Immunology, University of Heidelberg, Heidelberg, Germany – sequence: 7 givenname: Paulina surname: Richter-Pechanska fullname: Richter-Pechanska, Paulina organization: Department of Pediatric Oncology, Hematology and Immunology, University of Heidelberg, Heidelberg, Germany – sequence: 8 givenname: Blerim surname: Marovca fullname: Marovca, Blerim organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 9 givenname: Orrin surname: Pail fullname: Pail, Orrin organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 10 givenname: Silvia surname: Jenni fullname: Jenni, Silvia organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 11 givenname: Ernesto surname: Diaz-Flores fullname: Diaz-Flores, Ernesto organization: Department of Pediatrics and Helen Diller Family Comprehensive Cancer Center, University of California–San Francisco, San Francisco, CA – sequence: 12 givenname: Bill H. surname: Chang fullname: Chang, Bill H. organization: Division of Hematology and Oncology, Department of Pediatrics, Doernbecher Children's Hospital, Oregon Health & Science University, Portland, OR – sequence: 13 givenname: Timothy J. orcidid: 0000-0002-4843-4639 surname: Brown fullname: Brown, Timothy J. organization: Division of Hematology and Oncology, Department of Medicine, The University of Texas Southwestern Medical Center, Dallas, TX – sequence: 14 givenname: Robert H. surname: Collins fullname: Collins, Robert H. organization: Division of Hematology and Oncology, Department of Medicine, The University of Texas Southwestern Medical Center, Dallas, TX – sequence: 15 givenname: Sebastian surname: Uhrig fullname: Uhrig, Sebastian organization: German Cancer Research Center, Heidelberg, Germany – sequence: 16 givenname: Gnana P. surname: Balasubramanian fullname: Balasubramanian, Gnana P. organization: German Cancer Research Center, Heidelberg, Germany – sequence: 17 givenname: Obul R. surname: Bandapalli fullname: Bandapalli, Obul R. organization: Department of Pediatric Oncology, Hematology and Immunology, University of Heidelberg, Heidelberg, Germany – sequence: 18 givenname: Salome surname: Higi fullname: Higi, Salome organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 19 givenname: Sabrina surname: Eugster fullname: Eugster, Sabrina organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 20 givenname: Pamela surname: Voegeli fullname: Voegeli, Pamela organization: Institute of Forensic Medicine, University of Zurich, Zurich, Switzerland – sequence: 21 givenname: Mauro surname: Delorenzi fullname: Delorenzi, Mauro organization: Swiss Institute of Bioinformatics, Lausanne, Switzerland – sequence: 22 givenname: Gunnar surname: Cario fullname: Cario, Gunnar organization: Department of Pediatrics, University Medical Centre Schleswig-Holstein, Kiel, Germany – sequence: 23 givenname: Mignon L. surname: Loh fullname: Loh, Mignon L. organization: Department of Pediatrics, University of California–San Francisco, San Francisco, CA – sequence: 24 givenname: Martin surname: Schrappe fullname: Schrappe, Martin organization: Department of Pediatrics, University Medical Centre Schleswig-Holstein, Kiel, Germany – sequence: 25 givenname: Martin surname: Stanulla fullname: Stanulla, Martin organization: Department of Pediatric Hematology and Oncology, Hannover Medical School, Hannover, Germany – sequence: 26 givenname: Andreas E. surname: Kulozik fullname: Kulozik, Andreas E. organization: Department of Pediatric Oncology, Hematology and Immunology, University of Heidelberg, Heidelberg, Germany – sequence: 27 givenname: Martina U. surname: Muckenthaler fullname: Muckenthaler, Martina U. organization: Department of Pediatric Oncology, Hematology and Immunology, University of Heidelberg, Heidelberg, Germany – sequence: 28 givenname: Vaskar surname: Saha fullname: Saha, Vaskar organization: Division of Molecular and Clinical Cancer Sciences, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom – sequence: 29 givenname: Julie A. surname: Irving fullname: Irving, Julie A. organization: Northern Institute for Cancer Research, Newcastle University, Newcastle upon Tyne, United Kingdom – sequence: 30 givenname: Roland surname: Meisel fullname: Meisel, Roland organization: Division of Pediatric Stem Cell Therapy, Clinic for Pediatric Oncology, Hematology and Clinical Immunology, Medical Faculty, Heinrich Heine University, Düsseldorf, Germany – sequence: 31 givenname: Thomas surname: Radimerski fullname: Radimerski, Thomas organization: Disease Area Oncology, Novartis Institutes for Biomedical Research, Basel, Switzerland – sequence: 32 givenname: Arend surname: Von Stackelberg fullname: Von Stackelberg, Arend organization: German Cancer Research Center, Heidelberg, Germany – sequence: 33 givenname: Cornelia surname: Eckert fullname: Eckert, Cornelia organization: German Cancer Research Center, Heidelberg, Germany – sequence: 34 givenname: Jeffrey W. surname: Tyner fullname: Tyner, Jeffrey W. organization: Department of Cell, Developmental and Cancer Biology, Oregon Health & Science University, Portland, OR – sequence: 35 givenname: Peter surname: Horvath fullname: Horvath, Peter organization: Synthetic and Systems Biology Unit, Hungarian Academy of Sciences, Biological Research Center, Szeged, Hungary – sequence: 36 givenname: Beat C. surname: Bornhauser fullname: Bornhauser, Beat C. organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland – sequence: 37 givenname: Jean-Pierre orcidid: 0000-0001-6571-6227 surname: Bourquin fullname: Bourquin, Jean-Pierre email: jean-pierre.bourquin@kispi.uzh.ch organization: Department of Oncology, University Children's Hospital Zurich, Zurich, Switzerland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28122742$$D View this record in MEDLINE/PubMed |
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| Snippet | Drug sensitivity and resistance testing on diagnostic leukemia samples should provide important functional information to guide actionable target and biomarker... Ex vivo drug profiling captures disease-relevant features and relevant sensitivity to therapeutic agents in ALL. A subset of drug-resistant T-ALL without... Ex vivo drug profiling captures disease-relevant features and relevant sensitivity to therapeutic agents in ALL. A subset of drug-resistant T-ALL without... |
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| SubjectTerms | Antineoplastic Agents - pharmacology Antineoplastic Combined Chemotherapy Protocols - pharmacology Cells, Cultured Coculture Techniques Drug Resistance, Neoplasm Heterografts Humans Lymphoid Neoplasia Mesenchymal Stem Cells - pathology Precursor Cell Lymphoblastic Leukemia-Lymphoma - drug therapy Precursor Cell Lymphoblastic Leukemia-Lymphoma - pathology |
| Title | Ex vivo drug response profiling detects recurrent sensitivity patterns in drug-resistant acute lymphoblastic leukemia |
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