Potent efficacy of combined PI3K/mTOR and JAK or ABL inhibition in murine xenograft models of Ph-like acute lymphoblastic leukemia

Philadelphia chromosome (Ph)-like B-cell acute lymphoblastic leukemia (Ph-like ALL) is associated with activated JAK/STAT, Abelson kinase (ABL), and/or phosphatidylinositol 3-kinase (PI3K) signaling and poor clinical outcomes. PI3K pathway signaling inhibitors have been minimally investigated in Ph-...

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Veröffentlicht in:Blood Jg. 129; H. 2; S. 177 - 187
Hauptverfasser: Tasian, Sarah K, Teachey, David T, Li, Yong, Shen, Feng, Harvey, Richard C, Chen, I-Ming, Ryan, Theresa, Vincent, Tiffaney L, Willman, Cheryl L, Perl, Alexander E, Hunger, Stephen P, Loh, Mignon L, Carroll, Martin, Grupp, Stephan A
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Veröffentlicht: United States 12.01.2017
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ISSN:1528-0020
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Abstract Philadelphia chromosome (Ph)-like B-cell acute lymphoblastic leukemia (Ph-like ALL) is associated with activated JAK/STAT, Abelson kinase (ABL), and/or phosphatidylinositol 3-kinase (PI3K) signaling and poor clinical outcomes. PI3K pathway signaling inhibitors have been minimally investigated in Ph-like ALL. We hypothesized that targeted inhibition of PI3Kα, PI3Kδ, PI3K/mTOR, or target of rapamycin complex 1/2 (TORC1/TORC2) would decrease leukemia proliferation and abrogate aberrant kinase signaling and that combined PI3K pathway and JAK inhibition or PI3K pathway and SRC/ABL inhibition would have superior efficacy compared to inhibitor monotherapy. We treated 10 childhood ALL patient-derived xenograft models harboring various Ph-like genomic alterations with 4 discrete PI3K pathway protein inhibitors and observed marked leukemia reduction and in vivo signaling inhibition in all models. Treatment with dual PI3K/mTOR inhibitor gedatolisib resulted in near eradication of ALL in cytokine receptor-like factor 2 (CRLF2)/JAK-mutant models with mean 92.2% (range, 86.0%-99.4%) reduction vs vehicle controls (P < .0001) and in prolonged animal survival. Gedatolisib also inhibited ALL proliferation in ABL/platelet-derived growth factor receptor (PDGFR)-mutant models with mean 66.9% (range, 42.0%-87.6%) reduction vs vehicle (P < .0001). Combined gedatolisib and ruxolitinib treatment of CRLF2/JAK-mutant models more effectively inhibited ALL proliferation than either inhibitor alone (P < .001) and further enhanced survival. Similarly, superior efficacy of combined gedatolisib and dasatinib was observed in ABL/PDGFR-mutant models (P < .001). Overall, PI3K/mTOR inhibition potently decreased ALL burden in vivo; antileukemia activity was further enhanced with combination inhibitor therapy. Clinical trials testing combinations of kinase inhibitors in Ph-like ALL patients are indicated.
AbstractList Philadelphia chromosome (Ph)-like B-cell acute lymphoblastic leukemia (Ph-like ALL) is associated with activated JAK/STAT, Abelson kinase (ABL), and/or phosphatidylinositol 3-kinase (PI3K) signaling and poor clinical outcomes. PI3K pathway signaling inhibitors have been minimally investigated in Ph-like ALL. We hypothesized that targeted inhibition of PI3Kα, PI3Kδ, PI3K/mTOR, or target of rapamycin complex 1/2 (TORC1/TORC2) would decrease leukemia proliferation and abrogate aberrant kinase signaling and that combined PI3K pathway and JAK inhibition or PI3K pathway and SRC/ABL inhibition would have superior efficacy compared to inhibitor monotherapy. We treated 10 childhood ALL patient-derived xenograft models harboring various Ph-like genomic alterations with 4 discrete PI3K pathway protein inhibitors and observed marked leukemia reduction and in vivo signaling inhibition in all models. Treatment with dual PI3K/mTOR inhibitor gedatolisib resulted in near eradication of ALL in cytokine receptor-like factor 2 (CRLF2)/JAK-mutant models with mean 92.2% (range, 86.0%-99.4%) reduction vs vehicle controls (P < .0001) and in prolonged animal survival. Gedatolisib also inhibited ALL proliferation in ABL/platelet-derived growth factor receptor (PDGFR)-mutant models with mean 66.9% (range, 42.0%-87.6%) reduction vs vehicle (P < .0001). Combined gedatolisib and ruxolitinib treatment of CRLF2/JAK-mutant models more effectively inhibited ALL proliferation than either inhibitor alone (P < .001) and further enhanced survival. Similarly, superior efficacy of combined gedatolisib and dasatinib was observed in ABL/PDGFR-mutant models (P < .001). Overall, PI3K/mTOR inhibition potently decreased ALL burden in vivo; antileukemia activity was further enhanced with combination inhibitor therapy. Clinical trials testing combinations of kinase inhibitors in Ph-like ALL patients are indicated.
Author Harvey, Richard C
Willman, Cheryl L
Chen, I-Ming
Li, Yong
Tasian, Sarah K
Teachey, David T
Grupp, Stephan A
Vincent, Tiffaney L
Shen, Feng
Perl, Alexander E
Loh, Mignon L
Hunger, Stephen P
Carroll, Martin
Ryan, Theresa
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  surname: Tasian
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  organization: Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA
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  organization: Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA
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  organization: Division of Oncology, Department of Pediatrics, Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Philadelphia, PA
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  organization: Division of Oncology, Department of Pediatrics, Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Philadelphia, PA
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  fullname: Harvey, Richard C
  organization: Department of Pathology, University of New Mexico, Albuquerque, NM
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  organization: Department of Pathology, University of New Mexico, Albuquerque, NM
– sequence: 10
  givenname: Alexander E
  surname: Perl
  fullname: Perl, Alexander E
  organization: Division of Hematology, Department of Medicine, Abramson Cancer Center, University of Pennsylvania, Philadelphia, PA; and
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  surname: Carroll
  fullname: Carroll, Martin
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  givenname: Stephan A
  surname: Grupp
  fullname: Grupp, Stephan A
  organization: Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27777238$$D View this record in MEDLINE/PubMed
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Snippet Philadelphia chromosome (Ph)-like B-cell acute lymphoblastic leukemia (Ph-like ALL) is associated with activated JAK/STAT, Abelson kinase (ABL), and/or...
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SubjectTerms Animals
Antineoplastic Agents - pharmacology
Cell Proliferation - drug effects
Humans
Janus Kinases - antagonists & inhibitors
Mice
Phosphoinositide-3 Kinase Inhibitors
Precursor Cell Lymphoblastic Leukemia-Lymphoma - pathology
Protein Kinase Inhibitors - pharmacology
Proto-Oncogene Proteins c-abl - antagonists & inhibitors
Random Allocation
Signal Transduction - drug effects
TOR Serine-Threonine Kinases - antagonists & inhibitors
Xenograft Model Antitumor Assays
Title Potent efficacy of combined PI3K/mTOR and JAK or ABL inhibition in murine xenograft models of Ph-like acute lymphoblastic leukemia
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