Coordinate regulation of residual bone marrow function by paracrine trafficking of AML exosomes
We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an in vitro transfer, AML exosomes produce proangiogenic changes in bystander cells. We reasoned that paracrine exosome trafficking may have a broad...
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| Published in: | Leukemia Vol. 29; no. 12; pp. 2285 - 2295 |
|---|---|
| Main Authors: | , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
01.12.2015
Nature Publishing Group |
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| ISSN: | 0887-6924, 1476-5551 |
| Online Access: | Get full text |
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| Abstract | We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an
in vitro
transfer, AML exosomes produce proangiogenic changes in bystander cells. We reasoned that paracrine exosome trafficking may have a broader role in shaping the leukemic niche. In a series of
in vitro
studies and murine xenografts, we demonstrate that AML exosomes downregulate critical retention factors (
Scf
,
Cxcl12
) in stromal cells, leading to hematopoietic stem and progenitor cell (HSPC) mobilization from the bone marrow. Exosome trafficking also regulates HSPC directly, and we demonstrate declining clonogenicity, loss of CXCR4 and c-Kit expression, and the consistent repression of several hematopoietic transcription factors, including
c-Myb
,
Cebp-β
and
Hoxa-9
. Additional experiments using a model of extramedullary AML or direct intrafemoral injection of purified exosomes reveal that the erosion of HSPC function can occur independent of direct cell–cell contact with leukemia cells. Finally, using a novel multiplex proteomics technique, we identified candidate pathways involved in the direct exosome-mediated modulation of HSPC function. In aggregate, this work suggests that AML exosomes participate in the suppression of residual hematopoietic function that precedes widespread leukemic invasion of the bone marrow directly and indirectly via stromal components. |
|---|---|
| AbstractList | We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an
in vitro
transfer, AML exosomes produce proangiogenic changes in bystander cells. We reasoned that paracrine exosome trafficking may have a broader role in shaping the leukemic niche. In a series of
in vitro
studies and murine xenografts, we demonstrate that AML exosomes downregulate critical retention factors (
Scf
,
Cxcl12
) in stromal cells, leading to hematopoietic stem and progenitor cell (HSPC) mobilization from the bone marrow. Exosome trafficking also regulates HSPC directly, and we demonstrate declining clonogenicity, loss of CXCR4 and c-Kit expression, and the consistent repression of several hematopoietic transcription factors, including
c-Myb
,
Cebp-β
and
Hoxa-9
. Additional experiments using a model of extramedullary AML or direct intrafemoral injection of purified exosomes reveal that the erosion of HSPC function can occur independent of direct cell–cell contact with leukemia cells. Finally, using a novel multiplex proteomics technique, we identified candidate pathways involved in the direct exosome-mediated modulation of HSPC function. In aggregate, this work suggests that AML exosomes participate in the suppression of residual hematopoietic function that precedes widespread leukemic invasion of the bone marrow directly and indirectly via stromal components. We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an in vitro transfer, AML exosomes produce proangiogenic changes in bystander cells. We reasoned that paracrine exosome trafficking may have a broader role in shaping the leukemic niche. In a series of in vitro studies and murine xenografts, we demonstrate that AML exosomes downregulate critical retention factors (Scf, Cxcl12) in stromal cells, leading to hematopoietic stem and progenitor cell (HSPC) mobilization from the bone marrow. Exosome trafficking also regulates HSPC directly, and we demonstrate declining clonogenicity, loss of CXCR4 and c-Kit expression, and the consistent repression of several hematopoietic transcription factors, including c-Myb, Cebp- beta and Hoxa-9. Additional experiments using a model of extramedullary AML or direct intrafemoral injection of purified exosomes reveal that the erosion of HSPC function can occur independent of direct cell-cell contact with leukemia cells. Finally, using a novel multiplex proteomics technique, we identified candidate pathways involved in the direct exosome-mediated modulation of HSPC function. In aggregate, this work suggests that AML exosomes participate in the suppression of residual hematopoietic function that precedes widespread leukemic invasion of the bone marrow directly and indirectly via stromal components. We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an in vitro transfer, AML exosomes produce proangiogenic changes in bystander cells. We reasoned that paracrine exosome trafficking may have a broader role in shaping the leukemic niche. In a series of in vitro studies and murine xenografts, we demonstrate that AML exosomes downregulate critical retention factors (Scf, Cxcl12) in stromal cells, leading to hematopoietic stem and progenitor cell (HSPC) mobilization from the bone marrow. Exosome trafficking also regulates HSPC directly, and we demonstrate declining clonogenicity, loss of CXCR4 and c-Kit expression, and the consistent repression of several hematopoietic transcription factors, including c-Myb, Cebp-β and Hoxa-9. Additional experiments using a model of extramedullary AML or direct intrafemoral injection of purified exosomes reveal that the erosion of HSPC function can occur independent of direct cell-cell contact with leukemia cells. Finally, using a novel multiplex proteomics technique, we identified candidate pathways involved in the direct exosome-mediated modulation of HSPC function. In aggregate, this work suggests that AML exosomes participate in the suppression of residual hematopoietic function that precedes widespread leukemic invasion of the bone marrow directly and indirectly via stromal components. We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an in vitro transfer, AML exosomes produce proangiogenic changes in bystander cells. We reasoned that paracrine exosome trafficking may have a broader role in shaping the leukemic niche. In a series of in vitro studies and murine xenografts, we demonstrate that AML exosomes downregulate critical retention factors (Scf, Cxcl12) in stromal cells, leading to hematopoietic stem and progenitor cell (HSPC) mobilization from the bone marrow. Exosome trafficking also regulates HSPC directly, and we demonstrate declining clonogenicity, loss of CXCR4 and c-Kit expression, and the consistent repression of several hematopoietic transcription factors, including c-Myb, Cebp-β and Hoxa-9. Additional experiments using a model of extramedullary AML or direct intrafemoral injection of purified exosomes reveal that the erosion of HSPC function can occur independent of direct cell-cell contact with leukemia cells. Finally, using a novel multiplex proteomics technique, we identified candidate pathways involved in the direct exosome-mediated modulation of HSPC function. In aggregate, this work suggests that AML exosomes participate in the suppression of residual hematopoietic function that precedes widespread leukemic invasion of the bone marrow directly and indirectly via stromal components. Leukemia (2015) 29, 2285-2295;doi:10.1038/leu.2015.163 |
| Audience | Academic |
| Author | Chevillet, J R Chang, B H Loriaux, M M Narla, A Hornick, N I Mori, T Goloviznina, N A Kamimae- Lanning, A N Huan, J Roberts, C T Kurre, P David, L L Wilmarth, P A |
| AuthorAffiliation | 2 Papé Family Pediatric Research Institute, Oregon Health & Science University, Portland, OR, USA 5 Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA 3 Oregon Stem Cell Center, Oregon Health & Science University, Portland, OR, USA 6 Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, WA, USA 7 Division of Hematology/Oncology, Stanford University, Palo Alto, CA, USA 1 Department of Pediatrics, Oregon Health & Science University, Portland, OR, USA 8 Department of Medicine, Oregon Health & Science University, Portland, OR, USA 4 Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, OR, USA 9 Oregon National Primate Research Center, Beaverton, OR, USA |
| AuthorAffiliation_xml | – name: 3 Oregon Stem Cell Center, Oregon Health & Science University, Portland, OR, USA – name: 7 Division of Hematology/Oncology, Stanford University, Palo Alto, CA, USA – name: 8 Department of Medicine, Oregon Health & Science University, Portland, OR, USA – name: 4 Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, OR, USA – name: 5 Knight Cancer Institute, Oregon Health & Science University, Portland, OR, USA – name: 1 Department of Pediatrics, Oregon Health & Science University, Portland, OR, USA – name: 6 Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, WA, USA – name: 9 Oregon National Primate Research Center, Beaverton, OR, USA – name: 2 Papé Family Pediatric Research Institute, Oregon Health & Science University, Portland, OR, USA |
| Author_xml | – sequence: 1 givenname: J surname: Huan fullname: Huan, J organization: Department of Pediatrics, Oregon Health & Science University, Papé Family Pediatric Research Institute, Oregon Health & Science University, Oregon Stem Cell Center, Oregon Health & Science University – sequence: 2 givenname: N I surname: Hornick fullname: Hornick, N I organization: Department of Pediatrics, Oregon Health & Science University, Papé Family Pediatric Research Institute, Oregon Health & Science University, Oregon Stem Cell Center, Oregon Health & Science University – sequence: 3 givenname: N A surname: Goloviznina fullname: Goloviznina, N A organization: Department of Pediatrics, Oregon Health & Science University, Papé Family Pediatric Research Institute, Oregon Health & Science University, Oregon Stem Cell Center, Oregon Health & Science University – sequence: 4 givenname: A N surname: Kamimae- Lanning fullname: Kamimae- Lanning, A N organization: Department of Pediatrics, Oregon Health & Science University, Papé Family Pediatric Research Institute, Oregon Health & Science University, Oregon Stem Cell Center, Oregon Health & Science University – sequence: 5 givenname: L L surname: David fullname: David, L L organization: Department of Biochemistry and Molecular Biology, Oregon Health & Science University – sequence: 6 givenname: P A surname: Wilmarth fullname: Wilmarth, P A organization: Department of Biochemistry and Molecular Biology, Oregon Health & Science University – sequence: 7 givenname: T surname: Mori fullname: Mori, T organization: Knight Cancer Institute, Oregon Health & Science University – sequence: 8 givenname: J R surname: Chevillet fullname: Chevillet, J R organization: Division of Human Biology, Fred Hutchinson Cancer Research Center – sequence: 9 givenname: A surname: Narla fullname: Narla, A organization: Division of Hematology/Oncology, Stanford University – sequence: 10 givenname: C T surname: Roberts fullname: Roberts, C T organization: Department of Pediatrics, Oregon Health & Science University, Department of Medicine, Oregon Health & Science University, Oregon National Primate Research Center – sequence: 11 givenname: M M surname: Loriaux fullname: Loriaux, M M organization: Knight Cancer Institute, Oregon Health & Science University, Department of Medicine, Oregon Health & Science University – sequence: 12 givenname: B H surname: Chang fullname: Chang, B H organization: Department of Pediatrics, Oregon Health & Science University, Knight Cancer Institute, Oregon Health & Science University – sequence: 13 givenname: P surname: Kurre fullname: Kurre, P email: kurrepe@ohsu.edu organization: Department of Pediatrics, Oregon Health & Science University, Papé Family Pediatric Research Institute, Oregon Health & Science University, Oregon Stem Cell Center, Oregon Health & Science University, Knight Cancer Institute, Oregon Health & Science University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26108689$$D View this record in MEDLINE/PubMed |
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| PublicationTitle | Leukemia |
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| Publisher | Nature Publishing Group UK Nature Publishing Group |
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| Snippet | We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an
in... We recently demonstrated that acute myeloid leukemia (AML) cell lines and patient-derived blasts release exosomes that carry RNA and protein; following an in... |
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| Title | Coordinate regulation of residual bone marrow function by paracrine trafficking of AML exosomes |
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