Engraftment and Reconstitution of Hematopoiesis Is Dependent on VEGFR2-Mediated Regeneration of Sinusoidal Endothelial Cells
Myelosuppression damages the bone marrow (BM) vascular niche, but it is unclear how regeneration of bone marrow vessels contributes to engraftment of transplanted hematopoietic stem and progenitor cells (HSPCs) and restoration of hematopoiesis. We found that chemotherapy and sublethal irradiation in...
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| Published in | Cell stem cell Vol. 4; no. 3; pp. 263 - 274 |
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| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Cambridge, MA
Elsevier Inc
06.03.2009
Cell Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Myelosuppression damages the bone marrow (BM) vascular niche, but it is unclear how regeneration of bone marrow vessels contributes to engraftment of transplanted hematopoietic stem and progenitor cells (HSPCs) and restoration of hematopoiesis. We found that chemotherapy and sublethal irradiation induced minor regression of BM sinusoidal endothelial cells (SECs), while lethal irradiation induced severe regression of SECs and required BM transplantation (BMT) for regeneration. Within the BM, VEGFR2 expression specifically demarcated a continuous network of arterioles and SECs, with arterioles uniquely expressing Sca1 and SECs uniquely expressing VEGFR3. Conditional deletion of VEGFR2 in adult mice blocked regeneration of SECs in sublethally irradiated animals and prevented hematopoietic reconstitution. Similarly, inhibition of VEGFR2 signaling in lethally irradiated wild-type mice rescued with BMT severely impaired SEC reconstruction and prevented engraftment and reconstitution of HSPCs. Therefore, regeneration of SECs via VEGFR2 signaling is essential for engraftment of HSPCs and restoration of hematopoiesis. |
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| AbstractList | Myelosuppression damages the bone marrow (BM) vascular niche, but it is unclear how regeneration of bone marrow vessels contributes to engraftment of transplanted hematopoietic stem and progenitor cells (HSPCs) and restoration of hematopoiesis. We found that chemotherapy and sublethal irradiation induced minor regression of BM sinusoidal endothelial cells (SECs), while lethal irradiation induced severe regression of SECs and required BM transplantation (BMT) for regeneration. Within the BM, VEGFR2 expression specifically demarcated a continuous network of arterioles and SECs, with arterioles uniquely expressing Sca1 and SECs uniquely expressing VEGFR3. Conditional deletion of VEGFR2 in adult mice blocked regeneration of SECs in sublethally irradiated animals and prevented hematopoietic reconstitution. Similarly, inhibition of VEGFR2 signaling in lethally irradiated wild-type mice rescued with BMT severely impaired SEC reconstruction and prevented engraftment and reconstitution of HSPCs. Therefore, regeneration of SECs via VEGFR2 signaling is essential for engraftment of HSPCs and restoration of hematopoiesis. The phenotypic attributes and molecular determinants for the regeneration of bone marrow (BM) sinusoidal endothelial cells (SECs) and their contribution to hematopoiesis are unknown. We show that after myelosuppression VEGFR2 activation promotes reassembly of regressed SECs, reconstituting hematopoietic stem and progenitor cells (HSPCs). VEGFR2 and VEGFR3 expression are restricted to BM vasculature, demarcating a continuous network of VEGFR2 + VEGFR3 + Sca1 − SECs and VEGFR2 + VEGFR3 − Sca1 + arterioles. While chemotherapy (5FU) and sublethal irradiation (650 rad) induce minor SEC regression, lethal irradiation (950 rad) induces severe regression of SECs requiring BM transplantation (BMT) for regeneration. Conditional deletion of VEGFR2 in adult mice blocks regeneration of SECs in sublethally irradiated animals, preventing hematopoietic reconstitution. Inhibition of VEGFR2 signaling in lethally irradiated wild type mice rescued with BMT severely impairs SEC reconstruction, preventing engraftment and reconstitution of HSPCs. Therefore, activation of VEGFR2 is critical for regeneration of VEGFR3 + Sca1 − SECs that are essential for engraftment and restoration of HSPCs and hematopoiesis. Myelosuppression damages the bone marrow (BM) vascular niche, but it is unclear how regeneration of bone marrow vessels contributes to engraftment of transplanted hematopoietic stem and progenitor cells (HSPCs) and restoration of hematopoiesis. We found that chemotherapy and sublethal irradiation induced minor regression of BM sinusoidal endothelial cells (SECs), while lethal irradiation induced severe regression of SECs and required BM transplantation (BMT) for regeneration. Within the BM, VEGFR2 expression specifically demarcated a continuous network of arterioles and SECs, with arterioles uniquely expressing Sca1 and SECs uniquely expressing VEGFR3. Conditional deletion of VEGFR2 in adult mice blocked regeneration of SECs in sublethally irradiated animals and prevented hematopoietic reconstitution. Similarly, inhibition of VEGFR2 signaling in lethally irradiated wild-type mice rescued with BMT severely impaired SEC reconstruction and prevented engraftment and reconstitution of HSPCs. Therefore, regeneration of SECs via VEGFR2 signaling is essential for engraftment of HSPCs and restoration of hematopoiesis. |
| Author | Rosenwaks, Zev Sato, Thomas N. Kranz, Andrea Shido, Koji Witte, Larry Nolan, Daniel J. Pytowski, Bronislaw Rafii, Shahin Butler, Jason M. Kopp, Hans-Georg Petit, Isabelle Hooper, Andrea T. Kobayashi, Mariko Wu, Yan Iida, Kaoruko Zhu, Zhenping Mittal, Vivek Yanger, Kilangsungla James, Daylon |
| AuthorAffiliation | 4 Department of Surgery, Weill Cornell Medical College New York, NY 10065 3 ImClone Systems Incorporated, 180 Varick Street, New York, NY 10014 1 Howard Hughes Medical Institute, Ansary Stem Cell Institute, and Department of Genetic Medicine, Weill Cornell Medical College, New York, NY 10065 2 Department of Cell and Developmental Biology, Weill Cornell Medical College, New York, NY, 10065 |
| AuthorAffiliation_xml | – name: 2 Department of Cell and Developmental Biology, Weill Cornell Medical College, New York, NY, 10065 – name: 1 Howard Hughes Medical Institute, Ansary Stem Cell Institute, and Department of Genetic Medicine, Weill Cornell Medical College, New York, NY 10065 – name: 4 Department of Surgery, Weill Cornell Medical College New York, NY 10065 – name: 3 ImClone Systems Incorporated, 180 Varick Street, New York, NY 10014 |
| Author_xml | – sequence: 1 givenname: Andrea T. surname: Hooper fullname: Hooper, Andrea T. organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 2 givenname: Jason M. surname: Butler fullname: Butler, Jason M. organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 3 givenname: Daniel J. surname: Nolan fullname: Nolan, Daniel J. organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 4 givenname: Andrea surname: Kranz fullname: Kranz, Andrea organization: Department of Cell and Developmental Biology, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 5 givenname: Kaoruko surname: Iida fullname: Iida, Kaoruko organization: Department of Cell and Developmental Biology, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 6 givenname: Mariko surname: Kobayashi fullname: Kobayashi, Mariko organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 7 givenname: Hans-Georg surname: Kopp fullname: Kopp, Hans-Georg organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 8 givenname: Koji surname: Shido fullname: Shido, Koji organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 9 givenname: Isabelle surname: Petit fullname: Petit, Isabelle organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 10 givenname: Kilangsungla surname: Yanger fullname: Yanger, Kilangsungla organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 11 givenname: Daylon surname: James fullname: James, Daylon organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 12 givenname: Larry surname: Witte fullname: Witte, Larry organization: ImClone Systems Incorporated, 180 Varick Street, New York, NY 10014, USA – sequence: 13 givenname: Zhenping surname: Zhu fullname: Zhu, Zhenping organization: ImClone Systems Incorporated, 180 Varick Street, New York, NY 10014, USA – sequence: 14 givenname: Yan surname: Wu fullname: Wu, Yan organization: ImClone Systems Incorporated, 180 Varick Street, New York, NY 10014, USA – sequence: 15 givenname: Bronislaw surname: Pytowski fullname: Pytowski, Bronislaw organization: ImClone Systems Incorporated, 180 Varick Street, New York, NY 10014, USA – sequence: 16 givenname: Zev surname: Rosenwaks fullname: Rosenwaks, Zev organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 17 givenname: Vivek surname: Mittal fullname: Mittal, Vivek organization: Department of Surgery, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 18 givenname: Thomas N. surname: Sato fullname: Sato, Thomas N. organization: Department of Cell and Developmental Biology, Weill Cornell Medical College, New York, NY 10065, USA – sequence: 19 givenname: Shahin surname: Rafii fullname: Rafii, Shahin email: srafii@med.cornell.edu organization: Howard Hughes Medical Institute, Weill Cornell Medical College, New York, NY 10065, USA |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=21839879$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/19265665$$D View this record in MEDLINE/PubMed |
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| Snippet | Myelosuppression damages the bone marrow (BM) vascular niche, but it is unclear how regeneration of bone marrow vessels contributes to engraftment of... The phenotypic attributes and molecular determinants for the regeneration of bone marrow (BM) sinusoidal endothelial cells (SECs) and their contribution to... |
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| SubjectTerms | Animals Ataxin-1 Ataxins Biological and medical sciences Blood Vessels - physiology Bone Marrow - blood supply Cell differentiation, maturation, development, hematopoiesis Cell physiology Endothelium, Vascular - cytology Endothelium, Vascular - drug effects Endothelium, Vascular - physiology Endothelium, Vascular - radiation effects Fundamental and applied biological sciences. Psychology Hematopoiesis Hematopoietic Stem Cell Transplantation Hematopoietic Stem Cells - cytology Hematopoietic Stem Cells - metabolism Hematopoietic Stem Cells - physiology Mice Mice, Knockout Molecular and cellular biology Nerve Tissue Proteins - biosynthesis Nuclear Proteins - biosynthesis Regeneration Sequence Deletion Signal Transduction STEMCELL Vascular Endothelial Growth Factor Receptor-2 - genetics Vascular Endothelial Growth Factor Receptor-2 - metabolism Whole-Body Irradiation |
| Title | Engraftment and Reconstitution of Hematopoiesis Is Dependent on VEGFR2-Mediated Regeneration of Sinusoidal Endothelial Cells |
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