Vascular Endothelial Growth Factor and Angiopoietin-1 Stimulate Postnatal Hematopoiesis by Recruitment of Vasculogenic and Hematopoietic Stem Cells

doi:10.1084/jem.193.9.1005

Published online 30 April 2001.

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© The Rockefeller University Press, 0022-1007/2001/5/1005/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 9, May 7, 2001 1005-1014

Original Article

Vascular Endothelial Growth Factor and Angiopoietin-1 Stimulate Postnatal Hematopoiesis by Recruitment of Vasculogenic and Hematopoietic Stem Cells

Koichi Hattori^a,c, Sergio Dias^a, Beate Heissig^a, Neil R. Hackett^b, David Lyden^c, Masatoshi Tateno^d, Daniel J. Hicklin^e, Zhenping Zhu^e, Larry Witte^e, Ronald G. Crystal^b, Malcolm A.S. Moore^c, and Shahin Rafii^a
^a Division of Hematology-Oncology, Critical Care Medicine and Genetic Medicine Program, Cornell University Medical College, New York, New York 10021
^b Division of Pulmonary, Critical Care Medicine and Genetic Medicine Program, Cornell University Medical College, New York, New York 10021
^c Sloan-Kettering Institute for Cancer Research, New York, New York 10021
^d Department of Pathology, Sapporo City General Hospital, Sapporo 060-8604, Japan
^e ImClone Systems Inc., New York, New York 10014

Correspondence to: Shahin Rafii, Cornell University Medical College, Division of Hematology-Oncology, 1300 York Ave., Rm. C-606, New York, NY 10021. Tel:212-746-2070 Fax:212-746-8866 E-mail:srafii{at}mail.med.cornell.edu.

Tyrosine kinase receptors for angiogenic factors vascular endothelialgrowth factor (VEGF) and angiopoietin-1 (Ang-1) are expressednot only by endothelial cells but also by subsets of hematopoieticstem cells (HSCs). To further define their role in the regulationof postnatal hematopoiesis and vasculogenesis, VEGF and Ang-1plasma levels were elevated by injecting recombinant proteinor adenoviral vectors expressing soluble VEGF₁₆₅, matrix-boundVEGF₁₈₉, or Ang-1 into mice. VEGF₁₆₅, but not VEGF₁₈₉, induceda rapid mobilization of HSCs and VEGF receptor (VEGFR)2⁺ circulatingendothelial precursor cells (CEPs). In contrast, Ang-1 induceddelayed mobilization of CEPs and HSCs. Combined sustained elevationof Ang-1 and VEGF₁₆₅ was associated with an induction of hematopoiesisand increased marrow cellularity followed by proliferation ofcapillaries and expansion of sinusoidal space. Concomitant tothis vascular remodeling, there was a transient depletion ofhematopoietic activity in the marrow, which was compensatedby an increase in mobilization and recruitment of HSCs and CEPsto the spleen resulting in splenomegaly. Neutralizing monoclonalantibody to VEGFR2 completely inhibited VEGF₁₆₅, but not Ang-1–inducedmobilization and splenomegaly. These data suggest that temporaland regional activation of VEGF/VEGFR2 and Ang-1/Tie-2 signalingpathways are critical for mobilization and recruitment of HSCsand CEPs and may play a role in the physiology of postnatalangiogenesis and hematopoiesis.

Key Words: vascular endothelial growth factor, angiopoietin-1, angiogenesis,hematopoiesis, tyrosine kinase receptors

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