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Blood, 15 December 2000, Vol. 96, No. 13, pp. 4152-4159
HEMATOPOIESIS
Stromal-derived factor 1-induced megakaryocyte migration and
platelet production is dependent on matrix metalloproteinases
William J. Lane,
Sergio Dias,
Koichi Hattori,
Beate Heissig,
Margaret Choy,
Sina Y. Rabbany,
Jeanette Wood,
Malcolm A. S. Moore, and
Shahin Rafii
From the Division of Hematology-Oncology, Weill
Medical College of Cornell University, Ithaca, NY; the Bioengineering
Program, Hofstra University, Hempstead, NY; Oncology Research, Novartis
Pharma AG, Basel, Switzerland; and the Division of Developmental
Hematopoiesis, Sloan Kettering Cancer Center, New York, NY.
Despite the discovery of thrombopoietin (TPO) and its contribution
to megakaryocytopoiesis, the exact mechanisms and sites of platelet
production are unknown. It has been shown that mature megakaryocytes
(MKs) functionally express the stromal-derived factor 1 (SDF-1)
receptor, CXCR4. SDF-1-induced migration of mature MKs through
endothelial cell layers results in increased platelet production.
Because the migration of polyploid MKs from the bone marrow
microenvironment requires remodeling of the perivascular extracellular
matrix, it was hypothesized that mature polyploid MKs may express
matrix metalloproteinases (MMPs), facilitating their exit into the bone
marrow extravascular space. In this report, it is demonstrated that
SDF-1 induces the expression and release of gelatinase B (MMP-9) by
purified mature polyploid human MKs and an adeno-CXCR4-infected
megakaryocytic cell line. Neutralizing antibody to MMP-9, but not
MMP-2, blocked SDF-1-induced migration of MKs through reconstituted
basement membrane, suggesting that expression of MMP-9 is critical for
MK migration. Incubation of mature MKs with a synthetic MMP inhibitor,
5-phenyl-1,10-phenanthrolene, resulted in the inhibition of platelet
formation, suggesting that the expression of MMPs is not only critical
for megakaryocyte migration but also for subsequent platelet release.
Confirming these results, adeno-SDF-1 injection into normal mice
resulted in increased platelet counts, a process that could be blocked by a synthetic MMP inhibitor. These results suggest mobilization of MKs
involves sequential expression and activation of chemokine receptors
such as CXCR4, MMP-9, followed by transendothelial migration. MMP
inhibitors may have potential use in the treatment of thrombotic and
myeloproliferative disorders.
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