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J. Biol. Chem., Vol. 281, Issue 29, 20181-20189, July 21, 2006

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Absence of Erythroblast Macrophage Protein (Emp) Leads to Failure of Erythroblast Nuclear Extrusion^*

Shivani Soni¹, Shashi Bala¹, Babette Gwynn, Kenneth E. Sahr, Luanne L. Peters, and Manjit Hanspal²

From the Department of Medicine, Center for Cell Biology, Caritas St. Elizabeth's Medical Center, Tufts University School of Medicine, Boston, Massachusetts 02135 and the Jackson Laboratory, Bar Harbor, Maine 04609

In mammals, the functional unit for definitive erythropoiesis is the erythroblastic island, a multicellular structure composed of a central macrophage surrounded by developing erythroblasts. Erythroblast-macrophage interactions play a central role in the terminal maturation of erythroblasts, including enucleation. One possible mediator of this cell-cell interaction is the protein Emp (erythroblast macrophage protein). We used targeted gene inactivation to define the function of Emp during hematopoiesis. Emp null embryos die perinatally and show profound alterations in the hematopoietic system. A dramatic increase in the number of nucleated, immature erythrocytes is seen in the peripheral blood of Emp null fetuses. In the fetal liver virtually no erythroblastic islands are observed, and the number of F4/80-positive macrophages is substantially reduced. Those present lack cytoplasmic projections and are unable to interact with erythroblasts. Interestingly, wild type macrophages can bind Emp-deficient erythroblasts, but these erythroblasts do not extrude their nuclei, suggesting that Emp impacts enucleation in a cell autonomous fashion. Previous studies have implicated the actin cytoskeleton and its reorganization in both erythroblast enucleation as well as in macrophage development. We demonstrate that Emp associates with F-actin and that this interaction is important in the normal distribution of F-actin in both erythroblasts and macrophages. Thus, Emp appears to be required for erythroblast enucleation and in the development of the mature macrophages. The availability of an Emp null model provides a unique experimental system to study the enucleation process and to evaluate the function of macrophages in definitive erythropoiesis.

Received for publication, April 5, 2006 , and in revised form, May 12, 2006.

^* This work was supported by National Institutes of Health Grants AI 50600 (to M. H.) and HL075714 (to L. L. P.). A preliminary account of this work was presented in abstract form at the forty seventh Annual Meeting of the American Society of Hematology in Atlanta, GA, 2005. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These authors contributed equally to this work.

² To whom correspondence should be addressed: Center for Cell Biology, CBR 406, Caritas St. Elizabeth's Medical Center, Boston, MA 02135. Tel.: 617-789-2677; Fax: 617-789-3111; E-mail: manjit.hanspal{at}tufts.edu.

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