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      Heme Oxygenase-1: A Critical Link between Iron Metabolism, Erythropoiesis, and Development

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          Abstract

          The first mature cells to arise in the developing mammalian embryo belong to the erythroid lineage. This highlights the immediacy of the need for red blood cells during embryogenesis and for survival. Linked with this pressure is the necessity of the embryo to obtain and transport iron, synthesize hemoglobin, and then dispose of the potentially toxic heme via the stress-induced protein heme oxygenase-1 (HO-1, encoded by Hmox1 in the mouse). Null mutation of Hmox1 results in significant embryonic mortality as well as anemia and defective iron recycling. Here, we discuss the interrelated nature of this critical enzyme with iron trafficking, erythroid cell function, and embryonic survival.

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          Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse.

          J Palis, S. Robertson, M. Kennedy … (1999)
          In this study, we have mapped the onset of hematopoietic development in the mouse embryo using colony-forming progenitor assays and PCR-based gene expression analysis. With this approach, we demonstrate that commitment of embryonic cells to hematopoietic fates begins in proximal regions of the egg cylinder at the mid-primitive streak stage (E7.0) with the simultaneous appearance of primitive erythroid and macrophage progenitors. Development of these progenitors was associated with the expression of SCL/tal-1 and GATA-1, genes known to be involved in the development and maturation of the hematopoietic system. Kinetic analysis revealed the transient nature of the primitive erythroid lineage, as progenitors increased in number in the developing yolk sac until early somite-pair stages of development (E8.25) and then declined sharply to undetectable levels by 20 somite pairs (E9.0). Primitive erythroid progenitors were not detected in any other tissue at any stage of embryonic development. The early wave of primitive erythropoiesis was followed by the appearance of definitive erythroid progenitors (BFU-E) that were first detectable at 1-7 somite pairs (E8.25) exclusively within the yolk sac. The appearance of BFU-E was followed by the development of later stage definitive erythroid (CFU-E), mast cell and bipotential granulocyte/macrophage progenitors in the yolk sac. C-myb, a gene essential for definitive hematopoiesis, was expressed at low levels in the yolk sac just prior to and during the early development of these definitive erythroid progenitors. All hematopoietic activity was localized to the yolk sac until circulation was established (E8.5) at which time progenitors from all lineages were detected in the bloodstream and subsequently in the fetal liver following its development. This pattern of development suggests that definitive hematopoietic progenitors arise in the yolk sac, migrate through the bloodstream and seed the fetal liver to rapidly initiate the first phase of intraembryonic hematopoiesis. Together, these findings demonstrate that commitment to hematopoietic fates begins in early gastrulation, that the yolk sac is the only site of primitive erythropoiesis and that the yolk sac serves as the first source of definitive hematopoietic progenitors during embryonic development.
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            The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase.

            R Tenhunen, H Marver, R SCHMID (1968)
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              Erythroblastic islands: niches for erythropoiesis.

              Joel Anne Chasis, Narla Mohandas (2008)
              Erythroblastic islands, the specialized niches in which erythroid precursors proliferate, differentiate, and enucleate, were first described 50 years ago by analysis of transmission electron micrographs of bone marrow. These hematopoietic subcompartments are composed of erythroblasts surrounding a central macrophage. A hiatus of several decades followed, during which the importance of erythroblastic islands remained unrecognized as erythroid progenitors were shown to possess an autonomous differentiation program with a capacity to complete terminal differentiation in vitro in the presence of erythropoietin but without macrophages. However, as the extent of proliferation, differentiation, and enucleation efficiency documented in vivo could not be recapitulated in vitro, a resurgence of interest in erythroid niches has emerged. We now have an increased molecular understanding of processes operating within erythroid niches, including cell-cell and cell-extracellular matrix adhesion, positive and negative regulatory feedback, and central macrophage function. These features of erythroblast islands represent important contributors to normal erythroid development, as well as altered erythropoiesis found in such diverse diseases as anemia of inflammation and chronic disease, myelodysplasia, thalassemia, and malarial anemia. Coupling of historical, current, and future insights will be essential to understand the tightly regulated production of red cells both in steady state and stress erythropoiesis.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Adv Hematol
                Journal ID (publisher-id): AH
                Title: Advances in Hematology
                Publisher: Hindawi Publishing Corporation
                ISSN (Print): 1687-9104
                ISSN (Electronic): 1687-9112
                Publication date (Print): 2011
                Publication date (Electronic): 20 November 2011
                Volume: 2011
                Electronic Location Identifier: 473709
                Affiliations
                1Laboratory for Blood Cell Development, Disciplines of Physiology, Anatomy and Histology, School of Medical Sciences and Bosch Institute, University of Sydney, Medical Foundation Building, 92-94 Parramatta Road, Camperdown, NSW 2050, Australia
                2Center for Vascular Research, Discipline of Pathology, School of Medical Sciences and Bosch Institute, University of Sydney, Medical Foundation Building, 92–94 Parramatta Road, Camperdown, NSW 2050, Australia
                Author notes

                Academic Editor: S. Ballas

                Article
                DOI: 10.1155/2011/473709
                PMC ID: 3226344
                PubMed ID: 22162689
                SO-VID: 9c8625f8-de38-42fe-9818-13498c8f62dd
                Copyright © Copyright © 2011 Stuart T. Fraser et al.
                License:

                This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 28 June 2011
                Date revision received : 13 September 2011
                Date accepted : 15 September 2011
                Categories
                Subject: Review Article

                ScienceOpen disciplines: Hematology
                Data availability:
                ScienceOpen disciplines: Hematology

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