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Membrane assembly and remodeling during reticulocyte maturation
JA Chasis, M Prenant, A Leung and N Mohandas
Cancer Research Institute, University of California, San Francisco 94143.
Membrane skeletal and cytoskeletal remodeling occurs throughout erythroid
maturation. Microtubules and microfilaments have been identified
morphologically in the nucleated erythroblast but the functional capability
of these cytoskeletal structures during reticulocyte maturation has not
been studied. Reticulocytes are formed from orthochromatic normoblasts by
the process of nuclear extrusion. Two recognizable stages of reticulocyte
maturation follow. The least mature reticulocytes are motile and
multilobular, while the more mature reticulocytes are cup-shaped and
nonmotile. To study the respective roles of microtubules and microfilaments
in nuclear extrusion and cell motility, experiments were performed with
agents that perturb these structures. Following the injection into rats of
colchicine, a microtubule-disrupting substance, the number of normoblasts
arrested at the stage of nuclear extrusion increased linearly over four
hours. Similar results were obtained when bone marrow cells were incubated
in culture in the presence of colchicine. In contrast, cell motility was
dramatically decreased by cytochalasin B, a microfilament-disrupting agent,
but not by colchicine. These results imply that microtubules are essential
for the nuclear extrusion process, while microfilaments are essential for
cell motility. Simultaneous changes in membrane skeletal assembly were
assessed by measuring membrane deformability and stability, two properties
regulated by the skeletal proteins. In ektacytometric assays, membrane
deformability and mechanical stability of immature reticulocytes were
markedly decreased to approximately 10% of normal, while that of more
mature reticulocytes were nearly normal. Since the skeletal protein
organization regulates these membrane properties, our findings imply that
substantial membrane skeletal remodeling occurs during reticulocyte
maturation. Thus we have identified major remodeling of both skeletal and
cytoskeletal components during reticulocyte maturation.
Volume 74,
Issue 3,
pp. 1112-1120,
08/15/1989
Copyright © 1989 by The American Society of Hematology
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