A substantial body of data now indicate that megakaryocytopoiesis is regulated, like erythropoiesis, on at least two levels--a constitutive maintenance of progenitor cells and a megakaryocyte pool that respond to thrombopoietic stimuli in response to altered platelet demand. The above model is assembled on the following observations: (a) Megakaryocyte progenitors are not regulated by platelet mass and therefore are not controlled via thrombopoietin, (b) IL-3 is the most potent stimulator of megakaryocyte progenitor cells described thus far, and therefore is a likely candidate for in-vivo maintenance of progenitor cell numbers, (c) thrombopoietin is the major stimulus for megakaryocyte development into platelets with their subsequent release into the circulation. Can such a model meet physiological requirements? It is not clear that IL-3 can be produced in the bone marrow. At best it can be speculated that megakaryocyte progenitors are sustained by an "IL-3-like" or GM-CSF mechanism but the triggering mechanism may be membrane bound or via a separate molecule that activates a similar mechanism. It is quite possible that IL-3 has little to do with normal megakaryocytopoiesis, and that IL-3 levels are elevated only in immune responses that stimulate T cells to release IL-3. It is now known that IL-3 will stimulate all levels of megakaryocyte development, and this system may be a thrombopoietin-independent nonspecific mechanism of platelet formation. Such a concept demands that IL-3 can stimulate platelet release in the in-vivo thrombopoietin assay, as should appropriate stimulation in vivo by a strong and specific T-cell mitogen. A second hypothesis is that IL-3 may be involved in a synergistic pathway with either TSF or thrombopoietin, based on the synergy between these two types of activities in cell culture. This concept requires that IL-3 be produced in very low but active amounts in the bone marrow or by an IL-3-like mechanism. Amplification of the IL-3-type-induced signal would then depend on the second factor. This mode requires only low levels of IL-3 (may be sub-threshold by Northern blot analysis or biological assays). Synergy with thrombopoietin with IL-3 or an IL-3-like mechanism would mean that only low levels of thrombopoietin would also be required to sustain normal megakaryocytopoiesis. This concept fits earlier data where thrombopoiesis persists at reduced rates in transfusion-induced thrombocytotic mice. Thus, in thrombocytopenic conditions, when thrombopoietin levels become elevated, an increased rate of megakaryocytopoiesis would be observed.(ABSTRACT TRUNCATED AT 400 WORDS)