Myelopoiesis of the Amphibian Xenopus laevis Is Segregated to the Bone Marrow, Away From Their Hematopoietic Peripheral Liver

Abstract

Across vertebrates, hematopoiesis takes place within designated tissues, wherein committed myeloid progenitors further differentiate toward cells with megakaryocyte/erythroid potential (MEP) or those with granulocyte/macrophage potential (GMP). While the liver periphery (LP) of the Xenopus laevis amphibian functions as a principal site of hematopoiesis and contains MEPs, cells with GMP potential are instead segregated to the bone marrow (BM) of this animal. Presently, using gene expression and western blot analyses of blood cell lineage-specific transcription factors, we confirmed that while the X. laevis LP hosts hematopoietic stem cells and MEPs, their BM contains GMPs. In support of our hypothesis that cells bearing GMP potential originate from the frog LP and migrate through blood circulation to the BM in response to chemical cues; we demonstrated that medium conditioned by the X. laevis BM chemoattracts LP and peripheral blood cells. Compared to LP and by examining a comprehensive panel of chemokine genes, we showed that the X. laevis BM possessed greater expression of a single chemokine, CXCL12, the recombinant form of which was chemotactic to LP and peripheral blood cells and appeared to be a major chemotactic component within BM-conditioned medium. In confirmation of the hepatic origin of the cells that give rise to these frogs' GMPs, we also demonstrated that the X. laevis BM supported the growth of their LP-derived cells.

From Species to Regional and Local Specialization of Intestinal Macrophages

“…In the frog Xenopus laevis , the principal site of hematopoiesis is still the liver subcapsular region, but myelopoiesis, i.e., the differentiation of the granulocyte MF precursor (GMP) into granulocytes and MFs, occurs in the bone marrow (Grayfer and Robert, 2013 ; Yaparla et al, 2016 ). Precursors with GMP potential migrate from the liver to the bone marrow under the influence of chemokines enriched in the bone marrow, such as CXCL12 (Yaparla et al, 2019 ). MF differentiation is controlled through binding of the main MF growth factor, colony-stimulating factor-1 (CSF1) to its CSF1 receptor (CSF1R), which is almost exclusively expressed on committed MF precursors (Grayfer and Robert, 2016 ).…”

Hematopoiesis: A Layered Organization Across Chordate Species

“…The peripheral region of the liver was shown to be the primary hematopoietic organ throughout life containing HSC and erythroid progenitors, whereas the BM contains myeloid progenitors that respond to myeloid growth factors (Yaparla et al, 2019). Lymphocytes are produced in the thymus and the spleen in juvenile frogs, whereas the BM and the thymus have lymphopoietic activity in the adult (Greenhalgh et al, 1993).…”

Do blood parasites increase immature erythrocytes and mitosis in amphibians?

“…In Xenopus laevis, the aquatic toad, vascularization in bone marrow is rudimentary. In this species, erythropoiesis occurs in the liver (Nogawa-Kosaka et al, 2011;Okui et al, 2013), and myelopoiesis is restricted to the bone marrow (Yaparla, Reeves, & Grayfer, 2020). In terrestrial amphibians, as Lithobates catesbeianus, the bone marrow vascularization is more complex, similar to mammalian vascularization (Tanaka, 1976).…”