Abstract
Amphibians represent the first phylogenetic group to possess hematopoietic bone marrow. However, adult amphibian hematopoiesis has only been described in a few species and with conflicting data. Bone marrow, kidney, spleen, liver, gut, stomach, lung, tegument, and heart were therefore collected from adult Lithobates catesbeianus and investigated by light microscopy and immunohistochemical methods under confocal laser microscopy. Our study demonstrated active hematopoiesis in the bone marrow of vertebrae, femur, and fingers and in the kidney, but no hematopoietic activity inside other organs including the spleen and liver. Blood cells were identified as a heterogeneous cell population constituted by heterophils, basophils, eosinophils, monocytes, erythrocytic cells, lymphocytes, and their precursors. Cellular islets of the thrombocytic lineage occurred near sinusoids of the bone marrow. Antibodies against CD34, CD117, stem cell antigen, erythropoietin receptor, and the receptor for granulocyte colony-stimulating factor identified some cell populations, and some circulating immature cells were seen in the bloodstream. Thus, on the basis of these phylogenetic features, we propose that L. catesbeianus can be used as an important model for hematopoietic studies, since this anuran exhibits hematopoiesis characteristics both of lower vertebrates (renal hematopoiesis) and of higher vertebrates (bone marrow hematopoiesis).
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References
Almeida PG, Felsenburgh FA, Brito-Gitirana L de (2007) Morphological re-evaluation of the parotoid glands of Bufo ictericus (Amphibia, Anura, Bufonidae). Contrib Zool 76:145–152
Azevedo RA, Carvalho HF, Brito-Gitirana L de (2007) Hyaluronan localization in epidermal and dermal extracellular matrix of the Brazilian toad integument using the FITC-labeled hyaluronan probe. Micron (Oxford) 38:607–661
Baumhueter S, Dybdal N, Kyle C, Lasky LA (1994) Global expression of murine CD34, a sialomucin-like endothelial ligand for L-selectin. Blood 84:2554–2565
Bernaudin M, Marti HH, Roussel S, Divoux D, Nouvelot A, MacKenzie ET, Petit E (1999) A potential role for erythropoietin in focal permanent cerebral ischemia in mice. J Cereb Blood Flow Metab 19:643–651
Blair CH, Dong SS, Julian BA (1999) Expression of stem cell factor by osteoblasts in normal and hyperparathyroid bone: relation to ectopic mast cell differentiation. Virchows Arch 435:50–57
Bogomoletz W (1980) Advantages of the Sirius red staining method for amyloid and eosinophils. Arch Anat Cytol Pathol 28:252–253
Brandt J, Briddell RA, Srour EF, Leemhuis TB, Hoffman R (1992) Role of c-kit ligand in the expansion of human hematopoietic progenitor cells. Blood 79:634–641
Broudy VC, Morgan DA, Lin N, Zsebo KM, Jacobsen FW, Papayannopoulou T (1993) Stem cell factor influences the proliferation and erythroid differentiation of the MB-02 human erythroleukemia cell line by binding to a high-affinity c-kit receptor. Blood 82:436–444
Campbell FR (1970) Ultrastructure of the bone marrow of the frog. Am J Anat 129:329–356
Carson FL, Martin JH, Lynn JA (1973) Formalin fixation for electron microscopy: a re-evaluation. Am J Clin Pathol 59:365–373
Cianciarullo AM, Beçak W, Soares MJ (1999) Immunocytochemical mapping of the hemoglobin biosynthesis site in amphibian erythroid cells. Tissue Cell 31:342–348
Cianciarullo AM, Bertho AL, Meirelles MD (2000) Mitochondrial kinetics during amphibian erythropoiesis related to haeme synthesis. Cell Biol Int 24:183–192
Cumano A, Godin I (2007) Ontogeny of the hematopoietic system. Annu Rev Immunol 25:745–785
Curtis SK, Cowden RR, Nagel JW (1979) Ultrastructural and histochemical features of the thymus glands of the adult lungless salamander, Plethodon glutinosus (Caudata: Plethodontidae). J Morphol 160:241–274
D'Andrea AD, Zon LI (1990) Erythropoietin receptor. Subunit structure and activation. J Clin Invest 86:681–687
Demetri GD, Griffin JD (1991) Granulocyte colony-stimulating factor and its receptor. Blood 78:2791–2808
Duellmann WR, Trueb L (1994) Biology of amphibians. Johns Hopkins University Press, Baltimore
Frank G (1989) Granulopoiesis in tadpoles of Rana esculenta: ultrastructural observations on the developing granulocytes and on the development of eosinophil granules. J Anat 163:97–105
Gomori G (1936) Microchemical demonstration of iron. Am J Pathol 12:655–659
Gordon MY (1993) Human haemopoietic stem cell assays. Blood Rev 7:190–197
Götze KS, Schiemann M, Marz S, Jacobs VR, Debus G, Peschel C, Oostendorp RA (2007) CD133-enriched CD34− (CD33/CD38/CD71)− cord blood cells acquire CD34 prior to cell division and hematopoietic activity is exclusively associated with CD34 expression. Exp Hematol 35:1408–1414
Hadji-Azimi I, Coosemans V, Canicatti C (1987) Atlas of adult Xenopus laevis laevis hematology. Dev Comp Immunol 11:807–874
Heasman J (2006) Patterning the early Xenopus embryo development. Development 133:1205–1217
Huang X, Cho S, Spangrude GJ (2007) Hematopoietic stem cells: generation and self-renewal. Cell Death Differ 14:1851–1859
Jelkmann W (2007) Erythropoietin after a century of research: younger than ever. Eur J Hematol 78:183–205
Jordan HE (1919) The histology of the blood and the red bone-marrow of the leopard frog, Rana pipiens. Am J Anat 25:437–480
Jordan HE, Speidel CC (1923) Studies on lymphocytes. I. Effect of splenectomy, experimental hemorrhage and a hemolytic toxin in the frog. Am J Anat 32:155–187
Kao KR, Bernstein A (1995) Expression of Xkl-1, a Xenopus gene related to mammalian c-kit, in dorsal embryonic tissue. Mech Dev 50:57–69
Kierszenbaum AL (2002) Histology and cell biology: an introduction to pathology. Mosby, St. Louis
Krause DS, Fackler MJ, Civin CI, May WS (1996) CD34: structure, biology and clinical utility. Blood 87:1–13
Lennert K (1978) Malignant lymphomas other than Hodgkin’s disease: histology, cytology, ultrastructure, immunology. Springer, Berlin
Lillie RD, Fullmer HM (1976) Histopathological technic and practical histochemistry. McGraw-Hill, New York
Liu F, Poursine-Laurent J, Link DC (2000) Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF. Blood 95:3025–3031, 15
McManus JFA (1946) Histological demonstration of mucin after periodic acid. Nature 158:202
Maniatis GM, Ingram VM (1971) Erythropoiesis during amphibian metamorphosis. I. Site of maturation of erythrocytes in Rana catesbeiana. J Cell Biol 49:372–379
Mayer P (1903) Notiz über Hämateïn und Hämalaun. Z Wiss Mikrosk Mikrosk Tech 20:409
Meseguer J, Lozano MT, Agulleiro B (1985) Ultrastructure of the renal granulopoietic tissue of the Rana ridibunda tadpole. J Submicrosc Cytol 17:391–401
Nicola NA, Johnson GR (1982) The production of committed hemopoietic colony-forming cells from multipotential precursors in vitro. Blood 60:1019–1029
NIH (2001) Stem cells: scientific progress and future research directions. Department of Health and Human Services; http://stemcells.nih.gov/info/scireport/2001report (accessed 18 August 2008)
Ogawa M, Porter PN, Nakahata T (1983) Renewal and commitment to differentiation of hemopoietic stem cells: an interpretive review. Blood 61:823–829
Ong RC, Maéno M, Kung HF (1993) Murine stem cell factor stimulates erythropoietic differentiation of ventral mesoderm in Xenopus gastrula embryo. Exp Cell Res 205:326–330
Raucci F, Di Fiore MM (2007) The c-kit receptor protein in the testis of green frog Rana esculenta: seasonal changes in relationship to testosterone titres and spermatogonial proliferation. Reproduction 133:51–60
Raucci F, Di Fiore MM, Pinelli C, D'Aniello B, Luongo L, Polese G, Rastogi RK (2006) Proliferative activity in the frog brain: a PCNA-immunohistochemistry analysis. J Chem Neuroanat 32:127–142
Rodak BF (1995) Diagnostic hematology. Saunders, Philadelphia
Shoemaker VH, Nagy KA (1977) Osmoregulation in amphibians and reptiles. Annu Rev Physiol 39:449–471
Surbis AY (1978) Ultrastructural study of granulocytes of Bufo marinus. Florida Scientist 41:45–52
Tanaka Y (1976) Architecture of the marrow vasculature in three amphibian species and its significance in hematopoietic development. Am J Anat 145:485–497
Thomas N, Maclean N (1974) The blood as an erythropoietic organ in anaemic Xenopus. Experimentia 30:1083–1085, 15
Till JE, McCulloch EA, Siminovitch L (1964) A stochastic model of stem cell proliferation, based on the growth of spleen colony forming cells. Proc Nati Acad Sci USA 51:29–36
Uchiyama M, Kamijyo M, Katayama M, Matsuda K, Yoshizawa H (2001) Correlation of the habitats and the kidney structures in anuran amphibians. Zool Sci 18(Suppl):113
Wehrend A, Hetzel U, Huchzermeyer S, Klein C, Bostedt H (2004) Sirius red is able to selectively stain eosinophil granulocytes in bovine, ovine and equine cervical tissue. Anat Histol Embryol 33:180–182
Yergeau DA, Schmerer M, Kuliyev E, Evans T, Mead PE (2006) Cloning and expression pattern of the Xenopus erythropoietin receptor. Gene Expr Patterns 6:420–425
Zapata AG, Torroba M, Vicente A, Varas A, Sacedón R, Jiménez E (1995) The relevance of cell microenvironments for the appearance of lympho-haemopoietic tissues in primitive vertebrates. Histol Histopathol 10:761–778
Zucker-Franklin D, Greaves MF, Grossi CE, Marmont AM (1988) Atlas of blood cells: function and pathology, 2nd edn. Ermes, Milan
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de Abreu Manso, P.P., de Brito-Gitirana, L. & Pelajo-Machado, M. Localization of hematopoietic cells in the bullfrog (Lithobates catesbeianus). Cell Tissue Res 337, 301–312 (2009). https://doi.org/10.1007/s00441-009-0803-0
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DOI: https://doi.org/10.1007/s00441-009-0803-0