Ontogeny of Amphibian Hemopoietic Cells

  • James B. Turpen
  • Nicholas Cohen
  • Pierre Deparis
  • André Jaylet
  • Robert Tompkins
  • E. Peter Volpe

Abstract

The developmental origin of lymphoid cells of vertebrates continues to be a fascinating, perplexing problem. Historically, the disputable issues have revolved around two fundamental aspects: the origin of the precursors of the various types of differentiated blood cells and the lineal relationships among these different cell types. There are special features of amphibians that make them suitable for clarifying the embryogenesis of hemopoietic cells. An array of microsurgical techniques from experimental embryology can be used to marked advantage. In this chapter, we will review the contributions made by investigators who have used the tools of experimental embryology to gain insight into the ontogeny of vertebrate blood cells.

Keywords

Migration Meso Clarification Ster Hema 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Baldwin, F. M., 1918, Pharyngeal derivatives of Amblystoma, J. Morphol. 30:605.CrossRefGoogle Scholar
  2. Carpenter, K. L., and Turpen, J. B., 1979, Experimental studies on hemopoiesis in the pronephros of Rana pipiens, Differentiation 14:167.PubMedCrossRefGoogle Scholar
  3. Charlemagne, J., 1977, Thymus development in amphibians: Colonization of thymic endodermal rudiments by lymphoid stem-cells of mesenchymal origin in the urodele Pleurodeles waltlii Michah, Ann. Immunol. (Inst. Pasteur) 128C:897.Google Scholar
  4. Chertkov, J. L., Gelfand, I. M, Gurevitch, O. A., Lemeneva, L. N., and Udalov, G. A., 1979, Hybrid resistance to parental bone marrow transplantation—Adaptive modification of hemopoietic stem cell in a non-syngeneic environment, Proc. Natl. Acad. Sci. USA 76:2955.PubMedCrossRefGoogle Scholar
  5. Deparis, P., and Jaylet, A., 1975, Recherches sur l’origine des differentes lingnées de cellales sanguines chez l’amphibien Pleurodeles waltlii, J. Embiyol. Exp. Morphol 33:665.Google Scholar
  6. Deparis, P., and Jaylet, A., 1976, Thymic lymphocyte origin in the newt Pleurodeles waltlii studied by embryonic grafts between diploid and tetraploid embryos. Ann. Immunol. (Paris) 127C:827.Google Scholar
  7. Deparis, P., Beetschen, J. C., and Jaylet, A., 1975, Red blood cells and hemoglobin concentration in normal diploid and several types of polyploid Salamanders, Comp. Biochem. Physiol. 50A:263.CrossRefGoogle Scholar
  8. Desvaux, M., 1974, Etude de la morphogenese du thymus chez Pleurodeles waltlii Michah, Bull. Soc. Zool. 99:259.Google Scholar
  9. Fales, D. E., 1935, Experiments on the development of the pronephros of Amblystoma punctatum, J. Exp. tool. 72:147.Google Scholar
  10. Federici, H., 1926, Recherches expérimentales sur les pótentialities de l’îlot sanguin ches l’embryon de Rana fusca, Arch. Biol. 36:466.Google Scholar
  11. Fernald, R. L., 1943, The origin and development of the blood islands of Hyla regilla, Univ. Berkeley Calif. Publ. Zool. 51:129.Google Scholar
  12. Finnegan, C. V., 1953, Studies of erythropoesis in Salamander embryos, J. Exp. Zool. 123:379.CrossRefGoogle Scholar
  13. Fraser, E. A., 1950, The Development of the Vertebrate Excretory System, Biol. Rev. Cambridge Philos. Soc. 25:159.CrossRefGoogle Scholar
  14. Gallien, L., and Dorocher, M., 1957, Table chronologique du développement chez Pleurodeles waltlii Michah, Bull. Biol. Fr. Belg. 91:97.Google Scholar
  15. Goss, C. M., 1928, Experimental removal of the blood island of Amblystoma punctatum embryos, J. Exp. Zool. 52:45.CrossRefGoogle Scholar
  16. Hollyfield, J. G., 1966, The origin of erythroblasts in Rana pipiens tadpoles, Dev. Biol. 14:461.CrossRefGoogle Scholar
  17. Horton, J. D., 1970, Histogenesis of the lymphomyeloid complex in the larval leopard frog, Rana pipiens, J. Morphol. 134:1.CrossRefGoogle Scholar
  18. Jaylet, A., 1971, Modification du caryotype par une inversion péricentrique à l’état homozygote chez 1’Amphibien Urodele Pleurodeles waltlii Michah, Chromosoma 35:288.PubMedCrossRefGoogle Scholar
  19. Jaylet, A., 1972, Tétraploidie expérimentale chez le Triton Pleurodeles waltlii Michah, Chromosoma 38:173.PubMedCrossRefGoogle Scholar
  20. Jaylet, A., and Deparis, P., 1979, An investigation into the origin of the thymocytes of the newt Pleurodeles waltlii using grafts between normal animals with a marker chromosome, Dev. Comp. Immunol. 3:175.PubMedCrossRefGoogle Scholar
  21. Livini, F., 1902, Organi del sistema timo-tiroidea nella Salamandrina perspicillata, Arch. ltd. Anat. Embriol. 1:3.Google Scholar
  22. Maurer, F., 1888, Schilddrüse, Thymus and Kiemenreste der Amphibien, Morphol. Jahrb. 13:3.Google Scholar
  23. Metcalf, D., and Moore, M. A. S., 1971, Embryonic aspects of haemopoesis in: Haemopoietic Cells (A. Neuberger and E. L. Tatum, eds.), pp. 172–271. North-Holland, Amsterdam.Google Scholar
  24. Moore, M. A. S., and Owen, J. J. T., 1967, Stem cell migration in developing myeloid and lymphoid systems, Lancet 1:658.CrossRefGoogle Scholar
  25. Nagata, S., 1977, Electron microscopic study on the early histogenesis of thymus in the toad, Xenopus laevis, Cell Tissue Res. 179:87.Google Scholar
  26. Shumway, W., 1940, Stages in the normal development of Rana pipiens. I. External form, Anat. Rec. 78:139.CrossRefGoogle Scholar
  27. Slonimski, P., 1931, Recherches experimentales sur la genèse du sang chez les Amphibiens, Arch. Biol. 42:415.Google Scholar
  28. Stohr, P., 1931, Beobachtungen zur Organentwicklung bei erythroztentrei Amphibien larven, Arch. Entwicklungsmech. Org. 124:707.CrossRefGoogle Scholar
  29. Storti, E., 1935, Studio sull’ematopoiesi nella vita embrionale. I. Il periodo preepatico, Arch. Zool. Itd. 21:241.Google Scholar
  30. Taylor, A. C., and Kollros, J. J., 1946, Stages in the normal development of Rana pipiens larvae, Anat. Rec. 94:7.PubMedCrossRefGoogle Scholar
  31. Tochinai, S., 1978, Thymocyte stem cell inflow in Xenopus laevis after grafting diploid thymic rudiments into triploid tadpoles, Dev. Comp. Immunol. 2:627.PubMedCrossRefGoogle Scholar
  32. Tompkins, R., Reinschmidt, D., and Volpe, E. P., 1979, Colonization of the thymic primordium by migratory lymphocytoblasts in amphibian embryos, Dev. Comp. Immunol. 3:635.PubMedCrossRefGoogle Scholar
  33. Tompkins, R., Volpe, E. P., and Reinschmidt, D., 1980, Origin of hemopoietic stem cells in amphibian ontogeny, Development and Differentiation of Vertebrate Lymphocytes (J. D. Horton, ed.), pp. 25–34, Elsevier/North Holland, Amsterdam.Google Scholar
  34. Tournefier, A., 1973, Développment des organes lymphoides chez l’Amphibien Urodèle Triturus alpestris Laur.; tolérance des allograffes après la thymectomie larvaire, J. Embryol. Exp. Morphol. 29:383.PubMedGoogle Scholar
  35. Turpen, J. B., and Cohen, N., 1976b, Alternative sites of lymphopoiesis in the amphibian embryo, Ann. Immunol. (Inst. Pasteur) 127C:841.Google Scholar
  36. Turpen, J. B., and Knudson, C. M., 1982, Ontogeny of hematopoietic cells in Rana pipiens: Precursor cell migration during embryogenesis, Dev. Biol, 89:135.CrossRefGoogle Scholar
  37. Turpen, J. B., Volpe, E. P., and Cohen, N., 1973, Ontogeny and peripheralization of thymic lymphocytes, Science 182:931.PubMedCrossRefGoogle Scholar
  38. Turpen, J. B., Volpe, E. P., and Cohen, N., 1975, On the origin of thymic lymphocytes, Am. Zool. 15:51.Google Scholar
  39. Turpen, J. B., Volpe, E. P., and Cohen, N., 1977, Stem cell influx following heterotropic transplantation of the thymic primordia between frog embryos, Dev. Comp. Immunol. 1:255.PubMedCrossRefGoogle Scholar
  40. Turpen, J. B., Turpen, C. J., and Flajnik, M., 1979, Experimental analysis of hematopoietic cell development in the liver of larval Rana pipiens, Dev. Biol. 69:466.PubMedCrossRefGoogle Scholar
  41. Turpen, J. B., Knudson, C.M., and Hoefen, P. S., 1981, The early ontogeny of hematopoietic cells studied by grafting cytogenetically-labeled tissue anlagen: Localization of a prospective stem cell compartment, Dev. Biol. 85:99.PubMedCrossRefGoogle Scholar
  42. Volpe, E. P., and Turpen, J. B., 1975, Thymus: Central role in the immune system of the frog, Science 190:1101.PubMedCrossRefGoogle Scholar
  43. Volpe, E. P., Tompkins, R., and Reinschmidt, D., 1977, Experimental studies on embryonic derivation of thymic lymphocytes, in: Developmental Immunobiology (J. B. Solomon and J. D. Horton, eds.), pp. 109–114, Elsevier/North-Holland, Amsterdam.Google Scholar
  44. Volpe, E. P., Tompkins, R., and Reinschmidt, D., 1979, Clarification of studies on the origin of thymic lymphocytes, J. Exp. Zool. 208:57.PubMedCrossRefGoogle Scholar
  45. Volpe, E. P., Tompkins, R., and Reinschmidt, D. C., 1981, Evolutionary modifications of nephrogenic mesoderm to establish the embryonic centers of hemopoiesis, in: Aspects of Developmental and Comparative Immunology, (J. B. Solomon, ed.), pp. 192–201, Pergamon Press, Elmsford, N.Y.Google Scholar
  46. Webster, W. D., 1934, The development of the thymus bodies in Necturus maculosus J. Morphol. 56:295.CrossRefGoogle Scholar
  47. Yamada, T., 1937, Der determinationszustand des rumpfmesoderms in molchkeim nach der gas-trulation, Wilhelm Roux Arch. Entwicklungsmech. Org. 137:151.CrossRefGoogle Scholar
  48. Zettergren, L. D., Kubagawa, H., and Cooper, M. D., 1980, Development of B cells in Rana pipiens, in: Phytogeny of Immunological Memory (M. J. Manning, ed.), p. 177, Elsevier/North-Holland, Amsterdam.Google Scholar
  49. Zinkernagel, R. M., Callahan, G. N., Althage, A., Cooper, S., Klein, P. A., and Klein, J., 1978, On the thumus in the differentiation of “H-2 self-recognition” by T cells: Evidence for dual recognition?, J. Exp. Med. 147:882.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1982

Authors and Affiliations

  • James B. Turpen
    • 1
  • Nicholas Cohen
    • 2
  • Pierre Deparis
    • 3
  • André Jaylet
    • 3
  • Robert Tompkins
    • 4
  • E. Peter Volpe
    • 5
  1. 1.Department of BiologyPennsylvania State UniversityUniversity ParkUSA
  2. 2.Department of Microbiology, Division of ImmunologyUniversity of Rochester School of Medicine and DentistryRochesterUSA
  3. 3.Laboratoire de Biologie généraleUniversité Paul SabatierToulouse CedexFrance
  4. 4.Department of BiologyTulane UniversityNew OrleansUSA
  5. 5.Department of Basic Medical Sciences, School of MedicineMercer UniversityMaconUSA

Personalised recommendations