Skip to main content
Clinical and Experimental Immunology logoLink to Clinical and Experimental Immunology
. 1971 May;8(5):663–684.

Thymus-dependent and thymus-independent populations; origin, migratory patterns and lifespan*

Delphine M V Parrott, Maria de Sousa
PMCID: PMC1712985  PMID: 5581063

Abstract

It is now accepted that there are present within the peripheral lymphoid tissues of the mammal, lymphocytes which differ in their origin, migratory patterns and lifespan; two major groups have so far been defined, one of thymus-dependent or thymus-derived lymphocytes and another of thymus-independent or bone-marrow derived lymphocytes. These cells which are morphologically indistinguishable when free floating in the blood or lymph nevertheless segregate from one another into clearly defined compartments whilst resident in or passing through the lymph nodes, spleen or Peyer's patches. The purpose of this article is to summarize some of the experimental evidence for this segregation and to discuss its physiological and immunological implications. It is not intended to be an extensive review of the literature.

Full text

PDF
663

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Austin C. M. Patterns of migration of lymphoid cells. Aust J Exp Biol Med Sci. 1968 Oct;46(5):581–593. doi: 10.1038/icb.1968.165. [DOI] [PubMed] [Google Scholar]
  2. Benninghoff D. L., Tyler R. W., Everett N. B. Repopulation of irradiated lymph nodes by recirculating lymphocytes. Radiat Res. 1969 Feb;37(2):381–400. [PubMed] [Google Scholar]
  3. Berney S. N., Gesner B. M. The circulatory behaviour of normal and enzyme altered thymocytes in rats. Immunology. 1970 May;18(5):681–691. [PMC free article] [PubMed] [Google Scholar]
  4. Bianco C., Patrick R., Nussenzweig V. A population of lymphocytes bearing a membrane receptor for antigen-antibody-complement complexes. I. Separation and characterization. J Exp Med. 1970 Oct 1;132(4):702–720. doi: 10.1084/jem.132.4.702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brahim F., Osmond D. G. Migration of bone marrow lymphocytes demonstrated by selective bone marrow labeling with thymidine-H3. Anat Rec. 1970 Oct;168(2):139–159. doi: 10.1002/ar.1091680202. [DOI] [PubMed] [Google Scholar]
  6. CAFFREY R. W., RIEKE W. O., EVERETT N. B. Radioautographic studies of small lymphocytes in the thoracic duct of the rat. Acta Haematol. 1962;28:145–154. doi: 10.1159/000207257. [DOI] [PubMed] [Google Scholar]
  7. Cleveland W. W., Fogel B. J., Brown W. T., Kay H. E. Foetal thymic transplant in a case of Digeorge's syndrome. Lancet. 1968 Dec 7;2(7580):1211–1214. doi: 10.1016/s0140-6736(68)91694-2. [DOI] [PubMed] [Google Scholar]
  8. Coombs R. R., Gurner B. W., Janeway C. A., Jr, Wilson A. B., Gell P. G., Kelus A. S. Immunoglobulin determinants on the lymphocytes of normal rabbits. I. Demonstration by the mixed antiglobulin reaction of determinants recognized by anti-gamma, anti-mu, anti-Fab and anti-allotype sera, anti-As4 and anti-As6. Immunology. 1970 Mar;18(3):417–429. [PMC free article] [PubMed] [Google Scholar]
  9. Cunningham A. J., Smith J. B., Mercer E. H. Antibody formation by single cells from lymph nodes and efferent lymph of sheep. J Exp Med. 1966 Oct 1;124(4):701–714. doi: 10.1084/jem.124.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Davies A. J., Carter R. L., Leuchars E., Wallis V., Koller P. C. The morphology of immune reactions in normal, thymectomized and reconstituted mice. I. The response to sheep erythrocytes. Immunology. 1969 Jan;16(1):57–69. [PMC free article] [PubMed] [Google Scholar]
  11. Davies A. J., Carter R. L., Leuchars E., Wallis V. The morphology of immune reactions in normal, thymectomized and reconstituted mice. II. The response to oxazolone. Immunology. 1969 Jul;17(1):111–126. [PMC free article] [PubMed] [Google Scholar]
  12. Davies A. J. The thymus and the cellular basis of immunity. Transplant Rev. 1969;1:43–91. doi: 10.1111/j.1600-065x.1969.tb00136.x. [DOI] [PubMed] [Google Scholar]
  13. De Sousa M. A., Parrott D. M., Pantelouris E. M. The lymphoid tissues in mice with congenital aplasia of the thymus. Clin Exp Immunol. 1969 Jun;4(6):637–644. [PMC free article] [PubMed] [Google Scholar]
  14. Doenhoff M. J., Davies A. J., Leuchars E., Wallis V. The thymus and circulating lymphocytes of mice. Proc R Soc Lond B Biol Sci. 1970 Oct 13;176(1042):69–85. doi: 10.1098/rspb.1970.0035. [DOI] [PubMed] [Google Scholar]
  15. Dresser D. W., Taub R. N., Krantz A. R. The effect of localized injection of adjuvant material on the draining lymph node. II. Circulating lymphocytes. Immunology. 1970 May;18(5):663–670. [PMC free article] [PubMed] [Google Scholar]
  16. Dukor P., Bianco C., Nussenzweig V. Tissue localization of lymphocytes bearing a membrane receptor for antigen-antibody-complement complexes. Proc Natl Acad Sci U S A. 1970 Oct;67(2):991–997. doi: 10.1073/pnas.67.2.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dukor P., Miller J. F., House W., Allman V. Regeneration of thymus grafts. I. Histological and cytological aspects. Transplantation. 1965 Sep;3(5):639–668. doi: 10.1097/00007890-196509000-00006. [DOI] [PubMed] [Google Scholar]
  18. Dukor P., Miller J. F., Sacquet E. The immunological responsiveness of germ-free mice thymectomized at birth. II. Lymphoid tissue and histopathology. Clin Exp Immunol. 1968 Mar;3(3):191–212. [PMC free article] [PubMed] [Google Scholar]
  19. EVERETT N. B., CAFFREY R. W., RIEKE W. O. RECIRCULATION OF LYMPHOCYTES. Ann N Y Acad Sci. 1964 Feb 28;113:887–897. doi: 10.1111/j.1749-6632.1964.tb40710.x. [DOI] [PubMed] [Google Scholar]
  20. East J., De Sousa M. A., Parrott D. M., Jaquet H. Consequences of neonatal thymectomy in New Zealand black mice. Clin Exp Immunol. 1967 Mar;2(2):203–215. [PMC free article] [PubMed] [Google Scholar]
  21. Everett N. B., Tyler R. W. Lymphopoiesis in the thymus and other tissues: functional implications. Int Rev Cytol. 1967;22:205–237. doi: 10.1016/s0074-7696(08)61836-7. [DOI] [PubMed] [Google Scholar]
  22. Ford W. L. The immunological and migratory properties of the lymphocytes recirculating through the rat spleen. Br J Exp Pathol. 1969 Jun;50(3):257–269. [PMC free article] [PubMed] [Google Scholar]
  23. GOWANS J. L., KNIGHT E. J. THE ROUTE OF RE-CIRCULATION OF LYMPHOCYTES IN THE RAT. Proc R Soc Lond B Biol Sci. 1964 Jan 14;159:257–282. doi: 10.1098/rspb.1964.0001. [DOI] [PubMed] [Google Scholar]
  24. GOWANS J. L. The effect of the continuous re-infusion of lymph and lymphocytes on the output of lymphocytes from the thoracic duct of unanaesthetized rats. Br J Exp Pathol. 1957 Feb;38(1):67–78. [PMC free article] [PubMed] [Google Scholar]
  25. GOWANS J. L. The recirculation of lymphocytes from blood to lymph in the rat. J Physiol. 1959 Apr 23;146(1):54–69. doi: 10.1113/jphysiol.1959.sp006177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Goldschneider I., McGregor D. D. Migration of lymphocytes and thymocytes in the rat. I. The route of migration from blood to spleen and lymph nodes. J Exp Med. 1968 Jan 1;127(1):155–168. doi: 10.1084/jem.127.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Goldschneider I., McGregor D. D. Migration of lymphocytes and thymocytes in the rat. II. Circulation of lymphocytes and thymocytes from blood to lymph. Lab Invest. 1968 Apr;18(4):397–406. [PubMed] [Google Scholar]
  28. HANNA M. G., Jr GERMINAL CENTER CHANGES AND PLASMA CELL REACTION DURING THE PRIMARY IMMUNE RESPONSE. Int Arch Allergy Appl Immunol. 1965;26:230–251. doi: 10.1159/000229574. [DOI] [PubMed] [Google Scholar]
  29. Kelly R. H. Localization of afferent lymph cells within the draining node during a primary immune response. Nature. 1970 Aug 1;227(5257):510–513. doi: 10.1038/227510a0. [DOI] [PubMed] [Google Scholar]
  30. LEUCHARS E., CROSS A. M., DUKOR P. THE RESTORATION OF IMMUNOLOGICAL FUNCTION BY THYMUS GRAFTING IN THYMECTOMIZED IRRADIATED MICE. Transplantation. 1965 Jan;3:28–38. doi: 10.1097/00007890-196501000-00004. [DOI] [PubMed] [Google Scholar]
  31. Lance E. M., Taub R. N. Segregation of lymphocyte populations through differential migration. Nature. 1969 Mar 1;221(5183):841–843. doi: 10.1038/221841a0. [DOI] [PubMed] [Google Scholar]
  32. Linna T. J. Cell migration from the thymus to other lymphoid organs in hamsters of different ages. Blood. 1968 Jun;31(6):727–746. [PubMed] [Google Scholar]
  33. METCALF D., SPARROW N., NAKAMURA K., ISHIDATE M. The behaviour of thymus grafts in high and low leukaemia strains of mice. Aust J Exp Biol Med Sci. 1961 Oct;39:441–453. doi: 10.1038/icb.1961.45. [DOI] [PubMed] [Google Scholar]
  34. MILLER J. J., 3rd, NOSSAL G. J. ANTIGENS IN IMMUNITY. VI. THE PHAGOCYTIC RETICULUM OF LYMPH NODE FOLLICLES. J Exp Med. 1964 Dec 1;120:1075–1086. doi: 10.1084/jem.120.6.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Michalke W. D., Hess M. W., Riedwyl H. H., Stoner R. D., Cottier H. Thymic lymphopoiesis and cell loss in newborn mice. Blood. 1969 Apr;33(4):541–554. [PubMed] [Google Scholar]
  36. Micklem H. S., Ford C. E., Evans E. P., Gray J. Interrelationships of myeloid and lymphoid cells: studies with chromosome-marked cells transfused into lethally irradiated mice. Proc R Soc Lond B Biol Sci. 1966 Jul 19;165(998):78–102. doi: 10.1098/rspb.1966.0059. [DOI] [PubMed] [Google Scholar]
  37. OORT J., TURK J. L. A HISTOLOGICAL AND AUTORADIOGRAPHIC STUDY OF LYMPH NODES DURING THE DEVELOPMENT OF CONTACT SENSITIVITY IN THE GUINEA-PIG. Br J Exp Pathol. 1965 Apr;46:147–154. [PMC free article] [PubMed] [Google Scholar]
  38. PEPPER F. J. Transplantation of thymic tissue in inbred strains of mice. J Endocrinol. 1961 Jul;22:349–359. doi: 10.1677/joe.0.0220349. [DOI] [PubMed] [Google Scholar]
  39. Parrott D. M., de Sousa M. A. Changes in the thymus-dependent areas of lymph nodes after immunological stimulation. Nature. 1966 Dec 17;212(5068):1316–1317. doi: 10.1038/2121316a0. [DOI] [PubMed] [Google Scholar]
  40. Parrott D. M., de Sousa M. A. The persistence of donor-derived cells in thymus grafts, lymph nodes and spleens of recipient mice. Immunology. 1967 Aug;13(2):193–200. [PMC free article] [PubMed] [Google Scholar]
  41. Parrott D. V., De Sousa M. A., East J. Thymus-dependent areas in the lymphoid organs of neonatally thymectomized mice. J Exp Med. 1966 Jan 1;123(1):191–204. doi: 10.1084/jem.123.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. ROBINSON S. H., BRECHER G., LOURIE I. S., HALEY J. E. LEUKOCYTE LABELING IN RATS DURING AND AFTER CONTINUOUS INFUSION OF TRITIATED THYMIDINE: IMPLICATIONS FOR LYMPHOCYTE LONGEVITY AND DNA REUTILIZATION. Blood. 1965 Sep;26:281–295. [PubMed] [Google Scholar]
  43. Raff M. C. Two distinct populations of peripheral lymphocytes in mice distinguishable by immunofluorescence. Immunology. 1970 Oct;19(4):637–650. [PMC free article] [PubMed] [Google Scholar]
  44. Raff M. C., Wortis H. H. Thymus dependence of theta-bearing cells in the peripheral lymphoid tissues of mice. Immunology. 1970 Jun;18(6):931–942. [PMC free article] [PubMed] [Google Scholar]
  45. Sainte-Marie G., Messier B. Thymus and node labelling by intramediastinal injection of tritiated tracers and its bearing on present concepts of lymphocyte cytokinetics. Scand J Haematol. 1970;7(3):163–176. doi: 10.1111/j.1600-0609.1970.tb01884.x. [DOI] [PubMed] [Google Scholar]
  46. Sainte-Marie G., Sin Y. M. Reticular fiber pattern in the rat spleen. Rev Can Biol. 1968 Sep;27(3):273–275. [PubMed] [Google Scholar]
  47. Taub R. N., Lance E. M. Histopathological effects in mice of heterologous antilymphocyte serum. J Exp Med. 1968 Dec 1;128(6):1281–1307. doi: 10.1084/jem.128.6.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Tyler R. W., Everett N. B., Schwarz M. R. Effect of antilymphocytic serum on rat lymphocytes. J Immunol. 1969 Jan;102(1):179–186. [PubMed] [Google Scholar]
  49. WAKSMAN B. H., ARNASON B. G., JANKOVIC B. D. Role of the thymus in immune reactions in rats. III. Changes in the lymphoid organs of thymectomized rats. J Exp Med. 1962 Aug 1;116:187–206. doi: 10.1084/jem.116.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Weissman I. L. Thymus cell migration. J Exp Med. 1967 Aug 1;126(2):291–304. doi: 10.1084/jem.126.2.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. White R. G. Antigens and adjuvants. Proc R Soc Med. 1968 Jan;61(1):1–6. [PMC free article] [PubMed] [Google Scholar]
  52. Williams G. M., Nossal G. J. Ontogeny of the immune response. I. The development of the follicular antigen-trapping mechanism. J Exp Med. 1966 Jul 1;124(1):47–56. doi: 10.1084/jem.124.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Woodruff J. J., Gesner B. M. The effect of neuraminidase on the fate of transfused lymphocytes. J Exp Med. 1969 Mar 1;129(3):551–567. doi: 10.1084/jem.129.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Clinical and Experimental Immunology are provided here courtesy of British Society for Immunology

RESOURCES