Skip to main content
PMC home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1972 Oct 31;136(5):1008–1030. doi: 10.1084/jem.136.5.1008

MOUSE THYMUS-INDEPENDENT AND THYMUS-DERIVED LYMPHOID CELLS

II. ULTRASTRUCTURAL STUDIES

A Matter 1, B Lisowska-Bernstein 1, J E Ryser 1, J-P Lamelin 1, P Vassalli 1
PMCID: PMC2139311  PMID: 4563148

Abstract

The ultrastructural features of B-, T-, and surface Ig(sIg)-bearing cells have been studied on cell suspensions from lymphoid organs of mice at different stages of immunization. The cells were identified by exposure to rabbit antibodies against mouse-specific lymphocyte antigens (MSLA) or brain-associated θ antigen (BAθ) for T cells, mouse-specific bone marrow-derived lymphocyte antigens (MBLA) for B cells, and mouse Ig for sIg-bearing cells. The rabbit antibodies fixed on the cell surfaces were detected by peroxidase-labeled sheep anti-rabbit Ig antibodies or by a "bridge" technique using southern bean mosaic virus or bacteriophage T4 as the final markers. In some experiments, short-lived lymphoid cells were labeled in vivo with repeated tritiated thymidine and the ultrastructural detection of their surface antigens was combined with radioautography. MBLA+ lymphoid cells showed a whole range of ultrastructural patterns. Most were small and medium-sized lymphocytes with a clear cytoplasm containing mono- and polyribosomes, but they comprised also blasts and large cells with various amounts of endoplasmic reticulum, as well as plasma cells at different stages of maturation. sIg-bearing cells appeared to be identical with MBLA+ cells, except that sIg was less easily detectable on large blasts, and only very rarely observed on plasma cells. MSLA+ and BAθ+ cells fell into three categories. One of them (T1 cells) consisted of small to medium-sized lymphocytes with a clear cytoplasm and few organelles, mostly monoribosomes. A second consisted of large cells (T2 cells) characterized by numerous polyribosomes often in a "rosette"-like pattern, occasional dark, membrane-bound granules, and a developing "filamentous network." The third, very characteristic type, (T3 cells) was represented by dark small to medium-sized lymphocytes, usually containing large amounts of closely packed ribosomes and showing a striking accumulation of filamentous network, often condensed in large areas devoid of cell organelles. This filamentous network appeared to correspond to the cytochalasin B-sensitive system of microfilaments found in other cells and considered to be one of the contractile elements of the cell. The T3 lymphocytes showed frequently vesicles suggestive of a strong pinocytic activity, and assumed a variety of shapes, including uropods. Evidence is presented that T1 lymphocytes represent "virgin" T cells, T2 "activated," and T3 "differentiated" lymphocytes.

Full Text

The Full Text of this article is available as a PDF (2.4 MB).

Selected References

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

  1. Aoki T., Hämmerling U., De Harven E., Boyse E. A., Old L. J. Antigenic structure of cell surfaces. An immunoferritin study of the occurrence and topography of H-2' theta, and TL alloantigens on mouse cells. J Exp Med. 1969 Nov 1;130(5):979–1001. doi: 10.1084/jem.130.5.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Avrameas S., Bouteille M. Ultrastructural localization of antibody by antigen label with peroxidase. Exp Cell Res. 1968 Oct;53(1):166–176. doi: 10.1016/0014-4827(68)90364-9. [DOI] [PubMed] [Google Scholar]
  3. Avrameas S. Coupling of enzymes to proteins with glutaraldehyde. Use of the conjugates for the detection of antigens and antibodies. Immunochemistry. 1969 Jan;6(1):43–52. doi: 10.1016/0019-2791(69)90177-3. [DOI] [PubMed] [Google Scholar]
  4. Avrameas S. Immunoenzyme techniques: enzymes as markers for the localization of antigens and antibodies. Int Rev Cytol. 1970;27:349–385. doi: 10.1016/s0074-7696(08)61250-4. [DOI] [PubMed] [Google Scholar]
  5. Avrameas S., Leduc E. H. Detection of simultaneous antibody synthesis in plasma cells and specialized lymphocytes in rabbit lymph nodes. J Exp Med. 1970 Jun 1;131(6):1137–1168. doi: 10.1084/jem.131.6.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Avrameas S., Ternynck T. Peroxidase labelled antibody and Fab conjugates with enhanced intracellular penetration. Immunochemistry. 1971 Dec;8(12):1175–1179. doi: 10.1016/0019-2791(71)90395-8. [DOI] [PubMed] [Google Scholar]
  7. Axén R., Porath J., Ernback S. Chemical coupling of peptides and proteins to polysaccharides by means of cyanogen halides. Nature. 1967 Jun 24;214(5095):1302–1304. doi: 10.1038/2141302a0. [DOI] [PubMed] [Google Scholar]
  8. Blomgren H., Andersson B. Evidence for a small pool of immunocompetent cells in the mouse thymus. Exp Cell Res. 1969 Oct;57(2):185–192. doi: 10.1016/0014-4827(69)90140-2. [DOI] [PubMed] [Google Scholar]
  9. CARO L. G., VAN TUBERGEN R. P., KOLB J. A. High-resolution autoradiography. I. Methods. J Cell Biol. 1962 Nov;15:173–188. doi: 10.1083/jcb.15.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cerottini J. C., Brunner K. T. Reversible inhibition of lymphocyte-mediated cytotoxicity by cytochalasin B. Nat New Biol. 1972 Jun 28;237(78):272–273. doi: 10.1038/newbio237272a0. [DOI] [PubMed] [Google Scholar]
  11. Cohen J. J. Hydrocortisone resistance of activated initiator cells in graft versus host reactions. Nature. 1971 Jan 22;229(5282):274–275. doi: 10.1038/229274a0. [DOI] [PubMed] [Google Scholar]
  12. Davis W. C. H-2 antigen on cell membranes: an explanation for the alteration of distribution by indirect labeling techniques. Science. 1972 Mar 3;175(4025):1006–1008. doi: 10.1126/science.175.4025.1006. [DOI] [PubMed] [Google Scholar]
  13. Dickson R. C., Barnes S. L., Eiserling F. A. Structural proteins of bacteriophage T4. J Mol Biol. 1970 Nov 14;53(3):461–474. doi: 10.1016/0022-2836(70)90077-x. [DOI] [PubMed] [Google Scholar]
  14. Dumonde D. C. 'Lymphokines': molecular mediators of cellular immune responses in animals and man. Proc R Soc Med. 1970 Sep;63(9):899–902. [PMC free article] [PubMed] [Google Scholar]
  15. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  16. Hämmerling U., Aoki T., Wood H. A., Old L. J., Boyse E. A., de Harvin E. New visual markers of antibody for electron microscopy. Nature. 1969 Sep 13;223(5211):1158–1159. doi: 10.1038/2231158a0. [DOI] [PubMed] [Google Scholar]
  17. Hämmerling U., Rajewsky K. Evidence for surface-associated immunoglobulin on T and B lymphocytes. Eur J Immunol. 1971 Dec;1(6):447–452. doi: 10.1002/eji.1830010608. [DOI] [PubMed] [Google Scholar]
  18. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lamelin J. P., Lisowska-Bernstein B., Matter A., Ryser J. E., Vassalli P. Mouse thymus-independent and thymus-derived lymphoid cells. I. Immunofluorescent and functional studies. J Exp Med. 1972 Nov 1;136(5):984–1007. doi: 10.1084/jem.136.5.984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mason T. E., Phifer R. F., Spicer S. S., Swallow R. A., Dreskin R. B. An immunoglobulin-enzyme bridge method for localizing tissue antigens. J Histochem Cytochem. 1969 Sep;17(9):563–569. doi: 10.1177/17.9.563. [DOI] [PubMed] [Google Scholar]
  21. Miller J. F., Sprent J. Cell-to-cell interaction in the immune response. VI. Contribution of thymus-derived cells and antibody-forming cell precursors to immunological memory. J Exp Med. 1971 Jul 1;134(1):66–82. doi: 10.1084/jem.134.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Perkins W. D., Karnovsky M. J., Unanue E. R. An ultrastructural study of lymphocytes with surface-bound immunoglobulin. J Exp Med. 1972 Feb 1;135(2):267–276. doi: 10.1084/jem.135.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Spooner B. S., Yamada K. M., Wessells N. K. Microfilaments and cell locomotion. J Cell Biol. 1971 Jun;49(3):595–613. doi: 10.1083/jcb.49.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wessells N. K., Spooner B. S., Ash J. F., Bradley M. O., Luduena M. A., Taylor E. L., Wrenn J. T., Yamada K. Microfilaments in cellular and developmental processes. Science. 1971 Jan 15;171(3967):135–143. doi: 10.1126/science.171.3967.135. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES