Deep splenic lymphatic vessels in the mouse: a route of splenic exit for recirculating lymphocytes.

A study of pathways of lymphocyte migration through mouse spleen revealed lymphatic channels closely following arteries in trabeculae and white pulp. Because there is no detailed record of the layout of deep splenic lymphatics in the mouse, or other species, we present our observations in this paper, relating our findings to normal migratory pathways of lymphocytes through the spleen. Lymphatics draining the spleen are so inconspicuous that they often are not mentioned in anatomical discussions. The data presented clearly demonstrate 1) the existence and layout of deep lymphatic vessels in the mouse spleen, and 2) that migrating lymphocytes exit white pulp via these lymphatic vessels. CD4+ and CD8+ T cell subsets migrated proximally along the central artery from distal (dPALS) to proximal periarterial lymphatic sheaths (pPALS) and exited via deep lymphatic vessels that originate there. B cells migrated from dPALS to enter lymphatic nodules (NOD), thus segregated from T cells. B cells then migrated toward and exited via deep lymphatics. The appearance of labelled lymphocytes in lymph coincided with their disappearance from white pulp compartments. Labelled T cells were observed in splenic lymphatics as early as 1 hr after intravenous infusion but took, on average, about 6 hr. B cells took somewhat longer. Thus T and B cells entered and left white pulp through shared pathways, but took divergent intermediate routes through dedicated zones, pPALS for T cells, NOD for B cells.

[1]  J. Mitchell Lymphocyte circulation in the spleen. Marginal zone bridging channels and their possible role in cell traffic. , 1973, Immunology.

[2]  W L Ford,et al.  The recirculating lymphocyte pool of the rat: a systematic description of the migratory behaviour of recirculating lymphocytes. , 1983, Immunology.

[3]  J. Gowans,et al.  The role of lymphocytes in antibody formation II. the influence of lymphocyte migration on the initiation of antibody formation in the isolated, perfused spleen , 1967, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  T. Snook Deep lymphatics of the spleen , 1946, The Anatomical record.

[5]  J. Barcroft,et al.  Some factors involved in the concentration of blood by the spleen , 1928, The Journal of physiology.

[6]  V. Marchesi,et al.  The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study , 1964, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  A. Anderson,et al.  Specialized structure and metabolic activities of high endothelial venules in rat lymphatic tissues. , 1976, Immunology.

[8]  G. Goldberg The impregnation of the human spleen by particulate matter. A study of lymphogenic and hematogenic "involvement patterns" of the spleen. , 1961, American journal of clinical pathology.

[9]  W. L. Ford,et al.  THE TEMPO OF LYMPHOCYTE RECIRCULATION FROM BLOOD TO LYMPH IN THE RAT , 1972, Cell and tissue kinetics.

[10]  L. Wysocki,et al.  "Panning" for lymphocytes: a method for cell selection. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[11]  W. Hamilton,et al.  Lymphatic drainage of the spleen. , 1963, The American journal of physiology.

[12]  S. Licence,et al.  Patterns of migration of labelled blood lymphocyte subpopulations: evidence for two types of Peyer's patch in the young pig. , 1985, Advances in experimental medicine and biology.

[13]  J. Sprent,et al.  Circulating T and B lymphocytes of the mouse. I. Migratory properties. , 1973, Cellular immunology.

[14]  C. K. Drinker,et al.  THE FILTERING CAPACITY OF LYMPH NODES , 1934, The Journal of experimental medicine.

[15]  Tilney Nl Patterns of lymphatic drainage in the adult laboratory rat. , 1971 .

[16]  M. H. Knisely A method of illuminating living structures for microscopic study , 1936 .

[17]  E. J. Knight,et al.  The route of re-circulation of lymphocytes in the rat , 1964, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  T. Koshikawa,et al.  CELLULAR AND HUMORAL DYNAMICS IN THE PERIARTERIAL LYMPHATIC SHEATHS OF RAT SPLEENS , 1984, Acta pathologica japonica.

[19]  W. L. Ford,et al.  THE KINETICS OF LYMPHOCYTE RECIRCULATION WITHIN THE RAT SPLEEN , 1969 .

[20]  J. M. Yoffey,et al.  Lymphatics, lymph and the lymphomyeloid complex , 1970 .

[21]  Alexander A. Maximow,et al.  A Textbook of Histology , 1935, The Indian Medical Gazette.

[22]  H. von Boehmer,et al.  The separation of different cell classes from lymphoid organs. IX. A simple and rapid method for removal of damaged cells from lymphoid cell suspensions. , 1973, Journal of immunological methods.

[23]  L. Weiss,et al.  Deep splenic lymphatics in the marmot: An electron microscopic study , 1972, The Anatomical record.

[24]  L. Weiss,et al.  Mechanisms of splenic control of murine malaria: reticular cell activation and the development of a blood-spleen barrier. , 1986, The American journal of anatomy.

[25]  J. Bennink,et al.  [24] Collection of mouse thoracic duct lymphocytes , 1984 .

[26]  P. Herman,et al.  Microangiography of the white pulp of the spleen. , 1975, The American journal of roentgenology, radium therapy, and nuclear medicine.