Splenectomy of rats selectively reduces lymphocyte function-associated antigen 1 and intercellular adhesion molecule 1 expression on B-cell subsets in blood and lymph nodes

Abstract

IntroductionAntigens circulating in the blood are retained in the spleen and presented to a huge number of B and T cells migrating through its different compartments. 1,2 On removal of the spleen the incidence of severe infections increases both in children and adults, 3,4 and there are changes in many immunologic parameters. 5 One lasting change is a high increase in the number of B lymphocytes in the blood, an effect that is constantly observed both in humans 6 and in experimental animals, 7,8 and that comparably affects the 2 compartments of the blood, the peripheral and the marginal pools. 9 Because it is not known whether all or only certain blood B-cell subsets increase in number after the loss of the spleen, the numbers of naïve (IgD ϩ IgM ϩ ), memory (IgD Ϫ IgM high ), newly formed (NF; IgM high CD90 high ), early recirculating follicular (ERF; IgM low CD90 high ), recirculating follicular (RF; IgM low CD90 Ϫ ), and marginal zone (MZ; IgM high CD90 Ϫ ) phenotype B cells 10 were determined in blood, lymph nodes, and bone marrow of control and splenectomized animals. In principle, the splenectomy-induced increase in blood B-cell numbers could be due to an altered migration pattern or to increased proliferation of B cells caused, for example, by a latent infection.Because migration and proliferation of B cells are regulated by surface molecules, our hypothesis was that their expression might be altered by splenectomy. Therefore, the expression of molecules involved in initial adhesion of lymphocytes to the endothelium, in transmigration through the endothelium and the tissue, and in B-cell activation within the tissue was analyzed in all B-cell subsets in blood, lymph nodes, and bone marrow (␣ 4 -integrins, CD44, L-selectin, lymphocyte function-associated antigen1 [11][12][13][14] ). The functional consequences of possible changes in surface molecule expression were tested in vitro by adhesion assays and in vivo by following the traffic of labeled B cells from blood to thoracic duct lymph. In addition, the number of proliferating B cells was determined in the bone marrow, in the B-cell area of lymph nodes, and in the blood.Our data show that loss of the spleen leads to a decrease in LFA-1 and ICAM-1 expression of B cells but not T cells in blood and lymph nodes. This accelerates the migration of B cells through lymph nodes and results in higher numbers of B cells in the thoracic duct lymph and, subsequently, in the blood. Materials and methods AnimalsNormal rats (LEW/Ztm), rats with high numbers of B cells (BH.1L/Won 15 ), and rats lacking T cells (LEW/Ztm-rnu 16 ) were obtained from the Central Animal Facility at the Medical School of Hannover and were barriermaintained in a room with controlled environment (22 Ϯ 2°C, 55% Ϯ 5% relative humidity, 12-hour light/dark cycle). SplenectomySplenectomy was performed as described previously. 3,7 The animals were kept under barrier-maintained conditions for 3 months before analysis to allow recovery from the operation and adjustment to the asplenic situation. Sh...

Mesenteric lymph nodes are not required for an intestinal immunoglobulin A response to oral cholera toxin

“…[18][19][20] These patients have a high risk of fulminant infection and it is well known that the absence of the spleen leads to several changes in the presence and expression pattern of immune cells in other lymphoid organs. 21 Thus, the spleen plays a central role in the homoeostasis of the immune system.…”

Splenectomy and Salmonella Typhi Exposure Lead to Quantitative Alterations of Bone Marrow B220+ Cells and CD4+ T Cells on BALB/c Mice

“…A second possibility is that the higher migration rate and lower proliferation rate were responsible. [34] Massive migration of immature B cells into the peripheral circulation has also been described by Ellis et al [32] who reported that the high number of peripheral lymphocytes in their patients indicated a large amount of mature B lymphocytes. This was caused by the increased migration of newly formed B cells from the bone marrow which served as a homeostatic mechanism for the recovery of B cells in the peripheral circulation due to castration.…”

“…This result is also supported by the persistence of T cells and memory B cells that already exist in the lymphoid organs and an increase in Kupffer cell activity, indicating that the rate of proliferation was not affected. [38] Milićević et al [34] found that the migration and proliferation of B cells was influenced by surface molecules such as lymphocyte function-associated antigen 1 (LFA-1), intercellular adhesion molecule 1 (ICAM-1), L-selectin, 4-integrins, the IL-2-R chain, CD44, and MHC class II, which affects the initial attachment of B cells in the endothelium and their infiltration into the tissue. Removing the spleen caused a decrease in the expression of LFA-1 and ICAM-1 in B cells, which would support the acceleration of B cell migration to the peripheral organs and increase in blood circulation.…”

Analyzing the Migration of Labeled T Cells In Vivo: An Essential Approach with Challenging Features

“…It is not known whether they also contain sessile T-cell populations. During migration through lymphoid tissues, which lasts approximately 24 hours (Westermann et al, 2001a), T and B cells temporarily either up-or down-regulate the expression of adhesion molecules (Luettig et al, 2001;Milicevic et al, 2001), and they absorb surface molecules from other cell types (Flugel et al, 2001;Hwang et al, 2000). These changes are reversed before leaving the tissue.…”