Transfer of carbonic anhydrase-positive particles from the follicle-associated epithelium to lymphocytes of Peyer's patches in foetal sheep and lambs

Landsverk, Thor; Trevella, Wendy; Nicander, Lennart

doi:10.1007/bf00318665

Cited by 23 publications

(25 citation statements)

References 13 publications

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“…Carbonic anhydrase-positive material is also found in vesicles located in the apical cytoplasm of epithelial cells. These findings indicate that carbonic anhydrase-rich particles may contain components of the apical cell membrane (27). The present study demonstrates that infected lambs had reduced carbonic anhydrase reactivity in the FAE 3 weeks after infection, and this result may imply a reduced production of membrane-bound particles.…”

Section: Vol 9 2002 Lesions Of Ileal Peyer's Patches In Ovine Coccisupporting

confidence: 56%

“…Normal FAE function is probably important for the maintenance of follicle lymphopoiesis (22,27). The FAE is known to be active in the transcytosis of macromolecular antigens.…”

Section: Discussionmentioning

confidence: 99%

“…A characteristic of the membrane-bound particles produced in the ileal FAE is their reactivity for carbonic anhydrase. In healthy lambs, the ileal FAE shows strong carbonic anhydrase reactivity in the apical plasma cell membrane and along the basolateral membrane, even though the basolateral membrane itself is negative (25,27). Carbonic anhydrase-positive material is also found in vesicles located in the apical cytoplasm of epithelial cells.…”

Section: Vol 9 2002 Lesions Of Ileal Peyer's Patches In Ovine Coccimentioning

confidence: 96%

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Lymphocyte Depletion in Ileal Peyer’s Patch Follicles in Lambs Infected withEimeria ovinoidalis

Aleksandersen

Lie

Gjerde

et al. 2002

Clin Vaccine Immunol

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A total of 14 lambs were experimentally infected with Eimeria ovinoidalis in two separate experiments in two consecutive years. Nine lambs served as uninoculated controls. Material was collected from the ileum 2 weeks after infection in eight lambs and 3 weeks after infection in six lambs. Lambs examined 2 weeks after infection had normal follicles. After three weeks, the follicle-associated epithelium covering the lymphoid follicles of the ileal Peyer's patches showed fusions with adjacent absorptive epithelium, focal hyperplasia, and occasionally necrosis. Macrogametes, microgamonts, and oocysts were often found in the follicle-associated epithelium and the dome region. Various degrees of lymphocyte depletion were present in the ileal lymphoid follicles in all six infected lambs 3 weeks after infection, and four lambs had decreased follicle size. Reduced staining for leukocyte common antigen (CD45), B-cell markers, and the proliferation marker Ki-67 was present in these lambs. Application of the terminal deoxynucleotidyltransferase-mediated dUTP-biotin nick end labeling method for apoptotic cells revealed decreased staining in the ileal lymphoid follicles 3 weeks after infection. A marker of follicular dendritic cells, 5-nucleotidase, showed increased reactivity, probably due to condensation of reticular cells following loss of follicle lymphocytes. Reduced staining for carbonic anhydrase in the follicle-associated epithelium and the domes was present in all six lambs examined 3 weeks after infection, indicating decreased production of carbonic anhydrase-reactive 50-nm particles and a decreased lymphoproliferative stimulus. In conclusion, the present study shows that severe E. ovinoidalis infection in lambs causes lesions of the follicle-associated epithelium and may result in lymphocyte depletion and atrophy of the ileal Peyer's patch follicles.Coccidiosis in lambs is an intestinal infection characterized clinically by diarrhea and dehydration. A major cause of ovine coccidiosis is Eimeria ovinoidalis, but other species, such as Eimeria crandallis, may also be associated with this disease. Morphological changes in Eimeria sp. infections in lambs are characterized by inflammation, villus atrophy, epithelial hyperplasia, glandular loss, and mucosal collapse (8, 9, 11). Cellular immune responses play an important role in immunity against Eimeria spp., whereas humoral immunity probably represents a less important factor (3,46,51).Immunity is dependent on effective antigen detection, and the Peyer's patches are important for the generation of an immune response. Ruminants have two distinct types of Peyer's patches, the jejunal Peyer's patches and the ileal Peyer's patches (IPP), which differ in their development, cellular composition, and function (13,28,45). IPP have been attributed to have a role as a central lymphoid organ in the development of B cells, whereas a function in mucosal immune responses has been questioned (12, 36). The Peyer's patches of ruminants are outlined by a modified, follicle-associated ep...

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Section: Vol 9 2002 Lesions Of Ileal Peyer's Patches In Ovine Coccisupporting

confidence: 56%

“…Normal FAE function is probably important for the maintenance of follicle lymphopoiesis (22,27). The FAE is known to be active in the transcytosis of macromolecular antigens.…”

Section: Discussionmentioning

confidence: 99%

Section: Vol 9 2002 Lesions Of Ileal Peyer's Patches In Ovine Coccimentioning

confidence: 96%

See 1 more Smart Citation

Lymphocyte Depletion in Ileal Peyer’s Patch Follicles in Lambs Infected withEimeria ovinoidalis

Aleksandersen

Lie

Gjerde

et al. 2002

Clin Vaccine Immunol

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“…In sheep, the ileal Peyer's patch functions as an organ of post-rearrangement diversification (Reynaud et al, 1995;Weill and Reynaud, 1996) and is responsible for the vast majority of B-cell production (Reynolds and Morris, 1983;Gerber et al, 1986). The growth and function of the ileal Peyer's patch has been related to processes of epithelial differentiation (Landsverk, 1987;Landsverk et al, 1987Landsverk et al, , 1990 (Reynolds, 1985).…”

Section: Discussionmentioning

confidence: 99%

Development of Accessory Cells in B‐Cell Compartments Is Retarted in B‐Cell‐Depleted Fetal Sheep

Press

Reynolds

McClure

et al. 1997

Journal of Immunology Research

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(Halleraker et al., 1994). As sheep are only exposed to exogenous nonself antigens after birth because of the protection provided by a syndesmochorial placenta (Brambell, 1970;Boyd et al., 1976), it follows that factors other than exogenous nonself antigens are responsible for this modification.The interdependence of lymphoid-cell differentiation and stromal-cell development has been the subject of a number of studies. In man, rat and sheep, the early occurrence of FDCs was concomitant with B-cell aggregation and the appearance of primary follicles (Markgraf et al., 1982;Kroese et al., 1987;Halleraker et al., 1994 (Press et al., 1996) has allowed the investigation of the development of lymphoid and accessory-cell populations in a species shielded from exogenous antigen during gestation. In addition to FDCs in primary follicles, other accessory-cell populations that share a close association with B cells include the FDCs of gut-associated lymphoid follicles and macrophages of the marginal zone of the spleen. The aim of the present study was to characterize, using a panel of enzyme and immunohistochemical techniques, the accessory-cell populations in the lymphoid tissues of B-cell-depleted fetal sheep. RESULTS Ileal Peyer's Patch FolliclesThe small follicles in the ileal Peyer's patch of the Bcell-depleted fetuses demonstrated intense reactivity for the enzyme 5'nucleotidase (5'N), which was similar to the intensity of reactivity shown in the ileal Peyer's patch follicles of the untreated litter mates and the age-matched control fetuses (Figure 1). There was intense reactivity for magnesium-dependent adenosine triphosphatase (MgATPase) in some cells of the dome and interfollicular areas in the ileal Peyer's patch of the B-cell-depleted fetuses ( Figure 1). The dome region of ileal Peyer's patch of the Bcell-depleted fetuses showed increased reactivity for acid phosphatase whereas there was an absence of reactivity in the rudimentary follicle (Figure 1) There was also some reactivity for nonspecific esterase in the dome and interfollicular areas (not shown).A double immunofluorescence technique showed that the rudimentary follicles of the ileal Peyer' s patch in the B-cell-depleted fetuses showed strong staining for complement receptor-2 (CD21) and did not stain for IgM (not shown). Primary Follicles in the Spleen and Lymph NodesThe spleen and lymph nodes of the B-cell-depleted fetuses did not show the characteristic patterns of enzyme reactivity for 5'N, MgATPase, nonspecific esterase, and alkaline phosphatase that are associated with primary follicles (Figure 1). Serial step sectioning of the spleen and lymph nodes combined with staining for 5'N reactivity did not identify primary follicles in the B-cell-depleted fetuses. Primary follicles were readily identifiable by their typical pattern of enzyme reactivities in the control fetuses (Figure 1).The spleen and lymph nodes of B-cell-depleted fetuses contained a small population of CD21 cells.In the lymph nodes, most of these cells were scattered in the cortex, b...

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“…The cell population exhibited a close resemblance in its enzyme reactivity to that of the FAE of the ileal follicles (Landsverk, 1987;Landsverk et al, 1987Landsverk et al, , 1990. The definition of the enzyme histochemistry of the FAE is of particular advantage as large intestinal follicles sometimes lack a distinct dome structure and consequently the FAE may be difficult to define by morphological criteria.…”

Section: Discussionmentioning

confidence: 99%

Potassium-dependent p-nitrophenyl phosphatase and carbonic anhydrase reactivities suggest that lymphoid follicles in the large intestine of lambs are lined with a uniform type of epithelial cell distinct from the absorptive epithelium

1993

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The epithelium covering the large intestinal lymphoid follicles in fetal and postnatal lambs was examined for potassium-dependent p-nitrophenyl-phosphatase (K(+)-NPPase), carbonic anhydrase, magnesium-dependent adenosine triphosphatase (Mg(2+)-ATPase) and acid phosphatase. Reactivities for these enzymes indicated a homogenous population of cells in the follicle-associated epithelium (FAE), distinct from the absorptive epithelium. There were essentially no differences in the enzyme reactivities of the large intestinal FAE between fetuses in late gestation and postnatal lambs. The FAE showed a weak reaction for K(+)-NPPase and a variable staining for Mg(2+)-ATPase and acid phosphatase. In contrast, the adjacent absorptive epithelium demonstrated strong reactions for these enzymes. Carbonic anhydrase gave a strong reaction at the luminal and apparent basolateral cell borders of the large intestinal FAE. This distribution of reactivity for carbonic anhydrase resembled that found in the ileal FAE. In absorptive epithelial cells, only the luminal cell border reacted strongly for carbonic anhydrase. Serial sections of large intestinal tissue showed a variation in the basolateral staining of FAE from one section to the next, a finding which suggested that the reaction may be associated with transcytosis. The lymphoid follicles and domes of the large intestine showed a variable granular pattern of carbonic anhydrase staining, which also suggested a dependence on epithelial transcytosis.

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Transfer of carbonic anhydrase-positive particles from the follicle-associated epithelium to lymphocytes of Peyer's patches in foetal sheep and lambs

Cited by 23 publications

References 13 publications

Lymphocyte Depletion in Ileal Peyer’s Patch Follicles in Lambs Infected withEimeria ovinoidalis

Lymphocyte Depletion in Ileal Peyer’s Patch Follicles in Lambs Infected withEimeria ovinoidalis

Development of Accessory Cells in B‐Cell Compartments Is Retarted in B‐Cell‐Depleted Fetal Sheep

Potassium-dependent p-nitrophenyl phosphatase and carbonic anhydrase reactivities suggest that lymphoid follicles in the large intestine of lambs are lined with a uniform type of epithelial cell distinct from the absorptive epithelium

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