Carbonic anhydrase—a marker for particles shed from the epithelium to the lymphoid follicles of the ileal Peyer's patch in goat kids and lambs

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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“…Carbonic anhydrase is reported to show strong staining of the ileal FAE and of IPP follicle centers in ruminants (25). In accordance with …”

Section: Resultssupporting

confidence: 61%

“…6a), as described by Landsverk et al (25). In normal ileal lymphoid follicles, granular staining for carbonic anhydrase was present in the follicle centers (Fig.…”

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

confidence: 99%

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 FAE of ileal PP, however, has some unique characteristics. For example, they contain fifty nanometer membrane-bound particles that contain carbonic anhydrase; these are found in the ileal PP of both calves and lambs, but not in FAE of the jejunal PP [ 56,58]. In vitro studies of ileal epithelial cells from fetal lambs suggest that epithelial differentiation does not occur in the absence of lymphocytes [2].…”

Section: Follicle-associated Epithelium and Other Accessory Cells Of mentioning

confidence: 99%

The sheep and cattle Peyer’s patch as a site of B-cell development

et al. 2006

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-In sheep and cattle, the ileal Peyer's patch (PP), which extends one-two meters along the terminal small intestine, is a primary lymphoid organ of B-cell development. B-cell diversity in the ileal PP is thought to develop by combinatorial mechanisms, gene conversion and/or point mutation. These species also have jejunal PP that function more like secondary lymphoid tissues concerned with mucosal immune reactions. These two types of PP differ significantly in their histology, ontogeny and the extent of lymphocyte traffic. The prenatal development of follicles in the PP begins first in the jejunum during the middle of gestation and then in the ileum during late gestation. B-cells proliferate rapidly in the ileal PP follicle; up to five percent of these cells survive while the majority dies by apoptosis, perhaps driven by the influence of environmental antigen and/ or self-antigen. The surviving cells migrate from the ileal PP and populate the peripheral B-cell compartment. By adolescence, the ileal PP has involuted but the function of jejunal PP, compatible with a role as secondary lymphoid organ, continues throughout life. In this review, we focus on the development of PP as a site of B-cell repertoire generation, positive and negative B-cell selection, and the differences between ileal PP and jejunal PP.

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Carbonic anhydrase—a marker for particles shed from the epithelium to the lymphoid follicles of the ileal Peyer's patch in goat kids and lambs

Cited by 22 publications

References 10 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

The sheep and cattle Peyer’s patch as a site of B-cell development

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