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A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes.

Huang FP, Platt N, Wykes M, Major JR, Powell TJ, Jenkins CD, MacPherson GG - J. Exp. Med. (2000)

Bottom Line: Peyer's patches and mesenteric but not other lymph nodes contain many strongly NSE(+) DCs in interfollicular and T cell areas.Similar DCs are seen in the ileum and in T cell areas of mesenteric nodes in gnotobiotic rats.These results show that a distinct DC subset constitutively endocytoses and transports apoptotic cells to T cell areas and suggest a role for these DCs in inducing and maintaining peripheral self-tolerance.

View Article: PubMed Central - PubMed

Affiliation: Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom.

ABSTRACT
This study identifies a dendritic cell (DC) subset that constitutively transports apoptotic intestinal epithelial cell remnants to T cell areas of mesenteric lymph nodes in vivo. Rat intestinal lymph contains two DC populations. Both populations have typical DC morphology, are major histocompatibility complex class II(hi), and express OX62, CD11c, and B7. CD4(+)/OX41(+) DCs are strong antigen-presenting cells (APCs). CD4(-)/OX41(-) DCs are weak APCs and contain cytoplasmic apoptotic DNA, epithelial cell-restricted cytokeratins, and nonspecific esterase (NSE)(+) inclusions, not seen in OX41(+) DCs. Identical patterns of NSE electrophoretic variants exist in CD4(-)/OX41(-) DCs, intestinal epithelial cells, and mesenteric node DCs but not in other DC populations, macrophages, or tissues. Terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick-end labeling (TUNEL)-positive DCs and strongly NSE(+) DCs are present in intestinal lamina propria. Peyer's patches and mesenteric but not other lymph nodes contain many strongly NSE(+) DCs in interfollicular and T cell areas. Similar DCs are seen in the ileum and in T cell areas of mesenteric nodes in gnotobiotic rats. These results show that a distinct DC subset constitutively endocytoses and transports apoptotic cells to T cell areas and suggest a role for these DCs in inducing and maintaining peripheral self-tolerance.

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Cells with the characteristics of OX41−NSE+ L-DCs are present in PP and MLNs but not other nodes. (A) Cryosection of CLN reacted for NSE. Weakly positive cells are present, particularly in the follicles. (B) Cryosection of MLN reacted for NSE. Large numbers of large, irregular, strongly positive cells are present in the subcapsular sinus, interfollicular traffic areas, and the paracortical T cell area (T). (C) Cryosection of MLN reacted for NSE and labeled for MHC class II. The paracortex contains large numbers of large, irregular cells positive for both markers. (D) Cryosection of MLN labeled for NSE and OX62. The paracortex contains large numbers of large irregular cells positive for both markers. (E) Electron micrograph of MLN labeled for MHC class II. An MHC class II+ interdigitating cell in the paracortex contains large, dense cytoplasmic inclusions, similar to those seen in L-DCs. (F) Cryosection of PP labeled for NSE (red) and CD11c (blue). Several double-positive cells (<<) and one CD11c+NSE− cell (>) is present in the T cell area of the patch.
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Figure 4: Cells with the characteristics of OX41−NSE+ L-DCs are present in PP and MLNs but not other nodes. (A) Cryosection of CLN reacted for NSE. Weakly positive cells are present, particularly in the follicles. (B) Cryosection of MLN reacted for NSE. Large numbers of large, irregular, strongly positive cells are present in the subcapsular sinus, interfollicular traffic areas, and the paracortical T cell area (T). (C) Cryosection of MLN reacted for NSE and labeled for MHC class II. The paracortex contains large numbers of large, irregular cells positive for both markers. (D) Cryosection of MLN labeled for NSE and OX62. The paracortex contains large numbers of large irregular cells positive for both markers. (E) Electron micrograph of MLN labeled for MHC class II. An MHC class II+ interdigitating cell in the paracortex contains large, dense cytoplasmic inclusions, similar to those seen in L-DCs. (F) Cryosection of PP labeled for NSE (red) and CD11c (blue). Several double-positive cells (<<) and one CD11c+NSE− cell (>) is present in the T cell area of the patch.

Mentions: L-DCs derive from the small intestine 11. To identify the origins of IEC-containing L-DCs, cryostat sections of lamina propria (LP) and Peyer's patch (PP) were labeled for NSE and DC markers. Some large, irregular LP cells contained IEC-restricted cytokeratin (Fig. 3 A). Many NSE+ cells in the LP were negative for DC markers and are probably macrophages. However, some NSE+, large, irregular cells were CD11c+ (Fig. 3 B) or OX62+ (not shown). Some MHC class II+ or OX62+ cells in the LP contained apoptotic DNA (Fig. 3C and Fig. D). Thus, cells similar to OX41− L-DCs are present in the LP. In PP, similar cells were present at the base (Fig. 3 E) and underlying dome epithelium (not shown). Electron microscopic immunocytochemistry showed that some MHC class II+, irregular cells at the base contained apoptotic cells (Fig. 3 F) or large, electron dense granules similar to those in L-DCs and interdigitating DCs in MLNs (not shown; see Fig. 4 E).


A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes.

Huang FP, Platt N, Wykes M, Major JR, Powell TJ, Jenkins CD, MacPherson GG - J. Exp. Med. (2000)

Cells with the characteristics of OX41−NSE+ L-DCs are present in PP and MLNs but not other nodes. (A) Cryosection of CLN reacted for NSE. Weakly positive cells are present, particularly in the follicles. (B) Cryosection of MLN reacted for NSE. Large numbers of large, irregular, strongly positive cells are present in the subcapsular sinus, interfollicular traffic areas, and the paracortical T cell area (T). (C) Cryosection of MLN reacted for NSE and labeled for MHC class II. The paracortex contains large numbers of large, irregular cells positive for both markers. (D) Cryosection of MLN labeled for NSE and OX62. The paracortex contains large numbers of large irregular cells positive for both markers. (E) Electron micrograph of MLN labeled for MHC class II. An MHC class II+ interdigitating cell in the paracortex contains large, dense cytoplasmic inclusions, similar to those seen in L-DCs. (F) Cryosection of PP labeled for NSE (red) and CD11c (blue). Several double-positive cells (<<) and one CD11c+NSE− cell (>) is present in the T cell area of the patch.
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Related In: Results  -  Collection

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Figure 4: Cells with the characteristics of OX41−NSE+ L-DCs are present in PP and MLNs but not other nodes. (A) Cryosection of CLN reacted for NSE. Weakly positive cells are present, particularly in the follicles. (B) Cryosection of MLN reacted for NSE. Large numbers of large, irregular, strongly positive cells are present in the subcapsular sinus, interfollicular traffic areas, and the paracortical T cell area (T). (C) Cryosection of MLN reacted for NSE and labeled for MHC class II. The paracortex contains large numbers of large, irregular cells positive for both markers. (D) Cryosection of MLN labeled for NSE and OX62. The paracortex contains large numbers of large irregular cells positive for both markers. (E) Electron micrograph of MLN labeled for MHC class II. An MHC class II+ interdigitating cell in the paracortex contains large, dense cytoplasmic inclusions, similar to those seen in L-DCs. (F) Cryosection of PP labeled for NSE (red) and CD11c (blue). Several double-positive cells (<<) and one CD11c+NSE− cell (>) is present in the T cell area of the patch.
Mentions: L-DCs derive from the small intestine 11. To identify the origins of IEC-containing L-DCs, cryostat sections of lamina propria (LP) and Peyer's patch (PP) were labeled for NSE and DC markers. Some large, irregular LP cells contained IEC-restricted cytokeratin (Fig. 3 A). Many NSE+ cells in the LP were negative for DC markers and are probably macrophages. However, some NSE+, large, irregular cells were CD11c+ (Fig. 3 B) or OX62+ (not shown). Some MHC class II+ or OX62+ cells in the LP contained apoptotic DNA (Fig. 3C and Fig. D). Thus, cells similar to OX41− L-DCs are present in the LP. In PP, similar cells were present at the base (Fig. 3 E) and underlying dome epithelium (not shown). Electron microscopic immunocytochemistry showed that some MHC class II+, irregular cells at the base contained apoptotic cells (Fig. 3 F) or large, electron dense granules similar to those in L-DCs and interdigitating DCs in MLNs (not shown; see Fig. 4 E).

Bottom Line: Peyer's patches and mesenteric but not other lymph nodes contain many strongly NSE(+) DCs in interfollicular and T cell areas.Similar DCs are seen in the ileum and in T cell areas of mesenteric nodes in gnotobiotic rats.These results show that a distinct DC subset constitutively endocytoses and transports apoptotic cells to T cell areas and suggest a role for these DCs in inducing and maintaining peripheral self-tolerance.

View Article: PubMed Central - PubMed

Affiliation: Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom.

ABSTRACT
This study identifies a dendritic cell (DC) subset that constitutively transports apoptotic intestinal epithelial cell remnants to T cell areas of mesenteric lymph nodes in vivo. Rat intestinal lymph contains two DC populations. Both populations have typical DC morphology, are major histocompatibility complex class II(hi), and express OX62, CD11c, and B7. CD4(+)/OX41(+) DCs are strong antigen-presenting cells (APCs). CD4(-)/OX41(-) DCs are weak APCs and contain cytoplasmic apoptotic DNA, epithelial cell-restricted cytokeratins, and nonspecific esterase (NSE)(+) inclusions, not seen in OX41(+) DCs. Identical patterns of NSE electrophoretic variants exist in CD4(-)/OX41(-) DCs, intestinal epithelial cells, and mesenteric node DCs but not in other DC populations, macrophages, or tissues. Terminal deoxynucleotidyl transferase-mediated dUTP-biotin nick-end labeling (TUNEL)-positive DCs and strongly NSE(+) DCs are present in intestinal lamina propria. Peyer's patches and mesenteric but not other lymph nodes contain many strongly NSE(+) DCs in interfollicular and T cell areas. Similar DCs are seen in the ileum and in T cell areas of mesenteric nodes in gnotobiotic rats. These results show that a distinct DC subset constitutively endocytoses and transports apoptotic cells to T cell areas and suggest a role for these DCs in inducing and maintaining peripheral self-tolerance.

Show MeSH
Related in: MedlinePlus