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Spatial mapping of innate lymphoid cells in human lymphoid tissues and lymphoma at single-cell resolution
Nathalie Van Acker1,2, François-Xavier Frenois1,2, Pauline Gravelle1,2
1Department of Pathology, CHU of Toulouse, Imag'IN Platform, IUCT-Oncopole, Toulouse, France.
Insights
This study maps innate lymphoid cells (ILCs) and T helper (Th) cells in human tissues, revealing their locations and interactions. We found distinct ILC distributions and early Th cell programming in the thymus.
Area of Science:
- Immunology
- Cell Biology
- Histopathology
Background:
- The spatial distribution and organization of innate lymphoid cells (ILCs) within human lymphoid tissues are not fully understood.
- Investigating ILC interactions with T helper (Th) cells is crucial for understanding immune responses.
Purpose of the Study:
- To spatially map the distribution and compartmentalization of ILCs and Th cells in human lymphoid tissues at single-cell resolution.
- To analyze the proximity of ILCs to Th cells in both normal and neoplastic conditions.
Main Methods:
- Combined multiplex immunofluorescence and multispectral imaging.
- Advanced computer vision for whole-slide, single-cell resolution analysis.
- Comparative analysis of ILC and Th populations in normal versus follicular lymphoma tissues.
Main Results:
- ILC2s are predominant in the thymic medulla, while immature Th cells populate the cortex, with early Th2/Th17-like phenotypes observed.
- Peripheral ILC2s are abundant in lymph nodes and tonsils, with specific ILC subsets showing tissue-specific enrichment (e.g., ILC1/ILC3 in ileum/appendix).
- Follicular lymphoma exhibits significant perturbations in both ILC and Th cell populations compared to non-neoplastic tissues, with all ILCs found in close proximity to Th cells.
Conclusions:
- This study provides a comprehensive spatial map of ILCs and Th cells in human lymphoid tissues.
- The findings reveal tissue-specific ILC compartmentalization and unexpected early T cell programming.
- The developed histopathology tool aids in understanding immune cell organization in health and disease.
Abstract:
Innate lymphoid cells (ILC) distribution and compartmentalization in human lymphoid tissues are incompletely described. Through combined multiplex immunofluorescence, multispectral imaging, and advanced computer vision methods, we provide a map of ILCs at the whole-slide single-cell resolution level, and study their proximity to T helper (Th) cells. The results show that ILC2 predominates in thymic medulla; by contrast, immature Th cells prevail in the cortex. Unexpectedly, we find that Th2-like and Th17-like phenotypes appear before complete T cell receptor gene rearrangements in these immature thymocytes. In the periphery, ILC2 are more abundant in lymph nodes and tonsils, penetrating lymphoid follicles. NK cells are uncommon in lymphoid tissues but abundant in the spleen, whereas ILC1 and ILC3 predominate in the ileum and appendix. Under pathogenic conditions, a deep perturbation of both ILC and Th populations is seen in follicular lymphoma compared with non-neoplastic conditions. Lastly, all ILCs are preferentially in close proximity to their Th counterparts. In summary, our histopathology tool help present a spatial mapping of human ILCs and Th cells, in normal and neoplastic lymphoid tissues.
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