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Single-cell landscape of the cellular microenvironment in three different colonic polyp subtypes in children
Yafei Deng1,2, Canlin Li3, Lanlan Huang1,2
1Pediatrics Research Institute of Hunan Province and Hunan Provincial Key Laboratory of Children's Emergency Medicine, Hunan Children's Hospital, Changsha, China.
Insights
This study reveals distinct cellular microenvironments in pediatric colonic polyps, identifying specific cell types and pathways involved in solitary juvenile polyps (SJPs), juvenile polyposis syndrome (JPS), and Peutz-Jeghers syndrome (PJS). Findings offer new therapeutic targets for polyp recurrence.
Area of Science:
- Gastroenterology
- Immunology
- Cell Biology
Background:
- Limited understanding of the cellular microenvironment in pediatric colonic polyps, including solitary juvenile polyps (SJPs), juvenile polyposis syndrome (JPS), and Peutz-Jeghers syndrome (PJS).
- Heterogeneity in polyp subtypes suggests unique cellular compositions and interactions.
Purpose of the Study:
- To comprehensively analyze the cellular microenvironment of pediatric colonic polyps (SJPs, JPS, PJS) using advanced single-cell technologies.
- To identify shared and disease-specific cellular subsets, gene expression patterns, and intercellular communication networks within these polyps.
Main Methods:
- Single-cell RNA sequencing and multiplexed immunohistochemistry (mIHC) on normal colonic tissue and various pediatric polyp subtypes.
- Comparative analysis of cell populations, gene expression profiles, and signaling pathways across different polyp types and normal tissue.
Main Results:
- Identified distinct cellular compositions: increased myeloid cells in SJPs, endothelial cells in JPS, and epithelial cells in PJS.
- Observed shared features like increased memory B cells and epithelial-mesenchymal transition (EMT)-like colonocytes across all polyp types.
- Detailed immune cell infiltration patterns (neutrophils in SJPs, T cells in SJPs/JPS, NK T cells in PJS) and pathway activations (chemotaxis, interferon, nutrient absorption, TNF-α) in specific cell types and polyp subtypes.
- Revealed enhanced intercellular communication networks (e.g., TNF, VEGF, CXCL, collagen) within polyps.
Conclusions:
- Elucidated the heterogeneous cellular microenvironments of pediatric colonic polyp subtypes.
- Identified potential therapeutic targets for reducing polyp recurrence in children by understanding specific cellular and molecular mechanisms.
Background:
The understanding of the heterogeneous cellular microenvironment of colonic polyps in paediatric patients with solitary juvenile polyps (SJPs), polyposis syndrome (PJS) and Peutz-Jeghers syndrome (PJS) remains limited.
Methods:
We conducted single-cell RNA sequencing and multiplexed immunohistochemistry (mIHC) analyses on both normal colonic tissue and different types of colonic polyps obtained from paediatric patients.
Results:
We identified both shared and disease-specific cell subsets and expression patterns that played important roles in shaping the unique cellular microenvironments observed in each polyp subtype. As such, increased myeloid, endothelial and epithelial cells were the most prominent features of SJP, JPS and PJS polyps, respectively. Noticeably, memory B cells were increased, and a cluster of epithelial-mesenchymal transition (EMT)-like colonocytes existed across all polyp subtypes. Abundant neutrophil infiltration was observed in SJP polyps, while CX3CR1hi CD8+ T cells and regulatory T cells (Tregs) were predominant in SJP and JPS polyps, while GZMAhi natural killer T cells were predominant in PJS polyps. Compared with normal colonic tissues, myeloid cells exhibited specific induction of genes involved in chemotaxis and interferon-related pathways in SJP polyps, whereas fibroblasts in JPS polyps had upregulation of myofiber-associated genes and epithelial cells in PJS polyps exhibited induction of a series of nutrient absorption-related genes. In addition, the TNF-α response was uniformly upregulated in most cell subsets across all polyp subtypes, while endothelial cells and fibroblasts separately showed upregulated cell adhesion and EMT signalling in SJP and JPS polyps. Cell-cell interaction network analysis showed markedly enhanced intercellular communication, such as TNF, VEGF, CXCL and collagen signalling networks, among most cell subsets in polyps, especially SJP and JPS polyps.
Conclusion:
These findings strengthen our understanding of the heterogeneous cellular microenvironment of polyp subtypes and identify potential therapeutic approaches to reduce the recurrence of polyps in children.
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