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Analysis of matrisome expression patterns in murine and human dorsal root ganglia

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Abstract
The extracellular matrix (ECM) is a dynamic structure of molecules that can be divided into six different categories and are collectively called the matrisome. The ECM plays pivotal roles in physiological processes in many tissues, including the nervous system. Intriguingly, alterations in ECM molecules/pathways are associated with painful human conditions and murine pain models. Nevertheless, mechanistic insight into the interplay of normal or defective ECM and pain is largely lacking. The goal of this study was to integrate bulk, single-cell, and spatial RNA sequencing (RNAseq) datasets to investigate the expression and cellular origin of matrisome genes in male and female murine and human dorsal root ganglia (DRG). Bulk RNAseq showed that about 65% of all matrisome genes were expressed in both murine and human DRG, with proportionally more core matrisome genes (glycoproteins, collagens, and proteoglycans) expressed compared to matrisome-associated genes (ECM-affiliated genes, ECM regulators, and secreted factors). Single cell RNAseq on male murine DRG revealed the cellular origin of matrisome expression. Core matrisome genes, especially collagens, were expressed by fibroblasts whereas matrisome-associated genes were primarily expressed by neurons. Cell-cell communication network analysis with CellChat software predicted an important role for collagen signaling pathways in connecting vascular cell types and nociceptors in murine tissue, which we confirmed by analysis of spatial transcriptomic data from human DRG. RNAscope in situ hybridization and immunohistochemistry demonstrated expression of collagens in fibroblasts surrounding nociceptors in male and female human DRG. Finally, comparing human neuropathic pain samples with non-pain samples also showed differential expression of matrisome genes produced by both fibroblasts and by nociceptors. This study supports the idea that the DRG matrisome may contribute to neuronal signaling in both mouse and human, and that dysregulation of matrisome genes is associated with neuropathic pain.
Keywords
EXTRACELLULAR-MATRIX, NEUROPATHIC PAIN, RECEPTORS, ANNEXINS, SYSTEM, CELLS, MODEL, matrisome, dorsal root ganglion, nociceptor, cell-cell communication, extracellular matrix

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MLA
Vroman, Robin, et al. “Analysis of Matrisome Expression Patterns in Murine and Human Dorsal Root Ganglia.” FRONTIERS IN MOLECULAR NEUROSCIENCE, vol. 16, Frontiers Media SA, 2023, doi:10.3389/fnmol.2023.1232447.
APA
Vroman, R., Hunter, R. S., Wood, M. J., Davis, O. C., Malfait, Z., George, D. S., … Syx, D. (2023). Analysis of matrisome expression patterns in murine and human dorsal root ganglia. FRONTIERS IN MOLECULAR NEUROSCIENCE, 16. https://doi.org/10.3389/fnmol.2023.1232447
Chicago author-date
Vroman, Robin, Rahel S. Hunter, Matthew J. Wood, Olivia C. Davis, Zoë Malfait, Dale S. George, Dongjun Ren, et al. 2023. “Analysis of Matrisome Expression Patterns in Murine and Human Dorsal Root Ganglia.” FRONTIERS IN MOLECULAR NEUROSCIENCE 16. https://doi.org/10.3389/fnmol.2023.1232447.
Chicago author-date (all authors)
Vroman, Robin, Rahel S. Hunter, Matthew J. Wood, Olivia C. Davis, Zoë Malfait, Dale S. George, Dongjun Ren, Diana Tavares-Ferreira, Theodore J. Price, Richard J. Miller, Anne-Marie Malfait, Fransiska Malfait, Rachel E. Miller, and Delfien Syx. 2023. “Analysis of Matrisome Expression Patterns in Murine and Human Dorsal Root Ganglia.” FRONTIERS IN MOLECULAR NEUROSCIENCE 16. doi:10.3389/fnmol.2023.1232447.
Vancouver
1.
Vroman R, Hunter RS, Wood MJ, Davis OC, Malfait Z, George DS, et al. Analysis of matrisome expression patterns in murine and human dorsal root ganglia. FRONTIERS IN MOLECULAR NEUROSCIENCE. 2023;16.
IEEE
[1]
R. Vroman et al., “Analysis of matrisome expression patterns in murine and human dorsal root ganglia,” FRONTIERS IN MOLECULAR NEUROSCIENCE, vol. 16, 2023.
@article{01HGG7RT7FRJ7K5PA7B1MHHBD0,
  abstract     = {{The extracellular matrix (ECM) is a dynamic structure of molecules that can be divided into six different categories and are collectively called the matrisome. The ECM plays pivotal roles in physiological processes in many tissues, including the nervous system. Intriguingly, alterations in ECM molecules/pathways are associated with painful human conditions and murine pain models. Nevertheless, mechanistic insight into the interplay of normal or defective ECM and pain is largely lacking. The goal of this study was to integrate bulk, single-cell, and spatial RNA sequencing (RNAseq) datasets to investigate the expression and cellular origin of matrisome genes in male and female murine and human dorsal root ganglia (DRG). Bulk RNAseq showed that about 65% of all matrisome genes were expressed in both murine and human DRG, with proportionally more core matrisome genes (glycoproteins, collagens, and proteoglycans) expressed compared to matrisome-associated genes (ECM-affiliated genes, ECM regulators, and secreted factors). Single cell RNAseq on male murine DRG revealed the cellular origin of matrisome expression. Core matrisome genes, especially collagens, were expressed by fibroblasts whereas matrisome-associated genes were primarily expressed by neurons. Cell-cell communication network analysis with CellChat software predicted an important role for collagen signaling pathways in connecting vascular cell types and nociceptors in murine tissue, which we confirmed by analysis of spatial transcriptomic data from human DRG. RNAscope in situ hybridization and immunohistochemistry demonstrated expression of collagens in fibroblasts surrounding nociceptors in male and female human DRG. Finally, comparing human neuropathic pain samples with non-pain samples also showed differential expression of matrisome genes produced by both fibroblasts and by nociceptors. This study supports the idea that the DRG matrisome may contribute to neuronal signaling in both mouse and human, and that dysregulation of matrisome genes is associated with neuropathic pain.}},
  articleno    = {{1232447}},
  author       = {{Vroman, Robin and  Hunter, Rahel S. and  Wood, Matthew J. and  Davis, Olivia C. and Malfait, Zoë and  George, Dale S. and  Ren, Dongjun and  Tavares-Ferreira, Diana and  Price, Theodore J. and  Miller, Richard J. and Malfait, Anne-Marie and Malfait, Fransiska and Miller, Rachel E. and Syx, Delfien}},
  issn         = {{1662-5099}},
  journal      = {{FRONTIERS IN MOLECULAR NEUROSCIENCE}},
  keywords     = {{EXTRACELLULAR-MATRIX,NEUROPATHIC PAIN,RECEPTORS,ANNEXINS,SYSTEM,CELLS,MODEL,matrisome,dorsal root ganglion,nociceptor,cell-cell communication,extracellular matrix}},
  language     = {{eng}},
  pages        = {{18}},
  publisher    = {{Frontiers Media SA}},
  title        = {{Analysis of matrisome expression patterns in murine and human dorsal root ganglia}},
  url          = {{http://doi.org/10.3389/fnmol.2023.1232447}},
  volume       = {{16}},
  year         = {{2023}},
}

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