Cargando…

The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity

Schwannomatosis is a multiple tumor syndrome in which patients develop benign tumors along peripheral nerves throughout the body. The first symptom with which schwannomatosis patients often present, prior to discovery of tumors, is pain. This pain can be debilitating and is often inadequately allevi...

Descripción completa

Detalles Bibliográficos
Autores principales: Ostrow, Kimberly Laskie, Donaldson, Katelyn J., Caterina, Michael J., Belzberg, Allan, Hoke, Ahmet
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6739480/
https://www.ncbi.nlm.nih.gov/pubmed/31511601
http://dx.doi.org/10.1038/s41598-019-49705-w
_version_ 1783450953501900800
author Ostrow, Kimberly Laskie
Donaldson, Katelyn J.
Caterina, Michael J.
Belzberg, Allan
Hoke, Ahmet
author_facet Ostrow, Kimberly Laskie
Donaldson, Katelyn J.
Caterina, Michael J.
Belzberg, Allan
Hoke, Ahmet
author_sort Ostrow, Kimberly Laskie
collection PubMed
description Schwannomatosis is a multiple tumor syndrome in which patients develop benign tumors along peripheral nerves throughout the body. The first symptom with which schwannomatosis patients often present, prior to discovery of tumors, is pain. This pain can be debilitating and is often inadequately alleviated by pharmacological approaches. Schwannomatosis-associated pain can be localized to the area of a tumor, or widespread. Moreover, not all tumors are painful, and the occurrence of pain is often unrelated to tumor size or location. We speculate that some individual tumors, but not others, secrete factors that act on nearby nerves to augment nociception by producing neuronal sensitization or spontaneous neuronal firing. We created cell lines from human SWN tumors with varying degrees of pain. We have found that conditioned medium (CM) collected from painful SWN tumors, but not that from nonpainful SWN tumors, sensitized DRG neurons, causing increased sensitivity to depolarization by KCl, increased response to noxious TRPV1 and TRPA1 agonists and also upregulated the expression of pain-associated genes in DRG cultures. Multiple cytokines were also detected at higher levels in CM from painful tumors. Taken together our data demonstrate a differential ability of painful versus non-painful human schwannomatosis tumor cells to secrete factors that augment sensory neuron responsiveness, and thus identify a potential determinant of pain heterogeneity in schwannomatosis.
format Online
Article
Text
id pubmed-6739480
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-67394802019-09-22 The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity Ostrow, Kimberly Laskie Donaldson, Katelyn J. Caterina, Michael J. Belzberg, Allan Hoke, Ahmet Sci Rep Article Schwannomatosis is a multiple tumor syndrome in which patients develop benign tumors along peripheral nerves throughout the body. The first symptom with which schwannomatosis patients often present, prior to discovery of tumors, is pain. This pain can be debilitating and is often inadequately alleviated by pharmacological approaches. Schwannomatosis-associated pain can be localized to the area of a tumor, or widespread. Moreover, not all tumors are painful, and the occurrence of pain is often unrelated to tumor size or location. We speculate that some individual tumors, but not others, secrete factors that act on nearby nerves to augment nociception by producing neuronal sensitization or spontaneous neuronal firing. We created cell lines from human SWN tumors with varying degrees of pain. We have found that conditioned medium (CM) collected from painful SWN tumors, but not that from nonpainful SWN tumors, sensitized DRG neurons, causing increased sensitivity to depolarization by KCl, increased response to noxious TRPV1 and TRPA1 agonists and also upregulated the expression of pain-associated genes in DRG cultures. Multiple cytokines were also detected at higher levels in CM from painful tumors. Taken together our data demonstrate a differential ability of painful versus non-painful human schwannomatosis tumor cells to secrete factors that augment sensory neuron responsiveness, and thus identify a potential determinant of pain heterogeneity in schwannomatosis. Nature Publishing Group UK 2019-09-11 /pmc/articles/PMC6739480/ /pubmed/31511601 http://dx.doi.org/10.1038/s41598-019-49705-w Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Ostrow, Kimberly Laskie
Donaldson, Katelyn J.
Caterina, Michael J.
Belzberg, Allan
Hoke, Ahmet
The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity
title The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity
title_full The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity
title_fullStr The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity
title_full_unstemmed The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity
title_short The Secretomes of Painful Versus Nonpainful Human Schwannomatosis Tumor Cells Differentially Influence Sensory Neuron Gene Expression and Sensitivity
title_sort secretomes of painful versus nonpainful human schwannomatosis tumor cells differentially influence sensory neuron gene expression and sensitivity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6739480/
https://www.ncbi.nlm.nih.gov/pubmed/31511601
http://dx.doi.org/10.1038/s41598-019-49705-w
work_keys_str_mv AT ostrowkimberlylaskie thesecretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT donaldsonkatelynj thesecretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT caterinamichaelj thesecretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT belzbergallan thesecretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT hokeahmet thesecretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT ostrowkimberlylaskie secretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT donaldsonkatelynj secretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT caterinamichaelj secretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT belzbergallan secretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity
AT hokeahmet secretomesofpainfulversusnonpainfulhumanschwannomatosistumorcellsdifferentiallyinfluencesensoryneurongeneexpressionandsensitivity