Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.

Multiple studies report that melanomas are innervated tumors with sensory and sympathetic fibers where these neural fibers play crucial functional roles in tumor growth and metastasis with branch specificity. Yet there is no study which reports the direct neural recording and its pattern during in-v...

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Main Authors: Jay Shiralkar, Tiana Anthony, Grant A McCallum, Dominique M Durand
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0297281&type=printable
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author Jay Shiralkar
Tiana Anthony
Grant A McCallum
Dominique M Durand
author_facet Jay Shiralkar
Tiana Anthony
Grant A McCallum
Dominique M Durand
author_sort Jay Shiralkar
collection DOAJ
description Multiple studies report that melanomas are innervated tumors with sensory and sympathetic fibers where these neural fibers play crucial functional roles in tumor growth and metastasis with branch specificity. Yet there is no study which reports the direct neural recording and its pattern during in-vivo progression of the cancer. We performed daily neural recordings from male and female mice bearing orthotopic metastasizing- melanomas and melanomas with low metastatic poential, derived from B16-F10 and B16-F1 cells, respectively. Further, to explore the origins of neural activity, 6-Hydroxidopamine mediated chemical sympathectomy was performed followed by daily microneurographic recordings. We also performed the daily bioluminescent imaging to track in vivo growth of primary tumors and distant metastasis to the cranial area. Our results show that metastasizing tumors display high levels of neural activity while tumors with low metastatic potential lack it indicating that the presence of neural activity is linked to the metastasizing potential of the tumors. Moreover, the neural activity is not continuous over the tumor progression and has a sex-specific temporal patterns where males have two peaks of high neural activity while females show a single peak. The neural peak activity originated in peripheral sympathetic nerves as sympathectomy completely eliminated the peak activity in both sexes. Peak activities were highly correlated with the distant metastasis in both sexes. These results show that sympathetic neural activity is crucially involved in tumor metastasis and has sex-specific role in malignancy initiation.
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spelling doaj-art-60f2d00775ea476e9a696b0f5d5c686d2025-02-05T05:32:30ZengPublic Library of Science (PLoS)PLoS ONE1932-62032024-01-01192e029728110.1371/journal.pone.0297281Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.Jay ShiralkarTiana AnthonyGrant A McCallumDominique M DurandMultiple studies report that melanomas are innervated tumors with sensory and sympathetic fibers where these neural fibers play crucial functional roles in tumor growth and metastasis with branch specificity. Yet there is no study which reports the direct neural recording and its pattern during in-vivo progression of the cancer. We performed daily neural recordings from male and female mice bearing orthotopic metastasizing- melanomas and melanomas with low metastatic poential, derived from B16-F10 and B16-F1 cells, respectively. Further, to explore the origins of neural activity, 6-Hydroxidopamine mediated chemical sympathectomy was performed followed by daily microneurographic recordings. We also performed the daily bioluminescent imaging to track in vivo growth of primary tumors and distant metastasis to the cranial area. Our results show that metastasizing tumors display high levels of neural activity while tumors with low metastatic potential lack it indicating that the presence of neural activity is linked to the metastasizing potential of the tumors. Moreover, the neural activity is not continuous over the tumor progression and has a sex-specific temporal patterns where males have two peaks of high neural activity while females show a single peak. The neural peak activity originated in peripheral sympathetic nerves as sympathectomy completely eliminated the peak activity in both sexes. Peak activities were highly correlated with the distant metastasis in both sexes. These results show that sympathetic neural activity is crucially involved in tumor metastasis and has sex-specific role in malignancy initiation.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0297281&type=printable
spellingShingle Jay Shiralkar
Tiana Anthony
Grant A McCallum
Dominique M Durand
Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.
PLoS ONE
title Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.
title_full Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.
title_fullStr Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.
title_full_unstemmed Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.
title_short Neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential.
title_sort neural recordings can differentiate between spontaneously metastasizing melanomas and melanomas with low metastatic potential
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0297281&type=printable
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