Regeneration enhances metastasis: A novel role for neurovascular signaling in promoting melanoma brain metastasis

Roshini Prakash; Sivan Izraely; Nikita S. Thareja; Rex H. Lee; Maya Rappaport; Riki Kawaguchi; Orit Sagi-Assif; Shlomit Ben-Menachem; Tsipi Meshel; Michal Machnicki; Shuichi Ohe; Dave S. Hoon; Giovanni Coppola; Isaac P. Witz; S. Thomas Carmichael

doi:10.3389/fnins.2019.00297

Regeneration enhances metastasis: A novel role for neurovascular signaling in promoting melanoma brain metastasis

Roshini Prakash, Sivan Izraely, Nikita S. Thareja, Rex H. Lee, Maya Rappaport, Riki Kawaguchi, Orit Sagi-Assif, Shlomit Ben-Menachem, Tsipi Meshel, Michal Machnicki, Shuichi Ohe, Dave S. Hoon, Giovanni Coppola, Isaac P. Witz, S. Thomas Carmichael^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

14 Scopus citations

Abstract

Neural repair after stroke involves initiation of a cellular proliferative program in the form of angiogenesis, neurogenesis, and molecular growth signals in the surrounding tissue elements. This cellular environment constitutes a niche in which regeneration of new blood vessels and new neurons leads to partial tissue repair after stroke. Cancer metastasis has similar proliferative cellular events in the brain and other organs. Do cancer and CNS tissue repair share similar cellular processes? In this study, we identify a novel role of the regenerative neurovascular niche induced by stroke in promoting brain melanoma metastasis through enhancing cellular interactions with surrounding niche components. Repair-mediated neurovascular signaling induces metastatic cells to express genes crucial to metastasis. Mimicking stroke-like conditions in vitro displays an enhancement of metastatic migration potential and allows for the determination of cell-specific signals produced by the regenerative neurovascular niche. Comparative analysis of both in vitro and in vivo expression profiles reveals a major contribution of endothelial cells in mediating melanoma metastasis. These results point to a previously undiscovered role of the regenerative neurovascular niche in shaping the tumor microenvironment and brain metastatic landscape.

Original language	English
Article number	297
Journal	Frontiers in Neuroscience
Volume	13
Issue number	APR
DOIs	https://doi.org/10.3389/fnins.2019.00297
State	Published - 2019
Externally published	Yes

Bibliographical note

Publisher Copyright:
Copyright © 2019 Prakash, Izraely, Thareja, Lee, Rappaport, Kawaguchi, Sagi-Assif, Ben-Menachem, Meshel, Machnicki, Ohe, Hoon, Coppola, Witz and Carmichael. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Keywords

Angiogenesis
Astrocytosis
Gliosis
Neuroblast
Stroke

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.3389/fnins.2019.00297

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Prakash, R., Izraely, S., Thareja, N. S., Lee, R. H., Rappaport, M., Kawaguchi, R., Sagi-Assif, O., Ben-Menachem, S., Meshel, T., Machnicki, M., Ohe, S., Hoon, D. S., Coppola, G., Witz, I. P., & Thomas Carmichael, S. (2019). Regeneration enhances metastasis: A novel role for neurovascular signaling in promoting melanoma brain metastasis. Frontiers in Neuroscience, 13(APR), Article 297. https://doi.org/10.3389/fnins.2019.00297

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title = "Regeneration enhances metastasis: A novel role for neurovascular signaling in promoting melanoma brain metastasis",

abstract = "Neural repair after stroke involves initiation of a cellular proliferative program in the form of angiogenesis, neurogenesis, and molecular growth signals in the surrounding tissue elements. This cellular environment constitutes a niche in which regeneration of new blood vessels and new neurons leads to partial tissue repair after stroke. Cancer metastasis has similar proliferative cellular events in the brain and other organs. Do cancer and CNS tissue repair share similar cellular processes? In this study, we identify a novel role of the regenerative neurovascular niche induced by stroke in promoting brain melanoma metastasis through enhancing cellular interactions with surrounding niche components. Repair-mediated neurovascular signaling induces metastatic cells to express genes crucial to metastasis. Mimicking stroke-like conditions in vitro displays an enhancement of metastatic migration potential and allows for the determination of cell-specific signals produced by the regenerative neurovascular niche. Comparative analysis of both in vitro and in vivo expression profiles reveals a major contribution of endothelial cells in mediating melanoma metastasis. These results point to a previously undiscovered role of the regenerative neurovascular niche in shaping the tumor microenvironment and brain metastatic landscape.",

keywords = "Angiogenesis, Astrocytosis, Gliosis, Neuroblast, Stroke",

author = "Roshini Prakash and Sivan Izraely and Thareja, {Nikita S.} and Lee, {Rex H.} and Maya Rappaport and Riki Kawaguchi and Orit Sagi-Assif and Shlomit Ben-Menachem and Tsipi Meshel and Michal Machnicki and Shuichi Ohe and Hoon, {Dave S.} and Giovanni Coppola and Witz, {Isaac P.} and {Thomas Carmichael}, S.",

note = "Publisher Copyright: Copyright {\textcopyright} 2019 Prakash, Izraely, Thareja, Lee, Rappaport, Kawaguchi, Sagi-Assif, Ben-Menachem, Meshel, Machnicki, Ohe, Hoon, Coppola, Witz and Carmichael. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.",

year = "2019",

doi = "10.3389/fnins.2019.00297",

language = "אנגלית",

volume = "13",

journal = "Frontiers in Neuroscience",

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Prakash, R, Izraely, S, Thareja, NS, Lee, RH, Rappaport, M, Kawaguchi, R, Sagi-Assif, O, Ben-Menachem, S, Meshel, T, Machnicki, M, Ohe, S, Hoon, DS, Coppola, G, Witz, IP & Thomas Carmichael, S 2019, 'Regeneration enhances metastasis: A novel role for neurovascular signaling in promoting melanoma brain metastasis', Frontiers in Neuroscience, vol. 13, no. APR, 297. https://doi.org/10.3389/fnins.2019.00297

TY - JOUR

T1 - Regeneration enhances metastasis

T2 - A novel role for neurovascular signaling in promoting melanoma brain metastasis

AU - Prakash, Roshini

AU - Izraely, Sivan

AU - Thareja, Nikita S.

AU - Lee, Rex H.

AU - Rappaport, Maya

AU - Kawaguchi, Riki

AU - Sagi-Assif, Orit

AU - Ben-Menachem, Shlomit

AU - Meshel, Tsipi

AU - Machnicki, Michal

AU - Ohe, Shuichi

AU - Hoon, Dave S.

AU - Coppola, Giovanni

AU - Witz, Isaac P.

AU - Thomas Carmichael, S.

N1 - Publisher Copyright: Copyright © 2019 Prakash, Izraely, Thareja, Lee, Rappaport, Kawaguchi, Sagi-Assif, Ben-Menachem, Meshel, Machnicki, Ohe, Hoon, Coppola, Witz and Carmichael. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

PY - 2019

Y1 - 2019

N2 - Neural repair after stroke involves initiation of a cellular proliferative program in the form of angiogenesis, neurogenesis, and molecular growth signals in the surrounding tissue elements. This cellular environment constitutes a niche in which regeneration of new blood vessels and new neurons leads to partial tissue repair after stroke. Cancer metastasis has similar proliferative cellular events in the brain and other organs. Do cancer and CNS tissue repair share similar cellular processes? In this study, we identify a novel role of the regenerative neurovascular niche induced by stroke in promoting brain melanoma metastasis through enhancing cellular interactions with surrounding niche components. Repair-mediated neurovascular signaling induces metastatic cells to express genes crucial to metastasis. Mimicking stroke-like conditions in vitro displays an enhancement of metastatic migration potential and allows for the determination of cell-specific signals produced by the regenerative neurovascular niche. Comparative analysis of both in vitro and in vivo expression profiles reveals a major contribution of endothelial cells in mediating melanoma metastasis. These results point to a previously undiscovered role of the regenerative neurovascular niche in shaping the tumor microenvironment and brain metastatic landscape.

AB - Neural repair after stroke involves initiation of a cellular proliferative program in the form of angiogenesis, neurogenesis, and molecular growth signals in the surrounding tissue elements. This cellular environment constitutes a niche in which regeneration of new blood vessels and new neurons leads to partial tissue repair after stroke. Cancer metastasis has similar proliferative cellular events in the brain and other organs. Do cancer and CNS tissue repair share similar cellular processes? In this study, we identify a novel role of the regenerative neurovascular niche induced by stroke in promoting brain melanoma metastasis through enhancing cellular interactions with surrounding niche components. Repair-mediated neurovascular signaling induces metastatic cells to express genes crucial to metastasis. Mimicking stroke-like conditions in vitro displays an enhancement of metastatic migration potential and allows for the determination of cell-specific signals produced by the regenerative neurovascular niche. Comparative analysis of both in vitro and in vivo expression profiles reveals a major contribution of endothelial cells in mediating melanoma metastasis. These results point to a previously undiscovered role of the regenerative neurovascular niche in shaping the tumor microenvironment and brain metastatic landscape.

KW - Angiogenesis

KW - Astrocytosis

KW - Gliosis

KW - Neuroblast

KW - Stroke

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AN - SCOPUS:85068424656

SN - 1662-4548

VL - 13

JO - Frontiers in Neuroscience

JF - Frontiers in Neuroscience

IS - APR

M1 - 297

ER -

Regeneration enhances metastasis: A novel role for neurovascular signaling in promoting melanoma brain metastasis

Abstract

Bibliographical note

Keywords

UN SDGs

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