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Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus

Epidemiological evidence suggests that social interactions and especially bonding between couples influence tumorigenesis, yet whether this is due to lifestyle changes, homogamy (likelihood of individuals to marry people of similar health), or directly associated with host-induced effects in tumors...

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Autores principales: Naderi, Asieh, Soltanmaohammadi, Elham, Kaza, Vimala, Barlow, Shayne, Chatzistamou, Ioulia, Kiaris, Hippokratis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104960/
https://www.ncbi.nlm.nih.gov/pubmed/33960931
http://dx.doi.org/10.7554/eLife.64711
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author Naderi, Asieh
Soltanmaohammadi, Elham
Kaza, Vimala
Barlow, Shayne
Chatzistamou, Ioulia
Kiaris, Hippokratis
author_facet Naderi, Asieh
Soltanmaohammadi, Elham
Kaza, Vimala
Barlow, Shayne
Chatzistamou, Ioulia
Kiaris, Hippokratis
author_sort Naderi, Asieh
collection PubMed
description Epidemiological evidence suggests that social interactions and especially bonding between couples influence tumorigenesis, yet whether this is due to lifestyle changes, homogamy (likelihood of individuals to marry people of similar health), or directly associated with host-induced effects in tumors remains debatable. In the present study, we explored if tumorigenesis is associated with the bonding experience in monogamous rodents at which disruption of pair bonds is linked to anxiety and stress. Comparison of lung cancer cell spheroids that formed in the presence of sera from bonded and bond-disrupted deer mice showed that in monogamous Peromyscus polionotus and Peromyscus californicus, but not in polygamous Peromyscus maniculatus, the disruption of pair bonds altered the size and morphology of spheroids in a manner that is consistent with the acquisition of increased oncogenic potential. In vivo, consecutive transplantation of human lung cancer cells between P. californicus, differing in bonding experiences (n = 9 for bonded and n = 7 for bond-disrupted), and nude mice showed that bonding suppressed tumorigenicity in nude mice (p<0.05), suggesting that the protective effects of pair bonds persisted even after bonding ceased. Unsupervised hierarchical clustering indicated that the transcriptomes of lung cancer cells clustered according to the serum donors’ bonding history while differential gene expression analysis pointed to changes in cell adhesion and migration. The results highlight the pro-oncogenic effects of pair-bond disruption, point to the acquisition of expression signatures in cancer cells that are relevant to the bonding experiences of serum donors, and question the ability of conventional mouse models to capture the whole spectrum of the impact of the host in tumorigenesis.
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spelling pubmed-81049602021-05-11 Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus Naderi, Asieh Soltanmaohammadi, Elham Kaza, Vimala Barlow, Shayne Chatzistamou, Ioulia Kiaris, Hippokratis eLife Cancer Biology Epidemiological evidence suggests that social interactions and especially bonding between couples influence tumorigenesis, yet whether this is due to lifestyle changes, homogamy (likelihood of individuals to marry people of similar health), or directly associated with host-induced effects in tumors remains debatable. In the present study, we explored if tumorigenesis is associated with the bonding experience in monogamous rodents at which disruption of pair bonds is linked to anxiety and stress. Comparison of lung cancer cell spheroids that formed in the presence of sera from bonded and bond-disrupted deer mice showed that in monogamous Peromyscus polionotus and Peromyscus californicus, but not in polygamous Peromyscus maniculatus, the disruption of pair bonds altered the size and morphology of spheroids in a manner that is consistent with the acquisition of increased oncogenic potential. In vivo, consecutive transplantation of human lung cancer cells between P. californicus, differing in bonding experiences (n = 9 for bonded and n = 7 for bond-disrupted), and nude mice showed that bonding suppressed tumorigenicity in nude mice (p<0.05), suggesting that the protective effects of pair bonds persisted even after bonding ceased. Unsupervised hierarchical clustering indicated that the transcriptomes of lung cancer cells clustered according to the serum donors’ bonding history while differential gene expression analysis pointed to changes in cell adhesion and migration. The results highlight the pro-oncogenic effects of pair-bond disruption, point to the acquisition of expression signatures in cancer cells that are relevant to the bonding experiences of serum donors, and question the ability of conventional mouse models to capture the whole spectrum of the impact of the host in tumorigenesis. eLife Sciences Publications, Ltd 2021-05-07 /pmc/articles/PMC8104960/ /pubmed/33960931 http://dx.doi.org/10.7554/eLife.64711 Text en © 2021, Naderi et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cancer Biology
Naderi, Asieh
Soltanmaohammadi, Elham
Kaza, Vimala
Barlow, Shayne
Chatzistamou, Ioulia
Kiaris, Hippokratis
Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus
title Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus
title_full Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus
title_fullStr Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus
title_full_unstemmed Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus
title_short Persistent effects of pair bonding in lung cancer cell growth in monogamous Peromyscus californicus
title_sort persistent effects of pair bonding in lung cancer cell growth in monogamous peromyscus californicus
topic Cancer Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104960/
https://www.ncbi.nlm.nih.gov/pubmed/33960931
http://dx.doi.org/10.7554/eLife.64711
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