Cited by 8Cancer, Stress, Anesthesia, and Immune ResponseCancer Cells and MetastasisNeuroendocrine regulation and behavior

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

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Naderi, Asieh, Soltanmaohammadi, Elham, Kaza, Vimala, Barlow, Shayne, Chatzistamou, Ioulia, Kiaris, Hippokratis·2021·eLife

Abstract

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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Crossref · 10.7554/elife.64711

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  • OT, DA, AVP, and CRF all directly regulate secretions from the pituitary gland and are heavily implicated in pair bonding.

    “OT, DA, AVP, and CRF all directly regulate secretions from the pituitary gland and are heavily implicated in pair bonding.”

    From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [176]

    The Discussion describes oxytocin as having an essential role in social interactions and pair bonding. It does not establish the claimed roles of dopamine, vasopressin, or CRF in pair bonding, or say that all four directly regulate pituitary secretions (pages not provided). (LLM, conf=0.86)

    Experimental — accuracy not yet measured
  • Tumors transplanted from pair-bonded mice to immunocompromised virgin mice displayed less growth than tumors originating from mice with disrupted bonds.

    “Interestingly, tumors transplanted from pair-bonded mice to immunocompromised virgin mice displayed less growth than tumors originating from mice with disrupted bonds.”
  • Human lung cancer cells transplanted to pair-bonded mice showed less tumorigenesis compared to mice whose bond had been disrupted.

    “Human lung cancer cells that were transplanted to pair-bonded mice showed less tumorigenesis compared to mice whose bond had been disrupted, contributing to evidence of the detrimental effects of bond disruption.”
  • In monogamous Peromyscus mice, pair bonding has been shown to be protective against tumor growth.

    “In monogamous Peromyscus mice, pair bonding has been shown to be protective against tumor growth [176].”
  • A recent lung cancer study found that a factor in serum samples of bonded monogamous California mice decreased oncogenic potential of tumor cells when compared to serum samples from bond-disrupted animals.

    “A recent lung cancer study found that a factor in serum samples of bonded monogamous California mice decreased oncogenic potential of tumor cells when compared to serum samples from bond-disrupted animals (172).”

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Authors
Naderi, A., Soltanmaohammadi, E., Kaza, V., Barlow, S., Chatzistamou, I., & Kiaris, H.
Affiliations
  • University of South Carolina (US)
  • Department of Drug Discovery and Biomedical Sciences, College of Pharmacy, University of South Carolina, Columbia, United States
Corresponding author
Kiaris, Hippokratis
Venue
eLife
Published
2021-05-07
Volume
10
ISSN
2050-084X (ISSN-L)
OpenAlex
W3157143566
Cited by
8
References
52
Citations by year
2025: 1 · 2024: 2 · 2023: 3 · 2022: 1 · 2021: 1
FWCI
1.25
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Science Foundation (OIA-1736150)
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
  • Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords
pair bonding, monogamy, lung cancer, carcinogenesis, Peromyscus californicus, Peromyscus polionotus, deer mouse, cancer cell spheroids, cell adhesion, cell migration, stress and anxiety, mouse tumor model
MeSH terms
A549 Cells, Animals, Anxiety, Cell Adhesion, Cell Movement, Female, Humans, Lung Neoplasms, Male, Mice, Nude, Neoplasm Transplantation, Pair Bond, Peromyscus, Stress, Psychological, Cell Transplantation, Spheroids, Cellular, Gene Expression Profiling, Cell Proliferation, Mice, Carcinogenesis

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