Fusobacterium nucleatum infection modulates the transcriptome and epigenome of HCT116 colorectal cancer cells in an oxygen-dependent manner.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
08 May 2024
Historique:
received: 03 11 2023
accepted: 16 04 2024
medline: 9 5 2024
pubmed: 9 5 2024
entrez: 8 5 2024
Statut: epublish

Résumé

Fusobacterium nucleatum, a gram-negative oral bacterium, has been consistently validated as a strong contributor to the progression of several types of cancer, including colorectal (CRC) and pancreatic cancer. While previous in vitro studies have shown that intracellular F. nucleatum enhances malignant phenotypes such as cell migration, the dependence of this regulation on features of the tumor microenvironment (TME) such as oxygen levels are wholly uncharacterized. Here we examine the influence of hypoxia in facilitating F. nucleatum invasion and its effects on host responses focusing on changes in the global epigenome and transcriptome. Using a multiomic approach, we analyze epigenomic alterations of H3K27ac and global transcriptomic alterations sustained within a hypoxia and normoxia conditioned CRC cell line HCT116 at 24 h following initial infection with F. nucleatum. Our findings reveal that intracellular F. nucleatum activates signaling pathways and biological processes in host cells similar to those induced upon hypoxia conditioning in the absence of infection. Furthermore, we show that a hypoxic TME favors F. nucleatum invasion and persistence and therefore infection under hypoxia may amplify malignant transformation by exacerbating the effects induced by hypoxia alone. These results motivate future studies to investigate host-microbe interactions in tumor tissue relevant conditions that more accurately define parameters for targeted cancer therapies.

Identifiants

pubmed: 38720110
doi: 10.1038/s42003-024-06201-w
pii: 10.1038/s42003-024-06201-w
doi:

Substances chimiques

Oxygen S88TT14065

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

551

Subventions

Organisme : U.S. Department of Health & Human Services | NIH | National Cancer Institute (NCI)
ID : R21CA238630
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM143940
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)
ID : R01GM141096
Organisme : NSF | Directorate for Engineering (ENG/OAD)
ID : CBET-1652112

Informations de copyright

© 2024. The Author(s).

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Auteurs

Barath Udayasuryan (B)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Zirui Zhou (Z)

Department of Chemical Engineering, Virginia Tech, Blacksburg, VA, USA.

Raffae N Ahmad (RN)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Polina Sobol (P)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Chengyu Deng (C)

Department of Chemical Engineering, Virginia Tech, Blacksburg, VA, USA.

Tam T D Nguyen (TTD)

Department of Biochemistry, Virginia Tech, Blacksburg, VA, USA.

Shivanie Kodikalla (S)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Ryan Morrison (R)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Ishan Goswami (I)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Daniel J Slade (DJ)

Department of Biochemistry, Virginia Tech, Blacksburg, VA, USA.

Scott S Verbridge (SS)

School of Biomedical Engineering and Sciences, Virginia Tech-Wake Forest University, Blacksburg, VA, USA.

Chang Lu (C)

Department of Chemical Engineering, Virginia Tech, Blacksburg, VA, USA. changlu@vt.edu.

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