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Induction of APOBEC3-mediated genomic damage in urothelium implicates BK polyomavirus (BKPyV) as a hit-and-run driver for bladder cancer

Induction of APOBEC3-mediated genomic damage in urothelium implicates BK polyomavirus (BKPyV) as a hit-and-run driver for bladder cancer
Induction of APOBEC3-mediated genomic damage in urothelium implicates BK polyomavirus (BKPyV) as a hit-and-run driver for bladder cancer

Limited understanding of bladder cancer aetiopathology hampers progress in reducing incidence. Mutational signatures show the anti-viral apolipoprotein B mRNA editing enzyme catalytic polypeptide (APOBEC) enzymes are responsible for the preponderance of mutations in bladder tumour genomes, but no causative viral agent has been identified. BK polyomavirus (BKPyV) is a common childhood infection that remains latent in the adult kidney, where reactivation leads to viruria. This study provides missing mechanistic evidence linking reactivated BKPyV-infection to bladder cancer risk. We used a mitotically-quiescent, functionally-differentiated model of normal human urothelium to examine BKPyV-infection. BKPyV-infection led to significantly elevated APOBEC3A and APOBEC3B protein, increased deaminase activity and greater numbers of apurinic/apyrimidinic sites in the host urothelial genome. BKPyV Large T antigen (LT-Ag) stimulated re-entry from G0 into the cell cycle through inhibition of retinoblastoma protein and activation of EZH2, E2F1 and FOXM1, with cells arresting in G2. The single-stranded DNA displacement loops formed in urothelial cells during BKPyV-infection interacted with LT-Ag to provide a substrate for APOBEC3-activity. Addition of interferon gamma (IFNγ) to infected urothelium suppressed expression of the viral genome. These results support reactivated BKPyV infections in adults as a risk factor for bladder cancer in immune-insufficient populations.

APOBEC Deaminases/genetics, Adult, Antigens, Viral, Tumor, BK Virus/genetics, Child, Cytidine Deaminase/genetics, Humans, Minor Histocompatibility Antigens, Polyomavirus Infections/complications, Proteins, Urinary Bladder Neoplasms/genetics, Urothelium/pathology
0950-9232
2139-2151
Baker, Simon C.
39e632d1-a43a-4c6d-b4d5-493814437050
Mason, Andrew S.
2d3126eb-4c2e-43a8-a223-fe267ca7c7fc
Slip, Raphael G.
8bf4582f-1f42-4af2-9c5c-46f850d2b81e
Skinner, Katie T.
6a723310-7657-45eb-9986-7f1846a7fa18
Macdonald, Andrew
d4412c56-c045-4640-ae02-98336d1b5a0d
Masood, Omar
91f735a4-f672-488d-9b76-657004d7b85c
Harris, Reuben S.
52bd046f-9c2b-4526-a26b-f3f23e632dcd
Fenton, Tim R.
087260ba-f6a1-405a-85df-099d05810a84
Periyasamy, Manikandan
3a84a6c0-4e0f-47da-ada8-00d4d3c3d667
Ali, Simak
7d471c65-fb89-4edb-be44-965f39215a85
Southgate, Jennifer
24328d23-bcd3-4b92-8edc-53dab67e7ea1
et al.
Baker, Simon C.
39e632d1-a43a-4c6d-b4d5-493814437050
Mason, Andrew S.
2d3126eb-4c2e-43a8-a223-fe267ca7c7fc
Slip, Raphael G.
8bf4582f-1f42-4af2-9c5c-46f850d2b81e
Skinner, Katie T.
6a723310-7657-45eb-9986-7f1846a7fa18
Macdonald, Andrew
d4412c56-c045-4640-ae02-98336d1b5a0d
Masood, Omar
91f735a4-f672-488d-9b76-657004d7b85c
Harris, Reuben S.
52bd046f-9c2b-4526-a26b-f3f23e632dcd
Fenton, Tim R.
087260ba-f6a1-405a-85df-099d05810a84
Periyasamy, Manikandan
3a84a6c0-4e0f-47da-ada8-00d4d3c3d667
Ali, Simak
7d471c65-fb89-4edb-be44-965f39215a85
Southgate, Jennifer
24328d23-bcd3-4b92-8edc-53dab67e7ea1

Baker, Simon C., Mason, Andrew S. and Slip, Raphael G. , et al. (2022) Induction of APOBEC3-mediated genomic damage in urothelium implicates BK polyomavirus (BKPyV) as a hit-and-run driver for bladder cancer. Oncogene, 41 (15), 2139-2151. (doi:10.1038/s41388-022-02235-8).

Record type: Article

Abstract

Limited understanding of bladder cancer aetiopathology hampers progress in reducing incidence. Mutational signatures show the anti-viral apolipoprotein B mRNA editing enzyme catalytic polypeptide (APOBEC) enzymes are responsible for the preponderance of mutations in bladder tumour genomes, but no causative viral agent has been identified. BK polyomavirus (BKPyV) is a common childhood infection that remains latent in the adult kidney, where reactivation leads to viruria. This study provides missing mechanistic evidence linking reactivated BKPyV-infection to bladder cancer risk. We used a mitotically-quiescent, functionally-differentiated model of normal human urothelium to examine BKPyV-infection. BKPyV-infection led to significantly elevated APOBEC3A and APOBEC3B protein, increased deaminase activity and greater numbers of apurinic/apyrimidinic sites in the host urothelial genome. BKPyV Large T antigen (LT-Ag) stimulated re-entry from G0 into the cell cycle through inhibition of retinoblastoma protein and activation of EZH2, E2F1 and FOXM1, with cells arresting in G2. The single-stranded DNA displacement loops formed in urothelial cells during BKPyV-infection interacted with LT-Ag to provide a substrate for APOBEC3-activity. Addition of interferon gamma (IFNγ) to infected urothelium suppressed expression of the viral genome. These results support reactivated BKPyV infections in adults as a risk factor for bladder cancer in immune-insufficient populations.

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Accepted/In Press date: 4 February 2022
e-pub ahead of print date: 22 February 2022
Published date: 22 February 2022
Keywords: APOBEC Deaminases/genetics, Adult, Antigens, Viral, Tumor, BK Virus/genetics, Child, Cytidine Deaminase/genetics, Humans, Minor Histocompatibility Antigens, Polyomavirus Infections/complications, Proteins, Urinary Bladder Neoplasms/genetics, Urothelium/pathology

Identifiers

Local EPrints ID: 472887
URI: http://eprints.soton.ac.uk/id/eprint/472887
ISSN: 0950-9232
PURE UUID: 2daae13a-c7b9-46bc-87ce-35cd901d5fd6
ORCID for Tim R. Fenton: ORCID iD orcid.org/0000-0002-4737-8233

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Date deposited: 05 Jan 2023 17:39
Last modified: 14 May 2024 02:02

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Contributors

Author: Simon C. Baker
Author: Andrew S. Mason
Author: Raphael G. Slip
Author: Katie T. Skinner
Author: Andrew Macdonald
Author: Omar Masood
Author: Reuben S. Harris
Author: Tim R. Fenton ORCID iD
Author: Manikandan Periyasamy
Author: Simak Ali
Author: Jennifer Southgate
Corporate Author: et al.

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