Cutaneous β-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling

Tan, Min Jie Alvin; White, Elizabeth A.; Sowa, Mathew E.; Harper, J. Wade; Aster, Jon C.; Howley, Peter M.

doi:10.1073/pnas.1205991109

Cited by 132Cervical Cancer and HPV ResearchDevelopmental Biology and Gene RegulationGenomics and Chromatin Dynamics

Cutaneous β-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling

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Tan, Min Jie Alvin, White, Elizabeth A., Sowa, Mathew E., Harper, J. Wade, Aster, Jon C., Howley, Peter M.·2012·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1205991109PMC PMC3384212

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Abstract

The Notch signaling pathway is a key determinant in keratinocyte differentiation and growth cycle arrest, and has been reported to have a tumor suppressor function in skin. The papillomavirus life cycle is intricately linked to the differentiation status of keratinocytes. Papillomaviruses are associated with benign proliferative epithelial lesions in their respective hosts. Although human papillomaviruses (HPVs) associated with genital tract lesions have been extensively studied, studies of the cutaneous HPVs are more limited. In particular, it is well established that the E6 proteins of high-risk HPVs of the α-genus such as HPV16 and HPV18 mediate the degradation of p53 by its association with the ubiquitin ligase E6AP. In contrast, less is known about the cellular activities of the cutaneous HPVs of the β-genus. By using an unbiased proteomic approach, we identify MAML1 and other members of the Notch transcription complex as high-confidence cellular interacting proteins of E6 proteins of the β-genus HPVs and of the bovine papillomavirus type 1 associated with cutaneous fibropapillomas. We show that bovine papillomavirus type 1 and β-HPV E6 repress Notch transcriptional activation, and that this repression is dependent on an interaction with MAML1. Finally, we show that the expression levels of endogenous Notch target genes are repressed by β-HPV E6 proteins. These findings elucidate a mechanism of viral antagonism of Notch signaling, and suggest that Notch signaling is an important epithelial cell pathway target for the β-HPVs.

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The E6 protein of genus alpha HPV binds specifically to the cellular E6AP protein.
“the E6 protein of genus alpha HPV binds specifically to the cellular E6AP protein”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [69]
Both virus-host interactions are mediated by a similar motif in the cellular protein.
“Both virus–host interactions are mediated by a similar motif in the cellular protein”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [69]
The E6 protein of genus beta HPV binds specifically to cellular MAML1.
“while that of the genus beta HPV binds specifically to cellular MAML1.”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [69]
Both virus-host interactions may be responsible for the different cell type-specific tropisms of the two genera.
“and may be responsible for the different cell type-specific tropisms of the two genera”
From Proteomic approaches to uncovering virus–host protein interactions during the progression of viral infection (2016) · cites this paper as [69]

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Authors: Tan, M. J. A., White, E. A., Sowa, M. E., Harper, J. W., Aster, J. C., & Howley, P. M.
Affiliations: Harvard University (US)
Departments of Microbiology and Immunobiology and
Brigham and Women's Hospital (US)
Corresponding author: Howley, Peter M.
ORCID: Tan, Min Jie Alvin
White, Elizabeth A.
Sowa, Mathew E.
Harper, J. Wade
Aster, Jon C.
Howley, Peter M.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2012-04-30
Volume: 109
Issue: 23
Pages: E1473-80
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1205991109
PMC: PMC3384212
OpenAlex: W2020553511
Cited by: 132
References: 51
Citations by year: 2026: 2 · 2025: 4 · 2024: 7 · 2023: 9 · 2022: 6 · 2021: 8 · 2020: 13 · 2019: 10 · 2018: 7 · 2017: 17 · 2016: 9 · 2015: 10 · 2014: 13 · 2013: 11 · 2012: 6
FWCI: 9.54
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Brigham and Women's Hospital
National Institutes of Health
National Cancer Institute (P01 CA 50661, RC1CA145188, P01CA050661)
National Institute of General Medical Sciences (R01GM054137)
National Institute of Allergy and Infectious Diseases (F32AI080075)
Topics: Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: E6 oncoprotein, Notch signaling, MAML1, bovine papillomavirus type 1, keratinocyte differentiation, Notch target genes
MeSH terms: Animals, Cell Line, DNA-Binding Proteins, Humans, Luciferases, Oncogene Proteins, Viral, Plasmids, Transcription Factors, Transfection, Blotting, Western, Signal Transduction, Proteomics, Mice, Receptors, Notch, Betapapillomavirus, Real-Time Polymerase Chain Reaction

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Cutaneous β-human papillomavirus E6 proteins bind Mastermind-like coactivators and repress Notch signaling

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