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Volume 13
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10.3390/v13091824
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Article

Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues

by
Sarah Brendle
1,2,
Jingwei J. Li
1,2,
Nancy M. Cladel
1,2,
Debra A. Shearer
1,2,
Lynn R. Budgeon
1,2,
Karla K. Balogh
1,2,
Hannah Atkins
3,
Marina Costa-Fujishima
4,
Paul Lopez
4,
Neil D. Christensen
1,2,5,
John Doorbar
6,
Thomas T. Murooka
4 and
Jiafen Hu
1,2,*
1
The Jake Gittlen Laboratories for Cancer Research, Hershey, PA 17033, USA
2
Department of Pathology, Pennsylvania State University College of Medicine, Hershey, PA 17033, USA
3
Laboratory Medicine, Department of Pathology, Division of Comparative Medicine, University of North Carolina, Chapel Hill, NC 27599, USA
4
Department of Immunology, University of Manitoba, Winnipeg, MB R3E 0T5, Canada
5
Department of Microbiology and Immunology, Pennsylvania State University College of Medicine, Hershey, PA 17033, USA
6
Department of Pathology, Division of Virology, University of Cambridge, Tennis Court Road, Cambridge CB21 QP, UK
*
Author to whom correspondence should be addressed.
Viruses 2021, 13(9), 1824; https://doi.org/10.3390/v13091824
Submission received: 30 August 2021 / Revised: 8 September 2021 / Accepted: 10 September 2021 / Published: 14 September 2021
(This article belongs to the Section Animal Viruses)
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Abstract

Papillomavirus L1 and L2, the major and minor capsid proteins, play significant roles in viral assembly, entry, and propagation. In the current study, we investigate the impact of L1 and L2 on viral life cycle and tumor growth with a newly established mouse papillomavirus (MmuPV1) infection model. MmuPV1 L1 knockout, L2 knockout, and L1 plus L2 knockout mutant genomes (designated as L1ATGko-4m, L2ATGko, and L1-L2ATGko respectively) were generated. The mutants were examined for their ability to generate lesions in athymic nude mice. Viral activities were examined by qPCR, immunohistochemistry (IHC), in situ hybridization (ISH), and transmission electron microscopy (TEM) analyses. We demonstrated that viral DNA replication and tumor growth occurred at both cutaneous and mucosal sites infected with each of the mutants. Infections involving L1ATGko-4m, L2ATGko, and L1-L2ATGko mutant genomes generally resulted in smaller tumor sizes compared to infection with the wild type. The L1 protein was absent in L1ATGko-4m and L1-L2ATGko mutant-treated tissues, even though viral transcripts and E4 protein expression were robust. Therefore, L1 is not essential for MmuPV1-induced tumor growth, and this finding parallels our previous observations in the rabbit papillomavirus model. Very few viral particles were detected in L2ATGko mutant-infected tissues. Interestingly, the localization of L1 in lesions induced by L2ATGko was primarily cytoplasmic rather than nuclear. The findings support the hypothesis that the L2 gene influences the expression, location, transport, and assembly of the L1 protein in vivo.
Keywords: mouse papillomavirus; L1 mutant; L2 mutant; viral production; tumor growth; RCA; ISH; IHC; RNAscope; TEM; viral copy number; qPCR mouse papillomavirus; L1 mutant; L2 mutant; viral production; tumor growth; RCA; ISH; IHC; RNAscope; TEM; viral copy number; qPCR

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MDPI and ACS Style

Brendle, S.; Li, J.J.; Cladel, N.M.; Shearer, D.A.; Budgeon, L.R.; Balogh, K.K.; Atkins, H.; Costa-Fujishima, M.; Lopez, P.; Christensen, N.D.; et al. Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues. Viruses 2021, 13, 1824. https://doi.org/10.3390/v13091824

AMA Style

Brendle S, Li JJ, Cladel NM, Shearer DA, Budgeon LR, Balogh KK, Atkins H, Costa-Fujishima M, Lopez P, Christensen ND, et al. Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues. Viruses. 2021; 13(9):1824. https://doi.org/10.3390/v13091824

Chicago/Turabian Style

Brendle, Sarah, Jingwei J. Li, Nancy M. Cladel, Debra A. Shearer, Lynn R. Budgeon, Karla K. Balogh, Hannah Atkins, Marina Costa-Fujishima, Paul Lopez, Neil D. Christensen, and et al. 2021. "Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues" Viruses 13, no. 9: 1824. https://doi.org/10.3390/v13091824

APA Style

Brendle, S., Li, J. J., Cladel, N. M., Shearer, D. A., Budgeon, L. R., Balogh, K. K., Atkins, H., Costa-Fujishima, M., Lopez, P., Christensen, N. D., Doorbar, J., Murooka, T. T., & Hu, J. (2021). Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues. Viruses, 13(9), 1824. https://doi.org/10.3390/v13091824

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