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Biochemical and Functional Interactions of Human Papillomavirus Proteins with Polycomb Group Proteins

McLaughlin-Drubin, Margaret, Munger, Karl·2013·Viruses
DOI 10.3390/v5051231PMC PMC3712305
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Abstract

The role of enzymes involved in polycomb repression of gene transcription has been studied extensively in human cancer. Polycomb repressive complexes mediate oncogene-induced senescence, a principal innate cell-intrinsic tumor suppressor pathway that thwarts expansion of cells that have suffered oncogenic hits. Infections with human cancer viruses including human papillomaviruses (HPVs) and Epstein-Barr virus can trigger oncogene-induced senescence, and the viruses have evolved strategies to abrogate this response in order to establish an infection and reprogram their host cells to establish a long-term persistent infection. As a consequence of inhibiting polycomb repression and evading oncogene induced-senescence, HPV infected cells have an altered epigenetic program as evidenced by aberrant homeobox gene expression. Similar alterations are frequently observed in non-virus associated human cancers and may be harnessed for diagnosis and therapy.

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Figure 1 Cell division in a squamous epithelium. (A) Asymmetric cell division of a basal epithelial cell yields two unequal daughter cells. One remains an undifferentiated, DNA synthesis competent basal epithelial cell whereas the other daughter is a differentiating epithelial cell that will terminally withdraw from the cell division cycle. Human papillomaviruses (HPV) genomes segregated into such cells will retain these cells in a DNA replication competent state and complete their full replicative life cycle including viral progeny synthesis. (B) Symmetric cell division will yield two basal like cells. This mode of cell division is to replenish basal epithelial cell during wound healing. After the initial infection, HPVs establish a long-term persistent infection of these cells where the viral genome is maintained at a low copy number. The viral genome undergoes replication every time the cell replicates its genome. See text for details.
Figure 1 Cell division in a squamous epithelium. (A) Asymmetric cell division of a basal epithelial cell yields two unequal daughter cells. One remains an undifferentiated, DNA synthesis competent basal epithelial cell whereas the other daughter is a differentiating epithelial cell that will terminally withdraw from the cell division cycle. Human papillomaviruses (HPV) genomes segregated into such cells will retain these cells in a DNA replication competent state and complete their full replicative life cycle including viral progeny synthesis. (B) Symmetric cell division will yield two basal like cells. This mode of cell division is to replenish basal epithelial cell during wound healing. After the initial infection, HPVs establish a long-term persistent infection of these cells where the viral genome is maintained at a low copy number. The viral genome undergoes replication every time the cell replicates its genome. See text for details.CC BY · PubMed Central
Figure 2 Polycomb mediated silencing of gene expression. The polycomb repressive complex 2 (PRC2) silences chromatin by trimethylating lysine residue 27 (K27me3) of histone H3, causing chromatin compaction. H3K27me3 marked chromatin is bound by PRC1, which further silences gene expression by monoubiquitinating lysine residue 119 (K119Ub) of histone H2A.
Figure 2 Polycomb mediated silencing of gene expression. The polycomb repressive complex 2 (PRC2) silences chromatin by trimethylating lysine residue 27 (K27me3) of histone H3, causing chromatin compaction. H3K27me3 marked chromatin is bound by PRC1, which further silences gene expression by monoubiquitinating lysine residue 119 (K119Ub) of histone H2A.CC BY · PubMed Central
Figure 3 PRC2 mediated gene silencing is reversible. The EZH2 histone methyl transferase in PRC2 silences gene expression by adding the trimethyl mark on lysine residue 27 of histone H3, and this mark can be removed by one of the two H3K27 specific demethylases, KDM6A or KDM6B. See text for details.
Figure 3 PRC2 mediated gene silencing is reversible. The EZH2 histone methyl transferase in PRC2 silences gene expression by adding the trimethyl mark on lysine residue 27 of histone H3, and this mark can be removed by one of the two H3K27 specific demethylases, KDM6A or KDM6B. See text for details.CC BY · PubMed Central
Figure 4 HPV16 E7 causes increased KDM6A and KDM6B expression. E7 mediated KDM6A and KDM6B induction affects multiple transcriptional programs, including keratinocyte differentiation and cell identity. KDM6B induction represents a cellular defense response to E7 oncogene expression that is to trigger cell cycle arrest and senescence. HPV16 E7 short-circuits this response by targeting the retinoblastoma tumor suppressor for degradation. Several other viruses including EBV have developed strategies to subvert such cellular defense responses. See text for details.
Figure 4 HPV16 E7 causes increased KDM6A and KDM6B expression. E7 mediated KDM6A and KDM6B induction affects multiple transcriptional programs, including keratinocyte differentiation and cell identity. KDM6B induction represents a cellular defense response to E7 oncogene expression that is to trigger cell cycle arrest and senescence. HPV16 E7 short-circuits this response by targeting the retinoblastoma tumor suppressor for degradation. Several other viruses including EBV have developed strategies to subvert such cellular defense responses. See text for details.CC BY · PubMed Central
Figure 5 Induction and abrogation of the Oncogene Induced Senescence (OIS) tumor suppressor response by HPV16 E7. (A) The retinoblastoma tumor suppressor (pRB) pathway regulates S-phase cell cycle entry. Activity of pRB is regulated by phosphorylation by cyclin dependent kinase 4 or 6 (CDK4/6). CDK4/6 activity is activated by association with a D-type cyclin (CCND) and negatively regulated by association with one of several small molecule inhibitors (p16INK4A, p18INK4C and p19INK4D), which are induced in response to different growth suppressive stimuli. CDK4/6 phosphorylation of pRB at the G1/S boundary inactivates the transcriptional repressor activity of the pRB/E2F complex and signals S-phase entry. (B) Oncogenic stimuli such as RAS/RAF signaling or HPV16 E7 expression causes KDM6B expression and de-repression of p16INK4A expression, which inhibits CDK4/6 activity and pRB phosphorylation, causing G1 cell cycle arrest and senescence (OIS). (C) HPV16 E7 has evolved to evade OIS by targeting pRB for ubiquitin mediated proteasomal degradation.
Figure 5 Induction and abrogation of the Oncogene Induced Senescence (OIS) tumor suppressor response by HPV16 E7. (A) The retinoblastoma tumor suppressor (pRB) pathway regulates S-phase cell cycle entry. Activity of pRB is regulated by phosphorylation by cyclin dependent kinase 4 or 6 (CDK4/6). CDK4/6 activity is activated by association with a D-type cyclin (CCND) and negatively regulated by association with one of several small molecule inhibitors (p16INK4A, p18INK4C and p19INK4D), which are induced in response to different growth suppressive stimuli. CDK4/6 phosphorylation of pRB at the G1/S boundary inactivates the transcriptional repressor activity of the pRB/E2F complex and signals S-phase entry. (B) Oncogenic stimuli such as RAS/RAF signaling or HPV16 E7 expression causes KDM6B expression and de-repression of p16INK4A expression, which inhibits CDK4/6 activity and pRB phosphorylation, causing G1 cell cycle arrest and senescence (OIS). (C) HPV16 E7 has evolved to evade OIS by targeting pRB for ubiquitin mediated proteasomal degradation.CC BY · PubMed Central

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Metadata

Authors
McLaughlin-Drubin, M., & Munger, K.
Affiliations
Division of Infectious Diseases, Brigham and Women's Hospital and Department of Medicine, Harvard Medical School, 181 Longwood Avenue, MCP 861, Boston, MA 02115, USA
Venue
Viruses
Publisher
MDPI AG
Published
2013-05-14
Volume
5
Issue
5
Pages
1231-1249
ISSN
1999-4915
DOI
10.3390/v5051231
PMC
PMC3712305
Cited by
28
References
6
Language
en
Licence
creativecommons.org/licenses/by/3.0/ (vor)

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McLaughlin-Drubin, M., & Munger, K. (2013). Biochemical and Functional Interactions of Human Papillomavirus Proteins with Polycomb Group Proteins. Viruses. https://doi.org/10.3390/v5051231