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Mitotic control of human papillomavirus genome-containing cells is regulated by the function of the PDZ-binding motif of the E6 oncoprotein

Marsh, Elizabeth K., Delury, Craig P., Davies, Nicholas J., Weston, Christopher J., Miah, Mohammed A. L., Banks, Lawrence, Parish, Joanna L., Higgs, Martin R., Roberts, Sally·2017·Oncotarget
DOI 10.18632/oncotarget.14469PMC PMC5386700
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Figure 1 Loss of E6 PBM function is associated with enhanced frequency of nuclear atypia of viral genome-containing cells A. Southern analysis confirmed presence of HPV18 wild type (WT) and mutant (E6ΔPDZ) episomes migrating as supercoils (SC) and open circles (OC) in cells; the mutant genomes establish at a lower copy number than the WT genomes as shown previously (the images of the two lanes were taken from the same Southern blot at a single exposure) [27]. B. Phase contrast images of cells grown in monolayer culture, including untransfected donor cells (HFK), with fibroblast feeder cells (F). HPV18 genome-containing cells showing nuclear atypia (multinucleation) are identified (black dotted line). C. Bar graph, percentage of cells containing multiple nuclei; data (mean ± standard error of the mean) derived from random fields of view and cells from three independent donors. Student t test was used to determine the significance (**, P<0.01; ***, P<0.001; ****, P<0.0001). Total number of cells counted: HFK, 2000 cells; WT, 1400 cells; E6ΔPDZ, 1060 cells.
Figure 1 Loss of E6 PBM function is associated with enhanced frequency of nuclear atypia of viral genome-containing cells A. Southern analysis confirmed presence of HPV18 wild type (WT) and mutant (E6ΔPDZ) episomes migrating as supercoils (SC) and open circles (OC) in cells; the mutant genomes establish at a lower copy number than the WT genomes as shown previously (the images of the two lanes were taken from the same Southern blot at a single exposure) [27]. B. Phase contrast images of cells grown in monolayer culture, including untransfected donor cells (HFK), with fibroblast feeder cells (F). HPV18 genome-containing cells showing nuclear atypia (multinucleation) are identified (black dotted line). C. Bar graph, percentage of cells containing multiple nuclei; data (mean ± standard error of the mean) derived from random fields of view and cells from three independent donors. Student t test was used to determine the significance (**, P<0.01; ***, P<0.001; ****, P<0.0001). Total number of cells counted: HFK, 2000 cells; WT, 1400 cells; E6ΔPDZ, 1060 cells.CC BY · PubMed Central
Figure 2 Live cell microscopy shows that loss of E6 PBM function is associated with an increase in abnormal mitoses in viral genome-containing cells Examples of normal A. and abnormal B. mitoses from the live cell microscopy in cell lines harboring the WT or the E6ΔPDZ genomes (movies given in Supplementary Figure 1). Cells undergoing mitosis are identified with a white arrow and the time to complete mitosis is given. Note that in these examples of abnormal mitosis, the event is multipolar and the time taken to completion is much longer than for completion of normal cell division. C. Bar graph, percentage of mitoses that were normal or abnormal in each of the three donor backgrounds. Mitoses defined as normal if bipolar, had visible and equal separation of condensed chromatin and the time to completion of mitosis was not excessive; otherwise the mitotic event was scored as abnormal. Number of colonies counted was in the range of 14 to 23 and for each of the cell lines between 90-308 mitoses counted.
Figure 2 Live cell microscopy shows that loss of E6 PBM function is associated with an increase in abnormal mitoses in viral genome-containing cells Examples of normal A. and abnormal B. mitoses from the live cell microscopy in cell lines harboring the WT or the E6ΔPDZ genomes (movies given in Supplementary Figure 1). Cells undergoing mitosis are identified with a white arrow and the time to complete mitosis is given. Note that in these examples of abnormal mitosis, the event is multipolar and the time taken to completion is much longer than for completion of normal cell division. C. Bar graph, percentage of mitoses that were normal or abnormal in each of the three donor backgrounds. Mitoses defined as normal if bipolar, had visible and equal separation of condensed chromatin and the time to completion of mitosis was not excessive; otherwise the mitotic event was scored as abnormal. Number of colonies counted was in the range of 14 to 23 and for each of the cell lines between 90-308 mitoses counted.CC BY · PubMed Central
Figure 3 Loss of E6 PBM function leads to an enhancement in the frequency of abnormal cells progressing into anaphase and telophase A. Abnormal (bar graph i) or normal (bar graph ii) mitoses were scored in each stage of mitosis (prophase, metaphase, anaphase and telophase) by α-tubulin staining and counterstaining with DAPI. The data are derived from three independent experiments for each of the three donors and presented as a proportion of total abnormal (top graph) or normal (bottom graph) mitoses. For each experiment, a minimum of 200 cells per donor was counted. B. Examples of abnormal mitoses in HPV18 genome-containing cells showing spindle morphology (α-tubulin, green) and chromosomes (DAPI, blue). C. Individual mitotic abnormalities were scored by α-tubulin staining and counterstaining with DAPI. Only the data for anaphase and telophase abnormalities are shown. The data are derived from three independent experiments for each of the three donors, with a minimum of 100 abnormal mitotic cells scored for each experiment, and the data is shown as the mean (± standard error of the mean). The differences in the frequency of individual abnormalities between WT and E6ΔPDZ cells were not statistically significant. D. The frequency of the combined late (anaphase and telophase) mitotic abnormalities in the E6ΔPDZ genome containing cells shown relative to cells harboring the WT genomes. Student's t test was used to determine the significance (*, P<0.05).
Figure 3 Loss of E6 PBM function leads to an enhancement in the frequency of abnormal cells progressing into anaphase and telophase A. Abnormal (bar graph i) or normal (bar graph ii) mitoses were scored in each stage of mitosis (prophase, metaphase, anaphase and telophase) by α-tubulin staining and counterstaining with DAPI. The data are derived from three independent experiments for each of the three donors and presented as a proportion of total abnormal (top graph) or normal (bottom graph) mitoses. For each experiment, a minimum of 200 cells per donor was counted. B. Examples of abnormal mitoses in HPV18 genome-containing cells showing spindle morphology (α-tubulin, green) and chromosomes (DAPI, blue). C. Individual mitotic abnormalities were scored by α-tubulin staining and counterstaining with DAPI. Only the data for anaphase and telophase abnormalities are shown. The data are derived from three independent experiments for each of the three donors, with a minimum of 100 abnormal mitotic cells scored for each experiment, and the data is shown as the mean (± standard error of the mean). The differences in the frequency of individual abnormalities between WT and E6ΔPDZ cells were not statistically significant. D. The frequency of the combined late (anaphase and telophase) mitotic abnormalities in the E6ΔPDZ genome containing cells shown relative to cells harboring the WT genomes. Student's t test was used to determine the significance (*, P<0.05).CC BY · PubMed Central
Figure 4 Increased micronuclei formation associated with E6ΔPDZ genome-containing cells A. The proportion of cells containing micronuclei was scored from DAPI-stained cells. The data were collected from three independent experiments, with a minimum of 200 cells for each donor scored on each occasion. The data are shown as the mean (± standard error of the mean), and in all three donors the frequency was increased in E6ΔPDZ genome-containing cells (*, p<0.05); ns, not significant). B. Images of examples of CENPA positive and negative nuclei; in overlay CENPA (green), nuclei (blue). C. The proportion of cells with micronuclei containing centromeres was determined by immunofluorescence staining for CENPA. The data were collected from three independent experiments, with a minimum of 200 cells with micronuclei scored for each experiment, and shown as the mean (± standard error of the mean).
Figure 4 Increased micronuclei formation associated with E6ΔPDZ genome-containing cells A. The proportion of cells containing micronuclei was scored from DAPI-stained cells. The data were collected from three independent experiments, with a minimum of 200 cells for each donor scored on each occasion. The data are shown as the mean (± standard error of the mean), and in all three donors the frequency was increased in E6ΔPDZ genome-containing cells (*, p<0.05); ns, not significant). B. Images of examples of CENPA positive and negative nuclei; in overlay CENPA (green), nuclei (blue). C. The proportion of cells with micronuclei containing centromeres was determined by immunofluorescence staining for CENPA. The data were collected from three independent experiments, with a minimum of 200 cells with micronuclei scored for each experiment, and shown as the mean (± standard error of the mean).CC BY · PubMed Central
Figure 5 Increased aneuploidy of E6ΔPDZ genome-containing cells Interphase fluorescence in situ hybridization using centromere enumeration probes for chromosomes 10 and 12. The data were collected from three different cell passages, with a minimum of 200 cells with single nuclei scored for each cell passage and given as the percentage of nuclei with diploid or non-diploid chromosome copy number (mean ± standard error of the mean). The statistical significance of the increase in non-diploid copy number was: donor#1, ns; donor#2, p<0.01 for chromosome 10 and 12; donor#3, p<0.01 for chromosome 10 and p<0.05 for chromosome 12.
Figure 5 Increased aneuploidy of E6ΔPDZ genome-containing cells Interphase fluorescence in situ hybridization using centromere enumeration probes for chromosomes 10 and 12. The data were collected from three different cell passages, with a minimum of 200 cells with single nuclei scored for each cell passage and given as the percentage of nuclei with diploid or non-diploid chromosome copy number (mean ± standard error of the mean). The statistical significance of the increase in non-diploid copy number was: donor#1, ns; donor#2, p<0.01 for chromosome 10 and 12; donor#3, p<0.01 for chromosome 10 and p<0.05 for chromosome 12.CC BY · PubMed Central
Figure 6 Loss of E6 PBM function is associated with an alteration in the distribution of α-tubulin stained mitotic cells between basal and surpabasal cell layers of organotypic rafts Sections of organotypic raft cultures of A. untransfected HFK, B. HPV18 WT genome-containing cells and C. cells containing E6ΔPDZ genomes, were stained for α-tubulin (green), HPV18 E4 (red), and DNA (blue). Examples given in B and C were taken from multiple donors. The dotted white line in A, B and C indicates the junction between the basal cell layer and fibroblast embedded collagen matrix. D. The distribution of mitotic cells between the basal and suprabasal cell layers of organotypic rafts shown as a percentage of total α-tubulin stained mitotic cells (± standard error of the mean). Data were collected from three donors, and for each donor five sections of organotypic raft were analyzed (full thickness and entire length). Numbers of α-tubulin stained mitotic cells counted were 47 (HFK), 525 (WT) and 230 (E6ΔPDZ). Student's t test was used to determine significance (**, p<0.01). E. Sections were stained with γ-tubulin to visualize centrosomes and cells with visible centrosomes were scored for centrosome number. Rafts prepared from three different donors were analyzed; numbers of cells scored were: 1772 (HFK), 4022 (WT) and 2758 (E6ΔPDZ). Student's t test was used to determine significance (**, p<0.01; ***, p<0.001). Shown are examples of cells in E6ΔPDZ, WT rafts with >2 centrosomes, and an HFK raft with 2 centrosomes (red, γ-tubulin; blue, DAPI). The E6PDZ centrosomes are shown enlarged in the inset and the dotted white line indicates the junction between the basal cell layer and fibroblast embedded collagen matrix. Scale, 10 μm (inset 18.5 μm).
Figure 6 Loss of E6 PBM function is associated with an alteration in the distribution of α-tubulin stained mitotic cells between basal and surpabasal cell layers of organotypic rafts Sections of organotypic raft cultures of A. untransfected HFK, B. HPV18 WT genome-containing cells and C. cells containing E6ΔPDZ genomes, were stained for α-tubulin (green), HPV18 E4 (red), and DNA (blue). Examples given in B and C were taken from multiple donors. The dotted white line in A, B and C indicates the junction between the basal cell layer and fibroblast embedded collagen matrix. D. The distribution of mitotic cells between the basal and suprabasal cell layers of organotypic rafts shown as a percentage of total α-tubulin stained mitotic cells (± standard error of the mean). Data were collected from three donors, and for each donor five sections of organotypic raft were analyzed (full thickness and entire length). Numbers of α-tubulin stained mitotic cells counted were 47 (HFK), 525 (WT) and 230 (E6ΔPDZ). Student's t test was used to determine significance (**, p<0.01). E. Sections were stained with γ-tubulin to visualize centrosomes and cells with visible centrosomes were scored for centrosome number. Rafts prepared from three different donors were analyzed; numbers of cells scored were: 1772 (HFK), 4022 (WT) and 2758 (E6ΔPDZ). Student's t test was used to determine significance (**, p<0.01; ***, p<0.001). Shown are examples of cells in E6ΔPDZ, WT rafts with >2 centrosomes, and an HFK raft with 2 centrosomes (red, γ-tubulin; blue, DAPI). The E6PDZ centrosomes are shown enlarged in the inset and the dotted white line indicates the junction between the basal cell layer and fibroblast embedded collagen matrix. Scale, 10 μm (inset 18.5 μm).CC BY · PubMed Central

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Metadata

Authors
Marsh, E. K., Delury, C. P., Davies, N. J., Weston, C. J., Miah, M. A. L., Banks, L., Parish, J. L., Higgs, M. R., & Roberts, S.
Affiliations
  • Institute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, United Kingdom
  • Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, United Kingdom
  • International Centre for Genetic Engineering and Biotechnology, Padriciano, Trieste, Italy
Venue
Oncotarget
Publisher
Impact Journals, LLC
Published
2017-01-03
Volume
8
Issue
12
Pages
19491-19506
ISSN
1949-2553
DOI
10.18632/oncotarget.14469
PMC
PMC5386700
Cited by
16
References
2
Language
en

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CoChat. (2026). Citation check: Mitotic control of human papillomavirus genome-containing cells is regulated by the function of the PDZ-binding motif of the E6 oncoprotein. https://app.cochat.ai/papers/10.18632/oncotarget.14469
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Marsh, E. K., Delury, C. P., Davies, N. J., Weston, C. J., Miah, M. A. L., Banks, L., Parish, J. L., Higgs, M. R., & Roberts, S. (2017). Mitotic control of human papillomavirus genome-containing cells is regulated by the function of the PDZ-binding motif of the E6 oncoprotein. Oncotarget. https://doi.org/10.18632/oncotarget.14469