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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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Research works printed but not linked: 58

  1. Cogliano, 2009, A review of human carcinogens—Part B: biological agents, Lancet Oncol, 10, 321, 10.1016/S1470-2045(09)70096-8 · DOI · Paper page
  2. Lima, 2010, Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study, Lancet Oncol, 11, 1048, 10.1016/S1470-2045(10)70230-8 · DOI · Paper page
  3. Plummer, 2012, Global burden of cancers attributable to infections in 2008: a review and synthetic analysis, The Lancet Oncology, 13, 607, 10.1016/S1470-2045(12)70137-7 · DOI
  4. Mougin, 2011, Human papillomavirus genotype distribution in tonsil cancers, Head & neck oncology, 3, 6, 10.1186/1758-3284-3-6 · DOI
  5. Laimins, 2010, Human papillomavirus oncoproteins: pathways to transformation, Nature reviews Cancer, 10, 550, 10.1038/nrc2886 · DOI
  6. Thomas, 2012, Human tumour viruses and the deregulation of cell polarity in cancer, Nature reviews Cancer, 12, 877, 10.1038/nrc3400 · DOI
  7. Ishibashi, 1997, Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein, Proceedings of the National Academy of Sciences of the United States of America, 94, 11612, 10.1073/pnas.94.21.11612 · DOI · Paper page
  8. Lambert, 2007, The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities, Cancer research, 67, 1626, 10.1158/0008-5472.CAN-06-3344 · DOI
  9. Lambert, 2003, The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6's induction of epithelial hyperplasia in vivo, Journal of virology, 77, 6957, 10.1128/JVI.77.12.6957-6964.2003 · DOI
  10. Griep, 2003, Requirement of PDZ-containing proteins for cell cycle regulation and differentiation in the mouse lens epithelium, Molecular and cellular biology, 23, 8970, 10.1128/MCB.23.24.8970-8981.2003 · DOI
  11. Lee, 2008, Deletion of the PDZ motif of HPV16 E6 preventing immortalization and anchorage-independent growth in human tonsil epithelial cells, Head & neck, 30, 139, 10.1002/hed.20673 · DOI
  12. Iftner, 2009, Binding of PDZ proteins to HPV E6 proteins does neither correlate with epidemiological risk classification nor with the immortalization of foreskin keratinocytes, Virology, 387, 380, 10.1016/j.virol.2009.02.018 · DOI
  13. Lee, 2008, The PDZ binding motif of human papillomavirus type 16 E6 induces PTPN13 loss, which allows anchorage-independent growth and synergizes with ras for invasive growth, J Virol, 82, 2493, 10.1128/JVI.02188-07 · DOI
  14. Roberts, 2003, Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes, Journal of cell science, 116, 4925, 10.1242/jcs.00809 · DOI
  15. Banks, 1999, Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation, Oncogene, 18, 5487, 10.1038/sj.onc.1202920 · DOI · Paper page
  16. Gardiol, 2014, Human papillomavirus (HPV)-18 E6 oncoprotein interferes with the epithelial cell polarity Par3 protein, Molecular oncology, 8, 533, 10.1016/j.molonc.2014.01.002 · DOI
  17. Hampson, 2004, The PDZ protein Tip-1 is a gain of function target of the HPV16 E6 oncoprotein, Int J Oncol, 25, 1249
  18. Banks, 2000, Differential regulation of human papillomavirus E6 by protein kinase A: conditional degradation of human discs large protein by oncogenic E6, Oncogene, 19, 5884, 10.1038/sj.onc.1203988 · DOI
  19. Banks, 2013, High-risk human papillomavirus E6 oncoproteins interact with 14-3-3 zeta in a PDZ binding motif-dependent manner, Journal of virology, 87, 1586, 10.1128/JVI.02074-12 · DOI
  20. Silverstein, 2007, PATJ, a tight junction-associated PDZ protein, is a novel degradation target of high-risk human papillomavirus E6 and the alternatively spliced isoform 18 E6, Journal of virology, 81, 4080, 10.1128/JVI.02545-06 · DOI
  21. Huibregtse, 2000, Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase, Molecular and cellular biology, 20, 8244, 10.1128/MCB.20.21.8244-8253.2000 · DOI · Paper page
  22. Javier, 1997, Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein, Proceedings of the National Academy of Sciences of the United States of America, 94, 6670, 10.1073/pnas.94.13.6670 · DOI · Paper page
  23. Banks, 2002, Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation, Oncogene, 21, 5088, 10.1038/sj.onc.1205668 · DOI
  24. Javier, 2000, Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins, Oncogene, 19, 5270, 10.1038/sj.onc.1203906 · DOI · Paper page
  25. Lee, 2008, The PDZ binding motif of human papillomavirus type 16 E6 induces PTPN13 loss, which allows anchorage-independent growth and synergizes with ras for invasive growth, Journal of virology, 82, 2493, 10.1128/JVI.02188-07 · DOI
  26. Vande Pol, 2007, Degradation of tyrosine phosphatase PTPN3 (PTPH1) by association with oncogenic human papillomavirus E6 proteins, Journal of virology, 81, 2231, 10.1128/JVI.01979-06 · DOI
  27. Roberts, 2013, The role of protein kinase A regulation of the E6 PDZ binding domain during differentiation dependent life cycle of human papillomavirus type 18, Journal of virology, 87, 9463, 10.1128/JVI.01234-13 · DOI
  28. Doorbar, 2011, Stabilization of HPV16 E6 protein by PDZ proteins, and potential implications for genome maintenance, Virology, 414, 137, 10.1016/j.virol.2011.03.017 · DOI · Paper page
  29. Laimins, 2004, Role of the PDZ domain-binding motif of the oncoprotein E6 in the pathogenesis of human papillomavirus type 31, J Virol, 78, 12366, 10.1128/JVI.78.22.12366-12377.2004 · DOI · Paper page
  30. Munger, 2001, Centrosome abnormalities and genomic instability by episomal expression of human papillomavirus type 16 in raft cultures of human keratinocytes, Journal of virology, 75, 7712, 10.1128/JVI.75.16.7712-7716.2001 · DOI
  31. Munger, 2002, The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability, Cancer research, 62, 7075
  32. Laimins, 1998, Human papillomavirus oncoproteins E6 and E7 independently abrogate the mitotic spindle checkpoint, J Virol, 72, 1131, 10.1128/JVI.72.2.1131-1137.1998 · DOI
  33. McDougall, 2002, The human papillomavirus type 16 E6 oncogene induces premature mitotic chromosome segregation, Oncogene, 21, 7507, 10.1038/sj.onc.1205903 · DOI
  34. Munger, 2000, The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle, Proceedings of the National Academy of Sciences of the United States of America, 97, 10002, 10.1073/pnas.170093297 · DOI · Paper page
  35. Munger, 2001, Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype, Cancer research, 61, 2356
  36. Roberts, 2007, The full-length E1E4 protein of human papillomavirus type 18 modulates differentiation-dependent viral DNA amplification and late gene expression, Virology, 362, 453, 10.1016/j.virol.2007.01.005 · DOI
  37. McCance, 2010, Compromised spindle assembly checkpoint due to altered expression of Ubch10 and Cdc20 in human papillomavirus type 16 E6- and E7-expressing keratinocytes, Journal of virology, 84, 10956, 10.1128/JVI.00259-10 · DOI
  38. Munger, 1997, The human papillomavirus-16 E6 oncoprotein decreases the vigilance of mitotic checkpoints, Oncogene, 15, 3025, 10.1038/sj.onc.1201495 · DOI
  39. Galloway, 2014, Beta human papillomavirus E6 expression inhibits stabilization of p53 and increases tolerance of genomic instability, Journal of virology, 88, 6112, 10.1128/JVI.03808-13 · DOI
  40. Laimins, 2004, Role of the PDZ domain-binding motif of the oncoprotein E6 in the pathogenesis of human papillomavirus type 31, Journal of virology, 78, 12366, 10.1128/JVI.78.22.12366-12377.2004 · DOI · Paper page
  41. Vande Pol, 2014, Papillomavirus E6 PDZ interactions can be replaced by repression of p53 to promote episomal human papillomavirus genome maintenance, Journal of virology, 88, 3027, 10.1128/JVI.02360-13 · DOI
  42. Androphy, 2002, Genetic analysis of high-risk e6 in episomal maintenance of human papillomavirus genomes in primary human keratinocytes, J Virol, 76, 11359, 10.1128/JVI.76.22.11359-11364.2002 · DOI
  43. Banks, 2016, Analysis of multiple HPV E6 PDZ interactions defines type specific PDZ fingerprints that predict oncogenic potential, PLoS Pathog, 12, e1005766, 10.1371/journal.ppat.1005766 · DOI · Paper page
  44. Roberts, 2016, Viral Interactions with PDZ Domain-Containing Proteins-An Oncogenic Trait?, Pathogens, 5, 10.3390/pathogens5010008 · DOI · Paper page
  45. James, 2015, A study of PDZ protein expression during the human papillomavirus life cycle
  46. Lambert, 2005, Two distinct activities contribute to human papillomavirus 16 E6's oncogenic potential, Cancer research, 65, 8266, 10.1158/0008-5472.CAN-05-1651 · DOI
  47. Lee, 2014, Roles of the PDZ domain-binding motif of the human papillomavirus type 16 E6 on the immortalization and differentiation of primary human foreskin keratinocytes, Virus genes, 48, 224, 10.1007/s11262-013-1017-9 · DOI
  48. Prehoda, 2013, A NudE/14-3-3 pathway coordinates dynein and the kinesin Khc73 to position the mitotic spindle, Developmental cell, 26, 369, 10.1016/j.devcel.2013.07.021 · DOI
  49. Johnston, 2013, Discs large links spindle orientation to apical-basal polarity in Drosophila epithelia, Current biology: CB, 23, 1707, 10.1016/j.cub.2013.07.017 · DOI
  50. Fuchs, 2001, Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin, Cell, 104, 605, 10.1016/S0092-8674(01)00246-X · DOI · Paper page
  51. Munger, 2009, Human papillomavirus E7 protein deregulates mitosis via an association with nuclear mitotic apparatus protein 1, Journal of virology, 83, 1700, 10.1128/JVI.01971-08 · DOI · Paper page
  52. Trave, 2015, Targeting the two oncogenic functional sites of the HPV E6 oncoprotein with a high-affinity bivalent ligand, Angewandte Chemie, 10.1002/anie.201502646 · DOI
  53. Stonehouse, 2014, An RNA aptamer targets the PDZ binding motif of the HPV16 E6 oncoprotein, Cancers, 6, 1553, 10.3390/cancers6031553 · DOI
  54. Banks, 2015, Cancer-causing human papillomavirus E6 proteins display major differences in the phospho-regulation of their PDZ interactions, Journal of virology, 89, 1579, 10.1128/JVI.01961-14 · DOI
  55. Laimins, 2005, Differentiation of HPV-containing cells using organotypic “raft” culture or methylcellulose, Methods in molecular medicine, 119, 157, 10.1385/1-59259-982-6:157 · DOI
  56. Roberts, 2011, A cyclin-binding motif in human papillomavirus type 18 (HPV18) E1-E4 is necessary for association with CDK-cyclin complexes and G2/M cell cycle arrest of keratinocytes, but is not required for differentiation-dependent viral genome amplification or L1 capsid protein expression, Virology, 412, 196, 10.1016/j.virol.2011.01.007 · DOI
  57. Roberts, 2002, Changes in expression of the human homologue of the Drosophila discs large tumour suppressor protein in high-grade premalignant cervical neoplasias, Carcinogenesis, 23, 1791, 10.1093/carcin/23.11.1791 · DOI
  58. Gallimore, 2003, The ND10 component promyelocytic leukemia protein relocates to human papillomavirus type 1 E4 intranuclear inclusion bodies in cultured keratinocytes and in warts, Journal of virology, 77, 673, 10.1128/JVI.77.1.673-684.2003 · DOI

Cited by

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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