MECHANISMS OF EVACUATION OF THE HUMAN PAPILLOMA VIRUS FROM THE IMMUNE RESPONSE IN HIV-INFECTED PEOPLE

Tatiana V. Mahorina – PhD, researcher, laboratory of arthropod-borne viral infections and tick-borne encephalitis, Federal Budgetary Institution of Science “Federal Scientific Research Institute of Viral Infection “Virome” Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing”, Ekaterinburg, Russian Federation. E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.
Ksenia E. Boeva – junior researcher, laboratory of arthropod-borne viral infections and tick-borne encephalitis, Federal Budgetary Institution of Science “Federal Scientific Research Institute of Viral Infection “Virome” Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing”, Ekaterinburg, Russian Federation. E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.
Galina V. Malyshkina – junior researcher, laboratory of arthropod-borne viral infections and tick-borne encephalitis; Federal Budgetary Institution of Science “Federal Scientific Research Institute of Viral Infection “Virome” Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing”, Ekaterinburg, Russian Federation. E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.
Alexandr V. Semenov – Head of Federal Budgetary Institution of Science “Federal Scientific Research Institute of Viral Infection “Virome” Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing”, Ekaterinburg, Russian Federation; Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing; member of Russian Association of Allergologists and Clinical Immunologists (St. Petersburg Branch), professor of the experimental biology and biotechnology department, Institute of Natural Sciences and Mathematics of Ural Federal University named after the first President of Russia B. N. Yeltsin, Ekaterinburg, Russian Federation. E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.

1. Lefkowitz EJ, Dempsey DM, Hendrickson RC, et al. Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Research. 2018;46(D1):708-17. DOI: 10.1093/nar/gkx932
2. Bernard HU, Burk RD, Chen Z, et al. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2019;39(29):70-79. DOI: 0.1016/j.virol.2010.02.002
3. De Villiers EM. Classification of papilloma-viruses. Virology. 2004;324(1):17-27. DOI: 10.1016/j.virol. 2004.03.033
4. Szarewski A. Cervarix?: a bivalent vaccine against HPV types 16 and 18, with cross-protection against other high-risk HPV types. Expert Rev Vaccines. 2012;11(6):645-57. DOI: 10.1586/erv.12.42.
5. Zhai L, Tumban T. Gardasil-9?: A global survey of projected efficacy. Antiviral Research. 2016;130:101-9. DOI: 10.1016/j.antiviral.2016.03.016
6. Siegel RL, Miller KD, Jemal A. Cancer statistics. C.A // A Cancer Jourlan for Clinicans. 2017;67(1):7-30. DOI: 10.3322/caac.21387
7. Serrano B, Brotons M, Bosch FX, et al. Epidemiology and burden of HPV-related disease. Best Practice & Research Clinical Obstetrics & Gynaecology. 2018;47:14-26. DOI: 10.1016/j.bpobgyn.2017.08.006
8. Viarisio D, Gissmann L, Tommasino M. Human papillomaviruses and carcinogenesis: wellestablished and novel models. Current Opinion in Virology. 2017;26:56-62. DOI: 10.1016/j.coviro.2017.07.014
9. Brianti P, De Flammineis E, Mercuri SR. Review of HPV-related diseases and cancers. New Microbiologica. 2017;40(2):80-85. PMID: 28368072.
10. Crosbie EJ, Einstein MH, Franceschi S, et al. Human papillomavirus and cervical cancer. Lancet. 2013;382(9895):889-99. DOI: 10.1016/S0140-6736(13)60022-7
11. Daud II, Scott ME, Ma Y. Association between toll-like receptor expression and human papillomavirus type 16 persistence/ International Journal of Cancer. 2011;128(4):879-86. DOI: 10.1002/ijc.25400
12. Joseph AW, Cody JW, Dohun P. Evasion of host immune defenses by human papillomavirus. Virus Research. 2017;231:21-33. DOI: 10.1016/j.virusres.2016. 11.023
13. Haller O, Kochs G, Weber F. The interferon response circuit: induction and suppression by pathogenic viruses. Virology. 2006;344(1):119-30. DOI: 10.1016/ j.virol.2005.09.024
14. Tummers B, Goedemans R, Pelascini LP, et al. The interferon-related developmental regulator 1 is used by human papillomavirus to suppress NF?B activation. Nature Communications. 2015;6:6537. DOI: 10.1038/ncomms7537
15. Richards KH, Doble R, Wasson CW, et al. Human papillomavirus E7 oncoprotein increases production of the anti-inflammatory interleukin-18 binding protein in keratinocytes. Journal of Virology. 2014;88(8):4173-9. DOI: 10.1128/JVI.02546-13
16. Shurin GV, Ferri RL, Tourkova IL, et al. Loss of new chemokine CXCL14 in tumor tissue is associated with low infiltration by dendritic cells (DC), while restoration of human CXCL14 expression in tumor cells causes attraction of DC both in vitro and in vivo. Journal of Immunology. 2005;174(9):5490-8. DOI: 10.4049/jimmunol.174.9.5490
17. Cicchini L, Westrich JA, Xu T, et al. Suppression of antitumor immune responses by human papillomavirus through epigenetic downregulation of CXCL14. MBio. 2016;7(3):е00270-16. DOI: 10.1128/mBio.00270-16
18. Sotlar K, K?veker G, Aepinus C, et al. Human papillomavirus type 16-associated primary squamous cell carcinoma of the rectum. Gastroenterology. 2001;120(4):988-94. DOI: 10.1053/ gast.2001.22523
19. Fahey LM, Raff AB, Da Silva DM, et al. A major role for the minor capsid protein of human papillomavirus type 16 in immune escape. Journal of Immunology. 2009;183(10):6151-6. DOI: 10.4049/jimmunol.0902145
20. Amador-Molina A, Hernandez-Valencia JF, Lamoyi E, et al. Role of innate immunity against human papillomavirus (HPV) infections and effect of adjuvants in promoting specific immune response. Viruses. 2013;5(11):2624-42. https: 10.3390/v5112624
21. Orange JS. Natural killer cell deficiency. Journal of Allergy and Clinical Immunology. 2013;132(3):515-25. DOI: 10.1016/j.jaci.2013.07.020
22. Handisurya A, Day PM, Thompson CD, et al. Strain-specific properties and T cells regulate the susceptibility to papilloma induction by Mus musculus papillomavirus 1. PLOS Pathogens. 2014;10(8):e1004314. DOI: 10.1371/journal.ppat. 1004314
23. Uberoi A, Yoshida S, Frazer IH, et al. Role of ultraviolet radiation in papillomavirus-induced disease. PLOS Pathogens. 2016;12(5):e1005664. DOI: 10.1371/journal.ppat.1005664
24. Jackson SE, Mason GM, Wills MR. Human cytomegalovirus immunity and immune evasion. Virus Research. 2011;157(2):e1005664 151-60. DOI: 10.1016/j.virusres.2010.10.031
25. DiMaio D, Petti LM. The E5 proteins. Virology. 2013;445(1-2):99-114. DOI: 10.1016/j.virol.2013.05.006
26. Campo MS, Graham SV, Cortese MS, et al. HPV-16 E5 down-regulates expression of surface HLA class I and reduces recognition by CD8 T cells. Virology. 2010;407(1):137-42. DOI: 10.1016/j.virol.2010.07.044
27. Miura S, Kawana K, Schust DJ, et al. CD1d, a sentinel molecule bridging innate and adaptive immunity, is downregulated by the human papillomavirus (HPV) E5 protein: a possible mechanism for immune evasion by HPV. Journal of Virology. 2010;84(22):11614-23. DOI: 10.1128/JVI.01053-10
28. Ashrafi GH, Haghshenas M, Marchetti B, et al. E5 protein of human papillomavirus 16 downregulates HLA class I and interacts with the heavy chain via its first hydrophobic domain. International Journal of Cancer. 2006;119(9):2105-12. DOI: 10.1002/ijc.22089
29. Seitz H, Schmitt M, Bohmer G, et al. Natural variants in the major neutralizing epitope of human papillomavirus minor capsid protein L2. International Journal of Cancer. 2013;132(3):e139-48. DOI: 10.1002/ijc.27831
30. Strickler HD, Burk RD, Fazzari M, et al. Natural history and possible reactivation of human papillomavirus in human immunodeficiency virus-positive women. Journal of the National Cancer Institute. 2005;97(8):577-86. DOI: 10.1093/jnci/dji073
31. Wang CJ, Sparano J, Palefsky JM. Human immunodeficiency virus/AIDS, human papillomavirus, and anal cancer. Surgical Oncology Clinics of North America. 2017;26(1):17-31. DOI: 10.1016/j.soc.2016.07.010
32. Bonnet F, Ch?ne G. Evolving epidemiology of malignancies in HIV. Current Opinion in Oncology. 2008;20(5):534-40. DOI: 10.1097/CCO.0b013e32830a5080
33. Shiels MS, Cole SR, Kirk GD, et al. A meta-analysis of the incidence of non-AIDS cancers in HIV-infected individuals. Journal of Acquired Immune Deficiency Syndromes. 2009;52(5):611-22. DOI: 10.1097/QAI.0b013e3181b327ca
34. Williamson AL. The interaction between human immunodeficiency virus and human papillomaviruses in heterosexuals in Africa. Journal of Clinical Medicine. 2015;4(4):579-92. DOI: 10.3390/jcm4040579
35. Scott M, Nakagawa M, Moscicki AB. Cell-mediated immune response to human papillomavirus infection. Clinical and Diagnostic Laboratory Immunology. 2001;8(2):209-20. DOI: 10.1128/CDLI.8.2.209-220.2001
36. Alkhatib G. The biology of CCR5 and CXCR4. Current Opinion in HIV AIDS. 2009;4(2):96-103. DOI: 10.1097/COH.0b013e328324bbec
37. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood. 2006;107(5):1761-7. DOI: 10.1182/blood-2005-08-3182
38. Ansari AW, Heiken H, Moenkemeyer M, et al. Dichotomous effects of C-C chemokines in HIV-1 pathogenesis. Immunology Letters. 2007;110(1):1-5. DOI: 10.1016/j.imlet.2007.02.012
39. Rice AP. The HIV-1 Tat protein: mechanism of action and target for HIV-1 cure strategies. Current Pharmaceutical Design. 2017;23(28):4098-102. DOI: 10.2174/1381612823666170704130635
40. Palefsky J. Biology of HPV in HIV infection. Advances in Dental Research. 2006;19(1):99-105. DOI: 10.1177/ 154407370601900120
41. Das AT, Harwig A, Berkhout B. The HIV-1 Tat protein has a versatile role in activating viral transcription. Journal of Virology. 2011;85(18):9506-16. DOI: 10.1128/JVI.00650-11
42. Syrjanen S. Human papillomavirus infection and its association with HIV. Advances in Dental Research. 2011;23(1):84-89. DOI: 10.1177/0022034511399914
43. Barillari G, Palladino C, Bacigalupo I, et al. Entrance of the Tat protein of HIV-1 into human uterine cervical carcinoma cells causes upregulation of HPV-E6 expression and a decrease in p53 protein levels. Oncology Letters. 2016;12(4):2389-94. DOI: 10.3892/ol.2016.4921
44. Nyagol J, Leucci E, Onnis A, et al. The effects of HIV-1 Tat protein on cell cycle during cervical carcino-genesis. Cancer Biology and Therapy. 2006;5(6):684-90. DOI: 10.4161/cbt.5.6.2907
45. Nakagawa M, Stites DP, Palefsky JM, et al. CD4-positive and CD8-positive cytotoxic T lymphocytes contribute to human papillomavirus type 16 E6 and E7 responses. Clinical and Vaccine Immunology. 1999;6(4):494-8. DOI: 10.1128/CDLI.6.4.494-498.1999
46. Welters MJ, Kenter GG, Piersma SJ, et al. Induction of tumor-specific CD4+ and CD8+ T-cell immunity in cervical cancer patients by a human papillomavirus type 16 E6 and E7 long peptides vaccine. Clinical Cancer Research. 2008;14(1):178-87. DOI: 10.1158/1078-0432. CCR-07-1880
47. Maskey N, Thapa N, Maharjan M, et al. Infiltrating CD4 and CD8 lymphocytes in HPV infected uterine cervical milieu. Cancer Management and Research. 2019;11:7647-55. DOI: 10.2147/CMAR.S217264
48. Yaghoobi M, Le Gouvello S, Aloulou N, et al. FoxP3 overexpression and CD1a+ and CD3+ depletion in anal tissue as possible mechanisms for increased risk of human papillomavirus-related anal carcinoma in HIV infection. Colorectal Disease. 2011;13(7):768-73. DOI: 10.1111/j.1463-1318.2010.02283.x
49. Meier A, Bagchi A, Sidhu HK, et al. Upregulation of PD-L1 on monocytes and dendritic cells by HIV-1 derived TLR ligands. AIDS. 2008;22(5):655-8. DOI: 10.1097/QAD. 0b013e3282f4de23
50. Sobhani I, Walker F, Aparicio T, et al. Effect of anal epidermoid cancer-related viruses on the dendritic (Langerhans) cells of the human anal mucosa. Clinical Cancer Research. 2002;8(9):2862-9. PMID: 12231528.
51. Allouch S, Malki A, Allouch A, et al. High-risk HPV oncoproteins and PD-1/PD-L1 interplay in human cervical cancer: recent evidence and future directions. Frontiers in Oncology. 2020;10:914. DOI: 10.3389/fonc.2020.00914
52. Keir ME, Butte MJ, Freeman GJ, et al. PD-1 and its ligands in tolerance and immunity. Annual Review of Immunology. 2008;26:677-704. DOI: 10.1146/annurev.immunol.26.021607.090331
53. Matloubian M, Concepcion RJ, Ahmed R. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. Journal of Virology. 1994;68(12):8056-63. DOI: 10.1128/JVI.68.12.8056-8063.1994
54. Deeks SG, Tracy R, Douek DC. Systemic effects of inflammation on health during chronic HIV infection. Immunity. 2013;39(4):633-45. DOI: 10.1016/j.immuni.2013.10.001
55. Gulzar N, Copeland KF. CD8+ T-cells: function and response to HIV infection. Current HIV Research. 2004;2(1):23-37. DOI: 10.2174/1570162043485077
56. Day CL, Kaufmann DE, Kiepiela P, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature. 2006;443(7109):350-4. DOI: 10.1038/nature05115
57. Cockerham LR, Jain V, Sinclair E, et al. Programmed death-1 expression on CD4+ and CD8+ T cells in treated and untreated HIV disease. AIDS. 2014;28(12):1749-58. DOI: 10.1097/QAD.0000000000000314
58. Porichis F, Kaufmann DE. Role of PD-1 in HIV pathogenesis and as target for therapy. Current HIV/AIDS Reports. 2012;9(1):81-90. DOI: 10.1007/s11904-011-0106-4
59. Grabmeier-Pfistershammer K, Steinberger P, Rieger A, et al. Identification of PD-1 as a unique marker for failing immune reconstitution in HIV-1-infected patients on treatment. Journal of Acquired Immune Deficiency Syndromes. 2011;56(2):118-24. DOI: 10.1097/QAI.0b013e3181fbab9f
60. Papasavvas E, Surrey LF, Glencross DK, et al. High-risk oncogenic HPV genotype infection associates with increased immune activation and T cell exhaustion in ART-suppressed HIV-1-infected women. Oncoimmunology. 2016;5(5):е1128612. DOI: 10.1080/2162402X.2015.1128612