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Commentary

Moving forward with human papillomavirus immunotherapies

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Pages 2875-2880 | Received 25 May 2016, Accepted 05 Jun 2016, Published online: 26 Jul 2016

References

  • Zur Hausen H. Papillomaviruses in the causation of human cancers - a brief historical account. Virology 2009; 384(2):260-5; PMID:19135222; http://dx.doi.org/10.1016/j.virol.2008.11.046
  • Bosch FX, Broker TR, Forman D, Moscicki AB, GillisonML, Doorbar J, Stern PL, Stanley M, Arbyn M, Poljak M, et al. Comprehensive control of human papillomavirus infections and related diseases. Vaccine 2013; 31(Suppl 7):H1-31; http://dx.doi.org/10.1016/j.vaccine.2013.10.003
  • Stanley MA. Epithelial cell responses to infection with human papillomavirus. Clin Microbiol Rev 2012; 25(2):215-22; PMID:22491770; http://dx.doi.org/10.1128/CMR.05028-11
  • Skeate JG, Woodham AW, Einstein MH, Da Silva DM, Kast WM. Current therapeutic vaccination and immunotherapy strategies for HPV-related diseases. Hum Vaccin Immunother 2016; 12(6):1418-29: 1–12; PMID:26835746; http://dx.doi.org/10.1080/21645515.2015.1136039
  • Tran NP, Hung CF, Roden R, Wu TC. Control of HPV infection and related cancer through vaccination. Recent Results Cancer Res 2014; 193:149-71; PMID:24008298; http://dx.doi.org/10.1007/978-3-642-38965-8_9
  • Bagarazzi ML, Yan J, Morrow MP, Shen X, Parker RL, Lee JC, Giffear M, Pankhong P, Khan AS, Broderick KE, et al. Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses. Sci Transl Med 2012; 4(155):155ra38; http://dx.doi.org/10.1126/scitranslmed.3004414
  • Trimble CL, Morrow MP, Kraynyak KA, Shen X, DallasM, Yan J, Edwards L, Parker RL, Denny L, Giffear M, et al. Safety, efficacy, and immunogenicity of VGX-3100, a therapeutic synthetic DNA vaccine targeting human papillomavirus 16 and 18 E6 and E7 proteins for cervical intraepithelial neoplasia 2/3: a randomised, double-blind, placebo-controlled phase 2b trial. Lancet 2015; 86(10008):2078-88; http://dx.doi.org/10.1016/S0140-6736(15)00239-1
  • Kim TJ, Jin HT, Hur SY, Yang HG, Seo YB, Hong SR, Lee CW, Kim S, Woo JW, Park KS, et al. Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients. Nat Commun 2014; 5:5317; PMID:25354725; http://dx.doi.org/10.1038/ncomms6317
  • Maldonado L, Teague JE, Morrow MP, Jotova I, Wu TC, Wang C, Desmarais C, Boyer JD, Tycko B, Robins HS, et al. Intramuscular therapeutic vaccination targeting HPV16 induces T cell responses that localize in mucosal lesions. Sci Transl Med 2014; 6(221):221ra13; PMID:24477000; http://dx.doi.org/10.1126/scitranslmed.3007323
  • Baldwin PJ, van der Burg SH, Boswell CM, Offringa R, Hickling JK, Dobson J, Roberts JS, Latimer JA, Moseley RP, Coleman N, et al. Vaccinia-expressed human papillomavirus 16 and 18 e6 and e7 as a therapeutic vaccination for vulval and vaginal intraepithelial neoplasia. Clin Cancer Res 2003; 9(14):5205-13; PMID:14614000
  • Borysiewicz LK, Fiander A, Nimako M, Man S, Wilkinson GW, Westmoreland D, Evans AS, Adams M, Stacey SN, Boursnell ME, et al. A recombinant vaccinia virus encoding human papillomavirus types 16 and 18, E6 and E7 proteins as immunotherapy for cervical cancer. Lancet 1996; 347(9014):1523-7; PMID:8684105; http://dx.doi.org/10.1016/S0140-6736(96)90674-1
  • Brun JL, Dalstein V, Leveque J, Mathevet P, Raulic P, Baldauf JJ, Scholl S, Huynh B, Douvier S, Riethmuller D, et al. Regression of high-grade cervical intraepithelial neoplasia with TG4001 targeted immunotherapy. Am J Obstet Gynecol 2011; 204(2):169 e1-8; PMID:21284968; http://dx.doi.org/10.1016/j.ajog.2010.09.020
  • Kawana K, Adachi K, Kojima S, Taguchi A, TomioK, Yamashita A, Nishida H, Nagasaka K, Arimoto T, Yokoyama T, et al. Oral vaccination against HPV E7 for treatment of cervical intraepithelial neoplasia grade 3 (CIN3) elicits E7-specific mucosal immunity in the cervix of CIN3 patients. Vaccine 2014; 32(47):6233-9; PMID:25258102; http://dx.doi.org/10.1016/j.vaccine.2014.09.020
  • Frazer IH, Quinn M, Nicklin JL, Tan J, Perrin LC, Ng P, O'Connor VM, White O, Wendt N, Martin J, et al. Phase 1 study of HPV16-specific immunotherapy with E6E7 fusion protein and ISCOMATRIX adjuvant in women with cervical intraepithelial neoplasia. Vaccine 2004; 23(2):172-81; PMID:15531034; http://dx.doi.org/10.1016/j.vaccine.2004.05.013
  • Davidson EJ, Faulkner RL, Sehr P, Pawlita M, Smyth LJ, Burt DJ, Tomlinson AE, Hickling J, Kitchener HC, Stern PL. Effect of TA-CIN (HPV 16 L2E6E7) booster immunisation in vulval intraepithelial neoplasia patients previously vaccinated with TA-HPV (vaccinia virus encoding HPV 16/18 E6E7). Vaccine 2004; 22(21–22):2722-9; PMID:15246603; http://dx.doi.org/10.1016/j.vaccine.2004.01.049
  • de Jong A, O'Neill T, Khan AY, Kwappenberg KM, Chisholm SE, Whittle NR, Dobson JA, Jack LC, St Clair Roberts JA, Offringa R, et al. Enhancement of human papillomavirus (HPV) type 16 E6 and E7-specific T-cell immunity in healthy volunteers through vaccination with TA-CIN, an HPV16 L2E7E6 fusion protein vaccine. Vaccine 2002; 20(29–30):3456-64.;PMID:12297390; http://dx.doi.org/10.1016/S0264-410X(02)00350-X
  • de Vos van Steenwijk PJ, Ramwadhdoebe TH, Lowik MJ, van der Minne CE, Berends-van der Meer DM, Fathers LM, Valentijn AR, Oostendorp J, Fleuren GJ, Hellebrekers BW, et al. A placebo-controlled randomized HPV16 synthetic long-peptide vaccination study in women with high-grade cervical squamous intraepithelial lesions. Cancer Immunol Immunother 2012; 61(9):1485-92.;PMID:22684521; http://dx.doi.org/10.1007/s00262-012-1292-7
  • Kenter GG, Welters MJ, Valentijn AR, Lowik MJ, Berends-van der Meer DM, Vloon AP, Essahsah F, Fathers LM, Offringa R, et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Eng J Med 2009; 361(19):1838-47; http://dx.doi.org/10.1056/NEJMoa0810097
  • Coleman HN, Greenfield WW, Stratton SL, Vaughn R, Kieber A, Moerman-Herzog AM, Spencer HJ, Hitt WC, Quick CM, Hutchins LF, et al. Human papillomavirus type 16 viral load is decreased following a therapeutic vaccination. Cancer Immunol Immunother 2016; 65(5):563-73; PMID:26980480; http://dx.doi.org/10.1007/s00262-016-1821-x
  • Rosales R, Lopez-Contreras M, Rosales C, Magallanes-Molina JR, Gonzalez-Vergara R, Arroyo-Cazarez JM, Ricardez-Arenas A, Del Follo-Valencia A, Padilla-Arriaga S, Guerrero MV, et al. Regression of human papillomavirus intraepithelial lesions is induced by MVA E2 therapeutic vaccine. Hum Gene Ther 2014; 25(12):1035-49; PMID:25275724; http://dx.doi.org/10.1089/hum.2014.024
  • Garcia-Hernandez E, Gonzalez-Sanchez JL, Andrade-Manzano A, Contreras ML, Padilla S, Guzman CC, Jiménez R, Reyes L, Morosoli G, Verde ML, et al. Regression of papilloma high-grade lesions (CIN 2 and CIN 3) is stimulated by therapeutic vaccination with MVA E2 recombinant vaccine. Cancer Gene Ther 2006; 13(6):592-7; PMID:16456551; http://dx.doi.org/10.1038/sj.cgt.7700937
  • Stevanovic S, Draper LM, Langhan MM, Campbell TE, Kwong ML, Wunderlich JR, Dudley ME, Yang JC, Sherry RM, Kammula US, et al. Complete regression of metastatic cervical cancer after treatment with human papillomavirus-targeted tumor-infiltrating T cells. J Clin Oncol 2015; 33(14):1543-50; PMID:25823737; http://dx.doi.org/10.1200/JCO.2014.58.9093
  • Beutner KR, Spruance SL, Hougham AJ, Fox TL, OwensML, Douglas JM, Jr. Treatment of genital warts with an immune-response modifier (imiquimod). J Am Acad Dermatol 1998; 38(2 Pt 1):230-9.;PMID:9486679; http://dx.doi.org/10.1016/S0190-9622(98)70243-9
  • Schulze HJ, Cribier B, Requena L, Reifenberger J, Ferrandiz C, Garcia Diez A, Tebbs V, McRae S. Imiquimod 5% cream for the treatment of superficial basal cell carcinoma: results from a randomized vehicle-controlled phase III study in Europe. Br J Dermatol 2005; 152(5):939-47; PMID:15888150; http://dx.doi.org/10.1111/j.1365-2133.2005.06486.x
  • Pachman DR, Barton DL, Clayton AC, McGovern RM, Jefferies JA, Novotny PJ, Sloan JA, Loprinzi CL, Gostout BS. Randomized clinical trial of imiquimod: an adjunct to treating cervical dysplasia. Am J Obstet Gynecol 2012; 206(1):42 e1-7; PMID:21907959; http://dx.doi.org/10.1016/j.ajog.2011.06.105
  • Lin CT, Qiu JT, Wang CJ, Chang SD, Tang YH, Wu PJ, Jung SM, Huang CC, Chou HH, Jao MS, et al. Topical imiquimod treatment for human papillomavirus infection in patients with and without cervical/vaginal intraepithelial neoplasia. Taiwan J Obstet Gynecol 2012; 51(4):533-8; PMID:23276555; http://dx.doi.org/10.1016/j.tjog.2012.09.006
  • Grimm C, Polterauer S, Natter C, Rahhal J, Hefler L, Tempfer CB, Heinze G, Stary G, Reinthaller A, Speiser P. Treatment of cervical intraepithelial neoplasia with topical imiquimod: a randomized controlled trial. Obstet Gynecol 2012; 120(1):152-9; PMID:22914404; http://dx.doi.org/10.1097/AOG.0b013e31825bc6e8
  • Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8(4):247-58; PMID:18323851; http://dx.doi.org/10.1038/nri2274
  • Disis ML, Watt WC, Cecil DL. Th1 epitope selection for clinically effective cancer vaccines. Oncoimmunol 2014; 3(9):e954971; http://dx.doi.org/10.4161/21624011.2014.954971
  • Park CO, Kupper TS. The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat Med 2015; 21(7):688-97; PMID:26121195; http://dx.doi.org/10.1038/nm.3883
  • Sikorski M, Bobek M, Zrubek H, Marcinkiewicz J. Dynamics of selected MHC class I and II molecule expression in the course of HPV positive CIN treatment with the use of human recombinant IFN-gamma. Acta Obstet Gynecol Scand 2004; 83(3):299-307; PMID:14995928
  • Niebler M, Qian X, Hofler D, Kogosov V, Kaewprag J, Kaufmann AM, Ly R, Böhmer G, Zawatzky R, Rösl F, et al. Post-translational control of IL-1beta via the human papillomavirus type 16 E6 oncoprotein: a novel mechanism of innate immune escape mediated by the E3-ubiquitin ligase E6-AP and p53. PLoS Pathog 2013; 9(8):e1003536; PMID:23935506; http://dx.doi.org/10.1371/journal.ppat.1003536
  • Mezache L, Paniccia B, Nyinawabera A, Nuovo GJ. Enhanced expression of PD L1 in cervical intraepithelial neoplasia and cervical cancers. Mod Pathol 2015; 28(12):1594-602; PMID:26403783; http://dx.doi.org/10.1038/modpathol.2015.108
  • Syrjanen S, Naud P, Sarian L, Derchain S, Roteli-Martins C, Longatto-Filho A, Tatti S, Branca M, Erzen M, Hammes LS, et al. Immunosuppressive cytokine Interleukin-10 (IL-10) is up-regulated in high-grade CIN but not associated with high-risk human papillomavirus (HPV) at baseline, outcomes of HR-HPV infections or incident CIN in the LAMS cohort. Virchows Arch 2009; 455(6):505-15.;PMID:19908064; http://dx.doi.org/10.1007/s00428-009-0850-7
  • Bais AG, Beckmann I, Lindemans J, Ewing PC, MeijerCJ, Snijders PJ, Helmerhorst TJ. A shift to a peripheral Th2-type cytokine pattern during the carcinogenesis of cervical cancer becomes manifest in CIN III lesions. J Clin Pathol 2005; 58(10):1096-100; PMID:16189158; http://dx.doi.org/10.1136/jcp.2004.025072
  • Kojima S, Kawana K, Tomio K, Yamashita A, Taguchi A, Miura S, Adachi K, Nagamatsu T, Nagasaka K, Matsumoto Y, et al. The prevalence of cervical regulatory T cells in HPV-related cervical intraepithelial neoplasia (CIN) correlates inversely with spontaneous regression of CIN. Am J Reprod Immunol 2013; 69(2):134-41; PMID:23057776; http://dx.doi.org/10.1111/aji.12030
  • Trimble CL, Clark RA, Thoburn C, Hanson NC, Tassello J, Frosina D, Kos F, Teague J, Jiang Y, Barat NC, et al. Human papillomavirus 16-associated cervical intraepithelial neoplasia in humans excludes CD8 T cells from dysplastic epithelium. J Immunol 2010; 185(11):7107-14; PMID:21037100; http://dx.doi.org/10.4049/jimmunol.1002756
  • Leong CM, Doorbar J, Nindl I, Yoon HS, Hibma MH. Loss of epidermal Langerhans cells occurs in human papillomavirus α, gamma, and mu but not β genus infections. J Invest Dermatol 2010; 130(2):472-80.;PMID:19759549; http://dx.doi.org/10.1038/jid.2009.266
  • Piyathilake CJ, Ollberding NJ, Kumar R, Macaluso M, Alvarez RD, Morrow CD. Cervical microbiota associated with higher grade cervical intraepithelial neoplasia in women infected with High-Risk Human Papillomaviruses. Cancer Prev Res (Phila) 2016; 9(5):357-66; PMID:26935422; http://dx.doi.org/10.1158/1940-6207.CAPR-15-0350
  • Lee JE, Lee S, Lee H, Song YM, Lee K, Han MJ, Sung J, Ko G. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PloS One 2013; 8(5):e63514.;PMID:23717441; http://dx.doi.org/10.1371/journal.pone.0063514
  • Soong RS, Song L, Trieu J, Knoff J, He L, Tsai YC, Huh W, Chang YN, Cheng WF, Roden RB, et al. Toll-like receptor agonist imiquimod facilitates antigen-specific CD8+ T-cell accumulation in the genital tract leading to tumor control through IFNgamma. Clin Cancer Res 2014; 20(21):5456-67; PMID:24893628; http://dx.doi.org/10.1158/1078-0432.CCR-14-0344
  • Domingos-Pereira S, Decrausaz L, Derre L, Bobst M, Romero P, Schiller JT, Jichlinski P, Nardelli-Haefliger D. Intravaginal TLR agonists increase local vaccine-specific CD8 T cells and human papillomavirus-associated genital-tumor regression in mice. Mucosal Immunol 2013; 6(2):393-404; PMID:22968420; http://dx.doi.org/10.1038/mi.2012.83
  • Sharma P, Allison JP. The future of immune checkpoint therapy. Science 2015; 348(6230):56-61.;PMID:25838373; http://dx.doi.org/10.1126/science.aaa8172
  • Boutros C, Tarhini A, Routier E, Lambotte O, Ladurie FL, Carbonnel F, Izzeddine H, Marabelle A, Champiat S, Berdelou A, et al. Safety profiles of anti-CTLA-4 and anti-PD-1 antibodies alone and in combination. Nat Rev Clin Oncol 2016; PMID:27141885 [Epub ahead of print]
  • Li Z, Palaniyandi S, Zeng R, Tuo W, Roopenian DC, Zhu X. Transfer of IgG in the female genital tract by MHC class I-related neonatal Fc receptor (FcRn) confers protective immunity to vaginal infection. Proc Natl Acad Sci U S A 2011; 108(11):4388-93; PMID:21368166; http://dx.doi.org/10.1073/pnas.1012861108
  • Cuburu N, Wang K, Goodman KN, Pang YY, Thompson CD, Lowy DR, Cohen JI, Schiller JT. Topical herpes simplex virus 2 (HSV-2) vaccination with human papillomavirus vectors expressing gB/gD ectodomains induces genital-tissue-resident memory CD8+ T cells and reduces genital disease and viral shedding after HSV-2 challenge. J Virol 2015; 89(1):83-96; PMID:25320297; http://dx.doi.org/10.1128/JVI.02380-14
  • Cuburu N, Graham BS, Buck CB, Kines RC, Pang YY, Day PM, Lowy DR, Schiller JT. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J Clin Invest 2012; 122(12):4606-20; PMID:23143305; http://dx.doi.org/10.1172/JCI63287
  • Alvarez RD, Huh WK, Bae S, Lamb LS, Jr, Conner MG, Boyer J, Wang C, Hung CF, Sauter E, Paradis M, et al. A pilot study of pNGVL4a-CRT/E7(detox) for the treatment of patients with HPV16+ cervical intraepithelial neoplasia 2/3 (CIN2/3). Gynecol Oncol 2016; 140(2):245-52; PMID:26616223; http://dx.doi.org/10.1016/j.ygyno.2015.11.026
  • Ariotti S, Beltman JB, Chodaczek G, Hoekstra ME, van Beek AE, Gomez-Eerland R, Ritsma L, van Rheenen J, Marée AF, Zal T, et al. Tissue-resident memory CD8+ T cells continuously patrol skin epithelia to quickly recognize local antigen. Proc Natl Acad Sci U S A 2012; 109(48):19739-44; PMID:23150545; http://dx.doi.org/10.1073/pnas.1208927109
  • Feltkamp MC, Smits HL, Vierboom MP, Minnaar RP, de Jongh BM, Drijfhout JW, ter Schegget J, Melief CJ, Kast WM. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol 1993; 23(9):2242-9; PMID:7690326; http://dx.doi.org/10.1002/eji.1830230929
  • Lin KY, Guarnieri FG, Staveley-O'Carroll KF, Levitsky HI, August JT, Pardoll DM, Wu TC. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 1996; 56(1):21-6; PMID:8548765
  • Schaper ID, Marcuzzi GP, Weissenborn SJ, Kasper HU, Dries V, Smyth N, Fuchs P, Pfister H. Development of skin tumors in mice transgenic for early genes of human papillomavirus type 8. Cancer Res 2005; 65(4):1394-400; PMID:15735026; http://dx.doi.org/10.1158/0008-5472.CAN-04-3263
  • Lambert PF, Pan H, Pitot HC, Liem A, Jackson M, Griep AE. Epidermal cancer associated with expression of human papillomavirus type 16 E6 and E7 oncogenes in the skin of transgenic mice. Proc Natl Acad Sci U S A 1993; 90(12):5583-7; PMID:8390671; http://dx.doi.org/10.1073/pnas.90.12.5583
  • Zhong R, Pytynia M, Pelizzari C, Spiotto M. Bioluminescent imaging of HPV-positive oral tumor growth and its response to image-guided radiotherapy. Cancer Res 2014; 74(7):2073-81; PMID:24525739; http://dx.doi.org/10.1158/0008-5472.CAN-13-2993
  • Stern PL, van der Burg SH, Hampson IN, Broker TR, Fiander A, Lacey CJ, Kitchener HC, Einstein MH. Therapy of human papillomavirus-related disease. Vaccine 2012; 30(Suppl 5):F71-82.;PMID:23199967; http://dx.doi.org/10.1016/j.vaccine.2012.05.091
  • Richel O, de Vries HJ, van Noesel CJ, Dijkgraaf MG, Prins JM. Comparison of imiquimod, topical fluorouracil, and electrocautery for the treatment of anal intraepithelial neoplasia in HIV-positive men who have sex with men: an open-label, randomised controlled trial. Lancet Oncol 2013; 14(4):346-53; PMID:23499546; http://dx.doi.org/10.1016/S1470-2045(13)70067-6
  • Moscicki AB, Schiffman M, Kjaer S, Villa LL. Chapter 5: Updating the natural history of HPV and anogenital cancer. Vaccine 2006; 24(Suppl 3):S3/42-51; PMID:16950017
  • Dillon S, Sasagawa T, Crawford A, Prestidge J, Inder MK, Jerram J, Mercer AA, Hibma M. Resolution of cervical dysplasia is associated with T-cell proliferative responses to human papillomavirus type 16 E2. J General Virol 2007; 88(Pt 3):803-13; http://dx.doi.org/10.1099/vir.0.82678-0

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