Local HPV Recombinant Vaccinia Boost Following Priming with an HPV DNA Vaccine Enhances Local HPV-Specific CD8+ T-cell-Mediated Tumor Control in the Genital Tract

Clinical Cancer Research

Volumn 22, Issue 3, 2016, Pages 657-669

  Sun, Yun Yan ^a,b   Peng, Shiwen ^b   Han, Liping ^b,c   Qiu, Jin ^b,d   Song, Liwen ^b,d   Tsai, Yachea ^b   Yang, Benjamin ^b   Roden, Richard B S ^b   Trimble, Cornelia L ^b   Hung, Chien Fu ^b   Wu, T C ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c THE FIRST AFFILIATED HOSPITAL OF ZHENGZHOU UNIVERSITY   (China)

^d TENTH PEOPLE S HOSPITAL OF TONGJI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4BETA7 INTEGRIN; CHEMOKINE RECEPTOR CCR9; DNA VACCINE; INTEGRIN; UNCLASSIFIED DRUG; VACCINIA VACCINE; BIOLOGICAL MARKER; HUMAN PAPILLOMAVIRUS VACCINE, TA; PROTEIN E7; WART VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CONTROL; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL HOMING; CELL MIGRATION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; UTERINE CERVIX CANCER; ANIMAL; COMPLICATION; DENDRITIC CELL; DISEASE MODEL; GENETICS; GENITAL NEOPLASMS, FEMALE; HUMAN; IMMUNIZATION; IMMUNOLOGY; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; METABOLISM; MORTALITY; NEUTROPHIL CHEMOTAXIS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PHENOTYPE; SECONDARY IMMUNIZATION;

ANIMALS; BIOMARKERS; CD8-POSITIVE T-LYMPHOCYTES; CHEMOTAXIS, LEUKOCYTE; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; GENITAL NEOPLASMS, FEMALE; HUMANS; IMMUNIZATION; IMMUNIZATION, SECONDARY; IMMUNOPHENOTYPING; MICE; MICE, KNOCKOUT; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; PHENOTYPE; VACCINES, DNA;

EID: 84959036571     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-0234     Document Type: Article

References (47)

1. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
3. Trimble CL, Piantadosi S, Gravitt P, Ronnett B, Pizer E, Elko A, et al. Spontaneous regression of high-grade cervical dysplasia: Effects of human papillomavirus type and HLA phenotype. Clin Cancer Res 2005;11: 4717-23.
4. Yugawa T, Kiyono T. Molecular mechanisms of cervical carcinogenesis by high-risk human papillomaviruses: Novel functions of E6 and E7 oncoproteins. Rev Med Virol 2009;19:97-113.
5. Maldonado L, Teague JE, Morrow MP, Jotova I, Wu TC, Wang C, et al. Intramuscular therapeutic vaccination targeting HPV16 induces T cell responses that localize inmucosal lesions. Sci Transl Med 2014;6:221ra13.
6. Huh WK, Alvarez RD, Maldonado L, Wang C, Wu TC, Trimble C. Phase I evaluation of therapeutic HPV16 E7 vaccination before resection of HPV16+ CIN2/3. Gynecol Oncol 2014;133:28-9.
7. Trimble C, Lin CT, Hung CF, Pai S, Juang J, He L, et al. Comparison of the CD8+ T cell responses and antitumor effects generated by DNA vaccine administered through gene gun, biojector, and syringe. Vaccine 2003;21: 4036-42.
8. TrimbleCL, Peng S, Kos F, Gravitt P, Viscidi R, Sugar E, et al. A phase I trial of a human papillomavirus DNA vaccine for HPV16+ cervical intraepithelial neoplasia 2/3. Clin Cancer Res 2009;15:361-7.
9. Borysiewicz LK, Fiander A, Nimako M, Man S, Wilkinson GW, Westmoreland D, et al. A recombinant vaccinia virus encoding human papillomavirus types 16 and 18, E6 and E7 proteins as immunotherapy for cervical cancer. Lancet 1996;347:1523-7.
10. Kaufmann AM, Stern PL, Rankin EM, Sommer H, Nuessler V, Schneider A, et al. Safety and immunogenicity of TA-HPV, a recombinant vaccinia virus expressing modified human papillomavirus (HPV)-16 and HPV-18 E6 and E7 genes, in women with progressive cervical cancer. Clin Cancer Res 2002; 8:3676-85.
11. Davidson EJ, Boswell CM, Sehr P, Pawlita M, Tomlinson AE, McVey RJ, et al. Immunological and clinical responses in women with vulval intraepithelial neoplasia vaccinated with a vaccinia virus encoding human papillomavirus 16/18 oncoproteins. Cancer Res 2003;63:6032-41.
12. Smyth LJ, Van Poelgeest MI,Davidson EJ, Kwappenberg KM, BurtD, Sehr P, et al. Immunological responses in women with human papillomavirus type 16 (HPV-16)-associated anogenital intraepithelial neoplasia induced by heterologous prime-boost HPV-16 oncogene vaccination. Clin Cancer Res 2004;10:2954-61.
13. Fiander AN, Tristram AJ, Davidson EJ, Tomlinson AE, Man S, Baldwin PJ, et al. Prime-boost vaccination strategy in women with high-grade, noncervical anogenital intraepithelial neoplasia: Clinical results from a multicenter phase II trial. Int J Gynecol Cancer 2006;16:1075-81.
14. Chen CH, Wang TL, Hung CF, Pardoll DM, Wu TC. Boosting with recombinant vaccinia increases HPV-16 E7-specific T cell precursor frequencies of HPV-16 E7-expressing DNA vaccines. Vaccine 2000;18: 2015-22.
15. Hanke T, Neumann VC, Blanchard TJ, Sweeney P, Hill AV, Smith GL, et al. Effective induction of HIV-specific CTL by multi-epitope using gene gun in a combined vaccination regime. Vaccine 1999;17:589-96.
16. Schneider J, Gilbert SC, Blanchard TJ, Hanke T, Robson KJ, Hannan CM, et al. Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nat Med 1998;4:397-402.
17. Sedegah M, Jones TR, Kaur M, Hedstrom R, Hobart P, Tine JA, et al. Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. Proc Natl Acad Sci U S A 1998;95: 7648-53.
18. Hanke T, Blanchard TJ, Schneider J, Hannan CM, Becker M, Gilbert SC, et al. Enhancement of MHC class I-restricted peptide-specific T cell induction by a DNA prime/MVA boost vaccination regime. Vaccine 1998;16:439-45.
19. Kent SJ, Zhao A, Best SJ, Chandler JD, BoyleDB, RamshawIA. Enhanced T-cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant fowlpox virus. J Virol 1998; 72:10180-8.
20. Center SKCC. Vaccine Therapy With or Without Imiquimod in Treating Patients With Grade 3 Cervical Intraepithelial Neoplasia. In: Clinical-Trials.gov [Internet]. Bethesda, MD: National Library of Medicine (US); 2000 [cited 2013 Apr 18]. Available from: Http://clinicaltrials.gov/show/NCT00788164.
21. Woodland DL, Kohlmeier JE. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat Rev Immunol 2009;9:153-61.
22. Cauley LS, Lefrancois L. Guarding the perimeter: Protection of the mucosa by tissue-resident memory T cells. Mucosal Immunol 2013;6:14-23.
23. Nardelli-Haefliger D, Dudda JC, Romero P. Vaccination route matters for mucosal tumors. Sci Transl Med 2013;5:172fs4.
24. Sandoval F, TermeM, Nizard M, Badoual C, BureauMF, Freyburger L, et al. Mucosal imprinting of vaccine-induced CD8(+) T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med 2013;5:172ra20.
25. Lin KY, Guarnieri FG, Staveley-O'Carroll KF, Levitsky HI, August JT, Pardoll DM, et al. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 1996;56:21-6.
26. Huang B, Mao CP, Peng S, He L, Hung CF, Wu TC. Intradermal administration of DNA vaccines combining a strategy to bypass antigen processingwith a strategy to prolong dendritic cell survival enhancesDNAvaccine potency. Vaccine 2007;25:7824-31.
27. Soong RS, Song L, Trieu J, Knoff J, He L, Tsai YC, 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;20:5456-67.
28. Trimble CL, Clark RA, Thoburn C, Hanson NC, Tassello J, Frosina D, et al. Human papillomavirus 16-associated cervical intraepithelial neoplasia in humans excludes CD8 T cells from dysplastic epithelium. J Immunol 2010;185:7107-14.
29. Gorfu G, Rivera-Nieves J, Ley K. Role of beta7 integrins in intestinal lymphocyte homing and retention. Curr Mol Med 2009;9:836-50.
30. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004;21: 527-38.
31. Mima K, Hayashi H, Imai K, Kuroki H, Nakagawa S, Okabe H, et al. High CD44s expression is associated with the EMT expression profile and intrahepatic dissemination of hepatocellular carcinoma after local ablation therapy. J Hepatobiliary Pancreat Sci 2013;20:429-34.
32. Svensson M, Johansson-Lindbom B, Zapata F, Jaensson E, Austenaa LM, Blomhoff R, et al. Retinoic acid receptor signaling levels and antigen dose regulate gut homing receptor expression on CD8+ T cells. Mucosal Immunol 2008;1:38-48.
33. Zeng R, Oderup C, Yuan R, LeeM, Habtezion A, Hadeiba H, et al. Retinoic acid regulates the development of a gut-homing precursor for intestinal dendritic cells. Mucosal Immunol 2013;6:847-56.
34. Ruane D, Brane L, Reis BS, Cheong C, Poles J, Do Y, et al. Lung dendritic cells inducemigration of protective T cells to the gastrointestinal tract. J Exp Med 2013;210:1871-88.
35. Corona Gutierrez CM, Tinoco A, Lopez Contreras M, Navarro T, Calzado P, Vargas L, et al. Clinical protocol. A phase II study: Efficacy of the gene therapy of the MVA E2 recombinant virus in the treatment of precancerous lesions (NIC I and NIC II) associated with infection of oncogenic human papillomavirus. Hum Gene Ther 2002;13:1127-40.
36. Kanazawa T, Takashima Y,Hirayama S,OkadaH. Effects ofmenstrual cycle on gene transfection through mouse vagina for DNA vaccine. Int J Pharm 2008;360:164-70.
37. Skon CN, Lee JY, Anderson KG, Masopust D, Hogquist KA, Jameson SC. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat Immunol 2013;14:1285-93.
38. Zajac AJ, Harrington LE. Tissue-resident T cells lose their S1P1 exit visas. Cell Mol Immunol 2014;11:221-3.
39. Hadley GA, Higgins JM. Integrin alphaEbeta7: Molecular features and functional significance in the immunesystem. Adv ExpMed Biol 2014;819: 97-110.
40. Hammerschmidt SI, Friedrichsen M, Boelter J, Lyszkiewicz M, Kremmer E, Pabst O, et al. Retinoic acid induces homing of protective T and B cells to the gut after subcutaneous immunization in mice. J Clin Invest 2011; 121:3051-61.
41. Molenaar R, Greuter M, Van derMarel AP, Roozendaal R,Martin SF, Edele F, et al. Lymph node stromal cells support dendritic cell-induced gut-homing of T cells. J Immunol 2009;183:6395-402.
42. Bhat PV. Retinal dehydrogenase gene expression in stomach and small intestine of rats during postnatal development and in vitamin A deficiency. FEBS Lett 1998;426:260-2.
43. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 2007; 8:1086-94.
44. Cuburu N, Graham BS, Buck CB, Kines RC, Pang YY, Day PM, et al. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J Clin Invest 2012;122: 4606-20.
45. Jiang X, Clark RA, Liu L, Wagers AJ, Fuhlbrigge RC, Kupper TS. Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity. Nature 2012;483:227-31.
46. Belyakov IM, Ahlers JD, Brandwein BY, Earl P, Kelsall BL, Moss B, et al. The importance of local mucosal HIV-specific CD8(+) cytotoxic T lymphocytes for resistance to mucosal viral transmission in mice and enhancement of resistance by local administration of IL-12. J Clin Invest 1998;102: 2072-81.
47. Ledgerwood LG, Lal G, Zhang N, Garin A, Esses SJ, Ginhoux F, et al. The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat Immunol 2008;9:42-53.