Langerhans cells from women with cervical precancerous lesions become functionally responsive against human papillomavirus after activation with stabilized Poly-I:C

Clinical Immunology

Volumn 161, Issue 2, 2015, Pages 197-208

  Da Silva, Diane M ^a,b   Woodham, Andrew W ^b   Skeate, Joseph G ^a   Rijkee, Laurie K ^c   Taylor, Julia R ^b   Brand, Heike E ^b   Muderspach, Laila I ^a,b   Roman, Lynda D ^a,b   Yessaian, Annie A ^a,b   Pham, Huyen Q ^a,b   Matsuo, Koji ^a,b   Lin, Yvonne G ^a,b,f   McKee, Greg M ^d,g   Salazar, Andres M ^e   Martin Kast, W ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d Akela Pharma   (United States)

^e Oncovir Inc   (United States)

^f GENENTECH INC   (United States)

^g NONE   (United States)

Author keywords

HPV16; Human papillomavirus; Immune evasion; Langerhans cells

Indexed keywords

CHEMOKINE; CYTOKINE; POLYINOSINIC POLYCYTIDYLIC ACID; VIRUS DNA;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; IMMUNE EVASION; IMMUNE RESPONSE; LANGERHANS CELL; PRECANCER; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; UTERINE CERVIX CARCINOMA IN SITU; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MIDDLE AGED; PAPILLOMAVIRUS INFECTION; UTERINE CERVIX TUMOR; VIROLOGY;

ADULT; CD8-POSITIVE T-LYMPHOCYTES; CERVICAL INTRAEPITHELIAL NEOPLASIA; DNA, VIRAL; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; LANGERHANS CELLS; LYMPHOCYTE ACTIVATION; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; POLY I-C; UTERINE CERVICAL NEOPLASMS;

EID: 84942574633     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2015.09.003     Document Type: Article

References (77)

1. Walboomers J.M., Jacobs M.V., Manos M.M., Bosch F.X., Kummer J.A., Shah K.V., Snijders P.J., Peto J., Meijer C.J., Munoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 1999, 189:12-19.
2. Giuliano A.R., Harris R., Sedjo R.L., Baldwin S., Roe D., Papenfuss M.R., Abrahamsen M., Inserra P., Olvera S., Hatch K. Incidence, prevalence, and clearance of type-specific human papillomavirus infections: The Young Women's Health Study. J. Infect. Dis. 2002, 186:462-469.
3. Rodriguez A.C., Schiffman M., Herrero R., Wacholder S., Hildesheim A., Castle P.E., Solomon D., Burk R. Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections. J. Natl. Cancer Inst. 2008, 100:513-517.
4. Walker J.L., Wang S.S., Schiffman M., Solomon D. Predicting absolute risk of CIN3 during post-colposcopic follow-up: results from the ASCUS-LSIL Triage Study (ALTS). Am. J. Obstet. Gynecol. 2006, 195:341-348.
5. Massad L.S., Einstein M.H., Huh W.K., Katki H.A., Kinney W.K., Schiffman M., Solomon D., Wentzensen N., Lawson H.W. 2012 updated consensus guidelines for the management of abnormal cervical cancer screening tests and cancer precursors. Obstet. Gynecol. 2013, 121:829-846.
6. Fausch S.C., Da Silva D.M., Rudolf M.P., Kast W.M. Human papillomavirus virus-like particles do not activate Langerhans cells: a possible immune escape mechanism used by human papillomaviruses. J. Immunol. 2002, 169:3242-3249.
7. Fausch S.C., Fahey L.M., Da Silva D.M., Kast W.M. Human papillomavirus can escape immune recognition through Langerhans cell phosphoinositide 3-kinase activation. J. Immunol. 2005, 174:7172-7178.
8. Da Silva D.M., Movius C.A., Raff A.B., Brand H.E., Skeate J.G., Wong M.K., Kast W.M. Suppression of Langerhans cell activation is conserved amongst human papillomavirus alpha and beta genotypes, but not a mu genotype. Virology 2014, 452-453:279-286.
9. Artyomov M.N., Munk A., Gorvel L., Korenfeld D., Cella M., Tung T., Klechevsky E. Modular expression analysis reveals functional conservation between human Langerhans cells and mouse cross-priming dendritic cells. J. Exp. Med 2015.
10. Banchereau J., Thompson-Snipes L., Zurawski S., Blanck J.P., Cao Y., Clayton S., Gorvel J.P., Zurawski G., Klechevsky E. The differential production of cytokines by human Langerhans cells and dermal CD14(+) DCs controls CTL priming. Blood 2012, 119:5742-5749.
11. Klechevsky E., Morita R., Liu M., Cao Y., Coquery S., Thompson-Snipes L., Briere F., Chaussabel D., Zurawski G., Palucka A.K., Reiter Y., Banchereau J., Ueno H. Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity 2008, 29:497-510.
12. + hematopoietic progenitors stimulate greater cytolytic T lymphocyte activity in the absence of bioactive IL-12p70, by either single peptide presentation or cross-priming, than do dermal-interstitial or monocyte-derived dendritic cells. J. Immunol. 2004, 173:2780-2791.
13. Polak M.E., Newell L., Taraban V.Y., Pickard C., Healy E., Friedmann P.S., Al-Shamkhani A., Ardern-Jones M.R. CD70-CD27 interaction augments CD8+ T-cell activation by human epidermal Langerhans cells. J. Investig. Dermatol. 2012, 132:1636-1644.
14. Kaplan D.H. In vivo function of Langerhans cells and dermal dendritic cells. Trends Immunol. 2010, 31:446-451.
15. Chappert P., Schwartz R.H. Induction of T cell anergy: integration of environmental cues and infectious tolerance. Curr. Opin. Immunol. 2010, 22:552-559.
16. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
17. Randolph G.J., Ochando J., Partida-Sanchez S. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 2008, 26:293-316.
18. Malissen B., Tamoutounour S., Henri S. The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol. 2014, 14:417-428.
19. Fahey L.M., Raff A.B., Da Silva D.M., Kast W.M. Reversal of human papillomavirus-specific T cell immune suppression through TLR agonist treatment of Langerhans cells exposed to human papillomavirus type 16. J. Immunol. 2009, 182:2919-2928.
20. D.M. Da Silva, A.W. Woodham, L.K. Rijkee, J.G. Skeate, J.R. Taylor, M.E. Koopman, H.E. Brand, M.K. Wong, G.M. McKee, A.M. Salazar, W.M. Kast, Human papillomavirus-exposed Langerhans cells are activated by stabilized Poly-I:C, Papillomavirus Research, (2015) Epub ahead of print. doi:10.1016/j.pvr.2015.1005.1001.
21. Cheng Y.S., Xu F. Anticancer function of polyinosinic-polycytidylic acid. Cancer Biol. Ther. 2010, 10:1219-1223.
22. Flacher V., Bouschbacher M., Verronese E., Massacrier C., Sisirak V., Berthier-Vergnes O., de Saint-Vis B., Caux C., Dezutter-Dambuyant C., Lebecque S., Valladeau J. Human Langerhans cells express a specific TLR profile and differentially respond to viruses and Gram-positive bacteria. J. Immunol. 2006, 177:7959-7967.
23. Kawai T., Akira S. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 2008, 1143:1-20.
24. Matsumoto M., Seya T. TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv. Drug Deliv. Rev. 2008, 60:805-812.
25. + T cells producing IFN-gamma and IL-10. J. Investig. Dermatol. 2009, 129:1963-1971.
26. de Clercq E. Degradation of poly(inosinic acid)-poly(cytidylic acid) [(I)n-(C)n] by human plasma. Eur. J. Biochem. 1979, 93:165-172.
27. Levy H.B., Baer G., Baron S., Buckler C.E., Gibbs C.J., Iadarola M.J., London W.T., Rice J. A modified polyriboinosinic-polyribocytidylic acid complex that induces interferon in primates. J. Infect. Dis. 1975, 132:434-439.
28. Greenstone H.L., Nieland J.D., de Visser K.E., De Bruijn M.L., Kirnbauer R., Roden R.B., Lowy D.R., Kast W.M., Schiller J.T. Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:1800-1805.
29. Woodham A.W., Raff A.B., Da Silva D.M., Kast W.M. Molecular analysis of human papillomavirus virus-like particle activated Langerhans cells in vitro. Methods Mol. Biol. 2015, 1249:135-149.
30. Yan L., Woodham A.W., Da Silva D.M., Kast W.M. Functional analysis of HPV-like particle-activated Langerhans cells in vitro. Methods Mol. Biol. 2015, 1249:333-350.
31. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
32. Arikawa E., Sun Y., Wang J., Zhou Q., Ning B., Dial S.L., Guo L., Yang J. Cross-platform comparison of SYBR Green real-time PCR with TaqMan PCR, microarrays and other gene expression measurement technologies evaluated in the MicroArray Quality Control (MAQC) study. BMC Genomics 2008, 9:328.
33. Kast W.M., Brandt R.M., Sidney J., Drijfhout J.W., Kubo R.T., Grey H.M., Melief C.J., Sette A. Role of HLA-A motifs in identification of potential CTL epitopes in human papillomavirus type 16 E6 and E7 proteins. J. Immunol. 1994, 152:3904-3912.
34. De Vuyst H., Lillo F., Broutet N., Smith J.S. HIV, human papillomavirus, and cervical neoplasia and cancer in the era of highly active antiretroviral therapy. Eur. J. Cancer Prev. 2008, 17:545-554.
35. Smith J.S., Lindsay L., Hoots B., Keys J., Franceschi S., Winer R., Clifford G.M. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int. J. Cancer 2007, 121:621-632.
36. Greenstone H.L., Nieland J.D., de Visser K.E., De Bruijn M.L., Kirnbauer R., Roden R.B., Lowy D.R., Kast W.M., Schiller J.T. Chimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:1800-1805.
37. Salazar A.M., Erlich R.B., Mark A., Bhardwaj N., Herberman R.B. Therapeutic in situ autovaccination against solid cancers with intratumoral poly-ICLC: case report, hypothesis, and clinical trial. Cancer Immunol Res 2014, 2:720-724.
38. + T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J. Clin. Oncol. 2011, 29:330-336.
39. Prins R.M., Soto H., Konkankit V., Odesa S.K., Eskin A., Yong W.H., Nelson S.F., Liau L.M. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin. Cancer Res. 2011, 17:1603-1615.
40. Amit I., Garber M., Chevrier N., Leite A.P., Donner Y., Eisenhaure T., Guttman M., Grenier J.K., Li W., Zuk O., Schubert L.A., Birditt B., Shay T., Goren A., Zhang X., Smith Z., Deering R., McDonald R.C., Cabili M., Bernstein B.E., Rinn J.L., Meissner A., Root D.E., Hacohen N., Regev A. Unbiased reconstruction of a mammalian transcriptional network mediating pathogen responses. Science 2009, 326:257-263.
41. Caskey M., Lefebvre F., Filali-Mouhim A., Cameron M.J., Goulet J.P., Haddad E.K., Breton G., Trumpfheller C., Pollak S., Shimeliovich I., Duque-Alarcon A., Pan L., Nelkenbaum A., Salazar A.M., Schlesinger S.J., Steinman R.M., Sekaly R.P. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J. Exp. Med 2011, 208:2357-2366.
42. Abraham J., Stenger M. Cobas HPV test for first-line screening for cervical cancer. J Community Support Oncol 2014, 12:156-157.
43. Wright T.C., Stoler M.H., Behrens C.M., Sharma A., Zhang G., Wright T.L. Primary cervical cancer screening with human papillomavirus: end of study results from the ATHENA study using HPV as the first-line screening test. Gynecol. Oncol. 2015, 136:189-197.
44. Castle P.E., Stoler M.H., Wright T.C., Sharma A., Wright T.L., Behrens C.M. Performance of carcinogenic human papillomavirus (HPV) testing and HPV16 or HPV18 genotyping for cervical cancer screening of women aged 25years and older: a subanalysis of the ATHENA study. Lancet Oncol. 2011, 12:880-890.
45. Stoler M.H., Wright T.C., Sharma A., Apple R., Gutekunst K., Wright T.L. High-risk human papillomavirus testing in women with ASC-US cytology: results from the ATHENA HPV study. Am. J. Clin. Pathol. 2011, 135:468-475.
46. Stanley M.A. Epithelial cell responses to infection with human papillomavirus. Clin. Microbiol. Rev. 2012, 25:215-222.
47. Giannini S.L., Hubert P., Doyen J., Boniver J., Delvenne P. Influence of the mucosal epithelium microenvironment on Langerhans cells: implications for the development of squamous intraepithelial lesions of the cervix. Int. J. Cancer 2002, 97:654-659.
48. Mota F., Rayment N., Chong S., Singer A., Chain B. The antigen-presenting environment in normal and human papillomavirus (HPV)-related premalignant cervical epithelium. Clin. Exp. Immunol. 1999, 116:33-40.
49. Prata T.T., Bonin C.M., Ferreira A.M., Padovani C.T., Fernandes C.E., Machado A.P., Tozetti I.A. Local immunosuppression induced by high viral load of human papillomavirus: characterization of cellular phenotypes producing interleukin-10 in cervical neoplastic lesions. Immunology 2015.
50. Lenz P., Day P.M., Pang Y.Y., Frye S.A., Jensen P.N., Lowy D.R., Schiller J.T. Papillomavirus-like particles induce acute activation of dendritic cells. J. Immunol. 2001, 166:5346-5355.
51. Lenz P., Lowy D.R., Schiller J.T. Papillomavirus virus-like particles induce cytokines characteristic of innate immune responses in plasmacytoid dendritic cells. Eur. J. Immunol. 2005, 35:1548-1556.
52. Lenz P., Thompson C.D., Day P.M., Bacot S.M., Lowy D.R., Schiller J.T. Interaction of papillomavirus virus-like particles with human myeloid antigen-presenting cells. Clin. Immunol 2003, 106:231-237. Orlando Fla).
53. Rudolf M.P., Fausch S.C., Da Silva D.M., Kast W.M. Human dendritic cells are activated by chimeric human papillomavirus type-16 virus-like particles and induce epitope-specific human T cell responses in vitro. J. Immunol. 2001, 166:5917-5924.
54. Da Silva D.M., Fausch S.C., Verbeek J.S., Kast W.M. Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fc{gamma} receptors and contributes to acquisition of T cell immunity. J. Immunol. 2007, 178:7587-7597.
55. Fahey L.M., Raff A.B., Da Silva D.M., Kast W.M. A major role for the minor capsid protein of human papillomavirus type 16 in immune escape. J. Immunol. 2009, 183:6151-6156.
56. Woodham A.W., Raff A.B., Raff L.M., Da Silva D.M., Yan L., Skeate J.G., Wong M.K., Lin Y.G., Kast W.M. Inhibition of Langerhans cell maturation by human papillomavirus type 16: a novel role for the annexin A2 heterotetramer in immune suppression. J. Immunol. 2014, 192:4748-4757.
57. Levine A.S., Levy H.B. Phase I-II trials of poly IC stabilized with poly-l-lysine. Cancer Treat Rep 1978, 62:1907-1912.
58. Campo M.S., Graham S.V., Cortese M.S., Ashrafi G.H., Araibi E.H., Dornan E.S., Miners K., Nunes C., Man S. HPV-16 E5 down-regulates expression of surface HLA class I and reduces recognition by CD8 T cells. Virology 2010, 407:137-142.
59. Vambutas A., DeVoti J., Pinn W., Steinberg B.M., Bonagura V.R. Interaction of human papillomavirus type 11 E7 protein with TAP-1 results in the reduction of ATP-dependent peptide transport. Clin. Immunol 2001, 101:94-99. Orlando, Fla).
60. Sheu B.C., Chiou S.H., Chang W.C., Chow S.N., Lin H.H., Chen R.J., Huang S.C., Ho H.N., Hsu S.M. Integration of high-risk human papillomavirus DNA correlates with HLA genotype aberration and reduced HLA class I molecule expression in human cervical carcinoma. Clin. Immunol. 2005, 115:295-301. (Orlando, Fla).
61. Scholten K.B., Schreurs M.W., Ruizendaal J.J., Kueter E.W., Kramer D., Veenbergen S., Meijer C.J., Hooijberg E. Preservation and redirection of HPV16E7-specific T cell receptors for immunotherapy of cervical cancer. Clin. Immunol. 2005, 114:119-129.
62. Scholten K.B., Turksma A.W., Ruizendaal J.J., van den Hende M., van der Burg S.H., Heemskerk M.H., Meijer C.J., Hooijberg E. Generating HPV specific T helper cells for the treatment of HPV induced malignancies using TCR gene transfer. J. Transl. Med. 2011, 9:147.
63. Nakagawa M., Stites D.P., Patel S., Farhat S., Scott M., Hills N.K., Palefsky J.M., Moscicki A.B. Persistence of human papillomavirus type 16 infection is associated with lack of cytotoxic T lymphocyte response to the E6 antigens. J. Infect. Dis. 2000, 182:595-598.
64. Ressing M.E., van Driel W.J., Celis E., Sette A., Brandt M.P., Hartman M., Anholts J.D., Schreuder G.M., ter Harmsel W.B., Fleuren G.J., Trimbos B.J., Kast W.M., Melief C.J. Occasional memory cytotoxic T-cell responses of patients with human papillomavirus type 16-positive cervical lesions against a human leukocyte antigen-A 0201-restricted E7-encoded epitope. Cancer Res. 1996, 56:582-588.
65. Farhat S., Nakagawa M., Moscicki A.B. Cell-mediated immune responses to human papillomavirus 16 E6 and E7 antigens as measured by interferon gamma enzyme-linked immunospot in women with cleared or persistent human papillomavirus infection. Int. J. Gynecol. Cancer 2009, 19:508-512.
66. Renn C.N., Sanchez D.J., Ochoa M.T., Legaspi A.J., Oh C.K., Liu P.T., Krutzik S.R., Sieling P.A., Cheng G., Modlin R.L. TLR activation of Langerhans cell-like dendritic cells triggers an antiviral immune response. J. Immunol. 2006, 177:298-305.
67. Andersen J.M., Al-Khairy D., Ingalls R.R. Innate immunity at the mucosal surface: role of toll-like receptor 3 and toll-like receptor 9 in cervical epithelial cell responses to microbial pathogens. Biol. Reprod. 2006, 74:824-831.
68. Romani N., Holzmann S., Tripp C.H., Koch F., Stoitzner P. Langerhans cells-dendritic cells of the epidermis. APMIS 2003, 111:725-740.
69. Jimenez-Flores R., Mendez-Cruz R., Ojeda-Ortiz J., Munoz-Molina R., Balderas-Carrillo O., de la Luz Diaz-Soberanes M., Lebecque S., Saeland S., Daneri-Navarro A., Garcia-Carranca A., Ullrich S.E., Flores-Romo L. High-risk human papilloma virus infection decreases the frequency of dendritic Langerhans' cells in the human female genital tract. Immunology 2006, 117:220-228.
70. Leong C.M., Doorbar J., Nindl I., Yoon H.S., Hibma M.H. Deregulation of E-cadherin by human papillomavirus is not confined to high-risk, cancer-causing types. Br. J. Dermatol. 2010, 163:1253-1263.
71. Leong C.M., Doorbar J., Nindl I., Yoon H.S., Hibma M.H. Loss of epidermal Langerhans cells occurs in human papillomavirus alpha, gamma, and mu but not beta genus infections. J. Investig. Dermatol. 2010, 130:472-480.
72. DeCarlo C.A., Rosa B., Jackson R., Niccoli S., Escott N.G., Zehbe I. Toll-like receptor transcriptome in the HPV-positive cervical cancer microenvironment. Clin. Dev. Immunol. 2012, 2012:785825.
73. Scott M.E., Ma Y., Farhat S., Moscicki A.B. Expression of nucleic acid-sensing Toll-like receptors predicts HPV16 clearance associated with an E6-directed cell-mediated response. Int. J. Cancer 2015, 136:2402-2408.
74. Daud M.E., Scott Y., Ma S., Shiboski S., Farhat A.B. Moscicki, association between toll-like receptor expression and human papillomavirus type 16 persistence. Int. J. Cancer 2011, 128:879-886.
75. Hartman L.L., Crawford J.R., Makale M.T., Milburn M., Joshi S., Salazar A.M., Hasenauer B., VandenBerg S.R., MacDonald T.J., Durden D.L. Pediatric phase II trials of poly-ICLC in the management of newly diagnosed and recurrent brain tumors. J. Pediatr. Hematol. Oncol. 2014, 36:451-457.
76. Rosenfeld M.R., Chamberlain M.C., Grossman S.A., Peereboom D.M., Lesser G.J., Batchelor T.T., Desideri S., Salazar A.M., Ye X. A multi-institution phase II study of poly-ICLC and radiotherapy with concurrent and adjuvant temozolomide in adults with newly diagnosed glioblastoma. Neuro-Oncology 2010, 12:1071-1077.
77. Salazar A.M., Levy H.B., Ondra S., Kende M., Scherokman B., Brown D., Mena H., Martin N., Schwab K., Donovan D., Dougherty D., Pulliam M., Ippolito M., Graves M., Brown H., Ommaya A. Long-term treatment of malignant gliomas with intramuscularly administered polyinosinic-polycytidylic acid stabilized with polylysine and carboxymethylcellulose: an open pilot study. Neurosurgery 1996, 38:1096-1103. 1103-1094.