Alterations in classical and nonclassical HLA expression in recurrent and progressive HPV-induced usual vulvar intraepithelial neoplasia and implications for immunotherapy

International Journal of Cancer

Volumn 135, Issue 4, 2014, Pages 830-842

  Van Esch, E M G ^a   Tummers, B ^a   Baartmans, V ^a   Osse, E M ^a   Ter Haar, N ^a   Trietsch, M D ^a   Hellebrekers, B W J ^b   Holleboom, C A G ^c   Nagel, H T C ^c   Tan, L T ^c   Fleuren, G J ^a   Van Poelgeest, M I E ^a   Van Der Burg, S H ^a   Jordanova, E S ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b HAGA HOSPITAL   (Netherlands)

^c MEDICAL CENTER HAAGLANDEN   (Netherlands)

Author keywords

HLA expression; immunotherapy; microenvironment; uVIN; vulvar carcinoma

Indexed keywords

GAMMA INTERFERON; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; HLA B ANTIGEN; HLA C ANTIGEN; HLA E ANTIGEN; HLA G ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SYNTHETIC PEPTIDE; WART VIRUS VACCINE;

ADULT; AGED; ARTICLE; CANCER IMMUNOTHERAPY; CANCER RECURRENCE; CANCER STAGING; CELL CULTURE; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DOWN REGULATION; FEMALE; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; KERATINOCYTE; MAJOR CLINICAL STUDY; PRECANCER; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT RESPONSE; UPREGULATION; VACCINATION; VULVA CANCER; VULVAR INTRAEPITHELIAL NEOPLASIA;

HLA EXPRESSION; IMMUNOTHERAPY; MICROENVIRONMENT; UVIN; VULVAR CARCINOMA;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CARCINOMA; CASE-CONTROL STUDIES; COHORT STUDIES; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOTYPE; HLA ANTIGENS; HUMANS; IMMUNOTHERAPY; INTERFERON-GAMMA; KERATINOCYTES; LOSS OF HETEROZYGOSITY; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; RECURRENCE; VULVAR NEOPLASMS;

EID: 84902251245     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28713     Document Type: Article

References (50)

1. van de Nieuwenhof HP, van der Avoort IA, de Hullu JA,. Review of squamous premalignant vulvar lesions. Crit Rev Oncol Hematol 2008; 68: 131-56.
2. De Vuyst H, Clifford GM, Nascimento MC, et al. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis. Int J Cancer 2009; 124: 1626-36.
3. van Seters M, van Beurden M, de Craen AJ,. Is the assumed natural history of vulvar intraepithelial neoplasia III based on enough evidence? A systematic review of 3322 published patients. Gynecol Oncol 2005; 97: 645-51.
4. Hillemanns P, Wang X, Staehle S, et al. Evaluation of different treatment modalities for vulvar intraepithelial neoplasia (VIN): CO(2) laser vaporization, photodynamic therapy, excision and vulvectomy. Gynecol Oncol 2006; 100: 271-5.
5. van Poelgeest MI, van Seters M, van Beurden M, et al. Detection of human papillomavirus (HPV) 16-specific CD4+ T-cell immunity in patients with persistent HPV16-induced vulvar intraepithelial neoplasia in relation to clinical impact of imiquimod treatment. Clin Cancer Res 2005; 11: 5273-80.
6. Jones RW, Rowan DM, Stewart AW,. Vulvar intraepithelial neoplasia: aspects of the natural history and outcome in 405 women. Obstet Gynecol 2005; 106: 1319-26.
7. Woo YL, van den Hende M, Sterling JC, et al. A prospective study on the natural course of low-grade squamous intraepithelial lesions and the presence of HPV16 E2-, E6- and E7-specific T-cell responses. Int J Cancer 2010; 126: 133-41.
8. Farhat S, Nakagawa M, Moscicki AB,. 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: 508-12.
9. Bourgault Villada I, Moyal BM, Ziol M, et al. Spontaneous regression of grade 3 vulvar intraepithelial neoplasia associated with human papillomavirus-16-specific CD4(+) and CD8(+) T-cell responses. Cancer Res 2004; 64: 8761-6.
10. van Seters M, Beckmann I, Heijmans-Antonissen C, et al. Disturbed patterns of immunocompetent cells in usual-type vulvar intraepithelial neoplasia. Cancer Res 2008; 68: 6617-22.
11. Terlou A, van Seters M, KleinJan A, et al. Imiquimod-induced clearance of HPV is associated with normalization of immune cell counts in usual type vulvar intraepithelial neoplasia. Int J Cancer 2010; 127: 2831-40.
12. Abdel-Hady ES, Martin-Hirsch P, Duggan-Keen M, et al. Immunological and viral factors associated with the response of vulval intraepithelial neoplasia to photodynamic therapy. Cancer Res 2001; 61: 192-6.
13. Kenter GG, Welters MJ, Valentijn AR, et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 2009; 361: 1838-47.
14. van Seters M, van Beurden M, ten Kate FJ, et al. Treatment of vulvar intraepithelial neoplasia with topical imiquimod. N Engl J Med 2008; 358: 1465-73.
15. Daayana S, Elkord E, Winters U, et al. Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br J Cancer 2010; 102: 1129-36.
16. Winters U, Daayana S, Lear JT, et al. Clinical and immunologic results of a phase II trial of sequential imiquimod and photodynamic therapy for vulval intraepithelial neoplasia. Clin Cancer Res 2008; 14: 5292-9.
17. Daayana S, Winters U, Stern PL, et al. Clinical and immunological response to photodynamic therapy in the treatment of vulval intraepithelial neoplasia. Photochem Photobiol Sci 2011; 10: 802-9.
18. Welters MJ, Kenter GG, de Vos van Steenwijk PJ, et al. Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc Natl Acad Sci USA 2010; 107: 11895-9.
19. Jordanova ES, Gorter A, Ayachi O, et al. Human leukocyte antigen class I, MHC class I chain-related molecule A, and CD8+/regulatory T-cell ratio: which variable determines survival of cervical cancer patients? Clin Cancer Res 2008; 14: 2028-35.
20. Garrido F, Cabrera T, Aptsiauri N,. "Hard" and "soft" lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy. Int J Cancer 2010; 127: 249-56.
21. Brady CS, Bartholomew JS, Burt DJ, et al. Multiple mechanisms underlie HLA dysregulation in cervical cancer. Tissue Antigens 2000; 55: 401-11.
22. Vermeulen CF, Jordanova ES, Zomerdijk-Nooijen YA, et al. Frequent HLA class I loss is an early event in cervical carcinogenesis. Hum Immunol 2005; 66: 1167-73.
23. Koopman LA, Corver WE, van der Slik AR, et al. Multiple genetic alterations cause frequent and heterogeneous human histocompatibility leukocyte antigen class I loss in cervical cancer. J Exp Med 2000; 191: 961-76.
24. Torres-Aguilar H, Aguilar-Ruiz SR, Gonzalez-Perez G, et al. Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J Immunol 2010; 184: 1765-75.
25. Hilders CG, Munoz IM, Nooyen Y, et al. Altered HLA expression by metastatic cervical carcinoma cells as a factor in impaired immune surveillance. Gynecol Oncol 1995; 57: 366-75.
26. de Boer MA, Jordanova ES, van Poelgeest MI, et al. Circulating human papillomavirus type 16 specific T-cells are associated with HLA Class I expression on tumor cells, but not related to the amount of viral oncogene transcripts. Int J Cancer 2007; 121: 2711-15.
27. Gooden M, Lampen M, Jordanova ES, et al. HLA-E expression by gynecological cancers restrains tumor-infiltrating CD8(+) T lymphocytes. Proc Natl Acad Sci USA 2011; 108: 10656-61.
28. Spaans VM, Peters AA, Fleuren GJ, et al. HLA-E expression in cervical adenocarcinomas: association with improved long-term survival. J Transl Med 2012; 10: 184.
29. Dong DD, Yang H, Li K, et al. Human leukocyte antigen-G (HLA-G) expression in cervical lesions: association with cancer progression, HPV 16/18 infection, and host immune response. Reprod Sci 2010; 17: 718-23.
30. Gonzalez A, Rebmann V, LeMaoult J, et al. The immunosuppressive molecule HLA-G and its clinical implications. Crit Rev Clin Lab Sci 2012; 49: 63-84.
31. van den Brule AJ, Pol R, Fransen-Daalmeijer N, et al. GP5+/6+ PCR followed by reverse line blot analysis enables rapid and high-throughput identification of human papillomavirus genotypes. J Clin Microbiol 2002; 40: 779-87.
32. Kleter B, van Doorn LJ, Schrauwen L, et al. Development and clinical evaluation of a highly sensitive PCR-reverse hybridization line probe assay for detection and identification of anogenital human papillomavirus. J Clin Microbiol 1999; 37: 2508-17.
33. Ruiter DJ, Ferrier CM, van Muijen GN, et al. Quality control of immunohistochemical evaluation of tumour-associated plasminogen activators and related components. European BIOMED-1 Concerted Action on Clinical Relevance of Proteases in Tumour Invasion and Metastasis. Eur J Cancer 1998; 34: 1334-40.
34. Liu X, Ory V, Chapman S, et al. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. Am J Pathol 2012; 180: 599-607.
35. Yuan H, Myers S, Wang J, et al. Use of reprogrammed cells to identify therapy for respiratory papillomatosis. N Engl J Med 2012; 367: 1220-7.
36. van Esch EM, Dam MS, Osse EM, et al. Clinical characteristics associated with development of recurrence and progression in usual type vulvar intraepithelial neoplasia. Int J Gynecol Cancer 2013; 23: 1476-83.
37. Bontkes HJ, Walboomers JM, Meijer CJ, et al. Specific HLA class I down-regulation is an early event in cervical dysplasia associated with clinical progression. Lancet 1998; 351: 187-8.
38. Aptsiauri N, Carretero R, Garcia-Lora A, et al. Regressing and progressing metastatic lesions: resistance to immunotherapy is predetermined by irreversible HLA class I antigen alterations. Cancer Immunol Immunother 2008; 57: 1727-33.
39. Jochmus I, Durst M, Reid R, et al. Major histocompatibility complex and human papillomavirus type 16 E7 expression in high-grade vulvar lesions. Hum Pathol 1993; 24: 519-24.
40. Bos R, Sherman LA,. CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 2010; 70: 8368-77.
41. Goncalves MA, Le DM, Simoes RT, et al. Classical and non-classical HLA molecules and p16(INK4a) expression in precursors lesions and invasive cervical cancer. Eur J Obstet Gynecol Reprod Biol 2008; 141: 70-4.
42. Malmberg KJ, Levitsky V, Norell H, et al. IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J Clin Invest 2002; 110: 1515-23.
43. Mingari MC, Ponte M, Bertone S, et al. HLA class I-specific inhibitory receptors in human T lymphocytes: interleukin 15-induced expression of CD94/NKG2A in superantigen- or alloantigen-activated CD8+ T cells. Proc Natl Acad Sci USA 1998; 95: 1172-7.
44. Bertone S, Schiavetti F, Bellomo R, et al. Transforming growth factor-beta-induced expression of CD94/NKG2A inhibitory receptors in human T lymphocytes. Eur J Immunol 1999; 29: 23-9.
45. Guimaraes MC, Soares CP, Donadi EA, et al. Low expression of human histocompatibility soluble leukocyte antigen-G (HLA-G5) in invasive cervical cancer with and without metastasis, associated with papilloma virus (HPV). J Histochem Cytochem 2010; 58: 405-11.
46. Urosevic M, Kurrer MO, Kamarashev J, et al. Human leukocyte antigen G up-regulation in lung cancer associates with high-grade histology, human leukocyte antigen class I loss and interleukin-10 production. Am J Pathol 2001; 159: 817-24.
47. Urosevic M, Dummer R,. Human leukocyte antigen-G and cancer immunoediting. Cancer Res 2008; 68: 627-30.
48. Rodriguez JA, Galeano L, Palacios DM, et al. Altered HLA class I and HLA-G expression is associated with IL-10 expression in patients with cervical cancer. Pathobiology 2012; 79: 72-83.
49. Li XJ, Zhang X, Lin A, et al. Human leukocyte antigen-G (HLA-G) expression in cervical cancer lesions is associated with disease progression. Hum Immunol 2012; 73: 946-9.
50. Ye SR, Yang H, Li K, et al. Human leukocyte antigen G expression: as a significant prognostic indicator for patients with colorectal cancer. Mod Pathol 2007; 20: 375-83.