Expression of coinhibitory receptors on T cells in the microenvironment of usual vulvar intraepithelial neoplasia is related to proinflammatory effector T cells and an increased recurrence-free survival

International Journal of Cancer

Volumn 136, Issue 4, 2015, Pages E95-E106

  Van Esch, Edith M G ^a   Van Poelgeest, Mariette I E ^a   Kouwenberg, Simone ^a   Osse, E Michelle ^a   Trimbos, J Baptist M Z ^a   Fleuren, Gert Jan ^a   Jordanova, Ekaterina S ^a   Van Der Burg, Sjoerd H ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Coinhibitory receptors; HPV; Immunotherapy; TIM3; Usual VIN

Indexed keywords

ECALECTIN; GALECTIN 1; GALECTIN 3; INDOLEAMINE 2,3 DIOXYGENASE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; PEPTIDES AND PROTEINS; PROGRAMMED DEATH 1 RECEPTOR; T CELL IMMUNOGLOBULIN MUCIN 3; TBET PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; GALECTIN; HAVCR2 PROTEIN, HUMAN; LGALS1 PROTEIN, HUMAN; LGALS9 PROTEIN, HUMAN; MEMBRANE PROTEIN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C;

ARTICLE; CANCER RECURRENCE; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; EFFECTOR CELL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR MICROENVIRONMENT; VAGINAL INTRAEPITHELIAL NEOPLASIA; WART VIRUS; ADOLESCENT; ADULT; AGED; CARCINOMA IN SITU; CASE CONTROL STUDY; DISEASE FREE SURVIVAL; IMMUNOLOGY; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; NEUTROPHIL CHEMOTAXIS; PAPILLOMAVIRUS INFECTION; PROPORTIONAL HAZARDS MODEL; TUMOR RECURRENCE; VERY ELDERLY; VIROLOGY; VULVA TUMOR; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CARCINOMA IN SITU; CASE-CONTROL STUDIES; CHEMOTAXIS, LEUKOCYTE; DISEASE-FREE SURVIVAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GALECTIN 1; GALECTINS; HUMANS; KAPLAN-MEIER ESTIMATE; MEMBRANE PROTEINS; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; PAPILLOMAVIRUS INFECTIONS; PROPORTIONAL HAZARDS MODELS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT; VULVAR NEOPLASMS; YOUNG ADULT;

EID: 84918822711     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29174     Document Type: Article

References (50)

1. De Vuijst 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 metaanalysis. Int J Cancer 2009;124:1626-36
2. Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med 1997;102:3-8
3. Brown DR, Shew ML, Qadadri B, et al. A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis 2005;191:182-92
4. Ho GY, Bierman R, Beardsley L, et al. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 1998;338:423-8
5. van Poelgeest MI, Van Seters M, Van Beurden M, et al. Detection of human papillomavirus (HPV) 16-specific CD41 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. van der Burg SH, Melief CJ. Therapeutic vaccination against human papilloma virus induced malignancies. Curr Opin Immunol 2011;23:252-7
7. 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
8. 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
9. 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
10. 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
11. 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
12. 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
13. Davidson EJ, Boswell CM, Sehr P, 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
14. 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
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. Terlou A, Van SM, KleinJan A, et al. Imiquimodinduced clearance of HPV is associated with normalization of immune cell counts in usual type vulvar intraepithelial neoplasia. Int J Cancer 2010; 127:2831-40
17. 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
18. Singh K, Yeo Y, Honest H, et al. Antigen processing and correlation with immunological response in vulval intraepithelial neoplasia-A study of CD1a, CD54 and LN3 expression. Gynecol Oncol 2006;102:489-92
19. Uyttenhove C, Pilotte L, Theate I, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 2003;9: 1269-74
20. 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
21. Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol 2013;13:227-42
22. Anderson AC. Tim-3, a negative regulator of anti-tumor immunity. Curr Opin Immunol 2012; 24:213-6
23. Zou W, Chen L. Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol 2008;8:467-77
24. Keir ME, Butte MJ, Freeman GJ, et al. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008;26:677-704
25. Topalian SL, Hodi FS, Brahmer JR, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54
26. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366: 2455-65
27. Fourcade J, Sun Z, Benallaoua M, et al. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD81 T cell dysfunction in melanoma patients. J Exp Med 2010; 207:2175-86
28. Sakuishi K, Apetoh L, Sullivan JM, et al. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 2010;207:2187-94
29. Yan J, Zhang Y, Zhang JP, et al. Tim-3 expression defines regulatory T cells in human tumors. PLoS One 2013;8:e58006
30. Monney L, Sabatos CA, Gaglia JL, et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 2002;415:536-41
31. Zhu C, Anderson AC, Schubart A, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 2005;6: 1245-52
32. Rodriguez-Manzanet R, DeKruyff R, Kuchroo VK, et al. The costimulatory role of TIM molecules. Immunol Rev 2009;229:259-70
33. Rabinovich GA, Toscano MA. Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 2009;9:338-52
34. Rabinovich GA, Croci DO. Regulatory circuits mediated by lectin-glycan interactions in autoimmunity and cancer. Immunity 2012;36:322-35
35. Liu FT, Rabinovich GA. Galectins: regulators of acute and chronic inflammation. Ann N Y Acad Sci 2010;1183:158-82
36. Gieseke F, Kruchen A, Tzaribachev N, et al. Proinflammatory stimuli induce galectin-9 in human mesenchymal stromal cells to suppress Tcell proliferation. Eur J Immunol 2013;43:2741-9
37. Cedeno-Laurent F, Opperman M, Barthel SR, et al. Galectin-1 triggers an immunoregulatory signature in Th cells functionally defined by IL- 10 expression. J Immunol 2012;188:3127-37
38. Sheu BC, Chiou SH, Lin HH, et al. Up-regulation of inhibitory natural killer receptors CD94/ NKG2A with suppressed intracellular perforin expression of tumor-infiltrating CD81 T lymphocytes in human cervical carcinoma. Cancer Res 2005;65:2921-9
39. Gooden M, Lampen M, Jordanova ES, et al. HLA-E expression by gynecological cancers restrains tumor-infiltrating CD8(1) T lymphocytes. Proc Natl Acad Sci USA 2011;108:10656-61
40. van Esch EM, Tummers B, Baartmans V, et al. Alterations in classical and non-classical HLA expression in recurrent and progressive HPV induced vulvar intraepithelial neoplasia (uVIN) and implications for immunotherapy. Int J Cancer 2014;135:830-42
41. Sideri M, Jones RW, Wilkinson EJ, et al. Squamous vulvar intraepithelial neoplasia: 2004 modified terminology, ISSVD Vulvar Oncology Subcommittee. J Reprod Med 2005;50:807-10.
42. van Esch EM, Dam MC, Osse ME, 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.
43. Legat A, Speiser DE, Pircher H, et al. Inhibitory Receptor Expression Depends More Dominantly on Differentiation and Activation than "Exhaus Exhaustion" of Human CD8 T Cells. Front Immunol 2013;4:455.
44. McMahon CW, Zajac AJ, Jamieson AM, et al. Viral and bacterial infections induce expression of multiple NK cell receptors in responding CD8(1) T cells. J Immunol 2002;169:1444-52.
45. Byers AM, Andrews NP, Lukacher AE. CD94/NKG2A expression is associated with proliferative potential of CD8 T cells during persistent polyoma virus infection. J Immunol 2006;176:6121-9.
46. Cedeno-Laurent F, Dimitroff CJ. Evidence of a novel galectin-9-binding membrane glycoprotein ligand on T helper cells. Clin Immunol 2012;143:6-7.
47. Nagahara K, Arikawa T, Oomizu S, et al. Galectin-9 increases Tim-31 dendritic cells and CD81 T cells and enhances antitumor immunity via galectin-9-Tim-3 interactions. J Immunol 2008; 181:7660-9.
48. Dai SY, Nakagawa R, Itoh A, et al. Galectin-9 induces maturation of human monocyte-derived dendritic cells. J Immunol 2005;175:2974-81.
49. Gooden MJ, Wiersma VR, Samplonius DF, et al. Galectin-9 activates and expands human T-helper 1 cells. PLoS One 2013;8:e65616.
50. van Esch EM, van Poelgeest MI, Trimbos BJ, et al. Intraepithelial macrophage infiltration is related to a high number of regulatory T cells and promote a progressive course of HPV induced vulvar neoplasia. Int J Cancer 2014