HLA-E expression by gynecological cancers restrains tumor-infiltrating CD8 + T lymphocytes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 26, 2011, Pages 10656-10661

  Gooden, Marloes ^a   Lampen, Margit ^b   Jordanova, Ekaterina S ^b   Leffers, Ninke ^a   Trimbos, J Baptist ^b   Van Der Burg, Sjoerd H ^b   Nijman, Hans ^a   Van Hall, Thorbald ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cervical carcinoma; Immune surveillance; NK receptors; Ovarian carcinoma; Tumormilieu

Indexed keywords

BETA 2 MICROGLOBULIN; CD94 ANTIGEN; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; HLA E ANTIGEN; NATURAL KILLER CELL RECEPTOR NKG2A; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ANTIGEN DETECTION; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; OVARY CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; TISSUE SECTION; TUMOR ASSOCIATED LEUKOCYTE; UTERINE CERVIX CANCER;

CD8-POSITIVE T-LYMPHOCYTES; COHORT STUDIES; FEMALE; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOCYTES, TUMOR-INFILTRATING; OVARIAN NEOPLASMS; UTERINE CERVICAL NEOPLASMS;

EID: 79960587042     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1100354108     Document Type: Article

References (60)

1. Rodgers JR, Cook RG (2005) MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol 5:459-471. (Pubitemid 40835034)
2. van Hall T, Oliveira CC, Joosten SA, Ottenhoff TH (2010) The other Janus face of Qa-1 and HLA-E: Diverse peptide repertoires in times of stress. Microbes Infect 12:910-918.
3. Grimsley C, et al. (2002) Definitive high resolution typing of HLA-E allelic polymorphisms: Identifying potential errors in existing allele data. Tissue Antigens 60:206-212. (Pubitemid 35398823)
4. Strong RK, et al. (2003) HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J Biol Chem 278:5082-5090. (Pubitemid 36801018)
5. O'Callaghan CA, et al. (1998) Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol Cell 1:531-541. (Pubitemid 128374689)
6. Lee N, Goodlett DR, Ishitani A, Marquardt H, Geraghty DE (1998) HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J Immunol 160:4951-4960. (Pubitemid 28215330)
7. Braud VM, Allan DS, Wilson D, McMichael AJ (1998) TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr Biol 8:1-10. (Pubitemid 28056248)
8. Braud VM, et al. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795-799. (Pubitemid 28099678)
9. Speiser DE, et al. (1999) CD28-negative cytolytic effector T cells frequently express NK receptors and are present at variable proportions in circulating lymphocytes from healthy donors and melanoma patients. Eur J Immunol 29:1990-1999. (Pubitemid 29265555)
10. Zhou J, Matsuoka M, Cantor H, Homer R, Enelow RI (2008) Cutting edge: Engagement of NKG2A on CD8+ effector T cells limits immunopathology in influenza pneumonia. J Immunol 180:25-29.
11. Hu D, et al. (2004) Analysis of regulatory CD8 T cells in Qa-1-deficient mice. Nat Immunol 5:516-523. (Pubitemid 38660464)
12. Mingari MC, et al. (1998) 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 95:1172-1177. (Pubitemid 28124931)
13. Bertone S, et al. (1999) Transforming growth factor-beta-induced expression of CD94/ NKG2A inhibitory receptors in human T lymphocytes. Eur J Immunol 29:23-29. (Pubitemid 29043518)
14. Menier C, et al. (2003) Characterization of monoclonal antibodies recognizing HLA-G or HLA-E: New tools to analyze the expression of nonclassical HLA class I molecules. Hum Immunol 64:315-326. (Pubitemid 36255272)
15. Coupel S, et al. (2007) Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood 109:2806-2814. (Pubitemid 46482075)
16. Derré L, et al. (2006) Expression and release of HLA-E by melanoma cells and melanocytes: Potential impact on the response of cytotoxic effector cells. J Immunol 177:3100-3107. (Pubitemid 44277827)
17. Perera L, et al. (2007) Expression of nonclassical class I molecules by intestinal epithelial cells. Inflamm Bowel Dis 13:298-307. (Pubitemid 46465911)
18. Ruiter DJ, et al. (1998) 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 34:1334-1340. (Pubitemid 28370922)
19. Leffers N, et al. (2009) Down-regulation of proteasomal subunit MB1 is an independent predictor of improved survival in ovarian cancer. Gynecol Oncol 113:256-263.
20. Leffers N, et al. (2009) Prognostic significance of tumor-infiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother 58:449-459.
21. Jordanova ES, et al. (2008) 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 14:2028-2035.
22. Mehta AM, Jordanova ES, Kenter GG, Ferrone S, Fleuren GJ (2008) Association of antigen processing machinery and HLA class I defects with clinicopathological outcome in cervical carcinoma. Cancer Immunol Immunother 57:197-206. (Pubitemid 350159921)
23. Kloetzel PM, Ossendorp F (2004) Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol 16:76-81.
24. Satoh A, et al. (2004) Epigenetic inactivation of class II transactivator (CIITA) is associated with the absence of interferon-gamma-induced HLA-DR expression in colorectal and gastric cancer cells. Oncogene 23:8876-8886. (Pubitemid 39657778)
25. Wright KL, Ting JP (2006) Epigenetic regulation of MHC-II and CIITA genes. Trends Immunol 27:405-412. (Pubitemid 44216195)
26. Levy EM, et al. (2008) Human leukocyte antigen-E protein is overexpressed in primary human colorectal cancer. Int J Oncol 32:633-641. (Pubitemid 351330470)
27. Braud V, Jones EY, McMichael A (1997) The human major histocompatibility complex class Ib molecule HLA-E binds signal sequence-derived peptides with primary anchor residues at positions 2 and 9. Eur J Immunol 27:1164-1169. (Pubitemid 27197219)
28. Walzer T, et al. (2007) Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Natl Acad Sci USA 104:3384-3389. (Pubitemid 46364168)
29. Dutta N, Majumder D, Gupta A, Mazumder DN, Banerjee S (2005) Analysis of human lymphocyte antigen class I expression in gastric cancer by reverse transcriptase-polymerase chain reaction. Hum Immunol 66:164-169. (Pubitemid 40208204)
30. Dutta N, Gupta A, Mazumder DN, Banerjee S (2006) Down-regulation of locus-specific human lymphocyte antigen class I expression in Epstein-Barr virus-associated gastric cancer: Implication for viral-induced immune evasion. Cancer 106:1685-1693.
31. Bianchini M, et al. (2006) Comparative study of gene expression by cDNA microarray in human colorectal cancer tissues and normal mucosa. Int J Oncol 29:83-94.
32. de Kruijf EM, et al. (2010) HLA-E and HLA-G expression in classical HLA class I-negative tumors is of prognostic value for clinical outcome of early breast cancer patients. J Immunol 185:7452-7459.
33. Sullivan LC, Clements CS, Rossjohn J, Brooks AG (2008) The major histocompatibility complex class Ib molecule HLA-E at the interface between innate and adaptive immunity. Tissue Antigens 72:415-424.
34. Li K, et al. (2009) Clinical significance of the NKG2D ligands, MICA/B and ULBP2 in ovarian cancer: High expression of ULBP2 is an indicator of poor prognosis. Cancer Immunol Immunother 58:641-652.
35. Liu M, et al. (2009) Classification using hierarchical clustering of tumor-infiltrating immune cells identifies poor prognostic ovarian cancers with high levels of COX expression. Mod Pathol 22:373-384.
36. Dong HP, et al. (2006) NK- and B-cell infiltration correlates with worse outcome in metastatic ovarian carcinoma. Am J Clin Pathol 125:451-458. (Pubitemid 43327717)
37. Garcia-Iglesias T, et al. (2009) Low NKp30, NKp46 and NKG2D expression and reduced cytotoxic activity on NK cells in cervical cancer and precursor lesions. BMC Cancer 9:186.
38. Textor S, et al. (2008) Activating NK cell receptor ligands are differentially expressed during progression to cervical cancer. Int J Cancer 123:2343-2353.
39. Papadopoulos N, et al. (2002) Gains and losses of CD8, CD20 and CD56 expression in tumor stroma-infiltrating lymphocytes compared with tumor-associated lymphocytes from ascitic fluid and lymphocytes from tumor draining lymph nodes in serous papillary ovarian carcinoma patients. Eur J Gynaecol Oncol 23:533-536. (Pubitemid 36069997)
40. Waldhauer I, Steinle A (2008) NK cells and cancer immunosurveillance. Oncogene 27:5932-5943.
41. Velardi A, Ruggeri L, Mancusi A, Aversa F, Christiansen FT (2009) Natural killer cell allorecognition of missing self in allogeneic hematopoietic transplantation: A tool for immunotherapy of leukemia. Curr Opin Immunol 21:525-530.
42. Tilburgs T, et al. (2009) Expression of NK cell receptors on decidual T cells in human pregnancy. J Reprod Immunol 80:22-32.
43. Chang WC, et al. (2005) Expression of inhibitory natural killer receptors on tumor-infiltrating CD8+ T lymphocyte lineage in human endometrial carcinoma. Int J Gynecol Cancer 15:1073-1080.
44. Sheu BC, et al. (2005) Up-regulation of inhibitory natural killer receptors CD94/NKG2A with suppressed intracellular perforin expression of tumor-infiltrating CD8+ T lymphocytes in human cervical carcinoma. Cancer Res 65:2921-2929.
45. Henriksen R, et al. (1995) Expression and prognostic significance of TGF-beta isotypes, latent TGF-beta 1 binding protein, TGF-beta type I and type II receptors, and endoglin in normal ovary and ovarian neoplasms. Lab Invest 73:213-220.
46. Santin AD, et al. (2001) Increased levels of interleukin-10 and transforming growth factor-beta in the plasma and ascitic fluid of patients with advanced ovarian cancer. BJOG 108:804-808. (Pubitemid 32695311)
47. Hazelbag S, Gorter A, Kenter GG, van den Broek L, Fleuren G (2002) Transforming growth factor-beta1 induces tumor stroma and reduces tumor infiltrate in cervical cancer. Hum Pathol 33:1193-1199. (Pubitemid 36020069)
48. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225-274.
49. Gumá M, et al. (2005) The CD94/NKG2C killer lectin-like receptor constitutes an alternative activation pathway for a subset of CD8+ T cells. Eur J Immunol 35:2071-2080. (Pubitemid 41015046)
50. Meresse B, et al. (2006) Reprogramming of CTLs into natural killer-like cells in celiac disease. J Exp Med 203:1343-1355. (Pubitemid 43736602)
51. van Stijn A, et al. (2008) Human cytomegalovirus infection induces a rapid and sustained change in the expression of NK cell receptors on CD8+ T cells. J Immunol 180:4550-4560.
52. Marín R, et al. (2003) Analysis of HLA-E expression in human tumors. Immunogenetics 54:767-775. (Pubitemid 36384471)
53. Mittelbronn M, et al. (2007) Elevated HLA-E levels in human glioblastomas but not in grade I to III astrocytomas correlate with infiltrating CD8+ cells. J Neuroimmunol 189:50-58. (Pubitemid 47379433)
54. Gonçalves MA, et al. (2008) Classical and non-classical HLA molecules and p16(INK4a) expression in precursors lesions and invasive cervical cancer. Eur J Obstet Gynecol Reprod Biol 141:70-74.
55. Hanak L, et al. (2009) Expression pattern of HLA class I antigens in renal cell carcinoma and primary cell line cultures: Methodological implications for immunotherapy. Med Sci Monit 15:CR638-CR643.
56. Malmberg KJ, et al. (2002) IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J Clin Invest 110:1515-1523.
57. Cannistra SA (2004) Cancer of the ovary. N Engl J Med 351:2519-2529.
58. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A (2009) Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability. Carcinogenesis 30:1073-1081.
59. Sato E, et al. (2005) Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 102:18538-18543. (Pubitemid 43011261)
60. Karim R, et al. (2009) Tumor-expressed B7-H1 and B7-DC in relation to PD-1+ T-cell infiltration and survival of patients with cervical carcinoma. Clin Cancer Res 15:6341-6347.