MICA/B and ULBP1 NKG2D ligands are independent predictors of good prognosis in cervical cancer

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Cho, Hanbyoul ^a,b   Chung, Joon Yong ^b   Kim, Sunghoon ^a,c   Braunschweig, Till ^b,d   Kang, Tae Heung ^e   Kim, Jennie ^b   Chung, Eun Joo ^b   Hewitt, Stephen M ^b   Kim, Jae Hoon ^a  

^a Yonsei University College of Medicine   (South Korea)

^b NATIONAL CANCER INSTITUTE   (United States)

^c Yonsei University College of Medicine   (South Korea)

^d RWTH AACHEN UNIVERSITY   (Germany)

^e Konkuk University   (South Korea)

Author keywords

Cervical cancer; Immunohistochemistry; NKG2D ligands; Tissue microarray

Indexed keywords

HLA A ANTIGEN; HLA B ANTIGEN; LIGAND; NATURAL KILLER CELL RECEPTOR NKG2D LIGAND; RETINOIC ACID EARLY TRANSCRIPT 1E; RETINOIC ACID EARLY TRANSCRIPT 1G; UL16 BINDING PROTEIN 1; UL16 BINDING PROTEIN 2; UL16 BINDING PROTEIN 3; UNCLASSIFIED DRUG; CARRIER PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HLA ANTIGEN CLASS 1; KLRK1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MHC CLASS I-RELATED CHAIN A; MICB ANTIGEN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; RAET1E PROTEIN, HUMAN; RAET1G PROTEIN, HUMAN; SIGNAL PEPTIDE; TUMOR MARKER; ULBP1 PROTEIN, HUMAN; ULBP2 PROTEIN, HUMAN; ULBP3 PROTEIN, HUMAN;

ADULT; ARTICLE; CANCER GRADING; CANCER GROWTH; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CERVICAL CANCER CELL LINE; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE FREE SURVIVAL; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MOLECULAR DYNAMICS; OVERALL SURVIVAL; PREDICTIVE VALUE; PROTEIN EXPRESSION; SURVIVAL RATE; SURVIVAL TIME; TISSUE MICROARRAY; TUMOR VOLUME; UPREGULATION; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU; CHEMISTRY; HELA CELL LINE; MIDDLE AGED; PATHOLOGY; PROGNOSIS; UTERINE CERVIX; UTERINE CERVIX TUMOR;

ADULT; BIOMARKERS, TUMOR; CARRIER PROTEINS; CERVICAL INTRAEPITHELIAL NEOPLASIA; CERVIX UTERI; DISEASE-FREE SURVIVAL; FEMALE; GPI-LINKED PROTEINS; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MEMBRANE PROTEINS; MIDDLE AGED; NEOPLASM STAGING; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PROGNOSIS; SURVIVAL RATE; TISSUE ARRAY ANALYSIS; TUMOR BURDEN; UTERINE CERVICAL NEOPLASMS;

EID: 84924694068     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-957     Document Type: Article

References (34)

1. Sankaranarayanan R, Ferlay J: Worldwide burden of gynaecological cancer: the size of the problem. Best Pract Res Clin Obstet Gynaecol 2006,20(2):207-225. 10.1016/j.bpobgyn.2005.10.007.
2. Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S: Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br J Cancer 2003,88(1):63-73. 10.1038/sj.bjc.6600688.
3. Dalstein V, Riethmuller D, Pretet JL, Le Bail CK, Sautiere JL, Carbillet JP, Kantelip B, Schaal JP, Mougin C: Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int J Cancer 2003,106(3):396-403. 10.1002/ijc.11222.
4. Snijders PJ, Steenbergen RD, Heideman DA, Meijer CJ: HPV-mediated cervical carcinogenesis: concepts and clinical implications. J Pathol 2006,208(2):152-164. 10.1002/path.1866.
5. Lee WC, Lee SY, Koo YJ, Kim TJ, Hur SY, Hong SR, Kim SS, Kee MK, Rhee JE, Lee JS, Choi HS, Cho CH, Kim KT, Park JS: Establishment of a Korea HPV cohort study. J Gynecol Oncol 2013,24(1):59-65. 10.3802/jgo.2013.24.1.59.
6. Ahdieh L, Munoz A, Vlahov D, Trimble CL, Timpson LA, Shah K: Cervical neoplasia and repeated positivity of human papillomavirus infection in human immunodeficiency virus-seropositive and -seronegative women. Am J Epidemiol 2000,151(12):1148-1157. 10.1093/oxfordjournals.aje.a010165.
7. Trinchieri G: Biology of natural killer cells. Adv Immunol 1989, 47:187-376.
8. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Che X, Iwashige H, Aridome K, Hokita S, Aikou T: Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000,88(3):577-583. 10.1002/(SICI)1097-0142(20000201)88:3<577::AID-CNCR13>3.0.CO;2-V.
9. Villegas FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, Jareno J, Zuil M, Callol L: Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 2002,35(1):23-28. 10.1016/S0169-5002(01)00292-6.
10. Garzetti GG, Ciavattini A, Muzzioli M, Goteri G, Mannello B, Romanini C, Fabris N: Natural killer cell activity in patients with invasive cervical carcinoma: importance of a longitudinal evaluation in follow-up. Gynecol Obstet Invest 1995,40(2):133-138. 10.1159/000292322.
11. Raulet DH: Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003,3(10):781-790. 10.1038/nri1199.
12. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T: Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A 1996,93(22):12445-12450. 10.1073/pnas.93.22.12445.
13. Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, Spies T, Kimura R, Miyagi T, Mochizuki K, Sasaki Y, Hayashi N: Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int J Cancer 2003,104(3):354-361. 10.1002/ijc.10966.
14. Textor S, Durst M, Jansen L, Accardi R, Tommasino M, Trunk MJ, Porgador A, Watzl C, Gissmann L, Cerwenka A: Activating NK cell receptor ligands are differentially expressed during progression to cervical cancer. Int J Cancer 2008,123(10):2343-2353. 10.1002/ijc.23733.
15. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, Biassoni R, Bottino C, Moretta L, Moretta A: Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci U S A 2003,100(7):4120-4125. 10.1073/pnas.0730640100.
16. Pende D, Rivera P, Marcenaro S, Chang CC, Biassoni R, Conte R, Kubin M, Cosman D, Ferrone S, Moretta L, Moretta A: Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res 2002,62(21):6178-6186.
17. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG: New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000,92(3):205-216. 10.1093/jnci/92.3.205.
18. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD: Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002,3(11):991-998. 10.1038/ni1102-991.
19. McGilvray RW, Eagle RA, Watson NF, Al-Attar A, Ball G, Jafferji I, Trowsdale J, Durrant LG: NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin Cancer Res 2009,15(22):6993-7002. 10.1158/1078-0432.CCR-09-0991.
20. Dunn GP, Old LJ, Schreiber RD: The three Es of cancer immunoediting. Annu Rev Immunol 2004, 22:329-360. 10.1146/annurev.immunol.22.012703.104803.
21. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD: IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001,410(6832):1107-1111. 10.1038/35074122.
22. Cerwenka A, Baron JL, Lanier LL: Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci U S A 2001,98(20):11521-11526. 10.1073/pnas.201238598.
23. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH: Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001,413(6852):165-171. 10.1038/35093109.
24. Smyth MJ, Swann J, Cretney E, Zerafa N, Yokoyama WM, Hayakawa Y: NKG2D function protects the host from tumor initiation. J Exp Med 2005,202(5):583-588. 10.1084/jem.20050994.
25. Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, Mandelboim M, Mandelboim O: Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 2008,9(9):1065-1073. 10.1038/ni.1642.
26. Gasser S, Orsulic S, Brown EJ, Raulet DH: The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005,436(7054):1186-1190. 10.1038/nature03884.
27. Armeanu S, Bitzer M, Lauer UM, Venturelli S, Pathil A, Krusch M, Kaiser S, Jobst J, Smirnow I, Wagner A, Steinle A, Salih HR: Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res 2005,65(14):6321-6329. 10.1158/0008-5472.CAN-04-4252.
28. Boissel N, Rea D, Tieng V, Dulphy N, Brun M, Cayuela JM, Rousselot P, Tamouza R, Le Bouteiller P, Mahon FX, Steinle A, Salih HR: BCR/ABL oncogene directly controls MHC class I chain-related molecule A expression in chronic myelogenous leukemia. J Immunol 2006,176(8):5108-5116. 10.4049/jimmunol.176.8.5108.
29. Li K, Mandai M, Hamanishi J, Matsumura N, Suzuki A, Yagi H, Yamaguchi K, Baba T, Fujii S, Konishi I: 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 2009,58(5):641-652. 10.1007/s00262-008-0585-3.
30. Eagle RA, Jafferji I, Barrow AD: Beyond stressed self: evidence for NKG2D ligand expression on healthy cells. Curr Immunol Rev 2009,5(1):22-34. 10.2174/157339509787314369.
31. Eagle RA, Traherne JA, Ashiru O, Wills MR, Trowsdale J: Regulation of NKG2D ligand gene expression. Hum Immunol 2006,67(3):159-169. 10.1016/j.humimm.2006.02.015.
32. Eagle RA, Trowsdale J: Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 2007,7(9):737-744. 10.1038/nri2144.
33. McGilvray RW, Eagle RA, Rolland P, Jafferji I, Trowsdale J, Durrant LG: ULBP2 and RAET1E NKG2D ligands are independent predictors of poor prognosis in ovarian cancer patients. Int J Cancer 2010,127(6):1412-1420. 10.1002/ijc.25156.
34. Cao W, Xi X, Hao Z, Li W, Kong Y, Cui L, Ma C, Ba D, He W: RAET1E2, a soluble isoform of the UL16-binding protein RAET1E produced by tumor cells, inhibits NKG2D-mediated NK cytotoxicity. J Biol Chem 2007,282(26):18922-18928. 10.1074/jbc. M702504200.