Augmented serum level of major histocompatibility complex class I-related chain A (MICA) protein and reduced NKG2D expression on NK and T cells in patients with cervical cancer and precursor lesions

BMC Cancer

Volumn 8, Issue , 2008, Pages

  Arreygue Garcia, Naela A ^a   Daneri Navarro, Adrian ^a   del Toro Arreola, Alicia ^b   Cid Arregui, Angel ^a   Gonzalez Ramella, Oscar ^c   Jave Suarez, Luis F ^c   Aguilar Lemarroy, Adriana ^c   Troyo Sanroman, Rogelio ^a   Bravo Cuellar, Alejandro ^c   Delgado Rizo, Vidal ^a   Garcia Iglesias, Trinidad ^a   Hernandez Flores, Georgina ^c   del Toro Arreola, Susana ^a  

^a UNIVERSITY OF GUADALAJARA   (Mexico)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY COMPLEX CLASS 1 RELATED CHAIN A PROTEIN; NATURAL KILLER CELL RECEPTOR NKG2D; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; IMMUNOGLOBULIN RECEPTOR; MHC CLASS I RELATED CHAIN A; MHC CLASS I-RELATED CHAIN A; NATURAL KILLER CELL ACTIVATING RECEPTORS;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CORRELATION COEFFICIENT; DONOR; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; MONONUCLEAR CELL; NATURAL KILLER CELL; PRECANCER; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; T LYMPHOCYTE; UTERINE CERVIX CANCER; BLOOD; COMPARATIVE STUDY; DISEASE COURSE; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MULTIVARIATE ANALYSIS; SQUAMOUS CELL CARCINOMA; UTERINE CERVIX TUMOR;

ADULT; CARCINOMA, SQUAMOUS CELL; DISEASE PROGRESSION; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; MIDDLE AGED; MULTIVARIATE ANALYSIS; PRECANCEROUS CONDITIONS; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES; UTERINE CERVICAL NEOPLASMS;

EID: 41449109639     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-8-16     Document Type: Article

References (63)

1. Boyle P Global burden of cancer Lancet 1997, 349(Suppl 2):SII23-6. 9164444
2. 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 16359925
3. Lazcano-Ponce EC Moss S Alonso de Ruiz P Salmeron Castro J Hernandez Avila M Cervical cancer screening in developing countries: Why is it ineffective? The case of Mexico Arch Med Res 1999, 30(3):240-250. 10.1016/S0188-0128(99)00006-8 10427875
4. zur Hausen H Papillomavirus infections--a major cause of human cancers Biochim Biophys Acta 1996, 1288(2):F55-78. 8876633
5. Munoz N Human papillomavirus and cancer: The epidemiological evidence J Clin Virol 2000, 19(1-2):1-5. 10.1016/S1386-6532(00)00125-6 11091143
6. Bosch FX Lorincz A Munoz N Meijer CJ Shah KV The causal relation between human papillomavirus and cervical cancer J Clin Pathol 2002, 55(4):244-265. 1769629 11919208
7. 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 12556961
8. Walboomers JM Jacobs MV Manos MM Bosch FX Kummer JA Shah KV Snijders PJ Peto J Meijer CJ Munoz N Human papillomavirus is a necessary cause of invasive cervical cancer worldwide J Pathol 1999, 189(1):12-19. 10.1002/ (SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F 10451482
9. Richardson H Kelsall G Tellier P Voyer H Abrahamowicz M Ferenczy A Coutlee F Franco EL The natural history of type-specific human papillomavirus infections in female university students Cancer Epidemiol Biomarkers Prev 2003, 12(6):485-490. 12814991
10. Ho GY Bierman R Beardsley L Chang CJ Burk RD Natural history of cervicovaginal papillomavirus infection in young women N Engl J Med 1998, 338(7):423-428. 10.1056/NEJM199802123380703 9459645
11. Sellors JW Karwalajtys TL Kaczorowski J Mahony JB Lytwyn A Chong S Sparrow J Lorincz A Incidence, clearance and predictors of human papillomavirus infection in women Cmaj 2003, 168(4):421-425. 143547 12591782
12. Richardson H Abrahamowicz M Tellier PP Kelsall G du Berger R Ferenczy A Coutlee F Franco EL Modifiable risk factors associated with clearance of type-specific cervical human papillomavirus infections in a cohort of university students Cancer Epidemiol Biomarkers Prev 2005, 14(5):1149-1156. 10.1158/1055-9965.EPI-04-0230 15894665
13. Dalstein V Riethmuller D Pretet JL Le Bail Carval K 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 12845680
14. Cuschieri KS Cubie HA Whitley MW Gilkison G Arends MJ Graham C McGoogan E Persistent high risk HPV infection associated with development of cervical neoplasia in a prospective population study J Clin Pathol 2005, 58(9):946-950. 10.1136/jcp.2004.022863 16126875
15. 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 16362994
16. Brummer O Hollwitz B Bohmer G Kuhnle H Petry KU Human papillomavirus-type persistence patterns predict the clinical outcome of cervical intraepithelial neoplasia Gynecol Oncol 2006, 16483642.
17. Smyth MJ Cretney E Kelly JM Westwood JA Street SE Yagita H Takeda K van Dommelen SL Degli-Esposti MA Hayakawa Y Activation of NK cell cytotoxicity Mol Immunol 2005, 42(4):501-510. 10.1016/ j.molimm.2004.07.034 15607806
18. Moretta L Bottino C Pende D Castriconi R Mingari MC Moretta A Surface NK receptors and their ligands on tumor cells Semin Immunol 2006, 18(3):151-158. 10.1016/j.smim.2006.03.002 16730454
19. Glienke J Sobanov Y Brostjan C Steffens C Nguyen C Lehrach H Hofer E Francis F The genomic organization of NKG2C, E, F, and D receptor genes in the human natural killer gene complex Immunogenetics 1998, 48(3):163-173. 10.1007/s002510050420 9683661
20. Jamieson AM Diefenbach A McMahon CW Xiong N Carlyle JR Raulet DH The role of the NKG2D immunoreceptor in immune cell activation and natural killing Immunity 2002, 17(1):19-29. 10.1016/S1074-7613(02)00333-3 12150888
21. 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 11557981
22. 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. 12414645
23. Carbone E Neri P Mesuraca M Fulciniti MT Otsuki T Pende D Groh V Spies T Pollio G Cosman D Catalano L Tassone P Rotoli B Venuta S HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells Blood 2005, 105(1):251-258. 10.1182/ blood-2004-04-1422 15328155
24. Robinson J Perez-Rodriguez M Waller MJ Cuillerier B Bahram S Yao Z Albert ED Madrigal JA Marsh SG MICA sequences 2000 Immunogenetics 2001, 53(2):150-169. 10.1007/s002510100303 11345592
25. Bahram S Bresnahan M Geraghty DE Spies T A second lineage of mammalian major histocompatibility complex class I genes Proc Natl Acad Sci U S A 1994, 91(14):6259-6263. 44180 8022771 10.1073/pnas.91.14.6259
26. 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. 38011 8901601 10.1073/pnas.93.22.12445
27. Vetter CS Groh V thor Straten P Spies T Brocker EB Becker JC Expression of stress-induced MHC class I related chain molecules on human melanoma J Invest Dermatol 2002, 118(4):600-605. 10.1046/j.1523-1747.2002.01700.x 11918705
28. Groh V Rhinehart R Secrist H Bauer S Grabstein KH Spies T Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB Proc Natl Acad Sci U S A 1999, 96(12):6879-6884. 22010 10359807 10.1073/pnas.96.12.6879
29. 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 12569559
30. Watson NF Spendlove I Madjd Z McGilvray R Green AR Ellis IO Scholefield JH Durrant LG Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients Int J Cancer 2006, 118(6):1445-1452. 10.1002/ijc.21510 16184547
31. Pende D Cantoni C Rivera P Vitale M Castriconi R Marcenaro S Nanni M Biassoni R Bottino C Moretta A Moretta L Role of NKG2D in tumor cell lysis mediated by human NK cells: Cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin Eur J Immunol 2001, 31(4):1076-1086. 10.1002/ 1521-4141(200104)31:4<1076::AID-IMMU1076>3.0.CO;2-Y 11298332
32. Moretta A Bottino C Vitale M Pende D Cantoni C Mingari MC Biassoni R Moretta L Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis Annu Rev Immunol 2001. 19:197-223. 10.1146/annurev.immunol.19.1.197 11244035
33. Bauer S Groh V Wu J Steinle A Phillips JH Lanier LL Spies T Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA Science 1999, 285(5428):727-729. 10.1126/science.285.5428.727 10426993
34. Jinushi M Takehara T Tatsumi T Hiramatsu N Sakamori R Yamaguchi S Hayashi N Impairment of natural killer cell and dendritic cell functions by the soluble form of MHC class I-related chain A in advanced human hepatocellular carcinomas J Hepatol 2005, 43(6):1013-1020. 10.1016/ j.jhep.2005.05.026 16168521
35. Doubrovina ES Doubrovin MM Vider E Sisson RB O'Reilly RJ Dupont B Vyas YM Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma J Immunol 2003, 171(12):6891-6899. 14662896
36. Wu JD Higgins LM Steinle A Cosman D Haugk K Plymate SR Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer J Clin Invest 2004, 114(4):560-568. 503776 15314693 10.1172/JCI200422206
37. Holdenrieder S Stieber P Peterfi A Nagel D Steinle A Salih HR Soluble MICA in malignant diseases Int J Cancer 2006, 118(3):684-687. 10.1002/ ijc.21382 16094621
38. Salih HR Antropius H Gieseke F Lutz SZ Kanz L Rammensee HG Steinle A Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia Blood 2003, 102(4):1389-1396. 10.1182/ blood-2003-01-0019 12714493
39. Groh V Wu J Yee C Spies T Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation Nature 2002, 419(6908):734-738. 10.1038/nature01112 12384702
40. Creasman WT New gynecologic cancer staging Gynecol Oncol 1995, 58(2):157-158. 10.1006/gyno.1995.1203 7622099
41. Moore DH Cervical cancer Obstet Gynecol 2006, 107(5):1152-1161. 16648423
42. Solomon D Davey D Kurman R Moriarty A O'Connor D Prey M Raab S Sherman M Wilbur D Wright T Jr. Young N The 2001 Bethesda System: Terminology for reporting results of cervical cytology Jama 2002, 287(16):2114-2119. 10.1001/jama.287.16.2114 11966386
43. Crothers BA The Bethesda System 2001: Update on terminology and application Clin Obstet Gynecol 2005, 48(1):98-107. 10.1097/ 01.grf.0000151572.99437.a5 15725862
44. Salih HR Rammensee HG Steinle A Cutting edge: Down-regulation of MICA on human tumors by proteolytic shedding J Immunol 2002, 169(8):4098-4102. 12370336
45. Daneri-Navarro A Del Toro-Arreola S Bravo-Cuellar A Cabrera N Orbach-Arbouys S Perez-Montfort R Proteolytic activity in extracts of invasive cervical carcinoma and precursor lesions Biomed Pharmacother 1995, 49(6):304-310. 10.1016/0753-3322(96)82648-5 7579013
46. Kaiser BK Yim D Chow IT Gonzalez S Dai Z Mann HH Strong RK Groh V Spies T Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands Nature 2007, 447(7143):482-486. 10.1038/nature05768 17495932
47. Torres LM Cabrera T Concha A Oliva MR Ruiz-Cabello F Garrido F HLA class I expression and HPV-16 sequences in premalignant and malignant lesions of the cervix Tissue Antigens 1993, 41(2):65-71. 8386400
48. Ryu KS Lee YS Kim BK Park YG Kim YW Hur SY Kim TE Kim IK Kim JW Alterations of HLA class I and II antigen expression in preinvasive, invasive and metastatic cervical cancers Exp Mol Med 2001, 33(3):136-144. 11642549
49. Lanier LL NK cell receptors Annu Rev Immunol 1998, 16:359-393. 10.1146/ annurev.immunol.16.1.359 9597134
50. Lanier LL NK cell recognition Annu Rev Immunol 2005, 23:225-274. 10.1146/ annurev.immunol.23.021704.115526 15771571
51. Lee JC Lee KM Kim DW Heo DS Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients J Immunol 2004, 172(12):7335-7340. 15187109
52. Friese MA Wischhusen J Wick W Weiler M Eisele G Steinle A Weller M RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo Cancer Res 2004, 64(20):7596-7603. 10.1158/0008-5472.CAN-04-1627 15492287
53. Tervahauta A Syrjanen S Yliskoski M Gold LI Syrjanen K Expression of transforming growth factor-beta 1 and -beta 2 in human papillomavirus (HPV)-associated lesions of the uterine cervix Gynecol Oncol 1994, 54(3):349-356. 10.1006/gyno.1994.1222 8088612
54. Shier MK Neely EB Ward MG Richards ME Manders EC Meyers C Howett MK Correlation of TGF beta 1 overexpression with down-regulation of proliferation-inducing molecules in HPV-11 transformed human tissue xenografts Anticancer Res 1999, 19(6B):4969-4976. 10697498 sue xenografts
55. Verneris MR Karami M Baker J Jayaswal A Negrin RS Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells Blood 2004, 103(8):3065-3072. 10.1182/blood-2003-06-2125 15070686
56. Allez M Tieng V Nakazawa A Treton X Pacault V Dulphy N Caillat-Zucman S Paul P Gornet JM Douay C Ravet S Tamouza R Charron D Lemann M Mayer L Toubert A CD4+NKG2D+ T cells in Crohn's disease mediate inflammatory and cytotoxic responses through MICA interactions Gastroenterology 2007, 132(7):2346-2358. 10.1053/j.gastro.2007.03.025 17570210
57. Osaki T Saito H Yoshikawa T Matsumoto S Tatebe S Tsujitani S Ikeguchi M Decreased NKG2D expression on CD8+ T cell is involved in immune evasion in patients with gastric cancer Clin Cancer Res 2007, 13(2 Pt 1):382-387. 10.1158/1078-0432.CCR-06-1454 17255258
58. Hunt JS Petroff MG McIntire RH Ober C HLA-G and immune tolerance in pregnancy Faseb J 2005, 19(7):681-693. 10.1096/fj.04-2078rev 15857883
59. Ugurel S Rebmann V Ferrone S Tilgen W Grosse-Wilde H Reinhold U Soluble human leukocyte antigen--G serum level is elevated in melanoma patients and is further increased by interferon-alpha immunotherapy Cancer 2001, 92(2):369-376. 10.1002/ 1097-0142(20010715)92:2<369::AID-CNCR1332>3.0.CO;2-U 11466692
60. Rebmann V Regel J Stolke D Grosse-Wilde H Secretion of sHLA-G molecules in malignancies Semin Cancer Biol 2003, 13(5):371-377. 10.1016/ S1044-579X(03)00028-2 14708717
61. Morandi F Levreri I Bocca P Galleni B Raffaghello L Ferrone S Prigione I Pistoia V Human neuroblastoma cells trigger an immunosuppressive program in monocytes by stimulating soluble HLA-G release Cancer Res 2007, 67(13):6433-6441. 10.1158/0008-5472.CAN-06-4588 17616704
62. Fournel S Aguerre-Girr M Huc X Lenfant F Alam A Toubert A Bensussan A Le Bouteiller P Cutting edge: Soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8 J Immunol 2000, 164(12):6100-6104. 10843658
63. Contini P Ghio M Poggi A Filaci G Indiveri F Ferrone S Puppo F Soluble HLA-A,-B,-C and -G molecules induce apoptosis in T and NK CD8+ cells and inhibit cytotoxic T cell activity through CD8 ligation Eur J Immunol 2003, 33(1):125-134; 10.1002/immu.200390015 12594841