The role of HLA-G in gastrointestinal inflammatory disease and malignancy

Seminars in Cancer Biology

Volumn 17, Issue 6, 2007, Pages 451-458

  Downs Kelly, Erinn ^a   Schade, Andrew E ^a   Hansel, Donna E ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Adenoma; Carcinoma; Colon; Gastrointestinal tract; HLA G; Inflammatory bowel disease; Pancreas

Indexed keywords

HLA G ANTIGEN;

ANTIGEN EXPRESSION; ANTIGEN FUNCTION; BILE DUCT CARCINOMA; CANCER GRADING; CANCER RISK; CANCER SURVIVAL; COLON ADENOMA; COLORECTAL CARCINOMA; CROHN DISEASE; DIGESTIVE SYSTEM CANCER; DIGESTIVE SYSTEM INFLAMMATION; ENTERITIS; GASTROINTESTINAL CARCINOMA; GASTROINTESTINAL TRACT; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MELANOMA; NATURAL KILLER CELL; PANCREAS ADENOCARCINOMA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RNA TRANSCRIPTION; STOMACH CARCINOMA; ULCERATIVE COLITIS;

CARCINOMA; GASTROINTESTINAL NEOPLASMS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; INFLAMMATORY BOWEL DISEASES; TUMOR ESCAPE;

EID: 35948974320     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2007.07.002     Document Type: Review

References (72)

1. Kovats S., Main E.K., Librach C., Stubblebine M., Fisher S.J., and DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 248 4952 (1990) 220-223
2. Ellis S.A., Palmer M.S., and McMichael A.J. Human trophoblast and the choriocarcinoma cell line BeWo express a truncated HLA Class I molecule. J Immunol 144 2 (1990) 731-735
3. Rouas-Freiss N., Goncalves R.M., Menier C., Dausset J., and Carosella E.D.D. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci USA 94 21 (1997) 11520-11525
4. King A., Hiby S.E., Verma S., Burrows T., Gardner L., and Loke Y.W. Uterine NK cells and trophoblast HLA class I molecules. Am J Reprod Immunol 37 6 (1997) 459-462
5. Crisa L., McMaster M.T., Ishii J.K., Fisher S.J., and Salomon D.R. Identification of a thymic epithelial cell subset sharing expression of the class Ib HLA-G molecule with fetal trophoblasts. J Exp Med 186 2 (1997) 289-298
6. Le Discorde M., Moreau P., Sabatier P., Legeais J.M., and Carosella E.D. Expression of HLA-G in human cornea, an immune-privileged tissue. Hum Immunol 64 11 (2003) 1039-1044
7. Ito T., Ito N., Saathoff M., Stampachiacchiere B., Bettermann A., Bulfone-Paus S., et al. Immunology of the human nail apparatus: the nail matrix is a site of relative immune privilege. J Invest Dermatol 125 6 (2005) 1139-1148
8. Carosella E.D., Paul P., Moreau P., and Rouas-Freiss N. HLA-G and HLA-E: fundamental and pathophysiological aspects. Immunol Today 21 11 (2000) 532-534
9. Carosella E.D., Rouas-Freiss N., Paul P., and Dausset J. HLA-G: a tolerance molecule from the major histocompatibility complex. Immunol Today 20 2 (1999) 60-62
10. Rouas-Freiss N., Marchal R.E., Kirszenbaum M., Dausset J., and Carosella E.D. The alpha1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors?. Proc Natl Acad Sci USA 94 10 (1997) 5249-5254
11. Le Gal F.A., Riteau B., Sedlik C., Khalil-Daher I., Menier C., Dausset J., et al. HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes. Int Immunol 11 8 (1999) 1351-1356
12. Rouas-Freiss N., Khalil-Daher I., Riteau B., Menier C., Paul P., Dausset J., et al. The immunotolerance role of HLA-G. Semin Cancer Biol 9 1 (1999) 3-12
13. Marchal-Bras-Goncalves R., Rouas-Freiss N., Connan F., Choppin J., Dausset J., Carosella E.D., et al. A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity. Transplant Proc 33 3 (2001) 2355-2359
14. Lopez-Botet M., Navarro F., and Llano M. How do NK cells sense the expression of HLA-G class Ib molecules?. Semin Cancer Biol 9 1 (1999) 19-26
15. Colonna M., Navarro F., Bellon T., Llano M., Garcia P., Samaridis J., et al. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J Exp Med 186 11 (1997) 1809-1818
16. Saverino D., Fabbi M., Ghiotto F., Merlo A., Bruno S., Zarcone D., et al. The CD85/LIR-1/ILT2 inhibitory receptor is expressed by all human T lymphocytes and down-regulates their functions. J Immunol 165 7 (2000) 3742-3755
17. Ponte M., Cantoni C., Biassoni R., Tradori-Cappai A., Bentivoglio G., Vitale C., et al. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc Natl Acad Sci USA 96 10 (1999) 5674-5679
18. Rajagopalan S., and Long E.O. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 189 7 (1999) 1093-1100
19. Carosella E.D., Moreau P., Le Maoult J., Le Discorde M., Dausset J., and Rouas-Freiss N. HLA-G molecules: from maternal-fetal tolerance to tissue acceptance. Adv Immunol 81 (2003) 199-252
20. Bainbridge D.R., Ellis S.A., and Sargent I.L. HLA-G suppresses proliferation of CD4(+) T-lymphocytes. J Reprod Immunol 48 1 (2000) 17-26
21. Lila N., Rouas-Freiss N., Dausset J., Carpentier A., and Carosella E.D. Soluble HLA-G protein secreted by allo-specific CD4+ T cells suppresses the allo-proliferative response: a CD4+ T cell regulatory mechanism. Proc Natl Acad Sci USA 98 21 (2001) 12150-12155
22. Le Rond S., Azema C., Krawice-Radanne I., Durrbach A., Guettier C., Carosella E.D., et al. Evidence to support the role of HLA-G5 in allograft acceptance through induction of immunosuppressive/regulatory T cells. J Immunol 176 5 (2006) 3266-3276
23. Riteau B., Menier C., Khalil-Daher I., Sedlik C., Dausset J., Rouas-Freiss N., et al. HLA-G inhibits the allogeneic proliferative response. J Reprod Immunol 43 2 (1999) 203-211
24. LeMaoult J., Krawice-Radanne I., Dausset J., and Carosella E.D. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc Natl Acad Sci USA 101 18 (2004) 7064-7069
25. Fournel S., Aguerre-Girr M., Huc X., Lenfant F., Alam A., Toubert A., et al. Cutting edge: soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8. J Immunol 164 12 (2000) 6100-6104
26. Braud V.M., Allan D.S., O'Callaghan C.A., Soderstrom K., D'Andrea A., Ogg G.S., et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391 6669 (1998) 795-799
27. LeMaoult J., Caumartin J., Daouya M., Favier B., Le Rond S., Gonzalez A., et al. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood 109 5 (2007) 2040-2048
28. Caumartin J., Favier B., Daouya M., Guillard C., Moreau P., Carosella E.D., et al. Trogocytosis-based generation of suppressive NK cells. Embo J 26 5 (2007) 1423-1433
29. Moreau P., Adrian-Cabestre F., Menier C., Guiard V., Gourand L., Dausset J., et al. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int Immunol 11 5 (1999) 803-811
30. Urosevic M., Willers J., Mueller B., Kempf W., Burg G., and Dummer R. HLA-G protein up-regulation in primary cutaneous lymphomas is associated with interleukin-10 expression in large cell T-cell lymphomas and indolent B-cell lymphomas. Blood 99 2 (2002) 609-617
31. Moore K.W., de Waal Malefyt R., Coffman R.L., and O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19 (2001) 683-765
32. Ding Y.H., Fu S., Zamarin D., and Bromberg J. Interleukin-10. In: Thompson A.W., and Lotze M.T. (Eds). The cytokine handbook. 4th ed. (2003), Elsevier Science 603-625
33. Bernstein C.N., Blanchard J.F., Kliewer E., and Wajda A. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer 91 4 (2001) 854-862
34. Brandtzaeg P.H.G., Helgeland L., Nilsen E.M., and Rugtveit J. New insights into the immunopathology of human inflammatory bowel disease. Drugs Today 35 Suppl. A (1999) 33
35. Fiocchi C. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115 1 (1998) 182-205
36. Elson C.O. Commensal bacteria as targets in Crohn's disease. Gastroenterology 119 1 (2000) 254-257
37. Stallmach A., Strober W., MacDonald T.T., Lochs H., and Zeitz M. Induction and modulation of gastrointestinal inflammation. Immunol Today 19 10 (1998) 438-441
38. Shanahan F. Inflammatory bowel disease: immunodiagnostics, immunotherapeutics, and ecotherapeutics. Gastroenterology 120 3 (2001) 622-635
39. Dohi T., Fujihashi K., Rennert P.D., Iwatani K., Kiyono H., and McGhee J.R. Hapten-induced colitis is associated with colonic patch hypertrophy and T helper cell 2-type responses. J Exp Med 189 8 (1999) 1169-1180
40. Torres M.I., Le Discorde M., Lorite P., Rios A., Gassull M.A., Gil A., et al. Expression of HLA-G in inflammatory bowel disease provides a potential way to distinguish between ulcerative colitis and Crohn's disease. Int Immunol 16 4 (2004) 579-583
41. Dinarello C.A. Proinflammatory cytokines. Chest 118 2 (2000) 503-508
42. Opal S.M., and DePalo V.A. Anti-inflammatory cytokines. Chest 117 4 (2000) 1162-1172
43. Carosella E.D., Moreau P., Aractingi S., and Rouas-Freiss N. HLA-G: a shield against inflammatory aggression. Trends Immunol 22 10 (2001) 553-555
44. Paul P., Rouas-Freiss N., Khalil-Daher I., Moreau P., Riteau B., Le Gal F.A., et al. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci USA 95 8 (1998) 4510-4515
45. Paul P., Cabestre F.A., Le Gal F.A., Khalil-Daher I., Le Danff C., Schmid M., et al. Heterogeneity of HLA-G gene transcription and protein expression in malignant melanoma biopsies. Cancer Res 59 8 (1999) 1954-1960
46. Aractingi S., Kanitakis J., Euvrard S., Le Danff C., and Carosella E.D. Selective expression of HLA-G in malignant and premalignant skin specimens in kidney transplant recipients. Int J Cancer 106 2 (2003) 232-235
47. Ibrahim E.C., Guerra N., Lacombe M.J., Angevin E., Chouaib S., Carosella E.D., et al. Tumor-specific up-regulation of the nonclassical class I HLA-G antigen expression in renal carcinoma. Cancer Res 61 18 (2001) 6838-6845
48. Bukur J., Rebmann V., Grosse-Wilde H., Luboldt H., Ruebben H., Drexler I., et al. Functional role of human leukocyte antigen-G up-regulation in renal cell carcinoma. Cancer Res 63 14 (2003) 4107-4111
49. Bukur J., Malenica B., Huber C., and Seliger B. Altered expression of nonclassical HLA class Ib antigens in human renal cell carcinoma and its association with impaired immune response. Hum Immunol 64 11 (2003) 1081-1092
50. Ibrahim el C., Allory Y., Commo F., Gattegno B., Callard P., and Paul P. Altered pattern of major histocompatibility complex expression in renal carcinoma: tumor-specific expression of the nonclassical human leukocyte antigen-G molecule is restricted to clear cell carcinoma while up-regulation of other major histocompatibility complex antigens is primarily distributed in all subtypes of renal carcinoma. Am J Pathol 162 2 (2003) 501-508
51. Urosevic M., Kurrer M.O., Kamarashev J., Mueller B., Weder W., Burg G., 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 159 3 (2001) 817-824
52. Lefebvre S., Antoine M., Uzan S., McMaster M., Dausset J., Carosella E.D., et al. Specific activation of the non-classical class I histocompatibility HLA-G antigen and expression of the ILT2 inhibitory receptor in human breast cancer. J Pathol 196 3 (2002) 266-274
53. Davidson B., Risberg B., Berner A., Bedrossian C.W., and Reich R. The biological differences between ovarian serous carcinoma and diffuse peritoneal malignant mesothelioma. Semin Diagn Pathol 23 1 (2006) 35-43
54. El-Chennawi F.A., Auf F.A., El-Diasty A.M., El-Daim M.A., El-Sherbiny S.M., Ali A., et al. Expression of HLA-G in cancer bladder. Egypt J Immunol 12 1 (2005) 57-64
55. Hansel D.E., Rahman A., Wilentz R.E., Shih Ie M., McMaster M.T., Yeo C.J., et al. HLA-G upregulation in pre-malignant and malignant lesions of the gastrointestinal tract. Int J Gastrointest Cancer 35 1 (2005) 15-23
56. Fukushima Y., Oshika Y., Nakamura M., Tokunaga T., Hatanaka H., Abe Y., et al. Increased expression of human histocompatibility leukocyte antigen-G in colorectal cancer cells. Int J Mol Med 2 3 (1998) 349-351
57. Ye S.R., Yang H., Li K., Dong D.D., Lin X.M., and Yie S.M. Human leukocyte antigen G expression: as a significant prognostic indicator for patients with colorectal cancer. Mod Pathol 20 3 (2007) 375-383
58. Barrier B.F., Kendall B.S., Sharpe-Timms K.L., and Kost E.R. Characterization of human leukocyte antigen-G (HLA-G) expression in endometrial adenocarcinoma. Gynecol Oncol 103 1 (2006) 25-30
59. Rouas-Freiss N., Moreau P., Ferrone S., and Carosella E.D. HLA-G proteins in cancer: do they provide tumor cells with an escape mechanism?. Cancer Res 65 22 (2005) 10139-10144
60. Malmberg K.J., Levitsky V., Norell H., de Matos C.T., Carlsten M., Schedvins K., et al. IFN-gamma protects short-term ovarian carcinoma cell lines from CTL lysis via a CD94/NKG2A-dependent mechanism. J Clin Invest 110 10 (2002) 1515-1523
61. Hurks H.M., Valter M.M., Wilson L., Hilgert I., van den Elsen P.J., and Jager M.J. Uveal melanoma: no expression of HLA-G. Invest Ophthalmol Vis Sci 42 13 (2001) 3081-3084
62. Singer G., Kurman R.J., McMaster M.T., and Shih Ie M. HLA-G immunoreactivity is specific for intermediate trophoblast in gestational trophoblastic disease and can serve as a useful marker in differential diagnosis. Am J Surg Pathol 26 7 (2002) 914-920
63. Rebmann V., Regel J., Stolke D., and Grosse-Wilde H. Secretion of sHLA-G molecules in malignancies. Semin Cancer Biol 13 5 (2003) 371-377
64. Ugurel S., Rebmann V., Ferrone S., Tilgen W., Grosse-Wilde H., and Reinhold U. Soluble human leukocyte antigen-G serum level is elevated in melanoma patients and is further increased by interferon-alpha immunotherapy. Cancer 92 2 (2001) 369-376
65. Leelawat K., Engprasert S., Pongchai-rerk U., Tuchinda S., Suthipintawong C., and Leardkamolkarn V. No expression of human leukocyte antigen G (HLA-G) in colorectal cancer cells. J Med Assoc Thai 87 7 (2004) 816-818
66. Dutta N., Majumder D., Gupta A., Mazumder D.N., and Banerjee S. Analysis of human lymphocyte antigen class I expression in gastric cancer by reverse transcriptase-polymerase chain reaction. Hum Immunol 66 2 (2005) 164-169
67. Ishigami S., Natsugoe S., Miyazono F., Nakajo A., Tokuda K., Matsumoto M., et al. HLA-G expression in gastric cancer. Anticancer Res 26 3B (2006) 2467-2472
68. Ishigami S., Natsugoe S., Tokuda K., Nakajo A., Che X., Iwashige H., et al. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 88 3 (2000) 577-583
69. Yie S.M., Yang H., Ye S.R., Li K., Dong D.D., and Lin X.M. Expression of human leukocyte antigen G (HLA-G) correlates with poor prognosis in gastric carcinoma. Ann Surg Oncol (2007)
70. Bodger K., Bromelow K., Wyatt J.I., and Heatley R.V. Interleukin 10 in Helicobacter pylori associated gastritis: immunohistochemical localisation and in vitro effects on cytokine secretion. J Clin Pathol 54 4 (2001) 285-292
71. Bodger K., and Crabtree J.E. Helicobacter pylori and gastric inflammation. Br Med Bull 54 1 (1998) 139-150
72. Bodger K., Wyatt J.I., and Heatley R.V. Gastric mucosal secretion of interleukin-10: relations to histopathology, Helicobacter pylori status, and tumour necrosis factor-alpha secretion. Gut 40 6 (1997) 739-744