213
Views
3
CrossRef citations to date
0
Altmetric
Review

HLA-G expression in melanomas

ORCID Icon, , , , , , & show all
Pages 330-343 | Received 02 Nov 2020, Accepted 21 Dec 2020, Published online: 11 Jan 2021

References

  • Kovats S, Main EK, Librach C, et al. A. class I antigen, HLA-G, expressed in human trophoblasts. Science. 1990;248(4952):220–223. doi:10.1126/science.2326636.
  • Lin A, Yan WH. Heterogeneity of HLA-G expression in cancers: facing the challenges. Front Immunol. 2018;9:2164 doi:10.3389/fimmu.2018.02164.
  • Dahl M, Hviid TVF. Human leucocyte antigen class Ib molecules in pregnancy success and early pregnancy loss. Hum Reprod Update. 2012;18(1):92–109. doi:10.1093/humupd/dmr043.
  • Ferreira LMR, Meissner TB, Tilburgs T, et al. HLA-G: At the interface of maternal-fetal tolerance. Trends Immunol. 2017;38(4):272–286. doi:10.1016/j.it.2017.01.009.
  • Le Gal FA, Riteau B, Sedlik C, et al. HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes. Int Immunol. 1999;11(8):1351–1356. doi:10.1093/intimm/11.8.1351.
  • Selmani Z, Naji A, Zidi I, et al. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4 + CD25highFOXP3+ regulatory T cells. Stem Cells. 2008;26(1):212–222. doi:10.1634/stemcells.2007-0554.
  • González A, Rebmann V, LeMaoult J, et al. The immunosuppressive molecule HLA-G and its clinical implications. Crit Rev Clin Lab Sci. 2012;49(3):63–84. doi:10.3109/10408363.2012.677947.
  • da Silva GBRF, Silva TGA, Duarte RA, et al. Expression of the classical and nonclassical HLA molecules in breast cancer. Int J Breast Cancer. 2013;2013:250435). doi:10.1155/2013/250435.
  • Ye S-R, Yang H, Li K, et al. Human leukocyte antigen G expression: as a significant prognostic indicator for patients with colorectal cancer. Mod Pathol. 2007;20(3):375–383. doi:10.1038/modpathol.3800751.
  • Yie S-M, Yang H, Ye S-R, et al. Expression of HLA-G is associated with prognosis in esophageal squamous cell carcinoma. Am J Clin Pathol. 2007;128(6):1002–1009. doi:10.1309/JNCW1QLDFB6AM9WE.
  • Du L, Xiao X, Wang C, et al. Human leukocyte antigen-G is closely associated with tumor immune escape in gastric cancer by increasing local regulatory T cells. Cancer Sci. 2011;102(7):1272–1280. doi:10.1111/j.1349-7006.2011.01951.x.
  • Wang Y, Ye Z, Meng X-Q, et al. Expression of HLA-G in patients with hepatocellular carcinoma. Hepatobiliary Pancreat. Dis. Int. 2011;10(2):158–163. doi:10.1016/S1499-3872(11)60025-8.
  • Li X-J, Zhang X, Lin A, et al. Human leukocyte antigen-G (HLA-G) expression in cervical cancer lesions is associated with disease progression. Hum Immunol. 2012;73(9):946–949. doi:10.1016/j.humimm.2012.07.041.
  • Bijen CBM, Bantema-Joppe EJ, de Jong RA, et al. The prognostic role of classical and nonclassical MHC class I expression in endometrial cancer. Int J Cancer. 2010;126(6):1417–1427. doi:10.1002/ijc.24852.
  • Menier C, Prevot S, Carosella ED, et al. Human leukocyte antigen-G is expressed in advanced-stage ovarian carcinoma of high-grade histology. Hum Immunol. 2009;70(12):1006–1009. doi:10.1016/j.humimm.2009.07.021.
  • Wastowski IJ, Simões RT, Yaghi L, et al. Human leukocyte antigen-G is frequently expressed in glioblastoma and may be induced in vitro by combined 5-aza-2'-deoxycytidine and interferon-γ treatments: results from a multicentric study . Am J Pathol. 2013;182(2):540–552. doi:10.1016/j.ajpath.2012.10.021.
  • Spurny C, Kailayangiri S, Altvater B, et al. T cell infiltration into Ewing sarcomas is associated with local expression of immune-inhibitory HLA-G. Oncotarget. 2018;9(5):6536–6549. doi:10.18632/oncotarget.23815.
  • Caocci G, Greco M, Fanni D, et al. G, HLA-G expression and role in advanced-stage classical Hodgkin lymphoma. Eur J Histochem. 2016;60(2):2606 doi:10.4081/ejh.2016.2606.
  • Sukari A, Nagasaka M, Al-Hadidi A, et al. Cancer Immunology and Immunotherapy. Anticancer Res. 2016;36(11):5593–5606. doi:10.21873/anticanres.11144.
  • Rodig SJ, Gusenleitner D, Jackson DG, et al. MHC proteins confer differential sensitivity to CTLA-4 and PD-1 blockade in untreated metastatic melanoma. Sci Transl Med. 2018;10(450):eaar3342. doi:10.1126/scitranslmed.aar3342.
  • Ruiter DJ, Bergman W, Welvaart K, et al. Immunohistochemical analysis of malignant melanomas and nevocellular nevi with monoclonal antibodies to distinct monomorphic determinants of HLA antigens. Cancer Res. 1984;44(9):3930–3935.
  • Bröcker EB, Suter L, Brüggen J, et al. Phenotypic dynamics of tumor progression in human malignant melanoma. Int J Cancer. 1985;36(1):29–35. doi:10.1002/ijc.2910360106.
  • Ruiter DJ, Mattijssen V, Broecker EB, Ferrone S. MHC antigens in human melanomas. Semin Cancer Biol. 1991;2(1):35–45.
  • Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700 doi:10.1136/bmj.b2700.
  • Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–2012. doi:10.1001/jama.283.15.2008.
  • Ouzzani M, Hammady H, Fedorowicz Z, et al. Rayyan-a web and mobile app for systematic reviews. Syst Rev. 2016;5(1):210 doi:10.1186/s13643-016-0384-4.
  • Munn Z, Barker TH, Moola S, et al. Methodological quality of case series studies: an introduction to the JBI critical appraisal tool. JBI Evid Synth. 2020;18(10):2127–2133. doi:10.11124/JBISRIR-D-19-00099.
  • Paul P, Rouas-Freiss N, Khalil-Daher I, et al. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci U S A. 1998;95(8):4510–4515. doi:10.1073/pnas.95.8.4510.
  • Paul P, Cabestré FA, Le Gal FA, et al. Heterogeneity of HLA-G gene transcription and protein expression in malignant melanoma biopsies. Cancer Res. 1999;59(8):1954–1960.,
  • Rebmann V, Wagner S, Grosse-Wilde H. HLA-G expression in malignant melanoma. Semin Cancer Biol. 2007;17(6):422–429. doi:10.1016/j.semcancer.2007.06.010.
  • Bezuhly M, Howlett A, Colp P, et al. Quantitative HLA-G expression in metastasising and non-metastasising primary thin cutaneous melanomas. Dermatology. 2008;217(3):281–283. doi:10.1159/000150602.
  • Fang X, Zhang X, Li J. Up-regulation of human leukocyte antigen G expression in primary cutaneous malignant melanoma associated with host-vs-tumor immune response. J Huazhong Univ Sci Technolog Med Sci. 2008;28(2):219–221. doi:10.1007/s11596-008-0227-1.
  • Castillo MZ, Pereira NV, Guedes F, et al. Overexpression of Human Leukocyte Antigen-G and Interleukin 10 in acral lentiginous melanoma. J Dermatol Sci. 2017;88(1):149–152. doi:10.1016/j.jdermsci.2017.05.014.
  • Melsted WN, Johansen LL, Lock-Andersen J, et al. HLA class Ia and Ib molecules and FOXP3+ TILs in relation to the prognosis of malignant melanoma patients. Clin. Immunol. 2017;183:191–197. doi:10.1016/j.clim.2017.09.004.
  • van Weeghel C, Wierenga APA, Versluis M, et al. Do GNAQ and GNA11 Differentially Affect Inflammation and HLA Expression in Uveal Melanoma? Cancers (Basel). 2019;11(8):1127. doi:10.3390/cancers11081127.
  • Real LM, Cabrera T, Collado A, et al. Expression of HLA G in human tumors is not a frequent event. Int J Cancer. 1999;81(4):512–518. doi:10.1002/(SICI)1097-0215(19990517)81:4<512::AID-IJC2>3.0.CO;2-O.
  • Frumento G, Franchello S, Palmisano GL, et al. Melanomas and melanoma cell lines do not express HLA-G, and the expression cannot be induced by gammaIFN treatment. Tissue Antigens. 2000;56(1):30–37. doi:10.1034/j.1399-0039.2000.560104.x.
  • Wagner SN, Rebmann V, Willers CP, et al. Expression analysis of classic and non-classic HLA molecules before interferon alfa-2b treatment of melanoma. Lancet (London, England. 2000;356(9225):220–221. doi:10.1016/S0140-6736(00)02486-7.
  • Ugurel S, Rebmann V, Ferrone S, et al. 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. doi:10.1002/1097-0142(20010715)92:2<369::AID-CNCR1332>3.0.CO;2-U.
  • Hurks HM, Valter MM, Wilson L, et al. Uveal melanoma: no expression of HLA-G. Invest Ophthalmol Vis Sci. 2001;42(13):3081–3084.
  • Davies B, Hiby S, Gardner L, et al. HLA-G expression by tumors. Am J Reprod Immunol. 2001;45(2):103–107. doi:10.1111/j.8755-8920.2001.450207.x.
  • Anastassiou G, Rebmann V, Wagner S, et al. Expression of classic and nonclassic HLA class I antigens in uveal melanoma. Invest Ophthalmol Vis Sci. 2003;44(5):2016–2019. doi:10.1167/iovs.02-0810.
  • Ibrahim EC, Aractingi S, Allory Y, et al. Analysis of HLA antigen expression in benign and malignant melanocytic lesions reveals that upregulation of HLA-G expression correlates with malignant transformation, high inflammatory infiltration and HLA-A1 genotype. Int J Cancer. 2004;108(2):243–250. doi:10.1002/ijc.11456.
  • Yu Y, Wang Y, Feng M. Human leukocyte antigen-G1 inhibits natural killer cytotoxicity through blocking the activating signal transduction pathway and formation of activating immunologic synapse. Hum Immunol. 2008;69(1):16–23. doi:10.1016/j.humimm.2007.11.005.
  • Ketroussi F, Giuliani M, Bahri R, et al. Lymphocyte cell-cycle inhibition by HLA-G is mediated by phosphatase SHP-2 and acts on the mTOR pathway. PLoS One. 2011;6(8):e22776 doi:10.1371/journal.pone.0022776.
  • Lin A, Yan W-H, Xu H-H, et al. HLA-G expression in human ovarian carcinoma counteracts NK cell function. Ann Oncol Off J Eur Soc Med Oncol. 2007;18(11):1804–1809. doi:10.1093/annonc/mdm356.
  • Wiendl H, Mitsdoerffer M, Hofmeister V, et al. A functional role of HLA-G expression in human gliomas: an alternative strategy of immune escape. J Immunol. 2002;168(9):4772–4780. doi:10.4049/jimmunol.168.9.4772.
  • Carosella ED, Gregori S, Rouas-Freiss N, et al. The role of HLA-G in immunity and hematopoiesis. Cell Mol Life Sci. 2011;68(3):353–368. doi:10.1007/s00018-010-0579-0.
  • Moretta A, Bottino C, Vitale M, et al. Receptors for HLA class-I molecules in human natural killer cells. Annu Rev Immunol. 1996;14:619–648. doi:10.1146/annurev.immunol.14.1.619.
  • Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science. 2011;331(6024):1565–1570. doi:10.1126/science.1203486.
  • Johansen LL, Lock-Andersen J, Hviid TVF. The Pathophysiological Impact of HLA Class Ia and HLA-G Expression and Regulatory T Cells in Malignant Melanoma: A Review. J Immunol Res. 2016;2016:6829283. 2016, ). doi:10.1155/2016/6829283.
  • Chae YK, Arya A, Iams W, et al. Current landscape and future of dual anti-CTLA4 and PD-1/PD-L1 blockade immunotherapy in cancer; lessons learned from clinical trials with melanoma and non-small cell lung cancer (NSCLC). J Immunother Cancer. 2018;6(1):39 doi:10.1186/s40425-018-0349-3.
  • Onitilo AA, Wittig JA. Principles of Immunotherapy in Melanoma. Surg Clin North Am. 2020;100(1):161–173. doi:10.1016/j.suc.2019.09.009.
  • Chowdhury PS, Chamoto K, Honjo T. Combination therapy strategies for improving PD-1 blockade efficacy: a new era in cancer immunotherapy. J Intern Med. 2018;283(2):110–120. doi:10.1111/joim.12708.
  • Patel SA, Minn AJ. Combination Cancer Therapy with Immune Checkpoint Blockade: Mechanisms and Strategies. Immunity. 2018;48(3):417–433. doi:10.1016/j.immuni.2018.03.007.
  • Carretero R, Romero JM, Ruiz-Cabello F, et al. Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics. 2008;60(8):439–447. doi:10.1007/s00251-008-0303-5.
  • Chang C, Murphy SP, Ferrone S. Differential In Vivo and In Vitro HLA-G Expression in Melanoma Cells: Potential Mechanisms. 2003;64(11):1057–1063. doi:10.1016/j.humimm.2003.08.357
  • Rouas-Freiss N, Bruel S, Menier C, et al. Switch of HLA-G alternative splicing in a melanoma cell line causes loss of HLA-G1 expression and sensitivity to NK lysis. Int J Cancer. 2005;117(1):114–122. doi:10.1002/ijc.21151.
  • Pangault C, Amiot L, Caulet-Maugendre S, et al. HLA-G protein expression is not induced during malignant transformation. Tissue Antigens. 1999;53(4 Pt 1):335–346. doi:10.1034/j.1399-0039.1999.530403.x.
  • Apps R, Gardner L, Moffett A. A critical look at HLA-G. Trends Immunol. 2008;29(7):313–321. doi:10.1016/j.it.2008.02.012.
  • Swets M, Wouters A, Krijgsman D, et al. HLA-G protein expression in colorectal cancer evaluated by immunohistochemistry and western blot analysis: Its expression characteristics remain enigmatic. Clin Immunol. 2018;194:80–86. doi:10.1016/j.clim.2018.07.005.
  • Lin A, Chen H-X, Zhu C-C, et al. Aberrant human leucocyte antigen-G expression and its clinical relevance in hepatocellular carcinoma. J Cell Mol Med. 2010;14(8):2162–2171. doi:10.1111/j.1582-4934.2009.00917.x.
  • Vacca P, Pietra G, Tumino N, et al. Exploiting Human NK Cells in Tumor Therapy. Front Immunol. 2019;10:3013 doi:10.3389/fimmu.2019.03013.
  • Cortés-Hernández A, Alvarez-Salazar EK, Soldevila G. Chimeric Antigen Receptor (CAR) T Cell Therapy for Cancer. Challenges and Opportunities: An Overview. Methods Mol Biol. 2021;2174:219–244. doi:10.1007/978-1-0716-0759-6_14.
  • Wang Z, Wu Z, Liu Y, et al. New development in CAR-T cell therapy. J Hematol Oncol. 2017;10(1):53 doi:10.1186/s13045-017-0423-1.
  • Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507–1517. doi:10.1056/NEJMoa1407222.
  • Kalos M, Levine BL, Porter DL, et al. T. cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3(95):95ra73 doi:10.1126/scitranslmed.3002842.
  • Massa C, Seliger B. The tumor microenvironment: Thousand obstacles for effector T cells. Cell Immunol. 2019;343:103730 doi:10.1016/j.cellimm.2017.12.004.
  • Simon B, Uslu U. CAR-T cell therapy in melanoma: A future success story? Exp Dermatol. 2018;27(12):1315–1321. doi:10.1111/exd.13792.
  • Kailayangiri S, Altvater B, Spurny C, et al. Targeting Ewing sarcoma with activated and GD2-specific chimeric antigen receptor-engineered human NK cells induces upregulation of immune-inhibitory HLA-G. Oncoimmunology. 2017;6(1):e1250050. doi:10.1080/2162402X.2016.1250050.
  • Blom DJ, Luyten GP, Mooy C, et al. Human leukocyte antigen class I expression. Marker of poor prognosis in uveal melanoma. Invest Ophthalmol Vis Sci. 1997;38(9):1865–1872.
  • Blom DJ, Schurmans LR, De Waard-Siebinga I, et al. HLA expression in a primary uveal melanoma, its cell line, and four of its metastases. Br J Ophthalmol. 1997;81(11):989–993. doi:10.1136/bjo.81.11.989.
  • Zierhut M, Streilein JW, Schreiber H, et al. Immunology of ocular tumours. Immunol Today. 1999;20(11):482–485. doi:10.1016/S0167-5699(99)01513-3.
  • O’Callaghan CA. Molecular basis of human natural killer cell recognition of HLA-E (human leucocyte antigen-E) and its relevance to clearance of pathogen-infected and tumour cells. Clin Sci. (Lond). 2000;99(1):9–17. doi:10.1042/CS19990334.
  • Repp AC, Mayhew ES, Apte S, et al. Human uveal melanoma cells produce macrophage migration-inhibitory factor to prevent lysis by NK cells. J Immunol. 2000;165(2):710–715. doi:10.4049/jimmunol.165.2.710.
  • Apte RS, Mayhew E, Niederkorn JY. Local inhibition of natural killer cell activity promotes the progressive growth of intraocular tumors. Invest Ophthalmol Vis Sci. 1997;38(6):1277–1282.
  • Apte RS, Sinha D, Mayhew E, et al. Cutting edge: role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege. J Immunol. 1998;160(12):5693–5696.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.