Identification of novel microRNAs regulating HLA-G expression and investigating their clinical relevance in renal cell carcinoma

Oncotarget

Volumn 7, Issue 18, 2016, Pages 26866-26878

  Jasinski Bergner, Simon ^a   Reches, Adi ^b   Stoehr, Christine ^c   Massa, Chiara ^a   Gonschorek, Evamaria ^a   Huettelmaier, Stefan ^a   Braun, Juliane ^a   Wach, Sven ^c   Wullich, Bernd ^c   Spath, Verena ^b   Wang, Ena ^d   Marincola, Francesco M ^d   Mandelboim, Ofer ^b   Hartmann, Arndt ^c   Seliger, Barbara ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

Author keywords

HLA G; Immune escape; microRNA; Non classical HLA class I molecules; Renal cell carcinoma

Indexed keywords

HLA G ANTIGEN; MESSENGER RNA; MICRORNA; MICRORNA 548Q; MICRORNA 628-5P; UNCLASSIFIED DRUG; MIRN548 MICRORNA, HUMAN; MIRN628 MICRORNA, HUMAN; TRANSCRIPTOME; TUMOR MARKER;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EFFECTOR CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KIDNEY CARCINOMA; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; POLYMERASE CHAIN REACTION; RENAL CELL CARCINOMA CELL LINE; BIOSYNTHESIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; KIDNEY TUMOR; METABOLISM; RENAL CELL CARCINOMA;

BIOMARKERS, TUMOR; CARCINOMA, RENAL CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HLA-G ANTIGENS; HUMANS; KIDNEY NEOPLASMS; MICRORNAS; TRANSCRIPTOME;

EID: 84967329187     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8567     Document Type: Article

References (53)

1. Bukur J, Jasinski S and Seliger B. The role of classical and non-classical HLA class I antigens in human tumors. Semin Cancer Biol. 2012; 22:350-358.
2. Shiroishi M, Tsumoto K, Amano K, Shirakihara Y, Colonna M, Braud VM, Allan DS, Makadzange A, Rowland-Jones S, Willcox B, Jones EY, van der Merwe PA, Kumagai I and Maenaka K. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci U S A. 2003; 100:8856-8861.
3. Zhao L, Purandare B, Zhang J and Hantash BM. beta2-Microglobulin-free HLA-G activates natural killer cells by increasing cytotoxicity and proinflammatory cytokine production. Hum Immunol. 2013; 74:417-424.
4. Bainbridge DR, Ellis SA and Sargent IL. HLA-G suppresses proliferation of CD4(+) T-lymphocytes. J Reprod Immunol. 2000; 48:17-26.
5. Contini P, Ghio M, Poggi A, Filaci G, Indiveri F, Ferrone S and 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; 33:125-134.
6. Riteau B, Menier C, Khalil-Daher I, Sedlik C, Dausset J, Rouas-Freiss N and Carosella ED. HLA-G inhibits the allogeneic proliferative response. J Reprod Immunol. 1999; 43:203-211.
7. Bukur J and Seliger B. The role of HLA-G for protection of human renal cell-carcinoma cells from immune-mediated lysis: implications for immunotherapies. Semin Cancer Biol. 2003; 13:353-359.
8. Jasinski-Bergner S, Stoehr C, Bukur J, Massa C, Braun J, Huttelmaier S, Spath V, Wartenberg R, Legal W, Taubert H, Wach S, Wullich B, Hartmann A and Seliger B. Clinical relevance of miR-mediated HLA-G regulation and the associated immune cell infiltration in renal cell carcinoma. Oncoimmunology. 2015; 4:e1008805.
9. Bukur J, Rebmann V, Grosse-Wilde H, Luboldt H, Ruebben H, Drexler I, Sutter G, Huber C and Seliger B. Functional role of human leukocyte antigen-G up-regulation in renal cell carcinoma. Cancer Res. 2003; 63:4107-4111.
10. Nuckel H, Rebmann V, Durig J, Duhrsen U and Grosse-Wilde H. HLA-G expression is associated with an unfavorable outcome and immunodeficiency in chronic lymphocytic leukemia. Blood. 2005; 105:1694-1698.
11. Singer G, Rebmann V, Chen YC, Liu HT, Ali SZ, Reinsberg J, McMaster MT, Pfeiffer K, Chan DW, Wardelmann E, Grosse-Wilde H, Cheng CC, Kurman RJ and Shih Ie M. HLA-G is a potential tumor marker in malignant ascites. Clin Cancer Res. 2003; 9:4460-4464.
12. Rouas-Freiss N, Moreau P, LeMaoult J and Carosella ED. The dual role of HLA-G in cancer. J Immunol Res. 2014; 2014:359748.
13. Amiot L, Ferrone S, Grosse-Wilde H and Seliger B. Biology of HLA-G in cancer: a candidate molecule for therapeutic intervention? Cell Mol Life Sci. 2011; 68:417-431.
14. Manaster I, Goldman-Wohl D, Greenfield C, Nachmani D, Tsukerman P, Hamani Y, Yagel S and Mandelboim O. MiRNA-mediated control of HLA-G expression and function. PLoS One. 2012; 7:e33395.
15. Wang X, Li B, Wang J, Lei J, Liu C, Ma Y and Zhao H. Evidence that miR-133a causes recurrent spontaneous abortion by reducing HLA-G expression. Reprod Biomed Online. 2012; 25:415-424.
16. Jasinski-Bergner S, Mandelboim O and Seliger B. The role of microRNAs in the control of innate immune response in cancer. J Natl Cancer Inst. 2014; 106(10).
17. Jasinski-Bergner S, Stehle F, Gonschorek E, Kalich J, Schulz K, Huettelmaier S, Braun J and Seliger B. Identification of 14-3-3beta gene as a novel miR-152 target using a proteome-based approach. J Biol Chem. 2014; 289:31121-31135.
18. Kawakami K, Enokida H, Chiyomaru T, Tatarano S, Yoshino H, Kagara I, Gotanda T, Tachiwada T, Nishiyama K, Nohata N, Seki N and Nakagawa M. The functional significance of miR-1 and miR-133a in renal cell carcinoma. Eur J Cancer. 2012; 48:827-836.
19. Kinoshita T, Nohata N, Fuse M, Hanazawa T, Kikkawa N, Fujimura L, Watanabe-Takano H, Yamada Y, Yoshino H, Enokida H, Nakagawa M, Okamoto Y and Seki N. Tumor suppressive microRNA-133a regulates novel targets: moesin contributes to cancer cell proliferation and invasion in head and neck squamous cell carcinoma. Biochem Biophys Res Commun. 2012; 418:378-383.
20. Kojima S, Chiyomaru T, Kawakami K, Yoshino H, Enokida H, Nohata N, Fuse M, Ichikawa T, Naya Y, Nakagawa M and Seki N. Tumour suppressors miR-1 and miR-133a target the oncogenic function of purine nucleoside phosphorylase (PNP) in prostate cancer. Br J Cancer. 2012; 106:405-413.
21. Moriya Y, Nohata N, Kinoshita T, Mutallip M, Okamoto T, Yoshida S, Suzuki M, Yoshino I and Seki N. Tumor suppressive microRNA-133a regulates novel molecular networks in lung squamous cell carcinoma. J Hum Genet. 2012; 57:38-45.
22. Song YX, Yue ZY, Wang ZN, Xu YY, Luo Y, Xu HM, Zhang X, Jiang L, Xing CZ and Zhang Y. MicroRNA-148b is frequently down-regulated in gastric cancer and acts as a tumor suppressor by inhibiting cell proliferation. Mol Cancer. 2011; 10:1.
23. Tsuruta T, Kozaki K, Uesugi A, Furuta M, Hirasawa A, Imoto I, Susumu N, Aoki D and Inazawa J. miR-152 is a tumor suppressor microRNA that is silenced by DNA hypermethylation in endometrial cancer. Cancer Res. 2011; 71:6450-6462.
24. Xiang Y, Ma N, Wang D, Zhang Y, Zhou J, Wu G, Zhao R, Huang H, Wang X, Qiao Y, Li F, Han D, Wang L, Zhang G and Gao X. MiR-152 and miR-185 co-contribute to ovarian cancer cells cisplatin sensitivity by targeting DNMT1 directly: a novel epigenetic therapy independent of decitabine. Oncogene. 2014; 33:378-386.
25. Zhou X, Zhao F, Wang ZN, Song YX, Chang H, Chiang Y and Xu HM. Altered expression of miR-152 and miR-148a in ovarian cancer is related to cell proliferation. Oncol Rep. 2012; 27:447-454.
26. Zhou Y, Wu D, Tao J, Qu P, Zhou Z and Hou J. MicroRNA-133 inhibits cell proliferation, migration and invasion by targeting epidermal growth factor receptor and its downstream effector proteins in bladder cancer. Scand J Urol. 2013; 47:423-432.
27. Zhu C, Li J, Ding Q, Cheng G, Zhou H, Tao L, Cai H, Li P, Cao Q, Ju X, Meng X, Qin C, Hua L, Shao P and Yin C. miR-152 controls migration and invasive potential by targeting TGFalpha in prostate cancer cell lines. Prostate. 2013; 73:1082-1089.
28. Luck ME, Muljo SA and Collins CB. Prospects for Therapeutic Targeting of MicroRNAs in Human Immunological Diseases. J Immunol. 2015; 194:5047-5052.
29. Zaleska K. miRNA - Therapeutic tool in breast cancer? Where are we now? Rep Pract Oncol Radiother. 2015; 20:79-86.
30. Porto IO, Mendes-Junior CT, Felicio LP, Georg RC, Moreau P, Donadi EA, Chies JA and Castelli EC. MicroRNAs targeting the immunomodulatory HLA-G gene: a new survey searching for microRNAs with potential to regulate HLA-G. Mol Immunol. 2015; 65:230-241.
31. Braun J, Misiak D, Busch B, Krohn K and Huttelmaier S. Rapid identification of regulatory microRNAs by miTRAP (miRNA trapping by RNA in vitro affinity purification). Nucleic Acids Res. 2014; 42:e66.
32. Rehmsmeier M, Steffen P, Hochsmann M and Giegerich R. Fast and effective prediction of microRNA/target duplexes. RNA. 2004; 10:1507-1517.
33. Rothe K, Quandt D, Schubert K, Rossol M, Klingner M, Jasinski-Bergner S, Scholz R, Seliger B, Pierer M, Baerwald C and Wagner U. Latent CMV infection in rheumatoid arthritis increases frequencies of cytolytic LIR-1+ CD8+ T cells. Arthritis Rheumatol. 2016; 68:337-46.
34. Veit TD and Chies JA. Tolerance versus immune response -- microRNAs as important elements in the regulation of the HLA-G gene expression. Transpl Immunol. 2009; 20:229-231.
35. Brugiere O, Thabut G, Krawice-Radanne I, Rizzo R, Dauriat G, Danel C, Suberbielle C, Mal H, Stern M, Schilte C, Pretolani M, Carosella ED and Rouas-Freiss N. Role of HLA-G as a predictive marker of low risk of chronic rejection in lung transplant recipients: a clinical prospective study. Am J Transplant. 2015; 15:461-471.
36. LeMaoult J, Daouya M, Wu J, Loustau M, Horuzsko A and Carosella ED. Synthetic HLA-G proteins for therapeutic use in transplantation. FASEB J. 2013; 27:3643-3651.
37. Schulte JH, Marschall T, Martin M, Rosenstiel P, Mestdagh P, Schlierf S, Thor T, Vandesompele J, Eggert A, Schreiber S, Rahmann S and Schramm A. Deep sequencing reveals differential expression of microRNAs in favorable versus unfavorable neuroblastoma. Nucleic acids research. 2010; 38:5919-5928.
38. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S, Castoldi M, Soutschek J, Koteliansky V, Rosenwald A, Basson MA, Licht JD, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature. 2008; 456:980-984.
39. Xu LJ, Ouyang YB, Xiong X, Stary CM and Giffard RG. Post-stroke treatment with miR-181 antagomir reduces injury and improves long-term behavioral recovery in mice after focal cerebral ischemia. Exp Neurol. 2015; 264:1-7.
40. Israelow B, Mullokandov G, Agudo J, Sourisseau M, Bashir A, Maldonado AY, Dar AC, Brown BD and Evans MJ. Hepatitis C virus genetics affects miR-122 requirements and response to miR-122 inhibitors. Nat Commun. 2014; 5:5408.
41. Hydbring P and Badalian-Very G. Clinical applications of microRNAs. F1000Res. 2013; 2:136.
42. Oprea, II, Viola JR, Moreno PM, Simonson OE, Rodin S, Teller N, Tryggvason K, Lundin KE, Girnita L and Smith CI. Repeatable, Inducible Micro-RNA-Based Technology Tightly Controls Liver Transgene Expression. Mol Ther Nucleic Acids. 2014; 3:e172.
43. Loumagne L, Baudhuin J, Favier B, Montespan F, Carosella ED and Rouas-Freiss N. In vivo evidence that secretion of HLA-G by immunogenic tumor cells allows their evasion from immunosurveillance. Int J Cancer. 2014; 135:2107-2117.
44. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ and Guegler KJ. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic acids research. 2005; 33:e179.
45. Varkonyi-Gasic E, Wu R, Wood M, Walton EF and Hellens RP. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant methods. 2007; 3:12.
46. Real LM, Cabrera T, Collado A, Jimenez P, Garcia A, Ruiz-Cabello F and Garrido F. Expression of HLA G in human tumors is not a frequent event. Int J Cancer. 1999; 81:512-518.
47. Shimizu Y and DeMars R. Demonstration by class I gene transfer that reduced susceptibility of human cells to natural killer cell-mediated lysis is inversely correlated with HLA class I antigen expression. Eur J Immunol. 1989; 19:447-451.
48. Tsukerman P, Stern-Ginossar N, Gur C, Glasner A, Nachmani D, Bauman Y, Yamin R, Vitenshtein A, Stanietsky N, Bar-Mag T, Lankry D and Mandelboim O. MiR-10b downregulates the stress-induced cell surface molecule MICB, a critical ligand for cancer cell recognition by natural killer cells. Cancer Res. 2012; 72:5463-5472.
49. Mandelboim O, Reyburn HT, Vales-Gomez M, Pazmany L, Colonna M, Borsellino G and Strominger JL. Protection from lysis by natural killer cells of group 1 and 2 specificity is mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J Exp Med. 1996; 184:913-922.
50. Pavan L, Tarrade A, Hermouet A, Delouis C, Titeux M, Vidaud M, Therond P, Evain-Brion D and Fournier T. Human invasive trophoblasts transformed with simian virus 40 provide a new tool to study the role of PPARgamma in cell invasion process. Carcinogenesis. 2003; 24:1325-1336.
51. Zhang J, Zhang J, Liu LH, Zhou Y, Li YP, Shao ZH, Wu YJ, Li MJ, Fan YY and Shi HJ. Effects of miR-541 on neurite outgrowth during neuronal differentiation. Cell biochemistry and function. 2011; 29:279-286.
52. Haraguchi T, Ozaki Y, Iba H. Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucleic acids research. 2009; 37:e43.
53. Carosella ED, Gregori S, LeMaoult J. The tolerogenic interplay(s) among HLA-G, myeloid APCs, and regulatory cells. Blood. 2011 Dec 15;118:6499-505.