Export file:

Format

  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text

Content

  • Citation Only
  • Citation and Abstract

Main NK cell receptors and their ligands: regulation by microRNAs

1 Istituto Giannina Gaslini, Genova, Italy
2 Center for Advanced Biomaterials for Healthcare, IIT@CRIB, Istituto Italiano di Tecnologia, Napoli, Italy
3 Dipartimento di Medicina Sperimentale, University of Genova, Italy
4 Centro di Eccellenza per la Ricerca Biomedica (CEBR), University of Genova, Italy

Special Issues: Novel insights in NK cell receptors and their ligands in health and disease

The NK cells functions are finely tuned by several kinds of inhibitory and activating receptors, whose pattern of expression characterizes different NK subpopulations and varies with the cell activation status. MicroRNAs have an important role in tightly regulating the expression of NK receptors and, analogously, the expression of their ligands in target cells. The relevance of the microRNA-mediated control is highlighted by the dysregulation of these pathways observed in cancer and virus-infected cells. Here we review our current knowledge of the microRNAs involved in the regulation of NK receptors, as well as that of the corresponding cellular ligands.
  Figure/Table
  Supplementary
  Article Metrics

Keywords NK cells; microRNAs; NK receptors; NK receptor ligands; TGF-β1

Citation: Stefano Regis, Fabio Caliendo, Alessandra Dondero, Francesca Bellora, Beatrice Casu, Cristina Bottino, Roberta Castriconi. Main NK cell receptors and their ligands: regulation by microRNAs. AIMS Allergy and Immunology, 2018, 2(2): 98-112. doi: 10.3934/Allergy.2018.2.98

References

  • 1. Freud AG, Mundy-Bosse BL, Yu J, et al. (2017) The broad spectrum of human natural killer cell diversity. Immunity 47: 820–833.    
  • 2. Björkström NK, Ljunggren HG, Michaëlsson J (2016) Emerging insights into natural killer cells in human peripheral tissues. Nat Rev Immunol 16: 310–320.    
  • 3. Joncker NT, Fernandez NC, Treiner E, et al. (2009) NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J Immunol 182: 4572–4580.    
  • 4. Brodin P, Kärre K, Höglund P (2009) NK cell education: not an on-off switch but a tunable rheostat. Trends Immunol 30: 143–149.    
  • 5. Bartel DP (2018) Metazoan microRNAs. Cell 173: 20–51.    
  • 6. Pickup M, Novitskiy S, Moses HL (2013) The roles of TGFβ in the tumour microenvironment. Nat Rev Cancer 13: 788–799.    
  • 7. Zingoni A, Molfetta R, Fionda C, et al. (2018) NKG2D and its ligands: "One for all, all for one". Front Immunol 9: 1–12.    
  • 8. Castriconi R, Cantoni C, Chiesa MD, et al. (2003) 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 USA 100: 4120–4125.    
  • 9. Castriconi R, Dondero A, Bellora F, et al. (2013) Neuroblastoma-derived TGF-β1 modulates the chemokine receptor repertoire of human resting NK cells. J Immunol 190: 5321–5328.    
  • 10. Lee JC, Lee KM, Ahn YO, et al. (2011) A possible mechanism of impaired NK cytotoxicity in cancer patients: down-regulation of DAP10 by TGF-beta1. Tumori 97: 350–357.    
  • 11. Espinoza JL, Takami A, Yoshioka K, et al. (2012) Human microRNA-1245 down-regulates the NKG2D receptor in natural killer cells and impairs NKG2D-mediated functions. Haematologica 97: 1295–1303.    
  • 12. Tomasello E, Vivier E (2005) KARAP/DAP12/TYROBP: three names and a multiplicity of biological functions. Eur J Immunol 35: 1670–1677.    
  • 13. Donatelli SS, Zhou JM, Gilvary DL, et al. (2014) TGF-β-inducible microRNA-183 silences tumor-associated natural killer cells. Proc Natl Acad Sci USA 111: 4203–4208.    
  • 14. Huntington ND, Tabarias H, Fairfax K, et al. (2007) NK Cell Maturation and Peripheral Homeostasis Is Associated with KLRG1 Up-Regulation. J Immunol 178: 4764–4770.    
  • 15. Jonjic S (2010) Functional plasticity and robustness are essential characteristics of biological systems: Lessons learned from KLRG1-deficient mice. Eur J Immunol 40: 1241–1243.    
  • 16. Cipolla GA, Park JK, de Oliveira LA, et al. (2016) A 3'UTR polymorphism marks differential KLRG1 mRNA levels through disruption of a miR-584-5p binding site and associates with pemphigus foliaceus susceptibility. Biochim Biophys Acta 1859: 1306–1313.    
  • 17. Gallois A, Silva I, Osman I, et al. (2014) Reversal of natural killer cell exhaustion by TIM-3 blockade. Oncoimmunology 3: e946365.    
  • 18. Cheng YQ, Ren JP, Zhao J, et al. (2015) MicroRNA-155 regulates interferon-γ production in natural killer cells via Tim-3 signalling in chronic hepatitis C virus infection. Immunology 145: 485–497.    
  • 19. Pesce S, Greppi M, Tabellini G, et al. (2017) Identification of a subset of human natural killer cells expressing high levels of programmed death 1: A phenotypic and functional characterization. J Allergy Clin Immunol 139: 335–346.    
  • 20. Okazaki T, Chikuma S, Iwai Y, et al. (2013) A rheostat for immune responses: the unique properties of PD-1 and their advantages for clinical application. Nat Immunol 14: 1212–1218.    
  • 21. Zhang G, Li N, Li Z, et al. (2015) MicroRNA-4717 differentially interacts with its polymorphic target in the PD1 3' untranslated region: A mechanism for regulating PD-1 expression and function in HBV-associated liver diseases. Oncotarget 6: 18933–18944.
  • 22. Wei J, Nduom EK, Kong LY, et al. (2016) MiR-138 exerts anti-glioma efficacy by targeting immune checkpoints. Neuro-Oncol 18: 639–648.    
  • 23. Li Q, Johnston N, Zheng X, et al. (2016) MiR-28 modulates exhaustive differentiation of T cells through silencing programmed cell death-1 and regulating cytokine secretion. Oncotarget 7: 53735–53750.
  • 24. Davis ZB, Vallera DA, Miller JS, et al. (2017) Natural killer cells unleashed: Checkpoint receptor blockade and BiKE/TriKE utilization in NK-mediated anti-tumor immunotherapy. Semin Immunol 31: 64–75.    
  • 25. Sonkoly E, Janson P, Majuri ML, et al. (2010) MiR-155 is overexpressed in patients with atopic dermatitis and modulates T-cell proliferative responses by targeting cytotoxic T lymphocyte-associated antigen 4. J Allergy Clin Immunol 126: 581–589.    
  • 26. Griffith JW, Sokol CL, Luster AD (2014) Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol 32: 659–702.    
  • 27. Sciumè G, De Angelis G, Benigni G, et al. (2011) CX3CR1 expression defines 2 KLRG1+ mouse NK-cell subsets with distinct functional properties and positioning in the bone marrow. Blood 117: 4467–4475.    
  • 28. Ponzetta A, Sciumè G, Benigni G, et al. (2013) CX3CR1 regulates the maintenance of KLRG1+ NK cells into the bone marrow by promoting their entry into circulation. J Immunol 191: 5684–5694.    
  • 29. Regis S, Caliendo F, Dondero A, et al. (2017) TGF-β1 downregulates the expression of CX3CR1 by inducing miR-27a-5p in primary human NK cells. Front Immunol 8: 868.    
  • 30. Allenspach E, Rawlings DJ, Scharenberg AM, (2003) X-Linked Severe Combined Immunodeficiency, In: GeneReviews®, eds. M. P. Adam, H. H. Ardinger, R. A. Pagon, S. E. Wallace, L. J. Bean, K. Stephens, A. Amemiya (Seattle (WA): University of Washington, Seattle. Available at: http://www.ncbi.nlm.nih.gov/books/NBK1410/.
  • 31. Yun S, Lee SU, Kim JM, et al. (2014) Integrated mRNA-MicroRNA profiling of human NK cell differentiation identifies miR-583 as a negative regulator of IL2Rγ expression. PloS One 9: e108913.    
  • 32. Jasinski-Bergner S, Mandelboim O, Seliger B (2014) The role of microRNAs in the control of innate immune response in cancer. J Natl Cancer Inst 106: 165–193.    
  • 33. Elias S, Mandelboim O (2012) Battle of the midgets: innate microRNA networking. RNA Biol 9: 792–798.    
  • 34. Stern-Ginossar N, Gur C, Biton M, et al. (2008) Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 9: 1065.    
  • 35. Nachmani D, Lankry D, Wolf DG, et al. (2010) The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol 11: 806–813.    
  • 36. Heinemann A, Zhao F, Pechlivanis S, et al. (2012) Tumor suppressive microRNAs miR-34a/c control cancer cell expression of ULBP2, a stress-induced ligand of the natural killer cell receptor NKG2D. Cancer Res 72: 460–471.    
  • 37. Tsukerman P, Stern-Ginossar N, Gur C, et al. (2012) MiR-10b downregulates the stress-induced cell surface molecule MICB, a critical ligand for cancer cell recognition by natural killer cells. Cancer Res 72: 5463–5472.    
  • 38. Breunig C, Pahl J, Küblbeck M, et al. (2017) MicroRNA-519a-3p mediates apoptosis resistance in breast cancer cells and their escape from recognition by natural killer cells. Cell Death Dis 8: e2973.    
  • 39. Codo P, Weller M, Meister G, et al. (2014) MicroRNA-mediated down-regulation of NKG2D ligands contributes to glioma immune escape. Oncotarget 5: 7651–7662.
  • 40. Wang B, Wang Q, Wang Z, et al. (2014) Metastatic consequences of immune escape from nk cell cytotoxicity by human breast cancer stem cells. Cancer Res 74: 5746–5757.    
  • 41. Xie J, Liu M, Li Y, et al. (2014) Ovarian tumor-associated microRNA-20a decreases natural killer cell cytotoxicity by downregulating MICA/B expression. Cell Mol Immunol 11: 495–502.    
  • 42. Min D, Lv X, Wang X, et al. (2013) Downregulation of miR-302c and miR-520c by 1,25(OH)2D3 treatment enhances the susceptibility of tumour cells to natural killer cell-mediated cytotoxicity. Br J Cancer 109: 723–730.    
  • 43. Carosella ED, Gregori S, Rouas-Freiss N, et al. (2011) The role of HLA-G in immunity and hematopoiesis. Cell Mol Life Sci 68: 353–368.    
  • 44. Manaster I, Goldmanwohl D, Greenfield C, et al. (2012) MiRNA-mediated control of HLA-G expression and function. PloS One 7: e33395.    
  • 45. Morandi F, Ferretti E, Castriconi R, et al. (2011) Soluble HLA-G dampens CD94/NKG2A expression and function and differentially modulates chemotaxis and cytokine and chemokine secretion in CD56bright and CD56dim NK cells. Blood 118: 5840–5850.    
  • 46. Wang X, Li B, Wang J, et al. (2012) Evidence that miR-133a causes recurrent spontaneous abortion by reducing HLA-G expression. Reprod Biomed Online 25: 415–424.    
  • 47. Simon JB, Adi R, Christine S, et al. (2016) Identification of novel microRNAs regulating HLA-G expression and investigating their clinical relevance in renal cell carcinoma. Oncotarget 7: 26866–26878.
  • 48. Mori A, Nishi H, Sasaki T, et al. (2016) HLA-G expression is regulated by miR-365 in trophoblasts under hypoxic conditions. Placenta 45: 37–41.    
  • 49. Jasinski-Bergner S, Stoehr C, Bukur J, et al. (2015) Clinical relevance of miR-mediated HLA-G regulation and the associated immune cell infiltration in renal cell carcinoma. Oncoimmunology 4: e1008805.    
  • 50. Sun J, Chu H, Ji J, et al. (2016) Long non-coding RNA HOTAIR modulates HLA-G expression by absorbing miR-148a in human cervical cancer. Int J Oncol 49: 943–952.    
  • 51. Song B, Guan Z, Liu F, et al. (2015) Long non-coding RNA HOTAIR promotes HLA-G expression via inhibiting miR-152 in gastric cancer cells. Biochem Biophys Res Commun 464: 807–813.    
  • 52. Guan Z, Song B, Liu F, et al. (2015) TGF-β induces HLA-G expression through inhibiting miR-152 in gastric cancer cells. J Biomed Sci 22: 107.    
  • 53. Falco M, Moretta L, Moretta A, et al. (2013) KIR and KIR ligand polymorphism: a new area for clinical applications? Tissue Antigens 82: 363–373.    
  • 54. Kulkarni S, Savan R, Qi Y, et al. (2011) Differential microRNA regulation of HLA-C expression and its association with HIV control. Nature 472: 495–498.    
  • 55. Braud VM, Allan DS, O'Callaghan CA, et al. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391: 795–799.    
  • 56. Hammer Q, Rückert T, Borst EM, et al. (2018) Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells. Nat Immunol 19: 453–463.    
  • 57. Nachmani D, Zimmermann A, Djian EO, et al. (2014) MicroRNA editing facilitates immune elimination of HCMV infected cells. PloS Pathog 10: e1003963.    
  • 58. Dondero A, Casu B, Bellora F, et al. (2017) NK cells and multiple myeloma-associated endothelial cells: molecular interactions and influence of IL-27. Oncotarget 8: 35088–35102.
  • 59. Chen J, Jiang CC, Jin L, et al. (2016) Regulation of PD-L1: a novel role of pro-survival signalling in cancer. Ann Oncol 27: 409–416.    
  • 60. Grenda A, Krawczyk P (2017) New dancing couple: PD-L1 and MicroRNA. Scand J Immunol 86: 130–134.    
  • 61. Wang Q, Lin W, Tang X, et al. (2017) The roles of microRNAs in regulating the expression of PD-1/PD-L1 immune checkpoint. Int J Mol Sci 18: 2540–2550.    
  • 62. Smolle MA, Calin HN, Pichler M, et al. (2017) Noncoding RNAs and immune checkpoints-clinical implications as cancer therapeutics. FEBS J 284: 1952–1966.    
  • 63. Gong AY, Zhou R, Hu G, et al. (2009) MicroRNA-513 regulates B7-H1 translation and is involved in IFN-gamma-induced B7-H1 expression in cholangiocytes. J Immunol 182: 1325–1333.    
  • 64. Wang X, Li J, Dong K, et al. (2015) Tumor suppressor miR-34a targets PD-L1 and functions as a potential immunotherapeutic target in acute myeloid leukemia. Cell Signal 27: 443–452.    
  • 65. Chen L, Gibbons DL, Goswami S, et al. (2014) Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression. Nat Commun 5: 5241.    
  • 66. Zhao L, Yu H, Yi S, et al. (2016) The tumor suppressor miR-138-5p targets PD-L1 in colorectal cancer. Oncotarget 7: 45370–45384.
  • 67. Kao SC, Cheng YY, Williams M, et al. (2017) Tumor suppressor microRNAs contribute to the regulation of PD-L1 expression in malignant pleural mesothelioma. J Thorac Oncol Off Publ Int Assoc Study Lung Cancer 12: 1421–1433.
  • 68. Audrito V, Serra S, Stingi A, et al. (2017) PD-L1 up-regulation in melanoma increases disease aggressiveness and is mediated through miR-17-5p. Oncotarget 8: 15894–15911.
  • 69. Jia L, Xi Q, Wang H, et al. (2017) MiR-142-5p regulates tumor cell PD-L1 expression and enhances anti-tumor immunity. Biochem Biophys Res Commun 488: 425–431.    
  • 70. Xie WB, Liang LH, Wu KG, et al. (2018) MiR-140 expression regulates cell proliferation and targets PD-L1 in NSCLC. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 46: 654–663.    
  • 71. Xu S, Tao Z, Hai B, et al. (2016) MiR-424(322) reverses chemoresistance via T-cell immune response activation by blocking the PD-L1 immune checkpoint. Nat Commun 7: 11406.    
  • 72. Wang Y, Wang D, Xie G, et al. (2017) MicroRNA-152 regulates immune response via targeting B7-H1 in gastric carcinoma. Oncotarget 8: 28125–28134.
  • 73. Holla S, Stephen-Victor E, Prakhar P, et al. (2016) Mycobacteria-responsive sonic hedgehog signaling mediates programmed death-ligand 1- and prostaglandin E2-induced regulatory T cell expansion. Sci Rep 6: 24193.    
  • 74. Lee YH, Martin-Orozco N, Zheng P, et al. (2017) Inhibition of the B7-H3 immune checkpoint limits tumor growth by enhancing cytotoxic lymphocyte function. Cell Res 27: 1034–1045.    
  • 75. Leitner J, Klauser C, Pickl WF, et al. (2009) B7-H3 is a potent inhibitor of human T-cell activation: No evidence for B7-H3 and TREML2 interaction. Eur J Immunol 39: 1754–1764.    
  • 76. Castriconi R, Dondero A, Augugliaro R, et al. (2004) Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc Natl Acad Sci USA 101: 12640–12645.    
  • 77. Bottino C, Dondero A, Bellora F, et al. (2014) Natural killer cells and neuroblastoma: tumor recognition, escape mechanisms, and possible novel immunotherapeutic approaches. Front Immunol 5: 56.
  • 78. Ni L, Dong C (2017) New checkpoints in cancer immunotherapy. Immunol Rev 276: 52–65.    
  • 79. Gregorio A, Corrias MV, Castriconi R, et al. (2008) Small round blue cell tumours: diagnostic and prognostic usefulness of the expression of B7-H3 surface molecule. Histopathology 53: 73–80.    
  • 80. Xu H, Cheung IY, Guo HF, et al. (2009) MicroRNA miR-29 modulates expression of immunoinhibitory molecule B7-H3: potential implications for immune based therapy of human solid tumors. Cancer Res 69: 6275–6281.    
  • 81. Cheung IY, Farazi TA, Ostrovnaya I, et al. (2014) Deep MicroRNA sequencing reveals downregulation of miR-29a in neuroblastoma central nervous system metastasis. Gene Chromosome Canc 53: 803–814.    
  • 82. Wang J, Chong KK, Nakamura Y, et al. (2013) B7-H3 associated with tumor progression and epigenetic regulatory activity in cutaneous melanoma. J Invest Dermatol 133: 2050–2058.    
  • 83. Nygren MK, Tekle C, Ingebrigtsen VA, et al. (2014) Identifying microRNAs regulating B7-H3 in breast cancer: the clinical impact of microRNA-29c. Br J Cancer 110: 2072–2080.    
  • 84. Zhao J, Lei T, Xu C, et al. (2013) MicroRNA-187, down-regulated in clear cell renal cell carcinoma and associated with lower survival, inhibits cell growth and migration though targeting B7-H3. Biochem Biophys Res Commun 438: 439–444.    
  • 85. Zhou X, Mao Y, Zhu J, et al. (2016) TGF-β1 promotes colorectal cancer immune escape by elevating B7-H3 and B7-H4 via the miR-155/miR-143 axis. Oncotarget 7: 67196–67211.
  • 86. Wang L, Kang FB, Sun N, et al. (2016) The tumor suppressor miR-124 inhibits cell proliferation and invasion by targeting B7-H3 in osteosarcoma. Tumour Biol 37: 14939–14947.    
  • 87. Yuan SM, Li H, Yang M, et al. (2015) High intensity focused ultrasound enhances anti-tumor immunity by inhibiting the negative regulatory effect of miR-134 on CD86 in a murine melanoma model. Oncotarget 6: 37626–37637.
  • 88. Eichmüller SB, Osen W, Mandelboim O, et al. (2017) Immune modulatory microRNAs involved in tumor attack and tumor immune escape. J Natl Cancer Inst 109: djx034.
  • 89. Rupaimoole R, Slack FJ (2017) MicroRNA therapeutics: towards a new era for the management of cancer and other diseases. Nat Rev Drug Discov 16: 203–222.    
  • 90. van Zandwijk N, Pavlakis N, Kao SC, et al. (2017) Safety and activity of microRNA-loaded minicells in patients with recurrent malignant pleural mesothelioma: A first-in-man, phase 1, open-label, dose-escalation study. Lancet Oncol 18: 1386–1396.    
  • 91. Tran HC, Wan Z, Sheard MA, et al. (2017) TGFβR1 blockade with Galunisertib (LY2157299) enhances anti-neuroblastoma activity of the anti-GD2 antibody Dinutuximab (ch14.18) with natural killer cells. Clin Cancer Res 23: 804–813.

 

This article has been cited by

  • 1. Behnaz Valipour, Kobra Velaei, Ali Abedelahi, Mohammad Karimipour, Masoud Darabi, Hojjatollah Nozad Charoudeh, NK cells: An attractive candidate for cancer therapy, Journal of Cellular Physiology, 2019, 234, 11, 19352, 10.1002/jcp.28657
  • 2. Alireza Mardomi, Nabiallah Mohammadi, Hamid Tayebi Khosroshahi, Saeid Abediankenari, An update on potentials and promises of T cell co‐signaling molecules in transplantation, Journal of Cellular Physiology, 2019, 10.1002/jcp.29369

Reader Comments

your name: *   your email: *  

© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Copyright © AIMS Press All Rights Reserved