Leukemia Inhibitory Factor Suppresses NKG2D mRNA Expression and Presentation on Human Natural Killer Cells
-
Zahra Abdoli
,
Mohammad-Ali Assarehzadegan
,
Mohammad Hassan Pipelzadeh
,
Sara Iranparast
,
Nader Dashti Gerdabi
,
Mehdi Parsanahad
,
Ali Khodadadi
Abstract
Leukemia inhibitory factor (LIF) is a multi-functional cytokine secreted from cells such as lymphocytes and hepatocytes. This study aimed to evaluate the effect of LIF on natural killer group 2 member D (NKG2D) receptors' expression and presentation on natural killer (NK) cells.
For this purpose, peripheral blood mononuclear cells taken from 4 young male healthy blood donors were isolated and the effect of LIF (25 ng/mL) after 12, 24, and 48 hours of incubation, on NKG2D receptors expression and presentation was investigated using flow cytometry and real-time-polymerase chain reaction (PCR). All of the steps of the experiment were performed in duplicate.
After periods of 12, 24, and 48 hours, LIF reduced both the expression and presentation of the NKG2D receptor on NK cells.
The results suggest that this cytokine has a direct modulating activity on the body’s immune response through suppression of NKG2D receptor expression and presentation on NK cells.
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2. Lord KA, Abdollahi A, Thomas SM, Demarco M, Brugge JS, Hoffman-liebermann B, et al. Leukemia inhibitory factor and interleukin-6 trigger the same immediate early response, including tyrosine phosphorylation, upon induction of myeloid leukemia differentiation. Mol Cell Biol. 1991;11(9):4371-9.
3. Schere-Levy C, Buggiano V, Quaglino A, Gattelli A, Cirio MC, Piazzon I, Vanzulli S, Kordon EC. Leukemia inhibitory factor induces apoptosis of the mammary epithelial cells and participates in mouse mammary gland involution. Exp Cell Res. 2003;282(1):35-47.
4. Kobayashi R, Terakawa J, Kato Y, Azimi S, Inoue N, Ohmori Y, et al. The contribution of leukemia inhibitory factor (LIF) for embryo implantation differs among strains of mice. Immunobiology. 2014;1–10.
5. Bravo J, Staunton D, Heath JK, Jones EY. Crystal structure of a cytokine-binding region of gp130. EMBO J. 1998;17(6):1665-74.
6. Guignat L, Bertherat J. Leukemia inhibitory factor as an intrapituitary regulator of pro-opiomelanocortin gene expression and corticotrope ontogeny. Eur J Endocrinol. 1999;141(3):214–5.
7. Arreygue-Garcia N a, Daneri-Navarro A, del Toro-Arreola A, Cid-Arregui A, Gonzalez-Ramella O, Jave-Suarez LF, et al. 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. 2008;8:16.
8. Fine JH, Chen P, Mesci A, Allan DSJ, Gasser S, Raulet DH, et al. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res. 2010;70(18):7102–13.
9. Fernández-Messina L, Reyburn HT, Valés-Gómez M. Human NKG2D-ligands: Cell biology strategies to ensure immune recognition. Front Immunol. 2012;3:1–9.
10. González S, López-Soto A, Suarez-Alvarez B, López-Vázquez A, López-Larrea C. NKG2D ligands: key targets of the immune response. Trends Immunol. 2008;29(8):397-403.
11. Crane CA, Han SJ, Barry JJ, Ahn BJ, Lanier LL, Parsa AT. TGF-β downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro Oncology. 2010;12(1):7-13.
12. Burgess SJ, Marusina AI, Pathmanathan I, Borrego F, Coligan JE. IL-21 down-regulates NKG2D/DAP10 expression on human NK and CD8+ T cells. J Immunol. 2006;176(3):1490–7.
13. Fischer S, Keshavjee S, Liu M. Heparin interference with reverse transcriptase polymerase chain reaction of RNA extracted from lungs after ischemia-reperfusion. Transpl Int. 2000;13(2):146-50.
14. Bustin SA. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): Trends and problems. J Mol Endocrinol. 2002;29(1):23–39.
15. Salleh N, Giribabu N. Leukemia inhibitory factor: roles in embryo implantation and in nonhormonal contraception. Scientific World Journal. 2014:201514.
16. Krishnan T, Winship a., Sonderegger S, Menkhorst E, Horne a. W, Brown J, et al. The role of leukemia inhibitory factor in tubal ectopic pregnancy. Placenta. 2013;34(11):1014–9.
17. He Z, Li JJ, Zhen CH, Feng LY, Ding XY. Effect of leukemia inhibitory factor on embryonic stem cell differentiation: implications for supporting neuronal differentiation. Acta Pharmacol Sin. 2006;27(1):80-90.
18. Metcalfe, Su M. Axotrophin and leukaemia inhibitory factor (LIF) in transplantation tolerance. Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 2005;1461:1687-94.
19. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy [published correction appears in immunity. J Immunity. 2014;41(1):49-61.
20. Li X, Yang Q, Yu H, Wu L, Zhao Y, Zhang C. LIF promotes tumorigenesis and metastasis of breast cancer through the AKT-mTOR pathway ABSTRACT: 5(3):11–5.
21. Cao W, Yang Y, Wang Z, Liu A, Fang L, Wu F, et al. Leukemia inhibitory factor inhibits T helper 17 cell differentiation and confers treatment effects of neural progenitor cell therapy in autoimmune disease. J Immunity. 2011;35(2):273–84.
22. Sala Hojman, A, Seoane Suarez, J, Molecular mechanisms involved in the immunomodulation induced by LIF in cancer. Thesis, Universitat de Barcelona. 2016:104-6.
23. Imsoonthornruksa S, Noisa P, Parnpai R, Ketudat-Cairns M. A simple method for production and purification of soluble and biologically active recombinant human leukemia inhibitory factor (hLIF) fusion protein in Escherichia coli. J Biotechnol. 2011;151(4):295–302.
24. Duluc D, Delneste Y, Tan F, Moles MP, Grimaud L, Lenoir J, et al. Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood. 2007;110(13):4319–30.
25. Liu S-C, Chang Y-S. Role of leukemia inhibitory factor in nasopharyngeal carcinogenesis. Mol Cell Oncol. 2014;1(1):e29900.
26. Chaur-Dong Hsu, Erika Meaddough, Kristen Aversa, Shih-Fen Hong, Li-Cheng Lu, et al. Elevated amniotic fluid levels of leukemia inhibitory factor, interleukin 6, and interleukin 8 in intra-amniotic infection, Am J Obstet and Gynecol. 1998;179:1267-70.
27. Waring PM, Carroll GJ, Kandiah DA, Buirski G, Metcalf D. Increased levels of leukemia inhibitory factor in synovial fluid from patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum. 1993;36(7):911-5.
28. McKenzie RC, Szepietowski J. Cutaneous leukemia inhibitory factor and its potential role in the development of skin tumors. Dermatol Surg. 2004;30(2 Pt 2):279-90.
29. Slaets H, Hendriks JJ, Stinissen P, Kilpatrick TJ, Hellings N. Therapeutic potential of LIF in multiple sclerosis. Trends Mol Med. 2010;16(11):493–500.
30. Janssens K, Van den Haute C, Baekelandt V, Lucas S, van Horssen J, Somers V, et al. Leukemia inhibitory factor tips the immune balance towards regulatory T cells in multiple sclerosis. Brain Behav Immun. 2015;45:180–8.
31. Janssens K, Van Den Haute C, Baekelandt V, Van Horssen J, Van Wijmeersch B, Stinissen P, et al. Leukemia inhibitory factor shifts the immune balance towards regulatory T cells. J Neuroimmunol. 2014;275(1):155.
2. Lord KA, Abdollahi A, Thomas SM, Demarco M, Brugge JS, Hoffman-liebermann B, et al. Leukemia inhibitory factor and interleukin-6 trigger the same immediate early response, including tyrosine phosphorylation, upon induction of myeloid leukemia differentiation. Mol Cell Biol. 1991;11(9):4371-9.
3. Schere-Levy C, Buggiano V, Quaglino A, Gattelli A, Cirio MC, Piazzon I, Vanzulli S, Kordon EC. Leukemia inhibitory factor induces apoptosis of the mammary epithelial cells and participates in mouse mammary gland involution. Exp Cell Res. 2003;282(1):35-47.
4. Kobayashi R, Terakawa J, Kato Y, Azimi S, Inoue N, Ohmori Y, et al. The contribution of leukemia inhibitory factor (LIF) for embryo implantation differs among strains of mice. Immunobiology. 2014;1–10.
5. Bravo J, Staunton D, Heath JK, Jones EY. Crystal structure of a cytokine-binding region of gp130. EMBO J. 1998;17(6):1665-74.
6. Guignat L, Bertherat J. Leukemia inhibitory factor as an intrapituitary regulator of pro-opiomelanocortin gene expression and corticotrope ontogeny. Eur J Endocrinol. 1999;141(3):214–5.
7. Arreygue-Garcia N a, Daneri-Navarro A, del Toro-Arreola A, Cid-Arregui A, Gonzalez-Ramella O, Jave-Suarez LF, et al. 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. 2008;8:16.
8. Fine JH, Chen P, Mesci A, Allan DSJ, Gasser S, Raulet DH, et al. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res. 2010;70(18):7102–13.
9. Fernández-Messina L, Reyburn HT, Valés-Gómez M. Human NKG2D-ligands: Cell biology strategies to ensure immune recognition. Front Immunol. 2012;3:1–9.
10. González S, López-Soto A, Suarez-Alvarez B, López-Vázquez A, López-Larrea C. NKG2D ligands: key targets of the immune response. Trends Immunol. 2008;29(8):397-403.
11. Crane CA, Han SJ, Barry JJ, Ahn BJ, Lanier LL, Parsa AT. TGF-β downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro Oncology. 2010;12(1):7-13.
12. Burgess SJ, Marusina AI, Pathmanathan I, Borrego F, Coligan JE. IL-21 down-regulates NKG2D/DAP10 expression on human NK and CD8+ T cells. J Immunol. 2006;176(3):1490–7.
13. Fischer S, Keshavjee S, Liu M. Heparin interference with reverse transcriptase polymerase chain reaction of RNA extracted from lungs after ischemia-reperfusion. Transpl Int. 2000;13(2):146-50.
14. Bustin SA. Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): Trends and problems. J Mol Endocrinol. 2002;29(1):23–39.
15. Salleh N, Giribabu N. Leukemia inhibitory factor: roles in embryo implantation and in nonhormonal contraception. Scientific World Journal. 2014:201514.
16. Krishnan T, Winship a., Sonderegger S, Menkhorst E, Horne a. W, Brown J, et al. The role of leukemia inhibitory factor in tubal ectopic pregnancy. Placenta. 2013;34(11):1014–9.
17. He Z, Li JJ, Zhen CH, Feng LY, Ding XY. Effect of leukemia inhibitory factor on embryonic stem cell differentiation: implications for supporting neuronal differentiation. Acta Pharmacol Sin. 2006;27(1):80-90.
18. Metcalfe, Su M. Axotrophin and leukaemia inhibitory factor (LIF) in transplantation tolerance. Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 2005;1461:1687-94.
19. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy [published correction appears in immunity. J Immunity. 2014;41(1):49-61.
20. Li X, Yang Q, Yu H, Wu L, Zhao Y, Zhang C. LIF promotes tumorigenesis and metastasis of breast cancer through the AKT-mTOR pathway ABSTRACT: 5(3):11–5.
21. Cao W, Yang Y, Wang Z, Liu A, Fang L, Wu F, et al. Leukemia inhibitory factor inhibits T helper 17 cell differentiation and confers treatment effects of neural progenitor cell therapy in autoimmune disease. J Immunity. 2011;35(2):273–84.
22. Sala Hojman, A, Seoane Suarez, J, Molecular mechanisms involved in the immunomodulation induced by LIF in cancer. Thesis, Universitat de Barcelona. 2016:104-6.
23. Imsoonthornruksa S, Noisa P, Parnpai R, Ketudat-Cairns M. A simple method for production and purification of soluble and biologically active recombinant human leukemia inhibitory factor (hLIF) fusion protein in Escherichia coli. J Biotechnol. 2011;151(4):295–302.
24. Duluc D, Delneste Y, Tan F, Moles MP, Grimaud L, Lenoir J, et al. Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood. 2007;110(13):4319–30.
25. Liu S-C, Chang Y-S. Role of leukemia inhibitory factor in nasopharyngeal carcinogenesis. Mol Cell Oncol. 2014;1(1):e29900.
26. Chaur-Dong Hsu, Erika Meaddough, Kristen Aversa, Shih-Fen Hong, Li-Cheng Lu, et al. Elevated amniotic fluid levels of leukemia inhibitory factor, interleukin 6, and interleukin 8 in intra-amniotic infection, Am J Obstet and Gynecol. 1998;179:1267-70.
27. Waring PM, Carroll GJ, Kandiah DA, Buirski G, Metcalf D. Increased levels of leukemia inhibitory factor in synovial fluid from patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum. 1993;36(7):911-5.
28. McKenzie RC, Szepietowski J. Cutaneous leukemia inhibitory factor and its potential role in the development of skin tumors. Dermatol Surg. 2004;30(2 Pt 2):279-90.
29. Slaets H, Hendriks JJ, Stinissen P, Kilpatrick TJ, Hellings N. Therapeutic potential of LIF in multiple sclerosis. Trends Mol Med. 2010;16(11):493–500.
30. Janssens K, Van den Haute C, Baekelandt V, Lucas S, van Horssen J, Somers V, et al. Leukemia inhibitory factor tips the immune balance towards regulatory T cells in multiple sclerosis. Brain Behav Immun. 2015;45:180–8.
31. Janssens K, Van Den Haute C, Baekelandt V, Van Horssen J, Van Wijmeersch B, Stinissen P, et al. Leukemia inhibitory factor shifts the immune balance towards regulatory T cells. J Neuroimmunol. 2014;275(1):155.
| Files | ||
| Issue | Vol 20 No 1 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v20i1.5416 | |
| Keywords | ||
| Flow cytometry Leukemia inhibitory factor Natural killer cells NK cell lektin-like reseptor subfamily K | ||
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How to Cite
1.
Abdoli Z, Assarehzadegan M-A, Pipelzadeh MH, Iranparast S, Dashti Gerdabi N, Parsanahad M, Khodadadi A. Leukemia Inhibitory Factor Suppresses NKG2D mRNA Expression and Presentation on Human Natural Killer Cells. Iran J Allergy Asthma Immunol. 2021;20(1):98-105.
