DNA methyltransferase inhibition accelerates the immunomodulation and migration of human mesenchymal stem cells

Scientific Reports

Volumn 5, Issue , 2015, Pages 8020-

  Lee, Seunghee ^a   Kim, Hyung Sik ^a   Roh, Kyoung Hwan ^a   Lee, Byung Chul ^a   Shin, Tae Hoon ^a   Yoo, Ju Mi ^a   Kim, Yu Lee ^a   Yu, Kyung Rok ^a   Kang, Kyung Sun ^a   Seo, Kwang Won ^a  

^a Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; CHEMOKINE RECEPTOR CXCR2; CHEMOKINE RECEPTOR CXCR4; CYCLOOXYGENASE 2; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; ISOMERASE; PROSTAGLANDIN E SYNTHASE; PTGES PROTEIN, HUMAN; PTGS2 PROTEIN, HUMAN;

ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DNA METHYLATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; MESENCHYMAL STROMA CELL; METABOLISM; PROMOTER REGION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

AZACITIDINE; CELL MOVEMENT; CELL PROLIFERATION; CYCLOOXYGENASE 2; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOMODULATION; INTRAMOLECULAR OXIDOREDUCTASES; MESENCHYMAL STROMAL CELLS; PROMOTER REGIONS, GENETIC; PROSTAGLANDIN-E SYNTHASES; RECEPTORS, CXCR4; RECEPTORS, INTERLEUKIN-8B; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84923100736     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08020     Document Type: Article

References (59)

1. Murphy, M. B., Moncivais, K. & Caplan, A. I. Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp Mol Med 45, e54, doi:10.1038/emm.2013.94 (2013).
2. Kim, H. S. et al. Human umbilical cord blood mesenchymal stem cells reduce colitis in mice by activating NOD2 signaling to COX2. Gastroenterology 145, 1392-1403 e1391-1398 doi:10.1053/j.gastro.2013.08.033 (2013).
3. Kang, J. W. et al. Soluble factors-mediated immunomodulatory effects of canine adipose tissue-derived mesenchymal stem cells. Stem Cells Dev 17, 681-693, doi:10.1089/scd.2007.0153 (2008).
4. Bassi, E. J., Aita, C. A. & Camara, N. O. Immune regulatory properties of multipotent mesenchymal stromal cells: Where do we stand? World J Stem Cells 3, 1-8, doi:10.4252/wjsc.v3.i1.1 (2011).
5. Marquez-Curtis, L. A. & Janowska-Wieczorek, A. Enhancing the migration ability of mesenchymal stromal cells by targeting the SDF-1/CXCR4 axis. Biomed Res Int 2013, 561098, doi:10.1155/2013/561098 (2013).
6. Zhang, X. et al. Isolation and characterization of mesenchymal stem cells from human umbilical cord blood: reevaluation of critical factors for successful isolation and high ability to proliferate and differentiate to chondrocytes as compared to mesenchymal stem cells from bonemarrow and adipose tissue. J Cell Biochem 112, 1206-1218, doi:10.1002/jcb.23042 (2011).
7. Sioud, M.,Mobergslien, A., Boudabous, A. & Floisand, Y. Mesenchymal stem cellmediated T cell suppression occurs through secreted galectins. Int J Oncol 38, 385-390, doi:10.3892/ijo.2010.869 (2011).
8. Liu, G. Y. et al. Secreted galectin-3 as a possible biomarker for the immunomodulatory potential of human umbilical cord mesenchymal stromal cells. Cytotherapy 15, 1208-1217, doi:10.1016/j.jcyt.2013.05.011 (2013).
9. Sivanathan, K. N., Gronthos, S., Rojas-Canales, D., Thierry, B. & Coates, P. T. Interferon-gamma modification of mesenchymal stem cells: implications of autologous and allogeneic mesenchymal stem cell therapy in allotransplantation. Stem Cell Rev 10, 351-375, doi:10.1007/s12015-014-9495-2 (2014).
10. Pistoia, V. & Raffaghello, L. Unveiling the role of TNF-alpha in mesenchymal stromal cell-mediated immunosuppression. Eur J Immunol 44, 352-356, doi:10.1002/eji.201344372 (2014).
11. Fan, H. et al. Pre-treatment with IL-1beta enhances the efficacy of MSC transplantation in DSS-induced colitis. Cell Mol Immunol 9, 473-481, doi:10.1038/cmi.2012.40 (2012).
12. Duijvestein, M. et al. Pretreatment with interferon-gamma enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis. Stem Cells 29, 1549-1558, doi:10.1002/stem.698 (2011).
13. Li, H. et al. CCR7 guides migration of mesenchymal stem cell to secondary lymphoid organs: A novel approach to separate GvHD from GvL effect. Stem Cells, doi:10.1002/stem.1656 (2014).
14. Shen, W. et al. Intra-articular injection of human meniscus stem/progenitor cells promotes meniscus regeneration and ameliorates osteoarthritis through stromal cell-derived factor-1/CXCR4-mediated homing. Stem Cells Transl Med 3, 387-394, doi:10.5966/sctm.2012-0170 (2014).
15. Chen, W. et al. Overexpression of the mesenchymal stem cell Cxcr4 gene in irradiated mice increases the homing capacity of these cells. Cell Biochem Biophys 67, 1181-1191, doi:10.1007/s12013-013-9632-6 (2013).
16. Lee, S. et al. Histone deacetylase inhibitors decrease proliferation potential and multilineage differentiation capability of human mesenchymal stem cells. Cell Prolif 42, 711-720, doi:10.1111/j.1365-2184.2009.00633.x (2009).
17. Jung, J. W. et al. Histone deacetylase controls adult stem cell aging by balancing the expression of polycomb genes and jumonji domain containing 3. Cell Mol Life Sci 67, 1165-1176, doi:10.1007/s00018-009-0242-9 (2010).
18. Song, S. H.,Han, S. W.& Bang, Y. J. Epigenetic-based therapies in cancer: progress to date. Drugs 71, 2391-2403, doi:10.2165/11596690-000000000-00000 (2011).
19. Kristensen, L. S., Nielsen,H.M. & Hansen, L. L. Epigenetics and cancer treatment. Eur J Pharmacol 625, 131-142, doi:10.1016/j.ejphar.2009.10.011 (2009).
20. Griffiths, E. A. & Gore, S. D. DNA methyltransferase and histone deacetylase inhibitors in the treatment of myelodysplastic syndromes. Semin Hematol 45, 23-30, doi:10.1053/j.seminhematol.2007.11.007 (2008).
21. Claus, R. & Lubbert, M. Epigenetic targets in hematopoietic malignancies. Oncogene 22, 6489-6496, doi:10.1038/sj.onc.1206814 (2003).
22. Zhu, W. G.& Otterson, G. A. The interaction of histone deacetylase inhibitors and DNA methyltransferase inhibitors in the treatment of human cancer cells. Curr Med Chem Anticancer Agents 3, 187-199 (2003).
23. Zhang, Z. & Wu,W. S. Sodium butyrate promotes generation of human induced pluripotent stem cells through induction of the miR302/367 cluster. Stem Cells Dev 22, 2268-2277, doi:10.1089/scd.2012.0650 (2013).
24. Han, J., Sachdev, P. S. & Sidhu, K. S. A combined epigenetic and non-genetic approach for reprogramming human somatic cells. PLoS One 5, e12297, doi:10.1371/journal.pone.0012297 (2010).
25. De Carvalho, D. D., You, J. S. & Jones, P. A. DNA methylation and cellular reprogramming. Trends Cell Biol 20, 609-617, doi:10.1016/j.tcb.2010.08.003 (2010).
26. Katz, L. S., Geras-Raaka, E. & Gershengorn, M. C. Reprogramming adult human dermal fibroblasts to islet-like cells by epigenetic modification coupled to transcription factor modulation. Stem Cells Dev 22, 2551-2560, doi:10.1089/scd.2013.0134 (2013).
27. Ding, X., Wang, Y., Zhang, D., Guo, Z. & Zhang, Y. Increased pre-implantation development of cloned bovine embryos treated with 5-aza-2'-deoxycytidine and trichostatin A. Theriogenology 70, 622-630, doi:10.1016/j.theriogenology.2008.04.042 (2008).
28. Choi, J. et al . In vivo administration of hypomethylating agents mitigate graft-versus-host disease without sacrificing graft-versus-leukemia. Blood 116, 129-139, doi:10.1182/blood-2009-12-257253 (2010).
29. Hu, Y. et al. Decitabine facilitates the generation and immunosuppressive function of regulatory gammadeltaT cells derived from human peripheral blood mononuclear cells. Leukemia 27, 1580-1585, doi:10.1038/leu.2012.345 (2013).
30. Chen, K. et al. Human umbilical cord mesenchymal stem cells hUC-MSCs exert immunosuppressive activities through a PGE2-dependent mechanism. Clin Immunol 135, 448-458, doi:10.1016/j.clim.2010.01.015 (2010).
31. Yanez, R., Oviedo, A., Aldea, M., Bueren, J. A. & Lamana, M. L. Prostaglandin E2 plays a key role in the immunosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res 316, 3109-3123, doi:10.1016/j.yexcr.2010.08.008 (2010).
32. Ringe, J. et al. Towards in situ tissue repair: human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J Cell Biochem 101, 135-146, doi:10.1002/ jcb.21172 (2007).
33. Gong, J. et al. The SDF-1/CXCR4 axis regulates migration of transplanted bone marrow mesenchymal stem cells towards the pancreas in rats with acute pancreatitis. Mol Med Rep 9, 1575-1582, doi:10.3892/mmr.2014.2053 (2014).
34. Duffy, M. M. et al. Mesenchymal stem cell inhibition of T-helper 17 celldifferentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor. Eur J Immunol 41, 2840-2851, doi:10.1002/eji.201141499 (2011).
35. Boniface, K. et al. Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling. J Exp Med 206, 535-548, doi:10.1084/jem.20082293 (2009).
36. Tatara, R. et al. Mesenchymal stromal cells inhibit Th17 but not regulatory T-cell differentiation. Cytotherapy 13, 686-694, doi:10.3109/14653249.2010.542456 (2011).
37. Bouffi, C., Bony, C., Courties, G., Jorgensen, C. & Noel, D. IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One 5, e14247, doi:10.1371/journal.pone.0014247 (2010).
38. Fang, J. et al. Epigenetic changes mediated by microRNA miR29 activate cyclooxygenase 2 and lambda-1 interferon production during viral infection. J Virol 86, 1010-1020, doi:10.1128/JVI.06169-11 (2012).
39. Akhtar, M. et al. Promoter methylation regulates Helicobacter pylori-stimulated cyclooxygenase-2 expression in gastric epithelial cells. Cancer Res 61, 2399-2403 (2001).
40. Nahidi, L. et al. Inflammatory bowel disease therapies and gut function in a colitis mouse model. Biomed Res Int 2013, 909613, doi:10.1155/2013/909613 (2013).
41. Forster, C. Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130, 55-70, doi:10.1007/s00418-008-0424-9 (2008).
42. Williams, E. J. et al. Distribution of the interleukin-8 receptors, CXCR1 and CXCR2, in inflamed gut tissue. J Pathol 192, 533-539, doi:10.1002/1096-9896(2000)9999:9999<::AID-PATH732>3.0.CO;2-X (2000).
43. Leal, R. F. et al. Identification of inflammatory mediators in patients with Crohn's disease unresponsive to anti-TNFalpha therapy. Gut, doi:10.1136/gutjnl-2013- 306518 (2014).
44. Moser, B., Clark-Lewis, I., Zwahlen, R. & Baggiolini, M. Neutrophil-activating properties of the melanoma growth-stimulatory activity. J Exp Med 171, 1797-1802 (1990).
45. Schumacher, C., Clark-Lewis, I., Baggiolini, M.& Moser, B. High- and low-affinity binding of GRO alpha and neutrophil-activating peptide 2 to interleukin 8 receptors on human neutrophils. Proc Natl Acad Sci U S A 89, 10542-10546 (1992).
46. Xu, J., Chen, Q., Shi, C. & Yin, Z. Overexpression of CXCR1/CXCR2 on mesenchymal stromal cells may be an effective treatment for acute myocardial infarction. Cytotherapy 11, 990-991, doi:10.3109/14653240903233099 (2009).
47. Bleul, C. C., Fuhlbrigge, R. C., Casasnovas, J. M., Aiuti, A. & Springer, T. A. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 184, 1101-1109 (1996).
48. Gul-Uludag, H. et al. Cationic liposome-mediated CXCR4 gene delivery into hematopoietic stem/progenitor cells: implications for clinical transplantation and gene therapy. Stem Cells Dev 21, 1587-1596, doi:10.1089/scd.2011.0297 (2012).
49. Marquez-Curtis, L. A.,Gul-Uludag, H., Xu, P., Chen, J.& Janowska-Wieczorek,A. CXCR4 transfection of cord blood mesenchymal stromal cells with the use of cationic liposome enhances their migration toward stromal cell-derived factor-1. Cytotherapy 15, 840-849, doi:10.1016/j.jcyt.2013.02.009 (2013).
50. Stoicov, C., Li, H., Liu, J. H. & Houghton, J. Mesenchymal stem cells utilize CXCR4-SDF-1 signaling for acute, but not chronic, trafficking to gastric mucosal inflammation. Dig Dis Sci 58, 2466-2477, doi:10.1007/s10620-013-2782-y (2013).
51. Tao, Y. H., Ye, L.,Wang, Y. M. & Wang, Z. [Mechanism for promoting repair of renal ischemia reperfusion injury by mesenchymal stem cells]. Zhongguo Dang Dai Er Ke Za Zhi 15, 157-161 (2013).
52. Sun, Y. et al . Epigenetic regulation of spinal CXCR2 signaling in incisional hypersensitivity in mice. Anesthesiology 119, 1198-1208, doi:10.1097/ALN.0b013e31829ce340 (2013).
53. Kiguchi, N. et al. Epigenetic augmentation of the macrophage inflammatory protein 2/C-X-C chemokine receptor type 2 axis through histone H3 acetylation in injured peripheral nerves elicits neuropathic pain. J Pharmacol Exp Ther 340, 577-587, doi:10.1124/jpet.111.187724 (2012).
54. Irvine, R. A., Lin, I. G. & Hsieh, C. L. DNA methylation has a local effect on transcription and histone acetylation. Mol Cell Biol 22, 6689-6696 (2002).
55. Sato, N., Matsubayashi, H., Fukushima, N. & Goggins, M. The chemokine receptor CXCR4 is regulated by DNA methylation in pancreatic cancer. Cancer Biol Ther 4, 70-76 (2005).
56. van Deen, W. K., Oikonomopoulos, A. & Hommes, D. W. Stem cell therapy in inflammatory bowel disease: which, when and how? Curr Opin Gastroenterol 29, 384-390, doi:10.1097/MOG.0b013e328361f763 (2013).
57. Sempere, J. M. et al. Single cell-derived clones from human adipose stem cells present different immunomodulatory properties. Clin Exp Immunol 176, 255-265, doi:10.1111/cei.12270 (2014).
58. Nicklas, J. A. & Buel, E. Development of an Alu-based, real-time PCR method for quantitation of human DNA in forensic samples. J Forensic Sci 48, 936-944 (2003).
59. Hu, X. et al. Hypoxic preconditioning enhances bone marrow mesenchymal stem cell migration via Kv2.1 channel and FAK activation. Am J Physiol Cell Physiol 301, C362-372, doi:10.1152/ajpcell.00013.2010 (2011).