Mesenchymal stem cells increase skin graft survival time and up-regulate PD-L1 expression in splenocytes of mice

Immunology Letters

Volumn 182, Issue , 2017, Pages 39-49

  Moravej, Ali ^a,b   Geramizadeh, Bita ^a   Azarpira, Negar ^a   Zarnani, Amir Hassan ^c,d   Yaghobi, Ramin ^a   Kalani, Mehdi ^e   Khosravi, Maryam ^a   Kouhpayeh, Amin ^b   Karimi, Mohammad Hossein ^a  

^a SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b FASA UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d IRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

IDO; Immunomodulation; MSCs; PD L1; Transplantation

Indexed keywords

GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 2; MESSENGER RNA; PROGRAMMED DEATH 1 LIGAND 1; BIOLOGICAL MARKER; CD274 PROTEIN, HUMAN; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; BIOLOGICAL MONITORING; C57BL 6 MOUSE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; FULL THICKNESS SKIN GRAFT; GENE EXPRESSION; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL; IMMUNOMODULATION; INTERLEUKIN 10 BLOOD LEVEL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SKIN GRAFT; SKIN TRANSPLANTATION; SPLEEN CELL; SURVIVAL TIME; THERAPY EFFECT; UPREGULATION; ANIMAL; BLOOD; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; MESENCHYMAL STROMA CELL; METABOLISM; SPLEEN;

ANIMALS; B7-H1 ANTIGEN; BIOMARKERS; CYTOKINES; GENE EXPRESSION REGULATION; GRAFT SURVIVAL; IMMUNOMODULATION; IMMUNOPHENOTYPING; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE; SKIN TRANSPLANTATION; SPLEEN;

EID: 85009964765     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2017.01.005     Document Type: Article

References (35)

1. [1] Tzannou, I., Leen, A.M., Preventing stem cell transplantation-associated viral infections using T-cell therapy. Immunotherapy 7:7 (2015), 793–810.
2. [2] Karimi, M.H., Marzban, S., Hajiyan, M.R., Geramizadeh, B., Pourfathollah, A.A., Rajabiyan, M.H., Ebrahimnezhad, S., Effect of CD40 silenced dendritic cells by RNA interference on mice skin allograft rejection. Immunotherapy 7:2 (2015), 111–118.
3. [3] Yang, S.F., Xue, W.J., Lu, W.H., Xie, L.Y., Yin, A.P., Zheng, J., Sun, J.P., Li, Y., Induction of tolerance and prolongation of islet allograft survival by syngeneic hematopoietic stem cell transplantation in mice. Transpl. Immunol. 33:2 (2015), 130–139.
4. [4] Moreau, A., Alliot-Licht, B., Cuturi, M.C., Blancho, G., Tolerogenic dendritic cell therapy in organ transplantation. Transplant Int., 2016 [Epub ahead of print].
5. [5] Newick, K., O'Brien, S., Moon, E., Albelda, S.M., CAR T cell therapy for solid tumors. Annu. Rev. Med. 14 (2016), 139–152.
6. [6] Peak, T.C., Haney, N.M., Wang, W., DeLay, K.J., Hellstrom, W.J., Stem cell therapy for the treatment of Leydig cell dysfunction in primary hypogonadism. World J. Stem Cells 8:10 (2016), 306–315.
7. [7] Vavrova, K., Vrabcova, P., Filipp, D., Bartunkova, J., Horvath, R., Generation of T cell effectors using tumor cell-loaded dendritic cells for adoptive T cell therapy. Med. Oncol. (Northwood, London, England), 33(12), 2016, 136.
8. [8] Michelo, C.M., Fasse, E., van Cranenbroek, B., Linda, K., van der Meer, A., Abdelrazik, H., Joosten, I., Added effects of dexamethasone and mesenchymal stem cells on early Natural Killer cell activation. Transpl. Immunol. 37 (2016), 1–9.
9. [9] Yi, T., Song, S.U., Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications. Arch. Pharm. Res. 35:2 (2012), 213–221.
10. [10] Stagg, J., Galipeau, J., Mechanisms of immune modulation by mesenchymal stromal cells and clinical translation. Curr. Mol. Med. 13:5 (2013), 856–867.
11. [11] Okazaki, T., Honjo, T., PD-1 and PD-1 ligands: from discovery to clinical application. Int. Immunol. 19:7 (2007), 813–824.
12. [12] Li, M., Jiang, J., Fu, B., Chen, J., Xue, Q., Dong, W., Gu, Y., Tang, L., Xue, L., Fang, Q., Wang, M., Zhang, X., PD-L1 is increased in the spinal cord and infiltrating lymphocytes in experimental allergic encephalomyelitis. Neural Regen. Res. 8:35 (2013), 3296–3305.
13. [13] Meng, Q., Yang, P., Li, B., Zhou, H., Huang, X., Zhu, L., Ren, Y., Kijlstra, A., CD4 + PD-1+ T cells acting as regulatory cells during the induction of anterior chamber-associated immune deviation. Invest. Ophthalmol. Vis. Sci. 47:10 (2006), 4444–4452.
14. [14] Yamazaki, T., Akiba, H., Iwai, H., Matsuda, H., Aoki, M., Tanno, Y., Shin, T., Tsuchiya, H., Pardoll, D.M., Okumura, K., Azuma, M., Yagita, H., Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169:10 (2002), 5538–5545.
15. [15] Blazar, B.R., Carreno, B.M., Panoskaltsis-Mortari, A., Carter, L., Iwai, Y., Yagita, H., Nishimura, H., Taylor, P.A., Blockade of programmed death-1 engagement accelerates graft-versus-host disease lethality by an IFN-gamma-dependent mechanism. J. Immunol. 171:3 (2003), 1272–1277.
16. [16] O'Garra, A., Vieira, P., T(H)1 cells control themselves by producing interleukin-10. Nat. Rev. Immunol. 7:6 (2007), 425–428.
17. [17] Ito, T., Ueno, T., Clarkson, M.R., Yuan, X., Jurewicz, M.M., Yagita, H., Azuma, M., Sharpe, A.H., Auchincloss, H. Jr., Sayegh, M.H., Najafian, N., Analysis of the role of negative T cell costimulatory pathways in CD4 and CD8T cell-mediated alloimmune responses in vivo. J. Immunol. 174:11 (2005), 6648–6656.
18. [18] Guleria, I., Khosroshahi, A., Ansari, M.J., Habicht, A., Azuma, M., Yagita, H., Noelle, R.J., Coyle, A., Mellor, A.L., Khoury, S.J., Sayegh, M.H., A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 202:2 (2005), 231–237.
19. [19] Hof-Nahor, I., Leshansky, L., Shivtiel, S., Eldor, L., Aberdam, D., Itskovitz-Eldor, J., Berrih-Aknin, S., Human mesenchymal stem cells shift CD8+ T cells towards a suppressive phenotype by inducing tolerogenic monocytes. J. Cell Sci. 125:Pt. 19 (2012), 4640–4650.
20. [20] Mellor, A.L., Munn, D.H., IDO. expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4:10 (2004), 762–774.
21. [21] Wehner, R., Wehrum, D., Bornhauser, M., Zhao, S., Schakel, K., Bachmann, M.P., Platzbecker, U., Ehninger, G., Rieber, E.P., Schmitz, M., Mesenchymal stem cells efficiently inhibit the proinflammatory properties of 6-sulfo LacNAc dendritic cells. Haematologica 94:8 (2009), 1151–1156.
22. [22] Dokic, J., Tomic, S., Markovic, M., Milosavljevic, P., Colic, M., Mesenchymal stem cells from periapical lesions modulate differentiation and functional properties of monocyte-derived dendritic cells. Eur. J. Immunol. 43:7 (2013), 1862–1872.
23. [23] Cendales, L.C., Kanitakis, J., Schneeberger, S., Burns, C., Ruiz, P., Landin, L., Remmelink, M., Hewitt, C.W., Landgren, T., Lyons, B., Drachenberg, C.B., Solez, K., Kirk, A.D., Kleiner, D.E., Racusen, L., The Banff 2007 working classification of skin-containing composite tissue allograft pathology. Am. J. Transplant. 8:7 (2008), 1396–1400.
24. [24] Zhu, H., Guo, Z.K., Jiang, X.X., Li, H., Wang, X.Y., Yao, H.Y., Zhang, Y., Mao, N., A protocol for isolation and culture of mesenchymal stem cells from mouse compact bone. Nat. Protoc. 5:3 (2010), 550–560.
25. [25] Ben-Ami, E., Berrih-Aknin, S., Miller, A., Mesenchymal stem cells as an immunomodulatory therapeutic strategy for autoimmune diseases. Autoimmun. Rev. 10:7 (2011), 410–415.
26. [26] Popp, F.C., Eggenhofer, E., Renner, P., Slowik, P., Lang, S.A., Kaspar, H., Geissler, E.K., Piso, P., Schlitt, H.J., Dahlke, M.H., Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate. Transpl. Immunol. 20:1–2 (2008), 55–60.
27. [27] Zhou, H.P., Yi, D.H., Yu, S.Q., Sun, G.C., Cui, Q., Zhu, H.L., Liu, J.C., Zhang, J.Z., Wu, T.J., Administration of donor-derived mesenchymal stem cells can prolong the survival of rat cardiac allograft. Transplant. Proc. 38:9 (2006), 3046–3051.
28. [28] Larocca, R.A., Moraes-Vieira, P.M., Bassi, E.J., Semedo, P., de Almeida, D.C., da Silva, M.B., Thornley, T., Pacheco-Silva, A., Camara, N.O., Adipose tissue-derived mesenchymal stem cells increase skin allograft survival and inhibit Th-17 immune response. PLoS One, 8(10), 2013, e76396.
29. [29] Sbano, P., Cuccia, A., Mazzanti, B., Urbani, S., Giusti, B., Lapini, I., Rossi, L., Abbate, R., Marseglia, G., Nannetti, G., Torricelli, F., Miracco, C., Bosi, A., Fimiani, M., Saccardi, R., Use of donor bone marrow mesenchymal stem cells for treatment of skin allograft rejection in a preclinical rat model. Arch. Dermatol. Res. 300:3 (2008), 115–124.
30. [30] Engela, A.U., Baan, C.C., Dor, F.J., Weimar, W., Hoogduijn, M.J., On the interactions between mesenchymal stem cells and regulatory T cells for immunomodulation in transplantation. Front. Immunol., 3, 2012, 126.
31. [31] Gebler, A., Zabel, O., Seliger, B., The immunomodulatory capacity of mesenchymal stem cells. Trends Mol. Med. 18:2 (2012), 128–134.
32. [32] Trinchieri, G., Regulatory role of T cells producing both interferon gamma and interleukin 10 in persistent infection. J. Exp. Med. 194:10 (2001), F53–F57.
33. [33] Tanaka, K., Albin, M.J., Yuan, X., Yamaura, K., Habicht, A., Murayama, T., Grimm, M., Waaga, A.M., Ueno, T., Padera, R.F., Yagita, H., Azuma, M., Shin, T., Blazar, B.R., Rothstein, D.M., Sayegh, M.H., Najafian, N., PDL1 is required for peripheral transplantation tolerance and protection from chronic allograft rejection. J. Immunol. 179:8 (2007), 5204–5210.
34. [34] Moravej, A., Karimi, M.H., Geramizadeh, B., Azarpira, N., Zarnani, A., Yaghobi, R., Kalani, M., Khosravi, M., Mesenchymal stem cells increase skin graft survival time and up-regulate PD-L1 expression in splenocytes of mice. Transpl. Immunol., 2016 (in press).
35. [35] Hancharou, A.Y., Antonevich, N.H., DuBuske, L.M., Induction of tolerogenic dendritic cells using co-culture with human olfactory mucosa-derived mesenchymal stem cells. J. Allergy Clin. Immunol., 137(2), 2016, 115.