CD150 high Bone Marrow Tregs Maintain Hematopoietic Stem Cell Quiescence and Immune Privilege via Adenosine

Cell Stem Cell

Volumn 22, Issue 3, 2018, Pages 445-453.e5

  Hirata, Yuichi ^a   Furuhashi, Kazuhiro ^a   Ishii, Hiroshi ^a   Li, Hao Wei ^a   Pinho, Sandra ^b   Ding, Lei ^a   Robson, Simon C ^c   Frenette, Paul S ^b   Fujisaki, Joji ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ADENOSINE; CD150 ANTIGEN; CD39 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; NEUROPILIN; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FOXP3; SLAMF1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL PROTECTION; CELL SURFACE; CELLS; CONTROLLED STUDY; ENGRAFTMENT; HEMATOPOIETIC STEM CELL; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; INTRAVITAL MICROSCOPY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; IMMUNOLOGY; METABOLISM; STEM CELL NICHE;

ADENOSINE; ANIMALS; BONE MARROW CELLS; HEMATOPOIETIC STEM CELLS; MICE, INBRED C57BL; OXIDATIVE STRESS; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE FAMILY MEMBER 1; STEM CELL NICHE; T-LYMPHOCYTES, REGULATORY;

EID: 85042036471     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2018.01.017     Document Type: Article

References (45)

1. Arpaia, N., Green, J.A., Moltedo, B., Arvey, A., Hemmers, S., Yuan, S., Treuting, P.M., Rudensky, A.Y., A distinct function of regulatory T cells in tissue protection. Cell 162 (2015), 1078–1089.
2. Azab, A.K., Runnels, J.M., Pitsillides, C., Moreau, A.S., Azab, F., Leleu, X., Jia, X., Wright, R., Ospina, B., Carlson, A.L., et al. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 113 (2009), 4341–4351.
3. Bapat, S.P., Myoung Suh, J., Fang, S., Liu, S., Zhang, Y., Cheng, A., Zhou, C., Liang, Y., LeBlanc, M., Liddle, C., et al. Depletion of fat-resident Treg cells prevents age-associated insulin resistance. Nature 528 (2015), 137–141.
4. Burzyn, D., Kuswanto, W., Kolodin, D., Shadrach, J.L., Cerletti, M., Jang, Y., Sefik, E., Tan, T.G., Wagers, A.J., Benoist, C., Mathis, D., A special population of regulatory T cells potentiates muscle repair. Cell 155 (2013), 1282–1295.
5. Cao, H., Heazlewood, S.Y., Williams, B., Cardozo, D., Nigro, J., Oteiza, A., Nilsson, S.K., The role of CD44 in fetal and adult hematopoietic stem cell regulation. Haematologica 101 (2016), 26–37.
6. Chen, J.F., Eltzschig, H.K., Fredholm, B.B., Adenosine receptors as drug targets–what are the challenges?. Nat. Rev. Drug Discov. 12 (2013), 265–286.
7. 14 receptor modulates stress-induced hematopoietic stem/progenitor cell senescence. J. Clin. Invest. 124 (2014), 3159–3171.
8. Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S.E., Benoist, C., Mathis, D., PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 486 (2012), 549–553.
9. Deaglio, S., Dwyer, K.M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J.F., Enjyoji, K., Linden, J., Oukka, M., et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204 (2007), 1257–1265.
10. Ding, L., Morrison, S.J., Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495 (2013), 231–235.
11. Ding, L., Saunders, T.L., Enikolopov, G., Morrison, S.J., Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481 (2012), 457–462.
12. Fontenot, J.D., Rasmussen, J.P., Williams, L.M., Dooley, J.L., Farr, A.G., Rudensky, A.Y., Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 22 (2005), 329–341.
13. Fujisaki, J., Wu, J., Carlson, A.L., Silberstein, L., Putheti, P., Larocca, R., Gao, W., Saito, T.I., Lo Celso, C., Tsuyuzaki, H., et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474 (2011), 216–219.
14. Fukushima, N., Kohno, M., Kato, T., Kawamoto, S., Okuda, K., Misu, Y., Ueda, H., Melittin, a metabostatic peptide inhibiting Gs activity. Peptides 19 (1998), 811–819.
15. Geiger, H., de Haan, G., Florian, M.C., The ageing haematopoietic stem cell compartment. Nat. Rev. Immunol. 13 (2013), 376–389.
16. Hirata, Y., Li, H.W., Takahashi, K., Ishii, H., Sykes, M., Fujisaki, J., MHC class I expression by donor hematopoietic stem cells is required to prevent NK cell attack in allogeneic, but not syngeneic recipient mice. PLoS ONE, 10, 2015, e0141785.
17. Itkin, T., Gur-Cohen, S., Spencer, J.A., Schajnovitz, A., Ramasamy, S.K., Kusumbe, A.P., Ledergor, G., Jung, Y., Milo, I., Poulos, M.G., et al. Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature 532 (2016), 323–328.
18. Ito, H., Kurtz, J., Shaffer, J., Sykes, M., CD4 T cell-mediated alloresistance to fully MHC-mismatched allogeneic bone marrow engraftment is dependent on CD40-CD40 ligand interactions, and lasting T cell tolerance is induced by bone marrow transplantation with initial blockade of this pathway. J. Immunol. 166 (2001), 2970–2981.
19. Jing, L., Tamplin, O.J., Chen, M.J., Deng, Q., Patterson, S., Kim, P.G., Durand, E.M., McNeil, A., Green, J.M., Matsuura, S., et al. Adenosine signaling promotes hematopoietic stem and progenitor cell emergence. J. Exp. Med. 212 (2015), 649–663.
20. Jones, D.L., Wagers, A.J., No place like home: anatomy and function of the stem cell niche. Nat. Rev. Mol. Cell Biol. 9 (2008), 11–21.
21. Josefowicz, S.Z., Lu, L.F., Rudensky, A.Y., Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30 (2012), 531–564.
22. Juntilla, M.M., Patil, V.D., Calamito, M., Joshi, R.P., Birnbaum, M.J., Koretzky, G.A., AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115 (2010), 4030–4038.
23. Kiel, M.J., Yilmaz, O.H., Iwashita, T., Yilmaz, O.H., Terhorst, C., Morrison, S.J., SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121 (2005), 1109–1121.
24. Kunisaki, Y., Bruns, I., Scheiermann, C., Ahmed, J., Pinho, S., Zhang, D., Mizoguchi, T., Wei, Q., Lucas, D., Ito, K., et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502 (2013), 637–643.
25. Levine, A.G., Hemmers, S., Baptista, A.P., Schizas, M., Faire, M.B., Moltedo, B., Konopacki, C., Schmidt-Supprian, M., Germain, R.N., Treuting, P.M., Rudensky, A.Y., Suppression of lethal autoimmunity by regulatory T cells with a single TCR specificity. J. Exp. Med. 214 (2017), 609–622.
26. Lewandowski, D., Barroca, V., Ducongé F., Bayer, J., Van Nhieu, J.T., Pestourie, C., Fouchet, P., Tavitian, B., Roméo, P.H., In vivo cellular imaging pinpoints the role of reactive oxygen species in the early steps of adult hematopoietic reconstitution. Blood 115 (2010), 443–452.
27. Liu, J., Cao, L., Chen, J., Song, S., Lee, I.H., Quijano, C., Liu, H., Keyvanfar, K., Chen, H., Cao, L.Y., et al. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459 (2009), 387–392.
28. Lo Celso, C., Fleming, H.E., Wu, J.W., Zhao, C.X., Miake-Lye, S., Fujisaki, J., Côté D., Rowe, D.W., Lin, C.P., Scadden, D.T., Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457 (2009), 92–96.
29. Maj, T., Wang, W., Crespo, J., Zhang, H., Wang, W., Wei, S., Zhao, L., Vatan, L., Shao, I., Szeliga, W., et al. Oxidative stress controls regulatory T cell apoptosis and suppressor activity and PD-L1-blockade resistance in tumor. Nat. Immunol. 18 (2017), 1332–1341.
30. Miyamoto, K., Araki, K.Y., Naka, K., Arai, F., Takubo, K., Yamazaki, S., Matsuoka, S., Miyamoto, T., Ito, K., Ohmura, M., et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1 (2007), 101–112.
31. Morrison, S.J., Scadden, D.T., The bone marrow niche for haematopoietic stem cells. Nature 505 (2014), 327–334.
32. Nervi, B., Ramirez, P., Rettig, M.P., Uy, G.L., Holt, M.S., Ritchey, J.K., Prior, J.L., Piwnica-Worms, D., Bridger, G., Ley, T.J., DiPersio, J.F., Chemosensitization of acute myeloid leukemia (AML) following mobilization by the CXCR4 antagonist AMD3100. Blood 113 (2009), 6206–6214.
33. Nie, Y., Waite, J., Brewer, F., Sunshine, M.J., Littman, D.R., Zou, Y.R., The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 200 (2004), 1145–1156.
34. Niederkorn, J.Y., See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat. Immunol. 7 (2006), 354–359.
35. Ohta, A., A metabolic immune checkpoint: adenosine in tumor microenvironment. Front. Immunol., 7, 2016, 109.
36. Panduro, M., Benoist, C., Mathis, D., Tissue Tregs. Annu. Rev. Immunol. 34 (2016), 609–633.
37. Pilat, N., Baranyi, U., Klaus, C., Jaeckel, E., Mpofu, N., Wrba, F., Golshayan, D., Muehlbacher, F., Wekerle, T., Treg-therapy allows mixed chimerism and transplantation tolerance without cytoreductive conditioning. Am. J. Transplant. 10 (2010), 751–762.
38. Pilat, N., Klaus, C., Gattringer, M., Jaeckel, E., Wrba, F., Golshayan, D., Baranyi, U., Wekerle, T., Therapeutic efficacy of polyclonal tregs does not require rapamycin in a low-dose irradiation bone marrow transplantation model. Transplantation 92 (2011), 280–288.
39. Rubtsov, Y.P., Rasmussen, J.P., Chi, E.Y., Fontenot, J., Castelli, L., Ye, X., Treuting, P., Siewe, L., Roers, A., Henderson, W.R. Jr., et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28 (2008), 546–558.
40. Rudra, D., Egawa, T., Chong, M.M., Treuting, P., Littman, D.R., Rudensky, A.Y., Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 10 (2009), 1170–1177.
41. Schepers, K., Pietras, E.M., Reynaud, D., Flach, J., Binnewies, M., Garg, T., Wagers, A.J., Hsiao, E.C., Passegué E., Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 13 (2013), 285–299.
42. Schepers, K., Campbell, T.B., Passegué E., Normal and leukemic stem cell niches: insights and therapeutic opportunities. Cell Stem Cell 16 (2015), 254–267.
43. Steiner, D., Brunicki, N., Blazar, B.R., Bachar-Lustig, E., Reisner, Y., Tolerance induction by third-party “off-the-shelf” CD4+CD25+ Treg cells. Exp. Hematol. 34 (2006), 66–71.
44. Sugiyama, T., Kohara, H., Noda, M., Nagasawa, T., Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25 (2006), 977–988.
45. Zou, L., Barnett, B., Safah, H., Larussa, V.F., Evdemon-Hogan, M., Mottram, P., Wei, S., David, O., Curiel, T.J., Zou, W., Bone marrow is a reservoir for CD4+CD25+ regulatory T cells that traffic through CXCL12/CXCR4 signals. Cancer Res. 64 (2004), 8451–8455.