MSC and innate immune cell interactions: A lesson from human decidua

Immunology Letters

Volumn 168, Issue 2, 2015, Pages 170-174

  Vacca, Paola ^a   Montaldo, Elisa ^b   Vitale, Chiara ^a,c   Croxatto, Daniele ^a   Moretta, Lorenzo ^b   Mingari, Maria Cristina ^a,c  

^a UNIVERSITY OF GENOA   (Italy)

^b G GASLINI INSTITUTE   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

Decidual stromal cells; Feto maternal tolerance; Innate immunity; Innate lymphoid cells; NK cells; Pregnancy

Indexed keywords

GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOCLAST DIFFERENTIATION FACTOR; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL INTERACTION; CELL POPULATION; CELL PROLIFERATION; DECIDUA; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INNATE IMMUNITY; LEUKOCYTE MIGRATION; LYMPHOID CELL; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOLECULAR INTERACTION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; SIGNAL TRANSDUCTION; STROMA CELL; T LYMPHOCYTE ACTIVATION; BIOLOGICAL MODEL; CELL COMMUNICATION; CYTOLOGY; FEMALE; IMMUNE SYSTEM; IMMUNOLOGY; MESENCHYMAL STROMA CELL; PLACENTA; PREGNANCY;

CELL COMMUNICATION; DECIDUA; FEMALE; HUMANS; IMMUNE SYSTEM; MESENCHYMAL STROMAL CELLS; MODELS, IMMUNOLOGICAL; PLACENTA; PREGNANCY; STROMAL CELLS;

EID: 84949624000     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2015.05.006     Document Type: Article

References (66)

1. Balsamo M., Scordamaglia F., Pietra G., Manzini C., Cantoni C., Boitano M., et al. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:20847-20852.
2. Deans R.J., Moseley A.B. Mesenchymal stem cells: biology and potential clinical uses. Exp. Hematol. 2000, 28:875-884.
3. 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. 2013, 43:1862-1872.
4. Erices A., Conget P., Minguell J.J. Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 2000, 109:235-242.
5. Gronthos S., Franklin D.M., Leddy H.A., Robey P.G., Storms R.W., Gimble J.M. Surface protein characterization of human adipose tissue-derived stromal cells. J. Cell. Physiol. 2001, 189:54-63.
6. Olivares E.G., Montes M.J., Oliver C., Galindo J.A., Ruiz C. Cultured human decidual stromal cells express B7-1 (CD80) and B7-2 (CD86) and stimulate allogeneic T cells. Biol. Reprod. 1997, 57:609-615.
7. Uccelli A., Moretta L., Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur. J. Immunol. 2006, 36:2566-2573.
8. Xu X., Wang Q., Deng B., Wang H., Dong Z., Qu X., et al. Monocyte chemoattractant protein-1 secreted by decidual stromal cells inhibits NK cells cytotoxicity by up-regulating expression of SOCS3. PLOS ONE 2012, 7:e41869.
9. Kopen G.C., Prockop D.J., Phinney D.G. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:10711-10716.
10. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
11. Liu Z.J., Zhuge Y., Velazquez O.C. Trafficking and differentiation of mesenchymal stem cells. J. Cell. Biochem. 2009, 106:984-991.
12. Amsen D., Blander J.M., Lee G.R., Tanigaki K., Honjo T., Flavell R.A. Instruction of distinct CD4T helper cell fates by different notch ligands on antigen-presenting cells. Cell 2004, 117:515-526.
13. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006, 107:367-372.
14. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002, 99:3838-3843.
15. Liotta F., Angeli R., Cosmi L., Fili L., Manuelli C., Frosali F., et al. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells 2008, 26:279-289.
16. Spaggiari G.M., Abdelrazik H., Becchetti F., Moretta L. MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2. Blood 2009, 113:6576-6583.
17. Spaggiari G.M., Capobianco A., Abdelrazik H., Becchetti F., Mingari M.C., Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008, 111:1327-1333.
18. Glennie S., Soeiro I., Dyson P.J., Lam E.W., Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005, 105:2821-2827.
19. Ramasamy R., Fazekasova H., Lam E.W., Soeiro I., Lombardi G., Dazzi F. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation 2007, 83:71-76.
20. Spaggiari G.M., Capobianco A., Becchetti S., Mingari M.C., Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006, 107:1484-1490.
21. Augello A., Tasso R., Negrini S.M., Amateis A., Indiveri F., Cancedda R., et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur. J. Immunol. 2005, 35:1482-1490.
22. Kogler G., Radke T.F., Lefort A., Sensken S., Fischer J., Sorg R.V., et al. Cytokine production and hematopoiesis supporting activity of cord blood-derived unrestricted somatic stem cells. Exp. Hematol. 2005, 33:573-583.
23. Krampera M., Cosmi L., Angeli R., Pasini A., Liotta F., Andreini A., et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006, 24:386-398.
24. Ren G., Zhang L., Zhao X., Xu G., Zhang Y., Roberts A.I., et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008, 2:141-150.
25. Aggarwal S., Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005, 105:1815-1822.
26. Resnick I.B., Barkats C., Shapira M.Y., Stepensky P., Bloom A.I., Shimoni A., et al. Treatment of severe steroid resistant acute GVHD with mesenchymal stromal cells (MSC). Am. J. Blood Res. 2013, 3:225-238.
27. von Bonin M., Stolzel F., Goedecke A., Richter K., Wuschek N., Holig K., et al. Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysate-containing medium. Bone Marrow Transplant. 2009, 43:245-251.
28. Munoz-Suano A., Hamilton A.B., Betz A.G. Gimme shelter: the immune system during pregnancy. Immunol. Rev. 2011, 241:20-38.
29. Trowsdale J., Betz A.G. Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat. Immunol. 2006, 7:241-246.
30. Saito S., Nakashima A., Shima T., Ito M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am. J. Reprod. Immunol. 2010, 63:601-610.
31. Dimitrov R., Kyurkchiev D., Timeva T., Yunakova M., Stamenova M., Shterev A., et al. First-trimester human decidua contains a population of mesenchymal stem cells. Fertil. Steril. 2010, 93:210-219.
32. Liu W., Morschauser A., Zhang X., Lu X., Gleason J., He S., et al. Human placenta-derived adherent cells induce tolerogenic immune responses. Clin. Transl. Immunol. 2014, 3:e14.
33. Karlsson H., Erkers T., Nava S., Ruhm S., Westgren M., Ringden O. Stromal cells from term fetal membrane are highly suppressive in allogeneic settings in vitro. Clin. Exp. Immunol. 2012, 167:543-555.
34. Croxatto D., Vacca P., Canegallo F., Conte R., Venturini P.L., Moretta L., et al. Stromal cells from human decidua exert a strong inhibitory effect on NK cell function and dendritic cell differentiation. PLOS ONE 2014, 9:e89006.
35. Oliver C., Montes M.J., Galindo J.A., Ruiz C., Olivares E.G. Human decidual stromal cells express alpha-smooth muscle actin and show ultrastructural similarities with myofibroblasts. Hum. Reprod. 1999, 14:1599-1605.
36. King A. Uterine leukocytes and decidualization. Hum. Reprod. Update 2000, 6:28-36.
37. Can A., Tekelioglu M., Baltaci A. Expression of desmin and vimentin intermediate filaments in human decidual cells during first trimester pregnancy. Placenta 1995, 16:261-275.
38. Macias M.I., Grande J., Moreno A., Dominguez I., Bornstein R., Flores A.I. Isolation and characterization of true mesenchymal stem cells derived from human term decidua capable of multilineage differentiation into all 3 embryonic layers. Am. J. Obstet. Gynecol. 2010, 203:495. e9-e495. e423.
39. Nancy P., Tagliani E., Tay C.S., Asp P., Levy D.E., Erlebacher A. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science 2012, 336:1317-1321.
40. Erkers T., Nava S., Yosef J., Ringden O., Kaipe H. Decidual stromal cells promote regulatory T cells and suppress alloreactivity in a cell contact-dependent manner. Stem Cells Dev. 2013, 22:2596-2605.
41. Barabino S., Rolando M., Bentivoglio G., Mingari C., Zanardi S., Bellomo R., et al. Role of amniotic membrane transplantation for conjunctival reconstruction in ocular-cicatricial pemphigoid. Ophthalmology 2003, 110:474-480.
42. von Versen-Hoynck F., Hesselbarth U., Moller D.E. Application of sterilised human amnion for reconstruction of the ocular surface. Cell Tissue Bank. 2004, 5:57-65.
43. Kesting M.R., Wolff K.D., Hohlweg-Majert B., Steinstraesser L. The role of allogenic amniotic membrane in burn treatment. J. Burn Care Res. 2008, 29:907-916.
44. Moodley Y., Ilancheran S., Samuel C., Vaghjiani V., Atienza D., Williams E.D., et al. Human amnion epithelial cell transplantation abrogates lung fibrosis and augments repair. Am. J. Respir. Crit. Care Med. 2010, 182:643-651.
45. Vacca P., Mingari M.C., Moretta L. Natural killer cells in human pregnancy. J. Reprod. Immunol. 2013, 97:14-19.
46. Vacca P., Moretta L., Moretta A., Mingari M.C. Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. 2011, 32:517-523.
47. Parham P., Moffett A., Variable N.K. cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 2013, 13:133-144.
48. Spits H., Artis D., Colonna M., Diefenbach A., Di Santo J.P., Eberl G., et al. Innate lymphoid cells - a proposal for uniform nomenclature. Nat. Rev. Immunol. 2013, 13:145-149.
49. Montaldo E., Vacca P., Moretta L., Mingari M.C. Development of human natural killer cells and other innate lymphoid cells. Semin. Immunol. 2014, 26:107-113.
50. Vacca P., Montaldo E., Croxatto D., Loiacono F., Canegallo F., Venturini P.L., et al. Identification of diverse innate lymphoid cells in human decidua. Mucosal Immunol. 2015, 8:254-264.
51. Kammerer U., Eggert A.O., Kapp M., McLellan A.D., Geijtenbeek T.B., Dietl J., et al. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am. J. Pathol. 2003, 162:887-896.
52. Laskarin G., Cupurdija K., Tokmadzic V.S., Dorcic D., Dupor J., Juretic K., et al. The presence of functional mannose receptor on macrophages at the maternal-fetal interface. Hum. Reprod. 2005, 20:1057-1066.
53. Laskarin G., Redzovic A., Rubesa Z., Mantovani A., Allavena P., Haller H., et al. Decidual natural killer cell tuning by autologous dendritic cells. Am. J. Reprod. Immunol. 2008, 59:433-445.
54. Santoni A., Carlino C., Stabile H., Gismondi A. Mechanisms underlying recruitment and accumulation of decidual NK cells in uterus during pregnancy. Am. J. Reprod. Immunol. 2008, 59:417-424.
55. Carlino C., Stabile H., Morrone S., Bulla R., Soriani A., Agostinis C., et al. Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy. Blood 2008, 111:3108-3115.
56. - NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:3378-3383.
57. Cerdeira A.S., Rajakumar A., Royle C.M., Lo A., Husain Z., Thadhani R.I., et al. Conversion of peripheral blood NK cells to a decidual NK-like phenotype by a cocktail of defined factors. J. Immunol. 2013, 190:3939-3948.
58. Hu W.T., Li M.Q., Liu W., Jin L.P., Li D.J., Zhu X.Y. IL-33 enhances proliferation and invasiveness of decidual stromal cells by up-regulation of CCL2/CCR2 via NF-kappaB and ERK1/2 signaling. Mol. Hum. Reprod. 2014, 20:358-372.
59. Wang S., Cao C., Piao H., Li Y., Tao Y., Zhang X., et al. Tim-3 protects decidual stromal cells from toll-like receptor-mediated apoptosis and inflammatory reactions and promotes Th2 bias at the maternal-fetal interface. Sc. Rep. 2015, 5:9013.
60. Li Y.H., Zhou W.H., Tao Y., Wang S.C., Jiang Y.L., Zhang D., et al. The Galectin-9/Tim-3 pathway is involved in the regulation of NK cell function at the maternal-fetal interface in early pregnancy. Cell. Mol. Immunol. 2015, 10.1038/cmi.2014.126.
61. Male V., Hughes T., McClory S., Colucci F., Caligiuri M.A., Moffett A. Immature NK cells, capable of producing IL-22, are present in human uterine mucosa. J. Immunol. 2010, 185:3913-3918.
62. + hematopoietic precursors are present in human decidua and differentiate into natural killer cells upon interaction with stromal cells. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2402-2407.
63. Chiossone L., Vacca P., Orecchia P., Croxatto D., Damonte P., Astigiano S., et al. In vivo generation of decidual natural killer cells from resident hematopoietic progenitors. Haematologica 2014, 99:448-457.
64. + myelomonocytic cells results in induction of Tregs and immunosuppression. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11918-11923.
65. Meng Y.H., Li H., Chen X., Liu L.B., Shao J., Chang K.K., et al. RANKL promotes the growth of decidual stromal cells in an autocrine manner via CCL2/CCR2 interaction in human early pregnancy. Placenta 2013, 34:663-671.
66. Blois S.M., Barrientos G., Garcia M.G., Orsal A.S., Tometten M., Cordo-Russo R.I., et al. Interaction between dendritic cells and natural killer cells during pregnancy in mice. J. Mol. Med. 2008, 86:837-852.