Human mesenchymal stem cells derived from induced pluripotent stem cells down-regulate NK-cell cytolytic machinery

Blood

Volumn 118, Issue 12, 2011, Pages 3254-3262

  Giuliani, Massimo ^a   Oudrhiri, Noufissa ^b,c   Noman, Zaeem M ^d   Vernochet, Amelia ^a   Chouaib, Salem ^d   Azzarone, Bruno ^a   Durrbach, Antoine ^a   Bennaceur Griscelli, Annelise ^b  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b Centre National de la Recherche Scientifique   (France)

^c HÔPITAL PAUL BROUSSE   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOLYSIS; DEGRANULATION; DOWN REGULATION; EMBRYONIC STEM CELL; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; IMMUNOREGULATION; MESENCHYMAL STEM CELL; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TARGET CELL;

EID: 80053217109     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-12-325324     Document Type: Article

References (52)

1. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143-147. (Pubitemid 29282067)
2. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8(9):726-736.
3. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood. 2001;98(8):2396-2402.
4. Gotherstrom C, Ringden O,Westgren M, Tammik C, Le Blanc K. Immunomodulatory effects of human foetal liver-derived mesenchymal stem cells. Bone Marrow Transplant. 2003;32(3):265-272. (Pubitemid 36927077)
5. in 't Anker PS, Noort WA, Scherjon SA, et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica. 2003;88(8):845-852. (Pubitemid 37128084)
6. in't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells. 2004;22(7):1338-1345.
7. Li CD, Zhang WY, Li HL, et al. Mesenchymal stem cells derived from human placenta suppress allogeneic umbilical cord blood lymphocyte proliferation. Cell Res. 2005;15(7):539-547. (Pubitemid 41653924)
8. Barberi T, Willis LM, Socci ND, Studer L. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med. 2005;2(6):e161.
9. Brown SE, Tong W, Krebsbach PH. The derivation of mesenchymal stem cells from human embryonic stem cells. Cells Tissues Organs. 2009;189(1-4):256-260.
10. Olivier EN, Rybicki AC, Bouhassira EE. Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells. 2006;24(8):1914-1922. (Pubitemid 44474167)
11. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4):1815-1822. (Pubitemid 40223708)
12. Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99(10):3838-3843. (Pubitemid 34534559)
13. Le Blanc K, Rasmusson I, Gotherstrom C, et al. Mesenchymal stem cells inhibit the expression of CD25 (interleukin-2 receptor) and CD38 on phytohaemagglutinin-activated lymphocytes. Scand J Immunol. 2004;60(3):307-315. (Pubitemid 39141263)
14. Huangfu D, Osafune K, Maehr R, et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol. 2008;26(11):1269-1275.
15. Maherali N, Sridharan R, Xie W, et al. Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell. 2007;1(1):55-70.
16. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature. 2007;448(7151):313-317. (Pubitemid 47080336)
17. Park IH, Lerou PH, Zhao R, Huo H, Daley GQ. Generation of human-induced pluripotent stem cells. Nat Protoc. 2008;3(7):1180-1186.
18. Wernig M, Meissner A, Foreman R, et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature. 2007;448(7151):318- 324. (Pubitemid 47080337)
19. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318(5858):1917-1920.
20. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282(5391):1145-1147. (Pubitemid 28516247)
21. Amabile G, Meissner A. Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol Med. 2009;15(2):59-68.
22. Nishikawa S, Goldstein RA, Nierras CR. The promise of human induced pluripotent stem cells for research and therapy. Nat Rev Mol Cell Biol. 2008;9(9):725-729.
23. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell. 2007;1(1):39-49. (Pubitemid 46865811)
24. Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005;202(7):1001-1012. (Pubitemid 41396899)
25. Trivedi P, Hematti P. Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp Hematol. 2008;36(3):350-359.
26. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, 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(4):1484-1490. (Pubitemid 43242385)
27. Davis DM, Chiu I, Fassett M, Cohen GB, Mandelboim O, Strominger JL. The human natural killer cell immune synapse. Proc Natl Acad Sci U SA. 1999;96(26):15062-15067. (Pubitemid 30019765)
28. Orange JS, Harris KE, Andzelm MM, Valter MM, Geha RS, Strominger JL. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc Natl Acad Sci U S A. 2003;100(24):14151-14156. (Pubitemid 37499206)
29. Vyas YM, Maniar H, Dupont B. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol Rev. 2002;189:161-178. (Pubitemid 35448951)
30. Vivier E. Nunes JA, Vely F. Natural killer cell signaling pathways. Science. 2004;306(5701):1517-1519. (Pubitemid 39564941)
31. Wei S, Gamero AM, Liu JH, et al. Control of lytic function of mitogen-activated protein kinase/extracellular regulatory kinase 2 (ERK2) in a human natural killer cell line: identification of perforin and granzyme B mobilization by functional ERK2. J Exp Med. 1998;187(11):1753-1765.
32. Zompi S, Colucci F. Anatomy of a murder-signal transduction pathways leading to activation of natural killer cells. Immunol Lett. 2005;97(1):31-39. (Pubitemid 40038852)
33. Nasef A, Mathieu N, Chapel A, et al. Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G. Transplantation. 2007;84(2):231-237. (Pubitemid 47205757)
34. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, 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(3):1327-1333. (Pubitemid 351213419)
35. Crop MJ, Korevaar SS, De Kuiper R, et al. Human mesenchymal stem cells are susceptible to lysis by CD8+ T-cells and NK cells [published online ahead of print March 7, 2011]. Cell Transplant. doi: 10.3727/096368910X564076.
36. Yen BL, Chang CJ, Liu KJ, et al. Brief Report-human embryonic stem cell-derived mesenchymal progenitors (EMPs) possess strong immunosuppressive effects towards natural killer cells as well as T Lymphocytes. Stem Cells. 2009;27(2):451-456.
37. Bartholomew A, Sturgeon C, Siatskas M, et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002;30(1):42-48. (Pubitemid 34059216)
38. Koc ON, Gerson SL, Cooper BW, et al. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J Clin Oncol. 2000;18(2):307-316. (Pubitemid 30056419)
39. Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004;363(9419):1439-1441. (Pubitemid 38586721)
40. Ringden O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006;81(10):1390-1397. (Pubitemid 43847148)
41. Ruggeri L, Capanni M, Urbani E, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097-2100. (Pubitemid 34229476)
42. Kroemer A, Edtinger K, Li XC. The innate natural killer cells in transplant rejection and tolerance induction. Curr Opin Organ Transplant. 2008;13(4):339-343.
43. Ljunggren HG, Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today. 1990;11(7):237-244. (Pubitemid 20198988)
44. Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol. 2001;1(1):41-49. (Pubitemid 33741974)
45. Long EO. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol. 1999;17:875-904. (Pubitemid 29241142)
46. Moretta L, Moretta A. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J. 2004;23(2):255-259. (Pubitemid 38294490)
47. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131(5):861-872. (Pubitemid 350138099)
48. Chan EM, Ratanasirintrawoot S, Park IH, et al. Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells. Nat Biotechnol. 2009;27(11):1033-1037.
49. Cho HJ, Lee CS, Kwon YW, et al. Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation. Blood. 2010;116(3):386-395.
50. Sidhu KS. New approaches for the generation of induced pluripotent stem cells. Expert Opin Biol Ther. 2011;11(5):569-579.
51. Si-Tayeb K, Noto FK, Sepac A, et al. Generation of human induced pluripotent stem cells by simple transient transfection of plasmid DNA encoding reprogramming factors. BMC Dev Biol. 2010;10:81.
52. Sun N, Longaker MT, Wu JC. Human iPS cell-based therapy: considerations before clinical applications. Cell Cycle. 2010;9(5):880-885.