Fetal and adult multipotent mesenchymal stromal cells are killed by different pathways

References

• Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, . Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–7.
   PubMed Web of Science ®Google Scholar
• 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;98:2396–402.
   PubMed Web of Science ®Google Scholar
• In't Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, . 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;88:845–52.
   PubMed Web of Science ®Google Scholar
• Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, . Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002;30:42–8.
   PubMed Web of Science ®Google Scholar
• Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation. 2003;75:389–97.
   PubMed Web of Science ®Google Scholar
• Maitra B, Szekely E, Gjini K, Laughlin MJ, Dennis J, Haynesworth SE, . Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant. 2004;33:597–604.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol. 2003;57:11–20.
   PubMed Web of Science ®Google Scholar
• Gotherstrom C, Ringden O, Tammik C, Zetterberg E, Westgren M, Le Blanc K. Immunologic properties of human fetal mesenchymal stem cells. Am J Obstet Gynecol. 2004;190: 239–45.
   PubMedGoogle Scholar
• Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res. 2005;305:33–41.
   PubMed Web of Science ®Google Scholar
• Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, . Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA. 2003;100:8407–11.
   PubMed Web of Science ®Google Scholar
• Togel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol. 2005;289:F31–42.
   PubMed Web of Science ®Google Scholar
• Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, . Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005;106:1755–61.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, . Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet. 2008;371:1579–86.
   PubMed Web of Science ®Google Scholar
• Ringden O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lonnies H, . Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006;81:1390–7.
   PubMed Web of Science ®Google Scholar
• Martin PJ, Uberti JP, Soiffer RJ, Klingemann H, Waller EK and Daly, A.S. Prochymal improves response rates in patients with steroid-refractory acute graft versus host disease (SR-GVHD) involving the liver and gut: results of a randomized, placebo-controlled, multicenter phase III trial in GVHD. Biol Blood Marrow Transplant. 2010;16:S169–70.
   Web of Science ®Google Scholar
• Gotherstrom C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K. Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells. Haematologica. 2005;90:1017–26.
   PubMed Web of Science ®Google Scholar
• Chan J, O'Donoghue K, Gavina M, Torrente Y, Kennea N, Mehmet H, . Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells. 2006;24:1879–91.
   PubMed Web of Science ®Google Scholar
• Guillot PV, Gotherstrom C, Chan J, Kurata H, Fisk NM. Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells. 2007;25:646–54.
   PubMed Web of Science ®Google Scholar
• Guillot PV, De Bari C, Dell'accio F, Kurata H, Polak J, Fisk NM. Comparative osteogenic transcription profiling of various fetal and adult mesenchymal stem cell sources. Differentiation. 2008;76:946–57.
   PubMed Web of Science ®Google Scholar
• Zhang ZY, Teoh SH, Chong MS, Schantz JT, Fisk NM, Choolani MA, . Superior osteogenic capacity for bone tissue engineering of fetal compared to perinatal and adult mesenchymal stem cells. Stem Cells. 2008;27:126–37.
   Web of Science ®Google Scholar
• 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;32:265–72.
   PubMed Web of Science ®Google Scholar
• Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation. 2003;76:1208–13.
   PubMed Web of Science ®Google Scholar
• Poggi A, Prevosto C, Massaro AM, Negrini S, Urbani S, Pierri I, . Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: role of NKp30 and NKG2D receptors. J Immunol. 2005;175:6352–60.
   PubMed Web of Science ®Google Scholar
• 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;107:1484–90.
   PubMed Web of Science ®Google Scholar
• Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, . Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells. 2006;24:386–98.
   PubMed Web of Science ®Google Scholar
• Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells. 2006;24:74–85.
   PubMed Web of Science ®Google Scholar
• 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;111:1327–33.
   PubMed Web of Science ®Google Scholar
• Poggi A, Prevosto C, Zancolli M, Canevali P, Musso A, Zocchi MR. NKG2D and natural cytotoxicity receptors are involved in natural killer cell interaction with self-antigen presenting cells and stromal cells. Ann NY Acad Sci. 2007;1109: 47–57.
   PubMedGoogle Scholar
• Smyth MJ, Hayakawa Y, Takeda K, Yagita H. New aspects of natural-killer cell surveillance and therapy of cancer. Nat Rev Cancer. 2002;2:850–61.
   PubMed Web of Science ®Google Scholar
• Takeda K, Hayakawa Y, Smyth MJ, Kayagaki N, Yamaguchi N, Kakuta S, . Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat Med. 2001;7: 94–100.
   PubMed Web of Science ®Google Scholar
• Berg M, Lundqvist A, McCoy P Jr, Samsel L, Fan Y, Tawab A, . Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy. 2009;11:341–55.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Gotherstrom C, Ringden O, Hassan M, McMahon R, Horwitz E, . Fetal mesenchymal stem-cell engraftment in bone after in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation. 2005;79:1607–14.
   PubMed Web of Science ®Google Scholar
• Grassi F, Meneveri R, Gullberg M, Lopalco L, Rossi GB, Lanza P, . Human immunodeficiency virus type 1 gp120 mimics a hidden monomorphic epitope borne by class I major histocompatibility complex heavy chains. J Exp Med. 1991; 174:53–62.
   PubMed Web of Science ®Google Scholar
• Decker T, Lohmann-Matthes ML. A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods. 1988;115:61–9.
   PubMed Web of Science ®Google Scholar
• Korzeniewski C, Callewaert DM. An enzyme-release assay for natural cytotoxicity. J Immunol Methods. 1983;64:313–20.
   PubMed Web of Science ®Google Scholar
• Rasmusson I, Uhlin M, Le Blanc K, Levitsky V. Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes. J Leukoc Biol. 2007;82:887–93.
   PubMed Web of Science ®Google Scholar
• Kennea NL, Stratou C, Naparus A, Fisk NM, Mehmet H. Functional intrinsic and extrinsic apoptotic pathways in human fetal mesenchymal stem cells. Cell Death Differ. 2005;12:1439–41.
   Google Scholar
• Sasportas LS, Kasmieh R, Wakimoto H, Hingtgen S, van de Water JA, Mohapatra G, . Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc Natl Acad Sci USA. 2009;106: 4822–7.
   PubMed Web of Science ®Google Scholar
• Szegezdi E, O'Reilly A, Davy Y, Vawda R, Taylor DL, Murphy M, . Stem cells are resistant to TRAIL receptor-mediated apoptosis. J Cell Mol Med. 2008;13:4409–14.
   Google Scholar
• de Fries RU, Golub SH. Characteristics and mechanism of IFN-gamma-induced protection of human tumor cells from lysis by lymphokine-activated killer cells. J Immunol. 1988;140: 3686–93.
   PubMed Web of Science ®Google Scholar
• Maio M, Altomonte M, Tatake R, Zeff RA, Ferrone S. Reduction in susceptibility to natural killer cell-mediated lysis of human FO-1 melanoma cells after induction of HLA class I antigen expression by transfection with B2m gene. J Clin Invest. 1991;88:282–9.
   PubMed Web of Science ®Google Scholar
• Ramirez R, Solana R, Carracedo J, Alonso MC, Pena J. Mechanisms involved in NK resistance induced by interferon-gamma. Cell Immunol. 1992;140:248–56.
   PubMedGoogle Scholar
• Bui JD, Carayannopoulos LN, Lanier LL, Yokoyama WM, Schreiber RD. IFN-dependent down-regulation of the NKG2D ligand H60 on tumors. J Immunol. 2006;176:905–13.
   PubMedGoogle Scholar
• Taylor PA, McElmurry RT, Lees CJ, Harrison DE, Blazar BR. Allogenic fetal liver cells have a distinct competitive engraftment advantage over adult bone marrow cells when infused into fetal as compared with adult severe combined immunodeficient recipients. Blood. 2002;99:1870–2.
   PubMedGoogle Scholar
• Fukada S, Miyagoe-Suzuki Y, Tsukihara H, Yuasa K, Higuchi S, Ono S, . Muscle regeneration by reconstitution with bone marrow or fetal liver cells from green fluorescent protein-gene transgenic mice. J Cell Sci. 2002;115:1285–93.
   PubMed Web of Science ®Google Scholar
• Durkin ET, Jones KA, Rajesh D, Shaaban AF. Early chimerism threshold predicts sustained engraftment and NK-cell tolerance in prenatal allogeneic chimeras. Blood. 2008;112: 5245–53.
   Google Scholar