2,691
Views
20
CrossRef citations to date
0
Altmetric
REVIEW ARTICLE

Biotechnological and biomedical applications of mesenchymal stem cells as a therapeutic system

, , , , , , , , & show all
Pages 559-570 | Received 09 Sep 2014, Accepted 20 Sep 2014, Published online: 23 Oct 2014

References

  • Abdi R, Fiorina P, Adra CN, Atkinson M, Sayegh MH. 2008. Immunomodulation by mesenchymal stem cells a potential therapeutic strategy for type 1 diabetes. Diabetes. 57:1759–1767.
  • Aggarwal S, Pittenger MF. 2005. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 105:1815–1822.
  • Akbari A, Mozdarani H, Akhlaghpoor S, Pourfatollah A, Soleimani M. 2007. Evaluation of the homing of human CD34 + cells in mouse bone marrow using clinical MR imaging. Pak J Biol Sci. 10: 833–842.
  • Angoulvant D, Clerc A, Benchalal S, Galambrun C, Farre A, Bertrand Y, Eljaafari A 2004. Human mesenchymal stem cells suppress induction of cytotoxic response to alloantigens. Biorheology. 41:469–476.
  • Arikawa T, Omura K, Morita I 2004. Regulation of bone morphogenetic protein 2 expression by endogenous prostaglandin E2 in human mesenchymal stem cells. J Cell Physiol. 200:400–406.
  • Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, Pennesi G 2005. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol. 35:1482–1490.
  • Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature. 392:245–252.
  • Barry F, Boynton R, Murphy M, Zaia J. 2001. The SH-3 and SH-4 antibodies recognize distinct epitopes on CD73 from human mesenchymal stem cells. Biochem Biophys Res Commun. 289: 519–524.
  • Ben-Ami E, Berrih-Aknin S, Miller A. 2011. Mesenchymal stem cells as an immunomodulatory therapeutic strategy for autoimmune diseases. Autoimmun Rev. 10:410–415.
  • Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, et al 2005. Human mesenchymal stem cells alter antigen-presenting cell maturation, induce T-cell unresponsiveness. Blood. 105: 2214–2219.
  • Bingisser RM, Tilbrook PA, Holt PG, Kees UR 1998. Macrophage- derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol. 160: 5729–5734.
  • Breitbach M, Bostani T, Roell W, Xia Y, Dewald O, Nygren JM, et al. 2007. Potential risks of bone marrow cell transplantation into infarcted hearts. Blood. 110:1362–1369.
  • Bruder SP, Ricalton NS, Boynton RE, Connolly TJ, Jaiswal N, Zaia J, Barry FP. 1998. Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res. 13:655–663.
  • Bühring HJ, Battula VL, Treml S, Schewe B, Kanz L, Vogel W. 2007. Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci. 1106:262–271.
  • Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM 2001. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, bone marrow. Blood. 98:2396–2402.
  • Caplan AI, Dennis JE 2006. Mesenchymal stem cells as trophic mediators. J Cell Biochem. 98:1076–1084.
  • Chamberlain G, Fox J, Ashton B, Middleton J. 2007. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 25:2739–2749.
  • Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, et al. 2006. Human mesenchymal stem cells modulate B-cell functions. Blood. 107:367–372.
  • Dazzi F, Marelli Berg FM 2008. Mesenchymal stem cells for graft versus host disease: Close encounters with T cells. Eur J Immunol. 38:1479–1482.
  • Deans RJ, Moseley AB. 2000. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol. 28:875–884.
  • Delalat B, Pourfathollah AA, Soleimani M, Mozdarani H, Ghaemi SR, Movassaghpour AA, Kaviani S 2009. Isolation, ex vivo expansion of human umbilical cord blood-derived CD34 + stem cells, their cotransplantation with or without mesenchymal stem cells. Hematology. 14:125–132.
  • Deng W, Han Q, Liao L, You S, Deng H, Zhao RC 2005. Effects of allogeneic bone marrow-derived mesenchymal stem cells on T, B lymphocytes from BXSB mice. DNA Cell Biol. 24:458–463.
  • Devine MJ, Mierisch CM, Jang E, Anderson PC, Balian G. 2002. Transplanted bone marrow cells localize to fracture callus in a mouse model. J Orthop Res. 20:1232–1239.
  • Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, et al. 2002. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 99:3838–3843.
  • Ding Y, Xu D, Feng G, Bushell A, Muschel RJ, Wood KJ 2009. Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and-9. Diabetes. 58:1797–1806.
  • Djouad F, Charbonnier LM, Bouffi C, Louis Plence P, Bony C, Apparailly F, et al 2007. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin 6 dependent mechanism. Stem cells. 25:2025–2032.
  • Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, et al. 2003. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 102:3837–3844.
  • Du Z, Wei C, Cheng K, Han B, Yan J, Zhang M, et al. 2013. Mesenchymal stem cell–conditioned medium reduces liver injury, enhances regeneration in reduced-size rat liver transplantation. J Surg Res. 183:907–915.
  • English K, Barry FP, Field-Corbett CP, Mahon BP 2007. IFN-γ and TNF-α differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett. 110:91–100.
  • Fedyk ER, Jones D, Critchley HO, Phipps RP, Blieden TM, Springer TA 2001. Expression of stromal-derived factor-1 is decreased by IL-1, TNF, in dermal wound healing. J Immunol. 166:5749–5754.
  • Fickert S, Fiedler J, Brenner RE. 2004. Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Res Ther. 6:R422–R432.
  • Gebler A, Zabel O, Seliger B. 2012. The immunomodulatory capacity of mesenchymal stem cells. Trends Mol Med.18:128–134.
  • Gerdoni E, Gallo B, Casazza S, Musio S, Bonanni I, Pedemonte E, et al. 2007. Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol. 61:219–227.
  • Ghannam S, Bouffi C, Djouad F, Jorgensen C, Noël D. 2010a. Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications. Stem Cell Res Ther. 1:2.
  • Ghannam S, Pène J, Torcy-Moquet G, Jorgensen C, Yssel H 2010b. Mesenchymal stem cells inhibit human Th17 cell differentiation, function, induce a T regulatory cell phenotype. J Immunol. 185: 302–312.
  • Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F 2005. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 105:2821–2827.
  • Gonen-Gross T, Goldman-Wohl D, Huppertz B, Lankry D, Greenfield C, Natanson-Yaron S, et al. 2010. Inhibitory NK receptor recognition of HLA-G: regulation by contact residues and by cell specific expression at the fetal-maternal interface. PLoS One. 5:e8941.
  • González MA, Gonzalez Rey E, Rico L, Büscher D, Delgado M 2009. Treatment of experimental arthritis by inducing immune tolerance with human adipose derived mesenchymal stem cells. Arthritis Rheum. 60:1006–1019.
  • Groh ME, Maitra B, Szekely E, Koç ON 2005. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol. 33:928–934.
  • Gronthos S, Graves S, Ohta S, Simmons P. 1994. The STRO-1 + fraction of adult human bone marrow contains the osteogenic precursors. Blood84:4164–4173.
  • Groth CG, Ringdén O. 1984. Transplantation in relation to the treatment of inherited disease. Transplantation. 38:319–326.
  • Hirata Y, Sugita T, Gyo K, Yanagihara N 1993. Experimental vestibular neuritis induced by herpes simplex virus. Acta Otolaryngol Suppl. 113:79–81.
  • Hirohata S, Kikuchi H 2003. Behcet's disease. Arthritis Res Ther. 5: 139–146.
  • Hoogduijn MJ, Popp F, Verbeek R, Masoodi M, Nicolaou A, Baan C, Dahlke M-H 2010. The immunomodulatory properties of mesenchymal stem cells, their use for immunotherapy. Int Immunopharmacol. 10:1496–1500.
  • Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, et al. 2002. Isolated allogeneic bone marrow-derived mesenchymal cells engraft, stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci U S A. 99:8932–8937.
  • Horwitz EM, Maziarz RT, Kebriaei P 2011. MSCs in hematopoietic cell transplantation. Biol Blood Marrow Transplant. 17:S21–S29.
  • Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, et al. 1999. Transplantability, therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 5:309–313.
  • Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, et al. 2001. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood. 97:1227–1231.
  • Imhof BA, Aurrand-Lions M 2004. Adhesion mechanisms regulating the migration of monocytes. Nat Rev Immunol. 4:432–444.
  • Ivanova-Todorova E, Bochev I, Mourdjeva M, Dimitrov R, Bukarev D, Kyurkchiev S, et al. 2009. Adipose tissue-derived mesenchymal stem cells are more potent suppressors of dendritic cells differentiation compared to bone marrow-derived mesenchymal stem cells. Immunol Lett. 126:37–42.
  • Jiang X-X, Zhang Y, Liu B, Zhang S-X, Wu Y, Yu X-D, Mao N. 2005. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 105: 4120–4126.
  • Jorgensen C, Gordeladze J, Noel D. 2004. Tissue engineering through autologous mesenchymal stem cells. Curr Opin Biotechnol. 15:406–410.
  • Kapsimali VD, Kanakis MA, Vaiopoulos GA, Kaklamanis PG 2010. Etiopathogenesis of Behçet's disease with emphasison the role of immunological aberrations. Clin Rheumatol. 29:1211–1216.
  • Kim J, Hematti P. 2009. Mesenchymal stem cell–educated macrophages: A novel type of alternatively activated macrophages. Exp Hematol. 37:1445–1453.
  • Kitoh H, Kitakoji T, Tsuchiya H, Mitsuyama H, Nakamura H, Katoh M, Ishiguro N. 2004. Transplantation of marrow-derived mesenchymal stem cells and platelet-rich plasma during distraction osteogenesis—a preliminary result of three cases. Bone. 35:892–898.
  • Kong Q-F, Sun B, Bai S-S, Zhai D-X, Wang G-Y, Liu Y-M, et al. 2009. Administration of bone marrow stromal cells ameliorates experimental autoimmune myasthenia gravis by altering the balance of Th1/Th2/Th17/Treg cell subsets through the secretion of TGF. J Neuroimmunol. 207:83–91.
  • Koç ON, Gerson SL, Cooper BW, Dyhouse SM, Haynesworth SE, Caplan AI, Lazarus HM 2000. 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. 18:307–307.
  • Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, et al. 2006a. Role for interferon in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells. 24: 386–398.
  • Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, Dazzi F 2003. Bone marrow mesenchymal stem cells inhibit the response of naive, memory antigen-specific T cells to their cognate peptide. Blood. 101:3722–3729.
  • Krampera M, Pasini A, Pizzolo G, Cosmi L, Romagnani S, Annunziato F. 2006b. Regenerative and immunomodulatory potential of mesenchymal stem cells. Curr Opin Pharmacol. 6:435–441.
  • Krivit W, Peters C, Shapiro EG. 1999. Bone marrow transplantation as effective treatment of central nervous system disease in globoid cell leukodystrophy, metachromatic leukodystrophy, adrenoleukodystrophy, mannosidosis, fucosidosis, aspartylglucosaminuria, Hurler, Maroteaux-Lamy, and Sly syndromes, and Gaucher disease type III. Curr Opin Neurol. 12:167–176.
  • Lazarus H, Haynesworth S, Gerson S, Rosenthal N, Caplan A 1995. Ex vivo expansion, subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 16: 557–564.
  • Le Blanc K, Rasmusson I, Götherström C, Seidel C, Sundberg B, Sundin M, et al. 2004a. Mesenchymal stem cells inhibit the expression of CD25 (interleukin 2 receptor), CD38 on phytohaemagglutinin activated lymphocytes. Scand J Immunol. 60:307–315.
  • Le Blanc K, Rasmusson I, Sundberg B, Götherström C, Hassan M, Uzunel M, Ringdén O 2004b. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 363:439–1441.
  • Le Blanc K, Ringden O 2007. Immunomodulation by mesenchymal stem cells, clinical experience. J Intern Med. 262:509–525.
  • Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringdén O. 2003. HLA expression and immunologic propertiesof differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 31: 890–896.
  • Le Blanc K, Tammik L, Sundberg B, Haynesworth S, Ringden O 2003. Mesenchymal stem cells inhibit, stimulate mixed lymphocyte cultures, mitogenic responses independently of the major histocompatibility complex. Scand J Immunol. 57:11–20.
  • Lee JW, Gupta N, Serikov V, Matthay MA. 2009. Potential application of mesenchymal stem cells in acute lung injury. Expert Opin Biol Ther. 9:1259–1270.
  • Lee ST, Jang JH, Cheong JW, Kim JS, Maemg HY, Hahn JS, et al. 2002. Treatment of high risk acute myelogenous leukaemia by myeloablative chemoradiotherapy followed by co infusion of T cell depleted haematopoietic stem cells and culture expanded marrow mesenchymal stem cells from a related donor with one fully mismatched human leucocyte antigen haplotype. Br J Haematol. 118:1128–1131.
  • Lim J-H, Kim J-S, Yoon I-H, Shin J-S, Nam H-Y, Yang S-H, et al. 2010. Immunomodulation of delayed-type hypersensitivity responses by mesenchymal stem cells is associated with bystander T cell apoptosis in the draining lymph node. J Immunol. 185: 4022–4029.
  • Liu J, Lu X, Wan L, Li Y, Li S, Zeng L, et al. 2004. Suppression of human peripheral blood lymphocyte proliferation by immortalized mesenchymal stem cells derived from bone marrow of Banna Minipig inbred-line. Transplant Proc. 36:3272–3275.
  • Lotfinegad P. 2014. Immunomodulatory nature and site specific affinity of mesenchymal stem cells: a hope in cell therapy. Adv Pharm Bull. 4:5.
  • Luster AD, Alon R, von Andrian UH 2005. Immune cell migration in inflammation: present, future therapeutic targets. Nat Immunol. 6:1182–1190.
  • MacDonald GI, Augello A, De Bari C. 2011. Role of mesenchymal stem cells in reestablishing immunologic tolerance in autoimmune rheumatic diseases. Arthritis Rheum. 63:2547–2557.
  • Maccario R, Podestà M, Moretta A, Cometa A, Comoli P, Montagna D, et al. 2005. Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4 + T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica. 90:516–525.
  • Maitra B, Szekely E, Gjini K, Laughlin M, Dennis J, Haynesworth S, Koc O. 2004. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant. 33:597–604.
  • Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR, Mosca JD. 2003. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci. 10:228–241.
  • Mazaheri T, Esmaeilzadeh A, Mirzaei MH 2012. Introducing the immunomodulatory effects of mesenchymal stem cells in an experimental model of Behçet's disease. J Med Hypotheses Ideas. 6:23–27.
  • Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, et al. 1998. Impaired B-lymphopoiesis, myelopoiesis, derailed cerebellar neuron migration in CXCR4-and SDF-1-deficient mice. Proc Natl Acad Sci U S A. 95:9448–9453.
  • McTaggart SJ, Atkinson K 2007. Mesenchymal stem cells: Immunobiology, therapeutic potential in kidney disease (Review Article). Nephrology (Carlton). 12:44–52.
  • Meisel R, Zibert A, Laryea M, Göbel U, Däubener W, Dilloo D 2004. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase–mediated tryptophan degradation. Blood. 103:4619–4621.
  • Mellman I, Steinman RM. 2001. Dendritic cells-specialized and regulated antigen processing machines. Cell. 106:255–258.
  • Mohammadian M, Shamsasenjan K. 2013. Mesenchymal stem cells: new aspect in cell-based regenerative therapy. Adv Pharm Bull. 3:433.
  • Moriscot C, de Fraipont F, Richard MJ, Marchand M, Savatier P, Bosco D, et al. 2005. Human bone marrow mesenchymal stem cells can express insulin and key transcription factors of the endocrine pancreas developmental pathway upon genetic and/or microenvironmental manipulation in vitro. Stem Cells. 23:594–603.
  • Mueller SM, Glowacki J. 2001. Age related decline in the osteogenic potential of human bone marrow cells cultured in three dimensional collagen sponges. J Cell Biochem. 82:583–590.
  • Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. 1998. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 281:191–1193.
  • Nagai Y, Garrett KP, Ohta S, Bahrun U, Kouro T, Akira S, et al. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity. 24:801–812.
  • Nasef A, Zhang Y, Mazurier C, Bouchet S, Bensidhoum M, Francois S, et al. 2009. Selected Stro 1 enriched bone marrow stromal cells display a major suppressive effect on lymphocyte proliferation. Int J Lab Hematol. 31:9–19.
  • Nauta AJ, Fibbe WE 2007. Immunomodulatory properties of mesenchymal stromal cells. Blood. 110:3499–3506.
  • Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. 2006. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol. 177:2080–2087.
  • Otto W, Rao J. 2004. Tomorrow’s skeleton staff: mesenchymal stem cells and the repair of bone and cartilage. Cell Prolif. 37:97–110.
  • Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, et al. 1999. Dependence of human stem cell engraftment, repopulation of NOD/SCID mice on CXCR4. Science. 283:845–848.
  • Pevsner-Fischer M, Morad V, Cohen-Sfady M, Rousso-Noori L, Zanin-Zhorov A, Cohen S, et al. 2007. Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood. 109:1422–1432.
  • Pittenger MF, Martin BJ. 2004. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res. 95:9–20.
  • Potian JA, Aviv H, Ponzio NM, Harrison JS, Rameshwar P. 2003. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol. 171:3426–3434.
  • Pountos I, Corscadden D, Emery P, Giannoudis PV. 2007. Mesenchymal stem cell tissue engineering: techniques for isolation, expansion and application. Injury. 38:S23–S33.
  • Prigione I, Benvenuto F, Bocca P, Battistini L, Uccelli A, Pistoia V. 2009. Reciprocal interactions between human mesenchymal stem cells and T cells or invariant natural killer T cells. Stem Cells. 27:693–702.
  • Raffaghello L, Bianchi G, Bertolotto M, Montecucco F, Busca A, Dallegri F, et al. 2008. Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche. Stem Cells26:151–162.
  • Ramasamy R, Fazekasova H, Lam EW, Soeiro I, Lombardi G, Dazzi F. 2007. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation. 83:71–76.
  • Rasmusson I, Ringdén O, Sundberg B, Le Blanc K. 2003. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation. 76:1208–1213.
  • Ridger VC, Wagner BE, Wallace WA, Hellewell PG 2001. Differential effects of CD18, CD29, CD49 integrin subunit inhibition on neutrophil migration in pulmonary inflammation. J Immunol. 166:3484–3490.
  • Ruoslahti E 1984. Fibronectin in cell adhesion, invasion. Cancer Metastasis Rev. 3:43–51.
  • Ryan JM, Barry FP, Murphy JM, Mahon BP. 2005. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond). 2:8.
  • Ryan JM, Barry F, Murphy JM, Mahon BP. 2007. Interferon does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol. 149: 353–363.
  • Rüster B, Göttig S, Ludwig RJ, Bistrian R, Müller S, Seifried E, et al. 2006. Mesenchymal stem cells display coordinated rolling, adhesion behavior on endothelial cells. Blood. 108:3938–3944.
  • Sackstein R 2005. The lymphocyte homing receptors: gatekeepers of the multistep paradigm. Curr Opin Hematol. 12:444–450.
  • Sato K, Ozaki K, Mori M, Muroi K, Ozawa K 2010. Mesenchymal stromal cells for graft-versus-host disease: basic aspects and clinical outcomes. J Clin Exp Hematop. 50:79–89.
  • Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, et al. 2002. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells.J Clin Invest. 109:1291–1302.
  • Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, et al. 2008. Human leukocyte antigen G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte, natural killer function, to induce CD4 + CD25highFOXP3 + regulatory T cells. Stem Cells. 26:212–222.
  • Sensebe L, Krampera M, Schrezenmeier H, Bourin P, Giordano R 2010. Mesenchymal stem cells for clinical application. Vox Sang. 98:93–107.
  • Shi M, Liu ZW, Wang FS. 2011. Immunomodulatory properties and therapeutic application of mesenchymal stem cells. Clin Exp Immunol. 164:1–8.
  • Siegel G, Schäfer R, Dazzi F 2009. The immunosuppressive properties of mesenchymal stem cells. Transplantation87:S45–S49.
  • Sillence DO, Rimoin DL, Danks DM. 1978. Clinical variability in osteogenesis imperfecta-variable expressivity or genetic heterogeneity. Birth Defects Orig Artic Ser. 15:113–129.
  • Simmons PJ, Torok-Storb B. 1991. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood. 78:55–62.
  • Sotiropoulou PA, Perez SA, Gritzapis AD, Baxevanis CN, Papamichail M. 2006. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells. 24:74–85.
  • Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L. 2009. 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. 113:6576–6583.
  • Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. 2008. Mesenchymal stem cells inhibit natural killer–cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2, 3-dioxygenase and prostaglandin E2. Blood. 111:1327–1333.
  • Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, Moretta L. 2006. 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. 107:1484–1490.
  • Tolar J, Le Blanc K, Keating A, Blazar BR. 2010. Concise review: hitting the right spot with mesenchymal stromal cells. Stem Cells. 28: 1446–1455.
  • Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. 2003. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation. 75:389–397.
  • Tursen U 2009. Activation markers in Behcet disease. Turkderm- Archives of the Turkish Dermatology, Venerology. 43:74–86.
  • Tögel F, Hu Z, Weiss K, Isaac J, Lange C, Westenfelder C 2005. Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. Am J Physiol Renal Physiol. 289:F31–FF42.
  • Türsen ÜPathophysiology of the Behçet’s Disease. Pathol Res Int. 2012: 2011.
  • Urban VS, Kiss J, Kovacs J, Gocza E, Vas V, Monostori V, Uher F 2008. Mesenchymal stem cells cooperate with bone marrow cells in therapy of diabetes. Stem Cells. 26:244–253.
  • Valenick LV, Hsia HC, Schwarzbauer JE 2005. Fibronectin fragmentation promotes 4 1 integrin-mediated contraction of a fibrin– fibronectin provisional matrix. Exp Cell Res. 309:48–55.
  • Vija L, Farge D, Gautier J-F, Vexiau P, Dumitrache C, Bourgarit A, et al. 2009. Mesenchymal stem cells: Stem cell therapy perspectives for type 1 diabetes. Diabetes Metab. 35:85–93.
  • Vogel W, Grunebach F, Messam CA, Kanz L, Brugger W, Buhring HJ. 2003. Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica88:126–133.
  • Volarevic V, Al-Qahtani A, Arsenijevic N, Pajovic S, Lukic ML 2009. Interleukin-1 receptor antagonist (IL-1Ra), IL-1Ra producing mesenchymal stem cells as modulators of diabetogenesis. Autoimmunity. 43:255–263.
  • Volarevic V, Arsenijevic N, Lukic ML, Stojkovic M. 2011. Concise review: mesenchymal stem cell treatment of the complications of diabetes mellitus. Stem Cells. 29:5–10.
  • Wang M, Yang Y, Yang D, Luo F, Liang W, Guo S, Xu J. 2009. The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology. 126:220–232.
  • Waszak P, Alphonse R, Vadivel A, Ionescu L, Eaton F, Thébaud B 2012. Preconditioning enhances the paracrine effect of mesenchymal stem cells in preventing oxygen-induced neonatal lung injury in rats. Stem Cells Dev. 21:2789–2797.
  • Weil BR, Manukyan MC, Herrmann JL, Abarbanell AM, Poynter JA, Wang Y, Meldrum DR 2011. The immunomodulatory properties of mesenchymal stem cells: implications for surgical disease. J Surg Res. 167:78–86.
  • Werr J, Xie X, Hedqvist P, Ruoslahti E, Lindbom L 1998. 1 integrins are critically involved in neutrophil locomotion in extravascular tissue in vivo. J Exp Med. 187:2091–2096.
  • Woodside DG, Kram RM, Mitchell JS, Belsom T, Billard MJ, McIntyre BW, Vanderslice P 2006. Contrasting roles for domain 4 of VCAM-1 in the regulation of cell adhesion, soluble VCAM-1 binding to integrin 4 1. J Immunol. 176:5041–5049.
  • Xu G, Zhang Y, Zhang L, Ren G, Shi Y 2007. The role of IL-6 in inhibition of lymphocyte apoptosis by mesenchymal stem cells. Biochem Biophys Res Commun. 361:745–750.
  • Xu W, Zhang X, Qian H, Zhu W, Sun X, Hu J, et al. 2004. Mesenchymal stem cells from adult human bone marrow differentiate into a cardiomyocyte phenotype in vitro. Exp Biol Med (Maywood). 229:623–631.
  • Yagi H, Soto-Gutierrez A, Parekkadan B, Kitagawa Y, Tompkins RG, Kobayashi N, Yarmush ML. 2010. Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplant. 19:667.
  • Zhang W, Ge W, Li C, You S, Liao L, Han Q, et al 2004. Effects of mesenchymal stem cells on differentiation, maturation, function of human monocyte-derived dendritic cells. Stem Cells Dev. 13:263–271.
  • Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, et al. 2005. Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol. 195:16–26.
  • Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, et al. 2005. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 106:1755–1761.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.