Immunomodulatory properties of dental tissue-derived mesenchymal stem cells

Oral Diseases

Volumn 20, Issue 1, 2014, Pages 25-34

  Li, Z ^a   Jiang, C M ^a,b   An, S ^a,b   Cheng, Q ^a,b   Huang, Y F ^a,b   Wang, Y T ^a,b   Gou, Y C ^a,b   Xiao, L ^a,b   Yu, W J ^a,b   Wang, J ^a,b  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

Author keywords

Dental mesenchymal stem cells; Immunomodulation; Mesenchymal stem cells

Indexed keywords

5' NUCLEOTIDASE; ENDOGLIN; HLA G ANTIGEN; HLA G5 ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; MESSENGER RNA; PROSTAGLANDIN E2; THY 1 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ACUTE LUNG INJURY; ACUTE PANCREATITIS; ALLERGIC ASTHMA; ALLERGIC ENCEPHALOMYELITIS; APICAL PAPILLA; B LYMPHOCYTE; BRAIN ISCHEMIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL INTERACTION; CELL RENEWAL; CEREBROVASCULAR ACCIDENT; CHRONIC OBSTRUCTIVE LUNG DISEASE; CROHN DISEASE; CYTOTOXIC T LYMPHOCYTE; DECIDUOUS TOOTH; DENDRITIC CELL; DENTAL FOLLICLE; DENTAL PULP STEM CELL; DENTAL STEM CELL; DIABETES MELLITUS; GINGIVA; HEART INFARCTION; HUMAN; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIC COLITIS; KIDNEY FAILURE; KIDNEY INJURY; LIVER FIBROSIS; LIVER INJURY; LUNG FIBROSIS; MACROPHAGE; MESENCHYMAL STEM CELL; MULTIPLE SCLEROSIS; PERIODONTAL LIGAMENT; PERIODONTAL LIGAMENT STEM CELL; PERIODONTITIS; PHENOTYPE; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; REVIEW; RHEUMATOID ARTHRITIS; SEPSIS; SKIN ALLERGY; STEM CELL; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; T LYMPHOCYTE; TOOTH; TOOTH PULP; CYTOLOGY; IMMUNOLOGY; MESENCHYMAL STROMA CELL; TOOTH PAPILLA; TOOTH SAC;

DENTAL PAPILLA; DENTAL PULP; DENTAL SAC; GINGIVA; HUMANS; MESENCHYMAL STROMAL CELLS; PERIODONTAL LIGAMENT; TOOTH, DECIDUOUS;

EID: 84890117214     PISSN: 1354523X     EISSN: 16010825     Source Type: Journal    
DOI: 10.1111/odi.12086     Document Type: Review

References (111)

1. Aggarwal S, Pittenger MF (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105: 1815-1822.
2. Akiyama K, Chen C, Wang D et al (2012). Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 10: 544-555.
3. Asari S, Itakura S, Ferreri K et al (2009). Mesenchymal stem cells suppress B-cell terminal differentiation. Exp Hematol 37: 604-615.
4. Augello A, Tasso R, Negrini SM et al (2005). Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 35: 1482-1490.
5. Bartold PM, McCulloch CA, Narayanan AS, Pitaru S (2000). Tissue engineering: a new paradigm for periodontal regeneration based on molecular and cell biology. Periodontol 24: 253-269.
6. Benvenuto F, Ferrari S, Gerdoni E et al (2007). Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells 25: 1753-1760.
7. Beyth S, Borovsky Z, Mevorach D et al (2005). Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105: 2214-2219.
8. Boumaza I, Srinivasan S, Witt WT et al (2009). Autologous bone marrow-derived rat mesenchymal stem cells promote PDX-1 and insulin expression in the islets, alter T cell cytokine pattern and preserve regulatory T cells in the periphery and induce sustained normoglycemia. J Autoimmun 32: 33-42.
9. Brooke G, Cook M, Blair C et al (2007). Therapeutic applications of mesenchymal stromal cells. [Review] [148 refs]. Semin Cell Dev Biol 18: 846-858.
10. 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, and bone marrow. Blood 98: 2396-2402.
11. Caplan AI (1991). Mesenchymal stem cells. J Orthop Res 9: 641-650.
12. Ciccocioppo R, Bernardo ME, Sgarella A et al (2011). Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 60: 788-798.
13. Corcione A, Benvenuto F, Ferretti E et al (2006). Human mesenchymal stem cells modulate B-cell functions. Blood 107: 367-372.
14. Dayan V, Yannarelli G, Billia F et al (2011). Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/macrophages after acute myocardial infarction. Basic Res Cardiol 106: 1299-1310.
15. Di Nicola M, Carlo-Stella C, Magni M et al (2002). Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99: 3838-3843.
16. Ding G, Liu Y, An Y et al (2010a). Suppression of T cell proliferation by root apical papilla stem cells in vitro. Cells Tissues Organs 191: 357-364.
17. Ding G, Liu Y, Wang W et al (2010b). Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 28: 1829-1838.
18. Djouad F, Plence P, Bony C et al (2003). Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102: 3837-3844.
19. Dong F, Harvey J, Finan A, Weber K, Agarwal U, Penn MS (2012). Myocardial CXCR4 expression is required for mesenchymal stem cell mediated repair following acute myocardial infarction. Circulation 126: 314-324.
20. English K, Ryan JM, Tobin L, Murphy MJ, Barry FP, Mahon BP (2009). Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD4+CD25(High) forkhead box P3+ regulatory T cells. Clin Exp Immunol 156: 149-160.
21. Fan CG, Tang FW, Zhang QJ et al (2005). Characterization and neural differentiation of fetal lung mesenchymal stem cells. Cell Transplant 14: 311-321.
22. Fontenot JD, Gavin MA, Rudensky AY (2003). Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4: 330-336.
23. Fox JM, Chamberlain G, Ashton BA, Middleton J (2007). Recent advances into the understanding of mesenchymal stem cell trafficking. Br J of Haematol 137: 491-502.
24. Freyman T, Polin G, Osman H et al (2006). A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur Heart J 27: 1114-1122.
25. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV (1974). Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17: 331-340.
26. Garcia-Gomez I, Elvira G, Zapata AG et al (2010). Mesenchymal stem cells: biological properties and clinical applications. Expert Opin Biol Ther 10: 1453-1468.
27. Gerdoni E, Gallo B, Casazza S et al (2007). Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann Neurol 61: 219-227.
28. Giuliani M, Fleury M, Vernochet A et al (2011). Long-lasting inhibitory effects of fetal liver mesenchymal stem cells on T-lymphocyte proliferation. PLoS ONE 6: e19988. doi: 10.1371/journal.pone.0019988.
29. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA 97: 13625-13630.
30. Gucciardo L, Lories R, Ochsenbein-Kolble N, Done E, Zwijsen A, Deprest J (2009). Fetal mesenchymal stem cells: isolation, properties and potential use in perinatology and regenerative medicine. [Review] [58 refs]. BJOG 116: 166-172.
31. Hare JM, Traverse JH, Henry TD et al (2009). A randomized, double-blind, placebo-controlled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 54: 2277-2286.
32. Humphreys BD, Bonventre JV (2008). Mesenchymal stem cells in acute kidney injury. Ann Rev Med 59: 311-325.
33. Imberti B, Morigi M, Tomasoni S et al (2007). Insulin-like growth factor-1 sustains stem cell mediated renal repair. J Am Soc Nephrol 18: 2921-2928.
34. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C et al (2003). Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 102: 1548-1549.
35. Iwasaki A, Medzhitov R (2004). Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995.
36. Jiang XX, Zhang Y, Liu B et al (2005). Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105: 4120-4126.
37. Jung KH, Song SU, Yi T et al (2011). Human bone marrow-derived clonal mesenchymal stem cells inhibit inflammation and reduce acute pancreatitis in rats. Gastroenterology 140: 998-1008.
38. Kerkis I, Ambrosio CE, Kerkis A et al (2008). Early transplantation of human immature dental pulp stem cells from baby teeth to golden retriever muscular dystrophy (GRMD) dogs: local or systemic? J Transl Med 6: 35.
39. Kidd S, Spaeth E, Dembinski JL et al (2009). Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells 27: 2614-2623.
40. Kim HS, Kim KH, Kim SH et al (2010). Immunomodulatory effect of canine periodontal ligament stem cells on allogenic and xenogenic peripheral blood mononuclear cells. J Periodontal Implant Sci 40: 265-270.
41. Krampera M, Glennie S, Dyson J et al (2003). Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101: 3722-3729.
42. Kurozumi K, Nakamura K, Tamiya T et al (2005). Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. Mol Ther 11: 96-104.
43. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O (2003a). HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31: 890-896.
44. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O (2003b). Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 57: 11-20.
45. Lee S, An S, Kang TH et al (2011). Comparison of mesenchymal-like stem/progenitor cells derived from supernumerary teeth with stem cells from human exfoliated deciduous teeth. Regen Med 6: 689-699.
46. Lee EJ, Choi EK, Kang SK et al (2012). N-cadherin determines individual variations in the therapeutic efficacy of human umbilical cord blood-derived mesenchymal stem cells in a rat model of myocardial infarction. Mol Ther 20: 155-167.
47. Liu D, Xu J, Liu O et al (2012). Mesenchymal stem cells derived from inflamed periodontal ligaments exhibit impaired immunomodulation. J Clin Periodontol 24: 12009.
48. Mabed M, Shahin M (2012). Mesenchymal stem cell-based therapy for the treatment of type 1 diabetes mellitus. Curr Stem Cell Res Ther 7: 179-190.
49. Maccario R, Podesta M, Moretta A 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.
50. Malhotra A, Shanker A (2011). NK cells: immune cross-talk and therapeutic implications. Immunotherapy 3: 1143-1166.
51. Mannon PJ (2011). Remestemcel-L: human mesenchymal stem cells as an emerging therapy for Crohn's disease. Expert Opin Biol Ther 11: 1249-1256.
52. Mao JJ, Giannobile WV, Helms JA et al (2006). Craniofacial tissue engineering by stem cells. J Dent Res 85: 966-979.
53. Martinet L, Fleury-Cappellesso S, Gadelorge M et al (2009). A regulatory cross-talk between Vgamma9Vdelta2 T lymphocytes and mesenchymal stem cells. Eur J Immunol 39: 752-762.
54. Matthay MA, Thompson BT, Read EJ et al (2010). Therapeutic potential of mesenchymal stem cells for severe acute lung injury. Chest 138: 965-972.
55. Mei SH, Haitsma JJ, Dos Santos CC et al (2010). Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 182: 1047-1057.
56. Meisel R, Zibert A, Laryea M, Gobel U, Daubener 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.
57. Miura M, Gronthos S, Zhao M et al (2003). SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA 100: 5807-5812.
58. Morsczeck C, Gotz W, Schierholz J et al (2005). Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24: 155-165.
59. Morsczeck C, Vollner F, Saugspier M et al (2010). Comparison of human dental follicle cells (DFCs) and stem cells from human exfoliated deciduous teeth (SHED) after neural differentiation in vitro. Clin Oral Investig 14: 433-440.
60. Nauta AJ, Fibbe WE (2007). Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506.
61. Nesselmann C, Ma N, Bieback K et al (2008). Mesenchymal stem cells and cardiac repair. J Cell Mol Med 12: 1795-1810.
62. Ortiz LA, Dutreil M, Fattman C et al (2007). Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 104: 11002-11007.
63. Parekkadan B, van Poll D, Megeed Z et al (2007). Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells. Biochem Biophys Res Commun 363: 247-252.
64. Peng L, Ye L, Zhou XD (2009). Mesenchymal stem cells and tooth engineering. Int J Oral Sci 1: 6-12.
65. Phinney DG, Prockop DJ (2007). Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair-current views. Stem Cells 25: 2896-2902.
66. Pierdomenico L, Bonsi L, Calvitti M et al (2005). Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80: 836-842.
67. Pitaru S, Pritzki A, Bar-Kana I, Grosskopf A, Savion N, Narayanan AS (2002). Bone morphogenetic protein 2 induces the expression of cementum attachment protein in human periodontal ligament clones. Connect Tissue Res 43: 257-264.
68. Pittenger MF, Mackay AM, Beck SC et al (1999). Multilineage potential of adult human mesenchymal stem cells. Science (New York, NY.) 284: 143-147.
69. Plumas J, Chaperot L, Richard MJ, Molens JP, Bensa JC, Favrot MC (2005). Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 19: 1597-1604.
70. Poggi A, Prevosto C, Massaro AM et al (2005). Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: role of NKp30 and NKG2D receptors. J Immunol 175: 6352-6360.
71. 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.
72. Prasad VK, Lucas KG, Kleiner GI et al (2011). Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (Prochymal) in pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biol Blood Marrow Transplant 17: 534-541.
73. Ramasamy R, Tong CK, Seow HF, Vidyadaran S, Dazzi F (2008). The immunosuppressive effects of human bone marrow-derived mesenchymal stem cells target T cell proliferation but not its effector function. Cellular Immunol 251: 131-136.
74. Rasmusson I (2006). Immune modulation by mesenchymal stem cells. Exp Cell Res 312: 2169-2179.
75. Rasmusson I, Ringden 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.
76. Rasmusson I, Le Blanc K, Sundberg B, Ringden O (2007). Mesenchymal stem cells stimulate antibody secretion in human B cells. Scand J Immunol 65: 336-343.
77. Ren G, Su J, Zhang L et al (2009). Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 27: 1954-1962.
78. Rutella S, Danese S, Leone G (2006). Tolerogenic dendritic cells: cytokine modulation comes of age. Blood 108: 1435-1440.
79. Sato K, Ozaki K, Oh I et al (2007). Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109: 228-234.
80. Sattler C, Steinsdoerfer M, Offers M et al (2011). Inhibition of T-cell proliferation by murine multipotent mesenchymal stromal cells is mediated by CD39 expression and adenosine generation. Cell Transplant 20: 1221-1230.
81. Selmani Z, Naji A, Zidi I et al (2008). Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Stem Cells 26: 212-222.
82. Selmani Z, Naji A, Gaiffe E et al (2009). HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation 87: 15.
83. Seo BM, Miura M, Gronthos S et al (2004). Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364: 149-155.
84. Shimono M, Ishikawa T, Ishikawa H et al (2003). Regulatory mechanisms of periodontal regeneration. Microsc Res Tech 60: 491-502.
85. Siegel G, Schafer R, Dazzi F (2009). The immunosuppressive properties of mesenchymal stem cells. Transplantation 87: 15.
86. Sonoyama W, Liu Y, Fang D et al (2006). Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 20.
87. Sonoyama W, Liu Y, Yamaza T et al (2008). Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34: 166-171.
88. 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.
89. 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.
90. 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.
91. Su WR, Zhang QZ, Shi SH, Nguyen AL, Le AD (2011). Human gingiva-derived mesenchymal stromal cells attenuate contact hypersensitivity via prostaglandin E2-dependent mechanisms. Stem Cells 29: 1849-1860.
92. Sun L, Akiyama K, Zhang H et al (2009). Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 27: 1421-1432.
93. Tipnis S, Viswanathan C, Majumdar AS (2010). Immunosuppressive properties of human umbilical cord-derived mesenchymal stem cells: role of B7-H1 and IDO. Immunol Cell Biol 88: 795-806.
94. Tomar GB, Srivastava RK, Gupta N et al (2010). Human gingiva-derived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochem Biophys Res Commun 393: 377-383.
95. Traggiai E, Volpi S, Schena F et al (2008). Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients. Stem Cells 26: 562-569.
96. 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.
97. Uccelli A, Moretta L, Pistoia V (2006). Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 36: 2566-2573.
98. Uccelli A, Pistoia V, Moretta L (2007). Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol 28: 219-226.
99. Uccelli A, Moretta L, Pistoia V (2008). Mesenchymal stem cells in health and disease. Nature reviews. Immunology 8: 726-736.
100. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S (2009). Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 219: 667-676.
101. Wang L, Zhao Y, Shi S (2012). Interplay between Mesenchymal Stem Cells and Lymphocytes: implications for Immunotherapy and Tissue Regeneration. J Dent Res 91: 1003-1010.
102. Williams JT, Southerland SS, Souza J, Calcutt AF, Cartledge RG (1999). Cells isolated from adult human skeletal muscle capable of differentiating into multiple mesodermal phenotypes. Am Surg 65: 22-26.
103. Xu J, Wu W, Zhang L et al (2012). The Role of MicroRNA-146a in the Pathogenesis of the Diabetic Wound-Healing Impairment: Correction With Mesenchymal Stem Cell Treatment. Diabetes 61: 2906-2912.
104. Yamaza T, Miura Y, Bi Y et al (2008). Pharmacologic stem cell based intervention as a new approach to osteoporosis treatment in rodents. PLoS ONE 3: e2615. doi: 10.1371/journal.pone.0002615.
105. Yamaza T, Kentaro A, Chen C et al (2010). Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res Ther 1: 5.
106. Zappia E, Casazza S, Pedemonte E et al (2005). Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106: 1755-1761.
107. Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Le AD (2009). Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183: 7787-7798.
108. Zhang QZ, Su WR, Shi SH et al (2010). Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells 28: 1856-1868.
109. Zhao Y, Wang L, Jin Y, Shi S (2012). Fas ligand regulates the immunomodulatory properties of dental pulp stem cells. J Dent Res 91: 948-954.
110. Zhou DH, Huang SL, Huang K et al (2005). [Mesenchymal stem cells from human cord blood promote engraftment of human umbilical cord blood-derived CD34+ cells in NOD/SCID mice]. [Chinese]. Chung Hua Hsueh Yeh Hsueh Tsa Chih 26: 732-735.
111. Zuk PA, Zhu M, Mizuno H et al (2001). Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7: 211-228.