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Immunomodulatory Properties of Perinatal Tissue-Derived Mesenchymal Stem Cells

  • Seyed Mahmoud HashemiEmail author
  • Sara SoudiEmail author
Chapter
  • 417 Downloads
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

In recent years extraembryonic-derived mesenchymal stem cells have attracted a lot of attention because of their low immunogenicity and diverse immunomodulatory mechanisms that encourage their application in allogeneic cell transplantation and induction of immunosuppression. Different studies have designed to clarify the immunomodulatory properties of perinatal-isolated mesenchymal stem cells. In this review, we introduce the extraembryonic sources of MSCs including Wharton’s jelly, umbilical cord blood, amniotic membrane, amniotic fluid, and chorion-derived mesenchymal stem cells. Then the immunophenotype and immunogenic characteristic of each type of MSCs are explained. Finally, we address the cell membrane associated and secretory immunomodulatory molecules of perinatal tissue-derived MSCs that are responsible for their immunosuppressive properties in interaction with immune cells.

Keywords

Immunomodulatory properties Mesenchymal stem cells Perinatal stem cells Wharton’s jelly Amniotic membrane Umbilical cord blood stem cells 

References

  1. Abumaree MH et al (2013) Phenotypic and functional characterization of mesenchymal stem cells from chorionic villi of human term placenta. Stem Cell Rev 9(1):16–31PubMedCrossRefGoogle Scholar
  2. Akiyama K et al (2012) Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 10:544–555PubMedPubMedCentralCrossRefGoogle Scholar
  3. Akle CA et al (1981) Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet 318(8254):1003–1005CrossRefGoogle Scholar
  4. Alunno A et al (2014) In vitro immunomodulatory effects of microencapsulated umbilical cord Wharton jelly-derived mesenchymal stem cells in primary Sjögren’s syndrome. Rheumatology (United Kingdom) 54(1):163–168, http://www.rheumatology.oxfordjournals.org/cgi/doi/10.1093/rheumatology/keu292 CrossRefGoogle Scholar
  5. Alviano F et al (2007) Term Amniotic membrane is a high throughput source for multipotent Mesenchymal Stem Cells with the ability to differentiate into endothelial cells in vitro. BMC Dev Biol 7:11, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1810523&tool=pmcentrez&rendertype=abstract PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bailo M et al (2004) Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 78(10):1439–1448, http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=15599307 PubMedCrossRefGoogle Scholar
  7. Banas RA et al (2008) Immunogenicity and immunomodulatory effects of amnion-derived multipotent progenitor cells. Hum Immunol 69(6):321–328PubMedCrossRefGoogle Scholar
  8. Barcellos-Hoff MH, Dix TA (1996) Redox-mediated activation of latent transforming growth factor-beta 1. Mol Endocrinol (Baltimore, MD) 10(9):1077–1083Google Scholar
  9. Bieback K et al (2004) Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells (Dayton, Ohio) 22(4):625–634, http://www.ncbi.nlm.nih.gov/pubmed/15277708. Accessed 22 Apr 2016CrossRefGoogle Scholar
  10. Bilic G et al (2004) In vitro lesion repair by human amnion epithelial and mesenchymal cells. Am J Obstet Gynecol 190(1):87–92PubMedCrossRefGoogle Scholar
  11. Bilic G et al (2008) Comparative characterization of cultured human term amnion epithelial and mesenchymal stromal cells for application in cell therapy. Cell Transplant 17(8):955–968PubMedCrossRefGoogle Scholar
  12. Bongso A, Fong C (2013) The therapeutic potential, challenges and future clinical directions of stem cells from the Wharton’s Jelly of the human umbilical cord. Stem Cell Rev Rep 9(2):226–240, http://link.springer.com/10.1007/s12015-012-9418-z CrossRefGoogle Scholar
  13. Campbell KS, Purdy AK (2011) Structure/function of human killer cell immunoglobulin-like receptors: lessons from polymorphisms, evolution, crystal structures and mutations. Immunology 132(3):315–325PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cargnoni A et al (2009) Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycin-induced lung fibrosis. Cell Transplant 18(4):405–422PubMedCrossRefGoogle Scholar
  15. Cazac BB, Roes J (2000) TGF-β receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 13(4):443–451, http://www.cell.com/article/S1074761300000443/fulltext PubMedCrossRefGoogle Scholar
  16. Chan WK et al (2008) MHC expression kinetics and immunogenicity of mesenchymal stromal cells after short-term IFN-γ challenge. Exp Hematol 36(11):1551–1561CrossRefGoogle Scholar
  17. Chang C-J et al (2006) Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells 24(11):2466–2477PubMedCrossRefGoogle Scholar
  18. Chang CM et al (2007) Placenta-derived multipotent stem cells induced to differentiate into insulin-positive cells. Biochem Biophys Res Commun 357(2):414–420PubMedCrossRefGoogle Scholar
  19. Chao KC et al (2008) Islet-like clusters derived from mesenchymal stem cells in Wharton’s jelly of the human umbilical cord for transplantation to control type 1 diabetes. PLoS One 3(1):e1451PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chen K et al (2010) Human umbilical cord mesenchymal stem cells hUC-MSCs exert immunosuppressive activities through a PGE2-dependent mechanism. Clin Immunol 135(3):448–458, http://dx.doi.org/10.1016/j.clim.2010.01.015 PubMedCrossRefGoogle Scholar
  21. Chen P-M et al (2011a) Immunomodulatory properties of human adult and fetal multipotent mesenchymal stem cells. J Biomed Sci 18(1):49, http://www.jbiomedsci.com/content/18/1/49 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chen P-M et al (2011b) Immunomodulatory properties of human adult and fetal multipotent mesenchymal stem cells. J Biomed Sci 18(1):49, http://www.jbiomedsci.com/content/18/1/49 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Choi M et al (2013a) Proangiogenic features of Wharton’s jelly-derived mesenchymal stromal/stem cells and their ability to form functional vessels. Int J Biochem Cell Biol 45(3):560–570, http://dx.doi.org/10.1016/j.biocel.2012.12.001 PubMedCrossRefGoogle Scholar
  24. Choi M et al (2013b) Proangiogenic features of Wharton’s jelly-derived mesenchymal stromal/stem cells and their ability to form functional vessels. Int J Biochem Cell Biol 45(3):560–570PubMedCrossRefGoogle Scholar
  25. Contini P et al (2003) Soluble HLA-A,-B,-C and -G molecules induce apoptosis in T and NK CD8+ cells and inhibit cytotoxic T cell activity through CD8 ligation. Eur J Immunol 33(1):125–134, http://www.ncbi.nlm.nih.gov/pubmed/12594841. Accessed 21 Jun 2016PubMedCrossRefGoogle Scholar
  26. Danforth D, Hull RW (1958) The microscopic anatomy of the fetal membranes with particular reference to the detailed structure of the amnion. Am J Obstet Gynecol 75(3):536–547, discussion 548–550. http://www.ncbi.nlm.nih.gov/pubmed/13508744. Accessed 17 Jun 2016PubMedCrossRefGoogle Scholar
  27. Darby IA, Hewitson TD (2007) Fibroblast differentiation in wound healing and fibrosis. Int Rev Cytol 257:143–179PubMedCrossRefGoogle Scholar
  28. Demeure CE et al (1997) Prostaglandin E2 primes naive T cells for the production of anti-inflammatory cytokines. Eur J Immunol 27:3526–3531PubMedCrossRefGoogle Scholar
  29. Deuse T et al (2011) Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant 20(5):655–667PubMedCrossRefGoogle Scholar
  30. Donders R et al (2015) Human Wharton’s Jelly-derived stem cells display immunomodulatory properties and transiently improve rat experimental autoimmune encephalomyelitis. Cell Transplant 24(10):2077–2098, http://openurl.ingenta.com/content/xref?genre=article&issn=0963-6897&volume=24&issue=10&spage=2077 PubMedCrossRefGoogle Scholar
  31. Fan Y-P et al (2016) The therapeutic potential of human umbilical mesenchymal stem cells from Whartons Jelly in the treatment of rat peritoneal dialysis-induced fibrosis. Stem Cells Transl Med 5(2):235–247, http://stemcellstm.alphamedpress.org/cgi/doi/10.5966/sctm.2015-0001 PubMedCrossRefGoogle Scholar
  32. Flynn A, Barry F, O’Brien T (2007) UC blood-derived mesenchymal stromal cells: an overview. Cytotherapy 9(8):717–726, http://linkinghub.elsevier.com/retrieve/pii/S1465324907701408 PubMedCrossRefGoogle Scholar
  33. Fong CY et al (2007) Comparative growth behaviour and characterization of stem cells from human Wharton’s jelly. Reprod Biomed Online 15(6):708–718, http://linkinghub.elsevier.com/retrieve/pii/S1472648310605391 PubMedCrossRefGoogle Scholar
  34. Fukuchi Y et al (2004) Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22:649–658PubMedCrossRefGoogle Scholar
  35. Ganatra MA (2003) Amniotic membrane in surgery. J Pak Med Assoc 53(1):29–32PubMedGoogle Scholar
  36. Gong D et al (2012) TGFβ signaling plays a critical role in promoting alternative macrophage activation. BMC Immunol 13:31PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gros F et al (2008) Soluble HLA-G molecules impair natural killer/dendritic cell crosstalk via inhibition of dendritic cells. Eur J Immunol 38(3):742–749PubMedCrossRefGoogle Scholar
  38. Hashemi SM et al (2013) Comparative immunomodulatory properties of adipose-derived mesenchymal stem cells conditioned media from BALB/c, C57BL/6, and DBA mouse strains. J Cell Biochem 114(4):955–965, http://www.ncbi.nlm.nih.gov/pubmed/23225199. Accessed 11 Aug 2014PubMedCrossRefGoogle Scholar
  39. Hass R et al (2011) Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 9(1):12, http://www.biosignaling.com/content/9/1/12 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Heo JS et al (2016) Comparison of molecular profiles of human mesenchymal stem cells derived from bone marrow, umbilical cord blood, placenta and adipose tissue. Int J Mol Med 37(1):115–125, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4687432&tool=pmcentrez&rendertype=abstract PubMedGoogle Scholar
  41. Huang XP et al (2010) Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 122(23):2419–2429PubMedCrossRefGoogle Scholar
  42. Huang PY et al (2015) Xenograft of human umbilical mesenchymal stem cells from Wharton’s jelly as a potential therapy for rat pilocarpine-induced epilepsy. Brain Behav Immun 54:45–58, http://dx.doi.org/10.1016/j.bbi.2015.12.021 PubMedCrossRefGoogle Scholar
  43. Hunt JS et al (2005) HLA-G and immune tolerance in pregnancy. FASEB J 19(7):681–693PubMedCrossRefGoogle Scholar
  44. Hunt JS et al (2006) The role of HLA-G in human pregnancy. Reprod Biol Endocrinol 4(Suppl 1):S10PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hwang JH et al (2009) Comparison of cytokine expression in mesenchymal stem cells from human placenta, cord blood, and bone marrow. J Korean Med Sci 24(4):547–554, http://jkms.org/DOIx.php?id=10.3346/jkms.2009.24.4.547. Accessed 22 Apr 2016PubMedPubMedCentralCrossRefGoogle Scholar
  46. Ilancheran S et al (2007) Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod 77(3):577–588, http://www.ncbi.nlm.nih.gov/pubmed/17494917 PubMedCrossRefGoogle Scholar
  47. Ilancheran S, Moodley Y, Manuelpillai U (2009) Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta 30(1):2–10PubMedCrossRefGoogle Scholar
  48. In’t Anker PS et al (2004) Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells (Dayton, Ohio) 22(7):1338–1345, http://www.ncbi.nlm.nih.gov/pubmed/15579651 CrossRefGoogle Scholar
  49. Insausti CL et al (2010) The amniotic membrane as a source of stem cells. Histol Histopathol 25(1):91–98PubMedGoogle Scholar
  50. Insausti CL et al (2014) Amniotic membrane-derived stem cells: immunomodulatory properties and potential clinical application. Stem Cells Cloning 7(1):53–63PubMedPubMedCentralGoogle Scholar
  51. Jones EA et al (2002) Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349–3360PubMedCrossRefGoogle Scholar
  52. Jones GN et al (2012) Ontological differences in first compared to third trimester human fetal placental chorionic stem cells. PLoS One 7(9):e43395PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kalinski P (2012) Regulation of immune responses by prostaglandin E2. J Immunol (Baltimore, MD: 1950) 188(1):21–28, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3249979&tool=pmcentrez&rendertype=abstract\http://www.jimmunol.org/content/188/1/21.short CrossRefGoogle Scholar
  54. Kang JW et al (2012) Immunomodulatory effects of human amniotic membrane-derived mesenchymal stem cells. J Vet Sci 13(1):23–31PubMedPubMedCentralCrossRefGoogle Scholar
  55. Karahuseyinoglu S et al (2007) Biology of stem cells in human umbilical cord stroma: in situ and in vitro surveys. Stem Cells 25(2):319–331, http://www.ncbi.nlm.nih.gov/pubmed/17053211 PubMedCrossRefGoogle Scholar
  56. Kubo M et al (2001) Immunogenicity of human amniotic membrane in experimental xenotransplantation. Investig Ophthalmol Vis Sci 42(7):1539–1546Google Scholar
  57. Lagasse E et al (2000) Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6(11):1229–1234PubMedCrossRefGoogle Scholar
  58. Lee OK et al (2004) Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 103(5):1669–1675, http://www.bloodjournal.org/content/103/5/1669.abstract. Accessed 22 Apr 2016PubMedCrossRefGoogle Scholar
  59. Lee M-J et al (2010) Anti-fibrotic effect of chorionic plate-derived mesenchymal stem cells isolated from human placenta in a rat model of CCl(4)-injured liver: potential application to the treatment of hepatic diseases. J Cell Biochem 111(6):1453–1463, http://www.ncbi.nlm.nih.gov/pubmed/20830742. Accessed 25 Jun 2016PubMedCrossRefGoogle Scholar
  60. Lee JM et al (2012) Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells. Int Immunopharmacol 13(2):219–224, http://linkinghub.elsevier.com/retrieve/pii/S1567576912000975 PubMedCrossRefGoogle Scholar
  61. Lefebvre S et al (2000) Modulation of HLA-G expression in human thymic and amniotic epithelial cells. Hum Immunol 61(11):1095–1101PubMedCrossRefGoogle Scholar
  62. LeMaoult J et al (2007) Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood 109(5):2040–2048PubMedCrossRefGoogle Scholar
  63. Li MO, Flavell RA (2008) TGF-??: a master of all T cell trades. Cell 134(3):392–404PubMedPubMedCentralCrossRefGoogle Scholar
  64. Li H et al (2005) Immunosuppressive factors secreted by human amniotic epithelial cells. Investig Ophthalmol Vis Sci 46(3):900–907CrossRefGoogle Scholar
  65. Li C et al (2007) Human-placenta-derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cells. Cell Tissue Res 330(3):437–446PubMedCrossRefGoogle Scholar
  66. Li Y et al (2014) Differentiation of human amniotic fluid-derived mesenchymal stem cells into type II alveolar epithelial cells in vitro. Int J Mol Med 33(6):1507–1513PubMedGoogle Scholar
  67. Li L et al (2015) Characteristics of human amniotic fluid mesenchymal stem cells and their tropism to human ovarian cancer. PLoS One 10(4):e0123350PubMedPubMedCentralCrossRefGoogle Scholar
  68. Lila N et al (2001) Soluble HLA-G protein secreted by allo-specific CD4+ T cells suppresses the allo-proliferative response: a CD4+ T cell regulatory mechanism. Proc Natl Acad Sci U S A 98(21):12150–12155PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lisi A et al (2012) A combined synthetic-fibrin scaffold supports growth and cardiomyogenic commitment of human placental derived stem cells. PLoS One 7(4):e34284PubMedPubMedCentralCrossRefGoogle Scholar
  70. Liu CH, Hwang SM (2005) Cytokine interactions in mesenchymal stem cells from cord blood. Cytokine 32(6):270–279PubMedCrossRefGoogle Scholar
  71. Liu H et al (2009) Effects of different culture conditions on isolation and expansion of stem cells from second-trimester amniotic fluids. Zhonghua Fu Chan Ke Za Zhi 44(4):241–245PubMedGoogle Scholar
  72. Liu K-J et al (2011) Surface expression of HLA-G is involved in mediating immunomodulatory effects of placenta-derived multipotent cells (PDMCs) towards natural killer lymphocytes. Cell Transplant 20(11–12):1721–1730PubMedCrossRefGoogle Scholar
  73. Liu S et al (2012) Immune characterization of mesenchymal stem cells in human umbilical cord Wharton’s jelly and derived cartilage cells. Cell Immunol 278(1-2):35–44PubMedCrossRefGoogle Scholar
  74. López Y et al (2013) Wharton’s jelly or bone marrow mesenchymal stromal cells improve cardiac function following myocardial infarction for more than 32 weeks in a rat model: a preliminary report. Curr Stem Cell Res Ther 8:46–59, http://www.ncbi.nlm.nih.gov/pubmed/23270633\nC:\Users\Flo\AppData\Local\MendeleyLtd.\Mendeley Desktop\Downloaded\López et al. - 2013 - Wharton’s jelly or bone marrow mesenchymal stromal cells improve cardiac function following myocardial infarction.pdf PubMedCrossRefGoogle Scholar
  75. Lozito TP et al (2014) Human mesenchymal stem cells generate a distinct pericellular zone of MMP activities via binding of MMPs and secretion of high levels of TIMPs. Matrix Biol 34:132–143PubMedCrossRefGoogle Scholar
  76. Magatti M et al (2009) Amniotic mesenchymal tissue cells inhibit dendritic cell differentiation of peripheral blood and amnion resident monocytes. Cell Transplant 18(8):899–914PubMedCrossRefGoogle Scholar
  77. Mahic M et al (2006) FOXP3 + CD4 + CD25+ adaptive regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E2-dependent mechanism. J Immunol 177(1):246–254PubMedCrossRefGoogle Scholar
  78. Mamede A et al (2012) Amniotic membrane: from structure and functions to clinical applications. Cell Tissue Res 349(2):447–458PubMedCrossRefGoogle Scholar
  79. Manochantr S et al (2010) Isolation, characterization and neural differentiation potential of amnion derived mesenchymal stem cells. J Med Assoc Thai 93(Suppl 7):S183–S191, http://www.ncbi.nlm.nih.gov/pubmed/21294413 PubMedGoogle Scholar
  80. Mareschi K et al (2001) Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Haematologica 86(10):1099–1100, http://www.ncbi.nlm.nih.gov/pubmed/11602418. Accessed 4 Mar 2016PubMedGoogle Scholar
  81. Mazar J et al (2009) Cytotoxicity mediated by the Fas ligand (FasL)-activated apoptotic pathway in stem cells. J Biol Chem 284(33):22022–22028PubMedPubMedCentralCrossRefGoogle Scholar
  82. Medicetty S et al (2004) Transplantation of pig stem cells into rat brain: proliferation during the first 8 weeks. Exp Neurol 190(1):32–41PubMedCrossRefGoogle Scholar
  83. Menier C et al (2010) Recent advances on the non-classical major histocompatibility complex class i HLA-G molecule. Tissue Antigens 75(3):201–206PubMedCrossRefGoogle Scholar
  84. Miki T (2011) Amnion-derived stem cells: in quest of clinical applications. Stem Cell Res Ther 2(3):25, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3152995&tool=pmcentrez&rendertype=abstract PubMedPubMedCentralCrossRefGoogle Scholar
  85. Miki T, Strom SC (2006) Amnion-derived pluripotent/multipotent stem cells. Stem Cell Rev 2:133–142PubMedCrossRefGoogle Scholar
  86. Moorefield EC et al (2011) Cloned, CD117 selected human amniotic fluid stem cells are capable of modulating the immune response. PLoS One 6(10)Google Scholar
  87. Nurmenniemi S et al (2010) Toll-like receptor 9 ligands enhance mesenchymal stem cell invasion and expression of matrix metalloprotease-13. Exp Cell Res 316(16):2676–2682PubMedCrossRefGoogle Scholar
  88. Parolini O et al (2008) Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells (Dayton, Ohio) 26(2):300–311, http://www.ncbi.nlm.nih.gov/pubmed/17975221 CrossRefGoogle Scholar
  89. Parolini O et al (2009) Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? Regen Med 4(2):275–291PubMedCrossRefGoogle Scholar
  90. Portmann-Lanz CB et al (2006) Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 194(3):664–673PubMedCrossRefGoogle Scholar
  91. Prasanna SJ et al (2010) Pro-inflammatory cytokines, IFNγ and TNFα, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS One 5(2):e9016, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2814860&tool=pmcentrez&rendertype=abstract PubMedPubMedCentralCrossRefGoogle Scholar
  92. Ren G et al (2010) Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol 184:2321–2328PubMedPubMedCentralCrossRefGoogle Scholar
  93. Rennie K et al (2012a) Applications of amniotic membrane and fluid in stem cell biology and regenerative medicine. Stem Cells Int 2012. Article ID 721538, 13 pagesGoogle Scholar
  94. Rennie K et al (2012b) Applications of amniotic membrane and fluid in stem cell biology and regenerative medicine. Stem Cells Int 2012. Article ID 721538, 13 pagesGoogle Scholar
  95. Ries C et al (2007) MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines. Blood 109(9):4055–4063PubMedCrossRefGoogle Scholar
  96. Roelen DL et al (2009) Differential immunomodulatory effects of fetal versus maternal multipotent stromal cells. Hum Immunol 70(1):16–23PubMedCrossRefGoogle Scholar
  97. Roubelakis MG, Trohatou O, Anagnou NP (2012) Amniotic fluid and amniotic membrane stem cells: marker discovery. Stem Cells Int 2012, Article ID 107836, 9 pagesGoogle Scholar
  98. Saeidi M et al (2013) Immunomodulatory effects of human umbilical cord Wharton’s jelly-derived mesenchymal stem cells on differentiation, maturation and endocytosis of monocyte-derived dendritic cells. Iran J Allergy Asthma Immunol 12(1):37–49, http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=23454777&retmode=ref&cmd=prlinks. Accessed 3 Jun 2016PubMedGoogle Scholar
  99. Schu S et al (2012) Immunogenicity of allogeneic mesenchymal stem cells. J Cell Mol Med 16(9):2094–2103PubMedPubMedCentralCrossRefGoogle Scholar
  100. Secco M et al (2008) Multipotent stem cells from umbilical cord: cord is richer than blood! Stem Cells 26(1):146–150PubMedCrossRefGoogle Scholar
  101. Sheppard KA et al (2004) PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3?? Signalosome and downstream signaling to PKC?? FEBS Lett 574(1-3):37–41PubMedCrossRefGoogle Scholar
  102. Shi Y et al (2012) How mesenchymal stem cells interact with tissue immune responses. Trends Immunol 33(3):136–143, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3412175&tool=pmcentrez&rendertype=abstract. Accessed 4 Nov 2014PubMedPubMedCentralCrossRefGoogle Scholar
  103. Siegel N et al (2007) Stem cells in amniotic fluid as new tools to study human genetic diseases. Stem Cell Rev 3(4):256–264PubMedCrossRefGoogle Scholar
  104. Silini A et al (2013) Soluble factors of amnion-derived cells in treatment of inflammatory and fibrotic pathologies. Curr Stem Cell Res Ther 8(1):6–14, http://www.ncbi.nlm.nih.gov/pubmed/23270631 PubMedCrossRefGoogle Scholar
  105. Skardal A (2014) Amniotic fluid stem cells for wound healing. In: Atala A, Murphy SV (eds) Perinatal stem cells, vol XXIII. Springer, New York, pp 17–24Google Scholar
  106. Smith WL, Garavito RM, DeWitt DL (1996) Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem 271(52):33157–33160PubMedCrossRefGoogle Scholar
  107. Soncini M et al (2007) Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 1(4):296–305PubMedCrossRefGoogle Scholar
  108. Sorrell JM, Caplan AI (2010) Topical delivery of mesenchymal stem cells and their function in wounds. Stem Cell Res Ther 1(4):30PubMedPubMedCentralCrossRefGoogle Scholar
  109. Spaggiari GM et al (2008) Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 111:1327–1333PubMedCrossRefGoogle Scholar
  110. Spender LC et al (2009) TGF-beta induces apoptosis in human B cells by transcriptional regulation of BIK and BCL-XL. Cell Death Differ 16(4):593–602PubMedPubMedCentralCrossRefGoogle Scholar
  111. Sreeramkumar V, Fresno M, Cuesta N (2012) Prostaglandin E2 and T cells: friends or foes? Immunol Cell Biol 90(6):579–586, http://www.nature.com/doifinder/10.1038/icb.2011.75\http://www.ncbi.nlm.nih.gov/pubmed/21946663\http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC3389798 PubMedCrossRefGoogle Scholar
  112. Stagg J et al (2006) Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood 107(6):2570–2577PubMedCrossRefGoogle Scholar
  113. Subramanian A et al (2015) Comparative characterization of cells from the various compartments of the human umbilical cord shows that the Wharton’s Jelly compartment provides the best source of clinically utilizable mesenchymal stem cells. PLoS One 10(6):e0127992, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4464659&tool=pmcentrez&rendertype=abstract. Accessed 3 Jun 2016PubMedPubMedCentralCrossRefGoogle Scholar
  114. Sun L et al (2010) Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum 62(8):2467–2475PubMedCrossRefGoogle Scholar
  115. Taghizadeh RR, Cetrulo KJ, Cetrulo CL (2011) Wharton’s Jelly stem cells: future clinical applications. Placenta 32(Suppl 4):S311–S315PubMedCrossRefGoogle Scholar
  116. Tamagawa T, Ishiwata I, Saito S (2004) Establishment and characterization of a pluripotent stem cell line derived from human amniotic membranes and initiation of germ layers in vitro. Hum Cell 17(3):125–130PubMedCrossRefGoogle Scholar
  117. Tamagawa T et al (2007) Differentiation of mesenchymal cells derived from human amniotic membranes into hepatocyte-like cells in vitro. Hum Cell 20(3):77–84PubMedCrossRefGoogle Scholar
  118. 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(8):795–806, http://dx.doi.org/10.1038/icb.2010.47 PubMedCrossRefGoogle Scholar
  119. Troyer DL, Weiss ML (2008) Concise review: Wharton’s Jelly-derived cells are a primitive stromal cell population. Stem Cells 26:591–599PubMedCrossRefGoogle Scholar
  120. Tsai MS et al (2004) Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Hum Reprod 19(6):1450–1456PubMedCrossRefGoogle Scholar
  121. Tsai P et al (2009) The therapeutic potential of human umbilical mesenchymal stem cells from Wharton’s jelly in the treatment of rat liver fibrosis. Liver Transpl 15(5):484–495, http://www.ncbi.nlm.nih.gov/pubmed/19399744 PubMedCrossRefGoogle Scholar
  122. Ullah I, Baregundi Subbarao R, Rho G-J (2015) Human mesenchymal stem cells - current trends and future prospective. Biosci Rep 35(2):e00191, http://www.bioscirep.org/content/35/2/e00191.abstract PubMedPubMedCentralCrossRefGoogle Scholar
  123. Vivier E et al (2008) Functions of natural killer cells. Nat Immunol 9(5):503–510PubMedCrossRefGoogle Scholar
  124. Walker C et al (1983) Lymphokine regulation of activated (G1) lymphocytes. 1. Prostaglandin E2-induced inhibition of interleukin 2 production. J Immunol (Baltimore, MD : 1950) 130(4):1770–1773Google Scholar
  125. Wang HS et al (2004) Mesenchymal stem cells in the Wharton’s jelly of the human umbilical cord. Stem Cells 22(7):1330–1337PubMedCrossRefGoogle Scholar
  126. Wang D et al (2010a) CD14+ monocytes promote the immunosuppressive effect of human umbilical cord matrix stem cells. Exp Cell Res 316(15):2414–2423, http://dx.doi.org/10.1016/j.yexcr.2010.04.018 PubMedCrossRefGoogle Scholar
  127. Wang D et al (2010b) CD14+ monocytes promote the immunosuppressive effect of human umbilical cord matrix stem cells. Exp Cell Res 316(15):2414–2423PubMedCrossRefGoogle Scholar
  128. Wang J et al (2014) The subtype CD200-positive, chorionic mesenchymal stem cells from the placenta promote regeneration of human hepatocytes. Biotechnol Lett 36(6):1335–1341PubMedCrossRefGoogle Scholar
  129. Wei JP et al (2009) Human amniotic mesenchymal cells differentiate into chondrocytes. Cloning Stem Cells 11(1):19–26, http://www.ncbi.nlm.nih.gov/pubmed/19226212 PubMedCrossRefGoogle Scholar
  130. Weiss ML et al (2008) Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells (Dayton, Ohio) 26(11):2865–2874, http://www.ncbi.nlm.nih.gov/pubmed/18703664 CrossRefGoogle Scholar
  131. Westgren M et al (1995) Cytokines in fetal blood and amniotic fluid in Rh-immunized pregnancies. Obstet Gynecol 86(2):209–213PubMedCrossRefGoogle Scholar
  132. Wexler SA et al (2003) Adult bone marrow is a rich source of human mesenchymal “stem” cells but umbilical cord and mobilized adult blood are not. Br J Haematol 121(2):368–374, http://www.ncbi.nlm.nih.gov/pubmed/12694261. Accessed 22 Apr 2016PubMedCrossRefGoogle Scholar
  133. Witkowska-Zimny M, Wrobel E (2011) Perinatal sources of mesenchymal stem cells: Wharton’s jelly, amnion and chorion. Cell Mol Biol Lett 16(3):493–514PubMedCrossRefGoogle Scholar
  134. Wu KH et al (2007) Therapeutic potential of human umbilical cord derived stem cells in a rat myocardial infarction model. Ann Thorac Surg 83(4):1491–1498, http://www.ncbi.nlm.nih.gov/pubmed/17383364 PubMedCrossRefGoogle Scholar
  135. Yamaguchi Y et al (2005) Bone marrow cells differentiate into wound myofibroblasts and accelerate the healing of wounds with exposed bones when combined with an occlusive dressing. Br J Dermatol 152(4):616–622PubMedCrossRefGoogle Scholar
  136. Yañez R et al (2010) Prostaglandin E2 plays a key role in the immunosuppressive properties of adipose and bone marrow tissue-derived mesenchymal stromal cells. Exp Cell Res 316(19):3109–3123PubMedCrossRefGoogle Scholar
  137. Yang CC et al (2008) Transplantation of human umbilical mesenchymal stem cells from Wharton’s jelly after complete transection of the rat spinal cord. PLoS One 3(10):e3336PubMedPubMedCentralCrossRefGoogle Scholar
  138. Yang S-H et al (2009) Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10. Exp Mol Med 41:315–324PubMedPubMedCentralCrossRefGoogle Scholar
  139. Yang ZX et al (2013) CD106 identifies a subpopulation of mesenchymal stem cells with unique immunomodulatory properties. PLoS One 8(3):1–12Google Scholar
  140. Yousefi F et al (2016) In vivo immunomodulatory effects of adipose-derived mesenchymal stem cells conditioned medium in experimental autoimmune encephalomyelitis. Immunol Lett 172:94–105, http://www.sciencedirect.com/science/article/pii/S0165247816300256. Accessed 2 Mar 2016PubMedCrossRefGoogle Scholar
  141. Yu Q, Stamenkovic I (2000) Cell surface-localized matrix mealloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14:163–176PubMedPubMedCentralGoogle Scholar
  142. Zhao RC (2015) Stem cells: basics and clinical translation. Springer, NetherlandsCrossRefGoogle Scholar
  143. Zheng Y-B et al (2008) Characterization and hepatogenic differentiation of mesenchymal stem cells from human amniotic fluid and human bone marrow: a comparative study. Cell Biol Int 32(11):1439–1448PubMedCrossRefGoogle Scholar
  144. Zhou C et al (2011) Immunomodulatory effect of human umbilical cord Wharton’s jelly-derived mesenchymal stem cells on lymphocytes. Cell Immunol 272(1):33–38, http://www.ncbi.nlm.nih.gov/pubmed/22004796 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Immunology, Faculty of Medical SciencesTarbiat Modares UniversityTehranIran
  2. 2.Department of Immunology, School of MedicineShahid Beheshti University of Medical SciencesTehranIran

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