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Characteristics of Mesenchymal Stem Cells Derived from Amniotic Membrane: A Potential Candidate for Stem Cell-Based Therapy

  • Somaieh Kazemnejad
  • Manijeh Khanmohammadi
  • Amir-Hassan Zarnani
  • Mohammad Reza Bolouri
Chapter
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Nowadays, mesenchymal stem cells (MSCs) have elevated the hopes of patients excruciated with incurable and/or disabling diseases. Amniotic membrane-derived mesenchymal stem cells (AMSCs) have considerable advantages over clinically administrated MSCs like bone marrow in terms of availability, no ethical concerns, less DNA damage, higher proliferation ability that introduce them as a potential stem cells with clinical applications in the promising field of regenerative medicine. In this chapter, we analyzed the characteristics of AMSCs in terms of critical points considered for clinical application especially in comparison with MSCs retrieved from other sources. We also describe previous studies concerning the therapeutic applications and discuss potential pitfalls in research for AMSCs.

Keywords

Amniotic membrane Stem cells Differentiation Regenerative medicine 

Notes

Study Finding/Competing Interest

The authors indicate no potential conflict of interest.

References

  1. Albert ML, Jegathesan M, Darnell RB (2001) Dendritic cell maturation is required for the cross-tolerization of CD8+ T cells. Nat Immunol 2(11):1010–1017PubMedCrossRefGoogle Scholar
  2. Alviano F, Fossati V, Marchionni C, Arpinati M, Bonsi L, Franchina M, Lanzoni G, Cantoni S, Cavallini C, Bianchi F, Tazzari PL, Pasquinelli G, Foroni L, Ventura C, Grossi A, Bagnara GP (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 7:11PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bailo M, Soncini M, Vertua E, Signoroni PB, Sanzone S, Lombardi G, Arienti D, Calamani F, Zatti D, Paul P, Albertini A, Zorzi F, Cavagnini A, Candotti F, Wengler GS, Parolini O (2004) Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 78(10):1439–1448PubMedCrossRefGoogle Scholar
  4. Banas R, Miller C, Guzik L, Zeevi A (2014) Amnion-derived multipotent progenitor cells inhibit blood monocyte differentiation into mature dendritic cells. Cell Transplant 23(9):1111–1125PubMedCrossRefGoogle Scholar
  5. Benirschke K, Kaufman P (2000) Anatomy and pathology of the placental membranes. In: Benirschke K, Burton GJ, Baergen RN (eds) Pathology of the human placenta, 4th edn. Springer, New York, pp 281–334CrossRefGoogle Scholar
  6. Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, Galun E, Rachmilewitz J (2005) Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105(5):2214–2219PubMedCrossRefGoogle Scholar
  7. Bilic G, Zeisberger SM, Mallik AS, Zimmermann R, Zisch AH (2008) Comparative characterization of cultured human term amnion epithelial and mesenchymal stromal cells for application in cell therapy. Cell Transplant 17:955–968PubMedCrossRefGoogle Scholar
  8. Bozorgmehr M, Moazzeni SM, Salehnia M, Sheikhian A, Nikoo S, Zarnani AH (2014) Menstrual blood-derived stromal stem cells inhibit optimal generation and maturation of human monocyte-derived dendritic cells. Immunol Lett 162(2 Pt B):239–246PubMedCrossRefGoogle Scholar
  9. Brooke G, Rossetti T, Pelekanos R, Ilic N, Murray P, Hancock S, Antonenas V, Huang G, Gottlieb D, Bradstock K, Atkinson K (2009) Manufacturing of human placenta-derived mesenchymal stem cells for clinical trials. Br J Haematol 144(4):571–579PubMedCrossRefGoogle Scholar
  10. Cargnoni A, Gibelli L, Tosini A, Signoroni PB, Nassuato C, Arienti D, Lombardi G, Albertini A, Wengler GS, Parolini O (2009) Transplantation of allogeneic and xenogeneic placenta-derived cells reduces bleomycin-induced lung fibrosis. Cell Transplant 18(4):405–422PubMedCrossRefGoogle Scholar
  11. Carter L, Fouser LA, Jussif J, Fitz L, Deng B, Wood CR, Collins M, Honjo T, Freeman GJ, Carreno BM (2002) PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur J Immunol 32(3):634–643PubMedCrossRefGoogle Scholar
  12. Chang CJ, Yen ML, Chen YC, Chien CC, Huang HI, Bai CH, Yen BL (2006) Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells 24(11):2466–2477PubMedCrossRefGoogle Scholar
  13. Chang YJ, Hwang SM, Tseng CP, Cheng FC, Huang SH, Hsu LF, Hsu LW, Tsai MS (2010) Isolation of mesenchymal stem cells with neurogenic potential from the mesoderm of the amniotic membrane. Cells Tissues Organs 192(2):93–105PubMedCrossRefGoogle Scholar
  14. Chen L, Zhang W, Yue H, Han Q, Chen B, Shi M, Li J, Li B, You S, Shi Y, Zhao RC (2007) Effects of human mesenchymal stem cells on the differentiation of dendritic cells from CD34+ cells. Stem Cells Dev 16(5):719–731PubMedCrossRefGoogle Scholar
  15. Chen M, Wang X, Ye Z, Zhang Y, Zhou Y, Tan WS (2011) A modular approach to the engineering of a centimeter-sized bone tissue construct with human amniotic mesenchymal stem cells-laden microcarriers. Biomaterials 32(30):7532–7542PubMedCrossRefGoogle Scholar
  16. Chivu M, Dima SO, Stancu CI, Dobrea C, Uscatescu V, Necula LG, Bleotu C, Tanase C, Albulescu R, Ardeleanu C, Popescu I (2009) In vitro hepatic differentiation of human bone marrow mesenchymal stem cells under differential exposure to liver-specific factors. Transl Res 154:122–132PubMedCrossRefGoogle Scholar
  17. Choi YS, Matsuda K, Dusting GJ, Morrison WA, Dilley RJ (2010) Engineering cardiac tissue in vivo from human adipose-derived stem cells. Biomaterials 31:2236–2242PubMedCrossRefGoogle Scholar
  18. Darzi S, Zarnani AH, Jeddi-Tehrani M, Entezami K, Mirzadegan E, Akhondi MM, Talebi S, Khanmohammadi M, Kazemnejad S (2012) Osteogenic differentiation of stem cells derived from menstrual blood versus bone marrow in the presence of human platelet releasate. Tissue Eng Part A 18(15-16):1720–1728PubMedPubMedCentralCrossRefGoogle Scholar
  19. Díaz-Prado S, Muiños-López E, Hermida-Gómez T, Rendal-Vázquez ME, Fuentes-Boquete I, de Toro FJ, Blanco FJ (2010) Multilineage differentiation potential of cells isolated from the human amniotic membrane. J Cell Biochem 111:846–857PubMedCrossRefGoogle Scholar
  20. Díaz-Prado S, Muiños-López E, Hermida-Gómez T, Rendal-Vázquez ME, Fuentes-Boquete I, de Toro FJ, Blanco FJ (2011) Isolation and characterization of mesenchymal stem cells from human amniotic membrane. Tissue Eng Part C Methods 17(1):49–59PubMedCrossRefGoogle Scholar
  21. Dobreva MP, Pereira PN, Deprest J, Zwijsen A (2010) On the origin of amniotic stem cells: of mice and men. Int J Dev Biol 54(5):761–777PubMedCrossRefGoogle Scholar
  22. Erlebacher A (2013) Mechanisms of T cell tolerance towards the allogeneic fetus. Nat Rev Immunol 13(1):23–33PubMedCrossRefGoogle Scholar
  23. Favier B, Lemaoult J, Lesport E, Carosella ED (2010) ILT2/HLA-G interaction impairs NK-cell functions through the inhibition of the late but not the early events of the NK-cell activating synapse. FASEB J 24(3):689–699PubMedCrossRefGoogle Scholar
  24. Gao S, Ding J, Xiao HJ, Li ZQ, Chen Y, Zhou XS, Wang JE, Wu J, Shi WZ (2014) Anti-inflammatory and anti-apoptotic effect of combined treatment with methylprednisolone and amniotic membrane mesenchymal stem cells after spinal cord injury in rats. Neurochem Res 39(8):1544–1552PubMedCrossRefGoogle Scholar
  25. Ge X, Wang IN, Toma I, Sebastiano V, Liu J, Butte MJ, Reijo Pera RA, Yang PC (2012) Human amniotic mesenchymal stem cell-derived induced pluripotent stem cells may generate a universal source of cardiac cells. Stem Cells Dev 21(15):2798–2808PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ghieh F, Jurjus R, Ibrahim A, Geagea AG, Daouk H, El Baba B, Chams S, Matar M, Zein W, Jurjus A (2015) The use of stem cells in burn wound healing: a review. Biomed Res Int 2015:684084PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ghosh K, Kumar R, Singh J, Gahlawat SK, Kumar D, Selokar NL, Yadav SP, Gulati BR, Yadav PS (2015) Buffalo (Bubalus bubalis) term amniotic-membrane-derived cells exhibited mesenchymal stem cells characteristics in vitro. In Vitro Cell Dev Biol Anim 51(9):915–921PubMedCrossRefGoogle Scholar
  28. Gimble JM, Guilak F (2003) Adipose-derived adult stem cells: isolation, characterization and differentiation potential. Cytotherapy 5:362–369PubMedCrossRefGoogle Scholar
  29. Hu W, Guan FX, Li Y, Tang YJ, Yang F, Yang B (2013) New methods for inducing the differentiation of amniotic-derived mesenchymal stem cells into motor neuron precursor cells. Tissue Cell 45(5):295–305PubMedCrossRefGoogle Scholar
  30. Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U (2007) Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod 77:577–588PubMedCrossRefGoogle Scholar
  31. Ilancheran S, Moodley Y, Manuelpillai U (2009) Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta 30:2–10PubMedCrossRefGoogle Scholar
  32. In ‘t Anker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, Kanhai HH (2004) Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 22(7):1338–1345PubMedCrossRefGoogle Scholar
  33. Insausti CL, Blanquer M, García-Hernández AM, Castellanos G, Moraleda JM (2014) Amniotic membrane-derived stem cells: immunomodulatory properties and potential clinical application. Stem Cells Cloning 7:53–63PubMedPubMedCentralGoogle Scholar
  34. Jeddi-Tehrani M, Abbasi N, Dokouhaki P, Ghasemi J, Rezania S, Ostadkarampour M, Rabbani H, Akhondi MA, Fard ZT, Zarnani AH (2009) Indoleamine 2,3-dioxygenase is expressed in the endometrium of cycling mice throughout the oestrous cycle. J Reprod Immunol 80(1-2):41–48PubMedCrossRefGoogle Scholar
  35. Josefowicz SZ, Lu LF, Rudensky AY (2012) Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol 30:531–564PubMedCrossRefGoogle Scholar
  36. Kadam SS, Sudhakar M, Nair PD, Bhonde RR (2010) Reversal of experimental diabetes in mice by transplantation of neo-islets generated from human amnion-derived mesenchymal stromal cells using immuno-isolatory macrocapsules. Cytotherapy 12(8):982–991PubMedCrossRefGoogle Scholar
  37. Kamadjaja DB, Purwati, Rantam FA, Ferdiansyah, Pramono C (2014) The osteogenic capacity of human amniotic membrane mesenchymal stem cell (hAMSC) and potential for application in maxillofacial bone reconstruction in vitro study. J Biomed Sci Eng 7:497–503CrossRefGoogle Scholar
  38. Kang JW, Koo HC, Hwang SY, Kang SK, Ra JC, Lee MH, Park YH (2012a) Immunomodulatory effects of human amniotic membrane-derived mesenchymal stem cells. J Vet Sci 13(1):23–31PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kang NH, Hwang KA, Kim SU, Kim YB, Hyun SH, Jeung EB, Choi KC (2012b) Potential antitumor therapeutic strategies of human amniotic membrane and amniotic fluid-derived stem cells. Cancer Gene Ther 19(8):517–522PubMedCrossRefGoogle Scholar
  40. Kazemnejad S, Akhondi MM, Soleimani M, Zarnani AH, Khanmohammadi M, Darzi S (2012) Characterization and chondrogenic differentiation of menstrual blood-derived stem cells on a nanofibrous scaffold. Int J Artif Organs 35(1):55–66PubMedCrossRefGoogle Scholar
  41. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294–1301PubMedCrossRefGoogle Scholar
  42. Khanjani S, Khanmohammadi M, Zarnani AH, Akhondi MM, Ahani A, Ghaempanah Z, Naderi MM, Eghtesad S, Kazemnejad S (2014) Comparative evaluation of differentiation potential of menstrual blood- versus bone marrow-derived stem cells into hepatocyte-like cells. PLoS One 9(2):e86075PubMedPubMedCentralCrossRefGoogle Scholar
  43. Khanjani S, Khanmohammadi M, Zarnani AH, Talebi S, Edalatkhah H, Eghtesad S, Nikokar I, Kazemnejad S (2015) Efficient generation of functional hepatocyte-like cells from menstrual blood-derived stem cells. J Tissue Eng Regen Med 9(11):E124–E134PubMedCrossRefGoogle Scholar
  44. Khanmohammadi M, Khanjani S, Edalatkhah H, Zarnani AH, Heidari-Vala H, Soleimani M, Alimoghaddam K, Kazemnejad S (2014) Modified protocol for improvement of differentiation potential of menstrual blood-derived stem cells into adipogenic lineage. Cell Prolif 47(6):615–623PubMedCrossRefGoogle Scholar
  45. Kim HG, Choi OH (2011) Neovascularization in a mouse model via stem cells derived from human fetal amniotic membranes. Heart Vessels 26(2):196–205PubMedCrossRefGoogle Scholar
  46. Kim J, Kang HM, Kim H, Kim MR, Kwon HC, Gye MC, Kang SG, Yang HS, You J (2007) Ex vivo characteristics of human amniotic membrane-derived stem cells. Cloning Stem Cells 9(4):581–594PubMedCrossRefGoogle Scholar
  47. Kim SW, Zhang HZ, Kim CE, An HS, Kim JM, Kim MH (2012) Amniotic mesenchymal stem cells have robust angiogenic properties and are effective in treating hindlimb ischaemia. Cardiovasc Res 93(3):525–534PubMedCrossRefGoogle Scholar
  48. Kim KS, Kim HS, Park JM, Kim HW, Park MK, Lee HS, Lim DS, Lee TH, Chopp M, Moon J (2013a) Long-term immunomodulatory effect of amniotic stem cells in an Alzheimer’s disease model. Neurobiol Aging 34(10):2408–2420PubMedCrossRefGoogle Scholar
  49. Kim SW, Zhang HZ, Kim CE, Kim JM, Kim MH (2013b) Amniotic mesenchymal stem cells with robust chemotactic properties are effective in the treatment of a myocardial infarction model. Int J Cardiol 168(2):1062–1069PubMedCrossRefGoogle Scholar
  50. Kimura M, Toyoda M, Gojo S, Itakura Y, Kami D, Miyoshi S, Kyo S, Ono M, Umezawa A (2012) Allogeneic amniotic membrane-derived mesenchymal stromal cell transplantation in a porcine model of chronic myocardial ischemia. J Stem Cells Regen Med 8(3):171–180PubMedPubMedCentralGoogle Scholar
  51. Kmiecik G, Niklińska W, Kuć P, Pancewicz-Wojtkiewicz J, Fil D, Karwowska A, Karczewski J, Mackiewicz Z (2013) Fetal membranes as a source of stem cells. Adv Med Sci 58(2):185–195PubMedCrossRefGoogle Scholar
  52. Kögler G, Sensken S, Airey JA, Trapp T, Müschen M, Feldhahn N, Liedtke S, Sorg RV, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao J, Caplan AI, Colletti EJ, Almeida-Porada G, Müller HW, Zanjani E, Wernet P (2004) A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 200:123–135PubMedPubMedCentralCrossRefGoogle Scholar
  53. Koike C, Zhou K, Takeda Y, Fathy M, Okabe M, Yoshida T, Nakamura Y, Kato Y, Nikaido T (2014) Characterization of amniotic stem cells. Cell Reprogram 16(4):298–305PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 and memory antigen-specific T cells to their cognate peptide. Blood 101(9):3722–3729PubMedCrossRefGoogle Scholar
  55. Kronsteiner B, Wolbank S, Peterbauer A, Hackl C, Redl H, van Griensven M, Gabriel C (2011) Human mesenchymal stem cells from adipose tissue and amnion influence T-cells depending on stimulation method and presence of other immune cells. Stem Cells Dev 20(12):2115–2126PubMedCrossRefGoogle Scholar
  56. Kubo M, Sonoda Y, Muramatsu R, Usui M (2001) Immunogenicity of human amniotic membrane in experimental xenotransplantation. Invest Ophthalmol Vis Sci 42(7):1539–1546PubMedGoogle Scholar
  57. Kyurkchiev D, Bochev I, Ivanova-Todorova E, Mourdjeva M, Oreshkova T, Belemezova K, Kyurkchiev S (2014) Secretion of immunoregulatory cytokines by mesenchymal stem cells. World J Stem Cells 6(5):552–570PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lee AS, Tang C, Cao F, Xie X, van der Bogt K, Hwang A, Connolly AJ, Robbins RC, Wu JC (2009) Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8:2608–2612PubMedPubMedCentralCrossRefGoogle Scholar
  59. Li C, Zhang W, Jiang X, Mao N (2007) Human-placenta-derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cells. Cell Tissue Res 330(3):437–446PubMedCrossRefGoogle Scholar
  60. Li YP, Paczesny S, Lauret E, Poirault S, Bordigoni P, Mekhloufi F, Hequet O, Bertrand Y, Ou-Yang JP, Stoltz JF, Miossec P, Eljaafari A (2008a) Human mesenchymal stem cells license adult CD34+ hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathway. J Immunol 180(3):1598–1608PubMedCrossRefGoogle Scholar
  61. Li W, He H, Chen YT, Hayashida Y, Tseng SC (2008b) Reversal of myofibroblasts by amniotic membrane stromal extract. J Cell Physiol 215(3):657–664PubMedPubMedCentralCrossRefGoogle Scholar
  62. Li L, Tian H, Yue W, Zhu F, Li S, Li W (2011) Human mesenchymal stem cells play a dual role on tumor cell growth in vitro and in vivo. J Cell Physiol 226:1860–1867PubMedCrossRefGoogle Scholar
  63. Li F, Miao ZN, Xu YY, Zheng SY, Qin MD, Gu YZ, Zhang XG (2012) Transplantation of human amniotic mesenchymal stem cells in the treatment of focal cerebral ischemia. Mol Med Rep 6(3):625–630PubMedGoogle Scholar
  64. Li Y, Guo L, Ahn HS, Kim MH, Kim SW (2014) Amniotic mesenchymal stem cells display neurovascular tropism and aid in the recovery of injured peripheral nerves. J Cell Mol Med 18(6):1028–1034PubMedPubMedCentralCrossRefGoogle Scholar
  65. Li J, Koike-Soko C, Sugimoto J, Yoshida T, Okabe M, Nikaido T (2015) Human amnion-derived stem cells have immunosuppressive properties on NK Cells and monocytes. Cell Transplant 24(10):2065–2076PubMedCrossRefGoogle Scholar
  66. Lin X, Li HY, Chen LF, Liu BJ, Yao Y, Zhu WL (2013) Enhanced differentiation potential of human amniotic mesenchymal stromal cells by using three-dimensional culturing. Cell Tissue Res 352(3):523–535PubMedCrossRefGoogle Scholar
  67. Lindenmair A, Wolbank S, Stadler G, Meinl A, Peterbauer-Scherb A, Eibl J, Polin H, Gabriel C, van Griensven M, Redl H (2010) Osteogenic differentiation of intact human amniotic membrane. Biomaterials 31(33):8659–8665PubMedCrossRefGoogle Scholar
  68. Lu LL, Liu YJ, Yang SG et al (2006) Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica 91:1017–1026PubMedGoogle Scholar
  69. Lutz MB, Schuler G (2002) Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23(9):445–449PubMedCrossRefGoogle Scholar
  70. Lynge Nilsson L, Djurisic S, Hviid TV (2014) Controlling the immunological crosstalk during conception and pregnancy: HLA-G in reproduction. Front Immunol 5:198PubMedPubMedCentralCrossRefGoogle Scholar
  71. Magatti M, De Munari S, Vertua E, Gibelli L, Wengler GS, Parolini O (2008) Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem Cells 26:182–192PubMedCrossRefGoogle Scholar
  72. Magatti M, De Munari S, Vertua E, Nassauto C, Albertini A, Wengler GS, Parolini O (2009) Amniotic mesenchymal tissue cells inhibit dendritic cell differentiation of peripheral blood and amnion resident monocytes. Cell Transplant 18(8):899–914PubMedCrossRefGoogle Scholar
  73. Manuelpillai U, Moodley Y, Borlongan CV, Parolini O (2011) Amniotic membrane and amniotic cells: potential therapeutic tools to combat tissue inflammation and fibrosis? Placenta 32(Suppl 4):S320–S325PubMedCrossRefGoogle Scholar
  74. Marcus AJ, Coyne TM, Black IB, Woodbury D (2008) Fate of amnion-derived stem cells transplanted to the fetal rat brain: migration, survival and differentiation. J Cell Mol Med 12(4):1256–1264PubMedPubMedCentralCrossRefGoogle Scholar
  75. Marongiu F, Gramignoli R, Sun Q, Tahan V, Miki T, Dorko K, Ellis E, Strom SC (2010) Isolation of amniotic mesenchymal stem cells. Curr Protoc Stem Cell Biol Chapter 1:Unit 1E.5Google Scholar
  76. Maruyama N, Kokubo K, Shinbo T, Hirose M, Kobayashi M, Sakuragawa N, Kobayashi H (2013) Hypoxia enhances the induction of human amniotic mesenchymal side population cells into vascular endothelial lineage. Int J Mol Med 32(2):315–322PubMedGoogle Scholar
  77. Menetrier-Caux C, Montmain G, Dieu MC, Bain C, Favrot MC, Caux C, Blay JY (1998) Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor. Blood 92(12):4778–4791PubMedGoogle Scholar
  78. Murphy SP, Porrett PM, Turka LA (2011) Innate immunity in transplant tolerance and rejection. Immunol Rev 241(1):39–48PubMedCrossRefGoogle Scholar
  79. 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(4):2080–2087PubMedCrossRefGoogle Scholar
  80. Nikoo S, Ebtekar M, Jeddi-Tehrani M, Shervin A, Bozorgmehr M, Kazemnejad S, Zarnani AH (2012) Effect of menstrual blood-derived stromal stem cells on proliferative capacity of peripheral blood mononuclear cells in allogeneic mixed lymphocyte reaction. J Obstet Gynaecol Res 38(5):804–809PubMedCrossRefGoogle Scholar
  81. Onishi R, Ohnishi S, Higashi R, Watari M, Yamahara K, Okubo N, Nakagawa K, Katsurada T, Suda G, Natsuizaka M, Takeda H, Sakamoto N (2015) Human amnion-derived mesenchymal stem cell transplantation ameliorates dextran sulfate sodium-induced severe colitis in rats. Cell Transplant 24(12):2601–2614PubMedCrossRefGoogle Scholar
  82. Palamar M, Kaya E, Egrilmez S, Akalin T, Yagci A (2014) Amniotic membrane transplantation in surgical management of ocular surface squamous neoplasias: long-term results. Eye (Lond) 28(9):1131–1135CrossRefGoogle Scholar
  83. Paracchini V, Carbone A, Colombo F, Castellani S, Mazzucchelli S, Gioia SD, Degiorgio D, Seia M, Porretti L, Colombo C, Conese M (2012) Amniotic mesenchymal stemcells: a new source for hepatocyte-like cells and induction of CFTR expression by coculture with cystic fibrosis airway epithelial cells. J Biomed Biotechnol 2012:575471PubMedPubMedCentralCrossRefGoogle Scholar
  84. Parolini O, Alviano F, Bagnara GP, Bilic G, Bühring HJ, Evangelista M, Hennerbichler S, Liu B, Magatti M, Mao N, Miki T, Marongiu F, Nakajima H, Nikaido T, Portmann-Lanz CB, Sankar V, Soncini M, Stadler G, Surbek D, Takahashi TA, Redl H, Sakuragawa N, Wolbank S, Zeisberger S, Zisch A, Strom SC (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 26:300–311PubMedCrossRefGoogle Scholar
  85. Parolini O, Soncini M, Evangelista M, Schmidt D (2009) Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? Regen Med 4(2):275–291PubMedCrossRefGoogle Scholar
  86. Parry RV, Chemnitz JM, Frauwirth KA, Lanfranco AR, Braunstein I, Kobayashi SV, Linsley PS, Thompson CB, Riley JL (2005) CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol 25(21):9543–9553PubMedPubMedCentralCrossRefGoogle Scholar
  87. Phinney DG (2008) Isolation of mesenchymal stem cells from murine bone marrow by immunodepletion. Methods Mol Biol 449:171–186PubMedGoogle Scholar
  88. Pianta S, BonassiSignoroni P, Muradore I, Rodrigues MF, Rossi D, Silini A, Parolini O (2015) Amniotic membrane mesenchymal cells-derived factors skew T cell polarization toward Treg and downregulate Th1 and Th17 cells subsets. Stem Cell Rev 11(3):394PubMedCrossRefGoogle Scholar
  89. Pirjali T, Azarpira N, Ayatollahi M, Aghdaie MH, Geramizadeh B, Talai T (2013) Isolation and characterization of human mesenchymal stem cells derived from human umbilical cord Wharton’s jelly and amniotic membrane. Int J Organ Transplant Med 4(3):111–116PubMedPubMedCentralGoogle Scholar
  90. Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, Holzgreve W, Surbek DV (2006) Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 194(3):664–673PubMedCrossRefGoogle Scholar
  91. Rahimi M, Zarnani AH, Mohseni-Kouchesfehani H, Soltanghoraei H, Akhondi MM, Kazemnejad S (2014) Comparative evaluation of cardiac markers in differentiated cells from menstrual blood and bone marrow-derived stem cells in vitro. Mol Biotechnol 56(12):1151–1162PubMedCrossRefGoogle Scholar
  92. 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(1):71–76PubMedCrossRefGoogle Scholar
  93. Rennie K, Gruslin A, Hengstschläger M, Pei D, Cai J, Nikaido T, Bani-Yaghoub M (2012) Applications of amniotic membrane and fluid in stem cell biology and regenerative medicine. Stem Cells Int 2012:721538PubMedPubMedCentralCrossRefGoogle Scholar
  94. Resca E, Zavatti M, Maraldi T, Bertoni L, Beretti F, Guida M, La Sala GB, Guillot PV, David AL, Sebire NJ, De Pol A, De Coppi P (2015) Enrichment in c-Kit improved differentiation potential of amniotic membrane progenitor/stem cells. Placenta 36(1):18–26PubMedCrossRefGoogle Scholar
  95. Ristich V, Liang S, Zhang W, Wu J, Horuzsko A (2005) Tolerization of dendritic cells by HLA-G. Eur J Immunol 35(4):1133–1142PubMedCrossRefGoogle Scholar
  96. Roelen DL, van der Mast BJ, In ‘t Anker PS, Kleijburg C, Eikmans M, van Beelen E, de Groot-Swings GM, Fibbe WE, Kanhai HH, Scherjon SA, Claas FH (2009) Differential immunomodulatory effects of fetal versus maternal multipotent stromal cells. Hum Immunol 70(1):16–23PubMedCrossRefGoogle Scholar
  97. Rossi D, Pianta S, Magatti M, Sedlmayr P, Parolini O (2012) Characterization of the conditioned medium from amniotic membrane cells: prostaglandins as key effectors of its immunomodulatory activity. PLoS One 7(10):e46956PubMedPubMedCentralCrossRefGoogle Scholar
  98. Roubelakis MG, Trohatou O, Anagnou NP (2012) Amniotic fluid and amniotic membrane stem cells: marker discovery. Stem Cells Int 2012:107836PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sanberg PR, Eve DJ, Willing AE, Garbuzova-Davis S, Tan J, Sanberg CD, Allickson JG, Cruz LE, Borlongan CV (2011) The treatment of neurodegenerative disorders using umbilical cord blood and menstrual blood-derived stem cells. Cell Transpl 20:85–94CrossRefGoogle Scholar
  100. Seo MS, Park SB, Kim HS, Kang JG, Chae JS, Kang KS (2013) Isolation and characterization of equine amniotic membrane-derived mesenchymal stem cells. J Vet Sci 14(2):151–159PubMedPubMedCentralCrossRefGoogle Scholar
  101. Shojaeian J, Moazzeni SM, Nikoo S, Bozorgmehr M, Nikougoftar M, Zarnani AH (2007) Immunosuppressive effect of pregnant mouse serum on allostimulatory activity of dendritic cells. J Reprod Immunol 75(1):23–31PubMedCrossRefGoogle Scholar
  102. Singh R, Chacharkar MP (2011) Dried gamma-irradiated amniotic membrane as dressing in burn wound care. J Tissue Viability 20(2):49–54PubMedCrossRefGoogle Scholar
  103. Soncini M, Vertua E, Gibelli L, Zorzi F, Denegri M, Albertini A, Wengler GS, Parolini O (2007) Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 1:296–305PubMedCrossRefGoogle Scholar
  104. 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(3):1327–1333PubMedCrossRefGoogle Scholar
  105. Stadler G, Hennerbichler S, Lindenmair A, Peterbauer A, Hofer K, van Griensven M, Gabriel C, Redl H, Wolbank S (2008) Phenotypic shift of human amniotic epithelial cells in culture is associated with reduced osteogenic differentiation in vitro. Cytotherapy 10:743–752PubMedCrossRefGoogle Scholar
  106. Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21:685–711PubMedCrossRefGoogle Scholar
  107. Sun H, Hou Z, Yang H, Meng M, Li P, Zou Q, Yang L, Chen Y, Chai H, Zhong H, Yang ZZ, Zhao J, Lai L, Jiang X, Xiao Z (2014) Multiple systemic transplantations of human amniotic mesenchymal stem cells exert therapeutic effects in an ALS mouse model. Cell Tissue Res 357(3):571–582PubMedCrossRefGoogle Scholar
  108. Tabatabaei M, Mosaffa N, Nikoo S, Bozorgmehr M, Ghods R, Kazemnejad S, Rezania S, Keshavarzi B, Arefi S, Ramezani-Tehrani F, Mirzadegan E, Zarnani AH (2014) Isolation and partial characterization of human amniotic epithelial cells: the effect of trypsin. Avicenna J Med Biotechnol 6(1):10–20PubMedPubMedCentralGoogle Scholar
  109. Taghizadeh RR, Cetrulo KJ, Cetrulo CL (2011) Wharton’s jelly stem cells: future clinical applications. Placenta 32(Suppl 4):S311–S315PubMedCrossRefGoogle Scholar
  110. 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
  111. Tamagawa T, Oi S, Ishiwata I, Ishikawa H, Nakamura Y (2007) Differentiation of mesenchymal cells derived from human amniotic membranes into hepatocyte-like cells in vitro. Hum Cell 20(3):77–84PubMedCrossRefGoogle Scholar
  112. Tamagawa T, Ishiwata I, Ishikawa H, Nakamura Y (2008) Induced in vitro differentiation of neural-like cells from human amnion-derived fibroblast-like cells. Hum Cell 21(2):38–45PubMedCrossRefGoogle Scholar
  113. Tao J, Ji F, Liu B, Wang F, Dong F, Zhu Y (2012) Improvement of deficits by transplantation of lentiviral vector-modified human amniotic mesenchymal cells after cerebral ischemia in rats. Brain Res 1448:1–10PubMedCrossRefGoogle Scholar
  114. Teng Z, Yoshida T, Okabe M, Toda A, Higuchi O, Nogami M, Yoneda N, Zhou K, Kyo S, Kiyono T, Nikaido T (2013) Establishment of immortalized human amniotic mesenchymal stem cells. Cell Transplant 22(2):267–278PubMedCrossRefGoogle Scholar
  115. Toda A, Okabe M, Yoshida T, Nikaido T (2007) The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J Pharmacol Sci 105:215–228PubMedCrossRefGoogle Scholar
  116. Tsai MS, Hwang SM, Chen KD, Lee YS, Hsu LW, Chang YJ, Wang CN, Peng HH, Chang YL, Chao AS, Chang SD, Lee KD, Wang TH, Wang HS, Soong YK (2007) Functional network analysis of the transcriptomes of mesenchymal stem cells derived from amniotic fluid, amniotic membrane, cord blood, and bone marrow. Stem Cells 25(10):2511–2523PubMedCrossRefGoogle Scholar
  117. Tsuji H, Miyoshi S, Ikegami Y, Hida N, Asada H, Togashi I, Suzuki J, Satake M, Nakamizo H, Tanaka M, Mori T, Segawa K, Nishiyama N, Inoue J, Makino H, Miyado K, Ogawa S, Yoshimura Y, Umezawa A (2010) Xenografted human amniotic membrane-derived mesenchymal stem cells are immunologically tolerated and transdifferentiated into cardiomyocytes. Circ Res 106(10):1613–1623PubMedCrossRefGoogle Scholar
  118. Vidane AS, Souza AF, Sampaio RV, Bressan FF, Pieri NC, Martins DS, Meirelles FV, Miglino MA, Ambrósio CE (2009) Cat amniotic membrane multipotent cells are nontumorigenic and are safe for use in cell transplantation. Stem Cells Cloning 7:71–78Google Scholar
  119. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008) Functions of natural killer cells. Nat Immunol 9(5):503–510PubMedCrossRefGoogle Scholar
  120. Walther G, Gekas J, Bertrand OF (2009) Amniotic stem cells for cellular cardiomyoplasty: promises and premises. Catheter Cardiovasc Interv 73:917–924PubMedCrossRefGoogle Scholar
  121. Weiss ML, Anderson C, Medicetty S, Seshareddy KB, Weiss RJ, VanderWerff I, Troyer D, McIntosh KR (2008) Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells 26(11):2865–2874PubMedCrossRefGoogle Scholar
  122. Wolbank S, Peterbauer A, Fahrner M, Hennerbichler S, van Griensven M, Stadler G, Redl H, Gabriel C (2007) Dose-dependent immunomodulatory effect of human stem cells from amniotic membrane: a comparison with human mesenchymal stem cells from adipose tissue. Tissue Eng 13(6):1173–1183PubMedCrossRefGoogle Scholar
  123. Wu W, Lan Q, Lu H, Xu J, Zhu A, Fang W, Ge F, Hui G (2014) Human amnion mesenchymal cells negative co-stimulatory molecules PD-L1 expression and its capacity of modulating microglial activation of CNS. Cell Biochem Biophys 69(1):35–45PubMedCrossRefGoogle Scholar
  124. Xu M, Zhang B, Liu Y, Zhang J, Sheng H, Shi R, Liao L, Liu N, Hu J, Wang J, Ning H, Liu T, Zhang Y, Chen H (2014) The immunologic and hematopoietic profiles of mesenchymal stem cells derived from different sections of human umbilical cord. Acta Biochim Biophys Sin (Shanghai) 46(12):1056–1065CrossRefGoogle Scholar
  125. Zarnani AH, Moazzeni SM, Shokri F, Salehnia M, Dokouhaki P, Ghods R, Mahmoodi AR, Jeddi-Tehrani M (2008) Microenvironment of the feto-maternal interface protects the semiallogenic fetus through its immunomodulatory activity on dendritic cells. Fertil Steril 90(3):781–788PubMedCrossRefGoogle Scholar
  126. Zeng G, Wang G, Guan F, Chang K, Jiao H, Gao W, Xi S, Yang B (2011) Human amniotic membrane-derived mesenchymal stem cells labeled with superparamagnetic iron oxide nanoparticles: the effect on neuron-like differentiation in vitro. Mol Cell Biochem 357(1-2):331–341PubMedCrossRefGoogle Scholar
  127. Zhang D, Jiang M, Miao D (2011) Transplanted human amniotic membrane-derived mesenchymal stem cells ameliorate carbon tetrachloride-induced liver cirrhosis in mouse. PLoS One 6(2):e16789PubMedPubMedCentralCrossRefGoogle Scholar
  128. Zhao P, Ise H, Hongo M, Ota M, Konishi I, Nikaido T (2005) Human amniotic mesenchymal cells have some characteristics of cardiomyocytes. Transplantation 79(5):528–535PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Somaieh Kazemnejad
    • 1
  • Manijeh Khanmohammadi
    • 1
  • Amir-Hassan Zarnani
    • 2
    • 3
  • Mohammad Reza Bolouri
    • 3
  1. 1.Reproductive Biotechnology Research CenterAvicenna Research Institute, ACECRTehranIran
  2. 2.Department of Immunology, School of Public HealthTehran University of Medical SciencesTehranIran
  3. 3.Immunology Research CenterIran University of Medical SciencesTehranIran

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