Abstract
Human placental decidua basalis originates from the maternal side of the placenta and has been described as a source of mesenchymal stem cells (MSCs). However, for its application in tissue regeneration and repair, the transplantation-potential-related biological properties of decidua-basalis-derived mesenchymal stem cells (DBMSCs) remain to be elucidated. We obtained DBMSCs through enzymatic digestion and density gradient centrifugation and confirmed their capacity to differentiate into cell types of the mesodermal lineage, such as osteoblasts, adipocytes and chondroblasts. Karyotype analysis showed that the isolated DBMSCs maintained chromosomal stability after long-term culture in vitro. Growth kinetics and ultrastructural observation revealed a high level of DBMSC proliferative activity. In addition, DBMSCs showed immunosuppressive properties by suppressing both mitogen- and alloantigen-induced peripheral lymphocyte proliferation. All of these properties suggest that DBMSCs, which are abundant and easily accessible, are a novel potential source of seed cells for cell transplantation treatments.
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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 78:1439–1448
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 24:2466–2477
Clarke MF, Fuller M (2006) Stem cells and cancer: two faces of Eve. Cell 124:1111–1115
Conway DS, Pearce LA, Chin BS, Hart RG, Lip GY (2002) Plasma von Willebrand factor and soluble p-selectin as indices of endothelial damage and platelet activation in 1321 patients with nonvalvular atrial fibrillation: relationship to stroke risk factors. Circulation 106:1962–1967
Ding DC, Shyu WC, Lin SZ (2011) Mesenchymal stem cells. Cell Transplant 20:5–14
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317
Hori J, Wang M, Kamiya K, Takahashi H, Sakuragawa N (2006) Immunological characteristics of amniotic epithelium. Cornea 25:S53–S58
Horwitz EM, Andreef M, Frassoni F (2007) Mesenchymal stromal cells. Biol Blood Marrow Transplant 13:53–57
Huang YC, Yang ZM, Chen XH, Tan MY, Wang J, Li XQ, Xie HQ, Deng L (2009) Isolation of mesenchymal stem cells from human placental decidua basalis and resistance to hypoxia and serum deprivation. Stem Cell Rev 5:247–255
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 77:577–588
Ilancheran S, Moodley Y, Manuelpillai U (2009) Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta 30:2–10
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 22:1338–1345
Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, Markham AF, Jack A, Emery P, McGonagle D (2002) Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349–3360
Junker JP, Sommar P, Skog M, Johnson H, Kratz G (2010) Adipogenic, chondrogenic and osteogenic differentiation of clonally derived human dermal fibroblasts. Cells Tissues Organs 191:105–118
Kakishita K, Nakao N, Sakuragawa N, Itakura T (2003) Implantation of human amniotic epithelial cells prevents the degeneration of nigral dopamine neurons in rats with 6-hydroxydopamine lesions. Brain Res 980:48–56
Kaplan JM, Youd ME, Lodie TA (2011) Immunomodulatory activity of mesenchymal stem cells. Curr Stem Cell Res Ther 6:297–316
Laurent LC, Ulitsky I, Slavin I, Tran H, Schork A, Morey R, Lynch C, Harness JV, Lee S, Barrero MJ, Ku S, Martynova M, Semechkin R, Galat V, Gottesfeld J, Izpisua Belmonte JC, Murry C, Keirstead HS, Park HS, Schmidt U, Laslett AL, Muller FJ, Nievergelt CM, Shamir R, Loring JF (2011) Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 8:106–118
Le Blanc K, Ringden O (2007) Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 262:509–525
Li H, Fan X, Kovi RC, Jo Y, Moquin B, Konz R, Stoicov C, Kurt-Jones E, Grossman SR, Lyle S, Rogers AB, Montrose M, Houghton J (2007) Spontaneous expression of embryonic factors and p53 point mutations in aged mesenchymal stem cells: a model of age-related tumorigenesis in mice. Cancer Res 67:10889–10898
Li M, Zhang SZ, Guo YW, Cai YQ, Yan ZJ, Zou Z, Jiang XD, Ke YQ, He XY, Jin ZL, Lu GH, Su DQ (2010) Human umbilical vein-derived dopaminergic-like cell transplantation with nerve growth factor ameliorates motor dysfunction in a rat model of Parkinson’s disease. Neurochem Res 35:1522–1529
Lindner U, Kramer J, Rohwedel J, Schlenke P (2010) Mesenchymal stem or stromal cells: toward a better understanding of their biology? Transfus Med Hemother 37:75–83
Martin FT, Dwyer RM, Kelly J, Khan S, Murphy JM, Curran C, Miller N, Hennessy E, Dockery P, Barry FP, O’Brien T, Kerin MJ (2010) Potential role of mesenchymal stem cells (MSCs) in the breast tumour microenvironment: stimulation of epithelial to mesenchymal transition (EMT). Breast Cancer Res Treat 124:317–326
Meisner LF, Johnson JA (2008) Protocols for cytogenetic studies of human embryonic stem cells. Methods 45:133–141
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
Park JS, Chu JS, Cheng C, Chen F, Chen D, Li S (2004) Differential effects of equiaxial and uniaxial strain on mesenchymal stem cells. Biotechnol Bioeng 88:359–368
Rubio D, Garcia-Castro J, Martin MC, Fuente R de la, Cigudosa JC, Lloyd AC, Bernad A (2005) Spontaneous human adult stem cell transformation. Cancer Res 65:3035–3039
Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, Itoh M, Kuniyasu Y, Nomura T, Toda M, Takahashi T (2001) Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 182:18–32
Sankar V, Muthusamy R (2003) Role of human amniotic epithelial cell transplantation in spinal cord injury repair research. Neuroscience 118:11–17
Satija NK, Singh VK, Verma YK, Gupta P, Sharma S, Afrin F, Sharma M, Sharma P, Tripathi RP, Gurudutta GU (2009) Mesenchymal stem cell-based therapy: a new paradigm in regenerative medicine. J Cell Mol Med 13:4385–4402
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 1:296–305
Venkataramana NK, Kumar SK, Balaraju S, Radhakrishnan RC, Bansal A, Dixit A, Rao DK, Das M, Jan M, Gupta PK, Totey SM (2010) Open-labeled study of unilateral autologous bone-marrow-derived mesenchymal stem cell transplantation in Parkinson’s disease. Transl Res 155:62–70
Wei JP, Zhang TS, Kawa S, Aizawa T, Ota M, Akaike T, Kato K, Konishi I, Nikaido T (2003) Human amnion-isolated cells normalize blood glucose in streptozotocin-induced diabetic mice. Cell Transplant 12:545–552
Wolbank S, Peterbauer A, Fahrner M, Hennerbichler S, Griensven M van, 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 13:1173–1183
Yang Y, Rossi FM, Putnins EE (2007) Ex vivo expansion of rat bone marrow mesenchymal stromal cells on microcarrier beads in spin culture. Biomaterials 28:3110–3120
Zhang J, Li Y, Chen J, Cui Y, Lu M, Elias SB, Mitchell JB, Hammill L, Vanguri P, Chopp M (2005) Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Exp Neurol 195:16–26
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
Zhao P, Ise H, Hongo M, Ota M, Konishi I, Nikaido T (2005) Human amniotic mesenchymal cells have some characteristics of cardiomyocytes. Transplantation 79:528–535
Zhou D, Jiang X, Xu R, Cai Y, Hu J, Xu G, Zou Y, Zeng Y (2008a) Assessing the cytoskeletal system and its elements in C6 glioma cells and astrocytes by atomic force microscopy. Cell Mol Neurobiol 28:895–905
Zhou K, Zhang H, Jin O, Feng X, Yao G, Hou Y, Sun L (2008b) Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr mice. Cell Mol Immunol 5:417–424
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We thank Ms. Jin Xu from the Medical Languages Center of Southern Medical University for her proofreading of this paper.
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This study was supported by the National Natural Science Foundation of China (no. 81172416/H1618) and Sci-Tech Research Projects of Guangdong Province (no. 2009B030801375).
The authors declare no competing financial interests.
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Lu, G., Zhu, S., Ke, Y. et al. Transplantation-potential-related biological properties of decidua basalis mesenchymal stem cells from maternal human term placenta. Cell Tissue Res 352, 301–312 (2013). https://doi.org/10.1007/s00441-013-1560-7
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DOI: https://doi.org/10.1007/s00441-013-1560-7