Chorion mesenchymal stem cells show superior differentiation, immunosuppressive, and angiogenic potentials in comparison with haploidentical maternal placental cells

Stem Cells Translational Medicine

Volumn 4, Issue 10, 2015, Pages 1109-1121

  González, Paz L ^a,b   Carvajal, Catalina ^a   Cuenca, Jimena ^a,b   Alcayaga Miranda, Francisca ^a,b   Figueroa, Fernando E ^a   Bartolucci, Jorge ^a,b   Salazar Aravena, Lorena ^a,b   Khoury, Maroun ^a,b,c  

^a UNIVERSIDAD DE LOS ANDES   (Chile)

^b Chilean Consortium for Regenerative Medicine   (Chile)

^c Clínica Universidad de Los Andes ^*  (Chile)

Author keywords

Angiogenic potential; Chorion; Decidua; Fetal; Immunosuppression; Maternal; Mesenchymal stem cells; Placental cells; Umbilical cord

Indexed keywords

ANGIOGENIC FACTOR; CD56 ANTIGEN; SCATTER FACTOR; VASCULOTROPIN; NCAM1 PROTEIN, HUMAN;

ANGIOGENESIS; ANGIOGENESIS ASSAY; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHORION CELL; CLONOGENESIS; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOSUPPRESSIVE TREATMENT; MALE; MATRIGEL PLUG ASSAY; MESENCHYMAL STEM CELL; PLACENTA; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; T LYMPHOCYTE; TUBE FORMATION ASSAY; WST-1 ASSAY; ANTIBODY SPECIFICITY; BIOSYNTHESIS; CELL CULTURE; CHORION; COMPARATIVE STUDY; CYTOLOGY; DECIDUA; FEMALE; FETUS; FETUS BLOOD; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MESENCHYMAL STROMA CELL; NEWBORN;

ANTIGENS, CD56; CELL DIFFERENTIATION; CELLS, CULTURED; CHORION; DECIDUA; FEMALE; FETAL BLOOD; FETUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOSUPPRESSION; INFANT, NEWBORN; MALE; MESENCHYMAL STROMAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; ORGAN SPECIFICITY; REGENERATIVE MEDICINE; T-LYMPHOCYTES;

EID: 84942155415     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0022     Document Type: Article

References (70)

1. Corselli M, Chen CW, Crisan M et al. Perivascular ancestors of adult multipotent stem cells. Arterioscler Thromb Vasc Biol 2010;30: 1104-1109.
2. Pacini S, Petrini I. Are MSCs angiogenic cells? New insights on human nestin-positive bone marrow-derived multipotent cells. Front Cell Dev Biol 2014;2:20.
3. Fehrer C, Lepperdinger G. Mesenchymal stem cell aging. Exp Gerontol 2005;40:926-930.
4. Macias MI, Grande J, Moreno A et al. Isolation and characterization of true mesenchymal stemcells derived from human term decidua capableofmultilineagedifferentiationintoall3embryonic layers. Am J Obstet Gynecol 2010;203: 495.e9-495.e23.
5. Bieback K, Brinkmann I. Mesenchymal stromal cells from human perinatal tissues: From biology to cell therapy. World J Stem Cells 2010;2:81-92.
6. Parolini O, Alviano F, Bagnara GP et al. Concise review: Isolation and characterization of cells from human term placenta: Outcome of the first international Workshop on Placenta Derived Stem Cells. STEM CELLS 2008;26:300-311.
7. Hemberger M, Yang W, Natale D et al. Stem cells from fetal membranes-A workshop report. Placenta 2008;29(suppl A):S17-S19.
8. Marcus AJ, Woodbury D. Fetal stem cells from extra-embryonic tissues: Do not discard. J Cell Mol Med 2008;12:730-742.
9. Broxmeyer HE, Srour E, Orschell C et al. Cord blood stem and progenitor cells. Methods Enzymol 2006;419:439-473.
10. McNiece IK, Almeida-Porada G, Shpall EJ et al. Ex vivo expanded cord blood cells provide rapid engraftment in fetal sheep but lack longterm engrafting potential. Exp Hematol 2002; 30:612-616.
11. Bossolasco P, Montemurro T, Cova L et al. Molecular and phenotypic characterization of human amniotic fluid cells and their differentiation potential. Cell Res 2006;16: 329-336.
12. Roubelakis MG, Pappa KI, Bitsika V et al. Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: Comparison to bone marrow mesenchymal stem cells. Stem Cells Dev 2007; 16:931-952.
13. Tamagawa T, Oi S, Ishiwata I et al. Differentiation of mesenchymal cells derived from human amniotic membranes into hepatocytelike cells in vitro. Hum Cell 2007;20:77-84.
14. Wang H-S, Hung S-C, Peng S-T et al. Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. STEM CELLS 2004;22: 1330-1337.
15. Portmann-Lanz CB, Schoeberlein A, Huber A et al. Placental mesenchymal stem cells as potential autologous graft for pre-and perinatal neuroregeneration. Am J Obstet Gynecol 2006;194:664-673.
16. Soncini M, Vertua E, Gibelli L et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 2007;1:296-305.
17. Fukuchi Y, Nakajima H, Sugiyama D et al. Human placenta-derived cells have mesenchymal stem/progenitor cell potential. STEM CELLS 2004;22:649-658.
18. Igura K, Zhang X, Takahashi K et al. Isolation and characterization of mesenchymal progenitor cells from chorionic villi of human placenta. Cytotherapy 2004;6:543-553.
19. Huang Y-C, Yang Z-M, Chen X-H et al. Isolation of mesenchymal stem cells from human placental decidua basalis and resistance to hypoxia and serum deprivation. Stem Cell Rev 2009; 5:247-255.
20. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. STEM CELLS 2004;22:1338-1345.
21. Zhang Z, Lin H, Shi M et al. Human umbilical cord mesenchymal stem cells improve liver function and ascites in decompensated liver cirrhosis patients. J Gastroenterol Hepatol 2012; 27(suppl 2):112-120.
22. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells inhuman umbilical cord blood. Br J Haematol 2000;109:235-242.
23. Nazarov I, Lee JW, Soupene E et al. Multipotent stromal stem cells from human placenta demonstrate high therapeutic potential. STEM CELLS TRANSLATIONAL MEDICINE 2012;1:359-372.
24. Park S, Kim E, Koh S-E et al. Dopaminergic differentiation of neural progenitors derived from placental mesenchymal stem cells in the brains of Parkinson's disease model rats and alleviation of asymmetric rotational behavior. Brain Res 2012;1466:158-166.
25. Lu GH, Yong WS, Xu ZM et al. Human placental decidua basalis-derived mesenchymal stem cells differentiate into dopamine neuron-like cells with no response to longterm culture in vitro. Neuroreport 2012;23: 513-518.
26. Suşman S, Soriţău O, Rus-Ciucă D et al. Placental stem cell differentiation into islets of Langerhans-like glucagon-secreting cells. Rom J Morphol Embryol 2010;51:733-738.
27. Prather WR, Toren A, Meiron M et al. The role of placental-derived adherent stromal cell (PLX-PAD) in the treatment of critical limb ischemia. Cytotherapy 2009;11:427-434.
28. Kinzer M, Hingerl K, König J et al. Mesenchymal stromal cells from the human placenta promote neovascularization in a mouse model in vivo. Placenta 2014;35:517-519.
29. Ventura C, Cantoni S, Bianchi F et al. Hyaluronan mixed esters of butyric and retinoic acid drive cardiac and endothelial fate in term placenta human mesenchymal stem cells and enhance cardiac repair in infarcted rat hearts. J Biol Chem 2007;282:14243-14252.
30. Mayer L, Pandak WM, Melmed GY et al. Safety and tolerability of human placenta-derived cells (PDA001) in treatment-resistant Crohn's disease: A phase 1 study. Inflamm Bowel Dis 2013; 19:754-760.
31. Chambers DC, Enever D, Ilic N et al. A phase 1b study of placenta-derived mesenchymal stromal cells in patients with idiopathic pulmonary fibrosis. Respirology 2014;19:1013-1018.
32. Ramot Y, Meiron M, Toren A et al. Safety and biodistribution profile of placental-derived mesenchymal stromal cells (PLX-PAD) following intramuscular delivery. Toxicol Pathol 2009;37: 606-616.
33. Kim EY, Lee KB, Kim MK. Thepotentialof mesenchymal stem cells derived from amniotic membrane and amniotic fluid for neuronal regenerative therapy. BMB Rep 2014;47: 135-140.
34. Hass R, Kasper C, Böhm S et al. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 2011;9:12-25.
35. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stemcells. Nat Rev Mol Cell Biol 2011;12:126-131.
36. Wegmeyer H, Bröske A-M, Leddin M et al. Mesenchymal stromal cell characteristics vary depending on their origin. Stem Cells Dev 2013;22:2606-2618.
37. Li Y, Charif N, Mainard D et al. Donor's age dependent proliferation decrease of human bone marrow mesenchymal stem cells is linked to diminished clonogenicity. Biomed Mater Eng 2014;24(suppl):47-52.
38. Siddappa R, Licht R, van Blitterswijk C et al. Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering. J Orthop Res 2007;25:1029-1041.
39. Alcayaga-Miranda F, Cuenca J, Luz-Crawford P et al. Characterization of menstrual stem cells: Angiogenic effect, migration and hematopoietic stem cell support in comparison with bone marrow mesenchymal stem cells. Stem Cell Res Ther 2015;6:32.
40. Heazlewood CF, Sherrell H, Ryan J et al. High incidence of contaminating maternal cell overgrowth in human placental mesenchymal stem/stromal cell cultures: A systematic review. STEM CELLS TRANSLATIONAL MEDICINE 2014;3:1305-1311.
41. Dmitrieva RI, Minullina IR, Bilibina AA et al. Bone marrow-and subcutaneous adipose tissuederivedmesenchymal stemcells:Differences and similarities. Cell Cycle 2012;11:377-383.
42. Foy KC, Liu Z, Phillips G et al. Combination treatment with HER-2 and VEGF peptide mimics induces potent anti-tumor and anti-angiogenic responses in vitro and in vivo. J Biol Chem 2011; 286:13626-13637.
43. Wang L, Yang Y, Zhu Y et al. Characterization of placenta-derived mesenchymal stem cells cultured in autologous human cord blood serum. Mol Med Rep 2012;6:760-766.
44. Kern S, Eichler H, Stoeve J et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. STEM CELLS 2006;24:1294-1301.
45. Hwang JH, Shim SS, Seok OS et al. Comparison of cytokine expression inmesenchymal stem cells from human placenta, cord blood, and bone marrow. J Korean Med Sci 2009;24:547-554.
46. Castro-Manrreza ME, Mayani H, Monroy-García A et al. Humanmesenchymal stromal cells fromadult and neonatal sources: A comparative in vitro analysis of their immunosuppressive properties against T cells. Stem Cells Dev 2014; 23:1217-1232.
47. Kim MJ, Shin KS, Jeon JH et al. Human chorionic-plate-derived mesenchymal stem cells and Wharton's jelly-derived mesenchymal stem cells: A comparative analysis of their potential as placenta-derived stem cells. Cell Tissue Res 2011;346:53-64.
48. Wulf GG, Viereck V, Hemmerlein B et al. Mesengenic progenitor cells derived from human placenta. Tissue Eng 2004;10:1136-1147.
49. Lo YMD, Lau TK, Chan LYS et al. Quantitative analysis of the bidirectional fetomaternal transfer of nucleated cells and plasma DNA. Clin Chem 2000;46:1301-1309.
50. Srivatsa B, Srivatsa S, Johnson KL et al. Maternal cell microchimerism in newborn tissues. J Pediatr 2003;142:31-35.
51. Chen CP, Lee MY, Huang JP et al. Trafficking of multipotent mesenchymal stromal cells from maternal circulation through the placenta involves vascular endothelial growth factor receptor-1 and integrins. STEM CELLS 2008;26:550-561.
52. Battula VL, Treml S, Bareiss PM et al. Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-Haematologica 2009;94:173-184.
53. Mariotti E, Mirabelli P, Abate G et al. Comparative characteristics of mesenchymal stem cells from human bone marrow and placenta: CD10, CD49d, and CD56 make a difference. Stem Cells Dev 2008;17:1039-1041.
54. Kaltz N, Ringe J, Holzwarth C et al. Novel markers of mesenchymal stem cells defined by genome-wide gene expression analysis of stromal cells from different sources. Exp Cell Res 2010;316:2609-2617.
55. Chang Y-J, Shih DT, Tseng C-P et al. Disparate mesenchyme-lineage tendencies in mesenchymal stemcells fromhumanbonemarrow andumbilical cord blood. STEM CELLS 2006;24:679-685.
56. Barlow S, Brooke G, Chatterjee K et al. Comparison of human placenta-and bone marrow-derived multipotent mesenchymal stem cells. Stem Cells Dev 2008;17:1095-1107.
57. Gordeladze JO, Drevon CA, Syversen U et al. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: Impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem 2002;85:825-836.
58. Meisel R, Zibert A, Laryea M et al. Human bone marrow stromal cells inhibit allogeneic T-cellresponses by indoleamine 2, 3-dioxygenasemediated tryptophan degradation. Blood 2004; 103:4619-4621.
59. Aggarwal S, Pittenger MF. Humanmesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
60. Krampera M, Cosmi L, Angeli R et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. STEM CELLS 2006;24:386-398.
61. Selmani Z, Naji A, Zidi I et al. Human leukocyte antigen-G5secretionbyhumanmesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4 +CD25high FOXP3+ regulatory T cells. STEM CELLS 2008;26:212-222.
62. Cuerquis J, Romieu-Mourez R, François M et al. Human mesenchymal stromal cells transiently increase cytokine production by activated T cells before suppressing T-cell proliferation: Effect of interferon-g and tumor necrosis factor-a stimulation. Cytotherapy 2014;16: 191-202.
63. Lee JM, Jung J, Lee HJ et al. Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells. Int Immunopharmacol 2012;13:219-224.
64. Fazekasova H, Lechler R, Langford K et al. Placenta-derived MSCs are partially immunogenic and less immunomodulatory than bone marrow-derived MSCs. J Tissue Eng Regen Med 2011;5:684-694.
65. Lu G, Zhu S, Ke Y et al. Transplantationpotential-related biological properties of decidua basalis mesenchymal stem cells from maternal human term placenta. Cell Tissue Res 2013;352:301-312.
66. Erkers T, Nava S, Yosef J et al. Decidual stromal cells promote regulatory T cells and suppress alloreactivity in a cell contactdependent manner. Stem Cells Dev 2013; 22:2596-2605.
67. Han ZB, Wang YW, Wang T et al. [Isolation and biological characteristics of mesenchymal stem cells derived from human placenta decidua basalis]. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2013;21:754-759.
68. Zhu Y, Yang Y, Zhang Y et al. Placental mesenchymal stem cells of fetal and maternal origins demonstrate different therapeutic potentials. Stem Cell Res Ther 2014;5:48.
69. Wang Y, Zhao S. Vascular Biology of the Placenta. San Rafael, CA: Morgan & Claypool Life Sciences, 2010.
70. Tran TC, Kimura K, Nagano M et al. Identification of human placenta-derived mesenchymal stem cells involved in reendothelialization. J Cell Physiol 2011;226: 224-235.