Immune regulatory properties of CD117pos amniotic fluid stem cells vary according to gestational age

Stem Cells and Development

Volumn 24, Issue 1, 2015, Pages 132-143

  Di Trapani, Mariano ^a   Bassi, Giulio ^a   Fontana, Emanuela ^b   Giacomello, Luca ^b   Pozzobon, Michela ^c   Guillot, Pascale V ^d,e   De Coppi, Paolo ^c,e   Krampera, Mauro ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HLA ANTIGEN CLASS 1; STEM CELL FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

AMNIOTIC FLUID CELL; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRUCTURE; CELLS BY BODY ANATOMY; CYTOTOXICITY; FIRST TRIMESTER PREGNANCY; GERM LAYER; GESTATIONAL AGE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOPHENOTYPING; IMMUNOREGULATION; LYMPHOCYTE PROLIFERATION; MOLECULAR MECHANICS; NATURAL KILLER CELL; SENSITIVITY ANALYSIS; T LYMPHOCYTE; AMNION FLUID; CELL PROLIFERATION; CLINICAL TRIAL; COCULTURE; CYTOLOGY; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE; MULTIPOTENT STEM CELL; PREGNANCY; THIRD TRIMESTER PREGNANCY;

AMNIOTIC FLUID; CELL PROLIFERATION; COCULTURE TECHNIQUES; FEMALE; GESTATIONAL AGE; HUMANS; IMMUNE TOLERANCE; LYMPHOCYTES; MULTIPOTENT STEM CELLS; PREGNANCY; PREGNANCY TRIMESTER, THIRD; PROTO-ONCOGENE PROTEINS C-KIT;

EID: 84919807905     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0234     Document Type: Article

References (47)

1. Prusa AR, E Marton, M Rosner, G Bernaschek and M Hengstschlager. (2003). Oct-4-expressing cells in human amniotic fluid: a new source for stem cell research? Hum Reprod 18:1489-1493.
2. Karlmark KR, A Freilinger, E Marton, M Rosner, G Lubec and M Hengstschlager. (2005). Activation of ectopic Oct-4 and Rex-1 promoters in human amniotic fluid cells. Int J Mol Med 16:987-992.
3. Tsai MS, SM Hwang, YL Tsai, FC Cheng, JL Lee and YJ Chang. (2006). Clonal amniotic fluid-derived stem cells express characteristics of both mesenchymal and neural stem cells. Biol Reprod 74:545-551.
4. De Coppi P, G Bartsch, Jr., MM Siddiqui, T Xu, CC Santos, L Perin, G Mostoslavsky, AC Serre, EY Snyder, et al. (2007). Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25:100-106.
5. Pozzobon M, M Piccoli, AA Schiavo, A Atala and P De Coppi. (2013). Isolation of c-Kit + human amniotic fluid stem cells from second trimester. Methods Mol Biol 1035:191-198.
6. Cananzi M and P De Coppi. (2012). CD117( + ) amniotic fluid stem cells: state of the art and future perspectives. Organogenesis 8:77-88.
7. Sedrakyan S, S Da Sacco, A Milanesi, L Shiri, A Petrosyan, R Varimezova, D Warburton, KV Lemley, RE De Filippo and L Perin. (2012). Injection of amniotic fluid stem cells delays progression of renal fibrosis. J Am Soc Nephrol 23:661-673.
8. Moschidou D, S Mukherjee, MP Blundell, K Drews, GN Jones, H Abdulrazzak, B Nowakowska, A Phoolchund, K Lay, et al. (2012). Valproic acid confers functional pluripotency to human amniotic fluid stem cells in a transgenefree approach. Mol Ther 20:1953-1967.
9. Moschidou D, S Mukherjee, MP Blundell, GN Jones, AJ Atala, AJ Thrasher, NM Fisk, P De Coppi and PV Guillot. (2013). Human mid-trimester amniotic fluid stem cells cultured under embryonic stem cell conditions with valproic acid acquire pluripotent characteristics. Stem Cells Dev 22:444-458.
10. Carraro G, L Perin, S Sedrakyan, S Giuliani, C Tiozzo, J Lee, G Turcatel, SP De Langhe, B Driscoll, et al. (2008). Human amniotic fluid stem cells can integrate and differentiate into epithelial lung lineages. Stem Cells 26:2902-2911.
11. Ghionzoli M, M Cananzi, A Zani, CA Rossi, FF Leon, A Pierro, S Eaton and P De Coppi. (2010). Amniotic fluid stem cell migration after intraperitoneal injection in pup rats: implication for therapy. Pediatr Surg Int 26:79-84.
12. Bollini S, M Pozzobon, M Nobles, J Riegler, X Dong, M Piccoli, A Chiavegato, AN Price, M Ghionzoli, et al. (2011). In vitro and in vivo cardiomyogenic differentiation of amniotic fluid stem cells. Stem Cell Rev 7:364-380.
13. Piccoli M, C Franzin, E Bertin, L Urbani, B Blaauw, A Repele, E Taschin, A Cenedese, GF Zanon, et al. (2012). Amniotic fluid stem cells restore the muscle cell niche in a HSA-Cre, Smn(F7/F7) mouse model. Stem Cells 30:1675-1684.
14. Riccio M, T Maraldi, A Pisciotta, GB La Sala, A Ferrari, G Bruzzesi, A Motta, C Migliaresi and A De Pol. (2012). Fibroin scaffold repairs critical-size bone defects in vivo supported by human amniotic fluid and dental pulp stem cells. Tissue Eng Part A 18:1006-1013.
15. Rodrigues MT, BK Lee, SJ Lee, ME Gomes, RL Reis, A Atala and JJ Yoo. (2012). The effect of differentiation stage of amniotic fluid stem cells on bone regeneration. Biomaterials 33:6069-6078.
16. Rota C, B Imberti, M Pozzobon, M Piccoli, P De Coppi, A Atala, E Gagliardini, C Xinaris, V Benedetti, et al. (2012). Human amniotic fluid stem cell preconditioning improves their regenerative potential. Stem Cells Dev 21:1911-1923.
17. Krampera M. (2011). Mesenchymal stromal cell ?licensing': a multistep process. Leukemia 25:1408-1414.
18. Moorefield EC, EE McKee, L Solchaga, G Orlando, JJ Yoo, S Walker, ME Furth and CE Bishop. (2011). Cloned, CD117 selected human amniotic fluid stem cells are capable of modulating the immune response. PLoS One 6:e26535.
19. Gosemann JH, JF Kuebler, M Pozzobon, C Neunaber, JH Hensel, M Ghionzoli, P de Coppi, BM Ure and G Holze. (2012). Activation of regulatory T cells during inflammatory response is not an exclusive property of stem cells. PLoS One 7:e35512.
20. Di Trapani M, G Bassi, M Ricciardi, E Fontana, F Bifari, L Pacelli, L Giacomello, M Pozzobon, F Feron, et al. (2013). Comparative study of immune regulatory properties of stem cells derived from different tissues. Stem Cells Dev 22:2990-3002.
21. Sessarego N, A Parodi, M Podesta, F Benvenuto, M Mogni, V Raviolo, M Lituania, A Kunkl, G Ferlazzo, et al. (2008). Multipotent mesenchymal stromal cells from amniotic fluid: solid perspectives for clinical application. Haematologica 93:339-346.
22. Moschidou D, K Drews, A Eddaoudi, J Adjaye, P De Coppi and PV Guillot. (2013). Molecular signature of human amniotic fluid stem cells during fetal development. Curr Stem Cell Res Ther 8:73-81.
23. Menard C, L Pacelli, G Bassi, J Dulong, F Bifari, I Bezier, J Zanoncello, M Ricciardi, M Latour, et al. (2013). Clinicalgrade mesenchymal stromal cells produced under various good manufacturing practice processes differ in their immunomodulatory properties: standardization of immune quality controls. Stem Cells Dev 22:1789-1801.
24. Ren G, X Zhao, L Zhang, J Zhang, A L'Huillier, W Ling, AI Roberts, AD Le, S Shi, C Shao and Y Shi. (2010). Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol 184:2321-2328.
25. Augello A, R Tasso, SM Negrini, A Amateis, F Indiveri, R Cancedda and G Pennesi. (2005). Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 35:1482-1490.
26. Luz-Crawford P, D Noel, X Fernandez, M Khoury, F Figueroa, F Carrion, C Jorgensen and F Djouad. (2012). Mesenchymal stem cells repress Th17 molecular program through the PD-1 pathway. PLoS One 7:e45272.
27. Najar M, G Raicevic, HF Kazan, C De Bruyn, D Bron, M Toungouz and L Lagneaux. (2012). Immune-related antigens, surface molecules and regulatory factors in human-derived mesenchymal stromal cells: the expression and impact of inflammatory priming. Stem Cell Rev 8:1188-1198.
28. Krampera M, L Cosmi, R Angeli, A Pasini, F Liotta, A Andreini, V Santarlasci, B Mazzinghi, G Pizzolo, et al. (2006). Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24:386-398.
29. Meisel R, A Zibert, M Laryea, U Gobel, W Daubener and D Dilloo. (2004). Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenasemediated tryptophan degradation. Blood 103:4619-4621.
30. Su J, X Chen, Y Huang, W Li, J Li, K Cao, G Cao, L Zhang, F Li, et al. (2014). Phylogenetic distinction of iNOS and IDO function in mesenchymal stem cell-mediated immunosuppression in mammalian species. Cell Death Differ 21:388-396.
31. Spaggiari GM, A Capobianco, S Becchetti, MC Mingari and L Moretta. (2006). Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NKcell proliferation. Blood 107:1484-1490.
32. Benvenuto F, S Ferrari, E Gerdoni, F Gualandi, F Frassoni, V Pistoia, G Mancardi and A Uccelli. (2007). Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells 25:1753-1760.
33. Polchert D, J Sobinsky, G Douglas, M Kidd, A Moadsiri, E Reina, K Genrich, S Mehrotra, S Setty, B Smith and A Bartholomew. (2008). IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol 38:1745-1755.
34. Rafei M, E Birman, K Forner and J Galipeau. (2009). Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol Ther 17:1799-1803.
35. Gonzalez MA, E Gonzalez-Rey, L Rico, D Buscher and M Delgado. (2009). Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology 136:978-989.
36. Sun L, K Akiyama, H Zhang, T Yamaza, Y Hou, S Zhao, T Xu, A Le and S Shi. (2009). Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 27:1421-1432.
37. Ball LM, ME Bernardo, H Roelofs, A Lankester, A Cometa, RM Egeler, F Locatelli and WE Fibbe. (2007). Cotransplantation of ex vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stemcell transplantation. Blood 110:2764-2767.
38. Le Blanc K, F Frassoni, L Ball, F Locatelli, H Roelofs, I Lewis, E Lanino, B Sundberg, ME Bernardo, et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371:1579-1586.
39. Duijvestein M, AC Vos, H Roelofs, ME Wildenberg, BB Wendrich, HW Verspaget, EM Kooy-Winkelaar, F Koning, JJ Zwaginga, et al. (2010). Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 59:1662-1669.
40. Ciccocioppo R, ME Bernardo, A Sgarella, R Maccario, MA Avanzini, C Ubezio, A Minelli, C Alvisi, A Vanoli, et al. (2011). Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 60:788-798.
41. Stubbendorff M, T Deuse, X Hua, TT Phan, K Bieback, K Atkinson, TH Eiermann, J Velden, C Schroder, et al. (2013). Immunological properties of extraembryonic human mesenchymal stromal cells derived from gestational tissue. Stem Cells Dev 22:2619-2629.
42. Weiss ML, C Anderson, S Medicetty, KB Seshareddy, RJ Weiss, I VanderWerff, D Troyer and KR McIntosh. (2008). Immune properties of human umbilical cord Wharton's jelly-derived cells. Stem Cells 26:2865-2874.
43. Yamahara K, K Harada, M Ohshima, S Ishikane, S Ohnishi, H Tsuda, K Otani, A Taguchi, T Soma, et al. (2014). Comparison of angiogenic, cytoprotective, and immunosuppressive properties of human amnion-and chorionderived mesenchymal stem cells. PLoS One 9:e88319.
44. Valli A,M Rosner, C Fuchs, N Siegel, CE Bishop, H Dolznig, U Madel, W Feichtinger, A Atala and M Hengstschlager. (2010). Embryoid body formation of human amniotic fluid stem cells depends on mTOR. Oncogene 29:966-977.
45. Ma X, S Zhang, J Zhou, B Chen, Y Shang, T Gao, X Wang, H Xie and F Chen. (2012). Clone-derived human AFamniotic fluid stem cells are capable of skeletal myogenic differentiation in vitro and in vivo. J Tissue Eng Regen Med 6:598-613.
46. Bottai D, G Scesa, D Cigognini, R Adami, E Nicora, S Abrignani, AM Di Giulio and A Gorio. (2014). Third trimester NG2-positive amniotic fluid cells are effective in improving repair in spinal cord injury. Exp Neurol 254:121-133.
47. Sidney LE, MJ Branch, SE Dunphy, HS Dua and A Hopkinson. (2014). Concise review: evidence for CD34 as a common marker for diverse progenitors. Stem Cells 32: 1380-1389.