Endothelial properties of third-Trimester amniotic fluid stem cells cultured in hypoxia

Stem Cell Research and Therapy

Volumn 6, Issue 1, 2015, Pages

  Schiavo, Andrea Alex ^a,b   Franzin, Chiara ^a   Albiero, Mattia ^b,c   Piccoli, Martina ^a   Spiro, Giovanna ^a,b   Bertin, Enrica ^a   Urbani, Luca ^a,d   Visentin, Silvia ^b   Cosmi, Erich ^b   Fadini, Gian Paolo ^b,c   De Coppi, Paolo ^d   Pozzobon, Michela ^a  

^a Foundation Institute of Pediatric Research Citt della Speranza   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

c Kit; Endothelial dysfunction; Fetal stem cells; Ischemia; Tissue regeneration

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN;

ADULT; AMNIOTIC FLUID STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CAROTID ARTERY DISEASE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; FEMALE; HINDLIMB; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIMB ISCHEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECOND TRIMESTER PREGNANCY; STEM CELL CULTURE; THIRD TRIMESTER PREGNANCY; AMNION FLUID; ANGIOGENESIS; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CYTOLOGY; ENDOTHELIAL PROGENITOR CELL; ISCHEMIA; KNOCKOUT MOUSE; PHYSIOLOGY; PREGNANCY; TRANSPLANTATION; VASCULARIZATION;

AMNIOTIC FLUID; ANIMALS; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL PROGENITOR CELLS; FEMALE; HINDLIMB; HUMANS; ISCHEMIA; MICE, INBRED BALB C; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PREGNANCY; PREGNANCY TRIMESTER, THIRD;

EID: 84945895817     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-015-0204-0     Document Type: Article

References (52)

1. Matsuzawa Y, Guddeti RR, Kwon TG, Lerman LO, Lerman A. Treating coronary disease and the impact of endothelial dysfunction. Prog Cardiovasc Dis. 2015;57:431-42. doi:10.1016/j.pcad.2014.10.004.
2. Shen WC, Liang CJ, Wu VC, Wang SH, Young GH, Lai IR, et al. Endothelial progenitor cells derived from Wharton's jelly of the umbilical cord reduces ischemia-induced hind limb injury in diabetic mice by inducing HIF-1alpha/IL-8 expression. Stem Cells Dev. 2013;22:1408-18. doi:10.1089/scd.2012.0445.
3. Prasain N, Lee MR, Vemula S, Meador JL, Yoshimoto M, Ferkowicz MJ, et al. Differentiation of human pluripotent stem cells to cells similar to cordblood endothelial colony-forming cells. Nat Biotechnol. 2014;32:1151-7. doi:10.1038/nbt.3048.
4. De Coppi P, Bartsch Jr G, Siddiqui MM, Xu T, Santos CC, Perin L, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25:100-6. doi:10.1038/nbt1274.
5. Ditadi A, de Coppi P, Picone O, Gautreau L, Smati R, Six E, et al. Human and murine amniotic fluid c-Kit+Lin-cells display hematopoietic activity. Blood. 2009;113:3953-60. doi:10.1182/blood-2008-10-182105.
6. Moschidou D, Mukherjee S, Blundell MP, Drews K, Jones GN, Abdulrazzak H, et al. Valproic acid confers functional pluripotency to human amniotic fluid stem cells in a transgene-free approach. Mol Ther. 2012;20:1953-67. doi:10.1038/mt.2012.117.
7. Prusa AR, Hengstschlager M. Amniotic fluid cells and human stem cell research: A new connection. Med Sci Monit. 2002;8:RA253-7.
8. Di Trapani M, Bassi G, Ricciardi M, Fontana E, Bifari F, Pacelli L, et al. Comparative study of immune regulatory properties of stem cells derived from different tissues. Stem Cells Dev. 2013;22:2990-3002. doi:10.1089/scd.2013.0204.
9. Klemmt PA, Vafaizadeh V, Groner B. The potential of amniotic fluid stem cells for cellular therapy and tissue engineering. Expert Opin Biol Ther. 2011;11:1297-314. doi:10.1517/14712598.2011.587800.
10. You Q, Cai L, Zheng J, Tong X, Zhang D, Zhang Y. Isolation of human mesenchymal stem cells from third-Trimester amniotic fluid. Int J Gynaecol Obstet. 2008;103:149-52. doi:10.1016/j.ijgo.2008.06.012.
11. Phermthai T, Odglun Y, Julavijitphong S, Titapant V, Chuenwattana P, Vantanasiri C, et al. A novel method to derive amniotic fluid stem cells for therapeutic purposes. BMC Cell Biol. 2010;11:79. doi:10.1186/1471-2121-11-79.
12. You Q, Tong X, Guan Y, Zhang D, Huang M, Zhang Y, et al. The biological characteristics of human third trimester amniotic fluid stem cells. J Int Med Res. 2009;37:105-12.
13. Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: A critical component of the stem cell niche. Cell Stem Cell. 2010;7:150-61. doi:10.1016/j.stem.2010.07.007.
14. Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T. Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol. 2006;207:331-9. doi:10.1002/jcp.20571.
15. Urbani L, Piccoli M, Franzin C, Pozzobon M, De Coppi P. Hypoxia increases mouse satellite cell clone proliferation maintaining both in vitro and in vivo heterogeneity and myogenic potential. PLoS One. 2012;7:e49860. doi:10.1371/journal.pone.0049860.
16. O'Neill TM, Wamhoff BR, Owens GK, Skalak TC. Paracrine Effect of Bone Marrow Cells on Hypoxia-Mediated Vascular Growth. FASEB J. 2006;20(Meeting Abstract Supplement):A716.
17. Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol. 2008;9:285-96. doi:10.1038/nrm2354.
18. Pozzobon M, Piccoli M, Schiavo AA, Atala A, De Coppi P. Isolation of c-Kit+ human amniotic fluid stem cells from second trimester. Methods Mol Biol. 2013;1035:191-8. doi:10.1007/978-1-62703-508-8-16.
19. Arnaoutova I, George J, Kleinman HK, Benton G. The endothelial cell tube formation assay on basement membrane turns 20: state of the science and the art. Angiogenesis. 2009;12:267-74. doi:10.1007/s10456-009-9146-4.
20. Rasband WS. ImageJ. U. S. National Institutes of Health, Bethesda, MD, USA. 1997-2014. http://imagej.nih.gov/ij/. Accessed 1 Apr 2012 2012.
21. Carpentier G. Angiogenesis Analyzer for ImageJ. 2012. http://image.bio. methods.free.fr/ImageJ/?Angiogenesis-Analyzer-for-ImageJ&lang=en. Accessed 1 Nov 2012 2012.
22. Voyta JC, Via DP, Butterfield CE, Zetter BR. Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J Cell Biol. 1984;99:2034-40.
23. Fadini GP, Albiero M, Menegazzo L, Boscaro E, Pagnin E, Iori E, et al. The redox enzyme p66Shc contributes to diabetes and ischemia-induced delay in cutaneous wound healing. Diabetes. 2010;59:2306-14. doi:10.2337/db09-1727.
24. Brouchet L, Krust A, Dupont S, Chambon P, Bayard F, Arnal JF. Estradiol accelerates reendothelialization in mouse carotid artery through estrogen receptor-Alpha but not estrogen receptor-beta. Circulation. 2001;103:423-8.
25. Lindner V, Fingerle J, Reidy MA. Mouse model of arterial injury. Circ Res. 1993;73:792-6.
26. Di Trapani M, Bassi G, Fontana E, Giacomello L, Pozzobon M, Guillot PV, et al. Immune regulatory properties of CD117(pos) amniotic fluid stem cells vary according to gestational age. Stem Cells Dev. 2015;24:132-43. doi:10.1089/scd.2014.0234.
27. Kuci S, Kuci Z, Kreyenberg H, Deak E, Putsch K, Huenecke S, et al. CD271 antigen defines a subset of multipotent stromal cells with immunosuppressive and lymphohematopoietic engraftment-promoting properties. Haematologica. 2010;95:651-9. doi:10.3324/haematol.2009.015065.
28. Ginsberg M, James D, Ding BS, Nolan D, Geng F, Butler JM, et al. Efficient direct reprogramming of mature amniotic cells into endothelial cells by ETS factors and TGFbeta suppression. Cell. 2012;151:559-75. doi:10.1016/j.cell.2012.09.032.
29. Wang S, Olson EN. AngiomiRs-key regulators of angiogenesis. Curr Opin Genet Dev. 2009;19:205-11. doi:10.1016/j.gde.2009.04.002.
30. Bottai D, Cigognini D, Nicora E, Moro M, Grimoldi MG, Adami R, et al. Third trimester amniotic fluid cells with the capacity to develop neural phenotypes and with heterogeneity among sub-populations. Restor Neurol Neurosci. 2012;30:55-68. doi:10.3233/RNN-2011-0620.
31. Ma T, Grayson WL, Frohlich M, Vunjak-Novakovic G. Hypoxia and stem cellbased engineering of mesenchymal tissues. Biotechnol Prog. 2009;25:32-42. doi:10.1002/btpr.128.
32. Lloyd-Griffith C, Duffy GP, O'Brien FJ. Investigating the effect of hypoxic culture on the endothelial differentiation of human amniotic fluid-derived stem cells. J Anat. 2015 Mar 31. doi: 10.1111/joa.12283. [Epub ahead of print].
33. Keene JD. RNA regulons: coordination of post-Transcriptional events. Nat Rev Genet. 2007;8:533-43. doi:10.1038/nrg2111.
34. Nicoli S, Standley C, Walker P, Hurlstone A, Fogarty KE, Lawson ND. MicroRNA-mediated integration of haemodynamics and Vegf signalling during angiogenesis. Nature. 2010;464:1196-200. doi:10.1038/nature08889.
35. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, et al. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272-84. doi:10.1016/j.devcel.2008.07.008.
36. Alaiti MA, Ishikawa M, Masuda H, Simon DI, Jain MK, Asahara T, et al. Up-regulation of miR-210 by vascular endothelial growth factor in ex vivo expanded CD34+ cells enhances cell-mediated angiogenesis. J Cell Mol Med. 2012;16:2413-21. doi:10.1111/j.1582-4934.2012.01557.x.
37. Vasilatou D, Papageorgiou S, Pappa V, Papageorgiou E, Dervenoulas J. The role of microRNAs in normal and malignant hematopoiesis. Eur J Haematol. 2010;84:1-16. doi:10.1111/j.1600-0609.2009.01348.x.
38. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, et al. MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 2006;108:3068-71. doi:10.1182/blood-2006-01-012369.
39. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells. 2004;22:377-84. doi:10.1634/stemcells.22-3-377.
40. Qin Y, Zhou P, Zhou C, Li J, Gao WQ. The adipose-derived lineage-negative cells are enriched mesenchymal stem cells and promote limb ischemia recovery in mice. Stem Cells Dev. 2014;23:363-71. doi:10.1089/scd.2013.0212.
41. Yamahara K, Harada K, Ohshima M, Ishikane S, Ohnishi S, Tsuda H, et al. Comparison of angiogenic, cytoprotective, and immunosuppressive properties of human amnion-And chorion-derived mesenchymal stem cells. PLoS One. 2014;9:e88319. doi:10.1371/journal.pone.0088319.
42. James D, Nam HS, Seandel M, Nolan D, Janovitz T, Tomishima M, et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat Biotechnol. 2010;28:161-6. doi:10.1038/nbt.1605.
43. Bollini S, Cheung KK, Riegler J, Dong X, Smart N, Ghionzoli M, et al. Amniotic fluid stem cells are cardioprotective following acute myocardial infarction. Stem Cells Dev. 2011;20:1985-94. doi:10.1089/scd.2010.0424.
44. Pederiva F, Ghionzoli M, Pierro A, De Coppi P, Tovar JA. Amniotic fluid stem cells rescue both in vitro and in vivo growth, innervation, and motility in nitrofen-exposed hypoplastic rat lungs through paracrine effects. Cell Transplant. 2013;22:1683-94. doi:10.3727/096368912X657756.
45. Rota C, Imberti B, Pozzobon M, Piccoli M, De Coppi P, Atala A, et al. Human amniotic fluid stem cell preconditioning improves their regenerative potential. Stem Cells Dev. 2012;21:1911-23. doi:10.1089/scd.2011.0333.
46. Zani A, Cananzi M, Fascetti-Leon F, Lauriti G, Smith VV, Bollini S, et al. Amniotic fluid stem cells improve survival and enhance repair of damaged intestine in necrotising enterocolitis via a COX-2 dependent mechanism. Gut. 2014;63:300-9. doi:10.1136/gutjnl-2012-303735.
47. Mirabella T, Cilli M, Carlone S, Cancedda R, Gentili C. Amniotic liquid derived stem cells as reservoir of secreted angiogenic factors capable of stimulating neo-Arteriogenesis in an ischemic model. Biomaterials. 2011;32:3689-99. doi:10.1016/j.biomaterials.2011.01.071.
48. Carmeliet P, Moons L, Stassen JM, De Mol M, Bouche A, van den Oord JJ, et al. Vascular wound healing and neointima formation induced by perivascular electric injury in mice. Am J Pathol. 1997;150:761-76.
49. Hagensen MK, Raarup MK, Mortensen MB, Thim T, Nyengaard JR, Falk E, et al. Circulating endothelial progenitor cells do not contribute to regeneration of endothelium after murine arterial injury. Cardiovasc Res. 2012;93:223-31. doi:10.1093/cvr/cvr278.
50. Timmermans F, Plum J, Yoder MC, Ingram DA, Vandekerckhove B, Case J. Endothelial progenitor cells: identity defined? J Cell Mol Med. 2009;13:87-102. doi:10.1111/j.1582-4934.2008.00598.x.
51. Krankel N, Kuschnerus K, Muller M, Speer T, Mocharla P, Madeddu P, et al. Novel insights into the critical role of bradykinin and the kinin B2 receptor for vascular recruitment of circulating endothelial repair-promoting mononuclear cell subsets: Alterations in patients with coronary disease. Circulation. 2013;127:594-603. doi:10.1161/CIRCULATIONAHA.112.118117.
52. Schatteman GC, Dunnwald M, Jiao C. Biology of bone marrow-derived endothelial cell precursors. Am J Physiol Heart Circ Physiol. 2007;292:H1-H18. doi:10.1152/ajpheart.00662.2006