Intact human amniotic membrane differentiated towards the chondrogenic lineage

Cell and Tissue Banking

Volumn 15, Issue 2, 2014, Pages 213-225

  Lindenmair, Andrea ^a,b,c   Nürnberger, Sylvia ^a,c,d,e   Stadler, Guido ^a,c   Meinl, Alexandra ^a,c,e   Hackl, Christa ^b,c   Eibl, Johann ^f   Gabriel, Christian ^b,c   Hennerbichler, Simone ^b,c   Redl, Heinz ^a,c   Wolbank, Susanne ^a,c  

^a LUDWIG BOLTZMANN INSTITUTE FOR EXPERIMENTAL AND CLINICAL TRAUMATOLOGY   (Austria)

^b Red Cross Blood Transfusion Service of Upper Austria Austrian Cluster for Tissue Regeneration   (Austria)

^c Austrian Cluster for Tissue Regeneration   (Austria)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

^e Bernhard Gottlieb School of Dentistry   (Austria)

^f Bio Products and Bio Engineering AG   (Austria)

Author keywords

Amniotic membrane; Cartilage; Chondrogenic; Differentiation; Human; Tissue engineering

Indexed keywords

AMNION; CARTILAGE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CHONDROGENESIS; CYTOLOGY; FEMALE; HUMAN; PHYSIOLOGY; PLACENTA; PREGNANCY; STEM CELL;

AMNION; CARTILAGE; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHONDROGENESIS; FEMALE; HUMANS; PLACENTA; PREGNANCY; STEM CELLS;

EID: 84902544395     PISSN: 13899333     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10561-014-9454-9     Document Type: Article

References (85)

1. Akiyama H (2008) Control of chondrogenesis by the transcription factor Sox9. Mod Rheumatol 18:213-219
2. Akle CA, Adinolfi M, Welsh KI, Leibowitz S, McColl I (1981) Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet 2:1003-1005
3. 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 7:11
4. Arora M, Jaroudi KA, Hamilton CJ, Dayel F (1994) Controlled comparison of interceed and amniotic membrane graft in the prevention of postoperative adhesions in the rabbit uterine horn model. Eur J Obstet Gynecol Reprod Biol 55:179-182
5. Arya SK, Bhala S, Malik A, Sood S (2010) Role of amniotic membrane transplantation in ocular surface disorders. Nepal J Ophthalmol 2:145-153
6. Banerjee A, Nurnberger S, Hennerbichler S, Riedl S, Schuh CM, Hacobian A, Teuschl A, Eibl J, Redl H, Wolbank S (2013) In toto differentiation of human amniotic membrane towards the Schwann cell lineage. Cell Tissue Bank. doi: 10.1007/s10561-013-9401-1
7. Bosserhoff AK, Kaufmann M, Kaluza B, Bartke I, Zirngibl H, Hein R, Stolz W, Buettner R (1997) Melanoma-inhibiting activity, a novel serum marker for progression of malignant melanoma. Cancer Res 57:3149-3153
8. Buckley CT, Kelly DJ (2012) Expansion in the presence of FGF-2 enhances the functional development of cartilaginous tissues engineered using infrapatellar fat pad derived MSCs. J Mech Behav Biomed Mater 11:102-111
9. Cheng T, Yang C, Weber N, Kim HT, Kuo AC (2012) Fibroblast growth factor 2 enhances the kinetics of mesenchymal stem cell chondrogenesis. Biochem Biophys Res Commun 426:544-550
10. Dhall K (1984) Amnion graft for treatment of congenital absence of the vagina. Br J Obstet Gynaecol 91:279-282
11. Diaz-Prado S, Muinos-Lopez E, Hermida-Gomez T, Rendal-Vazquez ME, Fuentes-Boquete I, de Toro FJ, Blanco FJ (2010a) Isolation and characterization of Mesenchymal Stem Cells from Human Amniotic Membrane. Tissue Eng Part C Methods 17(1):49-59
12. Diaz-Prado S, Rendal-Vazquez ME, Muinos-Lopez E, Hermida-Gomez T, Rodriguez-Cabarcos M, Fuentes-Boquete I, de Toro FJ, Blanco FJ (2010b) Potential use of the human amniotic membrane as a scaffold in human articular cartilage repair. Cell Tissue Bank 11:183-195
13. Dua HS, Gomes JA, King AJ, Maharajan VS (2004) The amniotic membrane in ophthalmology. Surv Ophthalmol 49:51-77
14. Faulk WP, Matthews R, Stevens PJ, Bennett JP, Burgos H, Hsi BL (1980) Human amnion as an adjunct in wound healing. Lancet 1:1156-1158
15. Gajiwala K, Gajiwala AL (2004) Evaluation of lyophilised, gamma-irradiated amnion as a biological dressing. Cell Tissue Bank 5:73-80
16. Ganatra MA (2003) Amniotic membrane in surgery. J Pak Med Assoc 53:29-32
17. Gomes JA, Romano A, Santos MS, Dua HS (2005) Amniotic membrane use in ophthalmology. Curr Opin Ophthalmol 16:233-240
18. Gruss JS, Jirsch DW (1978) Human amniotic membrane: a versatile wound dressing. Can Med Assoc J 118:1237-1246
19. Hamdi H, Boitard SE, Planat-Benard V, Pouly J, Neamatalla H, Joanne P, Perier MC, Bellamy V, Casteilla L, Li Z, Hagege AA, Mericskay M, Menasche P, Agbulut O (2013) Efficacy of epicardially delivered adipose stroma cell sheets in dilated cardiomyopathy. Cardiovasc Res
20. Handorf AM, Li WJ (2011) Fibroblast growth factor-2 primes human mesenchymal stem cells for enhanced chondrogenesis. PLoS One 6:e22887
21. Hao Y, Ma DH, Hwang DG, Kim WS, Zhang F (2000) Identification of antiangiogenic and antiinflammatory proteins in human amniotic membrane. Cornea 19:348-352
22. He Q, Li Q, Chen B, Wang Z (2002) Repair of flexor tendon defects of rabbit with tissue engineering method. Chin J Traumatol 5:200-208
23. Hennerbichler S, Reichl B, Pleiner D, Gabriel C, Eibl J, Redl H (2007) The influence of various storage conditions on cell viability in amniotic membrane. Cell Tissue Bank 8:1-8
24. Hildner F, Peterbauer A, Wolbank S, Nurnberger S, Marlovits S, Redl H, van Griensven M, Gabriel C (2010) FGF-2 abolishes the chondrogenic effect of combined BMP-6 and TGF-beta in human adipose derived stem cells. J Biomed Mater Res A 94:978-987
25. Hopkinson A, Shanmuganathan VA, Gray T, Yeung AM, Lowe J, James DK, Dua HS (2008) Optimization of amniotic membrane (AM) denuding for tissue engineering. Tissue Eng Part C Methods 14:371-381
26. Kabiri A, Esfandiari E, Hashemibeni B, Kazemi M, Mardani M, Esmaeili A (2012) Effects of FGF-2 on human adipose tissue derived adult stem cells morphology and chondrogenesis enhancement in Transwell culture. Biochem Biophys Res Commun 424:234-238
27. Kang JW, Koo HC, Hwang SY, Kang SK, Ra JC, Lee MH, Park YH (2012) Immunomodulatory effects of human amniotic membrane-derived mesenchymal stem cells. J Vet Sci 13:23-31
28. Kim JC, Tseng SC (1995) The effects on inhibition of corneal neovascularization after human amniotic membrane transplantation in severely damaged rabbit corneas. Korean J Ophthalmol 9:32-46
29. Kim YJ, Sah RL, Doong JY, Grodzinsky AJ (1988) Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174:168-176
30. Kim JH, Lee MC, Seong SC, Park KH, Lee S (2011) Enhanced proliferation and chondrogenic differentiation of human synovium-derived stem cells expanded with basic fibroblast growth factor. Tissue Eng Part A 17:991-1002
31. Kock L, van Donkelaar CC, Ito K (2012) Tissue engineering of functional articular cartilage: the current status. Cell Tissue Res 347:613-627
32. Kronsteiner B, Peterbauer-Scherb A, Grillari-Voglauer R, Redl H, Gabriel C, van Griensven M, Wolbank S (2011a) Human mesenchymal stem cells and renal tubular epithelial cells differentially influence monocyte-derived dendritic cell differentiation and maturation. Cell Immunol 267:30-38
33. Kronsteiner B, Wolbank S, Peterbauer A, Hackl C, Redl H, van Griensven M, Gabriel C (2011b) 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 20:2115-2126
34. Lambeth LS, Cummins DM, Doran TJ, Sinclair AH, Smith CA (2013) Overexpression of aromatase alone is sufficient for ovarian development in genetically male chicken embryos. PLoS One 8:e68362
35. Lefebvre V, Smits P (2005) Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 75:200-212
36. Li Q, Liu T, Zhang L, Liu Y, Zhang W, Liu W, Cao Y, Zhou G (2011) The role of bFGF in down-regulating alpha-SMA expression of chondrogenically induced BMSCs and preventing the shrinkage of BMSC engineered cartilage. Biomaterials 32:4773-4781
37. 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 31:8659-8665
38. Lindenmair A, Hatlapatka T, Kollwig G, Hennerbichler S, Gabriel C, Wolbank S, Redl H, Kasper C (2012) Mesenchymal stem or stromal cells from amnion and umbilical cord tissue and their potential for clinical applications. Cells 1:1061-1088
39. Maeda S, Fujitomo T, Okabe T, Wakitani S, Takagi M (2011) Shrinkage-free preparation of scaffold-free cartilage-like disk-shaped cell sheet using human bone marrow mesenchymal stem cells. J Biosci Bioeng 111:489-492
40. Magatti M, De MS, Vertua E, Gibelli L, Wengler GS, Parolini O (2008) Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem Cells 26:182-192
41. Magatti M, De MS, 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 18:899-914
42. Mendes LF, Pirraco RP, Szymczyk W, Frias AM, Santos TC, Reis RL, Marques AP (2012) Perivascular-like cells contribute to the stability of the vascular network of osteogenic tissue formed from cell sheet-based constructs. PLoS One 7:e41051
43. Miki T, Lehmann T, Cai H, Stolz DB, Strom SC (2005) Stem cell characteristics of amniotic epithelial cells. Stem Cells 23:1549-1559
44. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, Ishino K, Ishida H, Shimizu T, Kangawa K, Sano S, Okano T, Kitamura S, Mori H (2006) Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 12:459-465
45. Mligiliche N, Endo K, Okamoto K, Fujimoto E, Ide C (2002) Extracellular matrix of human amnion manufactured into tubes as conduits for peripheral nerve regeneration. J Biomed Mater Res 63:591-600
46. Narita T, Shintani Y, Ikebe C, Kaneko M, Harada N, Tshuma N, Takahashi K, Campbell NG, Coppen SR, Yashiro K, Sawa Y, Suzuki K (2013a) The use of cell-sheet technique eliminates arrhythmogenicity of skeletal myoblast-based therapy to the heart with enhanced therapeutic effects. Int J Cardiol 168(1):261-269
47. Narita T, Shintani Y, Ikebe C, Kaneko M, Campbell NG, Coppen SR, Uppal R, Sawa Y, Yashiro K, Suzuki K (2013b) The use of scaffold-free cell sheet technique to refine mesenchymal stromal cell-based therapy for heart failure. Mol Ther 21:860-867
48. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM (2008) Properties of the amniotic membrane for potential use in tissue engineering. Eur Cell Mater 15:88-99
49. Nisolle M, Donnez J (1992) Vaginoplasty using amniotic membranes in cases of vaginal agenesis or after vaginectomy. J Gynecol Surg 8:25-30
50. Parolini O, Alviano F, Bagnara GP, Bilic G, Buhring 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 26:300-311
51. Peacock JD, Huk DJ, Ediriweera HN, Lincoln J (2011) Sox9 transcriptionally represses Spp1 to prevent matrix mineralization in maturing heart valves and chondrocytes. PLoS One 6:e26769
52. Perrier E, Ronziere MC, Bareille R, Pinzano A, Mallein-Gerin F, Freyria AM (2011) Analysis of collagen expression during chondrogenic induction of human bone marrow mesenchymal stem cells. Biotechnol Lett 33:2091-2101
53. Petter-Puchner AH, Fortelny RH, Mika K, Hennerbichler S, Redl H, Gabriel C (2011) Human vital amniotic membrane reduces adhesions in experimental intraperitoneal onlay mesh repair. Surg Endosc 25:2125-2131
54. Philip J, Hackl F, Canseco JA, Kamel RA, Kiwanuka E, Diaz-Siso JR, Caterson EJ, Junker JP, Eriksson E (2013) Amnion-derived multipotent progenitor cells improve achilles tendon repair in rats. Eplasty 13:e31
55. Poghosyan T, Gajoux S, Vanneaux V, Bruneval P, Domet T, Lecourt S, Jarraya M, Sfeir R, Larghero J, Cattan P (2013) In vitro development and characterization of a tissue engineered conduit resembling esophageal wall using human and pig skeletal myoblast, oral epithelial cells and biologic scaffolds. Tissue Eng Part A 19(19-20):2242-2252
56. 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 194:664-673
57. Pratama G, Vaghjiani V, Tee JY, Liu YH, Chan J, Tan C, Murthi P, Gargett C, Manuelpillai U (2011) Changes in culture expanded human amniotic epithelial cells: implications for potential therapeutic applications. PLoS One 6:e26136
58. Rennekampff HO, Dohrmann P, Fory R, Fandrich F (1994) Evaluation of amniotic membrane as adhesion prophylaxis in a novel surgical gastroschisis model. J Invest Surg 7:187-193
59. Riau AK, Beuerman RW, Lim LS, Mehta JS (2010) Preservation, sterilization and de-epithelialization of human amniotic membrane for use in ocular surface reconstruction. Biomaterials 31:216-225
60. Ricci E, Vanosi G, Lindenmair A, Hennerbichler S, Peterbauer-Scherb A, Wolbank S, Cargnoni A, Signoroni PB, Campagnol M, Gabriel C, Redl H, Parolini O (2013) Anti-fibrotic effects of fresh and cryopreserved human amniotic membrane in a rat liver fibrosis model. Cell Tissue Bank 14(3):475-488
61. Rommel N, Rohleder NH, Gabriel C, Hennerbichler S, Bauer F, Mucke T, Kolk A, Loeffelbein DJ, Wolff KD, Kesting MR (2013) Secondary correction of posttraumatic orbital wall adhesions by membranes laminated with amniotic membrane. Br J Oral Maxillofac Surg 51(8):e224-e229
62. Sakuragawa N, Yoshikawa H, Sasaki M (1992) Amniotic tissue transplantation: clinical and biochemical evaluations for some lysosomal storage diseases. Brain Dev 14:7-11
63. Solchaga LA, Penick K, Goldberg VM, Caplan AI, Welter JF (2010) Fibroblast growth factor-2 enhances proliferation and delays loss of chondrogenic potential in human adult bone-marrow-derived mesenchymal stem cells. Tissue Eng Part A 16:1009-1019
64. Spoerl E, Wollensak G, Reber F, Pillunat L (2004) Cross-linking of human amniotic membrane by glutaraldehyde. Ophthalmic Res 36:71-77
65. 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 10:743-752
66. Subrahmanyam M (1995) Amniotic membrane as a cover for microskin grafts. Br J Plast Surg 48:477-478
67. Sudo K, Kanno M, Miharada K, Ogawa S, Hiroyama T, Saijo K, Nakamura Y (2007) Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells 25:1610-1617
68. Takagi R, Yamato M, Kanai N, Murakami D, Kondo M, Ishii T, Ohki T, Namiki H, Yamamoto M, Okano T (2012) Cell sheet technology for regeneration of esophageal mucosa. World J Gastroenterol 18:5145-5150
69. Tallheden T, Karlsson C, Brunner A, Van Der Lee J, Hagg R, Tommasini R, Lindahl A (2004) Gene expression during redifferentiation of human articular chondrocytes. Osteoarthritis Cartilage 12:525-535
70. Tosi GM, Massaro-Giordano M, Caporossi A, Toti P (2005) Amniotic membrane transplantation in ocular surface disorders. J Cell Physiol 202:849-851
71. Tuei VC, Ha JS, Ha CE (2011) Effects of human serum albumin complexed with free fatty acids on cell viability and insulin secretion in the hamster pancreatic beta-cell line HIT-T15. Life Sci 88:810-818
72. Tylki-Szymanska A, Maciejko D, Kidawa M, Jablonska-Budaj U, Czartoryska B (1985) Amniotic tissue transplantation as a trial of treatment in some lysosomal storage diseases. J Inherit Metab Dis 8:101-104
73. Wainwright EN, Jorgensen JS, Kim Y, Truong V, Bagheri-Fam S, Davidson T, Svingen T, Fernandez-Valverde SL, McClelland KS, Taft RJ, Harley VR, Koopman P, Wilhelm D (2013) SOX9 regulates microRNA miR-202-5p/3p expression during mouse testis differentiation. Biol Reprod 89(2):34
74. Ward DJ, Bennett JP, Burgos H, Fabre J (1989) The healing of chronic venous leg ulcers with prepared human amnion. Br J Plast Surg 42:463-467
75. Wei JP, Nawata M, Wakitani S, Kametani K, Ota M, Toda A, Konishi I, Ebara S, Nikaido T (2009) Human amniotic mesenchymal cells differentiate into chondrocytes. Cloning Stem Cells 11:19-26
76. Wilshaw SP, Kearney JN, Fisher J, Ingham E (2006) Production of an acellular amniotic membrane matrix for use in tissue engineering. Tissue Eng 12:2117-2129
77. 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 13:1173-1183
78. Wolbank S, Hildner F, Redl H, van Griensven M, Gabriel C, Hennerbichler S (2009) Impact of human amniotic membrane preparation on release of angiogenic factors. J Tissue Eng Regen Med 3:651-654
79. Yang J, Yamato M, Nishida K, Ohki T, Kanzaki M, Sekine H, Shimizu T, Okano T (2006) Cell delivery in regenerative medicine: the cell sheet engineering approach. J Control Release 116:193-203
80. Yeager AM, Singer HS, Buck JR, Matalon R, Brennan S, O'Toole SO, Moser HW (1985) A therapeutic trial of amniotic epithelial cell implantation in patients with lysosomal storage diseases. Am J Med Genet 22:347-355
81. Yokoi H, Yan YL, Miller MR, BreMiller RA, Catchen JM, Johnson EA, Postlethwait JH (2009) Expression profiling of zebrafish sox9 mutants reveals that Sox9 is required for retinal differentiation. Dev Biol 329:1-15
82. Yokoyama A, Muneta T, Nimura A, Koga H, Mochizuki T, Hata Y, Sekiya I (2007) FGF2 and dexamethasone increase the production of hyaluronan in two-dimensional culture of elastic cartilage-derived cells: in vitro analyses and in vivo cartilage formation. Cell Tissue Res 329:469-478
83. Young RL, Cota J, Zund G, Mason BA, Wheeler JM (1991) The use of an amniotic membrane graft to prevent postoperative adhesions. Fertil Steril 55:624-628
84. Zhou J, Yu G, Cao C, Pang J, Chen X (2011) Bone morphogenetic protein-7 promotes chondrogenesis in human amniotic epithelial cells. Int Orthop 35:941-948
85. Zimmermann D (2000) Versican. In: Iozzo RV (ed) Proteoglycans: structure, biology and molecular interactions. Taylor & Francis, London, pp 327-342