Skip to main content

Advertisement

Log in

Intact human amniotic membrane differentiated towards the chondrogenic lineage

  • Original Paper
  • Published:
Cell and Tissue Banking Aims and scope Submit manuscript

Abstract

Human amniotic membrane (hAM) represents a tissue that is well established as biomaterial in the clinics with potential for new applications in regenerative medicine. For tissue engineering (TE) strategies, cells are usually combined with inductive factors and a carrier substrate. We have previously recognized that hAM represents a natural, preformed sheet including highly potent stem cells. In the present approach for cartilage regeneration we have induced chondrogenesis in hAM in vitro. For this, hAM biopsies were cultured for up to 56 days under chondrogenic conditions. The induced hAM was characterized for remaining viability, glycosaminoglycan (GAG) accumulation using histochemical analysis, and a quantitative assay. Collagen I, II and X was immunohistochemically determined and cartilage-specific mRNA expression of (sex determining region Y-) box 9, cartilage oligomeric matrix protein (COMP), aggrecan (AGC1), versican (CSPG2), COL1A1, COL9A2, melanoma inhibitory activity (MIA), and cartilage-linking protein 1 (CRTL1) analyzed by quantitative real-time polymerase chain reaction. Human AM was successfully induced to accumulate GAG, as demonstrated by Alcianblue staining and a significant (p < 0.001) increase of GAG/viability under chondrogenic conditions peaking in a 29.9 ± 0.9-fold induction on day 56. Further, upon chondrogenic induction collagen II positive areas were identified within histological sections and cartilage-specific markers including COMP, AGC1, CSPG2, COL1A1, COL9A2, MIA, and CRTL1 were found upregulated at mRNA level. This is the first study, demonstrating that upon in vitro induction viable human amnion expresses cartilage-specific markers and accumulates GAGs within the biomatrix. This is a promising first step towards a potential use of living hAM for cartilage TE.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akiyama H (2008) Control of chondrogenesis by the transcription factor Sox9. Mod Rheumatol 18:213–219

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Arya SK, Bhala S, Malik A, Sood S (2010) Role of amniotic membrane transplantation in ocular surface disorders. Nepal J Ophthalmol 2:145–153

    CAS  PubMed  Google Scholar 

  • 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

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dhall K (1984) Amnion graft for treatment of congenital absence of the vagina. Br J Obstet Gynaecol 91:279–282

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Dua HS, Gomes JA, King AJ, Maharajan VS (2004) The amniotic membrane in ophthalmology. Surv Ophthalmol 49:51–77

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gajiwala K, Gajiwala AL (2004) Evaluation of lyophilised, gamma-irradiated amnion as a biological dressing. Cell Tissue Bank 5:73–80

    Article  PubMed  Google Scholar 

  • Ganatra MA (2003) Amniotic membrane in surgery. J Pak Med Assoc 53:29–32

    CAS  PubMed  Google Scholar 

  • Gomes JA, Romano A, Santos MS, Dua HS (2005) Amniotic membrane use in ophthalmology. Curr Opin Ophthalmol 16:233–240

    Article  PubMed  Google Scholar 

  • Gruss JS, Jirsch DW (1978) Human amniotic membrane: a versatile wound dressing. Can Med Assoc J 118:1237–1246

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

  • Handorf AM, Li WJ (2011) Fibroblast growth factor-2 primes human mesenchymal stem cells for enhanced chondrogenesis. PLoS One 6:e22887

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kim YJ, Sah RL, Doong JY, Grodzinsky AJ (1988) Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174:168–176

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kock L, van Donkelaar CC, Ito K (2012) Tissue engineering of functional articular cartilage: the current status. Cell Tissue Res 347:613–627

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lefebvre V, Smits P (2005) Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 75:200–212

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miki T, Lehmann T, Cai H, Stolz DB, Strom SC (2005) Stem cell characteristics of amniotic epithelial cells. Stem Cells 23:1549–1559

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Nisolle M, Donnez J (1992) Vaginoplasty using amniotic membranes in cases of vaginal agenesis or after vaginectomy. J Gynecol Surg 8:25–30

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

  • Sakuragawa N, Yoshikawa H, Sasaki M (1992) Amniotic tissue transplantation: clinical and biochemical evaluations for some lysosomal storage diseases. Brain Dev 14:7–11

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Spoerl E, Wollensak G, Reber F, Pillunat L (2004) Cross-linking of human amniotic membrane by glutaraldehyde. Ophthalmic Res 36:71–77

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Subrahmanyam M (1995) Amniotic membrane as a cover for microskin grafts. Br J Plast Surg 48:477–478

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Tosi GM, Massaro-Giordano M, Caporossi A, Toti P (2005) Amniotic membrane transplantation in ocular surface disorders. J Cell Physiol 202:849–851

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Zimmermann D (2000) Versican. In: Iozzo RV (ed) Proteoglycans: structure, biology and molecular interactions. Taylor & Francis, London, pp 327–342

    Google Scholar 

Download references

Acknowledgments

This work has been supported by the European scientific grant NovusSanguis of the Fondation Jerôme LeJeune and the FIT-IT 2011 grant (NanoDetect) of the Austrian Research Promotion Agency (FFG). We thank Florian Hildner for technical assistance and input during manuscript preparation.

Disclosure

We would like to disclose that the co-authors Johann Eibl and Heinz Redl own the patent rights for “Process for differentiating stem cells of the amniotic membrane”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvia Nürnberger.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lindenmair, A., Nürnberger, S., Stadler, G. et al. Intact human amniotic membrane differentiated towards the chondrogenic lineage. Cell Tissue Bank 15, 213–225 (2014). https://doi.org/10.1007/s10561-014-9454-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10561-014-9454-9

Keywords

Navigation