The amniotic membrane as a biological scaffold, its preparation and use in regenerative medicine in Slovenia

  • Tina Cirman Blood Transfusion Center of Slovenia, Ljubljana, Slovenia
  • Taja Železnik Ramuta Institute of Cell Biology, Faculty of Medicine, University of Ljubljana, Ljubljana, Sloveni
  • Zala Lužnik Department of Ophthalmology, University Medical Centre Ljubljana, Ljubljana, Slovenia
  • Marko Hawlina Department of Ophthalmology, University Medical Centre Ljubljana, Ljubljana, Slovenia
  • Petra Schollmayer Department of Ophthalmology, University Medical Centre Ljubljana, Ljubljana, Slovenia
  • Dragica Smrke Division of surgery, University Medical Centre Ljubljana, Ljubljana, Slovenia
  • Mateja Erdani Kreft Institute of Cell Biology, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia
Keywords: Amniotic membrane, scaffold, regenerative medicine, ophtalmology, dermatology, urology, stem cells

Abstract

Background: Amniotic membrane is the innermost layer of the placenta, surrounding and protecting the embryo (AM). AM is a multilayered tissue, composed of amniotic epithelial cells, amniotic mesenchymal stromal cells, basal lamina, and stroma. AM's properties, which are the result of its structural features, render it extremely useful for therapeutic purposes, most notably in ophthalmology since it enhances epithelialization, is a substrate for cell growth, decreases fibrosis and tissue neovascularization and has antimicrobial properties. Due to its mechanical properties, which are mostly a result of the basal lamina's and stroma's extracellular matrix, AM is used increasingly as a biological scaffold in regenerative medicine.

 

Conclusions: Regenerative medicine is an interdisciplinary field of research and clinical applications, utilising principles of biological and engineering sciences in the development of viable tissue or organ replacements. In regenerative medicine, we distinguish three approaches: 1) engraftment of functional cells (including stem cells) into the damaged or defective tissue; 2) reshaping of the damaged or defective tissue using synthetic or natural materials, and 3)  tissue engineering i.e. use of scaffolds for the enhancement of the growth of tissue-specific cells and development of new, regenerated tissue. Furthermore, we present the use of AM as a biological scaffold in regenerative medicine in Slovenia.

 

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Author Biography

Tina Cirman, Blood Transfusion Center of Slovenia, Ljubljana, Slovenia

Inštitut za biologijo celice, Medicinska fakulteta, Univerza v Ljubljani, Ljubljana

References

Méhats C, Schmitz T, Marcellin L, Breuiller-Fouché M. [Biochemistry of fetal membranes rupture]. Gynécol Obstét Fertil. 2011 Jun;39(6):365–9. https://doi.org/10.1016/j.gyobfe.2011.04.006 PMID:21602079

Dua HS, Gomes JA, King AJ, Maharajan VS. The amniotic membrane in ophthalmology. Surv Ophthalmol. 2004 Jan-Feb;49(1):51–77. https://doi.org/10.1016/j.survophthal.2003.10.004PMID:14711440

Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM. Properties of the amniotic membrane for potential use in tissue engineering. Eur Cell Mater. 2008 Apr;15:88–99. https://doi.org/10.22203/eCM.v015a07 PMID:18446690

Ockleford C, Malak T, Hubbard A, Bracken K, Burton SA, Bright N, et al. Confocal and conventional immunofluorescence and ultrastructural localisation of intracellular strength-giving components of human amniochorion. J Anat. 1993 Dec;183(Pt 3):483–505. PMID:7507914

Kobayashi K, Miwa H, Yasui M. Inflammatory mediators weaken the amniotic membrane barrier through disruption of tight junctions. J Physiol. 2010 Dec;588(Pt 24):4859–69. https://doi.org/10.1113/jphysiol.2010.197764 PMID:21041526

Fukuda K, Chikama T, Nakamura M, Nishida T. Differential distribution of subchains of the basement membrane components type IV collagen and laminin among the amniotic membrane, cornea, and conjunctiva. Cornea. 1999 Jan;18(1):73–9. https://doi.org/10.1097/00003226-199901000-00013 PMID:9894941

Meinert M, Eriksen GV, Petersen AC, Helmig RB, Laurent C, Uldbjerg N, et al. Proteoglycans and hyaluronan in human fetal membranes. Am J Obstet Gynecol. 2001 Mar;184(4):679–85. https://doi.org/10.1067/mob.2001.110294 PMID:11262472

Wolf HJ, Schmidt W, Drenckhahn D. Immunocytochemical analysis of the cytoskeleton of the human amniotic epithelium. Cell Tissue Res. 1991 Nov;266(2):385–9. https://doi.org/10.1007/BF00318194 PMID:1764730

Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, Macvicar J. Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta. 1993 Jul-Aug;14(4):385–406. https://doi.org/10.1016/S0143-4004(05)80460-6 PMID:8248033

Kolega J, Manabe M, Sun TT. Basement membrane heterogeneity and variation in corneal epithelial differentiation. Differentiation. 1989 Oct;42(1):54–63. https://doi.org/10.1111/j.1432-0436.1989.tb00607.x PMID:2695378

Gipson IK, Spurr-Michaud SJ, Tisdale AS. Anchoring fibrils form a complex network in human and rabbit cornea. Invest Ophthalmol Vis Sci. 1987 Feb;28(2):212–20. PMID:8591898

Endo K, Nakamura T, Kawasaki S, Kinoshita S. Human amniotic membrane, like corneal epithelial basement membrane, manifests the alpha5 chain of type IV collagen. Invest Ophthalmol Vis Sci. 2004 Jun;45(6):1771–4. https://doi.org/10.1167/iovs.03-0952PMID:15161839

Riau AK, Beuerman RW, Lim LS, Mehta JS. Preservation, sterilization and de-epithelialization of human amniotic membrane for use in ocular surface reconstruction. Biomaterials. 2010 Jan;31(2):216–25. https://doi.org/10.1016/j.biomaterials.2009.09.034PMID:19781769

Meller D, Tseng SC. Conjunctival epithelial cell differentiation on amniotic membrane. Invest Ophthalmol Vis Sci. 1999 Apr;40(5):878–86. PMID:10102284

Velez I, Parker WB, Siegel MA, Hernandez M. Cryopreserved amniotic membrane for modulation of periodontal soft tissue healing: a pilot study. J Periodontol. 2010 Dec;81(12):1797–804. https://doi.org/10.1902/jop.2010.100060 PMID:20629549

Choi JA, Jin HJ, Jung S, Yang E, Choi JS, Chung SH, et al. Effects of amniotic membrane suspension in human corneal wound healing in vitro. Mol Vis. 2009 Nov;15:2230–8. PMID:19907665

Dua HS, Azuara-Blanco A. Amniotic membrane transplantation. Br J Ophthalmol. 1999 Jun;83(6):748–52. https://doi.org/10.1136/bjo.83.6.748 PMID:10340988

Ohshima M, Tokunaga K, Sato S, Maeno M, Otsuka K. Laminin- and fibronectin-like molecules produced by periodontal ligament fibroblasts under serum-free culture are potent chemoattractants for gingival epithelial cells. J Periodontal Res. 2003 Apr;38(2):175–81. https://doi.org/10.1034/j.1600-0765.2003.01628.x PMID:12608912

Koizumi NJ, Inatomi TJ, Sotozono CJ, Fullwood NJ, Quantock AJ, Kinoshita S. Growth factor mRNA and protein in preserved human amniotic membrane. Curr Eye Res. 2000 Mar;20(3):173–7. https://doi.org/10.1076/0271-3683(200003)2031-9FT173 PMID:10694891

Li J, Koike-Soko C, Sugimoto J, Yoshida T, Okabe M, Nikaido T. Human Amnion-Derived Stem Cells Have Immunosuppressive Properties on NK Cells and Monocytes. Cell Transplant. 2015;24(10):2065–76. https://doi.org/10.3727/096368914X685230 PMID:25333453

Li H, Niederkorn JY, Neelam S, Mayhew E, Word RA, McCulley JP, et al. Immunosuppressive factors secreted by human amniotic epithelial cells. Invest Ophthalmol Vis Sci. 2005 Mar;46(3):900–7. https://doi.org/10.1167/iovs.04-0495 PMID:15728546

Gicquel JJ, Dua HS, Brodie A, Mohammed I, Suleman H, Lazutina E, et al. Epidermal growth factor variations in amniotic membrane used for ex vivo tissue constructs. Tissue Eng Part A. 2009 Aug;15(8):1919–27. https://doi.org/10.1089/ten.tea.2008.0432 PMID:19196134

Koizumi N, Fullwood NJ, Bairaktaris G, Inatomi T, Kinoshita S, Quantock AJ. Cultivation of corneal epithelial cells on intact and denuded human amniotic membrane. Invest Ophthalmol Vis Sci. 2000 Aug;41(9):2506–13. PMID:10937561

Russo A, Bonci P, Bonci P. The effects of different preservation processes on the total protein and growth factor content in a new biological product developed from human amniotic membrane. Cell Tissue Bank. 2012 Jun;13(2):353–61. https://doi.org/10.1007/s10561-011-9261-5 PMID:21681392

Cirman T, Beltram M, Schollmayer P, Rožman P, Kreft ME. Amniotic membrane properties and current practice of amniotic membrane use in ophthalmology in Slovenia. Cell Tissue Bank. 2014 Jun;15(2):177–92. https://doi.org/10.1007/s10561-013-9417-6 PMID:24352631

Hao Y, Ma DH, Hwang DG, Kim WS, Zhang F. Identification of antiangiogenic and antiinflammatory proteins in human amniotic membrane. Cornea. 2000 May;19(3):348–52. https://doi.org/10.1097/00003226-200005000-00018 PMID:10832697

Fidel PL Jr, Romero R, Ramirez M, Cutright J, Edwin SS, LaMarche S, et al. Interleukin-1 receptor antagonist (IL-1ra) production by human amnion, chorion, and decidua. Am J Reprod Immunol. 1994 Aug;32(1):1–7. https://doi.org/10.1111/j.1600-0897.1994.tb00872.xPMID:7945810

Dragin U, Kreft ME. Amniotic membrane in tissue engineering and regenerative medicine. Zdravn vestn. 2010;79(10):8707–715.

Solomon A, Rosenblatt M, Monroy D, Ji Z, Pflugfelder SC, Tseng SC. Suppression of interleukin 1α and interleukin 1β in human limbal epithelial cells cultured on the amniotic membrane stromal matrix. Br J Ophthalmol. 2001 Apr;85(4):444–9. https://doi.org/10.1136/bjo.85.4.444 PMID:11264135

Heiligenhaus A, Bauer D, Meller D, Steuhl KP, Tseng SC. Improvement of HSV-1 necrotizing keratitis with amniotic membrane transplantation. Invest Ophthalmol Vis Sci. 2001 Aug;42(9):1969–74. PMID:11481259

Sippel KC, Ma JJ, Foster CS. Amniotic membrane surgery. Curr Opin Ophthalmol. 2001 Aug;12(4):269–81. https://doi.org/10.1097/00055735-200108000-00006 PMID:11507340

He H, Li W, Chen SY, Zhang S, Chen YT, Hayashida Y, et al. Suppression of activation and induction of apoptosis in RAW264.7 cells by amniotic membrane extract. Invest Ophthalmol Vis Sci. 2008;49(10):4468v75.

Kim HS, Cho JH, Park HW, Yoon H, Kim MS, Kim SC. Endotoxin-neutralizing antimicrobial proteins of the human placenta. J Immunol. 2002;168(5):2356v64.

Buhimschi IA, Jabr M, Buhimschi CS, Petkova AP, Weiner CP, Saed GM. The novel antimicrobial peptide beta3-defensin is produced by the amnion: a possible role of the fetal membranes in innate immunity of the amniotic cavity. Am J Obstet Gynecol. 2004 Nov;191(5):1678–87. https://doi.org/10.1016/j.ajog.2004.03.081 PMID:15547542

King AE, Paltoo A, Kelly RW, Sallenave JM, Bocking AD, Challis JR. Expression of natural antimicrobials by human placenta and fetal membranes. Placenta. 2007 Feb-Mar;28(2-3):161–9. https://doi.org/10.1016/j.placenta.2006.01.006 PMID:16513165

Ni J, Abrahamson M, Zhang M, Fernandez MA, Grubb A, Su J, et al. Cystatin E is a novel human cysteine proteinase inhibitor with structural resemblance to family 2 cystatins. J Biol Chem. 1997 Apr;272(16):10853–8. https://doi.org/10.1074/jbc.272.16.10853 PMID:9099741

Akle CA, Adinolfi M, Welsh KI, Leibowitz S, McColl I. Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet. 1981 Nov;2(8254):1003–5. https://doi.org/10.1016/S0140-6736(81)91212-5 PMID:6118474

Kubo M, Sonoda Y, Muramatsu R, Usui M. Immunogenicity of human amniotic membrane in experimental xenotransplantation. Invest Ophthalmol Vis Sci. 2001 Jun;42(7):1539–46. PMID:11381058

Hammer A, Hutter H, Blaschitz A, Mahnert W, Hartmann M, Uchanska-Ziegler B, et al. Amnion epithelial cells, in contrast to trophoblast cells, express all classical HLA class I molecules together with HLA-G. Am J Reprod Immunol. 1997 Feb;37(2):161–71. https://doi.org/10.1111/j.1600-0897.1997.tb00208.x PMID:9083612

Langer R, Vacanti J. Advances in tissue engineering. J Pediatr Surg. 2016 Jan;51(1):8–12. https://doi.org/10.1016/j.jpedsurg.2015.10.022 PMID:26711689

Mungadi IA. Bioengineering tissue for organ repair, regeneration, and renewal. J Surg Tech Case Rep. 2012 Jul;4(2):77–8. https://doi.org/10.4103/2006-8808.110247 PMID:23741579

Nakanishi Y, Chen G, Komuro H, Ushida T, Kaneko S, Tateishi T, et al. Tissue-engineered urinary bladder wall using PLGA mesh-collagen hybrid scaffolds: a comparison study of collagen sponge and gel as a scaffold. J Pediatr Surg. 2003 Dec;38(12):1781–4. https://doi.org/10.1016/j.jpedsurg.2003.08.034 PMID:14666467

Heidary Rouchi A, Mahdavi-Mazdeh M. Regenerative Medicine in Organ and Tissue Transplantation: Shortly and Practically Achievable? Int J Organ Transplant Med. 2015;6(3):93–8. PMID:26306154

Mano JF, Silva GA, Azevedo HS, Malafaya PB, Sousa RA, Silva SS, et al. Natural origin biodegradable systems in tissue engineering and regenerative medicine: present status and some moving trends. J R Soc Interface. 2007 Dec;4(17):999–1030. https://doi.org/10.1098/rsif.2007.0220 PMID:17412675

O’Brien FJ. Biomaterials and scaffolds for tissue engineering. Mater Today. 2011;14(3):88–95. https://doi.org/10.1016/S1369-7021(11)70058-X.

Vunjak-Novakovic G. The fundamentals of tissue engineering: scaffolds and bioreactors. Novartis Found Symp. 2003;249:34-46; discussion-51, 170-4, 239-41. https://doi.org/10.1002/0470867973.ch4.

Hsiao YC, Lee HW, Chen YT, Young TH, Yang TL. The impact of compositional topography of amniotic membrane scaffold on tissue morphogenesis of salivary gland. Biomaterials. 2011 Jul;32(19):4424–32. https://doi.org/10.1016/j.biomaterials.2011.02.057PMID:21439637

Feng Y, Borrelli M, Reichl S, Schrader S, Geerling G. Review of alternative carrier materials for ocular surface reconstruction. Curr Eye Res. 2014 Jun;39(6):541–52. https://doi.org/10.3109/02713683.2013.853803 PMID:24405104

Ramuta TZ, Kreft ME. Human Amniotic Membrane and Amniotic Membrane-Derived Cells: How Far Are We from Their Use in Regenerative and Reconstructive Urology? Cell Transplant. 2018 Jan;27(1):77–92. https://doi.org/10.1177/0963689717725528 PMID:29562770

Madhavan HN, Priya K, Malathi J, Joseph PR. Preparation of amniotic membrane for ocular surface reconstruction. Indian J Ophthalmol. 2002 Sep;50(3):227–31. PMID:12355703

Adds PJ, Hunt CJ, Dart JK. Amniotic membrane grafts, “fresh” or frozen? A clinical and in vitro comparison. Br J Ophthalmol. 2001 Aug;85(8):905–7. https://doi.org/10.1136/bjo.85.8.905 PMID:11466241

Adds PJ, Hunt C, Hartley S. Bacterial contamination of amniotic membrane. Br J Ophthalmol. 2001 Feb;85(2):228–30. https://doi.org/10.1136/bjo.85.2.228 PMID:11159493

Thomasen H, Pauklin M, Steuhl KP, Meller D. Comparison of cryopreserved and air-dried human amniotic membrane for ophthalmologic applications. Graefes Arch Clin Exp Ophthalmol. 2009 Dec;247(12):1691–700. https://doi.org/10.1007/s00417-009-1162-yPMID:19693529

Rahman I, Said DG, Maharajan VS, Dua HS. Amniotic membrane in ophthalmology: indications and limitations. Eye (Lond). 2009 Oct;23(10):1954–61. https://doi.org/10.1038/eye.2008.410 PMID:19169225

von Versen-Höynck F, Syring C, Bachmann S, Möller DE. The influence of different preservation and sterilisation steps on the histological properties of amnion allografts—light and scanning electron microscopic studies. Cell Tissue Bank. 2004;5(1):45–56. https://doi.org/10.1023/B:CATB.0000022276.47180.96 PMID:15256839

Hennerbichler S, Reichl B, Pleiner D, Gabriel C, Eibl J, Redl H. The influence of various storage conditions on cell viability in amniotic membrane. Cell Tissue Bank. 2007;8(1):1–8. https://doi.org/10.1007/s10561-006-9002-3 PMID:16807768

Ricci E, Vanosi G, Lindenmair A, Hennerbichler S, Peterbauer-Scherb A, Wolbank S, et al. Anti-fibrotic effects of fresh and cryopreserved human amniotic membrane in a rat liver fibrosis model. Cell Tissue Bank. 2013 Sep;14(3):475–88. https://doi.org/10.1007/s10561-012-9337-xPMID:22926336

Kruse FE, Joussen AM, Rohrschneider K, You L, Sinn B, Baumann J, et al. Cryopreserved human amniotic membrane for ocular surface reconstruction. Graefes Arch Clin Exp Ophthalmol. 2000 Jan;238(1):68–75. https://doi.org/10.1007/s004170050012 PMID:10664056

Wolbank S, Hildner F, Redl H, van Griensven M, Gabriel C, Hennerbichler S. Impact of human amniotic membrane preparation on release of angiogenic factors. J Tissue Eng Regen Med. 2009 Dec;3(8):651–4. https://doi.org/10.1002/term.207 PMID:19701933

Shortt AJ, Secker GA, Lomas RJ, Wilshaw SP, Kearney JN, Tuft SJ, et al. The effect of amniotic membrane preparation method on its ability to serve as a substrate for the ex-vivo expansion of limbal epithelial cells. Biomaterials. 2009 Feb;30(6):1056–65. https://doi.org/10.1016/j.biomaterials.2008.10.048 PMID:19019426

Niknejad H, Deihim T, Solati-Hashjin M, Peirovi H. The effects of preservation procedures on amniotic membrane’s ability to serve as a substrate for cultivation of endothelial cells. Cryobiology. 2011 Dec;63(3):145–51. https://doi.org/10.1016/j.cryobiol.2011.08.003PMID:21884690

Rodríguez-Ares MT, López-Valladares MJ, Touriño R, Vieites B, Gude F, Silva MT, et al. Effects of lyophilization on human amniotic membrane. Acta Ophthalmol. 2009 Jun;87(4):396–403. https://doi.org/10.1111/j.1755-3768.2008.01261.x PMID:18937812

Hopkinson A, Shanmuganathan VA, Gray T, Yeung AM, Lowe J, James DK, et al. Optimization of amniotic membrane (AM) denuding for tissue engineering. Tissue Eng Part C Methods. 2008 Dec;14(4):371–81. https://doi.org/10.1089/ten.tec.2008.0315 PMID:18821842

Jerman UD, Veranič P, Kreft ME. Amniotic membrane scaffolds enable the development of tissue-engineered urothelium with molecular and ultrastructural properties comparable to that of native urothelium. Tissue Eng Part C Methods. 2014 Apr;20(4):317–27. https://doi.org/10.1089/ten.tec.2013.0298 PMID:23947657

Chau DY, Brown SV, Mather ML, Hutter V, Tint NL, Dua HS, et al. Tissue transglutaminase (TG-2) modified amniotic membrane: a novel scaffold for biomedical applications. Biomed Mater. 2012 Aug;7(4):045011. https://doi.org/10.1088/1748-6041/7/4/045011 PMID:22652528

Adamowicz J, Pokrywczyńska M, Tworkiewicz J, Kowalczyk T, van Breda SV, Tyloch D, et al. New Amniotic Membrane Based Biocomposite for Future Application in Reconstructive Urology. PLoS One. 2016 Jan;11(1):e0146012. https://doi.org/10.1371/journal.pone.0146012PMID:26766636

Ma DH, Lai JY, Cheng HY, Tsai CC, Yeh LK. Carbodiimide cross-linked amniotic membranes for cultivation of limbal epithelial cells. Biomaterials. 2010 Sep;31(25):6647–58. https://doi.org/10.1016/j.biomaterials.2010.05.034 PMID:20541801

Lai JY, Wang PR, Luo LJ, Chen ST. Stabilization of collagen nanofibers with L-lysine improves the ability of carbodiimide cross-linked amniotic membranes to preserve limbal epithelial progenitor cells. Int J Nanomedicine. 2014 Nov;9:5117–30. https://doi.org/10.2147/IJN.S69689 PMID:25395849

Miki T, Lehmann T, Cai H, Stolz DB, Strom SC. Stem cell characteristics of amniotic epithelial cells. Stem Cells. 2005 Nov-Dec;23(10):1549–59. https://doi.org/10.1634/stemcells.2004-0357 PMID:16081662

Kang NH, Hwang KA, Kim SU, Kim YB, Hyun SH, Jeung EB, et al. Potential antitumor therapeutic strategies of human amniotic membrane and amniotic fluid-derived stem cells. Cancer Gene Ther. 2012 Aug;19(8):517–22. https://doi.org/10.1038/cgt.2012.30PMID:22653384

Simerman AA, Perone MJ, Gimeno ML, Dumesic DA, Chazenbalk GD. A mystery unraveled: nontumorigenic pluripotent stem cells in human adult tissues. Expert Opin Biol Ther. 2014 Jul;14(7):917–29. https://doi.org/10.1517/14712598.2014.900538 PMID:24745973

Parolini O, Soncini M, Evangelista M, Schmidt D. Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? Regen Med. 2009 Mar;4(2):275–91. https://doi.org/10.2217/17460751.4.2.275 PMID:19317646

Parolini O, Alviano F, Bagnara GP, Bilic G, Bühring HJ, Evangelista M, 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 Feb;26(2):300–11. https://doi.org/10.1634/stemcells.2007-0594 PMID:17975221

Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U. Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod. 2007 Sep;77(3):577–88. https://doi.org/10.1095/biolreprod.106.055244 PMID:17494917

Pianta S, Bonassi Signoroni P, Muradore I, Rodrigues MF, Rossi D, Silini A, et al. Amniotic membrane mesenchymal cells-derived factors skew T cell polarization toward Treg and downregulate Th1 and Th17 cells subsets. Stem Cell Rev. 2015 Jun;11(3):394–407. https://doi.org/10.1007/s12015-014-9558-4 PMID:25348066

Silini AR, Cargnoni A, Magatti M, Pianta S, Parolini O. The Long Path of Human Placenta, and Its Derivatives, in Regenerative Medicine. Front Bioeng Biotechnol. 2015 Oct;3:162. https://doi.org/10.3389/fbioe.2015.00162 PMID:26539433

Zaslavsky A, Baek KH, Lynch RC, Short S, Grillo J, Folkman J, et al. Platelet-derived thrombospondin-1 is a critical negative regulator and potential biomarker of angiogenesis. Blood. 2010 Jun;115(22):4605–13. https://doi.org/10.1182/blood-2009-09-242065PMID:20086246

Niknejad H, Paeini-Vayghan G, Tehrani FA, Khayat-Khoei M, Peirovi H. Side dependent effects of the human amnion on angiogenesis. Placenta. 2013 Apr;34(4):340–5. https://doi.org/10.1016/j.placenta.2013.02.001 PMID:23465536

De D, Kmiecik G, Cargnoni A, Parolini O. Placenta-Derived Cells and Their Therapeutic Applications. V: Templeton NS, ur. Gene and Cell Therapy. Združene države Amerike: CRC Press; 2015. p. 773–94.

Puangsricharern V, Tseng SC. Cytologic evidence of corneal diseases with limbal stem cell deficiency. Ophthalmology. 1995 Oct;102(10):1476–85. https://doi.org/10.1016/S0161-6420(95)30842-1 PMID:9097795

Bakhtiari P, Djalilian A. Update on limbal stem cell transplantation. Middle East Afr J Ophthalmol. 2010 Jan;17(1):9–14. PMID:20543931

Meller D, Pires RT, Tseng SC. Ex vivo preservation and expansion of human limbal epithelial stem cells on amniotic membrane cultures. Br J Ophthalmol. 2002 Apr;86(4):463–71. https://doi.org/10.1136/bjo.86.4.463 PMID:11914219

Li W, Hayashida Y, He H, Kuo CL, Tseng SC. The fate of limbal epithelial progenitor cells during explant culture on intact amniotic membrane. Invest Ophthalmol Vis Sci. 2007 Feb;48(2):605–13. https://doi.org/10.1167/iovs.06-0514 PMID:17251456

Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, De Luca M. Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet. 1997 Apr;349(9057):990–3. https://doi.org/10.1016/S0140-6736(96)11188-0 PMID:9100626

Grueterich M, Tseng SC. Human limbal progenitor cells expanded on intact amniotic membrane ex vivo. Arch Ophthalmol. 2002 Jun;120(6):783–90. https://doi.org/10.1001/archopht.120.6.783 PMID:12049584

Zakaria N, Koppen C, Van Tendeloo V, Berneman Z, Hopkinson A, Tassignon MJ. Standardized limbal epithelial stem cell graft generation and transplantation. Tissue Eng Part C Methods. 2010 Oct;16(5):921–7. https://doi.org/10.1089/ten.tec.2009.0634 PMID:19916804

Lužnik Z, Hawlina M, Maličev E, Bertolin M, Kopitar AN, Ihan A, et al. Effect of Cryopreserved Amniotic Membrane Orientation on the Expression of Limbal Mesenchymal and Epithelial Stem Cell Markers in Prolonged Limbal Explant Cultures. PLoS One. 2016 Oct;11(10):e0164408. https://doi.org/10.1371/journal.pone.0164408 PMID:27723792

Baylis O, Figueiredo F, Henein C, Lako M, Ahmad S. 13 years of cultured limbal epithelial cell therapy: a review of the outcomes. J Cell Biochem. 2011 Apr;112(4):993–1002. https://doi.org/10.1002/jcb.23028 PMID:21308743

Ahmad S, Osei-Bempong C, Dana R, Jurkunas U. The culture and transplantation of human limbal stem cells. J Cell Physiol. 2010 Oct;225(1):15–9. https://doi.org/10.1002/jcp.22251PMID:20506173

Koizumi N, Rigby H, Fullwood NJ, Kawasaki S, Tanioka H, Koizumi K, et al. Comparison of intact and denuded amniotic membrane as a substrate for cell-suspension culture of human limbal epithelial cells. Graefes Arch Clin Exp Ophthalmol. 2007 Jan;245(1):123–34. https://doi.org/10.1007/s00417-005-0095-3 PMID:16612639

Mikek K, Pfeifer V, Drnovšek-Olup B. Amniotic Membrane Transplantation in the Ocular Surgery. Zdrav Vestn. 2004;73:4.

Di Iorio E, Ferrari S, Fasolo A, Böhm E, Ponzin D, Barbaro V. Techniques for culture and assessment of limbal stem cell grafts. Ocul Surf. 2010 Jul;8(3):146–53. https://doi.org/10.1016/S1542-0124(12)70225-2 PMID:20712971

Burman S, Sangwan V. Cultivated limbal stem cell transplantation for ocular surface reconstruction. Clin Ophthalmol. 2008 Sep;2(3):489–502. PMID:19668747

Szabó DJ, Noer A, Nagymihály R, Josifovska N, Andjelic S, Veréb Z, et al. Long-Term Cultures of Human Cornea Limbal Explants Form 3D Structures Ex Vivo - Implications for Tissue Engineering and Clinical Applications. PLoS One. 2015 Nov;10(11):e0143053. https://doi.org/10.1371/journal.pone.0143053 PMID:26580800

Birder L, Andersson KE. Urothelial signaling. Physiol Rev. 2013 Apr;93(2):653–80. https://doi.org/10.1152/physrev.00030.2012 PMID:23589830

Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, et al. Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am J Physiol Renal Physiol. 2004 Aug;287(2):F305–18. https://doi.org/10.1152/ajprenal.00341.2003PMID:15068973

Hicks RM. The mammalian urinary bladder: an accommodating organ. Biol Rev Camb Philos Soc. 1975 May;50(2):215–46. https://doi.org/10.1111/j.1469-185X.1975.tb01057.xPMID:1100129

Paner GP, Ro JY, Wojcik EM, Venkataraman G, Datta MW, Amin MB. Further characterization of the muscle layers and lamina propria of the urinary bladder by systematic histologic mapping: implications for pathologic staging of invasive urothelial carcinoma. Am J Surg Pathol. 2007 Sep;31(9):1420–9. https://doi.org/10.1097/PAS.0b013e3180588283PMID:17721199

Romih R, Korošec P, de Mello W Jr, Jezernik K. Differentiation of epithelial cells in the urinary tract. Cell Tissue Res. 2005 May;320(2):259–68. https://doi.org/10.1007/s00441-004-1005-4 PMID:15778856

Mahfouz W, Elsalmy S, Corcos J, Fayed AS. Fundamentals of bladder tissue engineering. Afr J Urol. 2013;19(2):51–7. https://doi.org/10.1016/j.afju.2013.01.006.

El-Taji OM, Khattak AQ, Hussain SA. Bladder reconstruction: the past, present and future. Oncol Lett. 2015 Jul;10(1):3–10. https://doi.org/10.3892/ol.2015.3161 PMID:26170968

Onkološki inštitut Ljubljana. Rak sečnega mehurja, ledvičnega meha in sečevoda. Onkološki inštitut; 2016 [cited 2017 Dec 2]. Available from: https://www.onko-i.si/za_javnost_in_bolnike/vrste_raka/urogenitalni_raki/#c23082016

Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006 Apr;367(9518):1241–6. https://doi.org/10.1016/S0140-6736(06)68438-9 PMID:16631879

Rožman P, Semenič D, Smrke DM. The Role of Platelet Gel in Regenerative Medicine. V: Wislet-Gendebien S, ed. Advances in Regenerative Medicine: InTech. 2011. 105.

Park JE, Barbul A. Understanding the role of immune regulation in wound healing. Am J Surg. 2004 May;187(5 5A):11S–6S. https://doi.org/10.1016/S0002-9610(03)00296-4PMID:15147986

Koob TJ, Rennert R, Zabek N, Massee M, Lim JJ, Temenoff JS, et al. Biological properties of dehydrated human amnion/chorion composite graft: implications for chronic wound healing. Int Wound J. 2013 Oct;10(5):493–500. https://doi.org/10.1111/iwj.12140 PMID:23902526

Uçakhan OO, Köklü G, Firat E. Nonpreserved human amniotic membrane transplantation in acute and chronic chemical eye injuries. Cornea. 2002 Mar;21(2):169–72. https://doi.org/10.1097/00003226-200203000-00008 PMID:11862088

Mejía LF, Acosta C, Santamaría JP. Use of nonpreserved human amniotic membrane for the reconstruction of the ocular surface. Cornea. 2000 May;19(3):288–91. https://doi.org/10.1097/00003226-200005000-00006 PMID:10832685

Forbes J, Fetterolf DE. Dehydrated amniotic membrane allografts for the treatment of chronic wounds: a case series. J Wound Care. 2012 Jun;21(6):290–6. https://doi.org/10.12968/jowc.2012.21.6.290 PMID:22886294

Sheikh ES, Sheikh ES, Fetterolf DE. Use of dehydrated human amniotic membrane allografts to promote healing in patients with refractory non healing wounds. Int Wound J. 2014 Dec;11(6):711–7. https://doi.org/10.1111/iwj.12035 PMID:23409746

Zelen CM, Serena TE, Denoziere G, Fetterolf DE. A prospective randomised comparative parallel study of amniotic membrane wound graft in the management of diabetic foot ulcers. Int Wound J. 2013 Oct;10(5):502–7. https://doi.org/10.1111/iwj.12097 PMID:23742102

Zelen CM. An evaluation of dehydrated human amniotic membrane allografts in patients with DFUs. J Wound Care. 2013;22(7):347-8, 50–1.

Zelen CM, Serena TE, Snyder RJ. A prospective, randomised comparative study of weekly versus biweekly application of dehydrated human amnion/chorion membrane allograft in the management of diabetic foot ulcers. Int Wound J. 2014 Apr;11(2):122–8. https://doi.org/10.1111/iwj.12242 PMID:24618401

Ciringer M, Frangež I, Smrke D. Najnovejša metoda zdravljenja ran z alograftom amnijske membrane. In: Smrke D, Nikolič J, ur. Sodobni pristopi za učinkovito zdravljenje okuženih kirurških in kroničnih ran; 2014 Apr 24-25; Portorož, Slovenija. Klinični oddelek za kirurške okužbe, Kirurška klinika, Univerzitetni klinični center; 2014. p. 48-51.

Frangež I, Smrke D. Amniotic membrane allograft, new technology in chronic wound treatment. Wound management. Sarajevo: Doktor Magazin; 2014. p. 23.

Willett NJ, Thote T, Lin AS, Moran S, Raji Y, Sridaran S, et al. Intra-articular injection of micronized dehydrated human amnion/chorion membrane attenuates osteoarthritis development. Arthritis Res Ther. 2014 Feb;16(1):R47. https://doi.org/10.1186/ar4476PMID:24499554

Patel VR, Samavedi S, Bates AS, Kumar A, Coelho R, Rocco B, et al. Dehydrated Human Amnion/Chorion Membrane Allograft Nerve Wrap Around the Prostatic Neurovascular Bundle Accelerates Early Return to Continence and Potency Following Robot-assisted Radical Prostatectomy: Propensity Score-matched Analysis. Eur Urol. 2015 Jun;67(6):977–80. https://doi.org/10.1016/j.eururo.2015.01.012 PMID:25613153

Lužnik Z. Vzgoja in opredelitev človeških limbalnih epitelijskih matičnih celic (PhD Thesis). Ljubljana: Z. Lužnik; 2017.

Grueterich M, Espana EM, Tseng SC. Ex vivo expansion of limbal epithelial stem cells: amniotic membrane serving as a stem cell niche. Surv Ophthalmol. 2003 Nov-Dec;48(6):631–46. https://doi.org/10.1016/j.survophthal.2003.08.003 PMID:14609709

Shortt AJ, Secker GA, Notara MD, Limb GA, Khaw PT, Tuft SJ, et al. Transplantation of ex vivo cultured limbal epithelial stem cells: a review of techniques and clinical results. Surv Ophthalmol. 2007 Sep-Oct;52(5):483–502. https://doi.org/10.1016/j.survophthal.2007.06.013PMID:17719371

Tsai RJ, Li L, Chen J. Reconstruction of damaged corneas by transplantation of autologous limbal epithelial cells(1). Am J Ophthalmol. 2000 Oct;130(4):543. https://doi.org/10.1016/S0002-9394(00)00746-7 PMID:11024443

Sharma S, Tandon R, Mohanty S, Sharma N, M V, Sen S, et al. Culture of corneal limbal epithelial stem cells: experience from benchtop to bedside in a tertiary care hospital in India. Cornea. 2011 Nov;30(11):1223–32. https://doi.org/10.1097/ICO.0b013e3181dc81f1PMID:21808195

Mariappan I, Maddileti S, Savy S, Tiwari S, Gaddipati S, Fatima A, et al. In vitro culture and expansion of human limbal epithelial cells. Nat Protoc. 2010 Aug;5(8):1470–9. https://doi.org/10.1038/nprot.2010.115 PMID:20671730

Ang LP, Tanioka H, Kawasaki S, Ang LP, Yamasaki K, Do TP, et al. Cultivated human conjunctival epithelial transplantation for total limbal stem cell deficiency. Invest Ophthalmol Vis Sci. 2010 Feb;51(2):758–64. https://doi.org/10.1167/iovs.09-3379 PMID:19643956

Pathak M, Olstad OK, Drolsum L, Moe MC, Smorodinova N, Kalasova S, et al. The effect of culture medium and carrier on explant culture of human limbal epithelium: A comparison of ultrastructure, keratin profile and gene expression. Exp Eye Res. 2016 Dec;153:122–32. https://doi.org/10.1016/j.exer.2016.09.012 PMID:27702552

Zakaria N, Possemiers T, Dhubhghaill SN, Leysen I, Rozema J, Koppen C, et al. Results of a phase I/II clinical trial: standardized, non-xenogenic, cultivated limbal stem cell transplantation. J Transl Med. 2014 Mar;12(1):58. https://doi.org/10.1186/1479-5876-12-58PMID:24589151

Vazirani J, Basu S, Kenia H, Ali MH, Kacham S, Mariappan I, et al. Unilateral partial limbal stem cell deficiency: contralateral versus ipsilateral autologous cultivated limbal epithelial transplantation. Am J Ophthalmol. 2014;157(3):584-90.e1–2. https://doi.org/10.1016/j.ajo.2013.11.011.

Krishnamurithy G, Shilpa PN, Ahmad RE, Sulaiman S, Ng CL, Kamarul T. Human amniotic membrane as a chondrocyte carrier vehicle/substrate: in vitro study. J Biomed Mater Res A. 2011 Dec;99(3):500–6. https://doi.org/10.1002/jbm.a.33184 PMID:21913317

Díaz-Prado S, Rendal-Vázquez ME, Muiños-López E, Hermida-Gómez T, Rodríguez-Cabarcos M, Fuentes-Boquete I, et al. Potential use of the human amniotic membrane as a scaffold in human articular cartilage repair. Cell Tissue Bank. 2010 May;11(2):183–95. https://doi.org/10.1007/s10561-009-9144-1 PMID:20386989

Jin CZ, Park SR, Choi BH, Lee KY, Kang CK, Min BH. Human amniotic membrane as a delivery matrix for articular cartilage repair. Tissue Eng. 2007 Apr;13(4):693–702. https://doi.org/10.1089/ten.2006.0184 PMID:17269856

Mahmoudi-Rad M, Abolhasani E, Moravvej H, Mahmoudi-Rad N, Mirdamadi Y. Acellular amniotic membrane: an appropriate scaffold for fibroblast proliferation. Clin Exp Dermatol. 2013 Aug;38(6):646–51. https://doi.org/10.1111/ced.12087 PMID:23837938

Huang G, Ji S, Luo P, Liu H, Zhu S, Wang G, et al. Accelerated expansion of epidermal keratinocyte and improved dermal reconstruction achieved by engineered amniotic membrane. Cell Transplant. 2013;22(10):1831–44. https://doi.org/10.3727/096368912X657945PMID:23067579

Redondo P, Giménez de Azcarate A, Marqués L, García-Guzman M, Andreu E, Prósper F. Amniotic membrane as a scaffold for melanocyte transplantation in patients with stable vitiligo. Dermatol Res Pract. 2011;2011:532139. https://doi.org/10.1155/2011/532139 PMID:21869882

Sharifiaghdas F, Hamzehiesfahani N, Moghadasali R, Ghaemimanesh F, Baharvand H. Human amniotic membrane as a suitable matrix for growth of mouse urothelial cells in comparison with human peritoneal and omentum membranes. Urol J. 2007;4(2):71–8. PMID:17701925

Wilshaw SP, Kearney J, Fisher J, Ingham E. Biocompatibility and potential of acellular human amniotic membrane to support the attachment and proliferation of allogeneic cells. Tissue Eng Part A. 2008 Apr;14(4):463–72. https://doi.org/10.1089/tea.2007.0145PMID:18370928

Gholipourmalekabadi M, Sameni M, Radenkovic D, Mozafari M, Mossahebi-Mohammadi M, Seifalian A. Decellularized human amniotic membrane: how viable is it as a delivery system for human adipose tissue-derived stromal cells? Cell Prolif. 2016 Feb;49(1):115–21. https://doi.org/10.1111/cpr.12240 PMID:26840647

Chehelcheraghi F, Eimani H, Homayoonsadraie S, Torkaman G, Amini A, Alavi Majd H, et al. Effects of Acellular Amniotic Membrane Matrix and Bone Marrow-Derived Mesenchymal Stem Cells in Improving Random Skin Flap Survival in Rats. Iran Red Crescent Med J. 2016 Jun;18(6):e25588. https://doi.org/10.5812/ircmj.25588 PMID:27621924

Tan SL, Sulaiman S, Pingguan-Murphy B, Selvaratnam L, Tai CC, Kamarul T. Human amnion as a novel cell delivery vehicle for chondrogenic mesenchymal stem cells. Cell Tissue Bank. 2011 Feb;12(1):59–70. https://doi.org/10.1007/s10561-009-9164-x PMID:19953328

Dobrowolski D, Orzechowska-Wylegala B, Wowra B, Wroblewska-Czajka E, Grolik M, Szczubialka K, et al. Cultivated Oral Mucosa Epithelium in Ocular Surface Reconstruction in Aniridia Patients. BioMed Res Int. 2015;2015:281870. https://doi.org/10.1155/2015/281870PMID:26451366

Amemiya T, Nakamura T, Yamamoto T, Kinoshita S, Kanamura N. Autologous transplantation of oral mucosal epithelial cell sheets cultured on an amniotic membrane substrate for intraoral mucosal defects. PLoS One. 2015 Apr;10(4):e0125391. https://doi.org/10.1371/journal.pone.0125391 PMID:25915046

Tiwari S, Ali MJ, Balla MM, Naik MN, Honavar SG, Reddy VA, et al. Establishing human lacrimal gland cultures with secretory function. PLoS One. 2012;7(1):e29458. https://doi.org/10.1371/journal.pone.0029458 PMID:22253725

Schrader S, Wedel T, Kremling C, Laqua H, Geerling G. Amniotic membrane as a carrier for lacrimal gland acinar cells. Graefes Arch Clin Exp Ophthalmol. 2007 Nov;245(11):1699–704. https://doi.org/10.1007/s00417-007-0612-7 PMID:17562065

Sanluis-Verdes A, Sanluis-Verdes N, Manso-Revilla MJ, Castro-Castro AM, Pombo-Otero J, Fraga-Mariño M, et al. Tissue engineering for neurodegenerative diseases using human amniotic membrane and umbilical cord. Cell Tissue Bank. 2017 Mar;18(1):1–15. https://doi.org/10.1007/s10561-016-9595-0 PMID:27830445

Mayer WJ, Grüterich M, Kook D, Sigg W, Kernt M, Messmer EM, et al. Modification of amniotic membrane as a depot carrier for bevacizumab - an in-vitro model for a slow release mechanism. Curr Eye Res. 2013 Apr;38(4):445–50. https://doi.org/10.3109/02713683.2012.757326 PMID:23405870

Published
2019-01-20
How to Cite
1.
Cirman T, Železnik Ramuta T, Lužnik Z, Hawlina M, Schollmayer P, Smrke D, Kreft M. The amniotic membrane as a biological scaffold, its preparation and use in regenerative medicine in Slovenia. TEST ZdravVestn [Internet]. 20Jan.2019 [cited 29Mar.2024];87(11-12):530–546. Available from: http://vestnik-dev.szd.si/index.php/ZdravVest/article/view/2684