J. Biomedical Science and Engineering, 2013, 6, 1178-1185 JBiSE http://dx.doi.org/10.4236/jbise.2013.612147 Published Online December 2013 (http://www.scirp.org/journal/jbise/) Amniotic membrane as a potent source of stem cells and a matrix for engineering heart tissue* Julio Cesar Francisco1,2#, Ricardo Correa Cunha2, Rossana Baggio Simeoni3, Luiz Cesar Guarita-Souza3, Reginaldo Justino Ferreira1,4#, Ana Carolina Irioda2, Carolina Maria C. Oliveira Souza2, Garikipati Venkata Naga Srikanth5, Soniya Nityanand5, Juan Carlos Chachques6, Katherine Athayde Teixeira de Carvalho1,2† 1Bioprocess Engineering and Biotechnology Department, Federal University of Paraná, Curitiba, Brazil 2Cell Therapy and Biotechnology in Regenerative Medicine Research Group, Pelé Pequeno Príncipe Institute, Curitiba, Brazil 3Experimental Laboratory of Institute of Biological and Health Sciences, Pontificial Catholic University of Paraná (PUCPR), Rua Imaculada Conceição, Curitiba, Brazil 4Federal University of Technology, Curitiba, Brazil 5Department of Hematology, Stem Cell Research Faculty, Sanjay Gandhi Post-Graduate Institute of Medical Sciences, Lucknow, India 6Laboratory of Biosurgical Research, Pompidou Hospital, University of Paris Descartes, Paris, France Email: †katherinecarv@gmail.com Received 28 September 2013; revised 1 November 2013; accepted 19 November 2013 Copyright © 2013 Julio Cesar Francisco et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In accordance of the Creative Commons Attribution License all Copyrights © 2013 are reserved for SCIRP and the owner of the intellectual property Julio Cesar Francisco et al. All Copyright © 2013 are guarded by law and by SCIRP as a guardian. ABSTRACT Existing therapies for the treatment of chronic heart failure still have some limitations and there is a pressing need for the development of new therapeutic modalities. The amniotic membrane has been used for the treatment of various diseases, such as con- junctive defects; however, the mechanisms behind its repair functions are still unclear. Regenerative medi- cine is seeking newer alternatives and among them, biomaterials have emerged in recent years for devel- oping and manipulating molecules, cells, tissues or organs grown in laboratories in order to replace hu- man body part s. Many such ma terials have b een used for this purpose, either synthetically or biologically, in order to provide new medical devices. This review provides a wider view of the regeneration potential of the use of amniotic membrane as a potential biomate- rial to facilitate the implementation of new research in surgical procedures. Amniotic membrane appears to be an alternative source of stem cells as well as an excellent biomaterial for cell-based therapeutic ap- plications in engineering heart tissue. Keywords: Amniotic Membrane; Heart; Tissue; Engineering; Stem Cells 1. INTRODUCTION The therapeutic options which are currently available for the treatment of some chronic cardiovascular diseases are still limited and palliative, highlighting the need for the development of new therapeutic modalities. Recent ex- perimental studies have shown great potential, indicating the possibility of myocardial regeneration by the trans- plantation of biomaterials, and this has emerged as an alternative to existing therapies for heart injuries [1]. Amniotic membrane (AM) and amniotic fluid (AF) have attracted increasing attention in recent years as a possible reservoir for stem cells and also as promising sources of stem or progenitor cells that could be useful in clinical application in regenerative medicine [2,3]. Roubelakis et al. (2012) emphasised that AF and AM stem cells have the immunophenotypic characteristics of both adult mesenchymal stem cells and also embryonic stem cells. Consequently, these cells have been difficult to identify as they do not have markers and phenotypes. Roubelakis et al. (2012) proposed the use of a novel ap- proach to identify them, based on transcriptomic, pro- teomic, or secretome analyses [4]. Dobreva et al. (2012) *Potential conflict of Interests: The authors declare that there are no conflicts of interest. Sources of funding: This study had no external sources of funding. #Post-graduate students of the Bioprocess Engineering and Biotechnol- ogy Department, Federal University of Paraná, Curitiba, Paraná, Brazil. †Corresponding author. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 1179 studied mice, and suggested the use of periostin as a biomarker of AM [5]. AM has been routinely used in several clinical studies for the treatment of burns on the skin, ulcers and, pre- dominantly in ophthalmology, for the treatment of eye- piece surface disorders. Its use is based on its ability to improve the process of epithelisation, as well as reducing the inflammatory processes, angiogenesis and scarring alopecia [3,6,7]. Tissue-engineered technology provides the possibility of the enhanced recovery of injured tissues and organs. In general, this technology involves the selection of an appropriate substrate cultivation to sustain and promote the growth of a particular injured tissue. Three-dimen- sional substrates can be prepared, depending on the tis- sue in question. Several types of scaffolds are used: syn- thetic polymers that are not degradable; degradable syn- thetic polymers; collagen gel, without pores; non-human collagen gel, with human collagen tissue pores, and de- cellularised (cadaverous) [8]. In summary, none of the above-mentioned materials is entirely satisfactory in all respects, i.e. none are immu- nogenic, antitumoral, resistance and low cost. For this reason it is necessary to enhance a material for its use as a substrate for tissue engineering. The implant composed of a collagen matrix seeded with cells, has demonstrated benefits in cardiac tissue, especially when compared to implants using isolated cells, without matrix. These benefits are extended when they are combined with other components of the ex- tracellular matrix, such as growth factors. The amniotic fluid matrix has advantages because it has a surface area for cell cultivation with porosity, capillary growth, sta- bility for mechanical support, biodegradability, and low immunogenicity [9-13]. Many materials have been used for this purpose, whether biological or synthetic, with the aim of produc- ing new medical biomaterials. The purpose of this review is to provide a broader view of the basic biology of am- niotic membrane and its potential for use in cardiac re- generation. 2. AMNIOTIC MEMBRANE Human AM has been used as a biomaterial for surgical reconstruction for almost 100 years. There has been in- creasing interest in studying the biology of AM because it could eventually aid in the treatment of many ailments and improve the quality of human life. Thus, AM exhib- its tremendous potential for therapeutic purposes due to its absorption, high biocompatibility, regenerative capac- ity and ease of implementation. It is easily accessible and is without ethical concerns [14]. The use of amniotic membrane originated at the be- ginning of the twentieth century, when, in 1910, Davis used it as surgical material for skin transplantation and subsequently for treating small skin defects in human patients [15]. In 1940, Roth described the transplantation of amniotic membrane for the first time in the repair of siblefaro and conjunctival defects [16]. In 1946, Sorby and Symons reported good results from the use of AM in the treatment of acute chemical burns, as well in other areas of medicine such as in the development of surgical dressings; the reconstruction of the oral cavity, bladder, tympanoplasty, arthroplasty and onfalocele; and pre- venting tissue adhesion in surgery of the head, abdomen, pelvis, vagina and larynx [6-12,16,17]. The aforemen- tioned authors introduced the use of AM in ophthalmic surgery in experimental model and described the ability of AM to enhance wound healing, and epithelisation, noting an increase in the use of AM as a biomaterial in surgeries in recent decades. Similar data were submitted by other authors over the following years (Table 1) [15, 18-25]. 3. BASIC STRUCTURE The fetal membrane is composed of two main layers: the chorion, which is the outer layer of the placental mem- Table 1. Amniotic membrane as a potential biomaterial for various organs and tissues. Studies in humans and animals. Reference Treatment of AM Species Organs/tissues Davis (1910) [15] Fresh Human Skin Tseng et al. (1998) [18] Cryopreserved Human Eyes Azuara-Blanco et al. (1999) [19] Cryopreserved Human Eyes Chen et al. (2000) [20] Cryopreserved Human Eyes Mligiliche et al. (2002) [21] Decellularised matrix Rat Peripheral nerve Tamagawa et al. (2004) [22] Fresh amniotic cells Mouse Hepatocyte Lo et al. (2007) [23] Fresh decellularised matrix Rabbit Skin Zao et al. (2005) [24] Amniotic Cells Rat Heart Tsujhi et al. (2010) [25] Amniotic Cells Rat Heart Copyright © 2013 SciRes. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 1180 brane which comes into contact with the maternal cells, and the AM, the innermost layer, which has intimate contact with the fetus, separated from it only by amniotic fluid. In the human species, AM appears 7 to 8 days after conception. Its thickness ranges from 0.02 mm to 0.5 mm and it has not direct blood supply or vascularisation [26]. Human AM, or amnion, is a translucent membrane composed of a layer of simple epithelium cells firmly adhered to the innermost layer, called the mesenchymal layer, which is composed of three layers: compact, spongy and fibroblastic. These layers contain large amounts of collagen (type IV and V) laminin and a thick basal layer as an array, without vascularity. Externally, the amnion is located in the chorion, comprising a con- nective tissue that presents fetal vessels (chorioallantoic) (Figure 1) [19]. Amniotic cells have numerous microvilli on their api- cal and ventral faces, extending their cellular processes to the basal membrane, and are known as podocytes. These cellular junctions are processes of adhesion to the basal membrane, of the hemidesmosome type with all their tonofilaments, and are located beneath the basal membrane, being material that is partially amorphous and microfibilar [27]. The basement membrane thickness in human tissue consists of type III, IV, VII collagen, elastin, fibronectin, perlecan and several other integrin complexes. The base- ment membrane is known for its healing, neovascularisa- tion and anti-fibrosis properties [1,28]. Many pinocytic vesicles are found in the cytoplasm of cells from the AM, with, organelles in abundance, in- cluding nonlipid reticulum and Golgi apparatus. The cell cores have an irregular configuration and indents in the nuclear membrane, with large and homogeneous nucleoli, suggesting nucleolar activity. The ultra-structure of the amniotic membrane epithelium has specialised roles, such as the epithelium lining and as epithelial secretory with intense intercellular transport and trans-cellular ac- tivities. AM could be used to reduce inflammation in scars, enhancing the healing of wounds, and to serve as a substrate for proliferation and differentiation [29,30]. 4. BIOLOGICAL PROPERTIES Amniotic membrane has several biological properties; it reduces bacterial count and promotes the healing of in- fected wounds. This membrane is part of an important group of β-defensin antimicrobial peptides that are ex- pressed in mucosal surfaces by epithelial cells and leu- kocytes, which are part of the innate immune system [31]. Its antibacterial property is attributed to its ability to ad- here to the surface of wounds, to protect injuries and to reduce pain [32]. The innate immune system has evolved to eliminate microorganisms from entry in the tissues, oute Epithelium Basement membrane Layer Fibroblastic layer Sponge layer inne Figure 1. Histological scheme of human amniotic membrane showing its five layers. creating antigens that are needed to produce an adaptive immune response. The absence of leucocytes in the am- nion allows the use of the halo-transplant procedure, which does not induce rejection. The amniotic membrane stroma has several proteases that can inhibit the invasion of inflammatory cells, which might cause the rapid proc- ess of apoptosis [6]. Studies have shown the antimicrobial properties of anmiotic membrane and amniotic fluid in the healing process. The antimicrobial effect of amnion and chorion has been demonstrated against large numbers of bacte- rium, including Streptococcus Group A, Staphylococci aureus, Escherichia coli and Pseudomonas aeruginosa [33]. Since 1960, there have been many reports demon- strating biological membranes as an implant material. Other studies have reported that biological membranes are organic in nature, inert, and composed almost exclu- sively of collagen, showing low antigenicity [34]. When amniotic membrane is preserved, it is regarded as an inert tissue with non-viable cells. The ability of this membrane to repair tissues occurs through the presence of growth factors and cytokines [33]. Other studies using AM have revealed the presence of various growth factors in the membrane epithelium, such as epidermal growth factor (EGF); transforming growth factor-β1 (TGF-β1); keratinocyte growth factor (KGF); fibroblastic growth factor (β-FGF); and hepatocyte growth factor (HGF), which act in facilitating cellular migration [35]. Bigbie et al. (1991) demonstrated the role of AM in the removal of granulation tissue and in promoting the decrease of exudation in wounds when they were treated with this membrane. According to Solomon et al. (2001), AM suppresses the expression of cellular epitopes as IL-1 α and IL-1 β cytocines. Another unique property of amniotic membrane is that it does not induce immune Copyright © 2013 SciRes. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 1181 rejection after transplantation because it does not express the histocompatibility antigens HLA-A, B, or DR, which makes it an excellent option for grafting [35-38]. Hao et al. (2000) reported that AM secretes some an- giogenic factors, such as vascular endothelial growth factor (VEGF); interleukin-8 (IL-8); angiogenin; inter- feron-γ; interleukin-6 (IL-6); basic fibroblast growth factor (bFGF); epidermal growth factor (EGF) and platelet-derived growth factor (PDGF) [21,22]. It has also been demonstrated that some anti-angiogenic factors are released, such as IL-1 receptor antagonist, TIMP3 and TIMP4 [23]. Based on these data, AM can posses angiogenic and anti-angiogenic properties [38]. Perlecan induces high affinity binding of fibroblast growth factor (FGF)-2 to heparansulfate deficient cells or to soluble FGF receptors; it also possesses angiogenic properties [28]. Regarding the issue of low immunogenicity, clinical signs of acute infection and rejection were not observed when amniotic membrane was transplanted in volunteers [10]. The expression of MHC Class I antigens in AM is still controversial. Although it has been reported that HLA-A, B, C and DR was detected in amniotic epithelial cell culture, the detection of Class 1 antigens in nearly all cells from the amniotic membrane has been subsequently reported [10]. In addition, from the observation that am- niotics cells disappeared without signs of reaction or rejection, it has been speculated that the short existence of these cells on the eyepiece surface may be related to the process of apoptosis [10,11]. There are reports in the literature of the several factors that are involved in the antifibrotic effect of amniotic membrane. Fibroblasts are responsible for the process of healing in wounds enabled by the transforming growth factor-β (TGF-β); the amniotic membrane has a regula- tory mechanism of TGF-β and therefore reduces fibrosis [39,40]. Akle (1981) and Tamagawa (2004) reported that there was no evidence of tumorigenicity tests when they were isolated from amniotic membrane cells and transplanted in human volunteers to analyse immunogenicity [10,22]. Azuara-Blanco et al. (1999) and Dual et al. (2004) reported that amniotic membrane must be collected from a healthy donor who shows no signs of any type of infec- tion, and through caesarean section, where its processing must be performed under sterile conditions [19,26]. Amniotic membrane contains two different types of cells: amnion epithelial cells (AECs) and amnion mes- enchymal stromal cells (AMSCs). Human AECs (hAECs) are positive for the epithelial markers, cytokeratin 1, 2, 3, 4, 5, 6, 7, 8, 10, 13, 14, 15, 16 and 19 [40]. hAECs ex- press embryonic stem cell markers, such as OCT-4, Nanog, Sox-2, Rex-1, SSEA3, SSEA4, TRA-1-60 and TRA-1-81, and other antigens such as ABCG2/BCRP (a member of the ATP-binding cassette super family), CD9, CD24, E-Cadherin, Integrin a6 and b and c-met (receptor growth factor of the hepatocyte) [41-45]. AMSCs express classical MSC markers (CD90, CD44, CD73, CD166, CD105 and CD29), as described for bone marrow stromal cells with the absence of hematopoietic markers (CD34 and CD45) and the concomitant lack of monocyte (CD114), macrophage (CD11) and fibroblast markers. Human AMSCs (hAMSCs) also express low levels of HLA-ABC but they do not express HLA-DR. AMSCs are also positive for the pluripotency markers Oct-4 and Nanog [43-49]. 5. MECHANICAL PROPERTIES Amniotic membrane has great mechanical strength, which makes it an attractive biomaterial to be used in surgery. This membrane is capable of supporting the load of the pressure of amniotic fluid and repetitive smaller loads, such as Braxton Hicks contractions during preg- nancy. In most cases, AM is able to withstand loads equal or close to physiological levels, soon after a transplant, in order to ensure its resistance. In addition, mechanical signals can be important mediators of differentiation for some progenitor cells; AM creates a suitable environ- ment in the location of new transplanted tissue and it can increase the strength of the graft, with high levels of ri- gidity to resist the stress induced during tissue growth [23,41]. Other biomechanical properties of the amniotic fluid matrix, such as elasticity, rigidity and viscoelasticity, depend on the type of proteoglycans, collagen and elastin, which are important properties, the lack of which can promote intima layer hyperplasia and occlusion of the arteries [42]. 6. IN VITRO CARDIOGENIC DIFFERENTIATION The cardiogenic differentiation of human amniotic epithelial cells (hAECs) was first demonstrated by Miki et al. (2005). The RT-PCR of the cardiac-specific genes, atrial and ventricular myosin light chain 2 (MLC-2A and MLC-2V), and the transcription factors GATA-4 and Nkx 2.5 were expressed in hAECs that were cultured in media supplemented with ascorbic acid for 14 days. Dif- ferentiated cardiomyocytes have also expressed α-actinin, which has been demonstrated by immunocytochemistry [50]. Ilancheran et al. (2007) showed that freshly isolated native hAECs, and those grown under standard condi- tions, also expressed the mRNAs of genes that are im- portant for the specification of the cardiomyoctyic line- age, such as GATA4, and function, including ANP, Copyright © 2013 SciRes. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 1182 MYL7, CACNA1C, and KCND3. However, ultrastruc- tural analysis analysis has revealed that features consis- tent with relatively mature cardiomyocytes, such as myo- filaments, myofibrils, H bands and T tubules, were pre- sent only in differentiated cells [42]. The myogenic differentiation of hAMSCs has been determined by RT-PCR since Portmann-Lanz et al. (2006) demonstrated the mRNA expression of myogenic transcription factors such as myoD and myogenin, and the protein expression of desmin in hAMSCs after induc- tion with differentiation media [51]. Fetal maternal stem cell transfer appears to be a criti- cal mechanism in the maternal response to cardiac injury. Furthermore, caudal-related homeobox2 (Cdx2) cells have been identified as a novel cell type for potential use in cardiovascular regenerative therapy [52]. The use of amniotic membrane as a source for cardiac regeneration offers excellent advantages in that it is in plentiful supply and it can be applied immediately, with- out the need for any cell isolation, which makes it eco- nomical. In addition, amniotic membrane has good pre- servability and is immunologically tolerated in alloge- neic conditions; it has shown cardiogenic differentiation in vitro and in vivo. 7. PREPARATION AND PRESERVATION Kim and Tseng, in 1995 and 1998, proposed a method for the preparation and preservation of amniotic mem- brane, consisting of collecting the placenta through cae- sarean section in an environment free from contamina- tion, removing clots through rinsing with saline solution, separating the chorion amnion manually, and inserting it into nitrocelullose with the epithelial surface upwards. In most studies, the preservation of the membrane follows the protocol in which the membrane is prepared with antibiotics and antifungals and kept in medium contain- ing antibiotics and glycerol at −80˚C [7]. There are reports in the literature about other methods of preservation and storage of amniotic membrane, in- cluding freeze-drying, dry air, treatment with glutaral- dehyde, dispase, gamma irradiation [53]. Dual et al. (2004) and Mejia et al. (2002) reported that both pre- served and non-preserved amniotic membrane can be stored. Dimethyl sulfoxide (DMSO) has been used as an alternative to the preservation of amniotic membrane by replacing the rinsing with saline and antibiotics; Azuara- Blanco et al. (1999) used DMSO to 4, 8 and 10, while Kubo et al. (2001) used the same product to 0.5, 1.0 and 1.5 M for the washing membrane. After such treatment, it may be stored in 1.5 M DMSO to −80˚C for several months [11,19,26,54]. Trehalose is a reductor disaccharide, which is present in high concentrations in various organisms and is capa- ble of surviving almost complete dehydration [55]. Na- kamura et al. (2008) used it to stabilise and preserve cell membrane proteins. Some studies have demonstrated the combination of freeze-drying and gamma irradiation of AM as an efficient sterilisation technique. However, the use of a chemical family of organic peroxides, peracetic acid, is usually used as a sterilising agent against many viruses, bacterium and spores, due to its high oxidation potential and non-toxic waste generation. In a study by Wilshaw et al. (2006), the use of peracetic acid to steril- ise human skin was effective, as it preserved the ex- tracellular matrix components, such as type IV collagen, laminin, fibronectin, elastin and glycosaminoglycans. Furthermore, there was no significant reduction in volt- age, resistance and elasticity after the treatment of amni- otic membrane with peracetic acid [56]. Souza et al. (2004) reported the contamination of am- niotic membrane after caesarean section delivery. These authors also described the contamination of amniotic fluid in 13 of 23 patients with intact membranes and sug- gested aseptic care before handling the membrane. Dual et al. (2004) argue that there is a risk of infection, and that disinfecting procedures must be performed, not only in preparation and storage, but also during clinical use [25,57]. The use of amniotic membrane associated with tissue bioengineering is a powerful tool in the repair, protection and reconstruction of various organs and tissues. 8. ENGINEERING HEART TISSUE Cargnoni et al. (2009) used a fragment of AM that was applied to the left ventricle after coronary artery ligation by ischaemia in rats. Seven days after the transplant, the rats treated with amniotic membrane showed a greater preservation of cardiac dimensions and cardiac contrac- tile element function, and they had improved in terms of the largest left ventricle ejection fraction shortening and thickening of the wall. It has been suggested that the use of amniotic membrane can be the vehicle for the supply of cells that are able to produce soluble factors and car- dioprotectors, and this reinforces the notion that this tis- sue is a source of cells with clinical potential that has not been fully revealed [58]. A study was performed using transplanted amniotic membrane cells (cells that are derived from the meso- dermal lineage). When these cells were transplanted into rat myocardium in myocardial infarction, the analysis of heart function demonstrated that 2 and 6 weeks after the implantation there was no attenuation or improvement of dilation of the left ventricular dilatation and maintenance of cardiac dysfunction, when compared to the control group [59]. Zhao et al. (2005) used isolated cells from amniotic membrane that were analysed by the PCR technique for the detection of specific cardiac genes and subsequently Copyright © 2013 SciRes. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 1183 transplanted them in heart infarction in murine model. They described that the cells from the amniotic mem- brane survived in scar tissue for at least two months af- terwards and these cell were differentiated from cells with characteristics of cardiomyocytes [24]. Lionetti et al. (2010) reported that transplantation of human amnion-derived mesenchymal stem cells with hyaluron in mixed esters of butyric and retinoic acid con- ditions in rat injured myocardium, differentiated into cardiomyocyte phenotype and increased the capillary density of the infarcted myocardium [60]. Tsujhi et al. (2010) studied stem cells derived from rat heart that were transplanted in AM and were able to be transdiferenciated in cardiomyocytes. They demonstrated immunological tolerance in vivo for four weeks after the transplant. Those experiments were performed without the use of immunosuppressive agents [29]. Studies suggest that the cells of AM have some com- mon characteristics with cardiomyocytes, and there is the possibility of them being suitable for cellular cardio- myoplasty, although their characteristics and potential are not yet completely understood [24,49]. In the poten- tial alternative therapeutic applications in engineering heart tissue, there should be kinds of disadvantages to be taken into consideration: allogeneic reactions and the virus contamination of AM, as Cytomegalovirus [61]. Those conditions can be avoided with the use of immu- nosuppressant and gamma radiation into End-products: matrix or cells, respectively. 9. CONCLUSION AM is an alternative source of stem cells, which is par- ticularly interesting due to its ability to differentiate, low immunogenicity, low carcinogenicity, as well as being without any ethical concerns. AM has great potential for therapeutic applications in regenerating heart tissue and is a potential source of mesenchymal stem cells, as well as the source of biocompatible matrix. REFERENCES [1] Chachques, J.C. (2011) Development of bioartificial myo- cardium using stem cells and nanobiotechnology tem- plates. Cardiology Research and Practice, 2011, Article ID: 806795. http://dx.doi.org/10.4061/2011/806795 [2] Toda, A., Okabe, M., Yoshida, T. and Nikaido, T. (2007) The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. Journal of Pharma- cology Sciences, 105, 215-218. [3] Insausti, C.L., Blanquer, M., Bleda, P., Iniesta, P., Ma- jado, M.J., Castellanos, G. and Moraleda, J.M. (2010) The amniotic membrane as a source of stem cells. His- tology and Histopathology, 25, 91-98. [4] Roubelakis, M.G., Trohatou, O. and Anagnou, N.P. (2012) Amniotic fluid and aminiotic membrane stem cells: Marker discovery. Stem Cells International, 2012, Article ID: 107836. http://dx.doi.org/10.1155/2012/107836 [5] Dobreva, M.P., Lhoest, L., Pereira, P.N., Umans, L., Camus, A., Lopes, S.M.C.S. and Zwijsen, A. (2012) Pe- riostin as a biomarker of the amniotic membrane. Stem Cells International, 2012, Article ID: 987185. http://dx.doi.org/10.1155/2012/987185 [6] Trelford, J.D. and Trelford-Sauder, M. (1979) The amn- ion in surgery, past and present. American Journal of Ob- stetrics & Gynecology, 134, 833-845. [7] Kim, J.C. and Tseng, S.C. (1995) Transplantation of pre- served human amniotic membrane for surface reconstruc- tion in severely damaged rabbit corneas. Cornea, 14, 473- 484. http://dx.doi.org/10.1097/00003226-199509000-00006 [8] Lindenmair, A., Wolbank, S., Stadler, G., Meinl, A., Pe- terbauer-Scherb, A., Eibl, J., Polin, H., Gabriel, C., Gri- ensven, M. and Redl, H. (2010) Osteogenic differentia- tion of intact human amniotic membrane. Biomaterials, 31, 8659-8665. http://dx.doi.org/10.1016/j.biomaterials.2010.07.090 [9] Zimmermann, W.H. and Eschenhagen, T. (2003) Cardiac tissue engineering for replacement therapy. Heart Failure Reviews, 8, 259-269. http://dx.doi.org/10.1023/A:1024725818835 [10] Akle, C.A., Adinolfi, M., Welsh, K.I., Leibowitz, S. and McColl, I. (1981) Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lan- cet, 318, 1003-1005. http://dx.doi.org/10.1016/S0140-6736(81)91212-5 [11] Kubo, M., Sonoda, Y., Muramatsu, R. and Usui, M. (2001) Immunogenicity of human amniotic membrane in experimental xenotransplantation. Investigative Ophthal- mology & Visual Science, 42, 1539-1546. [12] Niknejad, H., Peirovi, H., Jorjani, M., Ahmadiani, A., Ghanavi, J. and Seifalian, A.M. (2008) Properties of the amniotic membrane for potential use in tissue engineering. European Cells and Materials Journal, 15, 88-99. [13] Zhang, D.G., Jiang, M.Y. and Miao, D.S. (2011) Trans- planted human amniotic membrane-derived mesenchymal stem cells ameliorate carbon tetrachloride-induced liver cirrhosis in mouse. PLoS One, 6, Article ID: e16789. [14] Lindenmair, A., Hatlapatka, T., Kollwig, G., Henner- bichler, S., Gabriel, C., Wolbank, S., Redl, H. and Kasper, C. (2012) Mesenchymal stem or stromal cells from am- nion and umbilical cord tissue and their potential for clinical applications. Cells, 1, 1061-1088. http://dx.doi.org/10.3390/cells1041061 [15] Davis, J.W. (1910) Skin transplantation with a review of 550 cases at the Johns Hopkins Hospital. Johns Hopkins Medical Journal, 15, 307. [16] Roth, A.D. (1940) Plastic repair of conjunctival defects with fetal membrane. Archives of Ophthalmology, 23, 522-525. http://dx.doi.org/10.1001/archopht.1940.00860130586006 [17] Sorsby, A. and Symons, H.M. (1946) Amniotic mem- brane grafts in caustic burns of the eye (Burns of the Copyright © 2013 SciRes. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 1184 second degree). British Journal of Ophthalmology, 30, 337-345. http://dx.doi.org/10.1136/bjo.30.6.337 [18] Tseng, S.C., Prabhasawat, P., Barton, K., Gray, T. and Meller, D. (1998) Amniotic membrane transplantation with or without limbal allografts for corneal surface re- construction in patients with limbal stem cell deficiency. Archives of Ophthalmology, 116, 431-441. http://dx.doi.org/10.1001/archopht.116.4.431 [19] Azuara-Blanco, A., Pillai, C.T. and Dua, H.S. (1999) Amniotic membrane transplantation for ocular surface reconstruction. British Journal of Ophthalmology, 83, 399-402. http://dx.doi.org/10.1136/bjo.83.4.399 [20] Chen, H.J., Pires, R.T. and Tseng, S.C. (2000) Amniotic membrane transplantation for severe neurotrophic corneal ulcers. British Journal of Ophthalmology, 84, 826-833. http://dx.doi.org/10.1136/bjo.84.8.826 [21] Mligiliche, N., Endo, K., Okamoto, K., Fujimoto, E. and Ide, C. (2002) Extracellular matrix of human amnion ma- nufactured into tubes as conduits for peripheral nerve re- generation. Journal ofBiomedical Material Research, 63, 591-600. http://dx.doi.org/10.1002/jbm.10349 [22] Tamagawa, T., Ishiwata, I. and Saito, S. (2004) Estab- lishment and characterization of a pluripotent stem cell line derived from human amniotic membranes and initia- tion of germ layers in vitro. Human Cell, 17, 125-130. http://dx.doi.org/10.1111/j.1749-0774.2004.tb00028.x [23] Lo, V. and Pope, E. (2009) Amniotic membrane use in dermatology. International Journal of Dermatology, 48, 935-940. http://dx.doi.org/10.1111/j.1365-4632.2009.04173.x [24] Zhao, P., Ise, H., Hongo, M., Ota, M., Konishi, I. and Nikaido, T. (2005) Human amniotic mesenchymal cells have some characteristics of cardiomyocytes. Transplan- tation, 79, 528-535. http://dx.doi.org/10.1097/01.TP.0000149503.92433.39 [25] Tsuji, H., Miyoshi, S., Ikegami, Y., Hida, N., Asada, H., Togashi, I., Suzuki, J., Satake, M., Nakamizo, H., Tanaka, M., Mori, T., Segawa, K., Nishiyama, N., Inoue, J., Ma- kino, H., Miyado, K., Ogawa, S., Yoshimura, Y. and Umezawa, A. (2010) Xenografted human amniotic mem- brane-derived mesenchymal stem cells are immunologi- cally tolerated and transdifferentiated into cardiomyo- cytes. Circulation Research, 106, 1613-1623. http://dx.doi.org/10.1161/CIRCRESAHA.109.205260 [26] Dual, H.S. and Azuara-Blanco, A. (1999) Amniotic mem- brane transplantation. British Journal of Ophthalmology, 83, 748-752. http://dx.doi.org/10.1136/bjo.83.6.748 [27] Wynn, R.M. and Corbett, J.R. (1969) Ultrastructure of the canine placenta and amnion. American Journal of Obstetrics & Gynecology, 103, 878-887. [28] Segev, A., Nili, N. and Strauss, B.H. (2004) The role of perlecan in arterial injury and angiogenesis. Cardiovas- cular Research, 63, 603-610. http://dx.doi.org/10.1016/j.cardiores.2004.03.028 [29] Sachs, B.P. and Stern, C.M. (1979) Activity and charac- terization of a low molecular fraction present in human amniotic fluid with broad spectrum antibacterial activity. British Journal of Obstetrics & Gynecology, 86, 81-86. http://dx.doi.org/10.1111/j.1471-0528.1979.tb10572.x [30] Kim, J.C. and Tseng, S.C. (1995) The effects on inhibi- tion of corneal neovascularization after human amniotic membrane transplantation in severely damaged rabbit corneas. Korean Journal of Ophthalmology, 9, 32-46. [31] Krisanaprakornkit, S., Weinberg, A., Perez, C.N. and Dale, B.A. (1998) Expression of the peptide antibiotic human beta-defensin 1 in cultured gingival epithelial cells and gingival tissue. Infection and Immunity, 66, 4222- 4228. [32] Talmi, Y.P., Sigler, L., Inge, E., Finkelstein, Y. and Zo- har, Y. (1991) Antibacterial properties of human amniotic membranes. Placenta, 12, 285-288. http://dx.doi.org/10.1016/0143-4004(91)90010-D [33] Dua, H.S., Gomes, J.A., King, A.J. and Maharajan, V.S. (2004) The amniotic membrane in ophthalmology. Survey of Ophthalmology, 49, 51-77. http://dx.doi.org/10.1016/j.survophthal.2003.10.004 [34] Cen, L., Liu, W., Cui, W., Zhang, W. and Cao, Y. (2008) Collagen tissue engineering: Development of novel bio- materials and applications. Pediatric Research, 63, 492- 496. http://dx.doi.org/10.1203/PDR.0b013e31816c5bc3 [35] Koizumi, N., Fullwood, N.J., Bairaktaris, G., Inatomi, T., Kinoshita, S. and Quantock, A.J. (2000) Cultivation of corneal epithelial cells on intact and denuded human am- niotic membrane. Investigative Ophthalmology & Visual Science, 41, 2506-2513. [36] Hopper, R.A., Woodhouse, K. and Semple, J.L. (2003) Acellularization of human placenta with preservation of the basement membrane: A potential matrix for tissue en- gineering. Annals of Plastic Surgery, 51, 598-602. http://dx.doi.org/10.1097/01.sap.0000095658.46675.76 [37] Shortt, A.J., Secker, G.A., Lomas, R.J., Wilshaw, S.P., Kearney, J.N., Tuft, S.J. and Daniels, J.T. (2008) The ef- fect of amniotic membrane preparation method on its ability to serve as a substrate for the ex-vivo expansion of limbal epithelial cells. Biomaterials, 30, 1056-1065. http://dx.doi.org/10.1016/j.biomaterials.2008.10.048 [38] Bigbie, R.B., Schumacher, J., Swaim, S.F., Purohit, R.C. and Wright, J.C. (1991) Effects of amnion and live yeast cell derivative on second-intention healing in horses. American Journal of Veterinary Research, 52, 1376-1382. [39] Solomon, A., Rosenblatt, M., Monroy, D., Ji, Z., Pflug- felder, S.C. and Tseng, S.C. (2001) Suppression of inter- leukin 1alpha and interleukin 1beta in human limbal epithelial cells cultured on the amniotic membrane stro- mal matrix. British Journal of Ophthalmology, 85, 444- 449. http://dx.doi.org/10.1136/bjo.85.4.444 [40] Hao, Y., Ma, D.H., Hwang, D.G., Kim, W.S. and Zhang, F. (2000) Identification of antiangiogenic and antiinflam- matory proteins in human amniotic membrane. Cornea, 19, 348-352. http://dx.doi.org/10.1097/00003226-200005000-00018 [41] Díaz-Prado, S., Muiños-López, E., Hermida-Gomez, T., Rendal-Vazquez, M.E., Fuentes-Boquete, I., de Toro, F.J. and Blanco, F.J. (2011) Isolation and characterization of mesenchymal stem cells from human amniotic membrane. Tissue Engineering Part C: Methods, 17, 49-59. http://dx.doi.org/10.1089/ten.tec.2010.0136 [42] Ilancheran, S., Moodley, Y. and Manuelpillai, U. (2009) Copyright © 2013 SciRes. OPEN ACCESS
J. C. Francisco et al. / J. Biomedical Science and Engineering 6 (2013) 1178-1185 Copyright © 2013 SciRes. 1185 OPEN ACCESS Human fetal membranes: A source of stem cells for tissue regeneration and repair? Placenta, 30, 2-10. http://dx.doi.org/10.1016/j.placenta.2008.09.009 [43] Parolini, O., Soncini, M., Evangelista, M. and Schmidt, D. (2009) Amniotic membrane and amniotic fluid-derived cells: Potential tools for regenerative medicine? Regen- erative Medicine, 4, 275-291. http://dx.doi.org/10.2217/17460751.4.2.275 [44] Niknejad, H., Peirovi, H., Jorjani, M., Ahmadiani, A., Ghanavi, J. and Seifalian, A.M. (2009) Properties of the amniotic membrane for potential use in tissue engineering. European Cells & Materials Journal, 15, 88-99. [45] Insausti, C.L., Blanquer, M., Bleda, P., Iniesta, P., Ma- jado, M.J., Castellanos, G. and Moraleda, J.M. (2010) The amniotic membrane as a source of stem cells. His- tology and Histopathology, 25, 91-98. [46] Kobayashi, M., Yakuwa, T., Sasaki, K., Sato, K., Kikuchi, A., Kamo, I., Yokoyama, Y. and Sakuragawa, N. (2008) Multilineage potential of side population cells from hu- man amnion mesenchymal layer. Cell Transplantion, 17, 291-301. http://dx.doi.org/10.3727/096368908784153904 [47] Mihu, C.M., RusCiuča, D., Soritău, O., Susman, S. and Mihu, D. (2009) Isolation and characterization of mesen- chymal stem cells from the amniotic membrane. Roma- nian Journal of Morphology and Embryology, 50, 73-77. [48] Miki, T. and Strom, S.C. (2006) Amnion-derived pluri- potent/multipotent stem cells. Stem Cell Reviews, 2, 133- 142. http://dx.doi.org/10.1007/s12015-006-0020-0 [49] Paracchini, V., Carbone, A., Colombo, F., Castellani, S., Mazzucchelli, S., Di Gioia, S., Degiorgio, D., Seia, M., Porretti, L., Colombo, C. and Conese, M. (2012) Amniotic mesenchymal stem cells: A new source for hepatocyte- like cells and induction of CFTR expression by coculture with cystic fibrosis airway epithelial cells. Journal of Bio- medicine and Biotechnology, 2012, Article ID: 575471. http://dx.doi.org/10.1155/2012/575471 [50] Miki, T., Lehmann, T., Cai, H., Stolz, D.B. and Strom, S.C. (2005) Stem cell characteristics of amniotic epithe- lial cells. Stem Cells, 23, 1549-1559. http://dx.doi.org/10.1634/stemcells.2004-0357 [51] Portmann-Lanz, C.B., Schoeberlein, A., Huber, A., Sager, R., Malek, A., Holzgreve, W. and Surbek, D.V. (2006) Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. American Journal of Obstetrics & Gynecology, 194, 664-673. http://dx.doi.org/10.1016/j.ajog.2006.01.101 [52] Kara, R.J., Bolli, P., Karakikes, I., Matsunaga, I., Tripodi, J., Tanweer, O., Altman, P., Shachter, N.S., Nakano, A., Najfeld, V. and Chaudhry, H.W. (2012) Fetal cells traffic to injured maternal myocardium and undergo cardiac dif- ferentiation. Circulation Research, 110, 82-93. http://dx.doi.org/10.1161/CIRCRESAHA.111.249037 [53] Choi, T.H. and Tseng, S.C. (2001) In Vivo and in Vitro demonstration of epithelial cell-induced myofibroblast dif- ferentiation of keratocytes and an inhibitory effect by am- niotic membrane. Cornea, 20, 197-204. http://dx.doi.org/10.1097/00003226-200103000-00019 [54] Mejia, L.F., Santamaria, J.P. and Acosta, C. (2002) Sym- ptomatic management of postoperative bullous keratopa- thy with nonpreserved human amniotic membrane. Cor- nea, 21, 342-345. http://dx.doi.org/10.1097/00003226-200205000-00002 [55] Nakamura, T., Sekiyama, E., Takaoka, M., Bentley, A.J., Yokoi, N., Fullwood, N.J. and Kinoshita, S. (2008) The use of trehalose-treated freeze-dried amniotic membrane for ocular surface reconstruction. Biomaterials, 29, 3729-3737. http://dx.doi.org/10.1016/j.biomaterials.2008.05.023 [56] Wilshaw, S.P., Kearney, J.N., Fisher, J. and Ingham, E. (2006) Production of an acellular amniotic membrane ma- trix for use in tissue engineering. Tissue Engineering, 12, 2117-2129. http://dx.doi.org/10.1089/ten.2006.12.2117 [57] Souza, C.E.B., Engel, D.P., Branco, B.C., Hofling-Lima, A.L., Freitas, D., Gomes, J.A.P. and Souza, L.B. (2004) Evaluation of microbiological contamination of amniotic membrane and amniotic fluid. Arquivos Brasileiros de Oftalmologia, 67, 709-712. http://dx.doi.org/10.1590/S0004-27492004000500003 [58] Cargnoni, A., Di Marcello, M., Campagnol, M., Nassuato, C., Albertini, A. and Parolini, O. (2009) Amniotic mem- brane patching promotes ischemic rat heart repair. Cell Transplantation, 18, 1147-1159. http://dx.doi.org/10.3727/096368909X12483162196764 [59] Fujimoto, K.L., Miki, T., Liu, L.J., Hashizume, R., Strom, S.C., Wagner, W.R., Keller, B.B. and Tobita, K. (2009) Naive rat amnion-derived cell transplantation improved left ventricular function and reduced myocardial scar of postinfarcted heart. Cell Transplantation, 18, 477-486. http://dx.doi.org/10.3727/096368909788809785 [60] Lionetti, V., Cantoni, S., Cavallini, C., Bianchi, F., Valen- te, S., Frascari, I., Olivi, E., Aquaro, G.D., Bonavita, F., Scarlata, I., Maioli, M., Vaccari, V., Tassinari, R., Bartoli, A., Recchia, F.A., Pasquinelli, G. and Ventura, C. (2010) Hyaluronan mixed esters of butyric and retinoic acid af- fording myocardial survival and repair without stem cell transplantation. The Journal of Biological Chemistry, 285, 9949-9961. http://dx.doi.org/10.1074/jbc.M109.087254 [61] Matsunaga, S., Uchide, N., Shono, M., Ohyama, K., Ta- keichi, M. and Toyoda, H. (2013) Differences in permis- sive cytomegalovirus infection between primary cultured human fetal membrane chorion and amnion cells. Bio- logical and Pharmaceutical Bulletin, 36, 1715-1721. http://dx.doi.org/10.1248/bpb.b13-00200
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