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Application of Human Amniotic Epithelial Cells in Regenerative Medicine: a Systematic Review Qiuwan Zhang and Dongmei Lai*

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Application of Human Amniotic Epithelial Cells in Regenerative Medicine: a Systematic Review Qiuwan Zhang and Dongmei Lai* Zhang and Lai Stem Cell Research & Therapy (2020) 11:439 https://doi.org/10.1186/s13287-020-01951-w REVIEW Open Access Application of human amniotic epithelial cells in regenerative medicine: a systematic review Qiuwan Zhang and Dongmei Lai* Abstract Human amniotic epithelial cells (hAECs) derived from placental tissues have gained considerable attention in the field of regenerative medicine. hAECs possess embryonic stem cell-like proliferation and differentiation capabilities, and adult stem cell-like immunomodulatory properties. Compared with other types of stem cell, hAECs have special advantages, including easy isolation, plentiful numbers, the obviation of ethical debates, and non-immunogenic and non-tumorigenic properties. During the past two decades, the therapeutic potential of hAECs for treatment of various diseases has been extensively investigated. Accumulating evidence has demonstrated that hAEC transplantation helps to repair and rebuild the function of damaged tissues and organs by different molecular mechanisms. This systematic review focused on summarizing the biological characteristics of hAECs, therapeutic applications, and recent advances in treating various tissue injuries and disorders. Relevant studies published in English from 2000 to 2020 describing the role of hAECs in diseases and phenotypes were comprehensively sought out using PubMed, MEDLINE, and Google Scholar. According to the research content, we described the major hAEC characteristics, including induced differentiation plasticity, homing and differentiation, paracrine function, and immunomodulatory properties. We also summarized the current status of clinical research and discussed the prospects of hAEC-based transplantation therapies. In this review, we provide a comprehensive understanding of the therapeutic potential of hAECs, including their use for cell replacement therapy as well as secreted cytokine and exosome biotherapy. Moreover, we showed that the powerful immune-regulatory function of hAECs reveals even more possibilities for their application in the treatment of immune-related diseases. In the future, establishing the optimal culture procedure, achieving precise and accurate treatment, and enhancing the therapeutic potential by utilizing appropriate preconditioning and/or biomaterials would be new challenges for further investigation. Keywords: Human amniotic/amnion epithelial cells, Cell transplantation, Differentiation, Paracrine properties, Immunomodulation, Regenerative medicine * Correspondence: [email protected] The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University; Shanghai Key Laboratory of Embryo Original Diseases; Shanghai Municipal Key Clinical Speciality, 145, Guang-Yuan Road, Shanghai 200030, People’s Republic of China © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhang and Lai Stem Cell Research & Therapy (2020) 11:439 Page 2 of 16 Background exhibit unlimited proliferation due to the lack of tel- Human amniotic/amnion epithelial cells (hAECs) are de- omerase activity and no risk of tumorigenesis in vivo rived from the innermost layer of the term placenta clos- [16]. Moreover, hAECs have tri-mesodermal lineage dif- est to the fetus, and they have been shown to have the ferentiation potential; they can produce osteogenic, adi- potential to be seed cells for allogeneic cell therapies. pogenic, and chondrogenic lineages under appropriate Over the past 20 years, interest has been growing regard- culture conditions [17]. Notably, hAECs have low ex- ing the utility of hAECs in regenerative medicine due to pression levels of human leukocyte antigens (including their proliferative capacity, multilineage differentiation HLA-A, HLA-B, and HLA-C and HLA-DR), which are potential, ease of access, and safety. Advances in stem key antigens involved in recipient rejection [1, 18]. A cell-based approaches have revealed that hAECs are study confirmed that intravenous administration of perinatal stem cells that possess embryonic stem cell- hAECs did not result in hemolysis, allergic reactions, like properties and the ability to be induced to differenti- toxicity, or tumor formation, which demonstrated that ate. As promising seed stem cell, hAECs have been hAECs were systematically safe [19]. Thus, hAECs are widely used to treat various diseases through transplant- considered a promising source of stem cells for regen- ation therapy. Evidence supported by animal studies has erative medicine. revealed that hAECs show therapeutic potential for To safely and effectively use hAECs to repair the treatment of many diseases, including neurological dis- function of injured tissues and treat diseases, it is es- orders [1–4], lung injury [5, 6], liver injury [7], diabetes sential that they are of high quality. Currently, the [8], acute kidney failure [9], cardiovascular diseases [10], trypsin/EDTA technique is the most efficient for wound healing [11], healing of stage III pressure ulcers obtaining viable hAECs for subsequent culture [20, [12], intrauterine adhesion [13], and premature ovarian 21]. The key aspects involved in the isolation of hAECs failure (POF) [14]. Although hAECs have exhibited good with high yield, viability, and purity have been previ- therapeutic efficacy, they possess differences in differen- ously summarized [22]. Meanwhile, standard manufac- tiation potential, secretory function, and immunomodu- turing and cryopreservation process were established latory activity under different conditions, producing that resulted in the isolation of highly purified hAECs specific effects depending on their application. In this re- with reproducible and high viability in accordance with view, we mainly examined the literature about the thera- current good manufacturing procedure (GMP) require- peutic potential of hAECs and summarized the different ments [23]. In addition, a study found that epidermal repair mechanisms in injured tissues and disorders; we growth factor (EGF) was a strong mitogen that pro- also discussed the induced differentiation plasticity, moted the proliferation of hAECs by regulating the cell homing and differentiation, paracrine function, and im- cycle rather than inducing differentiation in the munomodulatory capacity of hAECs. Finally, we de- process of culture in vitro [24]. Although primary scribed the current research strategies and proposed hAECs strongly expressed stemness-related genes for new prospects for hAEC-based clinical applications in OCT-4, Sox-2, and Nanog, these gene expression levels the future. gradually declined with an increase in passage number [25]. Study revealed that cultured hAECs underwent Methods epithelial to mesenchymal transition (EMT) through Comprehensive literature searches using PubMed, the autocrine production of TGF-beta (TGF-β)[26]. MEDLINE, or Google Scholar were performed to iden- Moreover, TNF-alpha (TNF-α) and matrix metallopro- tify articles for review written in English focusing on the teinase (MMP) could induce EMT of hAECs [27]. biology of hAECs and the role of hAECs in injured tis- Therefore, researchers have tried to explore different sues, diseases, and regenerative medicine. culture methods to maintain stemness and avoid EMT occurrence. A study found that hAECs were cultured Biological characteristics of hAECs in substitute serum medium (SSM) in which fetal calf hAECs are obtained from the amniotic membrane of serum (FCS) was replaced by knockout serum replace- term placentas, which are discarded after birth. Thus, ment (SR), contributing to maintain stem cell charac- hAECs are readily available, require no invasive proce- teristics for up to 4 passages [28]. Furthermore, dures for harvesting, and avoid relevant ethical issues. xenobiotic-free medium was used for the culture of Isolated hAECs express surface markers of embryonic hAECs to eliminate the effects of growth factors [29]. stem cells such as stage-specific embryonic antigen-3 Meanwhile, a serum-free protocol established for and 4 (SSEA-3 and SSEA-4), octamer-binding transcrip- hAEC isolation and culture resulted in better cell tion factor-4 (OCT-4), and tumor rejection antigen1-60 growth than that achieved by a traditional culture sys- and 1-80 (TRA1-60 and TRA1-80) [15]. Although tem with serum [19], which made the clinical applica- hAECs possess stem cell-like characteristics, they do not tions of hAECs more feasible. Zhang and Lai Stem Cell Research & Therapy (2020) 11:439 Page 3 of 16 Although the biological characteristics
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