Article

Human amniotic epithelial stem cell is a cell therapy candidate for preventing acute graft-versus-host disease

Peng-jie Yang1, Xiang-yu Zhao2, Yao-hui Kou1,3, Jia Liu1,3, Xiang-yi Ren1,3, Yuan-yuan Zhang2, Zhi-dong Wang2, Zhen Ge4, Wei-xin Yuan3,5, Chen Qiu1,3, Bing Tan1,3, Qin Liu5, Yan-na Shi3, Yuan-qing Jiang1,3, Cong Qiu1,3, Li-he Guo5,6, Jin-ying Li1,3, Xiao-jun Huang2,7, Lu-yang Yu1,3
1 MOE Laboratory of Biosystems Homeostasis & Protection of College of Life Sciences, Key Laboratory of Cardiovascular Intervention and Regenerative Medicine of Zhejiang Province of Sir Run Run Shaw Hospital, Zhejiang University, Hangzhou 310058, China
2 Peking University Institute of Hematology, Beijing Key Laboratory of Hematopoietic Stem Cell Transplantation, Peking University People’s Hospital, Peking University, Beijing 100044, China
3 College of Life Sciences-iCell Biotechnology Regenerative Biomedicine Laboratory, Joint Research Centre for Engineering Biology, Zhejiang University-University of Edinburgh Institute, Zhejiang University, Hangzhou 314400, China
4 School of Pharmaceutical Sciences, Hangzhou Medical College, Hangzhou 310013, China
5 Shanghai iCELL Biotechnology Co. Ltd, Shanghai 200335, China
6 Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China
7 Peking-Tsinghua Center for Life Sciences, Beijing 100084, China
Correspondence to: Jin-ying Li: jinyingli@zju.edu.cn, Xiao-jun Huang: xjhrm@medmail.com.cn, Lu-yang Yu: luyangyu@zju.edu.cn,
DOI: 10.1038/s41401-024-01283-y
Received: 18 August 2023
Accepted: 1 April 2024
Advance online: 27 May 2024

Abstract

Graft-versus-host disease (GVHD), an immunological disorder that arises from donor T cell activation through recognition of host alloantigens, is the major limitation in the application of allogeneic hematopoietic stem cell transplantation (allo-HSCT). Traditional immunosuppressive agents can relieve GVHD, but they induce serious side effects. It is highly required to explore alternative therapeutic strategy. Human amniotic epithelial stem cells (hAESCs) were recently considered as an ideal source for cell therapy with special immune regulatory property. In this study, we evaluated the therapeutic role of hAESCs in the treatment of GVHD, based on our previous developed cGMP-grade hAESCs product. Humanized mouse model of acute GVHD (aGVHD) was established by injection of huPBMCs via the tail vein. For prevention or treatment of aGVHD, hAESCs were injected to the mice on day -1 or on day 7 post-PBMC infusion, respectively. We showed that hAESCs infusion significantly alleviated the disease phenotype, increased the survival rate of aGVHD mice, and ameliorated pathological injuries in aGVHD target organs. We demonstrated that hAESCs directly induced CD4+ T cell polarization, in which Th1 and Th17 subsets were downregulated, and Treg subset was elevated. Correspondingly, the levels of a series of pro-inflammatory cytokines were reduced while the levels of the anti-inflammatory cytokines were upregulated in the presence of hAESCs. We found that hAESCs regulated CD4+ subset polarization in a paracrine mode, in which TGFβ and PGE2 were selectively secreted to mediate Treg elevation and Th1/Th17 inhibition, respectively. In addition, transplanted hAESCs preserved the graft-versus-leukemia (GVL) effect by inhibiting leukemia cell growth. More intriguingly, hAESCs infusion in HSCT patients displayed potential anti-GVHD effect with no safety concerns and confirmed the immunoregulatory mechanisms in the preclinical study. We conclude that hAESCs infusion is a promising therapeutic strategy for post-HSCT GVHD without compromising the GVL effect. The clinical trial was registered at www.clinicaltrials.gov as #NCT03764228.
Keywords: graft-versus-host disease; hematopoietic stem cell transplantation; human amniotic epithelial stem cells; immunomodulation

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