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Article: The role of innate immunity in the long-term outcome of lung transplantation.

Kawashima, Mitsuaki / Juvet, Stephen C

2020 Volume 8, Issue 6, Page(s) 412

Abstract: Long-term survival after lung transplantation remains suboptimal due to chronic lung allograft dysfunction (CLAD), a progressive scarring process affecting the graft. Although anti-donor alloimmunity is central to the pathogenesis of CLAD, its underlying ...

Abstract	Long-term survival after lung transplantation remains suboptimal due to chronic lung allograft dysfunction (CLAD), a progressive scarring process affecting the graft. Although anti-donor alloimmunity is central to the pathogenesis of CLAD, its underlying mechanisms are not fully elucidated and it is neither preventable nor treatable using currently available immunosuppression. Recent evidence has shown that innate immune stimuli are fundamental to the development of CLAD. Here, we examine long-standing assumptions and new concepts linking innate immune activation to late lung allograft fibrosis.
Language	English
Publishing date	2020-04-29
Publishing country	China
Document type	Journal Article ; Review
ZDB-ID	2893931-1
ISSN	2305-5847 ; 2305-5839
ISSN (online)	2305-5847
ISSN	2305-5839
DOI	10.21037/atm.2020.03.20
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Murine Intrapulmonary Tracheal Transplantation: A Model for Investigating Obliterative Airway Disease After Lung Transplantation.

Suzuki, Yamato / Juvet, Stephen / Liu, Mingyao / Keshavjee, Shaf

Journal of visualized experiments : JoVE

2023 , Issue 201

Abstract: Murine intrapulmonary tracheal transplantation (IPTT) is used as a model of obliterative airway disease (OAD) following lung transplantation. Initially reported by our team, this model has gained use in the study of OAD due to its high technical ... ...

Abstract	Murine intrapulmonary tracheal transplantation (IPTT) is used as a model of obliterative airway disease (OAD) following lung transplantation. Initially reported by our team, this model has gained use in the study of OAD due to its high technical reproducibility and suitability for investigating immunological behaviors and therapeutic interventions. In the IPTT model, a rodent tracheal graft is directly inserted into the recipient's lung through the pleura. This model is distinct from the heterotopic tracheal transplantation (HTT) model, wherein grafts are transplanted into subcutaneous or omental sites, and from the orthotopic tracheal transplantation (OTT) model in which the donor trachea replaces the recipient's trachea. Successful implementation of the IPTT model requires advanced anesthetic and surgical skills. Anesthetic skills include endotracheal intubation of the recipient, setting appropriate ventilatory parameters, and appropriately timed extubation after recovery from anesthesia. Surgical skills are essential for precise graft placement within the lung and for ensuring effective sealing of the visceral pleura to prevent air leakage and bleeding. In general, the learning process takes approximately 2 months. In contrast to the HTT and OTT models, in the IPTT model, the allograft airway develops airway obliteration in the relevant lung microenvironment. This allows investigators to study lung-specific immunological and angiogenic processes involved in airway obliteration after lung transplantation. Furthermore, this model is also unique in that it exhibits tertiary lymphoid organs (TLOs), which are also seen in human lung allografts. TLOs are comprised of T and B cell populations and characterized by the presence of high endothelial venules that direct immune cell recruitment; therefore, they are likely to play a crucial role in graft acceptance and rejection. We conclude that the IPTT model is a useful tool for studying intrapulmonary immune and profibrotic pathways involved in the development of airway obliteration in the lung transplant allograft.
MeSH term(s)	Humans ; Mice ; Animals ; Bronchiolitis Obliterans/etiology ; Bronchiolitis Obliterans/surgery ; Trachea/transplantation ; Reproducibility of Results ; Lung Transplantation/adverse effects ; Anesthetics ; Mice, Inbred C57BL ; Mice, Inbred BALB C ; Disease Models, Animal
Chemical Substances	Anesthetics
Language	English
Publishing date	2023-11-10
Publishing country	United States
Document type	Journal Article ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/65953
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Article: Unlocking the potential of RNA-based therapeutics in the lung: current status and future directions.

Man, H S Jeffrey / Moosa, Vaneeza A / Singh, Anand / Wu, Licun / Granton, John T / Juvet, Stephen C / Hoang, Chuong D / de Perrot, Marc

Frontiers in genetics

2023 Volume 14, Page(s) 1281538

Abstract: Awareness of RNA-based therapies has increased after the widespread adoption of mRNA vaccines against SARS-CoV-2 during the COVID-19 pandemic. These mRNA vaccines had a significant impact on reducing lung disease and mortality. They highlighted the ... ...

Abstract	Awareness of RNA-based therapies has increased after the widespread adoption of mRNA vaccines against SARS-CoV-2 during the COVID-19 pandemic. These mRNA vaccines had a significant impact on reducing lung disease and mortality. They highlighted the potential for rapid development of RNA-based therapies and advances in nanoparticle delivery systems. Along with the rapid advancement in RNA biology, including the description of noncoding RNAs as major products of the genome, this success presents an opportunity to highlight the potential of RNA as a therapeutic modality. Here, we review the expanding compendium of RNA-based therapies, their mechanisms of action and examples of application in the lung. The airways provide a convenient conduit for drug delivery to the lungs with decreased systemic exposure. This review will also describe other delivery methods, including local delivery to the pleura and delivery vehicles that can target the lung after systemic administration, each providing access options that are advantageous for a specific application. We present clinical trials of RNA-based therapy in lung disease and potential areas for future directions. This review aims to provide an overview that will bring together researchers and clinicians to advance this burgeoning field.
Language	English
Publishing date	2023-11-23
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2606823-0
ISSN	1664-8021
ISSN	1664-8021
DOI	10.3389/fgene.2023.1281538
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Article ; Online: Robust segregation of donor and recipient cells from single-cell RNA-sequencing of transplant samples

Gavin W. Wilson / Allen Duong / Sajad Moshkelgosha / Gary Bader / Shaf Keshavjee / Tereza Martinu / Stephen C. Juvet / Jonathan C. Yeung

Frontiers in Transplantation, Vol

2023 Volume 2

Abstract: BackgroundSingle-cell RNA-sequencing (scRNA-seq) technology has revealed novel cell populations in organs, uncovered regulatory relationships between genes, and allowed for tracking of cell lineage trajectory during development. It demonstrates promise ... ...

Abstract	BackgroundSingle-cell RNA-sequencing (scRNA-seq) technology has revealed novel cell populations in organs, uncovered regulatory relationships between genes, and allowed for tracking of cell lineage trajectory during development. It demonstrates promise as a method to better understand transplant biology; however, fundamental bioinformatic tools for its use in the context of transplantation have not been developed. One major need has been a robust method to identify cells as being either donor or recipient genotype origin, and ideally without the need to separately sequence the donor and recipient.MethodsWe implemented a novel two-stage genotype discovery method (scTx) optimized for transplant samples by being robust to disparities in cell number and cell type. Using both in silico and real-world scRNA-seq transplant data, we benchmarked our method against existing demultiplexing methods to profile their limitations in terms of sequencing depth, donor and recipient cell imbalance, and single nucleotide variant input selection.ResultsUsing in silico data, scTx could more accurately separate donor from recipient cells and at much lower genotype ratios than existing methods. This was further validated using solid-organ scRNA-seq data where scTx could more reliably identify when a second genotype was present and at lower numbers of cells from a second genotype.ConclusionscTx introduces the capability to accurately segregate donor and recipient gene expression at the single-cell level from scRNA-seq data without the need to separately genotype the donor and recipient. This will facilitate the use of scRNA-seq in the context of transplantation.
Keywords	single-cell RNA-sequencing ; solid-organ transplantation ; bioinformatics ; application ; donor and recipient genotypes ; Specialties of internal medicine ; RC581-951
Subject code	610
Language	English
Publishing date	2023-06-01T00:00:00Z
Publisher	Frontiers Media S.A.
Document type	Article ; Online
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Article ; Online: Donor IL-17 receptor A regulates LPS-potentiated acute and chronic murine lung allograft rejection.

Watanabe, Tatsuaki / Juvet, Stephen C / Berra, Gregory / Havlin, Jan / Zhong, Wenshan / Boonstra, Kristen / Daigneault, Tina / Horie, Miho / Konoeda, Chihiro / Teskey, Grace / Guan, Zehong / Hwang, David M / Liu, Mingyao / Keshavjee, Shaf / Martinu, Tereza

JCI insight

2023 Volume 8, Issue 21

Abstract: Chronic lung allograft dysfunction (CLAD) is a major complication after lung transplantation that results from a complex interplay of innate inflammatory and alloimmune factors, culminating in parenchymal and/or obliterative airway fibrosis. Excessive IL- ...

Abstract	Chronic lung allograft dysfunction (CLAD) is a major complication after lung transplantation that results from a complex interplay of innate inflammatory and alloimmune factors, culminating in parenchymal and/or obliterative airway fibrosis. Excessive IL-17A signaling and chronic inflammation have been recognized as key factors in these pathological processes. Herein, we developed a model of repeated airway inflammation in mouse minor alloantigen-mismatched single-lung transplantation. Repeated intratracheal LPS instillations augmented pulmonary IL-17A expression. LPS also increased acute rejection, airway epithelial damage, and obliterative airway fibrosis, similar to human explanted lung allografts with antecedent episodes of airway infection. We then investigated the role of donor and recipient IL-17 receptor A (IL-17RA) in this context. Donor IL-17RA deficiency significantly attenuated acute rejection and CLAD features, whereas recipient IL-17RA deficiency only slightly reduced airway obliteration in LPS allografts. IL-17RA immunofluorescence positive staining was greater in human CLAD lungs compared with control human lung specimens, with localization to fibroblasts and myofibroblasts, which was also seen in mouse LPS allografts. Taken together, repeated airway inflammation after lung transplantation caused local airway epithelial damage, with persistent elevation of IL-17A and IL-17RA expression and particular involvement of IL-17RA on donor structural cells in development of fibrosis.
MeSH term(s)	Mice ; Humans ; Animals ; Interleukin-17/metabolism ; Receptors, Interleukin-17/metabolism ; Lipopolysaccharides/toxicity ; Lipopolysaccharides/metabolism ; Pulmonary Fibrosis/pathology ; Lung/pathology ; Inflammation/metabolism ; Fibrosis ; Respiratory Tract Infections/metabolism ; Allografts
Chemical Substances	Interleukin-17 ; Receptors, Interleukin-17 ; Lipopolysaccharides
Language	English
Publishing date	2023-11-08
Publishing country	United States
Document type	Journal Article
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.158002
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Article ; Online: Donor Batf3 inhibits murine lung allograft rejection and airway fibrosis.

Watanabe, Tatsuaki / Lam, Christina / Oliver, Jillian / Oishi, Hisashi / Teskey, Grace / Beber, Samuel / Boonstra, Kristen / Mauricio Umaña, Juan / Buhari, Hifza / Joe, Betty / Guan, Zehong / Horie, Miho / Keshavjee, Shaf / Martinu, Tereza / Juvet, Stephen C

Mucosal immunology

2023 Volume 16, Issue 2, Page(s) 104–120

Abstract: Chronic lung allograft dysfunction (CLAD) limits survival after lung transplantation. Noxious stimuli entering the airways foster CLAD development. Classical dendritic cells (cDCs) link innate and adaptive immunity and exhibit regional and functional ... ...

Abstract	Chronic lung allograft dysfunction (CLAD) limits survival after lung transplantation. Noxious stimuli entering the airways foster CLAD development. Classical dendritic cells (cDCs) link innate and adaptive immunity and exhibit regional and functional specialization in the lung. The transcription factor basic leucine zipper ATF-like 3 (BATF3) is absolutely required for the development of type 1 cDCs (cDC1s), which reside in the airway epithelium and have variable responses depending on the context. We studied the role of BATF3 in a mouse minor alloantigen-mismatched orthotopic lung transplant model of CLAD with and without airway inflammation triggered by repeated administration of intratracheal lipopolysaccharide (LPS). We found that cDC1s accumulated in allografts compared with isografts and that donor cDC1s were gradually replaced by recipient cDC1s. LPS administration increased the number of cDC1s and enhanced their state of activation. We found that Batf3
MeSH term(s)	Animals ; Mice ; Allografts ; Fibrosis ; Graft Rejection/drug therapy ; Lipopolysaccharides ; Lung/pathology ; Lung Transplantation ; Mice, Inbred C57BL ; Pulmonary Fibrosis/pathology ; Transplantation, Homologous
Chemical Substances	Lipopolysaccharides ; Batf protein, mouse
Language	English
Publishing date	2023-02-25
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2411370-0
ISSN	1935-3456 ; 1933-0219
ISSN (online)	1935-3456
ISSN	1933-0219
DOI	10.1016/j.mucimm.2023.02.004
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Zs.A 6796: Show issues

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Article ; Online: Donor and recipient human leukocyte antigen-G polymorphisms modulate the risk of adverse immunologic events following lung transplantation.

Riddell, Peter / Ma, Jin / Lazarte, Julieta / Birriel, Daniella / Ulahannan, Ambily / Ghany, Rasheed / Delgado, Diego / Rao, Vivek / Keshavjee, Shaf / Martinu, Tereza / Tikkanen, Jussi / Juvet, Stephen C

American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons

2023 Volume 23, Issue 3, Page(s) 393–400

Abstract: The long-term benefits of lung transplantation (LTx) are limited by pathogenic alloimmune responses that drive injury, inflammation, and chronic dysfunction. Human leukocyte antigen-G (HLA-G) plays a key role in the modulation of these pathways. This ... ...

Abstract	The long-term benefits of lung transplantation (LTx) are limited by pathogenic alloimmune responses that drive injury, inflammation, and chronic dysfunction. Human leukocyte antigen-G (HLA-G) plays a key role in the modulation of these pathways. This study assesses the impact of the HLA-G genotype on immunologic risk and survival following LTx. This retrospective cohort study included 289 bilateral LTx. Recipient and donor HLA-G genotypes were analyzed to identify associations with de novo donor-specific antibodies, acute rejection, chronic lung allograft dysfunction, and allograft survival. We further assessed these associations, both individually and in paired analysis, based on a grouped haplotype classification of HLA-G expression. Donor HLA-G single nucleotide polymorphisms were associated with allograft injury, the onset of chronic lung allograft dysfunction following injury, and allograft survival. Recipient HLA-G single nucleotide polymorphisms were associated with allograft injury, cellular rejection, and donor-specific antibody formation. "Low HLA-G expression" donor haplotypes were associated with impaired allograft survival, as were "low HLA-G expression" donor-recipient haplotype pairs. This study provides compelling evidence for the role of HLA-G in modulating immunologic risk after LTx. Our results highlight the importance of both donor and recipient HLA-G genotypes on the overall risk profile and underscore the lasting influence of donor genotype on lung transplant outcomes.
MeSH term(s)	Humans ; HLA-G Antigens ; Retrospective Studies ; Graft Rejection ; Tissue Donors ; Lung Transplantation/adverse effects ; HLA Antigens ; Graft Survival
Chemical Substances	HLA-G Antigens ; HLA Antigens
Language	English
Publishing date	2023-01-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2060594-8
ISSN	1600-6143 ; 1600-6135
ISSN (online)	1600-6143
ISSN	1600-6135
DOI	10.1016/j.ajt.2022.12.008
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Zs.A 5542: Show issues

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Article ; Online: Recipient bone marrow-derived IL-17 receptor A-positive cells drive allograft fibrosis in a mouse intrapulmonary tracheal transplantation model.

Watanabe, Tatsuaki / Juvet, Stephen C / Boonstra, Kristen / Guan, Zehong / Joe, Betty / Teskey, Grace / Keshavjee, Shaf / Martinu, Tereza

Transplant immunology

2021 Volume 69, Page(s) 101467

Abstract: ... knockout mice. After engraftment, allogeneic IPTTs were performed using the chimeric and BALB/c mice ...

Abstract	IL-17A is implicated in the pathogenesis of chronic lung allograft dysfunction, which limits survival after lung transplantation. While many cells express the IL-17 receptor A (IL-17RA) which is the main receptor for IL-17A, the cellular targets of IL-17A in development of post-transplant fibrosis are unknown. The purpose of this study was to determine whether IL-17RA expression by donor or recipient structural or bone marrow (BM) cells is required for the development of allograft fibrosis in a mouse intrapulmonary tracheal transplantation (IPTT) model. BM chimeras were generated using C57BL/6 and IL-17RA-knockout mice. After engraftment, allogeneic IPTTs were performed using the chimeric and BALB/c mice as donors or recipients. This allowed us to assess the effect of IL-17RA deficiency in recipient BM, recipient structural, donor BM, or donor structural compartments separately. Tracheal grafts, the surrounding lung, and mediastinal lymph nodes were assessed 28 days after IPTT. Only recipient BM IL-17RA deficiency resulted in attenuation of tracheal graft obliteration. In the setting of recipient BM IL-17RA deficiency, T cells and neutrophils were decreased in mediastinal lymph nodes. Additionally, recipient BM IL-17RA deficiency was associated with increased B220
MeSH term(s)	Allografts ; Animals ; Bone Marrow ; Bone Marrow Transplantation ; Fibrosis ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Receptors, Interleukin-17
Chemical Substances	Receptors, Interleukin-17
Language	English
Publishing date	2021-09-20
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1160846-8
ISSN	1878-5492 ; 0966-3274
ISSN (online)	1878-5492
ISSN	0966-3274
DOI	10.1016/j.trim.2021.101467
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Zs.A 3784: Show issues

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Article ; Online: Lung transplantation for late-onset non-infectious chronic pulmonary complications of allogenic hematopoietic stem cell transplant.

Riddell, Peter / Vasudevan-Nampoothiri, Ram / Ma, Jin / Singer, Lianne G / Lipton, Jeff H / Juvet, Stephen C

Respiratory research

2021 Volume 22, Issue 1, Page(s) 101

Abstract: Background: Late onset non-infectious pulmonary complications (LONIPCs) following allogenic hematopoietic stem cell transplantation (allo-HSCT) confer a significant mortality risk. Lung transplantation (LTx) has the potential to provide survival benefit ...

Abstract	Background: Late onset non-infectious pulmonary complications (LONIPCs) following allogenic hematopoietic stem cell transplantation (allo-HSCT) confer a significant mortality risk. Lung transplantation (LTx) has the potential to provide survival benefit but the impact of prior allo-HSCT on post-LTx outcomes is not well studied. Methods: This retrospective, single-centre cohort study assessed the post-LTx outcomes of adults with LONIPCs of allo-HSCT. Outcomes of LTx for LONIPCs were compared to propensity-score matched LTx controls (n = 38, non-HSCT) and recipients of re-LTx (n = 70) for chronic lung allograft dysfunction (CLAD). Results: Nineteen patients underwent DLTx for LONIPCs of allo-HSCT between 2003 and 2019. Post-LTx survival was 50% at 5-years. Survival to 1-year post-LTx was similar to matched controls (p = 0.473). Survival, conditional on 1-year survival, was lower in the allo-HSCT cohort (p = 0.034). An increased risk of death due to infection was identified in the allo-HSCT cohort compared to matched controls (p = 0.003). Compared to re-LTx recipients, the allo-HSCT cohort had superior survival to 1-year post-LTx (p = 0.034) but conditional 1-year survival was similar (p = 0.145). Conclusion: This study identifies an increased risk of post-LTx mortality in recipients with previous allo-HSCT, associated with infection. It supports the hypothesis that allo-HSCT LTx recipients are relatively more immunosuppressed than patients undergoing LTx for other indications. Optimisation of post-LTx immunosuppressive and antimicrobial strategies to account for this finding should be considered.
MeSH term(s)	Adolescent ; Adult ; Biopsy ; Bronchoscopy ; Chronic Disease ; Female ; Follow-Up Studies ; Hematopoietic Stem Cell Transplantation/adverse effects ; Humans ; Lung/pathology ; Lung Transplantation/methods ; Male ; Middle Aged ; Postoperative Complications ; Primary Graft Dysfunction/diagnosis ; Primary Graft Dysfunction/etiology ; Primary Graft Dysfunction/surgery ; Propensity Score ; Retrospective Studies ; Risk Factors ; Time Factors ; Transplant Recipients ; Transplantation, Homologous/adverse effects ; Young Adult
Language	English
Publishing date	2021-04-07
Publishing country	England
Document type	Journal Article
ZDB-ID	2041675-1
ISSN	1465-993X ; 1465-9921
ISSN (online)	1465-993X
ISSN	1465-9921
DOI	10.1186/s12931-021-01699-8
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Article ; Online: Ex vivo

Miyamoto, Ei / Takahagi, Akihiro / Ohsumi, Akihiro / Martinu, Tereza / Hwang, David / Boonstra, Kristen M / Joe, Betty / Umana, Juan Mauricio / Bei, Ke F / Vosoughi, Daniel / Liu, Mingyao / Cypel, Marcelo / Keshavjee, Shaf / Juvet, Stephen C

The European respiratory journal

2022 Volume 59, Issue 4

Abstract: Background: Survival after lung transplantation (LTx) is hampered by uncontrolled inflammation and alloimmunity. Regulatory T-cells (Tregs) are being studied as a cellular therapy in solid organ transplantation. Whether these systemically administered ... ...

Abstract	Background: Survival after lung transplantation (LTx) is hampered by uncontrolled inflammation and alloimmunity. Regulatory T-cells (Tregs) are being studied as a cellular therapy in solid organ transplantation. Whether these systemically administered Tregs can function at the appropriate location and time is an important concern. We hypothesised that Methods: In a rat model, Wistar Kyoto (WKy) CD4 Results: Rat Tregs entered the lung parenchyma and retained suppressive function. Expanded Tregs had no adverse effect on donor lung physiology during EVLP; lung water as measured by wet-to-dry weight ratio was reduced by Treg therapy. The administered cells remained in the graft at 3 days post-transplant where they reduced activation of intra-graft effector CD4 Conclusions: Pre-transplant Treg administration can inhibit alloimmunity within the lung allograft at early time points post-transplant. Our organ-directed approach has potential for clinical translation.
MeSH term(s)	Animals ; Lung ; Lung Transplantation/adverse effects ; Perfusion/adverse effects ; Rats ; T-Lymphocytes, Regulatory ; Tissue Donors
Language	English
Publishing date	2022-04-14
Publishing country	England
Document type	Journal Article
ZDB-ID	639359-7
ISSN	1399-3003 ; 0903-1936
ISSN (online)	1399-3003
ISSN	0903-1936
DOI	10.1183/13993003.00798-2021
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