Update on the immunological mechanisms of primary graft dysfunction and chronic lung allograft dysfunction.
Journal
Current opinion in organ transplantation
ISSN: 1531-7013
Titre abrégé: Curr Opin Organ Transplant
Pays: United States
ID NLM: 9717388
Informations de publication
Date de publication:
17 Oct 2024
17 Oct 2024
Historique:
medline:
18
10
2024
pubmed:
18
10
2024
entrez:
18
10
2024
Statut:
aheadofprint
Résumé
Primary graft dysfunction (PGD) and chronic lung allograft dysfunction (CLAD) are the leading causes of graft loss in lung transplant recipients. The development of mouse lung transplant models has allowed for the genetic dissection of cellular and molecular pathways that prevent graft survival. This review provides an overview into recent mechanistic insights into PGD and CLAD. Mouse orthotopic lung transplant models and investigations of human lung transplant recipeints have revealed new molecular and cellular targets that promote PGD and CLAD. Donor and recipient-derived innate immune cells promote PGD and CLAD. PGD is driven by communication between classical monocytes and tissue-resident nonclassical monocytes activating alveolar macrophages to release chemokines that recruit neutrophils. Products of cell damage trigger neutrophil NET release, which together with NK cells, antibodies and complement, that further promote PGD. The development of CLAD involves circuits that activate B cells, CD8+ T cells, classical monocytes, and eosinophils. Effective targeted management of PGD and CLAD in lung transplant recipient to improve their long-term outcome remains a critical unmet need. Current mechanistic studies and therapeutic studies in mouse models and humans identify new possibilities for prevention and treatment.
Identifiants
pubmed: 39422603
doi: 10.1097/MOT.0000000000001175
pii: 00075200-990000000-00145
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.
Références
Valapour M, Lehr CJ, Schladt DP, et al. OPTN/SRTR 2022 annual data report: lung. Am J Transplant 2024; 24:S394–S456.
Snell GI, Yusen RD, Weill D, et al. Report of the ISHLT working group on primary lung graft dysfunction, part I: definition and grading—a 2016 consensus group statement of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 2017; 36:1097–1103.
Chacon-Alberty L, Fernandez R, Jindra P, et al. Primary graft dysfunction in lung transplantation: a review of mechanisms and future applications. Transplantation 2023; 107:1687–1697.
Kreisel D, Sugimoto S, Tietjens J, et al. Bcl3 prevents acute inflammatory lung injury in mice by restraining emergency granulopoiesis. J Clin Invest 2011; 121:265–276.
Sayah DM, Mallavia B, Liu F, et al. Neutrophil extracellular traps are pathogenic in primary graft dysfunction after lung transplantation. Am J Respir Crit Care Med 2015; 191:455–463.
Scozzi D, Wang X, Liao F, et al. Neutrophil extracellular trap fragments stimulate innate immune responses that prevent lung transplant tolerance. Am J Transplant 2019; 19:1011–1023.
Gao W, Zhao J, Kim H, et al. α1-Antitrypsin inhibits ischemia reperfusion-induced lung injury by reducing inflammatory response and cell death. J Heart Lung Transplant 2014; 33:309–315.
Iskender I, Sakamoto J, Nakajima D, et al. Human α1-antitrypsin improves early posttransplant lung function: Preclinical studies in a pig lung transplant model. J Heart Lung Transplant 2016; 35:913–921.
Gotzfried J, Smirnova NF, Morrone C, et al. Preservation with alpha(1)-antitrypsin improves primary graft function of murine lung transplants. J Heart Lung Transplant 2018; 37:1021–1028.
Nakata K, Okazaki M, Shimizu D, et al. Protective effects of anti-HMGB1 monoclonal antibody on lung ischemia reperfusion injury in mice. Biochem Biophys Res Commun 2021; 573:164–170.
Entezari M, Javdan M, Antoine DJ, et al. Inhibition of extracellular HMGB1 attenuates hyperoxia-induced inflammatory acute lung injury. Redox Biol 2014; 2:314–322.
Mallavia B, Liu F, Lefrancais E, et al. Mitochondrial DNA stimulates TLR9-dependent neutrophil extracellular trap formation in primary graft dysfunction. Am J Respir Cell Mol Biol 2020; 62:364–372.
Scozzi D, Ibrahim M, Liao F, et al. Mitochondrial damage-associated molecular patterns released by lung transplants are associated with primary graft dysfunction. Am J Transplant 2019; 19:1464–1477.
Patel AA, Zhang Y, Fullerton JN, et al. The fate and lifespan of human monocyte subsets in steady state and systemic inflammation. J Exp Med 2017; 214:1913–1923.
Zheng Z, Chiu S, Akbarpour M, et al. Donor pulmonary intravascular nonclassical monocytes recruit recipient neutrophils and mediate primary lung allograft dysfunction. Sci Transl Med 2017; 9:eaal4508.
Hanna RN, Carlin LM, Hubbeling HG, et al. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C- monocytes. Nat Immunol 2011; 12:778–785.
Querrey M, Chiu S, Lecuona E, et al. CD11b suppresses TLR activation of nonclassical monocytes to reduce primary graft dysfunction after lung transplantation. J Clin Invest 2022; 132:e157262.
Kurihara C, Lecuona E, Wu Q, et al. Crosstalk between nonclassical monocytes and alveolar macrophages mediates transplant ischemia-reperfusion injury through classical monocyte recruitment. JCI Insight 2021; 6:147282.
Hsiao HM, Fernandez R, Tanaka S, et al. Spleen-derived classical monocytes mediate lung ischemia-reperfusion injury through IL-1beta. J Clin Invest 2018; 128:2833–2847.
Li W, Terada Y, Tyurina YY, et al. Necroptosis triggers spatially restricted neutrophil-mediated vascular damage during lung ischemia reperfusion injury. Proc Natl Acad Sci USA 2022; 119:e2111537119.
Calabrese DR, Tsao T, Magnen M, et al. NKG2D receptor activation drives primary graft dysfunction severity and poor lung transplantation outcomes. JCI Insight 2022; 7:e164603.
Calabrese DR, Aminian E, Mallavia B, et al. Natural killer cells activated through NKG2D mediate lung ischemia-reperfusion injury. J Clin Invest 2021; 131:137047.
Santos J, Wang P, Shemesh A, et al. CCR5 drives NK cell-associated airway damage in pulmonary ischemia-reperfusion injury. JCI Insight 2023; 8:e173716.
Iwata T, Philipovskiy A, Fisher AJ, et al. Antitype V collagen humoral immunity in lung transplant primary graft dysfunction. J Immunol 2008; 181:5738–5747.
Bharat A, Saini D, Steward N, et al. Antibodies to self-antigens predispose to primary lung allograft dysfunction and chronic rejection. Ann Thorac Surg 2010; 90:1094–1101.
Kulkarni HS, Ramphal K, Ma L, et al. Local complement activation is associated with primary graft dysfunction after lung transplantation. JCI Insight 2020; 5:138358.
Li C, Patel K, Tu Z, et al. A novel injury site-natural antibody targeted complement inhibitor protects against lung transplant injury. Am J Transplant 2021; 21:2067–2078.
Yang W, Cerier EJ, Nunez-Santana FL, et al. IL-1beta-dependent extravasation of preexisting lung-restricted autoantibodies during lung transplantation activates complement and mediates primary graft dysfunction. J Clin Invest 2022; 132:e157975.
Verleden GM, Vos R, Verleden SE, et al. Survival determinants in lung transplant patients with chronic allograft dysfunction. Transplantation 2011; 92:703–708.
Sato M, Waddell TK, Wagnetz U, et al. Restrictive allograft syndrome (RAS): a novel form of chronic lung allograft dysfunction. J Heart Lung Transplant 2011; 30:735–742.
Verleden GM, Glanville AR, Lease ED, et al. Chronic lung allograft dysfunction: definition, diagnostic criteria, and approaches to treatment—a consensus report from the Pulmonary Council of the ISHLT. J Heart Lung Transplant 2019; 38:493–503.
Daud SA, Yusen RD, Meyers BF, et al. Impact of immediate primary lung allograft dysfunction on bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2007; 175:507–513.
Wong W, Johnson B, Cheng PC, et al. Primary graft dysfunction grade 3 following pediatric lung transplantation is associated with chronic lung allograft dysfunction. J Heart Lung Transplant 2023; 42:669–678.
Witt CA, Gaut JP, Yusen RD, et al. Acute antibody-mediated rejection after lung transplantation. J Heart Lung Transplant 2013; 32:1034–1040.
Levine DJ, Glanville AR, Aboyoun C, et al. Antibody-mediated rejection of the lung: a consensus report of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 2016; 35:397–406.
Girnita AL, Duquesnoy R, Yousem SA, et al. HLA-specific antibodies are risk factors for lymphocytic bronchiolitis and chronic lung allograft dysfunction. Am J Transplant 2005; 5:131–138.
Keller M, Yang S, Ponor L, et al. Preemptive treatment of de novo donor-specific antibodies in lung transplant patients reduces subsequent risk of chronic lung allograft dysfunction or death. Am J Transplant 2023; 23:559–564.
Ehrsam JP, Schuurmans MM, Laager M, et al. Recipient comorbidities for prediction of primary graft dysfunction, chronic allograft dysfunction and survival after lung transplantation. Transpl Int 2022; 35:10451.
Marty PK, Yetmar ZA, Gerberi DJ, et al. Risk factors and outcomes of nontuberculous mycobacteria infection in lung transplant recipients: a systematic review and meta-analysis. J Heart Lung Transplant 2023; 42:264–274.
Gallagher HM, Sarwar G, Tse T, et al. Erratic tacrolimus exposure, assessed using the standard deviation of trough blood levels, predicts chronic lung allograft dysfunction and survival. J Heart Lung Transplant 2015; 34:1442–1448.
Royer PJ, Olivera-Botello G, Koutsokera A, et al. Chronic lung allograft dysfunction: a systematic review of mechanisms. Transplantation 2016; 100:1803–1814.
Meloni F, Vitulo P, Bianco AM, et al. Regulatory CD4+CD25+ T cells in the peripheral blood of lung transplant recipients: correlation with transplant outcome. Transplantation 2004; 77:762–766.
Bhorade SM, Chen H, Molinero L, et al. Decreased percentage of CD4+FoxP3+ cells in bronchoalveolar lavage from lung transplant recipients correlates with development of bronchiolitis obliterans syndrome. Transplantation 2010; 90:540–546.
Gregson AL, Hoji A, Palchevskiy V, et al. Protection against bronchiolitis obliterans syndrome is associated with allograft CCR7+ CD45RA- T regulatory cells. PLoS One 2010; 5:e11354.
Durand M, Lacoste P, Danger R, et al. High circulating CD4(+)CD25(hi)FOXP3(+) T-cell sub-population early after lung transplantation is associated with development of bronchiolitis obliterans syndrome. J Heart Lung Transplant 2018; 37:770–781.
Liu Z, Liao F, Zhu J, et al. Reprogramming alveolar macrophage responses to TGF-beta reveals CCR2+ monocyte activity that promotes bronchiolitis obliterans syndrome. J Clin Invest 2022; 132:e159229.
Liu Z, Liao F, Scozzi D, et al. An obligatory role for club cells in preventing obliterative bronchiolitis in lung transplants. JCI Insight 2019; 5:124732.
Li W, Bribriesco AC, Nava RG, et al. Lung transplant acceptance is facilitated by early events in the graft and is associated with lymphoid neogenesis. Mucosal Immunol 2012; 5:544–554.
Li W, Gauthier JM, Higashikubo R, et al. Bronchus-associated lymphoid tissue-resident Foxp3+ T lymphocytes prevent antibody-mediated lung rejection. J Clin Invest 2019; 129:556–568.
Tanaka S, Gauthier JM, Fuchs A, et al. IL-22 is required for the induction of bronchus-associated lymphoid tissue in tolerant lung allografts. Am J Transplant 2020; 20:1251–1261.
Savage TM, Fortson KT, de Los Santos-Alexis K, et al. Amphiregulin from regulatory T cells promotes liver fibrosis and insulin resistance in nonalcoholic steatohepatitis. Immunity 2024; 57:303–318. e6.
Snyder ME, Moghbeli K, Bondonese A, et al. Modulation of tissue resident memory T cells by glucocorticoids after acute cellular rejection in lung transplantation. J Exp Med 2022; 219:e20212059.
Calabrese DR, Ekstrand CA, Yellamilli S, et al. Macrophage and CD8 T cell discordance are associated with acute lung allograft dysfunction progression. J Heart Lung Transplant 2024; 43:1074–1086.
Misumi K, Wheeler DS, Aoki Y, et al. Humoral immune responses mediate the development of a restrictive phenotype of chronic lung allograft dysfunction. JCI Insight 2020; 5:136533.
Noorchashm H, Reed AJ, Rostami SY, et al. B cell-mediated antigen presentation is required for the pathogenesis of acute cardiac allograft rejection. J Immunol 2006; 177:7715–7722.
Todd JL, Weber JM, Kelly FL, et al. BAL fluid eosinophilia associates with chronic lung allograft dysfunction risk: a multicenter study. Chest 2023; 164:670–681.
Mei Z, Khalil MA, Guo Y, et al. Eosinophils restrain humoral alloimmunity after lung transplantation. JCI Insight 2024; 9:e168911.
Misharin AV, Morales-Nebreda L, Reyfman PA, et al. Monocyte-derived alveolar macrophages drive lung fibrosis and persist in the lung over the life span. J Exp Med 2017; 214:2387–2404.
Yamaguchi Y, Mann Dm Fau-Ruoslahti E, Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 1990; 346:281–284.