Microbiota in heart and lung transplantation: implications for innate-adaptive immune interface.
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:
01 12 2021
01 12 2021
Historique:
pubmed:
26
9
2021
medline:
9
11
2021
entrez:
25
9
2021
Statut:
ppublish
Résumé
Transplantation continues to be the only treatment option for end-stage organ failure when other interventions have failed. Although short-term outcomes have improved due to advances in perioperative care, long-term outcomes continue to be adversely affected by chronic rejection. Little is known about the role microbiota play in modulating alloimmune responses and potentially contributing to graft failure. Initial data have identified a correlation between specific changes of the recipient and/or donor microbiota and transplant outcomes. In this review, we will focus on recent findings concerning the complex interplay between microbiota and the innate immune system after heart and lung transplantation. Gut microbiome derangements in heart failure promote an inflammatory state and have lasting effects on the innate immune system, with an observed association between increased levels of microbiota-dependent metabolites and acute rejection after cardiac transplantation. The lung allograft microbiome interacts with components of the innate immune system, such as toll-like receptor signalling pathways, NKG2C+ natural killer cells and the NLRP3 inflammasome, to alter posttransplant outcomes, which may result in the development of chronic rejection. The innate immune system is influenced by alterations in the microbiome before and after heart and lung transplantation, thereby offering potential therapeutic targets for prolonging allograft survival.
Identifiants
pubmed: 34561360
doi: 10.1097/MOT.0000000000000923
pii: 00075200-202112000-00007
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
609-614Subventions
Organisme : NHLBI NIH HHS
ID : R01 HL094601
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL151078
Pays : United States
Informations de copyright
Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.
Références
Sandek A, Bauditz J, Swidsinski A, et al. Altered intestinal function in patients with chronic heart failure. J Am Coll Cardiol 2007; 50:1561–1569.
Luedde M, Winkler T, Heinsen FA, et al. Heart failure is associated with depletion of core intestinal microbiota. ESC Hear Fail 2017; 4:282–290.
Kamo T, Akazawa H, Suda W, et al. Dysbiosis and compositional alterations with aging in the gut microbiota of patients with heart failure. PLoS One 2017; 12:e0174099.
Peschel T, Schönauer M, Thiele H, et al. Invasive assessment of bacterial endotoxin and inflammatory cytokines in patients with acute heart failure. Eur J Heart Fail 2003; 5:609–614.
Sandek A, Bjarnason I, Volk HD, et al. Studies on bacterial endotoxin and intestinal absorption function in patients with chronic heart failure. Int J Cardiol 2012; 157:80–85.
Jenq RR, Taur Y, Devlin SM, et al. Intestinal blautia is associated with reduced death from graft-versus-host disease. Biol Blood Marrow Transplant 2015; 21:1373–1383.
Leonel AJ, Alvarez-Leite JI. Butyrate: implications for intestinal function. Curr Opin Clin Nutr Metab Care 2012; 15:474–479.
Pasini E, Aquilani R, Testa C, et al. Pathogenic gut flora in patients with chronic heart failure. JACC Hear Fail 2016; 4:220–227.
Ahmad AF, Dwivedi G, O’Gara F, et al. The gut microbiome and cardiovascular disease: current knowledge and clinical potential. Am J Physiol Heart Circ Physiol 2019; 317:H923–H938.
Yuzefpolskaya M, Bohn B, Nasiri M, et al. Gut microbiota, endotoxemia, inflammation, and oxidative stress in patients with heart failure, left ventricular assist device, and transplant. J Hear Lung Transplant 2020; 39:880–890.
Trøseid M, Mayerhofer CCK, Broch K, et al. The carnitine-butyrobetaine-TMAO pathway after cardiac transplant: Impact on cardiac allograft vasculopathy and acute rejection. J Hear Lung Transplant 2019; 38:1097–1103.
Bromberg JS, Hittle L, Xiong Y, et al. Gut microbiota-dependent modulation of innate immunity and lymph node remodeling affects cardiac allograft outcomes. JCI Insight 2018; 3:1–19.
Hayes D, Cherikh WS, Chambers DC, et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: twenty-second pediatric lung and heart-lung transplantation report: 2019; Focus theme: donor and recipient size match. J Hear Lung Transplant 2019; 38:1015–1027.
Kawashima M, Juvet SC. The role of innate immunity in the long-term outcome of lung transplantation. Ann Transl Med 2020; 8:412–1412.
Botha P, Archer L, Anderson RL, et al. Pseudomonas aeruginosa colonization of the allograft after lung transplantation and the risk of bronchiolitis obliterans syndrome. Transplantation 2008; 85:771–774.
Gottlieb J, Mattner F, Weissbrodt H, et al. Impact of graft colonization with gram-negative bacteria after lung transplantation on the development of bronchiolitis obliterans syndrome in recipients with cystic fibrosis. Respir Med 2009; 103:743–749.
Combs MP, Wheeler DS, Luth JE, et al. Lung microbiota predict chronic rejection in healthy lung transplant recipients: a prospective cohort study. Lancet Respir Med 2021; 9:601–612.
Kulkarni HS, Tsui K, Sunder S, et al. Pseudomonas aeruginosa and acute rejection independently increase the risk of donor-specific antibodies after lung transplantation. Am J Transplant 2020; 20:1028–1038.
Verleden SE, Vanaudenaerde BM, Emonds MP, et al. Donor-specific and -nonspecific HLA antibodies and outcome post lung transplantation. Eur Respir J 2017; 50:509–529.
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; 5:1–17.
Weigt SS, Elashoff RM, Huang C, et al. Aspergillus colonization of the lung allograft is a risk factor for bronchiolitis obliterans syndrome. Am J Transplant 2009; 9:1903–1911.
Young JC, Chehoud C, Bittinger K, et al. Viral metagenomics reveal blooms of anelloviruses in the respiratory tract of lung transplant recipients. Am J Transplant 2015; 15:200–209.
Blatter JA, Takahashi T, Mittler B, et al. Anellovirus dynamics are associated with primary graft dysfunction in lung transplantation. Transplant Direct 2020; 6:e521.
Bernasconi E, Pattaroni C, Koutsokera A, et al. Airway microbiota determines innate cell inflammatory or tissue remodeling profiles in lung transplantation. Am J Respir Crit Care Med 2016; 194:1252–1263.
Mouraux S, Bernasconi E, Pattaroni C, et al. Airway microbiota signals anabolic and catabolic remodeling in the transplanted lung. J Allergy Clin Immunol 2018; 141:718–729.e7.
Schott C, Weigt SS, Turturice BA, Metwally A, et al. Bronchiolitis obliterans syndrome susceptibility and the pulmonary microbiome. J Hear Lung Transplant 2018; 37:1131–1140.
Willner DL, Hugenholtz P, Yerkovich ST, et al. Reestablishment of recipient-associated microbiota in the lung allograft is linked to reduced risk of bronchiolitis obliterans syndrome. Am J Respir Crit Care Med 2013; 187:640–647.
Tanaka S, Gauthier JM, Terada Y, et al. Bacterial products in donor airways prevent the induction of lung transplant tolerance. Am J Transplant 2021; 21:353–361.
Akbarpour M, Lecuona E, Chiu SF, et al. Residual endotoxin induces primary graft dysfunction through ischemia/reperfusion-primed alveolar macrophages. J Clin Invest 2020; 140:4456–4469.
Evers A, Atanasova S, Fuchs-Moll G, et al. Adaptive and innate immune responses in a rat orthotopic lung transplant model of chronic lung allograft dysfunction. Transpl Int 2015; 28:95–107.
Yamamoto S, Nava RG, Zhu J, et al. Cutting edge: Pseudomonas aeruginosa abolishes established lung transplant tolerance by stimulating B7 expression on neutrophils. J Immunol 2012; 189:4221–4225.
Jungraithmayr W, Codarri L, Bouchaud G, et al. Cytokine complex-expanded natural killer cells improve allogeneic lung transplant function via depletion of donor dendritic cells. Am J Respir Crit Care Med 2013; 187:1349–1359.
Greenland JR, Jewell NP, Gottschall M, et al. Bronchoalveolar lavage cell immunophenotyping facilitates diagnosis of lung allograft rejection. Am J Transplant 2014; 14:831–840.
Fildes JE, Yonan N, Tunstall K, et al. Natural killer cells in peripheral blood and lung tissue are associated with chronic rejection after lung transplantation. J Hear Lung Transplant 2008; 27:203–207.
Calabrese DR, Chong T, Wang A, et al. NKG2C natural killer cells in bronchoalveolar lavage are associated with cytomegalovirus viremia and poor outcomes in lung allograft recipients. Transplantation 2019; 103:493–501.
Gregson AL, Wang X, Weigt SS, et al. Interaction between pseudomonas and CXC chemokines increases risk of bronchiolitis obliterans syndrome and death in lung transplantation. Am J Respir Crit Care Med 2013; 187:518–526.
Borthwick LA, Suwara MI, Carnell SC, et al. Pseudomonas aeruginosa induced airway epithelial injury drives fibroblast activation: a mechanism in chronic lung allograft dysfunction. Am J Transplant 2016; 16:1751–1765.
Weigt SS, Elashoff RM, Keane MP, et al. Altered levels of CC chemokines during pulmonary CMV predict BOS and mortality postlung transplantation. Am J Transplant 2008; 8:1512–1522.
Gugliandolo E, Fusco R, Ginestra G, et al. Involvement of TLR4 and PPAR-α receptors in host response and NLRP3 inflammasome activation, against pulmonary infection with Pseudomonas aeruginosa. Shock 2019; 51:221–227.
Xu KY, Tong S, Wu CY, et al. Nlrp3 inflammasome inhibitor MCC950 ameliorates obliterative bronchiolitis by inhibiting Th1/Th17 response and promoting Treg response after orthotopic tracheal transplantation in Mice. Transplantation 2020; 104:E151–E163.
D’amico R, Fusco R, Cordaro M, et al. Modulation of NLRP3 inflammasome through formyl peptide receptor 1 (Fpr-1) pathway as a new therapeutic target in bronchiolitis obliterans syndrome. Int J Mol Sci 2020; 21:1–17.