Ficolin A derived from local macrophages and neutrophils protects against lipopolysaccharide-induced acute lung injury by activating complement.
Complement
LPS
ficolin
innate immunity
lung injury
myeloid cells
Journal
Immunology and cell biology
ISSN: 1440-1711
Titre abrégé: Immunol Cell Biol
Pays: United States
ID NLM: 8706300
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
07
12
2019
revised:
22
04
2020
accepted:
23
04
2020
pubmed:
28
4
2020
medline:
25
8
2021
entrez:
28
4
2020
Statut:
ppublish
Résumé
Ficolins are important and widely distributed pattern recognition molecules that can induce lectin complement pathway activation and initiate the innate immune response. Although ficolins can bind lipopolysaccharide (LPS) in vitro, the sources, dynamic changes and roles of local ficolins in LPS-induced pulmonary inflammation and injury remain poorly understood. In this study, we established a ficolin knockout mouse model by clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9 (CRISPR/Cas9) technology, and used flow cytometry and hematoxylin and eosin staining to study the expressions and roles of local ficolins in LPS-induced pulmonary inflammation and injury. Our results show that besides ficolin B (FcnB), ficolin A (FcnA) is also expressed in leukocytes from the bone marrow, peripheral blood, lung and spleen. Further analyses showed that macrophages and neutrophils are the main sources of FcnA and FcnB, and T and B cells also express a small amount of FcnB. The intranasal administration of LPS induced local pulmonary inflammation with the increased recruitment of macrophages and neutrophils. LPS stimulation induced increased expression of FcnA and FcnB in neutrophils at the acute stage and in macrophages at the late stage. The severity of the lung injury and local inflammation of Fcna
Substances chimiques
Lectins
0
Lipopolysaccharides
0
Complement System Proteins
9007-36-7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
595-606Informations de copyright
© 2020 Australian and New Zealand Society for Immunology Inc.
Références
Beutler B, Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 2003; 3: 169-176.
Akira S, Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006; 124: 783-801.
Beutler B, Jiang Z, Georgel P, et al. Genetic analysis of host resistance: toll-like receptor signaling and immunity at large. Annu Rev Immunol 2006; 24: 353-389.
Speyer CL, Neff TA, Warner RL, et al. Regulatory effects of iNOS on acute lung inflammatory responses in mice. Am J Pathol 2003; 163: 2319-2328.
Knapp S, Florquin S, Golenbock DT, Van Der Poll T. Pulmonary lipopolysaccharide (LPS)-binding protein inhibits the LPS-induced lung inflammation in vivo. J Immunol 2006; 176: 3189-3195.
Jia X, Cao B, An Y, Zhang X, Wang C. Rapamycin ameliorates lipopolysaccharide-induced acute lung injury by inhibiting IL-1β and IL-18 production. Int Immunopharmacol 2019; 67: 211-219.
Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010; 11: 785-797.
Walport MJ. Complement. N Engl J Med 2001; 344: 1058-1066.
Triantafilou M, Hughes TR, Morgan BP, Triantafilou K. Complementing the inflammasome. Immunology 2016; 147: 152-164.
Dunkelberger JR, Song WC. Complement and its role in innate and adaptive immune responses. Cell Res 2010; 20: 34-50.
Lachmann PJ. The amplification loop of the complement pathways. Adv Immunol 2009; 104: 115-149.
Fujita T. Evolution of the lectin-complement pathway and its role in innate immunity. Nat Rev Immunol 2002; 2: 346-353.
Howard M, Farrar CA, Sacks SH. Structural and functional diversity of collectins and ficolins and their relationship to disease. Semin Immunopathol 2017; 40: 75-85.
Zhang XL, Ali MA. Ficolins: structure, function and associated diseases. In: Lambris JD ed. Current Topics in Complement II. New York, NY: Springer; 2008: 99-109.
Garred P, Genster N, Pilely K, et al. A journey through the lectin pathway of complement-MBL and beyond. Immunol Rev 2016; 274: 74-97.
Endo Y, Liu Y, Kanno K, Takahashi M, Matsushita M, Fujita T. Identification of the mouse H-ficolin gene as a pseudogene and orthology between mouse ficolins A/B and human L-/M-ficolins. Genomics 2004; 84: 737-744.
Hunold K, Weber-Steffens D, Runza VL, Jensenius JC, Mannel DN. Functional analysis of mouse ficolin-B and detection in neutrophils. Immunobiology 2012; 217: 982-985.
Liu Y, Endo Y, Homma S, Kanno K, Yaginuma H, Fujita T. Ficolin A and ficolin B are expressed in distinct ontogenic patterns and cell types in the mouse. Mol Immunol 2005; 42: 1265-1273.
Adler SC, Rosbjerg A, Hebbelstrup JB, Krogfelt KA, Garred P. The lectin complement pathway is involved in protection against Enteroaggregative Escherichia coli infection. Front Immunol 2018; 9: 1153-1164.
Genster N, Praestekjaer CE, Rosbjerg A, Pilely K, Cowland JB, Garred P. Ficolins promote fungal clearance in vivo and modulate the inflammatory cytokine response in host defense against Aspergillus fumigatus. J Innate Immun 2016; 8: 579-588.
Luo F, Sun X, Wang Y, et al. Ficolin-2 defends against virulent Mycobacteria tuberculosis infection in vivo, and its insufficiency is associated with infection in humans. PLoS One 2013; 8: e73859.
Boldt AB, Sanchez MI, Stahlke ER, et al. Susceptibility to leprosy is associated with M-ficolin polymorphisms. J Clin Immunol 2013; 33: 210-219.
Pan Q, Chen H, Wang F, et al. L-ficolin binds to the glycoproteins hemagglutinin and neuraminidase and inhibits influenza A virus infection both in vitro and in vivo. J Innate Immun 2012; 4: 312-324.
Ali Y, Lynch NJ, Haleem KS, et al. The lectin pathway of complement activation is a critical component of the innate immune response to pneumococcal infection. PLoS Pathog 2012; 8: e1002793.
Genster N, Ostrup O, Schjalm C, et al. Ficolins do not alter host immune responses to lipopolysaccharide-induced inflammation in vivo. Sci Rep 2017; 7: 3852.
Jarlhelt I, Genster N, Kirketerp MN, Skjoedt MO, Garred PT. The ficolin response to LPS challenge in mice. Mol Immunol 2019; 108: 121-127.
Plovsing RR, Berg RM, Munthe FL, et al. Alveolar recruitment of ficolin-3 in response to acute pulmonary inflammation in humans. Immunobiology 2016; 221: 690-697.
Endo Y, Matsushita M, Fujita T. New insights into the role of ficolins in the lectin pathway of innate immunity. Int Rev Cel Mol Bio 2015; 316: 49-110.
Weber SD, Hunold K, Kurschner J, et al. Immature mouse granulocytic myeloid cells are characterized by production of ficolin-B. Mol Immunol 2013; 56: 488-496.
Doi K, Leelahavanichkul A, Yuen PS, Star RA. Animal models of sepsis and sepsis-induced kidney injury. J Clin Invest 2009; 119: 2868-2878.
Buras JA, Holzmann B, Sitkovsky M. Animal models of sepsis: setting the stage. Nat Rev Drug Discov 2005; 4: 854-865.
Bolger MS, Ross DS, Jiang H, et al. Complement levels and activity in the normal and LPS-injured lung. Am J Physiol-Lung C 2007; 292: 748-759.
Drouin SM, Kildsgaard J, Haviland J, et al. Expression of the complement anaphylatoxin C3a and C5a receptors on bronchial epithelial and smooth muscle cells in models of sepsis and asthma. J Immunol 2001; 166: 2025-2032.
Bidula S, Sexton DW, Schelenz S. Ficolins and the recognition of pathogenic microorganisms: an overview of the innate immune response and contribution of single nucleotide polymorphisms. J Immunol Res 2019; 1-13. https://doi.org/10.1155/2019/3205072.
Endo Y, Takahashi M, Iwak D, et al. Mice deficient in ficolin, a lectin complement pathway recognition molecule, are susceptible to Streptococcus pneumoniae infection. J Immunol 2012; 189: 5860-5866.
Vassal SE, Lacroix M, Gout E, et al. Human L-ficolin recognizes phosphocholine moieties of pneumococcal teichoic acid. J Immunol 2014; 193: 5699-5708.
Verma A, White M, Vathipadiekal V, et al. Human H-Ficolin inhibits replication of seasonal and pandemic influenza A viruses. J Immunol 2012; 189: 2478-2487.
White MR, Tripathi S, Verma A, et al. Collectins, H-ficolin and LL-37 reduce influence viral replication in human monocytes and modulate virus-induced cytokine production. Innate Immun 2017; 23: 77-88.
Thiel S. Complement activating soluble pattern recognition molecules with collagen-like regions, mannan-binding lectin, ficolins and associated proteins. Mol Immunol 2007; 44: 3875-3888.
Seyfarth J, Garred P, Madsen HO. Extra-hepatic transcription of the human mannose-binding lectin gene (mbl2) and the MBL-associated serine protease 1-3 genes. Mol Immunol 2006; 43: 962-971.
Munthe FL, Hummelshoj T, Honore C, et al. Immunodeficiency associated with FCN3 mutation and ficolin-3 deficiency. N Engl J Med 2009; 360: 2637-2644.
Fujimori Y, Harumiya S, Fukumoto Y, et al. Molecular cloning and characterization of mouse ficolin-A. Biochem Biophys Res Commun 1998; 244: 796-800.
Liu Y, Endo Y, Iwaki D, et al. Human M-Ficolin is a secretory protein that activates the lectin complement pathway. J Immunol 2005; 175: 3150-3156.
Honoré C, Rørvig S, Munthe FL, et al. The innate pattern recognition molecule ficolin-1 is secreted by monocytes/macrophages and is circulating in human plasma. Mol Immunol 2008; 45: 2782-2789.