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And in Vivo Species in Mouse Macrophages Legionella Caspase-1 but Not Caspase-11 Is Required for NLRC4-Mediated Pyroptosis and Restriction of Infection by Flagellated Legionella Species in Mouse Macrophages This information is current as and In Vivo of September 29, 2021. Daiane M. Cerqueira, Marcelo S. F. Pereira, Alexandre L. N. Silva, Larissa D. Cunha and Dario S. Zamboni J Immunol 2015; 195:2303-2311; Prepublished online 31 July 2015; Downloaded from doi: 10.4049/jimmunol.1501223 http://www.jimmunol.org/content/195/5/2303 http://www.jimmunol.org/ References This article cites 47 articles, 19 of which you can access for free at: http://www.jimmunol.org/content/195/5/2303.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 29, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2015 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Caspase-1 but Not Caspase-11 Is Required for NLRC4-Mediated Pyroptosis and Restriction of Infection by Flagellated Legionella Species in Mouse Macrophages and In Vivo Daiane M. Cerqueira, Marcelo S. F. Pereira, Alexandre L. N. Silva, Larissa D. Cunha, and Dario S. Zamboni Gram-negative bacteria from the Legionella genus are intracellular pathogens that cause a severe form of pneumonia called Legionnaires’ disease. The bacteria replicate intracellularly in macrophages, and the restriction of bacterial replication by these cells is critical for host resistance. The activation of the NAIP5/NLRC4 inflammasome, which is readily triggered in response to Downloaded from bacterial flagellin, is essential for the restriction of bacterial replication in murine macrophages. Once activated, this inflamma- some induces pore formation and pyroptosis and facilitates the restriction of bacterial replication in macrophages. Because investigations related to the NLRC4-mediated restriction of Legionella replication were performed using mice double deficient for caspase-1 and caspase-11, we assessed the participation of caspase-1 and caspase-11 in the functions of the NLRC4 inflam- masome and the restriction of Legionella replication in macrophages and in vivo. By using several species of Legionella and mice singly deficient for caspase-1 or caspase-11, we demonstrated that caspase-1 but not caspase-11 was required for pore formation, http://www.jimmunol.org/ pyroptosis, and restriction of Legionella replication in macrophages and in vivo. By generating F1 mice in a mixed 129 3 C57BL/6 background deficient (129 3 Casp-112/2) or sufficient (129 3 C57BL/6) for caspase-11 expression, we found that caspase-11 was dispensable for the restriction of Legionella pneumophila replication in macrophages and in vivo. Thus, although caspase-11 participates in flagellin-independent noncanonical activation of the NLRP3 inflammasome, it is dispensable for the activities of the NLRC4 inflammasome. In contrast, functional caspase-1 is necessary and sufficient to trigger flagellin/NLRC4-mediated restric- tion of Legionella spp. infection in macrophages and in vivo. The Journal of Immunology, 2015, 195: 2303–2311. egionella pneumophila is a Gram-negative bacterium that individuals, and the elderly) (1, 2). Once it reaches the lung, causes a severe pneumonia named Legionnaires’ disease. L. pneumophila is able to infect alveolar macrophages using the by guest on September 29, 2021 L L. pneumophila is commonly found in soil and aquatic same subset of genes used for amoeba infection. Immediately after environments, where it infects a variety of protozoa, including encountering the alveolar macrophages, bacterial effector proteins several species of free-living amoebae (reviewed in Refs. 1, 2). are delivered into the macrophage cytoplasm through the type IV Human contamination often occurs by inhalation of contaminated secretion system Dot/Icm. One of the many function of these ef- water droplets containing Legionella and/or infected amoebae. fector proteins is the subversion of the normal trafficking of the Legionnaires’ disease generally affects individuals in risk groups Legionella-containing vacuole (LCV). Thus, vesicles from the (i.e., patients with chronic lung diseases, immunocompromised endoplasmic reticulum are recruited to the LCV to create a fa- vorable niche for bacterial replication inside the macrophages Department of Cell Biology, School of Medicine of Ribeira˜o Preto, University of Sa˜o (reviewed in Refs. 3–5). Paulo, Ribeira˜o Preto, Sa˜o Paulo 14049-900, Brazil In contrast to human cells, macrophages from most mouse Received for publication June 1, 2015. Accepted for publication July 7, 2015. strains are resistant to L. pneumophila infection, with the excep- This work was supported by the Pew Program in Biomedical Sciences, Conselho tion of the A/J mouse strain (6). The A/J strain has a mutation in Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico/Instituto Nacional de Cieˆncia the naip5/birc1e gene that encodes a receptor belonging to the e Tecnologia em Vacinas, Fundac¸a˜o de Amparo ao Ensino, Pesquisa e Assisteˆncia do Hospital das Clı´nicas da Faculdade de Medicina de Ribeira˜o Preto da Universidade Nod-like receptor (NLR) family (7, 8). These preliminary obser- de Sa˜o Paulo, and by Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo Grants vations launched a successful line of investigations using 2013/08216-2 and 2014/04684-4 (to D.S.Z.). D.M.C. (2012/16941-6), M.S.F.P. L. pneumophila and its mutants as models to dissect the biology of (2011/22617-4), A.L.N.S. (2012/15932-3), and L.D.C. (2012/14456-3) are supported by fellowships from the Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo. the NLR family members (reviewed in Refs. 9, 10). The initial D.S.Z. is a Research Fellow of the Conselho Nacional de Desenvolvimento Cientı´fico NLR report demonstrated that NAIP5 was linked to caspase-1 e Tecnolo´gico. activation in a process that was similar to NLRC4, which is an- Address correspondence and reprint requests to Prof. Dario S. Zamboni, Depar- tamento de Biologia Celular e Molecular e Bioagentes Patogeˆnicos, Faculdade other member of the NLR family (11). These conclusions were 2 2 de Medicina de Ribeira˜o Preto, Universidade de Sa˜o Paulo, Avenida Bandeir- validated by the generation of Naip5 / mice (12). Additionally, antes 3900, Ribeira˜oPreto,Sa˜o Paulo 14049-900. Brazil. E-mail address: studies with Salmonella Typhimurium and L. pneumophila [email protected] revealed that the bacterial flagellin functioned as an agonist for the Abbreviations used in this article: BCYE, buffered charcoal–yeast extract; BMDM, bone marrow–derived macrophage; LCV, Legionella-containing vacuole; LDH, lac- NAIP5/NLRC4 signaling platform (13–17). Moreover, this inflam- tate dehydrogenase; MOI, multiplicity of infection; NLR, Nod-like receptor; WT, masomewasreportedtobethekeyforrestrictionofL. pneumophila wild-type. replication in mouse macrophages and in vivo (11, 13, 16–19). Copyright Ó 2015 by The American Association of Immunologists, Inc. 0022-1767/15/$25.00 Once activated, this inflammasome promotes the formation of www.jimmunol.org/cgi/doi/10.4049/jimmunol.1501223 2304 CASPASE-1–MEDIATED RESTRICTION OF LEGIONELLA INFECTION pores in the macrophage membrane (16, 17, 20); this process grown at 37˚C in BCYE agar plates. After 48 h, they were diluted in sterile culminates in the induction of an inflammatory form of cell water and the OD at 600 nm was measured in a spectrophotometer (Bio- death termed pyroptosis (reviewed in Ref. 21). The mechanisms Photometer; Eppendorf, Hamburg, Germany) to determine the bacterial concentration in the solution. underlying NLRC4-mediated host resistance to L. pneumophila infection are still unclear, but pyroptosis has been proposed to Western blot analysis be directly involved in host resistance (22). Furthermore, the Bone marrow-derived macrophages (BMDMs) were prepared from the in- NLRC4 inflammasome was reported to trigger the restriction of dicated mice and differentiated in L929 cell–conditioned medium as pre- bacterial replication by additional processes dependent on fla- viously described (29). BMDMs were replated in RPMI 1640 medium supplemented with 10% (v/v) FBS and 5% (v/v) L929 cell–conditioned gellin but independent of caspase-1 and caspase-11 (18). medium in 48-well plates (1 3 106 per well). These BMDMs were infected Another pathway for caspase-1 activation has been reported with bacterial strains at a multiplicity of infection (MOI) of 10 for the in- in addition to the flagellin-mediated activation of the NLRC4 dicated times. Cell lysates and supernatants were subjected to SDS-PAGE inflammasome. Several Gram-negative bacteria were demonstrated analysis and Western blotting. Primary Abs used included a rat monoclonal to be able to trigger caspase-1 activation via a process that required against the p20 subunit of caspase-1 (Genentech, clone 4B4) and a rat monoclonal against caspase-11 (Abcam, Cambridge, MA), both at a 1:500 caspase-11 (the so-called noncanonical pathway for the activation dilution. Loading control blot was performed using a rabbit polyclonal anti- of the NLRP3/ASC/caspase-1 inflammasome) (23, 24). This path- actin Ab (Sigma-Aldrich, St. Louis, MO, catalog no. A2066) at a 1:1000 way effectively accounted for caspase-1 activation in response to dilution. An HRP-conjugated secondary Ab (Kirkegaard and Perry Labo- L. pneumophila (25). Active caspase-11 triggers the formation of ratories, Gaithersburg, MD) was used for detection at a 1:3000 dilution.
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