Inflammasome activation and CCR2-mediated monocyte-derived dendritic cell recruitment restrict Legionella pneumophila infection

被引:7
作者
Ataide, Marco A. [1 ]
Manin, Graziele Z. [1 ]
Oliveira, Samuel S. [1 ]
Guerra, Rhanoica O. [1 ]
Zamboni, Dario S. [1 ]
机构
[1] Univ Sao Paulo, Ribeirao Preto Med Sch, Dept Cell Biol, Ribeirao Preto, SP, Brazil
基金
巴西圣保罗研究基金会;
关键词
CCR2; innate immunity; Legionella; monocyte-derived dendritic cell; NLRC4-inflammasome; ALVEOLAR MACROPHAGES; LEGIONNAIRES-DISEASE; MOUSE MACROPHAGES; RECOGNITION; FLAGELLIN; LONGBEACHAE; NLRC4; DIFFERENTIATION; CONTRIBUTES; PYROPTOSIS;
D O I
10.1002/eji.202249985
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Flagellin-induced NAIP/NLRC4 inflammasome activation and pyroptosis are critical events restricting Legionella pneumophila infection. However, the cellular and molecular dynamics of the in vivo responses against this bacterium are still unclear. We have found temporal coordination of two independent innate immunity pathways in controlling Legionella infection, the inflammasome activation and the CCR2-mediated Mo-DC recruitment. Inflammasome activation was an important player at the early stage of infection by lowering the numbers of bacteria for an efficient bacterial clearance conferred by the Mo-DC at the late stage of the infection. Mo-DC emergence highly depended on CCR2-signaling and dispensed inflammasome activation and pyroptosis. Also, Mo-DC compartment did not rely on the inflammasome machinery to deliver proper immune responses and was the most abundant cytokine-producing among the monocyte-derived cells in the infected lung. Importantly, when the CCR2- and NLRC4-dependent axes of response were simultaneously ablated, we observed an aggravated bacterial burden in the lung of infected mice. Taken together, we showed that inflammasome activation and CCR2-mediated immune response interplay in distinct pathways to restrict pulmonary bacterial infection. These findings extend our understanding of the in vivo integration and cooperation of different innate immunity arms in controlling infectious agents.
引用
收藏
页数:13
相关论文
共 47 条
[1]   Murine Hind Limb Long Bone Dissection and Bone Marrow Isolation [J].
Amend, Sarah R. ;
Valkenburg, Kenneth C. ;
Pienta, Kenneth J. .
JOVE-JOURNAL OF VISUALIZED EXPERIMENTS, 2016, (110)
[2]   Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf [J].
Amer, Amal ;
Franchi, Luigi ;
Kanneganti, Thirumala-Devi ;
Body-Malapel, Mathilde ;
Ozoren, Nesrin ;
Brady, Graham ;
Meshinchi, Sasha ;
Jagirdar, Rajesh ;
Gewirtz, Andrew ;
Akira, Shizuo ;
Nunez, Gabriel .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2006, 281 (46) :35217-35223
[3]   Genetic susceptibility and caspase activation in mouse and human macrophages are distinct for Legionella longbeachae and L-pneumophila [J].
Asare, Rexford ;
Santic, Marina ;
Gobin, Ivana ;
Doric, Mijenko ;
Suttles, Jill ;
Graham, James E. ;
Price, Christopher D. ;
Abu Kwaik, Yousef .
INFECTION AND IMMUNITY, 2007, 75 (04) :1933-1945
[4]   Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice [J].
Boring, L ;
Gosling, J ;
Chensue, SW ;
Kunkel, SL ;
Farese, RV ;
Broxmeyer, HE ;
Charo, IF .
JOURNAL OF CLINICAL INVESTIGATION, 1997, 100 (10) :2552-2561
[5]   Cooperation between Monocyte-Derived Cells and Lymphoid Cells in the Acute Response to a Bacterial Lung Pathogen [J].
Brown, Andrew S. ;
Yang, Chao ;
Fung, Ka Yee ;
Bachem, Annabell ;
Bourges, Dorothee ;
Bedoui, Sammy ;
Hartland, Elizabeth L. ;
van Driel, Ian R. .
PLOS PATHOGENS, 2016, 12 (06)
[6]   Inflammasomes: mechanism of assembly, regulation and signalling [J].
Broz, Petr ;
Dixit, Vishva M. .
NATURE REVIEWS IMMUNOLOGY, 2016, 16 (07) :407-420
[7]   Neutrophils and Ly6Chi monocytes collaborate in generating an optimal cytokine response that protects against pulmonary Legionella pneumophila infection [J].
Casson, Cierra N. ;
Doerner, Jessica L. ;
Copenhaver, Alan M. ;
Ramirez, Jasmine ;
Holmgren, Alicia M. ;
Boyer, Mark A. ;
Siddarthan, Ingharan J. ;
Rouhanifard, Sara H. ;
Raj, Arjun ;
Shin, Sunny .
PLOS PATHOGENS, 2017, 13 (04)
[8]   Analysis of the Legionella longbeachae Genome and Transcriptome Uncovers Unique Strategies to Cause Legionnaires' Disease [J].
Cazalet, Christel ;
Gomez-Valero, Laura ;
Rusniok, Christophe ;
Lomma, Mariella ;
Dervins-Ravault, Delphine ;
Newton, Hayley J. ;
Sansom, Fiona M. ;
Jarraud, Sophie ;
Zidane, Nora ;
Ma, Laurence ;
Bouchier, Christiane ;
Etienne, Jerome ;
Hartland, Elizabeth L. ;
Buchrieser, Carmen .
PLOS GENETICS, 2010, 6 (02)
[9]   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 [J].
Cerqueira, Daiane M. ;
Pereira, Marcelo S. F. ;
Silva, Alexandre L. N. ;
Cunha, Larissa D. ;
Zamboni, Dario S. .
JOURNAL OF IMMUNOLOGY, 2015, 195 (05) :2303-2311
[10]   Microbial Stimulation Fully Differentiates Monocytes to DC-SIGN/CD209+ Dendritic Cells for Immune T Cell Areas [J].
Cheong, Cheolho ;
Matos, Ines ;
Choi, Jae-Hoon ;
Dandamudi, Durga Bhavani ;
Shrestha, Elina ;
Longhi, M. Paula ;
Jeffrey, Kate L. ;
Anthony, Robert M. ;
Kluger, Courtney ;
Nchinda, Godwin ;
Koh, Hyein ;
Rodriguez, Anthony ;
Idoyaga, Juliana ;
Pack, Maggi ;
Velinzon, Klara ;
Park, Chae Gyu ;
Steinman, Ralph M. .
CELL, 2010, 143 (03) :416-429