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Porcine Alveolar Macrophages’ Nitric Oxide Synthase-Mediated Generation of Nitric Oxide Exerts Important Defensive Effects against Glaesserella parasuis Infection

by Qi Cao 1,2,3,4, Huan Wang 1,2,3,4, Wenbin Wei 1,2,3,4, Yujin Lv 1,2,3,5, Zhao Wen 1,2,3,4, Xiaojuan Xu 1,2,3,4, Xuwang Cai 1,2,3,4, Huanchun Chen 1,2,3,4 and Xiangru Wang 1,2,3,4,*
1
State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, Hubei, China
2
Key Laboratory of Preventive Veterinary Medicine in Hubei Province, The Cooperative Innovation Center for Sustainable Pig Production, Wuhan 430070, Hubei, China
3
Key Laboratory of Development of Veterinary Diagnostic Products, Ministry of Agriculture of the People’s Republic of China, Wuhan 430070, Hubei, China
4
International Research Center for Animal Disease, Ministry of Science and Technology of the People’s Republic of China, Wuhan 430070, Hubei, China
5
College of Veterinary Medicine, Henan University of Animal Husbandry and Economy, Zhengzhou 471000, Henan, China
*
Author to whom correspondence should be addressed.
Pathogens 2019, 8(4), 234; https://doi.org/10.3390/pathogens8040234
Received: 22 October 2019 / Revised: 8 November 2019 / Accepted: 11 November 2019 / Published: 13 November 2019
Glaesserella parasuis is a habitual bacterium of pigs’ upper respiratory tracts. Its infection initiates with the invasion and colonization of the lower respiratory tracts of pigs, and develops as the bacteria survive host pulmonary defenses and clearance by alveolar macrophages. Alveolar macrophage-derived nitric oxide (NO) is recognized as an important mediator that exerts antimicrobial activity as well as immunomodulatory effects. In this study, we investigated the effects and the signaling pathway of NO generation in porcine alveolar macrophages 3D4/21 during G. parasuis infection. We demonstrated a time and dose-dependent generation of NO in 3D4/21 cells by G. parasuis, and showed that NO production required bacterial viability and nitric oxide synthase 2 upregulation, which was largely contributed by G. parasuis-induced nuclear factor-κB signaling’s activation. Moreover, the porcine alveolar macrophage-derived NO exhibited prominent bacteriostatic effects against G. parasuis and positive host immunomodulation effects by inducing the production of cytokines and chemokines during infection. G. parasuis in turn, selectively upregulated several nitrate reductase genes to better survive this NO stress, revealing a battle of wits during the bacteria–host interactions. To our knowledge, this is the first direct demonstration of NO production and its anti-infection effects in alveolar macrophages with G. parasuis infection. View Full-Text
Keywords: Glaesserella parasuis; porcine alveolar macrophages; nitric oxide; NOS2; NF-κB signaling Glaesserella parasuis; porcine alveolar macrophages; nitric oxide; NOS2; NF-κB signaling
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Cao, Q.; Wang, H.; Wei, W.; Lv, Y.; Wen, Z.; Xu, X.; Cai, X.; Chen, H.; Wang, X. Porcine Alveolar Macrophages’ Nitric Oxide Synthase-Mediated Generation of Nitric Oxide Exerts Important Defensive Effects against Glaesserella parasuis Infection. Pathogens 2019, 8, 234.

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