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Degraded neutrophil extracellular traps promote the growth of Actinobacillus pleuropneumoniae.
Cell Death Dis 2019; 10(9):657CD

Abstract

Actinobacillus pleuropneumoniae (A.pp) causes severe pneumonia associated with enormous economic loss in pigs. Peracute diseased pigs die in <24 h with pneumonia. Neutrophils are the prominent innate immune cell in this infection that massively infiltrate the infected lung. Here we show that neutrophils release neutrophil extracellular traps (NETs) as response to A.pp infection. Numerous NET-markers were identified in bronchoalveolar lavage fluid (BALF) of A.pp-infected piglets in vivo, however, most NET fibers are degraded. Importantly, A.pp is able to enhance its growth rate in the presence of NETs that have been degraded by nucleases efficiently. A.pp itself releases no nuclease, but we identified host nucleases as sources that degrade NETs after A.pp infection. Furthermore, the nucleases of co-infecting pathogens like Streptococcus suis increase growth of A.pp in presence of porcine NETs. Thus, A.pp is not only evading the antimicrobial activity of NETs, A.pp is rather additionally using parts of NETs as growth factor thereby taking advantage of host nucleases as DNase1 or nucleases of co-infecting bacteria, which degrade NETs. This effect can be diminished by inhibiting the bacterial adenosine synthase indicating that degraded NETs serve as a source for NAD, which is required by A.pp for its growth. A similar phenotype was found for the human pathogen Haemophilus (H.) influenzae and its growth in the presence of human neutrophils. H. influenzae benefits from host nucleases in the presence of neutrophils. These data shed light on the detrimental effects of NETs during host immune response against certain bacterial species that require and/or efficiently take advantage of degraded DNA material, which has been provided by host nuclease or nucleases of other co-infecting bacteria, as growth source.

Authors+Show Affiliations

Department of Physiological Chemistry, University of Veterinary Medicine Hannover, Hannover, Germany. nicole.de.buhr@tiho-hannover.de. Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, Germany. nicole.de.buhr@tiho-hannover.de.Department of Physiological Chemistry, University of Veterinary Medicine Hannover, Hannover, Germany. Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, Germany.Department of Physiological Chemistry, University of Veterinary Medicine Hannover, Hannover, Germany. Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, Germany.Department of Physiological Chemistry, University of Veterinary Medicine Hannover, Hannover, Germany. Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, Germany.Clinic for Swine, Small Ruminants, Forensic Medicine and Ambulatory Service, University of Veterinary Medicine Hannover, Hannover, Germany.Institute of Medical Microbiology, University Hospital Münster, Münster, Germany.Clinic for Swine, Small Ruminants, Forensic Medicine and Ambulatory Service, University of Veterinary Medicine Hannover, Hannover, Germany.Institute for Microbiology, University of Veterinary Medicine Hannover, Hannover, Germany.Field Station for Epidemiology, University of Veterinary Medicine Hannover, Bakum, Germany. Isabel.hennig-pauka@tiho-hannover.de.Department of Physiological Chemistry, University of Veterinary Medicine Hannover, Hannover, Germany. maren.von.koeckritz-blickwede@tiho-hannover.de. Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Hannover, Germany. maren.von.koeckritz-blickwede@tiho-hannover.de.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31506432

Citation

de Buhr, Nicole, et al. "Degraded Neutrophil Extracellular Traps Promote the Growth of Actinobacillus Pleuropneumoniae." Cell Death & Disease, vol. 10, no. 9, 2019, p. 657.
de Buhr N, Bonilla MC, Pfeiffer J, et al. Degraded neutrophil extracellular traps promote the growth of Actinobacillus pleuropneumoniae. Cell Death Dis. 2019;10(9):657.
de Buhr, N., Bonilla, M. C., Pfeiffer, J., Akhdar, S., Schwennen, C., Kahl, B. C., ... von Köckritz-Blickwede, M. (2019). Degraded neutrophil extracellular traps promote the growth of Actinobacillus pleuropneumoniae. Cell Death & Disease, 10(9), p. 657. doi:10.1038/s41419-019-1895-4.
de Buhr N, et al. Degraded Neutrophil Extracellular Traps Promote the Growth of Actinobacillus Pleuropneumoniae. Cell Death Dis. 2019 Sep 10;10(9):657. PubMed PMID: 31506432.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Degraded neutrophil extracellular traps promote the growth of Actinobacillus pleuropneumoniae. AU - de Buhr,Nicole, AU - Bonilla,Marta C, AU - Pfeiffer,Jessica, AU - Akhdar,Silke, AU - Schwennen,Cornelia, AU - Kahl,Barbara C, AU - Waldmann,Karl-Heinz, AU - Valentin-Weigand,Peter, AU - Hennig-Pauka,Isabel, AU - von Köckritz-Blickwede,Maren, Y1 - 2019/09/10/ PY - 2019/04/11/received PY - 2019/08/12/accepted PY - 2019/08/03/revised PY - 2019/9/12/entrez PY - 2019/9/12/pubmed PY - 2019/9/12/medline SP - 657 EP - 657 JF - Cell death & disease JO - Cell Death Dis VL - 10 IS - 9 N2 - Actinobacillus pleuropneumoniae (A.pp) causes severe pneumonia associated with enormous economic loss in pigs. Peracute diseased pigs die in <24 h with pneumonia. Neutrophils are the prominent innate immune cell in this infection that massively infiltrate the infected lung. Here we show that neutrophils release neutrophil extracellular traps (NETs) as response to A.pp infection. Numerous NET-markers were identified in bronchoalveolar lavage fluid (BALF) of A.pp-infected piglets in vivo, however, most NET fibers are degraded. Importantly, A.pp is able to enhance its growth rate in the presence of NETs that have been degraded by nucleases efficiently. A.pp itself releases no nuclease, but we identified host nucleases as sources that degrade NETs after A.pp infection. Furthermore, the nucleases of co-infecting pathogens like Streptococcus suis increase growth of A.pp in presence of porcine NETs. Thus, A.pp is not only evading the antimicrobial activity of NETs, A.pp is rather additionally using parts of NETs as growth factor thereby taking advantage of host nucleases as DNase1 or nucleases of co-infecting bacteria, which degrade NETs. This effect can be diminished by inhibiting the bacterial adenosine synthase indicating that degraded NETs serve as a source for NAD, which is required by A.pp for its growth. A similar phenotype was found for the human pathogen Haemophilus (H.) influenzae and its growth in the presence of human neutrophils. H. influenzae benefits from host nucleases in the presence of neutrophils. These data shed light on the detrimental effects of NETs during host immune response against certain bacterial species that require and/or efficiently take advantage of degraded DNA material, which has been provided by host nuclease or nucleases of other co-infecting bacteria, as growth source. SN - 2041-4889 UR - https://www.unboundmedicine.com/medline/citation/31506432/Degraded_neutrophil_extracellular_traps_promote_the_growth_of_Actinobacillus_pleuropneumoniae L2 - http://dx.doi.org/10.1038/s41419-019-1895-4 DB - PRIME DP - Unbound Medicine ER -