Neuraminidase is a host-directed approach to regulate neutrophil responses in sepsis and COVID-19.
COVID-19
SARS-CoV-2
metalloproteinase-9
neuraminidase
neutrophil
oseltamivir
sepsis
sialic acid
zanamivir
Journal
British journal of pharmacology
ISSN: 1476-5381
Titre abrégé: Br J Pharmacol
Pays: England
ID NLM: 7502536
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
29
07
2022
received:
16
03
2022
accepted:
16
08
2022
medline:
3
5
2023
pubmed:
17
12
2022
entrez:
16
12
2022
Statut:
ppublish
Résumé
Neutrophil overstimulation plays a crucial role in tissue damage during severe infections. Because pathogen-derived neuraminidase (NEU) stimulates neutrophils, we investigated whether host NEU can be targeted to regulate the neutrophil dysregulation observed in severe infections. The effects of NEU inhibitors on lipopolysaccharide (LPS)-stimulated neutrophils from healthy donors or COVID-19 patients were determined by evaluating the shedding of surface sialic acids, cell activation, and reactive oxygen species (ROS) production. Re-analysis of single-cell RNA sequencing of respiratory tract samples from COVID-19 patients also was carried out. The effects of oseltamivir on sepsis and betacoronavirus-induced acute lung injury were evaluated in murine models. Oseltamivir and zanamivir constrained host NEU activity, surface sialic acid release, cell activation, and ROS production by LPS-activated human neutrophils. Mechanistically, LPS increased the interaction of NEU1 with matrix metalloproteinase 9 (MMP-9). Inhibition of MMP-9 prevented LPS-induced NEU activity and neutrophil response. In vivo, treatment with oseltamivir fine-tuned neutrophil migration and improved infection control as well as host survival in peritonitis and pneumonia sepsis. NEU1 also is highly expressed in neutrophils from COVID-19 patients, and treatment of whole-blood samples from these patients with either oseltamivir or zanamivir reduced neutrophil overactivation. Oseltamivir treatment of intranasally infected mice with the mouse hepatitis coronavirus 3 (MHV-3) decreased lung neutrophil infiltration, viral load, and tissue damage. These findings suggest that interplay of NEU1-MMP-9 induces neutrophil overactivation. In vivo, NEU may serve as a host-directed target to dampen neutrophil dysfunction during severe infections.
Sections du résumé
BACKGROUND AND PURPOSE
Neutrophil overstimulation plays a crucial role in tissue damage during severe infections. Because pathogen-derived neuraminidase (NEU) stimulates neutrophils, we investigated whether host NEU can be targeted to regulate the neutrophil dysregulation observed in severe infections.
EXPERIMENTAL APPROACH
The effects of NEU inhibitors on lipopolysaccharide (LPS)-stimulated neutrophils from healthy donors or COVID-19 patients were determined by evaluating the shedding of surface sialic acids, cell activation, and reactive oxygen species (ROS) production. Re-analysis of single-cell RNA sequencing of respiratory tract samples from COVID-19 patients also was carried out. The effects of oseltamivir on sepsis and betacoronavirus-induced acute lung injury were evaluated in murine models.
KEY RESULTS
Oseltamivir and zanamivir constrained host NEU activity, surface sialic acid release, cell activation, and ROS production by LPS-activated human neutrophils. Mechanistically, LPS increased the interaction of NEU1 with matrix metalloproteinase 9 (MMP-9). Inhibition of MMP-9 prevented LPS-induced NEU activity and neutrophil response. In vivo, treatment with oseltamivir fine-tuned neutrophil migration and improved infection control as well as host survival in peritonitis and pneumonia sepsis. NEU1 also is highly expressed in neutrophils from COVID-19 patients, and treatment of whole-blood samples from these patients with either oseltamivir or zanamivir reduced neutrophil overactivation. Oseltamivir treatment of intranasally infected mice with the mouse hepatitis coronavirus 3 (MHV-3) decreased lung neutrophil infiltration, viral load, and tissue damage.
CONCLUSION AND IMPLICATIONS
These findings suggest that interplay of NEU1-MMP-9 induces neutrophil overactivation. In vivo, NEU may serve as a host-directed target to dampen neutrophil dysfunction during severe infections.
Identifiants
pubmed: 36526272
doi: 10.1111/bph.16013
pmc: PMC9877938
doi:
Substances chimiques
Oseltamivir
20O93L6F9H
Zanamivir
L6O3XI777I
Neuraminidase
EC 3.2.1.18
Matrix Metalloproteinase 9
EC 3.4.24.35
Reactive Oxygen Species
0
Lipopolysaccharides
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1460-1481Subventions
Organisme : Howard Hughes Medical Institute
ID : 55007412
Pays : United States
Informations de copyright
© 2022 British Pharmacological Society.
Références
Abdulkhalek, S., Amith, S. R., Franchuk, S. L., Jayanth, P., Guo, M., Finlay, T., Gilmour, A., Guzzo, C., Gee, K., Beyaert, R., & Szewczuk, M. R. (2011). Neu1 sialidase and matrix metalloproteinase-9 cross-talk is essential for toll-like receptor activation and cellular signaling. Journal of Biological Chemistry, 286(42), 36532-36549. https://doi.org/10.1074/jbc.M111.237578
Alexander, S. P., Cosentino, B. J., Schooley, R. L., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Pawson, A. J., Southan, C., Davies, J. A., Annett, S., Boison, D., Burns, K. E., Dessauer, C., Gertsch, J., Helsby, N. A., Izzo, A. A., … Wong, S. S. (2021). The Concise Guide to PHARMACOLOGY 2021/22: Enzymes. British Journal of Pharmacology, 178(Suppl 1), S313-S411. https://doi.org/10.1111/bph.15542
Alves-Filho, J. C., Spiller, F., & Cunha, F. Q. (2010). Neutrophil paralysis in sepsis. Shock, 34, 15-21. https://doi.org/10.1097/SHK.0b013e3181e7e61b
Amith, S. R., Jayanth, P., Franchuk, S., Finlay, T., Seyrantepe, V., Beyaert, R., Pshezhetsky, A. V., & Szewczuk, M. R. (2010). Neu1 desialylation of sialyl α-2,3-linked β-galactosyl residues of TOLL-like receptor 4 is essential for receptor activation and cellular signaling. Cellular Signaling, 22, 314-324. https://doi.org/10.1016/j.cellsig.2009.09.038
Amith, S. R., Jayanth, P., Franchuk, S., Siddiqui, S., Seyrantepe, V., Gee, K., Basta, S., Beyaert, R., Pshezhetsky, A. V., & Szewczuk, M. R. (2009). Dependence of pathogen molecule-induced toll-like receptor activation and cell function on Neu1 sialidase. Glycoconjugate Journal, 26, 1197-1212. https://doi.org/10.1007/s10719-009-9239-8
Andrade, A. C. D. S. P., Campolina-Silva, G. H., Queiroz-Junior, C. M., de Oliveira, L. C., Lacerda, L. S. B., Gaggino, J. C. P., de Souza, F. R. O., de Meira Chaves, I., Passos, I. B., Teixeira, D. C., Bittencourt-Silva, P. G., Valadão, P. A. C., Rossi-Oliveira, L., Antunes, M. M., Figueiredo, A. F. A., Wnuk, N. T., Temerozo, J. R., Ferreira, A. C., Cramer, A., … Costa, V. V. (2021). A biosafety level 2 mouse model for studying betacoronavirus-induced acute lung damage and systemic manifestations. Journal of Virology, 95(22), e0127621. https://doi.org/10.1128/JVI.01276-21
Arora, D. J. S., & Henrichon, M. (1994). Superoxide anion production in influenza protein-activated NADPH oxidase of human polymorphonuclear leukocytes. The Journal of Infectious Diseases, 169, 1129-1133. https://doi.org/10.1093/infdis/169.5.1129
Blander, J. M., & Medzhitov, R. (2004). Regulation of phagosome maturation by signals from toll-like receptors. Science, 304, 1014-1018. https://doi.org/10.1126/science.1096158
Butler, C. C., van der Velden, A. W., Bongard, E., Saville, B. R., Holmes, J., Coenen, S., Cook, J., Francis, N. A., Lewis, R. J., Godycki-Cwirko, M., Llor, C., Chlabicz, S., Lionis, C., Seifert, B., Sundvall, P. D., Colliers, A., Aabenhus, R., Bjerrum, L., Jonassen Harbin, N., … Verheij, T. J. (2020). Oseltamivir plus usual care versus usual care for influenza-like illness in primary care: An open-label, pragmatic, randomised controlled trial. The Lancet, 395, 42-52. https://doi.org/10.1016/S0140-6736(19)32982-4
Cass, L. M., Efthymiopoulos, C., & Bye, A. (1999). Pharmacokinetics of zanamivir after intravenous, oral, inhaled or intranasal administration to healthy volunteers. Clinical Pharmacokinetics, 36(Suppl 1), 1-11.
Cassini-Vieira, P., Moreira, C. F., da Silva, M. F., & da Silva Barcelos, L. (2015). Estimation of wound tissue neutrophil and macrophage accumulation by measuring myeloperoxidase (MPO) and N-acetyl-β-d-glucosaminidase (NAG) activities. Bioprotocols, 5, e1662.
Chang, Y.-C., Uchiyama, S., Varki, A., & Nizet, V. (2012). Leukocyte inflammatory responses provoked by pneumococcal sialidase. MBio, 3, e00220-e00211.
Chen, G.-Y., Brown, N. K., Wu, W., Khedri, Z., Yu, H., Chen, X., van de Vlekkert, D., D'Azzo, A., Zheng, P., & Liu, Y. (2014). Broad and direct interaction between TLR and Siglec families of pattern recognition receptors and its regulation by Neu1. eLife, 3, e04066. https://doi.org/10.7554/eLife.04066
Chen, L., Long, X., Xu, Q., Tan, J., Wang, G., Cao, Y., Wei, J., Luo, H., Zhu, H., Huang, L., Meng, F., Huang, L., Wang, N., Zhou, X., Zhao, L., Chen, X., Mao, Z., Chen, C., Li, Z., … Zhou, J. (2020). Elevated serum levels of S100A8/A9 and HMGB1 at hospital admission are correlated with inferior clinical outcomes in COVID-19 patients. Cellular & Molecular Immunology, 17(9), 992-994. https://doi.org/10.1038/s41423-020-0492-x
Chiba, S. (2021). Effect of early oseltamivir on outpatients without hypoxia with suspected COVID-19. Wiener Klinische Wochenschrift, 133(7-8), 292-297.
Chou, E. H., Mann, S., Hsu, T.-C., Hsu, W.-T., Liu, C. C.-Y., Bhakta, T., Hassani, D. M., & Lee, C. C. (2020). Incidence, trends, and outcomes of infection sites among hospitalizations of sepsis: A nationwide study. PLoS ONE, 15(1), e0227752. https://doi.org/10.1371/journal.pone.0227752
Chua, R. L., Lukassen, S., Trump, S., Hennig, B. P., Wendisch, D., Pott, F., Debnath, O., Thürmann, L., Kurth, F., Völker, M. T., Kazmierski, J., Timmermann, B., Twardziok, S., Schneider, S., Machleidt, F., Müller-Redetzky, H., Maier, M., Krannich, A., Schmidt, S., … Eils, R. (2020). COVID-19 severity correlates with airway epithelium-immune cell interactions identified by single-cell analysis. Nature Biotechnology, 38(8), 970-979. https://doi.org/10.1038/s41587-020-0602-4
Cross, A. S., Sakarya, S., Rifat, S., Held, T. K., Drysdale, B.-E., Grange, P. A., Cassels, F. J., Wang, L. X., Stamatos, N., Farese, A., Casey, D., Powell, J., Bhattacharjee, A. K., Kleinberg, M., & Goldblum, S. E. (2003). Recruitment of murine neutrophils in vivo through endogenous sialidase activity. Journal of Biological Chemistry, 278(6), 4112-4120. https://doi.org/10.1074/jbc.M207591200
Cross, A. S., & Wright, D. G. (1991). Mobilization of sialidase from intracellular stores to the surface of human neutrophils and its role in stimulated adhesion responses of these cells. Journal of Clinical Investigation, 88, 2067-2076. https://doi.org/10.1172/JCI115536
Curtis, M., Alexander, S., Cirino, G., Docherty, J., George, C., Giembycz, M., Hoyer, D., Insel, P., Izzo, A., Ji, Y., MacEwan, D., Sobey, C., Stanford, S., Teixeira, M., Wonnacott, S., & Ahluwalia, A. (2018). Experimental design and analysis and their reporting II: Updated and simplified guidance for authors and peer reviewers. British Journal of Pharmacology, 175(7), 987-993. https://doi.org/10.1111/BPH.14153
Davies, B. E. (2010). Pharmacokinetics of oseltamivir: An oral antiviral for the treatment and prophylaxis of influenza in diverse populations. Journal of Antimicrobial Chemotherapy, 65(Suppl 2), ii5-ii10. https://doi.org/10.1093/jac/dkq015
Dib, K., Tikhonova, I. G., Ivetic, A., & Schu, P. (2017). The cytoplasmic tail of L-selectin interacts with the adaptor-protein complex AP-1 subunit μ1A via a novel basic binding motif. Journal of Biological Chemistry, 292, 6703-6714. https://doi.org/10.1074/jbc.M116.768598
Duffy, D., Rouilly, V., Libri, V., Hasan, M., Beitz, B., David, M., Urrutia, A., Bisiaux, A., LaBrie, S. T., Dubois, A., Boneca, I. G., Delval, C., Thomas, S., Rogge, L., Schmolz, M., Quintana-Murci, L., Albert, M. L., Abel, L., Alcover, A., … Albert, M. L. (2014). Functional analysis via standardized whole-blood stimulation systems defines the boundaries of a healthy immune response to complex stimuli. Immunity, 40(3), 436-450. https://doi.org/10.1016/j.immuni.2014.03.002
Feng, C., Stamatos, N. M., Dragan, A. I., Medvedev, A., Whitford, M., Zhang, L., Song, C., Rallabhandi, P., Cole, L., Nhu, Q. M., Vogel, S. N., Geddes, C. D., & Cross, A. S. (2012). Sialyl residues modulate LPS-mediated signaling through the toll-like receptor 4 complex. PLoS ONE, 7(4), e32359. https://doi.org/10.1371/journal.pone.0032359
Feng, C., Zhang, L., Almulki, L., Faez, S., Whitford, M., Hafezi-Moghadam, A., & Cross, A. S. (2011). Endogenous PMN sialidase activity exposes activation epitope on CD11b/CD18 which enhances its binding interaction with ICAM-1. Journal of Leukocyte Biology, 90(2), 313-321. https://doi.org/10.1189/jlb.1210708
Glanz, V. Y., Myasoedova, V. A., Grechko, A. V., & Orekhov, A. N. (2019). Sialidase activity in human pathologies. European Journal of Pharmacology, 842, 345-350. https://doi.org/10.1016/j.ejphar.2018.11.014
Guan, W., Ni, Z., Hu, Y., Liang, W., Ou, C., He, J., Liu, L., Shan, H., Lei, C. L., Hui, D. S. C., Du, B., Li, L. J., Zeng, G., Yuen, K. Y., Chen, R. C., Tang, C. L., Wang, T., Chen, P. Y., Xiang, J., … China Medical Treatment Expert Group for Covid-19. (2020). Clinical characteristics of coronavirus disease 2019 in China. New England Journal of Medicine, 382(18), 1708-1720. https://doi.org/10.1056/NEJMoa2002032
Guo, Q., Zhao, Y., Li, J., Liu, J., Yang, X., Guo, X., Kuang, M., Xia, H., Zhang, Z., Cao, L., Luo, Y., Bao, L., Wang, X., Wei, X., Deng, W., Wang, N., Chen, L., Chen, J., Zhu, H., … You, F. (2021). Induction of alarmin S100A8/A9 mediates activation of aberrant neutrophils in the pathogenesis of COVID-19. Cell Host & Microbe, 29(2), 222-235.e4. https://doi.org/10.1016/j.chom.2020.12.016
Henricks, P. A., Van Erne-van der Tol, M. E., & Verhoef, J. (1982). Partial removal of sialic acid enhances phagocytosis and the generation of superoxide and chemiluminescence by polymorphonuclear leukocytes. Journal of Immunology, 129, 745-750.
Jutila, M. A., Rott, L., Berg, E. L., & Butcher, E. C. (1989). Function and regulation of the neutrophil MEL-14 antigen in vivo: Comparison with LFA-1 and MAC-1. Journal of Immunology, 143, 3318-3324.
Knibbs, R. N., Goldstein, I. J., Ratcliffe, R. M., & Shibuya, N. (1991). Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. Journal of Biological Chemistry, 266, 83-88. https://doi.org/10.1016/S0021-9258(18)52405-4
Kuri-Cervantes, L., Pampena, M. B., Meng, W., Rosenfeld, A. M., Ittner, C. A. G., Weisman, A. R., Agyekum, R. S., Mathew, D., Baxter, A. E., Vella, L. A., Kuthuru, O., Apostolidis, S. A., Bershaw, L., Dougherty, J., Greenplate, A. R., Pattekar, A., Kim, J., Han, N., Gouma, S., … Betts, M. R. (2020). Comprehensive mapping of immune perturbations associated with severe COVID-19. Science Immunology, 5(49), eabd7114. https://doi.org/10.1126/sciimmunol.abd7114
Leliefeld, P. H. C., Wessels, C. M., Leenen, L. P. H., Koenderman, L., & Pillay, J. (2016). The role of neutrophils in immune dysfunction during severe inflammation. Critical Care, 20, 73.
Lilley, E., Stanford, S. C., Kendall, D. E., Alexander, S. P. H., Cirino, G., Docherty, J. R., George, C. H., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Sobey, C. G., Stefanska, B., Stephens, G., Teixeira, M., & Ahluwalia, A. (2020). ARRIVE 2.0 and the British Journal of Pharmacology: Updated guidance for 2020. British Journal of Pharmacology, 177, 3611-3616. https://doi.org/10.1111/bph.15178
Lipničanová, S., Chmelová, D., Ondrejovič, M., Frecer, V., & Miertuš, S. (2020). Diversity of sialidases found in the human body-A review. International Journal of Biological Macromolecules, 148, 857-868. https://doi.org/10.1016/j.ijbiomac.2020.01.123
Liu, J., Zhang, S., Wu, Z., Shang, Y., Dong, X., Li, G., Zhang, L., Chen, Y., Ye, X., Du, H., Liu, Y., Wang, T., Huang, S., Chen, L., Wen, Z., Qu, J., & Chen, D. (2020). Clinical outcomes of COVID-19 in Wuhan, China: A large cohort study. Annals of Intensive Care, 10(1), 99. https://doi.org/10.1186/s13613-020-00706-3
Macauley, M. S., Crocker, P. R., & Paulson, J. C. (2014). Siglec-mediated regulation of immune cell function in disease. Nature Reviews Immunology, 14, 653-666. https://doi.org/10.1038/nri3737
Messerer, D. A. C., Vidoni, L., Erber, M., Stratmann, A. E. P., Bauer, J. M., Braun, C. K., Hug, S., Adler, A., Nilsson Ekdahl, K., Nilsson, B., Barth, E., Radermacher, P., & Huber-Lang, M. (2020). Animal-free human whole blood sepsis model to study changes in innate immunity. Frontiers in Immunology, 11, 571992. https://doi.org/10.3389/fimmu.2020.571992
Mills, E. L., Debets-Ossenkopp, Y., Verbrugh, H. A., & Verhoef, J. (1981). Initiation of the respiratory burst of human neutrophils by influenza virus. Infection and Immunity, 32, 1200-1205. https://doi.org/10.1128/iai.32.3.1200-1205.1981
Mittal, M., Siddiqui, M. R., Tran, K., Reddy, S. P., & Malik, A. B. (2014). Reactive oxygen species in inflammation and tissue injury. Antioxidants & Redox Signaling, 20, 1126-1167. https://doi.org/10.1089/ars.2012.5149
Mócsai, A. (2013). Diverse novel functions of neutrophils in immunity, inflammation, and beyond. Journal of Experimental Medicine, 210, 1283-1299. https://doi.org/10.1084/jem.20122220
Movsisyan, L. D., & Macauley, M. S. (2020). Structural advances of Siglecs: Insight into synthetic glycan ligands for immunomodulation. Organic and Biomolecular Chemistry, 18, 5784-5797. https://doi.org/10.1039/D0OB01116A
Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macleod, M., … Würbel, H. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biology, 18(7), e3000410. https://doi.org/10.1371/journal.pbio.3000410
Petri, B., Phillipson, M., & Kubes, P. (2008). The physiology of leukocyte recruitment: An in vivo perspective. Journal of Immunology, 180, 6439-6446. https://doi.org/10.4049/jimmunol.180.10.6439
Pshezhetsky, A. V., & Hinek, A. (2011). Where catabolism meets signalling: Neuraminidase 1 as a modulator of cell receptors. Glycoconjugate Journal, 28, 441-452. https://doi.org/10.1007/s10719-011-9350-5
Rhodes, A., Evans, L. E., Alhazzani, W., Levy, M. M., Antonelli, M., Ferrer, R., Kumar, A., Sevransky, J. E., Sprung, C. L., Nunnally, M. E., Rochwerg, B., Rubenfeld, G. D., Angus, D. C., Annane, D., Beale, R. J., Bellinghan, G. J., Bernard, G. R., Chiche, J. D., Coopersmith, C., … Dellinger, R. P. (2017). Surviving Sepsis Campaign: International guidelines for management of sepsis and septic shock: 2016. Intensive Care Medicine, 43(3), 304-377. https://doi.org/10.1007/s00134-017-4683-6
Rifat, S., Kang, T. J., Mann, D., Zhang, L., Puche, A. C., Stamatos, N. M., Goldblum, S. E., Brossmer, R., & Cross, A. S. (2008). Expression of sialyltransferase activity on intact human neutrophils. Journal of Leukocyte Biology, 84(4), 1075-1081. https://doi.org/10.1189/jlb.0706462
Rittirsch, D., Huber-Lang, M. S., Flierl, M. A., & Ward, P. A. (2009). Immunodesign of experimental sepsis by cecal ligation and puncture. Nature Protocols, 4, 31-36. https://doi.org/10.1038/nprot.2008.214
Sakarya, S. (2004). Mobilization of neutrophil sialidase activity desialylates the pulmonary vascular endothelial surface and increases resting neutrophil adhesion to and migration across the endothelium. Glycobiology, 14, 481-494. https://doi.org/10.1093/glycob/cwh065
Schmidt, T., Zündorf, J., Grüger, T., Brandenburg, K., Reiners, A.-L., Zinserling, J., & Schnitzler, N. (2012). CD66b overexpression and homotypic aggregation of human peripheral blood neutrophils after activation by a gram-positive stimulus. Journal of Leukocyte Biology, 91(5), 791-802. https://doi.org/10.1189/jlb.0911483
Schulte-Schrepping, J., Reusch, N., Paclik, D., Baßler, K., Schlickeiser, S., Zhang, B., Krämer, B., Krammer, T., Brumhard, S., Bonaguro, L., de Domenico, E., Wendisch, D., Grasshoff, M., Kapellos, T. S., Beckstette, M., Pecht, T., Saglam, A., Dietrich, O., Mei, H. E., … Ziebuhr, J. (2020). Severe COVID-19 is marked by a dysregulated myeloid cell compartment. Cell, 182(6), 1419-1440.e23. https://doi.org/10.1016/j.cell.2020.08.001
Segal, A. W. (2005). How neutrophils kill microbes. Annual Review of Immunology, 23, 197-223. https://doi.org/10.1146/annurev.immunol.23.021704.115653
Sheu, C.-C., Gong, M. N., Zhai, R., Chen, F., Bajwa, E. K., Clardy, P. F., Gallagher, D. C., Thompson, B. T., & Christiani, D. C. (2010). Clinical characteristics and outcomes of sepsis-related vs non-sepsis-related ARDS. Chest, 138(3), 559-567. https://doi.org/10.1378/chest.09-2933
Silvin, A., Chapuis, N., Dunsmore, G., Goubet, A.-G., Dubuisson, A., Derosa, L., Almire, C., Hénon, C., Kosmider, O., Droin, N., Rameau, P., Catelain, C., Alfaro, A., Dussiau, C., Friedrich, C., Sourdeau, E., Marin, N., Szwebel, T. A., Cantin, D., … Solary, E. (2020). Elevated calprotectin and abnormal myeloid cell subsets discriminate severe from mild COVID-19. Cell, 182(6), 1401-1418.e18. https://doi.org/10.1016/j.cell.2020.08.002
Smutova, V., Albohy, A., Pan, X., Korchagina, E., Miyagi, T., Bovin, N., Cairo, C. W., & Pshezhetsky, A. V. (2014). Structural basis for substrate specificity of mammalian neuraminidases. PLoS ONE, 9(9), e106320. https://doi.org/10.1371/journal.pone.0106320
Sônego, F., Castanheira, F. V., Ferreira, R. G., Kanashiro, A., Leite, C. A., Nascimento, D. C., Colon, D. F., Borges, V. D., Alves-Filho, J. C., & Cunha, F. Q. (2016). Paradoxical roles of the neutrophil in sepsis: Protective and deleterious. Frontiers in Immunology, 7, 1-7.
Spiller, F., Carlos, D., Souto, F. O., de Freitas, A., Soares, F. S., Vieira, S. M., Paula, F. J. A., Alves-Filho, J. C., & Cunha, F. Q. (2012). α1-Acid glycoprotein decreases neutrophil migration and increases susceptibility to sepsis in diabetic mice. Diabetes, 61(6), 1584-1591. https://doi.org/10.2337/db11-0825
Spiller, F., Orrico, M. I. L., Nascimento, D. C., Czaikoski, P. G., Souto, F. O., Alves-Filho, J. C., Freitas, A., Carlos, D., Montenegro, M. F., Neto, A. F., Ferreira, S. H., Rossi, M. A., Hothersall, J. S., Assreuy, J., & Cunha, F. Q. (2010). Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. American Journal of Respiratory and Critical Care Medicine, 182(3), 360-368. https://doi.org/10.1164/rccm.200907-1145OC
Steevels, T. A. M., & Meyaard, L. (2011). Immune inhibitory receptors: Essential regulators of phagocyte function. European Journal of Immunology, 41, 575-587. https://doi.org/10.1002/eji.201041179
Suzuki, H., Kurita, T., & Kakinuma, K. (1982). Effects of neuraminidase on O2 consumption and release of O2 and H2O2 from phagocytosing human polymorphonuclear leukocytes. Blood, 60, 446-453. https://doi.org/10.1182/blood.V60.2.446.446
Tan, J., Yuan, Y., Xu, C., Song, C., Liu, D., Ma, D., & Gao, Q. (2021). A retrospective comparison of drugs against COVID-19. Virus Research, 294, 198262. https://doi.org/10.1016/j.virusres.2020.198262
Tan, Q., Duan, L., Ma, Y., Wu, F., Huang, Q., Mao, K., Xiao, W., Xia, H., Zhang, S., Zhou, E., Ma, P., Song, S., Li, Y., Zhao, Z., Sun, Y., Li, Z., Geng, W., Yin, Z., & Jin, Y. (2020). Is oseltamivir suitable for fighting against COVID-19: In silico assessment, in vitro and retrospective study. Bioorganic Chemistry, 104, 104257. https://doi.org/10.1016/j.bioorg.2020.104257
Varki, A. (2008). Sialic acids in human health and disease. Trends in Molecular Medicine, 14, 351-360. https://doi.org/10.1016/j.molmed.2008.06.002
Varki, A., & Gagneux, P. (2012). Multifarious roles of sialic acids in immunity. Annals of the New York Academy of Sciences, 1253, 16-36. https://doi.org/10.1111/j.1749-6632.2012.06517.x
Veras, F. P., Pontelli, M. C., Silva, C. M., Toller-Kawahisa, J. E., de Lima, M., Nascimento, D. C., Schneider, A. H., Caetité, D., Tavares, L. A., Paiva, I. M., Rosales, R., Colón, D., Martins, R., Castro, I. A., Almeida, G. M., Lopes, M. I. F., Benatti, M. N., Bonjorno, L. P., Giannini, M. C., … Cunha, F. Q. (2020). SARS-CoV-2-triggered neutrophil extracellular traps mediate COVID-19 pathology. Journal of Experimental Medicine, 217(12), e20201129. https://doi.org/10.1084/jem.20201129
Vimr, E. R., & Troy, F. A. (1985). Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. Journal of Bacteriology, 164, 845-853. https://doi.org/10.1128/jb.164.2.845-853.1985
Vogl, T., Stratis, A., Wixler, V., Völler, T., Thurainayagam, S., Jorch, S. K., Zenker, S., Dreiling, A., Chakraborty, D., Fröhling, M., Paruzel, P., Wehmeyer, C., Hermann, S., Papantonopoulou, O., Geyer, C., Loser, K., Schäfers, M., Ludwig, S., Stoll, M., … Roth, J. (2018). Autoinhibitory regulation of S100A8/S100A9 alarmin activity locally restricts sterile inflammation. Journal of Clinical Investigation, 128(5), 1852-1866. https://doi.org/10.1172/JCI89867
Wang, T., du, Z., Zhu, F., Cao, Z., An, Y., Gao, Y., & Jiang, B. (2020). Comorbidities and multi-organ injuries in the treatment of COVID-19. The Lancet, 395(10228), e52. https://doi.org/10.1016/S0140-6736(20)30558-4
Wilk, A. J., Rustagi, A., Zhao, N. Q., Roque, J., Martínez-Colón, G. J., McKechnie, J. L., Ivison, G. T., Ranganath, T., Vergara, R., Hollis, T., Simpson, L. J., Grant, P., Subramanian, A., Rogers, A. J., & Blish, C. A. (2020). A single-cell atlas of the peripheral immune response in patients with severe COVID-19. Nature Medicine, 26(7), 1070-1076. https://doi.org/10.1038/s41591-020-0944-y
Witko-Sarsat, V., Mocek, J., Bouayad, D., Tamassia, N., Ribeil, J.-A., Candalh, C., Davezac, N., Reuter, N., Mouthon, L., Hermine, O., Pederzoli-Ribeil, M., & Cassatella, M. A. (2010). Proliferating cell nuclear antigen acts as a cytoplasmic platform controlling human neutrophil survival. Journal of Experimental Medicine, 207(12), 2631-2645. https://doi.org/10.1084/jem.20092241
Worthen, G. S., Schwab, B., Elson, E. L., & Downey, G. P. (1989). Mechanics of stimulated neutrophils: Cell stiffening induces retention in capillaries. Science, 245, 183-186. https://doi.org/10.1126/science.2749255
Yang, W. H., Heithoff, D. M., Aziz, P. V., Haslund-Gourley, B., Westman, J. S., Narisawa, S., Pinkerton, A. B., Millán, J. L., Nizet, V., Mahan, M. J., & Marth, J. D. (2018). Accelerated aging and clearance of host anti-inflammatory enzymes by discrete pathogens fuels sepsis. Cell Host & Microbe, 24(4), 500-513.e5. https://doi.org/10.1016/j.chom.2018.09.011