Modulation of oxidative and nitrosative stress attenuates microvascular hyperpermeability in ovine model of Pseudomonas aeruginosa sepsis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 12 2021
14 12 2021
Historique:
received:
08
08
2021
accepted:
18
11
2021
entrez:
15
12
2021
pubmed:
16
12
2021
medline:
28
1
2022
Statut:
epublish
Résumé
In sepsis, microvascular hyperpermeability caused by oxidative/nitrosative stress (O&NS) plays an important role in tissue edema leading to multi-organ dysfunctions and increased mortality. We hypothesized that a novel compound R-107, a modulator of O&NS, effectively ameliorates the severity of microvascular hyperpermeability and preserves multi-organ function in ovine sepsis model. Sepsis was induced in twenty-two adult female Merino sheep by intravenous infusion of Pseudomonas aeruginosa (PA) (1 × 10
Identifiants
pubmed: 34907252
doi: 10.1038/s41598-021-03320-w
pii: 10.1038/s41598-021-03320-w
pmc: PMC8671546
doi:
Substances chimiques
Free Radical Scavengers
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
23966Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM097480
Pays : United States
Informations de copyright
© 2021. The Author(s).
Références
Singer, M. et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA 23, 801–10 (2016).
doi: 10.1001/jama.2016.0287
Fleischmann, C. et al. International forum of acute care trialists. Assessment of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. Am. J. Respir. Crit. Care Med. 193(3), 259–72 (2016).
pubmed: 26414292
doi: 10.1164/rccm.201504-0781OC
Cohen, J. et al. Sepsis: a roadmap for future research. Lancet Infect. Dis. 15(5), 581–614 (2015).
pubmed: 25932591
doi: 10.1016/S1473-3099(15)70112-X
Rhee, C. et al. Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009–2014. JAMA 318(13), 1241–1249 (2017).
pubmed: 28903154
pmcid: 5710396
doi: 10.1001/jama.2017.13836
Rhee, C. et al. Prevalence, underlying causes, and preventability of sepsis-associated mortality in US acute care hospitals. JAMA Netw. Open. 2(2), e187571 (2019).
pubmed: 30768188
pmcid: 6484603
doi: 10.1001/jamanetworkopen.2018.7571
Luhr, R., Cao, Y., Söderquist, B. & Cajander, S. Trends in sepsis mortality over time in randomised sepsis trials: a systematic literature review and meta-analysis of mortality in the control arm, 2002–2016. Crit. Care. 23(1), 241 (2019).
pubmed: 31269976
pmcid: 6610784
doi: 10.1186/s13054-019-2528-0
Huet, O., Dupic, L., Harrois, A. & Duranteau, J. Oxidative stress and endothelial dysfunction during sepsis. Front. Biosci. (Landmark Ed). 1(16), 1986–1995 (2011).
doi: 10.2741/3835
Coletta, C. et al. Endothelial dysfunction is a potential contributor to multiple organ failure and mortality in aged mice subjected to septic shock: preclinical studies in a murine model of cecal ligation and puncture. Crit. Care. 18(5), 511 (2014).
pubmed: 25223540
pmcid: 4177582
doi: 10.1186/s13054-014-0511-3
Lee, W. L. & Liles, W. C. Endothelial activation, dysfunction and permeability during severe infections. Curr. Opin. Hematol. 18(3), 191–196 (2011).
pubmed: 21423012
doi: 10.1097/MOH.0b013e328345a3d1
Prauchner, C. A. Oxidative stress in sepsis: pathophysiological implications justifying antioxidant co-therapy. Burns 43(3), 471–485 (2017).
pubmed: 28034666
doi: 10.1016/j.burns.2016.09.023
Pascual-Ramirez, J. & Koutrouvelis, A. The nitric oxide pathway antagonists in septic shock: meta-analysis of controlled clinical trials. J. Crit. Care. 51, 34–38 (2019).
pubmed: 30738285
doi: 10.1016/j.jcrc.2019.01.013
López, A. et al. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit. Care Med. 32(1), 21–30 (2004).
pubmed: 14707556
doi: 10.1097/01.CCM.0000105581.01815.C6
Chelkeba, L. et al. The effect of parenteral selenium on outcomes of mechanically ventilated patients following sepsis: a prospective randomized clinical trial. Ann. Intensive Care. 5(1), 29 (2015).
pubmed: 26429356
pmcid: 4591221
doi: 10.1186/s13613-015-0071-y
Fujii, T. et al. Effect of vitamin C, hydrocortisone, and thiamine vs hydrocortisone alone on time alive and free of vasopressor support among patients with septic shock: the Vitamins randomized clinical trial. JAMA 323(5), 423–431 (2020).
pubmed: 31950979
pmcid: 7029761
doi: 10.1001/jama.2019.22176
Marshall, J. C. Why have clinical trials in sepsis failed?. Trends Mol Med. 20(4), 195–203 (2014).
pubmed: 24581450
doi: 10.1016/j.molmed.2014.01.007
Cui, X. et al. Neuronal nitric oxide synthase deficiency decreases survival in bacterial peritonitis and sepsis. Intensive Care Med. 33(11), 1993–2003 (2007).
pubmed: 17684724
pmcid: 3380429
doi: 10.1007/s00134-007-0814-9
Saia, R. S., Anselmo-Franci, J. A. & Carnio, E. C. Hypothermia during endotoxemic shock in female mice lacking inducible nitric oxide synthase. Shock 29(1), 119–126 (2008).
pubmed: 17621253
doi: 10.1097/shk.0b013e31805cdc96
Tirosh, O., Artan, A., Aharoni-Simon, M., Ramadori, G. & Madar, Z. Impaired liver glucose production in a murine model of steatosis and endotoxemia: protection by inducible nitric oxide synthase. Antioxid Redox Signal. 13(1), 13–26 (2010).
pubmed: 19951063
doi: 10.1089/ars.2009.2789
Wang, W. et al. Endothelial nitric oxide synthase-deficient mice exhibit increased susceptibility to endotoxin-induced acute renal failure. Am. J. Physiol. Renal. Physiol. 287(5), F1044–F1048 (2004).
pubmed: 15475535
doi: 10.1152/ajprenal.00136.2004
Soriano, F. G., Lorigados, C. B., Pacher, P. & Szabo, C. Effects of a potent peroxynitrite decomposition catalyst in murine models of endotoxemia and sepsis. Shock 35(6), 560–566 (2011).
pubmed: 21263378
pmcid: 3096695
doi: 10.1097/SHK.0b013e31820fe5d5
Ito, H. et al. R-100 improves pulmonary function and systemic fluid balance in sheep with combined smoke-inhalation injury and Pseudomonas aeruginosa sepsis. J. Transl. Med. 15(1), 266 (2017).
pubmed: 29282084
pmcid: 5745620
doi: 10.1186/s12967-017-1366-6
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M. & Altman, D. G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8(6), e1000412 (2010).
pubmed: 20613859
pmcid: 2893951
doi: 10.1371/journal.pbio.1000412
Maybauer, M. O. et al. The selective vasopressin type 1a receptor agonist selepressin (FE 202158) blocks vascular leak in ovine severe sepsis. Crit. Care Med. 42(7), e525–e533 (2014).
pubmed: 24674922
pmcid: 4346299
doi: 10.1097/CCM.0000000000000300
Fukuda, S. et al. Modulation of peroxynitrite reduces norepinephrine requirements in ovine MRSA septic shock. Shock 52(5), e92–e99 (2019).
pubmed: 30499879
doi: 10.1097/SHK.0000000000001297
Nemzek, J. A., Hugunin, K. M. & Opp, M. R. Modeling sepsis in the laboratory: merging sound science with animal well-being. Comp. Med. 58(2), 120–128 (2008).
pubmed: 18524169
pmcid: 2703167
Guillon, A. et al. Preclinical septic shock research: why we need an animal ICU. Ann Intensive Care. 9(1), 66 (2019).
pubmed: 31183570
pmcid: 6557957
doi: 10.1186/s13613-019-0543-6
Enkhbaatar, P. et al. Comparison of gene expression by sheep and human blood stimulated with the TLR4 agonists lipopolysaccharide and monophosphoryl lipid A. PLoS One. 10(12), e0144345 (2015).
pubmed: 26640957
pmcid: 4671644
doi: 10.1371/journal.pone.0144345
Han, X. et al. Implications of centers for medicare & medicaid services severe sepsis and septic shock early management bundle and initial lactate measurement on the management of sepsis. Chest 154(2), 302–308 (2018).
pubmed: 29804795
pmcid: 6113629
doi: 10.1016/j.chest.2018.03.025
Fukuda, S. et al. Monophosphoryl lipid A attenuates multiorgan dysfunction during post-burn Pseudomonas aeruginosa pneumonia In sheep. Shock 53(3), 307–316 (2020).
pubmed: 31045990
pmcid: 6937402
doi: 10.1097/SHK.0000000000001364
Leary S. et al. AVMA Guidelines for the Euthanasia of Animals: 2013 Edition. American Veterinary Medical Association. Schaumburg, Illinois, USA, (2013).
Pearce, M. L., Yamashita, J. & Beazell, J. Measurement of pulmonary edema. Circ. Res. 16, 482–488 (1965).
pubmed: 14289157
doi: 10.1161/01.RES.16.5.482
Brandenburg, K. S. et al. Inhibition of Pseudomonas aeruginosa biofilm formation on wound dressings. Wound Repair Regen. 23(6), 842–854 (2015).
pubmed: 26342168
pmcid: 4980578
doi: 10.1111/wrr.12365
Pacher, P., Beckman, J. S. & Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev. 87(1), 315–424 (2007).
pubmed: 17237348
doi: 10.1152/physrev.00029.2006
Yano, K. et al. Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J. Exp. Med. 203(6), 1447–58 (2006).
pubmed: 16702604
pmcid: 2118329
doi: 10.1084/jem.20060375
Lange, M. et al. Assessment of vascular permeability in an ovine model of acute lung injury and pneumonia-induced Pseudomonas aeruginosa sepsis. Crit. Care Med. 36(4), 1284–1289 (2008).
pubmed: 18379256
doi: 10.1097/CCM.0b013e318169ef74
Niimi, Y. et al. Omega-7 oil increases telomerase activity and accelerates healing of grafted burn and donor site wounds. Sci. Rep. 11(1), 975 (2021).
pubmed: 33441597
pmcid: 7806965
doi: 10.1038/s41598-020-79597-0
Enkhbaatar, P. et al. Novel ovine model of methicillin-resistant Staphylococcus aureus-induced pneumonia and sepsis. Shock 29(5), 642–649 (2008).
pubmed: 17885644
doi: 10.1097/SHK.0b013e318158125b
Sirvent, J. M., Ferri, C., Baró, A., Murcia, C. & Lorencio, C. Fluid balance in sepsis and septic shock as a determining factor of mortality. Am. J. Emerg. Med. 33(2), 186–189 (2015).
pubmed: 25483379
doi: 10.1016/j.ajem.2014.11.016
Vincent, J. L., De Backer, D. & Wiedermann, C. J. Fluid management in sepsis: the potential beneficial effects of albumin. J. Crit. Care. 35, 161–167 (2016).
pubmed: 27481753
doi: 10.1016/j.jcrc.2016.04.019
Sakr, Y. et al. Intensive care over nations investigators. Higher fluid balance increases the risk of death from sepsis: results from a large international audit. Crit. Care Med. 45(3), 386–94 (2017).
pubmed: 27922878
doi: 10.1097/CCM.0000000000002189
Tigabu, B. M., Davari, M., Kebriaeezadeh, A. & Mojtahedzadeh, M. Fluid volume, fluid balance and patient outcome in severe sepsis and septic shock: a systematic review. J. Crit. Care. 48, 153–159 (2018).
pubmed: 30199843
doi: 10.1016/j.jcrc.2018.08.018
Silversides, J. A. et al. Conservative fluid management or deresuscitation for patients with sepsis or acute respiratory distress syndrome following the resuscitation phase of critical illness: a systematic review and meta-analysis. Intensive Care Med. 43(2), 155–170 (2017).
pubmed: 27734109
doi: 10.1007/s00134-016-4573-3
Ince, C. et al. ADQI XIV Workgroup. The endothelium in sepsis. Shock 45(3), 259–270 (2016).
pubmed: 26871664
pmcid: 5281063
doi: 10.1097/SHK.0000000000000473
Uchimido, R., Schmidt, E. P. & Shapiro, N. I. The glycocalyx: a novel diagnostic and therapeutic target in sepsis. Crit. Care. 23(1), 16 (2019).
pubmed: 30654825
pmcid: 6337861
doi: 10.1186/s13054-018-2292-6
Becker, B. F., Jacob, M., Leipert, S., Salmon, A. H. J. & Chappell, D. Degradation of the endothelial glycocalyx in clinical settings: searching for the sheddases. Br. J. Clin. Pharmacol. 80(3), 389–402 (2015).
pubmed: 25778676
pmcid: 4574825
doi: 10.1111/bcp.12629
Paulus, P., Jennewein, C. & Zacharowski, K. Biomarkers of endothelial dysfunction: can they help us deciphering systemic inflammation and sepsis?. Biomarkers 16(Suppl 1), S11-21 (2011).
pubmed: 21707440
doi: 10.3109/1354750X.2011.587893
Savery, M. D., Jiang, J. X., Park, P. W. & Damiano, E. R. The endothelial glycocalyx in syndecan-1 deficient mice. Microvasc. Res. 87, 83–91 (2013).
pubmed: 23428342
pmcid: 3627742
doi: 10.1016/j.mvr.2013.02.001
Martin, L., Koczera, P., Zechendorf, E. & Schuerholz, T. The endothelial glycocalyx: new diagnostic and therapeutic approaches in sepsis. Biomed. Res. Int. 2016, 3758278 (2016).
pubmed: 27699168
pmcid: 5028820
doi: 10.1155/2016/3758278
Nelson, A., Johansson, J., Tydén, J. & Bodelsson, M. Circulating syndecans during critical illness. APMIS 125(5), 468–475 (2017).
pubmed: 28256016
doi: 10.1111/apm.12662
Steppan, J. et al. Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix. J. Surg. Res. 165(1), 136–141 (2011).
pubmed: 19560161
doi: 10.1016/j.jss.2009.04.034
Bermejo-Martin, J. F. et al. Shared features of endothelial dysfunction between sepsis and its preceding risk factors (aging and chronic disease). J. Clin. Med. 7(11), 400 (2018).
pmcid: 6262336
doi: 10.3390/jcm7110400
Lubkin, A. & Torres, V. J. Bacteria and endothelial cells: a toxic relationship. Curr. Opin. Microbiol. 35, 58–63 (2017).
pubmed: 28013162
doi: 10.1016/j.mib.2016.11.008
Saliba, A. M. et al. Implications of oxidative stress in the cytotoxicity of Pseudomonas aeruginosa ExoU. Microbes Infect. 8(2), 450–459 (2006).
pubmed: 16293434
doi: 10.1016/j.micinf.2005.07.011