Bacterial Porins and Their Procoagulant Role: Implication in the Pathophysiology of Several Thrombotic Complications during Sepsis
Abstract
:1. Introduction
2. Sepsis-Induced Coagulopathy
3. Coagulation Factors and Their Antibacterial Role during Sepsis
4. Toxins
5. Endotoxin
6. Porins
7. Association among Sepsis and VTE
8. Association among Infection and DIC
9. Association among Sepsis and TMA
10. Plasma Exchange and Toxins
11. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Marston, H.D.; Dixon, D.M.; Knisely, J.M.; Palmore, T.N.; Fauci, A.S. Antimicrobial resistance. JAMA 2016, 316, 1193–1204. [Google Scholar] [CrossRef] [PubMed]
- Brown, E.D.; Wright, G.D. Antibacterial drug discovery in the resistance era. Nature 2016, 529, 336–343. [Google Scholar] [CrossRef]
- Khakpour, S.; Wilhelmsen, K.; Hellman, J. Vascular endothelial cell toll-like receptor pathways in sepsis. Innate Immun. 2015, 21, 827–846. [Google Scholar] [CrossRef]
- Chen, F.; Zou, L.; Williams, B.; Chao, W. Targeting toll-like receptors in sepsis: From bench to clinical trials. Antioxid. Redox Signal. 2021, 35, 1324–1339. [Google Scholar] [CrossRef]
- Dahlbäck, B. Blood coagulation. Lancet 2000, 335, 1627–1632. [Google Scholar] [CrossRef]
- Goel, R.; Krishnamurti, L. Mortality, health care utilization and associated diagnoses in hospitalized patients with haemophilia in the United States: First reported nationwide estimates. Haemophilia 2012, 18, 688–692. [Google Scholar] [CrossRef] [PubMed]
- Girolami, A.; Santarossa, C.; Cosi, E.; Ferrari, S.; Lombardi, A.M. Acquired isolated FVII deficiency: An underestimated and potentially important laboratory finding. Clin. Appl. Thromb. Hemost. 2016, 22, 705–711. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Li, X.; Li, L.; Zhang, T.; Zhang, Q.; Wu, F.; Wang, D.; Hu, H.; Tian, C.; Liao, D.; et al. Coagulation factors VII, IX and X are effective antibacterial proteins against drug-resistant Gram-negative bacteria. Cell Res. 2019, 29, 711–724. [Google Scholar] [CrossRef]
- Amalakuhan, B.; Habib, S.A.; Mangat, M.; Reyes, L.F.; Rodriguez, A.H.; Hinojosa, C.A.; Soni, N.J.; Gilley, R.P.; Bustamante, C.A.; Anzueto, A.; et al. Endothelial adhesion molecules and multiple organ failure in patients with severe sepsis. Cytokine 2016, 88, 267–273. [Google Scholar] [CrossRef]
- De Groot, B.L.; Grubmüller, H. Water permeation across biological membranes: Mechanism and dynamics of aquaporin-1 and GlpF. Science 2001, 294, 2353–2357. [Google Scholar] [CrossRef]
- Hub, J.S.; de Groot, B.L. Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc. Natl. Acad. Sci. USA 2008, 105, 1198–1203. [Google Scholar] [CrossRef]
- Zeidel, M.L.; Ambudkar, S.V.; Smith, B.L.; Agre, P. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 1992, 31, 7436–7440. [Google Scholar] [CrossRef] [PubMed]
- Preston, G.M.; Carroll, T.P.; Guggino, W.B.; Agre, P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 1992, 256, 385–387. [Google Scholar] [CrossRef]
- Verkman, A.S.; Anderson, M.O.; Papadopoulos, M.C. Aquaporins: Important but elusive drug targets. Nat. Rev. Drug Discov. 2014, 13, 259–277. [Google Scholar] [CrossRef] [PubMed]
- Di Micco, B.; Di Micco, P.; Lepretti, M.; Stiuso, P.; Donnarumma, G.; Iovene, M.R.; Capasso, R.; Tufano, M.A. Hyperproduction of fibrin and inefficacy of antithrombin III and alpha2 macroglobulin in the presence of bacterial porins. Int. J. Exp. Pathol. 2005, 86, 241–245. [Google Scholar] [CrossRef] [PubMed]
- Di Micco, B.; Metafora, S.; Colonna, G.; Cartenì, M.; Ragone, R.; Macalello, M.A.; Di Micco, P.; Baroni, A.; Catalanotti, P.; Tufano, M.A. Porins from Salmonella typhimurium accelerate human blood coagulation in vitro by selective stimulation of thrombin activity: Implication in septic shock DIC pathogenesis. J. Endotoxin Res. 2001, 7, 211–217. [Google Scholar] [CrossRef] [PubMed]
- Bone, R.C. Sepsis and the systemic inflammatory response syndrome (SIRS). JAMA 1995, 273, 155–156. [Google Scholar] [CrossRef] [PubMed]
- Beltrani, B.; Natividad, R. Function and Biogenesis of Lipopolysaccharides. EcoSal. Plus 2018, 10, 1128. [Google Scholar]
- Karima, R.; Matsumoto, S.; Higashi, H.; Matsushima, K. The molecular pathogenesis of endotoxic shock and organ failure. Mol. Med. 1999, 5, 123–132. [Google Scholar] [CrossRef] [PubMed]
- Evans, L.; Rhodes, A.; Alhazzani, W.; Antonelli, M.; Coopersmith, C.M.; French, C.; Machado, F.R.; Mcintyre, L.; Ostermann, M.; Prescott, H.C.; et al. Surviving sepsis campaign: International guidelines for management of sepsis and septic shock 2021. Intensive Care Med. 2021, 47, 1181–1247. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Zhang, H.; Qu, M.; Nan, K.; Cao, H.; Cata, J.P.; Chen, W.; Miao, C. Review: The Emerging Role of Neutrophil Extracellular Traps in Sepsis and Sepsis-Associated Thrombosis. Front. Cell. Infect. Microbiol. 2021, 11, 653228. [Google Scholar] [CrossRef]
- Abrams, S.T.; Morton, B.; Alhamdi, Y.; Alsabani, M.; Lane, S.; Welters, I.D.; Wang, G.; Toh, C.H. A Novel Assay for Neutrophil Extracellular Trap Formation Independently Predicts Disseminated Intravascular Coagulation and Mortality in Critically Ill Patients. Am. J. Respir. Crit. Care Med. 2019, 200, 869–880. [Google Scholar] [CrossRef] [PubMed]
- Vazquez-Garza, E.; Jerjes-Sanchez, C.; Navarrete, A.; Joya-Harrison, J.; Rodriguez, D. Venous thromboembolism: Thrombosis, inflammation, and immunothrombosis for clinicians. J. Thromb. Thrombolysis 2017, 44, 377–385. [Google Scholar] [CrossRef]
- Khan, F.; Tritschler, T.; Kahn, S.R.; Rodger, M.A. Venous thromboembolism. Lancet 2021, 398, 64–77. [Google Scholar] [CrossRef]
- Saghazadeh, A.; Hafizi, S.; Rezaei, N. Inflammation in venous thromboembolism: Cause or consequence? Int. Immunopharmacol. 2015, 28, 655–665. [Google Scholar] [CrossRef] [PubMed]
- Tanguay, J.F.; Geoffroy, P.; Sirois, M.G.; Libersan, D.; Kumar, A.; Schaub, R.G.; Merhi, Y. Prevention of in-stent restenosis via reduction of thrombo-inflammatory reactions with recombinant P-selectin glycoprotein ligand-1. Thromb. Haemost. 2004, 91, 1186–1193. [Google Scholar] [CrossRef] [PubMed]
- Blair, P.; Rex, S.; Vitseva, O.; Beaulieu, L.; Tanriverdi, K.; Chakrabarti, S.; Hayashi, C.; Genco, C.A.; Iafrati, M.; Freedman, J.E. Stimulation of Toll-like receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circ. Res. 2009, 104, 346–354. [Google Scholar] [CrossRef]
- Engelmann, B.; Massberg, S. Thrombosis as an intravascular effector of innate immunity. Nat. Rev. Immunol. 2013, 13, 34–45. [Google Scholar] [CrossRef]
- Chang, J.C. Sepsis and septic shock: Endothelial molecular pathogenesis associated with vascular microthrombotic disease. Thromb. J. 2019, 17, 10. [Google Scholar] [CrossRef]
- Chang, J.C. Pathogenesis of Two Faces of DVT: New Identity of Venous Thromboembolism as Combined Micro-Macrothrombosis via Unifying Mechanism Based on “Two-Path Unifying Theory” of Hemostasis and “Two-Activation Theory of the Endothelium”. Life 2022, 12, 220. [Google Scholar] [CrossRef] [PubMed]
- Yasuda, N.; Goto, K.; Ohchi, Y.; Abe, T.; Koga, H.; Kitano, T. The efficacy and safety of antithrombin and recombinant human thrombomodulin combination therapy in patients with severe sepsis and disseminated intravascular coagulation. J. Crit. Care 2016, 36, 29–34. [Google Scholar] [CrossRef] [PubMed]
- Martí-Carvajal, A.J.; Solà, I.; Gluud, C.; Lathyris, D.; Cardona, A.F. Human recombinant protein C for severe sepsis and septic shock in adult and paediatric patients. Cochrane Database Syst. Rev. 2012, 12, CD004388. [Google Scholar] [CrossRef]
- Qin, X.; Zhang, W.; Zhu, X.; Hu, X.; Zhou, W. Early Fresh Frozen Plasma Transfusion: Is It Associated with Improved Outcomes of Patients With Sepsis? Front. Med. 2021, 8, 754859. [Google Scholar] [CrossRef]
- Fan, Y.; Jiang, M.; Gong, D.; Zou, C. Efficacy and safety of low-molecular-weight heparin in patients with sepsis: A meta-analysis of randomized controlled trials. Sci. Rep. 2016, 6, 25984. [Google Scholar] [CrossRef]
- Di Micco, P.; Imbalzano, E.; Russo, V.; Attena, E.; Mandaliti, V.; Orlando, L.; Lombardi, M.; Di Micco, G.; Camporese, G.; Annunziata, S.; et al. Heparin and SARS-CoV-2: Multiple Pathophysiological Links. Viruses 2021, 13, 2486. [Google Scholar] [CrossRef]
- Sillen, M.; Declerck, P.J. Thrombin Activatable Fibrinolysis Inhibitor (TAFI): An Updated Narrative Review. Int. J. Mol. Sci. 2021, 22, 3670. [Google Scholar] [CrossRef] [PubMed]
- Lang, T.; Zawada, A.M.; Theis, L.; Braun, J.; Ottillinger, B.; Kopperschmidt, P.; Gagel, A.; Kotanko, P.; Stauss-Grabo, M.; Kennedy, J.P.; et al. Hemodiafiltration: Technical and Medical Insights. Bioengineering 2023, 10, 145. [Google Scholar] [CrossRef] [PubMed]
- Di Micco, B.; Colonna, G.; Porta, R.; Metafora, S. Rat protein SV-IV (seminal vesicle protein No. 4) accelerates human blood coagulation in vitro by selective inhibition of antithrombin III. Biochem. Pharmacol. 1994, 48, 345–352. [Google Scholar] [CrossRef]
Bacteria Involved in Sepsis | |
---|---|
Gram-positive bacteria | Methicillin-sensitive Staphylococcus aureus (MSSA), methicillin-resistant Staphylococcus aureus (MRSA), Staphylococcus epidermidis, Staphylococcus spp., Streptococcus pneumoniae, Streptococcus pyogenes, Streptococcus agalactiae, Streptococcus dysgalactiae spp. equisimilis (SDSE), Streptococcus anginosus, Streptococcus constellatus, Streptococcus spp., Enterococcus faecalis, Enterococcus faecium, Enterococcus spp., other gram-positive cocci, Clostridium difficile, Clostridium perfringens, Clostridium tetani, Clostridium spp., other gram-positive rods |
Gram-negative bacteria | Moraxella catarrhalis, Neisseria meningitidis, Neisseria spp., Acinetobacter baumannii, Acinetobacter spp., Aeromonas hydrophila, Aeromonas spp., Bacteroides fragilis, Bacteroides spp., Burkholderia cepacia, Burkholderia spp., Citrobacter freundii, Citrobacter spp., Escherichia coli, Enterobacter spp., Haemophilus influenzae, Klebsiella pneumoniae, Klebsiella oxytoca, Klebsiella spp., Legionella pneumophila, Legionella spp., Pseudomonas aeruginosa, Pseudomonas spp., Proteus mirabilis, Proteus spp., Rickettsia spp., Salmonella enteritidis, Salmonella spp., Serratia marcescens, Serratia spp., Stenotrophomonas maltophilia, Stenotrophomonas spp., Vibrio vulnificus, Vibrio cholerae, Vibrio spp., gram-negative rods |
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Siniscalchi, C.; Perrella, A.; Trama, U.; Bernardi, F.F.; Imbalzano, E.; Camporese, G.; Russo, V.; Scudiero, O.; Meschi, T.; Di Micco, P. Bacterial Porins and Their Procoagulant Role: Implication in the Pathophysiology of Several Thrombotic Complications during Sepsis. Toxins 2024, 16, 368. https://doi.org/10.3390/toxins16080368
Siniscalchi C, Perrella A, Trama U, Bernardi FF, Imbalzano E, Camporese G, Russo V, Scudiero O, Meschi T, Di Micco P. Bacterial Porins and Their Procoagulant Role: Implication in the Pathophysiology of Several Thrombotic Complications during Sepsis. Toxins. 2024; 16(8):368. https://doi.org/10.3390/toxins16080368
Chicago/Turabian StyleSiniscalchi, Carmine, Alessandro Perrella, Ugo Trama, Francesca Futura Bernardi, Egidio Imbalzano, Giuseppe Camporese, Vincenzo Russo, Olga Scudiero, Tiziana Meschi, and Pierpaolo Di Micco. 2024. "Bacterial Porins and Their Procoagulant Role: Implication in the Pathophysiology of Several Thrombotic Complications during Sepsis" Toxins 16, no. 8: 368. https://doi.org/10.3390/toxins16080368