Serum proteases prevent bacterial biofilm formation: role of kallikrein and plasmin

References

• Bryers JD. Medical biofilms. Biotechnol Bioeng. 2008;100(1):1–18.
   PubMed Web of Science ®Google Scholar
• Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov. 2003;2(2):114–122.
   PubMed Web of Science ®Google Scholar
• Uruén C, Chopo-Escuin G, Tommassen J, et al. Biofilms as promoters of bacterial antibiotic resistance and tolerance. Antibiotics (Basel). 2020;10(1):3.
   PubMed Web of Science ®Google Scholar
• Thomas WE, Trintchina E, Forero M, et al. Bacterial adhesion to target cells enhanced by shear force. Cell 2002;109(7):913–923.
   PubMed Web of Science ®Google Scholar
• Mikaty G, Soyer M, Mairey E, et al. Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLoS Pathog. 2009;5(2):e1000314.
   PubMed Web of Science ®Google Scholar
• Campoccia D, Mirzaei R, Montanaro L, et al. Hijacking of immune defences by biofilms: a multifront strategy. Biofouling 2019;35(10):1055–1074.
   PubMed Web of Science ®Google Scholar
• Santos-Neto JF, Ferreira VM, Feitosa CA, et al. Carriage prevalence of Neisseria meningitidis in the Americas in the 21st century: a systematic review. Braz J Infect Dis. 2019;23(4):254–267.
   PubMed Web of Science ®Google Scholar
• Sim RJ, Harrison MM, Moxon ER, et al. Underestimation of meningococci in tonsillar tissue by nasopharyngeal swabbing. Lancet 2000;356(9242):1653–1654.
   PubMed Web of Science ®Google Scholar
• Rouphael NG, Stephens DS. Neisseria meningitidis: biology, microbiology, and epidemiology. Methods Mol Biol. 2012;799:1–20.
   PubMedGoogle Scholar
• Arenas J, Tommassen J. Meningococcal biofilm formation: let´s stick together. Trends Microbiol. 2017;25(2):113–124
   PubMed Web of Science ®Google Scholar
• Lappann M, Claus H, van Alen T, et al. A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol Microbiol. 2010;75(6):1355–1371.
   PubMed Web of Science ®Google Scholar
• Arenas J, Nijland R, Rodriguez FJ, et al. Involvement of three meningococcal surface-exposed proteins, the heparin-binding protein NhbA, the alpha-peptide of IgA protease and the autotransporter protease NalP, in initiation of biofilm formation. Mol Microbiol. 2013;87(2):254–268.
   PubMed Web of Science ®Google Scholar
• Arenas J, Cano S, Nijland R, et al. The meningococcal autotransporter AutA is implicated in autoaggregation and biofilm formation. Environ Microbiol. 2015;17(4):1321–1337.
   PubMed Web of Science ®Google Scholar
• Arenas J, Paganelli FL, Rodríguez-Castaño P, et al. Expression of the gene for autotransporter AutB of Neisseria meningitidis affects biofilm formation and epithelial transmigration. Front Cell Infect Microbiol. 2016;6:162.
   PubMed Web of Science ®Google Scholar
• Tommassen J, Arenas J. Biological functions of the secretome of Neisseria meningitidis. Frontiers in Cellular and Infection Microbiology. 2017;7:256.
   PubMed Web of Science ®Google Scholar
• Rappuoli R, Pizza M, Masignani V, et al. Meningococcal B vaccine (4CMenB): the journey from research to real world experience. Expert Rev Vaccines. 2018;17(12):1111–1121.
   PubMed Web of Science ®Google Scholar
• Esposito V, Musi V, de Chiara C, et al. Structure of the C-terminal domain of Neisseria heparin binding antigen (NHBA), one of the main antigens of a novel vaccine against Neisseria meningitidis. J Biol Chem. 2011;286(48):41767–41775.
   PubMed Web of Science ®Google Scholar
• Serruto D, Spadafina T, Ciucchi L, et al. Neisseria meningitidis GNA2132, a heparin-binding protein that induces protective immunity in humans. Proc Natl Acad Sci USA. 2010;107(8):3770–3775.
   PubMed Web of Science ®Google Scholar
• Vacca I, Del Tordello E, Gasperini G, et al. Neisserial heparin binding antigen (NHBA) contributes to the adhesion of Neisseria meningitidis to human epithelial cells. PLoS One. 2016;11(10):e0162878.
   PubMed Web of Science ®Google Scholar
• Casellato A, Rossi Paccani S, Barrile R, et al. The C2 fragment from Neisseria meningitidis antigen NHBA increases endothelial permeability by destabilizing adherens junctions. Cell Microbiol. 2014;16(6):925–937.
   PubMed Web of Science ®Google Scholar
• Saunders NJ, Jeffries AC, Peden JF, et al. Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol. 2000;37(1):207–215.
   PubMed Web of Science ®Google Scholar
• van Ulsen P, van Alphen L, Ten Hove J, et al. A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol Microbiol. 2003;50(3):1017–1030.
   PubMed Web of Science ®Google Scholar
• Langereis J, Hermans PWM. Novel concepts in nontypeable Haemophilus influenzae biofilm formation.FEMS Microbiol Lett. 2013; 346:81–89.
   PubMed Web of Science ®Google Scholar
• Archer NA, Mazaitis MJ, Costerton JW, et al. Staphylococcus aureus biofilms. Virulence 2011;2(5):445–459.
   PubMed Web of Science ®Google Scholar
• Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev. 2020;84(3):e00026–19.
   PubMed Web of Science ®Google Scholar
• Mann EE, Rice KC, Boles BR, et al. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS One. 2009;4(6):e5822.
   PubMed Web of Science ®Google Scholar
• Dengler V, Foulston L, DeFrancesco AS, et al. An electrostatic net model for the role of extracellular DNA in biofilm formation by Staphylococcus aureus. J Bacteriol. 2015;197(24):3779–3787.
   PubMed Web of Science ®Google Scholar
• Cattelan N, Dubey P, Arnal L, et al. Bordetella biofilms: a lifestyle leading to persistent infections. Pathog Dis. 2016;74(1):ftv108.
   PubMed Web of Science ®Google Scholar
• Serra DO, Conover MS, Arnal L, et al. FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS One. 2011;6(12):e28811.
   PubMed Web of Science ®Google Scholar
• de Maat S, Björkqvist J, Suffritti C, et al. Plasmin is a natural trigger for bradykinin production in patients with hereditary angioedema with factor XII mutations. J Allergy Clin Immunol. 2016;138(5):1414–1423.
   PubMed Web of Science ®Google Scholar
• Roussel-Jazédé V, Arenas J, Langereis JD, et al. Variable processing of the IgA protease autotransporter at the cell surface of Neisseria meningitidis. Microbiology 2014;160(11):2421–2431.
   PubMed Web of Science ®Google Scholar
• Coutte L, Antoine R, Drobecq H, et al. Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion. Embo J. 2001;20(18):5040–5048.
   PubMed Web of Science ®Google Scholar
• Verwey WF, Thiele EH, Sage DN, et al. A simplified liquid culture medium for the growth of Hemophilus pertussis. J Bacteriol. 1949;58(2):127–134.
   Web of Science ®Google Scholar
• Pérez-Ortega J, Rodríguez A, Ribes E, et al. Interstrain cooperation in meningococcal biofilms: role of autotransporters NalP and AutA. Front Microbiol. 2017;8:434.
   PubMed Web of Science ®Google Scholar
• Heydorn A, Nielsen AT, Hentzer M, et al. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 2000;146(10):2395–2397.
   PubMedGoogle Scholar
• Frye SA, Beyene GT, Namouchi A, et al. The helicase DinG responds to stress due to DNA double strand breaks. PLoS One. 2017;12(11):e0187900.
   PubMed Web of Science ®Google Scholar
• Beyene GT, Kalayou S, Riaz T, et al. Comparative proteomic analysis of Neisseria meningitidis wildtype and dprA null mutant strains links DNA processing to pilus biogenesis. BMC Microbiol. 2017;21(1):96.
   Google Scholar
• Di Fede M, Biagini M, Cartocci E, et al. Neisseria Heparin Binding Antigen is targeted by the human alternative pathway C3-convertase. PLoS One. 2018;13(3):e0194662.
   PubMed Web of Science ®Google Scholar
• Pantano E, Marchi S, Biagini M, et al. NHBA is processed by kallikrein from human saliva. PLoS One. 2019;14(8):e0203234.
   PubMed Web of Science ®Google Scholar
• Sierro DO, Conover MS, Arnal L, et al. FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS One. 2011;6(12):e28811.
   PubMed Web of Science ®Google Scholar
• Nash ZM, Cotter PA. Regulated, sequential processing by multiple proteases is required for proper maturation and release of Bordetella filamentous hemagglutinin. Mol Microbiol. 2019;112(3):820–836.
   PubMed Web of Science ®Google Scholar
• Weidmann H, Heikaus L, Long AT, et al. The plasma contact system, a protease cascade at the nexus of inflammation, coagulation and immunity. Biochim Biophys Acta Mol Cell Res. 2017;1864(11):2118–2127.
   PubMed Web of Science ®Google Scholar
• Kalinska M, Meyer-Hoffert U, Kantyka T, et al. Kallikreins - The melting pot of activity and function. Biochimie 2016;122:270–282.
   PubMed Web of Science ®Google Scholar
• Lima AR, Alves FM, Angelo PF, et al. S(1)’ and S(2)’ subsite specificities of human plasma kallikrein and tissue kallikrein 1 for the hydrolysis of peptides derived from the bradykinin domain of human kininogen. Biol Chem. 2008;389(12):1487–1494.
   PubMed Web of Science ®Google Scholar
• Kurachi K, Davie EW. Activation of human factor XI (plasma thromboplastin antecedent) by factor XIIa (activated Hageman factor). Biochemistry 1977;16(26):5831–5839.
   PubMed Web of Science ®Google Scholar
• Steichen CT, Cho C, Shao JQ, et al. The Neisseria gonorrhoeae biofilm matrix contains DNA, and an endogenous nuclease controls its incorporation. Infect Immun. 2011;79(4):1504–1511.
   PubMed Web of Science ®Google Scholar
• Semchenko EA, Mubaiwa TD, Day CJ, et al. Role of the gonococcal neisserial heparin binding antigen in microcolony formation, and serum resistance and adherence to epithelial cells. J Infect Dis. 2020;221(10):1612–1622.
   PubMed Web of Science ®Google Scholar
• Pohlner J, Langenberg U, Wölk U, et al. Uptake and nuclear transport of Neisseria IgA1 protease-associated alpha-proteins in human cells. Mol Microbiol. 1995;17(6):1073–1083.
   PubMed Web of Science ®Google Scholar
• Besbes A, Le Goff S, Antunes A, et al. Hyperinvasive meningococci induce intra-nuclear cleavage of the NF-κB protein p65/RelA by meningococcal IgA protease. PLoS Pathog. 2015;11(8):e1005078.
   PubMed Web of Science ®Google Scholar
• Yu H, Muñoz EM, Edens RE, et al. Kinetic studies on the interactions of heparin and complement proteins using surface plasmon resonance. Biochim Biophys Acta. 2005;1726(2):168–176.
   PubMed Web of Science ®Google Scholar
• Duensing TD, Wing JS, van Putten JP. Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect Immun. 1999;67(9):4463–4468.
   PubMed Web of Science ®Google Scholar
• Menozzi FD, Gantiez C, Locht C. Interaction of the Bordetella pertussis filamentous hemagglutinin with heparin. FEMS Microbiol Lett. 1991;78(1):59–64.
   PubMed Web of Science ®Google Scholar
• Conover MS, Meenu M, Deora R. Extracellular DNA is essential for maintaining bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS One. 2011;6(2):e16861.
   PubMed Web of Science ®Google Scholar
• Inatsuka CS, Julio SM, Cotter PA. Bordetella filamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity. Proc Natl Acad Sci USA. 2005;102(51):18578–18583.
   PubMed Web of Science ®Google Scholar
• Nicholson TL, Brockmeier SL, Loving C. Contribution of Bordetella bronchiseptica filamentous hemagglutinin and pertactin to respiratory disease in swine. Infect Immun. 2009;77(5):2136–2146.
   PubMed Web of Science ®Google Scholar
• Hovingh ES, de Maat S, Cloherty APM, et al. Virulence associated gene 8 of Bordetella pertussis enhances contact system activity by inhibiting the regulatory function of complement regulator C1 inhibitor. Front Immunol. 2018;4:1172.
   Google Scholar
• Małgorzata P, Wiater A, Bachanek T, et al. Enzymes in therapy of biofilm-related oral diseases. Biotechnol Appl Biochem. 2017;64(3):337–346.
   PubMed Web of Science ®Google Scholar
• Kaplan JB, Kaplan. Biofilm dispersal: mechanisms, clinical implications, and potential therapeutic uses. J Dent Res. 2010;89(3):205–218.
   PubMed Web of Science ®Google Scholar
• Bos MP, Tommassen J. Viability of a capsule- and lipopolysaccharide-deficient mutant of Neisseria meningitidis. Infect Immun. 2005;73(9):6194–6197.
   PubMed Web of Science ®Google Scholar
• Nizet V, Colina KF, Almquist JR, et al. A virulent nonencapsulated Haemophilus influenzae. J Infect Dis. 1996;173(1):180–186.
   PubMed Web of Science ®Google Scholar
• Boake WC. Antistaphylocoagulase in experimental staphylococcal infections. J Immunol. 1956;76:89–96.
   PubMed Web of Science ®Google Scholar
• King AJ, Berbers G, van Oirschot HF, et al. Role of the polymorphic region 1 of the Bordetella pertussis protein pertactin in immunity. Microbiology 2001;147(11):2885–2895.
   PubMedGoogle Scholar