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FACIN, a Double-Edged Sword of The FACIN, a Double-Edged Sword of the Emerging Periodontal Pathogen Filifactor alocis : A Metabolic Enzyme Moonlighting as a Complement Inhibitor This information is current as of September 29, 2021. Monika Jusko, Beata Miedziak, David Ermert, Michal Magda, Ben C. King, Ewa Bielecka, Kristian Riesbeck, Sigrun Eick, Jan Potempa and Anna M. Blom J Immunol 2016; 197:3245-3259; Prepublished online 16 September 2016; Downloaded from doi: 10.4049/jimmunol.1600739 http://www.jimmunol.org/content/197/8/3245 http://www.jimmunol.org/ References This article cites 55 articles, 19 of which you can access for free at: http://www.jimmunol.org/content/197/8/3245.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists by guest on September 29, 2021 • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2016 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology FACIN, a Double-Edged Sword of the Emerging Periodontal Pathogen Filifactor alocis: A Metabolic Enzyme Moonlighting as a Complement Inhibitor Monika Jusko,* Beata Miedziak,* David Ermert,* Michal Magda,* Ben C. King,* Ewa Bielecka,*,† Kristian Riesbeck,‡ Sigrun Eick,x Jan Potempa,†,{ and Anna M. Blom* Periodontal disease is one of the most common inflammatory infectious diseases worldwide and it is associated with other syn- dromes, such as cardiovascular disease or rheumatoid arthritis. Recent advances in sequencing allowed for identification of novel periodontopathogens such as Gram-positive Filifactor alocis, but its virulence mechanisms remain largely unknown. We confirmed that F. alocis is a prevalent species in periodontitis patients, and we also observed strong correlation of this bacterium with clinical parameters, highlighting its role in the pathogenesis of the disease. Further, we found that preincubation of human serum with Downloaded from F. alocis resulted in abolished bactericidal activity and that F. alocis was surviving readily in full blood. We demonstrated that one of the key contributors to F. alocis complement resistance is a unique protein, FACIN (F. alocis complement inhibitor), which binds to C3, resulting in suppression of all complement pathways. Interestingly, FACIN is a nonclassical cell surface protein, a cytosolic enzyme acetylornithine transaminase, for which we now identified a moonlighting function. FACIN binds to C3 alone, but more importantly it also captures activated complement factor 3 within the complex with factor B, thereby locking in the convertase in an inactive state. Because of the indispensable role of alternative pathway convertase in amplifying complement http://www.jimmunol.org/ cascades, its inhibition by FACIN results in a very potent downregulation of activated complement factor 3 opsonization on the pathogen surface, accompanied by reduction of downstream C5 cleavage. The Journal of Immunology, 2016, 197: 3245–3259. he oral microbiome consists of .600 prevalent bacterial based methods identified several bacterial clusters within a com- taxa (1), and unlike the other human microbiomes, it plex subgingival bacterial plaque (biofilm) and pointed out the T eventually causes a disease in the majority of individuals importance of three major consensus periodontopathogens: Tan- during their lifetime. The complex interactions of oral bacteria nerella forsythia, Porphyromonas gingivalis, and Treponema with human immune defenses result in chronic inflammation, denticola (8), collectively named as red complex. Subsequently, progressive destruction of periodontal tissues, pocket formation, those three Gram-negative species and their virulence factors have by guest on September 29, 2021 bone resorption, and in severe cases, tooth loss. Gingivitis (gin- been intensively studied, aiming at the identification of patho- gival inflammation without any bone loss and no pockets .3 mm) genesis mechanisms. affects .50% of the adult population, and periodontitis (three or More recent research resulted in a concept that periodontitis is a more teeth with pockets $4 mm) is present in 30% of adults, with result of a dysbiosis in the oral microbiota, leading to the formation ∼8% of severe cases suffering complete loss of dentition (2). of a pathogenic biofilm of an altered composition and increased Furthermore, periodontitis has been proven to be a significant risk bacterial counts, which, in turn, causes complement-dependent factor of systemic diseases, such as coronary heart disease, obe- inflammation of tooth-supporting tissues leading eventually to sity, atherosclerosis, and rheumatoid arthritis (3–7). Periodontitis alveolar bone loss (9, 10). A trigger for such alterations in the oral has traditionally been viewed as an infectious disease; however, biofilm can be provided by low-abundant keystone pathogens, as identification of a single bacterial species etiologic for the pro- shown for P. gingivalis in mouse models of periodontitis (9). gression of the disease has been unsuccessful. Instead, culture- Subsequent periodontal destruction can then be mediated by *Section of Protein Chemistry, Department of Translational Medicine, Lund University, UMO-2011/01/B/NZ6/00268 and 2012/04/A/NZ1/00051, and the Polish Ministry 205 02 Malmo¨, Sweden; †Department of Microbiology, Faculty of Biochemistry, of Science and Higher Education Grant 2975/7.PR/13/2014/2. B.M. and M.M. are Biophysics and Biotechnology, Jagiellonian University, 30-387 Krakow, Poland; students at the University of Rzeszo´w, Poland. The Faculty of Biochemistry, Biophys- ‡Section of Clinical Microbiology, Department of Translational Medicine, Lund Univer- ics and Biotechnology of Jagiellonian University is a partner of the Leading National x sity, 202 13 Malmo¨, Sweden; Laboratory of Oral Microbiology, Department of Peri- Research Center supported by the Ministry of Science and Higher Education. odontology, University of Bern, 3010 Bern, Switzerland; and {Centre for Oral Health and Address correspondence and reprint requests to Prof. Anna M. Blom, Section of Systemic Diseases, University of Louisville School of Dentistry, Louisville, KY 40202 Protein Chemistry, Department of Translational Medicine, Lund University, Inga ORCIDs: 0000-0003-4600-9070 (D.E.); 0000-0001-6776-8741 (B.C.K.); 0000-0002- Maria Nilsson Street 53, S-205 02 Malmo¨, Sweden. E-mail address: anna. 2631-6711 (E.B.); 0000-0001-6274-6965 (K.R.); 0000-0002-4619-2461 (S.E.); 0000- [email protected] 0002-1348-1734 (A.M.B.). Abbreviations used in this article: AP, alternative pathway; C3b, activated com- Received for publication April 25, 2016. Accepted for publication August 20, 2016. plement factor 3; CP, classical pathway; DAF, decay-accelerating factor; FACIN, F. alocis complement inhibitor; FB, factor B; FD, factor D; GCF, gingival crevicular This work was supported by Swedish Research Council Grant K2012-66X-14928-09- fluid; GluD, glutamate dehydrogenase; GMFI, geometric mean fluorescence inten- 5, Swedish Government Funds for Clinical Research, the Torsten So¨derberg Founda- sity; GVB2+, barbiturate buffer with dextrose and gelatin; LB, Luria–Bertani; LP, tion, the O¨ sterlund Foundation, the Greta and Johan Kock Foundation, the Gustav V lectin pathway; MAC, membrane attack complex; NCBI, National Center for Bio- 80-Year Anniversary Foundation, the Knut and Alice Wallenberg Foundation, and the technology Information; NHS, normal human serum; pAb, polyclonal Ab; PVDF, Inga-Britt and Arne Lundberg Foundation. J.P. is supported by European Commission polyvinylidene difluoride. Grants P7-HEALTH-F3-2012-306029 TRIGGER and FP7-PEOPLE-2011-ITN-290246 RAPID National Institutes of Health, National Institute of Dental and Craniofacial Ó Research Grants DE 09761, DE 022597, and DE023207, Science Center, Poland Grants Copyright 2016 by The American Association of Immunologists, Inc. 0022-1767/16/$30.00 www.jimmunol.org/cgi/doi/10.4049/jimmunol.1600739 3246 FILIFACTOR ALOCIS INHIBITS THE COMPLEMENT SYSTEM pathobionts, commensals that begin to thrive under inflammatory lornithine transaminase involved in arginine catabolism. Further- conditions and evoke disease-associated symptoms (11, 12). Fur- more, we describe that in addition to its indispensable metabolic thermore, recent advances in sequencing techniques allowed for function for the bacterium, the protein provides compelling defense identification of novel species within the subgingival dental biofilm, against complement. To underline its novel role in immune evasion, which had previously been unrecognized because of culture diffi- we named it FACIN,thatis,F. a loc is complement inhibitor. culties (13–15). These facts facilitated complex comparative studies of bacterial communities between health and disease, and pointed Materials and Methods out shifts at all taxonomic levels, identifying species correlated with Determination of F. alocis and mRNA expression of disease states (16–18). NAD-specific
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