497
Views
4
CrossRef citations to date
0
Altmetric
Review Articles

The complement system as a key modulator of the oral microbiome in health and disease

ORCID Icon, ORCID Icon & ORCID Icon
Pages 138-167 | Received 03 Oct 2022, Accepted 23 Dec 2022, Published online: 09 Jan 2023

References

  • Abranches J, Miller JH, Martinez AR, Simpson-Haidaris PJ, Burne RA, Lemos JA. 2011. The collagen-binding protein Cnm is required for Streptococcus mutans adherence to and intracellular invasion of human coronary artery endothelial cells. Infect Immun. 79(6):2277–2284.
  • Agarwal V, Ahl J, Riesbeck K, Blom AM. 2013. An alternative role of C1q in bacterial infections: facilitating Streptococcus pneumoniae adherence and invasion of host cells. J Immunol. 191(8):4235–4245.
  • Agrawal A, Singh PP, Bottazzi B, Garlanda C, Mantovani A. 2009. Pattern recognition by pentraxins. Adv Exp Med Biol. 653:98–116.
  • Aleru O, Barber MF. 2020. Battlefronts of evolutionary conflict between bacteria and animal hosts. PLoS Pathog. 16(9):e1008797.
  • Ali YM, Lynch NJ, Haleem KS, Fujita T, Endo Y, Hansen S, Holmskov U, Takahashi K, Stahl GL, Dudler T, et al. 2012. The lectin pathway of complement activation is a critical component of the innate immune response to pneumococcal infection. PLoS Pathog. 8(7):e1002793.
  • Alves LA, de Carli TR, Harth-Chu EN, Mariano FS, Höfling JF, Stipp RN, Mattos-Graner RO. 2019. Oral streptococci show diversity in resistance to complement immunity. J Med Microbiol. 68(4):600–608.
  • Alves LA, Ganguly T, Harth-Chú ÉN, Kajfasz J, Lemos JA, Abranches J, Mattos-Graner RO. 2020. PepO is a target of the two-component systems VicRK and CovR required for systemic virulence of Streptococcus mutans. Virulence. 11(1):521–536.
  • Alves LA, Harth-Chu EN, Palma TH, Stipp RN, Mariano FS, Höfling JF, Abranches J, Mattos-Graner RO. 2017. The two-component system VicRK regulates functions associated with Streptococcus mutans resistance to complement immunity. Mol Oral Microbiol. 32(5):419–431.
  • Alves LA, Nomura R, Mariano FS, Harth-Chu EN, Stipp RN, Nakano K, Mattos-Graner RO. 2016. CovR regulates Streptococcus mutans susceptibility to complement immunity and survival in blood. Infect Immun. 84(11):3206–3219.
  • Alves LA, Salvatierra GC, Freitas VA, Höfling JF, Bastos DC, Araujo TLS, Mattos-Graner RO. 2022. Diversity in phenotypes associated with host persistence and systemic virulence in Streptococcus sanguinis strains. Front Microbiol. 13:875581.
  • Andoh A, Fujiyama Y, Kimura T, Uchihara H, Sakumoto H, Okabe H, Bamba T. 1997. Molecular characterization of complement components (C3, C4, and factor B) in human saliva. J Clin Immunol. 17(5):404–407.
  • Andre GO, Converso TR, Politano WR, Ferraz LF, Ribeiro ML, Leite LC, Darrieux M. 2017. Role of Streptococcus pneumoniae proteins in evasion of complement-mediated immunity. Front Microbiol. 8:224.
  • Androvitsanea A, Stylianou K, Drosataki E, Petrakis I. 2021. The pathophysiological role of heat shock response in autoimmunity: a literature review. Cells. 10(10):2626.
  • Araújo Alves L, Ganguly T, Mattos-Graner RO, Kajfasz J, Harth-Chu EN, Lemos JA, Abranches J. 2018. CovR and VicRKX regulate transcription of the collagen binding protein Cnm of Streptococcus mutans. J Bacteriol. 200(23):e00141–e00218.
  • Arbore G, Kemper C, Kolev M. 2017. Intracellular complement - the complosome - in immune cell regulation. Mol Immunol. 89:2–9.
  • Asakawa R, Komatsuzawa H, Kawai T, Yamada S, Goncalves RB, Izumi S, Fujiwara T, Nakano Y, Suzuki N, Uchida Y, et al. 2003. Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol. 50(4):1125–1139.
  • Astasov-Frauenhoffer M, Varenganayil MM, Decho AW, Waltimo T, Braissant O. 2017. Exopolysaccharides regulate calcium flow in cariogenic biofilms. PLoS One. 12(10):e0186256.
  • Avilés-Reyes A, Miller JH, Lemos JA, Abranches J. 2017. Collagen-binding proteins of Streptococcus mutans and related streptococci. Mol Oral Microbiol. 32(2):89–106.
  • Bajic G, Degn SE, Thiel S, Andersen GR. 2015. Complement activation, regulation, and molecular basis for complement-related diseases. EMBO J. 34(22):2735–2757.
  • Baker SP, Nulton TJ, Kitten T. 2019. Genomic, phenotypic, and virulence analysis of Streptococcus sanguinis oral and infective-endocarditis isolates. Infect Immun. 87(1):e00703–18.
  • Bamashmous S, Kotsakis GA, Kerns KA, Leroux BG, Zenobia C, Chen D, Trivedi HM, McLean JS, Darveau RP. 2021. Human variation in gingival inflammation. Proc Natl Acad Sci USA. 118(27):e2012578118.
  • Banas JA, Russell RR, Ferretti JJ. 1990. Sequence analysis of the gene for the glucan-binding protein of Streptococcus mutans Ingbritt. Infect Immun. 58(3):667–673.
  • Banas JA, Vickerman MM. 2003. Glucan-binding proteins of the oral streptococci. Crit Rev Oral Biol Med. 14(2):89–99.
  • Barnett TC, Cole JN, Rivera-Hernandez T, Henningham A, Paton JC, Nizet V, Walker MJ. 2015. Streptococcal toxins: role in pathogenesis and disease. Cell Microbiol. 17(12):1721–1741.
  • Barthel D, Schindler S, Zipfel PF. 2012. Plasminogen is a complement inhibitor. J Biol Chem. 287(22):18831–18842.
  • Bartlett B, Ludewick HP, Verma S, Corrales-Medina VF, Waterer G, Lee S, Dwivedi G. 2022. Cardiovascular changes after pneumonia in a dual disease mouse model. Sci Rep. 12(1):11124.
  • Beikler T, Peters U, Prior K, Eisenacher M, Flemmig TF. 2008. Gene expression in periodontal tissues following treatment. BMC Med Genomics. 1:30.
  • Belda-Ferre P, Williamson J, Simón-Soro Á, Artacho A, Jensen ON, Mira A. 2015. The human oral metaproteome reveals potential biomarkers for caries disease. Proteomics. 15(20):3497–3507.
  • Belstrøm D, Jersie-Christensen RR, Lyon D, Damgaard C, Jensen LJ, Holmstrup P, Olsen JV. 2016. Metaproteomics of saliva identifies human protein markers specific for individuals with periodontitis and dental caries compared to orally healthy controls. PeerJ. 4:e2433.
  • Benis N, Wells JM, Smits MA, Kar SK, van der Hee B, Dos Santos VAPM, Suarez-Diez M, Schokker D. 2019. High-level integration of murine intestinal transcriptomics data highlights the importance of the complement system in mucosal homeostasis. BMC Genomics. 20(1):1028.
  • Bennike TB, Fatou B, Angelidou A, Diray-Arce J, Falsafi R, Ford R, Gill EE, van Haren SD, Idoko OT, Lee AH, et al. 2020. Preparing for life: plasma proteome changes and immune system development during the first week of human life. Front Immunol. 11:578505.
  • Berends ET, Dekkers JF, Nijland R, Kuipers A, Soppe JA, van Strijp JA, Rooijakkers SH. 2013. Distinct localization of the complement C5b-9 complex on Gram-positive bacteria. Cell Microbiol. 15(12):1955–1968.
  • Birmingham DJ, Hebert LA. 2001. CR1 and CR1-like: the primate immune adherence receptors. Immunol Rev. 180:100–111.
  • Biswas I, Drake L, Biswas S. 2007. Regulation of gbpC expression in Streptococcus mutans. J Bacteriol. 189(18):6521–6531.
  • Biswas S, Biswas I. 2006. Regulation of the glucosyltransferase (gtfBC) operon by CovR in Streptococcus mutans. J Bacteriol. 188(3):988–998.
  • Blatt AZ, Pathan S, Ferreira VP. 2016. Properdin: a tightly regulated critical inflammatory modulator. Immunol Rev. 274(1):172–190.
  • Boackle RJ, Connor MH, Vesely J. 1993. High molecular weight non-immunoglobulin salivary agglutinins (NIA) bind C1Q globular heads and have the potential to activate the first complement component. Mol Immunol. 30(3):309–319.
  • Bossi F, Tripodo C, Rizzi L, Bulla R, Agostinis C, Guarnotta C, Munaut C, Baldassarre G, Papa G, Zorzet S, et al. 2014. C1q as a unique player in angiogenesis with therapeutic implication in wound healing. Proc Natl Acad Sci USA. 111(11):4209–4214.
  • Bowen WH, Burne RA, Wu H, Koo H. 2018. Oral biofilms: pathogens, matrix, and polymicrobial interactions in microenvironments. Trends Microbiol. 26(3):229–242.
  • Bowen WH, Koo H. 2011. Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res. 45(1):69–86.
  • Brady LJ, Crowley PJ, Ma JK, Kelly C, Lee SF, Lehner T, Bleiweis AS. 1991. Restriction fragment length polymorphisms and sequence variation within the spaP gene of Streptococcus mutans serotype c isolates. Infect Immun. 59(5):1803–1810.
  • Brady LJ, Maddocks SE, Larson MR, Forsgren N, Persson K, Deivanayagam CC, Jenkinson HF. 2010. The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Mol Microbiol. 77(2):276–286.
  • Brady LJ, Piacentini DA, Crowley PJ, Oyston PC, Bleiweis AS. 1992. Differentiation of salivary agglutinin-mediated adherence and aggregation of mutans streptococci by use of monoclonal antibodies against the major surface adhesin P1. Infect Immun. 60(3):1008–1017.
  • Brown CK, Gu ZY, Matsuka YV, Purushothaman SS, Winter LA, Cleary PP, Olmsted SB, Ohlendorf DH, Earhart CA. 2005. Structure of the streptococcal cell wall C5a peptidase. Proc Natl Acad Sci USA. 102(51):18391–18396.
  • Cagliani R, Forni D, Filippi G, Mozzi A, De Gioia L, Pontremoli C, Pozzoli U, Bresolin N, Clerici M, Sironi M. 2016. The mammalian complement system as an epitome of host-pathogen genetic conflicts. Mol Ecol. 25(6):1324–1339.
  • Camargo TM, Stipp RN, Alves LA, Harth-Chu EN, Höfling JF, Mattos-Graner RO. 2018. Novel two-component system of Streptococcus sanguinis affecting functions associated with viability in saliva and biofilm formation. Infect Immun. 86(4):e00942–e01017.
  • Camous L, Roumenina L, Bigot S, Brachemi S, Frémeaux-Bacchi V, Lesavre P, Halbwachs-Mecarelli L. 2011. Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood. 117(4):1340–1349.
  • Chai L, Song YQ, Zee KY, Leung WK. 2010. Single nucleotide polymorphisms of complement component 5 and periodontitis. J Periodontal Res. 45(3):301–308.
  • Chang AM, Liu Q, Hajjar AM, Greer A, McLean JS, Darveau RP. 2019. Toll-like receptor-2 and -4 responses regulate neutrophil infiltration into the junctional epithelium and significantly contribute to the composition of the oral microbiota. J Periodontol. 90(10):1202–1212.
  • Chang WC, White MR, Moyo P, McClear S, Thiel S, Hartshorn KL, Takahashi K. 2010. Lack of the pattern recognition molecule mannose-binding lectin increases susceptibility to influenza A virus infection. BMC Immunol. 11:64.
  • Chehoud C, Rafail S, Tyldsley AS, Seykora JT, Lambris JD, Grice EA. 2013. Complement modulates the cutaneous microbiome and inflammatory milieu. Proc Natl Acad Sci USA. 110(37):15061–15066.
  • Chen T, Siddiqui H, Olsen I. 2017. In silico comparison of 19 Porphyromonas gingivalis strains in genomics, phylogenetics, phylogenomics and functional genomics. Front Cell Infect Microbiol. 7:28.
  • Cheng Q, Nelson D, Zhu S, Fischetti VA. 2005. Removal of group B streptococci colonizing the vagina and oropharynx of mice with a bacteriophage lytic enzyme. Antimicrob Agents Chemother. 49(1):111–117.
  • Cheng Q, Stafslien D, Purushothaman SS, Cleary P. 2002. The group B streptococcal C5a peptidase is both a specific protease and an invasin. Infect Immun. 70(5):2408–2413. Erratum in: Infect Immun 2002;70(6):3309.
  • Cho SB, Zheng Z, Ahn KJ, Choi MJ, Cho S, Kim DY, Lee HS, Bang D. 2013. Serum IgA reactivity against GroEL of Streptococcus sanguinis and human heterogeneous nuclear ribonucleoprotein A2/B1 in patients with Behçet disease. Br J Dermatol. 168(5):977–983.
  • Choi YJ, Kim JE, Lee SJ, Gong JE, Son HJ, Hong JT, Hwang DY. 2021. Dysbiosis of fecal microbiota from complement 3 knockout mice with constipation phenotypes contributes to development of defecation delay. Front Physiol. 12:650789.
  • Choteau L, Parny M, François N, Bertin B, Fumery M, Dubuquoy L, Takahashi K, Colombel JF, Jouault T, Poulain D, et al. 2016. Role of mannose-binding lectin in intestinal homeostasis and fungal elimination. Mucosal Immunol. 9(3):767–776.
  • Cole MF, Evans M, Fitzsimmons S, Johnson J, Pearce C, Sheridan MJ, Wientzen R, Bowden G. 1994. Pioneer oral streptococci produce immunoglobulin A1 protease. Infect Immun. 62(6):2165–2168.
  • Cole MF, Hsu SD, Baum BJ, Bowen WH, Sierra LI, Aquirre M, Gillespie G. 1981. Specific and nonspecific immune factors in dental plaque fluid and saliva from young and old populations. Infect Immun. 31(3):998–1002.
  • Curtis MA, Zenobia C, Darveau RP. 2011. The relationship of the oral microbiotia to periodontal health and disease. Cell Host Microbe. 10(4):302–306.
  • Daigo K, Inforzato A, Barajon I, Garlanda C, Bottazzi B, Meri S, Mantovani A. 2016. Pentraxins in the activation and regulation of innate immunity. Immunol Rev. 274(1):202–217.
  • Darveau RP, Pham TT, Lemley K, Reife RA, Bainbridge BW, Coats SR, Howald WN, Way SS, Hajjar AM. 2004. Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both toll-like receptors 2 and 4. Infect Immun. 72(9):5041–5051.
  • Dashper SG, Mitchell HL, Seers CA, Gladman SL, Seemann T, Bulach DM, Chandry PS, Cross KJ, Cleal SM, Reynolds EC. 2017. Porphyromonas gingivalis uses specific domain rearrangements and allelic exchange to generate diversity in surface virulence factors. Front Microbiol. 8:48.
  • Davis AE 3rd, Cai S, Liu D. 2007. C1 inhibitor: biologic activities that are independent of protease inhibition. Immunobiology. 212(4-5):313–323.
  • Domenech M, García E, Prieto A, Moscoso M. 2013. Insight into the composition of the intercellular matrix of Streptococcus pneumoniae biofilms. Environ Microbiol. 15(2):502–516.
  • Domenech M, Ramos-Sevillano E, García E, Moscoso M, Yuste J. 2013. Biofilm formation avoids complement immunity and phagocytosis of Streptococcus pneumoniae. Infect Immun. 81(7):2606–2615.
  • Dunkelberger JR, Song WC. 2010. Complement and its role in innate and adaptive immune responses. Cell Res. 20(1):34–50.
  • Dunn AB, Dunlop AL, Hogue CJ, Miller A, Corwin EJ. 2017. The microbiome and complement activation: a mechanistic model for preterm birth. Biol Res Nurs. 19(3):295–307.
  • Duque C, Stipp RN, Wang B, Smith DJ, Höfling JF, Kuramitsu HK, Duncan MJ, Mattos-Graner RO. 2011. Downregulation of GbpB, a component of the VicRK regulon, affects biofilm formation and cell surface characteristics of Streptococcus mutans. Infect Immun. 79(2):786–796.
  • Enersen M, Olsen I, Caugant DA. 2008. Genetic diversity of Porphyromonas gingivalis isolates recovered from single "refractory" periodontitis sites. Appl Environ Microbiol. 74(18):5817–5821.
  • Ericson T, Rundegren J. 1983. Characterization of a salivary agglutinin reacting with a serotype c strain of Streptococcus mutans. Eur J Biochem. 133(2):255–261.
  • Ermert D, Blom AM. 2016. C4b-binding protein: the good, the bad and the deadly. Novel functions of an old friend. Immunol Lett. 169:82–92.
  • Fábián TK, Hermann P, Beck A, Fejérdy P, Fábián G. 2012. Salivary defense proteins: their network and role in innate and acquired oral immunity. Int J Mol Sci. 13(4):4295–4320.
  • Farries TC, Atkinson JP. 1991. Evolution of the complement system. Immunol Today. 12(9):295–300.
  • Fernie-King BA, Seilly DJ, Willers C, Würzner R, Davies A, Lachmann PJ. 2001. Streptococcal inhibitor of complement (SIC) inhibits the membrane attack complex by preventing uptake of C567 onto cell membranes. Immunology. 103(3):390–398.
  • Ferreira VP, Pangburn MK, Cortés C. 2010. Complement control protein factor H: the good, the bad, and the inadequate. Mol Immunol. 47(13):2187–2197.
  • Fourie KR, Wilson HL. 2020. Understanding GroEL and DnaK stress response proteins as antigens for bacterial diseases. Vaccines. 8(4):773.
  • Gammazza AM, Bucchieri F, Grimaldi LM, Benigno A, de Macario EC, Macario AJ, Zummo G, Cappello F. 2012. The molecular anatomy of human Hsp60 and its similarity with that of bacterial orthologs and acetylcholine receptor reveal a potential pathogenetic role of anti-chaperonin immunity in myasthenia gravis. Cell Mol Neurobiol. 32(6):943–947.
  • Garred P, Genster N, Pilely K, Bayarri-Olmos R, Rosbjerg A, Ma YJ, Skjoedt MO. 2016. A journey through the lectin pathway of complement-MBL and beyond. Immunol Rev. 274(1):74–97.
  • Garred P, Tenner AJ, Mollnes TE. 2021. Therapeutic targeting of the complement system: from rare diseases to pandemics. Pharmacol Rev. 73(2):792–827.
  • GBD 2017 Oral Disorders Collaborators, Bernabe E, Marcenes W, Hernandez CR, Bailey J, Abreu LG, Alipour V, Amini S, Arabloo J, Arefi Z, et al. 2020. Global, regional, and national levels and trends in burden of oral conditions from 1990 to 2017: a systematic analysis for the Global Burden of Disease 2017 Study. J Dent Res. 99(4):362–373.
  • Ghias MH, Hyde MJ, Tomalin LE, Morgan BP, Alavi A, Lowes MA, Piguet V. 2020. Role of the complement pathway in inflammatory skin diseases: a focus on hidradenitis suppurativa. J Invest Dermatol. 140(3):531.e1–536.e1.
  • Giammarinaro P, Paton JC. 2002. Role of RegM, a homologue of the catabolite repressor protein CcpA, in the virulence of Streptococcus pneumoniae. Infect Immun. 70(10):5454–5461.
  • Giang J, Seelen MAJ, van Doorn MBA, Rissmann R, Prens EP, Damman J. 2018. Complement activation in inflammatory skin diseases. Front Immunol. 9:639.
  • Gleich-Theurer U, Aymanns S, Haas G, Mauerer S, Vogt J, Spellerberg B. 2009. Human serum induces streptococcal c5a peptidase expression. Infect Immun. 77(9):3817–3825.
  • Greer A, Irie K, Hashim A, Leroux BG, Chang AM, Curtis MA, Darveau RP. 2016. Site-specific neutrophil migration and CXCL2 expression in periodontal tissue. J Dent Res. 95(8):946–952.
  • Hajishengallis G, Hasturk H, Lambris JD, Apatzidou DA, Belibasakis GN, Bostanci N, Corby PM, Cutler CW, D’Aiuto F, Hajishengallis E, et al. 2021. C3-targeted therapy in periodontal disease: moving closer to the clinic. Trends Immunol. 42(10):856–864.
  • Hajishengallis G, Kajikawa T, Hajishengallis E, Maekawa T, Reis ES, Mastellos DC, Yancopoulou D, Hasturk H, Lambris JD. 2019. Complement-dependent mechanisms and interventions in periodontal disease. Front Immunol. 10:406.
  • Hajishengallis G, Lambris JD. 2016. More than complementing Tolls: complement-Toll-like receptor synergy and crosstalk in innate immunity and inflammation. Immunol Rev. 274(1):233–244.
  • Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, McIntosh ML, Alsam A, Kirkwood KL, Lambris JD, et al. 2011. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe. 10(5):497–506.
  • Hajishengallis G, Maekawa T, Abe T, Hajishengallis E, Lambris JD. 2015. Complement involvement in periodontitis: molecular mechanisms and rational therapeutic approaches. Adv Exp Med Biol. 865:57–74.
  • Hajishengallis G, Tapping RI, Harokopakis E, Nishiyama S, Ratti P, Schifferle RE, Lyle EA, Triantafilou M, Triantafilou K, Yoshimura F. 2006. Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Toll-like receptor 2-centred pattern recognition apparatus. Cell Microbiol. 8(10):1557–1570.
  • Harth-Chu EN, Alves LA, Theobaldo JD, Salomão MF, Höfling JF, King WF, Smith DJ, Mattos-Graner RO. 2019. PcsB expression diversity influences on Streptococcus mitis phenotypes associated with host persistence and virulence. Front Microbiol. 10:2567.
  • Hasegawa M, Yada S, Liu MZ, Kamada N, Muñoz-Planillo R, Do N, Núñez G, Inohara N. 2014. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage. Immunity. 41(4):620–632.
  • Hashizume-Takizawa T, Yamaguchi Y, Kobayashi R, Shinozaki-Kuwahara N, Saito M, Kurita-Ochiai T. 2019. Oral challenge with Streptococcus sanguinis induces aortic inflammation and accelerates atherosclerosis in spontaneously hyperlipidemic mice. Biochem Biophys Res Commun. 520(3):507–513.
  • Herrero ER, Slomka V, Boon N, Bernaerts K, Hernandez-Sanabria E, Quirynen M, Teughels W. 2016. Dysbiosis by neutralizing commensal mediated inhibition of pathobionts. Sci Rep. 6:38179.
  • Hickey MJ, Kubes P. 2009. Intravascular immunity: the host-pathogen encounter in blood vessels. Nat Rev Immunol. 9(5):364–375.
  • Honda-Ogawa M, Sumitomo T, Mori Y, Hamd DT, Ogawa T, Yamaguchi M, Nakata M, Kawabata S. 2017. Streptococcus pyogenes endopeptidase O contributes to evasion from complement-mediated bacteriolysis via binding to human complement factor C1q. J Biol Chem. 292(10):4244–4254.
  • Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science. 291(5505):881–884.
  • Hostetter MK, Dunny G, Nandiwada L. 2004 Jan 13. Human complement C3-degrading protein from Streptococcus pneumoniae. United States patent number 6,676,943. University of Minessota Inventors: Margaret K. Hostetter, Garry Dunny, Lakshmi S. Nandiwada. https://patents.google.com/patent/JP2001517449A/en.
  • Hovingh ES, van den Broek B, Jongerius I. 2016. Hijacking complement regulatory proteins for bacterial immune evasion. Front Microbiol. 7:2004.
  • Hovingh ES, van den Broek B, Kuipers B, Pinelli E, Rooijakkers SHM, Jongerius I. 2017. Acquisition of C1 inhibitor by Bordetella pertussis virulence associated gene 8 results in C2 and C4 consumption away from the bacterial surface. PLoS Pathog. 13(7):e1006531.
  • Howden BP, McEvoy CR, Allen DL, Chua K, Gao W, Harrison PF, Bell J, Coombs G, Bennett-Wood V, Porter JL, et al. 2011. Evolution of multidrug resistance during Staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog. 7(11):e1002359.
  • Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature. 486(7402):207–214.
  • Invernizzi R, Lloyd CM, Molyneaux PL. 2020. Respiratory microbiome and epithelial interactions shape immunity in the lungs. Immunology. 160(2):171–182.
  • Itzek A, Chen Z, Merritt J, Kreth J. 2017. Effect of salivary agglutination on oral streptococcal clearance by human polymorphonuclear neutrophil granulocytes. Mol Oral Microbiol. 32(3):197–210.
  • Jakubovics NS, Yassin SA, Rickard AH. 2014. Community interactions of oral streptococci. Adv Appl Microbiol. 87:43–110.
  • James BH, Papakyriacou P, Gardener MJ, Gliddon L, Weston CJ, Lalor PF. 2021. The contribution of liver sinusoidal endothelial cells to clearance of therapeutic antibody. Front Physiol. 12:753833.
  • Jeffery CJ. 2018. Protein moonlighting: what is it, and why is it important? Phil Trans R Soc B. 373(1738):20160523.
  • Johansson ME, Hansson GC. 2016. Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol. 16(10):639–649.
  • John CM, Liu M, Phillips NJ, Yang Z, Funk CR, Zimmerman LI, Griffiss JM, Stein DC, Jarvis GA. 2012. Lack of lipid A pyrophosphorylation and functional lptA reduces inflammation by Neisseria commensals. Infect Immun. 80(11):4014–4026.
  • Jusko M, Potempa J, Mizgalska D, Bielecka E, Ksiazek M, Riesbeck K, Garred P, Eick S, Blom AM. 2015. A metalloproteinase mirolysin of Tannerella forsythia inhibits all pathways of the complement system. J Immunol. 195(5):2231–2240.
  • Kaczorowski DJ, Afrazi A, Scott MJ, Kwak JH, Gill R, Edmonds RD, Liu Y, Fan J, Billiar TR. 2010. Pivotal advance: the pattern recognition receptor ligands lipopolysaccharide and polyinosine-polycytidylic acid stimulate factor B synthesis by the macrophage through distinct but overlapping mechanisms. J Leukoc Biol. 88(4):609–618.
  • Kahler CM, Nawrocki KL, Anandan A, Vrielink A, Shafer WM. 2018. Structure-function relationships of the Neisserial EptA enzyme responsible for phosphoethanolamine decoration of lipid a: rationale for drug targeting. Front Microbiol. 9:1922.
  • Kampinga HH, Craig EA. 2010. The HSP70 chaperone machinery: j proteins as drivers of functional specificity. Nat Rev Mol Cell Biol. 11(8):579–592. Erratum in: Nat Rev Mol Cell Biol. 2010;11(10):750.
  • Kaur G, Grover V, Bhaskar N, Kaur RK, Jain A. 2018. Periodontal infectogenomics. Inflamm Regen. 38:8.
  • Kemper C, Atkinson JP, Hourcade DE. 2010. Properdin: emerging roles of a pattern-recognition molecule. Annu Rev Immunol. 28:131–155.
  • Klein MI, Hwang G, Santos PH, Campanella OH, Koo H. 2015. Streptococcus mutans-derived extracellular matrix in cariogenic oral biofilms. Front Cell Infect Microbiol. 5:10.
  • Kolev M, Le Friec G, Kemper C. 2014. Complement–tapping into new sites and effector systems. Nat Rev Immunol. 14(12):811–820.
  • Kopp ZA, Jain U, Van Limbergen J, Stadnyk AW. 2015. Do antimicrobial peptides and complement collaborate in the intestinal mucosa? Front Immunol. 6:17.
  • Kouser L, Madhukaran SP, Shastri A, Saraon A, Ferluga J, Al-Mozaini M, Kishore U. 2015. Emerging and novel functions of complement protein C1q. Front Immunol. 6:317.
  • Kreth J, Giacaman RA, Raghavan R, Merritt J. 2017. The road less traveled - defining molecular commensalism with Streptococcus sanguinis. Mol Oral Microbiol. 32(3):181–196.
  • Kreth J, Merritt J, Qi F. 2009. Bacterial and host interactions of oral streptococci. DNA Cell Biol. 28(8):397–403.
  • Kuipers S, Aerts PC, Dijk H. 2003. Differential microorganism-induced mannose-binding lectin activation. FEMS Immunol Med Microbiol. 36(1-2):33–39.
  • Lai KN, Tang SC, Schena FP, Novak J, Tomino Y, Fogo AB, Glassock RJ. 2016. IgA nephropathy. Nat Rev Dis Primers. 2:16001.
  • Lambris JD, Ricklin D, Geisbrecht BV. 2008. Complement evasion by human pathogens. Nat Rev Microbiol. 6(2):132–142.
  • Lamont RJ, Koo H, Hajishengallis G. 2018. The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol. 16(12):745–759.
  • Langeggen H, Berge KE, Johnson E, Hetland G. 2002. Human umbilical vein endothelial cells express complement receptor 1 (CD35) and complement receptor 4 (CD11c/CD18) in vitro. Inflammation. 26(3):103–110.
  • Langeggen H, Pausa M, Johnson E, Casarsa C, Tedesco F. 2000. The endothelium is an extrahepatic site of synthesis of the seventh component of the complement system. Clin Exp Immunol. 121(1):69–76.
  • Leito JT, Ligtenberg AJ, van Houdt M, van den Berg TK, Wouters D. 2011. The bacteria binding glycoprotein salivary agglutinin (SAG/gp340) activates complement via the lectin pathway. Mol Immunol. 49(1-2):185–190.
  • Lewis LA, Choudhury B, Balthazar JT, Martin LE, Ram S, Rice PA, Stephens DS, Carlson R, Shafer WM. 2009. Phosphoethanolamine substitution of lipid A and resistance of Neisseria gonorrhoeae to cationic antimicrobial peptides and complement-mediated killing by normal human serum. Infect Immun. 77(3):1112–1120.
  • Lewis LA, Ram S. 2020. Complement interactions with the pathogenic Neisseriae: clinical features, deficiency states, and evasion mechanisms. FEBS Lett. 594(16):2670–2694.
  • Lewis LA, Shafer WM, Dutta Ray T, Ram S, Rice PA. 2013. Phosphoethanolamine residues on the lipid A moiety of Neisseria gonorrhoeae lipooligosaccharide modulate binding of complement inhibitors and resistance to complement killing. Infect Immun. 81(1):33–42.
  • Li L, Cong B, Yu X, Deng S, Liu M, Wang Y, Wang W, Gao M, Xu Y. 2021. The expression of membrane-bound complement regulatory proteins CD46, CD55 and CD59 in oral lichen planus. Arch Oral Biol. 124:105064.
  • Liang S, Krauss JL, Domon H, McIntosh ML, Hosur KB, Qu H, Li F, Tzekou A, Lambris JD, Hajishengallis G. 2011. The C5a receptor impairs IL-12-dependent clearance of Porphyromonas gingivalis and is required for induction of periodontal bone loss. J Immunol. 186(2):869–877.
  • Ligtenberg AJ, Veerman EC, Nieuw Amerongen AV, Mollenhauer J. 2007. Salivary agglutinin/glycoprotein-340/DMBT1: a single molecule with variable composition and with different functions in infection, inflammation and cancer. Biol Chem. 388(12):1275–1289.
  • Lim J, Iyer A, Suen JY, Seow V, Reid RC, Brown L, Fairlie DP. 2013. C5aR and C3aR antagonists each inhibit diet-induced obesity, metabolic dysfunction, and adipocyte and macrophage signaling. Faseb J. 27(2):822–831.
  • Lindholm M, Min Aung K, Nyunt Wai S, Oscarsson J. 2019. Role of OmpA1 and OmpA2 in Aggregatibacter actinomycetemcomitans and Aggregatibacter aphrophilus serum resistance. J Oral Microbiol. 11(1):1536192.
  • Liu G, Tang CM, Exley RM. 2015. Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus. Microbiology. 161(7):1297–1312.
  • Loimaranta V, Jakubovics NS, Hytönen J, Finne J, Jenkinson HF, Strömberg N. 2005. Fluid- or surface-phase human salivary scavenger protein gp340 exposes different bacterial recognition properties. Infect Immun. 73(4):2245–2252.
  • Lu K, Knutson CG, Wishnok JS, Fox JG, Tannenbaum SR. 2012. Serum metabolomics in a Helicobacter hepaticus mouse model of inflammatory bowel disease reveal important changes in the microbiome, serum peptides, and intermediary metabolism. J Proteome Res. 11(10):4916–4926.
  • Lukácsi S, Mácsik-Valent B, Nagy-Baló Z, Kovács KG, Kliment K, Bajtay Z, Erdei A. 2020. Utilization of complement receptors in immune cell-microbe interaction. FEBS Lett. 594(16):2695–2713.
  • Lynch DJ, Fountain TL, Mazurkiewicz JE, Banas JA. 2007. Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol Lett. 268(2):158–165.
  • Lynch NJ, Roscher S, Hartung T, Morath S, Matsushita M, Maennel DN, Kuraya M, Fujita T, Schwaeble WJ. 2004. L-ficolin specifically binds to lipoteichoic acid, a cell wall constituent of Gram-positive bacteria, and activates the lectin pathway of complement. J Immunol. 172(2):1198–1202.
  • Lynskey NN, Reglinski M, Calay D, Siggins MK, Mason JC, Botto M, Sriskandan S. 2017. Multi-functional mechanisms of immune evasion by the streptococcal complement inhibitor C5a peptidase. PLoS Pathog. 13(8):e1006493.
  • Lysenko ES, Ratner AJ, Nelson AL, Weiser JN. 2005. The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathog. 1(1):e1.
  • Ma YJ, Lee BL, Garred P. 2017. An overview of the synergy and crosstalk between pentraxins and collectins/ficolins: their functional relevance in complement activation. Exp Mol Med. 49(4):e320.
  • Marquart ME. 2021. Pathogenicity and virulence of Streptococcus pneumoniae: cutting to the chase on proteases. Virulence. 12(1):766–787.
  • Mattos-Graner RO, Duncan MJ. 2017. Two-component signal transduction systems in oral bacteria. J Oral Microbiol. 9(1):1400858.
  • Mattos-Graner RO, Jin S, King WF, Chen T, Smith DJ, Duncan MJ. 2001. Cloning of the Streptococcus mutans gene encoding glucan binding protein B and analysis of genetic diversity and protein production in clinical isolates. Infect Immun. 69(11):6931–6941.
  • Mattos-Graner RO, Porter KA, Smith DJ, Hosogi Y, Duncan MJ. 2006. Functional analysis of glucan binding protein B from Streptococcus mutans. J Bacteriol. 188(11):3813–3825.
  • Mattos-Graner RO, Smith DJ, King WF, Mayer MP. 2000. Water-insoluble glucan synthesis by mutans streptococcal strains correlates with caries incidence in 12- to 30-month-old children. J Dent Res. 79(6):1371–1377.
  • McDowell JV, Huang B, Fenno JC, Marconi RT. 2009. Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect Immun. 77(4):1417–1425.
  • Meisel JS, Sfyroera G, Bartow-McKenney C, Gimblet C, Bugayev J, Horwinski J, Kim B, Brestoff JR, Tyldsley AS, Zheng Q, et al. 2018. Commensal microbiota modulate gene expression in the skin. Microbiome. 6(1):20.
  • Merle NS, Church SE, Fremeaux-Bacchi V, Roumenina LT. 2015. Complement system part I - molecular mechanisms of activation and regulation. Front Immunol. 6:262.
  • Miller JH, Avilés-Reyes A, Scott-Anne K, Gregoire S, Watson GE, Sampson E, Progulske-Fox A, Koo H, Bowen WH, Lemos JA, et al. 2015. The collagen binding protein Cnm contributes to oral colonization and cariogenicity of Streptococcus mutans OMZ175. Infect Immun. 83(5):2001–2010.
  • Min H, Baek K, Lee A, Seok YJ, Choi Y. 2021. Genomic characterization of four Escherichia coli strains isolated from oral lichen planus biopsies. J Oral Microbiol. 13(1):1905958.
  • Misaki T, Naka S, Kuroda K, Nomura R, Shiooka T, Naito Y, Suzuki Y, Yasuda H, Isozaki T, Nakano K. 2015. Distribution of Streptococcus mutans strains with collagen-binding proteins in the oral cavity of IgA nephropathy patients. Clin Exp Nephrol. 19(5):844–850.
  • Mollenhauer J, Holmskov U, Wiemann S, Krebs I, Herbertz S, Madsen J, Kioschis P, Coy JF, Poustka A. 1999. The genomic structure of the DMBT1 gene: evidence for a region with susceptibility to genomic instability. Oncogene. 18(46):6233–6240.
  • Mollenhauer J, Wiemann S, Scheurlen W, Korn B, Hayashi Y, Wilgenbus KK, von Deimling A, Poustka A. 1997. DMBT1, a new member of the SRCR superfamily, on chromosome 10q25.3-26.1 is deleted in malignant brain tumours. Nat Genet. 17(1):32–39.
  • Momeni SS, Ghazal T, Grenett H, Whiddon J, Moser SA, Childers NK. 2019. Streptococcus mutans serotypes and collagen-binding proteins Cnm/Cbm in children with caries analysed by PCR. Mol Oral Microbiol. 34(2):64–73.
  • Morgan BP, Gasque P. 1997. Extrahepatic complement biosynthesis: where, when and why? Clin Exp Immunol. 107(1):1–7.
  • Morgan BP, Harris CL. 2015. Complement, a target for therapy in inflammatory and degenerative diseases. Nat Rev Drug Discov. 14(12):857–877.
  • Moutsopoulos NM, Konkel JE. 2018. Tissue-specific immunity at the oral mucosal barrier. Trends Immunol. 39(4):276–287.
  • Nagasawa Y, Misaki T, Ito S, Naka S, Wato K, Nomura R, Matsumoto-Nakano M, Nakano K. 2022. Title IgA nephropathy and oral bacterial species related to dental caries and periodontitis. IJMS. 23(2):725.
  • Nagasawa Y, Nomura R, Misaki T, Ito S, Naka S, Wato K, Okunaka M, Watabe M, Fushimi K, Tsuzuki K, et al. 2021. Relationship between IgA nephropathy and Porphyromonas gingivalis; red complex of periodontopathic bacterial species. IJMS. 22(23):13022.
  • Naginyte M, Do T, Meade J, Devine DA, Marsh PD. 2019. Enrichment of periodontal pathogens from the biofilms of healthy adults. Sci Rep. 9(1):5491.
  • Naka S, Wato K, Misaki T, Ito S, Matsuoka D, Nagasawa Y, Nomura R, Matsumoto-Nakano M, Nakano K. 2021. Streptococcus mutans induces IgA nephropathy-like glomerulonephritis in rats with severe dental caries. Sci Rep. 11(1):5784.
  • Nakano K, Inaba H, Nomura R, Nemoto H, Takeda M, Yoshioka H, Matsue H, Takahashi T, Taniguchi K, Amano A, et al. 2006. Detection of cariogenic Streptococcus mutans in extirpated heart valve and atheromatous plaque specimens. J Clin Microbiol. 44(9):3313–3317.
  • Nakano K, Nemoto H, Nomura R, Inaba H, Yoshioka H, Taniguchi K, Amano A, Ooshima T. 2009. Detection of oral bacteria in cardiovascular specimens. Oral Microbiol Immunol. 24(1):64–68.
  • Nakano K, Nomura R, Matsumoto M, Ooshima T. 2010. Roles of oral bacteria in cardiovascular diseases–from molecular mechanisms to clinical cases: cell-surface structures of novel serotype k Streptococcus mutans strains and their correlation to virulence. J Pharmacol Sci. 113(2):120–125.
  • Nakano K, Nomura R, Nemoto H, Mukai T, Yoshioka H, Shudo Y, Hata H, Toda K, Taniguchi K, Amano A, et al. 2007. Detection of novel serotype k Streptococcus mutans in infective endocarditis patients. J Med Microbiol. 56(Pt 10):1413–1415.
  • Nayak A, Ferluga J, Tsolaki AG, Kishore U. 2010. The non-classical functions of the classical complement pathway recognition subcomponent C1q. Immunol Lett. 131(2):139–150.
  • Neth O, Jack DL, Dodds AW, Holzel H, Klein NJ, Turner MW. 2000. Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun. 68(2):688–693.
  • Nilsson SC, Sim RB, Lea SM, Fremeaux-Bacchi V, Blom AM. 2011. Complement factor I in health and disease. Mol Immunol. 48(14):1611–1620.
  • Nishimoto AT, Rosch JW, Tuomanen EI. 2020. Pneumolysin: pathogenesis and therapeutic target. Front Microbiol. 11:1543.
  • Nobbs A, Kreth J. 2019. Genetics of sanguinis-group streptococci in health and disease. Microbiol Spectr. 7(1):1–15.
  • Nobbs AH, Lamont RJ, Jenkinson HF. 2009. Streptococcus adherence and colonization. Microbiol Mol Biol Rev. 73(3):407–450, Table of Contents. Table of Contents.
  • Nomura R, Nakano K, Naka S, Nemoto H, Masuda K, Lapirattanakul J, Alaluusua S, Matsumoto M, Kawabata S, Ooshima T. 2012. Identification and characterization of a collagen-binding protein, Cbm, in Streptococcus mutans. Mol Oral Microbiol. 27(4):308–323.
  • Nomura R, Otsugu M, Hamada M, Matayoshi S, Teramoto N, Iwashita N, Naka S, Matsumoto-Nakano M, Nakano K. 2020. Potential involvement of Streptococcus mutans possessing collagen binding protein Cnm in infective endocarditis. Sci Rep. 10(1):19118.
  • Oliveira LT, Alves LA, Harth-Chu EN, Nomura R, Nakano K, Mattos-Graner RO. 2021. VicRK and CovR polymorphisms in Streptococcus mutans strains associated with cardiovascular infections. J Med Microbiol. 70(12):1–12.
  • Olsen I, Chen T, Tribble GD. 2018. Genetic exchange and reassignment in Porphyromonas gingivalis. J Oral Microbiol. 10(1):1457373.
  • Olsen I, Singhrao SK. 2020. Is there a link between genetic defects in the complement cascade and Porphyromonas gingivalis in Alzheimer’s disease? J Oral Microbiol. 12(1):1676486.
  • Oroszlán M, Daha MR, Cervenak L, Prohászka Z, Füst G, Roos A. 2007. MBL and C1q compete for interaction with human endothelial cells. Mol Immunol. 44(6):1150–1158.
  • Oscarsson J, Claesson R, Lindholm M, Höglund Åberg C, Johansson A. 2019. Tools of Aggregatibacter actinomycetemcomitans to evade the host response. JCM. 8(7):1079.
  • Otsuji K, Fukuda K, Maruoka T, Ogawa M, Saito M. 2020. Acquisition of genetic mutations in Group A streptococci at infection site and subsequent systemic dissemination of the mutants with lethal mutations in a streptococcal toxic shock syndrome mouse model. Microb Pathog. 143:104116.
  • Oyelakin A, Horeth E, Song EC, Min S, Che M, Marzullo B, Lessard CJ, Rasmussen A, Radfar L, Scofield RH, et al. 2021. Transcriptomic and network analysis of minor salivary glands of patients with primary Sjögren’s syndrome. Front Immunol. 11:606268.
  • Park JI, Kim TY, Oh B, Cho H, Kim JE, Yoo SH, Lee JP, Kim YS, Chun J, Kim BS, et al. 2020. Comparative analysis of the tonsillar microbiota in IgA nephropathy and other glomerular diseases. Sci Rep. 10(1):16206.
  • Pavlova SI, Wilkening RV, Federle MJ, Lu Y, Schwartz J, Tao L. 2019. Streptococcus endopeptidases promote HPV infection in vitro. Microbiologyopen. 8(1):e00628.
  • Petrisko TJ, Gomez-Arboledas A, Tenner AJ. 2021. Complement as a powerful "influencer" in the brain during development, adulthood and neurological disorders. Adv Immunol. 152:157–222.
  • Polley S, Louzada S, Forni D, Sironi M, Balaskas T, Hains DS, Yang F, Hollox EJ. 2015. Evolution of the rapidly mutating human salivary agglutinin gene (DMBT1) and population subsistence strategy. Proc Natl Acad Sci USA. 112(16):5105–5110.
  • Potempa M, Potempa J. 2012. Protease-dependent mechanisms of complement evasion by bacterial pathogens. Biol Chem. 393(9):873–888.
  • Potempa M, Potempa J, Kantyka T, Nguyen KA, Wawrzonek K, Manandhar SP, Popadiak K, Riesbeck K, Eick S, Blom AM. 2009. Interpain A, a cysteine proteinase from Prevotella intermedia, inhibits complement by degrading complement factor C3. PLoS Pathog. 5(2):e1000316. Erratum in: PLoS Pathog. 2009;5(3).
  • Pothineni NVK, Subramany S, Kuriakose K, Shirazi LF, Romeo F, Shah PK, Mehta JL. 2017. Infections, atherosclerosis, and coronary heart disease. Eur Heart J. 38(43):3195–3201.
  • Pouw RB, Ricklin D. 2021. Tipping the balance: intricate roles of the complement system in disease and therapy. Semin Immunopathol. 43(6):757–771.
  • Prohászka Z, Singh M, Nagy K, Kiss E, Lakos G, Duba J, Füst G. 2002. Heat shock protein 70 is a potent activator of the human complement system. Cell Stress Chaper. 7(1):17–22.
  • Rajani R, Klein JL. 2020. Infective endocarditis: a contemporary update. Clin Med. 20(1):31–35.
  • Ramji DP, Davies TS. 2015. Cytokines in atherosclerosis: key players in all stages of disease and promising therapeutic targets. Cytokine Growth Factor Rev. 26(6):673–685.
  • Ramsey MM, Whiteley M. 2009. Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc Natl Acad Sci USA. 106(5):1578–1583.
  • Rautemaa R, Meri S. 1996. Protection of gingival epithelium against complement-mediated damage by strong expression of the membrane attack complex inhibitor protectin (CD59). J Dent Res. 75(1):568–574.
  • Reichhardt MP, Holmskov U, Meri S. 2017. SALSA-A dance on a slippery floor with changing partners. Mol Immunol. 89:100–110.
  • Reichhardt MP, Loimaranta V, Thiel S, Finne J, Meri S, Jarva H. 2012. The salivary scavenger and agglutinin binds MBL and regulates the lectin pathway of complement in solution and on surfaces. Front Immunol. 3:205.
  • Reichhardt MP, Meri S. 2016. SALSA: a regulator of the early steps of complement activation on mucosal surfaces. Front Immunol. 7:85.
  • Ricklin D, Hajishengallis G, Yang K, Lambris JD. 2010. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 11(9):785–797.
  • Ricklin D, Reis ES, Lambris JD. 2016. Complement in disease: a defence system turning offensive. Nat Rev Nephrol. 12(7):383–401.
  • Ritchie RF, Palomaki GE, Neveux LM, Navolotskaia O, Ledue TB, Craig WY. 2004. Reference distributions for complement proteins C3 and C4: a practical, simple and clinically relevant approach in a large cohort. J Clin Lab Anal. 18(1):1–8.
  • Rosenzweig R, Nillegoda NB, Mayer MP, Bukau B. 2019. The Hsp70 chaperone network. Nat Rev Mol Cell Biol. 20(11):665–680.
  • Rowe HM, Karlsson E, Echlin H, Chang TC, Wang L, van Opijnen T, Pounds SB, Schultz-Cherry S, Rosch JW. 2019. Bacterial factors required for transmission of Streptococcus pneumoniae in mammalian hosts. Cell Host Microbe. 25(6):884–891.e6.
  • Roy P, Orecchioni M, Ley K. 2022. How the immune system shapes atherosclerosis: roles of innate and adaptive immunity. Nat Rev Immunol. 22(4):251–265.
  • Rukke HV, Hegna IK, Petersen FC. 2012. Identification of a functional capsule locus in Streptococcus mitis. Mol Oral Microbiol. 27(2):95–108.
  • Rukke HV, Kalluru RS, Repnik U, Gerlini A, José RJ, Periselneris J, Marshall H, Griffiths G, Oggioni MR, Brown JS, et al. 2014. Protective role of the capsule and impact of serotype 4 switching on Streptococcus mitis. Infect Immun. 82(9):3790–3801.
  • Saitou M, Gaylord EA, Xu E, May AJ, Neznanova L, Nathan S, Grawe A, Chang J, Ryan W, Ruhl S, et al. 2020. Functional specialization of human salivary glands and origins of proteins intrinsic to human saliva. Cell Rep. 33(7):108402.
  • Samantha A, Vrielink A. 2020. Lipid A phosphoethanolamine transferase: regulation, structure and immune response. J Mol Biol. 432(18):5184–5196.
  • Sato Y, Okamoto K, Kagami A, Yamamoto Y, Igarashi T, Kizaki H. 2004. Streptococcus mutans strains harboring collagen-binding adhesin. J Dent Res. 83(7):534–539.
  • Sato Y, Yamamoto Y, Kizaki H. 1997. Cloning and sequence analysis of the gbpC gene encoding a novel glucan-binding protein of Streptococcus mutans. Infect Immun. 65(2):668–675.
  • Senadheera MD, Guggenheim B, Spatafora GA, Huang YC, Choi J, Hung DC, Treglown JS, Goodman SD, Ellen RP, Cvitkovitch DA. 2005. VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol. 187(12):4064–4076.
  • Shah DSH, Russell RRB. 2004. A novel glucan-binding protein with lipase activity from the oral pathogen Streptococcus mutans. Microbiology. 150(Pt 6):1947–1956.
  • Shainheit MG, Mulé M, Camilli A. 2014. The core promoter of the capsule operon of Streptococcus pneumoniae is necessary for colonization and invasive disease. Infect Immun. 82(2):694–705.
  • Shakhnovich EA, King SJ, Weiser JN. 2002. Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect Immun. 70(12):7161–7164.
  • Shapira J, Berenstein-Ajzman G, Engelhard D, Cahan S, Kalickman I, Barak V. 2003. Cytokine levels in gingival crevicular fluid of erupting primary teeth correlated with systemic disturbances accompanying teething. Pediatr Dent. 25(5):441–448.
  • Sharma S, Bhatnagar R, Gaur D. 2020. Complement evasion strategies of human pathogenic bacteria. Indian J Microbiol. 60(3):283–296.
  • Shim K, Begum R, Yang C, Wang H. 2020. Complement activation in obesity, insulin resistance, and type 2 diabetes mellitus. World J Diabetes. 11(1):1–12.
  • Shingu M, Nonaka S, Nishimukai H, Nobunaga M, Kitamura H, Tomo-Oka K. 1992. Activation of complement in normal serum by hydrogen peroxide and hydrogen peroxide-related oxygen radicals produced by activated neutrophils. Clin Exp Immunol. 90(1):72–78.
  • Shishido SN, Varahan S, Yuan K, Li X, Fleming SD. 2012. Humoral innate immune response and disease. Clin Immunol. 144(2):142–158.
  • Sina C, Kemper C, Derer S. 2018. The intestinal complement system in inflammatory bowel disease: shaping intestinal barrier function. Semin Immunol. 37:66–73.
  • Singh A, Wyant T, Anaya-Bergman C, Aduse-Opoku J, Brunner J, Laine ML, Curtis MA, Lewis JP. 2011. The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect Immun. 79(11):4533–4542.
  • Skov Sørensen UB, Yao K, Yang Y, Tettelin H, Kilian M. 2016. Capsular polysaccharide expression in commensal Streptococcus species: genetic and antigenic similarities to Streptococcus pneumoniae. mBio. 7(6):e01844–e01916.
  • Smith DJ, Akita H, King WF, Taubman MA. 1994. Purification and antigenicity of a novel glucan-binding protein of Streptococcus mutans. Infect Immun. 62(6):2545–2552.
  • Soares MP, Bach FH. 1999. C1q receptors and endothelial cell activation. J Lab Clin Med. 133(6):520–522.
  • Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. 1998. Microbial complexes in subgingival plaque. J Clin Periodontol. 25(2):134–144.
  • Sonesson M, Ericson D, Kinnby B, Wickström C. 2011. Glycoprotein 340 and sialic acid in minor-gland and whole saliva of children, adolescents, and adults. Eur J Oral Sci. 119(6):435–440.
  • Sorg RA, Gallay C, Van Maele L, Sirard JC, Veening JW. 2020. Synthetic gene-regulatory networks in the opportunistic human pathogen Streptococcus pneumoniae. Proc Natl Acad Sci USA. 117(44):27608–27619.
  • Stipp RN, Boisvert H, Smith DJ, Höfling JF, Duncan MJ, Mattos-Graner RO. 2013. CovR and VicRK regulate cell surface biogenesis genes required for biofilm formation in Streptococcus mutans. PLoS One. 8(3):e58271.
  • Suárez LJ, Arboleda S, Angelov N, Arce RM. 2021. Oral versus gastrointestinal mucosal immune niches in homeostasis and allostasis. Front Immunol. 12:705206.
  • Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM. 2006. Genome-wide analysis of group a streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog. 2(1):e5.
  • Sünderhauf A, Skibbe K, Preisker S, Ebbert K, Verschoor A, Karsten CM, Kemper C, Huber-Lang M, Basic M, Bleich A, et al. 2017. Regulation of epithelial cell expressed C3 in the intestine - relevance for the pathophysiology of inflammatory bowel disease? Mol Immunol. 90:227–238.
  • Thielens NM, Gaboriaud C, Rossi V. 2018. C1s. Chapter 11. In: Barnum S, Schein T, editors. The complement factsbook. 2nd ed. Cambridge, Massachusetts: Elsevier; p. 107–105.
  • Tikhomirova A, Kidd SP. 2013. Haemophilus influenzae and Streptococcus pneumoniae: living together in a biofilm. Pathog Dis. 69(2):114–126.
  • Toapanta FR, Ross TM. 2006. Complement-mediated activation of the adaptive immune responses: role of C3d in linking the innate and adaptive immunity. Immunol Res. 36(1-3):197–210.
  • Uriarte SM, Edmisson JS, Jimenez-Flores E. 2016. Human neutrophils and oral microbiota: a constant tug-of-war between a harmonious and a discordant coexistence. Immunol Rev. 273(1):282–298.
  • Valm AM. 2019. The structure of dental plaque microbial communities in the transition from health to dental caries and periodontal disease. J Mol Biol. 431(16):2957–2969.
  • Vasta GR, Quesenberry M, Ahmed H, O'Leary N. 1999. C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev Comp Immunol. 23(4-5):401–420.
  • Veldhuizen EJ, van Eijk M, Haagsman HP. 2011. The carbohydrate recognition domain of collectins. FEBS J. 278(20):3930–3941.
  • Venkatraman Girija U, Gingras AR, Marshall JE, Panchal R, Sheikh MA, Harper JA, Gál P, Schwaeble WJ, Mitchell DA, Moody PC, et al. 2013. Structural basis of the C1q/C1s interaction and its central role in assembly of the C1 complex of complement activation. Proc Natl Acad Sci USA. 110(34):13916–13920. Erratum in: Proc Natl Acad Sci USA. 2016;113(43):E6722–E6723.
  • Ventura TMDS, Cassiano LPS, Souza E Silva CM, Taira EA, Leite AL, Rios D, Buzalaf MAR. 2017. The proteomic profile of the acquired enamel pellicle according to its location in the dental arches. Arch Oral Biol. 79:20–29.
  • Wessels MR, Moses AE, Goldberg JB, DiCesare TJ. 1991. Hyaluronic acid capsule is a virulence factor for mucoid group A streptococci. Proc Natl Acad Sci USA. 88(19):8317–8321.
  • White JC, Niven CF Jr. 1946. Streptococcus S.B.E.: a Streptococcus associated with subacute bacterial endocarditis. J Bacteriol. 51(6):717–722.
  • Williams BD, Challacombe SJ, Slaney JM, Lachmann PJ, Lehner T. 1975. Immunoconglutinins and C3 in human saliva. Clin Exp Immunol. 19(3):423–433.
  • Wong EKS, Kavanagh D. 2018. Diseases of complement dysregulation-an overview. Semin Immunopathol. 40(1):49–64.
  • Wu H, Tang D, Zheng F, Li S, Zhang X, Yin L, Liu F, Dai Y. 2021. Identification of a novel interplay between intestinal bacteria and metabolites in Chinese patients with IgA nephropathy via integrated microbiome and metabolome approaches. Ann Transl Med. 9(1):32.
  • Wu K, Xu H, Zheng Y, Wang L, Zhang X, Yin Y. 2016. CpsR, a GntR family regulator, transcriptionally regulates capsular polysaccharide biosynthesis and governs bacterial virulence in Streptococcus pneumoniae. Sci Rep. 6:29255.
  • Xie CB, Jane-Wit D, Pober JS. Complement membrane attack complex: New roles, mechanisms of action, and therapeutic targets. Am J Pathol. 2020 Jun;190(6):1138-1150. doi: 10.1016/j.ajpath.2020.02.006. Epub 2020 Mar 16.
  • Xu RR, Yang WD, Niu KX, Wang B, Wang WM. 2018. An update on the evolution of glucosyltransferase (Gtf) genes in Streptococcus. Front Microbiol. 9:2979.
  • Yin W, Ghebrehiwet B, Peerschke EI. 2008. Expression of complement components and inhibitors on platelet microparticles. Platelets. 19(3):225–233.
  • Yongqing T, Drentin N, Duncan RC, Wijeyewickrema LC, Pike RN. 2012. Mannose-binding lectin serine proteases and associated proteins of the lectin pathway of complement: two genes, five proteins and many functions? Biochim Biophys Acta. 1824(1):253–262.
  • Yost S, Duran-Pinedo AE, Teles R, Krishnan K, Frias-Lopez J. 2015. Functional signatures of oral dysbiosis during periodontitis progression revealed by microbial metatranscriptome analysis. Genome Med. 7(1):27. Erratum in: Genome Med. 2015;7(1):111.
  • Yother J. 2011. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol. 65:563–581.
  • Yuste J, Botto M, Bottoms SE, Brown JS. 2007. Serum amyloid P aids complement-mediated immunity to Streptococcus pneumoniae. PLoS Pathog. 3(9):1208–1219.
  • Zaura E, Keijser BJ, Huse SM, Crielaard W. 2009. Defining the healthy "core microbiome" of oral microbial communities. BMC Microbiol. 9:259.
  • Zaura E, Nicu EA, Krom BP, Keijser BJ. 2014. Acquiring and maintaining a normal oral microbiome: current perspective. Front Cell Infect Microbiol. 4:85.
  • Zenobia C, Luo XL, Hashim A, Abe T, Jin L, Chang Y, Jin ZC, Sun JX, Hajishengallis G, Curtis MA, et al. 2013. Commensal bacteria-dependent select expression of CXCL2 contributes to periodontal tissue homeostasis. Cell Microbiol. 15(8):1419–1426.
  • Zhan Y, Zhang R, Lv H, Song X, Xu X, Chai L, Lv W, Shang Z, Jiang Y, Zhang R. 2014. Prioritization of candidate genes for periodontitis using multiple computational tools. J Periodontol. 85(8):1059–1069.
  • Zhang X, Kimura Y, Fang C, Zhou L, Sfyroera G, Lambris JD, Wetsel RA, Miwa T, Song WC. 2007. Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood. 110(1):228–236. Erratum in: Blood. 2007;110(12):3841.
  • Zheng D, Liwinski T, Elinav E. 2020. Interaction between microbiota and immunity in health and disease. Cell Res. 30(6):492–506.
  • Zheng W. 2017. Dissertation at intestinal complement modulates colitis by targeting the gut microbiota. Cambridge, Massachusetts: Harvard University, http://nrs.harvard.edu/urn-3:HUL.InstRepos:39945359 (Accessed date: Aug 18, 2022).
  • Zheng Y, Zhang X, Wang X, Wang L, Zhang J, Yin Y. 2017. ComE, an essential response regulator, negatively regulates the expression of the capsular polysaccharide locus and attenuates the bacterial virulence in Streptococcus pneumoniae. Front Microbiol. 8:277.
  • Zhu Y, Thangamani S, Ho B, Ding JL. 2005. The ancient origin of the complement system. EMBO J. 24(2):382–394.
  • Zhuang PL, Yu LX, Liao JK, Zhou Y, Lin HC. 2018. Relationship between the genetic polymorphisms of vicR and vicK Streptococcus mutans genes and early childhood caries in two-year-old children. BMC Oral Health. 18(1):39.
  • Zipfel PF, Skerka C. 2009. Complement regulators and inhibitory proteins. Nat Rev Immunol. 9(10):729–740.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.