Skip to main content
SpringerLink
Log in

Adherence and Invasion of Streptococci to Eukaryotic Cells and their Role in Disease Pathogenesis

  • Chapter
  • First Online:
Host-Pathogen Interactions in Streptococcal Diseases

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 368))

Abstract

Streptococcal adhesion, invasion, intracellular trafficking, dissemination, and persistence in eukaryotic cells have a variety of implications in the infection pathogenesis. While cell adhesion establishes the initial host contact, adhering bacteria exploit the host cell for their own benefit. Internalization into the host cell is an essential step for bacterial survival and subsequent dissemination and persistence, thus playing a key role in the course of infection. This chapter summarizes the current knowledge about the diverse mechanisms of streptococcal adhesion to and invasion into different eukaryotic cells and the impact on dissemination and persistence which is reflected by consequences for the pathogenesis of streptococcal infections.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abbot EL, Smith WD, Siou GP, Chriboga C, Smith RJ, Wilson JA, Hirts BH, Kehoe MA (2007) Pili mediate specific adhesion of Streptococcus pyogenes to human tonsils and skin. Cell Microbiol 9:1822–1833

    PubMed  CAS  Google Scholar 

  • Agerer F, Lux S, Michel A, Rohde M, Ohlsen K, Hauck CR (2005) Cellular invasion by Staphylococcus aureus reveals a functional link between focal adhesion kinase and cortactin in integrin-mediated internalisation. J Cell Sci 118:2189–2200

    PubMed  CAS  Google Scholar 

  • Amelung S, Nerlich A, Rohde M, Spellerberg B, Cole JN, Nizet V, Chhatwal GS, Talay SR. (2011) The FbaB-type fibronectin-binding protein of S. pyogenes promote specific invasion into endothelial cells. Cell Microbiol 13:1200–1211

    PubMed  CAS  Google Scholar 

  • Andre I, Persson J, Blom AM, Nilsson H, Drakenberg, T, Lindahl G, Linse S (2006) Streptococcal M protein: structural studies of the hypervariable regions, free and bound to human C4BP. Biochemistry 45:4559–4568

    PubMed  CAS  Google Scholar 

  • Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, Kanth A, Dahlberg S, Fernebro J, Moschioni M, Masignani V, Hultenby K, Taddei AR, Beiter K, Wartha F, von Euler A, Covacci A, Holden DW, Normark S, Rappuoli R, Henriques-Normark B (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA 103: 2857–2862

    PubMed  CAS  Google Scholar 

  • Beachey EH, Ofek I (1976) Epithelial cell binding of group A streptococci by lipoteichoic acid on fimbriae denuded of M protein. J Exp Med 143:759–771

    PubMed  CAS  Google Scholar 

  • Beall B, Facklam R, Thompson T (1996) Sequencing emm-specific PCR products for routine and accurate typing of group A streptococci. J Clin Microbiol 34:9533–958

    Google Scholar 

  • Benga L, Goethe R, Rohde M, Valentin-Weigand P (2004) Non-encapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cell Microbiol 6:867–881

    PubMed  CAS  Google Scholar 

  • Berkower C, Ravins M, Moses AE, Hanski E (1999) Expression of different group A streptococcal M proteins in an isogenic background demonstrates diversity in adherence to and invasion of eukaryotic cells. Mol Microbiol 31:1463–1475

    PubMed  CAS  Google Scholar 

  • Caparon MG, Stephens S, Olsen A, Scott JR (1991) Role of M protein in adherence of group A streptococci. Infect Immun 59:1811–1817

    PubMed  CAS  Google Scholar 

  • Carapetis (2005) Acute rheumatic fever. Lancet 366:155-168

    Google Scholar 

  • Chhatwal GS (2002) Anchorless adhesins and invasion of Gram-positive bacteria: a new class of virulence factors. Trends in Microbiol 10:205–208

    CAS  Google Scholar 

  • Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218:213–234

    Google Scholar 

  • Courtney HS, Hasty DL (1991) Aggregation of group A streptococci by human saliva and effect of saliva on streptococcal adherence to host cells. Infect Immun 59:1661–1666

    PubMed  CAS  Google Scholar 

  • Courtney HS, von Hunolstein C, Dale JB, Bronze MS, Beachey EH, Hasty DL (1992) Lipoteichoic acid and M protein: dual adhesins of group A streptococci. Microb Pathog 12:199–208

    PubMed  CAS  Google Scholar 

  • Courtney HS, Bronze M S, Dale JB, Hasty DL (1994) Analysis of the role of M24 protein in group A streptococcal adhesion and colonization by use of omega-interposon mutagenesis. Infect Immun 62:4868–4873

    PubMed  CAS  Google Scholar 

  • Courtney HS, Dale JB, Hasty DI (1996) Differential effects of the streptococcal fibronectin-binding protein, FBP54, on adhesion of group A streptococci to human buccal cells and HEp-2 tissue culture cells. Infect Immun 64:2415–2419

    PubMed  CAS  Google Scholar 

  • Courtney HS, Hasty DL, Dale JB (2002) Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann Med 34:77–87

    PubMed  CAS  Google Scholar 

  • Cremer MA, Rosloniec EF, Kang AH (1998) The cartilage collagens: a review of their structure, organization, and role in the pathogenesis of experimental arthritis in animals and in human rheumatic disease. J Mol Med 76:275–288

    PubMed  CAS  Google Scholar 

  • Crotty Alexander LE, Maisey HC, Timmer AM, Rooijakkers SHM, Gallo RL, von Köckritz-Blickwede M, Nizet V. (2010) M1T1 group A streptococci pili promote epithelial colonization but diminish systemic virulence through neutrophil extracellular entrapment. J Mol Med 88:371–381

    PubMed  CAS  Google Scholar 

  • Cue D, Dombek PE, Lam H, Cleary PP (1998) Streptococcus pyogenes serotype M1 encodes multiple pathways for entry into human epithelial cells. Infect Immun 66:4593–4601

    PubMed  CAS  Google Scholar 

  • Cue D, Southern SO, Southern PJ, Prabhakar J, Lorelli W, Smallheer JM, Mousa SA, Cleary PP (2000) A nonpeptide integrin antagonist can inhibit epithelial cell ingestion of Streptococcus pyogenes by blocking formation of integrin alpha 5beta 1-fibronectin-M1 protein complexes. Proc Natl Acad Sci USA 97:2858–2863

    PubMed  CAS  Google Scholar 

  • Cue D, Lam H, Cleary PP (2001) Genetic dissection of the Streptococcus pyogenes M1 protein: regions involved in fibronectin-binding and intracellular invasion. Microb Pathog 31:231–242

    PubMed  CAS  Google Scholar 

  • Cunningham MW (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13:470–511

    PubMed  CAS  Google Scholar 

  • Cywes C, Wessels MR (2001) Group A Streptococcus tissue invasion by CD44-mediated cell signalling. Nature 414:648–652

    PubMed  CAS  Google Scholar 

  • Cywes C, Stamenkovic I, Wessels MR (2000) CD44 as a receptor for colonization of the pharynx by group A Streptococcus. J Clin Invest 106:995–1002

    PubMed  CAS  Google Scholar 

  • Dale JB, Washburn RG, Marques MB, Wessels MR (1996) Hyaluronate capsule and surface M protein in resistance to opsonization of group A streptococci. Infect Immun 64:1495–1501

    PubMed  CAS  Google Scholar 

  • Darmstadt GL, Mentele L, Podbielski A, Rubens CE (2000) Role of group A streptococcal virulence factors in adherence to keratinocytes. Infect Immun 68:1215–1221

    PubMed  CAS  Google Scholar 

  • Debelle L, Tamburro AM (1999) Elastin: molecular description and function. Int J Biochem Cell Biol 31:261–272

    PubMed  CAS  Google Scholar 

  • Dempfle CE, Mosesson MW (2003) Theme issue: Fibrinogen and fibrin - structure, function, interactions and clinical applications. Thromb Haemost 89:599–600

    PubMed  CAS  Google Scholar 

  • Derbise A, Song YP, Parikh S, Fischetti VA, Pancholi V (2004) Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect Immun 72:94–105

    PubMed  CAS  Google Scholar 

  • Dinkla K, Rohde M, Jansen WTM, Kaplan EL, Chhatwal GS, Talay SR (2003a) Rheumatic fever-associated Streptococcus pyogenes isolates aggregate collagen. J Clin Invest 111:1905–1912

    PubMed  CAS  Google Scholar 

  • Dinkla K, Rohde M, Jansen WTM, Carapetis JR, Chhatwal GS, Talay SR (2003b) Streptococcus pyogenes recruits collagen via surface-bound fibronectin: a novel colonization and immune evasion mechanism. Mol Microbiol 47:861–869

    PubMed  CAS  Google Scholar 

  • Dombek PE, Cue D, Sedgewick J, Lam H, Ruschkowski S, Finlay BB, Cleary PP (1999) High-frequency intracellular invasion of epithelial cells by serotype M1 group A streptococci: M1 protein-mediated invasion and cytoskeletal rearrangements. Mol Microbiol 31:859–870

    PubMed  CAS  Google Scholar 

  • Doran KS, Engelson EJ, Khosravi A, Maisey HC, Fedtke I, Equils O, Michelsen KS, Arditi, M, Peschel A, Nizet V (2005) Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 115:2499–2507

    PubMed  CAS  Google Scholar 

  • Ellen RP, Gibbons RJ (1972) M protein-associated adherence of Streptococcus pyogenes to epithelial surfaces: prerequisite for virulence. Infect Immun 5:826–830

    PubMed  CAS  Google Scholar 

  • Ellen RP, Gibbons RJ (1974) Parameters affecting the adherence and tissue tropisms of Streptococcus pyogenes. Infect Immun 9:85–91

    PubMed  CAS  Google Scholar 

  • Falugi F, Zingaretti C, Pinto V, Mariani M, Amodeo A, Manetti G, Capo S, Musser JM, Orefici G, Margarit I, Telford L, Grandi G, Mora M (2008) Sequence variation in group A Streptococcus pili and associatition of pilus backbone types with Lancefield T serotypes. J Infect Dis 198:1834–1841

    PubMed  CAS  Google Scholar 

  • Fowler T, Wann ER, Joh D, Johansson S, Foster TJ, Höök M (2000) Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell beta1 integrins. Eur J Cell Biol 79:672–679

    PubMed  CAS  Google Scholar 

  • Frick IM, Crossin KL, Edelman GM, Björck L (1995) Protein H-a bacterial surface protein with affinity for both immunoglobulin and fibronectin type III domains. EMBO J 14:1674–1679

    PubMed  CAS  Google Scholar 

  • Frick IM, Mörgelin M, Björck L (2000) Virulent aggregates of Streptococus pyogenes are generated by hemophilic protein–protein interactions. Mol Microbiol 37:1232–1247

    PubMed  CAS  Google Scholar 

  • Frick IM, Schmidtchen A, Sjobring U (2003) Interactions between M proteins of Streptococcus pyogenes and glycosaminoglycans promote bacterial adhesion to host cells. Eur J Biochem 270:2303–2311

    PubMed  CAS  Google Scholar 

  • Gianfoldoni C, Censini S, Hilleringmann M, Moschioni M, Facciotti C, Pansegrau W, Masigani V, Covacci A, Rappuoli R, Barocchi MA, Rugiero P (2007) Streptococcus pneumoniae pilus subunits protect mice against lethal challange. Infect Immun 75:1059–1062

    Google Scholar 

  • Giannakis E, Jokiranta TS, Ormsby RJ, Duthy TG, Male DA, Christiansen D, Fischetti VA, Bagley C, Loveland BE, Gordon DL (2002) Identification of the streptococcal M protein binding site on membrane cofactor protein (CD46). J Immunol 168:4585–4592

    PubMed  CAS  Google Scholar 

  • Gibson CM, Caparon MG (1996) Insertional inactivation of Streptococcus pyogenes sod suggests that prtF is regulated in response to a superoxide signal. J Bacteriol 178:4688–4695

    PubMed  CAS  Google Scholar 

  • Gibson CM, Fogg G, Okada N, Geist RT, Hanski E, Caparon MG (1995) Regulation of host cell recognition in Streptococcus pyogenes. Dev Biol Stand 85:137–144

    PubMed  CAS  Google Scholar 

  • Greco R, De Martino L, Donnarumma G, Conte MP, Seganti L, Valenti P (1995) Invasion of cultured human cells by Streptococcus pyogenes. Res Microbiol 146:551–560

    PubMed  CAS  Google Scholar 

  • Hagman MM, Dale JB, Stevens DL (1999) Comparison of adherence to and penetration of a human laryngeal epithelial cell line by group A streptococci of various M protein types. FEMS Immunol Med Microbiol 23:195–204

    PubMed  CAS  Google Scholar 

  • Haidan A, Talay SR, Rohde M, Sriprakash KS, Currie BJ, Chhatwal GS (2000) Pharyngeal carriage of group C and group G streptococci and acute rheumatic fever in an Aboriginal population. Lancet 356:1167–1169

    PubMed  CAS  Google Scholar 

  • Handley PS, Carter PL, Fielding J (1984) Streptococcus salivarius strains carry either fibrils or fimbriae on the cell surface. J Bacteriol 157:64–72

    PubMed  CAS  Google Scholar 

  • Handley PS, Harty DW, Wyatt JE, Brown CR, Doran JP, Gibbs AC (1987) A comparison of the adhesion, coaggregation and cell-surface hydrophobicity properties of fibrillar and fimbriae strains of Streptococcus salivarius. J Gen Microbiol 133:3207–3217

    PubMed  CAS  Google Scholar 

  • Hanski E, Caparon M (1992) Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus. Proc Natl Acad Sci USA 89:6172–6176

    PubMed  CAS  Google Scholar 

  • Hasty DL, Ofek I, Courtney HS, Doyle RJ (1992) Multiple adhesins of streptococci. Infect Immun 60:2147–2152

    PubMed  CAS  Google Scholar 

  • Henningham A, Barnett TC, Maamary PG, Walker MJ (2012a) Pathogenesis of group A infections. Discov Med 13:329–342

    PubMed  Google Scholar 

  • Henningham A, Chiarot E, Gillen CM, Cole JN, Rohde M, Fulde M, Ramachandran V, Cork AJ, Hartas J, Magor G, Djordjevic SP, Cordwell SJ, Kobe B, Sriprakash KS, Nizet V, Chhatwal GS, Margarit IY, Batzloff MR, Walker MJ (2012b) Conserved anchorless surface proteins as group A vaccine candidates. J Mol Med (Epub ahead)

    Google Scholar 

  • Humtsoe JO, Kim JK, Xu,Y, Keene DR, Höök M, Lukomski S, Wary KK (2005) A streptococcal collagen-like protein interacts with the alpha2beta1 integrin and induces intracellular signaling. J Biol Chem 280:13848–13857

    PubMed  CAS  Google Scholar 

  • Hytonen J, Haataja S, Gerlach D, Podbielski A, Finne J (2001) The SpeB virulence factor of streptococcus pyogens, a multifuntional secreted and cell surface molecule with strepadhesin, laminin-binding and cysteine protease activity. Mol Microbiol 39:512–519

    PubMed  CAS  Google Scholar 

  • Isberg RR (1991) Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science 252:934–938

    PubMed  CAS  Google Scholar 

  • Isberg RR, Barnes P (2001) Subversion of integrins by enteropathogenic Yersinia. J Cell Sci 114:21–28

    PubMed  CAS  Google Scholar 

  • Isberg RR, Leong JM (1990). Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861–871

    PubMed  CAS  Google Scholar 

  • Jadoun J, Ozeri V, Burstein E, Skutelsky E, Hanski E, Sela S (1998) Protein F1 is required for efficient entry of Streptococcus pyogenes into epithelial cells. J Infect Dis 178:147–158

    PubMed  CAS  Google Scholar 

  • Jadoun J, Eyal O, Sela S (2002) Role of CsrR, hyaluronic acid, and SpeB in the internalization of Streptococcus pyogenes M type 3 strain by epithelial cells. Infect Immun 70:462–469

    PubMed  CAS  Google Scholar 

  • Jaffe J, Natanson-Yaron S, Caparon MG, Hanski E (1996) Protein F2, a novel fibronectin-binding protein from Streptococcus pyogenes, possesses two binding domains. Mol Microbiol 21:373–384

    PubMed  CAS  Google Scholar 

  • Jin H, Song YP, Boel G, Kochar J, Pancholi V (2005) Group A streptococcal surface GAPDH, SDH, recognizes uPAR/CD87 as its receptor on the human pharyngeal cell and mediates adherence to host cells J Biol Chem 350:27–41

    CAS  Google Scholar 

  • Johnson DR, Stevens DL, Kaplan EL (1992) Epidemiologic analysis of group A streptococcal serotypes associated with severe systemic infections, rheumatic fever, or uncomplicated pharyngitis. J Infect Dis 166: 374–382

    PubMed  CAS  Google Scholar 

  • Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN (2007) Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Science 318:1625–1628

    PubMed  CAS  Google Scholar 

  • Kaplan EL, Johnson DR, Cleary PP (1989) Group A streptococcal serotypes isolated from patients and sibling contacts during the resurgence of rheumatic fever in the United States in the mid-1980s. J Infect Dis 159:101–103

    PubMed  CAS  Google Scholar 

  • Kaplan EL, Chhatwal GS, Rohde M (2006) Reduced ability of penicillin to eradicate ingested group A streptococci from epithelial cells: clinical and pathogenetic implication. Clin Infect Dis 43:1398–1406

    PubMed  CAS  Google Scholar 

  • Kawabat S, Tamura Y, Murakami J, Teroa Y, Nakagawa I, Hamada S (2002) A novel, anchorless streptococcal surface protein that binds to human immunoglobulins. Biochem Biophys Res Comm 296:1329–1333

    Google Scholar 

  • Kinnby B, Booth NA, Svensater G (2008) Plasminogen binding by oral streptococci from dental plaque and inflammatory lesions. Microbiology 154:924–931

    PubMed  CAS  Google Scholar 

  • Kreikemeyer B, McIver KS, Podbielski A (2003) Virulence factor regulation and regulatory networks in Stretococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol 11:224–232

    PubMed  CAS  Google Scholar 

  • Kreikemeyer B, Oemcke S, Nakata M, Hoffrogge R, Podbielski A (2004a) Streptococcus pyogenes fibronectin-bindung protein F2: expression profile, binding characteristics, and impact on eukaryotic cell interactions. J Biol Chem 279:15850–15859

    PubMed  CAS  Google Scholar 

  • Kreikemeyer B, Klenk M, Podbielski A (2004b) The intracellular status of Streptococcus pyogenes; role of extracellular matrix-binding proteins and their regulation. Int J Med Micriobiol 294:177–188

    CAS  Google Scholar 

  • LaPenta D, Rubens C, Chi E, Cleary PP (1994) Group A streptococci efficiently invade human respiratory epithelial cells. Proc Natl Acad Sci USA 91:12115–12119

    PubMed  CAS  Google Scholar 

  • Lauer P, Rinaudo CD, Soriani M, Margarit I, Maione D, Rosini R, Taddei AR, Mora M, Rappuoli R, Grandi G, Telford JL (2005) Genome analysis reveals pili in Group B Streptococcus. Science 309:105

    PubMed  CAS  Google Scholar 

  • Leon O, Panos C (1990) Streptococcus pyogenes clinical isolates and lipoteichoic acid. Infect Immun 58:3779–3787

    PubMed  CAS  Google Scholar 

  • Maisey HC, Hensler M, Nizet V, Doran KS (2007) Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 189:1464–1467

    PubMed  CAS  Google Scholar 

  • Mandlik A, Swierczynski A, Das A., Ton-That H. (2007a) Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends in Microbiol 16:33–39

    Google Scholar 

  • Mandlik A, Swierczynski A, Das A, Ton-That H (2007b) Corynebacterium diphtheria employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 64:11–124

    Google Scholar 

  • Maraffini LA, Dedent AC, Schneewind O (2006) Sortases and the art of anchoring proteins to the envelope of gram-positive bacteria. Microbiol Mol Biol Rev 70:192–221

    Google Scholar 

  • Marjenberg ZR, Ellis IR, Hagan RM, Prabhakaran S, Höök M, Talay SR, Potts JR, Staunton D, Schwarz-Linek U (2011) Cooperative binding and activation of fibronectin by a bacterial surface protein. J Biol Chem 286:1884–1894

    PubMed  CAS  Google Scholar 

  • McArthur JD, Walker MJ (2006) Domains of group A streptococcal M protein that confer resistance to phagocytosis, opsonozation and protection: implications for vaccine development. Mol Microbiol 59:1–4

    PubMed  CAS  Google Scholar 

  • McNamara C, Zinkernagel AS, Machebeouf M, Cunningham M, Nizet V. (2008) Coiled-coil irregularities and instabilities in group A streptococcus M1 are required for virulence. Science 319: 1405–1408

    PubMed  CAS  Google Scholar 

  • Medina E, Rohde M, Chhatwal GS (2003a) Intracellular survival of Streptococcus pyogenes in polymorphonuclear cells results in increased bacterial virulence. Infect Immun 71:5376–5380

    PubMed  CAS  Google Scholar 

  • Medina E, Goldmann O, Toppel AW, Chhatwal GS (2003b) Survival of Streptococcus pyogenes within host phagocytic cells: a pathogenic mechanism for persistence and systemic invasion. J Infect Dis 187:597–603

    PubMed  Google Scholar 

  • Molinari G, Chhatwal GS (1999) Streptococcal invasion. Curr Opin Microbiol 2:56–61

    PubMed  CAS  Google Scholar 

  • Molinari G, Rohde M, Guzman CA, Chhatwal GS (2000) Two distinct pathways for the invasion of Streptococcus pyogenes in non-phagocytic cells. Cell Microbiol 2:145–154

    PubMed  CAS  Google Scholar 

  • Mora M, Bensi G, Capo S, Falugi F, Zingaretti C, Manetti AG, Maggi T, Taddei AR, Grandi G, Telford JL (2005) Group A streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci USA 102:15641–15646

    PubMed  CAS  Google Scholar 

  • Natanson S, Sela S, Moses AE, Musser JM, Caparon MG, Hanski, E (1995) Distribution of fibronectin-binding proteins among group A streptococci of different M types. J Infect Dis 171:871–878

    PubMed  CAS  Google Scholar 

  • Nerlich A, Rohde M, Talay, SR, Genth H, Just I, Chhatwal GS (2009) Invasion of endothelial cells by tisuue-invasive M3 type Group A streptococci requires Src kinase and activation of Rac1 by a phosphatidylinositol 3-kinase-independent mechanism. J Biol Chem 284:20319–20328

    PubMed  CAS  Google Scholar 

  • Nitsche DP, Johansson HM, Frick IM, Mörgelin, M (2006) Streptococcal protein FOG, a novel matrix adhesin interacting with collagen I in vivo. J Biol Chem 281:1670–1679

    PubMed  CAS  Google Scholar 

  • Nitsche-Schmitz DP, Rohde M, Chhatwal GS (2007) Invasion mechanisms of gram-positive pathogenic cocci. Thromb Haemost 98:488–496

    PubMed  CAS  Google Scholar 

  • Nobbs AH, Lamont RJ, Jenkinson HF (2009) Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73:407–450

    PubMed  CAS  Google Scholar 

  • Norton PM, Rolph C, Ward PN, Bentley RW, Leigh JA (1999) Epithelial invasion and cell lysis by virulent strains of Streptococcus suis is enhanced by the presence of suilysin. FEMS Immunol Med Microbiol 26:25–35

    PubMed  CAS  Google Scholar 

  • Oemcke S, Shannon O, Mörgelin M, Herwald H. (2010) Streptococcal M proteins and their role as virulence determninants. Clinica Chemica Acta 411:1172–1180

    Google Scholar 

  • Oesterlund A, Engstrand L (1997a) An intracellular sanctuary for Streptococcus pyogenes in human tonsillar epithelium-studies of asymptomatic carriers and in vitro cultured biopsies. Acta Otolaryngol 117:883–888

    Google Scholar 

  • Oesterlund A, Popa R, Nikkila T, Scheynius, A, Engstrand L (1997b) Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. Laryngoscope 107:640–647

    Google Scholar 

  • Okada N, Liszewski MK, Atkinson JP, Caparon M (1995) Membrane cofactor protein (CD46) is a keratinocyte receptor for the M protein of the group A Streptococcus. Biochem Biophys Res Commun 377:1128–1134

    Google Scholar 

  • Ozeri V, Tovi A, Burstein I, Natanson-Yaron S, Caparon MG, Yamada KM, Akiyama SK, Vlodavsky I, Hanski E (1996) A two-domain mechanism for group A streptococcal adherence through protein F to the extracellular matrix. EMBO J 15:989–998

    PubMed  CAS  Google Scholar 

  • Ozeri V, Rosenshine I, Mosher DF, Fässler R, Hanski E (1998) Roles of integrins and fibronectin in the entry of Streptococcus pyogenes into cells via protein F1. Mol Microbiol 30:625–637

    PubMed  CAS  Google Scholar 

  • Pancholi V, Fischetti VA (1992) A major surface protein on group A streptococci is a glyceraldehydes-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med 176:415–426

    PubMed  CAS  Google Scholar 

  • Pancholi V, Fischetti VA (1997) Regulation of the phosphorylation of human pharyngeal cell proteins by group A streptococcal surface dehydrogenase: signal transduction between streptococci and pharyngeal cells. J Exp Med 186:1633–1643

    PubMed  CAS  Google Scholar 

  • Pancholi V, Fischetti VA (1998) alpha-enolase, a novel strong plasminogen-(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem 273:14503–14515

    PubMed  CAS  Google Scholar 

  • Pankov R, Yamada KM (2002) Fibronectin at a glance. J Cell Sci 115:3861–3863

    PubMed  CAS  Google Scholar 

  • Patti JM, Höök M (1994) Microbial adhesions recognizing extracellular matrix molecules. Curr Opin Cell Biol 6:752–758

    PubMed  CAS  Google Scholar 

  • Pezzicoli A, Santi I, Lauer P, Rosini R, Rinaudo D, Grandi, G, Telford JL, Soriani M (2008) Pilus backbone contributes to group B Streptococcus paracellular translocation through epithelial cells. Infect Immun 198:890–898

    Google Scholar 

  • Podbielski A, Woischnik M, Leonard BA, Schmidt KH (1999) Characterization of nra, a global negative regulator gene in group A streptococci Mol Microbiol 31:1051–1064

    PubMed  CAS  Google Scholar 

  • Proft T, Baker EN (2009) Pili in gram-negative and gram-positive bacteria-structure, assembly and role in disease. Cell Mol Life Sci 66:613–635

    PubMed  CAS  Google Scholar 

  • Rezcallah M S, Hodges K, Gill DB, Atkinson JP, Wang B, Cleary PP (2005) Engagement of CD46 and alpha5beta1 integrin by group A streptococci is required for efficient invasion of epithelial cells. Cell Microbiol 7:645–653

    PubMed  CAS  Google Scholar 

  • Rocha CL, Fischetti VA (1999) Identification and characterization of a novel fibronectin-binding protein on the surface of group A streptococci. Infect Immun 67:2720–2728

    PubMed  CAS  Google Scholar 

  • Rohde M, Müller E, Chhatwal GS, Talay SR (2003) Host cell caveolae act as an entry-port for Group A streptococci. Cell Microbiol 5:323–342

    PubMed  CAS  Google Scholar 

  • Rohde M, Graham RM, Branitzki-Heinemann K, Borchers P, Preuss C, Schleicher I, Zähner D, Talay SR, Fulde M, Dinkla K, Chhatwal GS (2011) Differences in the aromatic domain of homologous streptococcal fibronectin-binding proteins trigger different cell invasion mechanisms and survival rates. Cell Microbiol 13:450–468

    PubMed  CAS  Google Scholar 

  • Rohde M, Talay SR, Rasmussen M (2012) Molecular mechanisms of Streptococcus dysgalactiae subsp. Equisimilis enabling intravascular persistence. Microbes Infect 14:329–334

    PubMed  CAS  Google Scholar 

  • Rosini R, Rinaudo CD, Soriani M, Lauer P, Mora M, Maione D, Taddei A, Santi I, Ghezzo C, Brettoni C, Buccato S, Margarit I, Grandi G, Telford JL. (2006) Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalacticae. Mol Microbiol 61:126–141

    PubMed  CAS  Google Scholar 

  • Rubens, CE, Smith S, Hulse M, Chi EY, van Belle G (1992) Respiratory epithelial cell invasion by group B streptococci. Infect Immun 60:5157–5163

    PubMed  CAS  Google Scholar 

  • Saulino ET, Bullitt E, Hultgren SJ (2000) Snapshots of usher mediated protein secretion and ordered pilus assembly. Proc Natl Acad Sci USA 97:9240–9245

    PubMed  CAS  Google Scholar 

  • Schneewind O, Mihaylova-Petkov D, Model P (1993) Cell wall sorting signals in surface proteins of gram-positive bacteria EMBO J 12:4803–4811

    PubMed  CAS  Google Scholar 

  • Schrager HM, Rheinwald JG, Wessels MR (1996) Hyaluronic acid capsule and the role of streptococcal entry into keratinocytes in invasive skin infection. J Clin Invest 98:1954–1958

    PubMed  CAS  Google Scholar 

  • Schrager HM, Alberti S, Cywes C, Dougherty GJ, Wessels MR (1998) Hyaluronic acid capsule modulates M protein-mediated adherence and acts as a ligand for attachment of group A Streptococcus to CD44 on human keratinocytes. J Clin Invest 101:1708–1716

    PubMed  CAS  Google Scholar 

  • Schvartz I, Seger D, Shaltiel S (1999) Vitronectin. Int J Biochem Cell Biol 31:539–544

    PubMed  CAS  Google Scholar 

  • Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, Briggs JA, Gough TS, Höök M, Campbell ID, Potts JR (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423:177–181

    PubMed  CAS  Google Scholar 

  • Schwarz-Linek U, Höök M, Potts JR (2004a) The molecular basis of fibronectin-mediated bacterial adherence to host cells Mol Microbiol 52:631–641

    PubMed  CAS  Google Scholar 

  • Schwarz-Linek U, Pilka ES, Pickford AR, Kim JH, Höök M, Campbell ID, Potts J R (2004b) High affinity streptococcal binding to human fibronectin requires specific recognition of sequential F1 modules. J Biol Chem 279:39017–39025

    PubMed  CAS  Google Scholar 

  • Scott JR, Zähner D (2006) Pili with strong attachments: Gram-positive bacteria do it differently Mol Microbiol 62:320–330

    PubMed  CAS  Google Scholar 

  • Seifert KN, McArthur WP, Bleiweis AS, Brady LJ (2003) Characterization of group B streptococcal glyceraldehydes-3-phosphate dehydrogenase: surface localization, enzymatic activity, and protein–protein interactions. Can J Microbiol 49:350–356

    PubMed  CAS  Google Scholar 

  • Sela S, Aviv A, Tovi A, Burstein I, Caparon MG, Hanski E (1993) Protein F: an adhesin of Streptococcus pyogenes binds fibronectin via two distinct domains. Mol Microbiol 10:1049–1055

    PubMed  CAS  Google Scholar 

  • Siemens N, Patenge N, Otto J, Fiedler T, Kreikemeyer B (2011) Streptococcus pyogenes M49 plasminogen/plasmin binding facilitates keratinocyte invasion via integrin–integrin-linked kinase (ILK) pathways and protects from macrophage killing. J Biol Chem 286:21612–21622

    PubMed  CAS  Google Scholar 

  • Simpson WA, Beachey EH (1983) Adherence of group A streptococci to fibronectin on oral epithelial cells. Infect Immun 39:275–279

    PubMed  CAS  Google Scholar 

  • Soriani M, Santi I, Taddei A, Rappuoli R, Grandi G, Telford JL (2008) Group B streptococci crosses human epithelial cells by a paracellular route. J Infect Dis 193:241–250

    Google Scholar 

  • Stinson M W, Alder S, Kumar S (2003) Invasion and killing of human endothelial cells by viridans group streptococci. Infect Immun 71:2365–2372

    PubMed  CAS  Google Scholar 

  • Sylvestky N, Raveh D, Schlesinger Y, Rudensky B, Yinnon AM (2002) Bacteremia due to beta-hemolytic Streptococcus group G: increasing incidence and clinical characteristics of patients. Am J Med 112:622–626

    Google Scholar 

  • Talay SR, Valentin-Weigand P, Jerlstrom PG, Timmis KN, Chhatwal GS (1992) Fibronectin-binding protein of Streptococcus pyogenes: sequence of the binding domain involved in adherence of streptococci to epithelial cells. Infect Immun 60: 3837–3844

    PubMed  CAS  Google Scholar 

  • Talay SR, Valentin-Weigand P, Timmis KN, Chhatwal GS (1994) Domain structure and conserved epitopes of Sfb protein, the fibronectin-binding adhesin of Streptococcus pyogenes. Mol Microbiol 13:531–539

    PubMed  CAS  Google Scholar 

  • Talay SR, Zock A, Rohde M, Molinari G, Oggioni M, Pozzi G, Guzman CA, Chhatwal GS (2000) Co-operative binding of human fibronectin to SfbI protein triggers streptococcal invasion into respiratory epithelial cells. Cell Microbiol 2:521–535

    PubMed  CAS  Google Scholar 

  • Talbot UM, Paton AW, and Paton JC (1996). Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infect Immun 64:3772–3777

    PubMed  CAS  Google Scholar 

  • Telford JT, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in Gram-positive pathogens. Nat Rev Microbiol 4:509–519

    PubMed  CAS  Google Scholar 

  • Terao Y, Kawabata S, Kunitomo E, Murakami J, Nakagawa I, Hamada S (2001) Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells, and the fba gene is positively transcribed under the Mga regulator. Mol Microbiol 42:75–86

    PubMed  CAS  Google Scholar 

  • Terao Y, Kawabata S, Nakata M, Nakagawa I, Hamada S (2002) Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J Biol Chem 277:47428–47435

    PubMed  CAS  Google Scholar 

  • Thulin P, Johansson L, Low DE, Gan BS, Kotb M, McGeer A, Norrby-Teglund A (2006) Viable Group A streptococci in macrophage during acut soft tissue infection. PLos Med 3:e53

    PubMed  Google Scholar 

  • Ton-That H, Marraffini LA, Schneewind O (2004) Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim Biophys Acta 1694:269–278

    PubMed  CAS  Google Scholar 

  • Towers RJ, Fagan PK, Talay SR, Currie BJ, Sriprakash KS, Walker MJ, Chhatwal GS (2003) Evolution of sfbI encoding streptococcal fibronectin-binding protein I: horizontal genetic transfer and gene mosaic structure. J Clin Microbiol 41:5398–5406

    PubMed  CAS  Google Scholar 

  • van Putten JP, Duensing, TD, and Cole RL (1998) Entry of OpaA+gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol Microbiol 29:369–379

    PubMed  Google Scholar 

  • Veasy LG, Tani LY, Daly JA, Korgenski K, Miner L, Bale J, Kaplan EL, Musser JM, Hill HR (2004) Temporal association of the appearance of mucoid strains of Streptococcus pyogenes with a continuing high incidence of rheumatic fever in Utah. Pediatrics 113, e168–172

    PubMed  Google Scholar 

  • Wessels MR, Bronze MS (1994) Critical role of the group A streptococcal capsule in pharyngeal colonization and infection in mice. Proc Natl Acad Sci USA 91:12238–12242

    PubMed  CAS  Google Scholar 

  • 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 88:8317–8321

    PubMed  CAS  Google Scholar 

  • Wessels MR, Goldberg JB, Moses AE, DiCesare TJ (1994) Effects on virulence of mutations in a locus essential for hyaluronic acid capsule expression in group A streptococci. Infect Immun 62:433–441

    PubMed  CAS  Google Scholar 

  • Wilson AT (1959) The relative importance of the capsule and the M-antigen in determining colony form of group A streptococci. J Exp Med 109:257–270

    PubMed  CAS  Google Scholar 

  • Wood DN, Chaussee MA, Chaussee MS, Buttaro BA (2005) Persistence of Streptococcus pyogenes in stationary-phase cultures. J Bacteriol 187:3319–3328

    PubMed  CAS  Google Scholar 

  • Wu H, Fives-Taylor PM (1999) Identification of dipeptide repeats and cell wall sorting signal in the fimbriae-associated adhesion, Fap1, of Streptococcus parasanguis. Mol Microbiol 34:1070–1081

    PubMed  CAS  Google Scholar 

  • Yanagawa R, Honda E (1976) Presence of pili in species of human and animal parasites and pathogens of the genus corynebacterium. Infect Immun 13:1293–1295

    PubMed  CAS  Google Scholar 

  • Yanagawa R, Otsuki K Tokui T (1968) Electron microscopy of fine structure of Corynebacterium renale with special reference to pili. Jpn J Vet Res 16:31–37

    PubMed  CAS  Google Scholar 

  • Yilmaz O, Yao L, Maeda K, Rose TM, Lewis EL, Duman M, Lamont RJ, Ojcius DM (2008) ATP scavenging by the intracellular pathogen Porphyromonas gingivalis inhibits P2X7-mediated host-cell apoptosis. Cell Microbiol 10:863–875

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medical Microbiology, Helmholtz Centre for Infection Research, Braunschweig, Germany

    Manfred Rohde & G. Singh Chhatwal

Authors
  1. Manfred Rohde
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Singh Chhatwal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manfred Rohde .

Editor information

Editors and Affiliations

  1. , Dept. of Medical Microbiology, Helmholtz Centre for Infection Research, Inhoffenstr. 7, Braunschweig, 38124, Germany

    G. Singh Chhatwal

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Rohde, M., Chhatwal, G.S. (2012). Adherence and Invasion of Streptococci to Eukaryotic Cells and their Role in Disease Pathogenesis. In: Chhatwal, G. (eds) Host-Pathogen Interactions in Streptococcal Diseases. Current Topics in Microbiology and Immunology, vol 368. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2012_281

Download citation

Publish with us

Policies and ethics

Search

Navigation