Blood group antigen recognition via the group a streptococcal m protein mediates host colonization

mBio

Volumn 8, Issue 1, 2017, Pages

  De Oliveira, David M P ^a   Hartley Tassell, Lauren ^b   Everest Dass, Arun ^c   Day, Christopher J ^b   Dabbs, Rebecca A ^a   Ve, Thomas ^b,d   Kobe, Bostjan ^d   Nizet, Victor ^e   Packer, Nicolle H ^c   Walker, Mark J ^d   Jennings, Michael P ^b   Sanderson Smith, Martina L ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c MACQUARIE UNIVERSITY   (Australia)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BLOOD GROUP A ANTIGEN; BLOOD GROUP ANTIGEN; BLOOD GROUP B ANTIGEN; BLOOD GROUP H ANTIGEN; GALACTOSE; GLYCAN; M PROTEIN; M1 PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL ANTIGEN; CARRIER PROTEIN; OUTER MEMBRANE PROTEIN; POLYSACCHARIDE; PROTEIN BINDING; STREPTOCOCCAL M PROTEIN;

ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTIGEN STRUCTURE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUTH EPITHELIUM CELL; MUTAGENESIS; NONHUMAN; PHENOTYPIC VARIATION; STREPTOCOCCUS GROUP A; CHEMISTRY; DNA MUTATIONAL ANALYSIS; EPITHELIUM CELL; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; STREPTOCOCCUS PYOGENES;

ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BLOOD GROUP ANTIGENS; CARRIER PROTEINS; DNA MUTATIONAL ANALYSIS; EPITHELIAL CELLS; POLYSACCHARIDES; PROTEIN BINDING; STREPTOCOCCUS PYOGENES;

EID: 85014837332     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02237-16     Document Type: Article

References (50)

1. Slomiany BL, Slomiany A. 1978. ABH-blood-group antigens and glycolipids of human saliva. Eur J Biochem 85:249–254. https://doi.org/10.1111/j.1432-1033.1978.tb12233.x.
2. De Leoz ML, Gaerlan SC, Strum JS, Dimapasoc LM, Mirmiran M, Tancredi DJ, Smilowitz JT, Kalanetra KM, Mills DA, German JB, Lebrilla CB, Underwood MA. 2012. Lacto-N-tetraose, fucosylation, and secretor status are highly variable in human milk oligosaccharides from women delivering preterm. J Proteome Res 11:4662–4672. https://doi.org/10.1021/pr3004979.
3. Everest-Dass AV, Jin D, Thaysen-Andersen M, Nevalainen H, Kolarich D, Packer NH. 2012. Comparative structural analysis of the glycosylation of salivary and buccal cell proteins: innate protection against infection by Candida albicans. Glycobiology 22:1465–1479. https://doi.org/10.1093/glycob/cws112.
4. Nishihara S, Hiraga T, Ikehara Y, Kudo T, Iwasaki H, Morozumi K, Akamatsu S, Tachikawa T, Narimatsu H. 1999. Molecular mechanisms of expression of Lewis b antigen and other type I Lewis antigens in human colorectal cancer. Glycobiology 9:607–616. https://doi.org/10.1093/glycob/9.6.607.
5. Yang N, Boettcher B. 1991. Conversion of the human blood group H antigen to A antigen in vitro. Immunol Cell Biol 69:111–118. https://doi.org/10.1038/icb.1991.17.
6. Persson M, Letts JA, Hosseini-Maaf B, Borisova SN, Palcic MM, Evans SV, Olsson ML. 2007. Structural effects of naturally occurring human blood group B galactosyltransferase mutations adjacent to the DXD motif. J Biol Chem 282:9564–9570. https://doi.org/10.1074/jbc.M610998200.
7. Jaff MS. 2010. Higher frequency of secretor phenotype in O blood group—its benefits in prevention and/or treatment of some diseases. Int J Nanomed 5:901–905. https://doi.org/10.2147/IJN.S13980.
8. Garratty G, Glynn SA, McEntire R, Retrovirus Epidemiology Donor Study. 2004. ABO and Rh(D) phenotype frequencies of different racial/ethnic groups in the United States. Transfusion 44:703–706. https://doi.org/10.1111/j.1537-2995.2004.03338.x.
9. Srikant RG, Kumar NS, Ravidhar. 2013. Distribution of blood groups in and around Bellary, Karnataka. Hematology 24:247–250.
10. Agrawal A, Tiwari AK, Mehta N, Bhattacharya P, Wankhede R, Tulsiani S, Kamath S. 2014. ABO and Rh (D) group distribution and gene frequency; the first multicentric study in India. Asian J Transfus Sci 8:121–125. https://doi.org/10.4103/0973-6247.137452.
11. Dean L (ed). 2005. Blood groups and red cell antigens. National Center for Biotechnology Information, Bethesda, MD.
12. Jaff MS. 2011. Relation between ABO blood groups and Helicobacter pylori infection in symptomatic patients. Clin Exp Gastroenterol 4:221–226. https://doi.org/10.2147/CEG.S23019.
13. Zierke M, Smieško M, Rabbani S, Aeschbacher T, Cutting B, Allain FH, Schubert M, Ernst B. 2013. Stabilization of branched oligosaccharides: Lewis(x) benefits from a nonconventional C-H···O hydrogen bond. J Am Chem Soc 135:13464–13472. https://doi.org/10.1021/ja4054702.
14. Day CJ, Tiralongo J, Hartnell RD, Logue CA, Wilson JC, von Itzstein M, Korolik V. 2009. Differential carbohydrate recognition by Campylobacter jejuni strain 11168: influences of temperature and growth conditions. PLoS One 4:e4927. https://doi.org/10.1371/journal.pone.0004927.
15. Newburg DS. 2000. Oligosaccharides in human milk and bacterial colonization. J Pediatr Gastroenterol Nutr 30(Suppl 2):S8–S17.
16. Barthelson R, Mobasseri A, Zopf D, Simon P. 1998. Adherence of Streptococcus pneumoniae to respiratory epithelial cells is inhibited by sialylated oligosaccharides. Infect Immun 66:1439–1444.
17. Giannasca KT, Giannasca PJ, Neutra MR. 1996. Adherence of Salmonella typhimurium to Caco-2 cells: identification of a glycoconjugate receptor. Infect Immun 64:135–145.
18. Saadi AT, Weir DM, Poxton IR, Stewart J, Essery SD, Blackwell CC, Raza MW, Busuttil A. 1994. Isolation of an adhesin from Staphylococcus aureus that binds Lewis a blood group antigen and its relevance to sudden infant death syndrome. FEMS Immunol Med Microbiol 8:315–320. https://doi.org/10.1111/j.1574-695X.1994.tb00458.x.
19. Hartley-Tassell LE, Shewell LK, Day CJ, Wilson JC, Sandhu R, Ketley JM, Korolik V. 2010. Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni. Mol Microbiol 75: 710–730. https://doi.org/10.1111/j.1365-2958.2009.07010.x.
20. Walker MJ, Barnett TC, McArthur JD, Cole JN, Gillen CM, Henningham A, Sriprakash KS, Sanderson-Smith ML, Nizet V. 2014. Disease manifestations and pathogenic mechanisms of group A Streptococcus. Clin Microbiol Rev 27:264–301. https://doi.org/10.1128/CMR.00101-13.
21. Sanderson-Smith M, De Oliveira DM, Guglielmini J, McMillan DJ, Vu T, Holien JK, Henningham A, Steer AC, Bessen DE, Dale JB, Curtis N, Beall BW, Walker MJ, Parker MW, Carapetis JR, Van Melderen L, Sriprakash KS, Smeesters PR, M Protein Study Group. 2014. A systematic and functional classification of Streptococcus pyogenes that serves as a new tool for molecular typing and vaccine development. J Infect Dis 210:1325–1338. https://doi.org/10.1093/infdis/jiu260.
22. McMillan DJ, Drèze PA, Vu T, Bessen DE, Guglielmini J, Steer AC, Carapetis JR, Van Melderen L, Sriprakash KS, Smeesters PR. 2013. Updated model of group A Streptococcus M proteins based on a comprehensive worldwide study. Clin Microbiol Infect 19:E222–E229. https://doi.org/10.1111/1469-0691.12134.
23. Frick IM, Schmidtchen A, Sjöbring U. 2003. Interactions between M proteins of Streptococcus pyogenes and glycosaminoglycans promote bacterial adhesion to host cells. Eur J Biochem 270:2303–2311. https://doi.org/10.1046/j.1432-1033.2003.03600.x.
24. Barnett TC, Liebl D, Seymour LM, Gillen CM, Lim JY, Larock CN, Davies MR, Schulz BL, Nizet V, Teasdale RD, Walker MJ. 2013. The globally disseminated M1T1 clone of group A Streptococcus evades autophagy for intracellular replication. Cell Host Microbe 14:675–682. https://doi.org/10.1016/j.chom.2013.11.003.
25. McNamara C, Zinkernagel AS, Macheboeuf P, Cunningham MW, Nizet V, Ghosh P. 2008. Coiled-coil irregularities and instabilities in group A Streptococcus M1 are required for virulence. Science 319:1405–1408. https://doi.org/10.1126/science.1154470.
26. Macheboeuf P, Buffalo C, Fu CY, Zinkernagel AS, Cole JN, Johnson JE, Nizet V, Ghosh P. 2011. Streptococcal M1 protein constructs a pathological host fibrinogen network. Nature 472:64–68. https://doi.org/10.1038/nature09967.
27. Bharmoria P, Trivedi TJ, Pabbathi A, Samanta A, Kumar A. 2015. Ionic liquid-induced all-alpha to alpha < beta conformational transition in cytochrome c with improved peroxidase activity in aqueous medium. Phys Chem Chem Phys 17:10189–10199. https://doi.org/10.1039/c4cp06044j.
28. Ogawa MY, Fan J, Fedorova A, Hong J, Kharenko OA, Kornilova AY, Lasey RC, Xie F. 2006. Electron-transfer functionality of synthetic coiled-coil metalloproteins. J Braz Chem Soc 17:1516–1521. https://doi.org/10.1590/S0103-50532006000800006.
29. Ryan PA, Pancholi V, Fischetti VA. 2001. Group A streptococci bind to mucin and human pharyngeal cells through sialic acid-containing receptors. Infect Immun 69:7402–7412. https://doi.org/10.1128/IAI.69.12.7402-7412.2001.
30. Uchiyama S, Andreoni F, Zürcher C, Schilcher K, Ender M, Madon J, Matt U, Ghosh P, Nizet V, Schuepbach RA, Zinkernagel AS. 2013. Coiled-coil irregularities of the M1 protein structure promote M1-fibrinogen interaction and influence group A Streptococcus host cell interactions and virulence. J Mol Med 91:861–869. https://doi.org/10.1007/s00109-013 -1012-6.
31. Johnson DR, Wotton JT, Shet A, Kaplan EL. 2002. A comparison of group A streptococci from invasive and uncomplicated infections: are virulent clones responsible for serious streptococcal infections? J Infect Dis 185:1586–1595. https://doi.org/10.1086/340576.
32. Nasser W, Beres SB, Olsen RJ, Dean MA, Rice KA, Long SW, Kristinsson KG, Gottfredsson M, Vuopio J, Raisanen K, Caugant DA, Steinbakk M, Low DE, McGeer A, Darenberg J, Henriques-Normark B, Van Beneden CA, Hoffmann S, Musser JM. 2014. Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences. Proc Natl Acad Sci U SA 111:E1768–E1776. https://doi.org/10.1073/pnas.1403138111.
33. Aziz RK, Kotb M. 2008. Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 14:1511–1517. https://doi.org/10.3201/eid1410.071660.
34. Demers B. 1993. Severe invasive group A streptococcal infections in Ontario, Canada: 1987–1991. Clin Infect Dis. 16:792–802.
35. Tyrrell GJ, Lovgren M, Kress B, Grimsrud K. 2005. Invasive group A streptococcal disease in Alberta, Canada (2000 to 2002). J Clin Microbiol 43:1678–1683. https://doi.org/10.1128/JCM.43.4.1678-1683.2005.
36. Luca-Harari B, Darenberg J, Neal S, Siljander T, Strakova L, Tanna A, Creti R, Ekelund K, Koliou M, Tassios PT, van der Linden M, Straut M, Vuopio-Varkila J, Bouvet A, Efstratiou A, Schalén C, Henriques-Normark B, Strep-EURO Study Group, Jasir A. 2009. Clinical and microbiological characteristics of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol 47:1155–1165. https://doi.org/10.1128/JCM.02155-08.
37. O’Loughlin RE, Roberson A, Cieslak PR, Lynfield R, Gershman K, Craig A, Albanese BA, Farley MM, Barrett NL, Spina NL, Beall B, Harrison LH, Reingold A, Van Beneden C, Active Bacterial Core Surveillance Team. 2007. The epidemiology of invasive group A streptococcal infection and potential vaccine implications: United States, 2000–2004. Clin Infect Dis 45:853–862. https://doi.org/10.1086/521264.
38. Steer AC, Law I, Matatolu L, Beall BW, Carapetis JR. 2009. Global emm type distribution of group A streptococci: systematic review and implications for vaccine development. Lancet Infect Dis 9:611–616. https://doi.org/10.1016/S1473-3099(09)70178-1.
39. Kaplan EL, Wotton JT, Johnson DR. 2001. Dynamic epidemiology of group A streptococcal serotypes associated with pharyngitis. Lancet 358:1334–1337. https://doi.org/10.1016/S0140-6736(01)06415-7.
40. Winters BD, Ramasubbu N, Stinson MW. 1993. Isolation and characterization of a Streptococcus pyogenes protein that binds to basal laminae of human cardiac muscle. Infect Immun 61:3259–3264.
41. Shewell LK, Harvey RM, Higgins MA, Day CJ, Hartley-Tassell LE, Chen AY, Gillen CM, James DB, Alonzo F, Torres VJ, Walker MJ, Paton AW, Paton JC, Jennings MP. 2014. The cholesterol-dependent cytolysins pneumolysin and streptolysin O require binding to red blood cell glycans for hemolytic activity. Proc Natl Acad Sci U S A 111:E5312–E5320. https://doi.org/10.1073/pnas.1412703111.
42. Anderson EL, Cole JN, Olson J, Ryba B, Ghosh P, Nizet V. 2014. The fibrinogen-binding M1 protein reduces pharyngeal cell adherence and colonization phenotypes of M1T1 group A Streptococcus. J Biol Chem 289:3539–3546. https://doi.org/10.1074/jbc.M113.529537.
43. Wang JR, Stinson MW. 1994. Streptococcal M6 protein binds to fucose-containing glycoproteins on cultured human epithelial cells. Infect Immun 62:1268–1274.
44. Wang JR, Stinson MW. 1994. Protein mediates streptococcal adhesion to HEp-2 cells. Infect Immun 62:442–448.
45. Böhm R, Fleming FE, Maggioni A, Dang VT, Holloway G, Coulson BS, von Itzstein M, Haselhorst T. 2015. Revisiting the role of histo-blood group antigens in rotavirus host-cell invasion. Nat Commun 6:5907. https://doi.org/10.1038/ncomms6907.
46. Herwald H, Cramer H, Mörgelin M, Russell W, Sollenberg U, Norrby-Teglund A, Flodgaard H, Lindbom L, Björck L. 2004. M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116:367–379. https://doi.org/10.1016/S0092-8674(04)00057-1.
47. Sanderson-Smith ML, Dowton M, Ranson M, Walker MJ. 2007. The plasminogen-binding group A streptococcal M protein-related protein Prp binds plasminogen via arginine and histidine residues. J Bacteriol 189:1435–1440. https://doi.org/10.1128/JB.01218-06.
48. Aziz RK, Pabst MJ, Jeng A, Kansal R, Low DE, Nizet V, Kotb M. 2004. Invasive M1T1 group A Streptococcus undergoes a phase-shift in vivo to prevent proteolytic degradation of multiple virulence factors by SpeB. Mol Microbiol 51:123–134. https://doi.org/10.1046/j.1365 -2958.2003.03797.x.
49. Lauth X, von Köckritz-Blickwede M, McNamara CW, Myskowski S, Zinkernagel AS, Beall B, Ghosh P, Gallo RL, Nizet V. 2009. M1 protein allows group A streptococcal survival in phagocyte extracellular traps through cathelicidin inhibition. J Innate Immun 1:202–214. https://doi.org/10.1159/000203645.
50. Ly D, Taylor JM, Tsatsaronis JA, Monteleone MM, Skora AS, Donald CA, Maddocks T, Nizet V, West NP, Ranson M, Walker MJ, McArthur JD, Sanderson-Smith ML. 2014. Plasmin(ogen) acquisition by group A Streptococcus protects against C3b-mediated neutrophil killing. J Innate Immun 6:240–250. https://doi.org/10.1159/000353754.