Cytosolic replication of group a Streptococcus in human macrophages

mBio

Volumn 7, Issue 2, 2016, Pages

  O’Neill, Alan M ^a   Thurston, Teresa L M ^a   Holden, David W ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PROPIDIUM IODIDE; PROTEIN P62; STREPTOLYSIN O; BACTERIAL PROTEIN; STREPTOLYSIN; VIRULENCE FACTOR;

ARTICLE; AUTOPHAGY; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL DIVISION; CELL FATE; CELL VACUOLE; CELL VIABILITY; COLONY FORMING UNIT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; MACROPHAGE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STREPTOCOCCUS GROUP A; TIME LAPSE IMAGING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHYSIOLOGY; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PYOGENES; U-937 CELL LINE;

BACTERIAL PROTEINS; CYTOSOL; HUMANS; MACROPHAGES; MICROBIAL VIABILITY; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; STREPTOLYSINS; U937 CELLS; VIRULENCE FACTORS;

EID: 84965057555     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00020-16     Document Type: Article

References (33)

1. 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. http://dx.doi.org/10.1128/IAI.69.12.7402-7412.2001.
2. Osterlund A, Engstrand L. 1995. Intracellular penetration and survival of Streptococcus pyogenes in respiratory epithelial cells in vitro. Acta Otolar-yngol 115:685-688. http://dx.doi.org/10.3109/00016489509139387.
3. Kaplan EL, Chhatwal GS, Rohde M. 2006. Reduced ability of penicillin to eradicate ingested group A streptococci from epithelial cells: clinical andpathogenetic implications. Clin Infect Dis 43:1398-1406. http://dx.doi.org/10.1086/508773.
4. Håkansson A, Bentley CC, Shakhnovic EA, Wessels MR. 2005. Cytolysin-dependent evasion of lysosomal killing. Proc Natl Acad Sci U S A 102:5192-5197. http://dx.doi.org/10.1073/pnas.0408721102.
5. Sakurai A, Maruyama F, Funao J, Nozawa T, Aikawa C, Okahashi N, Shintani S, Hamada S, Ooshima T, Nakagawa I. 2010. Specific behavior of intracellular Streptococcus pyogenes that has undergone autophagic degradation is associated with bacterial streptolysin O and host small G proteins Rab5 and Rab7. J Biol Chem 285:22666-22675. http://dx.doi.org/10.1074/jbc.M109.100131.
6. Osterlund A, Engstrand L. 1997. An intracellular sanctuary for Streptococcus pyogenes in human tonsillar epithelium—studies of asymptomatic carriers and in vitro cultured biopsies. Acta Otolaryngol 117:883-888. http://dx.doi.org/10.3109/00016489709114219.
7. Osterlund A, Popa R, Nikkilä T, Scheynius A, Engstrand L. 1997. Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. Laryngoscope 107:640-647. http://dx.doi.org/10.1097/00005537-199705000-00016.
8. Medina E, Goldmann O, Rohde M, Lengeling A, Chhatwal GS, Chhat-wals GS. 2001. Genetic control of susceptibility to group A streptococcal infection in mice. J Infect Dis 184:846-852. http://dx.doi.org/10.1086/323292.
9. Goldmann O, Rohde M, Chhatwal GS, Medina E. 2004. Role of macrophages in host resistance to group A streptococci. Infect Immun 72: 2956-2963. http://dx.doi.org/10.1128/IAI.72.5.2956-2963.2004.
10. Mishalian I, Ordan M, Peled A, Maly A, Eichenbaum MB, Ravins M, Aychek T, Jung S, Hanski E. 2011. Recruited macrophages control dissemination of group A Streptococcus from infected soft tissues. J Immunol 187:6022-6031. http://dx.doi.org/10.4049/jimmunol.1101385.
11. Thulin P, Johansson L, Low DE, Gan BS, Kotb M, McGeer A, Norrby-Teglund A. 2006. Viable group A streptococci in macrophages during acute soft tissue infection. PLoS Med 3:e53. http://dx.doi.org/10.1371/journal.pmed.0030053.
12. Staali L, Bauer S, Mörgelin M, Björck L, Tapper H. 2006. Streptococcus pyogenes bacteria modulate membrane traffic in human neutrophils and selectively inhibit azurophilic granule fusion with phagosomes. Cell Mi-crobiol 8:690-703. http://dx.doi.org/10.1111/j.1462-5822.2005.00662.x.
13. Hertzén E, Johansson L, Wallin R, Schmidt H, Kroll M, Rehn AP, Kotb M, Mörgelin M, Norrby-Teglund A. 2010. M1 protein-dependent intracellular trafficking promotes persistence and replication of Streptococcus pyogenes in macrophages. J Innate Immun 2:534-545. http://dx.doi.org/10.1159/000317635.
14. Feil SC, Ascher DB, Kuiper MJ, Tweten RK, Parker MW. 2014. Structural studies of Streptococcus pyogenes streptolysin O provide insights into the early steps of membrane penetration. J Mol Biol 426:785-792. http://dx.doi.org/10.1016/j.jmb.2013.11.020.
15. Harder J, Franchi L, Muñoz-Planillo R, Park J-H, Reimer T, Núñez G. 2009. Activation of the Nlrp3 inflammasome by Streptococcus pyogenes requires streptolysin O and NF-icB activation but proceeds independently of TLR signaling and P2X7 receptor. J Immunol 183:5823-5829. http://dx.doi.org/10.4049/jimmunol.0900444.
16. Timmer AM, Timmer JC, Pence MA, Hsu L-C, Ghochani M, Frey TG, Karin M, Salvesen GS, Nizet V. 2009. Streptolysin O promotes group A Streptococcus immune evasion by accelerated macrophage apoptosis. J Biol Chem 284:862-871. http://dx.doi.org/10.1074/jbc.M804632200.
17. Logsdon LK, Håkansson AP, Cortés G, Wessels MR. 2011. Streptolysin O inhibits clathrin-dependent internalization of group A Streptococcus. mBio 2:e00332-00310. http://dx.doi.org/10.1128/mBio.00332-10.
18. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, Hamada S, Yoshimori T. 2004. Autophagy defends cells against invading group A Streptococcus. Science 306:1037-1040. http://dx.doi.org/10.1126/science.1103966.
19. Bastiat-Sempe B, Love JF, Lomayesva N, Wessels MR. 2014. Streptolysin O and NAD-glycohydrolase prevent phagolysosome acidification and promote group A Streptococcus survival in macrophages. mBio 5:e01690-01614. http://dx.doi.org/10.1128/mBio.01690-14.
20. Lin AE, Beasley FC, Keller N, Hollands A, Urbano R, Troemel ER, Hoffman HM, Nizet V. 2015. A group A Streptococcus ADPribosyltransferase toxin stimulates a protective interleukin 1_-dependent macrophage immune response. mBio 6:e00133-e115. http://dx.doi.org/10.1128/mBio.00133-15.
21. Amer AO, Swanson MS. 2002. A phagosome of one’s own: a microbial guide to life in the macrophage. Curr Opin Microbiol 5:56-61. http://dx.doi.org/10.1016/S1369-5274(02)00286-2.
22. Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH. 2004. Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr Biol 14:806-811. http://dx.doi.org/10.1016/j.cub.2004.04.033.
23. Randow F. 2011. How cells deploy ubiquitin and autophagy to defend their cytosol from bacterial invasion. Autophagy 7:304-309. http://dx.doi.org/10.4161/auto.7.3.14539.
24. Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F. 2009.The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 10:1215-1221. http://dx.doi.org/10.1038/ni.1800.
25. Nozawa T, Aikawa C, Goda A, Maruyama F, Hamada S, Nakagawa I. 2012. The small GTPases Rab9A and Rab23 function at distinct steps in autophagy during group A Streptococcus infection. Cell Microbiol 14: 1149-1165. http://dx.doi.org/10.1111/j.1462-5822.2012.01792.x.
26. 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.http://dx.doi.org/10.1016/j.chom.2013.11.003.
27. Paz I, Sachse M, Dupont N, Mounier J, Cederfur C, Enninga J, Leffler H, Poirier F, Prevost MC, Lafont F, Sansonetti P. 2010. Galectin-3, a marker for vacuole lysis by invasive pathogens. Cell Microbiol 12: 530-544. http://dx.doi.org/10.1111/j.1462-5822.2009.01415.x.
28. Haanes EJ, Cleary PP. 1989. Identification of a divergent M protein gene and an M protein-related gene family in Streptococcus pyogenes serotype 49. J Bacteriol 171:6397-6408.
29. Bauer S, Tapper H. 2004. Membrane retrieval in neutrophils during phagocytosis: inhibition by M protein-expressing S. pyogenes bacteria. J Leukoc Biol 76:1142-1150. http://dx.doi.org/10.1189/jlb.0404260.
30. O’Seaghdha M, Wessels MR. 2013. Streptolysin O and its co-toxin NADglycohydrolase protect group A Streptococcus from xenophagic killing. PLoSP at hog9: e1003394. http://dx.doi.org/10.1371/journal.ppat.1003394.
31. Joubert P-E, Meiffren G, Grégoire IP, Pontini G, Richetta C, Flacher M, Azocar O, Vidalain P-O, Vidal M, Lotteau V, Codogno P, Rabourdin-Combe C, Faure M. 2009. Autophagy induction by the pathogen receptor CD46. Cell Host Microbe 6:354-366. http://dx.doi.org/10.1016/j.chom.2009.09.006.
32. Lu SL, Kuo CF, Chen HW, Yang YS, Liu CC, Anderson R, Wu JJ, Lin YS. 2015. Insufficient acidification of autophagosomes facilitates group A Streptococcus survival and growth in endothelial cells. mBio 6:e01435-15.http://dx.doi.org/10.1128/mBio.01435-15.
33. Kansal RG, McGeer A, Low DE, Norrby-Teglund A, Kotb M. 2000. Inverse relation between disease severity and expression of the streptococcal cysteine protease, SpeB, among clonal M1T1 isolates recovered from invasive group A streptococcal infection cases. Infect Immun 68: 6362-6369. http://dx.doi.org/10.1128/IAI.68.11.6362-6369.2000.