The Cholesterol-Dependent Cytolysin Pneumolysin from Streptococcus pneumoniae Binds to Lipid Raft Microdomains in Human Corneal Epithelial Cells

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Taylor, Sidney D ^a   Sanders, Melissa E ^a   Tullos, Nathan A ^a   Stray, Stephen J ^a   Norcross, Erin W ^a   McDaniel, Larry S ^a   Marquart, Mary E ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PNEUMOLYSIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL KERATITIS; BACTERIAL VIRULENCE; CELL SURFACE; CONFORMATIONAL TRANSITION; CORNEA EPITHELIUM; CYTOLYSIS; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LIPID RAFT; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PNEUMOCOCCAL INFECTION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; RESIDUE ANALYSIS; STREPTOCOCCUS PNEUMONIAE; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CELL LINE; CHOLESTEROL; EPITHELIUM, CORNEAL; HUMANS; MEMBRANE MICRODOMAINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PERFORIN; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN TRANSPORT; RABBITS; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PNEUMONIAE;

EID: 84875956336     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061300     Document Type: Article

References (49)

1. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, et al. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893-902.
2. Ahern JW, Raszka WV Jr, (2009) Meningitis from an uncommon serotype of Streptococcus pneumoniae in a young child. South Med J 102: 1189.
3. Antao VC, Hausdorff WP, (2009) Global epidemiology of pneumococcal disease--new prospects for vaccine control. Adv Exp Med Biol 634: 19-29.
4. Kisakye A, Makumbi I, Nansera D, Lewis R, Braka F, et al. (2009) Surveillance for Streptococcus pneumoniae meningitis in children aged <5 years: implications for immunization in Uganda. Clin Infect Dis 48Suppl 2: S153-161.
5. Yoshioka CR, Martinez MB, Brandileone MC, Ragazzi SB, Guerra ML, et al. (2011) Analysis of invasive pneumonia-causing strains of Streptococcus pneumoniae: serotypes and antimicrobial susceptibility. J Pediatr (Rio J) 87: 70-75.
6. Crum NF, Barrozo CP, Chapman FA, Ryan MA, Russell KL, (2004) An outbreak of conjunctivitis due to a novel unencapsulated Streptococcus pneumoniae among military trainees. Clin Infect Dis 39: 1148-1154.
7. Zegans ME, Sanchez PA, Likosky DS, Allar RT, Martin M, et al. (2009) Clinical features, outcomes, and costs of a conjunctivitis outbreak caused by the ST448 strain of Streptococcus pneumoniae. Cornea 28: 503-509.
8. Soriano F, Perez-Trallero E, Pallares R, Meseguer MA, Fleites A, et al. (2006) Streptococcus pneumoniae endophthalmitis: a study of 36 cases with special reference to antibiotic resistance and treatment options. Clin Microbiol Infect 12: 519-526.
9. Cid M, Sabates NR, (1997) Penicillin-resistant Streptococcus pneumoniae endophthalmitis. Am J Ophthalmol 123: 133-135.
10. Bhave P, Chamie G, (2008) Streptococcus pneumoniae keratitis. J Hosp Med 3: 353.
11. Dada T, Sharma N, Dada VK, Vajpayee RB, (2000) Pneumococcal keratitis after laser in situ keratomileusis. J Cataract Refract Surg 26: 460-461.
12. Lifshitz T, Levy J, Raiskup F, Klemperer I, Frucht-Pery J, (2005) Two cases of pneumococcal keratitis following myopic LASIK. J Refract Surg 21: 498-501.
13. Parmar P, Salman A, Kalavathy CM, Jesudasan CA, Thomas PA, (2003) Pneumococcal keratitis: a clinical profile. Clin Experiment Ophthalmol 31: 44-47.
14. Ramirez M, Hernandez-Quintela E, Beltran F, Naranjo-Tackman R, (2002) Pneumococcal keratitis at the flap interface after laser in situ keratomileusis. J Cataract Refract Surg 28: 550-552.
15. Kunimoto DY, Sharma S, Reddy MK, Gopinathan U, Jyothi J, et al. (1998) Microbial keratitis in children. Ophthalmology 105: 252-257.
16. Green M, Apel A, Stapleton F, (2008) Risk factors and causative organisms in microbial keratitis. Cornea 27: 22-27.
17. Marquart ME, Monds KS, McCormick CC, Dixon SN, Sanders ME, et al. (2007) Cholesterol as treatment for pneumococcal keratitis: cholesterol-specific inhibition of pneumolysin in the cornea. Invest Ophthalmol Vis Sci 48: 2661-2666.
18. Sanders ME, Tullos NA, Taylor SD, Norcross EW, King LB, et al. (2010) Moxifloxacin and cholesterol combined treatment of pneumococcal keratitis. Curr Eye Res 35: 1142-1147.
19. Alexander JE, Berry AM, Paton JC, Rubins JB, Andrew PW, et al. (1998) Amino acid changes affecting the activity of pneumolysin alter the behaviour of pneumococci in pneumonia. Microb Pathog 24: 167-174.
20. Alexander JE, Lock RA, Peeters CC, Poolman JT, Andrew PW, et al. (1994) Immunization of mice with pneumolysin toxoid confers a significant degree of protection against at least nine serotypes of Streptococcus pneumoniae. Infect Immun 62: 5683-5688.
21. Berry AM, Alexander JE, Mitchell TJ, Andrew PW, Hansman D, et al. (1995) Effect of defined point mutations in the pneumolysin gene on the virulence of Streptococcus pneumoniae. Infect Immun 63: 1969-1974.
22. Berry AM, Ogunniyi AD, Miller DC, Paton JC, (1999) Comparative virulence of Streptococcus pneumoniae strains with insertion-duplication, point, and deletion mutations in the pneumolysin gene. Infect Immun 67: 981-985.
23. Hirst RA, Kadioglu A, O'Callaghan C, Andrew PW, (2004) The role of pneumolysin in pneumococcal pneumonia and meningitis. Clin Exp Immunol 138: 195-201.
24. Tweten RK, (2005) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect Immun 73: 6199-6209.
25. Johnson MK, Geoffroy C, Alouf JE, (1980) Binding of cholesterol by sulfhydryl-activated cytolysins. Infect Immun 27: 97-101.
26. Ramachandran R, Heuck AP, Tweten RK, Johnson AE, (2002) Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin. Nat Struct Biol 9: 823-827.
27. Hotze EM, Tweten RK (2011) Membrane assembly of the cholesterol-dependent cytolysin pore complex. Biochim Biophys Acta.
28. Dang TX, Hotze EM, Rouiller I, Tweten RK, Wilson-Kubalek EM, (2005) Prepore to pore transition of a cholesterol-dependent cytolysin visualized by electron microscopy. J Struct Biol 150: 100-108.
29. Czajkowsky DM, Hotze EM, Shao Z, Tweten RK, (2004) Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane. EMBO J 23: 3206-3215.
30. Jacobs T, Cima-Cabal MD, Darji A, Mendez FJ, Vazquez F, et al. (1999) The conserved undecapeptide shared by thiol-activated cytolysins is involved in membrane binding. FEBS Lett 459: 463-466.
31. Sekino-Suzuki N, Nakamura M, Mitsui KI, Ohno-Iwashita Y, (1996) Contribution of individual tryptophan residues to the structure and activity of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin. Eur J Biochem 241: 941-947.
32. Giddings KS, Zhao J, Sims PJ, Tweten RK, (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat Struct Mol Biol 11: 1173-1178.
33. Soltani CE, Hotze EM, Johnson AE, Tweten RK, (2007) Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin. J Biol Chem 282: 15709-15716.
34. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK, (2010) Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci U S A 107: 4341-4346.
35. Brown DA, Rose JK, (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533-544.
36. Simons K, van Meer G, (1988) Lipid sorting in epithelial cells. Biochemistry 27: 6197-6202.
37. McMahon KA, Zhu M, Kwon SW, Liu P, Zhao Y, et al. (2006) Detergent-free caveolae proteome suggests an interaction with ER and mitochondria. Proteomics 6: 143-152.
38. Sprenger RR, Speijer D, Back JW, De Koster CG, Pannekoek H, et al. (2004) Comparative proteomics of human endothelial cell caveolae and rafts using two-dimensional gel electrophoresis and mass spectrometry. Electrophoresis 25: 156-172.
39. Foster LJ, De Hoog CL, Mann M, (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A 100: 5813-5818.
40. Brown DA, (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21: 430-439.
41. Thornton J, McDaniel LS, (2005) THP-1 monocytes up-regulate intercellular adhesion molecule 1 in response to pneumolysin from Streptococcus pneumoniae. Infect Immun 73: 6493-6498.
42. Sharma GD, He J, Bazan HE, (2003) p38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-talk activation between MAP kinase cascades. J Biol Chem 278: 21989-21997.
43. Kakazu A, Sharma G, Bazan HE, (2008) Association of protein tyrosine phosphatases (PTPs)-1B with c-Met receptor and modulation of corneal epithelial wound healing. Invest Ophthalmol Vis Sci 49: 2927-2935.
44. Norcross EW, Sanders ME, Moore QC, 3rd, Taylor SD, Tullos NA, et al (2011) Active Immunization with Pneumolysin versus 23-Valent Polysaccharide Vaccine for Streptococcus pneumoniae Keratitis. Invest Ophthalmol Vis Sci 52: 9232-9243.
45. Tweten RK, (1988) Nucleotide sequence of the gene for perfringolysin O (theta-toxin) from Clostridium perfringens: significant homology with the genes for streptolysin O and pneumolysin. Infect Immun 56: 3235-3240.
46. Soltani CE, Hotze EM, Johnson AE, Tweten RK, (2007) Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions. Proc Natl Acad Sci U S A 104: 20226-20231.
47. Shepard LA, Shatursky O, Johnson AE, Tweten RK, (2000) The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. Biochemistry 39: 10284-10293.
48. Gekara NO, Jacobs T, Chakraborty T, Weiss S, (2005) The cholesterol-dependent cytolysin listeriolysin O aggregates rafts via oligomerization. Cell Microbiol 7: 1345-1356.
49. Shimada Y, Maruya M, Iwashita S, Ohno-Iwashita Y, (2002) The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur J Biochem 269: 6195-6203.