Mouse, but Not Human, ApoB-100 Lipoprotein Cholesterol Is a Potent Innate Inhibitor of Streptococcus pneumoniae Pneumolysin

PLoS Pathogens

Volumn 10, Issue 9, 2014, Pages

  Wade, Kristin R ^a   Hotze, Eileen M ^a   Briles, David E ^b   Tweten, Rodney K ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN B100; BACTERIAL TOXIN; CHOLEST 4 EN 3 ONE; CHOLESTEROL OXIDASE; CYTOLYSIN; FLUORESCENT DYE; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; NEUTRALIZING ANTIBODY; PERFRINGOLYSIN O; PNEUMOLYSIN; PROTEINASE; STREPTOLYSIN O; TOXIN ANTIBODY; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN; BACTERIAL PROTEIN; CHOLESTEROL; LIPOPROTEIN; LIPOPROTEIN CHOLESTEROL; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STREPTOLYSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; CHANNEL GATING; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DENSITOMETRY; DETOXIFICATION; EC50; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; GUINEA PIG; HEMOLYSIS; HUMAN; IMMUNOPRECIPITATION; INNATE IMMUNITY; MOUSE; NONHUMAN; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PURIFICATION; RECOMBINANT PLASMID; SERUM BACTERICIDAL ANTIBODY ASSAY; STREPTOCOCCUS PNEUMONIAE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; CELL MEMBRANE; COMPARATIVE STUDY; DRUG EFFECTS; METABOLISM;

STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANTIBODIES, NEUTRALIZING; APOLIPOPROTEIN B-100; BACTERIAL PROTEINS; CELL MEMBRANE; CHOLESTEROL; GUINEA PIGS; HEMOLYSIS; HUMANS; LIPOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; STREPTOLYSINS;

EID: 84907572372     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004353     Document Type: Article

References (77)

1. Rothblat GH, Phillips MC, (2010) High-density lipoprotein heterogeneity and function in reverse cholesterol transport. Curr Opin Lipidol 21: 229–238.
2. Hevonoja T, Pentikainen MO, Hyvonen MT, Kovanen PT, Ala-Korpela M, (2000) Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim Biophys Acta 1488: 189–210.
3. Los FC, Randis TM, Aroian RV, Ratner AJ, (2013) Role of pore-forming toxins in bacterial infectious diseases. Microbiol Mol Biol Rev 77: 173–207.
4. 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.
5. Ohno-Iwashita Y, Iwamoto M, Mitsui K, Ando S, Iwashita S, (1991) A cytolysin, theta-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich region. J Biochem 110: 369–375.
6. Prigent D, Alouf JE, (1976) Interaction of steptolysin O with sterols. Biochim Biophys Acta 443: 288–300.
7. Hotze EM, Tweten RK, (2012) Membrane assembly of the cholesterol-dependent cytolysin pore complex. Biochim Biophys Acta 1818: 1028–1038.
8. Gelber SE, Aguilar JL, Lewis KL, Ratner AJ, (2008) Functional and phylogenetic characterization of Vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J Bacteriol 190: 3896–3903.
9. Rampersaud R, Planet PJ, Randis TM, Kulkarni R, Aguilar JL, et al. (2011) Inerolysin, a cholesterol-dependent cytolysin produced by Lactobacillus iners. J Bacteriol 193: 1034–1041.
10. Shumway CN, Klebanoff SJ, (1971) Purification of pneumolysin. Infect Immun 4: 388–392.
11. Geoffroy C, Alouf JE, (1983) Selective purification by thiol-disulfide interchange chromatography of alveolysin, a sulfhydryl-activated toxin of Bacillus alvei. Toxin properties and interaction with cholesterol and liposomes. J Biol Chem 258: 9968–9972.
12. Shannon JG, Ross CL, Koehler TM, Rest RF, (2003) Characterization of anthrolysin O, the Bacillus anthracis cholesterol-dependent cytolysin. Infect Immun 71: 3183–3189.
13. Jacobs T, Darji A, Frahm N, Rohde M, Wehland J, et al. (1998) Listeriolysin O: cholesterol inhibits cytolysis but not binding to cellular membranes. Mol Microbiol 28: 1081–1089.
14. Heuck AP, Savva CG, Holzenburg A, Johnson AE, (2007) Conformational Changes That Effect Oligomerization and Initiate Pore Formation Are Triggered throughout Perfringolysin O upon Binding to Cholesterol. J Biol Chem 282: 22629–22637.
15. Heuck AP, Hotze E, Tweten RK, Johnson AE, (2000) Mechanism of membrane insertion of a multimeric b-barrel protein: Perfringolysin O creates a pore using ordered and coupled conformational changes. Molec Cell 6: 1233–1242.
16. Flanagan JJ, Tweten RK, Johnson AE, Heuck AP, (2009) Cholesterol exposure at the membrane surface is necessary and sufficient to trigger perfringolysin O binding. Biochemistry 48: 3977–3987.
17. Nelson LD, Johnson AE, London E, (2008) How interaction of perfringolysin O with membranes is controlled by sterol structure, lipid structure, and physiological low pH: insights into the origin of perfringolysin O-lipid raft interaction. J Biol Chem 283: 4632–4642.
18. Zitzer A, Bittman R, Verbicky CA, Erukulla RK, Bhakdi S, et al. (2001) Coupling of cholesterol and cone-shaped lipids in bilayers augments membrane permeabilization by the cholesterol-specific toxins streptolysin O and Vibrio cholerae cytolysin. J Biol Chem 276: 14628–14633.
19. Prassl R, Laggner P, (2009) Molecular structure of low density lipoprotein: current status and future challenges. Eur Biophys J 38: 145–158.
20. Grass DS, Saini U, Felkner RH, Wallace RE, Lago WJ, et al. (1995) Transgenic mice expressing both human apolipoprotein B and human CETP have a lipoprotein cholesterol distribution similar to that of normolipidemic humans. J Lipid Res 36: 1082–1091.
21. Tweten RK, (2005) The cholesterol-dependent cytolysins; a family of versatile pore-forming toxins. Infect Immun 73: 6199–6209.
22. Balachandran P, Hollingshead SK, Paton JC, Briles DE, (2001) The autolytic enzyme LytA of Streptococcus pneumoniae is not responsible for releasing pneumolysin. J Bacteriol 183: 3108–3116.
23. Price KE, Camilli A, (2009) Pneumolysin localizes to the cell wall of Streptococcus pneumoniae. J Bacteriol 191: 2163–2168.
24. Price KE, Greene NG, Camilli A, (2012) Export requirements of pneumolysin in Streptococcus pneumoniae. J Bacteriol 194: 3651–3660.
25. Marriott HM, Mitchell TJ, Dockrell DH, (2008) Pneumolysin: a double-edged sword during the host-pathogen interaction. Curr Mol Med 8: 497–509.
26. Adegbola RA, Obaro SK, (2000) Diagnosis of childhood pneumonia in the tropics. Ann Trop Med Parasitol 94: 197–207.
27. Paton JC, Rowan KB, Ferrante A, (1984) Activation of human complement by the pneumococcal toxin pneumolysin. Infect Immun 43: 1085–1087.
28. Mitchell TJ, Andrew PW, Saunders FK, Smith AN, Boulnois GJ, (1991) Complement activation and antibody binding by pneumolysin via a region of the toxin homologous to a human acute-phase protein. Mol Microbiol 5: 1883–1888.
29. Jarva H, Jokiranta TS, Wurzner R, Meri S, (2003) Complement resistance mechanisms of streptococci. Mol Immunol 40: 95–107.
30. Yuste J, Botto M, Paton JC, Holden DW, Brown JS, (2005) Additive inhibition of complement deposition by pneumolysin and PspA facilitates Streptococcus pneumoniae septicemia. J Immunol 175: 1813–1819.
31. Francois RJ, (1965) Beta-haemolytic streptococci and antistreptolysin-O titres in patients with rheumatoid arthritis and a matched control group. Ann Rheum Dis 24: 369–377.
32. Klein GC, Baker CN, Jones WL, (1971) “Upper limits of normal” antistreptolysin O and antideoxyribonuclease B titers. Appl Microbiol 21: 999–1001.
33. Johnson MK, Callegan MC, Engel LS, O'Callaghan RJ, Hill JM, et al. (1995) Growth and virulence of a complement-activation-negative mutant of Streptococcus pneumoniae in the rabbit cornea. Curr Eye Res 14: 281–284.
34. Force E, Taberner F, Cabellos C, Ribes S, Domenech A, et al. (2008) Experimental study of meropenem in the therapy of cephalosporin-susceptible and -resistant pneumococcal meningitis. Eur J Clin Microbiol Infect Dis 27: 685–690.
35. Norcross EW, Sanders ME, Moore QC, 3rdTaylor 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.
36. Blank AL, Davis GL, VanDeWater TR, Ruben RJ, (1994) Acute Streptococcus pneumoniae meningogenic labyrinthitis. An experimental guinea pig model and literature review. Arch Otolaryngol Head Neck Surg 120: 1342–1346.
37. Kuo J, Douglas M, Ree HK, Lindberg AA, (1995) Characterization of a recombinant pneumolysin and its use as a protein carrier for pneumococcal type 18C conjugate vaccines. Infect Immun 63: 2706–2713.
38. Skinner LJ, Beurg M, Mitchell TJ, Darrouzet V, Aran JM, et al. (2004) Intracochlear perfusion of pneumolysin, a pneumococcal protein, rapidly abolishes auditory potentials in the Guinea pig cochlea. Acta Otolaryngol 124: 1000–1007.
39. Salha D, Szeto J, Myers L, Claus C, Sheung A, et al. (2012) Neutralizing antibodies elicited by a novel detoxified pneumolysin derivative, PlyD1, provide protection against both pneumococcal infection and lung injury. Infect Immun 80: 2212–2220.
40. Paton JC, Lock RA, Hansman DJ, (1983) Effect of immunization with pneumolysin on survival time of mice challenged with Streptococcus pneumoniae. Infect Immun 40: 548–552.
41. Goldman DL, Zeng W, Rivera J, Nakouzzi A, Casadevall A, (2008) Human serum contains a protease that protects against cytotoxic activity of Bacillus anthracis lethal toxin in vitro. Clin Vaccine Immunol 15: 970–973.
42. Moayeri M, Wiggins JF, Leppla SH, (2007) Anthrax protective antigen cleavage and clearance from the blood of mice and rats. Infect Immun 75: 5175–5184.
43. 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.
44. Shepard LA, Shatursky O, Johnson AE, Tweten RK, (2000) The mechanism of assembly and insertion of the membrane complex of the cholesterol-dependent cytolysin perfringolysin O: Formation of a large prepore complex. Biochemistry 39: 10284–10293.
45. Hotze EM, Wilson-Kubalek E, Farrand AJ, Bentsen L, Parker MW, et al. (2012) Monomer-monomer interactions propagate structural transitions necessary for pore formation by the cholesterol-dependent cytolysins. J Biol Chem 287: 24534–24543.
46. Hotze EM, Wilson-Kubalek EM, Rossjohn J, Parker MW, Johnson AE, et al. (2001) Arresting pore formation of a cholesterol-dependent cytolysin by disulfide trapping synchronizes the insertion of the transmembrane beta-sheet from a prepore intermediate. J Biol Chem 276: 8261–8268.
47. Harris RW, Sims PJ, Tweten RK, (1991) Kinetic aspects of the aggregation of Clostridium perfringens theta toxin on erythrocyte membranes: A fluorescence energy transfer study. J Biol Chem 266: 6936–6941.
48. Allen JK, Hensley WJ, Nicholls AV, Whitfield JB, (1979) An enzymic and centrifugal method for estimating high-density lipoprotein cholesterol. Clin Chem 25: 325–327.
49. Goulart C, da Silva TR, Rodriguez D, Politano WR, Leite LC, et al. (2013) Characterization of protective immune responses induced by pneumococcal surface protein A in fusion with pneumolysin derivatives. PLoS One 8: e59605.
50. Kovanen PT, Faust JR, Brown MS, Goldstein JL, (1979) Low density lipoprotein receptors in bovine adrenal cortex. I. Receptor-mediated uptake of low density lipoprotein and utilization of its cholesterol for steroid synthesis in cultured adrenocortical cells. Endocrinology 104: 599–609.
51. Lundberg J, Rudling M, Angelin B, (2013) Interstitial fluid lipoproteins. Curr Opin Lipidol 24: 327–331.
52. Cross CE, Forte TM, Gunther RA, Kramer GC, (1983) Lipoprotein distribution in sheep lung lymph. J Lab Clin Med 101: 641–650.
53. Benton KA, Everson MP, Briles DE, (1995) A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect Immun 63: 448–455.
54. Lindsay JR, Boorman GA, Collins MC, Hsu C-K, van Hoosier Jr GL, et al. (1991) Infectious diseases of mice and rats. : The National Academies Press.
55. Fallon MT, Reinhard MK, Gray BM, Davis TW, Lindsey JR, (1988) Inapparent Streptococcus pneumoniae type 35 infections in commercial rats and mice. Lab Anim Sci 38: 129–132.
56. Prigent D, Alouf JE, (1976) Interaction of streptolysin-O with sterols. Biochim Biophys Acta 443: 288–300.
57. Esterbauer H, Ramos P, (1996) Chemistry and pathophysiology of oxidation of LDL. Rev Physiol Biochem Pharmacol 127: 31–64.
58. Lund-Katz S, Phillips MC, (1984) Packing of cholesterol molecules in human high-density lipoproteins. Biochemistry 23: 1130–1138.
59. Lund-Katz S, Phillips MC, (1986) Packing of cholesterol molecules in human low-density lipoprotein. Biochemistry 25: 1562–1568.
60. Esterbauer H, Gebicki J, Puhl H, Jurgens G, (1992) The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med 13: 341–390.
61. Nelson LD, Chiantia S, London E, (2010) Perfringolysin O association with ordered lipid domains: implications for transmembrane protein raft affinity. Biophys J 99: 3255–3263.
62. Heuck AP, Tweten RK, Johnson AE, (2003) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J Biol Chem 278: 31218–31225.
63. 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.
64. 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.
65. Johnson BB, Moe PC, Wang D, Rossi K, Trigatti BL, et al. (2012) Modifications in perfringolysin O domain 4 alter the cholesterol concentration threshold required for binding. Biochemistry 51: 3373–3382.
66. Rigby C, (1976) Natural infections of guinea-pigs. Lab Anim 10: 119–142.
67. Imohl M, Reinert RR, Ocklenburg C, van der Linden M, (2010) Association of serotypes of Streptococcus pneumoniae with age in invasive pneumococcal disease. J Clin Microbiol 48: 1291–1296.
68. Holmlund E, Quiambao B, Ollgren J, Nohynek H, Kayhty H, (2006) Development of natural antibodies to pneumococcal surface protein A, pneumococcal surface adhesin A and pneumolysin in Filipino pregnant women and their infants in relation to pneumococcal carriage. Vaccine 24: 57–65.
69. Francis JP, Richmond PC, Pomat WS, Michael A, Keno H, et al. (2009) Maternal antibodies to pneumolysin but not to pneumococcal surface protein A delay early pneumococcal carriage in high-risk Papua New Guinean infants. Clin Vaccine Immunol 16: 1633–1638.
70. Briles DE, Ades E, Paton JC, Sampson JS, Carlone GM, et al. (2000) Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect Immun 68: 796–800.
71. Shepard LA, Heuck AP, Hamman BD, Rossjohn J, Parker MW, et al. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an alpha-helical to beta-sheet transition identified by fluorescence spectroscopy. Biochemistry 37: 14563–14574.
72. Hotze EM, Le HM, Sieber JR, Bruxvoort C, McInerney MJ, et al. (2013) Identification and characterization of the first cholesterol-dependent cytolysins from Gram-negative bacteria. Infect Immun 81: 216–225.
73. Zhou J, Montefiori DC, (1996) Complement-activating antibodies in sera from infected individuals and vaccinated volunteers that target human immunodeficiency virus type 1 to complement receptor type 1 (CR1, CD35). Virology 226: 13–21.
74. Shepard LA, Heuck AP, Hamman BD, Rossjohn J, Parker MW, et al. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an a-helical to b-sheet transition identified by fluorescence spectroscopy. Biochemistry 37: 14563–14574.
75. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophoton Int 11: 36–42.
76. Hotze EM, Heuck AP, Czajkowsky DM, Shao Z, Johnson AE, et al. (2002) Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J Biol Chem 277: 11597–11605.
77. 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.