Cholesterol lipids of borrelia burgdorferi form lipid rafts and are required for the bactericidal activity of a complement-independent antibody

Cell Host and Microbe

Volumn 8, Issue 4, 2010, Pages 331-342

  Larocca, Timothy J ^a   Crowley, Jameson T ^a   Cusack, Brian J ^a   Pathak, Priyadarshini ^a   Benach, Jordi ^b   London, Erwin ^a   Garcia Monco, Juan C ^a   Benach, Jorge L ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b ALBA SYNCHROTRON LIGHT SOURCE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; CB 2 ANTIBODY; CHOLESTEROL; GLYCOLIPID; LIPID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERICIDAL ACTIVITY; BORRELIA BURGDORFERI; MEMBRANE VESICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; SPIROCHETE; TEMPERATURE SENSITIVITY;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; CHOLESTEROL; COMPLEMENT SYSTEM PROTEINS; CYTOPLASMIC VESICLES; GLYCOLIPIDS; LYME DISEASE; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C3H;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; PROKARYOTA;

EID: 77958089989     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2010.09.001     Document Type: Article

References (57)

1. A.G. Ayuyan, and F.S. Cohen Raft composition at physiological temperature and pH in the absence of detergents Biophys. J. 94 2008 2654 2666
2. O. Bakht, P. Pathak, and E. London Effect of the structure of lipids favoring disordered domain formation on the stability of cholesterol-containing ordered domains (lipid rafts): identification of multiple raft-stabilization mechanisms Biophys. J. 93 2007 4307 4318
3. M. Becker, J. Bunikis, B.D. Lade, J.J. Dunn, A.G. Barbour, and C.L. Lawson Structural investigation of Borrelia burgdorferi OspB, a bactericidal Fab target J. Biol. Chem. 280 2005 17363 17370
4. J.T. Belisle, M.E. Brandt, J.D. Radolf, and M.V. Norgard Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins J. Bacteriol. 176 1994 2151 2157
5. G. Ben-Menachem, J. Kubler-Kielb, B. Coxon, A. Yergey, and R. Schneerson A newly discovered cholesteryl galactoside from Borrelia burgdorferi Proc. Natl. Acad. Sci. USA 100 2003 7913 7918
6. J.L. Benach, E.M. Bosler, J.P. Hanrahan, J.L. Coleman, G.S. Habicht, T.F. Bast, D.J. Cameron, J.L. Ziegler, A.G. Barbour, and W. Burgdorfer Spirochetes isolated from the blood of two patients with Lyme disease N. Engl. J. Med. 308 1983 740 742
7. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
8. L.K. Bockenstedt, S. Barthold, K. Deponte, N. Marcantonio, and F.S. Kantor Borrelia burgdorferi infection and immunity in mice deficient in the fifth component of complement Infect. Immun. 61 1993 2104 2107
9. M.E. Brandt, B.S. Riley, J.D. Radolf, and M.V. Norgard Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins Infect. Immun. 58 1990 983 991
10. R.E. Brown Sphingolipid organization in biomembranes: what physical studies of model membranes reveal J. Cell Sci. 111 1998 1 9
11. D.A. Brown, and E. London Structure and function of sphingolipid- and cholesterol-rich membrane rafts J. Biol. Chem. 275 2000 17221 17224
12. D.A. Brown, and J.K. Rose Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface Cell 68 1992 533 544
13. W. Burgdorfer, A.G. Barbour, S.F. Hayes, J.L. Benach, E. Grunwaldt, and J.P. Davis Lyme disease-a tick-borne spirochetosis? Science 216 1982 1317 1319
14. T. Bykowski, M.E. Woodman, A.E. Cooley, C.A. Brissette, R. Wallich, V. Brade, P. Kraiczy, and B. Stevenson Borrelia burgdorferi complement regulator-acquiring surface proteins (BbCRASPs): Expression patterns during the mammal-tick infection cycle Int. J. Med. Microbiol. 298 Suppl 1 2008 249 256
15. Z. Chen, and R.P. Rand The influence of cholesterol on phospholipid membrane curvature and bending elasticity Biophys. J. 73 1997 267 276
16. J.L. Coleman, R.C. Rogers, and J.L. Benach Selection of an escape variant of Borrelia burgdorferi by use of bactericidal monoclonal antibodies to OspB Infect. Immun. 60 1992 3098 3104
17. J.L. Coleman, L.I. Katona, C. Kuhlow, A. Toledo, N.A. Okan, R. Tokarz, and J.L. Benach Evidence that two ATP-dependent (Lon) proteases in Borrelia burgdorferi serve different functions PLoS Pathog. 5 2009 e1000676
18. S.E. Connolly, and J.L. Benach Cutting edge: the spirochetemia of murine relapsing fever is cleared by complement-independent bactericidal antibodies J. Immunol. 167 2001 3029 3032
19. S.E. Connolly, and J.L. Benach The versatile roles of antibodies in Borrelia infections Nat. Rev. Microbiol. 3 2005 411 420
20. S.E. Connolly, D.G. Thanassi, and J.L. Benach Generation of a complement-independent bactericidal IgM against a relapsing fever Borrelia J. Immunol. 172 2004 1191 1197
21. R.M. Epand Proteins and cholesterol-rich domains Biochim. Biophys. Acta 1778 2008 1576 1582
22. R. Escudero, M.L. Halluska, P.B. Backenson, J.L. Coleman, and J.L. Benach Characterization of the physiological requirements for the bactericidal effects of a monoclonal antibody to OspB of Borrelia burgdorferi by confocal microscopy Infect. Immun. 65 1997 1908 1915
23. A. Fujita, J. Cheng, M. Hirakawa, K. Furukawa, S. Kusunoki, and T. Fujimoto Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling Mol. Biol. Cell 18 2007 2112 2122
24. J.C. García Moncó, C.M. Wheeler, J.L. Benach, R.A. Furie, S.A. Lukehart, G. Stanek, and A.C. Steere Reactivity of neuroborreliosis patients (Lyme disease) to cardiolipin and gangliosides J. Neurol. Sci. 117 1993 206 214
25. J.C. Garcia-Monco, R.J. Seidman, and J.L. Benach Experimental immunization with Borrelia burgdorferi induces development of antibodies to gangliosides Infect. Immun. 63 1995 4130 4137
26. M. Haque, Y. Hirai, K. Yokota, and K. Oguma Steryl glycosides: a characteristic feature of the Helicobacter spp.? J. Bacteriol. 177 1995 5334 5337
27. Y. Hirai, M. Haque, T. Yoshida, K. Yokota, T. Yasuda, and K. Oguma Unique cholesteryl glucosides in Helicobacter pylori: composition and structural analysis J. Bacteriol. 177 1995 5327 5333
28. R.C. Johnson The spirochetes Annu. Rev. Microbiol. 31 1977 89 106
29. J.D. Jones, K.W. Bourell, M.V. Norgard, and J.D. Radolf Membrane topology of Borrelia burgdorferi and Treponema pallidum lipoproteins Infect. Immun. 63 1995 2424 2434
30. L.I. Katona, S. Ayalew, J.L. Coleman, and J.L. Benach A bactericidal monoclonal antibody elicits a change in its antigen, OspB of Borrelia burgdorferi, that can be detected by limited proteolysis J. Immunol. 164 2000 1425 1431
31. Y. Kinjo, E. Tupin, D. Wu, M. Fujio, R. Garcia-Navarro, M.R. Benhnia, D.M. Zajonc, G. Ben-Menachem, G.D. Ainge, and G.F. Painter Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria Nat. Immunol. 7 2006 978 986
32. T.J. LaRocca, and J.L. Benach The important and diverse roles of antibodies in the host response to Borrelia infections Curr. Top. Microbiol. Immunol. 319 2008 63 103
33. T.J. LaRocca, L.I. Katona, D.G. Thanassi, and J.L. Benach Bactericidal action of a complement-independent antibody against relapsing fever Borrelia resides in its variable region J. Immunol. 180 2008 6222 6228
34. T.J. LaRocca, D.J. Holthausen, C. Hsieh, C. Renken, C.A. Mannella, and J.L. Benach The bactericidal effect of a complement-independent antibody is osmolytic and specific to Borrelia Proc. Natl. Acad. Sci. USA 106 2009 10752 10757
35. H. Li, J.J. Dunn, B.J. Luft, and C.L. Lawson Crystal structure of Lyme disease antigen outer surface protein A complexed with an Fab Proc. Natl. Acad. Sci. USA 94 1997 3584 3589
36. M. Lin, and Y. Rikihisa Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid A biosynthesis and incorporate cholesterol for their survival Infect. Immun. 71 2003 5324 5331
37. B.P. Livermore, R.F. Bey, and R.C. Johnson Lipid metabolism of Borrelia hermsi Infect. Immun. 20 1978 215 220
38. E. London Insights into lipid raft structure and formation from experiments in model membranes Curr. Opin. Struct. Biol. 12 2002 480 486
39. E. London, and G.W. Feligenson A convenient and sensitive fluorescence assay for phospholipid vesicles using diphenylhexatriene Anal. Biochem. 88 1978 203 211
40. K. Newman Jr., and R.C. Johnson In vivo evidence that an intact lytic complement pathway is not essential for successful removal of circulating Borrelia turicatae from mouse blood Infect. Immun. 31 1981 465 469
41. B. Nichols Caveosomes and endocytosis of lipid rafts J. Cell Sci. 116 2003 4707 4714
42. L.J. Pike The challenge of lipid rafts J. Lipid Res. 50 Suppl 2009 S323 S328
43. J.D. Radolf, K.W. Bourell, D.R. Akins, J.S. Brusca, and M.V. Norgard Analysis of Borrelia burgdorferi membrane architecture by freeze-fracture electron microscopy J. Bacteriol. 176 1994 21 31
44. J.D. Radolf, M.S. Goldberg, K. Bourell, S.I. Baker, J.D. Jones, and M.V. Norgard Characterization of outer membranes isolated from Borrelia burgdorferi, the Lyme disease spirochete Infect. Immun. 63 1995 2154 2163
45. A. Sadziene, P.A. Thompson, and A.G. Barbour In vitro inhibition of Borrelia burgdorferi growth by antibodies J. Infect. Dis. 167 1993 165 172
46. C. Salaün, D.J. James, and L.H. Chamberlain Lipid rafts and the regulation of exocytosis Traffic 5 2004 255 264
47. N.W. Schröder, U. Schombel, H. Heine, U.B. Göbel, U. Zähringer, and R.R. Schumann Acylated cholesteryl galactoside as a novel immunogenic motif in Borrelia burgdorferi sensu stricto J. Biol. Chem. 278 2003 33645 33653
48. D.E. Shvartsman, M. Kotler, R.D. Tall, M.G. Roth, and Y.I. Henis Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts J. Cell Biol. 163 2003 879 888
49. P.F. Smith Biosynthesis of cholesteryl glucoside by Mycoplasma gallinarum J. Bacteriol. 108 1971 986 991
50. G. Stübs, V. Fingerle, B. Wilske, U.B. Göbel, U. Zähringer, R.R. Schumann, and N.W. Schröder Acylated cholesteryl galactosides are specific antigens of borrelia causing lyme disease and frequently induce antibodies in late stages of disease J. Biol. Chem. 284 2009 13326 13334
51. D.J. Trott, D.P. Alt, R.L. Zuerner, M.J. Wannemuehler, and T.B. Stanton The search for Brachyspira outer membrane proteins that interact with the host Anim. Health Res. Rev. 2 2001 19 30
52. Y. Wang, C. Thiele, and W.B. Huttner Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network Traffic 1 2000 952 962
53. C.M. Wheeler, J.C. Garcia Monco, J.L. Benach, M.G. Golightly, G.S. Habicht, and A.C. Steere Nonprotein antigens of Borrelia burgdorferi J. Infect. Dis. 167 1993 665 674
54. H.J. Willison, and P.G. Kennedy The fine specificity of anti-GM1 antibodies Q. J. Med. 86 1993 216 217
55. X. Xu, R. Bittman, G. Duportail, D. Heissler, C. Vilcheze, and E. London Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide J. Biol. Chem. 276 2001 33540 33546
56. J. Zhang, A. Pekosz, and R.A. Lamb Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins J. Virol. 74 2000 4634 4644 (Pubitemid 30237888)
57. R. Zidovetzki, and I. Levitan Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies Biochim. Biophys. Acta 1768 2007 1311 1324