Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide

Journal of Immunology

Volumn 160, Issue 11, 1998, Pages 5455-5464

  Sellati, Timothy J ^a   Bouis, Deborah A ^a   Kitchens, Richard L ^a   Darveau, Richard P ^b,f   Pugin, Jerome ^c   Ulevitch, Richard J ^d   Gangloff, Sophie C ^e   Goyert, Sanna M ^e   Norgard, Michael V ^a   Radolf, Justin D ^a,g  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e NORTH SHORE UNIVERSITY HOSPITAL   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

^g UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITRIOL; CD14 ANTIGEN; LIPOPOLYSACCHARIDE; LIPOPROTEIN;

ANIMAL CELL; ARTICLE; BORRELIA BURGDORFERI; CONTROLLED STUDY; HUMAN; HUMAN CELL; INFLAMMATION; LYME DISEASE; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN METABOLISM; SIGNAL TRANSDUCTION; SYPHILIS; TREPONEMA PALLIDUM;

ACUTE-PHASE PROTEINS; ANIMALS; ANTIBODIES, BLOCKING; ANTIGENS, CD14; BACTERIAL PROTEINS; BORRELIA BURGDORFERI GROUP; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; CHOLECALCIFEROL; FEMALE; HUMANS; IMMUNE SERA; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-8; LIPOPOLYSACCHARIDES; LIPOPROTEINS; MACROPHAGE ACTIVATION; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MONOCYTES; PEPTIDES; SIGNAL TRANSDUCTION; TREPONEMA PALLIDUM;

EID: 15444352709     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (77)

1. Lukehart, S. A., and K. K. Holmes. 1994. Syphilis. In Harrison's Principles of Internal Medicine, 13th Ed. E. Braunwald, K. J. Isselbacher, R. G. Petersdorf, J. D. Wilson, J. B. Martin, and A. S. Fauci. eds. McGraw-Hill, New York, p. 726.
2. Nocton, J. J., and A. C. Steere 1995. Lyme disease. Adv. Intern. Med. 40:69.
3. Duray, P. H. 1989. Histopathology of clinical phases of Lyme disease. Rheum. Dis. Clin. North Am. 15:691.
4. Takayama, K., R. J. Rothenberg, and A. G. Barbour. 1987. Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 55:2311.
5. Hardy, P. H., Jr., and J. Levin 1983. Lack of endotoxin in Borrelia hispanica and Treponema pallidum. Proc. Soc. Exp. Biol. Med. 174:47.
6. Hoffmann, P., S. Heinle, U. F. Schade, H. Loppnow, A. J. Ulmer, H.-D. Flad, G. Jung, and W. G. Bessler. 1988. Stimulation of human and murine adherent cells by bacterial lipoprotein and synthetic lipopeptide analogs. Immunobiology 177:158.
7. Melchers, F., V. Braun, and C. Galanos. 1975. The lipoprotein of the outer membrane of Escherichia coli: a B cell mitogen. J. Exp. Med. 142:473.
8. Bessler, W. G., M. Cox, A. Lex, B. Suhr, K.-H. Wiesmuller, and G. Jung. 1985. Synthetic lipopeptide analogs of bacterial lipoprotein are potent polyclonal activators for murine B lymphocytes. J. Immunol. 135:1900.
9. Radolf, J. D., M. V. Norgard, M. E. Brandt, R. D. Isaacs, P. A. Thompson, and B. Beutler. 1991. Lipoproteins of Borrelia burgdorferi and Treponema pallidum activate cachectin/tumor necrosis factor synthesis: analysis using a CAT reporter construct. J. Immunol. 147:1968.
10. Ma, Y., and J. J. Weis. 1993. Borrelia burgdorferi outer surface lipoproteins OspA and OspB possess B-cell, mitogenic, and cytokine-stimulalory properties. Infect. Immun. 61:3843.
11. DeOgny, L., B. C. Pramanik, L. L. Arndt, J. D. Jones, J. Rush, C. A. Slaughter. J. D. Radolf, and M. V. Norgard. 1994. Solid-phase synthesis of biologically-active lipopeptides as analogs for spirochetal lipoproteins. Pept. Res. 7:91.
12. Tai, K. F., Y. Ma, and J. J. Weis. 1994. Normal human B lymphocytes and mononuclear cells respond to the mitogenic and cy tokine-stimulatory activities of Borrelia burgdorferi and its lipoprotein OspA. Infect. Immun. 62:520.
13. Weis, J. J., Y. Ma, and L. F. Erdile. 1994. Biological activities of native and recombinant Borrelia burgdorferi outer surface protein A: dependence on lipid modification. Infect. Immun. 62:4632.
14. Radolf, J. D., L. L. Arndt, D. R. Akins, L. L. Curetty, M. E. Levi, Y. Shen, L. S. Davis, and M. V. Norgard. 1995. Treponema pallidum and Borrelia burg- dorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol. 154:2866.
15. Sellati, T. J., L. D. Abrescia, J. D. Radolf, and M. B. Furie. 1996. Outer surface lipoproteins of Borrelia burgdorferi activate vascular endothelium in vitro. Infect. Immun. 64:3180.
16. Norgard, M. V., L. L. Arndt, D. R. Akins, L. L. Curetty, D. A. Harrich, and J. D. Radolf. 1996. Activation of human monocylic cells by Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides proceeds via a pathway distinct from that of lipopolysaccharide but involves the transcriptional activator NF-κB. Infect. Immun. 64:3845.
17. Woolen, R. M., V. R. Modur, T. M. McIntyre, and J. J. Weis. 1996. Borrelia burgdorferi outer membrane protein A induces nuclear translocation of nuclear factor NF-κB and inflammatory activation in human endothelial cells. J. Immunol. 157:4584.
18. Theus, S. A., D. A. Harrich, R. Gaynor, J. D. Radolf, and M. V. Norgard 1998. Virulent Treponema pallidum, treponemal lipoproteins, and synthetic lipoprotein analogs (lipopeptides) induce human immunodeficiency virus-1 gene expression in monocyle/macrophages via nuclear translocation of NF-κB- J. Infect. Dis. 177:941.
19. Morrison, T. B., J. H. Weis, and J. J. Weis. 1997. Borrelia burgdorferi outer surface protein A (OspA) activates and primes human neutrophils. J. Immunol. 158:4838.
20. Norgard, M. V., B. S. Riley, J. A. Richardson, and J. D. Radolf. 1995. Dermal inflammation elicited by synthetic analogs of Treponema pallidum and Borrelia burgdorferi lipoproteins. Infect. Immun. 63:1507.
21. Cleveland, M. G., J. D. Gorham, T. L. Murphy, E.Tuomanen, and K. M. Murphy. 1996. Lipoteichoic acid preparations of Gram-positive bacteria induce interleukin-12 through a CD14-dependent pathway. Infect. Immun. 64:1906.
22. Gupta, D., T. N. Kirkland, S. Viriyakosol, and R. Dziarski. 1996. CD14 is a cell-activating receptor for bacterial peptidoglycan. J. Biol. Chem. 271:23310.
23. Jahr, T. G., L. Ryan, A. Sundan, H. S. Lichenstein, G. Skjak-Braek, and T. Espevik. 1997. Induction of tumor necrosis factor production from monocytes stimulated with mannuronic acid polymers and involvement of lipopolysaccharide-binding protein, CD14, and bactericidal/permeability-increasing factor. Infect. Immun. 65:89.
24. Kusunoki, T., E. Hailman, T. S. C. Juan, H. S. Lichenstein, and S. D. Wright. 1995. Molecules from Staphylococcus aureus that bind CD14 and stimulate innate immune responses. J. Exp. Med. 182:1673.
25. Pugin, J., I. D. Heumann, A. Tomasz, V. V. Kravchenko, Y. Akamatsu, M. Nishijima, M. P. Glauser, P. S. Tobias, and R. J. Ulevitch. 1994. CD14 is a pattern recognition receptor. Immunity 1:509.
26. Savedra, R., Jr., R. L. Delude, R. R. Ingalls, M. J. Fenton, and D. T. Golenbock. 1996. Mycobacterial lipoarabinomannan recognition requires a receptor that shares components of the endotoxin signaling system. J. Immunol. 157:2549.
27. Wright, S. D. 1995. CD14 and innate recognition of bacteria. J. Immunol. 155:6.
28. Wenzel, R. P., M. R. Pinsky, R. J. Ulevitch, and L. Young. 1996. Current understanding of sepsis. Clin. Infect. Dis. 22:407.
29. Corradin, S. B., J. Mauel, P. Gallay, D. Heumann, R. J. Ulevitch, and P. S. Tobias. 1992. Enhancement of murine macrophage binding of and response to bacterial lipopolysaccharide (LPS) by LPS-binding protein. J. Leukocyte Biol. 52:363.
30. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS-binding protein. Science 249:1431.
31. Haziot, A., S. Chen, E. Ferrera, M. G. Low, R. Silber, and S. M. Goyert. 1988. The monocyte differentiation antigen. CD14, is anchored to the cell membrane by a phosphatidylinositol linkage. J. Immunol. 141:547.
32. Hailman, E., H. S. Lichenstein, M. M. Wurfel, D. S. Miller, D. A. Johnson, M. Kelley, L. A. Busse, M. M. Zukowski, and S. D. Wright. 1994. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J. Exp. Med. 179:269.
33. Schumann, R. R., S. R. Leong, G. W. Flaggs, P. W. Gray, S. D. Wright, J. C. Mathison, P. S. Tobias, and R. J. Ulevitch. 1990. Structure and function of lipopolysaccharide-binding protein. Science 249:1429.
34. Ulevitch, R. J., and P. S. Tobias. 1995. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 13:437.
35. Frey, E., D. S. Miller, T. G. Jahr, A. Sundan, V. Bazil, T. Espevik, B. B. Finlay, and S. D. Wright. 1992. Soluble CD14 participates in the response of cells to lipopolysaccharide. J. Exp. Med. 176:1665.
36. Goldblum, S. E., T. W. Brann, X. Ding, J. Pugin, and P. S. Tobias. 1994. Lipopolysaccharide (LPS)-binding protein and soluble CD14 function as accessory molecules for LPS-induced changes in endothelial barrier function, in vitro. J. Clin. Invest. 93:692.
37. Haziot, A., G. W. Rong, J. Silver, and S. M. Goyert. 1993. Recombinant soluble CD14 mediates the activation of endothelial cells by lipopolysaccharide. J. Immunol. 151:1500.
38. Tsuchiya, S., M. Yamabe, Y. Yamaguchi, Y. Kobayashi, T. Konno, and K. Tada. 1980. Establishment and characterization of a human acute monocylic leukemia cell line (THP-1). Int. J. Cancer 26:171.
39. Kitchens, R. L., R. J. Ulevitch, and R. S. Munford. 1992. Lipopolysaccharide (LPS) partial structures inhibit responses to LPS in a human macrophage cell line without inhibiting LPS uptake by a CD14-mediated pathway. J. Exp. Med. 176:485.
40. Martin, T. R., S. M. Mongovin, P. S. Tobias, J. C. Mathison, A. M. Moriarty, D. J. Leturcq, and R. J. Ulevitch. 1994. The CD14 differentiation antigen mediates the development of endotoxin responsiveness during differentiation of mononuclear phagocytes. J. Leukocyte Biol. 56:1.
41. Lee, J. D., K. Kato, P. S. Tobias, T. N. Kirkland, and R. J. Ulevitch. 1992. Transfection of CD14 into 70Z/3 cells dramatically enhances the sensitivity to complexes of lipopolysaccharide (LPS) and LPS-binding protein. J. Exp. Med. 175:1697.
42. Munford, R. S., and C. L. Hall. 1989. Purification of acyloxyacyl hydrolase, a leukocyte enzyme that removes secondary acyl chains from bacterial lipopolysaccharides. J. Biol. Chem. 264:15613.
43. Jones, J. D., K. W. Bourell, M. V. Norgard, and J. D. Radolf. 1995. Membrane topology of Borrelia burgdorferi and Treponema pallidum lipoproteins. Infect. Immun. 63:2424.
44. Bergstrom, S., V. G. Bundoc, and A. G. Barbour. 1989. Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochaete Borrelia burgdorferi. Mol. Microbiol. 3:479.
45. Weigel, L. M., M. E. Brandt, and M. V. Norgard 1992. Analysis of the N-terminal region of the 47-kilodalton integral membrane lipoprotein of Treponema pallidum. Infect. Immun. 60:1568.
46. Golenbock, D. T., Y. Liu, F. H. Millham, M. W. Freeman, and R. A. Zoeller. 1993. Surface expression of human CD14 in Chinese hamster ovary fibroblasts imparts macrophage-like responsiveness to bacterial endotoxin. J. Biol. Chem. 268:22055.
47. Cunningham, M. D., C. Seachord, K. Ratcliffe, B. Bainbridge, A. Aruffo, and R. P. Darveau. 1996. Helicobacter pylori and Porphyromonas gingivalis lipopolysaccharides are poorly transferred to recombinant soluble CD 14. Infect. Immun. 64:3601.
48. Haziot, A., E. Ferrero, F. Königen, N. Hijiya, S. Yamamoto, J. Silver, C. L. Stewart, and S. M. Goyert. 1996. Resistance to endotoxin shock and reduced dissemination of Gram-negative bacteria in CD14-deficient mice. Immunity 4:407.
49. Baggiolini, M., P. Loetscher, and B. Moser. 1995. Interleukin-8 and the chemokine family. Int. J. Immunopharmacol. 17:103.
50. Zachariae, C. O. C., and K. Matsushima. 1997. Interleukin-8. In Encyclopedia of Immunology. I. M. Roitt and P. J. Delves, eds. Academic Press, London, p. 922.
51. Straubinger, R. K., A. F. Straubinger, L. Harter, R. H. Jacobson, Y. F. Chang, B. A. Summer, H. N. Erb, and M. J. G. Appel. 1997. Borrelia burgdorferi migrates into joint capsules and causes an up-regulation of interleukin-8 in synovial membranes of dogs experimentally infected with ticks. Infect, Immun. 65:1273.
52. Burns, M. J., T. J. Sellati, E. I. Teng, and M. B. Furie. 1997. Production of interleukin-8 (IL-8) by cultured endothelial cells in response to Borrelia burgdorferi occurs independently of secreted IL-1 and tumor necrosis factor α and is required for subsequent transendothelial migration of neutrophils. Infect. Immun. 65:1217.
53. Shimizu, T., Y. Ohtsuka, Y. Yanagihara, M. Kurimura, M. Takemoto, and K. Achiwa. 1991. Comparison of biologic activities of synthetic lipopentapeptide analogs of bacterial lipoprotein in mice. Mol. Biother. 3:46.
54. 3. J. Leukoc. Biol. 59:555.
55. 3. J. Immunol. 153:3276.
56. Haziot, A., E. Ferrero, X. Y. Lin, C. L. Stewart, and S. M. Goyert. 1995. CD14-deficient mice are exquisitely insensitive to the effects of LPS. Prog. Clin. Biol. Res. 392:349.
57. Perera, P.-Y., S. Vogel, G. R. Detore, A. Haziot, and S. M. Goyert. 1997. CD14-dependent and CD14-independent signaling pathways in murine macrophages from normal and CD14 knockout mice stimulated with lipopolysaccharide or taxol. J. Immunol. 158:4422.
58. Ebnet, K., K. D. Brown, U. K. Siebenlist, M. M. Simon, and S. Shaw. 1997. Borrelia burgdorferi activates nuclear factor-κB and is a potent inducer of chemokine and adhesion molecule gene expression in endothelial cells and fibroblasts. J. Immunol. 158:3285.
59. Haas, J. G., P. A. Baeuerle, G. Riethmuller, and H. W. Ziegler-Heitbrock. 1990. Molecular mechanisms in down-regulation of tumor necrosis factor expression. Proc. Natl. Acad. Sci. USA 87:9563.
60. Kitchens, R. L., and R. S. Munford. 1995. Enzymatically deacylated lipopolysaccharide (LPS) can antagonize LPS at multiple sites in the LPS recognition pathway. J. Biol. Chem. 270:9904.
61. Asch, E. S., D. I. Bujak, M. Weiss, M. G. Peterson, and A. Weinstein. 1994. Lyme disease: an infectious and postinfectious syndrome. J. Rheum. 21:454.
62. Shadick, N. A., C. B. Phillips, E. L. Logigian, A. C. Steere, R. F. Kaplan, V. P. Berardi, P. H. Duray, M. G. Larson, E. A. Wright, K. S. Ginsburg, J. N. Katz, and M. H. Liang. 1994. The long-term clinical outcomes of Lyme disease: a population-based retrospective cohort study. Ann. Intern. Med. 121:560.
63. Mühlradt, P. F., M. Kieß, H. Meyer, and G. Jung. 1997. Isolation, structure elucidation, and synthesis of a macrophage stimulatory lipopeptide from Mycoplasma fermentans acting at picomolar concentration. J. Exp. Med. 185:1951.
64. Akins, D. R., B. K. Purcell, M. Mitra, M. V. Norgard, and J. D. Radolf. 1993. Lipid modification of the 17-kilodalton membrane immunogen of Treponema pallidum determines macrophage activation as well as amphiphilicity. Infect. Immun. 61:1202.
65. Wooten, R. M., T. B. Morrison, J. H. Weis, R. Thieringer, and J. J. Weis. 1998. The role of CD14 in signaling mediated by outer membrane lipoproteins of Borrelia burgdorferi. J. Immunol. In Press.
66. Metzger, J. W., A. G. Beck-Sickinger, M. Loleit, M. Eckert, W. G. Bessler, and G. Jung. 1995. Synthetic S-(2,3-dihydroxypropyl)-cysteinyl peptides derived from the N-terminus of the cytochrome subunit of the photoreaction center of Rhodopseudomonas, viridis enhance murine splenocyte proliferation, J. Pept. Sci. 3:184.
67. Belisle, J. T., M. E. Brandt, J. D. Radolf, and M. V. Norgard. 1994. Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J. Bacterial. 176:2151.
68. Brandt, M. E., B. S. Riley, J. D. Radolf, and M. V. Norgard. 1990. Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins. Infect. Immun. 58:983.
69. Chamberlain, N. R., M. E. Brandt, A. L. Erwin, J. D. Radoif, and M. V. Norgard. 1989. Major integral membrane protein immunogens of Treponema pallidum are proteolipids. Infect. Immun. 57:2872.
70. de Silva, A. M., S. R. Telford, L. R. Brunet, S. W. Barthold, and E. Fikrig. 1996. Borrelia burgdorferi OspA is an arthropod-specific transmission-blocking lyme disease vaccine. J. Exp. Med. 183:271.
71. Montgomery, R. K., S. E. Malawista, K. J. M. Feen, and L. K. Bockenstedt. 1996. Direct demonstration of antigenic substitution of Borrelia burgdorferi ex vivo: exploration of the paradox of the early immune response to outer surface proteins A and C in Lyme disease. J. Exp. Med. 183:261.
72. Schwan, T. G., J. Piesman, W. T. Golde, M. C. Dolan, and P. A. Rosa. 1995. Induction of an outer surface protein on Borrelia burgdorferi during lick feeding. Proc. Natl. Acad. Sci. USA 92:2909.
73. Stevenson, B., T. G. Schwan, and P. A. Rosa. 1995. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:4535.
74. Akins, D. R., S. F. Porcella, T. G. Popova, D. Shevchenko, S. I. Baker, M. Li, M. V. Norgard, and J. D. Radolf 1995. Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homolog. Mol. Microbiol. 18:507.
75. + T cells. Immunol. Lett. 46:137.
76. Delude, R. L., R. Savedra, Jr., H. Zhao, R. Thieringer, S. Yamamoto, M. J. Fenton, and D. T. Golenbock. 1995. CD14 enhances cellular responses to endotoxin without imparting ligand-specific recognition. Proc. Natl. Acad. Sci. USA 92:9288.
77. Cauwels, A., E. Wan, M. Leisman, and E. Tuomanen. 1997. Coexistence of CD14-dependent and independent pathways for stimulalion of human monocytes by Gram-posilive bacteria. Infect. Immun. 65:3255.