Induction of pro- and anti-inflammatory cytokines by Borrelia burgdorferi lipoproteins in monocytes is mediated by CD14

Infection and Immunity

Volumn 67, Issue 1, 1999, Pages 140-147

  Giambartolomei, Guillermo H ^a,b   Dennis, Vida A ^a   Lasater, Barbara L ^a   Philipp, Mario T ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b Sociedad Argentina de Diabetes   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CD14 ANTIGEN; CYSTEINE; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOHEXAPEPTIDE; LIPOPROTEIN; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; PALMITIC ACID; UNCLASSIFIED DRUG;

ACYLATION; ARTICLE; B LYMPHOCYTE; BORRELIA BURGDORFERI; CONTROLLED STUDY; HUMAN; HUMAN CELL; INFLAMMATION; MONOCYTE; MONONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 0032921174     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.1.140-147.1999     Document Type: Article

References (53)

1. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 12:141-179.
2. Barthold, S. W., C. L. Sidman, and A. L. Smith. 1992. Lyme borreliosis in genetically resistant and susceptible mice with severe combined immunodeficiency. Am. J. Trop. Med. Hyg. 47:605-613.
3. Barthold, S. W., D. H. Persing, A. L. Armstrong, and R. A. Peeples. 1991. Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Am. J. Pathol. 139:263-273.
4. Berger, B. W. 1989. Dermatologic manifestations of Lyme disease. Rev. Infect. Dis. 11:S1475-S1481.
5. Cauwels, A., E. Wan, M. Leismann, and E. Tuomanen. 1997. Coexistence of CD14-dependent and -independent pathways for stimulation of human monocytes by gram-positive bacteria. Infect. Immun. 65:3255-3260.
6. Coyle, P. K. 1993. Pathogenesis of Lyme disease, p. 179-183. In S. Manning (ed.). Lyme disease. Mosby Year Book, St. Louis., Mo.
7. Defosse, D. L., and R. C. Johnson. 1992. In vitro and in vivo induction of tumor necrosis factor alpha by Borrelia burgdorferi. Infect. Immun. 60:1109-1113.
8. DeWaal Malefyt, R., J. Haanen, H. Spits, M. G. Roncolo, A. TeVelde, C. Fidgor, K. Johnson, R. Kastelein, H. Yssel, and J. E. DeVries. 1991. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 174:915-924.
9. England, J. D., R. P. Bohm, Jr., E. D. Roberts, and M. T. Philipp. 1997. Mononeuropathy multiplex in rhesus monkeys with chronic Lyme disease. Ann. Neurol. 41:375-384.
10. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, J. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. C. Venter, et al. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
11. Giambartolomei, G. H., V. A. Dennis, and M. T. Philipp. 1998. Borrelia burgdorferi stimulates the production of interleukin-10 in peripheral blood mononuclear cells from uninfected humans and rhesus monkeys. Infect. Immun. 66:2691-2697.
12. Giambartolomei, G. H., V. A. Dennis, B. L. Lasater, and M. T. Philipp. Unpublished data.
13. Habicht, G. S., L. I. Katona, and J. L. Benach. 1991. Cytokines and the pathogenesis of neuroborreliosis: Borrelia burgdorfen induces glioma cells to secrete interleukin-6. J. Infect. Dis. 164:568-574.
14. Haupl, T., S. Landgraf, P. Netusil, N. Biller, C. Capiau, P. Desmons, P. Hauser, and G. R. Burmester. 1997. Activation of monocytes by three OspA vaccine candidates: lipoprotein OspA is a potent stimulator of monokines. FEMS Immunol. Med. Microbiol. 19:15-23.
15. Hauschildt, S., P. Hoffmann, H. U. Beuscher, G. Dufhues, P. Heinrich, K. H. Wiesmuller, G. Jung, and W. G. Bessler. 1990. Activation of bone marrow-derived mouse macrophages by bacterial lipopeptide: cytokine production, phagocytosis and Ia expression. Eur. J. Immunol. 20:63-68.
16. 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 analogues. Immunobiology 177:158-170.
17. Honarvar, N., U. E. Schaible, C. Galanos, R. Wallich, and M. M. Simon. 1994. A 14,000 MW lipoprotein and a glycolipid-like structure of Borrelia burgdorferi induce proliferation and immunoglohulin production in mouse B cells at high frequencies. Immunology 82:389-396.
18. Kenefick, K. B., L. C. L. Lim, J. D. Alder, J. L. Schmitz, C. J. Czuprynski, and R. F. Schell. 1993. Induction of interleukin-1 release by high- and low-passage isolates of Borrelia burgdorferi. J. Infect. Dis. 167:1086-1092.
19. 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. 270:9904-9910.
20. 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. 176:485-494.
21. Labels, M. O., R. Landmann, J. P. Obrecht, and R. Obrist, 1991. Human B cells express membrane-bound and soluble forms of the CD14 myeloid antigen. Mol. Immunol. 28:115-122.
22. Lahesmaa, R., M. C. Shanafelt, L. Steinman, and G. Peltz. 1994. Immunopathogenesis of human inflammatory arthritis: lessons from Lyme and reactive arthritis. J. Infect. Dis. 170:978-985.
23. Ma, Y., and J. J. Weis. 1993. Borrelia burgdorferi outer surface lipoproteins OspA and OspB possess B-cell mitogenic and cytokine-stimulatory properties. Infect. Immun. 61:3843-3853.
24. Ma, Y., K. P. Seiler, K. Tai, L. Yang, M. Woods, and J. J. Weis. 1994. Outer surface lipoproteins of Borrelia burgdorferi stimulate nitric oxide production by the cytokine-inducible pathway. Infect. Immun. 62:3663-3671.
25. 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. 158:4838-4845.
26. Norgard, M. V., L. L. Arndt, D. R. Akins, L. L. Curetty, D. A. Harrich, and J. D. Radolf. 1996. Activation of human monocytic cells by Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipoproteins proceeds via a pathway distinct from that of lipopolysaccharide but involves the transcriptional activator NK-κB. Infect. Immun. 64:3845-3852.
27. Philipp, M. T. 1998. Studies on OspA: a source of new paradigms in Lyme disease research. Trends Microbiol. 6:44-47.
28. Philipp, M. T., M. K. Aydintug, R. P. Bohm, Jr., F. B. Cogswell, V. A. Dennis, N. Lanners, R. C. Lowrie, Jr., E. D. Roberts, M. D. Conway, M. Karaçorlu, G. A. Peyman, D. J. Gubler, B. J. B. Johnson, J. Piesman, and Y. Gu. 1993. Early and early-disseminated phases of Lyme disease in the rhesus monkey: a model for infection in humans Infect. Immun. 61:3047-3059.
29. Philipp, M. T., and B. J. B. Johnson. 1994. Animal models of Lyme disease: pathogenesis and immunoprophylaxis. Trends Microbiol. 2:431-437.
30. Piesman, J., T. N., Mather, R. J. Sinsky, and A. Spielman. 1987. Duration of tick attachment and Borrelia burgdorferi transmission. Clin. Microbiol. 25: 557-558.
31. Pober, J. S., and R. S. Cotran. 1990. The role of endothelial cells in inflammation. Transplantation 50:537-544.
32. Pugin, J., C. C. Schurer-Maly, D. Leturcq, A. Moriarty, R. J. Ulevitch, and P. S. Tobias. 1993. Lipopolysaccharide activation of human endothelial and epithelial cells is mediated by lipopolysaccharide-binding protein and soluble CD14. Proc. Natl. Acad. Sci. USA 90:2744-2748.
33. 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 burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol. 154:2865-2877.
34. 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. 147:1968-1974.
35. Roberts, E. D., R. Bohm, Jr., F. B. Cogswell, H. N. Lanners, R. C. Lowrie, Jr., L. Povinelli, J. Piesman, and M. T. Philipp. 1995. Chronic Lyme disease in the rhesus monkey. Lab. Investig. 72:146-160.
36. Roberts, E. D., R. P. Bohm, Jr., R. C. Lowrie, Jr., G. Habicht, L. Katona, J. Piesman, and M. T. Philipp. 1998. Pathogenesis of Lyme neuroborreliosis in the rhesus monkey: the early disseminated and chronic phases of disease in the peripheral nervous system. J. Infect. Dis. 78:722-732.
37. Schaible, U. E., S. Gay, C. Museteanu, M. D. Kramer, G. Zimmer, K. Eichmann, U. Museteanu, and M. M. Simon. 1990. Lyme borreliosis in the severe combined immunodeficiency (scid) mouse manifests predominantly in the joints, heart, and liver. Am. J. Pathol. 137:811-820.
38. Sellati, T. J., D. A. Bouis, R. L. Kitchens, R. P. Darveau, J. Pugin, R. J. Ulevitch, S. C. Gangloff, S. M. Goyert, M. V. Norgard, and J. D. Radolf. 1998. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J. Immunol. 160:5455-5464.
39. Steere, A. C. 1995. Musculoskeletal manifestations of Lyme disease. Am. J. Med. 98:44S-48S.
40. Tai, K., Y. Ma, and J. J. Weis. 1994. Normal human B lymphocytes and mononuclear cells respond to the mitogenic and cytokine-stimulatory activities of Borrelia burgdorferi and its lipoprotein OspA. Infect. Immun. 62:520-528.
41. Takayama, K., R. J. Rothenberg, and A. G. Barbour. 1987. Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 55:2311-2313.
42. Tatro, J. B., L. I. Romero, D. Beasley, A. C. Steere, and S. Reichlin, 1994. Borrelia burgdorferi and Escherichia coli lipopolysaccharides induce nitric oxide and interleukin-6 production in cultured rat brain cells. J. Infect. Dis. 169:1014-1022.
43. Tobias, P. S., K. Soldau, L. Kline, J. D. Lee, K. Kato, T. P. Martin, and R. J. Ulevitch. 1993. Cross-linking of lipopolysaccharide (LPS) to CD14 on THP-1 cells mediated by LPS-binding protein. J. Immunol. 150:3011-3021.
44. Tobias, P. S., K. Soldau, and R. J. Ulevitch. 1989. Identification of a lipid A binding site in the acute phase reactant lipopolysaccharide binding protein. J. Biol. Chem. 264:10867-10871.
45. Todd, R. F., III, A. Van Agthoven, S. F. Schlossman, and C. Terhorst. 1982. Structural analysis of differentiation antigens Mo1 and Mo2 on human monocytes. Hybridoma 1:329-337.
46. Tsuchiya, S., M. Yamabe, Y. Yamaguchi, Y. Kobayashi, T. Konno, and K. Tada. 1980. Establishment and characterization of a human acute monocyte leukemia cell line (THP-1). Int. J. Cancer 26:171-176.
47. Ulevitch, R. J., and P. S. Tobias. 1995. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 13:437-457.
48. Walz, B., C. Stevens, B. Zanker, L. Melton, S. C. Clark, M. Suthanthiran, and T. B. Storm. 1991. The role of interleukin-6 in mitogenic T-cell activation: detection of interleukin-2 heteronuclear RNA by polymerase chain reaction Cell. Immunol. 134:511-519.
49. Wang, P., P. Wu, M. I. Siegel, R. W. Egan, and M. M. Billah. 1995. Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J. Biol. Chem. 270:9558-9563.
50. 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-kappa B and inflammatory activation in human endothelial cells. J. Immunol. 157:4584-4590.
51. Wooten, R. M., T. B. Morrison, J. H. Weis, S. D. Wright, R. Thieringer, and J. J. Weis. 1998. The role of CD14 in signaling mediated by outer membrane lipoproteins of Borrelia burgdorferi. J. Immunol. 160:5485-5492.
52. 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 249:1431-1433.
53. Yang, L., J. H. Weis, E. Eichwald, C. P. Kolbert, D. H. Persing, and J. J. Weis. 1994. Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues. Infect. Immun. 62:492-500.