Transcriptional response of human dendritic cells to Borrelia garinii - Defective CD38 and CCR7 expression detected

Journal of Leukocyte Biology

Volumn 82, Issue 1, 2007, Pages 33-43

  Hartiala, Pauliina ^a   Hytönen, Jukka ^a   Pelkonen, Jenni ^a   Kimppa, Katja ^b   West, Anne ^b   Penttinen, Markus A ^a   Suhonen, Juha ^a,c   Lahesmaa, Riitta ^b   Viljanen, Matti K ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Gene expression; Lyme borreliosis

Indexed keywords

CD38 ANTIGEN; CHEMOKINE RECEPTOR CCR7; COMPLEMENTARY DNA; LIPOPOLYSACCHARIDE;

ARTICLE; BORRELIA GARINII; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL STIMULATION; CHEMOTAXIS; CONTROLLED STUDY; DENDRITIC CELL; DNA MICROARRAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPH NODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANTIGENS, CD38; BORRELIA BURGDORFERI GROUP; CHEMOTAXIS; DENDRITIC CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; LIPOPOLYSACCHARIDES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, CHEMOKINE; TRANSCRIPTION, GENETIC;

BORRELIA GARINII;

EID: 34347389239     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1106709     Document Type: Article

References (54)

1. Steere, A. C. (1989) Lyme disease. N. Engl. J. Med. 321, 586-596.
2. Steere, A. C., Glickstein, L. (2004) Elucidation of Lyme arthritis. Nat. Rev. Immunol. 4, 143-152.
3. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B., Palucka, K. (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811.
4. Forster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Muller, I., Wolf, E., Lipp, M. (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99, 23-33.
5. Martin-Fontecha, A., Sebastiani, S., Hopken, U. E., Uguccioni, M., Lipp, M., Lanzavecchia, A., Sallusto, F. (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198, 615-621.
6. Randolph, G. J., Sanchez-Schmitz, G., Angeli, V. (2005) Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances. Springer Semin. Immunopathol. 26, 273-287.
7. Frasca, L., Fedele, G., Deaglio, S., Capuano, C., Palazzo, R., Vaisitti, T., Malavasi, F., Ausiello, C. M. (2006) CD38 orchestrates migration, survival, and Th1 immune response of human mature dendritic cells. Blood 107, 2392-2399.
8. Partida-Sanchez, S., Goodrich, S., Kusser, K., Oppenheimer, N., Randall, T. D., Lund, F. E. (2004) Regulation of dendritic cell trafficking by the ADP-ribosyl cyclase CD38: impact on the development of humoral immunity. Immunity 20, 279-291.
9. Mullegger, R. R., McHugh, G., Ruthazer, R., Binder, B., Kerl, H., Steere, A. C. (2000) Differential expression of cytokine mRNA in skin specimens from patients with erythema migrans or acrodermatitis chronica atrophicans. J. Invest. Dermatol. 115, 1115-1123.
10. Steere, A. C., Bartenhagen, N. H., Craft, J. E., Hutchinson, G. J., Newman, J. H., Rahn, D. W., Sigal, L. H., Spieler, P. N., Stenn, K. S., Malawista, S. E. (1983) The early clinical manifestations of Lyme disease. Ann. Intern. Med. 99, 76-82.
11. Salazar, J. C., Pope, C. D., Sellati, T. J., Feder Jr., H. M., Kiely, T. G., Dardick, K. R., Buckman, R. L., Moore, M. W., Caimano, M. J., Pope, J. G., Krause, P. J., Radolf, J. D., Lyme Disease Network (2003) Coevolution of markers of innate and adaptive immunity in skin and peripheral blood of patients with erythema migrans. J. Immunol. 171, 2660-2670.
12. Barthold, S. W., Bockenstedt, L. K. (1993) Passive immunizing activity of sera from mice infected with Borrelia burgdorferi. Infect. Immun. 61, 4696-4702.
13. Schaible, U. E., Kramer, M. D., Eichmann, K., Modolell, M., Museteanu, C., Simon, M. M. (1990) Monoclonal antibodies specific for the outer surface protein A (OspA) of Borrelia burgdorferi prevent Lyme borreliosis in severe combined immunodeficiency (scid) mice. Proc. Natl. Acad. Sci. USA 87, 3768-3772.
14. Craft, J. E., Fischer, D. K., Shimamoto, G. T., Steere, A. C. (1986) Antigens of Borrelia burgdorferi recognized during Lyme disease. Appearance of a new immunoglobulin M response and expansion of the immunoglobulin G response late in the illness. J. Clin. Invest. 78, 934-939.
15. Dattwyler, R. J., Volkman, D. J., Luft, B. J., Halperin, J. J., Thomas, J., Golightly, M. G. (1988) Seronegative Lyme disease. Dissociation of specific T- and B-lymphocyte responses to Borrelia burgdorferi. N. Engl. J. Med. 319, 1441-1446.
16. Wilske, B., Preac-Mursic, V., Schierz, G., Busch, K. V. (1986) Immunochemical and immunological analysis of European Borrelia burgdorferi strains. Zentralbl. Bakteriol. Mikrobiol. Hyg. [A] 263, 92-102.
17. Oksi, J., Savolainen, J., Pene, J., Bousquet, J., Laippala, P., Viljanen, M. K. (1996) Decreased interleukin-4 and increased γ interferon production by peripheral blood mononuclear cells of patients with Lyme borreliosis. Infect. Immun. 64, 3620-3623.
18. Filgueira, L., Nestle, F. O., Rittig, M., Joller, H. I., Groscurth, P. (1996) Human dendritic cells phagocytose and process Borrelia burgdorferi. J. Immunol. 157, 2998-3005.
19. Suhonen, J., Komi, J., Soukka, J., Lassila, O., Viljanen, M. K. (2003) Interaction between Borrelia burgdorferi and immature human dendritic cells. Scand. J. Immunol. 58, 67-75.
20. Hulinska, D., Bartak, P., Hercogova, J., Hancil, J., Basta, J., Schramlova, J. (1994) Electron microscopy of Langerhans cells and Borrelia burgdorferi in Lyme disease patients. Zentralbl. Bakteriol. 280, 348-359.
21. Silberer, M., Koszik, F., Stingl, G., Aberer, E. (2000) Downregulation of class II molecules on epidermal Langerhans cells in Lyme borreliosis. Br. J. Dermatol. 143, 786-794.
22. Chaussabel, D., Semnani, R. T., McDowell, M. A., Sacks, D., Sher, A., Nutman, T. B. (2003) Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102, 672-681.
23. Huang, Q., Liu, D., Majewski, P., Schulte, L. C., Korn, J. M., Young, R. A., Lander, E. S., Hacohen, N. (2001) The plasticity of dendritic cell responses to pathogens and their components. Science 294, 870-875.
24. Jenner, R. G., Young, R. A. (2005) Insights into host responses against pathogens from transcriptional profiling. Nat. Rev. Microbiol. 3, 281-294.
25. Granucci, F., Vizzardelli, C., Pavelka, N., Feau, S., Persico, M., Virzi, E., Rescigno, M., Moro, G., Ricciardi-Castagnoli, P. (2001) Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat. Immunol. 2, 882-888.
26. Takayama, K., Rothenberg, R. J., Barbour, A. G. (1987) Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 55, 2311-2313.
27. Benach, J. L., Coleman, J. L., Garcia-Monco, J. C., Deponte, P. C. (1988) Biological activity of Borrelia burgdorferi antigens. Ann. N. Y. Acad. Sci. 539, 115-125.
28. Hirschfeld, M., Kirschning, C. J., Schwandner, R., Wesche, H., Weis, J. H., Wooten, R. M., Weis, J. J. (1999) Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by Toll-like receptor 2. J. Immunol. 163, 2382-2386.
29. Junttila, J., Peltomaa, M., Soini, H., Marjamäki, M., Viljanen, M. K. (1999) Prevalence of Borrelia burgdorferi in Ixodes ricinus ticks in urban recreational areas of Helsinki. J. Clin. Microbiol. 37, 1361-1365.
30. Nikula, T., West, A., Katajamaa, M., Lonnberg, T., Sara, R., Aittokallio, T., Nevalainen, O. S., Lahesmaa, R. (2005) A human ImmunoChip cDNA microarray provides a comprehensive tool to study immune responses. J. Immunol. Methods 303, 122-134.
31. Feinberg, M. W., Cao, Z., Wara, A. K., Lebedeva, M. A., Senbanerjee, S., Jain, M. K. (2005) Kruppel-like factor 4 is a mediator of proinflammatory signaling in macrophages. J. Biol. Chem. 280, 38247-38258.
32. Lund, F. E., Cockayne, D. A., Randall, T. D., Solvason, N., Schuber, F., Howard, M. C. (1998) CD38: a new paradigm in lymphocyte activation and signal transduction. Immunol. Rev. 161, 79-93.
33. Lee, H. C. (2000) Enzymatic functions and structures of CD38 and homologs. Chem. Immunol. 75, 39-59.
34. Deaglio, S., Dianzani, U., Horenstein, A. L., Fernandez, J. E., van Kooten, C., Bragardo, M., Funaro, A., Garbarino, G., Di Virgilio, F., Banchereau, J., Malavasi, S. (1996) Human CD38 ligand. A 120-KDA protein predominantly expressed on endothelial cells. J. Immunol. 156, 727-734.
35. Fedele, G., Frasca, L., Palazzo, R., Ferrero, E., Malavasi, F., Ausiello, C. M. (2004) CD38 is expressed on human mature monocyte-derived dendritic cells and is functionally involved in CD83 expression and IL-12 induction. Eur. J. Immunol. 34, 1342-1350.
36. Partida-Sanchez, S., Cockayne, D. A., Monard, S., Jacobson, E. L., Oppenheimer, N., Garvy, B., Kusser, K., Goodrich, S., Howard, M., Harmsen, A., Randall, T. D., Lund, F. E. (2001) Cyclic ADP-ribose production by CD38 regulates intracellular calcium release, extracellular calcium influx and chemotaxis in neutrophils and is required for bacterial clearance in vivo. Nat. Med. 7, 1209-1216.
37. Ato, M., Stager, S., Engwerda, C. R., Kaye, P. M. (2002) Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nat. Immunol. 3, 1185-1191.
38. Velan, B., Bar-Haim, E., Zauberman, A., Mamroud, E., Shafferman, A., Cohen, S. (2006) Discordance in the effects of Yersinia pestis on the dendritic cell functions manifested by induction of maturation and paralysis of migration. Infect. Immun. 74, 6365-6376.
39. Hagnerud, S., Manna, P. P., Cella, M., Stenberg, A., Frazier, W. A., Colonna, M., Oldenborg, P. A. (2006) Deficit of CD47 results in a defect of marginal zone dendritic cells, blunted immune response to particulate antigen and impairment of skin dendritic cell migration. J. Immunol. 176, 5772-5778.
40. Iwasaki, A., Medzhitov, R. (2004) Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5, 987-995.
41. Alexopoulou, L., Thomas, V., Schnare, M., Lobet, Y., Anguita, J., Schoen, R. T., Medzhitov, R., Fikrig, E., Flavell, R. A. (2002) Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1- and TLR2-deficient mice. Nat. Med. 8, 878-884.
42. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
43. Behera, A. K., Hildebrand, E., Uematsu, S., Akira, S., Coburn, J., Hu, L. T. (2006) Identification of a TLR-independent pathway for Borrelia burgdorferi-induced expression of matrix metalloproteinases and inflammatory mediators through binding to integrin α3β1. J. Immunol. 177, 657-664.
44. O'Neill, L. A. (2006) How Toll-like receptors signal: what we know and what we don't know. Curr. Opin. Immunol. 18, 3-9.
45. Ichiyasu, H., McCormack, J. M., McCarthy, K. M., Dombkowski, D., Preffer, F. I., Schneeberger, E. E. (2004) Matrix metalloproteinase-9-deficient dendritic cells have impaired migration through tracheal epithelial tight junctions. Am. J. Respir. Cell Mol. Biol. 30, 761-770.
46. Osman, M., Tortorella, M., Londei, M., Quaratino, S. (2002) Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases define the migratory characteristics of human monocyte-derived dendritic cells. Immunology 105, 73-82.
47. Vizzardelli, C., Pavelka, N., Luchini, A., Zanoni, I., Bendickson, L., Pelizzola, M., Beretta, O., Foti, M., Granucci, F., Nilsen-Hamilton, M., Ricciardi-Castagnoli, P. (2006) Effects of dexamethazone on LPS-induced activation and migration of mouse dendritic cells revealed by a genome-wide transcriptional analysis. Eur. J. Immunol. 36, 1504-1515.
48. McQuibban, G. A., Gong, J. H., Wong, J. P., Wallace, J. L., Clark-Lewis, I., Overall, C. M. (2002) Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood 100, 1160-1167.
49. Overall, C. M., McQuibban, G. A., Clark-Lewis, I. (2002) Discovery of chemokine substrates for matrix metalloproteinases by exosite scanning: a new tool for degradomics. Biol. Chem. 383, 1059-1066.
50. Kouwenhoven, M., Ozenci, V., Tjernlund, A., Pashenkov, M., Homman, M., Press, R., Link, H. (2002) Monocyte-derived dendritic cells express and secrete matrix-degrading metalloproteinases and their inhibitors and are imbalanced in multiple sclerosis. J. Neuroimmunol. 126, 161-171.
51. Uchi, H., Imayama, S., Kobayashi, Y., Furue, M. (1998) Langerhans cells express matrix metalloproteinase-9 in the human epidermis. J. Invest. Dermatol. 111, 1232-1233.
52. Gebbia, J. A., Coleman, J. L., Benach, J. L. (2001) Borrelia spirochetes upregulate release and activation of matrix metalloproteinase gelatinase B (MMP-9) and collagenase 1 (MMP-1) in human cells. Infect. Immun. 69, 456-462.
53. Zhao, Z., Chang, H., Trevino, R. P., Whren, K., Bhawan, J., Klempner, M. S. (2003) Selective up-regulation of matrix metalloproteinase-9 expression in human erythema migrans skin lesions of acute lyme disease. J. Infect. Dis. 188, 1098-1104.
54. Asbrink, E., Hovmark, A. (1985) Successful cultivation of spirochetes from skin lesions of patients with erythema chronicum migrans Afzelius and acrodermatitis chronica atrophicans. Acta Pathol. Microbiol. Immunol. Scand. [B] 93, 161-163.