Candida albicans triggers activation of distinct signaling pathways to establish a proinflammatory gene expression program in primary human endothelial cells

Journal of Immunology

Volumn 179, Issue 12, 2007, Pages 8435-8445

  Müller, Verena ^a   Viemann, Dorothee ^b   Schmidt, Marc ^a   Endres, Nicole ^a   Ludwig, Stephan ^b   Leverkus, Martin ^c   Roth, Johannes ^b   Goebeler, Matthias ^a,d  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOID DIFFERENTIATION FACTOR 88; OLIGONUCLEOTIDE; PATTERN RECOGNITION RECEPTOR; SIGNAL PEPTIDE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TRANSCRIPTOME;

ARTICLE; CANDIDA ALBICANS; CELL CONTACT; CELL DEATH; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CHEMOTAXIS; DNA MICROARRAY; ENDOTHELIUM CELL; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOPRECIPITATION; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA INTERFERENCE; SEPSIS; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; IMMUNITY; IMMUNOLOGY; INFLAMMATION; METABOLISM; MICROBIOLOGY;

CANDIDA ALBICANS; CELL LINE; ENDOTHELIAL CELLS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY; INFLAMMATION; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 40049105940     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.12.8435     Document Type: Article

References (52)

1. Wisplinghoff, H., T. Bischoff, S. M. Tallent, H. Seifert, R. P. Wenzel, and M. B. Edmond. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39: 309-317.
2. Filler, S. G., A. S. Pfunder, B. J. Spellberg, J. P. Spellberg, and J. E. Edwards, Jr. 1996. Candida albicans stimulates cytokine production and leukocyte adhesion molecule expression by endothelial cells. Infect. Immun. 64: 2609-2617.
3. Orozco, A. S., X. Zhou, and S. G. Filler. 2000. Mechanisms of proinflammatory response of endothelial cells to Candida albicans infection. Infect. Immun. 68: 1134-1141.
4. Cannom, R. R. M., S. W. French, D. Johnston, J. E. Edwards, and S. G. Filler. 2002. Candida albicans stimulates local expression of leukocyte adhesion molecules and cytokines in vivo. J. Infect. Dis. 186: 389-396.
5. Filler, S. G., J. N. Swerdloff, C. Hobbs, and P. M. Luckett. 1995. Penetration and damage of endothelial cells by Candida albicans. Infect. Immun. 63: 976-983.
6. Filler, S. G., and D. C. Sheppard. 2006. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2: e129.
7. Dostert, C., and J. Tschopp. 2007. DEteCTINg fungal pathogens. Nat. Immunol. 8: 17-18.
8. Netea, M. G., N. A. Gow, C. A. Munro, S. Bates, C. Collins, G. Ferwerda, R. P. Hobson, G. Bertram, H. B. Hughes, T. Jansen, et al. 2006. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J. Clin. Invest. 116: 1642-1650.
9. Taylor, P. R., S. V. Tsoni, J. A. Willment, K. M. Dennehy, M. Rosas, H. Findon, K. Haynes, C. Steele, M. Botto, S. Gordon, and G. D. Brown. 2007. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat. Immunol. 8: 31-38.
10. Saijo, S., N. Fujikado, T. Furuta, S. H. Chung, H. Kotaki, K. Seki, K. Sudo, S. Akira, Y. Adachi, N. Ohno, et al. 2007. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat. Immunol. 8: 39-46.
11. Denk, A., M. Goebeler, S. Schmid, I. Berberich, O. Ritz, D. Lindemann, S. Ludwig, and T. Wirth. 2001. Activation of NF-κB via the IκB kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J. Biol. Chem. 276: 28451-28458.
12. Viemann, D., M. Goebeler, S. Schmid, K. Klimmek, C. Sorg, S. Ludwig, and J. Roth. 2004. Transcriptional profiling of IKK2/NF-κB- and p38 MAP kinase-dependent gene expression in TNF-α-stimulated primary human endothelial cells. Blood 103: 3365-3373.
13. Rajeevan, M. S., D. G. Ranamukhaarachchi, S. D. Vernon, and E. R. Unger. 2001. Use of real-time quantitative PCR to validate the results of cDNA array and differential display PCR technologies. Methods 25: 443-451.
14. Liu, W., and D. A. Saint. 2002. A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics. Anal. Biochem. 302: 52-59.
15. Goebeler, M., A. Trautmann, A. Voss, E. B. Bröcker, A. Toksoy, and R. Gillitzer. 2001. Differential and sequential expression of multiple chemokines during elicitation of allergic contact hypersensitivity. Am. J. Pathol. 158: 431-440.
16. Schmidt, M., M. Goebeler, G. Posern, S. M. Feller, C. S. Seitz, E. B. Bröcker, U. R. Rapp, and S. Ludwig. 2000. Ras-independent activation of the Raf/MEK/Erk pathway upon calcium-induced differentiation of keratinocytes. J. Biol. Chem. 275: 41011-41017.
17. Viemann, D., M. Schmidt, K. Tenbrock, S. Schmid, V. Müller, K. Klimmek, S. Ludwig, J. Roth, and M. Goebeler. 2007. The contact allergen nickel triggers a unique inflammatory and proangiogenic gene expression pattern via activation of NF-κB and hypoxia-inducible factor-1α. J. Immunol. 178: 3198-3207.
18. Goebeler, M., K. Kilian, R. Gillitzer, M. Kunz, T. Yoshimura, E. B. Bröcker, U. R. Rapp, and S. Ludwig. 1999. The MKK6/p38 stress kinase cascade is critical for tumor necrosis factor-a-induced expression of monocyte-chemoattractant protein-1 in endothelial cells. Blood 93: 857-865.
19. Karin, M., and M. Delhase. 2000. The IκB kinase (IKK) and NF-κB: key elements of proinflammatory signalling. Semin. Immunol. 12: 85-98.
20. Leverkus, M., M. R. Sprick, T. Wachter, A. Denk, E. B. Bröcker, H. Walszak, and M. Neumann. 2003. TRAIL-induced apoptosis and gene induction in HaCaT keratinocytes: differential contribution of TRAIL receptors 1 and 2. J. Invest. Dermatol. 121: 149-155.
21. Goebeler, M., R. Gillitzer, K. Kilian, K. Utzel, E. B. Bröcker, U. R. Rapp, and S. Ludwig. 2001. Multiple signaling pathways regulate NF-κB-dependent transcription of the monocyte chemoattractant protein-1 (MCP-1) gene in primary endothelial cells. Blood 97: 46-55.
22. Hoffmann, E., O. Dittrich-Breiholz, H. Holtmann, and M. Kracht. 2002. Multiple control of interleukin-8 gene expression. J. Leukocyte Biol. 72: 847-855.
23. Cao, Z., W. J. Henzel, and X. Gao. 1996. IRAK: a kinase associated with the interleukin-1 receptor. Science 271: 1128-1131.
24. Morris, G. E., L. C. Parker, J. R. Ward, E. C. Jones, M. K. Whyte, C. E. Brightling, P. Bradding, S. K. Dower, and I. Sabroe. 2006. Cooperative molecular and cellular networks regulate Toll-like receptor-dependent inflammatory responses. FASEB J. 20: 2153-2155.
25. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4: 499-511.
26. Berman, J., and P. E. Sudbery. 2002. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3: 918-930.
27. Roeder, A., C. J. Kirschning, R. A. Rupec, M. Schaller, and H. C. Korting. 2004. Toll-like receptors and innate antifungal responses. Trends Microbiol. 12: 44-49.
28. Urban, C. F., S. Lourido, and A. Zychlinsky. 2006. How do microbes evade neutrophil killing? Cell. Microbiol. 8: 1687-1696.
29. Yang, D., Q. Chen, D. M. Hoover, P. Staley, K. D. Tucker, J. Lubkowski, and J. J. Oppenheim. 2003. Many chemokines including CCL20/MIP-3α display antimicrobial activity. J. Leukocyte Biol. 74: 448-455.
30. Dieu-Nosjean, M. C., C. Massacrier, B. Homey, B. Vanbervliet, J. J. Pin, A. Vicari, S. Lebecque, C. Dezutter-Dambuyant, D. Schmitt, A. Zlotnik, and C. Caux. 2000. Macrophage inflammatory protein 3α is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 192: 705-718.
31. Bellocchio, S., C. Montagnoli, S. Bozza, R. Gaziano, G. Rossi, S. S. Mambula, A. Vecchi, A. Mantovani, S. M. Levitz, and L. Romani. 2004. The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol. 172: 3059-3069.
32. Aigner, S., Z. M. Sthoeger, M. Fogel, E. Weber, J. Zarn, M. Ruppert, Y. Zeller, D. Vestweber, R. Stahel, M. Sammar, and P. Altevogt. 1997. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 89: 3385-3395.
33. Starlets, D., Y. Gore, I. Binsky, M. Haran, N. Harpaz, L. Shvidel, S. Becker-Herman, A. Berrebi, and I. Shachar. 2006. Cell-surface CD74 initiates a signaling cascade leading to cell proliferation and survival. Blood 107: 4807-4816.
34. Carballo, E., W. S. Lai, and P. J. Blackshear. 1998. Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281: 1001-1005.
35. Karin, M., Y. Yamamoto, and Q. M. Wang. 2004. The IKK NF-κB system: a treasure trove for drug development. Nat. Rev. Drug Discov. 3: 17-26.
36. Johnson, D. R., I. Douglas, A. Jahnke, S. Ghosh, and J. S. Pober. 1996. A sustained reduction in IκB-β may contribute to persistent NF-κB activation in human endothelial cells. J. Biol. Chem. 271: 16317-16322.
37. Zen, K., A. Karsan, T. Eunson, E. Yee, and J. M. Harlan. 1998. Lipopolysaccharide-induced NF-κB activation in human endothelial cells involves degradation of IκBα but not IκBβ. Exp. Cell Res. 243: 425-433.
38. Ashwell, J. D. 2006. The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat. Rev. Immunol. 6: 532-540.
39. Hippenstiel, S., S. Soeth, B. Kellas, O. Fuhrman, J. Seybold, M. Krüll, C. Eichel Streiber, M. Goebeler, S. Ludwig, and N. Suttorp. 2000. Rho proteins and the p38-MAPK pathway are important mediators for LPS-induced interleukin-8 expression in human endothelial cells. Blood 95: 3044-3051.
40. Frevel, M. A. E., T. Bakheet, A. M. Silva, J. G. Hissong, K. S. A. Khabar, and B. R. G. Williams. 2003. p38 mitogen-activated protein kinase-dependent and -independent signaling of mRNA stability of AU-rich element-containing transcripts. Mol. Cell Biol. 23: 425-436.
41. Schmitz, M. L., S. Bacher, and M. Kracht. 2001. IκB-independent control of NF-κB activity by modulatory phosphorylations. Trends Biochem. Sci. 26: 186-190.
42. Vermeulen, L., G. De Wilde, P. van Damme, W. Vanden Berghe, and G. Haegeman. 2003. Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22: 1313-1324.
43. Deva, R., P. Shankaranarayanan, R. Ciccoli, and S. Nigam. 2003. Candida albicans induces selectively transcriptional activation of cyclooxygenase-2 in HeLa cells: pivotal roles of toll-like receptors, p38 mitogen-activated protein kinase, and NF-κB. J. Immunol. 171: 3047-3055.
44. Netea, M. G., G. Ferwerda, C. A. van der Graaf, J. W. Van der Meer, and B. J. Kullberg. 2006. Recognition of fungal pathogens by toll-like receptors. Curr. Pharm. Des. 12: 4195-4201.
45. Romani, L., F. Bistoni, and P. Puccetti. 2002. Fungi, dendritic cells and receptors: a host perspective of fungal virulence. Trends Microbiol. 10: 508-514.
46. Faure, E., O. Equils, P. A. Sieling, L. Thomas, F. X. Zhang, C. J. Kirschning, N. Polentarutti, M. Muzio, and M. Arditi. 2000. Bacterial lipopolysaccharide activates NF-κB through toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells: differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem. 275: 11058-11063.
47. Sobanov, Y., A. Bernreiter, S. Derdak, D. Mechtcheriakova, B. Schweighofer, M. Duchler, F. Kalthoff, and E. Hofer. 2001. A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur. J. Immunol. 31: 3493-3503.
48. Gröger, M., W. Holnthoner, D. Maurer, S. Lechleitner, K. Wolff, B. B. Mayr, W. Lubitz, and P. Petzelbauer. 2000. Dermal microvascular endothelial cells express the 180-kDa macrophage mannose receptor in situ and in vitro. J. Immunol. 165: 5428-5434.
49. Kariko, K., H. Ni, J. Capodici, M. Lamphier, and D. Weissman. 2004. mRNA is an endogenous ligand for Toll-like receptor 3. J. Biol. Chem. 279: 12542-12550.
50. Brentano, F., O. Schorr, R. E. Gay, S. Gay, and D. Kyburz. 2005. RNA released from necrotic synovial fluid cells activates rheumatoid arthritis synovial fibroblasts via Toll-like receptor 3. Arthritis Rheum. 52: 2656-2665.
51. Marshak-Rothstein, A. 2006. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6: 823-835.
52. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413: 732-738.