Infection of human endothelial cells with spotted fever group rickettsiae stimulates cyclooxygenase 2 expression and release of vasoactive prostaglandins

Infection and Immunity

Volumn 74, Issue 9, 2006, Pages 5067-5074

  Rydkina, Elena ^a   Sahni, Abha ^a   Baggs, Raymond B ^a   Silverman, David J ^b   Sahni, Sanjeev K ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 6 OXOPROSTAGLANDIN F1 ALPHA; ANTIOXIDANT; CELL ADHESION MOLECULE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; CYTOKINE; HEME OXYGENASE; INDOMETACIN; ISOENZYME; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PROSTAGLANDIN; PROSTAGLANDIN E2; VASOACTIVE AGENT;

ARTICLE; BACTERIAL INFECTION; BLOOD VESSEL PERMEABILITY; BOUTONNEUSE FEVER; CELL CULTURE; CONTROLLED STUDY; DNA TRANSCRIPTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME REGULATION; EX VIVO STUDY; GENE EXPRESSION REGULATION; GENE INDUCTION; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; IN VITRO STUDY; INFECTION SENSITIVITY; INFLAMMATION; MICROANGIOPATHY; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROSTAGLANDIN SYNTHESIS; PROTEIN EXPRESSION; RICKETTSIA; RICKETTSIA CONORII; RICKETTSIA RICKETTSII; RICKETTSIOSIS; ROCKY MOUNTAIN SPOTTED FEVER; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TYPHUS; UMBILICAL CORD; VASCULAR ENDOTHELIUM; VASCULITIS;

6-KETOPROSTAGLANDIN F1 ALPHA; CELLS, CULTURED; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; DINOPROSTONE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEME OXYGENASE-1; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROSTAGLANDINS; RICKETTSIA RICKETTSII; RNA, MESSENGER; ROCKY MOUNTAIN SPOTTED FEVER; SIGNAL TRANSDUCTION;

EID: 33748075479     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00182-06     Document Type: Article

References (55)

1. Anguita, J., S. Samanta, S. K. Ananthanarayanan, B. Revilla, G. P. Geba, S. W. Barthold, and E. Fikrig. 2002. Cyclooxygenase 2 activity modulates the severity of murine Lyme arthritis. FEMS Immunol. Med. Microbiol. 34:187-191.
2. Appleby, S. B., A. Ristimaki, K. Neilson, K. Narko, and T. Hla. 1994. Structure of the human cyclo-oxygenase-2 gene. Biochem. J. 302:723-727.
3. Bach, F. H. 2005. Heme oxygenase-1: a therapeutic amplification funnel. FASEB J. 19:1216-1219.
4. 2. Proc. Natl. Acad. Sci. USA 95:7951-7956.
5. Barnett, J., J. Chow, D. Ives, M. Chiou, R. Mackenzie, E. Osen, B. Nguyen, S. Tsing, C. Bach, J. Freire, H. Chan, E. Sigal, and C. Ramesha. 1994. Purification, characterization and selective inhibition of human prostaglandin G/H synthase 1 and 2 expressed in the baculovirus system. Biochim. Biophys. Acta 1209:130-139.
6. Brueckmann, M., S. Horn, S. Lang, K. Fukudome, A. S. Nahrup, U. Hoffmann, J. J. Kaden, M. Borggrefe, K. K. Haase, and G. Huhle. 2005. Recombinant human activated protein C upregulates cyclooxygenase-2 expression in endothelial cells via binding to endothelial cell protein C receptor and activation of protease-activated receptor-1. Thromb. Haemost. 93:743-750.
7. Chan, F. K. 2003. COX-2 inhibition, Helicobacter pylori infection and the risk of gastrointestinal complications. Curr. Pharm. Des. 9:2213-2219.
8. Clifton, D. R., E. Rydkina, R. S. Freeman, and S. K. Sahni. 2005. NF-κB activation during Rickettsia rickettsii infection of endothelial cells involves the activation of catalytic IκB kinases IKKα and IKKβ and phosphorylation-proteolysis of the inhibitor protein IκBα. Infect. Immun. 73:155-165.
9. Clifton, D. R., E. Rydkina, H. Huyck, G. Pryhuber, R. S. Freeman, D. J. Silverman, and S. K. Sahni. 2005. Expression and secretion of chemotactic cytokines IL-8 and MCP-1 by human endothelial cells after Rickettsia rickettsii infection: regulation by nuclear transcription factor NF-κB. Int. J. Med. Microbiol. 295:267-278.
10. Courtney, M. A., P. J. Haidaris, V. J. Marder, and L. A. Sporn. 1996. Tissue factor mRNA expression in the endothelium of an intact umbilical vein. Blood 87:174-179.
11. Davidge, S. T. 2001. Prostaglandin H synthase and vascular function. Circ. Res. 89:650-660.
12. Demma, L. J., M. S. Traeger, W. L. Nicholson, C. D. Paddock, D. M. Blau, M. E. Eremeeva, G. A. Dasch, M. L. Levin, J. Singleton, Jr., S. R. Zaki, J. E. Cheek, D. L. Swerdlow, and J. H. McQuiston. 2005. Rocky Mountain spotted fever from an unexpected tick vector in Arizona. N. Engl. J. Med. 353:587-594.
13. Drancourt, M., M. C. Alessi, P. Y. Levy, I. Juhan-Vague, and D. Raoult. 1990. Secretion of tissue-type plasminogen activator and plasminogen activator inhibitor by Rickettsia conorii- and Rickettsia rickettsii-infected cultured endothelial cells. Infect. Immun. 58:2459-2463.
14. Dumler, J. S., and D. H. Walker. 2005. Rocky Mountain spotted fever-changing ecology and persisting virulence. N. Engl. J. Med. 353:551-553.
15. Eremeeva, M. E., G. A. Dasch, and D. J. Silverman. 2000. Interaction of rickettsiae with eukaryotic cells. Adhesion, entry, intracellular growth, and host cell responses. Subcell. Biochem. 33:479-516.
16. Eremeeva, M. E., G. A. Dasch, and D. J. Silverman. 2001. Quantitative analyses of variations in the injury of endothelial cells elicited by 11 isolates of Rickettsia rickettsii. Clin. Diagn. Lab. Immunol. 8:788-796.
17. Eremeeva, M. E., Z. Liang, C. Paddock, S. Zaki, J. G. Vandenbergh, G. A. Dasch, and D. J. Silverman. 2003. Rickettsia rickettsii infection in the pine vole, Microtus pinetorum: kinetics of infection and quantitation of antioxidant enzyme gene expression by RT-PCR. Ann. N. Y. Acad. Sci. 990:468-473.
18. Fukuda, E. Y., S. P. Lad, D. P. Mikolon, M. Iacobelli-Martinez, and E. Li. 2005. Activation of lipid metabolism contributes to interleukin-8 production during Chlamydia trachomatis infection of cervical epithelial cells. Infect. Immun. 73:4017-4024.
19. Ge, H., Y.-Y. E. Chuang, S. Zhao, M. Tong, M.-H. Tsai, J. J. Temenak, A. L. Richards, and W.-M. Ching. 2004. Comparative genomics of Rickettsia prowazekii Madrid E and Brein1 strains. J. Bacteriol. 186:556-565.
20. Ghannoum, M. A. 2000. Potential role of phospholipases in virulence and fungal pathogenesis. Clin. Microbiol. Rev. 13:122-143.
21. Haider, A., R. Olszanecki, R. Gryglewski, M. L. Schwartzman, E. Lianos, A. Kappas, A. Nasjletti, and N. G. Abraham. 2002. Regulation of cyclooxygenase by the heme-heme oxygenase system in microvessel endothelial cells. J. Pharmacol. Exp. Ther. 300:188-194.
22. Kaplanski, G., N. Teysseire, C. Farnarier, S. Kaplanski, J. C. Lissitzky, J. M. Durand, J. Soubeyrand, C. A. Dinarello, and P. Bongrand. 1995. IL-6 and IL-8 production from cultured human endothelial cells stimulated by infection with Rickettsia conorii via a cell-associated IL-1 alpha-dependent pathway. J. Clin. Investig. 96:2839-2844.
23. Kundu, N., Q. Yang, R. Dorsey, and A. M. Fulton. 2001. Increased cyclooxygenase-2 (cox-2) expression and activity in a murine model of metastatic breast cancer. Int. J. Cancer 93:681-686.
24. Kushida, T., G. Li Volti, S. Quan, A. Goodman, and N. G. Abraham. 2002. Role of human heme oxygenase-1 in attenuating TNF-α-mediated inflammation injury in endothelial cells. J. Cell. Biochem. 87:377-385.
25. Mark, K. S., W. J. Trickier, and D. W. Miller. 2001. Tumor necrosis factor-α induces cyclooxygenase-2 expression and prostaglandin release in brain microvessel endothelial cells. J. Pharmacol. Exp. Ther. 297:1051-1058.
26. Martinez, J. J., and P. Cossart. 2004. Early signaling events involved in the entry of Rickettsia conorii into mammalian cells. J. Cell Sci. 117:5097-5106.
27. Parola, P., C. D. Paddock, and D. Raoult. 2005. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin. Microbiol. Rev. 18:719-756.
28. Rasley, A., I. Marriott, C. R. Halberstadt, K. L. Bsot, and J. Anguita. 2004. Substance P augments Borrelia burgdorferi-induced prostaglandin E2 production by murine microglia. J. Immunol. 172:5707-5713.
29. Renesto, P., P. Dehoux, E. Gouin, L. Touqui, P. Cossart, and D. Raoult. 2003. Identification and characterization of a phospholipase D-superfamily gene in rickettsiae. J. Infect. Dis. 188:1276-1283.
30. Rydkina, E., A. Sahni, D. J. Silverman, and S. K. Sahni. 2002. Rickettsia rickettsii infection of cultured human endothelial cells induces heme oxygenase 1 expression. Infect. Immun. 70:4045-4052.
31. Rydkina, E., S. K. Sahni, L. A. Santucci, L. C. Turpin, R. B. Baggs, and D. J. Silverman. 2004. Selective modulation of antioxidant enzyme activities in host tissues during Rickettsia conorii infection. Microb. Pathog. 36:293-301.
32. Rydkina, E., D. J. Silverman, and S. K. Sahni. 2005. Activation of p38 stress-activated protein kinase during Rickettsia rickettsii infection of human endothelial cells: role in the induction of chemokine response. Cell. Microbiol. 7:1519-1530.
33. Sahni, S. K., D. J. Van Antwerp, M. E. Eremeeva, D. J. Silverman, V. J. Marder, and L. A. Sporn. 1998. Proteasome-independent activation of nuclear factor κB in cytoplasmic extracts from human endothelial cells by Rickettsia rickettsii. Infect. Immun. 66:1827-1833.
34. Sahni, S. K., L. C. Turpin, T. L. Brown, and L. A. Sporn. 1999. Involvement of protein kinase C in Rickettsia rickettsii-induced transcriptional activation of the host endothelial cell. Infect. Immun. 67:6418-6423.
35. Schmedtje, J. F., Jr., Y.-S. Ji, W.-L. Liu, R. N. DuBois, and M. S. Runge. 1997. Hypoxia induces cyclooxygenase-2 via the NF-κB p65 transcription factor in human vascular endothelial cells. J. Biol. Chem. 272:601-608.
36. Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659-667.
37. Shi, R. J., P. J. Simpson-Haidaris, N. B. Lerner, V. J. Marder, D. J. Silverman, and L. A. Sporn. 1998. Transcriptional regulation of endothelial cell tissue factor expression during Rickettsia rickettsii infection: involvement of the transcription factor NF-κB. Infect. Immun. 66:1070-1075.
38. Shi, R. J., P. J. Simpson-Haidaris, V. J. Marder, D. J. Silverman, and L. A. Sporn. 2000. Post-transcriptional regulation of endothelial cell plasminogen activator inhibitor-1 expression during Rickettsia rickettsii infection. Microb. Pathog. 28:127-133.
39. Silverman, D. J. 1984. Rickettsia rickettsii-induced cellular injury of human vascular endothelium in vitro. Infect. Immun. 44:545-553.
40. Sporn, L. A., R. J. Shi, S. O. Lawrence, D. J. Silverman, and V. J. Marder. 1991. Rickettsia rickettsii infection of cultured endothelial cells induces release of large von Willebrand factor multimers from Weibel-Palade bodies. Blood 78:2595-2602.
41. Sporn, L. A., S. K. Sahni, N. B. Lerner, V. J. Marder, D. J. Silverman, L. C. Turpin, and A. L. Schwab. 1997. Rickettsia rickettsii infection of cultured human endothelial cells induces NF-κB activation. Infect. Immun. 65:2786-2791.
42. Teysseire, N., D. Arnoux, F. George, J. Sampol, and D. Raoult. 1992. von Willebrand factor release and thrombomodulin and tissue factor expression in Rickettsia conorii-infected endothelial cells. Infect. Immun. 60:4388-4393.
43. Uchiya, K., and T. Nikai. 2004. Salmonella enterica serovar Typhimurium infection induces cyclooxygenase 2 expression in macrophages: involvement of Salmonella pathogenicity island 2. Infect. Immun. 72:6860-6869.
44. Valbuena, G., W. Bradford, and D. H. Walker. 2003. Expression analysis of the T-cell-targeting chemokines CXCL9 and CXCL10 in mice and humans with endothelial infections caused by rickettsiae of the spotted fever group. Am. J. Pathol. 163:1357-1369.
45. Valbuena, G., and D. H. Walker. 2004. Effect of blocking the CXCL9/10-CXCR3 chemokine system in the outcome of endothelial-target rickettsial infections. Am. J. Trop. Med. Hyg. 71:393-399.
46. Walker, D. H., G. A. Valbuena, and J. P. Olano. 2003. Pathogenic mechanisms of diseases caused by Rickettsia. Ann. N. Y. Acad. Sci. 990:1-11.
47. Walker, D. H. 2004. Ricketts creates rickettsiology, the study of vector-borne obligately intracellular bacteria. J. Infect. Dis. 189:938-955.
48. Walker, T. S., J. S. Brown, C. S. Hoover, and D. A. Morgan. 1990. Endothelial prostaglandin secretion: effects of typhus rickettsiae. J. Infect. Dis. 162:1136-1144.
49. Walker, T. S., M. W. Dersch, and W. E. White. 1991. Effects of typhus rickettsiae on peritoneal and alveolar macrophages: rickettsiae stimulate leukotriene and prostaglandin secretion. J. Infect. Dis. 163:568-573.
50. Walker, T. S., and G. E. Mellott. 1993. Rickettsial stimulation of endothelial platelet-activating factor synthesis. Infect. Immun. 61:2024-2029.
51. 2 in RNA replication. J. Virol. 79:9725-9734.
52. Whitworth, T., V. L. Popov, X. J. Yu, D. H. Walker, and D. H. Bouyer. 2005. Expression of the Rickettsia prowazekii pld or tlyC gene in Salmonella enterica serovar Typhimurium mediates phagosomal escape. Infect. Immun. 73:6668-6673.
53. Wu, C. Y., C. J. Wang, C. C. Tseng, H. P. Chen, M. S. Wu, J. T. Lin, H. Inoue, and G. H. Chen. 2005. Helicobacter pylori promote gastric cancer cells invasion through a NF-κB and COX-2-mediated pathway. World J. Gastroenterol. 11:3197-3203.
54. Wu, G., A. P. Mannam, J. Wu, S. Kirbis, J. L. Shie, C. Chen, R. J. Laham, F. W. Sellke, and J. Li. 2003. Hypoxia induces myocyte-dependent COX-2 regulation in endothelial cells: role of VEGF. Am. J. Physiol. Heart Circ. Physiol. 285:H2420-H2429.
55. 2 synthesis and attenuates chlamydial growth. J. Med. Microbiol. 52:409-415.