Divergent modulation of Chlamydia pneumoniae infection cycle in human monocytic and endothelial cells by iron, tryptophan availability and interferon gamma

Immunobiology

Volumn 215, Issue 9-10, 2010, Pages 842-848

  Bellmann Weiler, Rosa ^a   Martinz, Verena ^a   Kurz, Katharina ^a   Engl, Sabine ^a   Feistritzer, Clemens ^a   Fuchs, Dietmar ^b   Rupp, Jan ^c   Paldanius, Mika ^d   Weiss, Guenter ^a  

^a Department of Internal Medicine I   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY OF LÜBECK   (Germany)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

Chlamydia pneumoniae; Endothelial cells; Interferon; Iron; Kynurenine; Monocyte; Neopterin; Tryptophan

Indexed keywords

1 METHYLTRYPTOPHAN; GAMMA INTERFERON; IRON; N METHYLTRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; CELL COUNT; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL INCLUSION; CELL PROLIFERATION; CELL STRUCTURE; CHLAMYDIAL PNEUMONIA; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENRICHMENT CULTURE; ENZYME ACTIVITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; IRON METABOLISM; MONOCYTE; NONHUMAN; PRIORITY JOURNAL;

CELL GROWTH PROCESSES; CELL LINE; CHLAMYDOPHILA INFECTIONS; CHLAMYDOPHILA PNEUMONIAE; ENDOTHELIAL CELLS; ENZYME INHIBITORS; HUMANS; IMMUNOMODULATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; INTRANUCLEAR INCLUSION BODIES; IRON; MONOCYTES; TRYPTOPHAN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77955413703     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2010.05.021     Document Type: Article

References (62)

1. Abdelrahman Y.M., Belland R.J. The chlamydial developmental cycle. FEMS Microbiol. Rev. 2005, 29:949-959.
2. Andert S.E., Griesmacher A., Zuckermann A., Müller M.M. Neopterin release from human endothelial cells is triggered by interferon-gamma. Clin. Exp. Immunol. 1992, 88:555-558.
3. Al-Younes H.M., Rudel T., Brinkmann V., Szczepek A.J., Meyer T.F. Low iron availability modulates the course of Chlamydia pneumoniae infection. Cell Microbiol. 2001, 3:427-437.
4. Beatty W.L., Byrne G.I., Morrison R.P. Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc. Natl. Acad. Sci. USA 1993, 90:3998-4002.
5. Beatty W.L., Morrison R.P., Byrne G.I. Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 1994, 58:686-699.
6. Belland R.J., Nelson D.E., Virok D., Crane D.D., Hogan D., Sturdevant D., Beatty W.L., Caldwell H.D. Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc. Natl. Acad. Sci. USA 2003, 100:11596-15971.
7. Brandacher G., Margreiter R., Fuchs D. Clinical relevance of indoleamine 2,3-dioxygenase for alloimmunity and transplantation. Curr. Opin. Organ Transplant. 2008, 13:10-15.
8. Byrne G.I., Lehmann L.K., Landry G.J. Induction of tryptophan catabolism is the mechanism for gamma-interferon-mediated inhibition of intracellular Chlamydia psittaci replication in T24 cells. Infect. Immun. 1986, 53:347-351.
9. Campbell L.A., Kuo C.C. Cultivation and laboratory maintenance of Chlamydia pneumoniae. Curr. Protoc. Microbiol. 2009, Chapter 11: Unit 11B.1.
10. Caspar-Bauguil S., Puissant B., Nazzal D., Lefèvre J.C., Thomsen M., Salvayre R., Benoist H. Chlamydia pneumoniae induces interleukin-10 production that down-regulates major histocompatibility complex class I expression. J. Infect. Dis. 2000, 182:1394-1401.
11. Chatterjee S.S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T. Intracellular gene expression profile of Listeria monocytogenes. Infect. Immun. 2006, 74:1323-1338.
12. Cles L.D., Stamm W.E. Use of HL cells for improved isolation and passage of Chlamydia pneumoniae. J. Clin. Microbiol. 1990, 28:938-940.
13. Coles A.M., Reynolds D.J., Harper A., Devitt A., Pearce J.H. Low-nutrient induction of abnormal chlamydial development: a novel component of chlamydial pathogenesis?. FEMS Microbiol. Lett. 1993, 106:193-200.
14. Collins H.L. Withholding iron as a cellular defence mechanism-friend or foe?. Eur. J. Immunol. 2008, 38:1803-1806.
15. Freidank H.M., Billing H., Wiedmann-Al-Ahmad M. Influence of iron restriction on Chlamydia pneumoniae and C. trachomatis. J. Med. Microbiol. 2001, 50:223-227.
16. Gaenzer H., Marschang P., Sturm W., Neumayr G., Vogel W., Patsch J., Weiss G. Association between increased iron stores and impaired endothelial function in patients with hereditary hemochromatosis. J. Am. Coll. Cardiol. 2002, 40:2189-2194.
17. Griendling K.K., FitzGerald G.A. Oxidative stress and cardiovascular injury: Part I: basic mechanisms and in vivo monitoring of ROS. Circulation 2003, 108:1912-1916.
18. Griendling K.K., FitzGerald G.A. Oxidative stress and cardiovascular injury: Part II: animal and human studies. Circulation 2003, 108:2034-2040.
19. Heinemann M., Susa M., Simnacher U., Marre R., Essig A. Growth of Chlamydia pneumoniae induces cytokine production and expression of CD14 in a human monocytic cell line. Infect. Immun. 1996, 64:4872-4875.
20. Huber C., Batchelor J.R., Fuchs D., Hausen A., Lang A., Niederwieser D., Reibnegger G., Swetly P., Troppmair J., Wachter H. Immune response-associated production of neopterin. Release from macrophages primarily under control of interferon-gamma. J. Exp. Med. 1984, 160:310-316.
21. Jansen A., Yu J. Differential gene expression of pathogens inside infected hosts. Curr. Opin. Microbiol. 2006, 9:138-142.
22. Kalman S., Mitchell W., Marathe R., Lammel C., Fan J., Hyman R.W., Olinger L., Grimwood J., Davis R.W., Stephens R.S. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 1999, 21:385-389.
23. Kartikasari A.E., Georgiou N.A., de Geest M., van Kats-Renaud J.H., Bouwman J.J., van Asbeck B.S., Marx J.J., Visseren F.L. Iron enhances endothelial cell activation in response to Cytomegalovirus or Chlamydia pneumoniae infection. Eur. J. Clin. Invest. 2006, 36:743-752.
24. Kiechl S., Willeit J., Egger G., Poewe W., Oberhollenzer F. Body iron stores and the risk of carotid atherosclerosis: prospective results from the Bruneck study. Circulation 1997, 96:3300-3307.
25. Kiechl S., Egger G., Mayr M., Wiedermann C.J., Bonora E., Oberhollenzer F., Muggeo M., Xu Q., Wick G., Poewe W., Willeit J. Chronic infections and the risk of carotid atherosclerosis: prospective results from a large population study. Circulation 2001, 103:1064-1070.
26. Kuo C.C., Grayston J.T. A sensitive cell line, HL cells, for isolation and propagation of Chlamydia pneumoniae strain TWAR. J. Infect. Dis. 1990, 162:755-758.
27. Kuo C.C., Grayston J.T. Factors affecting viability and growth in HeLa 229 cells of Chlamydia sp. strain TWAR. J. Clin. Microbiol. 1988, 26:812-815.
28. Leinonen M., Saikku P. Evidence for infectious agents in cardiovascular disease and atherosclerosis. Lancet Infect. Dis. 2002, 2:11-17.
29. Ludwiczek S., Aigner E., Theurl I., Weiss G. Cytokine-mediated regulation of iron transport in human monocytic cells. Blood 2003, 101:4148-4154.
30. Maass M., Dalhoff K. Transport and storage conditions for cultural recovery of Chlamydia pneumoniae. J. Clin. Microbiol. 1995, 33:1793-1796.
31. Mellor A.L., Munn D.H. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 2004, 4:762-774.
32. Nairz M., Theurl I., Ludwiczek S., Theurl M., Mair S.M., Fritsche G., Weiss G. The co-ordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellular Salmonella typhimurium. Cell. Microbiol. 2007, 9:2126-2140.
33. Nairz M., Theurl I., Schroll A., Theurl M., Fritsche G., Lindner E., Seifert M., Crouch M.L., Hantke K., Akira S., Fang F.C., Weiss G. Absence of functional Hfe protects mice from invasive Salmonella enterica serovar Typhimurium infection via induction of lipocalin-2. Blood 2009, 114:3642-3651.
34. Nairz M., Fritsche G., Brunner P., Talasz H., Hantke K., Weiss G. Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur. J. Immunol. 2008, 38:1923-1936.
35. Ngeh J., Anand V., Gupta S. Chlamydia pneumoniae and atherosclerosis-what we know and what we don't. Clin. Microbiol. Infect. 2002, 8:2-13.
36. Njau F., Geffers R., Thalmann J., Haller H., Wagner A.D. Restriction of Chlamydia pneumoniae replication in human dendritic cell by activation of indoleamine 2,3-dioxygenase. Microbes Infect. 2009, 11:1002-1010.
37. Oexle H., Kaser A., Möst J., Bellmann-Weiler R., Werner E.R., Werner-Felmayer G., Weiss G. Pathways for the regulation of interferon-gamma-inducible genes by iron in human monocytic cells. J. Leukoc. Biol. 2003, 74:287-294.
38. Ouellette S.P., Hatch T.P., Abdelrahman Y.M., Rose L.A., Belland R.J., Byrne G.I. Global transcriptional upregulation in the absence of increased translation in Chlamydia during IFN gamma-mediated host cell tryptophan starvation. Mol. Microbiol. 2006, 62:1387-1401.
39. Paradkar P.N., De Domenico I., Durchfort N., Zohn I., Kaplan J., Ward D.M. Iron depletion limits intracellular bacterial growth in macrophages. Blood 2008, 112:866-874.
40. Raulston J.E. Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect. Immun. 1997, 65:4539-4547.
41. Recalcati S., Pometta R., Levi S., Conte D., Cairo G. Response of monocyte iron regulatory protein activity to inflammation: abnormal behavior in genetic hemochromatosis. Blood 1998, 91:2565-2572.
42. Rosen P. The synergism of gamma-interferon and tumor necrosis factor in whole body hyperthermia with vitamin C to control toxicity. Med. Hypotheses 1992, 38:257-258.
43. Rottenberg M.E., Gigliotti-Rothfuchs A., Wigzell H. The role of IFN-gamma in the outcome of chlamydial infection. Curr. Opin. Immunol. 2002, 14:444-451.
44. Schaible U.E., Kaufmann S.H. Iron and microbial infection. Nat. Rev. Microbiol. 2004, 2:946-953.
45. Schumacher A., Seljeflot I., Lerkerød A.B., Sommervoll L., Otterstad J.E., Arnesen H. Positive Chlamydia pneumoniae serology is associated with elevated levels of tumor necrosis factor alpha in patients with coronary heart disease. Atherosclerosis 2002, 164:153-160.
46. Sullivan J.L. Iron in arterial plaque: modifiable risk factor for atherosclerosis. Biochim. Biophys. Acta 2009, 1790:718-723.
47. Tatzber F., Rabl H., Koriska K., Erhart U., Puhl H., Waeg G., Krebs A., Esterbauer H. Elevated serum neopterin levels in atherosclerosis. Atherosclerosis 1991, 89:203-208.
48. Videm V., Wiseth R., Gunnes S., Madsen H.O., Garred P. Multiple inflammatory markers in patients with significant coronary artery disease. Int. J. Cardiol. 2007, 118:81-87.
49. Vink A., Poppen M., Schoneveld A.H., Roholl P.J., de Kleijn D.P., Borst C., Pasterkamp G. Distribution of Chlamydia pneumoniae in the human arterial system and its relation to the local amount of atherosclerosis within the individual. Circulation 2001, 103:1613-1617.
50. Visseren F.L., Verkerk M.S., van der Bruggen T., Marx J.J., van Asbeck B.S., Diepersloot R.J. Iron chelation and hydroxyl radical scavenging reduce the inflammatory response of endothelial cells after infection with Chlamydia pneumoniae or influenza A. Eur. J. Clin. Invest. 2002, 32(Suppl. 1):84-90.
51. Wang Y., Liu H., McKenzie G., Witting P.K., Stasch J.P., Hahn M., Changsirivathanathamrong D., Wu B.J., Ball H.J., Thomas S.R., Kapoor V., Celermajer D.S., Mellor A.L., Keaney J.F., Hunt N.H., Stocker R. Kynurenine is an endothelium-derived relaxing factor produced during inflammation. Nat. Med. 2010, 16(279-285).
52. Weinberg E.D. Iron depletion: a defense against intracellular infection and neoplasia. Life Sci. 1992, 50:1289-1297.
53. Weinberg E.D. Modulation of intramacrophage iron metabolism during microbial cell invasion. Microbes Infect. 2000, 2:85-89.
54. Weiss G., Fuchs D., Hausen A., Reibnegger G., Werner E.R., Werner-Felmayer G., Wachter H. Iron modulates interferon-gamma effects in the human myelomonocytic cell line THP-1. Exp. Hematol. 1992, 20:605-610.
55. Weiss G., Fuchs D., Hausen A., Reibnegger G., Werner E.R., Werner-Felmayer G., Semenitz E., Dierich M.P., Wachter H. Neopterin modulates toxicity mediated by reactive oxygen and chloride species. FEBS Lett. 1993, 321:89-92.
56. Weiss G., Willeit J., Kiechl S., Fuchs D., Jarosch E., Oberhollenzer F., Reibnegger G., Tilz G.P., Gerstenbrand F., Wachter H. Increased concentrations of neopterin in carotid atherosclerosis. Atherosclerosis 1994, 106:263-271.
57. Weiss G., Murr C., Zoller H., Haun M., Widner B., Ludescher C., Fuchs D. Modulation of neopterin formation and tryptophan degradation by Th1- and Th2-derived cytokines in human monocytic cells. Clin. Exp. Immunol. 1999, 116:435-440.
58. Weiss G., Diez-Ruiz A., Murr C., Theurl I., Fuchs D. Tryptophan metabolites as scavengers of reactive oxygen and chlorine species. Pteridines 2002, 13:140-144.
59. Weiss G. Iron and immunity: a double-edged sword. Eur. J. Clin. Invest. 2002, 32:70-78.
60. Weiss G. Modification of iron regulation by the inflammatory response. Best Pract. Res. Clin. Haematol. 2005, 18:183-201.
61. Widner B., Werner E.R., Schennach H., Wachter H., Fuchs D. Simultaneous measurement of serum tryptophan and kynurenine by HPLC. Clin. Chem. 1997, 43:2424-2426.
62. Yamaguchi H., Haranaga S., Widen R., Friedman H., Yamamoto Y. Chlamydia pneumoniae infection induces differentiation of monocytes into macrophages. Infect. Immun. 2002, 70:2392-2398.