Plasmodium falciparum: Effect of antimalarial drugs, malaria pigment (β-haematin) and Plasmodium falciparum lysate on monocyte GTP-cyclohydrolase 1 gene expression

Experimental Parasitology

Volumn 129, Issue 3, 2011, Pages 312-317

  Cumming, Bridgette M ^a   Watson, Gregory M F ^a   Goldring, J P Dean ^a  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

Antimalarial drugs; GTP cyclohydrolase 1; Malaria; Neopterin; Plasmodium falciparum

Indexed keywords

AMODIAQUINE; ANTIMALARIAL AGENT; ARTEMISIN; BETA HEMATIN; CHLOROQUINE; DOXYCYCLINE; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; HEMATIN; PRIMAQUINE; PYRIMETHAMINE; QUININE; UNCLASSIFIED DRUG;

ARTICLE; CELL LYSATE; CELL STRAIN U937; CONTROLLED STUDY; DOWN REGULATION; ERYTHROCYTE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANTIMALARIALS; ERYTHROCYTES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GTP CYCLOHYDROLASE; HEMEPROTEINS; HUMANS; INTERFERON-GAMMA; MICROSPHERES; MONOCYTES; PLASMODIUM FALCIPARUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; U937 CELLS;

PLASMODIUM FALCIPARUM;

EID: 80054729987     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2011.08.001     Document Type: Article

References (63)

1. Ash C. Macrophages at the center of infection. Parasitology Today 1991, 7:2-3.
2. Awandare G.A., Goka B., Boeuf P., Tetteh J.K.A., Kurtzhals J.A.L., Behr C., Akanmori B.D. Increased levels of inflammatory mediators in children with severe Plasmodium falciparum malaria with respiratory distress. Journal of Infectious Diseases 2006, 194:1438-1446.
3. Biemba G., Gordeuk V.R., Thuma P.E., Mabeza G.F., Weiss G. Prolonged macrophage activation and persistent anaemia in children with complicated malaria. Tropical and Medical International Health 1998, 3:60-65.
4. Brown A.E., Webster H.K., Teja-Isavadharm P., Keeratithakul D. Macrophage activation in falciparum malaria as measured by neopterin and interferon-gamma. Clinical Experimental Immunology 1990, 82:97-101.
5. Cazalis J., Bodet C., Gagnon G., Grenier D. Doxycycline reduces lipopolysaccharide-induced inflammatory mediator secretion in macrophage and ex vivo human whole blood models. Journal of Periodontology 2008, 79:1762-1768.
6. Celada A., Cruchaud A., Perrin L.H. Assessment of immune phagocytosis of Plasmodium falciparum infected red blood cells by human monocytes and polymorphonuclear leukocytes. A method for visualizing infected red blood cells ingested by phagocytes. Journal of Immunological Methods 1983, 63:263-271.
7. Chen Z., Cheng Y.M., Xu Y.F., Liao J., Zhang X.N., Hu Y.W., Zhang Q., Wang J.F., Zhang Z.Q., Shen F., Yuan Z.H. Expression profiles and function of Toll-like receptors 2 and 4 in peripheral blood mononuclear cells of chronic hepatitis B patients. Clinical Immunology 2008, 128:400-408.
8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 1987, 162:156-159.
9. Coskun O., Oter S., Yaman H., Kilic S., Kurt I., Eyigun C.P. Evaluating the validity of serum neopterin and chitotriosidase levels in follow-up Brucellosis patients. Internal Medicine 2010, 49:1111-1118.
10. Desjardins R.E., Doberstyn E.B., Wernsdorfer W.H. The treatment and prophylaxis of malaria. Malaria: Principles and Practice of Malariology 1988, 827-864. Churchill Livingstone, Edinburgh. W.H. Wernsdorfer, I.S. McGregor (Eds.).
11. Dondorp A.M., Fanello C.I., Hendriksen I.C., Gomes E., Seni A., Chhaganlal K.D., Bojang K., Olaosebikan R., Anunobi N., Maitland K., Kivaya E., Agbenyega T., Nguah S.B., Evans J., Gesase S., Kahabuka C., Mtove G., Nadjm B., Deen J., Mwanga-Amumpaire J., Nansumba M., Karema C., Umulisa N., Uwimana A., Mokuolu O.A., Adedoyin O.T., Johnson W.B., Tshefu A.K., Onyamboko M.A., Sakulthaew T., Ngum W.P., Silamut K., Stepniewska K., Woodrow C.J., Bethell D., Wills B., Oneko M., Peto T.E., von Seidlein L., Day N.P., White N.J. Artesunate versus quinine in the treatment of severe falciparum malaria in African children (AQUAMAT): an open-label, randomised trial. Lancet 2010, 376:1647-1657.
12. Dostert C., Guarda G., Romero J.F., Menu P., Gross O., Tardivel A., Suva M.L., Stehle J.C., Kopf M., Stamenkovic I., Corradin G., Tschopp J. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS One 2009, 4:e6510.
13. Egan T.J. Recent advances in understanding the mechanism of hemozoin (malaria pigment) formation. Journal of Inorganic Biochemistry 2008, 102:1288-1299.
14. Egan T.J., Ross D.C., Adams P.A. Quinoline anti-malarial drugs inhibit spontaneous formation of beta-haematin (malaria pigment). FEBS letters 1994, 352:54-57.
15. Facer C.A. Malaria antigens stimulate neopterin secretion by PBMC and U937 cells. Microbiology and Immunology 1995, 39:207-211.
16. Fiori P.L., Rappelli P., Mirkarimi S.N., Ginsburg H., Cappuccinelli P., Turrini F. Reduced microbicidal and antitumor activities, of human monocytes after ingestion of Plasmodium-falciparum-infected red-blood-cells. Parasite Immunology 1993, 15:647-655.
17. Gieseg S.P., Amit Z., Yang Y.T., Shchepetkina A., Katouah H. Oxidant production, oxLDL uptake, and CD36 levels in human monocyte-derived macrophages are downregulated by the macrophage-generated antioxidant 7,8-dihydroneopterin. Antioxidants and Redox Signaling 2010, 13:1525-1534.
18. Goldie P., Roth E.F., Oppenheim J., Vanderberg J.P. Biochemical characterization of Plasmodium falciparum hemozoin. The American Journal of Tropical Medicine and Hygiene 1990, 43:584-596.
19. Goldring J.P., Nemaorani S. Antimalarial drugs modulate the expression of monocyte receptors. International Journal of Immunopharmacology 1999, 21:599-607.
20. Goldring J.P., Ramoshebi L.N. Glucocorticoids, antioxidants and staurosporine modulate the adherence between monocytes and malaria infected erythrocytes. Inflammation Research 1999, 48:657-661.
21. Goldring J.D., Molyneux M.E., Taylor T., Wirima J., Hommel M. Plasmodium falciparum: diversity of isolates from Malawi in their cytoadherence to melanoma cells and monocytes in vitro. British Journal of Haematology 1992, 81:413-418.
22. Hay, S.I., Okiro, E.A., Gething, P.W., Patil, A.P., Tatem, A.J., Guerra, C.A., Snow, R.W., 2010. Estimating the global clinical burden of Plasmodium falciparum malaria in 2007. Plos Medicine 7, -e1000290.
23. Heller R., Unbehaun A., Schellenberg B., Mayer B., Werner-Felmayer G., Werner E.R. L-Ascorbic acid potentiates endothelial nitric oxide synthesis via a chemical stabilization of tetrahydrobiopterin. Journal of Biological Chemistry 2001, 276:40-47.
24. Hoffmann G., Wirleitner B., Fuchs D. Potential role of immune system activation-associated production of neopterin derivatives in humans. Inflammation Research 2003, 52:313-321.
25. 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. Journal of Experimental Medicine 1984, 160:310-316.
26. Jaramillo M., Godbout M., Olivier M. Hemozoin induces macrophage chemokine expression through oxidative stress-dependent and -independent mechanisms. The Journal of Immunology 2005, 174:475-484.
27. Jaramillo M., Bellemare M.J., Martel C., Shio M.T., Contreras A.P., Godbout M., Roger M., Gaudreault E., Gosselin J., Bohle D.S., Olivier M. Synthetic Plasmodium-like hemozoin activates the immune response: a morphology - function study. PLoS One 2009, 4:e6957.
28. Katusic Z.S., Stelter A., Milstien S. Cytokines stimulate GTP cyclohydrolase I gene expression in cultured human umbilical vein endothelial cells. Arteriosclerosis Thrombosis and Vascular Biology 1998, 18:27-32.
29. Kern P., Hemmer C.J., Vandamme J., Gruss H.J., Dietrich M. Elevated tumor necrosis factor-alpha and interleukin-6 serum levels as markers for complicated Plasmodium-falciparum malaria. American Journal of Medicine 1989, 87:139-143.
30. Kremsner P.G., Feldmeier H., Zotter G.M., Jansen-Rosseck R., Graninger W., Rocha R.M., Bienzle U. Immunological alterations in uncomplicated Plasmodium falciparum malaria. Relationship between parasitaemia and indicators of macrophage activation. Acta Tropica 1989, 46:351-359.
31. Kremsner P.G., Neifer S., Rasenack T., Bienzle U. Interference by antimalarial-drugs with the invitro production of reactive nitrogen intermediates by murine macrophages. Journal of Antimicrobial Chemotherapy 1993, 31:385-392.
32. Kremsner P.G., Winkler S., Wildling E., Prada J., Bienzle U., Graninger W., Nussler A.K. High plasma levels of nitrogen oxides are associated with severe disease and correlate with rapid parasitological and clinical cure in Plasmodium falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygeine 1996, 90:44-47.
33. Kwiatkowski D., Bate C. Inhibition of tumour necrosis factor (TNF) production by antimalarial drugs used in cerebral malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 1995, 89:215-216.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
35. Miller L.H., Baruch D.I., Marsh K., Doumbo O.K. The pathogenic basis of malaria. Nature 2002, 415:673-679.
36. Murr C., Fuchs D., Gossler W., Hausen A., Reibnegger G., Werner E.R., Werner-Felmayer G., Esterbauer H., Wachter H. Enhancement of hydrogen peroxide-induced luminol-dependent chemiluminescence by neopterin depends on the presence of iron chelator complexes. FEBS Letters 1994, 338:223-226.
37. Oexle H., Kaser A., Most 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. Journal of Leukocyte Biology 2003, 74:287-294.
38. Osorio L.M., Fonte L., Finlay C.M. Inhibition of human monocyte function by prophylactic doses of chloroquine. The American Journal of Tropical Medicine and Hygiene 1992, 46:165-168.
39. Parroche P., Lauw F.N., Goutagny N., Latz E., Monks B.G., Visintin A., Halmen K.A., Lamphier M., Olivier M., Bartholomeu D.C., Gazzinelli R.T., Golenbock D.T. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:1919-1924.
40. Reibnegger G., Boonpucknavig V., Fuchs D., Hausen A., Schmutzhard E., Wachter H. Urinary neopterin is elevated in patients with malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 1984, 78:545-546.
41. Ringwald P., Peyron F., Vuillez J.P., Touze J.E., Le Bras J., Deloron P. Levels of cytokines in plasma during Plasmodium falciparum malaria attacks. Journal of Clinical Microbiology 1991, 29:2076-2078.
42. Romagnani S. Human TH1 and TH2 subsets: doubt no more. Immunology Today 1991, 12:256-257.
43. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods in Molecular Biology 2000, 132:365-386.
44. Schrimpe A.C., Wright D.W. Comparative analysis of gene expression changes mediated by individual constituents of hemozoin. Chemical Research in Toxicology 2009, 22:433-445.
45. Schwarzer E., Arese P. Phagocytosis of malarial pigment hemozoin inhibits NADPH-oxidase activity in human monocyte-derived macrophages. Biochimica et Biophysica Acta 1996, 1316:169-175.
46. Schwarzer E., Turrini F., Ulliers D., Giribaldi G., Ginsburg H., Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. The Journal of Experimental Medicine 1992, 176:1033-1041.
47. Schwarzer E., Alessio M., Ulliers D., Arese P. Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infection and Immunity 1998, 66:1601-1606.
48. Shalmiev G., Krugliak M., Turrini F., Ginsburg H. Antimalarial drugs inhibit the phagocytosis of erythrocytes infected with Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 1996, 90:558-562.
49. Skorokhod O., Schwarzer E., Grune T., Arese P. Role of 4-hydroxynonenal in the hemozoin-mediated inhibition of differentiation of human monocytes to dendritic cells induced by GM-CSF/IL-4. Biofactors 2005, 24:283-289.
50. Sundstrom C., Nilsson K. Establishment and characterization of a human histiocytic lymphoma cell line (U-937). International Journal of Cancer 1976, 17:565-577.
51. te Witt R., van Wolfswinkel M.E., Petit P.L., van Hellemond J.J., Koelewijn R., van Belkum A., van Genderen P.J. Neopterin and procalcitonin are suitable biomarkers for exclusion of severe Plasmodium falciparum disease at the initial clinical assessment of travellers with imported malaria. Malaria Journal 2010, 9:255.
52. Tiemi Shio M., Eisenbarth S.C., Savaria M., Vinet A.F., Bellemare M.J., Harder K.W., Sutterwala F.S., Bohle D.S., Descoteaux A., Flavell R.A., Olivier M. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathogens 2009, 5:e1000559.
53. Vadas P., Taylor T.E., Chimsuku L., Goldring D., Stefanski E., Pruzanski W., Molyneux M.E. Increased serum phospholipase a(2) activity in Malawian children with falciparum-malaria. American Journal of Tropical Medicine and Hygiene 1993, 49:455-459.
54. Voss T. Extraction and Purification of Plasmodium Total RNA. Malaria methods and protocols 2002, 151-157. Humana Press, Inc., Totowa. D.L. Doolan (Ed.).
55. Wachter H., Fuchs D., Hausen A., Reibnegger G., Werner E.R. Neopterin as marker for activation of cellular immunity: immunologic basis and clinical application. Advances in Clinical Chemistry 1989, 27:81-141.
56. Wenisch C., Parschalk B., Zedwitz-Liebenstein K., Wernsdorfer W., Graninger W. The effect of artemisinin on granulocyte function assessed by flow cytometry. Journal of Antimicrobial Chemotherapy 1997, 39:99-101.
57. Werner E.R., Werner-Felmayer G., Fuchs D., Hausen A., Reibnegger G., Yim J.J., Pfleiderer W., Wachter H. Tetrahydrobiopterin biosynthetic activities in human macrophages, fibroblasts, THP-1, and T 24 cells. GTP-cyclohydrolase I is stimulated by interferon-gamma, and 6-pyruvoyl tetrahydropterin synthase and sepiapterin reductase are constitutively present. Journal of Biological Chemistry 1990, 265:3189-3192.
58. Wernsdorfer W.H. Antimalarial Drugs. Handbook of Malaria Infection in the Tropics. Associazione Italiana " Amici di R. Follereau" (AIFO) 1997, 151-198. Organizzazione per la Cooperazione Sanitaria Internazionale, Bologna. G. Carosi, F. Castelli (Eds.).
59. HO W. World Malaria Report 2008 2008, World Health Organisation, Geneva.
60. Widner B., Mayr C., Wirleitner B., Fuchs D. Oxidation of 7,8-dihydroneopterin by hypochlorous acid yields neopterin. Biochemistry and Biophysics Research Communications 2000, 275:307-311.
61. Winkler C., Frick B., Schroecksnadel K., Schennach H., Fuchs D. Food preservatives sodium sulfite and sorbic acid suppress mitogen-stimulated peripheral blood mononuclear cells. Food and Chemical Toxicology 2006, 44:2003-2007.
62. Winstanley P.A., Simooya O., Kofi-Ekue J.M., Walker O., Salako L.A., Edwards G., Orme M.L., Breckenridge A.M. The disposition of amodiaquine in Zambians and Nigerians with malaria. British Journal of Clinical Pharmacology 1990, 29:695-701.
63. Wirleitner B., Reider D., Ebner S., Bock G., Widner B., Jaeger M., Schennach H., Romani N., Fuchs D. Monocyte-derived dendritic cells release neopterin. Journal of Leukocyte Biology 2002, 72:1148-1153.