Digestive vacuoles of Plasmodium falciparum are selectively phagocytosed by and impair killing function of polymorphonuclear leukocytes

Blood

Volumn 118, Issue 18, 2011, Pages 4946-4956

  Dasari, Prasad ^a   Reiss, Karina ^b   Lingelbach, Klaus ^c   Baumeister, Stefan ^c   Lucius, Ralph ^b   Udomsangpetch, Rachanee ^d   Bhakdi, Sebastian Chakrit ^d   Bhakdi, Sucharit ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d Mahidol University ^*  (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL VIRULENCE; BLOODSTREAM INFECTION; CELL FUNCTION; CELL SELECTION; CELL VACUOLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; EXHAUSTION; HUMAN; HUMAN CELL; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SPECIES INVASION;

EID: 80855144793     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-05-353920     Document Type: Article

References (56)

1. Berendt AR, Tumer GD, Newbold CI. Cerebral malaria: the sequestration hypothesis. Parasitol Today. 1994;10(10):412-414. (Pubitemid 24306851)
2. MacPherson GG, Warrell MJ, White NJ, Looareesuwan S, Warrell DA. Human cerebral malaria. A quantitative ultrastructural analysis of parasitized erythrocyte sequestration. Am J Pathol. 1985; 119(3):385-401. (Pubitemid 15051887)
3. Bridges DJ, Bunn J, van Mourik JA, et al. Rapid activation of endothelial cells enables Plasmodium falciparum adhesion to platelet-decorated von Willebrand factor strings. Blood. 2010;115(7):1472-1474.
4. Srichaikul T, Puwasatien P, Karnjanajetanee J, Bokisch VA, Pawasatien P. Complement changes and disseminated intravascular coagulation in Plasmodium falciparum malaria. Lancet. 1975; 1(7910):770-772.
5. Neva FA, HowardWA, Glew RH, et al. Relationship of serum complement levels to events of the malarial paroxysm. J Clin Invest. 1974;54(2):451-460.
6. Helegbe GK, Goka BQ, Kurtzhals JA, et al. Complement activation in Ghanaian children with severe Plasmodium falciparum malaria. Malar J. 2007;6:165.
7. Moxon CA, Heyderman RS, Wassmer SC. Dysregulation of coagulation in cerebral malaria. Mol Biochem Parasitol. 2009;166(2):99-108.
8. Francischetti IM. Does activation of the blood coagulation cascade have a role in malaria pathogenesis? Trends Parasitol. 2008;24(6):258-263.
9. Ghosh K, Shetty S. Blood coagulation in falciparum malaria - a review. Parasitol Res. 2008; 102(4):571-576.
10. van der Heyde HC, Nolan J, Combes V, Gramaglia I, Grau GE. Aunified hypothesis for the genesis of cerebral malaria: sequestration, inflammation and hemostasis leading to microcirculatory dysfunction. Trends Parasitol. 2006;22(11):503-508. (Pubitemid 44479847)
11. Francischetti IM, Seydel KB, Monteiro RQ. Blood coagulation, inflammation, and malaria. Microcirculation. 2008;15(2):81-107. (Pubitemid 351228635)
12. Mabey DC, Brown A, Greenwood BM. Plasmodium falciparum malaria and Salmonella infections in Gambian children. J Infect Dis. 1987; 155(6):1319-1321. (Pubitemid 17080512)
13. Bronzan RN, Taylor TE, Mwenechanya J, et al. Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J Infect Dis. 2007;195(6):895-904. (Pubitemid 46363936)
14. Berkley J, Mwarumba S, Bramham K, Lowe B, Marsh K. Bacteraemia complicating severe malaria in children. Trans R Soc Trop Med Hyg. 1999;93(3):283-286. (Pubitemid 29348822)
15. Wykes MN, Good MF. What really happens to dendritic cells during malaria? Nat Rev Microbiol. 2008;6(11):864-870.
16. Bannister LH, Hopkins JM, Fowler RE, Krishna S, Mitchell GH. A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol Today. 2000;16(10):427- 433.
17. Pagola S, Stephens PW, Bohle DS, Kosar AD, Madsen SK. The structure of malaria pigment beta-haematin. Nature. 2000;404(6775):307-310.
18. Bohle DS, Kosar AD, Stephens PW. Phase homogeneity and crystal morphology of the malaria pigment beta-hematin. Acta Crystallogr D Biol Crystallogr. 2002;58(10 pt 1):1752-1756. (Pubitemid 35181084)
19. Pawluczkowycz AW, Lindorfer MA, Waitumbi JN, Taylor RP. Hematin promotes complement alternative pathway-mediated deposition of C3 activation fragments on human erythrocytes: potential implications for the pathogenesis of anemia in malaria. J Immunol. 2007;179(8):5543-5552.
20. Jaramillo M, Plante I, Ouellet N, Vandal K, Tessier PA, Olivier M. Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection. J Immunol. 2004;172(5):3101- 3110.
21. Pichyangkul S, Saengkrai P, Webster HK. Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factoralpha and interleukin-1 beta. Am J Trop Med Hyg. 1994;51(4):430-435. (Pubitemid 24324758)
22. Jaramillo M, Godbout M, Olivier M. Hemozoin induces macrophage chemokine expression through oxidative stress-dependent and -independent mechanisms. J Immunol. 2005;174(1): 475-484. (Pubitemid 40007437)
23. Parroche P, Lauw FN, Goutagny N, et al. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci U SA. 2007;104(6):1919-1924. (Pubitemid 46239879)
24. Griffith JW, Sun T, McIntosh MT, Bucala R. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J Immunol. 2009;183(8):5208-5220.
25. Carney CK, Schrimpe AC, Halfpenny K, et al. The basis of the immunomodulatory activity of malaria pigment (hemozoin). J Biol Inorg Chem. 2006; 11(7):917-929. (Pubitemid 44337592)
26. Nguyen PH, Day N, Pram TD, Ferguson DJ, White NJ. Intraleucocytic malaria pigment and prognosis in severe malaria. Trans R Soc Trop Med Hyg. 1995;89(2):200-204.
27. Lyke KE, Diallo DA, Dicko A, et al. Association of intraleukocytic Plasmodium falciparum malaria pigment with disease severity, clinical manifestations, and prognosis in severe malaria. Am J Trop Med Hyg. 2003;69(3):253-259.
28. Levesque MA, Sullivan AD, Meshnick SR. Splenic and hepatic hemozoin in mice after malaria parasite clearance. J Parasitol. 1999;85(3): 570-573. (Pubitemid 29279573)
29. Walev I, Tappe D, Gulbins E, Bhakdi S. Streptolysin O-permeabilized granulocytes shed L-selectin concomitantly with ceramide generation via neutral sphingomyelinase. J Leukoc Biol. 2000;68(6): 865-872.
30. Bhakdi S, Tranum-Jensen J. C5b-9 assembly: average binding of one C9 molecule to C5b-8 without poly-C9 formation generates a stable transmembrane pore. J Immunol. 1986;136(8): 2999-3005. (Pubitemid 16107209)
31. van der Heyde HC, Elloso MM, vande Waa J, Schell K, Weidanz WP. Use of hydroethidine and flow cytometry to assess the effects of leukocytes on the malarial parasite Plasmodium falciparum. Clin Diagn Lab Immunol. 1995;2(4):417-425.
32. Kumaratilake LM, Ferrante A, Rzepczyk CM. Tumor necrosis factor enhances neutrophil-mediated killing of Plasmodium falciparum. Infect Immun. 1990;58(3):788-793. (Pubitemid 20072646)
33. Martin E, Bhakdi S. Flow cytometric assay for quantifying opsonophagocytosis and killing of Staphylococcus aureus by peripheral blood leukocytes. J Clin Microbiol. 1992;30(9):2246-2255.
34. Goldberg DE, SlaterAF, Cerami A, Henderson GB. Hemoglobin degradation in the malaria parasite Plasmodium falciparum: an ordered process in a unique organelle. Proc Natl Acad Sci U S A. 1990;87(8):2931-2935.
35. Dluzewski AR, Ling IT, Hopkins JM, et al. Formation of the food vacuole in Plasmodium falciparum: a potential role for the 19 kDa fragment of merozoite surface protein 1 (MSP1(19)). PLoS One. 2008;3(8):e3085.
36. Celada A, Cruchaud A, Perrin LH. Phagocytosis of Plasmodium falciparum-parasitized erythrocytes by human polymorphonuclear leukocytes. J Parasitol. 1983;69(1):49-53. (Pubitemid 13164447)
37. Dockrell HM, Playfair JH. Killing of blood-stage murine malaria parasites by hydrogen peroxide. Infect Immun. 1983;39(1):456-459. (Pubitemid 13212552)
38. Jandl RC, Andre-Schwartz J, Borges-DuBois L, Kipnes RS, McMurrich BJ, Babior BM. Termination of the respiratory burst in human neutrophils. J Clin Invest. 1978;61(5):1176-1185. (Pubitemid 8324142)
39. Lee C, Miura K, Liu X, Zweier JL. Biphasic regulation of leukocyte superoxide generation by nitric oxide and peroxynitrite. J Biol Chem. 2000; 275(50):38965-38972. (Pubitemid 32058907)
40. Abkarian M, Massiera G, Berry L, Roques M, Braun-Breton C. A novel mechanism for egress of malarial parasites from red blood cells. Blood. 2011;117(15):4118-4124.
41. Elliott DA, McIntosh MT, Hosgood HD, 3rd, et al. Four distinct pathways of hemoglobin uptake in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A. 2008;105(7):2463- 2468.
42. Fidock DA, Nomura T, Talley AK, et al. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol Cell. 2000;6(4):861- 871.
43. Abu Bakar N, Klonis N, Hanssen E, Chan C, Tilley L. Digestive-vacuole genesis and endocytic processes in the early intraerythrocytic stages of Plasmodium falciparum. J Cell Sci. 2010;123(Pt 3):441-450.
44. 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. J Exp Med. 1992;176(4):1033-1041.
45. Skorokhod OA, Alessio M, Mordmuller B, Arese P, Schwarzer E. Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte- derived dendritic cells: a peroxisome proliferator- activated receptor-gamma-mediated effect. J Immunol. 2004;173(6):4066-4074. (Pubitemid 39280771)
46. Prato M, Giribaldi G, Polimeni M, Gallo V, Arese P. Phagocytosis of hemozoin enhances matrix metalloproteinase- 9 activity and TNF-alpha production in human monocytes: role of matrix metalloproteinases in the pathogenesis of falciparum malaria. J Immunol. 2005;175(10):6436-6442. (Pubitemid 41598884)
47. Giribaldi G, Prato M, Ulliers D, et al. Involvement of inflammatory chemokines in survival of human monocytes fed with malarial pigment. Infect Immun. 2010;78(11):4912-4921.
48. Prato M, Gallo V, Giribaldi G, Aldieri E, Arese P. Role of the NF-kappaB transcription pathway in the haemozoin- and 15-HETE-mediated activation of matrix metalloproteinase-9 in human adherent monocytes. Cell Microbiol. 2010;12(12): 1780-1791.
49. Wickramasinghe SN, Phillips RE, Looareesuwan S, Warrell DA, Hughes M. The bone marrow in human cerebral malaria: parasite sequestration within sinusoids. Br J Haematol. 1987;66(3):295- 306.
50. Glew RH, Atkinson JP, Frank MM, Collins WE, Neva FA. Serum complement and immunity in experimental simian malaria. I. Cyclical alterations in C4 related to schizont rupture. J Infect Dis. 1975;131(1):17-25.
51. Krettli AU, Nussenzweig V, Nussenzweig RS. Complement alterations in rodent malaria. Am J Trop Med Hyg. 1976;25(1):34-41.
52. Kumaratilake LM, Ferrante A. Opsonization and phagocytosis of Plasmodium falciparum merozoites measured by flow cytometry. Clin Diagn Lab Immunol. 2000;7(1):9-13. (Pubitemid 30051453)
53. Kumaratilake LM, Ferrante A, Jaeger T, Rzepczyk CM. Effects of cytokines, complement, and antibody on the neutrophil respiratory burst and phagocytic response to Plasmodium falciparum merozoites. Infect Immun. 1992;60(9): 3731-3738.
54. Lunel F, Druilhe P. Effector cells involved in nonspecific and antibody-dependent mechanisms directed against Plasmodium falciparum blood stages in vitro. Infect Immun. 1989;57(7):2043- 2049.
55. Bouharoun-Tayoun H, Attanath P, Sabchareon A, Chongsuphajaisiddhi T, Druilhe P. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J Exp Med. 1990;172(6): 1633-1641.
56. Joos C, Marrama L, Polson HE, et al. Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLoS One. 2010;5(3):e9871.