Acquisition of hemozoin by monocytes down-regulates interleukin-12 p40 (IL-12p40) transcripts and circulating IL-12p70 through an IL-10-dependent mechanism: In vivo and in vitro findings in severe malarial anemia

Infection and Immunity

Volumn 74, Issue 9, 2006, Pages 5249-5260

  Keller, Christopher C ^a,b   Yamo, Ouma ^c,d   Ouma, Collins ^c   Ong'echa, John Michael ^c   Ounah, David ^c   Hittner, James B ^e   Vulule, John M ^c   Perkins, Douglas J ^a,c  

^a UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^b LAKE ERIE COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

^c KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^d KENYATTA UNIVERSITY   (Kenya)

^e School of Business   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; GAMMA INTERFERON; HEMOGLOBIN; HEMOZOIN; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 12P40; INTERLEUKIN 12P70; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; RECOMBINANT INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

ANEMIA; ARTICLE; CHILDHOOD MORTALITY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMATOCRIT; HUMAN; IMMUNOPATHOGENESIS; IN VITRO STUDY; IN VIVO STUDY; KENYA; MAJOR CLINICAL STUDY; MALARIA FALCIPARUM; MALE; MONOCYTE; PARASITEMIA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRESCHOOL CHILD; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICAL ANALYSIS; TRANSCRIPTION REGULATION;

ANEMIA; ANIMALS; ANTIBODIES; ANTIGENS, CD14; CELLS, CULTURED; CHILD, PRESCHOOL; DOWN-REGULATION; FEMALE; HEMEPROTEINS; HUMANS; INFANT; INFANT, NEWBORN; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-12 SUBUNIT P40; MALARIA, FALCIPARUM; MALE; MONOCYTES; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PROTEIN SUBUNITS; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33748032407     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00843-06     Document Type: Article

References (49)

1. Arese, P., and E. Schwarzer. 1997. Malarial pigment (haemozoin): a very active 'inert' substance. Ann. Trop. Med. Parasitol. 91:501-516.
2. Aste-Amezaga, M., X. Ma, A. Sartori, and G. Trinchieri. 1998. Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J. Immunol. 160:5936-5944.
3. Biswas, S., M. G. Karmarkar, and Y. D. Sharma. 2001. Antibodies detected against Plasmodium falciparum haemozoin with inhibitory properties to cytokine production. FEMS Microbiol. Lett. 194:175-179.
4. Bloland, P. B., T. K. Ruebush, J. B. McCormick, J. Ayisi, D. A. Boriga, A. J. Oloo, R. Beach, W. Hawley, A. Lal, B. Nahlen, V. Udhayakumar, and C. C. Campbell. 1999. Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission. I. Description of study site, general methodology, and study population. Am. J. Trop. Med. Hyg. 60:635-640.
5. Breman, J. G., M. S. Alilio, and A. Mills. 2004. Conquering the intolerable burden of malaria: what's new, what's needed: a summary. Am. J. Trop. Med. Hyg. 71:1-15.
6. Chaiyaroj, S. C., A. S. Rutta, K. Muenthaisong, P. Watkins, M. Na Ubol, and S. Looareesuwan. 2004. Reduced levels of transforming growth factor-beta1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria. Acta Trop. 89:319-327.
7. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
8. Coban, C., K. J. Ishii, D. J. Sullivan, and N. Kumar. 2002. Purified malaria pigment (hemozoin) enhances dendritic cell maturation and modulates the isotype of antibodies induced by a DNA vaccine. Infect. Immun. 70:3939-3943.
9. Crutcher, J. M., M. M. Stevenson, M. Sedegah, and S. L. Hoffman. 1995. Interleukin-12 and malaria. Res. Immunol. 146:552-559.
10. D'Andrea, A., M. Rengaraju, N. M. Valiante, J. Chehimi, M. Kubin, M. Aste, S. H. Chan, M. Kobayashi, D. Young, E. Nickbarg, et al. 1992. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176:1387-1398.
11. Deshpande, P., and P. Shastry. 2004. Modulation of cytokine profiles by malaria pigment-hemozoin: role of IL-10 in suppression of proliferative responses of mitogen stimulated human PBMC. Cytokine 28:205-213.
12. Dodoo, D., F. M. Omer, J. Todd, B. D. Akanmori, K. A. Koram, and E. M. Riley. 2002. Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J. Infect. Dis. 185:971-979.
13. Egan, T. J., W. W. Mavuso, and K. K. Ncokazi. 2001. The mechanism of beta-hematin formation in acetate solution. Parallels between hemozoin formation and biomineralization processes. Biochemistry 40:204-213.
14. Hoffman, S. L., J. M. Crutcher, S. K. Puri, A. A. Ansari, F. Villinger, E. D. Franke, P. P. Singh, F. Finkelman, M. K. Gately, G. P. Dutta, and M. Sedegah. 1997. Sterile protection of monkeys against malaria after adminis-tration of interleukin-12. Nat. Med. 3:80-83.
15. Keller, C. C., G. C. Davenport, K. R. Dickman, J. B. Hittner, S. S. Kaplan, J. B. Weinberg, P. G. Kremsner, and D. J. Perkins. 2005. Suppression of prostaglandin E2 by malaria parasite products and antipyretics promotes over-production of TNF-α: association with the pathogenesis of childhood malarial anemia. J. Infect. Dis. 193:1384-1393.
16. Keller, C. C., J. B. Hittner, B. K. Nti, J. B. Weinberg, P. G. Kremsner, and D. J. Perkins. 2004. Reduced peripheral PGE2 biosynthesis in Plasmodium falciparum malaria occurs through hemozoin-induced suppression of blood mononuclear cell cyclooxygenase-2 gene expression via an interleukin-10- independent mechanism. Mol. Med. 10:45-54.
17. Keller, C. C., P. G. Kremsner, J. B. Hittner, M. A. Misukonis, J. B. Weinberg, and D. J. Perkins. 2004. Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells. Infect. Immun. 72:4868-4873.
18. Kobayashi, M., L. Fitz, M. Ryan, R. M. Hewick, S. C. Clark, S. Chan, R. London, F. Sherman, B. Perussia, and G. Trinchieri. 1989. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 170:827-845.
19. Kurtzhals, J. A., V. Adabayeri, B. Q. Goka, B. D. Akanmori, J. O. Oliver-Commey, F. K. Nkrumah, C. Behr, and L. Hviid. 1998. Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet 351:1768-1772.
20. Luty, A. J., D. J. Perkins, B. Lell, R. Schmidt-Ott, L. G. Lehman, D. Luckner, B. Greve, P. Matousek, K. Herbich, D. Schmid, J. B. Weinberg, and P. G. Kremsner. 2000. Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infect. Immun. 68:3909-3915.
21. Lyke, K. E., D. A. Diallo, A. Dicko, A. Kone, D. Coulibaly, A. Guindo, Y. Cissoko, L. Sangare, S. Coulibaly, B. Dakouo, T. E. Taylor, O. K. Doumbo, and C. V. Plowe. 2003. Association of intraleukocytic Plasmodium falciparum malaria pigment with disease severity, clinical manifestations, and prognosis in severe malaria. Am. J. Trop. Med. Hyg. 69:253-259.
22. Ma, X., J. Sun, E. Papasavvas, H. Riemann, S. Robertson, J. Marshall, R. T. Bailer, A. Moore, R. P. Donnelly, G. Trinchieri, and L. J. Montaner. 2000. Inhibition of IL-12 production in human monocyte-derived macrophages by TNF. J. Immunol. 164:1722-1729.
23. Malaguarnera, L., R. M. Imbesi, S. Pignatelli, J. Simpore, M. Malaguarnera, and S. Musumeci. 2002. Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease. Parasite Immunol. 24:387-389.
24. Malaguarnera, L., S. Pignatelli, M. Musumeci, J. Simpore, and S. Musumeci. 2002. Plasma levels of interleukin-18 and interleukin-12 in Plasmodium falciparum malaria. Parasite Immunol. 24:489-492.
25. Mohan, K., and M. M. Stevenson. 1998. Interleukin-12 corrects severe anemia during blood-stage Plasmodium chabaudi AS in susceptible A/J mice. Exp. Hematol. 26:45-52.
26. Mordmuller, B., F. Turrini, H. Long, P. G. Kremsner, and P. Arese. 1998. Neutrophils and monocytes from subjects with the Mediterranean G6PD variant: effect of Plasmodium falciparum hemozoin on G6PD activity, oxidative burst and cytokine production. Eur. Cytokine Netw. 9:239-245.
27. Murphy, S. C., and J. G. Breman. 2001. Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am. J. Trop. Med. Hyg. 64:57-67.
28. Musumeci, M., L. Malaguarnera, J. Simpore, A. Messina, and S. Musumeci. 2003. Modulation of immune response in Plasmodium falciparum malaria: role of IL-12, IL-18 and TGF-beta. Cytokine 21:172-178.
29. Ong'echa, J. M., C. C. Keller, T. Were, C. Ouma, R. O. Otieno, Z. Landis-Lewis, D. Ochiel, J. L. Slingluff, S. Mogere, G. A. Ogonji, A. S. Orago, J. M. Vulule, S. S. Kaplan, R. D. Day, and D. J. Perkins. 2006. Parasitemia, anemia, and malarial anemia in infants and young children in a rural holoendemic Plasmodium falciparum transmission area. Am. J. Trop. Med. Hyg. 74:376-385.
30. Othoro, C, A. Lal, B. Nahlen, D. Koech, A. Orago, and V. Udhayakumar. 1999. A low interleukin-10 tumor necrosis factor-α ratio is associated with malaria anemia in children residing in a holoendemic region in western Kenya. J. Infect. Dis. 179:279-282.
31. Otieno, R. O., C. Ouma, J. M. Ong'echa, C. C. Keller, T. Were, E. N. Waindi, M. G. Michaels, R. D. Day, J. M. Vulule, and D. J. Perkins. 2006. Increased severe anemia in HIV-1-exposed and HIV-1-positive infants and children during acute malaria. AIDS 20:275-280.
32. Pagola, S., P. W. Stephens, D. S. Bohle, A. D. Kosar, and S. K. Madsen. 2000. The structure of malaria pigment beta-haematin. Nature 404:307-310.
33. Perkins, D. J., P. G. Kremsner, and J. B. Weinberg. 2001. Inverse relationship of plasma prostaglandin E2 and blood mononuclear cell cyclooxygenase-2 with disease severity in children with Plasmodium falciparum malaria. J. Infect. Dis. 183:113-118.
34. Perkins, D. J., J. B. Weinberg, and P. G. Kremsner. 2000. Reduced interleukin-12 and transforming growth factor-beta1 in severe childhood malaria: relationship of cytokine balance with disease severity. J. Infect. Dis. 182:988-992.
35. Pichyangkul, S., P. Saengkrai, and H. K. Webster. 1994. Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factor-alpha and interleukin-1 beta. Am. J. Trop. Med. Hyg. 51:430-435.
36. Sam, H., and M. M. Stevenson. 1999. In vivo IL-12 production and IL-12 receptors beta1 and beta2 mRNA expression in the spleen are differentially up-regulated in resistant B6 and susceptible A/J mice during early blood-stage Plasmodium chabaudi AS malaria. J. Immunol. 162:1582-1589.
37. Schwarzer, E., M. Alessio, D. Ulliers, and P. Arese. 1998. Phagocytosis of the malarial pigment, hemozoin, impairs expression of major histocompatibility complex class II antigen, CD54, and CD11c in human monocytes. Infect. Immun. 66:1601-1606.
38. Scragg, I. G., M. Hensmann, C. A. Bate, and D. Kwiatkowski. 1999. Early cytokine induction by Plasmodium falciparum is not a classical endotoxin-like process. Eur. J. Immunol. 29:2636-2644.
39. Sedegah, M., F. Finkelman, and S. L. Hoffman. 1994. Interleukin 12 induxtion of interferon gamma-dependent protection against malaria. Proc. Natl. Acad. Sci. USA 91:10700-10702.
40. Sherry, B. A., G. Alava, K. J. Tracey, J. Martiney, A. Cerami, and A. F. Slater. 1995. Malaria-specific metabolite hemozoin mediates the release of several potent endogenous pyrogens (TNF, MIP-1 alpha, and MIP-1 beta) in vitro, and altered thermoregulation in vivo. J. Infiamm. 45:85-96.
41. Slater, A. F. 1992. Malaria pigment. Exp. Parasitol. 74:362-365.
42. Slater, A. F., W. J. Swiggard, B. R. Orton, W. D. Flitter, D. E. Goldberg, A. Cerami, and G. B. Henderson. 1991. An iron-carboxylate bond links the heme units of malaria pigment. Proc. Natl. Acad. Sci. USA 88:325-329.
43. Stevenson, M. M., and E. M. Riley. 2004. Innate immunity to malaria. Nat. Rev. Immunol. 4:169-180.
44. Stevenson, M. M., M. F. Tam, S. F. Wolf, and A. Sher. 1995. IL-12-induced protection against blood-stage Plasmodium chabaudi AS requires IFN-gamma and TNF-alpha and occurs via a nitric oxide-dependent mechanism. J. Immunol. 155:2545-2556.
45. Su, Z., and M. M. Stevenson. 2002. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J. Immunol. 168:1348-1355.
46. Urban, B. C., T. Mwangi, A. Ross, S. Kinyanjui, M. Mosobo, O. Kai, B. Lowe, K. Marsh, and D. J. Roberts. 2001. Peripheral blood dendritic cells in children with acute Plasmodium falciparum malaria. Blood 98:2859-2861.
47. 2 is a potent inhibitor of human interleukin 12 production. J. Exp. Med. 181:775-779.
48. Weinberg, J. B., J. J. Muscato, and J. E. Niedel. 1981. Monocyte chemotactic peptide receptor. Functional characteristics and ligand-induced regulation. J. Clin. Investig. 68:621-630.
49. Xu, X., K. Sumita, C. Feng, X. Xiong, H. Shen, S. Maruyama, M. Kanoh, and Y. Asano. 2001. Down-regulation of IL-12 p40 gene in Plasmodium berghei-infected mice. J. Immunol. 167:235-241.