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PMID: 12819048 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Nitric oxide production and mononuclear cell nitric oxide synthase activity in malaria-tolerant Papuan adults.

Infection and immunity ·Vol. 71 ·No. 7 ·2003-07-00 ·Pages 3682-9

Boutlis CS, Tjitra E, Maniboey H, Misukonis MA, Saunders JR, Suprianto S, Weinberg JB, Anstey NM

Abstract

Individuals living in regions of intense malaria transmission exhibit natural immunity that allows them to be without fever and other symptoms for most of the time despite frequent parasitization. Although this tolerance of parasitemia appears to be more effective in children than in adults (as evidenced by lower parasitemia fever thresholds with age), adults do exhibit a degree of tolerance but the mechanism(s) underlying this are unclear. Asymptomatic malaria-exposed children have higher levels of nitric oxide (NO) than children with severe disease, and NO has been proposed as a mediator of malarial tolerance. However, the ability of highly malaria-exposed asymptomatic adults to generate high-level basal NO is unknown, as is the relationship between NO and malaria tolerance in adults. The relationship between NO and malaria parasitemia was therefore determined in asymptomatic adults from Papua, Indonesia. Adults with Plasmodium falciparum parasitemia had markedly increased basal systemic NO production relative to aparasitemic Papuan controls, who in turn produced more NO than healthy controls from a region without malaria. Immunoglobulin E levels were universally elevated in malaria-exposed Papuan subjects, suggesting that the prevalence of intestinal parasitosis may be high and that nonmalarial infection may also contribute to high basal NO production. Basal peripheral blood mononuclear cell (PBMC) NO synthase activity was elevated in Papuans but poorly correlated with systemic NO production, suggesting that NO production in this setting arises not only from PBMCs but also from other tissue and cellular sources. NO production was associated with and may contribute to malaria tolerance in Papuan adults.

MeSH Terms
Adolescent Adult Female Humans Immunity, Innate Immunoglobulin E/blood Leukocytes, Mononuclear/enzymology Malaria/immunology,metabolism Male Nitric Oxide/biosynthesis Nitric Oxide Synthase/blood,genetics Nitric Oxide Synthase Type II Parasitemia/immunology Promoter Regions, Genetic Tumor Necrosis Factor-alpha/biosynthesis
Chemicals
Tumor Necrosis Factor-alpha Nitric Oxide Immunoglobulin E NOS2 protein, human Nitric Oxide Synthase Nitric Oxide Synthase Type II
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Boutlis Craig S
International Health Program, Division of Infectious Diseases, Menzies School of Health Research, Northern Territory University, Casuarina, Australia.
Tjitra Emiliana
Maniboey Helena
Misukonis Mary A
Saunders Jocelyn R
Suprianto Sri
Weinberg J Brice
Anstey Nicholas M
References (73)
73 references, click to expand
  1. Blood mononuclear cell nitric oxide production and plasma cytokine levels in healthy gabonese children with prior mild or severe malaria.
    Infect Immun. 1999 Sep;67(9):4977-81 PMID: 10456963
  2. Effects of age and parasitemia on nitric oxide production/leukocyte nitric oxide synthase type 2 expression in asymptomatic, malaria-exposed children.
    Am J Trop Med Hyg. 1999 Aug;61(2):253-8 PMID: 10463676
  3. Lipid peroxides, nitric oxide and essential fatty acids in patients with Plasmodium falciparum malaria.
    Prostaglandins Leukot Essent Fatty Acids. 1999 Oct;61(4):255-8 PMID: 10574650
  4. Ascaris lumbricoides infection is associated with protection from cerebral malaria.
    Parasite Immunol. 2000 Mar;22(3):107-13 PMID: 10672191
  5. Plasmodium falciparum clinical malaria: lessons from longitudinal studies in Senegal.
    Parassitologia. 1999 Sep;41(1-3):255-9 PMID: 10697865
  6. Schistosoma mansoni infection cancels the susceptibility to Plasmodium chabaudi through induction of type 1 immune responses in A/J mice.
    Int Immunol. 2000 Aug;12(8):1117-25 PMID: 10917886
  7. What does a single determination of malaria parasite density mean? A longitudinal survey in Mali.
    Trop Med Int Health. 2000 Jun;5(6):404-12 PMID: 10929139
  8. Inducible nitric oxide synthase expression is increased in the brain in fatal cerebral malaria.
    Histopathology. 2000 Sep;37(3):269-77 PMID: 10971704
  9. Human infection with Ascaris lumbricoides is associated with a polarized cytokine response.
    J Infect Dis. 2000 Oct;182(4):1207-13 PMID: 10979919
  10. Age- and species-specific duration of infection in asymptomatic malaria infections in Papua New Guinea.
    Parasitology. 2000 Sep;121 ( Pt 3):247-56 PMID: 11085245
  11. Requirement of mitogen-activated protein kinases and I kappa B phosphorylation for induction of proinflammatory cytokines synthesis by macrophages indicates functional similarity of receptors triggered by glycosylphosphatidylinositol anchors from parasitic protozoa and bacterial lipopolysaccharide.
    J Immunol. 2001 Mar 1;166(5):3423-31 PMID: 11207300
  12. Induction of cross-tolerance by lipopolysaccharide and highly purified lipoteichoic acid via different Toll-like receptors independent of paracrine mediators.
    J Immunol. 2001 Apr 15;166(8):5161-7 PMID: 11290799
  13. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite.
    J Immunol. 2001 Jul 1;167(1):416-23 PMID: 11418678
  14. Concomitant infections, parasites and immune responses.
    Parasitology. 2001;122 Suppl:S23-38 PMID: 11442193
  15. Heterologous immunity revisited.
    Parasitology. 2001;122 Suppl:S51-9 PMID: 11442196
  16. Nitric oxide and reactive nitrogen intermediates during lethal and nonlethal strains of murine malaria.
    Parasite Immunol. 2001 Sep;23(9):491-501 PMID: 11589778
  17. Age- and infection intensity-dependent cytokine and antibody production in human trichuriasis: the importance of IgE.
    J Infect Dis. 2002 Mar 1;185(5):665-72 PMID: 11865424
  18. Endotoxin tolerance: A review.
    Crit Care Med. 2002 Jan;30(1 Supp):S64-S73 PMID: 11891406
  19. Inducible nitric oxide synthase: from cloning to therapeutic applications.
    World J Surg. 2002 Jul;26(7):772-8 PMID: 11960209
  20. Allergy, parasites, and the hygiene hypothesis.
    Science. 2002 Apr 19;296(5567):490-4 PMID: 11964470
  21. Migration inhibitory factor in the cerebral and systemic endothelium in sepsis and malaria.
    Crit Care Med. 2002 May;30(5 Suppl):S263-7 PMID: 12004246
  22. Inducible nitric oxide synthase (iNOS) in endotoxemia: chimeric mice reveal different cellular sources in various tissues.
    FASEB J. 2002 Jul;16(9):1141-3 PMID: 12039841
  23. Malaria therapy reinoculation data suggest individual variation of an innate immune response and independent acquisition of antiparasitic and antitoxic immunities.
    Trans R Soc Trop Med Hyg. 2002 Mar-Apr;96(2):205-9 PMID: 12055817
  24. Inducible nitric oxide synthase is not required in the development of endotoxin tolerance in mice.
    Shock. 2002 Jun;17(6):478-84 PMID: 12069184
  25. Toll receptors, CD14, and macrophage activation and deactivation by LPS.
    Microbes Infect. 2002 Jul;4(9):903-14 PMID: 12106783
  26. Macrophage signaling by glycosylphosphatidylinositol-anchored mucin-like glycoproteins derived from Trypanosoma cruzi trypomastigotes.
    Microbes Infect. 2002 Jul;4(9):1015-25 PMID: 12106796
  27. Systemic nitric oxide production in human malaria. I. Analysis of NO metabolites in biological fluids.
    Methods Mol Med. 2002;72:461-7 PMID: 12125142
  28. Systemic nitric oxide production in human malaria. II. Analysis of mononuclear cell nitric oxide synthase type 2 antigen expression.
    Methods Mol Med. 2002;72:469-74 PMID: 12125143
  29. Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand.
    Am J Trop Med Hyg. 2002 Mar;66(3):304-9 PMID: 12139225
  30. Worms and malaria: noisy nuisances and silent benefits.
    Parasite Immunol. 2002 Jul;24(7):391-3 PMID: 12164826
  31. Evaluation of the pyrogenic threshold for Plasmodium falciparum malaria in naive individuals.
    Am J Trop Med Hyg. 2002 May;66(5):467-73 PMID: 12201578
  32. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum.
    Lancet. 2002 Aug 24;360(9333):610-7 PMID: 12241933
  33. Lipopolysaccharide rapidly traffics to and from the Golgi apparatus with the toll-like receptor 4-MD-2-CD14 complex in a process that is distinct from the initiation of signal transduction.
    J Biol Chem. 2002 Dec 6;277(49):47834-43 PMID: 12324469
  34. A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children.
    Lancet. 2002 Nov 9;360(9344):1468-75 PMID: 12433515
  35. Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production.
    Lancet. 2003 Feb 22;361(9358):676-8 PMID: 12606182
  36. Observations on the natural history of malaria in the semi-resistant West African.
    Trans R Soc Trop Med Hyg. 1958 Mar;52(2):152-68 PMID: 13543904
  37. MALARIA INDUCED ENDOTOXIN TOLERANCE.
    Proc Soc Exp Biol Med. 1965 Jan;118:283-7 PMID: 14254570
  38. Enhanced production of reactive nitrogen intermediates in human and murine malaria.
    Parasitol Today. 1995 Nov;11(11):409-10 PMID: 15275387
  39. Clinical and parasitological studies on malaria in Liberian adults living under intense malaria transmission.
    Ann Trop Med Parasitol. 1991 Dec;85(6):577-84 PMID: 1811434
  40. Biomedical survey in Irian Jaya (West Irian), Indonesia.
    Southeast Asian J Trop Med Public Health. 1977 Dec;8(4):532-6 PMID: 208184
  41. Human cysticercosis and intestinal parasitism amongst the Ekari people of Irian Jaya.
    J Trop Med Hyg. 1987 Dec;90(6):291-6 PMID: 3430662
  42. Criteria for diagnosing clinical malaria among a semi-immune population exposed to intense and perennial transmission.
    Trans R Soc Trop Med Hyg. 1985;79(4):435-42 PMID: 3909550
  43. Nitric oxide produced during murine listeriosis is protective.
    Infect Immun. 1994 Mar;62(3):1089-100 PMID: 7509315
  44. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages.
    Blood. 1995 Aug 1;86(3):1184-95 PMID: 7542498
  45. Nitric oxide expression in the spleen, but not in the liver, correlates with resistance to blood-stage malaria in mice.
    J Immunol. 1995 Dec 1;155(11):5306-13 PMID: 7594544
  46. Endotoxin-induced desensitization of mouse macrophages is mediated in part by nitric oxide production.
    Infect Immun. 1995 May;63(5):1863-9 PMID: 7729896
  47. Increased nitric oxide synthesis during the development of endotoxin tolerance.
    Shock. 1995 Feb;3(2):102-8 PMID: 7749936
  48. Relationships between Plasmodium falciparum infection and morbidity in a highly endemic area.
    Parasitology. 1994 Dec;109 ( Pt 5):539-49 PMID: 7831089
  49. Dynamics of malaria parasitaemia associated with febrile illness in children from a rural area of Madang, Papua New Guinea.
    Trans R Soc Trop Med Hyg. 1994 Mar-Apr;88(2):191-7 PMID: 8036670
  50. IgE elevation and IgE anti-malarial antibodies in Plasmodium falciparum malaria: association of high IgE levels with cerebral malaria.
    Clin Exp Immunol. 1994 Aug;97(2):284-92 PMID: 8050178
  51. Patients with Plasmodium falciparum malaria and Plasmodium vivax malaria show increased nitrite and nitrate plasma levels.
    J Infect Dis. 1994 Jun;169(6):1418-9 PMID: 8195636
  52. Role of nitric oxide pathway in the protection against lethal endotoxemia afforded by low doses of lipopolysaccharide.
    Biochem Biophys Res Commun. 1993 Mar 15;191(2):441-6 PMID: 8461002
  53. Glycosylphosphatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by a protein tyrosine kinase-dependent and protein kinase C-dependent signaling pathway.
    J Immunol. 1996 Mar 1;156(5):1897-1907 PMID: 8596042
  54. Evidence for an age-dependent pyrogenic threshold of Plasmodium falciparum parasitemia in highly endemic populations.
    Am J Trop Med Hyg. 1996 Jun;54(6):613-9 PMID: 8686780
  55. Effects of Plasmodium vinckei hemozoin on the production of oxygen radicals and nitrogen oxides in murine macrophages.
    Am J Trop Med Hyg. 1996 Jun;54(6):620-4 PMID: 8686781
  56. Intestinal parasites of humans in a highland community of Irian Jaya, Indonesia.
    Ann Trop Med Parasitol. 1996 Feb;90(1):49-53 PMID: 8729627
  57. High plasma levels of nitrogen oxides are associated with severe disease and correlate with rapid parasitological and clinical cure in Plasmodium falciparum malaria.
    Trans R Soc Trop Med Hyg. 1996 Jan-Feb;90(1):44-7 PMID: 8730311
  58. Nitric oxide in Tanzanian children with malaria: inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression.
    J Exp Med. 1996 Aug 1;184(2):557-67 PMID: 8760809
  59. Role of CD23 in NO production by human monocytic cells.
    Res Immunol. 1995 Nov-Dec;146(9):684-9 PMID: 8852611
  60. Does malarial tolerance, through nitric oxide, explain the low incidence of autoimmune disease in tropical Africa?
    Lancet. 1996 Nov 30;348(9040):1492-4 PMID: 8942781
  61. Immunoglobulin E, a pathogenic factor in Plasmodium falciparum malaria.
    Infect Immun. 1997 Jan;65(1):116-21 PMID: 8975900
  62. Nitrate levels in malaria.
    Trans R Soc Trop Med Hyg. 1997 Mar-Apr;91(2):238-40 PMID: 9196781
  63. The tumor necrosis factor alpha-stimulating region of galactose-inhibitable lectin of Entamoeba histolytica activates gamma interferon-primed macrophages for amebicidal activity mediated by nitric oxide.
    Infect Immun. 1997 Jul;65(7):2522-7 PMID: 9199414
  64. Genetic analysis of host-parasite coevolution in human malaria.
    Philos Trans R Soc Lond B Biol Sci. 1997 Sep 29;352(1359):1317-25 PMID: 9355123
  65. Host-parasite interaction and morbidity in malaria endemic areas.
    Philos Trans R Soc Lond B Biol Sci. 1997 Sep 29;352(1359):1385-94 PMID: 9355131
  66. Polymorphism in promoter region of inducible nitric oxide synthase gene and protection against malaria.
    Lancet. 1998 Jan 24;351(9098):265-6 PMID: 9457101
  67. Intestinal parasite infections after extended use of chloroquine or primaquine for malaria prevention.
    J Parasitol. 1998 Jun;84(3):626-9 PMID: 9645872
  68. Nitric oxides in plasma, urine, and cerebrospinal fluid in patients with severe falciparum malaria.
    Am J Trop Med Hyg. 1998 Sep;59(3):497-502 PMID: 9749651
  69. Reactive nitrogen intermediates and outcome in severe adult malaria.
    Trans R Soc Trop Med Hyg. 1998 Mar-Apr;92(2):170-5 PMID: 9764323
  70. Inducible nitric oxide synthase polymorphism and fatal cerebral malaria.
    Lancet. 1998 Oct 10;352(9135):1193-4 PMID: 9777841
  71. Altered immune responses in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections.
    Infect Immun. 1998 Nov;66(11):5167-74 PMID: 9784518
  72. Levels of circulating nitrate/nitrite and gamma interferon not increased in uncomplicated malaria.
    Infection. 1998 Sep-Oct;26(5):301-3 PMID: 9795789
  73. The ratio of reactive nitrogen intermediates to tumour necrosis factor and clinical outcome of falciparum malaria disease.
    Trans R Soc Trop Med Hyg. 1998 Jul-Aug;92(4):417-20 PMID: 9850396
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2003-07-00
Pages
3682-9
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC161965
Subset
IM
Grants
NIAID NIH HHS · R01 AI041764 · United States
NIAID NIH HHS · R01 AI41764 · United States
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