Low levels of mammalian TGF-β1 are protective against malaria parasite infection, a paradox clarified in the mosquito host

Experimental Parasitology

Volumn 118, Issue 2, 2008, Pages 290-296

  Luckhart, Shirley ^a   Lieber, Matthew J ^a   Singh, Naresh ^a   Zamora, Ruben ^b   Vodovotz, Yoram ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Anopheles stephensi; Anopheles stephensi nitric oxide synthase; AsNOS; d NAME; l NAME; Malaria; Mosquito; N nitro d arginine methyl ester; N nitro l arginine methyl ester; nitric oxide; Nitric oxide synthase; NO; Plasmodium falciparum; Protozoan; TGF 1; Transforming growth factor 1

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; TRANSFORMING GROWTH FACTOR BETA1;

ANOPHELES STEPHENSI; ARTICLE; BLOOD LEVEL; CATALYSIS; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; MALARIA; MAMMAL; MOSQUITO; NONHUMAN; PARASITE CONTROL; PARASITE DEVELOPMENT; PARASITOSIS; PLASMODIUM; PRIORITY JOURNAL;

ANIMALS; ANOPHELES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INSECT VECTORS; MALARIA; MICE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PLASMODIUM; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

ANOPHELES STEPHENSI; INVERTEBRATA; MAMMALIA; MUS; PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 37449010330     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2007.08.013     Document Type: Article

References (32)

1. Akman-Anderson L., Vodovotz Y., Zamora R., and Luckhart S. Bloodfeeding as an interface of mammalian and arthropod immunity. In: Beckage N. (Ed). Insect Immunology (2007), Elsevier, San Diego
2. Anstey N.M., Weinberg J.B., Hassanali M.Y., Mwaikambo E.D., Manyenga D., Misukonis M.A., Arnelle D.R., Hollis D., McDonald M.I., and Granger D.L. Nitric oxide in Tanzanian children with malaria: inverse relationship between malaria severity and nitric oxide production/nitric oxide synthase type 2 expression. Journal of Experimental Medicine 184 (1996) 557-567
3. Clark I.A., and Cowden W.B. The pathophysiology of falciparum malaria. Pharmacology and Therapeutics 99 (2003) 221-260
4. Crampton A., and Luckhart S. The role of As60A, a TGF-beta homolog, in Anopheles stephensi innate immunity and defense against Plasmodium infection. Infection, Genetics and Evolution 1 (2001) 131-141
5. Gramaglia I., Sobolewski P., Meays D., Contreras R., Nolan J.P., Frangos J.A., Intaglietta M., and van der Heyde H.C. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nature Medicine 12 (2006) 1417-1422
6. Griscavage J.M., Wilk S., and Ignarro L.J. Serine and cysteine proteinase inhibitors prevent nitric oxide production by activated macrophages by interfering with transcription of the inducible NO synthase gene. Biochemical and Biophysical Research Communications 215 (1995) 721-729
7. Grumbach I.M., Chen W., Mertens S.A., and Harrison D.G. A negative feedback mechanism involving nitric oxide and nuclear factor kappa-B modulates endothelial nitric oxide synthase transcription. Journal of Molecular and Cellular Cardiology 39 (2005) 595-603
8. Han Y.S., Thompson J., Kafatos F.C., and Barillas-Mury C. Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. The EMBO Journal 19 (2000) 6030-6040
9. Hobbs M.R., Udhayakumar V., Levesque M.C., Booth J., Roberts J.M., Tkachuk A.N., Pole A., Coon H., Kariuki S., Nahlen B.L., Mwaikambo E.D., Lal A.L., Granger D.L., Anstey N.M., and Weinberg J.B. A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children. Lancet 360 (2002) 1468-1475
10. Lim J., Gowda D.C., Krishnegowda G., and Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infection and Immunology 73 (2005) 2778-2789
11. Luckhart S., Crampton A.L., Zamora R., Lieber M.J., Dos Santos P.C., Peterson T.M., Emmith N., Lim J., Wink D.A., and Vodovotz Y. Mammalian transforming growth factor beta1 activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infection and Immunity 71 (2003) 3000-3009
12. Luckhart S., and Li K. Transcriptional complexity of the Anopheles stephensi nitric oxide synthase gene. Insect Biochemistry and Molecular Biology 31 (2001) 249-256
13. Luckhart S., and Rosenberg R. Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene 232 (1999) 25-34
14. Luckhart S., Vodovotz Y., Cui L., and Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Sciences of the United State of America 95 (1998) 5700-5705
15. Mellouk S., Hoffman S.L., Liu Z.Z., de la Vega P., Billiar T.R., and Nussler A.K. Nitric oxide-mediated antiplasmodial activity in human and murine hepatocytes induced by gamma interferon and the parasite itself: enhancement by exogenous tetrahydrobiopterin. Infection and Immunity 62 (1994) 4043-4046
16. Naotunne T.S., Karunaweera N.D., Mendis K.N., and Carter R. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78 (1993) 555-562
17. Omer F.M., Kurtzhals J.A., and Riley E.M. Maintaining the immunological balance in parasitic infections: a role for TGF-beta?. Parasitology Today 16 (2000) 18-23
18. Omer F.M., and Riley E.M. Transforming growth factor beta production is inversely correlated with severity of murine malaria infection. Journal of Experimental Medicine 188 (1998) 39-48
19. Perkins D.J., Weinberg J.B., and Kremsner P.G. Reduced interleukin-12 and transforming growth factor-beta1 in severe childhood malaria: relationship of cytokine balance with disease severity. Journal of Infectious Diseases 182 (2000) 988-992
20. Peterson T.M., Gow A.J., and Luckhart S. Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Radical Biology and Medicine 42 (2007) 132-142
21. Pino P., Vouldoukis I., Dugas N., Conti M., Nitcheu J., Traore B., Danis M., Dugas B., and Mazier D. Induction of the CD23/nitric oxide pathway in endothelial cells downregulates ICAM-1 expression and decreases cytoadherence of Plasmodium falciparum-infected erythrocytes. Cellular Microbiology 6 (2004) 839-848
22. Riley E.M., Wahl S., Perkins D.J., and Schofield L. Regulating immunity to malaria. Parasite Immunology 28 (2006) 35-49
23. Rockett K.A., Awburn M.M., Cowden W.B., and Clark I.A. Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infection and Immunity 59 (1991) 3280-3283
24. Sharma A., Eapen A., and Subbarao S.K. Parasite killing in Plasmodium vivax malaria by nitric oxide: implication of aspartic protease inhibition. The Journal of Biochemistry (Tokyo) 136 (2004) 329-334
25. Tsutsui N., and Kamiyama T. Transforming growth factor beta-induced failure of resistance to infection with blood-stage Plasmodium chabaudi in mice. Infection and Immunity 67 (1999) 2306-2311
26. Vodovotz Y. Control of nitric oxide production by transforming growth factor-beta1: mechanistic insights and potential relevance to human disease. Nitric Oxide 1 (1997) 3-17
27. Vodovotz Y. Deciphering the complexity of acute inflammation using mathematical models. Immunology Research 36 (2006) 237-245
28. Vodovotz Y., Bogdan C., Paik J., Xie Q.W., and Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor beta. Journal of Experimental Medicine 178 (1993) 605-613
29. Vodovotz Y., Zamora R., Lieber M.J., and Luckhart S. Cross-talk between nitric oxide and transforming growth factor-beta1 in malaria. Current Molecular Medicine 4 (2004) 787-797
30. Walther M., Tongren J.E., Andrews L., Korbel D., King E., Fletcher H., Andersen R.F., Bejon P., Thompson F., Dunachie S.J., Edele F., de Souza J.B., Sinden R.E., Gilbert S.C., Riley E.M., and Hill A.V. Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23 (2005) 287-296
31. Walther M., Woodruff J., Edele F., Jeffries D., Tongren J.E., King E., Andrews L., Bejon P., Gilbert S.C., De Souza J.B., Sinden R., Hill A.V., and Riley E.M. Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. Journal of Immunology 177 (2006) 5736-5745
32. Wenisch C., Parschalk B., Burgmann H., Looareesuwan S., and Graninger W. Decreased serum levels of TGF-beta in patients with acute Plasmodium falciparum malaria. Journal of Clinical Immunology 15 (1995) 69-73