Mitochondrial reactive oxygen species modulate mosquito susceptibility to Plasmodium infection

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Gonçalves, Renata L S ^a,b   Oliveira, Jose Henrique M ^a,b   Oliveira, Giselle A ^a   Andersen, John F ^a   Oliveira, Marcus F ^b   Oliveira, Pedro L ^b,c   Barillas Mury, Carolina ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c Instituto Nacional de Ciencia e Tecnologia em Entomologia Molecular   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES GAMBIAE MITOCHONDRIAL CARRIER 1; CARRIER PROTEIN; PROTON; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AEDES AEGYPTI; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOPHELES GAMBIAE; ARTICLE; EPITHELIUM; FEMALE; GENE SILENCING; INFECTION SENSITIVITY; MIDGUT; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOSQUITO; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PLASMODIUM BERGHEI INFECTION; PROTEIN FAMILY;

AEDES; ANIMALS; ANOPHELES GAMBIAE; ANTI-BACTERIAL AGENTS; CLONING, MOLECULAR; GENE SILENCING; HYDROGEN PEROXIDE; MALARIA; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CONFORMATION; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHYLOGENY; PLASMODIUM BERGHEI; PROTONS; PROTOZOAN PROTEINS; REACTIVE OXYGEN SPECIES; RNA, DOUBLE-STRANDED;

ANOPHELES GAMBIAE;

EID: 84864005183     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041083     Document Type: Article

References (47)

1. WHO (2011) World Malaria Report; WHO website available: http://www.who.int/malaria/world_malaria_report_2011/en/Accessed 2012 June 25.
2. Jaramillo-Gutierrez G, Rodrigues J, Ndikuyeze G, Povelones M, Molina-Cruz A, et al. (2009) Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes. BMC Microbiol 9: 154.
3. Blandin SA, Marois E, Levashina EA, (2008) Antimalarial responses in Anopheles gambiae: from a complement-like protein to a complement-like pathway. Cell Host Microbe 3: 364-374.
4. Han YS, Thompson J, Kafatos FC, Barillas-Mury C, (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J 19: 6030-6040.
5. Kumar S, Gupta L, Han YS, Barillas-Mury C, (2004) Inducible peroxidases mediate nitration of anopheles midgut cells undergoing apoptosis in response to Plasmodium invasion. J Biol Chem 279: 53475-53482.
6. Oliveira Gde A, Lieberman J, Barillas-Mury C, (2012) Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 335: 856-859.
7. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670.
8. Kumar S, Christophides GK, Cantera R, Charles B, Han YS, et al. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc Natl Acad Sci U S A 100: 14139-14144.
9. Molina-Cruz A, DeJong RJ, Charles B, Gupta L, Kumar S, et al. (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem 283: 3217-3223.
10. Babior BM, Lambeth JD, Nauseef W, (2002) The neutrophil NADPH oxidase. Arch Biochem Biophys 397: 342-344.
11. Lambeth JD, (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189.
12. Leto TL, Geiszt M, (2006) Role of Nox family NADPH oxidases in host defense. Antioxid Redox Signal 8: 1549-1561.
13. Ha EM, Oh CT, Bae YS, Lee WJ, (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847-850.
14. Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C, (2010) A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327: 1644-1648.
15. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, et al. (2000) Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26: 435-439.
16. Bai Y, Onuma H, Bai X, Medvedev AV, Misukonis M, et al. (2005) Persistent nuclear factor-kappa B activation in Ucp2-/- mice leads to enhanced nitric oxide and inflammatory cytokine production. J Biol Chem 280: 19062-19069.
17. West AP, Shadel GS, Ghosh S, (2011) Mitochondria in innate immune responses. Nat Rev Immunol 11: 389-402.
18. Seth RB, Sun L, Ea CK, Chen ZJ, (2005) Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
19. West AP, Brodsky IE, Rahner C, Woo DK, Erdjument-Bromage H, et al. (2011) TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 472: 476-480.
20. Bulua AC, Simon A, Maddipati R, Pelletier M, Park H, et al. (2011) Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associated periodic syndrome (TRAPS). J Exp Med 208: 519-533.
21. Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE, (2009) Mitochondria and reactive oxygen species. Free Radic Biol Med 47: 333-343.
22. Korshunov SS, Skulachev VP, Starkov AA, (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15-18.
23. Boveris A, Chance B, (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134: 707-716.
24. Negre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, et al. (1997) A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11: 809-815.
25. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, et al. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790.
26. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, et al. (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415: 96-99.
27. Chance B, Williams GR, (1955) Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem 217: 409-427.
28. Palmieri F, (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 447: 689-709.
29. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134: 112-123.
30. Brand MD, Pakay JL, Ocloo A, Kokoszka J, Wallace DC, et al. (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem J 392: 353-362.
31. Affourtit C, Jastroch M, Brand MD, (2011) Uncoupling protein-2 attenuates glucose-stimulated insulin secretion in INS-1E insulinoma cells by lowering mitochondrial reactive oxygen species. Free Radic Biol Med 50: 609-616.
32. Toime LJ, Brand MD, (2010) Uncoupling protein-3 lowers reactive oxygen species production in isolated mitochondria. Free Radic Biol Med 49: 606-611.
33. Goncalves RL, Machado AC, Paiva-Silva GO, Sorgine MH, Momoli MM, et al. (2009) Blood-feeding induces reversible functional changes in flight muscle mitochondria of Aedes aegypti mosquito. PLoS One 4: e7854.
34. Oliveira JH, Goncalves RL, Oliveira GA, Oliveira PL, Oliveira MF, et al. (2011) Energy metabolism affects susceptibility of Anopheles gambiae mosquitoes to Plasmodium infection. Insect Biochem Mol Biol 41: 349-355.
35. Franke-Fayard B, Trueman H, Ramesar J, Mendoza J, van der Keur M, et al. (2004) A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137: 23-33.
36. Billker O, Shaw MK, Margos G, Sinden RE, (1997) The roles of temperature, pH and mosquito factors as triggers of male and female gametogenesis of Plasmodium berghei in vitro. Parasitology 115 (Pt 1): 1-7.
37. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
38. Oliveira JH, Goncalves RL, Lara FA, Dias FA, Gandara AC, et al. (2011) Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog 7: e1001320.
39. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
40. Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, et al. (1997) Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science 276: 425-428.
41. Luk E, Carroll M, Baker M, Culotta VC, (2003) Manganese activation of superoxide dismutase 2 in Saccharomyces cerevisiae requires MTM1, a member of the mitochondrial carrier family. Proc Natl Acad Sci U S A 100: 10353-10357.
42. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trezeguet V, Lauquin GJ, et al. (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426: 39-44.
43. Jaramillo-Gutierrez G, Molina-Cruz A, Kumar S, Barillas-Mury C, (2010) The Anopheles gambiae oxidation resistance 1 (OXR1) gene regulates expression of enzymes that detoxify reactive oxygen species. PLoS One 5: e11168.
44. Nilsson R, Schultz IJ, Pierce EL, Soltis KA, Naranuntarat A, et al. (2009) Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis. Cell Metab 10: 119-130.
45. Shabalina IG, Kramarova TV, Nedergaard J, Cannon B, (2006) Carboxyatractyloside effects on brown-fat mitochondria imply that the adenine nucleotide translocator isoforms ANT1 and ANT2 may be responsible for basal and fatty-acid-induced uncoupling respectively. Biochem J 399: 405-414.
46. Yu XX, Lewin DA, Zhong A, Brush J, Schow PW, et al. (2001) Overexpression of the human 2-oxoglutarate carrier lowers mitochondrial membrane potential in HEK-293 cells: contrast with the unique cold-induced mitochondrial carrier CGI-69. Biochem J 353: 369-375.
47. Ishida I, Kubo H, Suzuki S, Suzuki T, Akashi S, et al. (2002) Hypoxia diminishes toll-like receptor 4 expression through reactive oxygen species generated by mitochondria in endothelial cells. J Immunol 169: 2069-2075.