Biglutaminyl-biliverdin IX alpha as a heme degradation product in the dengue fever insect-vector Aedes aegypti

Biochemistry

Volumn 46, Issue 23, 2007, Pages 6822-6829

  Pereira, Luiza O R ^a   Oliveira, Pedro L ^a   Almeida, Igor C ^b,c   Paiva Silva, Gabriela O ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF TEXAS AT EL PASO   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION SPECTROSCOPY; DEGRADATION; ENZYME ACTIVITY; LIGHT ABSORPTION; MOLECULAR STRUCTURE; OXIDANTS;

AEDES AEGYPTI; INSECT VECTORS; OXYGENASE;

HEMOGLOBIN;

BILIVERDIN; CARBON MONOXIDE; CYSTEINE; FERROUS ION; GLUTAMINE; HEME; HEME OXYGENASE; HEMOGLOBIN; OXIDIZING AGENT; PORPHYRIN;

ADAPTATION; AEDES AEGYPTI; ARTICLE; DENGUE; DISEASE CARRIER; ELECTROSPRAY MASS SPECTROMETRY; ENZYME MECHANISM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVERSED PHASE LIQUID CHROMATOGRAPHY; RHODNIUS; STRUCTURE ANALYSIS;

AEDES; ANIMALS; BILE PIGMENTS; BILIVERDINE; DENGUE; HEME; INSECT PROTEINS; INSECT VECTORS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PIGMENTS, BIOLOGICAL;

AEDES AEGYPTI; ANIMALIA; HEXAPODA; MAMMALIA; TRIATOMINAE;

EID: 34250202215     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700011d     Document Type: Article

References (47)

1. Gubler, D. J. (1998) Dengue and dengue hemorrhagic fever, Clin. Microbiol. Rev. 11, 480-496.
2. Briegel, H., and Lea, A. O. (1975) Relationship between protein and proteolytic activity in the midgut of mosquitoes, J. Insect Physiol. 21, 1597-1604.
3. Ryter, S. W., and Tyrrell, R. M. (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties, Free Radical Biol. Med. 28, 289-309.
4. Schmitt, T. H., Frezzatti, W. A., Jr., and Schreier, S. (1993) Hemin-induced lipid membrane disorder and increased permeability: a molecular model for the mechanism of cell lysis, Arch. Biochem. Biophys. 307, 96-103.
5. Graça-Souza, A. V., Maya-Monteiro, C., Paiva-Silva, G. O., Braz, G. R., Paes, M. C. Sorgine, M. H., Oliveira, M. F., and Oliveira, P. L. (2006) Adaptations against heme toxicity in blood-feeding arthropods, Insect Biochem. Mol. Biol. 36, 322-335.
6. Dansa-Petretski, M., Ribeiro, J. M., Atella, G. C., Masuda, H., and Oliveira, P. L. (1995) Antioxidant role of Rhodnius prolixus heme-binding protein. Protection against heme-induced lipid peroxidation, J. Biol. Chem. 270, 10893-10896.
7. Maya-Monteiro, C. M., Daffre, S., Logullo, C., Lara, F. A., Alves, E. W. Capurro, M. L., Zingali, R., Almeida, I. C., and Oliveira, P. L. (2000) HeLp, a heme lipoprotein from the hemolymph of the cattle tick, Boophilus microplus, J. Biol. Chem. 275, 36584-36589.
8. Paes, M. C., Oliveira, M. B., and Oliveira, P. L. (2001) Hydrogen peroxide detoxification in the midgut of the blood-sucking insect, Rhodnius prolixus, Arch. Insect Biochem. Physiol. 48, 63-71.
9. Oliveira, M. F., Silva, J. R. Dansa-Petretski, M., de Souza, W., Lins, U., Braga, C. M., Masuda, H., and Oliveira, P. L. (1999) Haem detoxification by an insect, Nature 400, 517-518.
10. Lara, F. A., Lins, U., Paiva-Silva, G., Almeida, I. C.,, Braga, C. M., Miguens, F. C., Oliveira, P. L., and Dansa-Petretski, M. (2003) A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome, J. Exp. Biol. 206, 1707-1715.
11. Lara, F. A., Lins, U., Bechara, G. H., and Oliveira, P. L. (2005) Tracing heme in a living cell: hemoglobin degradation and heme traffic in digest cells of the cattle tick Boophilus microplus, J. Exp. Biol. 208, 3093-3101.
12. Pascoa, V., Oliveira, P. L., Dansa-Petretski, M., Silva, J. R., Alvarenga, P. H., Jacobs-Lorena, M., and Lemos, F. J. (2002) Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion, Insect Biochem. Mol. Biol. 32, 517-523.
13. Devenport, M., Alvarenga, P. H., Shao, L., Fujioka, H., Bianconi, M. L., Oliveira, P. L., and Jacobs-Lorena, M. (2006) Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein, Biochemistry 45, 9540-9549.
14. Ortiz de Montellano, P. R., and Wilks, A. (2000) Heme Oxygenase: Structure and Mechanism, Adv. Inorg. Chem. 51, 359-407.
15. Ortiz de Montellano, P. R. (2000) The mechanism of heme oxygenase, Curr. Opin. Chem. Biol. 4, 221-227.
16. Kutty, R. K., and Maines, M. D. (1981) Purification and characterization of biliverdin reductase from rat liver, J. Biol. Chem. 256, 3956-3962.
17. Billing, B. H., Cole, P. G., and Lathe, G. H. (1957) The excretion of bilirubin as a diglucuronide giving the direct van den Bergh reaction, Biochem. J. 65, 774-784.
18. Paiva-Silva, G. O., Cruz-Oliveira, C., Nakayasu, E. S., Maya-Monteiro, C. M., Dunkov, B. C., Masuda, H., Almeida, I. C., and Oliveira, P. L. (2006) A heme-degradation pathway in a blood-sucking insect, Proc. Natl. Acad. Sci. U.S.A. 103, 8030-8035.
19. Garcia, E. S., Macarini, J. D., Garcia, M. L., and Ubatuba, F. B. (1975) Feeding of Rhodnius prolixus in the laboratory, An. Acad. Bras. Cienc. 47, 537-545.
20. Noriega, F. G., and Wells, M. A. (1999) A molecular view of trypsin synthesis in the midgut of Aedes aegypti, J. Insect Physiol. 45, 613-620.
21. Niittynen, M., Tuomisto, J. T., Auriola, S., Pohjanvirta, R., Syrjala, P., Simanainen, U., Viluksela, M., and Tuomisto, J. (2003) 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD)-induced accumulation of biliverdin and hepatic peliosis in rats, Toxicol. Sci. 71, 112-123.
22. Kayser, H. (1985) Pigments, in Comprehensive Insect Physiology, Biochemistry and Pharmacology (Kerkut, G. A., and Gilbert, L. I., Eds.) Vol. 10, pp 367-415, Pergamon Press, Oxford.
23. Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. (1997) An Elicitor of Plant Volatiles from Beet Armyworm Oral Secretion, Science 276, 945-949.
24. Trinh, M. U., Blake, J., Harrison, J. R., Gerace, R., Ranieri, E., Fletcher, J. M., and Johnson, D. W. (2003) Quantification of glutamine in dried blood spots and plasma by tandem mass spectrometry for the biochemical diagnosis and monitoring of ornithine transcarbamylase deficiency, Clin. Chem. 49, 681-684.
25. McDonagh, A. (2001) Turning green to gold, Nat. Struct. Biol. 8, 198-200.
26. Ribeiro, J. M. (1995) Blood-feeding arthropods: live syringes or invertebrate pharmacologists?, Infect. Agents. Dis. 4, 143-152.
27. Schuller, D. J., Wilks, A., Ortiz, de Montellano, P. R., and Poulos, T. L. (1999) Crystal structure of human heme oxygenase-1, Nat. Struct. Biol. 6, 860-867.
28. Smartt, C. T., Chiles, J., Lowenberger, C., and Christensen, B. M. (1998) Biochemical analysis of a blood meal-induced Aedes aegypti glutamine synthetase gene, Insect Biochem. Mol. Biol. 28, 935-945.
29. Shao, L., Devenport, M., and Jacobs-Lorena, M. (2001) The peritrophic matrix of hematophagous insects, Arch. Insect Biochem. Physiol. 47, 119-125.
30. Goldstrohm, D. A., Pennington, J. E., and Wells, M. A. (2003) The role of hemolymph proline as a nitrogen sink during blood meal digestion by the mosquito Aedes aegypti, J. Insect Physiol. 49, 115-121.
31. Laik, C. G., Alborn, H. T., and Tumlinson, J. H. 3rd (2003) Rapid biosynthesis of N-linolenoyl-L-glutamine, an elicitor of plant volatiles, by membrane-associated enzyme(s) in Manduca sexta, Proc. Natl. Acad. Sci. U.S.A. 100, 7027-7032.
32. Paré, P. W., Alborn, H. T., and Tumlinson, J. H. (1998) Concerted biosynthesis of an insect elicitor of plant volatiles, Proc. Natl. Acad. Sci. U.S.A. 95, 13971-13975.
33. Kumar, S., and Bandyopadhyay, U. (2005) Free heme toxicity and its detoxification systems in human, Toxicol. Lett. 157, 175-188.
34. McDonagh, A. F. (1972) Evidence for singlet oxygen quenching by biliverdin IX-alpha dimethyl ester and its relevance to bilirubin photo-oxidation, Biochem. Biophys. Res. Commun. 48, 408-415.
35. Stocker, R., Yamamoto, Y., McDonagh, A. F., Glazer, A. N. and Ames, B. N. (1987) Bilirubin is an antioxidant of possible physiological importance, Science 235, 1043-1046.
36. Graiça-Souza, A.V., Barja-Fidalgo, C. Anuda, M. A. B., de Freitas, M. S. and Oliveira, P. L. (2002) Neutrophil activation by heme: implications for inflammatory processes, Blood 99, 4160-4165.
37. Otterbein, L. E., Bach, F. H., Alam, J., Soares, M., Tao Lu, H., Wysk, M., Davis, R. J., Flavell, R. A., and Choi, A. M. (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway, Nat. Med. 6, 422-428.
38. Brouard, S., Berberat, P. O., Tobiasch, E., Seldon, M. P., Bach, F. H., and Soares, M. P. (2002) Heme oxygenase-1-derived carbon monoxide requires the activation of transcription factor NF-kappa B to protect endothelial cells from tumor necrosis factor-alpha-mediated apoptosis, J. Biol. Chem. 277, 17950-17961.
39. Ryter, S. W., and Choi, A. M. (2005) Heme oxygenase-1: redox regulation of a stress protein in lung and cell culture models, Antioxid. Redox Signaling 7, 80-91.
40. Yamashita, K., McDaid, J., Ollinger, R., Tsui, T. Y., Berberat, P. O., Usheva, A., Csizmadia, E., Smith, R. N., Soares, M. P., and Bach, F. H. (2004) Biliverdin, a natural product of heme catabolism, induces tolerance to cardiac allografts, FASEB J. 18, 765-767.
41. Wilks, A. and Schmitt, M. P. (1998) Expression and characterization of a heme oxygenase (Hmu O) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle, J. Biol. Chem. 273, 837-841.
42. Zhu, W., Wilks, A., and Stojiljkovic, I. (2000) Degradation of heme in gram-negative bacteria: the product of the hemO gene of Neisseriae is a heme oxygenase, J. Bacterial. 182, 6783-6790.
43. Ratliff, M., Zhu, W., Deshmukh, R., Wilks, A., and Stojiljkovic, I. (2001) Homologues of neisserial heme oxygenase in Gram-negative bacteria: degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa, J Bacterial. 183, 6394-6403.
44. Dunkov, B. C., Georgieva, T., Yoshiga, T., Hall, M., and Law, JH. (2002) Aedes aegypti ferritin heavy chain homologue: feeding of iron or blood influences message levels, lengths and subunit abundance, J. Insect Sci. 2, 7.
45. Gêiser, D. L., Chavez, C. A., Flores-Munguia, R., Winzerling, J. J., and Pham, D. Q. (2003) Aedes aegypti ferritin, Eur. J. Biochem. 270, 3667-3674.
46. Law, J. H. (2002) Insects, oxygen, and iron, Biochem. Biophys. Res. Commun. 19, 1191-1195.
47. Kumar, S., Christophides, G. K., Camera, R., Charles, B., Han, Y. S., Meister, S., Dimopoulos, G., Kafatos, F. C., and Barillas-Mury, C. (2003) The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae, Proc. Natl. Acad. Sci. U.S.A. 100, 14139-14144.