Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein

Biochemistry

Volumn 45, Issue 31, 2006, Pages 9540-9549

  Davenport, Martin ^a   Alvarenga, Patricia H ^b   Shao, Li ^c   Fujioka, Hisashi ^d   Bianconi, M Lucia ^b   Oliveira, Pedro L ^b   Jacobs Lorena, Marcelo ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; ELECTRON MICROSCOPY; FLUORESCENCE; GENES; HEAVY METALS; IMMUNOLOGY; MOLECULAR STRUCTURE; SPECTROPHOTOMETRY;

AEDES AEGYPTI; AEIMUCI; IMMUNOELECTRON MICROSCOPY; MOSQUITO LARVAE;

PROTEINS;

AGAROSE; BINDING PROTEIN; CHITIN; GENE PRODUCT; HEAVY METAL; HEME; MUCIN 1; PROTEIN AEIMUCI; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AEDES AEGYPTI; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; DETOXIFICATION; DIGESTION; EXPOSURE; FEMALE; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; LARVA; MICROCALORIMETRY; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TITRIMETRY;

AEDES; AMINO ACID SEQUENCE; ANIMALS; CHITIN; CIRCULAR DICHROISM; FEMALE; HEME; INSECT PROTEINS; INTESTINES; MICROSCOPY, IMMUNOELECTRON; MOLECULAR SEQUENCE DATA; MUCINS; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

AEDES AEGYPTI;

EID: 33747090621     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0605991     Document Type: Article

References (55)

1. Peters, W. (1992) Peritrophic membranes, in Zoophysiology (Bradshaw, D., Burggren, W., Heller, H. C., Ishii, S., Langer, H., Neuweiler, G., and Randall, D. J., Eds.) Vol. 130, Springer-Verlag, Berlin, Germany.
2. Tellam, R. L. (1996) The peritrophic matrix, in Biology of Insect Midgut, 1st ed. (Lehane, M. J., and Billingsley, P. F., Eds.) pp 86-114, Chapman and Hall, London, U.K.
3. Lehane, M. J. (1997) Peritrophic matrix structure and function, Annu. Rev. Entomol. 42, 525-550.
4. Terra, W. R. (2001) The origins and functions of the insect peritrophic membrane and peritrophic gel, Arch. Insect. Biochem. Physiol. 47, 47-61.
5. Wang, P., and Granados, R. R. (2001) Molecular structure of the peritrophic membrane (PM): Identification of potential PM target sites for insect control, Arch. Insect Biochem. Physiol. 47, 110-118.
6. Romoser, W. J. (1996) The vector alimentar system, in The Biology of Disease Vectors, 1st ed. (Beaty, B. J., and Marquadt, W. C., Eds.) pp 298-317, University Press of Colorado, Boulder, CO.
7. Tappel, A. L. (1955) Unsaturated lipid oxidation catalyzed by hematin compounds, J. Biol. Chem. 217, 721-733.
8. Vincent, S. H., Grady, R. W., Shaklai, N., Snider, J. M., and Muller-Eberhard U. (1988) The influence of heme-binding proteins in heme-catalyzed oxidations, Arch. Biochem. Biophys. 265, 539-550.
9. Aft, R. L., and Mueller, G. C. (1984) Hemin-mediated oxidative degradation of proteins, J. Biol. Chem. 259, 301-305.
10. Vincent, S. H. (1989) Oxidative effects of heme and porphyrins on proteins and lipids, Semin. Hematol. 26, 105-113.
11. Aft, R. L., and Mueller, G. C. (1983) Hemin-mediated DNA strand scission, J. Biol. Chem. 258, 12069-12072.
12. Chou, A. C., and Fitch, C. D. (1980) Hemolysis of mouse erythrocytes by ferriprotoporphyrin IX and chloroquine. Chemotherapeutic implications, J. Clin. Invest. 66, 856-858.
13. Chou, A. C., and Fitch, C. D. (1981) Mechanism of hemolysis induced by ferriprotoporphyrin IX, J. Clin. Invest. 68, 672-677.
14. Chiu, D., and Lubin, B. (1989) Oxidative hemoglobin denaturation and RBC destruction: The effect of heme on red cell membranes, Semin. Hematol. 26, 128-135.
15. 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.
16. Slater, A. F., Swiggard, W. J., Orton, B. R., Flitter, W. D., Goldberg, D. E., Cerami, A., and Henderson, G. B. (1991) An iron-carboxylate bond links the heme units of malaria pigment, Proc. Natl. Acad. Sci. U.S.A. 88, 325-329.
17. Páscoa, V., Oliveira, P. L., Dansa-Petretski, M., Silva, J. R., Alvarenga, P. H., Jacobs-Lorena, M., and Lemos, F. J. A. (2002) Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion, Insect Biochem. Mol. Biol. 32, 517-523.
18. Tellam, R. L., Wijffels, G., and Willadsen, P. (1999) Peritrophic matrix proteins, Insect Biochem. Mol. Biol. 29, 87-101.
19. Rayms-Keller, A., McGaw, M., Oray, C., Carlson, J. O., and Beaty, B. J. (2000) Molecular cloning and characterization of a metal responsive Aedes aegypti intestinal mucin cDNA, Insect Mol. Biol. 9, 419-426.
20. Muller, P. Y., Studer, E., and Miserez, A. R. (2001) Molecular BioComuting Suite: A word processor add-in for the analysis and manipulation of nucleic acid and protein sequence data, Biotechniques 31, 1306-1313.
21. Einarson, M. B. (2001) Detection of protein-protein interactions using far Western with GST fusion proteins, in Molecular Cloning: A Laboratory Manual, 3rd ed. (Sambrook, J., and Russell, D. W., Eds.) pp 18.48-18.54, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Devenport, M., Fujioka, H., and Jacobs-Lorena, M. (2004) Storage and secretion of the peritrophic matrix protein Ag-Aper1 and trypsin in the midgut of Anopheles gambiae, Insect. Mol. Biol. 13, 349-358.
23. Frangioni, J. V., and Neel, B. G. (1993) Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins, Anal. Biochem. 210, 179-187.
24. Tsutsui, K., and Mueller, G. C. (1982) Affinity chromatography of heme binding proteins: An improved method for the synthesis of hemin agarose, Anal. Biochem. 121, 244-250.
25. Sreerama N., and Woody, R. W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism, Anal. Biochem. 209, 32-44.
26. Geourjon, C., and Deleage, D. (1995) SOPMA: Significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments, Comput. Appl. Biosci. 11, 681-684.
27. Shao, L., Devenport, M., Fujioka, H., Ghosh, A., and Jacobs-Lorena, M. (2005) Identification and characterization of a novel peritrophic matrix protein, Ae-Aper50, and the microvillar membrane protein, AEG12, from the mosquito, Aedes aegypti, Insect Biochem. Mol. Biol. 35, 947-959.
28. Morlais, I., and Severson, D. W. (2001) Identification of a polymorphic mucin-like gene expressed in the midgut of the mosquito Aedes aegypti, using an integrated bulked segregant and differential display analysis, Genetics 158, 1125-1136.
29. Morlais, I., and Severson, D. W. (2003) Intraspecific DNA variation in nuclear genes of the mosquito Aedes aegypti, Insect Mol. Biol. 12, 631-639.
30. 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.
31. Villalon, J. M., Ghosh, A., and Jacobs-Lorena, M. (2003) The peritrophic matrix limits the rate of digestion in adult Anopheles stephensi and Aedes aegypti mosquitoes, J. Insect Physiol. 49, 891-895.
32. Ibrahim, G. H., Smartt, C. T., Kiley, L. M., and Christensen, B. M. (2000) Cloning and characterization of a chitin synthase cDNA from the mosquito Aedes aegypti, Insect Biochem. Mol. Biol. 12, 1213-1222.
33. Stohler, H. (1957) Analyse des infektionsverlaufes von Plasmodium gallinaceum im darme von Aedes aegypti, Acta Trop. 14, 302-352.
34. Freyvogel, T. A., and Staubli, W. (1965) The formation of the peritrophic membrane in culicidae, Acta Trop. 22, 118-147.
35. Perrone, J. B., and Spielman, A. (1988) Time and site of assembly of the peritrophic membrane of the mosquito Aedes aegypti, Cell Tissue Res. 252, 473-478.
36. Wang, P., Li, G., and Granados, R. R. (2004) Identification of two new peritrophic membrane proteins from larval Trichoplusia ni: Structural characteristics and their functions in the protease rich insect gut, Insect Biochem. Mol. Biol. 34, 215-227.
37. Elvin, C. M., Vuocolo, T., Pearson, R. D., East, I. J., Riding, G. A., Eisemann, C. H., and Tellam, R. L. (1996) Characterization of a major peritrophic membrane protein, peritrophin-44, from the larvae of Lucilia cuprina. cDNA and deduced amino acid sequences, J. Biol. Chem. 271, 8925-8935.
38. Wang, P., and Granados, R. R. (2000) Calcofluor disrupts the midgut defense system in insects, Insect Biochem. Mol. Biol. 30, 135-143.
39. Zhang, L., and Guarente, L. (1995) Heme binds to a short sequence that serves a regulatory function in diverse proteins, EMBO J. 14, 313-320.
40. Billingsley, P. F., and Rudin, W. (1992) The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species, J. Parasitol. 78, 430-440.
41. Bertram, D. S., and Bird, R. G. (1961) Studies on mosquito-borne viruses in their vectors. I. The normal fine structure of the midgut epithelium of the adult female Aedes aegypti (L.) and the functional significance of its modification following a blood meal, Trans. R. Soc. Trop. Med. Hyg. 55, 404-423.
42. Staubli, W., Freyvogel, T. A., and Suter, J. (1966) Structural modification of the endoplasmic reticulum of midgut epithelial cells of mosquitoes in relation to blood intake, J. Microsc. 5, 189-204.
43. Barbehenn, R. V. (2001) Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals, Arch. Insect. Biochem. Physiol. 47, 86-99.
44. Barbehenn, R. V., and Stannard, J. (2004) Antioxidant defense of the midgut epithelium by the peritrophic envelope in caterpillars, J. Insect Physiol. 50, 783-790.
45. Oliveira, M. F., Silva, J. R., Dansa-Petretski, M., de Souza, W., Lins, U., Braga, C. M. S., Masuda, H., and Oliveira, P. L. (1999) Heme detoxification by an insect, Nature 400, 517-518.
46. Shen, Z., and Jacobs-Lorena, M. (1998) A type I peritrophic matrix protein from the malaria vector Anopheles gambiae binds to chitin. Cloning, expression, and characterization, J. Biol. Chem. 273, 17665-17670.
47. Schorderet, S., Pearson, R. D., Vuocolo, T., Eisemann, C., Riding, G. A., and Tellam, R. L. (1998) cDNA and deduced amino acid sequences of a peritrophic membrane glycoprotein, "peritrophin-48", from the larvae of Lucilia cuprina, Insect Biochem. Mol. Biol. 25, 99-111.
48. Bock, K. W., de Matteis, F., and Aldridge, W. N., Eds. (1978) Heme and Hemoproteins, Springer-Verlag, New York.
49. McCoubrey, W. K., Jr., Huang, T. J., and Maines, M. D. (1997) Heme oxygenase-2 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis, J. Biol. Chem. 272, 12568-12574.
50. Lathrop, J. T., and Timko, M. P. (1993) Regulation by heme of mitochondrial protein transport through a conserved amino acid motif, Science 259, 522-525.
51. Huang, T. J., McCoubrey, W. K., Jr., and Maines, M. D. (2001) Heme oxygenase-2 interaction with metalloporphyrins: Function of heme regulatory motifs, Antioxid. Redox Signaling 3, 685-696.
52. Shen, Z., and Jacobs-Lorena, M. (1999) Evolution of chitin-binding proteins in invertebrates, J. Mol. Evol. 48, 341-347.
53. Dyson, H. J., and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol. 6, 197-208.
54. Choi, C. Y., Cerda, J. F., Chu, H,. Babcock, G. T., and Marietta, M. A. (1999) Spectroscopic characterization of the heme-binding sites in Plasmodium falciparum histidine-rich protein 2, Biochemistry 38, 16916-16924.
55. Moskalyk, L. A., Oo, M. M., and Jacobs-Lorena, M. (1996) Peritrophic matrix proteins of Anopheles gambiae and Aedes aegypti, Insect Mol. Biol. 5, 261-268.