Fate of blood meal iron in mosquitoes

Journal of Insect Physiology

Volumn 53, Issue 11, 2007, Pages 1169-1178

  Zhou, Guoli ^a   Kohlhepp, Pete ^a   Geiser, Dawn ^a   Frasquillo, Maria del Carmen ^b   Vazquez Moreno, Luz ^b   Winzerling, Joy J ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b CENTRO DE INVESTIGACIÓN EN ALIMENTACIÓN Y DESARROLLO   (Mexico)

Author keywords

Blood meal; Egg iron reserve; Ferritin; Heme iron; Iron transport; Transferrin iron

Indexed keywords

IRON; TRANSFERRIN;

BLOOD; EGG; IRON; MASS SPECTROMETRY; MOSQUITO; PROTEIN;

AEDES; ANIMAL; ARTICLE; BLOOD; FEMALE; METABOLISM; OOCYTE; OVARY;

AEDES; ANIMALS; BLOOD; FEMALE; IRON; OVARY; OVUM; TRANSFERRIN;

AEDES AEGYPTI; ANIMALIA; VERTEBRATA;

EID: 35548958227     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2007.06.009     Document Type: Article

References (65)

1. Arredondo M., Munoz P., Mura C.V., and Nunez M.T. HFE inhibits apical iron uptake by intestinal epithelial (Caco-2) cells. The FASEB Journal 15 (2001) 1276-1278
2. Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Struhl K. Current Protocols in Molecular Biology Volume: 3 (2001), Wiley, Massachusetts General Hospital, Harvard Medical School, USA pp. 16.11.10
3. Beerntsen B.T., and Christensen B.M. Dirofilaria immitis: effect on hemolymph polypeptide synthesis in Aedes aegypti during melanotic encapsulation reactions against microfilariae. Experimental Parasitology 71 (1990) 406-414
4. Bottke W. Isolation and properties of vitellogenic ferritin from snails. Journal of Cell Science 58 (1982) 225-240
5. Braz G.R., Moreira M.F., Masuda H., and Oliveira P.L. Rhodnius heme-binding protein (RHBP) is a heme source for embryonic development in the blood-sucking bug Rhodnius prolixus (Hemiptera, Reduviidae). Insect Biochemistry and Molecular Biology 32 (2002) 361-367
6. Davis B.J. Disc electrophoresis II. Method and application to human serum proteins. Annuals of New York Academic Sciences 121 (1964) 404-427
7. Devenport M., Fujioka H., and Jacobs-Lorena M. Storage and secretion of the peritrophic matrix protein Ag-Aper1 and trypsin in the midgut of Anopheles gambiae. Insect Molecular Biology 13 (2004) 349-358
8. Devenport M., Fujioka H., Donnelly-Doman M., Shen Z., and Jacobs-Lorena M. Storage and secretion of Ag-Aper14, a novel peritrophic matrix protein, and Ag-Muc1 from the mosquito Anopheles gambiae. Cell and Tissue Research 320 (2005) 175-185
9. Devenport M., Alvarenga P.H., Shao L., Fujioka H., Bianconi M.L., Oliveira P.L., and Jacobs-Lorena M. Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry 45 (2006) 9540-9549
10. Dumont J.N. Oogenesis in Xenopus laevis (Daudin). VI. The route of injected tracer transport in the follicle and developing oocyte. Journal of Experimental Zoology 204 (1978) 193-217
11. Dunkov B.C., Zhang D., Choumarov K., Winzerling J.J., and Law J.H. Isolation and characterization of mosquito ferritin and cloning of a cDNA that encodes one subunit. Archives of Insect Biochemistry and Physiology 29 (1995) 293-307
12. Dunkov B.C., Georgieva T., Yoshiga T., Hall M., and Law J.H. Aedes aegypti ferritin heavy chain homologue: feeding of iron or blood influences message levels, lengths and subunit abundance. Journal of Insect Science 2 (2002) 1-9
13. Elbirt K.K., and Bonkovsky H.L. Heme oxygenase: recent advances in understanding its regulation and role. Proceedings of the Association of American Physicians 111 (1999) 438-447
14. Fallon A.M., and Sun D. Exploration of mosquito immunity using cells in culture. Insect Biochemistry and Molecular Biology 31 (2001) 263-278
15. Fleming R.E. Advances in understanding the molecular basis for the regulation of dietary iron absorption. Current Opinion in Gastroenterology 21 (2005) 201-206
16. Fleming R.E., and Bacon B.R. Orchestration of iron homeostasis. The New England Journal of Medicine 352 (2005) 1741-1744
17. Geiser D.L., Chavez C.A., Flores-Munguia R., Winzerling J.J., and Pham D.Q. Aedes aegypti ferritin. European Journal of Biochemistry 270 (2003) 3667-3674
18. Geiser, D.L., Mayo, J.J., Winzerling, J.J., 2005. Pilot Study: The Regulation by Iron of a Putative Divalent Metal Transporter in Anopheles gambiae Larval Cells, MOS55. Experimental Biology, San Diego, CA, Federation of American Societies for Experimental Biology.
19. Geiser D.L., Zhang D., and Winzerling J.J. Secreted ferritin: mosquito defense against iron overload?. Insect Biochemistry and Molecular Biology 36 (2006) 177-187
20. Geiser, D.L., Mayo, J.J., Winzerling, J.J., 2007a. The unique regulation of Aedes aegypti larval cell ferritin by iron. Insect Biochemistry and Molecular Biology, in press.
21. Geiser, D.L., Shen, M., Mayo, J., Winzerling, J., 2007b. Mosquito cells regulate iron by secreting iron-loaded ferritin. Insect Biochemistry and Molecular Biology, submitted.
22. Georgieva T., Dunkov B.C., Dimov S., Ralchev K., and Law J.H. Drosophila melanogaster ferritin: cDNA encoding a light chain homologue, temporal and tissue specific expression of both subunit types. Insect Biochemistry and Molecular Biology 32 (2002) 295-302
23. Hagedorn H.H., Turner S., Hagedorn E.A., Pontecorvo F., Greenbaum P., Pfeiffer D., Flanagan T.R., and Wheelock G. Postemergence growth of the ovarian follicles of Aedes aegypti. Journal of Insect Physiology 23 (1977) 203-206
24. Harizanova N., Georgieva T., Dunkov B.C., Yoshiga T., and Law J.H. Aedes aegypti transferrin: gene structure, expression pattern, and regulation. Insect Molecular Biology 14 (2005) 79-88
25. Kim B.S., Lee C.H., Yun C.Y., Yeo S.M., Park W.M., and Kim H.R. Characterization and immunological analysis of ferritin from the hemolymph of Galleria mellonella. Comparative Biochemistry and Physiology A 129 (2001) 501-509
26. Kogan P.H. Substitute blood meal for investigating and maintaining Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 27 (1990) 709-712
27. Kurama T., Kurata S., and Natori S. Molecular characterization of an insect transferrin and its selective incorporation into eggs during oogenesis. European Journal of Biochemistry 228 (1995) 229-235
28. Kurokawa H., J. C. Dewan J.C., Mikami B., Sacchettini J.C., and Hirose M. Crystal structure of hen apo-ovotransferrin. Both lobes adopt an open conformation upon loss of iron. Journal of Biological Chemistry 274 (1999) 28445-28452
29. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
30. Locke M., and Leung H. The induction and distribution of an insect ferritin-a new function for the endoplasmic reticulum. Tissue and Cell 16 (1984) 739-766
31. Locke M., Ketola-Pirie C., and Nichol H. Vacuolar apoferritin synthesis by the fat body of an insect (Calpodes ethlius). Journal of Insect Physiology 37 (1991) 297-309
32. Lowenberger C.A. Form, function and phylogenetic relationships of mosquito immune peptides. Advanced Experimental Medicine and Biology 484 (2001) 113-129
33. Lowenberger C.A. Innate immune response of Aedes aegypti. Insect Biochemistry and Molecular Biology 31 (2001) 219-229
34. +-coupled metal-ion transporters NRAMP1 and DMT1. Pflugers Archiv-European Journal of Physiology 447 (2004) 571-579
35. 2+ transport and uncoupled fluxes. Pflugers Archiv-European Journal of Physiology 451 (2006) 544-558
36. Martinez-Barnetche, J., Solache, M.G., Lecona, A.N., Tello, A.T., Rodriguez, M.D.C., Gamba, G., Vazquez, N., Rodriguez, M.H., Lanz-Mendoza, H., 2007. Cloning and functional characterization of the Anopheles albimanus DMT1/NRAMP homolog: implications in iron metabolism in mosquitoes. Insect Biochemistry and Molecular Biology, in press.
37. Nasr N.M., and Fallon A.M. Detection of lysozyme-like enzymatic activity secreted by an immune-responsive mosquito cell line. Journal of Invertebrate Pathology 82 (2003) 162-166
38. Nichol H., and Locke M. The localization of ferritin in insects. Tissue and Cell 22 (1990) 767-777
39. Nichol H., and Locke M. Secreted ferritin subunits are of two kinds in insects: molecular cloning of cDNAs encoding two major subunits of secreted ferritin from Calpodes ethlius. Insect Biochemistry and Molecular Biology 29 (1999) 999-1013
40. Paiva-Silva G.O., Sorgine M.H., Benedetti C.E., Meneghini R., Almeida I.C., Machado E.A., Dansa-Petretshi M., Yepiz-Plascencia G., Law J.H., Oliveira P.L., and Masuda H. On the biosynthesis of Rhodnius prolixus heme-binding protein. Insect Biochemistry and Molecular Biology 32 (2002) 1533-1541
41. Pascoa V., Oliveira P.L., Dansa-Petretski M., Silva J.R., Alvarenga P.H., Jacobs-Lorena M., and Lemos F.J. Aedes aegypti peritrophic matrix and its interaction with heme during blood digestion. Insect Biochemistry and Molecular Biology 32 (2002) 517-523
42. Pham D.Q., and Chavez C.A. The ferritin light-chain homologue promoter in Aedes aegypti. Insect Molecular Biology 14 (2005) 263-270
43. Pham D.Q., Winzerling J.J., Dodson M.S., and Law J.H. Transcriptional control is relevant in the modulation of mosquito ferritin synthesis by iron. European Journal of Biochemistry 266 (1999) 236-240
44. Pham D.Q., Brown S.E., Knudson D.L., Winzerling J.J., Dodson M.S., and Shaffer J.J. Structure and location of a ferritin gene of the yellow fever mosquito Aedes aegypti. European Journal of Biochemistry 267 (2000) 3885-3890
45. Pham D.Q., Blachuta B.J., Nichol H., and Winzerling J.J. Ribonucleotide reductase subunits from the yellow fever mosquito, Aedes aegypti: cloning and expression. Insect Biochemistry and Molecular Biology 32 (2002) 1037-1044
46. Pham D.Q., Shaffer J.J., Chavez C.A., and Douglass P.L. Identification and mapping of the promoter for the gene encoding the ferritin heavy-chain homologue of the yellow fever mosquito Aedes aegypti. Insect Biochemistry and Molecular Biology 33 (2003) 51-62
47. Pham D.Q., Douglass P.L., Chavez C.A., and Shaffer J.J. Regulation of the ferritin heavy-chain homologue gene in the yellow fever mosquito, Aedes aegypti. Insect Molecular Biology 14 (2005) 223-236
48. Pham D.Q., Kos P.J., Mayo J.J., and Winzerling J.J. Regulation of the ribonucleotide reductase small subunit (R2) in the yellow fever mosquito, Aedes aegypti. Gene 372 (2006) 182-190
49. Pintor M., Ferreiros C.M., and Criado M.T. Characterization of the transferrin-iron uptake system in Neisseria meningitides. FEMS Microbiology Letters 112 (1993) 159-165
50. Ponka P. Cell biology of heme. American Journal of the Medical Sciences 318 (1999) 241-256
51. Reilly C. Iron. In: Reilly C. (Ed). The Nutritional Trace Metals (2004), Blackwell Publishing, Oxford, UK 35-81 (Chapter 2)
52. Ryter S.W., Otterbein L.E., Morse D., and Choi A.M. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Molecular and Cellular Biochemistry 234-235 (2002) 249-263
53. Sargent P.J., Farnaud S., and Evans R.W. Structure/function overview of proteins involved in iron storage and transport. Current Medicinal Chemistry 12 (2005) 2683-2693
54. Sharma S., Dimasi D., Broer S., Kumar R., and Della N.G. Heme carrier protein 1 (HCP1) expression and functional analysis in the retina and retinal pigment epithelium. Experimental Cell Research 313 (2007) 1251-1259
55. Shayeghi M., Latunde-Dada G.O., Oakhill J.S., Laftah A.H., Takeuchi K., Halliday N., Khan Y., Warley A., McCann F.E., Hider R.C., Frazer D.M., Anderson G.J., Vulpe C.D., Simpson R.J., and McKie A.T. Identification of an intestinal heme transporter. Cell 122 (2005) 789-801
56. Simonson C., Brener D., and DeVoe I.W. Expression of a high-affinity mechanism for acquisition of transferrin iron by Neisseria meningitides. Infection and Immunity 36 (1982) 107-113
57. Taketani S. Aquisition, mobilization and utilization of cellular iron and heme: endless findings and growing evidence of tight regulation. Tohoku Journal of Experimental Medicine 205 (2005) 297-318
58. Vinogradov S.N., Kosinski T.F., and Zak B. Complexometric determination of iron in heme proteins with 4-(2-pyridylazo) resorcinol. Analytic Biochemistry 120 (1982) 111-112
59. Wessling-Resnick M. Iron imports. III. Transfer of iron from the mucosa into circulation. American Journal of Physiology-Gastrointestinal and Liver Physiology 290 (2006) G1-G6
60. Winzerling J.J., and Pham D.Q. Iron metabolism in insect disease vectors: mining the Anopheles gambiae translated protein database. Insect Biochemistry and Molecular Biology 36 (2006) 310-321
61. Yoshiga T., Hernandez V.P., Fallon A.M., and Law J.H. Mosquito transferrin: an acute-phase protein that is upregulated upon infection. The Proceedings of the National Academy of Sciences in the United States of America 94 (1997) 12337-12342
62. Zak O., and Aisen P. Iron release from transferrin, its C-lobe, and their complexes with transferrin receptor: presence of N-lobe accelerates release from C-lobe at endosomal pH. Biochemistry 42 (2003) 12330-12334
63. Zhang D., Dimopoulos G., Wolf A., Minana B., Kafatos F.C., and Winzerling J.J. Cloning and molecular characterization of two mosquito iron regulatory proteins. Insect Biochemistry and Molecular Biology 32 (2002) 579-589
64. 14C]-labeled meal protein amino acids in Aedes aegypti mosquitoes. Journal of Insect Physiology 50 (2004) 337-349
65. Ziegler R., and Van Antwerpen R. Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology 36 (2006) 264-272