Iron loaded ferritin secretion and inhibition by CI-976 in Aedes aegypti larval cells

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 152, Issue 4, 2009, Pages 352-363

  Geiser, Dawn L ^a   Shen, Meng Chieh ^a   Mayo, Jonathan J ^a   Winzerling, Joy J ^a  

^a Environmental Research Laboratory   (United States)

Author keywords

Aedes aegypti; CI 976; Ferritin; Iron; Mosquito; Secretion

Indexed keywords

2,2 DIMETHYL N (2,4,6 TRIMETHOXYPHENYL)DODECANAMIDE; ACYLTRANSFERASE; CERAMIDE; FERRITIN; IRON; LYSOPHOSPHOLIPID;

AEDES AEGYPTI; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; IRON TRANSPORT; LARVA; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AEDES AEGYPTI; DIPTERA; MAMMALIA;

EID: 60649099959     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2009.01.002     Document Type: Article

References (77)

1. Adams P.C., and Chau L.A. Hepatic ferritin uptake and hepatic iron. Hepatology 11 (1990) 805-808
2. Aisen P. Ferritin receptors and the role of ferritin in iron transport. Targeted Diagn. Ther. 4 (1991) 339-354
3. Ali A., Zhang Q., Dai J., and Huang X. Calcein as a fluorescent iron chemosensor for the determination of low molecular weight iron in biological fluids. BioMetals 16 (2003) 285-293
4. Ausubel F., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., and Stuhl K. Current Protocols in Molecular Biology (1998), John Wiley and Sons, Inc, New York
5. Balla J., Vercellotti G.M., Jeney V., Yachie A., Varga Z., Jacob H.S., Eaton J.W., and Balla G. Heme, heme oxygenase, and ferritin: how the vascular endothelium survives (and dies) in an iron-rich environment. Antioxid. Redox Signal. 9 (2007) 2119-2137
6. Beard J.L., Murray-Kolb L.E., Rosales F.J., Solomons N.W., and Angelilli M.L. Interpretation of serum ferritin concentrations as indicators of total-body iron stores in survey populations: the role of biomarkers for the acute phase response. Am. J. Clin. Nutr. 84 (2006) 1498-1505
7. Bou-Abdallah F., Zhao G., Mayne H.R., Arosio P., and Chasteen N.D. Origin of the unusual kinetics of iron deposition in human H-chain ferritin. J. Am. Chem. Soc. 127 (2005) 3885-3893
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
9. Bresgen N., Ohlenschlager I., Fiedler B., Wacht N., Zach S., Dunkelmann B., Arosio P., Kuffner E., Lottspeich F., and Eckl P.M. Ferritin-a mediator of apoptosis?. J. Cell. Physiol. 212 (2007) 157-164
10. Brown W.J., and Schmidt J.A. Use of acyltransferase inhibitors to block vesicular traffic between the ER and Golgi complex. Methods Enzymol. 404 (2005) 115-125
11. Brown W.J., Plutner H., Drecktrah D., Judson B.L., and Balch W.E. The lysophospholipid acyltransferase antagonist CI-976 inhibits a late step in COPII vesicle budding. Traffic 9 (2008) 786-797
12. Celis J.E. Cell Biology: a Laboratory Handbook (1998), Academic Press, San Diego
13. Chambers K., and Brown W.J. Characterization of a novel CI-976-sensitive lysophospholipid acyltransferase that is associated with the Golgi complex. Biochem. Biophys. Res. Commun. 313 (2004) 681-686
14. Chambers K., Judson B., and Brown W.J. A unique lysophospholipid acyltransferase (LPAT) antagonist, CI-976, affects secretory and endocytic membrane trafficking pathways. J. Cell Sci. 118 (2005) 3061-3071
15. Chasteen N.D., and Harrison P.M. Mineralization in ferritin: an efficient means of iron storage. J. Struct. Biol. 126 (1999) 182-194
16. Colbourne J.K., Eads B.D., Shaw J., Bohuski E., Bauer D.J., and Andrews J. Sampling Daphnia's expressed genes: preservation, expansion and invention of crustacean genes with reference to insect genomes. BMC Genomics 8 (2007) 217
17. Collins T.J. ImageJ for microscopy. Biotechniques 43 (2007) 25-30
18. Cooper M.S., D'Amico L.A., and Henry C.A. Confocal microscopic analysis of morphogenetic movements. Methods Cell Biol. 59 (1999) 179-204
19. De Domenico I., Vaughn M.B., Li L., Bagley D., Musci G., Ward D.M., and Kaplan J. Ferroportin-mediated mobilization of ferritin iron precedes ferritin degradation by the proteasome. EMBO J. 25 (2006) 5396-5404
20. De Zoysa M., and Lee J. Two ferritin subunits from disk abalone (Haliotis discus discus): cloning, characterization and expression analysis. Fish Shellfish Immunol. 23 (2007) 624-635
21. Dinter A., and Berger E.G. Golgi-disturbing agents. Histochem. Cell Biol. 109 (1998) 571-590
22. Donaldson J.G., Honda A., and Weigert R. Multiple activities for Arf1 at the Golgi complex. Biochim. Biophys. Acta 1744 (2005) 364-373
23. Drecktrah D., Chambers K., Racoosin E.L., Cluett E.B., Gucwa A., Jackson B., and Brown W.J. Inhibition of a Golgi complex lysophospholipid acyltransferase induces membrane tubule formation and retrograde trafficking. Mol. Biol. Cell 14 (2003) 3459-3469
24. Dunkov B., and Georgieva T. Insect iron binding proteins: insights from the genomes. Insect Biochem. Mol. Biol. 36 (2006) 300-309
25. 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. Arch. Insect Biochem. Physiol. 29 (1995) 293-307
26. 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. J. Insect Sci. 2 (2002) 7-17
27. Dunn L.L., Rahmanto Y.S., and Richardson D.R. Iron uptake and metabolism in the new millennium. Trends Cell Biol. 17 (2007) 93-100
28. Edmunds M.W. Mosquito-borne infectious diseases: an update for clinicians. 2005 American College of Nurse Practitioners National Clinical Conference, Palm Springs, CA (2005)
29. Ferreira C., Bucchini D., Martin M.-E., Levi S., and Arosio P. Early embryonic lethality of H ferritin gene deletion in mice. J. Biol. Chem. 275 (2000) 3021-3024
30. Geiser D.L., Chavez C.A., Flores-Munguia R.F., Winzerling J.J., and Pham D.Q. Aedes aegypti ferritin: a cytotoxic protector against iron and oxidative challenge?. Eur. J. Biochem. 270 (2003) 1-8
31. Geiser D.L., Zhang D., and Winzerling J.J. Secreted ferritin: mosquito defense against iron overload?. Insect Biochem. Mol. Biol. 36 (2006) 177-187
32. Geiser D.L., Mayo J.J., and Winzerling J.J. The unique regulation of Aedes aegypti larval cell ferritin by iron. Insect Biochem. Mol. Biol. 37 (2007) 418-429
33. Ghosh S., Hevi S., and Chuck S.L. Regulated secretion of glycosylated human ferritin from hepatocytes. Blood 103 (2004) 2369-2376
34. Hamburger A.E., West A.P.J., Hamburger Z.A., Hamburger P., and Bjorkman P.J. Crystal structure of a secreted insect ferritin reveals a symmetrical arrangement of heavy and light chains. J. Mol. Biol. 349 (2005) 558-569
35. Hentze M.W., Muckenthaler M.U., and Andrews N.C. Balancing acts: molecular control of mammalian iron metabolism. Cell 117 (2004) 285-297
36. Huebers H.A., Huebers E., Finch C., Webb B.A., Truman J.W., Riddiford L.M., Martin A.W., and Massover W.H. Iron binding proteins and their roles in the tobacco hornworm Manduca sexta (L). J. Comp. Physiol., B. Biochem. Syst. Environ. Physiol. 158 (1988) 291-300
37. Jacob, M., 2001. Scientists target return of infectious diseases. GenetEngin News 21, 11-80.
38. Kidane T.Z., Sauble E., and Linder M.C. Release of iron from ferritin requires lysosomal activity. Am. J. Physiol., Cell Physiol. 291 (2006) C445-C455
39. Koorts A.M., and Viljoen M. Ferritin and ferritin isoforms I: structure-function relationships, synthesis, degradation and secretion. Arch. Physiol. Biochem. 113 (2007) 30-54
40. Koorts A.M., and Viljoen M. Ferritin and ferritin isoforms II: protection against uncontrolled cellular proliferation, oxidative damage and inflammatory processes. Arch. Physiol. Biochem. 113 (2007) 55-64
41. Kuromi H., and Kidokoro Y. Exocytosis and endocytosis of synaptic vesicles and functional roles of vesicle pools: lessons from the Drosophila neuromuscular junction. Neuroscientist 11 (2005) 138-147
42. Levi S., Cozzi A., and Arosio P. Neuroferritinopathy: a neurodegenerative disorder associated with L-ferritin mutation. Best Pract. Res. Clin. Haematol. 18 (2005) 265-276
43. Li M., Saren G., and Zhang S. Identification and expression of a ferritin homolog in amphioxus Branchiostoma belcheri: evidence for its dual role in immune response and iron metabolism. Comp. Biochem. Physiol. B 150 (2008) 263-270
44. Locke M. Surface membranes, Golgi complexes, and vacuolar systems. Annu. Rev. Entomol. 48 (2003) 1-27
45. MacKenzie E.L., Iwasaki K., and Tsuji Y. Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid. Redox Signal. 10 (2008) 997-1030
46. Markwell M.A., Haas S.M., Bieber L.L., and Tolbert N.E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87 (1978) 206-210
47. Missirlis F., Holmberg S., Georgieva T., Dunkov B.C., Rouault T.A., and Law J.H. Characterization of mitochondrial ferritin in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 5893-5898
48. Missirlis F., Kosmidis S., Brody T., Mavrakis M., Holmberg S., Odenwald W.F., Skoulakis E.M., and Rouault T.A. Homeostatic mechanisms for iron storage revealed by genetic manipulations and live imaging of Drosophila ferritin. Genetics 177 (2007) 89-100
49. Nichol H., Law J.H., and Winzerling J.J. Iron metabolism in insects. Annu. Rev. Entomol. 47 (2002) 535-559
50. Ong S.T., Ho J.Z., Ho B., and Ding J.L. Iron-withholding strategy in innate immunity. Immunobiology 211 (2006) 295-314
51. Osterloh K., and Aisen P. Pathways in the binding and uptake of ferritin by hepatocytes. Biochim. Biophys. Acta 1011 (1989) 40-45
52. Pagano R.E., Martin O.C., Kang H.C., and Haugland R.P. A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J. Cell Biol. 113 (1991) 1267-1279
53. Paskewitz S.M., and Shi L. The hemolymph proteome of Anopheles gambiae. Insect Biochem. Mol. Biol. 35 (2005) 815-824
54. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
55. Pham D.Q., and Chavez C.A. The ferritin light-chain homologue promoter in Aedes aegypti. Insect Mol. Biol. 14 (2005) 263-270
56. Pham D.Q.-D., 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 Biochem. Mol. Biol. 33 (2003) 51-62
57. 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 Mol. Biol. 14 (2005) 223-236
58. Qiu G.F., Zheng L., and Liu P. Transcriptional regulation of ferritin mRNA levels by iron in the freshwater giant prawn, Macrobrachium rosenbergii. Comp. Biochem. Physiol. B 150 (2008) 320-325
59. Ramm G.A., Powell L.W., and Halliday J.W. Pathways of intracellular trafficking and release of ferritin by the liver in vivo: the effect of chloroquine and cytochalasin D. Hepatology 19 (1994) 504-513
60. Recalcati S., Invernizzi P., Arosio P., and Cairo G. New functions for an iron storage protein: the role of ferritin in immunity and autoimmunity. J. Autoimmun. 30 (2008) 84-89
61. Richardson D., and Baker E. Two mechanisms of iron uptake from transferrin by melanoma cells. J. Biol. Chem. 267 (1992) 13972-13979
62. Sammarco M.C., Ditch S., Banerjee A., and Grabczyk E. Ferritin L and H subunits are differentially regulated on a post-transcriptional level. J. Biol. Chem. 283 (2008) 4578-4587
63. Santambrogio P., Biasiotto G., Sanvito F., Olivieri S., Arosio P., and Levi S. Mitochondrial ferritin expression in adult mouse tissues. J. Histochem. Cytochem. 55 (2007) 1129-1137
64. Strickler-Dinglasan P.M., Guz N., Attardo G., and Aksoy S. Molecular characterization of iron binding proteins from Glossina morsitans morsitans (Diptera: Glossinidae). Insect Biochem. Mol. Biol. 36 (2006) 921-933
65. Surguladze N., Patton S., Cozzi A., Fried M.G., and Connor J.R. Characterization of nuclear ferritin and mechanism of translocation. Biochem. J. 388 (2005) 731-740
66. Tang B.L., Wang Y., Ong Y.S., and Hong W. COPII and exit from the endoplasmic reticulum. Biochim. Biophys. Acta 1744 (2005) 293-303
67. Tatur J., Hagen W.R., and Matias P.M. Crystal structure of the ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus. J. Biol. Inorg. Chem. 12 (2007) 615-630
68. Tenopoulou M., Kurz T., Doulias P.T., Galaris D., and Brunk U.T. Does the calcein-AM method assay the total cellular 'labile iron pool' or only a fraction of it?. Biochem. J. 403 (2007) 261-266
69. Theil E.C., Matzapetakis M., and Liu X. Ferritins: iron/oxygen biominerals in protein nanocages. J. Biol. Inorg. Chem. 11 (2006) 803-810
70. Thompson K., Menzies S., Muckenthaler M., Torti F.M., Wood T., Torti S.V., Hentze M.W., Beard J., and Connor J. Mouse brains deficient in H-ferritin have normal iron concentration but a protein profile of iron deficiency and increased evidence of oxidative stress. J. Neurosci. Res. 71 (2003) 46-63
71. Tran T.N., Eubanks S.K., Schaffer K.J., Zhou C.Y., and Linder M.C. Secretion of ferritin by rat hepatoma cells and its regulation by inflammatory cytokines and iron. Blood 90 (1997) 4979-4986
72. Vidal R., Miravalle L., Gao X., Barbeito A.G., Baraibar M.A., Hekmatyar S.K., Widel M., Bansal N., Delisle M.B., and Ghetti B. Expression of a mutant form of the ferritin light chain gene induces neurodegeneration and iron overload in transgenic mice. J. Neurosci. 28 (2008) 60-67
73. Vierstraete E., Verleyen P., Baggerman G., D'Hertog W., Van den Bergh G., Arckens L., De Loof A., and Schoofs L. A proteomic approach for the analysis of instantly released wound and immune proteins in Drosophila melanogaster hemolymph. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 470-475
74. Winzerling J.J., and Pham D.Q. Iron metabolism in insect disease vectors: mining the Anopheles gambiae translated protein database. Insect Biochem. Mol. Biol. 36 (2006) 310-321
75. Worwood M., Dawkins S., Wagstaff M., and Jacobs A. The purification and properties of ferritin from human serum. Biochem. J. 157 (1976) 97-103
76. Yamanishi H., Kimura S., Hata N., Iyama S., Kanakura Y., and Iwatani Y. Evaluation of a model of latent pathologic factors in relation to serum ferritin elevation. Clin. Biochem. 40 (2007) 359-364
77. Zhou G., Kohlhepp P., Geiser D., Frasquillo Mdel C., Vazquez-Moreno L., and Winzerling J.J. Fate of blood meal iron in mosquitoes. J. Insect Physiol. 53 (2007) 1169-1178