Identification and analysis of a Scophthalmus maximus ferritin that is regulated at transcription level by oxidative stress and bacterial infection

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 156, Issue 3, 2010, Pages 222-228

  Zheng, Wen jiang ^a,b   Hu, Yong hua ^a   Sun, Li ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Ferritin; Iron; Oxidative stress; Scophthalmus maximus

Indexed keywords

CERULOPLASMIN; COMPLEMENTARY DNA; FERRITIN; FERRITIN M; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; COMPUTER MODEL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA SEQUENCE; IRON BINDING CAPACITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION; TURBOT; UPREGULATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA; SCOPHTHALMIDAE; SCOPHTHALMUS MAXIMUS;

EID: 77953124293     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.03.012     Document Type: Article

References (49)

1. Andersen O., Dehli A., Standal H., Giskegjerde T.A., Karstensen R., Roervik K.A. Two ferritin subunits of Atlantic salmon (Salmo salar): cloning of the liver cDNAs and antibody preparation. Mol. Mar. Biol. Biotechnol. 1995, 4:164-170.
2. Andersen O., Pantopoulos K., Kao H.T., Muckenthaler M., Youson J.H., Pieribone V. Regulation of iron metabolism in the sanguivore lamprey Lampetra fluviatilis-molecular cloning of two ferritin subunits and two iron-regulatory proteins (IRP) reveals evolutionary conservation of the iron-regulatory element (IRE)/IRP regulatory system. Eur. J. Biochem. 1998, 254:223-229.
3. Andrews S.C., Arosio P., Bottke W., Briat J.F., Darl M., Harrison P.M., Laulhere J.P., Levi S., Lobreaux S., Yewdall S.J. Structure, function, and evolution of ferritins. J. Inorg. Biochem. 1992, 47:161-174.
4. Arosio P., Ingrassia R., Cavadini P. Ferritins: a family of molecules for iron storage, antioxidation and more. Biochim. Biophys. Acta 2009, 1790:589-599.
5. Bou-Abdallah F., Papaefthymiou G.C., Scheswohl D.M., Stanga S.D., Arosio P., Chasteen N.D. mu-1, 2-Peroxobridged di-iron (III) dimer formation in human H-chain ferritin. Biochem. J. 2002, 364:57-63.
6. Briat J.F., Lobreaux S., Grignon N., Vansuyt G. Regulation of plant ferritin synthesis: how and why. Cell. Mol. Life Sci. 1999, 56:155-166.
7. Cairo G., Bardella L., Schiaffonati L., Arosio P., Levi S., Bernelli-Zazzera A. Multiple mechanisms of iron-induced ferritin synthesis in HeLa cells. Biochem. Biophys. Res. Commun. 1985, 133:314-321.
8. Cairo G., Rappocciolo E., Tacchini L., Schiaffonati L. Expression of the genes for the ferritin H and L subunits in rat liver and heart. Evidence for tissue-specific regulations at pre- and post-translational levels. Biochem. J. 1991, 275:813-816.
9. Cozzi A., Corsi B., Levi S., Santambrogio P., Albertini A., Arosio P. Overexpression of wild type and mutated human ferritin H-chain in HeLa cells. In vivo role of ferritin ferroxidase activity. J. Biol. Chem. 2000, 275:25122-25129.
10. Cozzi A., Corsi B., Levi S., Santambrogio P., Biasiotto G., Arosio P. Analysis of the biologic functions of H- and L-ferritins in HeLa cells by transfection with siRNAs and cDNAs: evidence for a proliferative role of L-ferritin. Blood 2004, 103:2377-2383.
11. De Zoysa M., Lee J. Two ferritin subunits from disk abalone (Haliotis discus discus): cloning, characterization and expression analysis. Fish Shellfish Immunol. 2007, 23:624-635.
12. Dickey L.F., Sreedharan S., Theil E.C., Didsbury J.R., Wang Y.H., Kaufman R.E. Differences in the regulation of messenger RNA for housekeeping and specialized-cell ferritin. J. Biol. Chem. 1987, 262:7901-7907.
13. Epsztejn S., Glickstein H., Picard V., Slotki I.N., Breuer W., Beaumont C., Cabantchik Z.I. H-ferritin subunit overexpression in erythroid cells reduces the oxidative stress response and induces multidrug resistance properties. Blood 1999, 94:3593-3603.
14. Feng C.Y., Johnson S.C., Hori T.S., Rise M., Hall J.R., Gamperl A.K., Hubert S., Kimball J., Bowman S., Rise M.L. Identification and analysis of differentially expressed genes in immune tissues of Atlantic cod stimulated with formalin-killed, atypical Aeromonas salmonicida. Physiol. Genomics 2009, 37:149-163.
15. Giorgi A., Mignogna G., Bellapadrona G., Gattoni M., Chiaraluce R., Consalvi V., Chiancone E., Stefanini S. The unusual co-assembly of H- and M-chains in the ferritin molecule from the Antarctic teleosts Trematomus bernacchii and Trematomus newnesi. Arch. Biochem. Biophys. 2008, 478:69-74.
16. Harrison P.M., Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1996, 1275:161-203.
17. Hentze M.W., Kühn L.C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:8175-8182.
18. Hentze M.W., Rouault T.A., Harford J.B., Klausner R.D. Oxidation-reduction and the molecular mechanism of a regulatory RNA-protein interaction. Science 1989, 244:357-359.
19. Hintze K.J., Theil E.C. Cellular regulation and molecular interactions of the ferritins. Cell. Mol. Life Sci. 2006, 63:591-600.
20. Jiao X., Zhang M., Hu Y., Sun L. Construction and evaluation of DNA vaccines encoding Edwardsiella tarda antigens. Vaccine 2009, 27:5195-5202.
21. Kanner J., Doll L. Ferritin in turkey muscle tissue: a source of catalytic iron ions for lipid peroxidation?. J. Agric. Food Chem. 1991, 39:247-249.
22. Knovich M.A., Storey J.A., Coffman L.G., Torti S.V., Torti F.M. Ferritin for the clinician. Blood Rev. 2009, 23:95-104.
23. Kozak M. An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987, 15:8125-8148.
24. Lawson D.M., Artymiuk P.J., Yewdall S.J., Smith J.M.A., Livingstone J.C., Treffry A., Luzzago A., Levi S., Arosio P., Cesareni G. Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts. Nature 1991, 349:541-544.
25. Leggett B.A., Fletcher L.M., Ramm G.A., Powell L.W., Halliday J.W. Differential regulation of ferritin H and L subunit mRNA during inflammation and long-term iron overload. J. Gastroenterol. Hepatol. 1993, 8:21-27.
26. Levi S., Luzzago A., Cesareni G., Cozzi A., Franceschinelli F., Albertini A., Arosio P. Mechanism of ferritin iron uptake: activity of the H-chain and deletion mapping of the ferro-oxidase site. A study of iron uptake and ferro-oxidase activity of human liver, recombinant H-chain ferritins, and of two H-chain deletion mutants. J. Biol. Chem. 1988, 263:18086-18092.
27. Levi S., Santambrogio P., Cozzi A., Rovida E., Corsi B., Tamborini E., Spada S., Albertini A., Arosio P. The role of the L-chain in ferritin iron incorporation: studies of homo and heteropolymers. J. Mol. Biol. 1994, 238:649-654.
28. Mignogna G., Chiaraluce R., Consalvi V., Cavallo S., Stefanini S., Chiancone E. Ferritin from the spleen of the Antarctic teleost Trematomus bernacchii is an M-type homopolymer. Eur. J. Biochem. 2002, 269:1600-1606.
29. Muckenthaler M., Richter A., Gunkel N., Riedel D., Polycarpou-Schwarz M., Hentze S., Falkenhahn M., Stremmel W., Ansorge W., Hentze M.W. Relationships and distinctions in iron-regulatory networks responding to interrelated signals. Blood 2003, 101:3690-3698.
30. Muller J.P., Vedel M., Monnot M.J., Touzet N., Wegnez M. Molecular cloning and expression of ferritin mRNA in heavy metal-poisoned Xenopus laevis cells. DNA Cell Biol. 1991, 10:571-579.
31. Neves J.V., Wilson J.M., Rodrigues P.N.S. Transferrin and ferritin response to bacterial infection: the role of the liver and brain in fish. Dev. Comp. Immunol. 2009, 33:848-857.
32. Orino K., Watanabe K. Molecular, physiological and clinical aspects of the iron storage protein ferritin. Vet. J. 2008, 178:191-201.
33. Peatman E., Baoprasertkul P., Terhune J., Xu P., Nandi S., Kucuktas H., Li P., Wang S., Somridhivej B., Dunham R. Expression analysis of the acute phase response in channel catfish (Ictalurus punctatus) after infection with a Gram-negative bacterium. Dev. Comp. Immunol. 2007, 31:1183-1196.
34. Prieto-álamo M.J., Abril N., Osuna-Jiménez I., Pueyo C. Solea senegalensis genes responding to lipopolysaccharide and copper sulphate challenges: large-scale identification by suppression subtractive hybridization and absolute quantification of transcriptional profiles by real-time RT-PCR. Aquat. Toxicol. 2009, 91:31231-31239.
35. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor, NY. 2nd ed.
36. Santambrogio P., Levi S., Arosio P., Palagi L., Vecchio G., Lawson D.M., Yewdall S.J., Artymiuk P.J., Harrison P.M., Jappelli R. Evidence that a salt bridge in the light chain contributes to the physical stability difference between heavy and light human ferritins. J. Biol. Chem. 1992, 267:14077-14083.
37. Santambrogio P., Levi S., Cozzi A., Rovida E., Albertini A., Arosio P. Production and characterization of recombinant heteropolymers of human ferritin H and L chains. J. Biol. Chem. 1993, 268:12744-12748.
38. Santambrogio P., Levi S., Cozzi A., Corsi B., Arosio P. Evidence that the specificity of iron incorporation into homopolymers of human ferritin L- and H-chains is conferred by the nucleation and ferroxidase centres. Biochem. J. 1996, 314:139-144.
39. Schmid A., Kloas W., Reinecke M. Establishment of a primary liver cell culture from a teleost, Oreochromis mossambicus, the tilapia: a valid tool for physiological studies. Animal Cell Technology: Products from Cells, Cells as Products 1999, 143-145. Springer, Netherlands. A. Bernard, B. Griffiths, W. Noé, F. Wurm (Eds.).
40. Scudiero R., Trinchella F., Riggio M., Parisi E. Structure and expression of genes involved in transport and storage of iron in red-blooded and hemoglobin-less Antarctic notothenioids. Gene 2007, 397:1-11.
41. Theil E.C., Eisenstein R.S. Combinatorial mRNA regulation: iron regulatory proteins and iso-iron-responsive elements (Iso-IREs). J. Biol. Chem. 2000, 275:40659-40662.
42. Tsuji Y., Ayaki H., Whitman S.P., Morrow C.S., Torti S.V., Torti F.M. Coordinate transcriptional and translational regulation of ferritin in response to oxidative stress. Mol. Cell. Biol. 2000, 20:5818-5827.
43. Ulvik R.J. Relevance of ferritin-binding sites on isolated mitochondria to the mobilization of iron from ferritin. Biochim. Biophys. Acta 1982, 715:42-51.
44. White K., Munro H.N. Induction of ferritin subunit synthesis by iron is regulated at both the transcriptional and translational levels. J. Biol. Chem. 1988, 263:8938-8942.
45. Zhang W.W., Sun L. Cloning, characterization, and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl. Environ. Microbiol. 2007, 73:2825-2831.
46. Zhang M., Sun K., Sun L. Regulation of autoinducer 2 production and luxS expression in a pathogenic Edwardsiella tarda strain. Microbiology 2008, 154:2060-2069.
47. Zhang W.W., Sun K., Cheng S., Sun L. Characterization of DegQVh, a serine protease and a protective immunogen from a pathogenic Vibrio harveyi strain. Appl. Environ. Microbiol. 2008, 74:6254-6262.
48. Zhao G., Ceci P., Ilari A., Giangiacomo L., Laue T.M., Chiancone E., Chasteen N.D. Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J. Biol. Chem. 2002, 277:27689-27696.
49. Zhao G., Bou-Abdallah F., Arosio P., Levi S., Janus-Chandler C., Chasteen N.D. Multiple pathways for mineral core formation in mammalian apoferritin. The role of hydrogen peroxide. Biochemistry 2003, 42:3142-3150.