MIF from mussel: Coding sequence, phylogeny, polymorphism, 3D model and regulation of expression

Developmental and Comparative Immunology

Volumn 36, Issue 4, 2012, Pages 688-696

  Parisi, Maria Giovanna ^a   Toubiana, Mylène ^b   Mangano, Valentina ^a   Parrinello, Nicolò ^a   Cammarata, Matteo ^a   Roch, Philippe ^b  

^a UNIVERSITY OF PALERMO   (Italy)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Bacteria; Bivalve; Challenge; Cytokine; Fungus; Gene regulation; Innate immunity; Macrophage; Mollusk; Mytilus; Q PCR

Indexed keywords

ISOMERASE; MACROPHAGE MIGRATION INHIBITION FACTOR; OXIDOREDUCTASE; TAUTOMERASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ABALONE; ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOMPHALARIA GLABRATA; BLOOD CELL; CANDIDA ALBICANS; CARBOXY TERMINAL SEQUENCE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EXPRESSED SEQUENCE TAG; FUSARIUM OXYSPORUM; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; ITALY; LISTONELLA ANGUILLARUM; MICROCOCCUS LUTEUS; MIF GENE; MOLECULAR WEIGHT; MUSSEL; MYTILUS GALLOPROVINCIALIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PINCTADA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; VIBRIO; VIBRIO SPLENDIDUS;

ANIMALIA; BIOMPHALARIA GLABRATA; BIVALVIA; CANDIDA ALBICANS; CHLAMYS FARRERI; FUNGI; HALIOTIS; IXODIDA; MYTILUS; MYTILUS GALLOPROVINCIALIS; PINCTADA FUCATA; VERTEBRATA;

EID: 84856469016     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.10.014     Document Type: Article

References (58)

1. Abe R., Peng T., Sailors J., Bucala R., Metz C.N. Regulation of the CTL response by macrophage migration inhibitory factor. J. Immunol. 2001, 166:747-753.
2. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
3. Bacher M., Meinhardt A., Lan H.Y., Dhabhar F.S., Mu W., Metz C.N., Chesney J.A., Gemsa D., Donnelly T., Atkins R.C., Bucala R. MIF expression in the rat brain: implications for neuronal function. Mol. Med. 1998, 4:217-230.
4. Baeza Garcia A., Pierce R.J., Gourbal B., Werkmeister E., Colinet D., Reichhart J.M., Dissous C., Coustau C. Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog. 2010, 6.
5. Benigni F., Atsumi T., Calandra T., Metz C., Echtenacher B., Peng T., Bucala R. The proinflammatory mediator macrophage migration inhibitory factor induces glucose catabolism in muscle. J. Clin. Invest. 2000, 106:1291-1300.
6. Beschin A., Bilej M., Torreele E., De Baetselier P. On the existence of cytokines in invertebrates. Cell. Mol. Life Sci. 2001, 58:801-814.
7. Bowen C.J., Jaworski D.C., Wasala N.B., Coons L.B. Macrophage migration inhibitory factor expression and protein localization in Amblyomma americanum (Ixodidae). Exp. Appl. Acarol. 2010, 50:343-352.
8. Calandra T., Echtenacher B., Roy D.L., Pugin J., Metz C.N., Hultner L., Heumann D., Mannel D., Bucala R., Glauser M.P. Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat. Med. 2000, 6:164-170.
9. Canesi L., Betti M., Ciacci C., Lorusso L.C., Pruzzo C., Gallo G. Cell signaling in the immune response of mussel hemocytes. Invert. Survey J. 2006, 3:40-49.
10. Cellura C., Toubiana M., Parrinello N., Roch P. Specific expression of antimicrobial peptide and HSP70 genes in response to heat-shock and several bacterial challenges in mussels. Fish Shellfish Immunol. 2007, 22:340-350.
11. Chaisavaneeyakorn S., Lucchi N., Abramowsky C., Othoro C., Chaiyaroj S.C., Shi Y.P., Nahlen B.L., Peterson D.S., Moore J.M., Udhayakumar V. Immunohistological characterization of macrophage migration inhibitory factor expression in Plasmodium falciparum-infected placentas. Infect. Immun. 2005, 73:3287-3293.
12. Costa M.M., Dios S., Alonso-Gutierrez J., Romero A., Novoa B., Figueras A. Evidence of high individual diversity on myticin C in mussel (Mytilus galloprovincialis). Dev. Comp. Immunol. 2009, 33:162-170.
13. Cui S., Zhang D., Jiang S., Pu H., Hu Y., Guo H., Chen M., Su T., Zhu C. A macrophage migration inhibitory factor like oxidoreductase from pearl oyster Pinctada fucata involved in innate immune responses. Fish Shellfish Immunol. 2011, 31:173-181.
14. del Vecchio M.T., Tripodi S.A., Arcuri F., Pergola L., Hako L., Vatti R., Cintorino M. Macrophage migration inhibitory factor in prostatic adenocarcinoma: correlation with tumor grading and combination endocrine treatment-related changes. Prostate 2000, 45:51-57.
15. Fingerle-Rowson G., Koch P., Bikoff R., Lin X., Metz C.N., Dhabhar F.S., Meinhardt A., Bucala R. Regulation of macrophage migration inhibitory factor expression by glucocorticoids in vivo. Am. J. Pathol. 2003, 162:47-56.
16. Flieger O., Engling A., Bucala R., Lue H., Nickel W., Bernhagen J. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett. 2003, 551:78-86.
17. Garcia J.S., Maldonado Junior A., Bidau C.J., Correa Ldos R., Lanfredi R.M., Coelho P.M. The effect of early infection with Echinostoma paraensei on the interaction of Schistosoma mansoni with Biomphalaria glabrata and Biomphalaria tenagophila. Mem. Inst. Oswaldo Cruz 2010, 105:499-503.
18. Gerdol M., Manfrin C., De Moro G., Figueras A., Novoa B., Venier P., Pallavicini A. The C1q domain containing proteins of the Mediterranean mussel Mytilus galloprovincialis: a widespread and diverse family of immune-related molecules. Dev. Comp. Immunol. 2011, 35:635-643.
19. Gestal C., Pallavicini A., Venier P., Novoa B., Figueras A. MgC1q, a novel C1q-domain-containing protein involved in the immune response of Mytilus galloprovincialis. Dev. Comp. Immunol. 2010, 34:926-934.
20. Gueguen Y., Cadoret J.P., Flament D., Barreau-Roumiguiere C., Girardot A.L., Garnier J., Hoareau A., Bachere E., Escoubas J.M. Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster, Crassostrea gigas. Gene 2003, 303:139-145.
21. Javeed A., Zhao Y., Zhao Y. Macrophage-migration inhibitory factor: role in inflammatory diseases and graft rejection. Inflamm. Res. 2008, 57:45-50.
22. Kibiki G.S., van der Ven A.J., Geurts-Moespot A., Shao J., Calandra T., Sweep F.C., Dolmans W.M. Serum and BAL macrophage migration inhibitory factor levels in HIV infected Tanzanians with pulmonary tuberculosis or other lung diseases. Clin. Immunol. 2007, 123:60-65.
23. Kleemann R., Kapurniotu A., Frank R.W., Gessner A., Mischke R., Flieger O., Juttner S., Brunner H., Bernhagen J. Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J. Mol. Biol. 1998, 280:85-102.
24. Lafuente L., Gregory W., Allen J., Maizels R. MIF homologues from a filarial nematode parasite synergize with IL-4 to induce alternative activation of host macrophages. J. Leukoc. Biol. 2009, 85.
25. Li F., Huang S., Wang L., Yang J., Zhang H., Qiu L., Li L., Song L. A macrophage migration inhibitory factor like gene from scallop Chlamys farreri: involvement in immune response and wound healing. Dev. Comp. Immunol. 2011, 35:62-71.
26. Li H., Parisi M.G., Toubiana M., Cammarata M., Roch P. Lysozyme gene expression and hemocyte behaviour in the Mediterranean mussel, Mytilus galloprovincialis, after injection of various bacteria or temperature stresses. Fish Shellfish Immunol. 2008, 25:143-152.
27. Li W.W., Jin X.K., He L., Wang Y., Chen L.L., Jiang H., Wang Q. Molecular cloning, characterization and expression analysis of macrophage migration inhibitory protein (MIF) in Chinese mitten crab, Eriocheir sinensis. Fish Shellfish Immunol. 2011, 30:324-329.
28. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
29. Mao Y., Xu B., Su Y., Zhang Z., Ding S., Wang D., Wang J. Cloning and mRNA expression of macrophage migration inhibitory factor (MIF) gene of large yellow croaker (Pseudosciaena crocea). Acta Oceanol. Sinica 2010, 29:63-73.
30. Mitta G., Galinier R., Tisseyre P., Allienne J.F., Girerd-Chambaz Y., Guillou F., Bouchut A., Coustau C. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev. Comp. Immunol. 2005, 29:393-407.
31. Oddo M., Calandra T., Bucala R., Meylan P.R. Macrophage migration inhibitory factor reduces the growth of virulent Mycobacterium tuberculosis in human macrophages. Infect. Immun. 2005, 73:3783-3786.
32. Onodera S., Suzuki K., Matsuno T., Kaneda K., Takagi M., Nishihira J. Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 1997, 92:131-137.
33. Ottaviani E. Molluscan immunorecognition. Invert. Survey J. 2006, 3:50-63.
34. Pallavicini A., Costa M.M., Gestal C., Dreos R., Figueras A., Venier P., Novoa B. High sequence variability of myticin transcripts in hemocytes of immune-stimulated mussels suggests ancient host-pathogen interactions. Dev. Comp. Immunol. 2008, 32:213-226.
35. Parisi M.G., Li H., Toubiana M., Parrinello N., Cammarata M., Roch P. Polymorphism of mytilin B mRNA is not translated into mature peptide. Mol. Immunol. 2009, 46:384-392.
36. Park E.M., Kim Y.O., Nam B.H., Kong H.J., Kim W.J., Lee S.J., Kong I.S., Choi T.J. Cloning, characterization and expression analysis of the gene for a putative lipopolysaccharide-induced TNF-alpha factor of the Pacific oyster, Crassostrea gigas. Fish Shellfish Immunol. 2008, 24:11-17.
37. Park H., Ahn I.Y., Kim H., Cheon J., Kim M. Analysis of ESTs and expression of two peroxiredoxins in the thermally stressed Antarctic bivalve Laternula elliptica. Fish Shellfish Immunol. 2008, 25:550-559.
38. Parrinello N., Vizzini A., Arizza V., Salerno G., Parrinello D., Cammarata M., Giaramita F.T., Vazzana M. Enhanced expression of a cloned and sequenced Ciona intestinalis TNFalpha-like (CiTNF alpha) gene during the LPS-induced inflammatory response. Cell Tissue Res. 2008, 334:305-317.
39. Pastrana D.V., Raghavan N., FitzGerald P., Eisinger S.W., Metz C., Bucala R., Schleimer R.P., Bickel C., Scott A.L. Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infect. Immun. 1998, 66:5955-5963.
40. Prieto-Lafuente L., Gregory W.F., Allen J.E., Maizels R.M. MIF homologues from a filarial nematode parasite synergize with IL-4 to induce alternative activation of host macrophages. J. Leukoc. Biol. 2009, 85:844-854.
41. Roberts S., Goetz G., White S., Goetz F. Analysis of genes isolated from plated hemocytes of the Pacific oyster, Crassostreas gigas. Mar. Biotechnol. (NY) 2009, 11:24-44.
42. Roberts S., Gueguen Y., de Lorgeril J., Goetz F. Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure. Dev. Comp. Immunol. 2008, 32:1099-1104.
43. Roger T., Ding X., Chanson A.L., Renner P., Calandra T. Regulation of constitutive and microbial pathogen-induced human macrophage migration inhibitory factor (MIF) gene expression. Eur. J. Immunol. 2007, 37:3509-3521.
44. Roger T., Froidevaux C., Martin C., Calandra T. Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of Toll-like receptor 4 (TLR4). J. Endotoxin Res. 2003, 9:119-123.
45. Romero A., Dios S., Poisa-Beiro L., Costa M.M., Posada D., Figueras A., Novoa B. Individual sequence variability and functional activities of fibrinogen-related proteins (FREPs) in the Mediterranean mussel (Mytilus galloprovincialis) suggest ancient and complex immune recognition models in invertebrates. Dev. Comp. Immunol. 2011, 35:334-344.
46. Song L., Xu W., Li C., Li H., Wu L., Xiang J., Guo X. Development of expressed sequence tags from the Bay Scallop, Argopecten irradians irradians. Mar. Biotechnol. (NY) 2006, 8:161-169.
47. Sonthi, M., Toubiana, M., Pallavicini, A., Venier, P., Roch, P., 2011. Diversity of coding sequences and gene structures of the antifungal peptide mytimycin (MytM) from the Mediterranean mussel, Mytilus galloprovincialis. Mar. Biotechnol. (NY).
48. Sun H.W., Bernhagen J., Bucala R., Lolis E. Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc. Natl. Acad. Sci. USA 1996, 93:5191-5196.
49. Swope M.D., Lolis E. Macrophage migration inhibitory factor: cytokine, hormone, or enzyme?. Rev. Physiol. Biochem. Pharmacol. 1999, 139:1-32.
50. Torreilles J., Guérin M.-C., Roch P. Modified Alsever's solution is not a good medium for reactive oxygen metabolite study in bivalves. Fish Shellfish Immunol. 1999, 8:65-69.
51. Umemiya R., Hatta T., Liao M., Tanaka M., Zhou J., Inoue N., Fujisaki K. Haemaphysalis longicornis: molecular characterization of a homologue of the macrophage migration inhibitory factor from the partially fed ticks. Exp. Parasitol. 2007, 115:135-142.
52. Venier P., De Pitta C., Bernante F., Varotto L., De Nardi B., Bovo G., Roch P., Novoa B., Figueras A., Pallavicini A., Lanfranchi G. MytiBase: a knowledgebase of mussel (M. galloprovincialis) transcribed sequences. BMC Genomics 2009, 10:72.
53. Venier P., Pallavicini A., De Nardi B., Lanfranchi G. Towards a catalogue of genes transcribed in multiple tissues of Mytilus galloprovincialis. Gene 2003, 314:29-40.
54. Venier P., Varotto L., Rosani U., Millino C., Celegato B., Bernante F., Lanfranchi G., Novoa B., Roch P., Figueras A., Pallavicini A. Insights into the innate immunity of the Mediterranean mussel Mytilus galloprovincialis. BMC Genomics 2011, 12:69.
55. Wang B., Zhang Z., Wang Y., Zou Z., Wang G., Wang S., Jia X., Lin P. Molecular cloning and characterization of macrophage migration inhibitory factor from small abalone Haliotis diversicolor supertexta. Fish Shellfish Immunol. 2009, 27:57-64.
56. Wang L., Song L., Zhao J., Qiu L., Zhang H., Xu W., Li H., Li C., Wu L., Guo X. Expressed sequence tags from the zhikong scallop (Chlamys farreri): discovery and annotation of host-defense genes. Fish Shellfish Immunol. 2009, 26:744-750.
57. Wu Z., Boonmars T., Nagano I., Nakada T., Takahashi Y. Molecular expression and characterization of a homologue of host cytokine macrophage migration inhibitory factor from Trichinella spp. J. Parasitol. 2003, 89:507-515.
58. Yu Y., Qiu L., Song L., Zhao J., Ni D., Zhang Y., Xu W. Molecular cloning and characterization of a putative lipopolysaccharide-induced TNF-alpha factor (LITAF) gene homologue from Zhikong scallop Chlamys farreri. Fish Shellfish Immunol. 2007, 23:419-429.