NMR characterization of structure, backbone dynamics, and glutathione binding of the human macrophage migration inhibitory factor (MIF)

Protein Science

Volumn 5, Issue 10, 1996, Pages 2095-2103

  Mühlhahn, Peter ^a   Bernhagen, Jürgen ^b   Czisch, Michael ^a   Georgescu, Julia ^a   Renner, Christian ^a   Ross, Alfred ^a   Bucala, Richard ^c   Holak, Tad A ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF STUTTGART   (Germany)

^c PICOWER INST FOR MEDICAL RESEARCH   (United States)

Author keywords

backbone dynamics; glutathione binding; human macrophage migration inhibitory factor; structure

Indexed keywords

GLUTATHIONE; MACROPHAGE MIGRATION INHIBITION FACTOR;

ANTIBODY SPECIFICITY; ARTICLE; CONFORMATIONAL TRANSITION; DISULFIDE BOND; ENDOTOXEMIA; MEDIATOR RELEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RECEPTOR AFFINITY; T LYMPHOCYTE ACTIVATION;

EID: 0029860105     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560051016     Document Type: Article

References (61)

1. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: The central helix is flexible. Biochemistry 31:5269-5278.
2. Bax A, Davis DG. 1985. MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J Magn Reson 65:355-360.
3. Bax A, Grzesiek S. 1993. Methodological advances in protein NMR. Acc Chem Res 26:131-138.
4. Bernhagen J, Bacher M, Calandra T, Metz CN, Doty S, Donnelly T, Bucala R. 1996. An essential role for macrophage migration inhibitory factor (MIF) in the delayed-type hypersensitivity reaction. J Exp Med 183:277-282.
5. Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R. 1993. MIF is a pituitary-derived cytokine that potentiates endotoxemia. Nature 365:756-759.
6. Bernhagen J, Kapurniotu A, Stoeva S, Voelter W, Bucala. 1995. Conformational and disulfide bond analysis of macrophage migration inhibitory factor (MIF). Peptides 1994:572-573.
7. Bernhagen J, Mitchell RA, Calandra T, Voelter W, Cerami A, Bucala R. 1994. Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF). Biochemistry 33: 14144-14155.
8. Bernstein R, Cieslar C, Ross A, Oschkinat H, Freund J, Holak TA. 1993. Computer-assisted assignment of multidimensional NMR spectra of proteins: Application to 3D NOESY-HMQC and TOCSY-HMQC spectra. J Biol NMR 3:245-251.
9. Blocki FA, Schlievert PM, Wackett LP. 1992. Rat liver protein linking chemical and immunological detoxification systems. Nature 360:269-270.
10. Bloom BR, Bennett B. 1966. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153:80-82.
11. Calandra T, Bernhagen J, Metz CN, Spiegel L, Bacher M, Donnelly T, Cerami A, Bucala R. 1995. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377:68-71.
12. Calandra T, Bernhagen J, Mitchell RA, Bucala R. 1994. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 179:1895-1902.
13. 1H spectroscopy. Biochemistry 29:321-338.
14. Cieslar C, Ross A, Zink T, Holak TA. 1993. Efficiency in multidimensional NMR by optimized recording of time point-phase pairs in evolution periods and their selective linear transformation. J Magn Reson Series B 101:97-101.
15. 1H NMR spectroscopy. Biochemistry 27:7387-7401.
16. Clore GM, Szabo A, Bax A, Kay LE, Driscoll PC, Gronenborn AM. 1990b. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J Am Chem Soc 112:4989-4991.
17. 15N NMR relaxation measurements. Protein Sci 3:855-862.
18. David J. 1966. Delayed hypersensitivity in vitro: Its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc Natl Acad Sci USA 56:72-77.
19. 15N NMR relaxation measurements with a molecular dynamics simulation: Backbone dynamics of the glucocorticoid receptor DNA-binding domain. Proteins Struct Funct Genet 17:375-390.
20. 15N NMR relaxation. Biochemistry 33:5984-6003.
21. Galat A, Riviere S, Bouet F. 1993. Purification of macrophage migration inhibitory factor (MIF) from bovine brain cytosol. FEBS Lett 319:233-236.
22. Grzesiek S, Bax A. 1992. Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J Magn Reson 96:432-440.
23. 15N-enriched proteins. J Biomol NMR 3:185-204.
24. Guèron M, Plateau P, Decorps M. 1991. Solvent signal suppression in NMR. Prog NMR Spectrosc 23:135-209.
25. Hoffman DW, Spicer LD. 1991. Isotopic labeling of specific amino acid types as an aid to NMR spectrum assignment of the methione repressor protein. In: Villafranca JJ, ed. Techniques in protein chemistry II. San Diego: Academic Press. pp 409-419.
26. 15N spectra of larger proteins. Heteronuclear triple resonance three dimensional NMR spectroscopy: Application to calmodulin. Biochemistry 29:4659-4667.
27. Jahnke W, Baur M, Gemmecker G, Kessler H. 1995a. Improved accuracy of NMR structures by a modified NOESY-HSQC experiment. J Magn Reson B106:86-88.
28. Jahnke W, Kessler H. 1995b. Modified triple-resonance NMR experiments with optimized sensitivity for rapidly exchanging protons. Angew Chem Int Ed Engl 34,4:469-471.
29. Jeener J, Meier BH, Bachman P, Ernst RR. 1979. Investigation of exchange processes by two-dimensional NMR spectroscopy. J Chem Phys 71:4546-4553.
30. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease. Biochemistry 28:8972-8979.
31. 2O samples of proteins. J Magn Reson B101:333-337.
32. Lanahan A, Williams JB, Sanders LK, Nathans D. 1992. Growth factor-induced delayed early response genes. Mol Cell Biol 12:3919-3929.
33. Lipari G, Szabo A. 1982a. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J Am Chem Soc 104:4546-4559.
34. Lipari G, Szabo A. 1982b. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J Am Chem Soc 104:4559-4570.
35. 1II spin-spin coupling constants in proteins. Biochem Biophys Res Commun 113:967-974.
36. Mitchell RA, Bacher M, Bernhagen J, Pushkarskaya T, Seldin M, Bucala R. 1995. Cloning and characterization of the gene for mouse MIF. J Immunol 154:3863-3870.
37. Mori S, Abeygunawardana C, Johnson MN, van Zijl PCM. 1995. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J Magn Reson B108:94-98.
38. Muchmore DC, McIntosh LP, Russell CB, Anderson DE, Dahlquist FW. 1989. Expression and nitrogen-15 labeling of proteins for proton and nitrogen-15 nuclear magnetic resonance. Methods in Enzymology 177:44-73.
39. Nishihara J, Kuriyama T, Nishino H, Ishibashi T, Sakai M, Nishi S. 1993. Purification and characterization of human macrophage migration inhibitory factor: Evidence for specific binding to glutathione and formation of subunit structure. Biochem Mol Biol Internat 31:841-850.
40. Nishihara J, Kuriyama T, Sakai M, Nishi S, Ohki S-Y, Hikichi K. 1995. The structure and physicochemical properties of rat liver macrophage migration inhibitory factor. Biochim Biophys Acta 1247:159-162.
41. Nishino T, Bernhagen J, Shiiki H, Calandra T, Dohi K, Bucala R. 1995. Localization of macrophage migration inhibitory factor (MIF) to secretory granules within the corticotrophic and thyrotrophic cells of the pituitary gland. Mol Medicine 1:781-788.
42. 15N spectroscopy. J Mag Reson 87:488-501.
43. Palmer AG, Cavanagh J, Byrd RA, Rance M. 1992. Sensitivity improvement in three-dimensional heteronuclear correlation NMR spectroscopy. J Magn Reson 96:415-424.
44. Pearson WR. 1994. MIF proteins are not glutathione transferase homologs. Protein Sci 3: 525-527.
45. Plateau P, Guèron M. 1982. Exchangeable proton NMR without base-line distortion using new strong-pulse sequences. J Am Chem Soc 104:7310-7311.
46. 15N-enriched proteins using constant-time evolution. J Magn Reson 94:209-213.
47. 15N NMR relaxation measurement on human interleukin-4. Biochemistry 31:10431-10437.
48. Rosengren E, Bucala R, Åman P, Jacobsson L, Odh G, Metz CN, Rorsman H. 1996. The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol Medicine 2:143-149.
49. Sakai M, Nishihira J, Hibiya Y, Koyama Y, Nishi S. 1994. Glutathione binding rat-liver 13K protein is the homolog of the macrophage-migration inhibitory factor. Bio Mol Biol Int 33:439-446.
50. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. 2S. J Am Chem Soc 112:1280-1281.
52. 15N HSQC experiments optimized to retain full sensitivity. J Magn Reson A102:241-245.
53. 13C nuclear magnetic resonance chemical shifts. J Am Chem Soc 113:5490-5492.
54. 15N NMR relaxation measurements. Biochemistry 31:4394-4406.
55. Suzuki M, Sugimoto H, Nakagawa A, Tanaka I, Nishihira J, Sakai M. 1996. Crystal structure of the macrophage migration inhibitory factor from rat liver. Nature Struct Biol 3:259-265.
56. Weiser WY, Temple PA, Witek-Gianotti JS, Rembold HG, Clark SC, David JR. 1989. Molecular cloning of the cDNA encoding a human macrophage migration inhibitory factor. Proc Natl Acad Sci USA 86:7522-7531.
57. Wishart DS, Sykes BD, Richards FM. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J Mol Biol 222:311-333.
58. Wistow GJ, Shaughnessy MP, Lee DC, Hodin J, Zelenka. 1993. A macrophage migration inhibitory factor is expressed in the differentiating cells of the eye lens. Proc Natl Acad Sci USA 90:1272-1280.
59. Wüthrich K. 1986. NMR of proteins and nucleic acids. New York: Wiley.
60. Zeng FY, Weiser WY, Kratzin H, Stahl B, Karas M, Gabius HJ. 1993. The major binding-protein of the interferon antagonist sarcolectin in human placenta is a macrophage-migration inhibitory factor. Archiv Bioch Biophys 303: 74-80.
61. Zink T, Ross A, Lüers K, Cieslar C, Rudolph R, Holak TA. 1994. Structure and dynamics of the human granulocyte colony-stimulating factor determined by NMR spectroscopy. Loop mobility in a four-helix-bundle protein. Biochemistry 33:8453-8463.