Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: Indications for a new role of MIF in sperm maturation

Molecular Human Reproduction

Volumn 10, Issue 8, 2004, Pages 605-611

  Eickhoff, Regina ^a   Baldauf, Christina ^a   Koyro, Hans Werner ^a   Wennemuth, Gunther ^b   Suga, Yasushi ^c   Seitz, Jürgen ^b   Henkel, Ralf ^a   Meinhardt, Andreas ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c JUNTENDO UNIVERSITY   (Japan)

Author keywords

Inhibitory factor; Migration; Sperm; Zinc

Indexed keywords

MACROPHAGE MIGRATION INHIBITION FACTOR; THIOL GROUP; TRACE METAL; ZINC;

ANIMAL CELL; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CELL ISOLATION; CELL STIMULATION; CELL VACUOLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CULTURE MEDIUM; EPIDIDYMIS TAIL; FLAGELLUM; INCUBATION TIME; MALE; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SPERMATOZOON MATURATION; SPERMATOZOON MIDPIECE; STATISTICAL SIGNIFICANCE;

ANIMALS; CATTLE; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; OXIDATION-REDUCTION; PROTEIN DISULFIDE REDUCTASE (GLUTATHIONE); RATS; RATS, WISTAR; SPERM MATURATION; SPERMATOZOA; ZINC;

CAPUT;

EID: 4344643732     PISSN: 13609947     EISSN: None     Source Type: Journal    
DOI: 10.1093/molehr/gah075     Document Type: Article

References (43)

1. Baccetti B, Pallini V and Burrini AG (1973) The accessory fibers of the sperm tail. I. Structure and chemical composition of bull coarse fibers. J Submicrosc Cytol 5,237-256.
2. Baccetti B, Pallini V and Burrini AG (1976) The accessory fibers of the sperm tail. II. Their role in binding zinc in mammals and cephalopods. J Ultrastruct Res 54,261-275.
3. Baltz JM, Pallini V and Burrini AG (1990) Dense fibres protect mammalian sperm against damage. Biol Reprod 43,485-491.
4. Bedford JM and Calvin HI (1974) Changes in -S-S- linked structures of the sperm tail during epididymal maturation, with comparative observations in sub-mammalian species. J Exp Zool 187,181-204.
5. Bendrat K, Al-Abed Y, Callaway DJ, Peng T, Calandra T, Metz CN and Bucala R (1997) Biochemical and mutational investigations of the enzymatic activity of macrophage migration inhibitory factor. Biochemistry 36,15356-15362.
6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72,248-254.
7. Calandra T and Roger T (2003) Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3,791-800.
8. Calvin HI and Bedford JM (1971) Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J Reprod Fertil Suppl 13 (Suppl 13),65-75.
9. Calvin HI and Bleau G (1974) Zinc-thiol complexes in keratin-like structures of rat spermatozoa. Exp Cell Res 86,280-284.
10. Calvin HI, Hwang FH and Wohlrab H (1975) Localization of zinc in a dense fiber-connecting piece fraction of rat sperm tails analogous chemically to hair keratin. Biol Reprod 13,228-239.
11. Chandler ML and Varandani PT (1975) Insulin degradation. XV. Use of different assay methods for the study of mechanism of action of glutathione-insulin transhydrogenase. Biochim Biophys Acta 397, 307-317.
12. Eickhoff R, Wilhelm B, Renneberg H, Wennemuth G, Bacher M, Linder D, Bucala R, Seitz J and Meinhardt A (2001) Purification and characterization of macrophage migration inhibitory factor as a secretory protein from rat epididymis: evidences for alternative release and transfer to spermatozoa. Mol Med 7,27-35.
13. Fornes MW, Barbieri A, Sosa MA and Bertini F (1991) First observations on enzymatic activity and protein content of vesicles separated from rat epididymal fluid. Andrologia 23,347-351.
14. Frenette G, Lessard C and Sullivan R (2002) Selected proteins of 'prostasome-like particles' from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 67,308-313.
15. Frenette G, Lessard C, Madore E, Fortier MA and Sullivan R (2003) Aldose Reductase and Macrophage Migration Inhibitory Factor Are Associated to Epididymosomes and Spermatozoa in the Bovine Epididymis. Biol Reprod 69,1586-1592.
16. Henkel R, Bittner J, Weber R, Huther F and Miska W (1999) Relevance of zinc in human sperm flagella and its relation to motility. Fertil Steril 71,1138-1143.
17. Henkel R, Baldauf C and Schill WB (2003a) Resorption of the element zinc from spermatozoa by the epididymal epithelium. Reprod Domest Anim 38,97-101.
18. Henkel RR, Defosse K, Koyro HW, Weissmann N and Schill WB (2003b) Estimate of oxygen consumption and intracellular zinc concentration of human spermatozoa in relation to motility. Asian J Androl 5,3-8.
19. Hermanowski-Vosatka A, Mundt SS, Ayala JM, Goyal S, Hanlon WA, Czerwinski RM, Wright SD and Whitman CP (1999) Enzymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration. Biochemistry 38,12841-12849.
20. Holmgren A (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem 254,9627-9632.
21. Jung H, Kim T, Chae HZ, Kim KT and Ha H (2001) Regulation of macrophage migration inhibitory factor and thiol-specific antioxidant protein PAG by direct interaction. J Biol Chem 276,15504-15510.
22. Kaminska B, Rozewicka L, Dominiak B, Mielnicka M and Mikulska D (1987) Zinc content in epididymal spermatozoa of metoclopramide-treated rats. Andrologia 19,677-683.
23. Kirchoff C and Hale G (1996) Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Mol Hum Reprod 2,177-184.
24. Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Juttner S, Brunner H and Bernhagen J (1998a) Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol 280,85-102.
25. Kleemann R, Mischke R, Kapurniotu A, Brunner H and Bernhagen J (1998b) Specific reduction of insulin disulfides by macrophage migration inhibitory factor (MIF) with glutathione and dihydrolipoamide: potential role in cellular redox processes. FEBS Lett 430,191-196.
26. Kleemann R, Kapurniotu A, Mischke R, Held J and Bernhagen J (1999) Characterization of catalytic centre mutants of macrophage migration inhibitory factor (MIF) and comparison to Cys81Ser MIF. Eur J Biochem 261,753-766.
27. Kleemann R, Hausser A, Geiger G, Mischke R, Burger-Kentischer A, Flieger O, Johannes FJ, Roger T, Calandra T, Kapurniotu A, Grell M, Finkelmeier D, Brunner H and Bernhagen J (2000) Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 408,211-216.
28. Legare C, Berube B, Boue F, Lefievre L, Morales CR, El-Alfy M and Sullivan R (1999) Hamster sperm antigen P26 h is a phosphatidylinositol-anchored protein. Mol Reprod Dev 52,225-233.
29. Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA and Bucala R (2003) MIF signal transduction initiated by binding to CD74. J Exp Med 197,1467-1476.
30. Lindemann CB and Kanous KS (1995) 'Geometric clutch' hypothesis of axonemal function: key issues and testable predictions. Cell Motil Cytoskeleton 31,1-8.
31. Lolis E and Bucala R (2003) Macrophage migration inhibitory factor. Expert Opin Ther Targets 7,153-164.
32. Meinhardt A, Bacher M, McFarlane JR, Metz CN, Seitz J, Hedger MP, de Kretser DM and Bucala R (1996) Macrophage migration inhibitory factor production by Leydig cells: evidence for a role in the regulation of testicular function. Endocrinology 137,5090-5095.
33. Meinhardt A, Bacher M, Wennemuth G, Eickhoff R and Hedger M (2000) Macrophage migration inhibitory factor (MIF) as a paracrine mediator in the interaction of testicular somatic cells. Andrologia 32,46-48.
34. Nguyen MT, Beck J, Lue H, Funfzig H, Kleemann R, Koolwijk P, Kapurniotu A and Bernhagen J (2003a) A sixteen residue peptide fragment of macrophage migration inhibitory factor, MIF(50-65), exhibits redox activity and has MIF-like biological functions. J Biol Chem.
35. Nguyen MT, Lue H, Kleemann R, Thiele M, Tolle G, Finkelmeier D, Wagner E, Braun A and Bernhagen J (2003b) The cytokine macrophage migration inhibitory factor reduces pro-oxidative stress-induced apoptosis. J Immunol 170,3337-3347.
36. Ogawa H, Taneda A, Kanaoka Y and Sekine T (1979) The histochemical distribution of protein bound sulfhydryl groups in human epidermis by the new staining method. J Histochem Cytochem 27,942-946.
37. Quinn P, Kerin JF and Warnes GM (1985) Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid. Fertil Steril 44,493-498.
38. Rosengren E, Bucala R, Aman P, Jacobsson L, Odh G, Metz CN and Rorsman H (1996) The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol Med 2,143-149.
39. Rosengren E, Aman P, Thelin S, Hansson C, Ahlfors S, Bjork P, Jacobsson L and Rorsman H (1997) The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase. FEBS Lett 417,85-88.
40. Serres C, Escalier D and David G (1983) Ultrastructural morphometry of the human sperm flagellum with a stereological analysis of the lengths of the dense fibres. Biol Cell 49,153-161.
41. Swope M, Sun HW, Blake PR and Lolis E (1998) Direct link between cytokine activity and a catalytic site for macrophage migration inhibitory factor. EMBO J 17,3534-3541.
42. Wroblewski N, Schill WB and Henkel R (2003) Metal chelators change the human sperm motility pattern. Fertil Steril 79 (Suppl 3),1584-1589.
43. Yeung CH, Cooper TG, Oberpenning F, Schulze H and Nieschlag E (1993) Changes in movement characteristics of human spermatozoa along the length of the epididymis. Biol Reprod 49,274-280.