The 12 kD FK506 binding protein FKBP12 is released in the male reproductive tract and stimulates sperm motility

Molecular Medicine

Volumn 4, Issue 8, 1998, Pages 502-514

  Walensky, Loren D ^a   Dawson, Ted M ^a   Steiner, Joseph P ^b   Sabatini, David M ^c   Suarez, Juan D ^d   Klinefelter, Gary R ^d   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GUILFORD PHARMACEUTICALS INC   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FK 506 BINDING PROTEIN; IMMUNOPHILIN; TACROLIMUS;

ANIMAL TISSUE; ARTICLE; EPIDIDYMIS; MALE; MALE GENITAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; RAT; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; VAS DEFERENS; AFFINITY CHROMATOGRAPHY; ANIMAL; ANTIBODY SPECIFICITY; METABOLISM; PHYSIOLOGY; SPERMATOZOON; SPRAGUE DAWLEY RAT;

ANIMALS; CHROMATOGRAPHY, AFFINITY; GENITALIA, MALE; IMMUNOPHILINS; MALE; ORGAN SPECIFICITY; RATS; RATS, SPRAGUE-DAWLEY; SPERM MATURATION; SPERM MOTILITY; SPERMATOZOA; TACROLIMUS; TACROLIMUS BINDING PROTEINS;

EID: 0031596330     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.1007/bf03401755     Document Type: Article

References (62)

1. Freinz F, Albers MW, Galat A, et al. (1991) Rapamycin and FK506 binding proteins (immunophilins). J. Am. Chem. Soc. 113: 1409-1411.
2. Galat A. (1993) Peptidylproline cis-trans-isomerases: immunophilins. Eur. J. Biochem. 216: 689-707.
3. Fruman DA, Burakoff SJ, Bierer BE. (1994) Immunophilins in protein folding and immunosuppression. FASEB J. 8: 391-400.
4. Marks AR. (1996) Cellular functions of immunophilins. Physiol. Rev. 76: 631-649.
5. Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW. (1994) Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Nature 226: 544-546.
6. Harding MW, Galat A, Uehling DE, Schreiber SL. (1989) A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341: 758-760.
7. Sewell TJ, Lam E, Martin MM, et al. (1994) Inhibition of calcineurin by a novel FK-506-binding protein. J. Biol. Chem. 269: 21094-21102.
8. Jin YJ, Albers MW, Lane WS, Bierer BE, Schreiber SL, Burakoff SJ. (1991) Molecular cloning of a membrane-associated human FK506- and rapamycin-binding protein, FKBP-13. Proc. Natl. Acad. Sci. U.S.A. 88: 6677-6681.
9. Galat A, Lane WS, Standaert RF, Schreiber SL. (1992) A rapamycin-selective 25-kDa immunophilin. Biochemisty 31: 2427-2434.
10. Lebeau M-C, Massol N, Herrick J, Faber LE, Renoir J-M, Radanyi C, Baulieu E-E. (1992) P59, an hsp 90-binding protein: cloning and sequencing of its cDNA and preparation of a peptid-derived polyclonal antibody. J.Biol. Chem. 267: 4281-4284.
11. Coss MC, Winterstein D, Sowder RcN, Simek SL. (1995) Molecular cloning, DNA sequence analysis, and biochemical characterization of a novel 65-kDa FK506-binding protein (FKBP65). J. Biol. Chem. 270: 29336-29341.
12. Harrison RK, Stein RL. (1990) Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemisty 29: 3813-3816.
13. Rosen MK, Standaert RF, Galat A, Nakatsuka M, Schreiber SL. (1990) Inhibition of FKBP rotamase activity by immunosuppressant FK506: twisted amide surrogate. Science 248: 863-866.
14. Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL. (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66: 807-815.
15. Fruman DA, Klee CB, Bierer BE, Burakoff SJ. (1992) Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A. Proc. Natl. Acad. Sci. U.S.A. 89: 3686-3690.
16. McCaffrey PG, Perrino BA, Soderling TR, Rao A. (1993) NF-ATp, a T lymphocyte DNA-binding protein that is a target for calcineurin and immunosuppressive drugs. J. Biol. Chem. 268: 3747-3752.
17. Sabatini DM, Erdjument-Bromage H, Lui M, Tempst P, Snyder SH. (1994) RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 78: 35-43.
18. Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL. (1994) A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369: 756-758.
19. Chiu MI, Katz H, Berlin V. (1994) RAPT1, a mammalian homolog of yeast Tor, interacts with FKBP12/rapamycin complex. Proc. Natl. Acad. Sci. U.S.A. 91: 12574-12578.
20. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM. (1988) RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl. Acad. Sci. U.S.A. 95: 1432-1437.
21. Brunn GJ, Hudson CC, Sekulic A, et al. (1997) Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277: 99-101.
22. Dawson TM, Steiner JP, Lyons WE, Fotuhi M, Blue M, Snyder SH. (1994) The immunophilins, FK506 binding protein and cyclophilin, are discretely localized in the brain: relationship to calcineurin. Neuroscience 62: 569-580.
23. Steiner JP, Dawson TM, Fotuhi M, Glatt CE, Snowman AM, Cohen N, Snyder SH. (1992) High brain densities of the immunophilin FKBP colocalized with calcineurin. Nature 358: 584-587.
24. Sabatini DM, Lai MM, Snyder SH. (1997) Neural roles of immunophilins and their ligands. Mol. Neurobiol. 15: 223-239.
25. Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Marks AR. (1992) FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267: 9474-9477.
26. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, Snyder SH. (1995) Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. U.S.A. 92: 1784-1788.
27. Walensky LD, Gascard P, Fields ME, Blackshaw S, Conboy JG, Mohandas N, Snyder SH. (1998) The 13 kDa FK506 binding protein, FKBP13, interacts with a novel homologue of the erythrocyte membrane cytoskeletal prtein 4.1. J. Cell. Biol. 141: 143-153.
28. Dawson TM, Steiner JP, Dawson VL, Dinerman JL, Uhl GR, Snyder SH. (1993) Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc. Natl. Acad. Sci. U.S.A. 90: 9808-9812.
29. Lyons WE, George EB, Dawson TM, Steiner JP, Snyder SH. (1994) Immunosuppressant FK506 promotes neunte outgrowth in cultures of PC12 cells and sensory ganglia. Proc. Natl. Acad. Sci. U.S.A. 91: 3191-3195.
30. Steiner JP, Connolly MA, Valentine HL, Hamilton GS, Dawson TM, Hester L, Snyder SH. (1997) Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A. Nat. Med. 3: 421-428.
31. Gold BG, Storm-Dickerson T, Austin DR. (1994) The immunosuppresant FK506 increases functional recovery and nerve regeneration following peripheral nerve injury. Restor. Neurol 6: 287-296.
32. Gold BG, Katoh K, Storm-Dickerson T. (1995) The immunosuppressant FK506 increases the rate of axonal regeneration in rat sciatic nerve. J. Neurosci. 15: 7509-7516.
33. Gold BG, Zeleny-Pooley M, Wang M-S, Chaturvedi P, Armistead DM. (1997) A nonimmunosuppressant FKBP12 ligand increases nerve regeneration. Exp. Neurol. 147: 269-278.
34. Pow DV, Crook DK. (1993) Extremely high titre polyclonal antisera against small neurotransmitter molecules: rapid production, characterization and use in light- and electron-microscopic immunocytochemistry. J. Neurosci. Methods 48: 51-63.
35. Jones R, Shalgi R, Hoyland J, Phillips D. (1990) Topographical rearrangement of a plasma membrane antigen during capacitation of rat spermatozoa in vitro. Dev. Biol. 139: 349-362.
36. Jin YJ, Burakoff SJ. (1993) The 25-kDa FK506-binding protein is localized in the nucleus and associates with casein kinase II and nucleolin. Proc. Natl. Acad. Sci. U.S.A. 90: 7769-7773.
37. 35S-Methionine. Biol. Reprod. 43: 113-120.
38. Del Rio AG. (1979) Macromolecular secretion into various segments of the guinea pig epididymis. Arch. Androl. 3: 231-237.
39. 35S-methionine in the mouse. Biol. Reprod. 43: 121-129.
40. Skudlarek MD, Orgebin-Crist MC. (1986) Glycosidases in cultured rat epididymal cells: enzyme activity, synthesis, and secretion. Biol Reprod. 35: 167-178.
41. Klinefelter GR, Hamilton DW. (1985) Synthesis and secretion of proteins by perifused caput epididymal tubules and association of secreted proteins with spermatozoa. Biol. Reprod. 33: 1017-1027.
42. Cornwall GA, Vindivich D, Tillman S, Chang TS. (1988) The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro. Biol. Reprod. 39: 141-155.
43. Cameron AC, Nucifora FC, Fung ET, Livingston DJ, Aldape RA, Ross CA, Snyder SH. (1997) FKBP12 binds the inositol 1,4,5-trisphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J. Biol. Chem. 272: 27582-27588.
44. Slott VL, Suarez JD, Perreault SD. (1991) Rat sperm motility analysis: methodologic considerations. Reprod. Toxicol. 5: 449-458.
45. Klinefelter GR, Gray EG, Suarez JD. (1991) The method of sperm collection significantly influences sperm motion parameters following ethane dimethansulphonate adminstration in the rat. Reprod. Toxicol. 5: 39-44.
46. Yeung CH, Oberlander G, Cooper TH. (1992) Characterization of the motility of rat spermatozoa by computer-aided objective measurement. J. Reprod. Fertil. 96: 427-441.
47. Yeung CH, Cooper TG, Oberpenning F, Schulze H, Nieschlag E. (1993) Changes in movement characteristics of human spermatozoa along the length of the epididymis. Biol. Reprod. 49: 274-280.
48. Cooper TG. (1995) Role of the epididymis in mediating changes in the male gamete during maturation. Adv. Exp. Med. Biol. 377: 87-101.
49. Jones R, Brown CR, Von Glos KI, Parker MG. (1980) Hormonal regulation of protein synthesis in the rat epididymis. Biochem. J. 188: 667-676.
50. Brooks DE. (1983) Effect of androgens on protein synthesis and secretion in various regions of the rat epididymis as analysed by two-dimensional gel electrophoresis. Mol. Cell. Endocrinol. 29: 255-270.
51. 2+ signaling in neutrophils by the mast cell-released immunophilin FKBP12. Proc. Natl. Acad. Sci. U.S.A. 92: 3435-3438.
52. Walensky LD, Snyder SH. (1995) Inositol 1,4,5-trisphosphate receptors selectively localized to the acrosome of mammalian sperm. J. Cell Biol. 130: 857-869.
53. Hoskins DD, Vijayaraghavan S. 1990. A new theory on the acquisition of sperm motility during epididymal transit. In: Gangnon C/ (ed) Controls of Sperm Motility: Biological and Clinical Aspects. CRC Press, Boston, pp. 53-62.
54. Manin M, Lecher P, Martinez A, Tournadre S, Jean C. (1995) Exportation of mouse vas deferens protein, a protein without a signal peptide, from mouse vas deferens epithelium: a model of apocrine secretion. Biol. Reprod. 52: 50-62.
55. Steinhoff M, Eicheler W, Holterhus PM, Rausch U, Seitz J, Aumuller G. (1994) Hormonally induced changes in apocrine secretion of transglutaminase in the rat dorsal prostate and coagulating gland. Eur. J. Cell Biol. 65: 45-59.
56. Aumuller G, Adler G. (1979) Experimental studies of apocrine secretion in the dorsal prostate epithelium of the rat. Cell Tissue Res. 198: 145-158.
57. Rennenberg H, Konrad L, Aumuller G. (1995) Immunohistochemistry of secretory particles ("vesiculosomes") from the epithelium of bovine seminal vesicles and ampulla of the vas deferens. Acta Anat. 153: 273-281.
58. Hisatomi A, Fujihira S, Fujimoto Y, Fujii T, Mine Y, Ohara K. (1996) Effect of Prograf (FK506) on spermatogenesis in rats. Toxicology 109: 75-83.
59. Yeung CH, Cooper TG, Nieschlag E. (1997) Human epididymal secreted protein CD52 on ejaculated spermatozoa: correlations with semen characteristics and the effect of its antibody. Mol. Hum. Reprod. 3: 1045-1051.
60. Kanwar KC, Yanagimachi R, Lopata A. (1979) Effects of human seminal plasma on fertilizing capacity of human spermatozoa. Fertil. Steril. 31: 321-327.
61. Bavister BD, Rogers BJ, Yanagimachi R. (1978) The effects of cauda epididymal plasma on the motility and acrosome reaction of hamster and guinea pig spermatozoa in vitro. Biol. Reprod. 19: 358-363.
62. Boue F, Biais J, Sullivan R. (1996) Surface localization of P34H an epididymal protein, during maturation, capacitation, and acrosome reaction of human spermatozoa. Biol. Reprod. 54: 1009-1017.