The 13-kD FK506 binding protein, FKBP13, interacts with a novel homologue of the erythrocyte membrane cytoskeletal protein 4.1

Journal of Cell Biology

Volumn 141, Issue 1, 1998, Pages 143-153

  Walensky, Loren D ^a   Gascard, Philippe ^b   Fields, Michael E ^a   Blackshaw, Seth ^a   Conboy, John G ^b   Mohandas, Narla ^b   Snyder, Solomon H ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG BINDING PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN; TACROLIMUS;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; ERYTHROCYTE MEMBRANE; MEMBRANE VESICLE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SEQUENCE HOMOLOGY; SOUTHERN BLOTTING;

AGING; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BRAIN; CARRIER PROTEINS; CLONING, MOLECULAR; CYTOSKELETAL PROTEINS; ERYTHROCYTE MEMBRANE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; HIPPOCAMPUS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; ORGAN SPECIFICITY; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TACROLIMUS; TACROLIMUS BINDING PROTEINS; TRANSCRIPTION FACTORS;

EID: 0032489868     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.1.143     Document Type: Article

References (58)

1. Albers, M.W., C.T. Walsh, and S.L. Schreiber. 1990. Substrate specificity for the human rotamase FKBP: a view of FK506 and rapamycin as leucine-(twisted amide)-proline mimics. J. Org. Chem. 55:4984-4986.
2. Alloisio, N., N. Dalla Venezia, A. Rana, K. Andrabi, P. Texier, F. Gilsanz, J.P. Cartron, J. Delaunay, and A.H. Chishti. 1993. Evidence that red blood cell protein p55 may participate in the skeleton-membrane linkage that involves protein 4.1 and glycophorin C. Blood. 82:1323-1327.
3. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1990. Current Protocols in Molecular Biology. John Wiley, New York.
4. Baklouti, F., S.C. Huang, T.J. Vulliamy, J. Delaunay, and E.J. Benz, Jr. 1997. Organization of the human protein 4.1 genomic locus: new insights into the tissue-specific alternative splicing of the pre-mRNA. Genomics. 39:289-302.
5. Bennett, V. 1983. Proteins involved in membrane-cytoskeleton association in human erythrocytes: spectrin, ankyrin and band 3. Methods Enzymol. 96:313-324.
6. Beutler, E., C. West, and K.G. Blume. 1976. The removal of leukocytes and platelets from whole blood. J. Lab. Clin. Med. 88:328-333.
7. Blackshaw, S., and S.H. Snyder. 1997. Developmental expression pattern of phototransduction components in mammalian pineal implies a light-sensing function. J. Neurosci. 17:8074-8082.
8. Bush, K.T., B.A. Henrickson, and S.K. Nigam. 1994. Induction of the FK506-binding protein, FKBP13, under conditions which misfold proteins in the endoplasmic reticulum. Biochem. J. (Tokyo). 303:705-708.
9. Cameron, A.C., F.C. Nucifora, E.T. Fung, D.J. Livingston, R.A. Aldape, C.A. Ross, and S.H. Snyder. 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.
10. 2+ flux. Cell. 83:463-472.
11. Cameron, A.M., J.P. Steiner, D.M. Sabatini, A.I. Kaplin, L.D. Walensky, and S.H. Snyder. 1995. Immunophilin FK506 binding protein associated with inositol 1,4,5-trisphosphate receptor modulates calcium flux. Proc. Natl. Acad. Sci. USA. 92:1784-1788.
12. Chevray, P.M., and D. Nathans. 1992. Protein interaction cloning in yeast: Identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl. Acad. Sci. USA. 89:5789-5793.
13. Cohen, C.M., and P. Gascard. 1992. Regulation and post-translational modification of erythrocyte membrane and membrane-skeletal proteins. Sem. Hematol. 29:244-292.
14. Conboy, J., Y.W. Kan, S.B. Shohet, and N. Mohandas. 1986. Molecular cloning of protein 4.1, a major structural element of the human erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. USA. 83:9512-9516.
15. Conboy, J.G. 1993. Structure, function, and molecular genetics of erythroid membrane skeletal protein 4.1 in normal and abnormal red blood cells. Semin. Hematol. 30:58-73.
16. Conboy, J.G., J. Chan, N. Mohandas, and Y.W. Kan. 1988. Multiple protein 4.1 isoforms produced by alternative splicing in human erythroid cells. Proc. Natl. Acad. Sci. USA. 85:9062-9065.
17. Conboy, J.G., J.Y. Chan, J.A. Chasis, Y.W. Kan, and N. Mohandas. 1991. Tissue- and development-specific alternative RNA splicing regulates expression of multiple isoforms of erythroid membrane protein 4.1. J. Biol. Chem. 266:8273-8280.
18. Conboy, J.G., R. Shitamoto, M. Parra, R. Winardi, A. Kabra, J. Smith, and N. Mohandas. 1991. Hereditary elliptocytosis due to both qualitative and quantitative defects in membrane skeletal protein 4.1. Blood. 78:2438-2443.
19. Constantinescu, E., C. Heltianu, and M. Simionescu. 1986. Immunological detection of an analogue of the erythroid protein 4.1 in endothelial cells. Cell Biol. Int. Rep. 10:861-868.
20. Correas, I., T.L. Leto, D.W. Speicher, and V.T. Marchesi. 1986. Identification of the functional site of erythrocyte protein 4.1 involved in spectrin-actin associations. J. Biol. Chem. 261:3310-3315.
21. Correas, I., D.W. Speicher, and V.T. Marchesi. 1986. Structure of the spectrin-actin binding site of erythrocyte protein 4.1. J. Biol. Chem. 261: 13362-13366.
22. Cunningham, E.B. 1995. The human erythrocyte membrane contains a novel 12-kDa inositolphosphate-binding protein that is an immunophilin. Biochem. Biophys. Res. Commun. 215:212-218.
23. Danilov, Y.N., R. Fennell, E. Ling, and C.M. Cohen. 1990. Selective modulation of band 4.1 binding to erythrocyte membranes by protein kinase C. J. Biol. Chem. 265:2556-2562.
24. Davies, G.E., and C.M. Cohen. 1985. Platelets contain proteins immunologically related to red cell spectrin and protein 4.1. Blood. 65:52-59.
25. Freinz, F., M.W. Albers, A. Galat, R.F. Standaert, W.S. Lane, S.J. Burakoff, B.E. Bierer, and S.L. Schreiber. 1991. Rapamycin and FK506 binding proteins (immunophilins). J. Am. Chem. Soc. 113:1409-1411.
26. Fruman, D.A., C.B. Klee, B.E. Bierer, and S.J. Burakoff. 1992. Calcineurin phosphatase activity in T lymphocytes is inhibited by FK 506 and cyclosporin A. Proc. Natl. Acad. Sci. USA. 89:3686-3690.
27. Futer, O., M.T. DeCenzo, R.A. Aldape, and D.J. Livingston. 1995. FK506 binding protein mutational analysis. J. Biol. Chem. 270:18935-18940.
28. Galat, A. 1993. Peptidylproline cis-trans-isomerases: immunophilins. Eur. J. Biochem. 216:689-707.
29. Gascard, P., and C.M. Cohen. 1994. Absence of high-affinity band 4.1 binding sites from membranes of glycophorin C- and D-deficient (Leach phenotype) erythrocytes. Blood. 83:1102-1108.
30. Goodman, S.R., L.A. Casoria, D.B. Coleman, and I.S. Zagon. 1984. Identification and location of brain protein 4.1. Science. 224:1433-1436.
31. Handschumacher, R.E., M.W. Harding, J. Rice, R.J. Drugge, and D.W. Speicher. 1994. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Nature. 226:544-546.
32. Harding, M.W., A. Galat, D.E. Uehling, and S.L. Schreiber. 1989. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature. 341:758-760.
33. Harrison, R.K., and R.L. Stein. 1990. Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry. 29:3813-3816.
34. Horton, R.M., H.D. Hunt, S.N. Ho, J.K. Pullen, and L.R. Pease. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene. 77:61-68.
35. Huang, J.P., C.J. Tang, G.H. Kou, V.T. Marchesi, E.J. Benz, Jr., and T.K. Tang. 1993. Genomic structure of the locus encoding protein 4.1. Structural basis for complex combinational patterns of tissue-specific alternative RNA splicing. J. Biol. Chem. 268:3758-3766.
36. Jayaraman, T., A.M. Brillantes, A.P. Timerman, S. Fleischer, H. Erdjument-Bromage, P. Tempst, and A.R. Marks. 1992. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267:9474-9477.
37. Jin, Y.J., M.W. Albers, W.S. Lane, B.E. Bierer, S.L. Schreiber, and S.J. Burakoff. 1991. Molecular cloning of a membrane-associated human FK506- and rapamycin-binding protein, FKBP-13. Proc. Natl. Acad. Sci. USA. 88:6677-6681.
38. Kay, J.E., E. Sampare-Kwateng, F. Geraghty, and G.Y. Morgan. 1991. Uptake of FK506 by lymphocytes and erythrocytes. Transplant Proc. 23:2760-2762.
39. Krauss, S.W., C.A. Larabell, S. Lockett, P. Gascard, S. Penman, N. Mohandas, and J.A. Chasis. 1997. Structural protein 4.1 in the nucleus of human cells: dynamic rearrangements during cell division. J. Cell. Biol. 137:275-289.
40. Leto., T.L., and V.T. Marchesi. 1984. A structural model of human erythrocyte protein 4.1. J. Biol. Chem. 259:4603-4608.
41. Li, X.J., S.H. Li, A.H. Sharp, F.C.J. Nucifora, G. Schilling, A. Lanahan, P. Worley, S.H. Snyder, and C.A. Ross. 1995. A huntingtin-associated protein enriched in brain with implications for pathology. Nature. 378:398-402.
42. Liu, J., J.D. Farmer, Jr., W.S. Lane, J. Friedman, I. Weissman, and S.L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell. 66:807-815.
43. Liu, J., M.W. Albers, T.J. Wandless, S. Luan, D.G. Alberg, P.J. Belshaw, P. Cohen, C. MacKintosh, C.B. Klee, and S.L. Schreiber. 1992. Inhibition of T cell signaling by immunophilin-ligand complexes correlates with loss of calcineurin phosphatase activity. Biochemistry. 31:3896-3901.
44. Marfatia, S.M., R.A. Leu, D. Branton, and A.H. Chishti. 1995. Identification of the protein 4.1 binding interface on glycophorin C and p55, a homologue of the Drosophila discs-large tumor suppressor protein. J. Biol. Chem. 270:715-719.
45. McCombie, W.R., C. Heiner, J.M. Kelly, M.G. Fitzgerald, and J.D. Gocayne. 1992. Rapid and reliable fluorescent cycle sequencing of double stranded templates. DNA Seq. 2:289-296.
46. Nigam, S.K., Y.J. Jin, M.J. Jin, K.T. Bush, B.E. Bierer, and S.J. Burakoff. 1993. Localization of the FK506-binding protein, FKBP13, to the lumen of the endoplasmic reticulum. Biochem. J. (Tokyo). 294:511-515.
47. Parra, M., P. Gascard, L.D. Walensky, S.H. Snyder, N. Mohandas, and J.G. Conboy. 1998. Identification and characterization of a novel widely expressed homologue of the erythroid membrane skeletal protein 4.1. Genomics. In press.
48. Partaledis, J.A., and V. Berlin. 1993. The FKB2 gene of Saccharomyces cerevisiae, encoding the immunosuppressant-binding protein FKBP-13, is regulated in response to accumulation of unfolded proteins in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 90:5450-5454.
49. Pasternack, G.R., R.A. Anderson, T.L. Leto, and V.T. Marchesi. 1985. Interactions between protein 4.1 and band 3. An alternative binding site for an element of the membrane skeleton. J. Biol. Chem. 260:3676-3683.
50. Pow, D.V., and D.K. Crook. 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.
51. Rosen, M.K., R.F. Standaert, A. Galat, M. Nakatsuka, and S.L. Schreiber. 1990. Inhibition of FKBP rotamase activity by immunosuppressant FK506: twisted amide surrogate. Science. 248:863-866.
52. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 545 pp.
53. Schultz, L.W., P.K., Martin, J. Liang, S.L. Schreiber, and J. Clardy. 1994. Atomic structure of the immunophilin FKBP13-FK506 complex: insights into the composite binding surface for calcineurin. J. Am. Chem. Soc. 116:3129-3130.
54. Sihag, R.K., L.W. Wang, A.M. Cataldo, M. Hamlin, C.M. Cohen, and R.A. Nixon. 1994. Evidence for the association of protein 4.1 immunoreactive forms with neurofibrillary tangles in Alzheimer's disease brains. Brain Res. 656:14-26.
55. Smith, L.M., J.Z. Sander, R.J. Kaiser, P. Hughes, C. Dodd, C.R. Connel, C. Heiner, S.B. Kent, and L.E. Hood. 1986. Fluorescence detection in automated sequence analysis. Nature. 321:674-679.
56. Vassar, R., J. Ngai, and R. Axel. 1993. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell. 74:309-318.
57. Wang, T., P.K. Donahoe, and A.S. Zervos. 1994. Specific interaction of type I receptors of the TGFβ family with the immunophilin FKBP-12. Science. 265:674-676.
58. Wang, T., B. Li, P.D. Danielson, P.C. Shah, S. Rockwell, R.J. Lechleider, J. Martin, T. Manganaro, and P.K. Donahoe. 1996. The immunophilin FKBP12 functions as a common inhibitor of the TGFβ family of type I receptors. Cell. 86:435-444.