Brain proteins interacting with the tetramerization region of non-erythroid alpha spectrin

• Autorzy: Oh Y , Fung L.W.-M.
• Języki publikacji: EN

Abstrakty

EN

The N-terminal region of non-erythroid alpha spectrin (SpαII) is responsible for interacting with its binding partner, beta spectrin, to form functional spectrin tetramers. We used a yeast-two-hybrid system, with an N-terminal segment of alpha spectrin representing the functional tetramerization site, as a bait to screen human brain c-DNA library for proteins that interact with the alpha spectrin segment. In addition to several beta spectrin isoforms, we identified 14 proteins that interact with SpαII. Seven of the 14 were matched to 6 known proteins: Duo protein, Lysyl-tRNA synthetase, TBP associated factor 1, two isoforms (b and c) of a protein kinase A interacting protein and Zinc finger protein 333 (2 different segments). Four of the 6 proteins are located primarily in the nucleus, suggesting that spectrin plays important roles in nuclear functions. The remaining 7 proteins were unknown to the protein data base. Structural predictions show that many of the 14 proteins consist of a large portion of unstructured regions, suggesting that many of these proteins fold into a rather flexible conformation. It is interesting to note that all but 3 of the 14 proteins are predicted to consist of one to four coiled coils (amphiphilic helices). A mutation in SpαII, V22D, which interferes with the coiled coil bundling of SpαII with beta spectrin, also affects SpαII interaction with Duo protein, TBP associated factor 1 and Lysyl-tRNA synthetase, suggesting that they may compete with beta spectrin for interaction with SpαII. Future structural and functional studies of these proteins to provide interaction mechanisms will no doubt lead to a better understanding of brain physiology and pathophysiology.

Słowa kluczowe

EN

spectrin; brain protein; tetramerization site; protein-protein interaction; yeast two-hybrid system; spectrin mutation; brain physiology; brain pathophysiology

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2007
• Tom: 12
• Numer: 4
• Opis fizyczny: p.604-620,fig.,ref.

Twórcy

autor

Oh Y

• University of Illinois at Chicago, 845 W.Taylor Street, MC 111, Chicaco, IL 60607, USA

autor

Fung L.W.-M.

Bibliografia

• 1. Yu, J., Fischman, D.A. and Steck, T.L. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J. Supramol. Struct. 1 (1973) 233-248.
• 2. Mohandas, N., Chasis, J.A. and Shohet, S.B. The influence of membrane skeleton on red cell deformability, membrane material properties, and shape. Semin. Hematol. 20 (1983) 225-242.
• 3. Park, S., Caffrey, M.S., Johnson, M.E. and Fung, L.W. Solution structural studies on human erythrocyte alpha-spectrin tetramerization site. J. Biol. Chem. 278 (2003) 21837-21844.
• 4. Yan, Y., Winograd, E., Viel, A., Cronin, T., Harrison, S.C. and Branton, D. Crystal structure of the repetitive segments of spectrin. Science 262 (1993) 2027-2030.
• 5. Pascual, J., Pfuhl, M., Rivas, G., Pastore, A. and Saraste, M. The spectrin repeat folds into a three-helix bundle in solution. FEBS Lett. 383 (1996) 201-207.
• 6. Mehboob, S., Luo, B.H., Johnson, M.E. and Fung, L.W.-M. Conformational studies of the tetramerization site of the human erythroid spectrin by cysteine-scanning spin-labeling EPR methods. Biochemistry 44 (2005) 15898-15905.
• 7. Mehboob, S., Luo, B.H. and Fung, L.W.-M. αβ spectrin association: A model system to mimic helical bundling at the tetramerization site. Biochemistry 40 (2001) 12457-12464.
• 8. Hiller, G. and Weber, K. Spectrin is absent in various tissue culture cells. Nature 266 (1977) 181-183.
• 9. Beck, K.A. and Nelson, W.J. A spectrin membrane skeleton of the Golgi complex. Biochim. Biophys. Acta. 1404 (1998) 153-160.
• 10. Goodman, S.R. Discovery of nonerythroid spectrin to the demonstration of its key role in synaptic transmission. Brain Res. Bull. 50 (1999) 345-346.
• 11. De Matteis, M.A. and Morrow, J.S. Spectrin tethers and mesh in the biosynthetic pathway. J. Cell Sci. 113 (2000) 2331-2343.
• 12. Gascard, P. and Mohandas N. New insights into functions of erythroid proteins in nonerythroid cells. Curr. Opin. Hematol. 7 (2000) 123-129.
• 13. Kordeli, E. The spectrin-based skeleton at the postsynaptic membrane of the neuromuscular junction. Microsc. Res. Tech. 49 (2000) 101-107.
• 14. Bennett, V. and Baines, A.J. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81 (2001) 1353-1392.
• 15. Giorgi, M., Cianci, C., Gallagher, P. and Morrow, J.S. Spectrin oligomerization is cooperatively coupled to membrane assembly: A linkage targeted by many hereditary hemolytic anemias? Exp. Mol. Pathol. 70 (2001) 215-230.
• 16. Djinovic-Carugo, K., Gautel, M., Ylanne, J. and Young, P. The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett. 513 (2002) 119-123.
• 17. Lee, J.K., Coyne, R.S., Dubreuil, R.R., Goldstein, L.S. and Branton, D. Cell shape and interaction defects in alpha-spectrin mutants of Drosophila melanogaster. J. Cell Biol. 123 (1993) 1797-1809.
• 18. Pinder, J.C. and Baines, A.J. A protein accumulator. Nature 406 (2000) 253-254.
• 19. McMahon, L.W., Sangerman, J., Goodman, S.R., Kumaresan, K. and Lambert, M.W. Human alpha spectrin II and the FANCA, FANCC and FANCG proteins bind to DNA containing psoralen interstrand cross-links. Biochemistry 40 (2001) 7025-7034.
• 20. Sridharan, D.M., McMahon, L.W. and Lambert, M.W. alphaII-Spectrin interacts with five groups of functionally important proteins in the nucleus. Cell Biol. Int. 30 (2006) 866-878
• 21. Goodman, S.R., Zimmer, W.E., Clark, M.B., Zagon, I.S., Barker, J.E. and Bloom, M.L. Brain spectrin: of mice and men. Brain Res. Bull. 36 (1995) 593-606.
• 22. Kanda, K., Tanaka, T. and Sobue, K. Calspectin (fodrin or nonerythroid spectrin)-actin interaction: a possible involvement of 4.1-related protein. Biochem. Biophys. Res. Commun. 140 (1986) 1051-1058.
• 23. Tsukita, S., Tsukita, S., Ishikawa, H., Kurokawa, M., Morimoto, K., Sobue, K. and Kakiuchi, S. Binding sites of calmodulin and actin on the brain spectrin, calspectin. J. Cell Biol. 97 (1983) 574-578.
• 24. Sobue, K., Kanda, K. and Kakiuchi, S. Solubilization and partial purification of protein kinase systems from brain membranes that phosphorylate calspectin. A spectrin-like calmodulin-binding protein (fodrin). FEBS Lett. 150 (1982) 185-190.
• 25. Riederer, B.M., Lopresti, L.L., Krebs, K.E., Zagon, I.S. and Goodman, S.R. Brain spectrin(240/235) and brain spectrin(240/235E): conservation of structure and location within mammalian neural tissue. Brain Res Bull. 21 (1988) 607-616.
• 26. Ohara, O., Ohara, R., Yamakawa, H., Nakajima, D. and Nakayama, M. Characterization of a new beta-spectrin gene which is predominantly expressed in brain. Brain Res. Mol. Brain Res. 57 (1998) 181-192.
• 27. Stankewich, M.C., Tse, W.T., Peters, L.L., Ch'ng, Y., John, K.M., Stabach, P.R., Devarajan, P., Morrow, J.S. and Lux, S.E. A widely expressed betaIII spectrin associated with Golgi and cytoplasmic vesicles. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 14158-14163.
• 28. Levine, J. and Willard, M. Fodrin: axonally transported polypeptides associated with the internal periphery of many cells. J. Cell. Biol. 90 (1981) 631-642.
• 29. Burridge, K., Kelly, T. and Mangeat, P. Nonerythrocyte spectrins: actinmembrane attachment proteins occurring in many cell types. J. Cell. Biol. 95 (1982) 478-486.
• 30. Bachs, O., Lanini, L., Serratosa, J., Coll, M.J., Bastos, R., Aligue, R., Rius, E. and Carafoli, E. Calmodulin-binding proteins in the nuclei of quiescent and proliferatively activated rat liver cells. J. Biol. Chem. 265 (1990) 18595-18600.
• 31. Vendrell, M., Aligue, R., Bachs, O. and Seratosa, J. Presence of calmodulin and calmodulin-binding proteins in the nuclei of brain cells. J. Neurochem. 57 (1991) 622-628.
• 32. Sumandea, C.A. and Fung, L.W.-M. Mutational Effects at the Tetramerization Site of Nonerythroid Alpha Spectrin. Mol. Brain Res. 136 (2005) 81-90.
• 33. Tse, W.T., Tang, J., Jin, O., Korsgren, C., John, K.M., Kung, A.L., Gwynn, B., Peters, L.L. and Lux, S.E. A new spectrin, beta IV, has a major truncated isoform that associates with promyelocytic leukemia protein nuclear bodies and the nuclear matrix. J. Biol. Chem. 276 (2001) 23974-23985.
• 34. Nagase, T., Kikuno, R., Hattori, A., Kondo, Y., Okumura, K. and Ohara, O. Prediction of the coding sequences of unidentified human genes. XIX. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 7 (2000) 347-355.
• 35. Colomer, V., Engelender, S., Sharp, A.H., Duan, K., Cooper, J.K., Lanahan, A., Lyford, G., Worley, P. and Ross, C.A. Huntingtin-associated protein 1 (HAP1) binds to a Trio-like polypeptide, with a rac1 guanine nucleotide exchange factor domain. Hum. Mol. Genet. 6 (1997) 1519-1525.
• 36. Freist, W. and Gauss, D.H. Lysyl-tRNA synthetase. Biol. Chem. Hoppe. Seyler. 376 (1995) 451-472.
• 37. Tolkunova, E., Park, H., Xia, J., King, M.P. and Davidson, E. The human lysyltRNA synthetase gene encodes both the cytoplasmic and mitochondrial enzymes by means of an unusual alternative splicing of the primary transcript. J. Biol. Chem. 275 (2000) 35063-35069.
• 38. Hisatake, K., Hasegawa, S., Takada, R., Nakatani, Y., Horikoshi, M., Roeder, R.G. The p250 subunit of native TATA box-binding factor TFIID is the cellcycle regulatory protein CCG1. Nature 362 (1993) 179-181.
• 39. Jacobson, R.H., Ladurner, A.G., King, D.S., Tjian, R. Structure and function of a human TAFII250 double bromodomain module. Science 288 (2000) 1422- 1425.
• 40. Maile, T., Kwoczynski, S., Katzenberger, R.J., Wassarman, D.A., Sauer, F. TAF1 activates transcription by phosphorylation of serine 33 in histone H2B. Science 304 (2004) 1010-1014.
• 41. Tian, Y., Breedveld, G.J., Huang, S., Oostra, B.A., Heutink, P. and Lo, W.H. Characterization of ZNF333, a novel double KRAB domain containing zinc finger gene on human chromosome 19p13.1. Biochim. Biophys. Acta. 1577 (2002) 121-125.
• 42. Jing, Z., Liu, Y., Dong, M., Hu, S. and Huang, S. Identification of the DNA binding element of the human ZNF333 protein. J. Biochem. Mol. Biol. 37 (2004) 663-670.
• 43. Sastri, M., Barraclough, D.M., Carmichael, P.T. and Taylor, S.S. A-kinaseinteracting protein localizes protein kinase A in the nucleus. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 349-354.
• 44. Narayan, V.A., Kriwacki, R.W. and Caradonna, J.P. Structures of zinc finger domains from transcription factor Sp1. Insights into sequence-specific proteinDNA recognition. J Biol. Chem. 272 (1997) 7801-7809.
• 45. Yang, M., Wu, Z. and Field, S. Protein-protein interactions analyzed with the yeast two-hybrid system. Nucleic Acid Res. 23 (1995) 1152-1156.
• 46. Mehboob, S., Jacob, J., May, M., Kotula, L., Thiyagarajan, P., Johnson, M.E. and Fung, L.W.-M. Structural analysis of the alpha N-terminal region of erythroid and nonerythroid spectrins by small-angle X-ray scattering. Biochemistry 42 (2003) 14702-14710.
• 47. Adamson, J.G., Zhou, N.E. and Hodges, R.S. Structure, function and application of the coiled-coil protein folding motif. Curr. Opin. Biotechnol. 4 (1993) 428- 437.
• 48. McMahon, L.W., Walsh, C.E. and Lambert, M.W. Human alpha spectrin II and the Fanconi anemia proteins FANCA and FANCC interact to form a nuclear complex. J. Biol. Chem. 274 (1999) 32904-32908.
• 49. Sridharan, D., Brown, M., Lambert, W.C., McMahon, L.W. and Lambert, M.W. Nonerythroid alphaII spectrin is required for recruitment of FANCA and XPF to nuclear foci induced by DNA interstrand cross-links. J. Cell. Sci. 116 (2003) 823-835.
• 50. Lallena, M.J. and Correas, I. Transcription-dependent redistribution of nuclear protein 4.1 to SC35-enriched nuclear domains. J. Cell Sci. 110 (1997) 239-247.
• 51. Lallena, M.J., Martinez, C., Valcarcel, J. and Correas, I. Functional association of nuclear protein 4.1 with pre-mRNA splicing factors. J. Cell Sci. 111 (1998) 1963-1971.
• 52. Mattagajasingh, S.N., Huang, S.C., Hartenstein, J.S., Snyder, M., Marchesi, V.T. and Benz, E.J. A nonerythroid isoform of protein 4.1R interacts with the nuclear mitotic apparatus (NuMA) protein. J. Cell Biol. 5 (1999) 29-43.
• 53. Ye, K., Compton, D.A., Lai, M.M., Walensky, L.D. and Snyder, S.H. Protein 4.1N binding to nuclear mitotic apparatus protein in PC12 cells mediates the antiproliferative actions of nerve growth factor. J. Neurosci. 19 (1999) 10747- 10756.
• 54. Carmo-Fonseca, M. The contribution of nuclear compartmentalization to gene regulation. Cell 108 (2002) 513-521.
• 55. Chubb, J.R. and Bickmore, W.A. Considering nuclear compartmentalization in the light of nuclear dynamics. Cell 112 (2003) 403-406.
• 56. Palstra, R.J., Tolhuis, B., Splinter, E., Nijmeijer, R., Grosveld, F. and de Laat, W. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35 (2003) 190-194.