The yeast penta-EF protein Pef1p is involved in cation-dependent budding and cell polarization

Molecular Microbiology

Volumn 65, Issue 4, 2007, Pages 1122-1138

  Vernarecci, Stefano ^a,b   Colotti, Gianni ^a   Ornaghi, Prisca ^a   Schiebel, Elmar ^c   Chiancone, Emilia ^a,d   Filetici, Patrizia ^a  

^a CNR   (Italy)

^b Dipartimento di Genetica e Biologia Molecolare   (Italy)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN PEF1P; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL BUDDING; CELL POLARITY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CALCIUM; CALCIUM-BINDING PROTEINS; CELL POLARITY; CELL WALL; CHELATING AGENTS; DIMERIZATION; EF HAND MOTIFS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHYLOGENY; PROTEIN BINDING; RECOMBINANT PROTEINS; REPRODUCTION, ASEXUAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN; ZINC;

ASCOMYCOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; VERTEBRATA;

EID: 34547663702     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05852.x     Document Type: Article

References (83)

1. Alonso-Monge, R., Real, E., Wojda, I., Bebelman, J.P., Mager, W.H. Siderius, M. (2001) Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects. Mol Microbiol 41 : 717 730.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
3. André, I. Linse, S. (2002) Measurement of Ca2+-binding constants of proteins and presentation of the CaLigator software. Anal Biochem 305 : 195 205.
4. Bidlingmaier, S., Weiss, E.L., Seidel, C., Drubin, D.G. Snyder, M. (2001) The Cbk1p pathway is important for polarized cell growth and cell separation in Saccharomyces cerevisiae. Mol Cell Biol 21 : 2449 2462.
5. Blanchard, H., Li, Y., Cygler, M., Kay, C.M., Simon, J., Arthur, C., et al. (1996) Ca(2+)-binding domain VI of rat calpain is a homodimer in solution: hydrodynamic, crystallization and preliminary X-ray diffraction studies. Protein Sci 3 : 535 537.
6. Blanchard, H., Grochulski, P., Li, Y., Arthur, J.S., Davies, P.L., Elce, J.S. Cygler, M. (1997) Structure of a calpain Ca (2+)-binding domain reveals a novel EF-hand and Ca (2+)-induced conformational changes. Nat Struct Biol 7 : 532 538.
7. Blumenschein, T.M. Reinach, F.C. (2000) Analysis of affinity and specificity in an EF-hand site using double mutant cycles. Biochemistry 39 : 3603 3610.
8. Bogomolnaya, L.M., Pathak, R., Guo, J. Polymenis, M. (2006) Roles of the RAM signaling network in cell cycle progression in Saccharomyces cerevisiae. Curr Genet 49 : 384 392.
9. Bonneau, N., Ozier-Kalogeropoulos, O., Li, G., Labouesse, M., Minvielle-Sebastia, L. Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 7 : 609 615.
10. Bultynck, G., Heath, V.L., Majeed, A.P., Galan, J.M., Haguenauer-Tsapis, R. Cyert, M.S. (2006) Slm1 and Slm2 are novel substrates of the calcineurin phosphatase required for heat stress-induced endocytosis of the yeast uracil permease. Mol Cell Biol 12 : 4729 4745.
11. Cabib, E. (2004) The septation apparatus, a chitin-requiring machine in budding yeast. Arch Biochem Biophys 426 : 201 207.
12. Chou, P.Y. Fasman, G.D. (1974) Prediction of protein conformation. Biochemistry 13 : 222 245.
13. Collis, L.P., Meyers, M.B., Zhang, J., Phoon, C.K., Sobie, E.A., Coetzee, W.A. Fishman, G.I. (2007) Expression of a sorcin missense mutation in the heart modulates excitation-contraction coupling. FASEB J 21 : 475 487.
14. Colman-Lerner, A., Chin, T.E. Brent, R. (2001) Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107 : 739 750.
15. Cunningham, K.W. Fink, G.R. (1994) Ca2+ transport in Saccharomyces cerevisiae. J Exp Biol 196 : 157 166.
16. Cyert, M.S. (2001) Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Annu Rev Genet 35 : 647 672.
17. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6 : 1948 1954.
18. Farrell, E.F., Antaramian, A., Benkusky, N., Zhu, X., Rueda, A., Gomez, A.M. Valdivia, H.H. (2004) Regulation of cardiac excitation-contraction coupling by sorcin, a novel modulator of ryanodine receptors. Biol Res 37 : 609 612.
19. Finn, R.D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., et al. (2006) Pfam: clans, webtools and services. Nucleic Acids Res 34 : 247 251.
20. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D. Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook. Walker J.M. (ed.). Totowa, NJ : Humana Press, pp. 571 607.
21. Geissler, S., Pereira, G., Spang, A., Knop, M., Soues, S., Kilmartin, J. Schiebel, E. (1996) The spindle pole body component Spc98p interacts with the gamma-tubulin-like Tub4p of Saccharomyces cerevisiae at the sites of microtubule attachment. EMBO J 15 : 3899 3911.
22. Gray, J.V., Ogas, J.P., Kamada, Y., Stone, M., Levin, D.E. Herskowitz, I. (1997) A role for the Pkc1 MAP kinase pathway of Saccharomyces cerevisiae in bud emergence and identification of a putative upstream regulator. EMBO J 16 : 4924 4937.
23. Halachmi, D. Eilam, Y. (1993) Calcium homeostasis in yeast cells exposed to high concentrations of calcium. Roles of vacuolar H(+)-ATPase and cellular ATP. FEBS Lett 316 : 73 78.
24. Hansen, C., Tarabykina, S., la Cour, J.M., Lollike, K. Berchtold, M.W. (2003) The PEF family proteins sorcin and grancalcin interact in vivo and in vitro. FEBS Lett 545 : 151 154.
25. Hayashi, M., Fukuzawa, T., Sorimachi, H. Maeda, T. (2005) Constitutive activation of the pH-responsive Rim101 pathway in yeast mutants defective in late steps of the MVB/ESCRT pathway. Mol Cell Biol 25 : 9478 9490.
26. Higgins, D., Thompson, J., Gibson, T., Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 : 4673 4680.
27. Hosfield, C.M., Elce, J.S., Davies, P.L. Jia, Z. (1999) Crystal structure of calpain reveals the structural basis for Ca (2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J 18 : 6880 6889.
28. Hulo, N., Bairoch, A., Bulliard, V., Cerutti, L., De Castro, E., Langendijk-Genevaux, P.S., et al. (2006) The PROSITE database. Nucleic Acids Res 34 : D227 D230.
29. Hwa Lim, H., Yeong, F.M. Surana, U. (2003) Inactivation of mitotic kinase triggers translocation of MEN components to mother-daughter neck in yeast. Mol Biol Cell 11 : 4734 4743.
30. Iida, H., Sakaguchi, S., Yagawa, Y. Anraku, Y. (1990) Cell cycle control by Ca2+ in Saccharomyces cerevisiae. J Biol Chem 265 : 21216 21222.
31. Ilari, A., Johnson, K.A., Nastopoulos, V., Verzili, D., Zamparelli, C., Colotti, G., et al. (2002) The crystal structure of the sorcin calcium binding domain provides a model of Ca2+-dependent processes in the full-length protein. J Mol Biol 317 : 447 458.
32. Irazoqui, J.E. Lew, D.J. (2004) Polarity establishment in yeast. J Cell Sci 117 : 2169 2171.
33. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 11 : 947 962.
34. Jia, J., Tarabykina, S., Hansen, C., Berchtold, M. Cygler, M. (2001) Structure of apoptosis-linked protein ALG-2: insights into Ca2+-induced changes in penta-EF-hand proteins. Structure 9 : 267 275.
35. Kabsch, W. Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 : 2577 2637.
36. Kahl, C.R. Means, A.R. (2003) Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr Rev 24 : 719 736.
37. Karplus, K., Karchin, R., Draper, J., Casper, J., Mandel, D., Diekhans, M. Hughey, R. (2003) Combining local-structure, fold-recognition, and new fold methods for protein structure prediction. Proteins 53 (Suppl. 6 491 496.
38. Katoh, K., Suzuki, H., Terasawa, Y., Mizuno, T., Yasuda, J., Shibata, H. Maki, M. (2005) The penta-EF-hand protein ALG-2 interacts directly with the ESCRT-I component TSG101, and Ca2+-dependently co-localizes to aberrant endosomes with dominant-negative AAA ATPase SKD1/Vps4B. Biochem J 391 : 677 685.
39. Kemp, H.A. Sprague, G.F. Jr (2003) Far3 and five interacting proteins prevent premature recovery from pheromone arrest in the budding yeast Saccharomyces cerevisiae. Mol Cell Biol 23 : 1750 1763.
40. Kitaura, Y., Watanabe, M., Satoh, H., Kawai, T., Hitomi, K. Maki, M. (1999) Peflin, a novel member of the five-EF-hand-protein family, is similar to the apoptosis-linked gene 2 (ALG-2) protein but possesses nonapeptide repeats in the N-terminal hydrophobic region. Biochem Biophys Res Commun 263 : 68 75.
41. Kitaura, Y., Matsumoto, S., Satoh, H., Hitomi, K. Maki, M. (2001) Peflin and ALG-2, members of the penta-EF-hand protein family, form a heterodimer that dissociates in a Ca2+-dependent manner. J Biol Chem 276 : 14053 14058.
42. Kitaura, Y., Satoh, H., Takahashi, H., Shibata, H. Maki, M. (2002) Both ALG-2 and peflin, penta-EF-hand (PEF) proteins, are stabilized by dimerization through their fifth EF-hand regions. Arch Biochem Biophys 399 : 12 18.
43. Knop, M. Schiebel, E. (1998) Receptors determine the cellular localization of a gamma-tubulin complex and thereby the site of microtubule formation. EMBO J 17 : 3952 3967.
44. Knop, M., Siegers, K., Pereira, G., Zachariae, W., Winsor, B., Nasmyth, K. Schiebel, E. (1999) Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 10 : 963 972.
45. Kubler, E., Schimmoller, F. Riezman, H. (1994) Calcium-independent calmodulin requirement for endocytosis in yeast. EMBO J 13 : 5539 5546.
46. La Cour, J.M., Mollerup, J. Berchtold, M.W. (2007) ALG-2 oscillates in subcellular localization, unitemporally with calcium oscillations. Biochem Biophys Res Commun 353 : 1063 1067.
47. Letunic, I., Copley, R.R., Pils, B., Pinkert, S., Schultz, J. Bork, P. (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34 : D257 D260.
48. Lin, G.D., Chattopadhyay, D., Maki, M., Wang, K.K.W., Carson, M., Jin, L., et al. (1997) Crystal structure of calcium bound domain of calpain at 1.9 Å resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nat Struct Biol 4 : 539 547.
49. Lo, K.W.H., Zhang, Q., Li, M. Zhang, M. (1999) Apoptosis-linked gene product ALG-2 is a new member of the calpain small subunit subfamily of Ca2+-binding proteins. Biochemistry 38 : 7498 7508.
50. Lollike, K., Johnsen, A.H., Durussel, I., Borregaard, N. Cox, J.A. (2001) Biochemical characterization of the penta-EF-hand protein grancalcin and identification of 1-plastin as a binding partner. J Biol Chem 276 : 17762 17769.
51. Longtine, M.S., McKenzie, A., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 : 953 961.
52. Maki, M., Narayana, S.V. Hitomi, K. (1997) A growing family of the Ca2+-binding proteins with five EF-hand motifs. Biochem J 328 : 718 720.
53. Maki, M., Kitaura, Y., Satoh, H., Ohkouchi, S. Shibata, H. (2002) Structures, functions and molecular evolution of the penta-EF-hand Ca2+-binding proteins. Biochim Biophys Acta 1600 : 51 60.
54. Meyers, M.B., Pickel, V.M., Sheu, S.S., Sharma, V.K., Scotto, K.W. Fishman, G.I. (1995) Association of sorcin with the cardiac ryanodine receptor. J Biol Chem 270 : 25333 25338.
55. Meyers, M.B., Fischer, A., Sun, Y.J., Lopes, C.M., Rohacs, T., Nakamura, T.Y., et al. (2003) Sorcin regulates excitation-contraction coupling in the hearth. J Biol Chem 278 : 28865 28871.
56. Miseta, A., Fu, L., Kellermayer, R., Buckley, J. Bedwell, D.M. (1999) The Golgi apparatus plays a significant role in the maintenance of Ca2+ homeostasis in the vps33Delta vacuolar biogenesis mutant of Saccharomyces cerevisiae. J Biol Chem 274 : 5939 5947.
57. Miyakawa, T. Mizunuma, M. (2007) Physiological roles of calcineurin in Saccharomyces cerevisiae with special emphasis on its roles in G2/M cell-cycle regulation. Biosci Biotechnol Biochem 71 : 633 645.
58. Mizunuma, M., Hirata, D. Miyakawa, T. (2005) Implication of Pkc1p protein kinase C in sustaining Cln2p level and polarized bud growth in response to calcium signaling in Saccharomyces cerevisiae. J Cell Sci 118 : 4219 4229.
59. Nakajima-Shimada, J., Iid, H., Tsuji, F.I. Anraku, Y. (1991) Monitoring of intracellular calcium in Saccharomyces cerevisiae with an apoaequorin cDNA expression system. Proc Natl Acad Sci USA 88 : 6878 6882.
60. Nelson, B., Kurischko, C., Horecka, J., Mody, M., Nair, P., Pratt, L., et al. (2003) RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol Biol Cell 9 : 3782 3803.
61. Ni, L. Snyder, M. (2001) A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol Biol Cell 12 : 2147 2170.
62. Norden, C., Mendoza, M., Dobbelaere, J., Kotwaliwale, C.V., Biggins, S. Barral, Y. (2006) The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125 : 85 98.
63. Ouali, M. King, R.D. (2000) Cascaded multiple classifiers for secondary structure prediction. Protein Sci 9 : 1162 1176.
64. Pereira, G. Schiebel, E. (2001) The role of the yeast spindle pole body and the mammalian centrosome in regulating late mitotic events. Curr Opin Cell Biol 13 : 762 769.
65. Pruyne, D., Legesse-Miller, A., Gao, L., Dong, Y. Bretscher, A. (2004) Mechanisms of polarized growth and organelle segregation in yeast. Annu Rev Cell Dev Biol 20 : 559 591.
66. Ram, A.F., Wolters, A., Ten Hoopen, R. Klis, F.M. (1994) A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to calcofluor white. Yeast 8 : 1019 1030.
67. Ravulapalli, R., Diaz, B.G., Campbell, R.L. Davies, P.L. (2005) Homodimerization of calpain 3 penta-EF-hand domain. Biochem J 388 : 585 591.
68. Schneper, L., Krauss, A., Miyamoto, R., Fang, S. Broach, J.R. (2004) The Ras/protein kinase A pathway acts in parallel with the Mob2/Cbk1 pathway to effect cell cycle progression and proper bud site selection. Eukaryot Cell 1 : 108 120.
69. Schramm, C., Janke, C. Schiebel, E. (2001) Molecular dissection of yeast spindle pole bodies by two hybrid, in vitro binding, and co-purification. Methods Cell Biol 67 : 71 94.
70. Schwede, T., Kopp, J., Guex, N. Peitsch, M.C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31 : 3381 3385.
71. Shibata, H., Yamada, K., Mizuno, T., Yorikawa, C., Takahashi, H., Satoh, H., et al. (2004) The penta-EF-hand protein ALG-2 interacts with a region containing PxY repeats in Alix/AIP1, which is required for the subcellular punctate distribution of the amino-terminal truncation form of Alix/AIP1. J Biochem (Tokyo) 135 : 117 128.
72. Shibata, H., Suzuki, H., Yoshida, H. Maki, M. (2007) ALG-2 directly binds Sec31A and localizes at endoplasmic reticulum exit sites in a Ca2+-dependent manner. Biochem Biophys Res Commun 353 : 756 763.
73. Shimizu, J., Yoda, K. Yamasaki, M. (1994) The hypo-osmolarity-sensitive phenotype of the Saccharomyces cerevisiae hpo2 mutant is due to a mutation in PKC1, which regulates expression of beta-glucanase. Mol Gen Genet 242 : 641 648.
74. Sikorski, R.S. Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122 : 19 27.
75. Sorimachi, H. Suzuki, J.J. (2001) The structure of calpain. J Biochem 129 : 653 664.
76. Uetz, P., Giot, L., Cagney, G., Mansfield, T.A., Judson, R.S., Knight, J.R., et al. (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403 : 623 627.
77. Varian, K.D. Janssen, P.M. (2007) Frequency dependent acceleration of relaxation involves decreased myofilament calcium sensitivity. Am J Physiol Heart Circ Physiol 292 : H2212 H2219.
78. Viladevall, L., Serrano, R., Ruiz, A., Domenech, G., Giraldo, J., Barcelo, A. Arino, J. (2004) Characterization of the calcium-mediated response to alkaline stress in Saccharomyces cerevisiae. J Biol Chem 279 : 43614 43624.
79. Vito, P., Laconà, E. D'Adamio, L. (1996) Interfering with apoptosis: Ca2+-binding protein ALG-2 and Alzheimer's disease gene ALG-3. Science 271 : 521 525.
80. Yamasaki, A., Tani, K., Yamamoto, A., Kitamura, N. Komada, M. (2006) The Ca2+-binding protein ALG-2 is recruited to endoplasmic reticulum exit sites by Sec31A and stabilizes the localization of Sec31A. Mol Biol Cell 17 : 4876 4887.
81. Yoshimoto, H., Saltsman, K., Gasch, A.P., Li, H.X., Ogawa, N., Botstein, D., et al. (2002) Genome-wide analysis of gene expression regulated by the calcineurin/Crz1p signaling pathway in Saccharomyces cerevisiae. J Biol Chem 277 : 31079 31088.
82. Zamparelli, C., Ilari, A., Verzili, D., Giangiacomo, L., Colotti, G., Pascarella, S. Chiancone, E. (2000) Structure-function relationships in sorcin, a member of the penta EF-hand family. Interaction of sorcin fragments with the ryanodine receptor and an Escherichia coli model system. Biochemistry 39 : 658 666.
83. Zhang, J.W., Parra, K.J., Liu, J. Kane, P.M. (1998) Characterization of a temperature-sensitive yeast vacuolar ATPase mutant with defects in actin distribution and bud morphology. J Biol Chem 273 : 8470 8480.