Nuclear ALG-2 protein interacts with Ca2+ homeostasis endoplasmic reticulum protein (CHERP) Ca2+-dependently and participates in regulation of alternative splicing of inositol trisphosphate receptor type 1 (IP3R1) Pre-mRNA

Journal of Biological Chemistry

Volumn 288, Issue 46, 2013, Pages 33361-33375

  Sasaki Osugi, Kanae ^a   Imoto, Chiaki ^a   Takahara, Terunao ^a   Shibata, Hideki ^a   Maki, Masatoshi ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE SPLICING; CO-IMMUNOPRECIPITATION ASSAYS; ENDOPLASMIC RETICULUM; IMMUNOPRECIPITATION ASSAYS; MICROSCOPIC ANALYSIS; POLYCLONAL ANTIBODY; POST-TRANSCRIPTIONAL REGULATIONS; TIME-LAPSE IMAGING;

ALCOHOLS; CELL DEATH; CELL MEMBRANES; DIGITAL STORAGE; MOLECULAR BIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PIGMENTS; POLYOLS; PROTEINS; RNA; SPECKLE; SUGARS;

CALCIUM;

APOPTOSIS LINKED GENE 2 PROTEIN; CALCIUM ION HOMEOSTASIS ENDOPLASMIC RETICULUM PROTEIN; REGULATOR PROTEIN; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; BIOACCUMULATION; CALCIUM TRANSPORT; CELL NUCLEUS; CONTROLLED STUDY; EXON; GENE; GENETIC REGULATION; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IP3R1 GENE; MOLECULAR IMAGING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA INTERFERENCE;

ALTERNATIVE SPLICING; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; NUCLEAR SPECKLES; PROTEIN-PROTEIN INTERACTIONS; RNA POLYMERASE II; SR PROTEINS; SUBCELLULAR ORGANELLES;

ALTERNATIVE SPLICING; APOPTOSIS REGULATORY PROTEINS; CALCIUM; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CELL NUCLEUS; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MEMBRANE PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; RNA PRECURSORS; RNA-BINDING PROTEINS;

EID: 84887835530     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.497479     Document Type: Article

References (54)

1. Vito, P., Lacanà, E., and D'Adamio, L. (1996) Interfering with apoptosis: Ca2+-binding protein ALG-2 and Alzheimer's disease gene ALG-3. Science 271, 521-525
2. Rao, R. V., Poksay, K. S., Castro-Obregon, S., Schilling, B., Row, R. H., del Rio, G., Gibson, B. W., Ellerby, H. M., and Bredesen, D. E. (2004) Molecular components of a cell death pathway activated by endoplasmic reticulum stress. J. Biol. Chem. 279, 177-187
3. Draeby, I., Woods, Y. L., la Cour, J. M., Mollerup, J., Bourdon, J. C., and Berchtold, M. W. (2007) The calcium binding protein ALG-2 binds and stabilizes Scotin, a p53-inducible gene product localized at the endoplas- mic reticulum membrane. Arch. Biochem. Biophys. 467, 87-94
4. Mahul-Mellier, A. L., Strappazzon, F., Petiot, A., Chatellard-Causse, C., Torch, S., Blot, B., Freeman, K., Kuhn, L., Garin, J., Verna, J. M., Fraboulet, S., and Sadoul, R. (2008) Alix and ALG-2 are involved in tumor necrosis factor receptor 1-induced cell death. J. Biol. Chem. 283, 34954-34965
5. Yamada, Y., Arao, T., Gotoda, T., Taniguchi, H., Oda, I., Shirao, K., Shimada, Y., Hamaguchi, T., Kato, K., Hamano, T., Koizumi, F., Tamura, T., Saito, D., Shimoda, T., Saka, M., Fukagawa, T., Katai, H., Sano, T., Sasako, M., and Nishio, K. (2008) Identification of prognostic biomarkers in gastric cancer using endoscopic biopsy samples. Cancer Sci. 99, 2193-2199
6. Aviel-Ronen, S., Coe, B. P., Lau, S. K., da Cunha Santos, G., Zhu, C. Q., Strumpf, D., Jurisica, I., Lam, W. L., and Tsao, M. S. (2008) Genomic markers for malignant progression in pulmonary adenocarcinoma with bronchioloalveolar features. Proc. Natl. Acad. Sci. U.S.A. 105, 10155-10160
7. Maki, M., Narayana, S. V., and Hitomi, K. (1997) A growing family of the Ca2-binding proteins with five EF-hand motifs. Biochem. J. 328, 718-720
8. Maki, M., Kitaura, Y., Satoh, H., Ohkouchi, S., and Shibata, H. (2002) Structures, functions and molecular evolution of the penta-EF-hand Ca2+-binding proteins. Biochim. Biophys. Acta 1600, 51-60
9. Missotten, M., Nichols, A., Rieger, K., and Sadoul, R. (1999) Alix, a novel mouse protein undergoing calcium-dependent interaction with the apoptosis- linked-gene 2 (ALG-2) protein. Cell Death Differ. 6, 124-129
10. Vito, P., Pellegrini, L., Guiet, C., and D'Adamio, L. (1999) Cloning of AIP1, a novel protein that associates with the apoptosis-linked gene ALG-2 in a Ca2+-dependent reaction. J. Biol. Chem. 274, 1533-1540
11. Yamasaki, A., Tani, K., Yamamoto, A., Kitamura, N., and 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
12. Shibata, H., Suzuki, H., Yoshida, H., and 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
13. Shibata, H., Suzuki, H., Kakiuchi, T., Inuzuka, T., Yoshida, H., Mizuno, T., and Maki, M. (2008) Identification of Alix-type and non-Alix-type ALG- 2-binding sites in human phospholipid scramblase 3: differential binding to an alternatively spliced isoform and amino acid-substituted mutants.J. Biol. Chem. 283, 9623-9632
14. Maki, M., Suzuki, H., and Shibata, H. (2011) Structure and function of ALG-2, a penta-EF-hand calcium-dependent adaptor protein. Sci. China Life Sci. 54, 770-779
15. Shibata, H., Yamada, K., Mizuno, T., Yorikawa, C., Takahashi, H., Satoh, H., Kitaura, Y., and Maki, M. (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. 135, 117-128
16. Suzuki, H., Kawasaki, M., Inuzuka, T., Okumura, M., Kakiuchi, T., Shibata, H., Wakatsuki, S., and Maki, M. (2008) Structural basis for Ca2+-dependent formation of ALG-2/Alix peptide complex: Ca2-/EF3-driven arginine switch mechanism. Structure 16, 1562-1573
17. Shibata, H., Inuzuka, T., Yoshida, H., Sugiura, H., Wada, I., and Maki, M. (2010) The ALG-2 binding site in Sec31A influences the retention kinetics of Sec31A at the endoplasmic reticulum exit sites as revealed by live-cell time-lapse imaging. Biosci. Biotechnol. Biochem. 74, 1819-1826
18. Osugi, K., Suzuki, H., Nomura, T., Ariumi, Y., Shibata, H., and Maki, M. (2012) Identification of the P-body component PATL1 as a novel ALG-2- interacting protein by in silico and far-Western screening of proline-rich proteins. J. Biochem. 151, 657-666
19. O'Rourke, F., Soons, K., Flaumenhauft, R., Watras, J., Baio-Larue, C., Matthews, E., and Feinstein, M. B. (1994) Ca2+ release by inositol 1,4,5-trisphosphate is blocked by the K+-channel blockers apamin and tetrapentylammonium ion, and a monoclonal antibody to a 63 kDa membrane protein: reversal of blockade by K+ ionophores nigericin and valinomycin and purification of the 63 kDa antibody-binding protein. Biochem. J. 300, 673-683
20. Laplante, J. M., O'Rourke, F., Lu, X., Fein, A., Olsen, A., and Feinstein, M. B. (2000) Cloning of human Ca2+ homeostasis endoplasmic reticulum protein (CHERP): regulated expression of antisense cDNA depletes CHERP, inhibits intracellular Ca2+ mobilization and decreases cell proliferation. Biochem. J. 348, 189-199
21. O'Rourke, F. A., LaPlante, J. M., and Feinstein, M. B. (2003) Antisensemediated loss of calcium homeostasis endoplasmic reticulum protein (CHERP; ERPROT213-21) impairs Ca2+ mobilization, nuclear factor of activated T-cells (NFAT) activation and cell proliferation in Jurkat T-lym-phocytes. Biochem. J. 373, 133-143
22. Ryan, T., Sharma, P., Ignatchenko, A., MacLennan, D. H., Kislinger, T., and Gramolini, A. O. (2011) Identification of novel ryanodine receptor 1 (RyR1) protein interaction with calcium homeostasis endoplasmic reticulum protein (CHERP). J. Biol. Chem. 286, 17060-17068
23. Will, C. L., Urlaub, H., Achsel, T., Gentzel, M., Wilm, M., and Lührmann, R. (2002) Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. EMBO J. 21, 4978-4988
24. Saitoh, N., Spahr, C. S., Patterson, S. D., Bubulya, P., Neuwald, A. F., and Spector, D. L. (2004) Proteomic analysis of interchromatin granule clusters. Mol. Biol. Cell 15, 3876-3890
25. Lin-Moshier, Y., Sebastian, P. J., Higgins, L., Sampson, N. D., Hewitt, J. E., and Marchant, J. S. (2013) Re-evaluation of the role of calcium homeostasis endoplasmic reticulum protein (CHERP) in cellular calcium signaling. J. Biol. Chem. 288, 355-367
26. Fu, X. D., and Maniatis, T. (1992) The 35-kDa mammalian splicing factor SC35 mediates specific interactions between U1 and U2 small nuclear ribonucleoprotein particles at the 3′ splice site. Proc. Natl. Acad. Sci. U.S.A. 89, 1725-1729
27. Zahler, A. M., Lane, W. S., Stolk, J. A., and Roth, M. B. (1992) SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev. 6, 837-847
28. Manley, J. L., and Krainer, A. R. (2010)Arational nomenclature for serine/ arginine-rich protein splicing factors (SR proteins). Genes Dev. 24, 1073-1074
29. Ghosh, G., and Adams, J. A. (2011) Phosphorylation mechanism and structure of serine-arginine protein kinases. FEBS J. 278, 587-597
30. Kremers, G. J., Goedhart, J., van den Heuvel, D. J., Gerritsen, H. C., and Gadella, T. W., Jr. (2007) Improved green and blue fluorescent proteins for expression in bacteria and mammalian cells. Biochemistry 46, 3775-3783
31. Okumura, M., Ichioka, F., Kobayashi, R., Suzuki, H., Yoshida, H., Shibata, H., and Maki, M. (2009) Penta-EF-hand protein ALG-2 functions as a Ca2+-dependent adaptor that bridges Alix and TSG101. Biochem. Biophys. Res. Commun. 386, 237-241
32. Zhao, Y., Araki, S., Wu, J., Teramoto, T., Chang, Y. F., Nakano, M., Abdelfattah, A. S., Fujiwara, M., Ishihara, T., Nagai, T., and Campbell, R. E. (2011) An expanded palette of genetically encoded Ca2+ indicators. Science 333, 1888-1891
33. Osugi, K., Shibata, H., and Maki, M. (2013) Biochemical and immunological detection of physical interactions between penta-EF-hand protein ALG-2 and its binding partners. Methods Mol. Biol. 963, 187-200
34. Spector, D. L., and Lamond, A. I. (2011) Nuclear speckles. Cold Spring Harb. Perspect. Biol. 3, pii: a000646
35. la Cour, J. M., Mollerup, J., and Berchtold, M. W. (2007) ALG-2 oscillates in subcellular localization, unitemporally with calcium oscillations. Biochem. Biophys. Res. Commun. 353, 1063-1067
36. Neugebauer, K. M., and Roth, M. B. (1997) Distribution of pre-mRNA splicing factors at sites of RNA polymerase II transcription. Genes Dev. 11, 1148-1159
37. Mathew, R., Hartmuth, K., Möhlmann, S., Urlaub, H., Ficner, R., and Lührmann, R. (2008) Phosphorylation of human PRP28 by SRPK2 is required for integration of the U4/U6-U5 tri-snRNP into the spliceosome. Nat. Struct. Mol. Biol. 15, 435-443
38. Muñoz, M. J., de la Mata, M., and Kornblihtt, A. R. (2010) The carboxy terminal domain of RNA polymerase II and alternative splicing. Trends Biochem. Sci. 35, 497-504
39. Danoff, S. K., Ferris, C. D., Donath, C., Fischer, G. A., Munemitsu, S., Ullrich, A., Snyder, S. H., and Ross, C. A. (1991) Inositol 1,4,5-trisphosphate receptors: distinct neuronal and nonneuronal forms derived by alternative splicing differ in phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 88, 2951-2955
40. Nakagawa, T., Shiota, C., Okano, H., and Mikoshiba, K. (1991) Differential localization of alternative spliced transcripts encoding inositol 1,4,5-trisphosphate receptors in mouse cerebellum and hippocampus: in situ hybridization study. J. Neurochem. 57, 1807-1810
41. Nucifora, F. C., Jr., Li, S. H., Danoff, S., Ullrich, A., and Ross, C. A. (1995) Molecular cloning of a cDNA for the human inositol 1,4,5-trisphosphate receptor type 1, and the identification of a third alternatively spliced variant. Brain. Res. Mol. Brain Res. 32, 291-296
42. Varjosalo, M., Keskitalo, S., Van Drogen, A., Nurkkala, H., Vichalkovski, A., Aebersold, R., and Gstaiger, M. (2013) The protein interaction landscape of the human CMGC kinase group. Cell Rep. 3, 1306-1320
43. Becker, R., Loll, B., and Meinhart, A. (2008) Snapshots of the RNA processing factor SCAF8 bound to different phosphorylated forms of the carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 283, 22659-22669
44. Das, R., Yu, J., Zhang, Z., Gygi, M. P., Krainer, A. R., Gygi, S. P., and Reed, R. (2007) SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Mol. Cell 26, 867-881
45. Montaville, P., Dai, Y., Cheung, C. Y., Giller, K., Becker, S., Michalak, M., Webb, S. E., Miller, A. L., and Krebs, J. (2006) Nuclear translocation of the calcium-binding protein ALG-2 induced by the RNA-binding protein RBM22. Biochim. Biophys. Acta 1763, 1335-1343
46. Rasche, N., Dybkov, O., Schmitzová, J., Akyildiz, B., Fabrizio, P., and Lührmann, R. (2012) Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre. EMBO J. 31, 1591-1604
47. Choi, J. Y., Beaman-Hall, C. M., and Vallano, M. L. (2004) Granule neurons in cerebellum express distinct splice variants of the inositol trisphosphate receptor that are modulated by calcium. Am. J. Physiol. Cell Physiol. 287, C971-C980
48. Schell, M. J., Danoff, S. K., and Ross, C. A. (1993) Inositol (1,4,5)-trisphosphate receptor: characterization of neuron-specific alternative splicing in rat brain and peripheral tissues. Brain Res. Mol. Brain Res. 17, 212-216
49. Wagner, L. E., 2nd, Li, W. H., and Yule, D. I. (2003) Phosphorylation of type-1 inositol 1,4,5-trisphosphate receptors by cyclic nucleotide-dependent protein kinases: a mutational analysis of the functionally important sites in the S2+ and S2 - splice variants. J. Biol. Chem. 278, 45811-45817
50. Xie, J., and Black, D. L. (2001) A CaMK IV responsive RNA element mediates depolarization-induced alternative splicing of ion channels. Nature 410, 936-939
51. Rozic-Kotliroff, G., and Zisapel, N. (2007) Ca2+-dependent splicing of neurexin IIα. Biochem. Biophys. Res. Commun. 352, 226-230
52. Li, Q., Lee, J. A., and Black, D. L. (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci. 8, 819-831
53. Xie, J. (2008) Control of alternative pre-mRNA splicing by Ca2+ signals. Biochim. Biophys. Acta 1779, 438-452
54. Krebs, J., Groenendyk, J., and Michalak, M. (2011) Ca2+-signaling, alternative splicing and endoplasmic reticulum stress responses. Neurochem. Res. 36, 1198-1211