A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs

RNA

Volumn 3, Issue 12, 1997, Pages 1374-1387

  Horowitz, David S ^a,b   Kobayashi, Ryuji ^a   Krainer, Adrian R ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Pre mRNA splicing; USA CyP; WD motif

Indexed keywords

COMPLEMENTARY DNA; CYCLOPHILIN; FUNGAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; NUCLEAR PROTEINS; PEPTIDES; PEPTIDYLPROLYL ISOMERASE; PROTEIN-SERINE-THREONINE KINASES; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

SACCHAROMYCES CEREVISIAE;

EID: 0031440025     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Abovich N, Legrain P, Rosbash M. 1990. The yeast PRP6 gene encodes a U4/U6 small nuclear ribonucleoprotein particle (snRNP) protein, and the PRP9 gene encodes a protein required for U2 snRNP binding. Mol Cell Biol 10:6417-6425.
2. Anderson SK, Gallinger S, Roder J, Frey J, Young HA, Ortaldo JR. 1993. A cyclophilin-related protein involved in the function of natural killer cells. Proc Natl Acad Sci USA 90:542-546.
3. Anthony JG, Weidenhammer EM, Woolford JL Jr. 1997. The yeast Prp3 protein is a U4/U6 snRNP protein necessary for integrity of the U4/U6 snRNP and the U4/U6.U5 tri-snRNP. RNA 3:1143-1152.
4. Ares M Jr, Weiser B. 1995. Rearrangement of snRNA structure during assembly and function of the spliceosome. Prog Nucleic Acid Res Mol Biol 50:131-159.
5. Ayadi L. Miller M. Banroques J. 1997. Mutations within the yeast U4/U6 snRNP protein Prp4 affect a late stage of spliceosome assembly RNA 3:197-209.
6. Baker EK, Collry NJ, Zuker CS. 1994. The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J 13:4886-4895.
7. Banroques J. Abelson JN. 1989. PRP4: A protein of the yeast U4/U6 small nuclear ribonucleoprotein particle. Mol Cell Biol 9:3710-3719.
8. Behrens SE, Lührmann R. 1991. Immunoaffinity purification of a [U4/U6.U5] tri-snRNP for human cells. Gents & Dev 5:1439-1452.
9. Black DL, Pinto AL. 1989. U5 small nuclear ribonucleoprotein: RNA structure analysis and ATP-dependent interaction with U4/U6. Mol Cell Biol 9:3350-3359.
10. Blencowe BJ, Carmo-Fonseca M, Behrens SE, Lührmann R, Lamond AI. 1993. Interaction of the human autoantigen p150 with splicing snRNPs. J Cell Sci 105:685-697.
11. Blencowe BJ, Sproat BS, Ryder U, Barabino S, Lamond AI. 1989. Antisense probing of the human U4/U6 snRNP with biotinylated 2′-OMe RNA oligonucleotides. Cell 59:531-539.
12. Bordonné R, Banroques J, Abelson J, Guthrie C. 1990. Domains of yeast U4 spliceosomal RNA required for PRP4 protein binding. snRNP-snRNP interactions, and pre-mRNA splicing in vivo. Genes & Dev 4:1185-1196.
13. Bose S, Weiki T, Bügl H, Buchner J. 1996. Chaperone function of Hsp90-associated proteins. Science 274:1715-1717.
14. Bourquin JP, Stagljar I, Meier P, Moosmann P, Silke J, Baechl T, Georgiev O, Schaffner W. 1997. A serine/arginine-rich nuclear matrix cyclophilin interacts with the C-terminal domain of RNA polymerase II. Nucleic Acids Res 25:2055-2061.
15. Braaten D, Franke EK, Luban J. 1996. Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J Virol 70:3551-3560.
16. Bringmann P, Appel B, Rinke J, Reuter R, Theissen H, Lührmann R. 1984. Evidence for the existence of snRNAs U4 and U6 in a single ribonucleoprotin complex and for their association by intermolecular base pairing. EMBO J 3:1357-1363.
17. Cheng SC, Abelson J. 1987. Spliceosome assembly in yeast. Genes & Dev 1:1014-1027.
18. Cooper M, Johnston LH, Beggs JD. 1995. Identification and characterization of Uss1p (Sdb23p): A novel U6 snRNA-associated protein with significant similarity to core proteins of small nuclear ribonucleoproteins. EMBO J 14:2066-2075.
19. Dalrymple MA, Petersen-Bjørn S, Friesen JD, Beggs JD. 1989. The product of the PRP4 gene of S. cerevisiae shows homology to β subunits of G proteins. Cell 58:811-812.
20. Dignam JD, Lebovitz RM, Reeder RG. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei, Nucleic Acids Res 11:1475-1489.
21. Duina AA, Marsh JA, Green RF. 1996. Identification of two CyP-40-like cyclophilins in Saccharonyces cerevisiae, one of which is required for normal growth. Yeast 12:943-952.
22. Fabnzio P, McPheeters DS, Abelson J. 1989. In vitro assembly of yeast U6 snRNP: A functional assay. Genes & Dev 3:2137-2150.
23. Fischer G, Wittman-Liebold B, Lang K, Kiefhaber T, Schmid FX. 1989. Cyclophilin and peptifyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337:476-478.
24. Franke EK, Yuan HEH, Luban J. 1994. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 374:359-362.
25. Freeman BC, Toft DO, Morimoto RJ. 1996. Molecular chaperone machines: Chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274:1718-1720.
26. Fujii T, Mimori T, Hama N, Suwa A, Akizuki M, Tojo T, Homma M. 1992. Characterization of autoantibodies that recognize U4/U6 small ribonucleoprotein particles in serum from a patient with primary Sjögren's syndrome. J Biol Chem 267:16412-16416.
27. Galat A, Metcalfe SM, 1995. Peptidylproline cis/trans isomerases. Prog Biophys Mol Biol 63:67-118.
28. Galisson F, Legrain P. 1993. The biochemical defects of prp4-1 and prp6-1 yeast splicing mutants reveal that the PRP6 protein is required for the accumulation of the [U4/U6.U5] tri-snRNP. Nucleic Adcis Res 21:1555-1562.
29. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, Hill CP. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285-1294.
30. GCG. 1996. Wisconsin Package Version 9.0. Madison, Wisconsin, USA: Genetics Computer Group.
31. Gething MJ, Sambcook J. 1992. Protein folding in the cell. Nature 355:33-45.
32. Gitti RK, Lee BM, Walker J, Summers MF, Yoo S, Sundquist WI. 1996. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273:231-235.
33. Gozani O, Patton JD, Reed R. 1994. A novel set of spliceosome-assiciated proteins and the essential splicing factor PSF bind stably to pre-mRNA prior to catalytic step II of the splicing reaction. EMBO J 13:3356-3367.
34. Handtchumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW, 1984. Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science 226:544-547.
35. Hashimoto C, Steitz JA. 1984. U4 and U6 RNAs coexist in a single small nuclear ribonucleoprotein particle. Nucleic Acids Res 9:3283-3293.
36. Henikoff S, Henikoff JG. 1994. Protein family classification based on searching a database of blocks. Genomics 19:97-107.
37. Hinterberger M, Pettersson I, Steitz JA. 1983. Isolation of small nuclear ribonucleoproteins containing U1, U2, U4, U5, and U6 RNAs. J Biol Chem 258:2604-2613.
38. Horowitz DS, Krainer AR. 1997. A human protein required for the second step of pre-mRNA splicing is functionally related to a yeast splicing favator. Genes & Dev 11:139-151.
39. Hu J, Xu Y, Schappert K, Harrington T, Wang A, Braga R, Mogridge J, Friesen JD. 1994. Mutational analysis of the PRP4 protein of Saccharomyces cerevisiae suggests domain structure and snRNP interactions. Nuclic Acids Res 22:1724-1734.
40. Hwang BJ, Chu G. 1996. Trichloroacetic acid precipitation by ultracentrifugation to concentrate dilute protein in viscous solution. Biotechniques 20:982-984.
41. Jendrisak JJ, Burgess RR. 1975. A new method for the large-scale purification of wheat germ DNA-dependent RNA poluymerase III. Biochemistry 14:4639-4645.
42. Kieffer LJ, Thalhammer T, Handschumacher RE. 1992. Isolation and characterization of a 40-kDa cyclophilin-related protein. J Biol Chem 367:5503-5507.
43. Konarska MM, Sharp PA. 1987. Interactions between small nuclear ribonucleoprotein particls in formation of spliceosomes. Cell 49:763-774.
44. Lambwright DG, Sondek J, Bohm A, Skiba NP, Hamm HE, Sigler PB. 1996. The 20 Å crystal structure of a heterotrimeric G protein. Nature 379:311-319.
45. Last RL, Maddock JR, Woolford JL Jr. 1987. Evidence for related functions of the RNA genes of Saccharomyces cerevisiae. Genetics 117:619-631.
46. Laube J, Fabrizio P, Teigelkamp S, Lane WS, Hartmann E, Lührmann R. 1996. The HeLa 200 kDa U5 snRNP-specific protein and its homologue in Saccharomyces cerevisiae are member of the DEXH-bpx protein family of putative RNA helicases. EMBO J 15:4001-4015.
47. Lauber J, Plessel G, Perhn S, Will CL, Fabrizio P, Gröning K, Lane WS, Lührmann R. 1997. The human U4/U6 snRNP contains 60 and 90 KD proteins that are structurally homologous to the yeast splicing factors Prp4p and Prp3p. RNA 3:936-941.
48. Lossky M, Anderson GJ, Jackson SP, Beggs J. 1987. Identification of a yeast snRNP protein and detection of snRNP-snRNp interactions. Cell 51:1019-1026.
49. Luban J. 1996. Absconding with the chaperone; Essential cyclophilin-Gag interaction in HIV-1 virions. Cell 87:1157-1159.
50. Lustig AJ, Lin RJ, Abelson J. 1986. The yeast RNA gene products are essential for mRNA splicing in vitro. Cell 47:953-963.
51. Maddock JR, Wiedenhammer EM, Adams CC, Lunz RL, Woolford JL Jr. 1994. Extragenic suppressors of Saccharomyces cerevisiae prp4 mutations identify a negative regulator of PRP genes. Genetics 136:833-847.
52. Madhani HD, Guthrie C. 1994. Dynamic RNA-RNA interactions in the spliceosome. Annu Rev Genet 28:1-26.
53. Marks AR. 1996. Cellular functions of immunophilins. Physiol Rev 76:631-649.
54. Mi H, Kops O, Zimmermann E, Jäschke A, Tropschug M. 1996. A nuclear RNA-binding cyclophilin in human T Cells. FEBS Lett 398:201-205.
55. Neer EJ, Schmidt CJ, Nambudripad R, Smith TF. 1994. The ancient regulatory-protein family of WD-repeat proteins. Nature 371:297-300.
56. Neer EJ, Smith TF. 1996. G protein heterodimers: New structures propel new questions. Cell 84:175-178.
57. Nestel FP, Colwill K, Harper S, Pawson T, Anderson SK. 1996. RS cyclophilins: Identification of and Nk-TRI related cyclophilin. Gene 180:151-155.
58. Nilsen TW. 1994. RNA-RNA interactions in the spliceosome: Unraveling the ties that bind. Cell 78:1-4.
59. Okano Y, Medsger TA Jr. 1991. Newly identified U4/U6 snRNP-binding proteins by serum autoantibodied from a patient with systemic sclerosis. J Immunol 146:535-542.
60. Page AP, MacNiven K, Hengartner MO. 1996. Cloning and biochemical characterization of the cyclophilin homologues from the free-living nematode Caenohabditis elegans. Biochem J 317:179-185.
61. Petersen-Bjørn S, Soltyk A, Beggs JD, Friesen JD. 1989. PRP4 (RNA4) from Saccharomyces cerevisiae: Its gene product is asspciated with the U4/U6 small nuclear ribonucleoprotein particle. Mol Cell Biol 9:3698-3709.
62. Rosbash M, Harris PK, Woolford JL, Teem JL. 1981. The effect of temperature-sensitive rna mutants on the transcription products from cloned ribosomal genes of yeast. Cell 24:679-686.
63. Rutherford SL, Zuker CS. 1994. Protein folding and the regulation of signaling pathways. Cell 79:1129-1132.
64. Schreiber SL, Crabtree DR. 1992. The mechanism of action of cyclosporin A and FK506. Immunol Today 13:136-142.
65. Shannon KW, Guthrie C. 1991 Suppressors of a U4 snRNA mutation define a novel U6 snRNP protein with RNA-binding motifs. Genes & Dev 5:773-785.
66. A protein βγ dimer at 2.1 Å resolution. Nature 379:369-374.
67. Stamnes MA, Rutherford SL, Zuker CS. 1992. Cyclophilins: A new family of proteins involved in intracellular folding. Trends Cell Biol 2:272-276.
68. Takahashi N, Hayano T, Suzuki M. 1989. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337:473-475.
69. Tam YC, Lee KR, Cheng SC. 1993. Yeast precursor mRNA processing protein PRP19 associates with the spliceosome concomitant with or just after the dissociation of U4 small nuclear RNA. Proc Natl Acad Sci USA 90:10821-10825.
70. Thali M, Bukovsky A, Kondo E, Rosenwirth B, Walsh CT, Sodroski J, Göttlinger HG. 1994. Functional association of cyclophilin A with HIV-1 virions. Nature 372:363-365.
71. Trandinh CC, Pao GM, Saier MH Jr. 1992. Structural and evolutionary relationships among the immunophilins: Two ubiquitous families of peptidyl-prolyl cis-trand isometases. FASEB J 6:3410-3420.
72. Utans U, Beherns SE, Lührmann R, Kole R, Krämer A. 1992. A splicing factor that is inactivated during in vivo heat shock is functionally equivalent to the [U4/U6-U5] triple snRNP-specific proteins. Genes & Dev 6:631-641.
73. 2. Cell 83:1047-1058.
74. Will CL, Lührmann R. 1997. snRNP structure and function. In: Krainer AR, ed. Eukaryotic mRNA processing. Oxford: IRL Press. pp 130-173.
75. Wu J, Matunis MJ, Kraemer D, Blobel G, Coutavas E. 1995. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leuclne-rich region. J Biol Chem 270:14209-14213.
76. Xu Y, Peterson-Bjørn S, Friesen JD. 1990. The PRP4 (RNA4) protein of Saccharomyces cerevisiae is associated with the 5′ portion of the U4 small nuclear RNA. Mol Cell Biol 10:1217-1225.
77. Yean SL, Lin RJ. 1991. U4 small nuclear RNA dissociates from a yeast spliceosome and does not particpate in the subsequent splicing reaction. Mol Cell Biol 11:5571-5577.
78. Yokoyama N, Hayashi N, Seki T, Panté N, Ohba T, Nishii K, Kuma K, Hayashida T, Miyata T, Aebi U, Fukui M, Nishimoto T. 1995. A giant nucleopore protein that binds Ran/TC4. Nature 376:184-188.
79. Zhao Y, Chen Y, Schutkowski M, Fischer G, Ke H. 1997. Cyclophilin A compleved with a fragment of HIV-1 gag protein: Insights into HIV-1 infectious activity. Structure 5:139-146.