Interchangeable SF3B1 inhibitors interfere with pre-mRNA splicing at multiple stages

RNA

Volumn 22, Issue 3, 2016, Pages 350-359

  Effenberger, Kerstin A ^a   Urabe, Veronica K ^a   Prichard, Beth E ^a   Ghosh, Arun K ^b,c   Jurica, Melissa S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PURDUE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Inhibitor; Pre mRNA splicing; SF3B1; Spliceosome

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOTOXIC AGENT; HEPARIN; OLIGONUCLEOTIDE; PROTEIN INHIBITOR; SF3B1 INHIBITOR; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; MESSENGER RNA; PHOSPHOPROTEIN; RNA PRECURSOR; RNA SPLICING FACTOR; SF3B1 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL CYCLE; CLINICAL ASSESSMENT; CLINICAL EVALUATION; CONFORMATIONAL TRANSITION; ENZYME INHIBITION; IN VITRO STUDY; INTRON; MOLECULAR RECOGNITION; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA SPLICING; SPLICEOSOME; ANTAGONISTS AND INHIBITORS; BINDING SITE; EXON; GENETICS; HUMAN; METABOLISM;

ADENOSINE TRIPHOSPHATE; BINDING SITES; EXONS; HUMANS; PHOSPHOPROTEINS; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA PRECURSORS; RNA SPLICING; RNA SPLICING FACTORS; RNA, MESSENGER;

EID: 84958691928     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.053108.115     Document Type: Article

References (54)

1. Agafonov DE, Deckert J, Wolf E, Odenwalder P, Bessonov S, Will CL, Urlaub H, Luhrmann R. 2011. Semiquantitative proteomic analysis of the human spliceosome via a novel two-dimensional gel electrophoresis method. Mol Cell Biol 31: 2667-2682.
2. Albert BJ, Mcpherson PA, O'Brien K, Czaicki NL, Destefino V, Osman S, Li M, Day BW, Grabowski PJ, Moore MJ, et al. 2009. Meayamycin inhibits pre-messenger RNA splicing and exhibits picomolar activity against multidrug-resistant cells. Mol Cancer Therapeutics 8: 2308-2318.
3. Anderson K, Moore MJ. 1997. Bimolecular exon ligation by the human spliceosome. Science 276: 1712-1716.
4. Arai K, Buonamici S, Chan B, Corson L, Endo A, Gerard B, Hao MH, Karr C, Kira K, Lee L, et al. 2014. Total synthesis of 6-deoxypladienolide D and assessment of splicing inhibitory activity in a mutant SF3B1 cancer cell line. Org Lett 16: 5560-5563.
5. Black DL, Steitz JA. 1986. Pre-mRNA splicing in vitro requires intact U4/U6 small nuclear ribonucleoprotein. Cell 46: 697-704.
6. Black DL, Chabot B, Steitz JA. 1985. U2 as well as U1 small nuclear ribonucleoproteins are involved in premessenger RNA splicing. Cell 42: 737-750.
7. 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.
8. Brosi R, Hauri HP, Kramer A. 1993. Separation of splicing factor SF3 into two components and purification of SF3a activity. J Biol Chem 268: 17640-17646.
9. Coltri P, Effenberger K, Chalkley RJ, Burlingame AL, Jurica MS. 2010. Breaking up the C complex spliceosome shows stable association of proteins with the lariat intron intermediate. PLoS One 6: e19061.
10. Convertini P, Shen M, Potter PM, Palacios G, Lagisetti C, de la Grange P, Horbinski C, Fondufe-Mittendorf YN, Webb TR, Stamm S. 2014. Sudemycin E influences alternative splicing and changes chromatin modifications. Nucleic Acids Res 42: 4947-4961.
11. Corrionero A, Minana B, Valcarcel J. 2011. Reduced fidelity of branch point recognition and alternative splicing induced by the anti-tumor drug spliceostatin A. Genes Dev 25: 445-459.
12. Dignam JD, Lebovitz RM, Roeder RD. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475-1489.
13. Effenberger KA, Perriman RJ, Bray WM, Lokey RS, AresMJr, Jurica MS. 2013. A high-throughput splicing assay identifies new classes of inhibitors of human and yeast spliceosomes. J Biomol Screen 18: 1110-1120.
14. Effenberger KA, Anderson DD, Bray WM, Prichard BE, Ma N, Adams MS, Ghosh AK, Jurica MS. 2014. Coherence between cellular responses and in vitro splicing inhibition for the anti-tumor drug pladienolide B and its analogs. J Biol Chem 289: 1938-1947.
15. Eskens FA, Ramos FJ, Burger H, O'Brien JP, Piera A, de Jonge MJ, Mizui Y, Wiemer EA, Carreras MJ, Baselga J, et al. 2013. Phase I, pharmacokinetic and pharmacodynamic study of the first-in-class spliceosome inhibitor E7107 in patients with advanced solid tumors. Clin Cancer Res 19: 6296-6304.
16. Fan L, Lagisetti C, Edwards CC, Webb TR, Potter PM. 2011. Sudemycins, novel small molecule analogues of FR901464, induce alternative gene splicing. ACS Chem Biol 6: 582-589.
17. Folco EG, Coil KE, Reed R. 2011. The anti-tumor drug E7107 reveals an essential role for SF3b in remodeling U2 snRNP to expose the branch point-binding region. Genes Dev 25: 440-444.
18. Gao Y, Vogt A, Forsyth CJ, Koide K. 2013. Comparison of splicing factor 3b inhibitors in human cells. Chembiochem 14: 49-52.
19. Ghosh AK, Anderson DD. 2012. Enantioselective total synthesis of pladienolide B: a potent spliceosome inhibitor. Org Lett 14: 4730-4733.
20. Ghosh AK, Chen ZH. 2013. Enantioselective syntheses of FR901464 and spliceostatin A: potent inhibitors of spliceosome. Org Lett 15: 5088-5091.
21. Ghosh AK, Li J. 2011. A stereoselective synthesis of (+)-herboxidiene/GEX1A. Org Lett 13: 66-69.
22. Ghosh AK, Chen ZH, Effenberger KA, Jurica MS. 2014a. Enantioselective total syntheses of FR901464 and spliceostatin A and evaluation of splicing activity of key derivatives. J Org Chem 79: 5697-5709.
23. Ghosh AK, Ma N, Effenberger KA, Jurica MS. 2014b. Total synthesis of GEX1Q1, assignment of C-5 stereoconfiguration and evaluation of spliceosome inhibitory activity. Org Lett 16: 3154-3157.
24. Ghosh AK, Veitschegger AM, Sheri VR, Effenberger KA, Prichard BE, Jurica MS. 2014c. Enantioselective synthesis of spliceostatin E and evaluation of biological activity. Org Lett 16: 6200-6203.
25. Gozani O, Feld R, Reed R. 1996. Evidence that sequence-independent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes Dev 10: 233-243.
26. Gozani O, Potashkin J, Reed R. 1998. A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol Cell Biol 18: 4752-4760.
27. Gundluru MK, Pourpak A, Cui X, Morris SW, Webb TR. 2011. Design, synthesis and initial biological evaluation of a novel pladienolide analog scaffold. Medchemcomm 2: 904-908.
28. Hasegawa M, Miura T, Kuzuya K, Inoue A, Won Ki S, Horinouchi S, Yoshida T, Kunoh T, Koseki K, Mino K, et al. 2011. Identification of SAP155 as the target of GEX1A (Herboxidiene), an antitumor natural product. ACS Chem Biol 6: 229-233.
29. He H, Ratnayake AS, Janso JE, He M, Yang HY, Loganzo F, Shor B, O'Donnell CJ, Koehn FE. 2014. Cytotoxic spliceostatins from Burkholderia sp. and their semisynthetic analogues. J Nat Prod 77: 1864-1870.
30. Hilliker AK, Mefford MA, Staley JP. 2007. U2 toggles iteratively between the stem IIa and stem IIc conformations to promote pre-mRNA splicing. Genes Dev 21: 821-834.
31. Ilagan JO, Chalkley RJ, Burlingame AL, Jurica MS. 2013. Rearrangements within human spliceosomes captured after exon ligation. RNA 19: 400-412.
32. Kaida D, Motoyoshi H, Tashiro E, Nojima T, Hagiwara M, Ishigami K, Watanabe H, Kitahara T, Yoshida T, Nakajima H, et al. 2007. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat Chem Biol 3: 576-583.
33. Konforti BB, Konarska MM. 1995. A short 5' splice site RNA oligo can participate in both steps of splicing in mammalian extracts. RNA 1: 815-827.
34. Kotake Y, Sagane K, Owa T, Mimori-Kiyosue Y, Shimizu H, Uesugi M, Ishihama Y, Iwata M, Mizui Y. 2007. Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat Chem Biol 3: 570-575.
35. Lagisetti C, Pourpak A, Jiang Q, Cui X, Goronga T, Morris SW, Webb TR. 2008. Antitumor compounds based on a natural product consensus pharmacophore. J Med Chem 51: 6220-6224.
36. Lagisetti C, Pourpak A, Goronga T, Jiang Q, Cui X, Hyle J, Lahti JM, Morris SW, Webb TR. 2009. Synthetic mRNA splicing modulator compounds with in vivo antitumor activity. J Med Chem 52: 6979-6990.
37. Lagisetti C, Palacios G, Goronga T, Freeman B, Caufield W, Webb TR. 2013. Optimization of antitumor modulators of pre-mRNA splicing. J Med Chem 56: 10033-10044.
38. Lagisetti C, Yermolina MV, Sharma LK, Palacios G, Prigaro BJ, Webb TR. 2014. Pre-mRNA splicing-modulatory pharmacophores: the total synthesis of herboxidiene, a pladienolide-herboxidiene hybrid analog and related derivatives. ACS Chem Biol 9: 643-648.
39. Lardelli RM, Thompson JX, Yates JR III, Stevens SW. 2010. Release of SF3 from the intron branchpoint activates the first step of premRNA splicing. RNA 16: 516-528.
40. Liu X, Biswas S, Berg MG, Antapli CM, Xie F, Wang Q, Tang MC, Tang GL, Zhang L, Dreyfuss G, et al. 2013. Genomics-guided discovery of thailanstatins A, B, and C As pre-mRNA splicing inhibitors and antiproliferative agents from Burkholderia thailandensis MSMB43. J Nat Prod 76: 685-693.
41. Mizui Y, Sakai T, Iwata M, Uenaka T, Okamoto K, Shimizu H, Yamori T, Yoshimatsu K, Asada M. 2004. Pladienolides, new substances from culture of Streptomyces platensis Mer-11107. III. In vitro and in vivo antitumor activities. J Antibiot (Tokyo) 57: 188-196.
42. Muller S, Mayer T, Sasse F, Maier ME. 2011. Synthesis of a pladienolide B analogue with the fully functionalized core structure. Org Lett 13: 3940-3943.
43. Nakajima H, Hori Y, Terano H, Okuhara M, Manda T, Matsumoto S, Shimomura K. 1996a. New antitumor substances, FR901463, FR901464 and FR901465. II. Activities against experimental tumors in mice and mechanism of action. J Antibiot (Tokyo) 49: 1204-1211.
44. Nakajima H, Sato B, Fujita T, Takase S, Terano H, Okuhara M. 1996b. New antitumor substances, FR901463, FR901464 and FR901465. I. Taxonomy, fermentation, isolation, physico-chemical properties and biological activities. J Antibiot (Tokyo) 49: 1196-1203.
45. Perriman RJ, Ares M Jr. 2007. Rearrangement of competing U2 RNA helices within the spliceosome promotes multiple steps in splicing. Genes Dev 21: 811-820.
46. Perriman R, Ares M Jr. 2010. Invariant U2 snRNA nucleotides form a stem loop to recognize the intron early in splicing. Mol Cell 38: 416-427.
47. Perriman R, Barta I, Voeltz GK, Abelson J, AresMJr. 2003. ATP requirement for Prp5p function is determined by Cus2p and the structure of U2 small nuclear RNA. Proc Natl Acad Sci 100: 13857-13862.
48. Roybal GA, Jurica MS. 2010. Spliceostatin A inhibits spliceosome assembly subsequent to prespliceosome formation. Nucleic Acids Res 38: 6664-6672.
49. Sakai Y, Tsujita T, Akiyama T, Yoshida T, Mizukami T, Akinaga S, Horinouchi S, Yoshida M, Yoshida T. 2002. GEX1 compounds, novel antitumor antibiotics related to herboxidiene, produced by Streptomyces sp. II. The effects on cell cycle progression and gene expression. J Antibiot (Tokyo) 55: 863-872.
50. Sakai T, Sameshima T, Matsufuji M, Kawamura N, Dobashi K, Mizui Y. 2004. Pladienolides, new substances from culture of Streptomyces platensis Mer-11107. I. Taxonomy, fermentation, isolation and screening. J Antibiot (Tokyo) 57: 173-179.
51. Villa R, Mandel AL, Jones BD, La Clair JJ, Burkart MD. 2012. Structure of FD-895 revealed through total synthesis. Org Lett 14: 5396-5399.
52. Villa R, Kashyap MK, Kumar D, Kipps TJ, Castro JE, La Clair JJ, Burkart MD. 2013. Stabilized cyclopropane analogs of the splicing inhibitor FD-895. J Med Chem 56: 6576-6582.
53. Wassarman DA, Steitz JA. 1992. Interactions of small nuclear RNA's with precursor messenger RNA during in vitro splicing. Science 257: 1918-1925.
54. Yoshida K, Ogawa S. 2014. Splicing factor mutations and cancer. Wiley Interdiscip Rev RNA 5: 445-459.