Multiple components of the spliceosome regulate Mcl1 activity in neuroblastoma

Cell Death and Disease

Volumn 5, Issue 2, 2014, Pages

  Laetsch, T W ^a   Liu, X ^a   Vu, A ^a   Sliozberg, M ^a   Vido, M ^a   Elci, O U ^b   Goldsmith, K C ^c,d   Hogarty, M D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c AFLAC   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

alternative splicing; Bcl2 family; Bcl2 inhibitors; embryonal tumor; experimental therapeutics

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; PROTEIN BCL 2; PROTEIN MCL 1; SMALL INTERFERING RNA;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IC 50; NEUROBLASTOMA; PRIORITY JOURNAL; SPLICEOSOME; TRANSESTERIFICATION;

ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; EYE PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MULTIPROTEIN COMPLEXES; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; NEUROBLASTOMA; PROTEASOME ENDOPEPTIDASE COMPLEX; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA INTERFERENCE; RNA-BINDING PROTEINS; TRANS-ACTIVATORS; TRANSFECTION; UBIQUITINS;

EID: 84896750323     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.40     Document Type: Article

References (61)

1. Youle RJ, Strasser A. The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9: 47-59.
2. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, Hsieh JJ et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 2006; 8: 1348-1358.
3. Goldsmith KC, Lestini BJ, Gross M, Ip L, Bhumbla A, Zhang X et al. BH3 response profiles from neuroblastoma mitochondria predict activity of small molecule Bcl-2 family antagonists. Cell Death Differ 2010; 17: 872-882.
4. Goldsmith KC, Gross M, Peirce S, Luyindula D, Liu X, Vu A et al. Mitochondrial Bcl-2 family dynamics define therapy response and resistance in neuroblastoma. Cancer Res 2012; 72: 2565-2577.
5. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, Belli BA et al. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 2005; 435: 677-681.
6. Lestini BJ, Goldsmith KC, Fluchel MN, Liu X, Chen NL, Goyal B et al. Mcl1 downregulation sensitizes neuroblastoma to cytotoxic chemotherapy and small molecule Bcl2-family antagonists. Cancer Biol Ther 2009; 8: 1587-1595.
7. Akgul C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 2009; 66: 1326-1336.
8. Bingle CD, Craig RW, Swales BM, Singleton V, Zhou P, Whyte MK. Exon skipping in Mcl-1 results in a bcl-2 homology domain 3 only gene product that promotes cell death. J Biol Chem 2000; 275: 22136-22146.
9. Bae J, Leo CP, Hsu SY, Hsueh AJ. MCL-1S, a splicing variant of the antiapoptotic BCL-2 family member MCL-1, encodes a proapoptotic protein possessing only the BH3 domain. J Biol Chem 2000; 275: 25255-25261.
10. Zhong Q, Gao W, Du F, Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005; 121: 1085-1095.
11. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY et al. Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 2007; 27: 4006-4017.
12. Inuzuka H, Fukushima H, Shaik S, Liu P, Lau AW, Wei W. Mcl-1 ubiquitination and destruction. Oncotarget 2011; 2: 239-244.
13. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: A post-Translational modification at the edge of life and death. Nat Rev Mol Cell Biol 2011; 12: 439-452.
14. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM et al. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 2009; 463: 103-107.
15. Ovaa H, Kessler BM, Rolen U, Galardy PJ, Ploegh HL, Masucci MG. Activity-based ubiquitin-specific protease (USP) profiling of virus-infected and malignant human cells. Proc Natl Acad Sci USA 2004; 101: 2253-2258.
16. McNally T, Huang Q, Janis RS, Liu Z, Olejniczak ET, Reilly RM. Structural analysis of UBL5, a novel ubiquitin-like modifier. Protein Sci 2003; 12: 1562-1566.
17. Beverly LJ, Lockwood WW, Shah PP, Erdjument-Bromage H, Varmus H. Ubiquitination, localization, and stability of an anti-Apoptotic BCL2-like protein, BCL2L10/BCLb, are regulated by Ubiquilin1. Proc Natl Acad Sci USA 2012; 109: E119-E126.
18. Mishra SK, Ammon T, Popowicz GM, Krajewski M, Nagel RJ, Ares Jr. M et al. Role of the ubiquitin-like protein Hub1 in splice-site usage and alternative splicing. Nature 2011; 474: 173-178.
19. Shieh JJ, Liu KT, Huang SW, Chen YJ, Hsieh TY. Modification of alternative splicing of Mcl-1 pre-mRNA using antisense morpholino oligonucleotides induces apoptosis in basal cell carcinoma cells. J Invest Dermatol 2009; 129: 2497-2506.
20. Apweiler R, Consortium TU. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res 2010; 38(Supplement 1 database issue): D142-D148.
21. Reed R, Hurt E. A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 2002; 108: 523-531.
22. Pinto AL, Steitz JA. The mammalian analogue of the yeast PRP8 splicing protein is present in the U4/5/6 small nuclear ribonucleoprotein particle and the spliceosome. Proc Natl Acad Sci USA 1989; 86: 8742-8746.
23. Whittaker E, Lossky M, Beggs JD. Affinity purification of spliceosomes reveals that the precursor RNA processing protein PRP8, a protein in the U5 small nuclear ribonucleoprotein particle, is a component of yeast spliceosomes. Proc Natl Acad Sci USA 1990; 87: 2216-2219.
24. Makarova OV, Makarov EM, Luhrmann R. The 65 and 110 kDa SR-related proteins of the U4/U6.U5 tri-snRNP are essential for the assembly of mature spliceosomes. EMBO J 2001; 20: 2553-2563.
25. Hegele A, Kamburov A, Grossmann A, Sourlis C, Wowro S, Weimann M et al. Dynamic protein-protein interaction wiring of the human spliceosome. Mol Cell 2012; 45: 567-580.
26. Kaida D, Motoyoshi H, Tashiro E, Nojima T, Hagiwara M, Ishigami K et al. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat Chem Biol 2007; 3: 576-583.
27. Berg MG, Wan L, Younis I, Diem MD, Soo M, Wang C et al. A quantitative high-Throughput in vitro splicing assay identifies inhibitors of spliceosome catalysis. Mol Cell Biol 2012; 32: 1271-1283.
28. Versteeg R. R2: Microarray analysis and visualization platform (http://r2.amc.nl).
29. Hanahan D,Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
30. Davids MS, Deng J, Wiestner A, Lannutti BJ, Wang L, Wu CJ et al. Decreased mitochondrial apoptotic priming underlies stroma-mediated treatment resistance in chronic lymphocytic leukemia. Blood 2012; 120: 3501-3509.
31. Roberts AW, Seymour JF, Brown JR, Wierda WG, Kipps TJ, Khaw SL et al. Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: Results of a phase I study of navitoclax in patients with relapsed or refractory disease. J Clin Oncol 2012; 30: 488-496.
32. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 2006; 10: 389-399.
33. Morales AA, Kurtoglu M, Matulis SM, Liu J, Siefker D, Gutman DM et al. Distribution of Bim determines Mcl-1 dependence or codependence with Bcl-xL/Bcl-2 in Mcl-1-expressing myeloma cells. Blood 2011; 118: 1329-1339.
34. D'Arcy P, Brnjic S, Olofsson MH, Fryknas M, Lindsten K, De Cesare M et al. Inhibition of proteasome deubiquitinating activity as a new cancer therapy. Nat Med 2011; 17: 1636-1640.
35. Sveda M, Castoralova M, Lipov J, Ruml T, Knejzlik Z. Human UBL5 protein interacts with coilin and meets the Cajal bodies. Biochem Biophys Res Commun 2013; 436: 240-245.
36. van der Feltz C, Anthony K, Brilot A, Pomeranz Krummel DA. Architecture of the spliceosome. Biochemistry (Mosc) 2012; 51: 3321-3333.
37. Roybal GA, Jurica MS. Spliceostatin A inhibits spliceosome assembly subsequent to prespliceosome formation. Nucleic Acids Res 2010; 38: 6664-6672.
38. Moore MJ, Wang Q, Kennedy CJ, Silver PA. An alternative splicing network links cell-cycle control to apoptosis. Cell 2010; 142: 625-636.
39. Gautrey HL, Tyson-Capper AJ. Regulation of Mcl-1 by SRSF1 and SRSF5 in cancer cells. PLoS One 2012; 7: E51497.
40. Michlewski G, Sanford JR, Caceres JF. The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Mol Cell 2008; 30: 179-189.
41. Mills JR, Hippo Y, Robert F, Chen SM, Malina A, Lin CJ et al. mTORC1 promotes survival through translational control of Mcl-1. Proc Natl Acad Sci USA 2008; 105: 10853-10858.
42. Schwerk C, Schulze-Osthoff K. Regulation of apoptosis by alternative pre-mRNA splicing. Mol Cell 2005; 19: 1-13.
43. Akgul C, Moulding DA, Edwards SW. Alternative splicing of Bcl-2-related genes: Functional consequences and potential therapeutic applications. Cell Mol Life Sci 2004; 61: 2189-2199.
44. Grabowski P. Alternative splicing takes shape during neuronal development. Curr Opin Genet Dev 2011; 21: 388-394.
45. Lim DA, Suarez-Farinas M, Naef F, Hacker CR, Menn B, Takebayashi H et al. In vivo transcriptional profile analysis reveals RNA splicing and chromatin remodeling as prominent processes for adult neurogenesis. Mol Cell Neurosci 2006; 31: 131-148.
46. An M, Henion PD. The zebrafish sf3b1b460 mutant reveals differential requirements for the sf3b1 pre-mRNA processing gene during neural crest development. Int J Dev Biol 2012; 56: 223-237.
47. Keightley MC, Crowhurst MO, Layton JE, Beilharz T, Markmiller S, Varma S et al. In vivo mutation of pre-mRNA processing factor 8 (Prpf8) affects transcript splicing, cell survival and myeloid differentiation. FEBS Lett 2013; 587: 2150-2157.
48. Pena V, Liu S, Bujnicki JM, Luhrmann R, Wahl MC. Structure of a multipartite protein-protein interaction domain in splicing factor prp8 and its link to retinitis pigmentosa. Mol Cell 2007; 25: 615-624.
49. Zhang B, Gojo I, Fenton RG. Myeloid cell factor-1 is a critical survival factor for multiple myeloma. Blood 2002; 99: 1885-1893.
50. Tiedemann RE, Zhu YX, Schmidt J, Shi CX, Sereduk C, Yin H et al. Identification of molecular vulnerabilities in human multiple myeloma cells by RNA interference lethality screening of the druggable genome. Cancer Res 2012; 72: 757-768.
51. Bonnal S, Vigevani L, Valcarcel J. The spliceosome as a target of novel antitumour drugs. Nat Rev Drug Discov 2012; 11: 847-859.
52. Maciejewski JP, Padgett RA. Defects in spliceosomal machinery: A new pathway of leukaemogenesis. Br J Haematol 2012; 158: 165-173.
53. Bergen III HR, Vasmatzis G, Cliby WA, Johnson KL, Oberg AL, Muddiman DC. Discovery of ovarian cancer biomarkers in serum using NanoLC electrospray ionization TOF and FT-ICR mass spectrometry. Dis Markers 2003; 19: 239-249.
54. van Alphen RJ, Wiemer EA, Burger H, Eskens FA. The spliceosome as target for anticancer treatment. Br J Cancer 2009; 100: 228-232.
55. Nakajima H, Hori Y, Terano H, Okuhara M, Manda T, Matsumoto S et al. New antitumor substances, FR901463, FR901464 and FR901465. II. Activities against experimental tumors in mice and mechanism of action. J Antibiot 1996; 49: 1204-1211.
56. Lagisetti C, Pourpak A, Goronga T, Jiang Q, Cui X, Hyle J et al. Synthetic mRNA splicing modulator compounds with in vivo antitumor activity. J Med Chem 2009; 52: 6979-6990.
57. Gao Y, Koide K. Chemical perturbation of Mcl-1 pre-mRNA splicing to induce apoptosis in cancer cells. ACS Chem Biol 2013; 8: 895-900.
58. Tumilowicz JJ, Nichols WW, Cholon JJ, Greene AE. Definition of a continuous human cell line derived from neuroblastoma. Cancer Res 1970; 30: 2110-2118.
59. Schlesinger HR, Gerson JM, Moorhead PS, Maguire H, Hummeler K. Establishment and characterization of human neuroblastoma cell lines. Cancer Res 1976; 36(9 pt.1): 3094-3100.
60. Kocak H, Ackermann S, Hero B, Kahlert Y, Oberthuer A, Juraeva D et al. Hox-C9 activates the intrinsic pathway of apoptosis and is associated with spontaneous regression in neuroblastoma. Cell Death Dis 2013; 4: E586.
61. Molenaar JJ, Domingo-Fernandez R, Ebus ME, Lindner S, Koster J, Drabek K et al. LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression. Nat Genetics 2012; 44: 1199-1206.