Discovery of a small molecule targeting IRA2 deletion in budding yeast and neurofibromin loss in malignant peripheral nerve sheath tumor cells

Molecular Cancer Therapeutics

Volumn 10, Issue 9, 2011, Pages 1740-1750

  Wood, Matthew ^a   Rawe, Melissa ^b   Johansson, Gunnar ^b   Pang, Shu ^a   Soderquist, Ryan S ^a   Patel, Ami V ^b   Nelson, Sandra ^c   Seibel, William ^c   Ratner, Nancy ^b   Sanchez, Yolanda ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NAB3 PROTEIN; NEUROFIBROMIN; RAS PROTEIN; RNA BINDING PROTEIN; RNA POLYMERASE II; TUMOR SUPPRESSOR PROTEIN; UC1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE DELETION; GENE INACTIVATION; GENE INTERACTION; MALIGNANT PERIPHERAL NERVE SHEATH TUMOR; NEUROFIBROMATOSIS; NONHUMAN; PERIPHERAL NERVE TUMOR; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CELL LINE; DRUG DISCOVERY; EPISTASIS, GENETIC; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GTPASE-ACTIVATING PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; NERVE SHEATH NEOPLASMS; NEUROFIBROMIN 1; NUCLEAR PROTEINS; PROTEIN KINASES; PYRAZOLES; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SENSITIVITY AND SPECIFICITY; SMALL MOLECULE LIBRARIES; THIOUREA; TRANSCRIPTION, GENETIC;

EID: 80052735880     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-11-0309     Document Type: Article

References (49)

1. Korf BR. Malignancy in neurofibromatosis type 1. Oncologist 2000;5:477-85.
2. Carroll SL, Ratner N.How does the Schwann cell lineage form tumors in NF1? Glia 2008;56:1590-605.
3. Ferner RE, Gutmann DH. International consensus statement on malignant peripheral nerve sheath tumors in neurofibromatosis. Cancer Res 2002;62:1573-7. (Pubitemid 34407825)
4. Evans DG, Baser ME, McGaughran J, Sharif S, Howard E, Moran A. Malignant peripheral nerve sheath tumors in neurofibromatosis 1. J Med Genet 2002;39:311-4. (Pubitemid 34526349)
5. McGaughran JM, Harris DI, Donnai D, Teare D, MacLeod R, Westerbeek R, et al. A clinical study of type 1 neurofibromatosis in north west England. J Med Genet 1999;36:197-203. (Pubitemid 29110448)
6. Porter DE, Prasad V, Foster L, Dall GF, Birch R, Grimer RJ. Survival in malignant peripheral nerve sheath tumors: a comparison between sporadic and neurofibromatosis type 1-associated tumors. Sarcoma 2009;2009:756395.
7. Rutkowski JL, Wu K, Gutmann DH, Boyer PJ, Legius E. Genetic and cellular defects contributing to benign tumor formation in neurofibromatosis type 1. Hum Mol Genet 2000;9:1059-66. (Pubitemid 30216011)
8. Zhu Y, Ghosh P, Charnay P, Burns DK, Parada LF. Neurofibromas in NF1: Schwann cell origin and role of tumor environment. Science 2002;296:920-2. (Pubitemid 34464899)
9. Wu J, Williams JP, Rizvi TA, Kordich JJ, Witte D, Meijer D, et al. Plexiform and dermal neurofibromas and pigmentation are caused by Nf1 loss in desert hedgehog-expressing cells. Cancer cell 2008;13:105-16. (Pubitemid 351163159)
10. Zheng H, Chang L, Patel N, Yang J, Lowe L, Burns DK, et al. Induction of abnormal proliferation by nonmyelinating schwann cells triggers neurofibroma formation. Cancer cell 2008;13:117-28. (Pubitemid 351163161)
11. Yang FC, Ingram DA, Chen S, Zhu Y, Yuan J, Li X, et al. Nf1-dependent tumors require a microenvironment containing Nf1+/- and c-kit-dependent bone marrow. Cell 2008;135:437-48.
12. Monk KR, Wu J, Williams JP, Finney BA, Fitzgerald ME, Filippi MD, et al. Mast cells can contribute to axon-glial dissociation and fibrosis in peripheral nerve. Neuron Glia Biol 2007;3:233-44. (Pubitemid 351594226)
13. Tanaka K, Nakafuku M, Satoh T, Marshall MS, Gibbs JB, Matsumoto K, et al. S. cerevisiae genes IRA1 and IRA2 encode proteins that may be functionally equivalent to mammalian ras GTPase activating protein. Cell 1990;60:803-7.
14. Mosch HU, Roberts RL, Fink GR. Ras2 signals via the Cdc42/Ste20/mitogen- activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1996;93:5352-6. (Pubitemid 26159453)
15. Toda T, Uno I, Ishikawa T, Powers S, Kataoka T, Broek D, et al. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell 1985;40:27-36. (Pubitemid 15169303)
16. Kim HA, Ratner N, Roberts TM, Stiles CD. Schwann cell proliferative responses to cAMP and Nf1 are mediated by cyclin D1. J Neurosci 2001;21:1110-6. (Pubitemid 32128756)
17. Xu Y, Chiamvimonvat N, Vazquez AE, Akunuru S, Ratner N, Yamoah EN. Gene-targeted deletion of neurofibromin enhances the expression of a transient outward K +current in Schwann cells: a protein kinase A-mediated mechanism. J Neurosci 2002;22:9194-202. (Pubitemid 35356162)
18. Steinmetz EJ, Conrad NK, Brow DA, Corden JL. RNA-binding protein Nrd1 directs poly(A)-independent 30-end formation of RNA polymerase II transcripts. Nature 2001;413:327-31. (Pubitemid 32905855)
19. Boeke JD, Trueheart J, Natsoulis G, Fink GR. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 1987;154:164-75.
20. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998;14:953-61. (Pubitemid 28328001)
21. Miller SJ, Rangwala F, Williams J, Ackerman P, Kong S, Jegga AG, et al. Large-scale molecular comparison of human schwann cells to malignant peripheral nerve sheath tumor cell lines and tissues. Cancer Res 2006;66:2584-91.
22. Singh N, Ma Z, Gemmill T, Wu X, Defiglio H, Rossettini A, et al. The Ess1 prolyl isomerase is required for transcription termination of small noncoding RNAs via the Nrd1 pathway. Mol Cell 2009;36:255-66.
23. Badache A, De Vries GH. Neurofibrosarcoma-derived Schwann cells overexpress platelet-derived growth factor (PDGF) receptors and are induced to proliferate byPDGFBB. J Cell Physiol 1998;177:334-42. (Pubitemid 28452834)
24. Dahlberg WK, Little JB, Fletcher JA, Suit HD, Okunieff P. Radiosensitivity in vitro of human soft tissue sarcoma cell lines and skin fibroblasts derived from the same patients. Int Journal Radiat Biol 1993;63:191-8. (Pubitemid 23042922)
25. Dunstan HM, Ludlow C, Goehle S, Cronk M, Szankasi P, Evans DR, et al. Cell-based assays for identification of novel double-strand break-inducing agents. J Natl Cancer Inst 2002;94:88-94. (Pubitemid 34121287)
26. Graham TR, Scott PA, Emr SD. Brefeldin A reversibly blocks early but not late protein transport steps in the yeast secretory pathway. EMBO J 1993;12:869-77. (Pubitemid 23095835)
27. Lee DH, Goldberg AL. Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J Biol Chem 1996;271:27280-4. (Pubitemid 26367280)
28. Abe F, Hiraki T. Mechanistic role of ergosterol in membrane rigidity and cycloheximide resistance in Saccharomyces cerevisiae. Biochim Biophys Acta2009;1788:743-52.
29. Gaber RF, Copple DM, Kennedy BK, Vidal M, Bard M. The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol Cell Biol 1989;9:3447-56. (Pubitemid 19189634)
30. Lopez G, Torres K, Liu J, Hernandez B, Young E, Belousov R, et al. Autophagic survival in resistance to histone deacetylase inhibitors: novel strategies to treat malignant peripheral nerve sheath tumors. Cancer Res 2011;71:185-96.
31. Subramanian S, Thayanithy V, West RB, Lee CH, Beck AH, Zhu S, et al. Genome-wide transcriptome analyses reveal p53 inactivation mediated loss of miR-34a expression in malignant peripheral nerve sheath tumors. J Pathol 2010;220:58-70.
32. Carroll KL, Pradhan DA, Granek JA, Clarke ND, Corden JL. Identification of cis elements directing termination of yeast nonpolyadenylated snoRNA transcripts. Mol Cell Biol 2004;24:6241-52. (Pubitemid 38891126)
33. Conrad NK, Wilson SM, Steinmetz EJ, Patturajan M, Brow DA, Swanson MS, et al. A yeast heterogeneous nuclear ribonucleoprotein complex associated with RNA polymerase II. Genetics 2000;154:557-71. (Pubitemid 30096580)
34. Arigo JT, Carroll KL, Ames JM, Corden JL. Regulation of yeast NRD1 expression by premature transcription termination. Mol Cell 2006;21:641-51. (Pubitemid 43290731)
35. Arigo JT, Eyler DE, Carroll KL, Corden JL. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Molecular Cell 2006;23:841-51. (Pubitemid 44344519)
36. Thiebaut M, Kisseleva-Romanova E, Rougemaille M, Boulay J, Libri D. Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance. Molecular Cell 2006;23:853-64. (Pubitemid 44344521)
37. Luo J, Emanuele MJ, Li D, Creighton CJ, Schlabach MR, Westbrook TF, et al. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009;137:835-48.
38. Gudipati RK, Villa T, Boulay J, Libri D. Phosphorylation of the RNA polymerase II C-terminal domain dictates transcription termination choice. Nat Struct Mol Biol 2008;15:786-94.
39. Vasiljeva L, Kim M, Mutschler H, Buratowski S, Meinhart A. The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat Struct Mol Biol 2008;15:795-804.
40. Howard SC, Hester A, Herman PK. The Ras/PKA signaling pathway may control RNA polymerase II elongation via the Spt4p/Spt5p complex in Saccharomyces cerevisiae. Genetics 2003;165:1059-70.
41. Howard SC, Budovskaya YV, Chang YW, Herman PK. The C-terminal domain of the largest subunit of RNA polymerase II is required for stationary phase entry and functionally interacts with the Ras/PKA signaling pathway. J Biol Chem 2002;277:19488-97. (Pubitemid 34967460)
42. Howard SC, Chang YW, Budovskaya YV, Herman PK. The Ras/PKA signaling pathway of Saccharomyces cerevisiae exhibits a functional interaction with the Sin4p complex of the RNA polymerase II holoenzyme. Genetics 2001;159:77-89. (Pubitemid 32923045)
43. Turbyville TJ, Gursel DB, Tuskan RG, Walrath JC, Lipschultz CA, Lockett SJ, et al. Schweinfurthin A selectively inhibits proliferation and Rho signaling in glioma and neurofibromatosis type 1 tumor cells in a NF1-GRD-dependent manner. Mol Cancer Ther 2010;9:1234-43.
44. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, et al. The genetic landscape of a cell. Science 2010;327:425-31.
45. Vasiljeva L, Buratowski S. Nrd1 interacts with the nuclear exosome for 30 processing of RNA polymerase II transcripts. Mol Cell 2006;21:239-48. (Pubitemid 43099939)
46. Houseley J, Kotovic K, El Hage A, Tollervey D. Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J 2007;26:4996-5006. (Pubitemid 350261284)
47. Johansson G, Mahller YY, Collins MH, Kim MO, Nobukuni T, Perentesis J, et al. Effective in vivo targeting of the mammalian target of rapamycin pathway in malignant peripheral nerve sheath tumors. Mol Cancer Ther 2008;7:1237-45.
48. Mahller YY, Vaikunth SS, Ripberger MC, Baird WH, Saeki Y, Cancelas JA, et al. Tissue inhibitor of metalloproteinase-3 via oncolytic herpes-virus inhibits tumor growth and vascular progenitors. Cancer Res 2008;68:1170-9. (Pubitemid 351272236)
49. Lorenz MC, Heitman J. Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog. EMBO J 1997;16:7008-18. (Pubitemid 27520801)