Mode of action and pharmacogenomic biomarkers for exceptional responders to didemnin B

Nature Chemical Biology

Volumn 11, Issue 6, 2015, Pages 401-408

  Potts, Malia B ^a   McMillan, Elizabeth A ^a   Rosales, Tracy I ^a   Kim, Hyun Seok ^a,e   Ou, Yi Hung ^a   Toombs, Jason E ^a   Brekken, Rolf A ^a   Minden, Mark D ^b,c   MacMillan, John B ^d   White, Michael A ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d UNIVERSITY OF TEXAS AT DALLAS   (United States)

^e Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; DDIT4 PROTEIN, HUMAN; DEPSIPEPTIDE; DIDEMNINS; EEF1A1 PROTEIN, HUMAN; ELONGATION FACTOR 1; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX; PPT1 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR;

ANTAGONISTS AND INHIBITORS; APOPTOSIS; DRUG EFFECTS; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HUMAN; METABOLISM; PHARMACOGENETICS; PROTEIN SYNTHESIS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BIOMARKERS; CELL LINE, TUMOR; DEPSIPEPTIDES; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MEMBRANE PROTEINS; MULTIPROTEIN COMPLEXES; PEPTIDE ELONGATION FACTOR 1; PHARMACOGENETICS; PROTEIN BIOSYNTHESIS; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS;

EID: 84937763466     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1797     Document Type: Article

References (54)

1. Newman, D.J. & Cragg, G.M. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J. Nat. Prod. 75, 311-335 (2012).
2. Potts, M.B. et al. Using functional signature ontology (FUSION) to identify mechanisms of action for natural products. Sci. Signal. 6, ra90 (2013).
3. Hu, Y. et al. Discoipyrroles A-D: isolation, structure determination, and synthesis of potent migration inhibitors from Bacillus hunanensis. J. Am. Chem. Soc. 135, 13387-13392 (2013).
4. Rinehart, K.L. Jr. et al. Didemnins: antiviral and antitumor depsipeptides from a Caribbean tunicate. Science 212, 933-935 (1981).
5. Rinehart, K.L. Jr., Gloer, J.B., Cook, J.C. Jr., Mizsak, S.A. & Scahill, T.A. Structures of the didemnins, antiviral and cytotoxic depsipeptides from a Caribbean tunicate. J. Am. Chem. Soc. 103, 1857-1859 (1981).
6. Lee, J., Currano, J.N., Carroll, P.J. & Joullie, M.M. Didemnins, tamandarins and related natural products. Nat. Prod. Rep. 29, 404-424 (2012).
7. Le Tourneau, C., Raymond, E. & Faivre, S. Aplidine: a paradigm of how to handle the activity and toxicity of a novel marine anticancer poison. Curr. Pharm. Des. 13, 3427-3439 (2007).
8. Vera, M.D. & Joullie, M.M. Natural products as probes of cell biology: 20 years of didemnin research. Med. Res. Rev. 22, 102-145 (2002).
9. Fritz, R.D., Varga, Z. & Radziwill, G. CNK1 is a novel Akt interaction partner that promotes cell proliferation through the Akt-FoxO signalling axis. Oncogene 29, 3575-3582 (2010).
10. Lim, J., Zhou, M., Veenstra, T.D. & Morrison, D.K. The CNK1 scaffold binds cytohesins and promotes insulin pathway signaling. Genes Dev. 24, 1496-1506 (2010).
11. Sridharan, S. & Basu, A. S6 kinase 2 promotes breast cancer cell survival via Akt. Cancer Res. 71, 2590-2599 (2011).
12. Katayama, K., Fujita, N. & Tsuruo, T. Akt/protein kinase B-dependent phosphorylation and inactivation of WEE1Hu promote cell cycle progression at G2/M transition. Mol. Cell. Biol. 25, 5725-5737 (2005).
13. Kaul, G., Pattan, G. & Rafeequi, T. Eukaryotic elongation factor-2 (eEF2): its regulation and peptide chain elongation. Cell Biochem. Funct. 29, 227-234 (2011).
14. Kefas, B. et al. microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Res. 68, 3566-3572 (2008).
15. Li, Z.Y., Na, H.M., Peng, G., Pu, J. & Liu, P. Alteration of microRNA expression correlates to fatty acid-mediated insulin resistance in mouse myoblasts. Mol. Biosyst. 7, 871-877 (2011).
16. Creevey, L. et al. MicroRNA-497 increases apoptosis in MYCN amplified neuroblastoma cells by targeting the key cell cycle regulator WEE1. Mol. Cancer 12, 23 (2013).
17. Guo, S.T. et al. MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer. Oncogene 32, 1910-1920 (2013).
18. He, Z. et al. Downregulation of miR-383 promotes glioma cell invasion by targeting insulin-like growth factor 1 receptor. Med. Oncol. 30, 557 (2013).
19. Gong, J.N. et al. The role, mechanism and potentially therapeutic application of microRNA-29 family in acute myeloid leukemia. Cell Death Differ. 21, 100-112 (2014).
20. Li, Y. et al. Epigenetic silencing of microRNA-193a contributes to leukemogenesis in t(8;21) acute myeloid leukemia by activating the PTEN/PI3K signal pathway. Blood 121, 499-509 (2013).
21. Shah, O.J., Wang, Z. & Hunter, T. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr. Biol. 14, 1650-1656 (2004).
22. Briaud, I. et al. Insulin receptor substrate-2 proteasomal degradation mediated by a mammalian target of rapamycin (mTOR)-induced negative feedback down-regulates protein kinase B-mediated signaling pathway in beta-cells. J. Biol. Chem. 280, 2282-2293 (2005).
23. Hsu, P.P. et al. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 332, 1317-1322 (2011).
24. Yu, Y. et al. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332, 1322-1326 (2011).
25. Crews, C.M., Collins, J.L., Lane, W.S., Snapper, M.L. & Schreiber, S.L. GTP-dependent binding of the antiproliferative agent didemnin to elongation factor 1 alpha. J. Biol. Chem. 269, 15411-15414 (1994).
26. Crews, C.M., Lane, W.S. & Schreiber, S.L. Didemnin binds to the protein palmitoyl thioesterase responsible for infantile neuronal ceroid lipofuscinosis. Proc. Natl. Acad. Sci. USA 93, 4316-4319 (1996).
27. SirDeshpande, B.V. & Toogood, P.L. Mechanism of protein synthesis inhibition by didemnin B in vitro. Biochemistry 34, 9177-9184 (1995).
28. Meng, L., Sin, N. & Crews, C.M. The antiproliferative agent didemnin B uncompetitively inhibits palmitoyl protein thioesterase. Biochemistry 37, 10488-10492 (1998).
29. Das, A.K. et al. Structural basis for the insensitivity of a serine enzyme (palmitoyl-protein thioesterase) to phenylmethylsulfonyl fluoride. J. Biol. Chem. 275, 23847-23851 (2000).
30. Blenis, J., Chung, J., Erikson, E., Alcorta, D.A. & Erikson, R.L. Distinct mechanisms for the activation of the RSK kinases/MAP2 kinase/pp90rsk and pp70-S6 kinase signaling systems are indicated by inhibition of protein synthesis. Cell Growth Differ. 2, 279-285 (1991).
31. Kimball, S.R., Do, A.N., Kutzler, L., Cavener, D.R. & Jefferson, L.S. Rapid turnover of the mTOR complex 1 (mTORC1) repressor REDD1 and activation of mTORC1 signaling following inhibition of protein synthesis. J. Biol. Chem. 283, 3465-3475 (2008).
32. Terada, N. et al. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc. Natl. Acad. Sci. USA 91, 11477-11481 (1994).
33. Gupta, P. et al. Disruption of PPT1 or PPT2 causes neuronal ceroid lipofuscinosis in knockout mice. Proc. Natl. Acad. Sci. USA 98, 13566-13571 (2001).
34. Voznyi, Y.V. et al. A new simple enzyme assay for pre- and postnatal diagnosis of infantile neuronal ceroid lipofuscinosis (INCL) and its variants. J. Med. Genet. 36, 471-474 (1999).
35. Pajic, A. et al. Cell cycle activation by c-myc in a Burkitt lymphoma model cell line. Int. J. Cancer 87, 787-793 (2000).
36. Grubb, D.R., Wolvetang, E.J. & Lawen, A. Didemnin B induces cell death by apoptosis: the fastest induction of apoptosis ever described. Biochem. Biophys. Res. Commun. 215, 1130-1136 (1995).
37. Collins, S. & Groudine, M. Amplification of endogenous myc-related DNA sequences in a human myeloid leukaemia cell line. Nature 298, 679-681 (1982).
38. Leary, R.J. et al. Integrated analysis of homozygous deletions, focal amplifications, and sequence alterations in breast and colorectal cancers. Proc. Natl. Acad. Sci. USA 105, 16224-16229 (2008).
39. Barretina, J. et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607 (2012).
40. Zou, H. & Hastie, T. Regularization and variable selection via the elastic net. J. R. Stat. Soc., B 67, 301-320 (2005).
41. Savukoski, M. et al. Defined chromosomal assignment of CLN5 demonstrates that at least four genetic loci are involved in the pathogenesis of human ceroid lipofuscinoses. Am. J. Hum. Genet. 55, 695-701 (1994).
42. Mamo, A., Jules, F., Dumaresq-Doiron, K., Costantino, S. & Lefrancois, S. The role of ceroid lipofuscinosis neuronal protein 5 (CLN5) in endosomal sorting. Mol. Cell. Biol. 32, 1855-1866 (2012).
43. Soares, D.C. & Abbott, C.M. Highly homologous eEF1A1 and eEF1A2 exhibit differential post-translational modification with significant enrichment around localised sites of sequence variation. Biol. Direct 8, 29 (2013).
44. Stumpf, C.R. & Ruggero, D. The cancerous translation apparatus. Curr. Opin. Genet. Dev. 21, 474-483 (2011).
45. Ribrag, V. et al. Multicenter phase II study of plitidepsin in patients with relapsed/refractory non-Hodgkin′s lymphoma. Haematologica 98, 357-363 (2013).
46. Suryani, S. et al. Cell and molecular determinants of in vivo efficacy of the BH3 mimetic ABT-263 against pediatric acute lymphoblastic leukemia xenografts. Clin. Cancer Res. 20, 4520-4531 (2014).
47. Belmar, J. & Fesik, S.W. Small molecule Mcl-1 inhibitors for the treatment of cancer. Pharmacol. Ther. 145, 76-84 (2015).
48. Robinson, D.R. et al. Functionally recurrent rearrangements of the MAST kinase and Notch gene families in breast cancer. Nat. Med. 17, 1646-1651 (2011).
49. Gazdar, A.F. et al. Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer. Int. J. Cancer 78, 766-774 (1998).
50. Hackett, A.J. et al. Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J. Natl. Cancer Inst. 58, 1795-1806 (1977).
51. Sjöblom, T. et al. The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274 (2006).
52. Gazdar, A.F., Girard, L., Lockwood, W.W., Lam, W.L. & Minna, J.D. Lung cancer cell lines as tools for biomedical discovery and research. J. Natl. Cancer Inst. 102, 1310-1321 (2010).
53. Klionsky, D.J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175 (2008).
54. Tsukimoto, M. et al. Bacterial production of the tunicate-derived antitumor cyclic depsipeptide didemnin B. J. Nat. Prod. 74, 2329-2331 (2011).