The anticancer natural product ophiobolin A induces cytotoxicity by covalent modification of phosphatidylethanolamine

eLife

Volumn 5, Issue 2016JULY, 2016, Pages

  Chidley, Christopher ^a,b   Trauger, Sunia A ^a   Birsoy, Kıvanç ^c   O’Shea, Erin K ^a,b  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; GENOMIC DNA; LIPOSOME; NATURAL PRODUCT; OPHIOBOLIN A; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BIOLOGICAL PRODUCT; LIPID BILAYER; SESTERTERPENE;

ARTICLE; CELL VIABILITY; CHEMICAL PHENOMENA; CONTROLLED STUDY; COVALENT MODIFICATION; CYTOLYSIS ASSAY; DNA ISOLATION; DRUG CYTOTOXICITY; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; KENNEDY PATHWAY; LIPID BILAYER; LIPID PEROXIDATION; LIQUID CHROMATOGRAPHY; LUCIFERASE ASSAY; MASS SPECTROMETRY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THIN LAYER CHROMATOGRAPHY; CELL LINE; CELL MEMBRANE; DRUG EFFECTS; METABOLISM;

ANTINEOPLASTIC AGENTS; BIOLOGICAL PRODUCTS; CELL LINE; CELL MEMBRANE; HUMANS; LIPID BILAYERS; PHOSPHATIDYLETHANOLAMINES; SESTERTERPENES;

EID: 84979544156     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.14601     Document Type: Article

References (63)

1. Adams J. 2004. The proteasome: a suitable antineoplastic target. Nature Reviews Cancer 4: 349-360. doi: 10.1038/nrc1361
2. Allen TM, Cleland LG. 1980. Serum-induced leakage of liposome contents. Biochimica Et Biophysica Acta 597: 418-426. doi: 10.1016/0005-2736(80)90118-2
3. Amarnath V, Amarnath K, Amarnath K, Davies S, Roberts LJ. 2004. Pyridoxamine: an extremely potent scavenger of 1,4-dicarbonyls. Chemical Research in Toxicology 17: 410-415. doi: 10.1021/tx0300535
4. Amarnath V, Amarnath K, Avance J, Stec DF, Voziyan P. 2015. 5'-O-Alkylpyridoxamines: lipophilic analogues of pyridoxamine are potent scavengers of 1,2-dicarbonyls. Chemical Research in Toxicology 28: 1469-1475. doi: 10.1021/acs.chemrestox.5b00148
5. Amarnath V, Amarnath K, Valentine WM, Eng MA, Graham DG. 1995. Intermediates in the Paal-Knorr synthesis of pyrroles. 4-Oxoaldehydes. Chemical Research in Toxicology 8: 234-238. doi: 10.1021/tx00044a008
6. Amarnath V, Amarnath K. 2015. Scavenging 4-oxo-2-nonenal. Chemical Research in Toxicology 28: 1888-1890. doi: 10.1021/acs.chemrestox.5b00301
7. Amarnath V, Anthony DC, Amarnath K, Valentine WM, Wetterau LA, Graham DG. 1991. Intermediates in the Paal-Knorr synthesis of pyrroles. The Journal of Organic Chemistry 56: 6924-6931. doi: 10.1021/jo00024a040
8. Au TK, Chick WS, Leung PC. 2000. The biology of ophiobolins. Life Sciences 67: 733-742. doi: 10.1016/S0024-3205(00)00668-8
9. Bergman AM, Pinedo HM, Peters GJ. 2002. Determinants of resistance to 2',2'-difluorodeoxycytidine (gemcitabine). Drug Resistance Updates 5: 19-33. doi: 10.1016/S1368-7646(02)00002-X
10. Bernoud-Hubac N, Fay LB, Armarnath V, Guichardant M, Bacot S, Davies SS, Roberts LJ, Lagarde M. 2004. Covalent binding of isoketals to ethanolamine phospholipids. Free Radical Biology and Medicine 37: 1604-1611. doi: 10.1016/j.freeradbiomed.2004.07.031
11. Birsoy K, Wang T, Possemato R, Yilmaz OH, Koch CE, Chen WW, Hutchins AW, Gultekin Y, Peterson TR, Carette JE, Brummelkamp TR, Clish CB, Sabatini DM. 2013. MCT1-mediated transport of a toxic molecule is an effective strategy for targeting glycolytic tumors. Nature Genetics 45: 104-108. doi: 10.1038/ng.2471
12. Bodoy S, Fotiadis D, Stoeger C, Kanai Y, Palacín M. 2013. The small SLC43 family: facilitator system l amino acid transporters and the orphan EEG1. Molecular Aspects of Medicine 34: 638-645. doi: 10.1016/j.mam.2012.12.006
13. Bunnage ME, Gilbert AM, Jones LH, Hett EC. 2015. Know your target, know your molecule. Nature Chemical Biology 11: 368-372. doi: 10.1038/nchembio.1813
14. Bury M, Girault A, Mégalizzi V, Spiegl-Kreinecker S, Mathieu V, Berger W, Evidente A, Kornienko A, Gailly P, Vandier C, Kiss R. 2013. Ophiobolin A induces paraptosis-like cell death in human glioblastoma cells by decreasing BKCa channel activity. Cell Death & Disease 4: e561. doi: 10.1038/cddis.2013.85
15. Bury M, Novo-Uzal E, Andolfi A, Cimini S, Wauthoz N, Heffeter P, Lallemand B, Avolio F, Delporte C, Cimmino A, Dubois J, Van Antwerpen P, Zonno MC, Vurro M, Poumay Y, Berger W, Evidente A, De Gara L, Kiss R, Locato V. 2013. Ophiobolin A, a sesterterpenoid fungal phytotoxin, displays higher in vitro growth-inhibitory effects in mammalian than in plant cells and displays in vivo antitumor activity. International Journal of Oncology 43: 575-585. doi: 10.3892/ijo.2013.1979
16. Cai J, Damaraju VL, Groulx N, Mowles D, Peng Y, Robins MJ, Cass CE, Gros P. 2008. Two distinct molecular mechanisms underlying cytarabine resistance in human leukemic cells. Cancer Research 68: 2349-2357. doi: 10.1158/0008-5472.CAN-07-5528
17. Carette JE, Guimaraes CP, Varadarajan M, Park AS, Wuethrich I, Godarova A, Kotecki M, Cochran BH, Spooner E, Ploegh HL, Brummelkamp TR. 2009. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326: 1231-1235. doi: 10.1126/science.1178955
18. Carette JE, Guimaraes CP, Wuethrich I, Blomen VA, Varadarajan M, Sun C, Bell G, Yuan B, Muellner MK, Nijman SM, Ploegh HL, Brummelkamp TR. 2011. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nature Biotechnology 29: 542-546. doi: 10.1038/nbt.1857
19. Chattopadhyay AK, Samaddar KR. 1976. Effects of Helminthosporium oryzae infection and ophiobolin on the cell membranes of host tissues. Physiological Plant Pathology 8: 131-139. doi: 10.1016/0048-4059(76)90046-1
20. Dasari R, Masi M, Lisy R, Ferdérin M, English LR, Cimmino A, Mathieu V, Brenner AJ, Kuhn JG, Whitten ST, Evidente A, Kiss R, Kornienko A. 2015. Fungal metabolite ophiobolin A as a promising anti-glioma agent: in vivo evaluation, structure-activity relationship and unique pyrrolylation of primary amines. Bioorganic & Medicinal Chemistry Letters 25: 4544-4548. doi: 10.1016/j.bmcl.2015.08.066
21. Eggert US. 2013. The why and how of phenotypic small-molecule screens. Nature Chemical Biology 9: 206-209. doi: 10.1038/nchembio.1206
22. Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry 226: 497-509.
23. Fujita K, Kubo I. 2005. Multifunctional action of antifungal polygodial against Saccharomyces cerevisiae: involvement of pyrrole formation on cell surface in antifungal action. Bioorganic & Medicinal Chemistry 13: 6742-6747. doi: 10.1016/j.bmc.2005.07.023
24. Gibellini F, Smith TK. 2010. The Kennedy pathway-De novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 62: 414-428. doi: 10.1002/iub.354
25. Gilbert LA, Horlbeck MA, Adamson B, Villalta JE, Chen Y, Whitehead EH, Guimaraes C, Panning B, Ploegh HL, Bassik MC, Qi LS, Kampmann M, Weissman JS. 2014. Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159: 647-661. doi: 10.1016/j.cell.2014.09.029
26. Gohil VM, Zhu L, Baker CD, Cracan V, Yaseen A, Jain M, Clish CB, Brookes PS, Bakovic M, Mootha VK. 2013. Meclizine inhibits mitochondrial respiration through direct targeting of cytosolic phosphoethanolamine metabolism. The Journal of Biological Chemistry 288: 35387-35395. doi: 10.1074/jbc.M113.489237
27. Grimsrud PA, Xie H, Griffin TJ, Bernlohr DA. 2008. Oxidative stress and covalent modification of protein with bioactive aldehydes. The Journal of Biological Chemistry 283: 21837-21841. doi: 10.1074/jbc.R700019200
28. Guichardant M, Bernoud-Hubac N, Chantegrel B, Deshayes C, Lagarde M. 2002. Aldehydes from n-6 fatty acid peroxidation. Effects on aminophospholipids. Prostaglandins, Leukotrienes, and Essential Fatty Acids 67: 147-149. doi: 10.1054/plef.2002.0412
29. Guichardant M, Taibi-Tronche P, Fay LB, Lagarde M. 1998. Covalent modifications of aminophospholipids by 4-hydroxynonenal. Free Radical Biology and Medicine 25: 1049-1056. doi: 10.1016/S0891-5849(98)00149-X
30. Guo L, Chen Z, Cox BE, Amarnath V, Epand RF, Epand RM, Davies SS. 2011. Phosphatidylethanolamines modified by g-ketoaldehyde (gKA) induce endoplasmic reticulum stress and endothelial activation. The Journal of Biological Chemistry 286: 18170-18180. doi: 10.1074/jbc.M110.213470
31. Harvey AL, Edrada-Ebel R, Quinn RJ. 2015. The re-emergence of natural products for drug discovery in the genomics era. Nature Reviews. Drug Discovery 14: 111-129. doi: 10.1038/nrd4510
32. Hermansson M, Hokynar K, Somerharju P. 2011. Mechanisms of glycerophospholipid homeostasis in mammalian cells. Progress in Lipid Research 50: 240-257. doi: 10.1016/j.plipres.2011.02.004
33. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25. doi: 10.1186/gb-2009-10-3-r25
34. Lee AY, St Onge RP, Proctor MJ, Wallace IM, Nile AH, Spagnuolo PA, Jitkova Y, Gronda M, Wu Y, Kim MK, Cheung-Ong K, Torres NP, Spear ED, Han MK, Schlecht U, Suresh S, Duby G, Heisler LE, Surendra A, Fung E, et al. 2014. Mapping the cellular response to small molecules using chemogenomic fitness signatures. Science 344: 208-211. doi: 10.1126/science.1250217
35. Leite NB, Aufderhorst-Roberts A, Palma MS, Connell SD, Ruggiero Neto J, Beales PA. 2015. PE and PS lipids synergistically enhance membrane poration by a peptide with anticancer properties. Biophysical Journal 109: 936-947. doi: 10.1016/j.bpj.2015.07.033
36. Leung PC, Taylor WA, Wang JH, Tipton CL. 1984. Ophiobolin A. A natural product inhibitor of calmodulin. The Journal of Biological Chemistry 259: 2742-2747.
37. Li Q, Shu Y. 2014. Role of solute carriers in response to anticancer drugs. Molecular and Cellular Therapies 2: 15. doi: 10.1186/2052-8426-2-15
38. Mao Q, Unadkat JD. 2015. Role of the breast cancer resistance protein (BCRP/ABCG2) in drug transport-an update. The AAPS Journal 17: 65-82. doi: 10.1208/s12248-014-9668-6
39. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, Piqani B, Eisenhaure TM, Luo B, Grenier JK, Carpenter AE, Foo SY, Stewart SA, Stockwell BR, Hacohen N, Hahn WC, Lander ES, Sabatini DM, Root DE. 2006. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124: 1283-1298. doi: 10.1016/j.cell.2006.01.040
40. Montecucco A, Biamonti G. 2007. Cellular response to etoposide treatment. Cancer Letters 252: 9-18. doi: 10.1016/j.canlet.2006.11.005
41. Newman DJ, Cragg GM. 2012. Natural products as sources of new drugs over the 30 years from 1981 to 2010. Journal of Natural Products 75: 311-335. doi: 10.1021/np200906s
42. Nijman SM. 2015. Functional genomics to uncover drug mechanism of action. Nature Chemical Biology 11: 942-948. doi: 10.1038/nchembio.1963
43. Pommier Y, Leo E, Zhang H, Marchand C. 2010. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chemistry & Biology 17: 421-433. doi: 10.1016/j.chembiol.2010.04.012
44. Pommier Y. 2006. Topoisomerase I inhibitors: camptothecins and beyond. Nature Reviews. Cancer 6: 789-802. doi: 10.1038/nrc1977
45. Reiling JH, Clish CB, Carette JE, Varadarajan M, Brummelkamp TR, Sabatini DM. 2011. A haploid genetic screen identifies the major facilitator domain containing 2A (MFSD2A) transporter as a key mediator in the response to tunicamycin. Proceedings of the National Academy of Sciences of the United States of America 108: 11756-11765. doi: 10.1073/pnas.1018098108
46. Riedl S, Zweytick D, Lohner K. 2011. Membrane-active host defense peptides-challenges and perspectives for the development of novel anticancer drugs. Chemistry and Physics of Lipids 164: 766-781. doi: 10.1016/j. chemphyslip.2011.09.004
47. Roemer T, Davies J, Giaever G, Nislow C. 2012. Bugs, drugs and chemical genomics. Nature Chemical Biology 8: 46-56. doi: 10.1038/nchembio.744
48. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320: 1496-1501. doi: 10.1126/science.1157535
49. Schenone M, Dančík V, Wagner BK, Clemons PA. 2013. Target identification and mechanism of action in chemical biology and drug discovery. Nature Chemical Biology 9: 232-240. doi: 10.1038/nchembio.1199
50. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F. 2014. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343: 84-87. doi: 10.1126/science.1247005
51. Shoemaker RH. 2006. The NCI60 human tumour cell line anticancer drug screen. Nature Reviews Cancer 6: 813-823. doi: 10.1038/nrc1951
52. Skipski VP, Peterson RF, Barclay M. 1964. Quantitative analysis of phospholipids by thin-layer chromatography. The Biochemical Journal 90: 374-378. doi: 10.1042/bj0900374
53. Smurnyy Y, Cai M, Wu H, McWhinnie E, Tallarico JA, Yang Y, Feng Y. 2014. DNA sequencing and CRISPR-Cas9 gene editing for target validation in mammalian cells. Nature Chemical Biology 10: 623-625. doi: 10.1038/nchembio.1550
54. Stafford JH, Thorpe PE. 2011. Increased exposure of phosphatidylethanolamine on the surface of tumor vascular endothelium. Neoplasia 13: 299-308. doi: 10.1593/neo.101366
55. Sullivan CB, Matafonova E, Roberts LJ, Amarnath V, Davies SS. 2010. Isoketals form cytotoxic phosphatidylethanolamine adducts in cells. Journal of Lipid Research 51: 999-1009. doi: 10.1194/jlr.M001040
56. Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF. 1984. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 226: 466-468. doi: 10.1126/science.6093249
57. Tipton CL, Paulsen PV, Betts RE. 1977. Effects of ophiobolin a on ion leakage and hexose uptake by maize roots. Plant Physiology 59: 907-910. doi: 10.1104/pp.59.5.907
58. Vance JE, Tasseva G. 2013. Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells. Biochimica Et Biophysica Acta 1831: 543-554. doi: 10.1016/j.bbalip.2012.08.016
59. Wang T, Wei JJ, Sabatini DM, Lander ES. 2014. Genetic screens in human cells using the CRISPR-Cas9 system. Science 343: 80-84. doi: 10.1126/science.1246981
60. Winter GE, Radic B, Mayor-Ruiz C, Blomen VA, Trefzer C, Kandasamy RK, Huber KV, Gridling M, Chen D, Klampfl T, Kralovics R, Kubicek S, Fernandez-Capetillo O, Brummelkamp TR, Superti-Furga G. 2014. The solute carrier SLC35F2 enables YM155-mediated DNA damage toxicity. Nature Chemical Biology 10: 768-773. doi: 10.1038/nchembio.1590
61. Zhang L, Rozek A, Hancock RE. 2001. Interaction of cationic antimicrobial peptides with model membranes. The Journal of Biological Chemistry 276: 35714-35722. doi: 10.1074/jbc.M104925200
62. Zhou X, Arthur G. 1992. Improved procedures for the determination of lipid phosphorus by malachite green. Journal of Lipid Research 33: 1233-1236.
63. Ziegler S, Pries V, Hedberg C, Waldmann H. 2013. Target identification for small bioactive molecules: finding the needle in the haystack. Angewandte Chemie 52: 2744-2792. doi: 10.1002/anie.201208749