Advertisement

Known Inhibitors of RNA Helicases and Their Therapeutic Potential

Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 2209)

Abstract

RNA helicases are proteins found in all kingdoms of life, and they are associated with all processes involving RNA from transcription to decay. They use NTP binding and hydrolysis to unwind duplexes, to remodel RNA structures and protein-RNA complexes, and to facilitate the unidirectional metabolism of biological processes. Viral, bacterial, and eukaryotic parasites have an intimate need for RNA helicases in their reproduction. Moreover, various disorders, like cancers, are often associated with a perturbation of the host’s helicase activity. Thus, RNA helicases provide a rich source of targets for the development of therapeutic or prophylactic drugs. In this review, we provide an overview of the different targeting strategies against helicases, the different types of compounds explored, the proposed inhibitory mechanisms of the compounds on the proteins, and the therapeutic potential of these compounds in the treatment of various disorders.

Key words

DExD/H-box DDX3 DDX2 NS3 Rocaglamide Pateamine A Hippuristanol Aminocholestanol Ring-expanded nucleosides Interface inhibitor 

Notes

Acknowledgments

This work was supported by the Centre National de la Recherche Scientifique, France, by the HelicaRN [2010 BLAN 1503 01] and HeliDEAD grants [ANR-13- BSV8-0009-01] from the Agence Nationale de la Recherche, France, and by the Initiative d’Excellence program from the French State [Grant DYNAMO, ANR-11-LABX-0011-01] to NKT. This work received financial support from PHC-Utique (CMCU 17G0820) and partially from the Ministry of Higher Education and Research in Tunisia (LR11IPT04 & LR16IPT04).

References

  1. 1.
    Silverman E, Edwalds-Gilbert G, Lin RJ (2003) DExD/H-box proteins and their partners: helping RNA helicases unwind. Gene 312:1–16.  https://doi.org/10.1016/s0378-1119(03)00626-7CrossRefPubMedGoogle Scholar
  2. 2.
    Tanner NK, Linder P (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 8(2):251–262.  https://doi.org/10.1016/s1097-2765(01)00329-xCrossRefPubMedGoogle Scholar
  3. 3.
    Jarmoskaite I, Russell R (2014) RNA helicase proteins as chaperones and remodelers. Annu Rev Biochem 83:697–725.  https://doi.org/10.1146/annurev-biochem-060713-035546CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Story RM, Steitz TA (1992) Structure of the recA protein-ADP complex. Nature 355(6358):374–376.  https://doi.org/10.1038/355374a0CrossRefPubMedGoogle Scholar
  5. 5.
    Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1(8):945–951CrossRefGoogle Scholar
  6. 6.
    Caruthers JM, McKay DB (2002) Helicase structure and mechanism. Curr Opin Struct Biol 12(1):123–133.  https://doi.org/10.1016/s0959-440x(02)00298-1CrossRefPubMedGoogle Scholar
  7. 7.
    Berger JM (2008) SnapShot: nucleic acid helicases and translocases. Cell 134(5):888–888.e881.  https://doi.org/10.1016/j.cell.2008.08.027CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Fairman-Williams ME, Guenther UP, Jankowsky E (2010) SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20(3):313–324.  https://doi.org/10.1016/j.sbi.2010.03.011CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    de la Cruz J, Kressler D, Linder P (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 24(5):192–198.  https://doi.org/10.1016/s0968-0004(99)01376-6CrossRefPubMedGoogle Scholar
  10. 10.
    Banroques J, Cordin O, Doere M, Linder P, Tanner NK (2011) Analyses of the functional regions of DEAD-box RNA «  helicases » with deletion and chimera constructs tested in vivo and in vitro. J Mol Biol 413(2):451–472.  https://doi.org/10.1016/j.jmb.2011.08.032CrossRefPubMedGoogle Scholar
  11. 11.
    Steimer L, Klostermeier D (2012) RNA helicases in infection and disease. RNA Biol 9(6):751–771.  https://doi.org/10.4161/rna.20090CrossRefPubMedGoogle Scholar
  12. 12.
    Bourgeois CF, Mortreux F, Auboeuf D (2016) The multiple functions of RNA helicases as drivers and regulators of gene expression. Nat Rev Mol Cell Biol 17(7):426–438.  https://doi.org/10.1038/nrm.2016.50CrossRefPubMedGoogle Scholar
  13. 13.
    Briguglio I, Piras S, Corona P, Carta A (2011) Inhibition of RNA helicases of ssRNA(+) virus belonging to Flaviviridae, Coronaviridae and Picornaviridae families. Int J Med Chem 2011:213135.  https://doi.org/10.1155/2011/213135CrossRefPubMedGoogle Scholar
  14. 14.
    Kwong AD, Rao BG, Jeang KT (2005) Viral and cellular RNA helicases as antiviral targets. Nat Rev Drug Discov 4(10):845–853.  https://doi.org/10.1038/nrd1853CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ranji A, Boris-Lawrie K (2010) RNA helicases: emerging roles in viral replication and the host innate response. RNA Biol 7(6):775–787.  https://doi.org/10.4161/rna.7.6.14249CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Mastrangelo E, Bolognesi M, Milani M (2012) Flaviviral helicase: insights into the mechanism of action of a motor protein. Biochem Biophys Res Commun 417(1):84–87.  https://doi.org/10.1016/j.bbrc.2011.11.060CrossRefPubMedGoogle Scholar
  17. 17.
    Fullam A, Schroder M (2013) DExD/H-box RNA helicases as mediators of anti-viral innate immunity and essential host factors for viral replication. Biochim Biophys Acta 1829(8):854–865.  https://doi.org/10.1016/j.bbagrm.2013.03.012CrossRefPubMedGoogle Scholar
  18. 18.
    Ariumi Y (2014) Multiple functions of DDX3 RNA helicase in gene regulation, tumorigenesis, and viral infection. Front Genet 5:423.  https://doi.org/10.3389/fgene.2014.00423CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Schroder M (2010) Human DEAD-box protein 3 has multiple functions in gene regulation and cell cycle control and is a prime target for viral manipulation. Biochem Pharmacol 79(3):297–306.  https://doi.org/10.1016/j.bcp.2009.08.032CrossRefPubMedGoogle Scholar
  20. 20.
    Marchat LA, Arzola-Rodriguez SI, Hernandez-de la Cruz O, Lopez-Rosas I, Lopez-Camarillo C (2015) DEAD/DExH-box RNA helicases in selected human parasites. Korean J Parasitol 53(5):583–595.  https://doi.org/10.3347/kjp.2015.53.5.583CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Tuteja R (2017) Unraveling the importance of the malaria parasite helicases. FEBS J 284(16):2592–2603.  https://doi.org/10.1111/febs.14109CrossRefPubMedGoogle Scholar
  22. 22.
    Gargantini PR, Lujan HD, Pereira CA (2012) In silico analysis of trypanosomatids’ helicases. FEMS Microbiol Lett 335(2):123–129.  https://doi.org/10.1111/j.1574-6968.2012.02644.xCrossRefPubMedGoogle Scholar
  23. 23.
    Abdelhaleem M (2004) Do human RNA helicases have a role in cancer? Biochim Biophys Acta 1704(1):37–46.  https://doi.org/10.1016/j.bbcan.2004.05.001CrossRefPubMedGoogle Scholar
  24. 24.
    Heerma van Voss MR, van Diest PJ, Raman V (2017) Targeting RNA helicases in cancer: the translation trap. Biochim Biophys Acta Rev Cancer 1868(2):510–520.  https://doi.org/10.1016/j.bbcan.2017.09.006CrossRefPubMedGoogle Scholar
  25. 25.
    Chu J, Pelletier J (2018) Therapeutic opportunities in eukaryotic translation. Cold Spring Harb Perspect Biol 10(6).  https://doi.org/10.1101/cshperspect.a032995
  26. 26.
    Zhao L, Mao Y, Zhou J, Zhao Y, Cao Y, Chen X (2016) Multifunctional DDX3: dual roles in various cancer development and its related signaling pathways. Am J Cancer Res 6(2):387–402PubMedPubMedCentralGoogle Scholar
  27. 27.
    Bol GM, Xie M, Raman V (2015) DDX3, a potential target for cancer treatment. Mol Cancer 14:188.  https://doi.org/10.1186/s12943-015-0461-7CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Chu J, Pelletier J (2015) Targeting the eIF4A RNA helicase as an anti-neoplastic approach. Biochim Biophys Acta 1849(7):781–791.  https://doi.org/10.1016/j.bbagrm.2014.09.006CrossRefPubMedGoogle Scholar
  29. 29.
    Bareclev C, Vaitkevicius K, Netterling S, Johansson J (2014) DExD-box RNA-helicases in Listeria monocytogenes are important for growth, ribosomal maturation, rRNA processing and virulence factor expression. RNA Biol 11(11):1457–1466.  https://doi.org/10.1080/15476286.2014.996099CrossRefPubMedGoogle Scholar
  30. 30.
    Cencic R, Pelletier J (2013) Throwing a monkey wrench in the motor: targeting DExH/D box proteins with small molecule inhibitors. Biochim Biophys Acta 1829(8):894–903.  https://doi.org/10.1016/j.bbagrm.2013.01.008CrossRefPubMedGoogle Scholar
  31. 31.
    Borowski P, Niebuhr A, Schmitz H, Hosmane RS, Bretner M, Siwecka MA, Kulikowski T (2002) NTPase/helicase of Flaviviridae: inhibitors and inhibition of the enzyme. Acta Biochim Pol 49(3):597–614CrossRefGoogle Scholar
  32. 32.
    Shadrick WR, Ndjomou J, Kolli R, Mukherjee S, Hanson AM, Frick DN (2013) Discovering new medicines targeting helicases: challenges and recent progress. J Biomol Screen 18(7):761–781.  https://doi.org/10.1177/1087057113482586CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Pommier Y, Kiselev E, Marchand C (2015) Interfacial inhibitors. Bioorg Med Chem Lett 25(18):3961–3965.  https://doi.org/10.1016/j.bmcl.2015.07.032CrossRefPubMedGoogle Scholar
  34. 34.
    Abdelkrim YZ, Harigua-Souiai E, Barhoumi M, Banroques J, Blondel A, Guizani I, Tanner NK (2018) The steroid derivative 6-aminocholestanol inhibits the DEAD-box helicase eIF4A (LieIF4A) from the Trypanosomatid parasite Leishmania by perturbing the RNA and ATP binding sites. Mol Biochem Parasitol 226:9–19.  https://doi.org/10.1016/j.molbiopara.2018.10.001CrossRefPubMedGoogle Scholar
  35. 35.
    Shiffman ML (2009) What future for ribavirin? Liver Int 29(Suppl 1):68–73.  https://doi.org/10.1111/j.1478-3231.2008.01936.xCrossRefPubMedGoogle Scholar
  36. 36.
    Zhang N, Chen HM, Koch V, Schmitz H, Liao CL, Bretner M, Bhadti VS, Fattom AI, Naso RB, Hosmane RS, Borowski P (2003) Ring-expanded ("fat") nucleoside and nucleotide analogues exhibit potent in vitro activity against flaviviridae NTPases/helicases, including those of the West Nile virus, hepatitis C virus, and Japanese encephalitis virus. J Med Chem 46(19):4149–4164.  https://doi.org/10.1021/jm030842jCrossRefPubMedGoogle Scholar
  37. 37.
    Yedavalli VS, Zhang N, Cai H, Zhang P, Starost MF, Hosmane RS, Jeang KT (2008) Ring expanded nucleoside analogues inhibit RNA helicase and intracellular human immunodeficiency virus type 1 replication. J Med Chem 51(16):5043–5051.  https://doi.org/10.1021/jm800332mCrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Maga G, Falchi F, Radi M, Botta L, Casaluce G, Bernardini M, Irannejad H, Manetti F, Garbelli A, Samuele A, Zanoli S, Este JA, Gonzalez E, Zucca E, Paolucci S, Baldanti F, De Rijck J, Debyser Z, Botta M (2011) Toward the discovery of novel anti-HIV drugs. Second-generation inhibitors of the cellular ATPase DDX3 with improved anti-HIV activity: synthesis, structure-activity relationship analysis, cytotoxicity studies, and target validation. Chem Med Chem 6(8):1371–1389.  https://doi.org/10.1002/cmdc.201100166CrossRefPubMedGoogle Scholar
  39. 39.
    Chan CH, Chen CM, Lee YW, You LR (2019) DNA damage, liver injury, and tumorigenesis: consequences of DDX3X loss. Mol Cancer Res 17(2):555–566.  https://doi.org/10.1158/1541-7786.mcr-18-0551CrossRefPubMedGoogle Scholar
  40. 40.
    Ditton HJ, Zimmer J, Kamp C, Rajpert-De Meyts E, Vogt PH (2004) The AZFa gene DBY (DDX3Y) is widely transcribed but the protein is limited to the male germ cells by translation control. Hum Mol Genet 13(19):2333–2341.  https://doi.org/10.1093/hmg/ddh240CrossRefPubMedGoogle Scholar
  41. 41.
    Maga G, Gemma S, Fattorusso C, Locatelli GA, Butini S, Persico M, Kukreja G, Romano MP, Chiasserini L, Savini L, Novellino E, Nacci V, Spadari S, Campiani G (2005) Specific targeting of hepatitis C virus NS3 RNA helicase. Discovery of the potent and selective competitive nucleotide-mimicking inhibitor QU663. Biochemistry 44(28):9637–9644.  https://doi.org/10.1021/bi047437uCrossRefPubMedGoogle Scholar
  42. 42.
    Preugschat F, Averett DR, Clarke BE, Porter DJ (1996) A steady-state and pre-steady-state kinetic analysis of the NTPase activity associated with the hepatitis C virus NS3 helicase domain. J Biol Chem 271(40):24449–24457.  https://doi.org/10.1074/jbc.271.40.24449CrossRefPubMedGoogle Scholar
  43. 43.
    Manfroni G, Paeshuyse J, Massari S, Zanoli S, Gatto B, Maga G, Tabarrini O, Cecchetti V, Fravolini A, Neyts J (2009) Inhibition of subgenomic hepatitis C virus RNA replication by acridone derivatives: identification of an NS3 helicase inhibitor. J Med Chem 52(10):3354–3365.  https://doi.org/10.1021/jm801608uCrossRefPubMedGoogle Scholar
  44. 44.
    Stankiewicz-Drogon A, Palchykovska LG, Kostina VG, Alexeeva IV, Shved AD, Boguszewska-Chachulska AM (2008) New acridone-4-carboxylic acid derivatives as potential inhibitors of hepatitis C virus infection. Bioorg Med Chem 16(19):8846–8852.  https://doi.org/10.1016/j.bmc.2008.08.074CrossRefPubMedGoogle Scholar
  45. 45.
    Yang SY (2010) Pharmacophore modeling and applications in drug discovery: challenges and recent advances. Drug Discov Today 15(11–12):444–450.  https://doi.org/10.1016/j.drudis.2010.03.013CrossRefPubMedGoogle Scholar
  46. 46.
    Radi M, Falchi F, Garbelli A, Samuele A, Bernardo V, Paolucci S, Baldanti F, Schenone S, Manetti F, Maga G, Botta M (2012) Discovery of the first small molecule inhibitor of human DDX3 specifically designed to target the RNA binding site: towards the next generation HIV-1 inhibitors. Bioorg Med Chem Lett 22(5):2094–2098.  https://doi.org/10.1016/j.bmcl.2011.12.135CrossRefPubMedGoogle Scholar
  47. 47.
    Fazi R, Tintori C, Brai A, Botta L, Selvaraj M, Garbelli A, Maga G, Botta M (2015) Homology model-based virtual screening for the identification of human helicase DDX3 inhibitors. J Chem Inf Model 55(11):2443–2454.  https://doi.org/10.1021/acs.jcim.5b00419CrossRefPubMedGoogle Scholar
  48. 48.
    Bol GM, Vesuna F, Xie M, Zeng J, Aziz K, Gandhi N, Levine A, Irving A, Korz D, Tantravedi S, Heerma van Voss MR, Gabrielson K, Bordt EA, Polster BM, Cope L, van der Groep P, Kondaskar A, Rudek MA, Hosmane RS, van der Wall E, van Diest PJ, Tran PT, Raman V (2015) Targeting DDX3 with a small molecule inhibitor for lung cancer therapy. EMBO Mol Med 7(5):648–669.  https://doi.org/10.15252/emmm.201404368CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Absmeier E, Santos KF, Wahl MC (2016) Functions and regulation of the Brr2 RNA helicase during splicing. Cell Cycle 15(24):3362–3377.  https://doi.org/10.1080/15384101.2016.1249549CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Cordin O, Beggs JD (2013) RNA helicases in splicing. RNA Biol 10(1):83–95.  https://doi.org/10.4161/rna.22547CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Iwatani-Yoshihara M, Ito M, Klein MG, Yamamoto T, Yonemori K, Tanaka T, Miwa M, Morishita D, Endo S, Tjhen R, Qin L, Nakanishi A, Maezaki H, Kawamoto T (2017) Discovery of allosteric inhibitors targeting the Spliceosomal RNA helicase Brr2. J Med Chem 60(13):5759–5771.  https://doi.org/10.1021/acs.jmedchem.7b00461CrossRefPubMedGoogle Scholar
  52. 52.
    Harigua-Souiai E, Abdelkrim YZ, Bassoumi-Jamoussi I, Zakraoui O, Bouvier G, Essafi-Benkhadir K, Banroques J, Desdouits N, Munier-Lehmann H, Barhoumi M, Tanner NK, Nilges M, Blondel A, Guizani I (2018) Identification of novel leishmanicidal molecules by virtual and biochemical screenings targeting Leishmania eukaryotic translation initiation factor 4A. PLoS Negl Trop Dis 12(1):e0006160.  https://doi.org/10.1371/journal.pntd.0006160CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Beuchet P, el Kihel L, Dherbomez M, Charles G, Letourneux Y (1998) Synthesis of 6(alpha, beta)-aminocholestanols as ergosterol biosynthesis inhibitors. Bioorg Med Chem Lett 8(24):3627–3630.  https://doi.org/10.1016/s0960-894x(98)00661-1CrossRefPubMedGoogle Scholar
  54. 54.
    Higa T, Tanaka J-I, Tsukitani Y, Kikuchi H (1981) Hippuristanols, cytotoxic polyoxygenated steroids from the gorgonian Isis hippuris. Chem Lett 10(11):1647–1650.  https://doi.org/10.1246/cl.1981.1647CrossRefGoogle Scholar
  55. 55.
    Bordeleau ME, Mori A, Oberer M, Lindqvist L, Chard LS, Higa T, Belsham GJ, Wagner G, Tanaka J, Pelletier J (2006) Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol 2(4):213–220.  https://doi.org/10.1038/nchembio776CrossRefPubMedGoogle Scholar
  56. 56.
    Lindqvist L, Oberer M, Reibarkh M, Cencic R, Bordeleau ME, Vogt E, Marintchev A, Tanaka J, Fagotto F, Altmann M, Wagner G, Pelletier J (2008) Selective pharmacological targeting of a DEAD box RNA helicase. PLoS One 3(2):e1583.  https://doi.org/10.1371/journal.pone.0001583CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Cencic R, Pelletier J (2016) Hippuristanol—a potent steroid inhibitor of eukaryotic initiation factor 4A. Translation (Austin) 4(1):e1137381.  https://doi.org/10.1080/21690731.2015.1137381CrossRefGoogle Scholar
  58. 58.
    Northcote PT, Blunt JW, Munro MHG (1991) Pateamine: a potent cytotoxin from the New Zealand marine sponge, Mycale sp. Tetrahedron Lett 32(44):6411–6414.  https://doi.org/10.1016/0040-4039(91)80182-6CrossRefGoogle Scholar
  59. 59.
    Bordeleau ME, Matthews J, Wojnar JM, Lindqvist L, Novac O, Jankowsky E, Sonenberg N, Northcote P, Teesdale-Spittle P, Pelletier J (2005) Stimulation of mammalian translation initiation factor eIF4A activity by a small molecule inhibitor of eukaryotic translation. Proc Natl Acad Sci U S A 102(30):10460–10465.  https://doi.org/10.1073/pnas.0504249102CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Low WK, Dang Y, Schneider-Poetsch T, Shi Z, Choi NS, Merrick WC, Romo D, Liu JO (2005) Inhibition of eukaryotic translation initiation by the marine natural product pateamine a. Mol Cell 20(5):709–722.  https://doi.org/10.1016/j.molcel.2005.10.008CrossRefPubMedGoogle Scholar
  61. 61.
    Low WK, Dang Y, Bhat S, Romo D, Liu JO (2007) Substrate-dependent targeting of eukaryotic translation initiation factor 4A by pateamine a: negation of domain-linker regulation of activity. Chem Biol 14(6):715–727.  https://doi.org/10.1016/j.chembiol.2007.05.012CrossRefPubMedGoogle Scholar
  62. 62.
    Dang Y, Low WK, Xu J, Gehring NH, Dietz HC, Romo D, Liu JO (2009) Inhibition of nonsense-mediated mRNA decay by the natural product pateamine a through eukaryotic initiation factor 4AIII. J Biol Chem 284(35):23613–23621.  https://doi.org/10.1074/jbc.M109.009985CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Bordeleau ME, Cencic R, Lindqvist L, Oberer M, Northcote P, Wagner G, Pelletier J (2006) RNA-mediated sequestration of the RNA helicase eIF4A by Pateamine a inhibits translation initiation. Chem Biol 13(12):1287–1295.  https://doi.org/10.1016/j.chembiol.2006.10.005CrossRefPubMedGoogle Scholar
  64. 64.
    Low WK, Li J, Zhu M, Kommaraju SS, Shah-Mittal J, Hull K, Liu JO, Romo D (2014) Second-generation derivatives of the eukaryotic translation initiation inhibitor pateamine a targeting eIF4A as potential anticancer agents. Bioorg Med Chem 22(1):116–125.  https://doi.org/10.1016/j.bmc.2013.11.046CrossRefPubMedGoogle Scholar
  65. 65.
    Lu King M, Chiang C-C, Ling H-C, Fujita E, Ochiai M, McPhail AT (1982) X-ray crystal structure of rocaglamide, a novel antileulemic 1H-cyclopenta[b]benzofuran from Aglaia elliptifolia. J Chem Soc Chem Commun 20:1150–1151.  https://doi.org/10.1039/C39820001150CrossRefGoogle Scholar
  66. 66.
    Pan L, Woodard JL, Lucas DM, Fuchs JR, Kinghorn AD (2014) Rocaglamide, silvestrol and structurally related bioactive compounds from Aglaia species. Nat Prod Rep 31(7):924–939.  https://doi.org/10.1039/c4np00006dCrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Ohse T, Ohba S, Yamamoto T, Koyano T, Umezawa K (1996) Cyclopentabenzofuran lignan protein synthesis inhibitors from Aglaia odorata. J Nat Prod 59(7):650–652.  https://doi.org/10.1021/np960346gCrossRefPubMedGoogle Scholar
  68. 68.
    Bordeleau ME, Robert F, Gerard B, Lindqvist L, Chen SM, Wendel HG, Brem B, Greger H, Lowe SW, Porco JA Jr, Pelletier J (2008) Therapeutic suppression of translation initiation modulates chemosensitivity in a mouse lymphoma model. J Clin Invest 118(7):2651–2660.  https://doi.org/10.1172/jci34753CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Sadlish H, Galicia-Vazquez G, Paris CG, Aust T, Bhullar B, Chang L, Helliwell SB, Hoepfner D, Knapp B, Riedl R, Roggo S, Schuierer S, Studer C, Porco JA Jr, Pelletier J, Movva NR (2013) Evidence for a functionally relevant rocaglamide binding site on the eIF4A-RNA complex. ACS Chem Biol 8(7):1519–1527.  https://doi.org/10.1021/cb400158tCrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Iwasaki S, Floor SN, Ingolia NT (2016) Rocaglates convert DEAD-box protein eIF4A into a sequence-selective translational repressor. Nature 534(7608):558–561.  https://doi.org/10.1038/nature17978CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Iwasaki S, Iwasaki W, Takahashi M, Sakamoto A, Watanabe C, Shichino Y, Floor SN, Fujiwara K, Mito M, Dodo K, Sodeoka M, Imataka H, Honma T, Fukuzawa K, Ito T, Ingolia NT (2019) The translation inhibitor Rocaglamide targets a bimolecular cavity between eIF4A and Polypurine RNA. Mol Cell 73(4):738–748.e739.  https://doi.org/10.1016/j.molcel.2018.11.026CrossRefPubMedGoogle Scholar
  72. 72.
    Linder P, Jankowsky E (2011) From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12(8):505–516.  https://doi.org/10.1038/nrm3154CrossRefPubMedGoogle Scholar
  73. 73.
    Tillotson J, Kedzior M, Guimaraes L, Ross AB, Peters TL, Ambrose AJ, Schmidlin CJ, Zhang DD, Costa-Lotufo LV, Rodriguez AD, Schatz JH, Chapman E (2017) ATP-competitive, marine derived natural products that target the DEAD box helicase, eIF4A. Bioorg Med Chem Lett 27(17):4082–4085.  https://doi.org/10.1016/j.bmcl.2017.07.045CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Rodriguez AD, Ramirez C, Rodriguez II (1999) Elisabatins a and B: new amphilectane-type diterpenes from the west Indian sea whip Pseudopterogorgia elisabethae. J Nat Prod 62(7):997–999.  https://doi.org/10.1021/np990090pCrossRefPubMedGoogle Scholar
  75. 75.
    Konig GM, Wright AD (1997) Sesquiterpene content of the antibacterial dichloromethane extract of the marine red alga Laurencia obtusa. Planta Med 63(2):186–187.  https://doi.org/10.1055/s-2006-957643CrossRefPubMedGoogle Scholar
  76. 76.
    Banroques J, Tanner NK (2015) Bioinformatics and biochemical methods to study the structural and functional elements of DEAD-box RNA helicases. Methods Mol Biol 1259:165–181.  https://doi.org/10.1007/978-1-4939-2214-7_11CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2021

Authors and Affiliations

  1. 1.Expression Génétique Microbienne, UMR8261 CNRSInstitut de Biologie Physico-Chimique, Université de ParisParisFrance
  2. 2.Molecular Epidemiology and Experimental Pathology (LR16IPT04), Institut Pasteur de Tunis/Université de Tunis el ManarTunis-BelvédèreTunisia
  3. 3.PSL Research UniversityParisFrance

Personalised recommendations