Microtubule disruption targets HIF-1α mRNA to cytoplasmic P-bodies for translational repression

Journal of Cell Biology

Volumn 192, Issue 1, 2011, Pages 83-99

  Carbonaro, Marisa ^a   O'Brate, Aurora ^a   Giannakakou, Paraskevi ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; COMPLEMENTARY DNA; CYCLOHEXIMIDE; GREEN FLUORESCENT PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MICRORNA; NOCODAZOLE; PACLITAXEL; VINBLASTINE;

ARTICLE; CANCER CELL CULTURE; CELL STRAIN MCF 7; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; HYPOXIA; MICROTUBULE; PRIORITY JOURNAL; RNA TRANSLATION; SOLID TUMOR; VASCULARIZATION; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; CHEMICAL PRECIPITATION; CYTOPLASMIC STRUCTURES; EUKARYOTIC INITIATION FACTOR-2; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICROTUBULES; NOCODAZOLE; PACLITAXEL; POLYMERIZATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RECOMBINANT FUSION PROTEINS; RNA TRANSPORT; RNA, MESSENGER; TUBULIN;

EID: 78651338243     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201004145     Document Type: Article

References (48)

1. Aizer, A., Y. Brody, L.W. Ler, N. Sonenberg, R.H. Singer, and Y. Shav-Tal. 2008. The dynamics of mammalian P body transport, assembly, and disassembly in vivo. Mol. Biol. Cell. 19:4154-4166.
2. Anderson, P., and N. Kedersha. 2002. Stressful initiations. J. Cell Sci. 115:3227-3234.
3. Andrei, M.A., D. Ingelfinger, R. Heintzmann, T. Achsel, R. Rivera-Pomar, and R. Lührmann. 2005. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA. 11:717-727. doi:10.1261/rna.2340405
4. Ashe, M.P., S.K. De Long, and A.B. Sachs. 2000. Glucose depletion rapidly inhibits translation initiation in yeast. Mol. Biol. Cell. 11:833-848.
5. Bhattacharyya, S.N., R. Habermacher, U. Martine, E.I. Closs, and W. Filipowicz. 2006. Stress-induced reversal of microRNA repression and mRNA P-body localization in human cells. Cold Spring Harb. Symp. Quant. Biol. 71:513-521. doi:10.1101/sqb.2006.71.038
6. Bratu, D.P., B.J. Cha, M.M. Mhlanga, F.R. Kramer, and S. Tyagi. 2003. Visualizing the distribution and transport of mRNAs in living cells. Proc. Natl. Acad. Sci. USA. 100:13308-13313. doi:10.1073/pnas.2233244100
7. Brengues, M., D. Teixeira, and R. Parker. 2005. Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science. 310:486-489. doi:10.1126/science.1115791
8. Cougot, N., S. Babajko, and B. Séraphin. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165:31-40. doi:10.1083/jcb.200309008
9. Escuin, D., E.R. Kline, and P. Giannakakou. 2005. Both microtubule-stabilizing and microtubule-destabilizing drugs inhibit hypoxia-inducible factor-1alpha accumulation and activity by disrupting microtubule function. Cancer Res. 65:9021-9028. doi:10.1158/0008-5472.CAN-04- 4095
10. Escuin, D., P.A. Burke, G. McMahon-Tobin, T. Hembrough, Y. Wang, A.A. Alcaraz, L.J. Leandro-García, C. Rodríguez-Antona, J.P. Snyder, T.M. Lavallee, and P. Giannakakou. 2009. The hematopoietic-specific beta1-tubulin is naturally resistant to 2-methoxyestradiol and protects patients from drug-induced myelosuppression. Cell Cycle. 8:3914-3924.
11. Feng, Y., D. Absher, D.E. Eberhart, V. Brown, H.E. Malter, and S.T. Warren. 1997. FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell. 1:109-118. doi:10.1016/S1097-2765(00)80012-X
12. Gascoigne, K.E., and S.S. Taylor. 2008. Cancer cells display profound intra- and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell. 14:111-122. doi:10.1016/j.ccr.2008.07.002
13. Giannakakou, P., D.L. Sackett, Y.K. Kang, Z. Zhan, J.T. Buters, T. Fojo, and M.S. Poruchynsky. 1997. Paclitaxel-resistant human ovarian cancer cells have mutant beta-tubulins that exhibit impaired paclitaxel-driven polymerization. J. Biol. Chem. 272:17118-17125. doi:10.1074/jbc.272.27.17118
14. Giannakakou, P., D.L. Sackett, Y. Ward, K.R. Webster, M.V. Blagosklonny, and T. Fojo. 2000. p53 is associated with cellular microtubules and is transported to the nucleus by dynein. Nat. Cell Biol. 2:709-717. doi:10.1038/35036335
15. Giannakakou, P., M. Nakano, K.C. Nicolaou, A. O'Brate, J. Yu, M.V. Blagosklonny, U.F. Greber, and T. Fojo. 2002. Enhanced microtubule-dependent trafficking and p53 nuclear accumulation by suppression of microtubule dynamics. Proc. Natl. Acad. Sci. USA. 99:10855-10860. doi:10.1073/pnas.132275599
16. Guppy, M., S. Brunner, and M. Buchanan. 2005. Metabolic depression: a response of cancer cells to hypoxia? Comp. Biochem. Physiol. B Biochem. Mol. Biol. 140:233-239. doi:10.1016/j.cbpc.2004.10.005
17. Jaakkola, P., D.R. Mole, Y.M. Tian, M.I. Wilson, J. Gielbert, S.J. Gaskell, H.F. Kriegsheim Av, H.F. Hebestreit, M. Mukherji, C.J. Schofield, et al. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 292:468-472. doi:10.1126/science.1059796
18. Jansen, R.P. 2001. mRNA localization: message on the move. Nat. Rev. Mol. Cell Biol. 2:247-256. doi:10.1038/35067016
19. Jordan, M.A., and L. Wilson. 2004. Microtubules as a target for anticancer drugs. Nat. Rev. Cancer. 4:253-265. doi:10.1038/nrc1317
20. Kavallaris, M. 2010. Microtubules and resistance to tubulin-binding agents. Nat. Rev. Cancer. 10:194-204. doi:10.1038/nrc2803
21. Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963-969. doi:10.1042/BST0300963
22. Kedersha, N., and P. Anderson. 2007. Mammalian stress granules and processing bodies. Methods Enzymol. 431:61-81. doi:10.1016/S0076-6879(07)31005-7
23. Kedersha, N., G. Stoecklin, M. Ayodele, P. Yacono, J. Lykke-Andersen, M.J. Fritzler, D. Scheuner, R.J. Kaufman, D.E. Golan, and P. Anderson. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:871-884. doi:10.1083/jcb.200502088
24. Lang, K.J., A. Kappel, and G.J. Goodall. 2002. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol. Biol. Cell. 13:1792-1801. doi:10.1091/mbc.02-02-0017
25. Leung, A.K., J.M. Calabrese, and P.A. Sharp. 2006. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. USA. 103:18125-18130. doi:10.1073/pnas.0608845103
26. Liu, J., F.V. Rivas, J. Wohlschlegel, J.R. Yates III, R. Parker, and G.J. Hannon. 2005a. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7:1261-1266.
27. Liu, J., M.A. Valencia-Sanchez, G.J. Hannon, and R. Parker. 2005b. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7:719-723. doi:10.1038/ncb1274
28. López de Heredia, M., and R.P. Jansen. 2004. mRNA localization and the cytoskeleton. Curr. Opin. Cell Biol. 16:80-85. doi:10.1016/j.ceb.2003.11. 002
29. Low, W.K., Y. Dang, T. Schneider-Poetsch, Z. Shi, N.S. Choi, W.C. Merrick, D. Romo, and J.O. Liu. 2005. Inhibition of eukaryotic translation initiation by the marine natural product pateamine A. Mol. Cell. 20:709-722. doi:10.1016/j.molcel.2005.10.008
30. Luke, B., C.M. Azzalin, N. Hug, A. Deplazes, M. Peter, and J. Lingner. 2007. Saccharomyces cerevisiae Ebs1p is a putative ortholog of human Smg7 and promotes nonsense-mediated mRNA decay. Nucleic Acids Res. 35:7688-7697. doi:10.1093/nar/gkm912
31. Mabjeesh, N.J., D. Escuin, T.M. LaVallee, V.S. Pribluda, G.M. Swartz, M.S. Johnson, M.T. Willard, H. Zhong, J.W. Simons, and P. Giannakakou. 2003. 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell. 3:363-375. doi:10.1016/S1535-6108(03)00077-1
32. Meister, G., M. Landthaler, L. Peters, P.Y. Chen, H. Urlaub, R. Lührmann, and T. Tuschl. 2005. Identification of novel argonaute-associated proteins. Curr. Biol. 15:2149-2155. doi:10.1016/j.cub.2005.10.048
33. Palacios, I.M., and D. St Johnston. 2001. Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu. Rev. Cell Dev. Biol. 17:569-614. doi:10.1146/annurev.cellbio.17.1.569
34. Pillai, R.S. 2005. MicroRNA function: multiple mechanisms for a tiny RNA? RNA. 11:1753-1761. doi:10.1261/rna.2248605
35. Pillai, R.S., S.N. Bhattacharyya, C.G. Artus, T. Zoller, N. Cougot, E. Basyuk, E. Bertrand, and W. Filipowicz. 2005. Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science. 309:1573-1576. doi:10.1126/science.1115079
36. Pouysségur, J., F. Dayan, and N.M. Mazure. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature. 441:437-443. doi:10.1038/nature04871
37. Schepens, B., S.A. Tinton, Y. Bruynooghe, R. Beyaert, and S. Cornelis. 2005. The polypyrimidine tract-binding protein stimulates HIF-1alpha IRES-mediated translation during hypoxia. Nucleic Acids Res. 33:6884-6894. doi:10.1093/nar/gki1000
38. Semenza, G.L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer. 3:721-732. doi:10.1038/nrc1187
39. Semenza, G.L., and G.L. Wang. 1992. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12:5447-5454.
40. Sen, G.L., and H.M. Blau. 2005. Argonaute 2/RISC resides in sites of mammalian mRNA decay known as cytoplasmic bodies. Nat. Cell Biol. 7:633-636. doi:10.1038/ncb1265
41. Sivan, G., N. Kedersha, and O. Elroy-Stein. 2007. Ribosomal slowdown mediates translational arrest during cellular division. Mol. Cell. Biol. 27:6639-6646. doi:10.1128/MCB.00798-07
42. Skipper, H.E. 1971. Kinetics of mammary tumor cell growth and implications for therapy. Cancer. 28:1479-1499. doi:10.1002/1097-0142(197112) 28:6〈1479::AID-CNCR2820280622〉3.0.CO;2-M
43. Sweet, T.J., B. Boyer, W. Hu, K.E. Baker, and J. Coller. 2007. Microtubule disruption stimulates P-body formation. RNA. 13:493-502. doi:10.1261/rna.355807
44. Teixeira, D., U. Sheth, M.A. Valencia-Sanchez, M. Brengues, and R. Parker. 2005. Processing bodies require RNA for assembly and contain non-translating mRNAs. RNA. 11:371-382. doi:10.1261/rna.7258505
45. Tenenbaum, S.A., P.J. Lager, C.C. Carson, and J.D. Keene. 2002. Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods. 26:191-198. doi:10.1016/S1046-2023(02)00022-1
46. Tomari, Y., and P.D. Zamore. 2005. Perspective: machines for RNAi. Genes Dev. 19:517-529. doi:10.1101/gad.1284105
47. Tyagi, S., and F.R. Kramer. 1996. Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 14:303-308. doi:10.1038/nbt0396- 303
48. Yu, J.H., W.H. Yang, T. Gulick, K.D. Bloch, and D.B. Bloch. 2005. Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA. 11:1795-1802. doi:10.1261/rna.2142405