Analysis of the influence of subcellular localization of the HIV Rev protein on Rev-dependent gene expression by multi-fluorescence live-cell imaging

Experimental Cell Research

Volumn 312, Issue 4, 2006, Pages 443-456

  Wolff, Horst ^a   Hadian, Kamyar ^a   Ziegler, Manja ^a   Weierich, Claudia ^b   Kramer Hammerle, Susanne ^a   Kleinschmidt, Andrea ^a   Erfle, Volker ^a   Brack Werner, Ruth ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

AQ FIND; Astrocyte; CFP; Function; HIV; Localization; mRFP1; Rev; YFP

Indexed keywords

REV PROTEIN;

ARTICLE; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLUORESCENCE; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; WILD TYPE;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 29144465638     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.11.020     Document Type: Article

References (75)

1. M.T. Bohnsack, K. Regener, B. Schwappach, R. Saffrich, E. Paraskeva, E. Hartmann, and D. Gorlich Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confine translation to the cytoplasm EMBO J. 21 2002 6205 6215
2. P.A. Bubulya, and D.L. Spector On the movements of nuclear components in living cells Exp. Cell Res. 296 2004 4 11
3. A.I. Lamond, and J.E. Sleeman Nuclear substructure and dynamics Curr. Biol. 13 2003 R825 R828
4. D.L. Spector Nuclear organization and gene expression Exp. Cell Res. 229 1996 189 197
5. J.C. Simpson, and R. Pepperkok Localizing the proteome Genome Biol. 4 2003 240
6. A. Kumar, S. Agarwal, J.A. Heyman, S. Matson, M. Heidtman, S. Piccirillo, L. Umansky, A. Drawid, R. Jansen, Y. Liu, K.H. Cheung, P. Miller, M. Gerstein, G.S. Roeder, and M. Snyder Subcellular localization of the yeast proteome Genes Dev. 16 2002 707 719
7. W.K. Huh, J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea Global analysis of protein localization in budding yeast Nature 425 2003 686 691
8. S. Wiemann, D. Arlt, W. Huber, R. Wellenreuther, S. Schleeger, A. Mehrle, S. Bechtel, M. Sauermann, U. Korf, R. Pepperkok, H. Sultmann, and A. Poustka From ORFeome to biology: a functional genomics pipeline Genome Res. 14 2004 2136 2144
9. B.E. Black, and B.M. Paschal Intranuclear organization and function of the androgen receptor Trends Endocrinol. Metab. 15 2004 411 417
10. T. Kino, E. Souvatzoglou, M.U. De Martino, M. Tsopanomihalu, Y. Wan, and G.P. Chrousos Protein 14-3-3sigma interacts with and favors cytoplasmic subcellular localization of the glucocorticoid receptor, acting as a negative regulator of the glucocorticoid signaling pathway J. Biol. Chem. 278 2003 25651 25656
11. M.S. Cyert Regulation of nuclear localization during signaling J. Biol. Chem. 276 2001 20805 20808
12. S.H. Lee, and M. Hannink Molecular mechanisms that regulate transcription factor localization suggest new targets for drug development Adv. Drug Delivery Rev. 55 2003 717 731
13. E.O. Freed, and M.A. Martin HIVs and their replication P.M. Howley Fields Virology 2001 Lippincott Williams and Wilkins Philadelphia
14. A. Seelamgari, A. Maddukuri, R. Berro, C. de la Fuente, K. Kehn, L. Deng, S. Dadgar, M.E. Bottazzi, E. Ghedin, A. Pumfery, and F. Kashanchi Role of viral regulatory and accessory proteins in HIV-1 replication Front. Biosci. 9 2004 2388 2413
15. T.J. Daly, K.S. Cook, G.S. Gray, T.E. Maione, and J.R. Rusche Specific binding of HIV-1 recombinant Rev protein to the Rev-responsive element in vitro Nature 342 1989 816 819
16. H. Wolff, R. Brack-Werner, M. Neumann, T. Werner, and R. Schneider Integrated functional and bioinformatics approach for the identification and experimental verification of RNA signals: application to HIV-1 INS Nucleic Acids Res. 31 2003 2839 2851
17. A.S. Zolotukhin, D. Michalowski, J. Bear, S.V. Smulevitch, A.M. Traish, R. Peng, J. Patton, I.N. Shatsky, and B.K. Felber PSF acts through the human immunodeficiency virus type 1 mRNA instability elements to regulate virus expression Mol. Cell. Biol. 23 2003 6618 6630
18. B.R. Cullen Nuclear mRNA export: insights from virology Trends Biochem. Sci. 28 2003 419 424
19. M. Neumann, B.K. Felber, A. Kleinschmidt, B. Froese, V. Erfle, G.N. Pavlakis, and R. Brack-Werner Restriction of human immunodeficiency virus type 1 production in a human astrocytoma cell line is associated with a cellular block in Rev function J. Virol. 69 1995 2159 2167
20. E. Ludwig, F.C. Silberstein, J. van Empel, V. Erfle, M. Neumann, and R. Brack-Werner Diminished rev-mediated stimulation of human immunodeficiency virus Type 1 protein synthesis is a hallmark of human astrocytes J. Virol. 73 1999 8279 8289
21. B.J. Winslow, and D. Trono The blocks to human immunodeficiency virus type 1 Tat and Rev functions in mouse cell lines are independent J. Virol. 67 1993 2349 2354
22. S.M. Marques, J.L. Veyrune, R.R. Shukla, and A. Kumar Restriction of human immunodeficiency virus type 1 Rev function in murine A9 cells involves the Rev C-terminal domain J. Virol. 77 2003 3084 3090
23. M. Neumann, E. Afonina, F. Ceccherini-Silberstein, S. Schlicht, V. Erfle, G.N. Pavlakis, and R. Brack-Werner Nucleocytoplasmic transport in human astrocytes: decreased nuclear uptake of the HIV Rev shuttle protein J. Cell Sci. 114 2001 1717 1729
24. B.E. Meyer, and M.H. Malim The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm Genes Dev. 8 1994 1538 1547
25. R.E. Campbell, O. Tour, A.E. Palmer, P.A. Steinbach, G.S. Baird, D.A. Zacharias, and R.Y. Tsien A monomeric red fluorescent protein Proc. Natl. Acad. Sci. 99 2002 7877 7882
26. R. Stauber, K. Horie, Development and applications of enhanced green fluorescent protein mutants, BioTechniques 24 (1998) 462-466, 468-471.
27. T. Kanda, K.F. Sullivan, and M.W. Geoffrey Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells Curr. Biol. 8 1998 377 385
28. E. Ludwig, F.C. Silberstein, J. van Empel, V. Erfle, M. Neumann, and R. Brack-Werner Diminished rev-mediated stimulation of human immunodeficiency virus type 1 protein synthesis is a hallmark of human astrocytes J. Virol. 73 1999 8279 8289
29. S. Kramer-Hammerle, F. Ceccherini-Silberstein, C. Bickel, H. Wolff, M. Vincendeau, T. Werner, V. Erfle, and R. Brack-Werner Identification of a novel Rev-interacting cellular protein BMC Cell Biol. 6 2005 20
30. M. Hadzopoulou-Cladaras, B.K. Felber, C. Cladaras, A. Athanassopoulos, A. Tse, and G.N. Pavlakis The rev (trs/art) protein of human immunodeficiency virus type 1 affects viral mRNA and protein expression via a cis-acting sequence in the env region J. Virol. 63 1989 1265 1274
31. B. Mermer, B.K. Felber, M. Campbell, and G.N. Pavlakis Identification of trans-dominant HIV-1 rev protein mutants by direct transfer of bacterially produced proteins into human cells Nucleic Acids Res. 18 1990 2037 2044
32. B. Wolff, J.J. Sanglier, and Y. Wang Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA Chem. Biol. 4 1997 139 147
33. H.P. Bogerd, A. Echarri, T.M. Ross, and B.R. Cullen Inhibition of human immunodeficiency virus Rev and human T-cell leukemia virus Rex function, but not Mason-Pfizer monkey virus constitutive transport element activity, by a mutant human nucleoporin targeted to Crm1 J. Virol. 72 1998 8627 8635
34. N. Kudo, B. Wolff, T. Sekimoto, E.P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1 Exp. Cell Res. 242 1998 540 547
35. M. Auer, H.U. Gremlich, J.M. Seifert, T.J. Daly, T.G. Parslow, G. Casari, and H. Gstach Helix-loop-helix motif in HIV-1 Rev Biochemistry 33 1994 2988 2996
36. M.V. Matz, A.F. Fradkov, Y.A. Labas, A.P. Savitsky, A.G. Zaraisky, M.L. Markelov, and S.A. Lukyanov Fluorescent proteins from nonbioluminescent Anthozoa species Nat. Biotechnol. 17 1999 969 973
37. R. Stauber, G.A. Gaitanaris, and G.N. Pavlakis Analysis of trafficking of Rev and transdominant Rev proteins in living cells using green fluorescent protein fusions: transdominant Rev blocks the export of Rev from the nucleus to the cytoplasm Virology 213 1995 439 449
38. S. Demart, F. Ceccherini-Silberstein, S. Schlicht, S. Walcher, H. Wolff, M. Neumann, V. Erfle, and R. Brack-Werner Analysis of nuclear targeting activities of transport signals in the human immunodeficiency virus Rev protein Exp. Cell Res. 291 2003 484 501
39. U. Liebel, V. Starkuviene, H. Erfle, J.C. Simpson, A. Poustka, S. Wiemann, and R. Pepperkok A microscope-based screening platform for large-scale functional protein analysis in intact cells FEBS Lett. 554 2003 394 398
40. J. Lippincott-Schwartz, and G.H. Patterson Development and use of fluorescent protein markers in living cells Science 300 2003 87 91
41. R.G. Schipper, and A.A. Verhofstad Distribution patterns of ornithine decarboxylase in cells and tissues: facts, problems, and postulates J. Histochem. Cytochem. 50 2002 1143 1160
42. M.D. Ledesma, C. Galvan, B. Hellias, C. Dotti, and P.H. Jensen Astrocytic but not neuronal increased expression and redistribution of parkin during unfolded protein stress J. Neurochem. 83 2002 1431 1440
43. M. Luo, C.W. Pang, A.E. Gerken, and T.G. Brock Multiple nuclear localization sequences allow modulation of 5-lipoxygenase nuclear import Traffic 5 2004 847 854
44. O. Coqueret New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol. 13 2003 65 70
45. T. Muranen, M. Gronholm, G.H. Renkema, and O. Carpen Cell cycle-dependent nucleocytoplasmic shuttling of the neurofibromatosis 2 tumour suppressor merlin Oncogene 24 2005 1150 1158
46. N. Yasuhara, E. Takeda, H. Inoue, I. Kotera, and Y. Yoneda Importin alpha/beta-mediated nuclear protein import is regulated in a cell cycle-dependent manner Exp. Cell Res. 297 2004 285 293
47. S. Malki, S. Nef, C. Notarnicola, L. Thevenet, S. Gasca, C. Mejean, P. Berta, F. Poulat, and B. Boizet-Bonhoure Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation EMBO J. 24 2005 1798 1809
48. A. O'Brate, and P. Giannakakou The importance of p53 location: nuclear or cytoplasmic zip code? Drug Resist. Updat. 6 2003 313 322
49. R. Lin, L. Yang, M. Arguello, C. Penafuerte, and J. Hiscott A CRM1-dependent nuclear export pathway is involved in the regulation of IRF-5 subcellular localization J. Biol. Chem. 280 2005 3088 3095
50. Y. Tao, X. Song, X. Deng, D. Xie, L.M. Lee, Y. Liu, W. Li, L. Li, L. Deng, Q. Wu, J. Gong, and Y. Cao Nuclear accumulation of epidermal growth factor receptor and acceleration of G1/S stage by Epstein-Barr-encoded oncoprotein latent membrane protein 1 Exp. Cell Res. 303 2005 240 251
51. J.M. Smith, and P.A. Koopman The ins and outs of transcriptional control: nucleocytoplasmic shuttling in development and disease Trends Genet. 20 2004 4 8
52. T. Reguly, and J.L. Wrana In or out? The dynamics of Smad nucleocytoplasmic shuttling Trends Cell Biol. 13 2003 216 220
53. A. Birbach, S.T. Bailey, S. Ghosh, and J.A. Schmid Cytosolic, nuclear and nucleolar localization signals determine subcellular distribution and activity of the NF-kappaB inducing kinase NIK J. Cell Sci. 117 2004 3615 3624
54. I. Niedick, N. Froese, A. Oumard, P.P. Mueller, M. Nourbakhsh, H. Hauser, and M. Koster Nucleolar localization and mobility analysis of the NF-kappaB repressing factor NRF J. Cell Sci. 117 2004 3447 3458
55. M.H. Malim, S. Bohnlein, J. Hauber, and B.R. Cullen Functional dissection of the HIV-1 Rev trans-activator-derivation of a trans-dominant repressor of Rev function Cell 58 1989 205 214
56. M.H. Malim, and B.R. Cullen HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency Cell 65 1991 241 248
57. K.S. Jeong, Y.S. Nam, and S. Venkatesan Deletions near the N-terminus of HIV-1 Rev reduce RNA binding affinity and dominantly interfere with Rev function irrespective of the RNA target Arch. Virol. 145 2000 2443 2467
58. J. Berger, C. Aepinus, M. Dobrovnik, B. Fleckenstein, J. Hauber, and E. Bohnlein Mutational analysis of functional domains in the HIV-1 Rev trans-regulatory protein Virology 183 1991 630 635
59. R.A. Furuta, S. Kubota, M. Maki, Y. Miyazaki, T. Hattori, and M. Hatanaka Use of a human immunodeficiency virus type 1 Rev mutant without nucleolar dysfunction as a candidate for potential AIDS therapy J. Virol. 69 1995 1591 1599
60. M. Hammerschmid, D. Palmeri, M. Ruhl, H. Jaksche, I. Weichselbraun, E. Bohnlein, M.H. Malim, and J. Hauber Scanning mutagenesis of the arginine-rich region of the human immunodeficiency virus type 1 Rev trans activator J. Virol. 68 1994 7329 7335
61. T.J. Hope, D. McDonald, X.J. Huang, J. Low, and T.G. Parslow Mutational analysis of the human immunodeficiency virus type 1 Rev transactivator: essential residues near the amino terminus J. Virol. 64 1990 5360 5366
62. L.K. Venkatesh, S. Mohammed, and G. Chinnadurai Functional domains of the HIV-1 rev gene required for trans-regulation and subcellular localization Virology 176 1990 39 47
63. S. Kubota, and R.J. Pomerantz A cis-acting peptide signal in human immunodeficiency virus type I Rev which inhibits nuclear entry of small proteins Oncogene 16 1998 1851 1861
64. T.T. Huang, N. Kudo, M. Yoshida, and S. Miyamoto A nuclear export signal in the N-terminal regulatory domain of IkappaBalpha controls cytoplasmic localization of inactive NF-kappaB/IkappaBalpha complexes Proc. Natl. Acad. Sci. U. S. A. 97 2000 1014 1019
65. Y. Shi, and J. Massague Mechanisms of TGF-beta signaling from cell membrane to the nucleus Cell 113 2003 685 700
66. A.L. Pranada, S. Metz, A. Herrmann, P.C. Heinrich, and G. Muller-Newen Real time analysis of STAT3 nucleocytoplasmic shuttling J. Biol. Chem. 279 2004 15114 15123
67. S. Rehberg, P. Lischka, G. Glaser, T. Stamminger, M. Wegner, and O. Rosorius Sox10 is an active nucleocytoplasmic shuttle protein, and shuttling is crucial for Sox10-mediated transactivation Mol. Cell. Biol. 22 2002 5826 5834
68. R.V. Kamath, D.J. Leary, and S. Huang Nucleocytoplasmic shuttling of polypyrimidine tract-binding protein is uncoupled from RNA export Mol. Biol. Cell 12 2001 3808 3820
69. J. Qin, W. Kang, B. Leung, and M. McLeod Ste11p, a high-mobility-group box DNA-binding protein, undergoes pheromone- and nutrient-regulated nuclear-cytoplasmic shuttling Mol. Cell. Biol. 23 2003 3253 3264
70. A. Michienzi, S. Li, J.A. Zaia, and J.J. Rossi A nucleolar TAR decoy inhibitor of HIV-1 replication Proc. Natl. Acad. Sci. U. S. A. 99 2002 14047 14052
71. D. Daelemans, S.V. Costes, E.H. Cho, R.A. Erwin-Cohen, S. Lockett, and G.N. Pavlakis In vivo HIV-1 Rev multimerization in the nucleolus and cytoplasm identified by fluorescence resonance energy transfer J. Biol. Chem. 279 2004 50167 50175
72. D. McDonald, T.J. Hope, and T.G. Parslow Posttranscriptional regulation by the human immunodeficiency virus type 1 Rev and human T-cell leukemia virus type I Rex proteins through a heterologous RNA binding site J. Virol. 66 1992 7232 7238
73. J. Kjems, and P. Askjaer Rev protein and its cellular partners Adv. Pharmacol. 48 2000 251 298
74. R.Y. Tsai, and R.D. McKay A multistep, GTP-driven mechanism controlling the dynamic cycling of nucleostemin J. Cell Biol. 168 2005 179 184
75. T. Misteli Going in GTP cycles in the nucleolus J. Cell Biol. 168 2005 177 178