The nucleolar detention pathway: A cellular strategy for regulating molecular networks

Cell Cycle

Volumn 11, Issue 11, 2012, Pages 2059-2062

  Audas, Timothy E ^a   Jacob, Mathieu D ^a   Lee, Stephen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Acidosis; Heat shock; Mobility; Noncoding RNA; Posttranslational regulation; Protein dynamics; Ribosomal intergenic spacer

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA POLYMERASE; MOLECULAR MARKER; UNTRANSLATED RNA;

BLEACHING; CELL FUNCTION; MOLECULAR DYNAMICS; NUCLEOLAR DETENTION PATHWAY; NUCLEOLUS; PROTEIN PROCESSING; REVIEW;

EID: 84861895048     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20140     Document Type: Review

References (41)

1. Axelrod D, Koppel DE, Schlessinger J, Elson E, Webb WW. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys J 1976; 16:1055-69; PMID:786399; http://dx.doi.org/10.1016/S0006- 3495(76)85755-4.
2. Elson EL, Schlessinger J, Koppel DE, Axelrod D, Webb WW. Measurement of lateral transport on cell surfaces. Prog Clin Biol Res 1976; 9:137-47; PMID:1030797.
3. Koppel DE, Axelrod D, Schlessinger J, Elson EL, Webb WW. Dynamics of f luorescence marker concentration as a probe of mobility. Biophys J 1976; 16:1315-29; PMID:974223; http://dx.doi.org/10.1016/S0006-3495(76)85776-1.
4. Schlessinger J, Koppel DE, Axelrod D, Jacobson K, Webb WW, Elson EL. Lateral transport on cell membranes: mobility of concanavalin A receptors on myoblasts. Proc Natl Acad Sci USA 1976; 73:2409-13; PMID:1065895; http://dx.doi.org/10.1073/pnas.73.7.2409.
5. Vaz WL, Jacobson K, Wu ES, Derzko Z. Lateral mobility of an amphipathic apolipoprotein, ApoCIII, bound to phosphatidylcholine bilayers with and without cholesterol. Proc Natl Acad Sci USA 1979; 76:5645-9; PMID:293667; http://dx.doi.org/10.1073/pnas.76.11.5645.
6. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 1992; 111:229-33; PMID:1347277; http://dx.doi.org/10.1016/0378-1119(92)90691-H.
7. Kedersha N, Cho MR, Li W, Yacono PW, Chen S, Gilks N, et al. Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 2000; 151:1257-68; PMID:11121440; http://dx.doi.org/10. 1083/jcb.151.6.1257.
8. Vikstrom KL, Lim SS, Goldman RD, Borisy GG. Steady state dynamics of intermediate filament networks. J Cell Biol 1992; 118:121-9; PMID:1618899; http://dx.doi.org/10.1083/jcb.118.1.121.
9. Cole NB, Smith CL, Sciaky N, Terasaki M, Edidin M, Lippincott-Schwartz J. Diffusional mobility of Golgi proteins in membranes of living cells. Science 1996; 273:797-801; PMID:8670420; http://dx.doi.org/10.1126/science.273.5276.797.
10. Dundr M, Hoffmann-Rohrer U, Hu Q, Grummt I, Rothblum LI, Phair RD, et al. A kinetic framework for a mammalian RNA polymerase in vivo. Science 2002; 298:1623-6; PMID:12446911; http://dx.doi.org/10.1126/science.1076164.
11. Phair RD, Misteli T. High mobility of proteins in the mammalian cell nucleus. Nature 2000; 404:604-9; PMID:10766243; http://dx.doi.org/10.1038/ 35007077.
12. Shav-Tal Y, Darzacq X, Shenoy SM, Fusco D, Janicki SM, Spector DL, et al. Dynamics of single mRNPs in nuclei of living cells. Science 2004; 304:1797-800; PMID:15205532; http://dx.doi.org/10.1126/science.1099754.
13. Misteli T. The concept of self-organization in cellular architecture. J Cell Biol 2001; 155:181-5; PMID:11604416; http://dx.doi.org/10.1083/jcb. 200108110.
14. Misteli T. Protein dynamics: implications for nuclear architecture and gene expression. Science 2001; 291:843-7; PMID:11225636; http://dx.doi.org/10. 1126/science.291.5505.843.
15. Politz JC, Tuft RA, Pederson T. Diffusion-based transport of nascent ribosomes in the nucleus. Mol Biol Cell 2003; 14:4805-12; PMID:12960421; http://dx.doi.org/10.1091/mbc.E03-06-0395.
16. Politz JC, Tuft RA, Pederson T, Singer RH. Movement of nuclear poly(A) RNA throughout the interchromatin space in living cells. Curr Biol 1999; 9:285-91; PMID:10209094; http://dx.doi.org/10.1016/S0960-9822(99)80136-5.
17. Walsh CT, Garneau-Tsodikova S, Gatto GJ Jr. Protein posttranslational modifications: the chemistry of proteome diversifications. Angew Chem Int Ed Engl 2005; 44:7342-72; PMID:16267872; http://dx.doi.org/10.1002/anie.200501023.
18. Ellenberg J, Siggia ED, Moreira JE, Smith CL, Presley JF, Worman HJ, et al. Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 1997; 138:1193-206; PMID:9298976; http://dx.doi.org/10.1083/jcb.138.6.1193.
19. Dobbelaere J, Gentry MS, Hallberg RL, Barral Y. Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev Cell 2003; 4:345-57; PMID:12636916; http://dx.doi.org/10.1016/S1534-5807(03)00061-3.
20. Tsai RY, McKay RD. A multistep, GTP-driven mechanism controlling the dynamic cycling of nucleostemin. J Cell Biol 2005; 168:179-84; PMID:15657390; http://dx.doi.org/10.1083/jcb.200409053.
21. Mekhail K, Khacho M, Carrigan A, Hache RR, Gunaratnam L, Lee S. Regulation of ubiquitin ligase dynamics by the nucleolus. J Cell Biol 2005; 170:733-44; PMID:16129783; http://dx.doi.org/10.1083/jcb.200506030.
22. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997; 420:25-7; PMID:9450543; http://dx.doi.org/10.1016/S0014-5793(97)01480-4.
23. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399:271-5; PMID:10353251; http://dx.doi. org/10.1038/20459.
24. Audas TE, Jacob MD, Lee S. Immobilization of proteins in the nucleolus by ribosomal intergenic spacer noncoding RNA. Mol Cell 2012; 45:147-57; PMID:22284675; http://dx.doi.org/10.1016/j.molcel.2011.12.012.
25. Fayolle C, Pourchet J, Cohen A, Pedeux R, Puisieux A, de Fromentel CC, et al. UVB-induced G2 arrest of human melanocytes involves Cdc2 sequestration by Gadd45a in nuclear speckles. Cell Cycle 2006; 5:1859-64; PMID:16931908; http://dx.doi.org/10.4161/cc.5.16.3119.
26. Stark LA, Dunlop MG. Nucleolar sequestration of RelA (p65) regulates NFkappaB-driven transcription and apoptosis. Mol Cell Biol 2005; 25:5985-6004; PMID:15988014; http://dx.doi.org/10.1128/MCB.25.14.5985-6004.2005.
27. Welch WJ, Feramisco JR. Nuclear and nucleolar localization of the 72,000-dalton heat shock protein in heat-shocked mammalian cells. J Biol Chem 1984; 259:4501-13; PMID:6368558.
28. Audas TE, Li Y, Liang G, Lu R. A novel protein, Luman/CREB3 recruitment factor, inhibits Luman activation of the unfolded protein response. Mol Cell Biol 2008; 28:3952-66; PMID:18391022; http://dx.doi.org/10.1128/MCB.01439-07.
29. Takahashi K, Yoshida N, Murakami N, Kawata K, Ishizaki H, Tanaka-Okamoto M, et al. Dynamic regulation of p53 subnuclear localization and senescence by MORC3. Mol Biol Cell 2007; 18:1701-9; PMID:17332504; http://dx.doi.org/10.1091/ mbc.E06-08-0747.
30. Strauss C, Goldberg M. Recruitment of proteins to DNA double-strand breaks: MDC1 directly recruits RAP80. Cell Cycle 2011; 10:2850-7; PMID:21857162; http://dx.doi.org/10.4161/cc.10.17.17341.
31. Peddibhotla S, Wei Z, Papineni R, Lam MH, Rosen JM, Zhang P. The DNA damage effector Chk1 kinase regulates Cdc14B nucleolar shuttling during cell cycle progression. Cell Cycle 2011; 10:671-9; PMID:21301228; http://dx.doi.org/10.4161/cc.10.4.14901.
32. Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, Lamond AI, et al. Nucleolar proteome dynamics. Nature 2005; 433:77-83; PMID:15635413; http://dx.doi.org/10.1038/nature03207.
33. Emmott E, Hiscox JA. Nucleolar targeting: the hub of the matter. EMBO Rep 2009; 10:231-8; PMID:19229283; http://dx.doi.org/10.1038/embor.2009.14.
34. Mekhail K, Rivero-Lopez L, Al-Masri A, Brandon C, Khacho M, Lee S. Identification of a common subnuclear localization signal. Mol Biol Cell 2007; 18:3966-77; PMID:17652456; http://dx.doi.org/10.1091/mbc.E07-03-0295.
35. Mekhail K, Gunaratnam L, Bonicalzi ME, Lee S. HIF activation by pH-dependent nucleolar sequestration of VHL. Nat Cell Biol 2004; 6:642-7; PMID:15181450; http://dx.doi.org/10.1038/ncb1144.
36. Mekhail K, Rivero-Lopez L, Khacho M, Lee S. Restriction of rRNA synthesis by VHL maintains energy equilibrium under hypoxia. Cell Cycle 2006; 5:2401-13; PMID:17102617; http://dx.doi.org/10.4161/cc.5.20.3387.
37. Ivanchuk SM, Mondal S, Rutka JT. p14ARF interacts with DAXX: effects on HDM2 and p53. Cell Cycle 2008; 7:1836-50; PMID:18583933; http://dx.doi.org/10. 4161/cc.7.12.6025.
38. Di Bacco A, Ouyang J, Lee HY, Catic A, Ploegh H, Gill G. The SUMO-specific protease SENP5 is required for cell division. Mol Cell Biol 2006; 26:4489-98; PMID:16738315; http://dx.doi.org/10.1128/MCB.02301-05.
39. Mattsson K, Pokrovskaja K, Kiss C, Klein G, Szekely L. Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation. Proc Natl Acad Sci USA 2001; 98:1012-7; PMID:11158586; http://dx.doi.org/10.1073/pnas.031566998.
40. Wong JM, Kusdra L, Collins K. Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat Cell Biol 2002; 4:731-6; PMID:12198499; http://dx.doi.org/10.1038/ncb846.
41. Mayer C, Schmitz KM, Li J, Grummt I, Santoro R. Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 2006; 22:351-61; PMID:16678107; http://dx.doi.org/10.1016/j.molcel.2006.03.028.