Nucleophosmin integrates within the nucleolus via multi-modal interactions with proteins displaying R-rich linear motifs and rRNA

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Mitrea, Diana M ^a   Cika, Jaclyn A ^a,b   Guy, Clifford S ^a   Ban, David ^a   Banerjee, Priya R ^c   Stanley, Christopher B ^d   Nourse, Amanda ^a   Deniz, Ashok A ^c   Kriwacki, Richard W ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOPHOSMIN; RIBOSOME RNA; NUCLEAR PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANIMAL CELL; ANISOTROPY; ARTICLE; BINDING AFFINITY; BIOINFORMATICS; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE SPECTROSCOPY; INTERNAL RIBOSOME ENTRY SITE; ISOTHERMAL TITRATION CALORIMETRY; MICROSCOPY; NEUTRON SCATTERING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOLAR LOCALIZATION SIGNAL; NUCLEOLUS; PHASE SEPARATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION; STOICHIOMETRY; ULTRACENTRIFUGATION; CHEMISTRY; HUMAN; METABOLISM; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION;

CELL NUCLEOLUS; HUMANS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; RNA, RIBOSOMAL;

EID: 84961279195     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13571.001     Document Type: Article

References (71)

1. Abragam A. 1961. Principles of Nuclear Magnetism. New York, NY: Oxford.
2. Ahmad Y, Boisvert F-M, Gregor P, Cobley A, Lamond AI. 2009. NOPdb: nucleolar proteome database-2008 update. Nucleic Acids Research 37:D181-D184. doi: 10.1093/nar/gkn804
3. Arai M, Ferreon JC, Wright PE. 2012. Quantitative analysis of multisite protein-ligand interactions by NMR: binding of intrinsically disordered p53 transactivation subdomains with the TAZ2 domain of CBP. Journal of the American Chemical Society 134:3792-3803. doi: 10.1021/ja209936u
4. Arnold O, Bilheux JC, Borreguero JM, Buts A, Campbell SI, Chapon L, Doucet M, Draper N, Ferraz Leal R, Gigg MA, Lynch VE, Markvardsen A, Mikkelson DJ, Mikkelson RL, Miller R, Palmen K, Parker P, Passos G, Perring TG, Peterson PF, Ren S, Reuter MA, Savici AT, Taylor JW, Taylor RJ, Tolchenov R, Zhou W, Zikovsky J, Campbell SI, Chapon L, Doucet M, Draper N, Ferraz Leal R, Gigg M. 2014. Mantid-data analysis and visualization package for neutron scattering and SR experiments. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment 764:156-166. doi: 10.1016/j.nima.2014.07.029
5. Bañuelos S, Lectez B, Taneva SG, Ormaza G, Alonso-Mariño M, Calle X, Urbaneja MA.2013.Recognitionof intermolecular g-quadruplexes by full length nucleophosmin. effect of a leukaemia-associated mutation. FEBS Letters 587:2254-2259. doi: 10.1016/j.febslet.2013.05.055
6. Bertwistle D, Sugimoto M, Sherr CJ. 2004. Physical and functional interactions of the arf tumor suppressor protein with Nucleophosmin/B23. Molecular and Cellular Biology 24:985-996. doi: 10.1128/MCB.24.3.985-996.2004
7. Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI. 2007. The multifunctional nucleolus. Nature Reviews. Molecular Cell Biology 8:574-585. doi: 10.1038/nrm2184
8. Brangwynne CP, Mitchison TJ, Hyman AA. 2011. Active liquid-like behavior of nucleoli determines their size and shape in xenopus laevis oocytes. Proceedings of the National Academy of Sciences of the United States of America 108:4334-4339. doi: 10.1073/pnas.1017150108
9. Cavanagh JC, Fairbrother WJ, Palmer AGr, Rance M, Skelton NJ. 2007. Principles and Practice: Protein NMR Spectroscopy (2nd ed).Burlington, MA: Reed Elsevier.
10. Chan PK. 1992. Characterization and cellular localization of nucleophosmin/B23 in HeLa cells treated with selected cytotoxic agents (studies of B23-translocation mechanism). Experimental Cell Research 203:174-181. doi: 10.1016/0014-4827(92)90053-B
11. Chen D, Huang S. 2001. Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. The Journal of Cell Biology 153:169-176. doi: 10.1083/jcb.153.1.169
12. Chiarella S, De Cola A, Scaglione GL, Carletti E, Graziano V, Barcaroli D, Lo Sterzo C, Di Matteo A, Di Ilio C, Falini B, Arcovito A, De Laurenzi V, Federici L. 2013. Nucleophosmin mutations alter its nucleolar localization by impairing g-quadruplex binding at ribosomal DNA. Nucleic Acids Research 41:3228-3239. doi: 10.1093/nar/gkt001
13. Christie M, Chang CW, Róna G, Smith KM, Stewart AG, Takeda AA, Fontes MR, Stewart M, Vértessy BG, Forwood JK, Kobe B. 2015. Structural biology and regulation of protein import into the nucleus. Journal of Molecular Biology. doi: 10.1016/j.jmb.2015.10.023
14. Colombo E, Bonetti P, Lazzerini Denchi E, Martinelli P, Zamponi R, Marine JC, Helin K, Falini B, Pelicci PG. 2005. Nucleophosmin is required for DNA integrity and p19Arf protein stability. Molecular and Cellular Biology 25: 8874-8886. doi: 10.1128/MCB.25.20.8874-8886.2005
15. Colombo E, Alcalay M, Pelicci PG. 2011. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene 30:2595-2609. doi: 10.1038/onc.2010.646
16. Delaglio F, Grzesiek S, Vuister G, Zhu G, Pfeifer J, Bax A. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. Journal of Biomolecular NMR 6:277-293. doi: 10.1007/BF00197809
17. Duan Z, Chen J, Xu H, Zhu J, Li Q, He L, Liu H, Hu S, Liu X. 2014. The nucleolar phosphoprotein B23 targets newcastle disease virus matrix protein to the nucleoli and facilitates viral replication. Virology 452-453:212-222. doi: 10.1016/j.virol.2014.01.011
18. Enomoto T, Lindstrom MS, Jin A, Ke H, Zhang Y. 2006. Essential role of the B23/NPM core domain in regulating ARF binding and B23 stability. The Journal of Biological Chemistry 281:18463-18472. doi: 10.1074/jbc.M602788200
19. Falini B, Bolli N, Shan J, Martelli MP, Liso A, Pucciarini A, Bigerna B, Pasqualucci L, Mannucci R, Rosati R, Gorello P, Diverio D, Roti G, Tiacci E, Cazzaniga G, Biondi A, Schnittger S, Haferlach T, Hiddemann W, Martelli MF, Gu W, Mecucci C, Nicoletti I. 2006. Both carboxy-terminus NES motif and mutated tryptophan(s) are crucial for aberrant nuclear export of nucleophosmin leukemic mutants in NPMc+ AML. Blood 107:4514-4523. doi: 10.1182/blood-2005-11-4745
20. Fankhauser C, Izaurralde E, Adachi Y, Wingfield P, Laemmli UK. 1991. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the rev response element. Molecular and Cellular Biology 11:2567-2575. doi: 10.1128/MCB.11.5.2567
21. Ferreon AC, Gambin Y, Lemke EA, Deniz AA. 2009. Interplay of alpha-synuclein binding and conformational switching probed by single-molecule fluorescence. Proceedings of the National Academy of Sciences of the United States of America 106:5645-5650. doi: 10.1073/pnas.0809232106
22. Ferreon AC, Ferreon JC, Wright PE, Deniz AA. 2013. Modulation of allostery by protein intrinsic disorder. Nature 498:390-394. doi: 10.1038/nature12294
23. Fromm SA, Kamenz J, Noldeke ER, Neu A, Zocher G, Sprangers R. 2014. In vitro reconstitution of a cellular phase-transition process that involves the mRNA decapping machinery. Angewandte Chemie International Edition 53:7354-7359. doi: 10.1002/anie.201402885
24. Grisendi S, Bernardi R, Rossi M, Cheng K, Khandker L, Manova K, Pandolfi PP 2005. Role of nucleophosmin in embryonic development and tumorigenesis. Nature 437:147-153. doi: 10.1038/nature03915
25. Grummitt CG, Townsley FM, Johnson CM, Warren AJ, Bycroft M. 2008. Structural consequences of nucleophosmin mutations in acute myeloid leukemia. The Journal of Biological Chemistry 283:23326-23332. doi: 10.1074/jbc.M801706200
26. Guinier A, Fournet G. 1955. Small-Angle Scattering of X-Rays. New York, NY: Wiley.
27. Gurtu V, Yan G, Zhang G. 1996. IRES bicistronic expression vectors for efficient creation of stable mammalian cell lines. Biochemical and Biophysical Research Communications 229:295-298. doi: 10.1006/bbrc.1996.1795
28. Hingorani K, Szebeni A, Olson MO. 2000. Mapping the functional domains of nucleolar protein B23. The Journal of Biological Chemistry 275:24451-24457. doi: 10.1074/jbc.M003278200
29. Hisaoka M, Nagata K, Okuwaki M. 2014. Intrinsically disordered regions of nucleophosmin/B23 regulate its RNA binding activity through their inter- and intra-molecular association. Nucleic Acids Research 42:1180-1195. doi: 10.1093/nar/gkt897
30. Holmberg Olausson K, Nistér M, Lindstrom MS. 2014. Loss of nucleolar histone chaperone NPM1 triggers rearrangement of heterochromatin and synergizes with a deficiency in DNA methyltransferase DNMT3A to drive ribosomal DNA transcription. The Journal of Biological Chemistry 289:34601-34619. doi: 10.1074/jbc.M114.569244
31. Huang DW, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37:1-13. doi: 10.1093/nar/gkn923
32. Huang DW, Sherman BT, Lempicki RA. 2008. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4:44-57. doi: 10.1038/nprot.2008.211
33. Jian Y, Gao Z, Sun J, Shen Q, Feng F, Jing Y, Yang C. 2009. RNA aptamers interfering with nucleophosmin oligomerization induce apoptosis of cancer cells. Oncogene 28:4201-4211. doi: 10.1038/onc.2009.275
34. Jones JA, Hodgkinson P, Barker AL, Hore PJ. 1996. Optimal sampling strategies for the measurement of spin-spin relaxation times. Journal of Magnetic Resonance, Series B 113:25-34. doi: 10.1006/jmrb.1996.0151
35. Kay LE, Torchia DA, Bax A. 1989. Backbone dynamics of proteins as studied by nitrogen-15 inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28:8972-8979. doi: 10.1021/bi00449a003
36. Kline SR. 2006. Reduction and analysis of SANS and USANS data using IGOR pro. Journal of Applied Crystallography 39:895-900. doi: 10.1107/S0021889806035059
37. Kroenke CD, Loria JP, Lee LK, Rance M, Palmer AG. 1998. Longitudinal and transverse 1H 15N dipolar/15 N chemical shift anisotropy relaxation interference: unambiguous determination of rotational diffusion tensors and chemical exchange effects in biological macromolecules. Journal of the American Chemical Society 120: 7905-7915. doi: 10.1021/ja980832l
38. Lakomek N-A, Ying J, Bax A. 2012. Measurement of 15N relaxation rates in perdeuterated proteins by TROSY- based methods. Journal of Biomolecular NMR 53:209-221. doi: 10.1007/s10858-012-9626-5
39. Lakomek N-A, Kaufman JD, Stahl SJ, Louis JM, Grishaev A, Wingfield PT, Bax A. 2013. Internal dynamics of the homotrimeric HIV-1 viral coat protein gp41 on multiple time scales. Angewandte Chemie International Edition 52:3911-3915. doi: 10.1002/anie.201207266
40. Lee LK, Rance M, Chazin WJ, Palmer AG. 1997. Rotational diffusion anisotropy of proteins from simultaneous analysis of 15N and 13C alpha nuclear spin relaxation. Journal of Biomolecular NMR 9:287-298.
41. Lee AL, Wand AJ. 1999. Assessing potential bias in the determination of rotational correlation times of proteins by NMR relaxation. Journal of Biomolecular NMR 13:101-112. doi: 10.1023/A:1008304220445
42. Lee C, Smith BA, Bandyopadhyay K, Gjerset RA. 2005. DNA damage disrupts the p14ARF-B23(nucleophosmin) interaction and triggers a transient subnuclear redistribution of p14ARF. Cancer Research 65:9834-9842. doi: 10.1158/0008-5472.CAN-05-1759
43. Lee D, Hilty C, Wider G, Wuthrich K. 2006. Effective rotational correlation times of proteins from NMR relaxation interference. Journal of Magnetic Resonance 178:72-76. doi: 10.1016/j.jmr.2005.08.014
44. Li P, Banjade S, Cheng HC, Kim S, Chen B, Guo L, Llaguno M, Hollingsworth JV, King DS, Banani SF, Russo PS, Jiang QX, Nixon BT, Rosen MK. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336-340. doi: 10.1038/nature10879
45. Lindstrom MS. 2011. NPM1/B23: a multifunctional chaperone in ribosome biogenesis and chromatin remodeling. Biochemistry Research International 2011. doi: 10.1155/2011/195209
46. Lindstrom MS. 2012. Elucidation of motifs in ribosomal protein S9 that mediate its nucleolar localization and binding to NPM1/nucleophosmin. PloS One 7:e52476. doi: 10.1371/journal.pone.0052476
47. Lipari G, Szabo A. 1982. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. theory and range of validity. Journal of the American Chemical Society 104:4546-4559. doi: 10.1021/ja00381a009
48. Lorieau JL, Louis JM, Bax A. 2011. Whole-body rocking motion of a fusion peptide in lipid bilayers from size- dispersed 15N NMR relaxation. Journal of the American Chemical Society 133:14184-14187. doi: 10.1021/ja2045309
49. Markin CJ, Spyracopoulos L. 2012. Accuracy and precision of protein-ligand interaction kinetics determined from chemical shift titrations. Journal of Biomolecular NMR 54:355-376. doi: 10.1007/s10858-012-9678-6
50. Mitrea DM, Grace CR, Buljan M, Yun M-K, Pytel NJ, Satumba J, Nourse A, Park C-G, Madan Babu M, White SW, Kriwacki RW. 2014. Structural polymorphism in the n-terminal oligomerization domain of NPM1. Proceedings of the National Academy of Sciences 111:4466-4471. doi: 10.1073/pnas.1321007111
51. Negi SS, Olson MO. 2006. Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23. Journal of Cell Science 119:3676-3685. doi: 10.1242/jcs.03090
52. Ortega A, García de la Torre J. 2005. Efficient, accurate calculation of rotational diffusion and NMR relaxation of globular proteins from atomic-level structures and approximate hydrodynamic calculations. Journal of the American Chemical Society 127:12764-12765. doi: 10.1021/ja053080l
53. Palmer AG. 2004. NMR characterization of the dynamics of biomacromolecules. Chemical Reviews 104:3623-3640. doi: 10.1021/cr030413t
54. Paron I, D’Elia A, D’Ambrosio C, Scaloni A, D’Aurizio F, Prescott A, Damante G, Tell G. 2004. A proteomic approach to identify early molecular targets of oxidative stress in human epithelial lens cells. The Biochemical Journal 378:929-937. doi: 10.1042/BJ20031190
55. Rosner M, Schipany K, Hengstschlager M. 2013. Merging high-quality biochemical fractionation with a refined flow cytometry approach to monitor nucleocytoplasmic protein expression throughout the unperturbed mammalian cell cycle. Nature Protocols 8:602-626. doi: 10.1038/nprot.2013.011
56. Rosorius O, Fries B, Stauber RH, Hirschmann N, Bevec D, Hauber J. 2000. Human ribosomal protein L5 contains defined nuclear localization and export signals. The Journal of Biological Chemistry 275:12061-12068.
57. Schuck P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophysical Journal 78:1606-1619. doi: 10.1016/S0006-3495(00)76713-0
58. Scott MS, Boisvert FM, McDowall MD, Lamond AI, Barton GJ. 2010. Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Research 38:7388-7399. doi: 10.1093/nar/gkq653
59. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, Tsien RY. 2004. Improved monomeric red, orange and yellow fluorescent proteins derived from discosoma sp. red fluorescent protein. Nature Biotechnology 22:1567-1572. doi: 10.1038/nbt1037
60. Svergun DI. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. Journal of Applied Crystallography 25:495-503. doi: 10.1107/S0021889892001663
61. Svergun D, Barberato C, Koch MHJ. 1995. CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. Journal of Applied Crystallography 28:768-773. doi: 10.1107/S0021889895007047
62. UniProt Consortium. 2014. Activities at the universal protein resource (uniProt). Nucleic Acids Research 42: D191-198. doi: 10.1093/nar/gkt1140
63. Wang D, Baumann A, Szebeni A, Olson MO. 1994. The nucleic acid binding activity of nucleolar protein B23.1 resides in its carboxyl-terminal end. The Journal of Biological Chemistry 269:30994-30998.
64. Weber SC, Brangwynne CP. 2015. Inverse size scaling of the nucleolus by a concentration-dependent phase transition. Current Biology 25:641-646. doi: 10.1016/j.cub.2015.01.012
65. Wignall GD, Bates FS. 1987. Absolute calibration of small-angle neutron scattering data. Journal of Applied Crystallography 20:28-40. doi: 10.1107/S0021889887087181
66. Yao L, Vogeli B, Ying J, Bax A. 2008. NMR determination of amide n-h equilibrium bond length from concerted dipolar coupling measurements. Journal of the American Chemical Society 130:16518-16520. doi: 10.1021/ja805654f
67. Yao L, Grishaev A, Cornilescu G, Bax A. 2010. Site-specific backbone amide (15)N chemical shift anisotropy tensors in a small protein from liquid crystal and cross-correlated relaxation measurements. Journal of the American Chemical Society 132:4295-4309. doi: 10.1021/ja910186u
68. Yao Z, Duan S, Hou D, Wang W, Wang G, Liu Y, Wen L, Wu M. 2010b. B23 acts as a nucleolar stress sensor and promotes cell survival through its dynamic interaction with hnRNPU and hnRNPA1. Oncogene 29:1821-1834. doi: 10.1038/onc.2009.473
69. Zhao JK, Gao CY, Liu D. 2010. The extended q -range small-angle neutron scattering diffractometer at the SNS. Journal of Applied Crystallography 43:1068-1077. doi: 10.1107/S002188981002217X
70. Zhao H, Brautigam CA, Ghirlando R, Schuck P. 2013. Overview of Current Methods in Sedimentation Velocity and Sedimentation Equilibrium Analytical Ultracentrifugation. John E Coligan [et al]. Current Protocols in Research article Protein Science, Chapter 20, Unit 20. Hoboken, NJ: John Wiley & Sons, Inc. p 12. doi: 10.1002/0471140864.ps2012s71
71. Zhao H, Ghirlando R, Alfonso C, Arisaka F, Attali I, Bain DL, Bakhtina MM, Becker DF, Bedwell GJ, Bekdemir A, Besong TM, Birck C, Brautigam CA, Brennerman W, Byron O, Bzowska A, Chaires JB, Chaton CT, Colfen H, Connaghan KD, Crowley KA, Curth U, Daviter T, Dean WL, Díez AI, Ebel C, Eckert DM, Eisele LE, Eisenstein E, England P, Escalante C, Fagan JA, Fairman R, Finn RM, Fischle W, de la Torre JG, Gor J, Gustafsson H, Hall D, Harding SE, Cifre JG, Herr AB, Howell EE, Isaac RS, Jao SC, Jose D, Kim SJ, Kokona B, Kornblatt JA, Kosek D, Krayukhina E, Krzizike D, Kusznir EA, Kwon H, Larson A, Laue TM, Le Roy A, Leech AP, Lilie H, Luger K, Luque-Ortega JR, Ma J, May CA, Maynard EL, Modrak-Wojcik A, Mok YF, Mucke N, Nagel-Steger L, Narlikar GJ, Noda M, Nourse A, Obsil T, Park CK, Park JK, Pawelek PD, Perdue EE, Perkins SJ, Perugini MA, Peterson CL, Peverelli MG, Piszczek G, Prag G, Prevelige PE, Raynal BD, Rezabkova L, Richter K, Ringel AE, Rosenberg R, Rowe AJ, Rufer AC, Scott DJ, Seravalli JG, Solovyova AS, Song R, Staunton D, Stoddard C, Stott K, Strauss HM, Streicher WW, Sumida JP, Swygert SG, Szczepanowski RH, Tessmer I, Toth RT, Tripathy A, Uchiyama S, Uebel SF, Unzai S, Gruber AV, von Hippel PH, Wandrey C, Wang SH, Weitzel SE, Wielgus-Kutrowska B, Wolberger C, Wolff M, Wright E, Wu YS, Wubben JM, Schuck P. 2015. A multilaboratory comparison of calibration accuracy and the performance of external references in analytical ultracentrifugation. PloS One 10: e0126420. doi: 10.1371/journal.pone.0126420