Dysregulation of RNA polymerase I transcription during disease

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 3-4, 2013, Pages 342-360

  Hannan, K M ^a   Sanij, E ^a,b   Rothblum, L I ^c   Hannan, R D ^a,b,d,e   Pearson, R B ^a,b,d  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d MONASH UNIVERSITY   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Atrophy; Cancer; Hypertrophy; Oncogene; Ribosomopathies; RNA polymerase I transcription

Indexed keywords

CISPLATIN; CX 5461; DACTINOMYCIN; DNA DIRECTED RNA POLYMERASE; FLUOROURACIL; IRINOTECAN; MITOMYCIN; QUARFLOXIN; TEMSIROLIMUS; TOPOTECAN; UNCLASSIFIED DRUG;

BLACKFAN DIAMOND ANEMIA; BLOOM SYNDROME; COCKAYNE SYNDROME; DE LANGE SYNDROME; DISEASE ASSOCIATION; DRUG MECHANISM; DYSKERATOSIS CONGENITA; GENE MUTATION; GENE THERAPY; HEART HYPERTROPHY; HUMAN; INDIAN CHILDHOOD CIRRHOSIS; KIDNEY HYPERTROPHY; MANDIBULOFACIAL DYSOSTOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA PROCESSING; ROBERTS SYNDROME; SHWACHMAN SYNDROME; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WERNER SYNDROME; X LINKED MENTAL RETARDATION;

ANIMALS; GENE EXPRESSION REGULATION; GENETIC DISEASES, INBORN; HUMANS; RIBOSOMAL PROTEINS; RNA POLYMERASE I; RNA, RIBOSOMAL; TRANSCRIPTION FACTORS, TFIII; TRANSCRIPTION, GENETIC;

EID: 84875234347     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.10.014     Document Type: Review

References (265)

1. Drygin D., Rice W.G., Grummt I. The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu. Rev. Pharmacol. Toxicol. 2010, 50:131-156.
2. Grummt I. Wisely chosen paths-regulation of rRNA synthesis: delivered on 30 June 2010 at the 35th FEBS Congress in Gothenburg, Sweden. FEBS J. 2010, 277:4626-4639.
3. White R.J. RNA polymerases I and III, non-coding RNAs and cancer. Trends Genet. 2008, 24:622-629.
4. Narla A., Ebert B.L. Translational medicine: ribosomopathies. Blood 2011, 118:4300-4301.
5. Chiabrando D., Tolosano E. Diamond Blackfan anemia at the crossroad between ribosome biogenesis and heme metabolism. Adv. Hematol. 2010, 2010:790632.
6. Ball S. Diamond Blackfan anemia. Hematology Am. Soc. Hematol. Educ. Program 2011, 2011:487-491.
7. Pellagatti A., Hellstrom-Lindberg E., Giagounidis A., Perry J., Malcovati L., Della Porta M.G., Jadersten M., Killick S., Fidler C., Cazzola M., Wainscoat J.S., Boultwood J. Haploinsufficiency of RPS14 in 5q- syndrome is associated with deregulation of ribosomal- and translation-related genes. Br. J. Haematol. 2008, 142:57-64.
8. Lin C.I., Yeh N.H. Treacle recruits RNA polymerase I complex to the nucleolus that is independent of UBF. Biochem. Biophys. Res. Commun. 2009, 386:396-401.
9. Trainor P.A., Dixon J., Dixon M.J. Treacher Collins syndrome: etiology, pathogenesis and prevention. Eur. J. Hum. Genet. 2009, 17:275-283.
10. Valdez B.C., Henning D., So R.B., Dixon J., Dixon M.J. The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10709-10714.
11. Grierson P.M., Lillard K., Behbehani G.K., Combs K.A., Bhattacharyya S., Acharya S., Groden J. BLM helicase facilitates RNA polymerase I-mediated ribosomal RNA transcription. Hum. Mol. Genet. 2012, 21:1172-1183.
12. Shiratori M., Suzuki T., Itoh C., Goto M., Furuichi Y., Matsumoto T. WRN helicase accelerates the transcription of ribosomal RNA as a component of an RNA polymerase I-associated complex. Oncogene 2002, 21:2447-2454.
13. Lutomska A., Lebedev A., Scharffetter-Kochanek K., Iben S. The transcriptional response to distinct growth factors is impaired in Werner syndrome cells. Exp. Gerontol. 2008, 43:820-826.
14. Ganapathi K.A., Austin K.M., Lee C.S., Dias A., Malsch M.M., Reed R., Shimamura A. The human Shwachman-Diamond syndrome protein, SBDS, associates with ribosomal RNA. Blood 2007, 110:1458-1465.
15. Yoon A., Peng G., Brandenburger Y., Zollo O., Xu W., Rego E., Ruggero D. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 2006, 312:902-906.
16. Ridanpaa M., van Eenennaam H., Pelin K., Chadwick R., Johnson C., Yuan B., vanVenrooij W., Pruijn G., Salmela R., Rockas S., Makitie O., Kaitila I., de la Chapelle A. Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia. Cell 2001, 104:195-203.
17. Thiel C.T., Rauch A. The molecular basis of the cartilage-hair hypoplasia-anauxetic dysplasia spectrum. Best Pract. Res. Clin. Endocrinol. Metab. 2011, 25:131-142.
18. Freed E.F., Baserga S.J. The C-terminus of Utp4, mutated in childhood cirrhosis, is essential for ribosome biogenesis. Nucleic Acids Res. 2010, 38:4798-4806.
19. Freed E.F., Prieto J.L., McCann K.L., McStay B., Baserga S.J. NOL11, implicated in the pathogenesis of North American Indian childhood cirrhosis, is required for pre-rRNA transcription and processing. PLoS Genet. 2012, 8:e1002892.
20. Meyer B., Wurm J.P., Kotter P., Leisegang M.S., Schilling V., Buchhaupt M., Held M., Bahr U., Karas M., Heckel A., Bohnsack M.T., Wohnert J., Entian K.D. The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of Psi1191 in yeast 18S rRNA. Nucleic Acids Res. 2011, 39:1526-1537.
21. Nousbeck J., Spiegel R., Ishida-Yamamoto A., Indelman M., Shani-Adir A., Adir N., Lipkin E., Bercovici S., Geiger D., van Steensel M.A., Steijlen P.M., Bergman R., Bindereif A., Choder M., Shalev S., Sprecher E. Alopecia, neurological defects, and endocrinopathy syndrome caused by decreased expression of RBM28, a nucleolar protein associated with ribosome biogenesis. Am. J. Hum. Genet. 2008, 82:1114-1121.
22. Bywater M.J., Poortinga G., Sanij E., Hein N., Peck A., Cullinane C., Wall M., Cluse L., Drygin D., Anderes K., Huser N., Proffitt C., Bliesath J., Haddach M., Schwaebe M.K., Ryckman D.M., Rice W.G., Schmitt C., Lowe S.W., Johnstone R.W., Pearson R.B., McArthur G.A., Hannan R.D. Inhibition of RNA polymerase I as a therapeutic strategy to promote cancer-specific activation of p53. Cancer Cell 2012, 22:51-65.
23. Drygin D., Lin A., Bliesath J., Ho C.B., O'Brien S.E., Proffitt C., Omori M., Haddach M., Schwaebe M.K., Siddiqui-Jain A., Streiner N., Quin J.E., Sanij E., Bywater M.J., Hannan R.D., Ryckman D., Anderes K., Rice W.G. Targeting RNA polymerase I with an oral small molecule CX-5461 inhibits ribosomal RNA synthesis and solid tumor growth. Cancer Res. 2011, 71:1418-1430.
24. Narla A., Ebert B.L. Ribosomopathies: human disorders of ribosome dysfunction. Blood 2010, 115:3196-3205.
25. Fumagalli S., Thomas G. The role of p53 in ribosomopathies. Semin. Hematol. 2011, 48:97-105.
26. Dixon J., Dixon M.J. Genetic background has a major effect on the penetrance and severity of craniofacial defects in mice heterozygous for the gene encoding the nucleolar protein Treacle. Dev. Dyn. 2004, 229:907-914.
27. Dixon J., Jones N.C., Sandell L.L., Jayasinghe S.M., Crane J., Rey J.P., Dixon M.J., Trainor P.A. Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13403-13408.
28. Jones N.C., Lynn M.L., Gaudenz K., Sakai D., Aoto K., Rey J.P., Glynn E.F., Ellington L., Du C., Dixon J., Dixon M.J., Trainor P.A. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 2008, 14:125-133.
29. Dauwerse J.G., Dixon J., Seland S., Ruivenkamp C.A., van Haeringen A., Hoefsloot L.H., Peters D.J., Boers A.C., Daumer-Haas C., Maiwald R., Zweier C., Kerr B., Cobo A.M., Toral J.F., Hoogeboom A.J., Lohmann D.R., Hehr U., Dixon M.J., Breuning M.H., Wieczorek D. Mutations in genes encoding subunits of RNA polymerases I and III cause Treacher Collins syndrome. Nat. Genet. 2011, 43:20-22.
30. Andersen J.S., Lam Y.W., Leung A.K., Ong S.E., Lyon C.E., Lamond A.I., Mann M. Nucleolar proteome dynamics. Nature 2005, 433:77-83.
31. Boisvert F.M., Ahmad Y., Gierlinski M., Charriere F., Lamont D., Scott M., Barton G., Lamond A.I. A quantitative spatial proteomics analysis of proteome turnover in human cells. Mol. Cell. Proteomics 2012, 11(M111):011429.
32. Edery P., Manach Y., Le Merrer M., Till M., Vignal A., Lyonnet S., Munnich A. Apparent genetic homogeneity of the Treacher Collins-Franceschetti syndrome. Am. J. Med. Genet. 1994, 52:174-177.
33. Conte C., D'Apice M.R., Rinaldi F., Gambardella S., Sangiuolo F., Novelli G. Novel mutations of TCOF1 gene in European patients with Treacher Collins syndrome. BMC Med. Genet. 2011, 12:125.
34. Dixon M.J., Read A.P., Donnai D., Colley A., Dixon J., Williamson R. The gene for Treacher Collins syndrome maps to the long arm of chromosome 5. Am. J. Hum. Genet. 1991, 49:17-22.
35. Marszalek-Kruk B.A., Wojcicki P., Smigiel R., Trzeciak W.H. Novel insertion in exon 5 of the TCOF1 gene in twin sisters with Treacher Collins syndrome. J. Appl. Genet. 2012, 53:279-282.
36. Sakai D., Dixon J., Dixon M.J., Trainor P.A. Mammalian neurogenesis requires Treacle-Plk1 for precise control of spindle orientation, mitotic progression, and maintenance of neural progenitor cells. PLoS Genet. 2012, 8:e1002566.
37. Tikoo S., Sengupta S. Time to bloom. Genome Integr. 2010, 1:14.
38. Rossi M.L., Ghosh A.K., Bohr V.A. Roles of Werner syndrome protein in protection of genome integrity. DNA Repair (Amst.) 2010, 9:331-344.
39. Chester N., Kuo F., Kozak C., O'Hara C.D., Leder P. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev. 1998, 12:3382-3393.
40. Lebel M., Leder P. A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13097-13102.
41. Lombard D.B., Beard C., Johnson B., Marciniak R.A., Dausman J., Bronson R., Buhlmann J.E., Lipman R., Curry R., Sharpe A., Jaenisch R., Guarente L. Mutations in the WRN gene in mice accelerate mortality in a p53-null background. Mol. Cell. Biol. 2000, 20:3286-3291.
42. Yankiwski V., Marciniak R.A., Guarente L., Neff N.F. Nuclear structure in normal and Bloom syndrome cells. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5214-5219.
43. Schawalder J., Paric E., Neff N.F. Telomere and ribosomal DNA repeats are chromosomal targets of the bloom syndrome DNA helicase. BMC Cell Biol. 2003, 4:15.
44. Wang Y., Smith K., Waldman B.C., Waldman A.S. Depletion of the bloom syndrome helicase stimulates homology-dependent repair at double-strand breaks in human chromosomes. DNA Repair (Amst.) 2011, 10:416-426.
45. Kaneko H., Fukao T., Kasahara K., Yamada T., Kondo N. Augmented cell death with Bloom syndrome helicase deficiency. Mol. Med. Rep. 2011, 4:607-609.
46. Natale V. A comprehensive description of the severity groups in Cockayne syndrome. Am. J. Med. Genet. A 2011, 155A:1081-1095.
47. Laugel V., Dalloz C., Durand M., Sauvanaud F., Kristensen U., Vincent M.C., Pasquier L., Odent S., Cormier-Daire V., Gener B., Tobias E.S., Tolmie J.L., Martin-Coignard D., Drouin-Garraud V., Heron D., Journel H., Raffo E., Vigneron J., Lyonnet S., Murday V., Gubser-Mercati D., Funalot B., Brueton L., Sanchez Del Pozo J., Munoz E., Gennery A.R., Salih M., Noruzinia M., Prescott K., Ramos L., Stark Z., Fieggen K., Chabrol B., Sarda P., Edery P., Bloch-Zupan A., Fawcett H., Pham D., Egly J.M., Lehmann A.R., Sarasin A., Dollfus H. Mutation update for the CSB/ERCC6 and CSA/ERCC8 genes involved in Cockayne syndrome. Hum. Mutat. 2010, 31:113-126.
48. Fousteri M., Vermeulen W., van Zeeland A.A., Mullenders L.H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 2006, 23:471-482.
49. Bradsher J., Auriol J., Proietti de Santis L., Iben S., Vonesch J.L., Grummt I., Egly J.M. CSB is a component of RNA pol I transcription. Mol. Cell 2002, 10:819-829.
50. Lebedev A., Scharffetter-Kochanek K., Iben S. Truncated Cockayne syndrome B protein represses elongation by RNA polymerase I. J. Mol. Biol. 2008, 382:266-274.
51. Assfalg R., Lebedev A., Gonzalez O.G., Schelling A., Koch S., Iben S. TFIIH is an elongation factor of RNA polymerase I. Nucleic Acids Res. 2012, 40:650-659.
52. Yuan X., Feng W., Imhof A., Grummt I., Zhou Y. Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Mol. Cell 2007, 27:585-595.
53. Latini P., Frontini M., Caputo M., Gregan J., Cipak L., Filippi S., Kumar V., Velez-Cruz R., Stefanini M., Proietti-De-Santis L. CSA and CSB proteins interact with p53 and regulate its Mdm2-dependent ubiquitination. Cell Cycle 2011, 10:3719-3730.
54. Lake R.J., Basheer A., Fan H.Y. Reciprocally regulated chromatin association of Cockayne syndrome protein B and p53 protein. J. Biol. Chem. 2011, 286:34951-34958.
55. Frontini M., Proietti-De-Santis L. Interaction between the Cockayne syndrome B and p53 proteins: implications for aging. Aging (Albany NY) 2012, 4:89-97.
56. Yu A., Fan H.Y., Liao D., Bailey A.D., Weiner A.M. Activation of p53 or loss of the Cockayne syndrome group B repair protein causes metaphase fragility of human U1, U2, and 5S genes. Mol. Cell 2000, 5:801-810.
57. Laumonnier F., Holbert S., Ronce N., Faravelli F., Lenzner S., Schwartz C.E., Lespinasse J., Van Esch H., Lacombe D., Goizet C., Phan-Dinh Tuy F., van Bokhoven H., Fryns J.P., Chelly J., Ropers H.H., Moraine C., Hamel B.C., Briault S. Mutations in PHF8 are associated with X linked mental retardation and cleft lip/cleft palate. J. Med. Genet. 2005, 42:780-786.
58. Lisik M.Z., Sieron A.L. X-linked mental retardation. Med. Sci. Monit. 2008, 14:RA221-RA229.
59. Dawson M.A., Bannister A.J. Demethylases go mental. Mol. Cell 2010, 38:155-157.
60. Abidi F.E., Miano M.G., Murray J.C., Schwartz C.E. A novel mutation in the PHF8 gene is associated with X-linked mental retardation with cleft lip/cleft palate. Clin. Genet. 2007, 72:19-22.
61. Kleine-Kohlbrecher D., Christensen J., Vandamme J., Abarrategui I., Bak M., Tommerup N., Shi X., Gozani O., Rappsilber J., Salcini A.E., Helin K. A functional link between the histone demethylase PHF8 and the transcription factor ZNF711 in X-linked mental retardation. Mol. Cell 2010, 38:165-178.
62. Loenarz C., Ge W., Coleman M.L., Rose N.R., Cooper C.D., Klose R.J., Ratcliffe P.J., Schofield C.J. PHF8, a gene associated with cleft lip/palate and mental retardation, encodes for an Nepsilon-dimethyl lysine demethylase. Hum. Mol. Genet. 2010, 19:217-222.
63. Qiu J., Shi G., Jia Y., Li J., Wu M., Dong S., Wong J. The X-linked mental retardation gene PHF8 is a histone demethylase involved in neuronal differentiation. Cell Res. 2010, 20:908-918.
64. Qi H.H., Sarkissian M., Hu G.Q., Wang Z., Bhattacharjee A., Gordon D.B., Gonzales M., Lan F., Ongusaha P.P., Huarte M., Yaghi N.K., Lim H., Garcia B.A., Brizuela L., Zhao K., Roberts T.M., Shi Y. Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 2010, 466:503-507.
65. Liu W., Tanasa B., Tyurina O.V., Zhou T.Y., Gassmann R., Liu W.T., Ohgi K.A., Benner C., Garcia-Bassets I., Aggarwal A.K., Desai A., Dorrestein P.C., Glass C.K., Rosenfeld M.G. PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression. Nature 2010, 466:508-512.
66. Feng W., Yonezawa M., Ye J., Jenuwein T., Grummt I. PHF8 activates transcription of rRNA genes through H3K4me3 binding and H3K9me1/2 demethylation. Nat. Struct. Mol. Biol. 2010, 17:445-450.
67. Zhu Z., Wang Y., Li X., Xu L., Wang X., Sun T., Dong X., Chen L., Mao H., Yu Y., Li J., Chen P.A., Chen C.D. PHF8 is a histone H3K9me2 demethylase regulating rRNA synthesis. Cell Res. 2010, 20:794-801.
68. Bose T., Lee K.K., Lu S., Xu B., Harris B., Slaughter B., Unruh J., Garrett A., McDowell W., Box A., Li H., Peak A., Ramachandran S., Seidel C., Gerton J.L. Cohesin proteins promote ribosomal RNA production and protein translation in yeast and human cells. PLoS Genet. 2012, 8:e1002749.
69. Ide S., Miyazaki T., Maki H., Kobayashi T. Abundance of ribosomal RNA gene copies maintains genome integrity. Science 2010, 327:693-696.
70. Liu J., Krantz I.D. Cohesin and human disease. Annu. Rev. Genomics Hum. Genet. 2008, 9:303-320.
71. Monnich M., Kuriger Z., Print C.G., Horsfield J.A. A zebrafish model of Roberts syndrome reveals that Esco2 depletion interferes with development by disrupting the cell cycle. PLoS One 2011, 6:e20051.
72. Najib S., Saint-Laurent N., Esteve J.P., Schulz S., Boutet-Robinet E., Fourmy D., Lattig J., Mollereau C., Pyronnet S., Susini C., Bousquet C. A switch of G protein-coupled receptor binding preference from phosphoinositide 3-kinase (PI3K)-p85 to filamin A negatively controls the PI3K pathway. Mol. Cell. Biol. 2012, 32:1004-1016.
73. Zhou A.X., Hartwig J.H., Akyurek L.M. Filamins in cell signaling, transcription and organ development. Trends Cell Biol. 2010, 20:113-123.
74. Velkova A., Carvalho M.A., Johnson J.O., Tavtigian S.V., Monteiro A.N. Identification of Filamin A as a BRCA1-interacting protein required for efficient DNA repair. Cell Cycle 2010, 9:1421-1433.
75. Yuan Y., Shen Z. Interaction with BRCA2 suggests a role for filamin-1 (hsFLNa) in DNA damage response. J. Biol. Chem. 2001, 276:48318-48324.
76. Yue J., Lu H., Liu J., Berwick M., Shen Z. Filamin-A as a marker and target for DNA damage based cancer therapy. DNA Repair (Amst.) 2012, 11:192-200.
77. Deng W., Lopez-Camacho C., Tang J.Y., Mendoza-Villanueva D., Maya-Mendoza A., Jackson D.A., Shore P. Cytoskeletal protein filamin A is a nucleolar protein that suppresses ribosomal RNA gene transcription. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1524-1529.
78. Shenoy N., Kessel R., Bhagat T., Bhattacharya S., Yu Y., McMahon C., Verma A. Alterations in the ribosomal machinery in cancer and hematologic disorders. J. Hematol. Oncol. 2012, 5:32.
79. Flygare J., Kiefer T., Miyake K., Utsugisawa T., Hamaguchi I., Da Costa L., Richter J., Davey E.J., Matsson H., Dahl N., Wiznerowicz M., Trono D., Karlsson S. Deficiency of ribosomal protein S19 in CD34+ cells generated by siRNA blocks erythroid development and mimics defects seen in Diamond-Blackfan anemia. Blood 2005, 105:4627-4634.
80. Matsson H., Davey E.J., Draptchinskaia N., Hamaguchi I., Ooka A., Leveen P., Forsberg E., Karlsson S., Dahl N. Targeted disruption of the ribosomal protein S19 gene is lethal prior to implantation. Mol. Cell. Biol. 2004, 24:4032-4037.
81. Miyake K., Flygare J., Kiefer T., Utsugisawa T., Richter J., Ma Z., Wiznerowicz M., Trono D., Karlsson S. Development of cellular models for ribosomal protein S19 (RPS19)-deficient Diamond-Blackfan anemia using inducible expression of siRNA against RPS19. Mol. Ther. 2005, 11:627-637.
82. Choesmel V., Fribourg S., Aguissa-Toure A.H., Pinaud N., Legrand P., Gazda H.T., Gleizes P.E. Mutation of ribosomal protein RPS24 in Diamond-Blackfan anemia results in a ribosome biogenesis disorder. Hum. Mol. Genet. 2008, 17:1253-1263.
83. Fumagalli S., Di Cara A., Neb-Gulati A., Natt F., Schwemberger S., Hall J., Babcock G.F., Bernardi R., Pandolfi P.P., Thomas G. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat. Cell Biol. 2009, 11:501-508.
84. Fumagalli S., Ivanenkov V.V., Teng T., Thomas G. Suprainduction of p53 by disruption of 40S and 60S ribosome biogenesis leads to the activation of a novel G2/M checkpoint. Genes Dev. 2012, 26:1028-1040.
85. Dutt S., Narla A., Lin K., Mullally A., Abayasekara N., Megerdichian C., Wilson F.H., Currie T., Khanna-Gupta A., Berliner N., Kutok J.L., Ebert B.L. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood 2011, 117:2567-2576.
86. Moniz H., Gastou M., Leblanc T., Hurtaud C., Cretien A., Lecluse Y., Raslova H., Larghero J., Croisille L., Faubladier M., Bluteau O., Lordier L., Tchernia G., Vainchenker W., Mohandas N., Da Costa L. Primary hematopoietic cells from DBA patients with mutations in RPL11 and RPS19 genes exhibit distinct erythroid phenotype in vitro. Cell Death Dis. 2012, 3:e356.
87. Sieff C.A., Yang J., Merida-Long L.B., Lodish H.F. Pathogenesis of the erythroid failure in Diamond Blackfan anaemia. Br. J. Haematol. 2010, 148:611-622.
88. Kraft C., Deplazes A., Sohrmann M., Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 2008, 10:602-610.
89. Duan X., Kelsen S.G., Clarkson A.B., Ji R., Merali S. SILAC analysis of oxidative stress-mediated proteins in human pneumocytes: new role for treacle. Proteomics 2010, 10:2165-2174.
90. Uhlen M., Oksvold P., Fagerberg L., Lundberg E., Jonasson K., Forsberg M., Zwahlen M., Kampf C., Wester K., Hober S., Wernerus H., Bjorling L., Ponten F. Towards a knowledge-based Human Protein Atlas. Nat. Biotechnol. 2010, 28:1248-1250.
91. Lempiainen H., Shore D. Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 2009, 21:855-863.
92. White R.J. RNA polymerases I and III, growth control and cancer. Nat. Rev. Mol. Cell Biol. 2005, 6:69-78.
93. Hannan R.D., Jenkins A., Jenkins A.K., Brandenburger Y. Cardiac hypertrophy: a matter of translation. Clin. Exp. Pharmacol. Physiol. 2003, 30:517-527.
94. Onyezili F.N. On two paradoxical side-effects of prednisolone in rats, ribosomal RNA biosyntheses, and a mechanism of action. Biochem. Pharmacol. 1986, 35:2309-2312.
95. Kuwahara K., Nishikimi T., Nakao K. Transcriptional regulation of the fetal cardiac gene program. J. Pharmacol. Sci. 2012, 119:198-203.
96. Hill J.A., Olson E.N. Cardiac plasticity. N. Engl. J. Med. 2008, 358:1370-1380.
97. Chein K.R., Grace A.A., Hunter J.J. Molecular Basis of Cardiac Hypertrophy and Failure 1998, WB Saunders Co., Philadelphia.
98. Stefanovsky V.Y., Pelletier G., Hannan R., Gagnon-Kugler T., Rothblum L.I., Moss T. An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol. Cell 2001, 8:1063-1073.
99. Sala V., Gallo S., Leo C., Gatti S., Gelb B.D., Crepaldi T. Signaling to cardiac hypertrophy: insights from human and mouse RASopathies. Mol. Med. 2012.
100. Morgan H.E., Siehl D., Chua B.H., Lautensack-Belser N. Faster protein and ribosome synthesis in hypertrophying heart. Basic Res. Cardiol. 1985, 80(Suppl. 2):115-118.
101. Siehl D., Chua B.H., Lautensack-Belser N., Morgan H.E. Faster protein and ribosome synthesis in thyroxine-induced hypertrophy of rat heart. Am. J. Physiol. 1985, 248:C309-C319.
102. McDermott P.J., Rothblum L.I., Smith S.D., Morgan H.E. Accelerated rates of ribosomal RNA synthesis during growth of contracting heart cells in culture. J. Biol. Chem. 1989, 264:18220-18227.
103. Hannan R.D., Luyken J., Rothblum L.I. Regulation of ribosomal DNA transcription during contraction-induced hypertrophy of neonatal cardiomyocytes. J. Biol. Chem. 1996, 271:3213-3220.
104. Hannan R.D., Luyken J., Rothblum L.I. Regulation of rDNA transcription factors during cardiomyocyte hypertrophy induced by adrenergic agents. J. Biol. Chem. 1995, 270:8290-8297.
105. Luyken J., Hannan R.D., Cheung J.Y., Rothblum L.I. Regulation of rDNA transcription during endothelin-1-induced hypertrophy of neonatal cardiomyocytes. Hyperphosphorylation of upstream binding factor, an rDNA transcription factor. Circ. Res. 1996, 78:354-361.
106. Hannan R.D., Stefanovsky V., Taylor L., Moss T., Rothblum L.I. Overexpression of the transcription factor UBF1 is sufficient to increase ribosomal DNA transcription in neonatal cardiomyocytes: implications for cardiac hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:8750-8755.
107. Brandenburger Y., Jenkins A., Autelitano D.J., Hannan R.D. Increased expression of UBF is a critical determinant for rRNA synthesis and hypertrophic growth of cardiac myocytes. FASEB J. 2001, 15:2051-2053.
108. Brandenburger Y., Arthur J.F., Woodcock E.A., Du X.J., Gao X.M., Autelitano D.J., Rothblum L.I., Hannan R.D. Cardiac hypertrophy in vivo is associated with increased expression of the ribosomal gene transcription factor UBF. FEBS Lett. 2003, 548:79-84.
109. Rosello-Lleti E., Rivera M., Cortes R., Azorin I., Sirera R., Martinez-Dolz L., Hove L., Cinca J., Lago F., Gonzalez-Juanatey J.R., Salvador A., Portoles M. Influence of heart failure on nucleolar organization and protein expression in human hearts. Biochem. Biophys. Res. Commun. 2012, 418:222-228.
110. Rohini A., Agrawal N., Koyani C.N., Singh R. Molecular targets and regulators of cardiac hypertrophy. Pharmacol. Res. 2010, 61:269-280.
111. Ruwhof C., van der Laarse A. Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways. Cardiovasc. Res. 2000, 47:23-37.
112. Chaudhary A., King W.G., Mattaliano M.D., Frost J.A., Diaz B., Morrison D.K., Cobb M.H., Marshall M.S., Brugge J.S. Phosphatidylinositol 3-kinase regulates Raf1 through Pak phosphorylation of serine 338. Curr. Biol. 2000, 10:551-554.
113. Pandit B., Sarkozy A., Pennacchio L.A., Carta C., Oishi K., Martinelli S., Pogna E.A., Schackwitz W., Ustaszewska A., Landstrom A., Bos J.M., Ommen S.R., Esposito G., Lepri F., Faul C., Mundel P., Lopez Siguero J.P., Tenconi R., Selicorni A., Rossi C., Mazzanti L., Torrente I., Marino B., Digilio M.C., Zampino G., Ackerman M.J., Dallapiccola B., Tartaglia M., Gelb B.D. Gain-of-function RAF1 mutations cause Noonan and LEOPARD syndromes with hypertrophic cardiomyopathy. Nat. Genet. 2007, 39:1007-1012.
114. Vettel C., Wittig K., Vogt A., Wuertz C.M., El-Armouche A., Lutz S., Wieland T. A novel player in cellular hypertrophy: G(i)betagamma/PI3K-dependent activation of the RacGEF TIAM-1 is required for alpha(1)-adrenoceptor induced hypertrophy in neonatal rat cardiomyocytes. J. Mol. Cell. Cardiol. 2012.
115. Zhong W., Mao S., Tobis S., Angelis E., Jordan M.C., Roos K.P., Fishbein M.C., de Alboran I.M., MacLellan W.R. Hypertrophic growth in cardiac myocytes is mediated by Myc through a Cyclin D2-dependent pathway. EMBO J. 2006, 25:3869-3879.
116. Xiao G., Mao S., Baumgarten G., Serrano J., Jordan M.C., Roos K.P., Fishbein M.C., MacLellan W.R. Inducible activation of c-Myc in adult myocardium in vivo provokes cardiac myocyte hypertrophy and reactivation of DNA synthesis. Circ. Res. 2001, 89:1122-1129.
117. Hershey J.C., Hautmann M., Thompson M.M., Rothblum L.I., Haystead T.A., Owens G.K. Angiotensin II-induced hypertrophy of rat vascular smooth muscle is associated with increased 18 S rRNA synthesis and phosphorylation of the rRNA transcription factor, upstream binding factor. J. Biol. Chem. 1995, 270:25096-25101.
118. Goodfellow S.J., Innes F., Derblay L.E., MacLellan W.R., Scott P.H., White R.J. Regulation of RNA polymerase III transcription during hypertrophic growth. EMBO J. 2006, 25:1522-1533.
119. Vallon V., Thomson S.C. Renal function in diabetic disease models: the tubular system in the pathophysiology of the diabetic kidney. Annu. Rev. Physiol. 2012, 74:351-375.
120. Mariappan M.M., D'Silva K., Lee M.J., Sataranatarajan K., Barnes J.L., Choudhury G.G., Kasinath B.S. Ribosomal biogenesis induction by high glucose requires activation of upstream binding factor in kidney glomerular epithelial cells. Am. J. Physiol. Renal Physiol. 2011, 300:F219-F230.
121. Melvin W.T., Kumar A., Malt R.A. Conservation of ribosomal RNA during compensatory renal hypertrophy. A major mechanism in RNA accretion. J. Cell Biol. 1976, 69:548-556.
122. Melvin W.T., Kumar A., Malt R.A. Synthesis and conservation of ribosomal proteins during compensatory renal hypertrophy. Biochem. J. 1980, 188:229-235.
123. Fanzani A., Conraads V.M., Penna F., Martinet W. Molecular and cellular mechanisms of skeletal muscle atrophy: an update. J. Cachexia Sarcopenia Muscle 2012, 3(3):163-179.
124. Powers S.K., Smuder A.J., Judge A.R. Oxidative stress and disuse muscle atrophy: cause or consequence?. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15:240-245.
125. Machida M., Takeda K., Yokono H., Ikemune S., Taniguchi Y., Kiyosawa H., Takemasa T. Reduction of ribosome biogenesis with activation of the mTOR pathway in denervated atrophic muscle. J. Cell. Physiol. 2012, 227:1569-1576.
126. von Walden F., Casagrande V., Ostlund Farrants A.K., Nader G.A. Mechanical loading induces the expression of a Pol I regulon at the onset of skeletal muscle hypertrophy. Am. J. Physiol. Cell Physiol. 2012, 302:C1523-C1530.
127. Poortinga G., Wall M., Sanij E., Siwicki K., Ellul J., Brown D., Holloway T.P., Hannan R.D., McArthur G.A. c-MYC coordinately regulates ribosomal gene chromatin remodeling and Pol I availability during granulocyte differentiation. Nucleic Acids Res. 2011, 39:3267-3281.
128. Shiue C.N., Arabi A., Wright A.P. Nucleolar organization, growth control and cancer. Epigenetics 2010, 5.
129. Williamson D., Lu Y.J., Fang C., Pritchard-Jones K., Shipley J. Nascent pre-rRNA overexpression correlates with an adverse prognosis in alveolar rhabdomyosarcoma. Genes Chromosomes Cancer 2006, 45:839-845.
130. Uemura M., Zheng Q., Koh C.M., Nelson W.G., Yegnasubramanian S., De Marzo A.M. Overexpression of ribosomal RNA in prostate cancer is common but not linked to rDNA promoter hypomethylation. Oncogene 2012, 31:1254-1263.
131. Cavanaugh A.H., Hempel W.M., Taylor L.J., Rogalsky V., Todorov G., Rothblum L.I. Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 1995, 374:177-180.
132. Hannan K.M., Sanij E., Hein N., Hannan R.D., Pearson R.B. Signaling to the ribosome in cancer-it is more than just mTORC1. IUBMB Life 2011, 63:79-85.
133. van Riggelen J., Yetil A., Felsher D.W. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat. Rev. Cancer 2010, 10:301-309.
134. Dang C.V. MYC on the path to cancer. Cell 2012, 149:22-35.
135. Gomez-Roman N., Felton-Edkins Z.A., Kenneth N.S., Goodfellow S.J., Athineos D., Zhang J., Ramsbottom B.A., Innes F., Kantidakis T., Kerr E.R., Brodie J., Grandori C., White R.J. Activation by c-Myc of transcription by RNA polymerases I, II and III. Biochem. Soc. Symp. 2006, 141-154.
136. Eilers M., Eisenman R.N. Myc's broad reach. Genes Dev. 2008, 22:2755-2766.
137. Soucek L., Evan G.I. The ups and downs of Myc biology. Curr. Opin. Genet. Dev. 2010, 20:91-95.
138. Varlakhanova N.V., Knoepfler P.S. Acting locally and globally: Myc's ever-expanding roles on chromatin. Cancer Res. 2009, 69:7487-7490.
139. Patel J.H., Loboda A.P., Showe M.K., Showe L.C., McMahon S.B. Analysis of genomic targets reveals complex functions of MYC. Nat. Rev. Cancer 2004, 4:562-568.
140. Poortinga G., Hannan K.M., Snelling H., Walkley C.R., Jenkins A., Sharkey K., Wall M., Brandenburger Y., Palatsides M., Pearson R.B., McArthur G.A., Hannan R.D. MAD1 and c-MYC regulate UBF and rDNA transcription during granulocyte differentiation. EMBO J. 2004, 23:3325-3335.
141. Sanij E., Poortinga G., Sharkey K., Hung S., Holloway T.P., Quin J., Robb E., Wong L.H., Thomas W.G., Stefanovsky V., Moss T., Rothblum L., Hannan K.M., McArthur G.A., Pearson R.B., Hannan R.D. UBF levels determine the number of active ribosomal RNA genes in mammals. J. Cell Biol. 2008, 183:1259-1274.
142. Sanij E., Hannan R.D. The role of UBF in regulating the structure and dynamics of transcriptionally active rDNA chromatin. Epigenetics 2009, 4:374-382.
143. Huang R., Wu T., Xu L., Liu A., Ji Y., Hu G. Upstream binding factor up-regulated in hepatocellular carcinoma is related to the survival and cisplatin-sensitivity of cancer cells. FASEB J. 2002, 16:293-301.
144. Arabi A., Wu S., Ridderstrale K., Bierhoff H., Shiue C., Fatyol K., Fahlen S., Hydbring P., Soderberg O., Grummt I., Larsson L.G., Wright A.P. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat. Cell Biol. 2005, 7:303-310.
145. Grandori C., Gomez-Roman N., Felton-Edkins Z.A., Ngouenet C., Galloway D.A., Eisenman R.N., White R.J. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 2005, 7:311-318.
146. Shiue C.N., Berkson R.G., Wright A.P. c-Myc induces changes in higher order rDNA structure on stimulation of quiescent cells. Oncogene 2009, 28:1833-1842.
147. Kenneth N.S., Ramsbottom B.A., Gomez-Roman N., Marshall L., Cole P.A., White R.J. TRRAP and GCN5 are used by c-Myc to activate RNA polymerase III transcription. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14917-14922.
148. Reikvam H., Hatfield K.J., Kittang A.O., Hovland R., Bruserud O. Acute myeloid leukemia with the t(8;21) translocation: clinical consequences and biological implications. J. Biomed. Biotechnol. 2011, 2011:104631.
149. Bakshi R., Zaidi S.K., Pande S., Hassan M.Q., Young D.W., Montecino M., Lian J.B., van Wijnen A.J., Stein J.L., Stein G.S. The leukemogenic t(8;21) fusion protein AML1-ETO controls rRNA genes and associates with nucleolar-organizing regions at mitotic chromosomes. J. Cell Sci. 2008, 121:3981-3990.
150. Li Z., Hann S.R. Nucleophosmin is essential for c-Myc nucleolar localization and c-Myc-mediated rDNA transcription. Oncogene 2012, 10.1038/onc.2012.227.
151. Colombo E., Alcalay M., Pelicci P.G. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene 2011, 30:2595-2609.
152. Meani N., Alcalay M. Role of nucleophosmin in acute myeloid leukemia. Expert. Rev. Anticancer. Ther. 2009, 9:1283-1294.
153. Rau R., Brown P. Nucleophosmin (NPM1) mutations in adult and childhood acute myeloid leukaemia: towards definition of a new leukaemia entity. Hematol. Oncol. 2009, 27:171-181.
154. Ramos-Echazabal G., Chinea G., Garcia-Fernandez R., Pons T. In silico studies of potential phosphoresidues in the human nucleophosmin/B23: its kinases and related biological processes. J. Cell. Biochem. 2012, 113:2364-2374.
155. Bergstralh D.T., Conti B.J., Moore C.B., Brickey W.J., Taxman D.J., Ting J.P. Global functional analysis of nucleophosmin in Taxol response, cancer, chromatin regulation, and ribosomal DNA transcription. Exp. Cell Res. 2007, 313:65-76.
156. Li Z., Hann S.R. The Myc-nucleophosmin-ARF network: a complex web unveiled. Cell Cycle 2009, 8:2703-2707.
157. Bertwistle D., Sugimoto M., Sherr C.J. Physical and functional interactions of the Arf tumor suppressor protein with nucleophosmin/B23. Mol. Cell. Biol. 2004, 24:985-996.
158. Kurki S., Peltonen K., Latonen L., Kiviharju T.M., Ojala P.M., Meek D., Laiho M. Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation. Cancer Cell 2004, 5:465-475.
159. Korgaonkar C., Hagen J., Tompkins V., Frazier A.A., Allamargot C., Quelle F.W., Quelle D.E. Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function. Mol. Cell. Biol. 2005, 25:1258-1271.
160. Blyth K., Vaillant F., Jenkins A., McDonald L., Pringle M.A., Huser C., Stein T., Neil J., Cameron E.R. Runx2 in normal tissues and cancer cells: a developing story. Blood Cells Mol. Dis. 2010, 45:117-123.
161. Young D.W., Hassan M.Q., Pratap J., Galindo M., Zaidi S.K., Lee S.H., Yang X., Xie R., Javed A., Underwood J.M., Furcinitti P., Imbalzano A.N., Penman S., Nickerson J.A., Montecino M.A., Lian J.B., Stein J.L., van Wijnen A.J., Stein G.S. Mitotic occupancy and lineage-specific transcriptional control of rRNA genes by Runx2. Nature 2007, 445:442-446.
162. Ali S.A., Dobson J.R., Lian J.B., Stein J.L., van Wijnen A.J., Zaidi S.K., Stein G.S. A RUNX2-HDAC1 co-repressor complex regulates rRNA gene expression by modulating UBF acetylation. J. Cell Sci. 2012, 125:2732-2739.
163. Chinnam M., Goodrich D.W. RB1, development, and cancer. Curr. Top. Dev. Biol. 2011, 94:129-169.
164. Manning A.L., Dyson N.J. pRB, a tumor suppressor with a stabilizing presence. Trends Cell Biol. 2011, 21:433-441.
165. Sun A., Bagella L., Tutton S., Romano G., Giordano A. From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J. Cell. Biochem. 2007, 102:1400-1404.
166. Polager S., Ginsberg D. E2F - at the crossroads of life and death. Trends Cell Biol. 2008, 18:528-535.
167. Chen H.Z., Tsai S.Y., Leone G. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat. Rev. Cancer 2009, 9:785-797.
168. Henley S.A., Dick F.A. The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle. Cell Div. 2012, 7:10.
169. Hannan K.M., Hannan R.D., Smith S.D., Jefferson L.S., Lun M., Rothblum L.I. Rb and p130 regulate RNA polymerase I transcription: Rb disrupts the interaction between UBF and SL-1. Oncogene 2000, 19:4988-4999.
170. Voit R., Schafer K., Grummt I. Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Mol. Cell. Biol. 1997, 17:4230-4237.
171. Hannan K.M., Kennedy B.K., Cavanaugh A.H., Hannan R.D., Hirschler-Laszkiewicz I., Jefferson L.S., Rothblum L.I. RNA polymerase I transcription in confluent cells: Rb downregulates rDNA transcription during confluence-induced cell cycle arrest. Oncogene 2000, 19:3487-3497.
172. White R.J., Trouche D., Martin K., Jackson S.P., Kouzarides T. Repression of RNA polymerase III transcription by the retinoblastoma protein. Nature 1996, 382:88-90.
173. Chu W.M., Wang Z., Roeder R.G., Schmid C.W. RNA polymerase III transcription repressed by Rb through its interactions with TFIIIB and TFIIIC2. J. Biol. Chem. 1997, 272:14755-14761.
174. Larminie C.G., Cairns C.A., Mital R., Martin K., Kouzarides T., Jackson S.P., White R.J. Mechanistic analysis of RNA polymerase III regulation by the retinoblastoma protein. EMBO J. 1997, 16:2061-2071.
175. Efeyan A., Serrano M. p53: guardian of the genome and policeman of the oncogenes. Cell Cycle 2007, 6:1006-1010.
176. Freed-Pastor W.A., Prives C. Mutant p53: one name, many proteins. Genes Dev. 2012, 26:1268-1286.
177. Zhang Y., Xiong Y., Yarbrough W.G. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 1998, 92:725-734.
178. Zhai W., Comai L. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol. Cell. Biol. 2000, 20:5930-5938.
179. Popov N., Gil J. Epigenetic regulation of the INK4b-ARF-INK4a locus: in sickness and in health. Epigenetics 2010, 5:685-690.
180. Dominguez-Brauer C., Brauer P.M., Chen Y.J., Pimkina J., Raychaudhuri P. Tumor suppression by ARF: gatekeeper and caretaker. Cell Cycle 2010, 9:86-89.
181. Matheu A., Maraver A., Serrano M. The Arf/p53 pathway in cancer and aging. Cancer Res. 2008, 68:6031-6034.
182. Sherr C.J. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 2006, 6:663-673.
183. Brady S.N., Yu Y., Maggi L.B., Weber J.D. ARF impedes NPM/B23 shuttling in an Mdm2-sensitive tumor suppressor pathway. Mol. Cell. Biol. 2004, 24:9327-9338.
184. Ayrault O., Andrique L., Fauvin D., Eymin B., Gazzeri S., Seite P. Human tumor suppressor p14ARF negatively regulates rRNA transcription and inhibits UBF1 transcription factor phosphorylation. Oncogene 2006, 25:7577-7586.
185. Lessard F., Morin F., Ivanchuk S., Langlois F., Stefanovsky V., Rutka J., Moss T. The ARF tumor suppressor controls ribosome biogenesis by regulating the RNA polymerase I transcription factor TTF-I. Mol. Cell 2010, 38:539-550.
186. Lessard F., Stefanovsky V., Tremblay M.G., Moss T. The cellular abundance of the essential transcription termination factor TTF-I regulates ribosome biogenesis and is determined by MDM2 ubiquitinylation. Nucleic Acids Res. 2012, 40:5357-5367.
187. Cheng Y., Liang P., Geng H., Wang Z., Li L., Cheng S.H., Ying J., Su X., Ng K.M., Ng M.H., Mok T.S., Chan A.T., Tao Q. A novel 19q13 nucleolar zinc finger protein suppresses tumor cell growth through inhibiting ribosome biogenesis and inducing apoptosis but is frequently silenced in multiple carcinomas. Mol. Cancer Res. 2012, 10(7):925-936.
188. Wang S., Cheng Y., Du W., Lu L., Zhou L., Wang H., Kang W., Li X., Tao Q., Sung J.J., Yu J. Zinc-finger protein 545 is a novel tumour suppressor that acts by inhibiting ribosomal RNA transcription in gastric cancer. Gut 2012, 10.1136/gutjnl-2011-301776.
189. Frescas D., Guardavaccaro D., Bassermann F., Koyama-Nasu R., Pagano M. JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes. Nature 2007, 450:309-313.
190. Pratilas C.A., Taylor B.S., Ye Q., Viale A., Sander C., Solit D.B., Rosen N. (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4519-4524.
191. Stefanovsky V.Y., Moss T. The splice variants of UBF differentially regulate RNA polymerase I transcription elongation in response to ERK phosphorylation. Nucleic Acids Res. 2008, 36:5093-5101.
192. Zhao J., Yuan X., Frodin M., Grummt I. ERK-dependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymerase I transcription and cell growth. Mol. Cell 2003, 11:405-413.
193. Sears R., Leone G., DeGregori J., Nevins J.R. Ras enhances Myc protein stability. Mol. Cell 1999, 3:169-179.
194. Johnson S.A., Dubeau L., Kawalek M., Dervan A., Schonthal A.H., Dang C.V., Johnson D.L. Increased expression of TATA-binding protein, the central transcription factor, can contribute to oncogenesis. Mol. Cell. Biol. 2003, 23:3043-3051.
195. Populo H., Lopes J.M., Soares P. The mTOR signalling pathway in human cancer. Int. J. Mol. Sci. 2012, 13:1886-1918.
196. Sheppard K., Kinross K.M., Solomon B., Pearson R.B., Phillips W.A. Targeting PI3 kinase/AKT/mTOR signaling in cancer. Crit. Rev. Oncog. 2012, 17:69-95.
197. Solomon B., Pearson R.B. Class IA phosphatidylinositol 3-kinase signaling in non-small cell lung cancer. J. Thorac. Oncol. 2009, 4:787-791.
198. Yuan T.L., Cantley L.C. PI3K pathway alterations in cancer: variations on a theme. Oncogene 2008, 27:5497-5510.
199. Hannan K.M., Brandenburger Y., Jenkins A., Sharkey K., Cavanaugh A., Rothblum L., Moss T., Poortinga G., McArthur G.A., Pearson R.B., Hannan R.D. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol. Cell. Biol. 2003, 23:8862-8877.
200. Mayer C., Zhao J., Yuan X., Grummt I. mTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev. 2004, 18:423-434.
201. Zhang C., Comai L., Johnson D.L. PTEN represses RNA Polymerase I transcription by disrupting the SL1 complex. Mol. Cell. Biol. 2005, 25:6899-6911.
202. Chan J.C., Hannan K.M., Riddell K., Ng P.Y., Peck A., Lee R.S., Hung S., Astle M.V., Bywater M., Wall M., Poortinga G., Jastrzebski K., Sheppard K.E., Hemmings B.A., Hall M.N., Johnstone R.W., McArthur G.A., Hannan R.D., Pearson R.B. AKT promotes rRNA synthesis and cooperates with c-MYC to stimulate ribosome biogenesis in cancer. Sci. Signal. 2011, 4:ra56.
203. McArthur G.A. The coming of age of MEK. Lancet Oncol. 2012, 13:744-745.
204. Cho Y.Y., Yao K., Kim H.G., Kang B.S., Zheng D., Bode A.M., Dong Z. Ribosomal S6 kinase 2 is a key regulator in tumor promoter induced cell transformation. Cancer Res. 2007, 67:8104-8112.
205. Kang S., Dong S., Gu T.L., Guo A., Cohen M.S., Lonial S., Khoury H.J., Fabbro D., Gilliland D.G., Bergsagel P.L., Taunton J., Polakiewicz R.D., Chen J. FGFR3 activates RSK2 to mediate hematopoietic transformation through tyrosine phosphorylation of RSK2 and activation of the MEK/ERK pathway. Cancer Cell 2007, 12:201-214.
206. Romeo Y., Zhang X., Roux P.P. Regulation and function of the RSK family of protein kinases. Biochem. J. 2012, 441:553-569.
207. Sabapathy K. Role of the JNK pathway in human diseases. Prog. Mol. Biol. Transl. Sci. 2012, 106:145-169.
208. Piazza F., Manni S., Ruzzene M., Pinna L.A., Gurrieri C., Semenzato G. Protein kinase CK2 in hematologic malignancies: reliance on a pivotal cell survival regulator by oncogenic signaling pathways. Leukemia 2012, 26:1174-1179.
209. Silva A., Jotta P.Y., Silveira A.B., Ribeiro D., Brandalise S.R., Yunes J.A., Barata J.T. Regulation of PTEN by CK2 and Notch1 in primary T-cell acute lymphoblastic leukemia: rationale for combined use of CK2- and gamma-secretase inhibitors. Haematologica 2010, 95:674-678.
210. Zhang S., Wang Y., Mao J.H., Hsieh D., Kim I.J., Hu L.M., Xu Z., Long H., Jablons D.M., You L. Inhibition of CK2alpha down-regulates Hedgehog/Gli signaling leading to a reduction of a stem-like side population in human lung cancer cells. PLoS One 2012, 7:e38996.
211. Ruzzene M., Pinna L.A. Addiction to protein kinase CK2: a common denominator of diverse cancer cells?. Biochim. Biophys. Acta 2010, 1804:499-504.
212. Tawfic S., Yu S., Wang H., Faust R., Davis A., Ahmed K. Protein kinase CK2 signal in neoplasia. Histol. Histopathol. 2001, 16:573-582.
213. Hundsdorfer C., Hemmerling H.J., Hamberger J., Le Borgne M., Bednarski P., Gotz C., Totzke F., Jose J. Novel indeno[1,2-b]indoloquinones as inhibitors of the human protein kinase CK2 with antiproliferative activity towards a broad panel of cancer cell lines. Biochem. Biophys. Res. Commun. 2012, 424:71-75.
214. Pierre F., Chua P.C., O'Brien S.E., Siddiqui-Jain A., Bourbon P., Haddach M., Michaux J., Nagasawa J., Schwaebe M.K., Stefan E., Vialettes A., Whitten J.P., Chen T.K., Darjania L., Stansfield R., Anderes K., Bliesath J., Drygin D., Ho C., Omori M., Proffitt C., Streiner N., Trent K., Rice W.G., Ryckman D.M. Discovery and SAR of 5-(3-chlorophenylamino)benzo[c][2,6]naphthyridine-8-carboxylic acid (CX-4945), the first clinical stage inhibitor of protein kinase CK2 for the treatment of cancer. J. Med. Chem. 2011, 54:635-654.
215. Pierre F., Chua P.C., O'Brien S.E., Siddiqui-Jain A., Bourbon P., Haddach M., Michaux J., Nagasawa J., Schwaebe M.K., Stefan E., Vialettes A., Whitten J.P., Chen T.K., Darjania L., Stansfield R., Bliesath J., Drygin D., Ho C., Omori M., Proffitt C., Streiner N., Rice W.G., Ryckman D.M., Anderes K. Pre-clinical characterization of CX-4945, a potent and selective small molecule inhibitor of CK2 for the treatment of cancer. Mol. Cell. Biochem. 2011, 356:37-43.
216. Hannan R.D., Hempel W.M., Cavanaugh A., Arino T., Dimitrov S.I., Moss T., Rothblum L. Affinity purification of mammalian RNA polymerase I. Identification of an associated kinase. J. Biol. Chem. 1998, 273:1257-1267.
217. Hannan R.D., Cavanaugh A., Hempel W.M., Moss T., Rothblum L. Identification of a mammalian RNA polymerase I holoenzyme containing components of the DNA repair/replication system. Nucleic Acids Res. 1999, 27:3720-3727.
218. Bierhoff H., Dundr M., Michels A.A., Grummt I. Phosphorylation by casein kinase 2 facilitates rRNA gene transcription by promoting dissociation of TIF-IA from elongating RNA polymerase I. Mol. Cell. Biol. 2008, 28:4988-4998.
219. Laferte A., Favry E., Sentenac A., Riva M., Carles C., Chedin S. The transcriptional activity of RNA polymerase I is a key determinant for the level of all ribosome components. Genes Dev. 2006, 20:2030-2040.
220. Stone A., Sutherland R.L., Musgrove E.A. Inhibitors of cell cycle kinases: recent advances and future prospects as cancer therapeutics. Crit. Rev. Oncog. 2012, 17:175-198.
221. Thway K., Flora R., Shah C., Olmos D., Fisher C. Diagnostic utility of p16, CDK4, and MDM2 as an immunohistochemical panel in distinguishing well-differentiated and dedifferentiated liposarcomas from other adipocytic tumors. Am. J. Surg. Pathol. 2012, 36:462-469.
222. Poomsawat S., Buajeeb W., Khovidhunkit S.O., Punyasingh J. Alteration in the expression of cdk4 and cdk6 proteins in oral cancer and premalignant lesions. J. Oral Pathol. Med. 2010, 39:793-799.
223. Wu A., Wu B., Guo J., Luo W., Wu D., Yang H., Zhen Y., Yu X., Wang H., Zhou Y., Liu Z., Fang W., Yang Z. Elevated expression of CDK4 in lung cancer. J. Transl. Med. 2011, 9:38.
224. Tang L.H., Contractor T., Clausen R., Klimstra D.S., Du Y.C., Allen P.J., Brennan M.F., Levine A.J., Harris C.R. Attenuation of the retinoblastoma pathway in pancreatic neuroendocrine tumors due to increased Cdk4/Cdk6. Clin. Cancer Res. 2012, 18(17):4612-4620.
225. Voit R., Hoffmann M., Grummt I. Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J. 1999, 18:1891-1899.
226. Voit R., Grummt I. Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:13631-13636.
227. Horiuchi D., Huskey N.E., Kusdra L., Wohlbold L., Merrick K.A., Zhang C., Creasman K.J., Shokat K.M., Fisher R.P., Goga A. Chemical-genetic analysis of cyclin dependent kinase 2 function reveals an important role in cellular transformation by multiple oncogenic pathways. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E1019-E1027.
228. Brown K.A., Samarajeewa N.U., Simpson E.R. Endocrine-related cancers and the role of AMPK. Mol. Cell. Endocrinol. 2012.
229. Carling D., Thornton C., Woods A., Sanders M.J. AMP-activated protein kinase: new regulation, new roles?. Biochem. J. 2012, 445:11-27.
230. Hardie D.G. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev. 2011, 25:1895-1908.
231. Li C., Liu V.W., Chiu P.M., Chan D.W., Ngan H.Y. Over-expressions of AMPK subunits in ovarian carcinomas with significant clinical implications. BMC Cancer 2012, 12:357.
232. Hardie D.G. AMP-activated protein kinase: a cellular energy sensor with a key role in metabolic disorders and in cancer. Biochem. Soc. Trans. 2011, 39:1-13.
233. Wu C.L., Qiang L., Han W., Ming M., Viollet B., He Y.Y. Role of AMPK in UVB-induced DNA damage repair and growth control. Oncogene 2012, 10.1038/onc.2012.279.
234. Hoppe S., Bierhoff H., Cado I., Weber A., Tiebe M., Grummt I., Voit R. AMP-activated protein kinase adapts rRNA synthesis to cellular energy supply. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17781-17786.
235. Kruhlak M., Crouch E.E., Orlov M., Montano C., Gorski S.A., Nussenzweig A., Misteli T., Phair R.D., Casellas R. The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature 2007, 447:730-734.
236. Negrini S., Gorgoulis V.G., Halazonetis T.D. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 2010, 11:220-228.
237. Thompson L.H. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutat. Res. 2012.
238. Greenman C., Stephens P., Smith R., Dalgliesh G.L., Hunter C., Bignell G., Davies H., Teague J., Butler A., Stevens C., Edkins S., O'Meara S., Vastrik I., Schmidt E.E., Avis T., Barthorpe S., Bhamra G., Buck G., Choudhury B., Clements J., Cole J., Dicks E., Forbes S., Gray K., Halliday K., Harrison R., Hills K., Hinton J., Jenkinson A., Jones D., Menzies A., Mironenko T., Perry J., Raine K., Richardson D., Shepherd R., Small A., Tofts C., Varian J., Webb T., West S., Widaa S., Yates A., Cahill D.P., Louis D.N., Goldstraw P., Nicholson A.G., Brasseur F., Looijenga L., Weber B.L., Chiew Y.E., DeFazio A., Greaves M.F., Green A.R., Campbell P., Birney E., Easton D.F., Chenevix-Trench G., Tan M.H., Khoo S.K., Teh B.T., Yuen S.T., Leung S.Y., Wooster R., Futreal P.A., Stratton M.R. Patterns of somatic mutation in human cancer genomes. Nature 2007, 446:153-158.
239. Ding L., Getz G., Wheeler D.A., Mardis E.R., McLellan M.D., Cibulskis K., Sougnez C., Greulich H., Muzny D.M., Morgan M.B., Fulton L., Fulton R.S., Zhang Q., Wendl M.C., Lawrence M.S., Larson D.E., Chen K., Dooling D.J., Sabo A., Hawes A.C., Shen H., Jhangiani S.N., Lewis L.R., Hall O., Zhu Y., Mathew T., Ren Y., Yao J., Scherer S.E., Clerc K., Metcalf G.A., Ng B., Milosavljevic A., Gonzalez-Garay M.L., Osborne J.R., Meyer R., Shi X., Tang Y., Koboldt D.C., Lin L., Abbott R., Miner T.L., Pohl C., Fewell G., Haipek C., Schmidt H., Dunford-Shore B.H., Kraja A., Crosby S.D., Sawyer C.S., Vickery T., Sander S., Robinson J., Winckler W., Baldwin J., Chirieac L.R., Dutt A., Fennell T., Hanna M., Johnson B.E., Onofrio R.C., Thomas R.K., Tonon G., Weir B.A., Zhao X., Ziaugra L., Zody M.C., Giordano T., Orringer M.B., Roth J.A., Spitz M.R., Wistuba B., Ozenberger P.J.Good, Chang A.C., Beer D.G., Watson M.A., Ladanyi M., Broderick S., Yoshizawa A., Travis W.D., Pao W., Province M.A., Weinstock G.M., Varmus H.E., Gabriel S.B., Lander E.S., Gibbs R.A., Meyerson M., Wilson R.K. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008, 455:1069-1075.
240. Mansouri L., Gunnarsson R., Sutton L.A., Ameur A., Hooper S.D., Mayrhofer M., Juliusson G., Isaksson A., Gyllensten U., Rosenquist R. Next generation RNA-sequencing in prognostic subsets of chronic lymphocytic leukemia. Am. J. Hematol. 2012, 87:737-740.
241. Roberts N.J., Jiao Y., Yu J., Kopelovich L., Petersen G.M., Bondy M.L., Gallinger S., Schwartz A.G., Syngal S., Cote M.L., Axilbund J., Schulick R., Ali S.Z., Eshleman J.R., Velculescu V.E., Goggins M., Vogelstein B., Papadopoulos N., Hruban R.H., Kinzler K.W., Klein A.P. ATM mutations in patients with hereditary pancreatic cancer. Cancer Discov. 2012, 2:41-46.
242. Gorski J.J., Pathak S., Panov K., Kasciukovic T., Panova T., Russell J., Zomerdijk J.C. A novel TBP-associated factor of SL1 functions in RNA polymerase I transcription. EMBO J. 2007, 26:1560-1568.
243. Schmitz K.M., Schmitt N., Hoffmann-Rohrer U., Schafer A., Grummt I., Mayer C. TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol. Cell 2009, 33:344-353.
244. Miller G., Panov K.I., Friedrich J.K., Trinkle-Mulcahy L., Lamond A.I., Zomerdijk J.C. hRRN3 is essential in the SL1-mediated recruitment of RNA Polymerase I to rRNA gene promoters. EMBO J. 2001, 20:1373-1382.
245. Hirschler-Laszkiewicz I., Cavanaugh A., Hu Q., Catania J., Avantaggiati M.L., Rothblum L.I. The role of acetylation in rDNA transcription. Nucleic Acids Res. 2001, 29:4114-4124.
246. Pelletier G., Stefanovsky V.Y., Faubladier M., Hirschler-Laszkiewicz I., Savard J., Rothblum L.I., Cote J., Moss T. Competitive recruitment of CBP and Rb-HDAC regulates UBF acetylation and ribosomal transcription. Mol. Cell 2000, 6:1059-1066.
247. Meraner J., Lechner M., Loidl A., Goralik-Schramel M., Voit R., Grummt I., Loidl P. Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I. Nucleic Acids Res. 2006, 34:1798-1806.
248. Kong R., Zhang L., Hu L., Peng Q., Han W., Du X., Ke Y. hALP, a novel transcriptional U three protein (t-UTP), activates RNA polymerase I transcription by binding and acetylating the upstream binding factor (UBF). J. Biol. Chem. 2011, 286:7139-7148.
249. Chi Y.H., Haller K., Peloponese J.M., Jeang K.T. Histone acetyltransferase hALP and nuclear membrane protein hsSUN1 function in de-condensation of mitotic chromosomes. J. Biol. Chem. 2007, 282:27447-27458.
250. Muth V., Nadaud S., Grummt I., Voit R. Acetylation of TAF(I)68, a subunit of TIF-IB/SL1, activates RNA polymerase I transcription. EMBO J. 2001, 20:1353-1362.
251. Gonugunta V.K., Nair B.C., Rajhans R., Sareddy G.R., Nair S.S., Vadlamudi R.K. Regulation of rDNA transcription by proto-oncogene PELP1. PLoS One 2011, 6:e21095.
252. Zhang Y., Smith A.D.t., Renfrow M.B., Schneider D.A. The RNA polymerase-associated factor 1 complex (Paf1C) directly increases the elongation rate of RNA polymerase I and is required for efficient regulation of rRNA synthesis. J. Biol. Chem. 2010, 285:14152-14159.
253. Zhang Y., Sikes M.L., Beyer A.L., Schneider D.A. The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2153-2158.
254. Drygin D., Siddiqui-Jain A., O'Brien S., Schwaebe M., Lin A., Bliesath J., Ho C.B., Proffitt C., Trent K., Whitten J.P., Lim J.K., Von Hoff D., Anderes K., Rice W.G. Anticancer activity of CX-3543: a direct inhibitor of rRNA biogenesis. Cancer Res. 2009, 69:7653-7661.
255. Boisvert F.M., van Koningsbruggen S., Navascues J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8:574-585.
256. Boisvert F.M., Lam Y.W., Lamont D., Lamond A.I. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 2010, 9:457-470.
257. Boisvert F.M., Lamond A.I. p53-Dependent subcellular proteome localization following DNA damage. Proteomics 2010, 10:4087-4097.
258. Emmott E., Hiscox J.A. Nucleolar targeting: the hub of the matter. EMBO Rep. 2009, 10:231-238.
259. Hein N., Sanij E., Quin J., Hannan K.M., Ganley A., Hannan R.D. The nucleolus and ribosomal genes in aging and senescence 2012, Senescence, Senescence Intech Open access, (ISBN 978-953-308-28-6 2012 Feb). T. Nagata (Ed.).
260. Boulon S., Westman B.J., Hutten S., Boisvert F.M., Lamond A.I. The nucleolus under stress. Mol. Cell 2010, 40:216-227.
261. Chi P., Allis C.D., Wang G.G. Covalent histone modifications-miswritten, misinterpreted and mis-erased in human cancers. Nat. Rev. Cancer 2010, 10:457-469.
262. Birch J.L., Zomerdijk J.C. Structure and function of ribosomal RNA gene chromatin. Biochem. Soc. Trans. 2008, 36:619-624.
263. McStay B., Grummt I. The epigenetics of rRNA genes: from molecular to chromosome biology. Annu. Rev. Cell Dev. Biol. 2008, 24:131-157.
264. van Koningsbruggen S., Gierlinski M., Schofield P., Martin D., Barton G.J., Ariyurek Y., den Dunnen J.T., Lamond A.I. High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol. Biol. Cell 2010, 21:3735-3748.
265. Paredes S., Maggert K.A. Ribosomal DNA contributes to global chromatin regulation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17829-17834.