Quantitative nucleolar proteomics reveals nuclear re-organization during stress- induced senescence in mouse fibroblast

BMC Cell Biology

Volumn 12, Issue , 2011, Pages

  Kar, Bishnupriya ^a   Liu, Baohua ^b   Zhou, Zhongjun ^b   Lam, Yun W ^a  

^a CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BUTYRIC ACID; DNA HELICASE II; HELICASE; LAMIN A; MITOXANTRONE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR PROTEIN; NUCLEOLAR PROTEIN; NUCLEOPHOSMIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL AGING; CELL NUCLEUS; CELL STRAIN 3T3; CELL STRESS; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; ISOTOPE LABELING; KNOCKOUT MOUSE; MASS SPECTROMETRY; MICROSCOPY; MOUSE; NONHUMAN; NUCLEOLUS; PEPTIDE MAPPING; PROTEIN ANALYSIS; PROTEIN TRANSPORT; PROTEOMICS; QUANTITATIVE ANALYSIS; UPREGULATION; VALIDATION PROCESS; AGING; ANIMAL; METABOLISM; MOUSE MUTANT;

MAMMALIA;

AGING; ANIMALS; CELL NUCLEOLUS; CELL NUCLEUS; FIBROBLASTS; ISOTOPE LABELING; MICE; MICE, KNOCKOUT; NIH 3T3 CELLS; NUCLEAR PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; PROTEOMICS;

EID: 80051504639     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-12-33     Document Type: Article

References (57)

1. Adams PD. Healing and hurting: molecular mechanisms, functions, and pathologies of cellular senescence. Mol Cell 2009, 36(1):2-14. 10.1016/j.molcel.2009.09.021, 19818705.
2. Shore D. Cellular senescence: lessons from yeast for human aging?. Curr Biol 1998, 8(6):R192-5. 10.1016/S0960-9822(98)70122-8, 9512411.
3. Terao Y, et al. Sodium butyrate induces growth arrest and senescence-like phenotypes in gynecologic cancer cells. Int J Cancer 2001, 94(2):257-67. 10.1002/ijc.1448, 11668507.
4. Xiao H, et al. Sodium butyrate induces NIH3T3 cells to senescence-like state and enhances promoter activity of p21WAF/CIP1 in p53-independent manner. Biochem Biophys Res Commun 1997, 237(2):457-60. 10.1006/bbrc.1997.7158, 9268733.
5. Coppe JP, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008, 6(12):2853-68. 2592359, 19053174.
6. Meng A, et al. Ionizing radiation and busulfan induce premature senescence in murine bone marrow hematopoietic cells. Cancer Res 2003, 63(17):5414-9.
7. Hong EH, et al. Ionizing radiation induces cellular senescence of articular chondrocytes via negative regulation of SIRT1 by p38 kinase. J Biol Chem 2010, 285(2):1283-95. 10.1074/jbc.M109.058628, 2801256, 19887452.
8. Mason DX, Jackson TJ, Lin AW. Molecular signature of oncogenic ras-induced senescence. Oncogene 2004, 23(57):9238-46.
9. Puzianowska-Kuznicka M, Kuznicki J. Genetic alterations in accelerated ageing syndromes. Do they play a role in natural ageing?. Int J Biochem Cell Biol 2005, 37(5):947-60. 10.1016/j.biocel.2004.10.011, 15743670.
10. Mattout A, et al. Nuclear lamins, diseases and aging. Curr Opin Cell Biol 2006, 18(3):335-41. 10.1016/j.ceb.2006.03.007, 16632339.
11. Mounkes LC, et al. A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 2003, 423(6937):298-301. 10.1038/nature01631, 12748643.
12. Cadinanos J, et al. From immature lamin to premature aging: molecular pathways and therapeutic opportunities. Cell Cycle 2005, 4(12):1732-5. 10.4161/cc.4.12.2202, 16258283.
13. Denecke J, et al. A homozygous ZMPSTE24 null mutation in combination with a heterozygous mutation in the LMNA gene causes Hutchinson-Gilford progeria syndrome (HGPS): insights into the pathophysiology of HGPS. Hum Mutat 2006, 27(6):524-31. 10.1002/humu.20315, 16671095.
14. Wiesel N, et al. Laminopathic mutations interfere with the assembly, localization, and dynamics of nuclear lamins. Proc Natl Acad Sci USA 2008, 105(1):180-5. 10.1073/pnas.0708974105, 2224182, 18162544.
15. Serrano M, et al. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997, 88(5):593-602. 10.1016/S0092-8674(00)81902-9, 9054499.
16. Szekely AM, et al. Werner protein recruits DNA polymerase delta to the nucleolus. Proc Natl Acad Sci USA 2000, 97(21):11365-70. 17206, 11027336.
17. van den Boom V, et al. DNA damage stabilizes interaction of CSB with the transcription elongation machinery. J Cell Biol 2004, 166(1):27-36. 10.1083/jcb.200401056, 2172148, 15226310.
18. Yankiwski V, et al. Nuclear structure in normal and Bloom syndrome cells. Proc Natl Acad Sci USA 2000, 97(10):5214-9. 10.1073/pnas.090525897, 25808, 10779560.
19. Woo LL, et al. The Rothmund-Thomson gene product RECQL4 localizes to the nucleolus in response to oxidative stress. Exp Cell Res 2006, 312(17):3443-57. 10.1016/j.yexcr.2006.07.023, 16949575.
20. Mochizuki Y, et al. Mouse dyskerin mutations affect accumulation of telomerase RNA and small nucleolar RNA, telomerase activity, and ribosomal RNA processing. Proc Natl Acad Sci USA 2004, 101(29):10756-61. 10.1073/pnas.0402560101, 490007, 15240872.
21. Heiss NS, et al. Dyskerin localizes to the nucleolus and its mislocalization is unlikely to play a role in the pathogenesis of dyskeratosis congenita. Hum Mol Genet 1999, 8(13):2515-24. 10.1093/hmg/8.13.2515, 10556300.
22. Chopra VS, Mishra RK. To SIR with Polycomb: linking silencing mechanisms. Bioessays 2005, 27(2):119-21. 10.1002/bies.20191, 15666358.
23. Tomlinson RL, et al. Cell cycle-regulated trafficking of human telomerase to telomeres. Mol Biol Cell 2006, 17(2):955-65. 1356603, 16339074.
24. Khurts S, et al. Nucleolin interacts with telomerase. J Biol Chem 2004, 279(49):51508-15. 10.1074/jbc.M407643200, 15371412.
25. Artandi SE, Attardi LD. Pathways connecting telomeres and p53 in senescence, apoptosis, and cancer. Biochem Biophys Res Commun 2005, 331(3):881-90. 10.1016/j.bbrc.2005.03.211, 15865944.
26. Rubbi CP, Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 2003, 22(22):6068-77. 10.1093/emboj/cdg579, 275437, 14609953.
27. Zhu Q, Yasumoto H, Tsai RY. Nucleostemin delays cellular senescence and negatively regulates TRF1 protein stability. Mol Cell Biol 2006, 26(24):9279-90. 10.1128/MCB.00724-06, 1698521, 17000763.
28. Scott M, et al. UV induces nucleolar translocation of ING1 through two distinct nucleolar targeting sequences. Nucleic Acids Res 2001, 29(10):2052-8. 10.1093/nar/29.10.2052, 55466, 11353074.
29. Lam YW, Trinkle-Mulcahy L, Lamond AI. The nucleolus. J Cell Sci 2005, 118(Pt 7):1335-7.
30. Andersen JS, et al. Nucleolar proteome dynamics. Nature 2005, 433(7021):77-83. 10.1038/nature03207, 15635413.
31. Lam YW, et al. Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol Cell Proteomics 2010, 9(1):117-30. 10.1074/mcp.M900338-MCP200, 2808258, 19812395.
32. Casafont I, et al. Nuclear organization and dynamics of transcription sites in rat sensory ganglia neurons detected by incorporation of 5'-fluorouridine into nascent RNA. Neuroscience 2006, 140(2):453-62. 10.1016/j.neuroscience.2006.02.030, 16563640.
33. Olsen JV, et al. Parts per million mass accuracy on an orbitrap mass spectrometer via lock mass injection into a C-trap. Molecular & Cellular Proteomics 42010-2021 2005,
34. Mortensen P, et al. MSQuant, an open source platform for mass spectrometry-based quantitative proteomics. J Proteome Res 2010, 9(1):393-403. 10.1021/pr900721e, 19888749.
35. Dimri GP, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995, 92(20):9363-7. 10.1073/pnas.92.20.9363, 40985, 7568133.
36. Andersen JS, et al. Directed proteomic analysis of the human nucleolus. Curr Biol 2002, 12(1):1-11. 10.1016/S0960-9822(01)00650-9, 11790298.
37. Scherl A, et al. Functional proteomic analysis of human nucleolus. Mol Biol Cell 2002, 13(11):4100-9. 10.1091/mbc.E02-05-0271, 133617, 12429849.
38. Staub E, et al. Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire. Bioessays 2004, 26(5):567-81. 10.1002/bies.20032, 15112237.
39. Derenzini M, et al. Structural and functional organization of ribosomal genes within the mammalian cell nucleolus. J Histochem Cytochem 2006, 54(2):131-45. 10.1369/jhc.5R6780.2005, 16204224.
40. Hui L, et al. p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway. Nat Genet 2007, 39(6):741-9. 10.1038/ng2033, 17468757.
41. Yogev O, et al. DNA damage-dependent translocation of B23 and p19 ARF is regulated by the Jun N-terminal kinase pathway. Cancer Res 2008, 68(5):1398-406. 10.1158/0008-5472.CAN-07-2865, 18316603.
42. Coppe JP, et al. Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J Biol Chem 2006, 281(40):29568-74. 10.1074/jbc.M603307200, 16880208.
43. Augustin E, et al. Imidazoacridinones arrest cell-cycle progression in the G2 phase of L1210 cells. Cancer Chemother Pharmacol 1996, 38(1):39-44. 10.1007/s002800050445, 8603450.
44. Ostlund C, et al. Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J Cell Sci 2001, 114(Pt 24):4435-45.
45. Duque G, Rivas D. Age-related changes in lamin A/C expression in the osteoarticular system: laminopathies as a potential new aging mechanism. Mech Ageing Dev 2006, 127(4):378-83. 10.1016/j.mad.2005.12.007, 16445967.
46. Worman HJ, Bonne G. "Laminopathies": a wide spectrum of human diseases. Exp Cell Res 2007, 313(10):2121-33. 10.1016/j.yexcr.2007.03.028, 2964355, 17467691.
47. Worman HJ, Courvalin JC. How do mutations in lamins A and C cause disease?. J Clin Invest 2004, 113(3):349-51. 324546, 14755330.
48. Scaffidi P, Misteli T. Lamin A-dependent nuclear defects in human aging. Science 2006, 312(5776):1059-63. 10.1126/science.1127168, 1855250, 16645051.
49. Raska I, et al. Analysis of ring-shaped nucleoli in serially sectioned human lymphocytes. Cell Tissue Res 1983, 234(3):707-11. 10.1007/BF00218661, 6661758.
50. Zhang R, et al. Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev Cell 2005, 8(1):19-30. 10.1016/j.devcel.2004.10.019, 15621527.
51. Stoldt S, et al. G1 phase-dependent nucleolar accumulation of human histone H1x. Biol Cell 2007, 99(10):541-52. 10.1042/BC20060117, 17868027.
52. Okuwaki M. The structure and functions of NPM1/Nucleophsmin/B23, a multifunctional nucleolar acidic protein. J Biochem 2008, 143(4):441-8.
53. Itahana K, et al. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell 2003, 12(5):1151-64. 10.1016/S1097-2765(03)00431-3, 14636574.
54. Kondo T, et al. Identification and characterization of nucleophosmin/B23/numatrin which binds the anti-oncogenic transcription factor IRF-1 and manifests oncogenic activity. Oncogene 1997, 15(11):1275-81. 10.1038/sj.onc.1201286, 9315094.
55. Boisvert FM, et al. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol Cell Proteomics 2010, 9(3):457-470. 10.1074/mcp.M900429-MCP200, 2849709, 20026476.
56. Boisvert FM, Lamond AI. p53-Dependent subcellular proteome localization following DNA damage. Proteomics 2010, 10(22):4087-4097. 10.1002/pmic.201000213, 21080495.
57. Yao Z, et al. B23 acts as a nucleolar stress sensor and promotes cell survival through its dynamic interaction with hnRNPU and hnRNPA1. Oncogene 2010, 29:1821-1834. 10.1038/onc.2009.473, 20101230.