The nuclear lamina promotes telomere aggregation and centromere peripheral localization during senescence of human mesenchymal stem cells

Journal of Cell Science

Volumn 121, Issue 24, 2008, Pages 4018-4028

  Raz, Vered ^a   Vermolen, Bart J ^b,c   Garini, Yuval ^c,d   Onderwater, Jos J M ^a   Mommaas Kienhuis, Mieke A ^a   Koster, Abraham J ^a   Young, Ian T ^c   Tanke, Hans ^a   Dirks, Roeland W ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d BAR ILAN UNIVERSITY   (Israel)

Author keywords

Cell senescence; Nuclear lamina; Spatial organization; Telomere aggregates

Indexed keywords

HISTONE H2AX; TELOMERASE REVERSE TRANSCRIPTASE;

ADULT; AGED; ARTICLE; CELL AGING; CELL NUCLEUS; CELLULAR DISTRIBUTION; CENTROMERE; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMAGE PROCESSING; MESENCHYMAL STEM CELL; MOLECULAR IMAGING; MUTANT; NUCLEAR LAMINA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SENESCENCE; TELOMERE;

BETA-GALACTOSIDASE; CELL AGING; CELL NUCLEUS; CELLS, CULTURED; CENTROMERE; HISTONES; HUMANS; MESENCHYMAL STEM CELLS; MICROSCOPY, ELECTRON, TRANSMISSION; NUCLEAR LAMINA; TELOMERASE; TELOMERE;

EID: 59349105194     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.034876     Document Type: Article

References (55)

1. Amrichova, J., Lukasova, E., Kozubek, S. and Kozubek, M. (2003). Nuclear and territorial topography of chromosome telomeres in human lymphocytes. Exp. Cell Res. 289, 11-26.
2. Baxter, M. A., Wynn, R. F., Jowitt, S. N., Wraith, J. E., Fairbairn, L. J. and Bellantuono, I. (2004). Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22, 675-682.
3. Ben Porath, I. and Weinberg, R. A. (2005). The signals and pathways activating cellular senescence. Int. J. Biochem. Cell Biol. 37, 961-976.
4. Bonab, M., Alimoghaddam, K., Talebian, F., Ghaffari, S., Ghavamzadeh, A. and Nikbin, B. (2006). Aging of mesenchymal stem cell in vitro. BMC Cell Biol. 7, 14-21.
5. Broers, J. L., Ramaekers, F. C., Bonne, G., Yaou, R. B. and Hutchison, C. J. (2006). Nuclear lamins: laminopathies and their role in premature ageing. Physiol. Rev. 86, 967-1008.
6. Capell, B. C. and Collins, F. S. (2006). Human laminopathies: nuclei gone genetically awry. Nat. Rev. Genet. 7, 940-952.
7. Carlotti, F., Bazuine, M., Kekarainen, T., Seppen, J., Pognonec, P., Maassen, J. A. and Hoeben, R. C. (2004). Lentiviral vectors efficiently transduce quiescent mature 3T3-L1 adipocytes. Mol. Ther. 9, 209-217.
8. Carlotti, F., Zaldumbide, A., Martin, P., Boulukos, K. E., Hoeben, R. C. and Pognonec, P. (2005). Development of an inducible suicide gene system based on human caspase 8. Cancer Gene Ther. 12, 627-639.
9. Cawthon, R. M. (2002). Telomere measurement by quantitative PCR. Nucleic Acids Res. 30, e47.
10. Chuang, T. C, Moshir, S., Garini, Y., Chuang, A. Y., Young, I. T., Vermolen, B., van den Doel, R., Mougey, V., Perrin, M., Braun, M., Kerr, P. D., Fest, T., Boukamp, P. and Mai, S. (2004). The three-dimensional organization of telomeres in the nucleus of mammalian cells. BMC. Biol. 2, 12-21.
11. Collado, M., Blasco, M. A. and Serrano, M. (2007). Cellular senescence in cancer and aging. Cell 130, 223-233.
12. Cowell, I. G., Sunter, N. J., Singh, P. B., Austin, C. A., Durkacz, B. W. and Tilby, M. J. (2007). gammaH2AX Foci Form Preferentially in Euchromatin after Ionising-Radiation. PLoS ONE 2, e1057.
13. Cremer, T., Kupper, K., Dietzel, S. and Fakan, S. (2004). Higher order chromatin architecture in the cell nucleus: on the way from structure to function. Biol. Cell. 96, 555-567.
14. Dhe-Paganon, S., Werner, E. D., Chi, Y. I. and Shoelson, S. E. (2002). Structure of the globular tail of nuclear lamin. J. Biol. Chem. 277, 17381-17384.
15. Dimri, G. P., Lee, X. H., Basile, G., Acosta, M., Scott, C., Roskelley, C., Medrano, E. E., Linskens, M., Rubelj, I., Pereirasmith, O. et al. (1995). A biomarker that identifies senescent human-cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92, 9363-9367.
16. Gerson, S. L. (1999). Mesenchymal stem cells: no longer second class marrow citizens. Nat. Med. 5, 262-264.
17. Gilchrist, S., Gilbert, N., Perry, P. and Bickmore, W. A. (2004). Nuclear organization of centromeric domains is not perturbed by inhibition of histone deacetylases. Chromosome. Res. 12, 505-516.
18. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K. and Wilson, K. L. (2005). The nuclear lamina comes of age. Nat. Rev. Mol. Cell. Biol. 6, 21-31.
19. Huang, S., Risques, R. A., Martin, G. M., Rabinovitch, P. S. and Oshima, J. (2008). Accelerated telomere shortening and replicative senescence in human fibroblasts overexpressing mutant and wild-type lamin A. Exp. Cell Res. 314, 82-91.
20. Huang, X., Tanaka, T., Kurose, A., Traganos, F. and Darzynkiewicz, Z. (2006). Constitutive histone H2AX phosphorylation on Ser-139 in cells untreated by genotoxic agents is cell-cycle phase specific and attenuated by scavenging reactive oxygen species. Int. J. Oncol. 29, 495-502.
21. Jacob, K. N., Baptista, F., dos Santos, H. G., Oshima, J., Agarwal, K. and Garg, A. (2005). Phenotypic heterogeneity in body fat distribution in patients with atypical Werner's syndrome due to heterozygous Arg133Leu lamin A/C mutation. J. Clin. Endocrinol. Metab. 90, 6699-6706.
22. Knaan-Shanzer, S., van de Watering, M. J. M., van der Velde, I., Goncalves, M. A. F. V., Valerio, D. and de Vries, A. A. F. (2005). Endowing human adenovirus serotype 5 vectors with fiber domains of species B greatly enhances gene transfer into human mesenchymal stem cells. Stem Cells. 23, 1598-1607.
23. Le Blanc, K. and Pittenger, M. (2005). Mesenchymal stem cells: progress toward promise. Cytotherapy 7, 36-45.
24. Luderus, M. E., van Steensel, B., Chong, L., Sibon, O. C., Cremers, F. F. and de Lange, T. (1996). Structure, subnuclear distribution, and nuclear matrix association of the mammalian telomeric complex. J. Cell Biol. 135, 867-881.
25. McManus, K. J. and Hendzel, M. J. (2005). ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol. Biol. Cell 16, 5013-5025.
26. Molenaar, C., Wiesmeijer, K., Verwoerd, N. P., Khazen, S., Eils, R., Tanke, H. J. and Dirks, R. W. (2003). Visualizing telomere dynamics in living mammalian cells using PNA probes. EMBO J. 22, 6631-6641.
27. Narita, M., Nunez, S., Heard, E., Narita, M., Lin, A. W., Hearn, S. A., Spector, D. L., Hannon, G. J. and Lowe, S. W. (2003). Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 113, 703-716.
28. Nelson, J. D., Denisenko, O. and Bomsztyk, K. (2006). Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 1, 179-185.
29. Parsch, D., Fellenberg, J., Brummendorf, T. H., Eschlbeck, A. M. and Richter, W. (2004). Telomere length and telomerase activity during expansion and differentiation of human mesenchymal stem cells and chondrocytes. J. Mol. Med. 82, 49-55.
30. Pickersgill, H., Kalverda, B., de Wit, E., Talhout, W., Fornerod, M. and van Steensel, B. (2006). Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38, 1005-1014.
31. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S. and Marshak, D. R. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147.
32. Raz, V., Carlotti, F., Vermolen, B. J., van der Poel, E., Sloos, W. C. R., Knaan-Shanzer, S., de Vries, A. A. F., Hoeben, R. C., Young, I. T., Tanke, H. J. et al. (2006). Changes in lamina structure are followed by spatial reorganization of heterochromatic regions in caspase-8-activated human mesenchymal stem cells. J. Cell Sci. 119, 4247-4256.
33. Reddy, K. L., Zullo, J. M., Bertolino, E. and Singh, H. (2008). Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 45, 243-247.
34. Scaffidi, P. and Misteli, T. (2006). Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063.
35. Scaffidi, P. and Misteli, T. (2008). Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat. Cell Biol. 10, 452-459.
36. Sedelnikova, O. A., Horikawa, I., Zimonjic, D. B., Popescu, N. C., Bonner, W. M. and Barrett, J. C. (2004). Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol. 6, 168-170.
37. Sexton, T., Schober, H., Fraser, P. and Gasser, S. M. (2007). Gene regulation through nuclear organization. Nat. Struct. Mol. Biol. 14, 1049-1055.
38. Shay, J. W. and Wright, W. E. (2007). Hallmarks of telomeres in ageing research. J. Pathol. 211, 114-123.
39. Shibata, K. R., Aoyama, T., Shima, Y., Fukiage, K., Otsuka, S., Furu, M., Kohno, Y., Ito, K., Fujibayashi, S., Neo, M. et al. (2007). Expression of the p16INK4A gene is associated closely with senescence of human mesenchymal stem cells and is potentially silenced by DNA methylation during in vitro expansion. Stem Cells 25, 2371-2382.
40. Shoeman, R. L. and Traub, P. (1990). The in vitro DNA-binding properties of purified nuclear lamin proteins and vimentin. J. Biol. Chem. 265, 9055-9061.
41. Solovei, I., Schermelleh, L., During, K., Engelhardt, A., Stein, S., Cremer, C. and Cremer, T. (2004). Differences in centromere positioning of cycling and postmitotic human cell types. Chromosoma 112, 410-423.
42. Stenderup, K., Justesen, J., Clausen, C. and Kassem, M. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33, 919-926.
43. Strelkov, S. V., Herrmann, H. and Aebi, U. (2003). Molecular architecture of intermediate filaments. Bioessays 25, 243-251.
44. Stuurman, N., de Graaf, A., Floore, A., Josso, A., Humbel, B., de Jong, L. and van Driel, R. (1992). A monoclonal antibody recognizing nuclear matrix-associated nuclear bodies. J. Cell Sci. 101, 773-784.
45. Sugimoto, K., Fukuda, R. and Himeno, M. (2000). Centromere/ kinetochore localization of human centromere protein A (CENP-A) exogenously expressed as a fusion to green fluorescent protein. Cell Struct. Funct. 25, 253-261.
46. Taddei, A., Hediger, F., Neumann, F. R. and Gasser, S. M. (2004). The function of nuclear architecture: a genetic approach. Annu. Rev. Genet. 38, 305-345.
47. Takahashi, A. and Ohnishi, T. (2005). Does γH2AX foci formation depend on the presence of DNA double strand breaks? Cancer Lett. 229, 171-179.
48. Takai, H., Smogorzewska, A. and de Lange, T. (2003). DNA damage foci at dysfunctional telomeres. Curr. Biol. 13, 1549-1556.
49. van der Heijden, F., Duin, P. R. W., de Ridder, D. and Tax, D. M. J. (2004). Classification, Parameter Estimation and State Estimation: An Engineering Approach Using Matlab. Wiley.
50. Vermolen, B. J., Garini, Y., Mai, S., Mougey, V., Fest, T., Chuang, T. C., Chuang, A. Y., Wark, L. and Young, I. T. (2005). Characterizing the three-dimensional organization of telomeres. Cytometry A 67, 144-150.
51. Vermolen, B. J., Garini, Y., Young, I. T., Dirks, R. W. and Raz, V. (2008). Segmentation and analysis of the three-dimensional redistribution of nuclear components in human mesenchymal stem cells. Cytometry A 73, 816-824.
52. Weierich, C., Brero, A., Stein, S., von Hase, J., Cremer, C., Cremer, T. and Solovei, I. (2003). Three-dimensional arrangements of centromeres and telomeres in nuclei of human and murine lymphocytes. Chromosome. Res. 11, 485-502.
53. Wiblin, A. E., Cui, W., Clark, A. J. and Bickmore, W. A. (2005). Distinctive nuclear organisation of centromeres and regions involved in pluripotency in human embryonic stem cells. J. Cell Sci. 118, 3861-3868.
54. Yan, P. (2004). Immunohistochemical localization of hTERT protein in human tissues. Histochem. Cell Biol. 121, 391-397.
55. Zimmermann, S., Voss, M., Kaiser, S., Kapp, U., Waller, C. F. and Martens, U. M. (2003). Lack of telomerase activity in human mesenchymal stem cells. Leukemia 1, 1146-1149.