DNA Damage Follows Repair Factor Depletion and Portends Genome Variation in Cancer Cells after Pore Migration

Current Biology

Volumn 27, Issue 2, 2017, Pages 210-223

  Irianto, Jerome ^a   Xia, Yuntao ^a   Pfeifer, Charlotte R ^a   Athirasala, Avathamsa ^a   Ji, Jiazheng ^a   Alvey, Cory ^a   Tewari, Manu ^a   Bennett, Rachel R ^a   Harding, Shane M ^a,b   Liu, Andrea J ^a   Greenberg, Roger A ^a,b   Discher, Dennis E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

cancer; copy number variation; DNA damage; DNA repair; extracellular matrix; lamina; migration; motility; nuclear envelope; rupture

Indexed keywords

TRANSCRIPTION FACTOR;

BONE TUMOR; CELL MOTION; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; GENETIC VARIATION; GENETICS; GENOMIC INSTABILITY; HUMAN; HUMAN GENOME; METABOLISM; OSTEOSARCOMA; PATHOLOGY; TUMOR CELL CULTURE;

BONE NEOPLASMS; CELL MOVEMENT; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; GENETIC VARIATION; GENOME, HUMAN; GENOMIC INSTABILITY; HUMANS; OSTEOSARCOMA; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 85008391993     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.11.049     Document Type: Article

References (50)

1. 1 Chamberlain, J.K., Lichtman, M.A., Marrow cell egress: specificity of the site of penetration into the sinus. Blood 52 (1978), 959–968.
2. 2 Harada, T., Swift, J., Irianto, J., Shin, J.W., Spinler, K.R., Athirasala, A., Diegmiller, R., Dingal, P.C., Ivanovska, I.L., Discher, D.E., Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J. Cell Biol. 204 (2014), 669–682.
3. 3 Raab, M., Gentili, M., de Belly, H., Thiam, H.R., Vargas, P., Jimenez, A.J., Lautenschlaeger, F., Voituriez, R., Lennon-Duménil, A.M., Manel, N., Piel, M., ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352 (2016), 359–362.
4. 4 Irianto, J., Pfeifer, C.R., Xia, Y., Athirasala, A., Ivanovska, I.L., Greenberg, R.E., Discher, D.E., Constricted cell migration causes nuclear lamina damage, DNA breaks, and squeeze-out of repair factors. bioRxiv, 2015, 10.1101/035626.
5. 5 Ogawa, H., Inouye, S., Tsuji, F.I., Yasuda, K., Umesono, K., Localization, trafficking, and temperature-dependence of the Aequorea green fluorescent protein in cultured vertebrate cells. Proc. Natl. Acad. Sci. USA 92 (1995), 11899–11903.
6. 6 Gonzalo, S., DNA damage and lamins. Adv. Exp. Med. Biol. 773 (2014), 377–399.
7. 7 Denais, C.M., Gilbert, R.M., Isermann, P., McGregor, A.L., te Lindert, M., Weigelin, B., Davidson, P.M., Friedl, P., Wolf, K., Lammerding, J., Nuclear envelope rupture and repair during cancer cell migration. Science 352 (2016), 353–358.
8. 8 Macůrek, L., Lindqvist, A., Voets, O., Kool, J., Vos, H.R., Medema, R.H., Wip1 phosphatase is associated with chromatin and dephosphorylates gammaH2AX to promote checkpoint inhibition. Oncogene 29 (2010), 2281–2291.
9. 9 Harding, S.M., Bristow, R.G., Discordance between phosphorylation and recruitment of 53BP1 in response to DNA double-strand breaks. Cell Cycle 11 (2012), 1432–1444.
10. 10 Alagoz, M., Katsuki, Y., Ogiwara, H., Ogi, T., Shibata, A., Kakarougkas, A., Jeggo, P., SETDB1, HP1 and SUV39 promote repositioning of 53BP1 to extend resection during homologous recombination in G2 cells. Nucleic Acids Res. 43 (2015), 7931–7944.
11. 11 Guo, C., Nakazawa, Y., Woodbine, L., Björkman, A., Shimada, M., Fawcett, H., Jia, N., Ohyama, K., Li, T.S., Nagayama, Y., et al. XRCC4 deficiency in human subjects causes a marked neurological phenotype but no overt immunodeficiency. J. Allergy Clin. Immunol. 136 (2015), 1007–1017.
12. 12 Shanbhag, N.M., Rafalska-Metcalf, I.U., Balane-Bolivar, C., Janicki, S.M., Greenberg, R.A., ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141 (2010), 970–981.
13. 13 Chen, X., Bahrami, A., Pappo, A., Easton, J., Dalton, J., Hedlund, E., Ellison, D., Shurtleff, S., Wu, G., Wei, L., et al., St. Jude Children's Research Hospital–Washington University Pediatric Cancer Genome Project. Recurrent somatic structural variations contribute to tumorigenesis in pediatric osteosarcoma. Cell Rep. 7 (2014), 104–112.
14. 14 Irianto, J., Pfeifer, C.R., Xia, Y., Discher, D.E., SnapShot: mechanosensing matrix. Cell 165 (2016), 1820–1820.e1.
15. 15 Kovac, M., Blattmann, C., Ribi, S., Smida, J., Mueller, N.S., Engert, F., Castro-Giner, F., Weischenfeldt, J., Kovacova, M., Krieg, A., et al. Exome sequencing of osteosarcoma reveals mutation signatures reminiscent of BRCA deficiency. Nat. Commun., 6, 2015, 8940.
16. 16 Swift, J., Ivanovska, I.L., Buxboim, A., Harada, T., Dingal, P.C., Pinter, J., Pajerowski, J.D., Spinler, K.R., Shin, J.W., Tewari, M., et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science, 341, 2013, 1240104.
17. 17 Olive, P.L., Banáth, J.P., Durand, R.E., Detection of etoposide resistance by measuring DNA damage in individual Chinese hamster cells. J. Natl. Cancer Inst. 82 (1990), 779–783.
18. 18 Hatch, E.M., Fischer, A.H., Deerinck, T.J., Hetzer, M.W., Catastrophic nuclear envelope collapse in cancer cell micronuclei. Cell 154 (2013), 47–60.
19. 19 Wu, J., Lu, L.Y., Yu, X., The role of BRCA1 in DNA damage response. Protein Cell 1 (2010), 117–123.
20. 20 Nussenzweig, A., Sokol, K., Burgman, P., Li, L., Li, G.C., Hypersensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival, and development. Proc. Natl. Acad. Sci. USA 94 (1997), 13588–13593.
21. 21 Irianto, J., Pfeifer, C.R., Bennett, R.R., Xia, Y., Ivanovska, I.L., Liu, A.J., Greenberg, R.A., Discher, D.E., Nuclear constriction segregates mobile nuclear proteins away from chromatin. Mol. Biol. Cell, 2016, 10.1091/mbc.E16-06-0428 Published online October 26, 2016.
22. 22 Difilippantonio, M.J., Zhu, J., Chen, H.T., Meffre, E., Nussenzweig, M.C., Max, E.E., Ried, T., Nussenzweig, A., DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 404 (2000), 510–514.
23. 23 Holstege, H., van Beers, E., Velds, A., Liu, X., Joosse, S.A., Klarenbeek, S., Schut, E., Kerkhoven, R., Klijn, C.N., Wessels, L.F., et al. Cross-species comparison of aCGH data from mouse and human BRCA1- and BRCA2-mutated breast cancers. BMC Cancer, 10, 2010, 455.
24. 24 Wang, Y., Putnam, C.D., Kane, M.F., Zhang, W., Edelmann, L., Russell, R., Carrión, D.V., Chin, L., Kucherlapati, R., Kolodner, R.D., Edelmann, W., Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability and cancer in mice. Nat. Genet. 37 (2005), 750–755.
25. 25 Dudgeon, C., Chan, C., Kang, W., Sun, Y., Emerson, R., Robins, H., Levine, A.J., The evolution of thymic lymphomas in p53 knockout mice. Genes Dev. 28 (2014), 2613–2620.
26. 26 Barlow, C., Hirotsune, S., Paylor, R., Liyanage, M., Eckhaus, M., Collins, F., Shiloh, Y., Crawley, J.N., Ried, T., Tagle, D., Wynshaw-Boris, A., Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86 (1996), 159–171.
27. 27 Dingal, P.C., Bradshaw, A.M., Cho, S., Raab, M., Buxboim, A., Swift, J., Discher, D.E., Fractal heterogeneity in minimal matrix models of scars modulates stiff-niche stem-cell responses via nuclear exit of a mechanorepressor. Nat. Mater. 14 (2015), 951–960.
28. 28 Hass, C.S., Gakhar, L., Wold, M.S., Functional characterization of a cancer causing mutation in human replication protein A. Mol. Cancer Res. 8 (2010), 1017–1026.
29. 29 Jeon, G.S., Kim, K.Y., Hwang, Y.J., Jung, M.K., An, S., Ouchi, M., Ouchi, T., Kowall, N., Lee, J., Ryu, H., Deregulation of BRCA1 leads to impaired spatiotemporal dynamics of γ-H2AX and DNA damage responses in Huntington's disease. Mol. Neurobiol. 45 (2012), 550–563.
30. 30 Jensen, R.B., Ozes, A., Kim, T., Estep, A., Kowalczykowski, S.C., BRCA2 is epistatic to the RAD51 paralogs in response to DNA damage. DNA Repair (Amst.) 12 (2013), 306–311.
31. 31 Vandersickel, V., Depuydt, J., Van Bockstaele, B., Perletti, G., Philippe, J., Thierens, H., Vral, A., Early increase of radiation-induced γH2AX foci in a human Ku70/80 knockdown cell line characterized by an enhanced radiosensitivity. J. Radiat. Res. (Tokyo) 51 (2010), 633–641.
32. 32 Fiszer-Kierzkowska, A., Vydra, N., Wysocka-Wycisk, A., Kronekova, Z., Jarząb, M., Lisowska, K.M., Krawczyk, Z., Liposome-based DNA carriers may induce cellular stress response and change gene expression pattern in transfected cells. BMC Mol. Biol., 12, 2011, 27.
33. 33 Chen, W.T., Ebelt, N.D., Stracker, T.H., Xhemalce, B., Van Den Berg, C.L., Miller, K.M., ATM regulation of IL-8 links oxidative stress to cancer cell migration and invasion. eLife, 4, 2015, e07270.
34. 34 Carter, N.P., Methods and strategies for analyzing copy number variation using DNA microarrays. Nat. Genet. 39:7, Suppl (2007), S16–S21.
35. 35 Qiu, Z., Zou, K., Zhuang, L., Qin, J., Li, H., Li, C., Zhang, Z., Chen, X., Cen, J., Meng, Z., et al. Hepatocellular carcinoma cell lines retain the genomic and transcriptomic landscapes of primary human cancers. Sci. Rep., 6, 2016, 27411.
36. 36 Thiagalingam, S., Laken, S., Willson, J.K., Markowitz, S.D., Kinzler, K.W., Vogelstein, B., Lengauer, C., Mechanisms underlying losses of heterozygosity in human colorectal cancers. Proc. Natl. Acad. Sci. USA 98 (2001), 2698–2702.
37. 37 Sankaranarayanan, P., Schomay, T.E., Aiello, K.A., Alter, O., Tensor GSVD of patient- and platform-matched tumor and normal DNA copy-number profiles uncovers chromosome arm-wide patterns of tumor-exclusive platform-consistent alterations encoding for cell transformation and predicting ovarian cancer survival. PLoS ONE, 10, 2015, e0121396.
38. 38 Jaenisch, R., Bird, A., Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33:Suppl (2003), 245–254.
39. 39 Huang, W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009), 44–57.
40. 40 Tilney, L.G., Gibbins, J.R., Microtubules in the formation and development of the primary mesenchyme in Arbacia punctulata. II. An experimental analysis of their role in development and maintenance of cell shape. J. Cell Biol. 41 (1969), 227–250.
41. 41 Rivera-Feliciano, J., Lee, K.H., Kong, S.W., Rajagopal, S., Ma, Q., Springer, Z., Izumo, S., Tabin, C.J., Pu, W.T., Development of heart valves requires Gata4 expression in endothelial-derived cells. Development 133 (2006), 3607–3618.
42. 42 Güemes, M., Garcia, A.J., Rigueur, D., Runke, S., Wang, W., Zhao, G., Mayorga, V.H., Atti, E., Tetradis, S., Péault, B., et al. GATA4 is essential for bone mineralization via ERα and TGFβ/BMP pathways. J. Bone Miner. Res. 29 (2014), 2676–2687.
43. 43 Engler, A.J., Sen, S., Sweeney, H.L., Discher, D.E., Matrix elasticity directs stem cell lineage specification. Cell 126 (2006), 677–689.
44. 44 Song, I., Kim, K., Kim, J.H., Lee, Y.K., Jung, H.J., Byun, H.O., Yoon, G., Kim, N., GATA4 negatively regulates osteoblast differentiation by downregulation of Runx2. BMB Rep. 47 (2014), 463–468.
45. 45 Irianto, J., Xia, Y., Pfeifer, C.R., Greenberg, R.A., Discher, D.E., As a nucleus enters a small pore, chromatin stretches and maintains integrity even with DNA breaks. Biophys. J., 2016, 10.1016/j.bpj.2016.09.047 Published online October 27, 2016.
46. 46 Maciejowski, J., Li, Y., Bosco, N., Campbell, P.J., de Lange, T., Chromothripsis and kataegis induced by telomere crisis. Cell 163 (2015), 1641–1654.
47. 47 De Vos, W.H., Houben, F., Kamps, M., Malhas, A., Verheyen, F., Cox, J., Manders, E.M., Verstraeten, V.L., van Steensel, M.A., Marcelis, C.L., et al. Repetitive disruptions of the nuclear envelope invoke temporary loss of cellular compartmentalization in laminopathies. Hum. Mol. Genet. 20 (2011), 4175–4186.
48. 48 Tamiello, C., Kamps, M.A., van den Wijngaard, A., Verstraeten, V.L., Baaijens, F.P., Broers, J.L., Bouten, C.C., Soft substrates normalize nuclear morphology and prevent nuclear rupture in fibroblasts from a laminopathy patient with compound heterozygous LMNA mutations. Nucleus 4 (2013), 61–73.
49. 49 Nuciforo, P.G., Luise, C., Capra, M., Pelosi, G., d'Adda di Fagagna, F., Complex engagement of DNA damage response pathways in human cancer and in lung tumor progression. Carcinogenesis 28 (2007), 2082–2088.
50. 50 Gerlinger, M., Rowan, A.J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366 (2012), 883–892.