Causes and Consequences of Nuclear Envelope Rupture and DNA Damage in Micronuclei

Ania Grodsky

Abstract


Micronuclei are small, aberrant nuclear compartments containing mis-segregated chromosomes or chromosomal fragments. During telophase, dysfunctional micronuclear envelope reassembly leaves the micronuclear envelope highly unstable and rupture-prone. Following rupture, micronuclei attempt to repair membrane gaps, but the process is typically unsuccessful and may promote the invasion of ER tubules into the interior of micronuclei. These abnormalities cause ruptured micronuclei to accumulate significant DNA damage in the form of both single-stranded DNA and double-stranded breaks. Because micronuclei are capable of promoting genome instability, it is essential to understand the sources of DNA damage and the mechanism through which it arises in these structures. In this review, I will explore the causes and consequences of micronuclear envelope rupture, beginning with the processes surrounding improper micronuclear envelope reassembly. I will then discuss micronuclear envelope rupture, attempted micronuclear envelope repair and its consequences, and the proposed causes of micronuclear DNA damage.


Keywords


Micronuclei, Micronuclear Envelope, Micronuclear Envelope Rupture, DNA Damage, ESCRT

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References


Senior, A., & Gerace, L. (1988). Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina. Journal of Cell Biology, 107(6), 2029–2036. https://doi.org/10.1083/jcb.107.6.2029

Zwerger, M., & Medalia, O. (2013). From lamins to lamina: A structural perspective. Histochemistry and Cell Biology, 140(1), 3–12. https://doi.org/10.1007/s00418-013-1104-y

Davies, B. S. J., Coffinier, C., Yang, S. H., Jung, H.-J., Fong, L. G., & Young, S. G. (2011). 3—Posttranslational Processing of Nuclear Lamins. In F. Tamanoi, C. A. Hrycyna, & M. O. Bergo (Eds.), The Enzymes (Vol. 29, pp. 21–41). Academic Press. https://doi.org/10.1016/B978-0-12-381339-8.00003-2

Gaillard, M.-C., & Reddy, K. L. (2018). 14—The Nuclear Lamina and Genome Organization. In C. Lavelle & J.-M. Victor (Eds.), Nuclear Architecture and Dynamics (Vol. 2, pp. 321–343). Academic Press. https://doi.org/10.1016/B978-0-12-803480-4.00014-4

Padiath, Q. S., & Fu, Y.-H. (2010). Chapter 14—Autosomal Dominant Leukodystrophy Caused by Lamin B1 Duplications: A Clinical and Molecular Case Study of Altered Nuclear Function and Disease. In G. V. Shivashankar (Ed.), Methods in Cell Biology (Vol. 98, pp. 337–357). Academic Press. https://doi.org/10.1016/S0091-679X(10)98014-X

Raices, M., & D’Angelo, M. A. (2012). Nuclear pore complex composition: A new regulator of tissue-specific and developmental functions. Nature Reviews. Molecular Cell Biology, 13(11), 687–699. https://doi.org/10.1038/nrm3461

Mudumbi, K. C., Schirmer, E. C., & Yang, W. (2016). Single-point single-molecule FRAP distinguishes inner and outer nuclear membrane protein distribution. Nature Communications, 7(1), 12562. https://doi.org/10.1038/ncomms12562

Pawar, S., & Kutay, U. (2021). The Diverse Cellular Functions of Inner Nuclear Membrane Proteins. Cold Spring Harbor Perspectives in Biology, a040477. https://doi.org/10.1101/cshperspect.a040477

Güttinger, S., Laurell, E., & Kutay, U. (2009). Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nature Reviews Molecular Cell Biology, 10(3), 178–191. https://doi.org/10.1038/nrm2641

Yang, L., Guan, T., & Gerace, L. (1997). Integral Membrane Proteins of the Nuclear Envelope Are Dispersed throughout the Endoplasmic Reticulum during Mitosis. Journal of Cell Biology, 137(6), 1199–1210. https://doi.org/10.1083/jcb.137.6.1199

Stick, R., Angres, B., Lehner, C. F., & Nigg, E. A. (1988). The fates of chicken nuclear lamin proteins during mitosis: Evidence for a reversible redistribution of lamin B2 between inner nuclear membrane and elements of the endoplasmic reticulum. Journal of Cell Biology, 107(2), 397–406. https://doi.org/10.1083/jcb.107.2.397

Bonassi, S., El-Zein, R., Bolognesi, C., & Fenech, M. (2011). Micronuclei frequency in peripheral blood lymphocytes and cancer risk: Evidence from human studies. Mutagenesis, 26(1), 93–100. https://doi.org/10.1093/mutage/geq075

Rao, X., Zhang, Y., Yi, Q., Hou, H., Xu, B., Chu, L., Huang, Y., Zhang, W., Fenech, M., & Shi, Q. (2008). Multiple origins of spontaneously arising micronuclei in HeLa cells: Direct evidence from long-term live cell imaging. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 646(1), 41–49. https://doi.org/10.1016/j.mrfmmm.2008.09.004

Guo, X., Ni, J., Liang, Z., Xue, J., Fenech, M. F., & Wang, X. (2019). The molecular origins and pathophysiological consequences of micronuclei: New insights into an age-old problem. Mutation Research/Reviews in Mutation Research, 779, 1–35. https://doi.org/10.1016/j.mrrev.2018.11.001

Liu, S., Kwon, M., Mannino, M., Yang, N., Renda, F., Khodjakov, A., & Pellman, D. (2018). Nuclear envelope assembly defects link mitotic errors to chromothripsis. Nature, 561(7724), 551–555. https://doi.org/10.1038/s41586-018-0534-z

Hatch, E. M., Fischer, A. H., Deerinck, T. J., & Hetzer, M. W. (2013). Catastrophic Nuclear Envelope Collapse in Cancer Cell Micronuclei. Cell, 154(1), 47–60. https://doi.org/10.1016/j.cell.2013.06.007

Maciejowski, J., Li, Y., Bosco, N., Campbell, P. J., & de Lange, T. (2015). Chromothripsis and Kataegis Induced by Telomere Crisis. Cell, 163(7), 1641–1654. PubMed. https://doi.org/10.1016/j.cell.2015.11.054

Zhang, C.-Z., Spektor, A., Cornils, H., Francis, J. M., Jackson, E. K., Liu, S., Meyerson, M., & Pellman, D. (2015). Chromothripsis from DNA damage in micronuclei. Nature, 522(7555), 179–184. https://doi.org/10.1038/nature14493

Ly, P., Teitz, L. S., Kim, D. H., Shoshani, O., Skaletsky, H., Fachinetti, D., Page, D. C., & Cleveland, D. W. (2017). Selective Y centromere inactivation triggers chromosome shattering in micronuclei and repair by non-homologous end joining. Nature Cell Biology, 19(1), 68–75. https://doi.org/10.1038/ncb3450

Ly, P., Brunner, S. F., Shoshani, O., Kim, D. H., Lan, W., Pyntikova, T., Flanagan, A. M., Behjati, S., Page, D. C., Campbell, P. J., & Cleveland, D. W. (2019). Chromosome segregation errors generate a diverse spectrum of simple and complex genomic rearrangements. Nature Genetics, 51(4), 705–715. https://doi.org/10.1038/s41588-019-0360-8

Dou, Z., Ghosh, K., Vizioli, M. G., Zhu, J., Sen, P., Wangensteen, K. J., Simithy, J., Lan, Y., Lin, Y., Zhou, Z., Capell, B. C., Xu, C., Xu, M., Kieckhaefer, J. E., Jiang, T., Shoshkes-Carmel, M., Tanim, K. M. A. A., Barber, G. N., Seykora, J. T., … Berger, S. L. (2017). Cytoplasmic chromatin triggers inflammation in senescence and cancer. Nature, 550(7676), 402–406. https://doi.org/10.1038/nature24050

Li, T., & Chen, Z. J. (2018). The cGAS–cGAMP–STING pathway connects DNA damage to inflammation, senescence, and cancer. The Journal of Experimental Medicine, 215(5), 1287–1299. https://doi.org/10.1084/jem.20180139

Lin, F., & Worman, H. J. (1993). Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. Journal of Biological Chemistry, 268(22), 16321–16326. https://doi.org/10.1016/S0021-9258(19)85424-8

Maass, K. K., Rosing, F., Ronchi, P., Willmund, K. V., Devens, F., Hergt, M., Herrmann, H., Lichter, P., & Ernst, A. (2018). Altered nuclear envelope structure and proteasome function of micronuclei. Experimental Cell Research, 371(2), 353–363. https://doi.org/10.1016/j.yexcr.2018.08.029

Kneissig, M., Keuper, K., de Pagter, M. S., van Roosmalen, M. J., Martin, J., Otto, H., Passerini, V., Campos Sparr, A., Renkens, I., Kropveld, F., Vasudevan, A., Sheltzer, J. M., Kloosterman, W. P., & Storchova, Z. (2019). Micronuclei-based model system reveals functional consequences of chromothripsis in human cells. ELife, 8, e50292. https://doi.org/10.7554/eLife.50292

Miyazaki, K., Ichikawa, Y., Saitoh, N., & Saitoh, H. (2020). Three Types of Nuclear Envelope Assemblies Associated with Micronuclei. CellBio, 9(1), 14–28. https://doi.org/10.4236/cellbio.2020.91002

Sepaniac, L. A., Martin, W., Dionne, L. A., Stearns, T. M., Reinholdt, L. G., & Stumpff, J. (2020). Micronuclei arising due to loss of KIF18A form stable micronuclear envelopes and do not promote tumorigenesis. BioRxiv, 2020.11.23.394924. https://doi.org/10.1101/2020.11.23.394924

Barton, L. J., Soshnev, A. A., & Geyer, P. K. (2015). Networking in the nucleus: A spotlight on LEM-domain proteins. Current Opinion in Cell Biology, 34, 1–8. https://doi.org/10.1016/j.ceb.2015.03.005

Wagner, N., & Krohne, G. (2007). LEM‐Domain Proteins: New Insights into Lamin‐Interacting Proteins. In International Review of Cytology (Vol. 261, pp. 1–46). Academic Press. https://doi.org/10.1016/S0074-7696(07)61001-8

Haraguchi, T., Koujin, T., Segura-Totten, M., Lee, K. K., Matsuoka, Y., Yoneda, Y., Wilson, K. L., & Hiraoka, Y. (2001). BAF is required for emerin assembly into the reforming nuclear envelope. Journal of Cell Science, 114(24), 4575–4585.

Halfmann, C. T., Sears, R. M., Katiyar, A., Busselman, B. W., Aman, L. K., Zhang, Q., O’Bryan, C. S., Angelini, T. E., Lele, T. P., & Roux, K. J. (2019). Repair of nuclear ruptures requires barrier-to-autointegration factor. Journal of Cell Biology, 218(7), 2136–2149. https://doi.org/10.1083/jcb.201901116

Young, A. M., Gunn, A. L., & Hatch, E. M. (2020). BAF facilitates interphase nuclear membrane repair through recruitment of nuclear transmembrane proteins. Molecular Biology of the Cell, 31(15), 1551–1560. https://doi.org/10.1091/mbc.E20-01-0009

Willan, J., Cleasby, A. J., Flores-Rodriguez, N., Stefani, F., Rinaldo, C., Pisciottani, A., Grant, E., Woodman, P., Bryant, H. E., & Ciani, B. (2019). ESCRT-III is necessary for the integrity of the nuclear envelope in micronuclei but is aberrant at ruptured micronuclear envelopes generating damage. Oncogenesis, 8(5), 1–14. https://doi.org/10.1038/s41389-019-0136-0

Haraguchi, T., Kojidani, T., Koujin, T., Shimi, T., Osakada, H., Mori, C., Yamamoto, A., & Hiraoka, Y. (2008). Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. Journal of Cell Science, 121(15), 2540–2554. https://doi.org/10.1242/jcs.033597

Dechat, T., Gajewski, A., Korbei, B., Gerlich, D., Daigle, N., Haraguchi, T., Furukawa, K., Ellenberg, J., & Foisner, R. (2004). LAP2α and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. Journal of Cell Science, 117(25), 6117–6128. https://doi.org/10.1242/jcs.01529

Mayr, M. I., Hümmer, S., Bormann, J., Grüner, T., Adio, S., Woehlke, G., & Mayer, T. U. (2007). The Human Kinesin Kif18A Is a Motile Microtubule Depolymerase Essential for Chromosome Congression. Current Biology, 17(6), 488–498. https://doi.org/10.1016/j.cub.2007.02.036

Stumpff, J., Dassow, G. von, Wagenbach, M., Asbury, C., & Wordeman, L. (2008). The Kinesin-8 Motor Kif18A Suppresses Kinetochore Movements to Control Mitotic Chromosome Alignment. Developmental Cell, 14(2), 252–262. https://doi.org/10.1016/j.devcel.2007.11.014

Afonso, O., Matos, I., Pereira, A. J., Aguiar, P., Lampson, M. A., & Maiato, H. (2014). Feedback control of chromosome separation by a midzone Aurora B gradient. Science, 345(6194), 332–336. https://doi.org/10.1126/science.1251121

de Castro, I. J., Gil, R. S., Ligammari, L., Giacinto, M. L. D., & Vagnarelli, P. (2017). CDK1 and PLK1 coordinate the disassembly and reassembly of the nuclear envelope in vertebrate mitosis. Oncotarget, 9(8), 7763–7773. https://doi.org/10.18632/oncotarget.23666

Hauf, S., Cole, R. W., LaTerra, S., Zimmer, C., Schnapp, G., Walter, R., Heckel, A., van Meel, J., Rieder, C. L., & Peters, J.-M. (2003). The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore–microtubule attachment and in maintaining the spindle assembly checkpoint. Journal of Cell Biology, 161(2), 281–294. https://doi.org/10.1083/jcb.200208092

Carmena, M., Pinson, X., Platani, M., Salloum, Z., Xu, Z., Clark, A., MacIsaac, F., Ogawa, H., Eggert, U., Glover, D. M., Archambault, V., & Earnshaw, W. C. (2012). The Chromosomal Passenger Complex Activates Polo Kinase at Centromeres. PLOS Biology, 10(1), e1001250. https://doi.org/10.1371/journal.pbio.1001250

Kurasawa, Y., Earnshaw, W. C., Mochizuki, Y., Dohmae, N., & Todokoro, K. (2004). Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. The EMBO Journal, 23(16), 3237–3248. https://doi.org/10.1038/sj.emboj.7600347

Fuller, B. G., Lampson, M. A., Foley, E. A., Rosasco-Nitcher, S., Le, K. V., Tobelmann, P., Brautigan, D. L., Stukenberg, P. T., & Kapoor, T. M. (2008). Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature, 453(7198), 1132–1136. https://doi.org/10.1038/nature06923

Hochegger, H., Hégarat, N., & Pereira-Leal, J. B. (n.d.). Aurora at the pole and equator: Overlapping functions of Aurora kinases in the mitotic spindle. Open Biology, 3(3), 120185. https://doi.org/10.1098/rsob.120185

Hu, C.-K., Coughlin, M., Field, C. M., & Mitchison, T. J. (2011). KIF4 Regulates Midzone Length during Cytokinesis. Current Biology, 21(10), 815–824. https://doi.org/10.1016/j.cub.2011.04.019

Xia, Y., Pfeifer, C. R., Zhu, K., Irianto, J., Liu, D., Pannell, K., Chen, E. J., Dooling, L. J., Tobin, M. P., Wang, M., Ivanovska, I. L., Smith, L. R., Greenberg, R. A., & Discher, D. E. (2019). Rescue of DNA damage after constricted migration reveals a mechano-regulated threshold for cell cycle. Journal of Cell Biology, 218(8), 2545–2563. https://doi.org/10.1083/jcb.201811100

Nmezi, B., Xu, J., Fu, R., Armiger, T. J., Rodriguez-Bey, G., Powell, J. S., Ma, H., Sullivan, M., Tu, Y., Chen, N. Y., Young, S. G., Stolz, D. B., Dahl, K. N., Liu, Y., & Padiath, Q. S. (2019). Concentric organization of A- and B-type lamins predicts their distinct roles in the spatial organization and stability of the nuclear lamina. Proceedings of the National Academy of Sciences, 116(10), 4307–4315. https://doi.org/10.1073/pnas.1810070116

Harada, T., Swift, J., Irianto, J., Shin, J.-W., Spinler, K. R., Athirasala, A., Diegmiller, R., Dingal, P. C. D. P., Ivanovska, I. L., & Discher, D. E. (2014). Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. The Journal of Cell Biology, 204(5), 669–682. https://doi.org/10.1083/jcb.201308029

Vargas, J. D., Hatch, E. M., Anderson, D. J., & Hetzer, M. W. (2012). Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus, 3(1), 88–100. https://doi.org/10.4161/nucl.18954

Vietri, M., Schultz, S. W., Bellanger, A., Jones, C. M., Petersen, L. I., Raiborg, C., Skarpen, E., Pedurupillay, C. R. J., Kjos, I., Kip, E., Timmer, R., Jain, A., Collas, P., Knorr, R. L., Grellscheid, S. N., Kusumaatmaja, H., Brech, A., Micci, F., Stenmark, H., & Campsteijn, C. (2020). Unrestrained ESCRT-III drives micronuclear catastrophe and chromosome fragmentation. Nature Cell Biology, 22(7), 856–867. https://doi.org/10.1038/s41556-020-0537-5

Mohr, L., Toufektchan, E., Chu, K., & Maciejowski, J. (2020). ER-directed TREX1 limits cGAS recognition of micronuclei. BioRxiv, 2020.05.18.102103. https://doi.org/10.1101/2020.05.18.102103

Denais, C. M., Gilbert, R. M., Isermann, P., McGregor, A. L., Lindert, M. te, Weigelin, B., Davidson, P. M., Friedl, P., Wolf, K., & Lammerding, J. (2016). Nuclear envelope rupture and repair during cancer cell migration. Science, 352(6283), 353–358. https://doi.org/10.1126/science.aad7297

Raab, M., Gentili, M., Belly, H. de, Thiam, H.-R., Vargas, P., Jimenez, A. J., Lautenschlaeger, F., Voituriez, R., Lennon-Duménil, A.-M., Manel, N., & Piel, M. (2016). ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science, 352(6283), 359–362. https://doi.org/10.1126/science.aad7611

Hatch, E. M., & Hetzer, M. W. (2016). Nuclear envelope rupture is induced by actin-based nucleus confinement. The Journal of Cell Biology, 215(1), 27–36. https://doi.org/10.1083/jcb.201603053

Umbreit, N. T., Zhang, C.-Z., Lynch, L. D., Blaine, L. J., Cheng, A. M., Tourdot, R., Sun, L., Almubarak, H. F., Judge, K., Mitchell, T. J., Spektor, A., & Pellman, D. (2020). Mechanisms generating cancer genome complexity from a single cell division error. Science, 368(6488), eaba0712. https://doi.org/10.1126/science.aba0712

Kutay, U., Izaurralde, E., Bischoff, F. R., Mattaj, I. W., & Görlich, D. (1997). Dominant-negative mutants of importin-β block multiple pathways of import and export through the nuclear pore complex. The EMBO Journal, 16(6), 1153–1163. https://doi.org/10.1093/emboj/16.6.1153

Fontes, M. R. M., Teh, T., & Kobe, B. (2000). Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-α11Edited by K. Nagai. Journal of Molecular Biology, 297(5), 1183–1194. https://doi.org/10.1006/jmbi.2000.3642

Fornerod, M., Ohno, M., Yoshida, M., & Mattaj, I. W. (1997). CRM1 Is an Export Receptor for Leucine-Rich Nuclear Export Signals. Cell, 90(6), 1051–1060. https://doi.org/10.1016/S0092-8674(00)80371-2

Güttler, T., Madl, T., Neumann, P., Deichsel, D., Corsini, L., Monecke, T., Ficner, R., Sattler, M., & Görlich, D. (2010). NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nature Structural & Molecular Biology, 17(11), 1367–1376. https://doi.org/10.1038/nsmb.1931

Askjaer, P., Bachi, A., Wilm, M., Bischoff, F. R., Weeks, D. L., Ogniewski, V., Ohno, M., Niehrs, C., Kjems, J., Mattaj, I. W., & Fornerod, M. (1999). RanGTP-Regulated Interactions of CRM1 with Nucleoporins and a Shuttling DEAD-Box Helicase. Molecular and Cellular Biology, 19(9), 6276–6285. https://doi.org/10.1128/MCB.19.9.6276

Barton, L. J., Wilmington, S. R., Martin, M. J., Skopec, H. M., Lovander, K. E., Pinto, B. S., & Geyer, P. K. (2014). Unique and Shared Functions of Nuclear Lamina LEM Domain Proteins in Drosophila. Genetics, 197(2), 653–665. https://doi.org/10.1534/genetics.114.162941

Segura-Totten, M., Kowalski, A. K., Craigie, R., & Wilson, K. L. (2002). Barrier-to-autointegration factor. The Journal of Cell Biology, 158(3), 475–485. https://doi.org/10.1083/jcb.200202019

Jamin, A., Wicklund, A., & Wiebe, M. S. (2014). Cell- and Virus-Mediated Regulation of the Barrier-to-Autointegration Factor’s Phosphorylation State Controls Its DNA Binding, Dimerization, Subcellular Localization, and Antipoxviral Activity. Journal of Virology, 88(10), 5342–5355. https://doi.org/10.1128/JVI.00427-14

Nichols, R. J., Wiebe, M. S., & Traktman, P. (2006). The Vaccinia-related Kinases Phosphorylate the N′ Terminus of BAF, Regulating Its Interaction with DNA and Its Retention in the Nucleus. Molecular Biology of the Cell, 17(5), 2451–2464. https://doi.org/10.1091/mbc.E05-12-1179

Chen, Q., Sun, L., & Chen, Z. J. (2016). Regulation and function of the cGAS–STING pathway of cytosolic DNA sensing. Nature Immunology, 17(10), 1142–1149. https://doi.org/10.1038/ni.3558

Mackenzie, K. J., Carroll, P., Martin, C.-A., Murina, O., Fluteau, A., Simpson, D. J., Olova, N., Sutcliffe, H., Rainger, J. K., Leitch, A., Osborn, R. T., Wheeler, A. P., Nowotny, M., Gilbert, N., Chandra, T., Reijns, M. A. M., & Jackson, A. P. (2017). CGAS surveillance of micronuclei links genome instability to innate immunity. Nature, 548(7668), 461–465. https://doi.org/10.1038/nature23449

Zhao, B., Xu, P., Rowlett, C. M., Jing, T., Shinde, O., Lei, Y., West, A. P., Liu, W. R., & Li, P. (2020). The molecular basis of tight nuclear tethering and inactivation of cGAS. Nature, 587(7835), 673–677. https://doi.org/10.1038/s41586-020-2749-z

Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Peng, W., Zhang, M. Q., & Zhao, K. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nature Genetics, 40(7), 897–903. https://doi.org/10.1038/ng.154

Karmodiya, K., Krebs, A. R., Oulad-Abdelghani, M., Kimura, H., & Tora, L. (2012). H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics, 13(1), 424. https://doi.org/10.1186/1471-2164-13-424

Chen, Y., Maciejowski, (2021). [Precision of H3K9Ac nuclear envelope rupture detection]. Unpublished data.

Lovett, D. B., Shekhar, N., Nickerson, J. A., Roux, K. J., & Lele, T. P. (2013). Modulation of Nuclear Shape by Substrate Rigidity. Cellular and Molecular Bioengineering, 6(2), 230–238. https://doi.org/10.1007/s12195-013-0270-2

Khatau, S. B., Hale, C. M., Stewart-Hutchinson, P. J., Patel, M. S., Stewart, C. L., Searson, P. C., Hodzic, D., & Wirtz, D. (2009). A perinuclear actin cap regulates nuclear shape. Proceedings of the National Academy of Sciences, 106(45), 19017–19022. https://doi.org/10.1073/pnas.0908686106

Earle, A. J., Kirby, T. J., Fedorchak, G. R., Isermann, P., Patel, J., Iruvanti, S., Moore, S. A., Bonne, G., Wallrath, L. L., & Lammerding, J. (2020). Mutant lamins cause nuclear envelope rupture and DNA damage in skeletal muscle cells. Nature Materials, 19(4), 464–473. https://doi.org/10.1038/s41563-019-0563-5

Thomas, C. H., Collier, J. H., Sfeir, C. S., & Healy, K. E. (2002). Engineering gene expression and protein synthesis by modulation of nuclear shape. Proceedings of the National Academy of Sciences, 99(4), 1972–1977. https://doi.org/10.1073/pnas.032668799

Vergani, L., Grattarola, M., & Nicolini, C. (2004). Modifications of chromatin structure and gene expression following induced alterations of cellular shape. The International Journal of Biochemistry & Cell Biology, 36(8), 1447–1461. https://doi.org/10.1016/j.biocel.2003.11.015

Burke, B., & Roux, K. J. (2009). Nuclei Take a Position: Managing Nuclear Location. Developmental Cell, 17(5), 587–597. https://doi.org/10.1016/j.devcel.2009.10.018

Starr, D. A. (2011). Watching nuclei move. BioArchitecture, 1(1), 9–13. https://doi.org/10.4161/bioa.1.1.14629

Fridolfsson, H. N., & Starr, D. A. (2010). Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. Journal of Cell Biology, 191(1), 115–128. https://doi.org/10.1083/jcb.201004118

Bone, C. R., & Starr, D. A. (2016). Nuclear migration events throughout development. Journal of Cell Science, 129(10), 1951–1961. https://doi.org/10.1242/jcs.179788

Roman, W., & Gomes, E. R. (2018). Nuclear positioning in skeletal muscle. Seminars in Cell & Developmental Biology, 82, 51–56. https://doi.org/10.1016/j.semcdb.2017.11.005

Scheffer, L. L., Sreetama, S. C., Sharma, N., Medikayala, S., Brown, K. J., Defour, A., & Jaiswal, J. K. (2014). Mechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair. Nature Communications, 5, 5646. https://doi.org/10.1038/ncomms6646

Isermann, P., & Lammerding, J. (2017). Consequences of a tight squeeze: Nuclear envelope rupture and repair. Nucleus, 8(3), 268–274. https://doi.org/10.1080/19491034.2017.1292191

Samwer, M., Schneider, M. W. G., Hoefler, R., Schmalhorst, P. S., Jude, J. G., Zuber, J., & Gerlich, D. W. (2017). DNA Cross-Bridging Shapes a Single Nucleus from a Set of Mitotic Chromosomes. Cell, 170(5), 956-972.e23. https://doi.org/10.1016/j.cell.2017.07.038

Gong, Y.-N., Guy, C., Olauson, H., Becker, J. U., Yang, M., Fitzgerald, P., Linkermann, A., & Green, D. R. (2017). ESCRT-III acts downstream of MLKL to regulate necroptotic cell death and its consequences. Cell, 169(2), 286-300.e16. https://doi.org/10.1016/j.cell.2017.03.020

Sønder, S. L., Boye, T. L., Tölle, R., Dengjel, J., Maeda, K., Jäättelä, M., Simonsen, A. C., Jaiswal, J. K., & Nylandsted, J. (2019). Annexin A7 is required for ESCRT III-mediated plasma membrane repair. Scientific Reports, 9. https://doi.org/10.1038/s41598-019-43143-4

Thaller, D. J., Allegretti, M., Borah, S., Ronchi, P., Beck, M., & Lusk, C. P. (2019). An ESCRT-LEM protein surveillance system is poised to directly monitor the nuclear envelope and nuclear transport system. ELife, 8, e45284. https://doi.org/10.7554/eLife.45284

Gu, M., LaJoie, D., Chen, O. S., von Appen, A., Ladinsky, M. S., Redd, M. J., Nikolova, L., Bjorkman, P. J., Sundquist, W. I., Ullman, K. S., & Frost, A. (2017). LEM2 recruits CHMP7 for ESCRT-mediated nuclear envelope closure in fission yeast and human cells. Proceedings of the National Academy of Sciences, 114(11), E2166. https://doi.org/10.1073/pnas.1613916114

Pieper, G. H., Sprenger, S., Teis, D., & Oliferenko, S. (2020). ESCRT-III/Vps4 Controls Heterochromatin-Nuclear Envelope Attachments. Developmental Cell, 53(1), 27-41.e6. https://doi.org/10.1016/j.devcel.2020.01.028

Lusk, C. P., & Ader, N. R. (2020). CHMPions of repair: Emerging perspectives on sensing and repairing the nuclear envelope barrier. Cell Nucleus, 64, 25–33. https://doi.org/10.1016/j.ceb.2020.01.011

Olmos, Y., & Carlton, J. (2016). The ESCRT machinery: New roles at new holes. Current Opinion in Cell Biology, 38, 1–11. https://doi.org/10.1016/j.ceb.2015.12.001

Shen, Q.-T., Schuh, A. L., Zheng, Y., Quinney, K., Wang, L., Hanna, M., Mitchell, J. C., Otegui, M. S., Ahlquist, P., Cui, Q., & Audhya, A. (2014). Structural analysis and modeling reveals new mechanisms governing ESCRT-III spiral filament assembly. Journal of Cell Biology, 206(6), 763–777. https://doi.org/10.1083/jcb.201403108

Shibata, Y., Voeltz, G. K., & Rapoport, T. A. (2006). Rough Sheets and Smooth Tubules. Cell, 126(3), 435–439. https://doi.org/10.1016/j.cell.2006.07.019

Terasaki, M. (2018). Axonal endoplasmic reticulum is very narrow. Journal of Cell Science, 131(4). https://doi.org/10.1242/jcs.210450

Olmos, Y., Hodgson, L., Mantell, J., Verkade, P., & Carlton, J. G. (2015). ESCRT-III controls nuclear envelope reformation. Nature, 522(7555), 236–239. https://doi.org/10.1038/nature14503

Penfield, L., Shankar, R., Szentgyörgyi, E., Laffitte, A., Mauro, M. S., Audhya, A., Müller-Reichert, T., & Bahmanyar, S. (2020). Regulated lipid synthesis and LEM2/CHMP7 jointly control nuclear envelope closure. Journal of Cell Biology, 219(e201908179). https://doi.org/10.1083/jcb.201908179

Bahmanyar, S., Biggs, R., Schuh, A. L., Desai, A., Müller-Reichert, T., Audhya, A., Dixon, J. E., & Oegema, K. (2014). Spatial control of phospholipid flux restricts endoplasmic reticulum sheet formation to allow nuclear envelope breakdown. Genes & Development, 28(2), 121–126.

Siniossoglou, S. (2013). Phospholipid metabolism and nuclear function: Roles of the lipin family of phosphatidic acid phosphatases. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1831(3), 575–581. https://doi.org/10.1016/j.bbalip.2012.09.014

Wolf, C., Rapp, A., Berndt, N., Staroske, W., Schuster, M., Dobrick-Mattheuer, M., Kretschmer, S., König, N., Kurth, T., Wieczorek, D., Kast, K., Cardoso, M. C., Günther, C., & Lee-Kirsch, M. A. (2016). RPA and Rad51 constitute a cell intrinsic mechanism to protect the cytosol from self DNA. Nature Communications, 7(1), 11752. https://doi.org/10.1038/ncomms11752

Chowdhury, D., Beresford, P. J., Zhu, P., Zhang, D., Sung, J.-S., Demple, B., Perrino, F. W., & Lieberman, J. (2006). The Exonuclease TREX1 Is in the SET Complex and Acts in Concert with NM23-H1 to Degrade DNA during Granzyme A-Mediated Cell Death. Molecular Cell, 23(1), 133–142. https://doi.org/10.1016/j.molcel.2006.06.005

Yuan, F., Dutta, T., Wang, L., Song, L., Gu, L., Qian, L., Benitez, A., Ning, S., Malhotra, A., Deutscher, M. P., & Zhang, Y. (2015). Human DNA Exonuclease TREX1 Is Also an Exoribonuclease That Acts on Single-stranded RNA*. Journal of Biological Chemistry, 290(21), 13344–13353. https://doi.org/10.1074/jbc.M115.653915

Crasta, K., Ganem, N. J., Dagher, R., Lantermann, A. B., Ivanova, E. V., Pan, Y., Nezi, L., Protopopov, A., Chowdhury, D., & Pellman, D. (2012). DNA breaks and chromosome pulverization from errors in mitosis. Nature, 482(7383), 53–58. https://doi.org/10.1038/nature10802

Tang, S., Pellman, D. (2020). [DNA damage in micronuclei requires APE1]. Unpublished data.

Dianov, G. L., Sleeth, K. M., Dianova, I. I., & Allinson, S. L. (2003). Repair of abasic sites in DNA. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 531(1), 157–163. https://doi.org/10.1016/j.mrfmmm.2003.09.003

Cortés-Ciriano, I., Lee, J. J.-K., Xi, R., Jain, D., Jung, Y. L., Yang, L., Gordenin, D., Klimczak, L. J., Zhang, C.-Z., Pellman, D. S., & Park, P. J. (2020). Comprehensive analysis of chromothripsis in 2,658 human cancers using whole-genome sequencing. Nature Genetics, 52(3), 331–341. https://doi.org/10.1038/s41588-019-0576-7

Barber, G. N. (2015). STING: Infection, inflammation and cancer. Nature Reviews Immunology, 15(12), 760–770. https://doi.org/10.1038/nri3921

Savitsky, D., Tamura, T., Yanai, H., & Taniguchi, T. (2010). Regulation of immunity and oncogenesis by the IRF transcription factor family. Cancer Immunology, Immunotherapy: CII, 59(4), 489–510. https://doi.org/10.1007/s00262-009-0804-6

Xia, Y., Shen, S., & Verma, I. M. (2014). NF-κB, an active player in human cancers. Cancer Immunology Research, 2(9), 823–830. https://doi.org/10.1158/2326-6066.CIR-14-0112




DOI: https://doi.org/10.7575/aiac.abcmed.v.9n.4p.12

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