Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response

Current Biology

Volumn 22, Issue 17, 2012, Pages 1609-1615

  Lei, Kai ^a   Zhu, Xiaoqiang ^a   Xu, Rener ^a   Shao, Chunlin ^b   Xu, Tian ^a,c   Zhuang, Yuan ^a,d   Han, Min ^a,e  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; PRKDC PROTEIN, MOUSE; SUN1 PROTEIN, MOUSE; SUN2 PROTEIN, MOUSE; TELOMERE BINDING PROTEIN;

ANIMAL; ARTICLE; CELL CULTURE; CELL PROLIFERATION; DNA DAMAGE; DNA REPAIR; GENETICS; GENOMIC INSTABILITY; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; DNA DAMAGE; DNA REPAIR; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; GENOMIC INSTABILITY; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; TELOMERE-BINDING PROTEINS;

MAMMALIA; MUS;

EID: 84866174261     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2012.06.043     Document Type: Article

References (40)

1. G.A. Garinis, G.T. van der Horst, J. Vijg, and J.H. Hoeijmakers DNA damage and ageing: new-age ideas for an age-old problem Nat. Cell Biol. 10 2008 1241 1247
2. A. Ciccia, and S.J. Elledge The DNA damage response: making it safe to play with knives Mol. Cell 40 2010 179 204
3. C.Y. Chen, Y.H. Chi, R.A. Mutalif, M.F. Starost, T.G. Myers, S.A. Anderson, C.L. Stewart, and K.T. Jeang Accumulation of the inner nuclear envelope protein Sun1 is pathogenic in progeric and dystrophic laminopathies Cell 149 2012 565 577
4. B.C. Capell, and F.S. Collins Human laminopathies: nuclei gone genetically awry Nat. Rev. Genet. 7 2006 940 952 (Pubitemid 44871397)
5. E. Weterings, and D.J. Chen DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J. Cell Biol. 179 2007 183 186 (Pubitemid 350004882)
6. T. Stiff, M. O'Driscoll, N. Rief, K. Iwabuchi, M. Löbrich, and P.A. Jeggo ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation Cancer Res. 64 2004 2390 2396 (Pubitemid 38523891)
7. C.J. Malone, W.D. Fixsen, H.R. Horvitz, and M. Han UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development Development 126 1999 3171 3181 (Pubitemid 29378180)
8. Y.B. Tzur, K.L. Wilson, and Y. Gruenbaum SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton Nat. Rev. Mol. Cell Biol. 7 2006 782 788 (Pubitemid 44450462)
9. H.J. Worman, and G.G. Gundersen Here come the SUNs: a nucleocytoskeletal missing link Trends Cell Biol. 16 2006 67 69 (Pubitemid 43247401)
10. K. Lei, X. Zhang, X. Ding, X. Guo, M. Chen, B. Zhu, T. Xu, Y. Zhuang, R. Xu, and M. Han SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice Proc. Natl. Acad. Sci. USA 106 2009 10207 10212
11. X. Zhang, K. Lei, X. Yuan, X. Wu, Y. Zhuang, T. Xu, R. Xu, and M. Han SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice Neuron 64 2009 173 187
12. J. Yu, K. Lei, M. Zhou, C.M. Craft, G. Xu, T. Xu, Y. Zhuang, R. Xu, and M. Han KASH protein Syne-2/Nesprin-2 and SUN proteins SUN1/2 mediate nuclear migration during mammalian retinal development Hum. Mol. Genet. 20 2011 1061 1073
13. R.W. Sobol, J.K. Horton, R. Kühn, H. Gu, R.K. Singhal, R. Prasad, K. Rajewsky, and S.H. Wilson Requirement of mammalian DNA polymerase-beta in base-excision repair Nature 379 1996 183 186 (Pubitemid 26020204)
14. T.T. Paull, E.P. Rogakou, V. Yamazaki, C.U. Kirchgessner, M. Gellert, and W.M. Bonner A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage Curr. Biol. 10 2000 886 895 (Pubitemid 30647617)
15. J.W. Harper, and S.J. Elledge The DNA damage response: ten years after Mol. Cell 28 2007 739 745 (Pubitemid 350217064)
16. F. d'Adda di Fagagna Living on a break: cellular senescence as a DNA-damage response Nat. Rev. Cancer 8 2008 512 522 (Pubitemid 351881854)
17. G.C. Smith, F. d'Adda di Fagagna, N.D. Lakin, and S.P. Jackson Cleavage and inactivation of ATM during apoptosis Mol. Cell. Biol. 19 1999 6076 6084 (Pubitemid 29399313)
18. M.P. Washburn, D. Wolters, and J.R. Yates 3rd Large-scale analysis of the yeast proteome by multidimensional protein identification technology Nat. Biotechnol. 19 2001 242 247 (Pubitemid 32220565)
19. V.C. Padmakumar, T. Libotte, W. Lu, H. Zaim, S. Abraham, A.A. Noegel, J. Gotzmann, R. Foisner, and I. Karakesisoglou The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope J. Cell Sci. 118 2005 3419 3430 (Pubitemid 41246097)
20. F. Haque, D.J. Lloyd, D.T. Smallwood, C.L. Dent, C.M. Shanahan, A.M. Fry, R.C. Trembath, and S. Shackleton SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton Mol. Cell. Biol. 26 2006 3738 3751 (Pubitemid 43726392)
21. M. Ketema, K. Wilhelmsen, I. Kuikman, H. Janssen, D. Hodzic, and A. Sonnenberg Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin J. Cell Sci. 120 2007 3384 3394 (Pubitemid 350028346)
22. D.A. Starr, and H.N. Fridolfsson Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges Annu. Rev. Cell Dev. Biol. 26 2010 421 444
23. S.H. Lee, and C.H. Kim DNA-dependent protein kinase complex: a multifunctional protein in DNA repair and damage checkpoint Mol. Cells 13 2002 159 166
24. D.B. Lombard, K.F. Chua, R. Mostoslavsky, S. Franco, M. Gostissa, and F.W. Alt DNA repair, genome stability, and aging Cell 120 2005 497 512 (Pubitemid 40269764)
25. G.H. Liu, B.Z. Barkho, S. Ruiz, D. Diep, J. Qu, S.L. Yang, A.D. Panopoulos, K. Suzuki, L. Kurian, and C. Walsh Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome Nature 472 2011 221 225
26. M. Koike, T. Awaji, M. Kataoka, G. Tsujimoto, T. Kartasova, A. Koike, and T. Shiomi Differential subcellular localization of DNA-dependent protein kinase components Ku and DNA-PKcs during mitosis J. Cell Sci. 112 1999 4031 4039 (Pubitemid 30119772)
27. X. Ding, R. Xu, J. Yu, T. Xu, Y. Zhuang, and M. Han SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice Dev. Cell 12 2007 863 872 (Pubitemid 46805916)
28. Y.H. Chi, L.I. Cheng, T. Myers, J.M. Ward, E. Williams, Q. Su, L. Faucette, J.Y. Wang, and K.T. Jeang Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA Development 136 2009 965 973
29. P. Oza, and C.L. Peterson Opening the DNA repair toolbox: localization of DNA double strand breaks to the nuclear periphery Cell Cycle 9 2010 43 49
30. K. Weis, G. Griffiths, and A.I. Lamond The endoplasmic reticulum calcium-binding protein of 55 kDa is a novel EF-hand protein retained in the endoplasmic reticulum by a carboxyl-terminal His-Asp-Glu-Leu motif J. Biol. Chem. 269 1994 19142 19150
31. F. Wei, Y. Xie, L. He, L. Tao, and D. Tang ERK1 and ERK2 kinases activate hydroxyurea-induced S-phase checkpoint in MCF7 cells by mediating ATR activation Cell. Signal. 23 2011 259 268
32. B. Burke, and C.L. Stewart The laminopathies: the functional architecture of the nucleus and its contribution to disease Annu. Rev. Genomics Hum. Genet. 7 2006 369 405 (Pubitemid 44627935)
33. H.J. Worman, C. Ostlund, and Y. Wang Diseases of the nuclear envelope Cold Spring Harb. Perspect. Biol. 2 2010 a000760
34. T. Dechat, K. Pfleghaar, K. Sengupta, T. Shimi, D.K. Shumaker, L. Solimando, and R.D. Goldman Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin Genes Dev. 22 2008 832 853 (Pubitemid 351482836)
35. S. Hasan, S. Güttinger, P. Mühlhäusser, F. Anderegg, S. Bürgler, and U. Kutay Nuclear envelope localization of human UNC84A does not require nuclear lamins FEBS Lett. 580 2006 1263 1268 (Pubitemid 43221987)
36. A. Méjat, V. Decostre, J. Li, L. Renou, A. Kesari, D. Hantaï, C.L. Stewart, X. Xiao, E. Hoffman, G. Bonne, and T. Misteli Lamin A/C-mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy J. Cell Biol. 184 2009 31 44
37. F. Haque, D. Mazzeo, J.T. Patel, D.T. Smallwood, J.A. Ellis, C.M. Shanahan, and S. Shackleton Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes J. Biol. Chem. 285 2010 3487 3498
38. I. Gonzalez-Suarez, A.B. Redwood, S.M. Perkins, B. Vermolen, D. Lichtensztejin, D.A. Grotsky, L. Morgado-Palacin, E.J. Gapud, B.P. Sleckman, and T. Sullivan Novel roles for A-type lamins in telomere biology and the DNA damage response pathway EMBO J. 28 2009 2414 2427
39. B. Liu, J. Wang, K.M. Chan, W.M. Tjia, W. Deng, X. Guan, J.D. Huang, K.M. Li, P.Y. Chau, and D.J. Chen Genomic instability in laminopathy-based premature aging Nat. Med. 11 2005 780 785 (Pubitemid 41021211)
40. H. Sun, N.T. Gulbagci, and R. Taneja Analysis of growth properties and cell cycle regulation using mouse embryonic fibroblast cells Methods Mol. Biol. 383 2007 311 319