Nuclear GIT2 Is an ATM Substrate and Promotes DNA Repair

REFERENCES

• Frappart PO, McKinnon PJ. 2006. Ataxia-telangiectasia and related diseases. Neuromolecular Med 8:495–511. http://dx.doi.org/10.1385/NMM:8:4:495.
   PubMedGoogle Scholar
• Madabhushi R, Pan L, Tsai LH. 2014. DNA damage and its links to neurodegeneration. Neuron 83:266–282. http://dx.doi.org/10.1016/j.neuron.2014.06.034.
   PubMed Web of Science ®Google Scholar
• McKinnon PJ. 2004. ATM and ataxia telangiectasia. EMBO Rep 5:772–776. http://dx.doi.org/10.1038/sj.embor.7400210.
   PubMed Web of Science ®Google Scholar
• Perlman S, Becker-Catania S, Gatti RA. 2003. Ataxia-telangiectasia: diagnosis and treatment. Semin Pediatr Neurol 10:173–182. http://dx.doi.org/10.1016/S1071-9091(03)00026-3.
   PubMedGoogle Scholar
• Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, Tagle DA, Smith S, Uziel T, Sfez S, Ashkenazi M, Pecker I, Frydman M, Harnik R, Patanjali SR, Simmons A, Clines GA, Sartiel A, Gatti RA, Chessa L, Sanal O, Lavin MF, Jaspers NG, Taylor AM, Arlett CF, Miki T, Weissman SM, Lovett M, Collins FS, Shiloh Y. 1995. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749–1753. http://dx.doi.org/10.1126/science.7792600.
   PubMed Web of Science ®Google Scholar
• Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, Smorodinsky NI, Prives C, Reiss Y, Shiloh Y, Ziv Y. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281:1674–1677. http://dx.doi.org/10.1126/science.281.5383.1674.
   PubMed Web of Science ®Google Scholar
• Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677–1679. http://dx.doi.org/10.1126/science.281.5383.1677.
   PubMed Web of Science ®Google Scholar
• Falck J, Coates J, Jackson SP. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605–611. http://dx.doi.org/10.1038/nature03442.
   PubMed Web of Science ®Google Scholar
• Lee JH, Paull TT. 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304:93–96. http://dx.doi.org/10.1126/science.1091496.
   PubMed Web of Science ®Google Scholar
• Lim DS, Kim ST, Xu B, Maser RS, Lin J, Petrini JH, Kastan MB. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613–617. http://dx.doi.org/10.1038/35007091.
   PubMed Web of Science ®Google Scholar
• Wu X, Ranganathan V, Weisman DS, Heine WF, Ciccone DN, O'Neill TB, Crick KE, Pierce KA, Lane WS, Rathbun G, Livingston DM, Weaver DT. 2000. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405:477–482. http://dx.doi.org/10.1038/35013089.
   PubMed Web of Science ®Google Scholar
• Gatei M, Sloper K, Sorensen C, Syljuasen R, Falck J, Hobson K, Savage K, Lukas J, Zhou BB, Bartek J, Khanna KK. 2003. Ataxia-telangiectasia-mutated (ATM) and NBS1-dependent phosphorylation of Chk1 on Ser-317 in response to ionizing radiation. J Biol Chem 278:14806–14811. http://dx.doi.org/10.1074/jbc.M210862200.
   PubMed Web of Science ®Google Scholar
• Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. 2000. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci U S A 97:10389–10394. http://dx.doi.org/10.1073/pnas.190030497.
   PubMed Web of Science ®Google Scholar
• Xu B, O'Donnell AH, Kim ST, Kastan MB. 2002. Phosphorylation of serine 1387 in Brca1 is specifically required for the Atm-mediated S-phase checkpoint after ionizing irradiation. Cancer Res 62:4588–4591.
   PubMed Web of Science ®Google Scholar
• Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 18:1423–1438. http://dx.doi.org/10.1101/gad.1200304.
   PubMed Web of Science ®Google Scholar
• Kamer I, Sarig R, Zaltsman Y, Niv H, Oberkovitz G, Regev L, Haimovich G, Lerenthal Y, Marcellus RC, Gross A. 2005. Proapoptotic BID is an ATM effector in the DNA-damage response. Cell 122:593–603. http://dx.doi.org/10.1016/j.cell.2005.06.014.
   PubMed Web of Science ®Google Scholar
• Sobeck A, Stone S, Landais I, de Graaf B, Hoatlin ME. 2009. The Fanconi anemia protein FANCM is controlled by FANCD2 and the ATR/ATM pathways. J Biol Chem 284:25560–25568. http://dx.doi.org/10.1074/jbc.M109.007690.
   PubMed Web of Science ®Google Scholar
• Wang H, Wang M, Bocker W, Iliakis G. 2005. Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cells exposed to ionizing radiation and treated with kinase inhibitors. J Cell Physiol 202:492–502. http://dx.doi.org/10.1002/jcp.20141.
   PubMed Web of Science ®Google Scholar
• Hoefen RJ, Berk BC. 2006. The multifunctional GIT family of proteins. J Cell Sci 119:1469–1475. http://dx.doi.org/10.1242/jcs.02925.
   PubMed Web of Science ®Google Scholar
• Premont RT, Claing A, Vitale N, Freeman JL, Pitcher JA, Patton WA, Moss J, Vaughan M, Lefkowitz RJ. 1998. β2-Adrenergic receptor regulation by GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc Natl Acad Sci U S A 95:14082–14087. http://dx.doi.org/10.1073/pnas.95.24.14082.
   PubMed Web of Science ®Google Scholar
• Premont RT, Claing A, Vitale N, Perry SJ, Lefkowitz RJ. 2000. The GIT family of ADP-ribosylation factor GTPase-activating proteins. Functional diversity of GIT2 through alternative splicing. J Biol Chem 275:22373–22380. http://dx.doi.org/10.1074/jbc.275.29.22373.
   PubMed Web of Science ®Google Scholar
• Manabe R, Kovalenko M, Webb DJ, Horwitz AR. 2002. GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J Cell Sci 115:1497–1510.
   PubMed Web of Science ®Google Scholar
• Zhao ZS, Manser E, Loo TH, Lim L. 2000. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol 20:6354–6363. http://dx.doi.org/10.1128/MCB.20.17.6354-6363.2000.
   PubMedGoogle Scholar
• Frank SR, Adelstein MR, Hansen SH. 2006. GIT2 represses Crk- and Rac1-regulated cell spreading and Cdc42-mediated focal adhesion turnover. EMBO J 25:1848–1859. http://dx.doi.org/10.1038/sj.emboj.7601092.
   PubMedGoogle Scholar
• Phee H, Dzhagalov I, Mollenauer M, Wang Y, Irvine DJ, Robey E, Weiss A. 2010. Regulation of thymocyte positive selection and motility by GIT2. Nat Immunol 11:503–511. http://dx.doi.org/10.1038/ni.1868.
   PubMedGoogle Scholar
• Mazaki Y, Hashimoto S, Tsujimura T, Morishige M, Hashimoto A, Aritake K, Yamada A, Nam JM, Kiyonari H, Nakao K, Sabe H. 2006. Neutrophil direction sensing and superoxide production linked by the GTPase-activating protein GIT2. Nat Immunol 7:724–731. http://dx.doi.org/10.1038/ni1349.
   PubMed Web of Science ®Google Scholar
• Zhang H, Webb DJ, Asmussen H, Horwitz AF. 2003. Synapse formation is regulated by the signaling adaptor GIT1. J Cell Biol 161:131–142. http://dx.doi.org/10.1083/jcb.200211002.
   PubMed Web of Science ®Google Scholar
• Zhang H, Webb DJ, Asmussen H, Niu S, Horwitz AF. 2005. A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J Neurosci 25:3379–3388. http://dx.doi.org/10.1523/JNEUROSCI.3553-04.2005.
   PubMed Web of Science ®Google Scholar
• Ko J, Kim S, Valtschanoff JG, Shin H, Lee JR, Sheng M, Premont RT, Weinberg RJ, Kim E. 2003. Interaction between liprin-alpha and GIT1 is required for AMPA receptor targeting. J Neurosci 23:1667–1677.
   PubMedGoogle Scholar
• Segura I, Essmann CL, Weinges S, Acker-Palmer A. 2007. Grb4 and GIT1 transduce ephrinB reverse signals modulating spine morphogenesis and synapse formation. Nat Neurosci 10:301–310. http://dx.doi.org/10.1038/nn1858.
   PubMed Web of Science ®Google Scholar
• Schmalzigaug R, Phee H, Davidson CE, Weiss A, Premont RT. 2007. Differential expression of the ARF GAP genes GIT1 and GIT2 in mouse tissues. J Histochem Cytochem 55:1039–1048. http://dx.doi.org/10.1369/jhc.7A7207.2007.
   PubMed Web of Science ®Google Scholar
• Chadwick W, Zhou Y, Park SS, Wang L, Mitchell N, Stone MD, Becker KG, Martin B, Maudsley S. 2010. Minimal peroxide exposure of neuronal cells induces multifaceted adaptive responses. PLoS One 5:e14352. http://dx.doi.org/10.1371/journal.pone.0014352.
   PubMedGoogle Scholar
• Chadwick W, Martin B, Chapter MC, Park SS, Wang L, Daimon CM, Brenneman R, Maudsley S. 2012. GIT2 acts as a potential keystone protein in functional hypothalamic networks associated with age-related phenotypic changes in rats. PLoS One 7:e36975. http://dx.doi.org/10.1371/journal.pone.0036975.
   PubMedGoogle Scholar
• Chadwick W, Mitchell N, Caroll J, Zhou Y, Park SS, Wang L, Becker KG, Zhang Y, Lehrmann E, Wood WH, III, Martin B, Maudsley S. 2011. Amitriptyline-mediated cognitive enhancement in aged 3×Tg Alzheimer's disease mice is associated with neurogenesis and neurotrophic activity. PLoS One 6:e21660. http://dx.doi.org/10.1371/journal.pone.0021660.
   PubMedGoogle Scholar
• Caffrey DR, Zhao J, Song Z, Schaffer ME, Haney SA, Subramanian RR, Seymour AB, Hughes JD. 2011. siRNA off-target effects can be reduced at concentrations that match their individual potency. PLoS One 6:e21503. http://dx.doi.org/10.1371/journal.pone.0021503.
   PubMed Web of Science ®Google Scholar
• Gerlitz G. 2010. HMGNs, DNA repair and cancer. Biochim Biophys Acta 1799:80–85. http://dx.doi.org/10.1016/j.bbagrm.2009.10.007.
   PubMedGoogle Scholar
• Kim ST, Lim DS, Canman CE, Kastan MB. 1999. Substrate specificities and identification of putative substrates of ATM kinase family members. J Biol Chem 274:37538–37543. http://dx.doi.org/10.1074/jbc.274.53.37538.
   PubMed Web of Science ®Google Scholar
• Kitagawa R, Kastan MB. 2005. The ATM-dependent DNA damage signaling pathway. Cold Spring Harbor Symp Quant Biol 70:99–109. http://dx.doi.org/10.1101/sqb.2005.70.002.
   PubMedGoogle Scholar
• Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5:675–679. http://dx.doi.org/10.1038/ncb1004.
   PubMed Web of Science ®Google Scholar
• Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10:886–895. http://dx.doi.org/10.1016/S0960-9822(00)00610-2.
   PubMed Web of Science ®Google Scholar
• Peng Z, Liao Z, Dziegielewska B, Matsumoto Y, Thomas S, Wan Y, Yang A, Tomkinson AE. 2012. Phosphorylation of serine 51 regulates the interaction of human DNA ligase I with replication factor C and its participation in DNA replication and repair. J Biol Chem 287:36711–36719. http://dx.doi.org/10.1074/jbc.M112.383570.
   PubMedGoogle Scholar
• Blagosklonny MV, Iglesias A, Zhan Z, Fojo T. 1998. Like p53, the proliferation-associated protein p120 accumulates in human cancer cells following exposure to anticancer drugs. Biochem Biophys Res Commun 244:368–373. http://dx.doi.org/10.1006/bbrc.1998.8278.
   PubMedGoogle Scholar
• Yabe D, Fukuda H, Aoki M, Yamada S, Takebayashi S, Shinkura R, Yamamoto N, Honjo T. 2007. Generation of a conditional knockout allele for mammalian Spen protein Mint/SHARP. Genesis 45:300–306. http://dx.doi.org/10.1002/dvg.20296.
   PubMed Web of Science ®Google Scholar
• Daley JM, Sung P. 2014. 53BP1, BRCA1, and the choice between recombination and end joining at DNA double-strand breaks. Mol Cell Biol 34:1380–1388. http://dx.doi.org/10.1128/MCB.01639-13.
   PubMed Web of Science ®Google Scholar
• Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961–966. http://dx.doi.org/10.1038/nature01446.
   PubMed Web of Science ®Google Scholar
• Hassa PO, Haenni SS, Elser M, Hottiger MO. 2006. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol Mol Biol Rev 70:789–829. http://dx.doi.org/10.1128/MMBR.00040-05.
   PubMed Web of Science ®Google Scholar
• Potaman VN, Shlyakhtenko LS, Oussatcheva EA, Lyubchenko YL, Soldatenkov VA. 2005. Specific binding of poly(ADP-ribose) polymerase-1 to cruciform hairpins. J Mol Biol 348:609–615. http://dx.doi.org/10.1016/j.jmb.2005.03.010.
   PubMedGoogle Scholar
• Shiloh Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3:155–168. http://dx.doi.org/10.1038/nrc1011.
   PubMed Web of Science ®Google Scholar
• Hornyik C, Terzi LC, Simpson GG. 2010. The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18:203–213. http://dx.doi.org/10.1016/j.devcel.2009.12.009.
   PubMed Web of Science ®Google Scholar
• Fonagy A, Swiderski C, Freeman JW. 1995. Nucleolar p120 is expressed as a delayed early response gene and is inducible by DNA-damaging agents. J Cell Physiol 164:634–643. http://dx.doi.org/10.1002/jcp.1041640322.
   PubMedGoogle Scholar
• Elder RM, Jayaraman A. 2012. Sequence-specific recognition of cancer drug-DNA adducts by HMGB1a repair protein. Biophys J 102:2331–2338. http://dx.doi.org/10.1016/j.bpj.2012.04.013.
   PubMed Web of Science ®Google Scholar
• Sareen A, Chaudhury I, Adams N, Sobeck A. 2012. Fanconi anemia proteins FANCD2 and FANCI exhibit different DNA damage responses during S-phase. Nucleic Acids Res 40:8425–8439. http://dx.doi.org/10.1093/nar/gks638.
   PubMedGoogle Scholar
• Masaoka A, Gassman NR, Kedar PS, Prasad R, Hou EW, Horton JK, Bustin M, Wilson SH. 2012. HMGN1 protein regulates poly(ADP-ribose) polymerase-1 (PARP-1) self-PARylation in mouse fibroblasts. J Biol Chem 287:27648–27658. http://dx.doi.org/10.1074/jbc.M112.370759.
   PubMedGoogle Scholar
• Franko J, Ashley C, Xiao W. 2001. Molecular cloning and functional characterization of two murine cDNAs which encode Ubc variants involved in DNA repair and mutagenesis. Biochim Biophys Acta 1519:70–77. http://dx.doi.org/10.1016/S0167-4781(01)00223-8.
   PubMedGoogle Scholar
• Janssens J, Etienne H, Idriss S, Azmi A, Martin B, Maudsley S. 2014. Systems-level G protein-coupled receptor therapy across a neurodegenerative continuum by the GLP-1 receptor system. Front Endocrinol 5:142. http://dx.doi.org/10.3389/fendo.2014.00142.
   PubMedGoogle Scholar