Differential dynamics of ATR-mediated checkpoint regulators

Journal of Nucleic Acids

Volumn 2010, Issue , 2010, Pages

  Warmerdam, Daniël O ^a   Kanaar, Roland ^a   Smits, Veronique A J ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b HOSPITAL UNIVERSITARIO DE CANARIAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; COMPLEMENTARY DNA; GREEN FLUORESCENT PROTEIN; HISTONE H2AX; PROTEIN RAD1; PROTEIN RAD17; PROTEIN RAD9; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN;

ARTICLE; BLEACHING; CELL CULTURE; CELL LINE; CELL SELECTION; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; ENZYME PHOSPHORYLATION; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE CONSTRUCT; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; ULTRAVIOLET RADIATION;

EID: 79951502221     PISSN: 20900201     EISSN: 2090021X     Source Type: Journal    
DOI: 10.4061/2010/319142     Document Type: Article

References (75)

1. Shiloh Y., ATM and related protein kinases: safeguarding genome integrity. Nature Reviews Cancer 2003 3 3 155 168 2-s2.0-0037365789 10.1038/nrc1011 (Pubitemid 37328868)
2. Huen M. S. Y., Sy S. M. H., Chen J., jchen8@mdanderson.org BRCA1 and its toolbox for the maintenance of genome integrity. Nature Reviews Molecular Cell Biology 2010 11 2 138 148 2-s2.0-34548825453 10.1038/nrm2831
3. Huen M. S. Y., Chen J., jchen8@mdanderson.org Assembly of checkpoint and repair machineries at DNA damage sites. Trends in Biochemical Sciences 2010 35 2 101 108 2-s2.0-0037468169 10.1016/j.tibs.2009.09.001
4. Zou L., Elledge S. J., Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003 300 5625 1542 1548 2-s2.0-0037567268 10.1126/science.1083430 (Pubitemid 36682880)
5. Zou L., Cortez D., Elledge S. J., Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes and Development 2002 16 2 198 208 2-s2.0-0037080675 10.1101/gad.950302 (Pubitemid 34075812)
6. Kondo T., Wakayama T., Naiki T., Matsumoto K., Sugimoto K., Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 2001 294 5543 867 870 2-s2.0-0035955398 10.1126/science. 1063827 (Pubitemid 33032107)
7. Melo J. A., Cohen J., Toczyski D. P., Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes and Development 2001 15 21 2809 2821 2-s2.0-0035498938 (Pubitemid 33042052)
8. Lee J., Kumagai A., Dunphy W. G., The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. Journal of Biological Chemistry 2007 282 38 28036 28044 2-s2.0-34948889415 10.1074/jbc.M704635200 (Pubitemid 47529479)
9. Delacroix S., Wagner J. M., Kobayashi M., Yamamoto K.-I., Karnitz L. M., The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes and Development 2007 21 12 1472 1477 2-s2.0-34250705797 10.1101/gad.1547007 (Pubitemid 46955719)
10. Majka J., Niedziela-Majka A., Burgers P. J., The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint. Molecular Cell 2006 24 6 891 901 2-s2.0-33845607102 10.1016/j.molcel.2006.11.027 (Pubitemid 44960097)
11. Zhou B.-B. S., Elledge S. J., The DNA damage response: putting checkpoints in perspective. Nature 2000 408 6811 433 439 2-s2.0-0034707047 10.1038/35044005
12. Shiotani B., Zou L., ATR signaling at a glance. Journal of Cell Science 2009 122 3 301 304 2-s2.0-65249139994 10.1242/jcs.035105
13. Harper J. W., Elledge S. J., The DNA damage response: ten years after. Molecular Cell 2007 28 5 739 745 2-s2.0-36749022214 10.1016/j.molcel.2007.11.015 (Pubitemid 350217064)
14. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M. B., Bartek J., Lukas J., Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. Journal of Cell Biology 2006 173 2 195 206 2-s2.0-33646117239 10.1083/jcb.200510130
15. Lukas C., Falck J., Bartkova J., Bartek J., Lukas J., Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nature Cell Biology 2003 5 3 255 260 2-s2.0-0037341599 10.1038/ncb945 (Pubitemid 36322254)
16. Essers J., Houtsmuller A. B., Kanaar R., Analysis of DNA recombination and repair proteins in living cells by photobleaching microscopy. Methods in Enzymology 2006 408 463 485 2-s2.0-33745221171 10.1016/S0076-6879(06)08029-3
17. Essers J., Houtsmuller A. B., Van Veelen L., Paulusma C., Nigg A. L., Pastink A., Vermeulen W., Hoeijmakers J. H. J., Kanaar R., Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO Journal 2002 21 8 2030 2037 2-s2.0-0037090535 10.1093/emboj/21.8.2030 (Pubitemid 34437200)
18. Van Veelen L. R., Cervelli T., Van De Rakt M. W., Theil A. F., Essers J., Kanaar R., Analysis of ionizing radiation-induced foci of DNA damage repair proteins. Mutation Research 2005 574 1-2 22 33 2-s2.0-19444376493 10.1016/j.mrfmmm.2005.01.019 (Pubitemid 40725965)
19. Lippincott-Schwartz J., Patterson G. H., Development and use of fluorescent protein markers in living cells. Science 2003 300 5616 87 91 2-s2.0-0037418882 10.1126/science.1082520 (Pubitemid 36423032)
20. Easwaran H. P., Leonhardt H., Cardoso M. C., Cell cycle markers for live cell analyses. Cell Cycle 2005 4 3 453 455 2-s2.0-22344448505 (Pubitemid 41359733)
21. Warmerdam D. O., Freire R., Kanaar R., Smits V. A. J., Cell cycle-dependent processing of DNA lesions controls localization of Rad9 to sites of genotoxic stress. Cell Cycle 2009 8 11 1765 1774 2-s2.0-66749120336
22. Bonilla C. Y., Melo J. A., Toczyski D. P., Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Molecular Cell 2008 30 3 267 276 2-s2.0-42949130159 10.1016/j.molcel.2008.03.023 (Pubitemid 351615321)
23. Lukas J., Lukas C., Bartek J., Mammalian cell cycle checkpoints: signalling pathways and their organization in space and time. DNA Repair 2004 3 8-9 997 1007 2-s2.0-3242890575 10.1016/j.dnarep.2004.03.006 (Pubitemid 38997942)
24. Soutoglou E., Misteli T., Activation of the cellular DNA damage response in the absence of DNA lesions. Science 2008 320 5882 1507 1510 2-s2.0-45849117573 10.1126/science.1159051 (Pubitemid 351929432)
25. Houtsmuller A. B., Rademakers S., Nigg A. L., Hoogstraten D., Hoeijmakers J. H. J., Vermeulen W., Action of DNA repair endonuclease ERCC1/XPF in living cells. Science 1999 284 5416 958 961 2-s2.0-0033532342 10.1126/science.284.5416. 958 (Pubitemid 29288433)
26. Zotter A., Luijsterburg M. S., Warmerdam D. O., Ibrahim S., Nigg A., Van Cappellen W. A., Hoeijmakers J. H. J., Van Driel R., Vermeulen W., Houtsmuller A. B., Recruitment of the nucleotide excision repair endonuclease XPG to sites of UV-induced DNA damage depends on functional TFIIH. Molecular and Cellular Biology 2006 26 23 8868 8879 2-s2.0-33845232596 10.1128/MCB.00695-06 (Pubitemid 44851945)
27. Luijsterburg M. S., Goedhart J., Moser J., Kool H., Geverts B., Houtsmuller A. B., Mullenders L. H. F., Vermeulen W., van Driel R., Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. Journal of Cell Science 2007 120 15 2706 2716 2-s2.0-34548266764 10.1242/jcs.008367 (Pubitemid 47323877)
28. Giglia-Mari G., Coin F., Ranish J. A., Hoogstraten D., Theil A., Wijgers N., Jaspers N. G. J., Raams A., Argentini M., Van Der Spek P. J., Botta E., Stefanini M., Egly J.-M., Aebersold R., Hoeijmakers J. H. J., Vermeulen W., A new, tenth subunit TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nature Genetics 2004 36 7 714 719 2-s2.0-3042781670 10.1038/ng1387 (Pubitemid 38886632)
29. Giglia-Mari G., Miquel C., Theil A. F., Mari P. O., Hoogstraten D., Ng J. M., Dinant C., Hoeijmakers J. H., Vermeulen W., Dynamic interaction of TTDA with TFIIH is stabilized by nucleotide excision repair in living cells. PLoS Biology 2006 4 6, article e156 2-s2.0-33746918738 10.1371/journal.pbio.0040156
30. Toueille M., El-Andaloussi N., Fouin I., Freire R., Funk D., Shevelev I., Friedrich-Heineken E., Villani G., Hottiger M. O., Hübscher U., The human Rad9/Rad1/Hus1 damage sensor clamp interacts with DNA polymerase β and increases its DNA substrate utilisation efficiency: implications for DNA repair. Nucleic Acids Research 2004 32 11 3316 3324 2-s2.0-4043133233 10.1093/nar/gkh652 (Pubitemid 39117448)
31. Rendtlew Danielson J. M., Larsen D. H., Schou K. B., Freire R., Falck J., Bartek J., Lukas J., HCLK2 is required for activity of the DNA damage response kinase ATR. Journal of Biological Chemistry 2009 284 7 4140 4147 2-s2.0-63249131734 10.1074/jbc.M808174200
32. Jones G. G., Reaper P. M., Pettitt A. R., Sherrington P. D., The ATR-p53 pathway is suppressed in noncycling normal and malignant lymphocytes. Oncogene 2004 23 10 1911 1921 2-s2.0-1842534256 10.1038/sj.onc.1207318 (Pubitemid 38445417)
33. Medhurst A. L., Warmerdam D. O., Akerman I., Verwayen E. H., Kanaar R., Smits V. A. J., Lakin N. D., ATR and Rad17 collaborate in modulating Rad9 localisation at sites of DNA damage. Journal of Cell Science 2008 121 23 3933 3940 2-s2.0-59349107234 10.1242/jcs.033688
34. Mendez J., Stillman B., Chromatin association of human origin recognition complex, Cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Molecular and Cellular Biology 2000 20 22 8602 8612 2-s2.0-0033756308 10.1128/MCB.20.22.8602-8612.2000
35. Smits V. A. J., Reaper P. M., Jackson S. P., Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Current Biology 2006 16 2 150 159 2-s2.0-30944435598 10.1016/j.cub.2005.11.066 (Pubitemid 43117429)
36. Dinant C., de Jager M., Essers J., van Cappellen W. A., Kanaar R., Houtsmuller A. B., Vermeulen W., Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. Journal of Cell Science 2007 120 15 2731 2740 2-s2.0-34548235023 10.1242/jcs.004523 (Pubitemid 47323879)
37. Essers J., Theil A. F., Baldeyron C., Van Cappellen W. A., Houtsmuller A. B., Kanaar R., Vermeulen W., Nuclear dynamics of PCNA in DNA replication and repair. Molecular and Cellular Biology 2005 25 21 9350 9359 2-s2.0-27144491909 10.1128/MCB.25.21.9350-9359.2005 (Pubitemid 41507836)
38. Tsien R. Y., The green fluorescent protein. Annual Review of Biochemistry 1998 67 509 544 2-s2.0-0031663369 10.1146/annurev.biochem.67.1.509 (Pubitemid 28411137)
39. Tsien R. Y., Miyawaki A., Seeing the machinery of live cells. Science 1998 280 5371 1954 1955 2-s2.0-0032546846 10.1126/science.280.5371.1954 (Pubitemid 28299406)
40. Giepmans B. N. G., Adams S. R., Ellisman M. H., Tsien R. Y., The fluorescent toolbox for assessing protein location and function. Science 2006 312 5771 217 224 2-s2.0-33645798851 10.1126/science.1124618
41. Heim R., Cubitt A. B., Tsien R. Y., Improved green fluorescence. Nature 1995 373 6516 663 664 2-s2.0-0028921834
42. Prescott M., Nowakowski S., Nagley P., Devenish R. J., The length of polypeptide linker affects the stability of green fluorescent protein fusion proteins. Analytical Biochemistry 1999 273 2 305 307 2-s2.0-0033543597 10.1006/abio.1999.4235 (Pubitemid 29430675)
43. O'Driscoll M., Ruiz-Perez V. L., Woods C. G., Jeggo P. A., Goodship J. A., A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nature Genetics 2003 33 4 497 501 2-s2.0-0345073699 10.1038/ng1129 (Pubitemid 36390012)
44. Weiss R. S., Enoch T., Leder P., Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes and Development 2000 14 15 1886 1898 2-s2.0-0033899767 (Pubitemid 30639522)
45. Weiss R. S., Leder P., Vaziri C., Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Molecular and Cellular Biology 2003 23 3 791 803 2-s2.0-0037304633 10.1128/MCB.23.3.791-803.2003 (Pubitemid 36133498)
46. Hopkins K. M., Auerbach W., Wang X. Y., Hande M. P., Hang H., Wolgemuth D. J., Joyner A. L., Lieberman H. B., Deletion of mouse Rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Molecular and Cellular Biology 2004 24 16 7235 7248 2-s2.0-3543028030 10.1128/MCB.24.16.7235-7248.2004 (Pubitemid 39014449)
47. Zachos G., Rainey M. D., Gillespie D. A. F., Chk1-dependent S-M checkpoint delay in vertebrate cells is linked to maintenance of viable replication structures. Molecular and Cellular Biology 2005 25 2 563 574 2-s2.0-11844300367 10.1128/MCB.25.2.563-574.2005 (Pubitemid 40096579)
48. Kitagawa R., Bakkenist C. J., McKinnon P. J., Kastan M. B., Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes and Development 2004 18 12 1423 1438 2-s2.0-2942687831 10.1101/gad.1200304 (Pubitemid 38780629)
49. Bekker-Jensen S., Lukas C., Melander F., Bartek J., Lukas J., Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. Journal of Cell Biology 2005 170 2 201 211 2-s2.0-22944462083 10.1083/jcb.200503043 (Pubitemid 41043803)
50. Bonner J. A., Lawrence T. S., Doxorubicin decreases the repair of radiation-induced DNA damage. International Journal of Radiation Biology 1990 57 1 55 64 2-s2.0-0025099314 (Pubitemid 20027031)
51. Majka J., Binz S. K., Wold M. S., Burgers P. M. J., Replication protein a directs loading of the DNA damage checkpoint clamp to 5′ -DNA junctions. Journal of Biological Chemistry 2006 281 38 27855 27861 2-s2.0-33748780358 10.1074/jbc.M605176200 (Pubitemid 44414497)
52. Zou L., Liu D., Elledge S. J., Replication protein A-mediated recruitment and activation of Rad17 complexes. Proceedings of the National Academy of Sciences of the United States of America 2003 100 24 13827 13832 2-s2.0-0345564858 10.1073/pnas.2336100100 (Pubitemid 37499151)
53. Majka J., Burgers P. M., Function of Rad17/Mec3/Ddc1 and its partial complexes in the DNA damage checkpoint. DNA Repair 2005 4 10 1189 1194 2-s2.0-24944495500 10.1016/j.dnarep.2005.07.008 (Pubitemid 41316596)
54. Modesti M., Kanaar R., Dna repair: spot(light)s on chromatin. Current Biology 2001 11 6 R229 R232 2-s2.0-0035916814 10.1016/S0960-9822(01)00112-9 (Pubitemid 32241511)
55. Marteijn J. A., Bekker-Jensen S., Mailand N., Lans H., Schwertman P., Gourdin A. M., Dantuma N. P., Lukas J., Vermeulen W., Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. The Journal of Cell Biology 2009 186 6 835 847 2-s2.0-70349944658 10.1083/jcb.200902150
56. Moné M. J., Volker M., Nikaido O., Mullenders L. H. F., Van Zeeland A. A., Verschure P. J., Manders E. M. M., Van Driel R., Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Reports 2001 2 11 1013 1017 2-s2.0-0035204187 10.1093/embo-reports/kve224 (Pubitemid 33130608)
57. Volker M., Moné M. J., Karmakar P., Van Hoffen A., Schul W., Vermeulen W., Hoeijmakers J. H. J., Van Driel R., Van Zeeland A. A., Mullenders L. H. F., Sequential assembly of the nucleotide excision repair factors in vivo. Molecular Cell 2001 8 1 213 224 2-s2.0-17944361949 10.1016/S1097-2765(01)00281- 7 (Pubitemid 32772919)
58. Moné M. J., Bernas T., Dinant C., Goedvree F. A., Manders E. M. M., Volker M., Houtsmuller A. B., Hoeijmakers J. H. J., Vermeulen W., Van Driel R., In vivo dynamics of chromatin-associated complex formation in mammalian nucleotide excision repair. Proceedings of the National Academy of Sciences of the United States of America 2004 101 45 15933 15937 2-s2.0-8644219594 10.1073/pnas.0403664101 (Pubitemid 39507905)
59. Mari P.-O., Florea B. I., Persengiev S. P., Verkaik N. S., Brüggenwirth H. T., Modesti M., Giglia-Mari G., Bezstarosti K., Demmers J. A. A., Luider T. M., Houtsmuller A. B., Van Gent D. C., Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proceedings of the National Academy of Sciences of the United States of America 2006 103 49 18597 18602 2-s2.0-33845484385 10.1073/pnas.0609061103 (Pubitemid 44913456)
60. Aten J. A., Stap J., Krawczyk P. M., Van Oven C. H., Hoebe R. A., Essers J., Kanaar R., Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 2004 303 5654 92 95 2-s2.0-0347988236 10.1126/science.1088845 (Pubitemid 38055778)
61. Stap J., Krawczyk P. M., Van Oven C. H., Barendsen G. W., Essers J., Kanaar R., Aten J. A., Induction of linear tracks of DNA double-strand breaks by α -particle irradiation of cells. Nature Methods 2008 5 3 261 266 2-s2.0-40149095090 10.1038/nmeth.f.206 (Pubitemid 351325651)
62. Williams E. S., Stap J., Essers J., Ponnaiya B., Luijsterburg M. S., Krawczyk P. M., Ullrich R. L., Aten J. A., j.a.aten@amc.uva.nl Bailey S. M., sbailey@colostate.edu DNA double-strand breaks are not sufficient to initiate recruitment of TRF2. Nature Genetics 2007 39 6 696 698 2-s2.0-33646117239 10.1038/ng0607-696 (Pubitemid 46848575)
63. Houtsmuller A. B., Fluorescence recovery after photobleaching: application to nuclear proteins. Advances in Biochemical Engineering/ Biotechnology 2005 95 177 199 2-s2.0-23944459610 10.1007/b102214 (Pubitemid 44617141)
64. Houtsmuller A. B., Vermeulen W., Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochemistry and Cell Biology 2001 115 1 13 21 2-s2.0-0035106336 (Pubitemid 32202049)
65. Stroppolo M. E., Falconi M., Caccuri A. M., Desideri A., Superefficient enzymes. Cellular and Molecular Life Sciences 2001 58 10 1451 1460 2-s2.0-0034793812 (Pubitemid 32964415)
66. Ricard J., Cornish-Bowden A., Co-operative and allosteric enzymes: 20 years on. European Journal of Biochemistry 1987 166 2 255 272 2-s2.0-0023655481
67. Zou L., Elledge S. J., Sensing and signaling DNA damage: roles of Rad17 and Rad9 complexes in the cellular response to DNA damage. Harvey Lectures 2001 97 1 15 2-s2.0-0642283646
68. Hanahan D., Weinberg R. A., The hallmarks of cancer. Cell 2000 100 1 57 70 2-s2.0-0034614637 (Pubitemid 30046295)
69. Doré A. S., Kilkenny M. L., Rzechorzek N. J., Pearl L. H., Crystal structure of the rad9-rad1-hus1 DNA damage checkpoint complex - implications for clamp loading and regulation. Molecular Cell 2009 34 6 735 745 2-s2.0-67649111979 10.1016/j.molcel.2009.04.027
70. Abraham R. T., Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes and Development 2001 15 17 2177 2196 2-s2.0-0035449355 10.1101/gad.914401 (Pubitemid 32843830)
71. Kumagai A., Lee J., Yoo H. Y., Dunphy W. G., TopBP1 activates the ATR-ATRIP complex. Cell 2006 124 5 943 955 2-s2.0-33644757806 10.1016/j.cell.2005.12.041 (Pubitemid 43344235)
72. Smits V. A. J., Spreading the signal: dissociation of Chk1 from chromatin. Cell Cycle 2006 5 10 1039 1043 2-s2.0-33646819704 (Pubitemid 43765295)
73. van Royen M. E., Farla P., Mattern K. A., Geverts B., Trapman J., Houtsmuller A. B., Fluorescence recovery after photobleaching (FRAP) to study nuclear protein dynamics in living cells. Methods in Molecular Biology 2009 464 363 385
74. Giglia-Mari G., Theil A. F., Mari P.-O., Mourgues S., Nonnekens J., Andrieux L. O., De Wit J., Miquel C., Wijgers N., Maas A., Fousteri M., Hoeijmakers J. H. J., Vermeulen W., Differentiation driven changes in the dynamic organization of basal transcription initiation. PLoS Biology 2009 7 10, article e1000220 2-s2.0-70350518308 10.1371/journal.pbio.1000220
75. Tan T. L. R., Essers J., Citterio E., Swagemakers S. M. A., De Wit J., Benson F. E., Hoeijmakers J. H. J., Kanaar R., Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Current Biology 1999 9 6 325 328 2-s2.0-0033602450 10.1016/S0960-9822(99)80142-0 (Pubitemid 29181840)