Rad54B targeting to DNA double-strand break repair sites requires complex formation with S100A11

Molecular Biology of the Cell

Volumn 19, Issue 7, 2008, Pages 2926-2935

  Murzik, Ulrike ^a   Hemmerich, Peter ^b   Weidtkamp Peters, Stefanie ^b,d   Ulbricht, Tobias ^b   Bussen, Wendy ^c,e   Hentschel, Julia ^a   Von Eggeling, Ferdinand ^a   Melle, Christian ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b FRITZ LIPMANN INSTITUTE   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; CALCIUM BINDING PROTEIN; DOUBLE STRANDED DNA; PROTEIN RAD54B; PROTEIN S100A11; RAD54 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL DAMAGE; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

APOPTOSIS; CELL CYCLE; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA HELICASES; DNA REPAIR; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; MICROSCOPY, CONFOCAL; NUCLEAR PROTEINS; PROTEOMICS; RECOMBINATION, GENETIC; S100 PROTEINS;

EID: 51349138301     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-11-1167     Document Type: Article

References (55)

1. Aliouat-Denis, C. M. et al. (2005). p53-independent regulation of p21Waf1/Cip1 expression and senescence by Chk2. Mol. Cancer Res. 3, 627-634.
2. Amaudeau, C., Lundin, C., and Helleday, T. (2001). DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 307, 1235-1245.
3. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M. B., Bartek, J., and Lukas, J. (2006). Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173, 195-206.
4. Bisotto, S., Lauriault, P., Duval, M., and Vincent, M. (1995). Colocalization of a high molecular mass phosphoprotein of the nuclear matrix (p255) with spliceosomes. J. Cell Sci. 108, 1873-1882.
5. 2+ binding S100 proteins in normal human skin and melanocytic lesions. Br. J. Dermatol. 137, 39-43.
6. Boukamp, P., Petrussevska, R. T., Breitkreutz, D., Hornung, J., Markham, A., and Fusenig, N. E. (1988). Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771.
7. Bouquet, F., Muller, C., and Salles, B. (2006). The loss of gammaH2AX signal is a marker of DNA double strand breaks repair only at low levels of DNA damage. Cell Cycle 5, 1116-1122.
8. Broome, A. M., Ryan, D., and Eckert, R. L. (2003). S100 protein subcellular localization during epidermal differentiation and psoriasis. J. Histochem. Cytochem. 51, 675-685.
9. Chai, B., Huang, J., Cairns, B. R., and Laurent, B. C. (2005). Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19, 1656-1661.
10. Chaurand, P., DaGue, B. B., Pearsall, R. S., Threadgill, D. W., and Caprioli, R. M. (2001). Strain-based sequence variations and structure analysis of murine prostate specific spermine binding protein using mass spectrometry. Proteomics 1, 1320-1326.
11. Chen, C. R., Wang, W., Rogoff, H. A., Li, X., Mang, W., and Li, C. J. (2005). Dual induction of apoptosis and senescence in cancer cells by Chk2 activation: checkpoint activation as a strategy against cancer. Cancer Res. 65, 6017-6021.
12. Donato, R. (2001). S100, a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 33, 637-668.
13. Dulic, V., Kaufmann, W. K., Wilson, S. J., Tlsty, T. D., Lees, E., Harper, J. W., Elledge, S. J., and Reed, S. I. (1994). p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76, 1013-1023.
14. Eckert, R. L., Broome, A. M., Ruse, M., Robinson, N., Ryan, D., and Lee, K. (2004). S100 proteins in the epidermis. J. Invest. Dermatol. 123, 23-33.
15. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. P., Parson, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. (1993). WAF1, a potential mediator of p53. Cell 75, 817-825.
16. Escher, N., Kob, R., Tenbaum, S. P., Eisold, M., Baniahmad, A., von Eggeling, F., and Melle, C. (2007). Various members of the E2F transcription factor family interact in vivo with the corepressor Alien. J. Proteome Res. 6, 1158-1164.
17. Fang, Z., Fu, Y., Liang, Y., Li, Z., Zhang, W., Jin, J., Yang, Y., and Zha, X. (2007). Increased expression of integrin beta1 subunit enhances p21(WAF1/Cip1) transcription through the Sp1 sites and p300-mediated histone acetylation in human hepatocellular carcinoma cells. J. Cell. Biochem. 101, 654-664.
18. Gartel, A. L., and Tyner, A. L. (1999). Transcriptional regulation of the p21(WAF1/CIP1) gene. Exp. Cell Res. 246, 280-289.
19. Gartel, A. L., and Tyner, A. L. (2002). The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol. Cancer Ther. 1, 639-649.
20. Hoeijmakers, J. H. (2001). Genome maintenance mechanisms for preventing cancer. Nature 411, 366-374.
21. Inada, H., Naka, M., Tanaka, T., Davey, G. E., and Heizmann, C. W. (1999). Human S100A11 exhibits differential steady-state RNA levels in various tissues and a distinct subcellular localization. Biochem. Biophys. Res. Commun. 263, 135-138.
22. Kegel, P., Riballo, E., Kühne, M., Jeggo, P. A., and Löbrich, M. (2007). X-irradiation of cells on glass slides has a dose doubling impact. DNA Repair 6, 1692-1697.
23. Kob, R., Baniahmad, A., Escher, N., von Eggeling, F., and Melle, C. (2007). Detection and identification of transcription factors as interaction partners of Alien in vivo. Cell Cycle 6, 393-396.
24. Lehman, T. A. et al. (1993). p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 14, 833-839.
25. Lehmann, R., Melle, C., Escher, N., and von Eggeling, F. (2005). Detection and identification of protein interactions of S100 proteins by ProteinChip technology. J. Proteome Res. 4, 1717-1721.
26. Lettier, G., Feng, Q., de Mayolo, A. A., Erdinez, N., Reid, R. J., Lisby, M., Mortensen, U. H., and Rothstein, R. (2006). The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet. 2, e194.
27. Manders, E.M.M., Verbeek, F. J., and Aten, J. A. (1993). Measurement of co-localization of objects in dual color confocal images. J. Microscopy 169, 375-382.
28. Markova, E., Schultz, N., and Belyaev, I. Y. (2007). Kinetics and dose-response of residual 53BP1/gamma-H2AX foci: xo-localization, relationship with DSB repair and clonogenic survival. Int. J. Radiat. Biol. 83, 319-329.
29. Melle, C., Ernst, G., Schimmel, B., Bleul, A., Mothes, H., Settmacher, U., and von Eggeling, F. (2006). Different expression of calgizzarin (S100A11) in normal colonic epithelium, adenoma and colorectal carcinoma. Int. J. Oncol. 28, 195-200.
30. Miyagawa, K., Tsuruga, T., Kinomura, A., Usui, K., Katsura, M., Tashiro, S., Mishima, H., and Tanaka, K. (2002). A role for RAD54B in homologous recombination in human cells. EMBO J. 21, 175-180.
31. Mogi, S., and Oh, D. H. (2006). gamma-H2AX formation in response to interstrand crosslinks requires XPF in human cells. DNA Repair 5, 731-740.
32. Otterlei, M., Bruheim, P., Ahn, B., Bussen, W., Karmakar, P., Bayton, K., and Bohr, V. A. (2006). Werner syndrome protein participates in a complex with RAD51, RAD54, RAD54B and ATR in response to ICL-induced replication arrest. J. Cell Sci. 119, 5137-5146.
33. Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M., and Bonner, W. M. (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10, 886-895.
34. Raderschall, E. et al. (2002). Formation of higher-order nuclear Rad51 structures is functionally linked to p21 expression and protection from DNA damage-induced apoptosis. J. Cell Sci. 115, 153-164.
35. Rogakou, E. P., Pilch, D. R., Orr, O. H., Ivanova, V. S., and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868.
36. Rogakou, E. P., Boon, C., Redon, C., and Bonner, W. M. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146, 905-916.
37. Rogakou, E. P., Nieves-Neira, W., Boon, C., Pommier, Y., and Bonner, W. M. (2000). Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J. Biol. Chem. 275, 9390-9395.
38. Rosenberger, S., Thorey, I. S., Werner, S., and Boukamp, P. (2007). A novel regulator of telomerase. S100A8 mediates differentiation-dependent and calcium-induced inhibition of telomerase activity in the human epidermal keratinocyte line HaCaT. J. Biol. Chem. 282, 6126-6135.
39. Sakaguchi, M., Miyazaki, M., Inoue, Y., Tsuji, T., Kouchi, H., Tanaka, T., Yamada, H., and Namba, M. (2000). Relationship between contact inhibition and intranuclear S100C of normal human fibroblasts. J. Cell Biol. 149, 1193-1206.
40. 2+-induced growth inhibition of human epidermal keratinocytes. J. Cell Biol. 163, 825-835.
41. Sakaguchi, M., Miyazaki, M., Sonegawa, H., Kashiwagi, M., Ohba, M., Kuroki, T., Namba, M., and Huh, N. H. (2004). PKCα mediates TGFβ-induced growth inhibition of human keratinocytes via phosphorylation of S100C/A11. J. Cell Biol. 164, 979-984.
42. Sakaguchi, M., Sonegawa, H., Murata, H., Kitazoe, M., Futami, J. I., Kataoka, K., Yamada, H., and Huh, N. H. (2008). S100A11, a dual mediator for growth regulation of human keratinocytes. Mol. Biol. Cell 19, 78-85.
43. Sarai, N., Kugawa, W., Kinebuchi, T., Kagawa, A., Tanaka, K., Miyagawa, K., Ikawa, S., Shibata, T., Kurumizaka, H., and Yokoyama, S. (2006). Stimulation of Dmc1-mediated DNA strand exchange by the human Rad54B protein. Nucleic Acids Res. 34, 4429-4437.
44. Schafer, B. W., and Heizmann, C. W. (1996). The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem. Sci. 21, 134-140.
45. Sedelnikova, O. A., Horikawa, I., Zimonjic, D. B., Popescu, N. C., Bonner, W. M., and Barrett, J. C. (2004). Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol. 6, 168-170.
46. Sehorn, M. G., Sigurdsson, S., Bussen, W., Unger, V. M., and Sung, P. (2004). Human meiotic recombinase DMC1 promotes ATP-dependent homologous DNA strand exchange. Nature 429, 433-437.
47. Somanathan, S., Suchyna, T. M., Siegel, A. J., Berezney, R. (2001). Targeting of PCNA to sites of DNA replication in the mammalian cell nucleus. J. Cell. Biochem. 81, 56-67.
48. Tanaka, K., Kagawa, W., Kinebuchi, T., Kurumizaka, H., H., and Miyagawa, K. (2002). Human Rad54B is a double-stranded DNA-dependent ATPase and has biochemical properties different from its structural homolog in yeast, Tid1/Rdh54. Nucleic Acids Res. 30, 1346-1353.
49. Tsuda, M., Watanabe, T., Seki, T., Kimura, T., Sawa, H., Minami, A., Akagi, T., Isobe, K., Nagashima, K., and Tanaka, S. (2005). Induction of p21(WAF1/CIP1) by human synovial sarcoma-associated chimeric oncoprotein SYTSSX1. Oncogene 24, 7984-7990.
50. van Ginkel, R. P., Gee, R. L., Walker, T. M., Hu, D. N., Weizmann, C. W., and Polans, A. S. (1998). The identification and differential expression of calcium-binding proteins associated with ocular melanoma. Biochim. Biophys. Acta 1448, 290-297.
51. von Mikecz, A., Zhang, S., Montminy, M., Tan, E. M., and Hemmerich, P. (2000). CREB-binding protein (CBP)/p300 and RNA polymerase II colocalize in transcriptionally active domains in the nucleus. J. Cell Biol. 150, 265-273.
52. Wesoly, J. et al. (2006). Different contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol. Cell. Biol. 26, 976-989.
53. Wolner, B., van Komen, S., Sung, P., and Peterson, C. L. (2003). Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12, 221-232.
54. 1 checkpoint in keratinocytes. Mol. Cell. Biol. 24, 10650-10660.
55. Xhao, X. O., Naka, M., Muneyuki, M., and Tanaka, T. (2000). Ca(2+)-dependent inhibition of actin-activated myosin ATPase activity by S100C (S100A11), a novel member of the S100 protein family. Biochem. Biophys. Res. Commun. 267, 77-79.