Abstract
The phenomenon of association of transcribed genes into so-called transcription factories and also the role of these associations in spatial organization of the eukaryotic genome are actively discussed in the modern literature. Some authors think that the association of transcribed genes into transcription factories constitutes a major factor supporting the function-dependent three-dimensional organization of the interphase genome. In spite of the obvious interest in the prob- lem of spatial organization of transcription in the eukaryotic cell nucleus, the number of experimental studies of transcrip- tional factories remains rather limited and the results of these studies are often contradictory. In the current review we have tried to critically re-evaluate the published experimental results that constitute the basis for current models and also the models themselves. We have especially analyzed the existing contradictions and attempted to explain them whenever possi- ble. We also discuss new models that can explain the biological significance of clustering of transcribed genes and show pos- sible mechanisms of the origin of transcription factories in the course of evolution.
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Miller, O. L., Jr., and Beatty, B. R. (1969) Science, 164, 955–957.
Hozak, P., Cook, P. R., Schofer, C., Mosgoller, W., and Wachtler, F. (1994) J. Cell. Sci., 107, 639–648.
Jackson, D. A., McCready, S. J., and Cook, P. R. (1981) Nature, 292, 552–555.
Razin, S. V., and Yarovaya, O. V. (1985) Exp. Cell Res., 158, 273–275.
Cook, P. R. (1989) Eur. J. Biochem., 185, 487–501.
Mirkovitch, J., Mirault, M.-E., and Laemmli, U. K. (1984) Cell, 39, 223–232.
Jackson, D. A., Dickinson, P., and Cook, P. R. (1990) Nucleic Acids Res., 18, 4385–4393.
Jackson, D. A., and Cook, P. R. (1985) EMBO J., 4, 919–925.
Cook, P. R., and Gove, F. (1992) Nucleic Acids Res., 20, 3591–3598.
Iborra, F. J., Pombo, A., McManus, J., Jackson, D. A., and Cook, P. R. (1996) Exp. Cell. Res., 229, 167–173.
Jackson, D. A., Hassan, A. B., Errington, R. J., and Cook, P. R. (1993) EMBO J., 12, 1059–1065.
Wansink, D. G., Schul, W., van der Kraan, I., van Steensel, B., van Driel, R., and de Jong, L. (1993) J. Cell. Biol., 122, 283–293.
Bregman, D. B., Du, L., van der Zee, S., and Warren, S. L. (1995) J. Cell. Biol., 129, 287–298.
Grande, M. A., van der Kraan, I., de Jong, L., and van Driel, R. (1997) J. Cell. Sci., 110, 1781–1791.
Hozak, P., Hassan, A. B., Jackson, D. A., and Cook, P. R. (1993) Cell, 73, 361–373.
Iborra, F. J., Pombo, A., Jackson, D. A., and Cook, P. R. (1996) J. Cell. Sci., 109, 1427–1436.
Jackson, D. A., Iborra, F. J., Manders, E. M., and Cook, P. R. (1998) Mol. Biol. Cell., 9, 1523–1536.
Mitchell, J. A., and Fraser, P. (2008) Genes Dev., 22, 20–25.
Hieda, M., Winstanley, H., Maini, P., Iborra, F. J., and Cook, P. R. (2005) Chromosome Res., 13, 135–144.
Kimura, H., Sugaya, K., and Cook, P. R. (2002) J. Cell. Biol., 159, 777–782.
Osborne, C. S., Chakalova, L., Brown, K. E., Carter, D., Horton, A., Debrand, E., Goyenechea, B., Mitchell, J. A., Lopes, S., Reik, W., and Fraser, P. (2004) Nat. Genet., 36, 1065–1071.
Osborne, C. S., Chakalova, L., Mitchell, J. A., Horton, A., Wood, A. L., Bolland, D. J., Corcoran, A. E., and Fraser, P. (2007) PLoS Biol., 5, e192.
Ragoczy, T., Bender, M. A., Telling, A., Byron, R., and Groudine, M. (2006) Genes Dev., 20, 1447–1457.
Schoenfelder, S., Sexton, T., Chakalova, L., Cope, N. F., Horton, A., Andrews, S., Kurukuti, S., Mitchell, J. A., Umlauf, D., Dimitrova, D. S., Eskiw, C. H., Luo, Y., Wei, C. L., Ruan, Y., Bieker, J. J., and Fraser, P. (2010) Nat. Genet., 42, 53–61.
Levsky, J. M., Shenoy, S. M., Chubb, J. R., Hall, C. B., Capodieci, P., and Singer, R. H. (2007) J. Cell. Biochem., 102, 609–617.
Levsky, J. M., Shenoy, S. M., Pezo, R. C., and Singer, R. H. (2002) Science, 297, 836–840.
Levsky, J. M., and Singer, R. H. (2003) Trends Cell. Biol., 13, 4–6.
Zhou, G. L., Xin, L., Song, W., Di, L. J., Liu, G., Wu, X. S., Liu, D. P., and Liang, C. C. (2006) Mol. Cell. Biol., 26, 5096–5105.
Chuang, C. H., Carpenter, A. E., Fuchsova, B., Johnson, T., de Lanerolle, P., and Belmont, A. S. (2006) Curr. Biol., 16, 825–831.
Brown, J. M., Leach, J., Reittie, J. E., Atzberger, A., Lee- Prudhoe, J., Wood, W. G., Higgs, D. R., Iborra, F. J., and Buckle, V. J. (2006) J. Cell. Biol., 172, 177–187.
Brown, J. M., Green, J., das Neves, R. P., Wallace, H. A., Smith, A. J., Hughes, J., Gray, N., Taylor, S., Wood, W. G., Higgs, D. R., Iborra, F. J., and Buckle, V. J. (2008) J. Cell. Biol., 182, 1083–1097.
Razin, S. V., and Gromova, I. I. (1995) Bioessays, 17, 443–450.
Martin, S., Failla, A. V., Spori, U., Cremer, C., and Pombo, A. (2004) Mol. Biol. Cell, 15, 2449–2455.
Cremer, T., Kurz, A., Zirbel, R., Dietzel, S., Rinke, B., Schrock, E., Speicher, M. R., Mathieu, U., Jauch, A., Emmerich, P., Scherthan, H., Ried, T., Cremer, C., and Lichter, P. (1993) Cold Spring Harb. Symp. Quant. Biol., 58, 777–792.
Bolzer, A., Kreth, G., Solovei, I., Koehler, D., Saracoglu, K., Fauth, C., Muller, S., Eils, R., Cremer, C., Speicher, M. R., and Cremer, T. (2005) PLoS Biol., 3, e157.
Tanabe, H., Habermann, F. A., Solovei, I., Cremer, M., and Cremer, T. (2002) Mutat. Res., 504, 37–45.
Gilbert, N., Gilchrist, S., and Bickmore, W. A. (2005) Int. Rev. Cytol., 242, 283–336.
Xu, M., and Cook, P. R. (2008) J. Cell. Biol., 181, 615–623.
Bartlett, J., Blagojevic, J., Carter, D., Eskiw, C., Fromaget, M., Job, C., Shamsher, M., Trindade, I. F., Xu, M., and Cook, P. R. (2006) Biochem. Soc. Symp., 67–75.
Fraser, P., and Bickmore, W. (2007) Nature, 447, 413–417.
Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002) Science, 295, 1306–1311.
De Laat, W., and Grosveld, F. (2003) Chromosome Res., 11, 447–459.
Kooren, J., Palstra, R. J., Klous, P., Splinter, E., von Lindern, M., Grosveld, F., and de Laat, W. (2007) J. Biol. Chem., 282, 16544–16552.
Splinter, E., Grosveld, F., and de Laat, W. (2004) Meth. Enzymol., 375, 493–507.
Zhao, Z., Tavoosidana, G., Sjolinder, M., Gondor, A., Mariano, P., Wang, S., Kanduri, C., Lezcano, M., Sandhu, K. S., Singh, U., Pant, V., Tiwari, V., Kurukuti, S., and Ohlsson, R. (2006) Nat. Genet., 38, 1341–1347.
Dostie, J., Richmond, T. A., Arnaout, R. A., Selzer, R. R., Lee, W. L., Honan, T. A., Rubio, E. D., Krumm, A., Lamb, J., Nusbaum, C., Green, R. D., and Dekker, J. (2006) Genome Res., 16, 1299–1309.
Tolhuis, B., Palstra, R. J., Splinter, E., Grosveld, F., and de Laat, W. (2002) Mol. Cell, 10, 1453–1465.
Palstra, R. J., Tolhuis, B., Splinter, E., Nijmeijer, R., Grosveld, F., and de Laat, W. (2003) Nat. Genet., 35, 190–194.
Noordermeer, D., and de Laat, W. (2008) IUBMB Life, 60, 824–833.
Schoenfelder, S., Clay, I., and Fraser, P. (2010) Curr. Opin. Genet. Dev., 20, 127–133.
Sexton, T., Umlauf, D., Kurukuti, S., and Fraser, P. (2007) Semin. Cell. Dev. Biol., 18, 691–697.
Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., van Steensel, B., and de Laat, W. (2006) Nat. Genet., 38, 1348–1354.
Lercher, M. J., Blumenthal, T., and Hurst, L. D. (2003) Genome Res., 13, 238–243.
Caron, H., van Schaik, B., van der Mee, M., Baas, F., Riggins, G., van Sluis, P., Hermus, M. C., van Asperen, R., Boon, K., Voute, P. A., Heisterkamp, S., van Kampen, A., and Versteeg, R. (2001) Science, 291, 1289–1292.
Spellman, P. T., and Rubin, G. M. (2002) J. Biol., 1, 5.
Boutanaev, A. M., Kalmykova, A. I., Shevelyov, Y. Y., and Nurminsky, D. I. (2002) Nature, 420, 666–669.
Lercher, M. J., Urrutia, A. O., and Hurst, L. D. (2002) Nat. Genet., 31, 180–183.
Li, Q., Lee, B. T., and Zhang, L. (2005) BMC Genomics, 6, 7.
Kalmykova, A. I., Nurminsky, D. I., Ryzhov, D. V., and Shevelyov, Y. Y. (2005) Nucleic Acids Res., 33, 1435–1444.
Paillisson, A., Dade, S., Callebaut, I., Bontoux, M., Dalbies-Tran, R., Vaiman, D., and Monget, P. (2005) BMC Genomics, 6, 76.
Yager, T. D., Dempsey, A. A., Tang, H., Stamatiou, D., Chao, S., Marshall, K. W., and Liew, C. C. (2004) Genomics, 84, 524–535.
Eskiw, C. H., Rapp, A., Carter, D. R., and Cook, P. R. (2008) J. Cell. Sci., 121, 1999–2007.
Jackson, D. A. (1997) Mol. Biol. Rep., 24, 209–220.
Kaufmann, S. H., Coffey, D. S., and Shaper, J. H. (1981) Exp. Cell. Res., 132, 105–123.
Kaufmann, S. H., and Shaper, J. H. (1991) Exp. Cell. Res., 192, 511–523.
Neri, L. M., Raymond, Y., Giordano, A., Borgatti, P., Marchisio, M., Capitani, S., and Martelli, A. M. (1999) J. Cell. Biochem., 75, 36–45.
Hancock, R. (2004) Biol. Cell, 96, 595–601.
Lawrence, J. B., and Singer, R. H. (1991) Semin. Cell. Biol., 2, 83–101.
Berezney, R., Mortillaro, M. J., Ma, H., Wei, X., and Samarabandu, J. (1995) Int. Rev. Cytol., 162A, 1–65.
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Original Russian Text © S. V. Razin, A. A. Gavrilov, O. V. Yarovaya, 2010, published in Biokhimiya, 2010, Vol. 75, No. 11, pp. 1477–1488.
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Razin, S.V., Gavrilov, A.A. & Yarovaya, O.V. Transcription Factories and Spatial Organization of Eukaryotic Genomes. Biochemistry Moscow 75, 1307–1315 (2010). https://doi.org/10.1134/S0006297910110015
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DOI: https://doi.org/10.1134/S0006297910110015