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Biochemistry (Moscow)

, Volume 77, Issue 13, pp 1409–1423 | Cite as

Domains of α- and β-globin genes in the context of the structural-functional organization of the eukaryotic genome

  • S. V. RazinEmail author
  • S. V. Ulianov
  • E. S. Ioudinkova
  • E. S. Gushchanskaya
  • A. A. Gavrilov
  • O. V. Iarovaia
Review

Abstract

The eukaryotic cell genome has a multilevel regulatory system of gene expression that includes stages of preliminary activation of genes or of extended genomic regions (switching them to potentially active states) and stages of final activation of promoters and maintaining their active status in cells of a certain lineage. Current views on the regulatory systems of transcription in eukaryotes have been formed based on results of systematic studies on a limited number of model systems, in particular, on the α- and β-globin gene domains of vertebrates. Unexpectedly, these genomic domains harboring genes responsible for the synthesis of different subunits of the same protein were found to have a fundamentally different organization inside chromatin. In this review, we analyze specific features of the organization of the α- and β-globin gene domains in vertebrates, as well as principles of activities of the regulatory systems in these domains. In the final part of the review, we attempt to answer the question how the evolution of α- and β-globin genes has led to segregation of these genes into two distinct types of chromatin domains situated on different chromosomes.

Key words

α- and β-globin genes genomic domains transcription regulation globin gene evolution 

Abbreviations

α-MRE

Major Regulatory Element of α-globin gene domain

DHS(s)

DNase I Hypersensitivity Site(s)

LCR

Locus Control Region

MCS

Multispecies Conserved Sequence

OR

Olfactory Receptor gene

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References

  1. 1.
    Razin, S. V., Iarovaia, O. V., Sjakste, N., Sjakste, T., Bagdoniene, L., Rynditch, A. V., Eivazova, E. R., Lipinski, M., and Vassetzky, Y. S. (2007) J. Mol. Biol., 369, 597–607.PubMedGoogle Scholar
  2. 2.
    Bodnar, J. W. (1988) J. Theor. Biol., 132, 479–507.PubMedGoogle Scholar
  3. 3.
    Goldman, M. A. (1988) Bioessays, 9, 50–55.PubMedGoogle Scholar
  4. 4.
    Weintraub, H., and Groudine, M. (1976) Science, 73, 848–856.Google Scholar
  5. 5.
    Forrester, W. C., Thompson, C., Elder, J. T., and Groudine, M. (1986) Proc. Natl. Acad. Sci. USA, 83, 1359–1363.PubMedGoogle Scholar
  6. 6.
    Lawson, G. M., Knoll, B. J., March, C. J., Woo, S. L. C., Tsai, M.-J., and O’Malley, B. W. (1982) J. Biol. Chem., 257, 1501–1507.PubMedGoogle Scholar
  7. 7.
    Krajewski, W. A., and Becker, P. B. (1998) Proc. Natl. Acad. Sci. USA, 95, 1540–1545.PubMedGoogle Scholar
  8. 8.
    Anguita, E., Johnson, C. A., Wood, W. G., Turner, B. M., and Higgs, D. R. (2001) Proc. Natl. Acad. Sci. USA, 98, 12114–12119.PubMedGoogle Scholar
  9. 9.
    Kellum, R., and Schedl, P. (1992) Mol. Cell. Biol., 12, 2424–2431.PubMedGoogle Scholar
  10. 10.
    Felsenfeld, G., Burgess-Beusse, B., Farrell, C., Gaszner, M., Ghirlando, R., Huang, S., Jin, C., Litt, M., Magdinier, F., Mutskov, V., Nakatani, Y., Tagami, H., West, A., and Yusufzai, T. (2004) Cold Spring Harb. Symp. Quant. Biol., 69, 245–250.PubMedGoogle Scholar
  11. 11.
    Wallace, J. A., and Felsenfeld, G. (2007) Curr. Opin. Genet. Dev., 17, 400–407.PubMedGoogle Scholar
  12. 12.
    Forrester, W. C., Epner, E., Driscoll, M. C., Enver, T., Brice, M., Papayannopoulou, T., and Groudine, M. (1990) Genes Dev., 4, 1637–1649.PubMedGoogle Scholar
  13. 13.
    Grosveld, F., van Assandelt, G. B., Greaves, D. R., and Kollias, B. (1987) Cell, 51, 975–985.PubMedGoogle Scholar
  14. 14.
    Razin, S. V., Farrell, C. M., and Recillas-Targa, F. (2003) Int. Rev. Cytol., 226, 63–125.PubMedGoogle Scholar
  15. 15.
    Craddock, C. F., Vyas, P., Sharpe, J. A., Ayyub, H., Wood, W. G., and Higgs, D. R. (1995) EMBO J., 14, 1718–1726.PubMedGoogle Scholar
  16. 16.
    Flint, J., Tufarelli, C., Peden, J., Clark, K., Daniels, R. J., Hardison, R., Miller, W., Philipsen, S., Tan-Un, K. C., McMorrow, T., Frampton, J., Alter, B. P., Frischauf, A. M., and Higgs, D. R. (2001) Hum. Mol. Genet., 10, 371–382.PubMedGoogle Scholar
  17. 17.
    Makalowska, I., Lin, C. F., and Makalowski, W. (2005) Comput. Biol. Chem., 29, 1–12.PubMedGoogle Scholar
  18. 18.
    Dillon, N., and Sabbatini, P. (2000) Bioessays, 22, 657–665.PubMedGoogle Scholar
  19. 19.
    Forget, B. G. (1998) Ann. N. Y. Acad. Sci., 850, 38–44.PubMedGoogle Scholar
  20. 20.
    Bulger, M., Bender, M., Farrell, C., Felsenfeld, G., Wertman, B., Groudine, M., and Hardison, R. (2000) Blood Cells Mol. Dis., 26, 490.Google Scholar
  21. 21.
    Schubeler, D., Francastel, C., Cimbora, D. M., Reik, A., Martin, D. I. K., and Groudine, M. (2000) Genes Dev., 14, 940–950.PubMedGoogle Scholar
  22. 22.
    Hanscombe, O., Whyatt, D., Fraser, P., Yannoutsos, N., Greaves, D., Dillon, N., and Grosveld, F. (1991) Genes Dev., 5, 1387–1394.PubMedGoogle Scholar
  23. 23.
    Hebbes, T. R., Clayton, A. L., Thorne, A. W., and Crane-Robinson, C. (1994) EMBO J., 13, 1823–1830.PubMedGoogle Scholar
  24. 24.
    Prioleau, M.-N., Nony, P., Simpson, M., and Felsenfeld, G. (1999) EMBO J., 18, 4035–4048.PubMedGoogle Scholar
  25. 25.
    Guerrero, G., Delgado-Olguin, P., Escamilla-Del-Arenal, M., Furlan-Magaril, M., Rebollar, E., De La Rosa-Velazquez, I. A., Soto-Reyes, E., Rincon-Arano, H., Valdes-Quezada, C., Valadez-Graham, V., and Recillas-Targa, F. (2007) Comp. Biochem. Physiol. A. Mol. Integr. Physiol., 147, 750–760.PubMedGoogle Scholar
  26. 26.
    Geyer, P. K. (1997) Curr. Opin. Genet. Dev., 7, 242–248.PubMedGoogle Scholar
  27. 27.
    West, A. G., Gaszner, M., and Felsenfeld, G. (2002) Genes Dev., 16, 271–288.PubMedGoogle Scholar
  28. 28.
    Chung, J. H., Whiteley, M., and Felsenfeld, G. (1993) Cell, 74, 505–514.PubMedGoogle Scholar
  29. 29.
    Recillas-Targa, F., Pikaart, M. J., Burgess-Beusse, B., Bell, A. C., Litt, M. D., West, A. G., Gaszner, M., and Felsenfeld, G. (2002) Proc. Natl. Acad. Sci. USA, 99, 6883–6888.PubMedGoogle Scholar
  30. 30.
    Chung, J. H., Bell, A. C., and Felsenfeld, G. (1997) Proc. Natl. Acad. Sci. USA, 94, 575–580.PubMedGoogle Scholar
  31. 31.
    Bell, A. C., West, A. G., and Felsenfeld, G. (1999) Cell, 98, 387–396.PubMedGoogle Scholar
  32. 32.
    Wendt, K. S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T., Yahata, K., Imamoto, F., Aburatani, H., Nakao, M., Imamoto, N., Maeshima, K., Shirahige, K., and Peters, J. M. (2008) Nature, 451, 796–801.PubMedGoogle Scholar
  33. 33.
    Xiao, T., Wallace, J., and Felsenfeld, G. (2011) Mol. Cell. Biol., 31, 2174–2183.PubMedGoogle Scholar
  34. 34.
    Huang, S., Li, X., Yusufzai, T. M., Qiu, Y., and Felsenfeld, G. (2007) Mol. Cell. Biol., 27, 7991–8002.PubMedGoogle Scholar
  35. 35.
    Li, X., Wang, S., Li, Y., Deng, C., Steiner, L. A., Xiao, H., Wu, C., Bungert, J., Gallagher, P. G., Felsenfeld, G., Qiu, Y., and Huang, S. (2011) Blood, 118, 1386–1394.PubMedGoogle Scholar
  36. 36.
    Saitoh, N., Bell, A. C., Recillas-Targa, F., West, A. G., Simpson, M., Pikaart, M., and Felsenfeld, G. (2000) EMBO J., 19, 2315–2322.PubMedGoogle Scholar
  37. 37.
    Farrell, C. M., West, A. G., and Felsenfeld, G. (2002) Mol. Cell. Biol., 22, 3820–3831.PubMedGoogle Scholar
  38. 38.
    Li, Q., and Stamatoyannopoulos, G. (1994) Blood, 84, 1399–1401.PubMedGoogle Scholar
  39. 39.
    Tanimoto, K., Liu, Q., Bungert, J., and Engel, J. D. (1999) Nature, 398, 344–348.PubMedGoogle Scholar
  40. 40.
    Li, Q., Zhang, M., Han, H., Rohde, A., and Stamatoyannopoulos, G. (2002) Nucleic Acids Res., 30, 2484–2491.PubMedGoogle Scholar
  41. 41.
    Talbot, D., Collis, P., Antoniou, M., Vidal, M., Grosveld, F., and Greaves, D. R. (1989) Nature, 338, 352–355.PubMedGoogle Scholar
  42. 42.
    Li, G., Lim, K. C., Engel, J. D., and Bungert, J. (1998) Genes Cells, 3, 415–429.PubMedGoogle Scholar
  43. 43.
    Cimbora, D. M., Schubeler, D., Reik, A., Hamilton, J., Francastel, C., Epner, E. M., and Groudine, M. (2000) Mol. Cell. Biol., 20, 5581–5591.PubMedGoogle Scholar
  44. 44.
    Philipsen, S., Talbot, D., Fraser, P., and Grosveld, F. (1990) EMBO J., 9, 2159–2167.PubMedGoogle Scholar
  45. 45.
    Ney, P. A., Sorrentino, B. P., McDonagh, K. T., and Nienhuis, A. W. (1990) Genes Dev., 4, 993–1006.PubMedGoogle Scholar
  46. 46.
    Strauss, E. C., and Orkin, S. H. (1992) Proc. Natl. Acad. Sci. USA, 89, 5809–5813.PubMedGoogle Scholar
  47. 47.
    Lowrey, C. H., Bodine, D. M., and Nienhuis, A. W. (1992) Proc. Natl. Acad. Sci. USA, 89, 1143–1147.PubMedGoogle Scholar
  48. 48.
    Stamatoyannopoulos, G., Goodwin, A., Joyce, T., and Lowrey, C. H. (1995) EMBO J., 14, 106–116.PubMedGoogle Scholar
  49. 49.
    Li, Q., Zhou, B., Powers, P., Enver, T., and Stamatoyannopoulos, G. (1990) Proc. Natl. Acad. Sci. USA, 87, 8207–8211.PubMedGoogle Scholar
  50. 50.
    Mason, M. M., Lee, E., Westphal, H., and Reitman, M. (1995) Mol. Cell. Biol., 15, 407–414.PubMedGoogle Scholar
  51. 51.
    Hardison, R., Slightom, J. L., Gumicio, D. L., Goodman, M., Stojanovic, N., and Miller, W. (1997) Gene, 205, 73–94.PubMedGoogle Scholar
  52. 52.
    Bulger, M., and Groudine, M. (1999) Genes Dev., 13, 2465–2477.PubMedGoogle Scholar
  53. 53.
    Peterson, K. R., and Stamatoyannopoulos, G. (1993) Mol. Cell. Biol., 13, 4836–4843.PubMedGoogle Scholar
  54. 54.
    Dillon, N., Trimborn, T., Stronboulis, J., Fraser, P., and Grosveld, F. (1997) Mol. Cell, 1, 131–139.PubMedGoogle Scholar
  55. 55.
    Wijgerde, M., Grosveld, F., and Fraser, P. (1995) Nature, 377, 209–213.PubMedGoogle Scholar
  56. 56.
    Gribnau, J., de Boer, E., Trimborn, T., Wijgerde, M., Milot, E., Grosveld, F., and Fraser, P. (1998) EMBO J., 17, 6020–6027.PubMedGoogle Scholar
  57. 57.
    Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002) Science, 295, 1306–1311.PubMedGoogle Scholar
  58. 58.
    De Laat, W., and Grosveld, F. (2003) Chromosome Res., 11, 447–459.PubMedGoogle Scholar
  59. 59.
    Tolhuis, B., Palstra, R. J., Splinter, E., Grosveld, F., and de Laat, W. (2002) Mol. Cell, 10, 1453–1465.PubMedGoogle Scholar
  60. 60.
    West, A. G., and Fraser, P. (2005) Hum. Mol. Genet., 14, 101–111.Google Scholar
  61. 61.
    De Laat, W., Klous, P., Kooren, J., Noordermeer, D., Palstra, R. J., Simonis, M., Splinter, E., and Grosveld, F. (2008) Curr. Top. Dev. Biol., 82, 117–139.PubMedGoogle Scholar
  62. 62.
    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.PubMedGoogle Scholar
  63. 63.
    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.PubMedGoogle Scholar
  64. 64.
    Armstrong, J. A., Bieker, J. J., and Chen, X. (1998) Cell, 95, 93–104.PubMedGoogle Scholar
  65. 65.
    Blobel, G. (2000) Blood, 95, 745–755.PubMedGoogle Scholar
  66. 66.
    Bresnick, E. H., and Tze, L. (1997) Proc. Natl. Acad. Sci. USA, 94, 4566–4571.PubMedGoogle Scholar
  67. 67.
    Forsberg, E. C., Johnson, K., Zaboikina, T. N., Mosser, E. A., and Bresnick, E. H. (1999) J. Biol. Chem., 274, 26850–26859.PubMedGoogle Scholar
  68. 68.
    Gribnau, G., Diderich, K., Pruzina, S., Calzolari, R., and Frazer, P. (2000) Mol. Cell, 5, 377–386.PubMedGoogle Scholar
  69. 69.
    Wilson, C. J., Chao, D. M., Imbalzano, A. N., Schnitzler, G. R., Kingston, R. E., and Yong, R. A. (1996) Cell, 84, 235–244.PubMedGoogle Scholar
  70. 70.
    Cho, H., Orphanides, G., Sun, X., Yang, X. J., Ogryzko, V., Lees, E., Nakatani, Y., and Reinberg, D. (1998) Mol. Cell. Biol., 18, 5355–5363.PubMedGoogle Scholar
  71. 71.
    Travers, A. (1999) Proc. Natl. Acad. Sci. USA, 96, 13634–13637.PubMedGoogle Scholar
  72. 72.
    Herendeen, D. R., Kassavetis, G. A., and Geiduschek, E. P. (1992) Science, 256, 1298–1303.PubMedGoogle Scholar
  73. 73.
    Forsberg, E. C., and Bresnick, E. H. (2001) Bioessays, 23, 820–830.PubMedGoogle Scholar
  74. 74.
    Hughes, J. R., Cheng, J. F., Ventress, N., Prabhakar, S., Clark, K., Anguita, E., De Gobbi, M., de Jong, P., Rubin, E., and Higgs, D. R. (2005) Proc. Natl. Acad. Sci. USA, 102, 9830–9835.PubMedGoogle Scholar
  75. 75.
    Tufarelli, C., Hardison, R., Miller, W., Hughes, J., Clark, K., Ventress, N., Frischauf, A. M., and Higgs, D. R. (2004) Genome Res., 14, 623–630.PubMedGoogle Scholar
  76. 76.
    Klochkov, D. B., Gavrilov, A. A., Vassetzky, Y. S., and Razin, S. V. (2009) Genomics, 93, 481–486.PubMedGoogle Scholar
  77. 77.
    Tufarelli, C., Frischauf, A. M., Hardison, R., Flint, J., and Higgs, D. R. (2001) Genomics, 71, 307–314.PubMedGoogle Scholar
  78. 78.
    Neklesa, T. K., and Davis, R. W. (2009) PLoS Genet., 5, e1000515.PubMedGoogle Scholar
  79. 79.
    Higgs, D. R., Wood, W. G., Jarman, A. P., Sharpe, J., Lida, J., Pretorius, I.-M., and Ayyub, H. (1990) Genes Dev., 4, 1588–1601.PubMedGoogle Scholar
  80. 80.
    Viprakasit, V., Harteveld, C. L., Ayyub, H., Stanley, J. S., Giordano, P. C., Wood, W. G., and Higgs, D. R. (2006) Blood, 107, 3811–3812.PubMedGoogle Scholar
  81. 81.
    Jarman, A. P., Wood, W. G., Sharpe, J. A., Gourdon, G., Ayyub, H., Higgs, and D. R. (1991) Mol. Cell. Biol., 11, 4679–4689.PubMedGoogle Scholar
  82. 82.
    Anguita, E., Sharpe, J. A., Sloane-Stanley, J. A., Tufarelli, C., Higgs, D. R., and Wood, W. G. (2002) Blood, 100, 3450–3456.PubMedGoogle Scholar
  83. 83.
    Chen, H., Lowrey, C. H., and Stamatoyannopoulos, G. (1997) Nucleic Acids Res., 25, 2917–2922.PubMedGoogle Scholar
  84. 84.
    De Gobbi, M., Anguita, E., Hughes, J., Sloane-Stanley, J. A., Sharpe, J. A., Koch, C. M., Dunham, I., Gibbons, R. J., Wood, W. G., and Higgs, D. R. (2007) Blood, 110, 4503–4510.PubMedGoogle Scholar
  85. 85.
    Igarashi, K., Itoh, K., Hayashi, N., Nishizawa, M., and Yamamoto, M. (1995) Proc. Natl. Acad. Sci. USA, 92, 7445–7449.PubMedGoogle Scholar
  86. 86.
    Knezetic, J., and Felsenfeld, G. (1989) Mol. Cell. Biol., 9, 893–901.PubMedGoogle Scholar
  87. 87.
    Philonenko, E. S., Klochkov, D. B., Borunova, V. V., Gavrilov, A. A., Razin, S. V., and Iarovaia, O. V. (2009) Nucleic Acids Res., 37, 7394–7406.PubMedGoogle Scholar
  88. 88.
    Razin, S. V., Kekelidze, M. G., Lukanidin, E. M., Scherrer, K., and Georgiev, G. P. (1986) Nucleic Acids Res., 14, 8189–8207.PubMedGoogle Scholar
  89. 89.
    Klochkov, D., Rincon-Arano, H., Ioudinkova, E. S., Valadez-Graham, V., Gavrilov, A., Recillas-Targa, F., and Razin, S. V. (2006) Mol. Cell. Biol., 26, 1589–1597.PubMedGoogle Scholar
  90. 90.
    Razin, S. V., Ioudinkova, E. S., and Scherrer, K. (2000) J. Mol. Biol., 209, 845–852.Google Scholar
  91. 91.
    Valadez-Graham, V., Razin, S. V., and Recillas-Targa, F. (2004) Nucleic Acids Res., 32, 1354–1362.PubMedGoogle Scholar
  92. 92.
    Furlan-Magaril, M., Rebollar, E., Guerrero, G., Fernandez, A., Molto, E., Gonzalez-Buendia, E., Cantero, M., Montoliu, L., and Recillas-Targa, F. (2011) Nucleic Acids Res., 39, 89–103.PubMedGoogle Scholar
  93. 93.
    Razin, S. V., Rynditch, A., Borunova, V., Ioudinkova, E., Smalko, V., and Scherrer, K. (2004) J. Cell. Biochem., 92, 445–457.PubMedGoogle Scholar
  94. 94.
    Gavrilov, A. A., and Razin, S. V. (2008) Nucleic Acids Res., 36, 4629–4640.PubMedGoogle Scholar
  95. 95.
    Vernimmen, D., De Gobbi, M., Sloane-Stanley, J. A., Wood, W. G., and Higgs, D. R. (2007) EMBO J., 26, 2041–2051.PubMedGoogle Scholar
  96. 96.
    Vernimmen, D., Marques-Kranc, F., Sharpe, J. A., Sloane-Stanley, J. A., Wood, W. G., Wallace, H. A., Smith, A. J., and Higgs, D. R. (2009) Blood, 114, 4253–4260.PubMedGoogle Scholar
  97. 97.
    Gavrilov, A. A., Zukher, I. S., Philonenko, E. S., Razin, S. V., and Iarovaia, O. V. (2010) Nucleic Acids Res., 38, 8051–8060.PubMedGoogle Scholar
  98. 98.
    Anguita, E., Hughes, J., Heyworth, C., Blobel, G. A., Wood, W. G., and Higgs, D. R. (2004) EMBO J., 23, 2841–2852.PubMedGoogle Scholar
  99. 99.
    Pal, S., Cantor, A. B., Johnson, K. D., Moran, T. B., Boyer, M. E., Orkin, S. H., and Bresnick, E. H. (2004) Proc. Natl. Acad. Sci. USA, 101, 980–985.PubMedGoogle Scholar
  100. 100.
    Liebhaber, S. A., Wang, Z., Cash, F. E., Monks, B., and Russell, J. E. (1996) Mol. Cell. Biol., 16, 2637–2646.PubMedGoogle Scholar
  101. 101.
    Knezetic, J. A., and Felsenfeld, G. (1993) Mol. Cell. Biol., 13, 4632–4639.PubMedGoogle Scholar
  102. 102.
    Singal, R., vanWert, J. M., and Ferdinand, L., Jr. (2002) Blood, 100, 4217–4222.PubMedGoogle Scholar
  103. 103.
    Sabath, D. E., Spangler, E. A., Rubin, E. M., and Stamatoyannopoulos, G. (1993) Blood, 82, 2899–2905.PubMedGoogle Scholar
  104. 104.
    Ioudinkova, E. S., Ulianov, S. V., Bunina, D., Iarovaia, O. V., Gavrilov, A. A., and Razin, S. V. (2011) Epigenetics, 6, 1481–1488.PubMedGoogle Scholar
  105. 105.
    Tang, Y., Wang, Z., Huang, Y., Liu, D. P., Liu, G., Shen, W., Tang, X., Feng, D., and Liang, C. C. (2006) Genes Cells, 11, 123–131.PubMedGoogle Scholar
  106. 106.
    Whitelaw, E., Hogben, P., Hanscombe, O., and Proudfoot, N. J. (1989) Mol. Cell. Biol., 9, 241–251.PubMedGoogle Scholar
  107. 107.
    Garrick, D., De Gobbi, M., Samara, V., Rugless, M., Holland, M., Ayyub, H., Lower, K., Sloane-Stanley, J., Gray, N., Koch, C., Dunham, I., and Higgs, D. R. (2008) Blood, 112, 3889–3899.PubMedGoogle Scholar
  108. 108.
    Lynch, M. D., Smith, A. J., De Gobbi, M., Flenley, M., Hughes, J. R., Vernimmen, D., Ayyub, H., Sharpe, J. A., Sloane-Stanley, J. A., Sutherland, L., Meek, S., Burdon, T., Gibbons, R. J., Garrick, D., and Higgs, D. R. (2011) EMBO J., Nov 4. doi: 10.1038/emboj.2011.399.Google Scholar
  109. 109.
    Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Gough, J., Dewilde, S., Moens, L., and Vanfleteren, J. R. (2006) BMC Evol. Biol., 6, 31.PubMedGoogle Scholar
  110. 110.
    Hoffmann, F. G., Opazo, J. C., and Storz, J. F. (2012) Mol. Biol. Evol., in press.Google Scholar
  111. 111.
    Maruyama, K., Yasumasu, S., Naruse, K., Mitani, H., Shima, A., and Iuchi, I. (2004) Gene, 335, 89–100.PubMedGoogle Scholar
  112. 112.
    Fuchs, C., Burmester, T., and Hankeln, T. (2006) Cytogenet. Genome Res., 112, 296–306.PubMedGoogle Scholar
  113. 113.
    Chan, F. Y., Robinson, J., Brownlie, A., Shivdasani, R. A., Donovan, A., Brugnara, C., Kim, J., Lau, B. C., Witkowska, H. E., and Zon, L. I. (1997) Blood, 89, 688–700.PubMedGoogle Scholar
  114. 114.
    Brownlie, A., Hersey, C., Oates, A. C., Paw, B. H., Falick, A. M., Witkowska, H. E., Flint, J., Higgs, D., Jessen, J., Bahary, N., Zhu, H., Lin, S., and Zon, L. (2003) Dev. Biol., 255, 48–61.PubMedGoogle Scholar
  115. 115.
    Jeffreys, A. J., Wilson, V., Wood, D., Simons, J. P., Kay, R. M., and Williams, J. G. (1980) Cell, 21, 555–564.PubMedGoogle Scholar
  116. 116.
    Wheeler, D., Hope, R. M., Cooper, S. J., Gooley, A. A., and Holland, R. A. (2004) J. Mol. Evol., 58, 642–652.PubMedGoogle Scholar
  117. 117.
    Wheeler, D., Hope, R., Cooper, S. B., Dolman, G., Webb, G. C., Bottema, C. D., Gooley, A. A., Goodman, M., and Holland, R. A. (2001) Proc. Natl. Acad. Sci. USA, 98, 1101–1106.PubMedGoogle Scholar
  118. 118.
    Patel, V. S., Cooper, S. J., Deakin, J. E., Fulton, B., Graves, T., Warren, W. C., Wilson, R. K., and Graves, J. A. (2008) BMC Biol., 6, 34.PubMedGoogle Scholar
  119. 119.
    Chong, S., Riggs, A. D., and Bonifer, C. (2002) Nucleic Acids Res., 30, 463–467.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  • S. V. Razin
    • 1
    • 2
    Email author
  • S. V. Ulianov
    • 2
  • E. S. Ioudinkova
    • 1
  • E. S. Gushchanskaya
    • 1
    • 2
  • A. A. Gavrilov
    • 1
    • 3
  • O. V. Iarovaia
    • 1
  1. 1.Institute of Gene BiologyRussian Academy of SciencesMoscowRussia
  2. 2.Biological FacultyLomonosov Moscow State UniversityMoscowRussia
  3. 3.Oslo University Medical Research Center in RussiaMoscowRussia

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