Biochemistry (Moscow)

, Volume 76, Issue 1, pp 131–146 | Cite as

Mutator effects and mutation signatures of editing deaminases produced in bacteria and yeast

  • A. G. Lada
  • C. Frahm Krick
  • S. G. Kozmin
  • V. I. Mayorov
  • T. S. Karpova
  • I. B. Rogozin
  • Y. I. PavlovEmail author


Enzymatic deamination of bases in DNA or RNA leads to an alteration of flow of genetic information. Adenosine deaminases edit RNA (ADARs, TADs). Specialized cytidine deaminases are involved in RNA/DNA editing in lipid metabolism (APOBEC1) and in innate (APOBEC3 family) and humoral (AID) immunity. APOBEC2 is required for proper muscle development and, along with AID, was implicated in demethylation of DNA. The functions of APOBEC4, APOBEC5, and other deaminases recently discovered by bioinformatics approaches are unknown. What is the basis for the diverse biological functions of enzymes with similar enzyme structure and the same principal enzymatic reaction? AID, APOBEC1, lamprey CDA1, and APOBEC3G enzymes cause uracil DNA glycosylase-dependent induction of mutations when overproduced ectopically in bacteria or yeast. APOBEC2, on the contrary, is nonmutagenic. We studied the effects of the expression of various deaminases in yeast and bacteria. The mutagenic specificities of four deaminases, hAID, rAPOBEC1, hAPOBEC3G, and lamprey CDA1, are strikingly different. This suggests the existence of an intrinsic component of deaminase targeting. The expression of yeast CDD1 and TAD2/TAD3, human APOBEC4, Xanthomonas oryzae APOBEC5, and deaminase encoded by Micromonas sp. gene MICPUN_56782 was nonmutagenic. A lack of a mutagenic effect for Cdd1 is expected because the enzyme functions in the salvage of pyrimidine nucleotides, and it is evolutionarily distant from RNA/DNA editing enzymes. The reason for inactivity of deaminases grouped with APOBEC2 is not obvious from their structures. This cannot be explained by protein insolubility and peculiarities of cellular distribution and requires further investigation.

Key words

editing deaminases mutagenesis immunity DNA repair 



adenosine deaminase


activation induced deaminase


apurinic/apyrimidinic nuclease


apolipoprotein B editase complex related enzyme


site, apurinic/apyrimidinic site


cytidine deaminase or various organisms


class switch recombination


gene conversion


green fluorescent protein


human immunodeficiency virus




Luria-Bertani medium


lithium dodecyl sulfate


leucine-rich repeats


endonuclease five


nuclear localization signal


open reading frame


Pteromyzon marinus cytidine deaminase


synthetic medium for yeast cultivation


sodium dodecyl sulfate


somatic hypermutation


tRNA adenosine deaminase


uracil-N-glycosylase or uracil-DNA-glycosylase


virus infectivity factor


variable lymphocyte receptors


complete medium for yeast cultivation


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

10541_2011_9364_MOESM1_ESM.pdf (129 kb)
Supplementary material, approximately 128 KB.


  1. 1.
    Hayaishi, O., and Kornberg, A. (1952) J. Biol. Chem., 197, 717–732.PubMedGoogle Scholar
  2. 2.
    Kornberg, A., and Baker, T. A. (1992) DNA Replication, W. H. Freeman, New York.Google Scholar
  3. 3.
    Sugiyama, E., Lee, S. J., Lee, S. S., Kim, W. Y., Kim, S. R., Tohkin, M., Hasegawa, R., Okuda, H., Kawamoto, M., Kamatani, N., Sawada, J., Kaniwa, N., Saito, Y., and Shin, J. G. (2009) Drug Metab. Pharmacokinet., 24, 553–556.PubMedCrossRefGoogle Scholar
  4. 4.
    Sauer, A. V., and Aiuti, A. (2009) Curr. Opin. Allergy Clin. Immunol., 9, 496–502.PubMedCrossRefGoogle Scholar
  5. 5.
    Pankratova, E. V., and Stepchenko, A. G. (2010) Genetika, 46, 5–13.PubMedGoogle Scholar
  6. 6.
    Neuberger, M. S., Harris, R. S., Di Noia, J., and Petersen-Mahrt, S. K. (2003) Trends Biochem. Sci., 28, 305–312.PubMedCrossRefGoogle Scholar
  7. 7.
    Harris, R. S., and Liddament, M. T. (2004) Nat. Rev. Immunol., 4, 868–877.PubMedCrossRefGoogle Scholar
  8. 8.
    Samaranayake, M., Bujnicki, J. M., Carpenter, M., and Bhagwat, A. S. (2006) Chem. Rev., 106, 700–719.PubMedCrossRefGoogle Scholar
  9. 9.
    Deng, W. (2010) Bioessays, 32, 385–387.PubMedCrossRefGoogle Scholar
  10. 10.
    Popp, C., Dean, W., Feng, S., Cokus, S. J., Andrews, S., Pellegrini, M., Jacobsen, S. E., and Reik, W. (2010) Nature, 463, 1101–1105.PubMedCrossRefGoogle Scholar
  11. 11.
    Teng, B., Burant, C. F., and Davidson, N. O. (1993) Science, 260, 1816–1819.PubMedCrossRefGoogle Scholar
  12. 12.
    Morrison, J. R., Paszty, C., Stevens, M. E., Hughes, S. D., Forte, T., Scott, J., and Rubin, E. M. (1996) Proc. Natl. Acad. Sci. USA, 93, 7154–7159.PubMedCrossRefGoogle Scholar
  13. 13.
    Milstein, C., and Rada, C. (1995) The Maturation of Immune Response, Academic Press, London.Google Scholar
  14. 14.
    Kinoshita, K., and Honjo, T. (2001) Nat. Rev. Mol. Cell Biol., 2, 493–503.PubMedCrossRefGoogle Scholar
  15. 15.
    Rogozin, I. B., and Kolchanov, N. A. (1992) Biochim. Biophys. Acta, 1171, 11–18.PubMedGoogle Scholar
  16. 16.
    Rogozin, I. B., Pavlov, Y. I., Bebenek, K., Matsuda, T., and Kunkel, T. A. (2001) Nat. Immunol., 2, 530–536.PubMedCrossRefGoogle Scholar
  17. 17.
    Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. (2000) Cell, 102, 553–563.PubMedCrossRefGoogle Scholar
  18. 18.
    Revy, P., Muto, T., Levy, Y., Geissmann, F., Plebani, A., Sanal, O., Catalan, N., Forveille, M., Dufourcq-Labelouse, R., Gennery, A., Tezcan, I., Ersoy, F., Kayserili, H., Ugazio, A. G., Brousse, N., Muramatsu, M., Notarangelo, L. D., Kinoshita, K., Honjo, T., Fischer, A., and Durandy, A. (2000) Cell, 102, 565–575.PubMedCrossRefGoogle Scholar
  19. 19.
    Durandy, A., and Honjo, T. (2001) Curr. Opin. Immunol., 13, 543–548.PubMedCrossRefGoogle Scholar
  20. 20.
    Yoshikawa, K., Okazaki, I. M., Eto, T., Kinoshita, K., Muramatsu, M., Nagaoka, H., and Honjo, T. (2002) Science, 296, 2033–2036.PubMedCrossRefGoogle Scholar
  21. 21.
    Okazaki, I. M., Kinoshita, K., Muramatsu, M., Yoshikawa, K., and Honjo, T. (2002) Nature, 416, 340–345.PubMedCrossRefGoogle Scholar
  22. 22.
    Arakawa, H., Hauschild, J., and Buerstedde, J. M. (2002) Science, 295, 1301–1306.PubMedCrossRefGoogle Scholar
  23. 23.
    Di Noia, J. M., and Neuberger, M. S. (2004) Eur. J. Immunol., 34, 504–508.PubMedCrossRefGoogle Scholar
  24. 24.
    Petersen-Mahrt, S. K., Harris, R. S., and Neuberger, M. S. (2002) Nature, 418, 99–103.PubMedCrossRefGoogle Scholar
  25. 25.
    Poltoratsky, V., Goodman, M. F., and Scharff, M. D. (2000) J. Exp. Med., 192, F27–30.PubMedCrossRefGoogle Scholar
  26. 26.
    Pavlov, Y. I., Rogozin, I. B., Galkin, A. P., Aksenova, A. Y., Hanaoka, F., Rada, C., and Kunkel, T. A. (2002) Proc. Natl. Acad. Sci. USA, 99, 9954–9959.PubMedCrossRefGoogle Scholar
  27. 27.
    Rada, C., Williams, G. T., Nilsen, H., Barnes, D. E., Lindahl, T., and Neuberger, M. S. (2002) Curr. Biol., 12, 1748–1755.PubMedCrossRefGoogle Scholar
  28. 28.
    Pham, P., Bransteitter, R., Petruska, J., and Goodman, M. F. (2003) Nature, 424, 103–107.PubMedCrossRefGoogle Scholar
  29. 29.
    Lada, A. G., Iyer, L. M., Rogozin, I. B., Aravind, L., and Pavlov, Iu. I. (2007) Genetika, 43, 1311–1327.PubMedGoogle Scholar
  30. 30.
    Pancer, Z., Amemiya, C. T., Ehrhardt, G. R., Ceitlin, J., Gartland, G. L., and Cooper, M. D. (2004) Nature, 430, 174–180.PubMedCrossRefGoogle Scholar
  31. 31.
    Alder, M. N., Rogozin, I. B., Iyer, L. M., Glazko, G. V., Cooper, M. D., and Pancer, Z. (2005) Science, 310, 1970–1973.PubMedCrossRefGoogle Scholar
  32. 32.
    Rogozin, I. B., Iyer, L. M., Liang, L., Glazko, G. V., Liston, V. G., Pavlov, Y. I., Aravind, L., and Pancer, Z. (2007) Nat. Immunol., 8, 647–656.PubMedCrossRefGoogle Scholar
  33. 33.
    Sheehy, A. M., Gaddis, N. C., Choi, J. D., and Malim, M. H. (2002) Nature, 418, 646–650.PubMedCrossRefGoogle Scholar
  34. 34.
    Sheehy, A. M., Gaddis, N. C., and Malim, M. H. (2003) Nat. Med., 9, 1404–1407; Epub 2003 Oct 1405.PubMedCrossRefGoogle Scholar
  35. 35.
    Harris, R. S., Petersen-Mahrt, S. K., and Neuberger, M. S. (2002) Mol. Cell, 10, 1247–1253.PubMedCrossRefGoogle Scholar
  36. 36.
    Lecossier, D., Bouchonnet, F., Clavel, F., and Hance, A. J. (2003) Science, 300, 1112.PubMedCrossRefGoogle Scholar
  37. 37.
    Yu, Q., Konig, R., Pillai, S., Chiles, K., Kearney, M., Palmer, S., Richman, D., Coffin, J. M., and Landau, N. R. (2004) Nat. Struct. Mol. Biol., 11, 435–442.PubMedCrossRefGoogle Scholar
  38. 38.
    Harris, R. S., Bishop, K. N., Sheehy, A. M., Craig, H. M., Petersen-Mahrt, S. K., Watt, I. N., Neuberger, M. S., and Malim, M. H. (2003) Cell, 113, 803–809.PubMedCrossRefGoogle Scholar
  39. 39.
    Chelico, L., Pham, P., Calabrese, P., and Goodman, M. F. (2006) Nat. Struct. Mol. Biol., 13, 392–399.PubMedCrossRefGoogle Scholar
  40. 40.
    Coker, H. A., and Petersen-Mahrt, S. K. (2007) DNA Repair (Amst), 6, 235–243.CrossRefGoogle Scholar
  41. 41.
    Stenglein, M. D., and Harris, R. S. (2006) J. Biol. Chem., 281, 16837–16841.PubMedCrossRefGoogle Scholar
  42. 42.
    Chiu, Y. L., and Greene, W. C. (2006) J. Biol. Chem., 281, 8309–8312.PubMedCrossRefGoogle Scholar
  43. 43.
    Yu, K., Huang, F. T., and Lieber, M. R. (2004) J. Biol. Chem., 279, 6496–6500; Epub 2003 Nov 6425.PubMedCrossRefGoogle Scholar
  44. 44.
    Beale, R. C., Petersen-Mahrt, S. K., Watt, I. N., Harris, R. S., Rada, C., and Neuberger, M. S. (2004) J. Mol. Biol., 337, 585–596.PubMedCrossRefGoogle Scholar
  45. 45.
    Rausch, J. W., Chelico, L., Goodman, M. F., and Le Grice, S. F. (2009) J. Biol. Chem., 284, 7047–7058.PubMedCrossRefGoogle Scholar
  46. 46.
    Carpenter, M. A., Rajagurubandara, E., Wijesinghe, P., and Bhagwat, A. S. (2010) DNA Repair (Amst), 9, 579–587.CrossRefGoogle Scholar
  47. 47.
    Holden, L. G., Prochnow, C., Chang, Y. P., Bransteitter, R., Chelico, L., Sen, U., Stevens, R. C., Goodman, M. F., and Chen, X. S. (2008) Nature, 456, 121–124.PubMedCrossRefGoogle Scholar
  48. 48.
    Harjes, E., Gross, P. J., Chen, K. M., Lu, Y., Shindo, K., Nowarski, R., Gross, J. D., Kotler, M., Harris, R. S., and Matsuo, H. (2009) J. Mol. Biol., 389, 819–832.PubMedCrossRefGoogle Scholar
  49. 49.
    Prochnow, C., Bransteitter, R., Klein, M. G., Goodman, M. F., and Chen, X. S. (2007) Nature, 445, 447–451.PubMedCrossRefGoogle Scholar
  50. 50.
    Autore, F., Bergeron, J. R., Malim, M. H., Fraternali, F., and Huthoff, H. (2010) PLoS One, 5, e11515.PubMedCrossRefGoogle Scholar
  51. 51.
    Sato, Y., Probst, H. C., Tatsumi, R., Ikeuchi, Y., Neuberger, M. S., and Rada, C. (2010) J. Biol. Chem., 285, 7111–7118.PubMedCrossRefGoogle Scholar
  52. 52.
    Etard, C., Roostalu, U., and Strahle, U. (2010) J. Cell Biol., 189, 527–539.PubMedCrossRefGoogle Scholar
  53. 53.
    Rai, K., Huggins, I. J., James, S. R., Karpf, A. R., Jones, D. A., and Cairns, B. R. (2008) Cell, 135, 1201–1212.PubMedCrossRefGoogle Scholar
  54. 54.
    Rubio, M. A., Pastar, I., Gaston, K. W., Ragone, F. L., Janzen, C. J., Cross, G. A., Papavasiliou, F. N., and Alfonzo, J. D. (2007) Proc. Natl. Acad. Sci. USA, 104, 7821–7826; Epub 2007 May 7821.PubMedCrossRefGoogle Scholar
  55. 55.
    Gerber, A. P., and Keller, W. (1999) Science, 286, 1146–1149.PubMedCrossRefGoogle Scholar
  56. 56.
    Johansson, E., Mejlhede, N., Neuhard, J., and Larsen, S. (2002) Biochemistry, 41, 2563–2570.PubMedCrossRefGoogle Scholar
  57. 57.
    Huthoff, H., and Malim, M. H. (2005) Virology, 334, 147–153.PubMedCrossRefGoogle Scholar
  58. 58.
    Kuratani, M., Ishii, R., Bessho, Y., Fukunaga, R., Sengoku, T., Shirouzu, M., Sekine, S., and Yokoyama, S. (2005) J. Biol. Chem., 280, 16002–16008.PubMedCrossRefGoogle Scholar
  59. 59.
    Losey, H. C., Ruthenburg, A. J., and Verdine, G. L. (2006) Nat. Struct. Mol. Biol., 13, 153–159.PubMedCrossRefGoogle Scholar
  60. 60.
    Chen, K. M., Harjes, E., Gross, P. J., Fahmy, A., Lu, Y., Shindo, K., Harris, R. S., and Matsuo, H. (2008) Nature, 452, 116–119.PubMedCrossRefGoogle Scholar
  61. 61.
    Rogozin, I. B., Basu, M. K., Jordan, I. K., Pavlov, Y. I., and Koonin, E. V. (2005) Cell Cycle, 4, 1281–1285.PubMedCrossRefGoogle Scholar
  62. 62.
    Conticello, S. G., Thomas, C. J., Petersen-Mahrt, S. K., and Neuberger, M. S. (2005) Mol. Biol. Evol., 22, 367–377; Epub 2004 Oct 2020.PubMedCrossRefGoogle Scholar
  63. 63.
    Conticello, S. G., Langlois, M. A., and Neuberger, M. S. (2007) Nat. Struct. Mol. Biol., 14, 7–9.PubMedCrossRefGoogle Scholar
  64. 64.
    Zhang, K. L., Mangeat, B., Ortiz, M., Zoete, V., Trono, D., Telenti, A., and Michielin, O. (2007) PLoS One, 2, e378.PubMedCrossRefGoogle Scholar
  65. 65.
    Betts, L., Xiang, S., Short, S. A., Wolfenden, R., and Carter, C. W., Jr. (1994) J. Mol. Biol., 235, 635–656.PubMedCrossRefGoogle Scholar
  66. 66.
    Mejlhede, N., and Neuhard, J. (2000) Biochemistry, 39, 7984–7989.PubMedCrossRefGoogle Scholar
  67. 67.
    Karcher, D., and Bock, R. (2009) RNA, 15, 1251–1257.PubMedCrossRefGoogle Scholar
  68. 68.
    Salone, V., Rudinger, M., Polsakiewicz, M., Hoffmann, B., Groth-Malonek, M., Szurek, B., Small, I., Knoop, V., and Lurin, C. (2007) FEBS Lett., 581, 4132–4138.PubMedCrossRefGoogle Scholar
  69. 69.
    Casadaban, M. J., and Cohen, S. N. (1980) J. Mol. Biol., 138, 179–207.PubMedCrossRefGoogle Scholar
  70. 70.
    Duncan, B. K. (1985) J. Bacteriol., 164, 689–695.PubMedGoogle Scholar
  71. 71.
    Shcherbakova, P. V., and Pavlov, Y. I. (1996) Genetics, 142, 717–726.PubMedGoogle Scholar
  72. 72.
    Calderon, I. L., Contopoulou, C. R., and Mortimer, R. K. (1984) Gene, 29, 69–76.PubMedCrossRefGoogle Scholar
  73. 73.
    Achilli, A., Matmati, N., Casalone, E., Morpurgo, G., Lucaccioni, A., Pavlov, Y. I., and Babudri, N. (2004) BMC Genet., 5, 34.PubMedCrossRefGoogle Scholar
  74. 74.
    Shcherbakova, P. V., and Kunkel, T. A. (1999) Mol. Cell Biol., 19, 3177–3183.PubMedGoogle Scholar
  75. 75.
    Kozmin, S. G., Sedletska, Y., Reynaud-Angelin, A., Gasparutto, D., and Sage, E. (2009) Nucleic Acids Res., 37, 1767–1777.PubMedCrossRefGoogle Scholar
  76. 76.
    Mayorov, V. I., Rogozin, I. B., Adkison, L. R., Frahm, C., Kunkel, T. A., and Pavlov, Y. I. (2005) BMC Immunol., 6, 10.PubMedCrossRefGoogle Scholar
  77. 77.
    Bennetzen, J. L., and Hall, B. D. (1982) J. Biol. Chem., 257, 3026–3031.PubMedGoogle Scholar
  78. 78.
    Jansen, R., Bussemaker, H. J., and Gerstein, M. (2003) Nucleic Acids Res., 31, 2242–2251.PubMedCrossRefGoogle Scholar
  79. 79.
    Karpova, T. S., Kim, M. J., Spriet, C., Nalley, K., Stasevich, T. J., Kherrouche, Z., Heliot, L., and McNally, J. G. (2008) Science, 319, 466–469.PubMedCrossRefGoogle Scholar
  80. 80.
    Chernoff, Y. O., Galkin, A. P., Lewitin, E., Chernova, T. A., Newnam, G. P., and Belenkiy, S. M. (2000) Mol. Microbiol., 35, 865–876.PubMedCrossRefGoogle Scholar
  81. 81.
    Dance, G. S., Beemiller, P., Yang, Y., Mater, D. V., Mian, I. S., and Smith, H. C. (2001) Nucleic Acids Res., 29, 1772–1780.PubMedCrossRefGoogle Scholar
  82. 82.
    Dance, G. S., Sowden, M. P., Yang, Y., and Smith, H. C. (2000) Nucleic Acids Res., 28, 424–429.PubMedCrossRefGoogle Scholar
  83. 83.
    Bransteitter, R., Pham, P., Scharff, M. D., and Goodman, M. F. (2003) Proc. Natl. Acad. Sci. USA, 100, 4102–4107.PubMedCrossRefGoogle Scholar
  84. 84.
    Poltoratsky, V. P., Wilson, S. H., Kunkel, T. A., and Pavlov, Y. I. (2004) J. Immunol., 172, 4308–4313.PubMedGoogle Scholar
  85. 85.
    Rogozin, I. B., and Pavlov, Y. I. (2003) Mutat. Res., 544, 65–85.PubMedCrossRefGoogle Scholar
  86. 86.
    Cole, C., Barber, J. D., and Barton, G. J. (2008) Nucleic Acids Res., 36, W197–201.PubMedCrossRefGoogle Scholar
  87. 87.
    Bhagwat, A. S. (2004) DNA Repair (Amst), 3, 85–89.CrossRefGoogle Scholar
  88. 88.
    Coker, H. A., Morgan, H. D., and Petersen-Mahrt, S. K. (2006) Meth. Enzymol., 408, 156–170.PubMedCrossRefGoogle Scholar
  89. 89.
    Chen, K. M., Martemyanova, N., Lu, Y., Shindo, K., Matsuo, H., and Harris, R. S. (2007) FEBS Lett., 581, 4761–4766.PubMedCrossRefGoogle Scholar
  90. 90.
    Sohail, A., Klapacz, J., Samaranayake, M., Ullah, A., and Bhagwat, A. S. (2003) Nucleic Acids Res., 31, 2990–2994.PubMedCrossRefGoogle Scholar
  91. 91.
    Rogozin, I. B., and Diaz, M. (2004) J. Immunol., 172, 3382–3384.PubMedGoogle Scholar
  92. 92.
    Schumacher, A. J., Nissley, D. V., and Harris, R. S. (2005) Proc. Natl. Acad. Sci. USA, 102, 9854–9859; Epub 2005 Jul 9856.PubMedCrossRefGoogle Scholar
  93. 93.
    Dutko, J. A., Schafer, A., Kenny, A. E., Cullen, B. R., and Curcio, M. J. (2005) Curr. Biol., 15, 661–666.PubMedCrossRefGoogle Scholar
  94. 94.
    Bransteitter, R., Pham, P., Calabrese, P., and Goodman, M. F. (2004) J. Biol. Chem., 14, 14.Google Scholar
  95. 95.
    Nowarski, R., Britan-Rosich, E., Shiloach, T., and Kotler, M. (2008) Nat. Struct. Mol. Biol., 15, 1059–1066.PubMedCrossRefGoogle Scholar
  96. 96.
    Suspene, R., Rusniok, C., Vartanian, J. P., and Wain-Hobson, S. (2006) Nucleic Acids Res., 34, 4677–4684.PubMedCrossRefGoogle Scholar
  97. 97.
    Sato, K., Izumi, T., Misawa, N., Kobayashi, T., Yamashita, Y., Ohmichi, M., Ito, M., Takaori-Kondo, A., and Koyanagi, Y. (2010) J. Virol., 84, 9546–9556.PubMedCrossRefGoogle Scholar
  98. 98.
    Chen, Z., Eggerman, T. L., Bocharov, A. V., Baranova, I. N., Vishnyakova, T. G., Csako, G., and Patterson, A. P. (2010) RNA, 16, 1040–1052.PubMedCrossRefGoogle Scholar
  99. 99.
    Pils, B., and Schultz, J. (2004) J. Mol. Biol., 340, 399–404.PubMedCrossRefGoogle Scholar
  100. 100.
    Edgell, D. R., Klenk, H. P., and Doolittle, W. F. (1997) J. Bacteriol., 179, 2632–2640.PubMedGoogle Scholar
  101. 101.
    Rogozin, I. B., Makarova, K. S., Pavlov, Y. I., and Koonin, E. V. (2008) Biol. Direct., 3, 32.PubMedCrossRefGoogle Scholar
  102. 102.
    Baranovskiy, A. G., Babayeva, N. D., Liston, V. G., Rogozin, I. B., Koonin, E. V., Pavlov, Y. I., Vassylyev, D. G., and Tahirov, T. H. (2008) Cell Cycle, 7, 3026–3036.PubMedCrossRefGoogle Scholar
  103. 103.
    Tahirov, T. H., Makarova, K. S., Rogozin, I. B., Pavlov, Y. I., and Koonin, E. V. (2009) Biol. Direct., 4, 11.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2011

Authors and Affiliations

  • A. G. Lada
    • 1
  • C. Frahm Krick
    • 1
  • S. G. Kozmin
    • 2
  • V. I. Mayorov
    • 3
  • T. S. Karpova
    • 4
  • I. B. Rogozin
    • 5
    • 6
  • Y. I. Pavlov
    • 1
    Email author
  1. 1.Eppley Institute for Research in Cancer and Allied DiseasesUniversity of Nebraska Medical CenterOmahaUSA
  2. 2.Department of Molecular Genetics and MicrobiologyDuke University Medical CenterDurhamUSA
  3. 3.Mercer University School of MedicineMaconUSA
  4. 4.Laboratory of Receptor Biology and Gene ExpressionNational Cancer Institute, Center for Cancer Research Core Imaging FacilityBethesdaUSA
  5. 5.National Center for Biotechnology Information, National Library of MedicineNational Institutes of HealthBethesdaUSA
  6. 6.Institute of Cytology and GeneticsNovosibirskRussia

Personalised recommendations