Skip to main content
Log in

Poly(A)-binding proteins: Structure, domain organization, and activity regulation

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

RNA-binding proteins are of vital importance for mRNA functioning. Among these, poly(A)-binding proteins (PABPs) are of special interest due to their participation in virtually all mRNA-dependent events that is caused by their high affinity for A-rich mRNA sequences. Apart from mRNAs, PABPs interact with many proteins, thus promoting their involvement in cellular events. In the nucleus, PABPs play a role in polyadenylation, determine the length of the poly(A) tail, and may be involved in mRNA export. In the cytoplasm, they participate in regulation of translation initiation and either protect mRNAs from decay through binding to their poly(A) tails or stimulate this decay by promoting mRNA inter-actions with deadenylase complex proteins. This review presents modern notions of the role of PABPs in mRNA-dependent events; peculiarities of regulation of PABP amount in the cell and activities are also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ARE:

AU-rich element

ARS:

adenine-rich autoregulatory sequence

Cp:

ceruloplasmin

CPE:

cytoplasmic polyadenylation element

CPEBP:

cytoplasmic polyadenylation element binding protein

CPSF:

cleavage and polyadenylation specificity factor

eIF:

eukaryotic initiation factor

EJC:

exon junction complex

eRF:

eukaryotic release factor

GAIT-element:

interferon γ-activated inhibitor of translation

hnRNP:

heterogeneous nuclear ribonucleoprotein

IFN-γ:

interferon γ

IRES:

internal ribosome entry site

MLLE:

C-terminal domain of PABP

Msi1:

Musashi 1

NMD:

nonsense mediated mRNA decay

PABPs:

poly(A)-binding proteins

Paip1/2:

PABP-interacting protein 1/2

PAM:

PABP-interacting motif

PAN2/3:

PABP-dependent poly(A)-specific ribonuclease 2/3

PAP:

poly(A) polymerase

PARN:

poly(A)-specific ribonuclease

PTC:

premature termination codon

RRM:

RNA recognition motif

TOP:

terminal oligopyrimidine track

UNR:

upstream of N-ras

UTR:

untranslated region

References

  1. Blobel, G. (1972) Biochem. Biophys. Res. Commun., 47, 88–95.

    CAS  PubMed  Google Scholar 

  2. Blobel, G. (1973) Proc. Natl. Acad. Sci. USA, 70, 924–928.

    CAS  PubMed  Google Scholar 

  3. Mangus, D. A., Evans, M. C., and Jacobson, A. (2003) Genome Biol., 4, 223.

    PubMed Central  PubMed  Google Scholar 

  4. Goss, D. J., and Kleiman, F. E. (2013) Wiley Interdiscip. Rev. RNA, 4, 167–179.

    CAS  PubMed  Google Scholar 

  5. Deo, R. C., Bonanno, J. B., Sonenberg, N., and Burley, S. K. (1999) Cell, 98, 835–845.

    CAS  PubMed  Google Scholar 

  6. Safaee, N., Kozlov, G., Noronha, A. M., Xie, J., Wilds, C. J., and Gehring, K. (2012) Mol. Cell, 48, 375–386.

    CAS  PubMed  Google Scholar 

  7. Kuhn, U., and Pieler, T. (1996) J. Mol. Biol., 256, 20–30.

    CAS  PubMed  Google Scholar 

  8. Burd, C. G., Matunis, E. L., and Dreyfuss, G. (1991) Mol. Cell Biol., 11, 3419–3424.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Khanam, T., Muddashetty, R. S., Kahvejian, A., Sonenberg, N., and Brosius, J. (2006) RNA Biol., 3, 170–177.

    CAS  PubMed  Google Scholar 

  10. Patel, G. P., and Bag, J. (2006) FEBS J., 273, 5678–5690.

    CAS  PubMed  Google Scholar 

  11. Sladic, R. T., Lagnado, C. A., Bagley, C. J., and Goodall, G. J. (2004) Eur. J. Biochem., 271, 450–457.

    CAS  PubMed  Google Scholar 

  12. Baer, B. W., and Kornberg, R. D. (1983) J. Cell Biol., 96, 717–721.

    CAS  PubMed  Google Scholar 

  13. Mullin, C., Duning, K., Barnekow, A., Richter, D., Kremerskothen, J., and Mohr, E. (2004) FEBS Lett., 576, 437–441.

    CAS  PubMed  Google Scholar 

  14. Von Der Haar, T., Ball, P. D., and McCarthy, J. E. (2000) J. Biol. Chem., 275, 30551–30555.

    Google Scholar 

  15. Wei, C. C., Balasta, M. L., Ren, J., and Goss, D. J. (1998) Biochemistry, 37, 1910–1916.

    CAS  PubMed  Google Scholar 

  16. Khaleghpour, K., Kahvejian, A., De Crescenzo, G., Roy, G., Svitkin, Y. V., Imataka, H., O’Connor-McCourt, M., and Sonenberg, N. (2001) Mol. Cell Biol., 21, 5200–5213.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Koloteva-Levine, N., Pinchasi, D., Pereman, I., Zur, A., Brandeis, M., and Elroy-Stein, O. (2004) Mol. Cell Biol., 24, 3577–3587.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Kozlov, G., Safaee, N., Rosenauer, A., and Gehring, K. (2010) J. Biol. Chem., 285, 13599–13606.

    CAS  PubMed  Google Scholar 

  19. Lessing, D., and Bonini, N. M. (2008) PLoS Biol., 6, e29.

    PubMed Central  PubMed  Google Scholar 

  20. Lu, J.-Y., Bergman, N., Sadri, N., and Schneider, R. J. (2006) RNA, 12, 883–893.

    CAS  PubMed  Google Scholar 

  21. Ilkow, C. S., Mancinelli, V., Beatch, M. D., and Hobman, T. C. (2008) J. Virol., 82, 4284–4294.

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Brune, C., Munchel, S. E., Fischer, N., Podtelejnikov, A. V., and Weis, K. (2005) RNA, 11, 517–531.

    CAS  PubMed  Google Scholar 

  23. Collier, B., Gorgoni, B., Loveridge, C., Cooke, H. J., and Gray, N. K. (2005) EMBO J., 24, 2656–2666.

    CAS  PubMed  Google Scholar 

  24. Bushell, M., Wood, W., Carpenter, G., Pain, V. M., Morley, S. J., and Clemens, M. J. (2001) J. Biol. Chem., 276, 23922–23928.

    CAS  PubMed  Google Scholar 

  25. Imataka, H., Gradi, A., and Sonenberg, N. (1998) EMBO J., 17, 7480–7489.

    CAS  PubMed  Google Scholar 

  26. Hoshino, S., Imai, M., Kobayashi, T., Uchida, N., and Katada, T. (1999) J. Biol. Chem., 274, 16677–16680.

    CAS  PubMed  Google Scholar 

  27. Uchida, N., Hoshino, S.-I., Imataka, H., Sonenberg, N., and Katada, T. (2002) J. Biol. Chem., 277, 50286–50292.

    CAS  PubMed  Google Scholar 

  28. Huntzinger, E., Braun, J. E., Heimstadt, S., Zekri, L., and Izaurralde, E. (2010) EMBO J., 29, 4146–4160.

    CAS  PubMed  Google Scholar 

  29. Hasgall, P. A., Hoogewijs, D., Faza, M. B., Panse, V. G., Wenger, R. H., and Camenisch, G. (2011) PLoS One, 6, e22107.

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Blagden, S. P., Gatt, M. K., Archambault, V., Lada, K., Ichihara, K., Lilley, K. S., Inoue, Y. H., and Glover, D. M. (2009) Dev. Biol., 334, 186–197.

    CAS  PubMed  Google Scholar 

  31. Yang, R., Gaidamakov, S. A., Xie, J., Lee, J., Martino, L., Kozlov, G., Crawford, A. K., Russo, A. N., Conte, M. R., Gehring, K., and Maraia, R. J. (2011) Mol. Cell Biol., 31, 542–556.

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Miroci, H., Schob, C., Kindler, S., Olschlager-Schutt, J., Fehr, S., Jungenitz, T., Schwarzacher, S. W., Bagni, C., and Mohr, E. (2012) J. Biol. Chem., 287, 1322–1334.

    CAS  PubMed  Google Scholar 

  33. Wang, X., Bai, J., Zhang, L., Wang, X., Li, Y., and Jiang, P. (2012) Antiviral Res., 96, 315–323.

    CAS  PubMed  Google Scholar 

  34. Roy, G., De Crescenzo, G., Khaleghpour, K., Kahvejian, A., O’Connor-McCourt, M., and Sonenberg, N. (2002) Mol. Cell Biol., 22, 3769–3782.

    CAS  PubMed Central  PubMed  Google Scholar 

  35. Berlanga, J. J., Baass, A., and Sonenberg, N. (2006) RNA, 12, 1556–1568.

    CAS  PubMed  Google Scholar 

  36. Siddiqui, N., Mangus, D. A., Chang, T.-C., Palermino, J.-M., Shyu, A.-B., and Gehring, K. (2007) J. Biol. Chem., 282, 25067–25075.

    CAS  PubMed  Google Scholar 

  37. Ezzeddine, N., Chang, T.-C., Zhu, W., Yamashita, A., Chen, C.-Y. A., Zhong, Z., Yamashita, Y., Zheng, D., and Shyu, A.-B. (2007) Mol. Cell Biol., 27, 7791–7801.

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Okochi, K., Suzuki, T., Inoue, J., Matsuda, S., and Yamamoto, T. (2005) Genes Cells, 10, 151–163.

    CAS  PubMed  Google Scholar 

  39. Chang, T.-C., Yamashita, A., Chen, C.-Y. A., Yamashita, Y., Zhu, W., Durdan, S., Kahvejian, A., Sonenberg, N., and Shyu, A.-B. (2004) Genes Dev., 18, 2010–2023.

    CAS  PubMed  Google Scholar 

  40. Lin, J., Fabian, M., Sonenberg, N., and Meller, A. (2012) Biophys. J., 102, 1427–1434.

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Melo, E. O., Dhalia, R., Martins de Sa, C., Standart, N., and De Melo Neto, O. P. (2003) J. Biol. Chem., 278, 46357–46368.

    CAS  PubMed  Google Scholar 

  42. Smith, R. W. P., and Gray, N. K. (2010) Biochem. J., 426, 1–12.

    CAS  PubMed  Google Scholar 

  43. Bonderoff, J. M., Larey, J. L., and Lloyd, R. E. (2008) J. Virol., 82, 9389–9399.

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Rivera, C. I., and Lloyd, R. E. (2008) Virology, 375, 59–72.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Kuyumcu-Martinez, N. M., Joachims, M., and Lloyd, R. E. (2002) J. Virol., 76, 2062–2074.

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Kozlov, G., De Crescenzo, G., Lim, N. S., Siddiqui, N., Fantus, D., Kahvejian, A., Trempe, J.-F., Elias, D., Ekiel, I., Sonenberg, N., O’Connor-McCourt, M., and Gehring, K. (2004) EMBO J., 23, 272–281.

    CAS  PubMed  Google Scholar 

  47. Kozlov, G., Menade, M., Rosenauer, A., Nguyen, L., and Gehring, K. (2010) J. Mol. Biol., 397, 397–407.

    CAS  PubMed  Google Scholar 

  48. Huang, K.-L., Chadee, A. B., Chen, C.-Y. A., Zhang, Y., and Shyu, A.-B. (2013) RNA, 19, 295–305.

    CAS  PubMed  Google Scholar 

  49. Kononenko, A. V., Mitkevich, V. A., Atkinson, G. C., Tenson, T., Dubovaya, V. I., Frolova, L. Y., Makarov, A. A., and Hauryliuk, V. (2010) Nucleic Acids Res., 38, 548–558.

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Keller, R. W., Kuhn, U., Aragon, M., Bornikova, L., Wahle, E., and Bear, D. G. (2000) J. Mol. Biol., 297, 569–583.

    CAS  PubMed  Google Scholar 

  51. Wahle, E., and Ruegsegger, U. (1999) FEMS Microbiol. Rev., 23, 277–295.

    CAS  PubMed  Google Scholar 

  52. Kuhn, U., Gundel, M., Knoth, A., Kerwitz, Y., Rudel, S., and Wahle, E. (2009) J. Biol. Chem., 284, 22803–22814.

    PubMed  Google Scholar 

  53. Chekanova, J. A., and Belostotsky, D. A. (2003) RNA, 9, 1476–1490.

    CAS  PubMed  Google Scholar 

  54. Lemay, J.-F., Lemieux, C., St-Andre, O., and Bachand, F. (2010) RNA Biol., 7, 291–295.

    CAS  PubMed  Google Scholar 

  55. Dunn, E. F., Hammell, C. M., Hodge, C. A., and Cole, C. N. (2005) Genes Dev., 19, 90–103.

    CAS  PubMed  Google Scholar 

  56. Hosoda, N., Lejeune, F., and Maquat, L. E. (2006) Mol. Cell Biol., 26, 3085–3097.

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Maquat, L. E., Hwang, J., Sato, H., and Tang, Y. (2010) Cold Spring Harb. Symp. Quant. Biol., 75, 127–134.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Sato, H., and Maquat, L. E. (2009) Genes Dev., 23, 2537–2550.

    CAS  PubMed  Google Scholar 

  59. Bhattacharjee, R. B., and Bag, J. (2012) PLoS One, 7, e53036.

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Richter, J. D., and Lasko, P. (2011) Cold Spring Harb. Perspect. Biol., 3, a002758.

    PubMed  Google Scholar 

  61. Darnell, J. C., and Richter, J. D. (2012) Cold Spring Harb. Perspect. Biol., 4, a012344.

    PubMed  Google Scholar 

  62. Richter, J. D. (2007) Trends Biochem. Sci., 32, 279–285.

    CAS  PubMed  Google Scholar 

  63. Kim, J. H., and Richter, J. D. (2006) Mol. Cell, 24, 173–183.

    CAS  PubMed  Google Scholar 

  64. Kuersten, S., and Goodwin, E. B. (2003) Nat. Rev. Genet., 4, 626–637.

    CAS  PubMed  Google Scholar 

  65. Tay, J., Hodgman, R., Sarkissian, M., and Richter, J. D. (2003) Genes Dev., 17, 1457–1462.

    CAS  PubMed  Google Scholar 

  66. Atkins, C. M., Nozaki, N., Shigeri, Y., and Soderling, T. R. (2004) J. Neurosci., 24, 5193–5201.

    CAS  PubMed  Google Scholar 

  67. Udagawa, T., Swanger, S. A., Takeuchi, K., Kim, J. H., Nalavadi, V., Shin, J., Lorenz, L. J., Zukin, R. S., Bassell, G. J., and Richter, J. D. (2012) Mol. Cell, 47, 253–266.

    CAS  PubMed Central  PubMed  Google Scholar 

  68. De Moor, C. H., and Richter, J. D. (1999) EMBO J., 18, 2294–2303.

    PubMed  Google Scholar 

  69. Groisman, I., Jung, M.-Y., Sarkissian, M., Cao, Q., and Richter, J. D. (2002) Cell, 109, 473–483.

    CAS  PubMed  Google Scholar 

  70. Gray, N. K., Coller, J. M., Dickson, K. S., and Wickens, M. (2000) EMBO J., 19, 4723–4733.

    CAS  PubMed  Google Scholar 

  71. Otero, L. J., Ashe, M. P., and Sachs, A. B. (1999) EMBO J., 18, 3153–3163.

    CAS  PubMed  Google Scholar 

  72. Wells, S. E., Hillner, P. E., Vale, R. D., and Sachs, A. B. (1998) Mol. Cell, 2, 135–140.

    CAS  PubMed  Google Scholar 

  73. Rajkowitsch, L., Vilela, C., Berthelot, K., Ramirez, C. V., and McCarthy, J. E. G. (2004) J. Mol. Biol., 335, 71–85.

    CAS  PubMed  Google Scholar 

  74. Kahvejian, A., Svitkin, Y. V., Sukarieh, R., M’Boutchou, M.-N., and Sonenberg, N. (2005) Genes & Development, 19, 104–113.

    CAS  Google Scholar 

  75. Borman, A. M., Michel, Y. M., Malnou, C. E., and Kean, K. M. (2002) J. Biol. Chem., 277, 36818–36824.

    CAS  PubMed  Google Scholar 

  76. Craig, A. W., Haghighat, A., Yu, A. T., and Sonenberg, N. (1998) Nature, 392, 520–523.

    CAS  PubMed  Google Scholar 

  77. Martineau, Y., Derry, M. C., Wang, X., Yanagiya, A., Berlanga, J. J., Shyu, A.-B., Imataka, H., Gehring, K., and Sonenberg, N. (2008) Mol. Cell Biol., 28, 6658–6667.

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Lim, N. S., Kozlov, G., Chang, T.-C., Groover, O., Siddiqui, N., Volpon, L., De Crescenzo, G., Shyu, A.-B., and Gehring, K. (2006) J. Biol. Chem., 281, 14376–14382.

    CAS  PubMed  Google Scholar 

  79. Yoshida, M., Yoshida, K., Kozlov, G., Lim, N. S., De Crescenzo, G., Pang, Z., Berlanga, J. J., Kahvejian, A., Gehring, K., Wing, S. S., and Sonenberg, N. (2006) EMBO J., 25, 1934–1944.

    CAS  PubMed  Google Scholar 

  80. Yanagiya, A., Delbes, G., Svitkin, Y. V., Robaire, B., and Sonenberg, N. (2010) J. Clin. Invest., 120, 3389–3400.

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Delbes, G., Yanagiya, A., Sonenberg, N., and Robaire, B. (2012) Biol. Reprod., 86, 95.

    PubMed  Google Scholar 

  82. Jacobson, A. (1996) Translational Control, Cold Spring Harbor Laboratory Press, Cold Spring Harbor,NY, 30, 451–480.

    CAS  Google Scholar 

  83. Proweller, A., and Butler, J. S. (1996) J. Biol. Chem., 271, 10859–10865.

    CAS  PubMed  Google Scholar 

  84. Searfoss, A., Dever, T. E., and Wickner, R. (2001) Mol. Cell Biol., 21, 4900–4908.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Padilla-Noriega, L., Paniagua, O., and Guzman-Leon, S. (2002) Virology, 298, 1–7.

    CAS  PubMed  Google Scholar 

  86. Piron, M., Vende, P., Cohen, J., and Poncet, D. (1998) EMBO J., 17, 5811–5821.

    CAS  PubMed  Google Scholar 

  87. Joachims, M., Van Breugel, P. C., and Lloyd, R. E. (1999) J. Virol., 73, 718–727.

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Kerekatte, V., Keiper, B. D., Badorff, C., Cai, A., Knowlton, K. U., and Rhoads, R. E. (1999) J. Virol., 73, 709–717.

    CAS  PubMed Central  PubMed  Google Scholar 

  89. Bradrick, S. S., Dobrikova, E. Y., Kaiser, C., Shveygert, M., and Gromeier, M. (2007) RNA, 13, 1582–1593.

    CAS  PubMed  Google Scholar 

  90. Perez, C., McKinney, C., Chulunbaatar, U., and Mohr, I. (2011) J. Virol., 85, 156–164.

    CAS  PubMed Central  PubMed  Google Scholar 

  91. McKinney, C., Perez, C., and Mohr, I. (2012) Proc. Natl. Acad. Sci. USA, 109, 5627–5632.

    CAS  PubMed  Google Scholar 

  92. Zhang, B., Morace, G., Gauss-Muller, V., and Kusov, Y. (2007) Nucleic Acids Res., 35, 5975–5984.

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Duncan, K. E., Strein, C., and Hentze, M. W. (2009) Mol. Cell, 36, 571–582.

    CAS  PubMed  Google Scholar 

  94. Mazumder, B., Seshadri, V., Imataka, H., Sonenberg, N., and Fox, P. L. (2001) Mol. Cell Biol., 21, 6440–6449.

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Mazumder, B., Sampath, P., Seshadri, V., Maitra, R. K., DiCorleto, P. E., and Fox, P. L. (2003) Cell, 115, 187–198.

    CAS  PubMed  Google Scholar 

  96. Sampath, P., Mazumder, B., Seshadri, V., Gerber, C. A., Chavatte, L., Kinter, M., Ting, S. M., Dignam, J. D., Kim, S., Driscoll, D. M., and Fox, P. L. (2004) Cell, 119, 195–208.

    CAS  PubMed  Google Scholar 

  97. Kapasi, P., Chaudhuri, S., Vyas, K., Baus, D., Komar, A. A., Fox, P. L., Merrick, W. C., and Mazumder, B. (2007) Mol. Cell, 25, 113–126.

    CAS  PubMed Central  PubMed  Google Scholar 

  98. Vyas, K., Chaudhuri, S., Leaman, D. W., Komar, A. A., Musiyenko, A., Barik, S., and Mazumder, B. (2009) Mol. Cell Biol., 29, 458–470.

    CAS  PubMed Central  PubMed  Google Scholar 

  99. Skabkina, O. V., Skabkin, M. A., Popova, N. V., Lyabin, D. N., Penalva, L. O., and Ovchinnikov, L. P. (2003) J. Biol. Chem., 278, 18191–18198.

    CAS  PubMed  Google Scholar 

  100. Skabkina, O. V., Lyabin, D. N., Skabkin, M. A., and Ovchinnikov, L. P. (2005) Mol. Cell Biol., 25, 3317–3323.

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Lyabin, D. N., Eliseeva, I. A., Skabkina, O. V., and Ovchinnikov, L. P. (2011) RNA Biol., 8, 883–892.

    CAS  PubMed  Google Scholar 

  102. Eliseeva, I. A., Ovchinnikov, L. P., and Lyabin, D. N. (2012) RNA Biol., 9, 1473–1487.

    CAS  PubMed  Google Scholar 

  103. Iwakawa, H.-O., Tajima, Y., Taniguchi, T., Kaido, M., Mise, K., Tomari, Y., Taniguchi, H., and Okuno, T. (2012) J. Virol., 86, 7836–7849.

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Polacek, C., Friebe, P., and Harris, E. (2009) J. Gen. Virol., 90, 687–692.

    CAS  PubMed  Google Scholar 

  105. Reynolds, N., Collier, B., Maratou, K., Bingham, V., Speed, R. M., Taggart, M., Semple, C. A., Gray, N. K., and Cooke, H. J. (2005) Hum. Mol. Genet., 14, 3899–3909.

    CAS  PubMed  Google Scholar 

  106. Kawahara, H., Imai, T., Imataka, H., Tsujimoto, M., Matsumoto, K., and Okano, H. (2008) J. Cell Biol., 181, 639–653.

    CAS  PubMed  Google Scholar 

  107. Ohyama, T., Nagata, T., Tsuda, K., Kobayashi, N., Imai, T., Okano, H., Yamazaki, T., and Katahira, M. (2011) Nucleic Acids Res., 40, 3218–3231.

    PubMed Central  PubMed  Google Scholar 

  108. Lim, C., Lee, J., Choi, C., Kilman, V. L., Kim, J., Park, S. M., Jang, S. K., Allada, R., and Choe, J. (2011) Nature, 470, 399–403.

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Singh, N., Morlock, H., and Hanes, S. D. (2011) Dev. Biol., 352, 104–115.

    CAS  PubMed  Google Scholar 

  110. Kulkarni, S. D., Muralidharan, B., Panda, A. C., Bakthavachalu, B., Vindu, A., and Seshadri, V. (2011) J. Biol. Chem., 286, 14146–14156.

    CAS  PubMed  Google Scholar 

  111. Clouse, K. N., Ferguson, S. B., and Schupbach, T. (2008) Dev. Biol., 313, 713–724.

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Ivanov, P. V., Gehring, N. H., Kunz, J. B., Hentze, M. W., and Kulozik, A. E. (2008) EMBO J., 27, 736–747.

    CAS  PubMed  Google Scholar 

  113. Singh, G., Rebbapragada, I., and Lykke-Andersen, J. (2008) PLoS Biol., 6, e111.

    PubMed Central  PubMed  Google Scholar 

  114. Parker, R., and Song, H. (2004) Nat. Struct. Mol. Biol., 11, 121–127.

    CAS  PubMed  Google Scholar 

  115. Brown, C. E., and Sachs, A. B. (1998) Mol. Cell Biol., 18, 6548–6559.

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Kuhn, U., and Wahle, E. (2004) Biochim. Biophys. Acta, 1678, 67–84.

    CAS  PubMed  Google Scholar 

  117. Ezzeddine, N., Chen, C.-Y. A., and Shyu, A.-B. (2012) Mol. Cell Biol., 32, 1089–1098.

    CAS  PubMed Central  PubMed  Google Scholar 

  118. Tritschler, F., Huntzinger, E., and Izaurralde, E. (2010) Nat. Rev. Mol. Cell Biol., 11, 379–384.

    CAS  PubMed  Google Scholar 

  119. Lai, E. C. (2003) Curr. Biol., 13, r925–936.

    CAS  PubMed  Google Scholar 

  120. Friedman, R. C., Farh, K. K.-H., Burge, C. B., and Bartel, D. P. (2009) Genome Res., 19, 92–105.

    CAS  PubMed  Google Scholar 

  121. Fabian, M. R., and Sonenberg, N. (2012) Nat. Struct. Mol. Biol., 19, 586–593.

    CAS  PubMed  Google Scholar 

  122. Bazzini, A. A., Lee, M. T., and Giraldez, A. J. (2012) Science, 336, 233–237.

    CAS  PubMed Central  PubMed  Google Scholar 

  123. Djuranovic, S., Nahvi, A., and Green, R. (2012) Science, 336, 237–240.

    CAS  PubMed  Google Scholar 

  124. Eulalio, A., Huntzinger, E., Nishihara, T., Rehwinkel, J., Fauser, M., and Izaurralde, E. (2009) RNA, 15, 21–32.

    CAS  PubMed  Google Scholar 

  125. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Filipowicz, W. (2006) Cell, 125, 1111–1124.

    CAS  PubMed  Google Scholar 

  126. Moretti, F., Kaiser, C., Zdanowicz-Specht, A., and Hentze, M. W. (2012) Nat. Struct. Mol. Biol., 19, 603–608.

    CAS  PubMed  Google Scholar 

  127. Fabian, M. R., Mathonnet, G., Sundermeier, T., Mathys, H., Zipprich, J. T., Svitkin, Y. V., Rivas, F., Jinek, M., Wohlschlegel, J., Doudna, J. A., Chen, C.-Y. A., Shyu, A.-B., Yates, J. R., Hannon, G. J., Filipowicz, W., Duchaine, T. F., and Sonenberg, N. (2009) Mol. Cell, 35, 868–880.

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Zekri, L., Huntzinger, E., Heimstadt, S., and Izaurralde, E. (2009) Mol. Cell Biol., 29, 6220–6231.

    CAS  PubMed Central  PubMed  Google Scholar 

  129. Zekri, L., Kuzuoglu-Ozturk, D., and Izaurralde, E. (2013) EMBO J., 32, 1052–1065.

    CAS  PubMed  Google Scholar 

  130. Fukaya, T., and Tomari, Y. (2011) EMBO J., 30, 4998–5009.

    CAS  PubMed  Google Scholar 

  131. Mishima, Y., Fukao, A., Kishimoto, T., Sakamoto, H., Fujiwara, T., and Inoue, K. (2012) Proc. Natl. Acad. Sci. USA, 109, 1104–1109.

    CAS  PubMed  Google Scholar 

  132. Sagliocco, F., Laloo, B., Cosson, B., Laborde, L., Castroviejo, M., Rosenbaum, J., Ripoche, J., and Grosset, C. (2006) Biochem. J., 400, 337–347.

    CAS  PubMed  Google Scholar 

  133. Wang, Z., and Kiledjian, M. (2000) Mol. Cell Biol., 20, 6334–6341.

    CAS  PubMed Central  PubMed  Google Scholar 

  134. Stefanizzi, I., and Canete-Soler, R. (2007) Brain Res., 1139, 15–28.

    CAS  PubMed  Google Scholar 

  135. Grosset, C., Chen, C. Y., Xu, N., Sonenberg, N., Jacquemin-Sablon, H., and Shyu, A. B. (2000) Cell, 103, 29–40.

    CAS  PubMed  Google Scholar 

  136. Vazquez-Pianzola, P., Urlaub, H., and Suter, B. (2011) Dev. Biol., 357, 404–418.

    CAS  PubMed  Google Scholar 

  137. Casper, I., Nowag, S., Koch, K., Hubrich, T., Bollmann, F., Henke, J., Schmitz, K., Kleinert, H., and Pautz, A. (2013) Nitric Oxide, 33, 6–17.

    CAS  PubMed  Google Scholar 

  138. Ma, S., Musa, T., and Bag, J. (2006) J. Biol. Chem., 281, 3145–3156.

    CAS  PubMed  Google Scholar 

  139. Brooks, S. A. (2010) Wiley Interdiscip. Rev. RNA, 1, 240–252.

    CAS  PubMed  Google Scholar 

  140. Svitkin, Y. V., Yanagiya, A., Karetnikov, A. E., Alain, T., Fabian, M. R., Khoutorsky, A., Perreault, S., Topisirovic, I., and Sonenberg, N. (2013) PLoS Biol., 11, e1001564.

    CAS  PubMed Central  PubMed  Google Scholar 

  141. Salaun, C., MacDonald, A. I., Larralde, O., Howard, L., Lochtie, K., Burgess, H. M., Brook, M., Malik, P., Gray, N. K., and Graham, S. V. (2010) J. Virol., 84, 8539–8548.

    CAS  PubMed Central  PubMed  Google Scholar 

  142. Burgess, H. M., Richardson, W. A., Anderson, R. C., Salaun, C., Graham, S. V., and Gray, N. K. (2011) J. Cell Sci., 124, 3344–3355.

    CAS  PubMed  Google Scholar 

  143. Ma, S., Bhattacharjee, R. B., and Bag, J. (2009) FEBS J., 276, 552–570.

    CAS  PubMed  Google Scholar 

  144. Dobrikova, E., Shveygert, M., Walters, R., and Gromeier, M. (2010) J. Virol., 84, 270–279.

    CAS  PubMed Central  PubMed  Google Scholar 

  145. Harb, M., Becker, M. M., Vitour, D., Baron, C. H., Vende, P., Brown, S. C., Bolte, S., Arold, S. T., and Poncet, D. (2008) J. Virol., 82, 11283–11293.

    CAS  PubMed Central  PubMed  Google Scholar 

  146. Mallet, P.-L., and Bachand, F. (2013) Traffic, 14, 282–294.

    CAS  PubMed  Google Scholar 

  147. Arnold, M. M., Brownback, C. S., Taraporewala, Z. F., and Patton, J. T. (2012) J. Gen. Virol., 93, 1483–1489.

    CAS  PubMed  Google Scholar 

  148. Bag, J., and Wu, J. (1996) Eur. J. Biochem., 237, 143–152.

    CAS  PubMed  Google Scholar 

  149. Bag, J. (2001) J. Biol. Chem., 276, 47352–47360.

    CAS  PubMed  Google Scholar 

  150. Patel, G. P., Ma, S., and Bag, J. (2005) Nucleic Acids Res., 33, 7074–7089.

    CAS  PubMed Central  PubMed  Google Scholar 

  151. Hornstein, E., Git, A., Braunstein, I., Avni, D., and Meyuhas, O. (1999) J. Biol. Chem., 274, 1708–1714.

    CAS  PubMed  Google Scholar 

  152. Huichalaf, C., Schoser, B., Schneider-Gold, C., Jin, B., Sarkar, P., and Timchenko, L. (2009) J. Neurosci., 29, 9042–9049.

    CAS  PubMed Central  PubMed  Google Scholar 

  153. Damgaard, C. K., and Lykke-Andersen, J. (2011) Genes Dev., 25, 2057–2068.

    CAS  PubMed  Google Scholar 

  154. Le, H., Browning, K. S., and Gallie, D. R. (2000) J. Biol. Chem., 275, 17452–17462.

    CAS  PubMed  Google Scholar 

  155. Friend, K., Brook, M., Bezirci, F. B., Sheets, M. D., Gray, N. K., and Seli, E. (2012) Biochem. J., 445, 93–100.

    CAS  PubMed  Google Scholar 

  156. Brook, M., McCracken, L., Reddington, J. P., Lu, Z.-L., Morrice, N. A., and Gray, N. K. (2012) Biochem. J., 441, 803–812.

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. P. Ovchinnikov.

Additional information

Published in Russian in Uspekhi Biologicheskoi Khimii, 2013, Vol. 53, pp. 3–34.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eliseeva, I.A., Lyabin, D.N. & Ovchinnikov, L.P. Poly(A)-binding proteins: Structure, domain organization, and activity regulation. Biochemistry Moscow 78, 1377–1391 (2013). https://doi.org/10.1134/S0006297913130014

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297913130014

Key words

Navigation