Journal of Bioenergetics and Biomembranes

, Volume 35, Issue 1, pp 31–40 | Cite as

Multiple Biochemical Activities of NM23/NDP Kinase in Gene Regulation

  • Edith H. Postel
Article

Abstract

NM23/NDPk proteins play critical roles in cancer and development; however, our understanding of the underlying biochemical mechanisms is still limited. This large family of highly conserved proteins are known to participate in many events related to DNA metabolism, including nucleotide binding and nucleoside triphosphate synthesis, DNA binding and transcription, and cleavage of DNA strands via covalent protein–DNA complexes. The chemistry of the DNA-cleavage reaction of NM23-H2/NDPk is characteristic of DNA repair enzymes. Both the DNA cleavage and the NDPk reactions are conserved between E. coli and the human enzymes, and several conserved amino acid side chains involved in catalysis are shared by these reactions. It is proposed here that NM23/NDP kinases are important regulators of gene expression during development and cancer via previously unrecognized roles in DNA repair and recombination, and via previously unrecognized pathways and mechanisms of genetic control.

NM23 NDP kinase nuclease DNA transcription DNA recombination DNA repair 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aebi, S., Kurdi-Haidar, B., Gordon, R., Cenni, B., Zheng, H., Fink, D., Christen, R. D., Boland, C. R., Koi, M., Fishel, R., and Howell, S. B. (1996). Cancer Res. 56, 3087-3090.PubMedGoogle Scholar
  2. Agou, F., Raveh, S., Mesnildrey, S., and Veron, M. (1999). J. Biol. Chem. 274, 19630-19638.PubMedGoogle Scholar
  3. Arnaud-Dabernat, S., Daniel, J-Y., Landry, M., Peuchant, K. M.,Boutbon, P. M., Le Floch, R., Larou, M., submitted.Google Scholar
  4. Berberich, S. J., and Postel, E. H. (1995). Oncogene 10, 2343-2347.PubMedGoogle Scholar
  5. Bernard, M. A., Ray, N. B., Olcott, M. C., Hendricks, S. P., and Mathews, C. K. (2000). J. Bioenerg. Biomembr. 32, 259-267.PubMedGoogle Scholar
  6. Boles, C., Hogan, M. (1987). Biochemistry 26, 367-376.PubMedGoogle Scholar
  7. Bruner, S. D., Norman, D. P. G., and Verdine, G. L. (2000). Nature 403, 859-866.PubMedGoogle Scholar
  8. Cho, S. J., Lee, N. S., Jung, Y. S., Lee, H., Lee, K. J., Kim, E., and Chae, S. K. (2001). Biochem. Biophys. Res. Commun. 289, 738-743.PubMedGoogle Scholar
  9. Cooney, M., Czernuszewicz, G., Postel, E., Flint, S. J., and Hogan, M. E. (1988). Science 242, 456-459.Google Scholar
  10. Cunningham, R. P. (1997). Mutat. Res. 383, 189-196.PubMedGoogle Scholar
  11. Dabernat, S., Bourbon, P.-M., Larou, M., Masse, K., Landry, M., Dierich, A., Lemeur, M., and Daniel, J.-Y. (1999). The Third International Congress of the Genetics, Biochemistry and Physiology of nm23/Nucleoside Diphosphate Kinase, T2.Google Scholar
  12. David, S. S., and Williams, S. D. (1998). Chem. Rev. 98, 1221-1262.PubMedGoogle Scholar
  13. Dianov, G. L., Souza-Pinto, N., Nyaga, S. G., Thybo, T., Stevnsner, T., and Bohr, V. A. (2001). Prog. Nucleic Acid Res. Mol. Biol. 68, 285-297.PubMedGoogle Scholar
  14. Dodson, M. L., Michaels, M. L., and Lloyd, R. S. (1994). J. Biol. Chem. 269, 32709-32712.PubMedGoogle Scholar
  15. Dogliotti, E., Fortini, P., Pascucci, B., and Parlanti, E. (2001). Prog. Nucleic Acid Res. Mol. Biol. 68, 3-27.PubMedGoogle Scholar
  16. Ferguson, A. W., Flatow, U., MacDonald, N. J., Larminat, F., Bohr, V. A., and Steeg, P. S. (1996). Cancer Res. 56, 2931-2935.PubMedGoogle Scholar
  17. Hailat, N., Keim, D. R., Melhem, R. F., Zhu, X., Eckerskorn, C., Brodeur, G. M., Reynolds, C. P., Seeger, R. C., Lottspeich, F., Strahler, J. R., and Hanash, S. M. (1991). J. Clin. Invest. 88, 341-345.PubMedGoogle Scholar
  18. Hartsough, M., and Steeg, P. S. (2000). J. Bioenerg. Biomembr. 32, 301.PubMedGoogle Scholar
  19. Hildebrandt, M., Lacombe, M.-L., Mesnildrey, S., and Véron, M. (1995). Nucleic Acids Res. 23, 3858-3864.PubMedGoogle Scholar
  20. House, P., Volk, D., Thiviyanathan, V., Manuel, R., Luxon, B., Gorenstein, D., and Lloyd, R. S. (2001). Prog. Nucleic Acid Res. Mol. Biol. 68, 349-364.PubMedGoogle Scholar
  21. Janin, J., Dumas, C., Morera, S., Xu, Y., Meyer, P., Chiadmi, M., and Cherfils, J. (2000). J. Bioenerg. Biomembr. 32, 215-225.PubMedGoogle Scholar
  22. Ji, L., Arcinas, M., and Boxer, L. M. (1995). J. Biol. Chem. 270, 13392-13398.PubMedGoogle Scholar
  23. Jiricny, J. (1996). Cancer Surv. 28, 47-68.PubMedGoogle Scholar
  24. Kolodner, R. D. (1995). Trends Biol. Sci. 20, 397-401.Google Scholar
  25. Krokan, H. E., Nilsen, H., Skorpen, F., Otterlei, M., and Slupphaug, G. (2000). FEBS Lett. 476, 73-77.PubMedGoogle Scholar
  26. Kunz, B. A., Kohalmi, S., Kunkel, T. A., Mathews, C. K., McIntosh, E. M., and Reidy, J. A. (1994). Mutat. Res. 318, 1-64.PubMedGoogle Scholar
  27. Lacombe, M.-L., Milon, L., Munier, A., Mehus, J. G., and Lambeth, D. O. (2000). J. Bioenerg. Biomembr. 32, 247-258.PubMedGoogle Scholar
  28. Lascu, I. (2000). J. Bioenerg. Biomembr. 32, 213-214.PubMedGoogle Scholar
  29. Lascu, I., Giartosio, A., Ransac, S., and Erent, M. (2000). J. Bioenerg. Biomembr. 32, 227-236.PubMedGoogle Scholar
  30. Leadon, S. A. (1999). “Transcription-coupled repair of DNA damage: Unanticipated players, unexpected complexities” Am. J. Hum. Genet. 64(5), 1259-1263.PubMedGoogle Scholar
  31. Le Page, F., Randrianarison, V., Marot, D., Cabannes, J., Perricaudet, M., Feunteun, J., and Sarasin, A. (2000). Cancer Res. 60, 5548-5552.PubMedGoogle Scholar
  32. Levit, M. N., Abramczyk, B. M., Stock, J. B., and Postel, E. H. (2002). J. Biol. Chem. 277, 5163-5167.PubMedGoogle Scholar
  33. Lindahl, T., and Wood, R. D. (1999). Science 286, 1897-1905.PubMedGoogle Scholar
  34. Lloyd, R. S., and Linn, S. (1993). Nucleases, 2nd edn., Cold Spring Harbor Laboratory Press, New York, pp. 263-316.Google Scholar
  35. Loeb, L. A. (1998). Adv. Cancer Res. 72, 25-56.PubMedGoogle Scholar
  36. Lombardi, D., Lacombe, M. L., and Paggi, M. G. (2000). J. Cell. Physiol. 182, 144-149.PubMedGoogle Scholar
  37. Lu, Q., Park, H., Egger, L. A., and Inouye, M. (1996). J. Biol. Chem. 271, 32886-32893.PubMedGoogle Scholar
  38. Lu, Q., Zhang, X., Almaula, N., Mathews, C., and Inouye, M. (1995). J. Mol. Biol. 254, 337-341.PubMedGoogle Scholar
  39. Ma, D., Xing, Z., Liu, B., Pedigo, N. G., Zimmer, S. G., Bai, Z., Postel, E. H., and Kaetzel, D. M. (2002). J. Biol. Chem. 277, 1560-1567.PubMedGoogle Scholar
  40. MacLachlan, T. K., Somasundaram, K., Sgagias, M., Shifman, Y., Muschel, R. J., Cowan, K. H., and El-Deiry, W. S. (2000). J. Biol. Che. 275, 2777-2785.Google Scholar
  41. Malins, D. C., Polissar, N. L., and Gunselman, S. J. (1996). Proc. Natl. Acad. Sci. U.S.A. 93, 2557-2563.PubMedGoogle Scholar
  42. Malins, D. C., Polissar, N. L., Schaefer, S., Su, Y., and Vinson, M. (1998). Proc. Natl. Acad. Sci. U.S.A. 95, 7637-7642.PubMedGoogle Scholar
  43. McCullough, A. K., Dodson, M. L., and Lloyd, R. S. (1999). Annu. Rev. Biochem. 68, 255-285.PubMedGoogle Scholar
  44. Michelotti, E. F., Tomonaga, T., Krutzsch, H., and Levens, D. (1995). J. Biol. Chem. 270, 9494-9499.PubMedGoogle Scholar
  45. Miller, J. H., Funchain, P., Clendenin, W., Huang, T., Nguyen, A., Wolff, E., Yeung, A., Chiang, J.-H., Garibyan, L., Slupska, M. M., and Yang, H. (2002). Genetics. 162, 5-13.PubMedGoogle Scholar
  46. Milon, L., Meyer, P., Chiadmi, M., Munier, A., Johansson, M., Karlsson, A., Lascu, I., Capeau, J., Janin, J. and Lacombe, M. L. (2000). J. Biol. Chem. 275, 14264-14272.PubMedGoogle Scholar
  47. Modrich, P. (1991). Annu. Rev. Genet. 25, 229-253.PubMedGoogle Scholar
  48. Modrich, P., and Lahue, R. (1996). Annu. Rev. Biochem. 65, 101-133.PubMedGoogle Scholar
  49. Mol, C. D., Parikh, S. S., Putnam, C. D., Lo, T. P., and Tainer, J. A. (1999). Annu. Rev. Biophys. Biomol. Struct. 28, 101-128.PubMedGoogle Scholar
  50. Moréa, S., Lacombe, M. L., Xu, Y., LeBras, G., and Janin, J. (1995). Structure 3, 1307-1314.PubMedGoogle Scholar
  51. Munier, A., Serres, C., Kann, M. L., Capeau, J., Fouquet, J. P., and Lacombe, M. L. (2001). The Fourth International Congress of the Genetics, Biochemistry and Physiology of NDP Kinase/NM23/AWD, T3, Tokyo, Japan.Google Scholar
  52. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. (2000). Cell 102, 553-563.PubMedGoogle Scholar
  53. Nash, H. M., Lu, R., Lane, W. S., and Verdine, G. L. (1997). Chem. Biol. 4, 693-702.PubMedGoogle Scholar
  54. Pongubala, J. M., and Atchison, M. L. (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 127-132.PubMedGoogle Scholar
  55. Postel, E. H. (1998). Int. J. Biochem. Cell. Biol. 30, 1291-1295.PubMedGoogle Scholar
  56. Postel, E. H. (1999). J. Biol. Chem. 274, 22821-22829.PubMedGoogle Scholar
  57. Postel, E. H. Abramczyk, B. A., Gursky, S. K., and Xu, Y. (2002). Biochemistry 41, 6330-6337.PubMedGoogle Scholar
  58. Postel, E. H., Abramczyk, B. M., Levit, M. N., and Kyin, S. (2000a). Proc. Natl. Acad. Sci. U.S.A. 97, 14194-14199.PubMedGoogle Scholar
  59. Postel, E. H., Berberich, S. J., Flint, S. J., and Ferrone, C. A. (1993). Science 261, 478-480.PubMedGoogle Scholar
  60. Postel, E. H., Berberich, S. J., Rooney, J. W., and Kaetzel, D. M. (2000b). J. Bioenerg. Biomembr. 32, 277-284.PubMedGoogle Scholar
  61. Postel, E. H., and Ferrone, C. A. (1994). J. Biol. Chem. 269, 8627-8630.PubMedGoogle Scholar
  62. Postel, E. H., Mango, S. E., and Flint, S. J. (1989). Mol. Cell. Biol. 9, 5123-5133.PubMedGoogle Scholar
  63. Postel, E. H., Weiss, V. H., Beneken, J., and Kirtane, A. (1996). Proc Natl. Acad. Sci. U.S.A. 93, 6892-6897.PubMedGoogle Scholar
  64. Sager, R. (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 952-955.PubMedGoogle Scholar
  65. Sanchez-Cespedes, M., Parrella, P., Nomoto, S., Cohen, D., Xiao, Y., Esteller, M., Jeronimo, C., Jordan, R. C., Nicol, T., Koch, W. M., Schoenberg, M., Mazzarelli, P., Fazio, V. M., and Sidransky, D. (2001). Cancer Res. 61, 7015-7019.PubMedGoogle Scholar
  66. Siddiqui-Jain, A., Grand, C. L., Bearss, D. J., and Hurley, L. H. (2003). Proc. Natl. Acad. Sci. 99, 11593-11598.Google Scholar
  67. Simonsson, T., Pribylova, M., and Vorlickova, M. (2000). Biochem. Biophys. Res. Commun. 278, 158-166.PubMedGoogle Scholar
  68. Singh, Y., et al., personal communication.Google Scholar
  69. Steeg, P. S., Bevilacqua, G., Kopper, L., Thorgeirsson, U. R., Talmadge, J. E., Liotta, L. A., and Sobel, M. E. (1998). J. Natl. Cancer Inst. 80, 200-205.Google Scholar
  70. Venturelli, D., Martinez, R., Melotti, P., Casella, I., Peschle, C., Cucco, C., Spampinato, G., Darzynkiewicz, Z., and Calabretta, B. (1995). Proc. Natl. Acad. Sci. U.S.A. 92, 7435-7439.PubMedGoogle Scholar
  71. Wagner, P. D., Steeg, P. S., and Vu, N. D. (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 9000-9005.PubMedGoogle Scholar
  72. Webb, P. A., Perisic, O., Mendola, C. E., Backer, J. M., and Williams, R. L. (1995). J. Mol. Biol. 251, 574-587.PubMedGoogle Scholar
  73. Zdraveski, Z. Z., Mello, J. A., Farinelli, C. K., Essigmann, J. M., and Marinus, M. G. (2002). J. Biol. Chem. 277, 1255-1260.PubMedGoogle Scholar
  74. Zhang, L., Zhou, W., Velculescu, V. E., Kern, S. E., Hruban, R. H., Hamilton, S. R., Vogelstein, B., and Kinzler, K. W. (1997). Science 276, 1268-1272.PubMedGoogle Scholar
  75. Zou, X., and Perlmutter, R. (2001). The Fourth International Congress of the Genetics, Biochemistry and Physiology of NDP Kinase/NM23/AWD Tokyo, Japan.Google Scholar

Copyright information

© Plenum Publishing Corporation 2003

Authors and Affiliations

  • Edith H. Postel
    • 1
  1. 1.Department of Molecular BiologyPrinceton UniversityPrinceton

Personalised recommendations