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.
Similar content being viewed by others
References
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.
Agou, F., Raveh, S., Mesnildrey, S., and Veron, M. (1999). J. Biol. Chem. 274, 19630-19638.
Arnaud-Dabernat, S., Daniel, J-Y., Landry, M., Peuchant, K. M.,Boutbon, P. M., Le Floch, R., Larou, M., submitted.
Berberich, S. J., and Postel, E. H. (1995). Oncogene 10, 2343-2347.
Bernard, M. A., Ray, N. B., Olcott, M. C., Hendricks, S. P., and Mathews, C. K. (2000). J. Bioenerg. Biomembr. 32, 259-267.
Boles, C., Hogan, M. (1987). Biochemistry 26, 367-376.
Bruner, S. D., Norman, D. P. G., and Verdine, G. L. (2000). Nature 403, 859-866.
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.
Cooney, M., Czernuszewicz, G., Postel, E., Flint, S. J., and Hogan, M. E. (1988). Science 242, 456-459.
Cunningham, R. P. (1997). Mutat. Res. 383, 189-196.
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.
David, S. S., and Williams, S. D. (1998). Chem. Rev. 98, 1221-1262.
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.
Dodson, M. L., Michaels, M. L., and Lloyd, R. S. (1994). J. Biol. Chem. 269, 32709-32712.
Dogliotti, E., Fortini, P., Pascucci, B., and Parlanti, E. (2001). Prog. Nucleic Acid Res. Mol. Biol. 68, 3-27.
Ferguson, A. W., Flatow, U., MacDonald, N. J., Larminat, F., Bohr, V. A., and Steeg, P. S. (1996). Cancer Res. 56, 2931-2935.
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.
Hartsough, M., and Steeg, P. S. (2000). J. Bioenerg. Biomembr. 32, 301.
Hildebrandt, M., Lacombe, M.-L., Mesnildrey, S., and Véron, M. (1995). Nucleic Acids Res. 23, 3858-3864.
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.
Janin, J., Dumas, C., Morera, S., Xu, Y., Meyer, P., Chiadmi, M., and Cherfils, J. (2000). J. Bioenerg. Biomembr. 32, 215-225.
Ji, L., Arcinas, M., and Boxer, L. M. (1995). J. Biol. Chem. 270, 13392-13398.
Jiricny, J. (1996). Cancer Surv. 28, 47-68.
Kolodner, R. D. (1995). Trends Biol. Sci. 20, 397-401.
Krokan, H. E., Nilsen, H., Skorpen, F., Otterlei, M., and Slupphaug, G. (2000). FEBS Lett. 476, 73-77.
Kunz, B. A., Kohalmi, S., Kunkel, T. A., Mathews, C. K., McIntosh, E. M., and Reidy, J. A. (1994). Mutat. Res. 318, 1-64.
Lacombe, M.-L., Milon, L., Munier, A., Mehus, J. G., and Lambeth, D. O. (2000). J. Bioenerg. Biomembr. 32, 247-258.
Lascu, I. (2000). J. Bioenerg. Biomembr. 32, 213-214.
Lascu, I., Giartosio, A., Ransac, S., and Erent, M. (2000). J. Bioenerg. Biomembr. 32, 227-236.
Leadon, S. A. (1999). “Transcription-coupled repair of DNA damage: Unanticipated players, unexpected complexities” Am. J. Hum. Genet. 64(5), 1259-1263.
Le Page, F., Randrianarison, V., Marot, D., Cabannes, J., Perricaudet, M., Feunteun, J., and Sarasin, A. (2000). Cancer Res. 60, 5548-5552.
Levit, M. N., Abramczyk, B. M., Stock, J. B., and Postel, E. H. (2002). J. Biol. Chem. 277, 5163-5167.
Lindahl, T., and Wood, R. D. (1999). Science 286, 1897-1905.
Lloyd, R. S., and Linn, S. (1993). Nucleases, 2nd edn., Cold Spring Harbor Laboratory Press, New York, pp. 263-316.
Loeb, L. A. (1998). Adv. Cancer Res. 72, 25-56.
Lombardi, D., Lacombe, M. L., and Paggi, M. G. (2000). J. Cell. Physiol. 182, 144-149.
Lu, Q., Park, H., Egger, L. A., and Inouye, M. (1996). J. Biol. Chem. 271, 32886-32893.
Lu, Q., Zhang, X., Almaula, N., Mathews, C., and Inouye, M. (1995). J. Mol. Biol. 254, 337-341.
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.
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.
Malins, D. C., Polissar, N. L., and Gunselman, S. J. (1996). Proc. Natl. Acad. Sci. U.S.A. 93, 2557-2563.
Malins, D. C., Polissar, N. L., Schaefer, S., Su, Y., and Vinson, M. (1998). Proc. Natl. Acad. Sci. U.S.A. 95, 7637-7642.
McCullough, A. K., Dodson, M. L., and Lloyd, R. S. (1999). Annu. Rev. Biochem. 68, 255-285.
Michelotti, E. F., Tomonaga, T., Krutzsch, H., and Levens, D. (1995). J. Biol. Chem. 270, 9494-9499.
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.
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.
Modrich, P. (1991). Annu. Rev. Genet. 25, 229-253.
Modrich, P., and Lahue, R. (1996). Annu. Rev. Biochem. 65, 101-133.
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.
Moréa, S., Lacombe, M. L., Xu, Y., LeBras, G., and Janin, J. (1995). Structure 3, 1307-1314.
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.
Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. (2000). Cell 102, 553-563.
Nash, H. M., Lu, R., Lane, W. S., and Verdine, G. L. (1997). Chem. Biol. 4, 693-702.
Pongubala, J. M., and Atchison, M. L. (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 127-132.
Postel, E. H. (1998). Int. J. Biochem. Cell. Biol. 30, 1291-1295.
Postel, E. H. (1999). J. Biol. Chem. 274, 22821-22829.
Postel, E. H. Abramczyk, B. A., Gursky, S. K., and Xu, Y. (2002). Biochemistry 41, 6330-6337.
Postel, E. H., Abramczyk, B. M., Levit, M. N., and Kyin, S. (2000a). Proc. Natl. Acad. Sci. U.S.A. 97, 14194-14199.
Postel, E. H., Berberich, S. J., Flint, S. J., and Ferrone, C. A. (1993). Science 261, 478-480.
Postel, E. H., Berberich, S. J., Rooney, J. W., and Kaetzel, D. M. (2000b). J. Bioenerg. Biomembr. 32, 277-284.
Postel, E. H., and Ferrone, C. A. (1994). J. Biol. Chem. 269, 8627-8630.
Postel, E. H., Mango, S. E., and Flint, S. J. (1989). Mol. Cell. Biol. 9, 5123-5133.
Postel, E. H., Weiss, V. H., Beneken, J., and Kirtane, A. (1996). Proc Natl. Acad. Sci. U.S.A. 93, 6892-6897.
Sager, R. (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 952-955.
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.
Siddiqui-Jain, A., Grand, C. L., Bearss, D. J., and Hurley, L. H. (2003). Proc. Natl. Acad. Sci. 99, 11593-11598.
Simonsson, T., Pribylova, M., and Vorlickova, M. (2000). Biochem. Biophys. Res. Commun. 278, 158-166.
Singh, Y., et al., personal communication.
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.
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.
Wagner, P. D., Steeg, P. S., and Vu, N. D. (1997). Proc. Natl. Acad. Sci. U.S.A. 94, 9000-9005.
Webb, P. A., Perisic, O., Mendola, C. E., Backer, J. M., and Williams, R. L. (1995). J. Mol. Biol. 251, 574-587.
Zdraveski, Z. Z., Mello, J. A., Farinelli, C. K., Essigmann, J. M., and Marinus, M. G. (2002). J. Biol. Chem. 277, 1255-1260.
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.
Zou, X., and Perlmutter, R. (2001). The Fourth International Congress of the Genetics, Biochemistry and Physiology of NDP Kinase/NM23/AWD Tokyo, Japan.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Postel, E.H. Multiple Biochemical Activities of NM23/NDP Kinase in Gene Regulation. J Bioenerg Biomembr 35, 31–40 (2003). https://doi.org/10.1023/A:1023485505621
Issue Date:
DOI: https://doi.org/10.1023/A:1023485505621