nm23: Unraveling its biological function in cell differentiation

Journal of Cellular Physiology

Volumn 182, Issue 2, 2000, Pages 144-149

  Lombardi, Daniela ^a,b   Lacombe, Marie Lise ^c   Paggi, Marco G ^b  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOSIDE DIPHOSPHATE KINASE; PHOSPHOTRANSFERASE; SERINE;

CANCER CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; ENZYME ACTIVITY; GENE FUNCTION; GENETIC TRANSCRIPTION; HEMATOPOIETIC CELL; HUMAN; METASTASIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TISSUE DIFFERENTIATION; TUMOR SUPPRESSOR GENE;

AGING; ANIMALS; CELL DIFFERENTIATION; HEMATOPOIETIC STEM CELLS; HUMANS; MONOMERIC GTP-BINDING PROTEINS; MULTIGENE FAMILY; NUCLEOSIDE-DIPHOSPHATE KINASE; SEQUENCE HOMOLOGY; TRANSCRIPTION FACTORS;

EID: 0033981611     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(200002)182:2<144::AID-JCP2>3.0.CO;2-6     Document Type: Review

References (68)

1. Agarwal RP, Robinson B, Parks RE. 1978. Nucleoside diphosphokinase from human erythrocytes. Methods Enzymol 51:376-386.
2. Amendola R, Martinez R, Negroni A, Venturelli D, Tanno B, Calabretta B, Raschellà G. 1997. DR-nm23 gene expression in neuroblastoma cells: relationship to integrin expression, adhesion characteristics, and differentiation. J Natl Cancer Inst 89:1300-1310.
3. Aryee DN, Simonitsch I, Mosberger I, Kos K, Mann G, Schlogl E, Potschger U, Gadner H, Radaszkiewicz T, Kovar H. 1996. Variability of nm23-H1/NDPK-A expression in human lymphomas and its relation to tumour aggressiveness. Br J Cancer 74:1693-1698.
4. Backer JM, Mendola CE, Kovesdi I, Fairhurst J, O'Hara B, Eddy RL, Jr, Shows TB, Mathew S, Murty VVVS, Chaganti RSK. 1993. Chromosomal localization and nucleoside diphosphate kinase activity of human metastasis-suppressor genes nm23-1 and nm23-2. Oncogene 8:497-502.
5. Biggs J, Tripoulas N, Hersperger E, Dearolf C, Shearn A. 1988. Analysis of the lethal interaction between the prune and Killer of prune mutations of Drosophila. Genes Dev 2:1333-1343.
6. Biggs J, Hersperger E, Steeg PS, Liotta LA, Shearn A. 1990. A Drosophila gene that is homologous to a mammalian gene associated with tumor metastasis codes for a nucleoside diphosphate kinase. Cell 63:933-940.
7. Chang CL, Zhu XX, Thoraval DH, Ungar D, Rawwas J, Hora N, Strahler JR, Hanash SM, Radany E. 1994. Nm23-H1 mutation in neuroblastoma. Nature 370:335-336.
8. Chiadmi M, Morera S, Lascu I, Dumas C, Lebras G, Veron M, Janin J. 993. Crystal structure of the Awd nucleoside diphosphate kinase from Drosophila. Structure 1:283-293.
9. Dabernat S, Larou M, Masse K, Hokfelt T, Mayer G, Daniel JY, Landry M. 1999. Cloning of a second nm23-M1 cDNA: expression in the central nervous system of adult mouse and comparison with nm23-M2 mRNA distribution. Brain Res Mol Brain Res 63:351-365.
10. De La Rosa A, Williams R, Steeg PS. 1995. Nm23/nucleoside diphosphate kinase: toward a structural and biochemical understanding of its biological functions. Bioessays 17:53-62.
11. b3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev Biol 129:159-168.
12. Engel M, Veron M, Theisinger B, Lacombe ML, Seib T, Dooley S, Welter C. 1995. A novel serine/threonine-specific protein phosphotransferase activity of Nm23/nucleoside-diphosphate kinase. Eur J Biochem 234:200-207.
13. Freije JMP, Blay P, MacDonald NJ, Manrow RE, Steeg PS. 1997. Site-directed mutation of Nm23-H1. Mutations lacking motility suppressive capacity upon transfection are deficient in histidine-dependent protein phosphotransferase pathways in vitro. J Biol Chem 272:5525-5532.
14. Garces E, Cleland WW. 1969. Kinetic studies of yeast nucleoside diphosphate kinase. Biochemistry 8:633-640.
15. Gervasi F, D'Agnano I, Vossio S, Zupi G, Sacchi A, Lombardi D. 1996. nm23 influences proliferation and differentiation of PC12 cells in response to nerve growth factor. Cell Growth Diff 7:1689-1695.
16. Gervasi F, Capozza F, Bruno T, Fanciulli M, Lombardi D. 1998. Identification of novel mRNA transcripts of the nm23-M1 gene that are modulated during mouse embryo development and are differently expressed in adult murine tissues. DNA Cell Biol 17:1047-1055.
17. Gilles AM, Presecan E, Vonica A, Lascu I. 1991. Nucleoside diphosphate kinase from human erythrocytes. Structural characterization of the two polypeptide chains responsible for heterogeneity of the hexameric enzyme. J Biol Chem 266:8784-8789.
18. Hailat N, Keim DR, Melhem RF, Zhu XX, Eckersckorn C, Brodeur GM, Reynols CP, Seeger RC, Lottspeich F, Strahler JR, Hanash NM. 1991. High levels of p19/nm23 protein in neuroblastoma are associated with advanced stage disease and with N-myc gene amplification. J Clin Invest 88:341-345.
19. Hildebrandt M, Lacombe M-L, Mesnildrey S, Veron M. 1995. A human NDP-kinase B specifically binds single-stranded poly-pyrimidine sequences. Nucleic Acids Res 23:3858-3864.
20. Howlett AR, Peterson OW, Steeg PS, Bissel MJ. 1994. A novel function for the nm23-H 1 gene: overexpression in human breast carcinoma cells leads to the formation of basement membrane and growth arrest. J Natl Cancer Inst 86:1839-1994.
21. Kantor JD, McCormick B, Steeg PS, Zetter BR. 1993. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res 53:1971-1973.
22. Lacombe ML, Wallet V, Troll H, Veron M. 1990. Functional Cloning of a Nucleoside Diphosphate Kinase from Dictyostelium discoideum. J Biol Chem 265:10012-10018.
23. Lacombe ML, Sastre-Garau X, Lascu I, Wallet V, Thiery JP, and Véron M. 1991. Overexpression of nucleoside diphosphate kinase (Nm23) in solid tumours. Eur J Cancer 27:1302-1307.
24. Lakso M, Steeg PS, Westphal H. 1992. Embryonic expression of nm23 during mouse organogenesis. Cell Growth Differ 3:873-879.
25. Lascu I, Chaffotte A, Limbourg-Bouchon B, Veron M. 1992. A Pro/Ser substitution in nucleoside diphosphate kinase of Drosophila melanogaster (mutation Killer of prune) affects stability but not catalytic efficiency of the enzyme. J Biol Chem 267:12775-12781.
26. Leone A, Flatow U, Richter King C, Sandeen MA, Margoulies IMK, Liotta LA, Steeg PS. 1991. Reduced tumor incidence, metastatic potential, and cytokine responsiveness of nm23 transfected melanoma cells. Cell 65:25-35.
27. Leone A, Flatow U, Vanhoutte K, Steeg PS. 1993a. Transfection of human nm23-H1 into the human MDA-MB-435 breast carcinoma cell line - effects on tumor metastatic potential, colonization and enzymatic activity. Oncogene 8:2325-2333.
28. Leone A, Seeger RC, Hong CM, Hu YY, Arboleda MJ, Brodeur GM, Stram D, Slamon DJ, Steeg PS. 1993b. Evidence for nm23 RNA overexpression, DNA amplification and mutation in aggressive childhood neuroblastomas. Oncogene 8:855-865.
29. Lombardi D, Sacchi A, D'Agostino G, Tibursi G. 1995. The association of the Nm23-M1 protein and β-tubulin correlates with cell differentiation. Exp Cell Res 217:267-271.
30. MacDonald NJ, De La Rosa A, Benedict MA, Freije JMP, Krutsch H, Steeg PS. 1993. A serine phosphorylation of Nm23, and not its nucleoside diphosphate kinase activity, correlates with suppression of tumor metastatic potential. J Biol Chem 268:25780-25789.
31. MacDonald NJ, Freije JMP, Stracke ML, Manrow RE, Steeg PS. 1996. Site-directed mutagenesis of nm23-H1. Mutation of Proline 96 or Serine 120 abrogates its motility inhibitory activity upon transfection into human breast carcinoma cells. J Biol Chem 271:25107-25116.
32. Martin KK, Pilkington GJ. 1998. Nm23: an invasion suppressor gene in CNS tumors? Anticancer Res 18:919-926.
33. Martinez JA, Prevot S, Nordlinger B, Nguyen TMA, Lacarriere Y, Munier A, Lascu I, Vaillant JC, Capeau J, Lacombe M. 1995. Overexpression of nm23-H1 and nm23-H2 genes in colorectal carcinomas and loss of nm23-H1 expression in advanced tumor stages. Gut 37:712-720.
34. Martinez R, Venturelli D, Perrotti D, Veronese ML, Kastury K, Druck T, Huebner K, Calabretta B. 1997. Gene structure, promoter activity and chromosomal location of the Dr-nm23 gene, a related member of the nm2S gene family. Cancer Res 57:1180-1187.
35. Milon L, Rousseau-Merck M, Munier A, Erent M, Lascu I, Capeau J, Lacombe M. 1997. nm23-H4, a new member of the human nm23/ nucleoside diphosphate kinase gene family localized on chromosome 16q13. Hum Genet 99:550-557.
36. Morera S, Lebras G, Lascu I, Lacombe ML, Veron M, Janin J. 1994. Refined x-ray structure of Dictyostelium discoideum nucleoside diphosphate kinase at 1.8 A resolution. J Mol Biol 243:873-890.
37. Morera S, Lacombe ML, Yingwu X, Lebras G, Janin J. 1995. X-ray structure of human nucleoside diphosphate kinase B complexed with GDP at 2 Å resolution. Structure 3:1307-1314.
38. Munier A, Féral C, Milon L, Phung-Ba Pinon V, Gyapay G, Capeau J, Guellaen G, Lacombe M-L. 1998. A new human nm23 homologue (nm23-H5) specifically expressed in testis germinal cells. FEBS Lett 434:289-294.
39. Munoz-Dorado J, Inouye M, Inouye S. 1990. Nucleoside diphosphate kinase from Myxococcus xanthus. II. Biological carachterization. J Biol Chem 265:2707-2712.
40. Nickerson JA, Wells WW. 1978. Association of nucleoside diphosphate kinase with microtubules. Biochem Biophys Res Commun 85:820-826.
41. 60Co irradiation. FEBS Lett 348:273-277.
42. Okabe-Kado J, Kasukabe T, Honma Y, Hayashi M, Henzel WJ, Hozumi M. 1992. Identity of a differentiation inhibiting factor for mouse myeloid leukemia cells with Nm23/nucleosidediphosphate kinase. Biochem Biophys Res Commun 182:987-994.
43. Okabe-Kado J, Kasukabe T, Hozumi M, Honma Y, Kimura N, Baba H, Urano T, Shiku H. 1995a. A new function of Nm23/NDP kinase as a differentiation inhibitory factor, which does not require it's kinase activity. FEBS Lett 363:311-315.
44. Okabe-Kado J, Kasukabe T, Baba H, Urano T, Shiku H, Honma Y. 1995b. Inhibitory action of nm23 proteins on induction of erythroid differentiation of human leukemia cells. Biochim Biophys Acta 1267:101-106.
45. Okabe-Kado J, Kasukabe T, Honma Y. 1998. Differentiation inhibitory factor Nm23 as a prognostic factor for acute myeloid leukemia. Leuk Lymphoma 32:19-28.
46. Okada K, Urano T, Goi T, Baba H, Yamaguchi A, Furukawa K, Shiku H. 1994. Isolation of human nm23 genomes and analysis of loss of heterozygosity in primary colorectal carcinomas using a specific genomic probe. Cancer Res 51:445-449.
47. Parks RE, Agarwal RP. 1973. Nucleoside diphosphokinases. In: Boyer PD, editor. The enzymes, volume 8. New York: Academic Press, pp. 307-333.
48. Penningroth SM, Kirschner MW. 1977. Nucleotide binding and phosphorylation in microtubule assembly in vitro. J Mol Biol 115:643-673.
49. Phung-Ba-Pinon V, Millot G, Munier A, Vassy J, Linares-Cruz G, Capeau J, Calvo F, Lacombe ML. 1999. Cytoskeletal association of the A and B nucleoside diphosphate kinases of interphasic but not mitotic human carcinoma cell lines: specific nuclear localization of the B subunit. Exp Cell Res 246:355-367.
50. Postel EH, Berberich SJ, Flint SJ, Ferrone CA. 1993. Human c-myc transcription factor PuF identified as nm23-H2 nucleoside diphosphate kinase, a candidate suppressor of tumor metastasis. Science 261:478-480.
51. Postel EH, Ferrone CA. 1994. Nucleoside diphosphate kinase enzyme activity of nm23-H2/PuF is not required for its DNA binding and in vitro transcriptional function. J Biol Chem 269:8627-8630.
52. Postel EH. 1998. Nm23-NDP kinase. Int J Biochem Cell B 30:1291-1295.
53. Rosengard AM, Krutzsch HC, Shearn A, Biggs JR, Barker E, Margulies IMK, King CR, Liotta LA, Steeg PS. 1989. Reduced Nm23/Awd protein in tumor metastasis and aberrant Drosophila development. Nature 342:177-180.
54. Stahl JA, Leone A, Rosengard AM, Porter L, Richter King C, Steeg PS. 1991. Identification of a second human nm23 gene, nm23-H2. Cancer Res 51:445-449.
55. Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, Sobel ME. 1988. Evidence for a novel gene associated with low tumor metastasic potential. J Natl Cancer Inst 80:200-204.
56. Timmons L, Hersperger E, Woodhouse E, Xu J, Liu LZ, Shearn A. 1993. The expression of the Drosophila awd gene during normal development and in neoplastic brain tumors caused by lgl mutations. Dev Biol 158:364-379.
57. Timmons L, Shearn A. 1997. prune/Killer of prune: a conditional dominant lethal interaction in Drosophila. Adv Genet 35:207-252.
58. Urano T, Takamiya K, Furukawa K, Shiku H. 1992. Molecular cloning and functional expression of the second mouse nm23/NDP kinase gene, nm23-M2. FEBS Lett 309:358-362.
59. Varesco L, Caligo MA, Simi P, Black DM, Nardini V, Casarino L, Rocchi M, Ferrara G, Solomon E, Bevilacqua G. 1992. The nm23 gene maps to human chromosome band 17q22 and shows a restriction fragment length polymorphism with. BglII. Genes Chromosomes Cancer 4:84-88.
60. Venturelli D, Martinez R, Melotti P, Casella I, Peschle C, Cucco C, Spampinato G, Darzynkiewicz Z, Calabretta B. 1995. Overexpression of DR-nm23, a protein encoded by a member of the nm23 gene family, inhibits granulocyte differentiation and induces apoptosis in 32Dc13 myeloid cells. Proc Natl Acad Sci USA 92:7435-7439.
61. Wagner PD, Vu ND. 1995. Phosphorylation of ATP-citrate lyase by nucleoside diphosphate kinase. J Biol Chem 270:21758-21764.
62. Wagner PD, Steeg PS, Vu ND. 1997. Two-component kinase-like activity of nm23 correlates with its motility-suppressing activity. Proc Natl Acad Sci USA 94:9000-9005.
63. Wallet V, Mutzel R, Troll H, Barzu O, Wurster B, Veron M, Lacombe M-L. 1990. Dictyostelium nucleoside diphosphate kinase highly homologous to Nm23 and Awd proteins involved in mammalian tumor metastasis and Drosophilia development. J Natl Cancer Inst 82: 1199-1201.
64. Webb PA, Perisic O, Mendola CE, Backer JM, Williams RL. 1995. The crystal structure of a human nucleoside diphosphate kinase, Nm23-H2. J Mol Biol 251:574-587.
65. Willems R, Van Bockstaele DR, Lardon F, Lenjou M, Nijs G, Snoeck H-W, Berneman ZN, Slegers H. 1998. Decrease in nucleoside diphosphate kinase (NDPK/nm23) expression during hematopoietic maturation. J Biol Chem 273:13663-13668.
66. Williams RL, Oren DA, Munoz-Dorado J, Inouye S, Inouye M, Arnold E. 1993. Crystal structure of Myxococcus xanthus nucleoside diphosphate kinase and its interaction with a nucleotide substrate at 2.0 Å resolution. J Mol Biol 234:1230-1247.
67. Yamashiro S, Urano T, Shiku K, Furukawa K. 1994. Alteration of nm23 gene expression during the induced differentiation of human leukemia cell lines. Oncogene 9:2461-2468.
68. k-pn, a homologue of the metastasis suppressor gene nm23, suppresses the Tum-1 haematopoietic oncogene. Nat Genet 4:195-201.