Cell and Tissue Research

, Volume 322, Issue 3, pp 365–378 | Cite as

Expression patterns of nm23 genes during mouse organogenesis

  • Lilian Amrein
  • Perrine Barraud
  • Jean-Yves Daniel
  • Yves Pérel
  • Marc Landry
Regular Article

Abstract

Nucleoside di-phosphate kinase enzyme (NDPK) isoforms, encoded by the nm23 family of genes, may be involved in various cellular differentiation and proliferation processes. We have therefore analyzed the expression of nm23-M1, -M2, -M3, and -M4 during embryonic mouse development. In situ hybridization data has revealed the differential expression of nm23 mRNA during organogenesis. Whereas nm23-M1 and -M3 are preferentially expressed in the nervous and sensory systems, nm23-M2 mRNA is found ubiquitously. Irrespective of the developmental state studied, nm23-M4 mRNA is only expressed at low levels in a few embryonic organs. In the cerebellum and cerebral cortex, nm23-M1, -M2, and -M3 are present in the neuronal differentiation layer, whereas nm23-M4 mRNA is distributed in the proliferating layer. Thus, nm23 mRNA is differentially expressed, and the diverse NDPK isoforms are sequentially involved in various developmental processes.

Keywords

Nucleoside diphosphate kinase nm23 Embryonic development Nervous system Differential expression Mouse (C57BL/6) 

References

  1. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–457CrossRefPubMedGoogle Scholar
  2. Amendola R, Martinez R, Negroni A, Venturelli D, Tanno B, Calabretta B, Raschella G (1997) DR-nm23 gene expression in neuroblastoma cells: relationship to integrin expression, adhesion characteristics, and differentiation. J Nat Cancer Inst 89:1300–1310CrossRefPubMedGoogle Scholar
  3. Arcinas M, Boxer LM (1994) Differential protein binding to the c-myc promoter during differentiation of hematopoietic cell lines. Oncogene 9:2699–2706PubMedGoogle Scholar
  4. Barraud P, Amrein L, Dobremez E, Dabernat S, Massé K, Larou M, Daniel JY, Landry M (2002) Differential expression of nm23 genes in adult mouse dorsal root ganglia. J Comp Neurol 444:306–323CrossRefPubMedGoogle Scholar
  5. Berberich SJ, Postel EH (1995) PuF/NM23-H2/NDPK-B transactivates a human c-myc promoter-CAT gene via a functional nuclease hypersensitive element. Oncogene 10:2343–2347PubMedGoogle Scholar
  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 63:933–940CrossRefPubMedGoogle Scholar
  7. Caviness VS Jr, Takahashi T (1995) Proliferative events in the cerebral ventricular zone. Brain Dev 17:159–163CrossRefPubMedGoogle Scholar
  8. Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82:631–641CrossRefPubMedGoogle Scholar
  9. Colvin JS, Feldman B, Nadeau JH, Goldfarb M, Ornitz DM (1999) Genomic organization and embryonic expression of the mouse fibroblast growth factor 9 gene. Dev Dyn 216:72–88CrossRefPubMedGoogle Scholar
  10. Coskun V, Luskin MB (2002) Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J Neurosci Res 69:795–802CrossRefPubMedGoogle Scholar
  11. Dabernat S, Larou M, Masse K, Dobremez E, Landry M, Mathieu C, Daniel JY (1999a) Organization and expression of mouse nm23-M1 gene. Comparison with nm23-M2 expression. Gene 236:221–230CrossRefPubMedGoogle Scholar
  12. Dabernat S, Larou M, Massé K, Hokfelt T, Mayer G, Daniel JY, Landry M (1999b) 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 63:351–365CrossRefPubMedGoogle Scholar
  13. Dagerlind A, Friberg K, Bean AJ, Hokfelt T (1992) Sensitive mRNA detection using unfixed tissue: combined radioactive and non-radioactive in situ hybridization histochemistry. Histochemistry 98:39–49PubMedCrossRefGoogle Scholar
  14. D'Angelo A, Zollo M (2004) Unraveling genes and pathways influenced by H-prune PDE overexpression: a model to study cellular motility. Cell Cycle 3:758–761PubMedGoogle Scholar
  15. Dearolf CR, Hersperger E, Shearn A (1988) Developmental consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev Biol 129:159–168CrossRefPubMedGoogle Scholar
  16. Feijen A, Goumans MJ, Eijnden-van Raaij AJ van den (1994) Expression of activin subunits, activin receptors and follistatin in postimplantation mouse embryos suggests specific developmental functions for different activins. Development 120:3621–3637PubMedGoogle Scholar
  17. Fukuchi T, Shimada N, Hanai N, Ishikawa N, Watanabe K, Kimura N (1994) Recombinant rat nucleoside diphosphate kinase isoforms-(alpha and beta)-purification, properties and application to immunological detection of native isoforms in rat tissues. Biochim Biophys Acta 1205:113–122PubMedGoogle Scholar
  18. 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 Differ 7:1689–1695PubMedGoogle Scholar
  19. 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 17:1047–1055PubMedCrossRefGoogle Scholar
  20. Hartsough MT, Steeg PS (2000) Nm23/nucleoside diphosphate kinase in human cancers. J Bioenerg Biomembr 32:301–308CrossRefPubMedGoogle Scholar
  21. Ishijima Y, Shimada N, Fukuda M, Miyazaki H, Orlov NY, Orlova TG, Yamada T, Kimura N (1999) Overexpression of nucleoside diphosphate kinases induces neurite outgrowth and their substitution to inactive forms leads to suppression of nerve growth factor- and dibutyryl cyclic AMP-induced effects in PC12D cells. FEBS Lett 445:155–159CrossRefPubMedGoogle Scholar
  22. Jankovski A, Sotelo C (1996) Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochronic and heterotopic transplantation. J Comp Neurol 371:376–396CrossRefPubMedGoogle Scholar
  23. Kargul GJ, Nagaraja R, Shimada T, Grahovac MJ, Lim MK, Nakashima H, Waeltz P, Ma P, Chen E, Schlessinger D, Ko MS (2000) Eleven densely clustered genes, six of them novel, in 176 kb of mouse t-complex DNA. Genome Res 10:916–923CrossRefPubMedGoogle Scholar
  24. Kimura N, Shimada N, Nomura K, Watanabe K (1990) Isolation and characterization of a cDNA clone encoding rat nucleoside diphosphate kinase. J Biol Chem 265:15744–15749PubMedGoogle Scholar
  25. Kimura N, Shimada N, Fukuda M, Ishijima Y, Miyazaki H, Ishii A, Takagi Y, Ishikawa N (2000) Regulation of cellular functions by nucleoside diphosphate kinases in mammals. J Bioenerg Biomembr 32:309–315CrossRefPubMedGoogle Scholar
  26. Kraeft SK, Traincart F, Mesnildrey S, Bourdais J, Veron M, Chen LB (1996) Nuclear localization of nucleoside diphosphate kinase type B (nm23-H2) in cultured cells. Exp Cell Res 227:63–69CrossRefPubMedGoogle Scholar
  27. Kuhar SG, Feng L, Vidan S, Ross ME, Hatten ME, Heintz N (1993) Changing patterns of gene expression define four stages of cerebellar granule neuron differentiation. Development 117:97–104PubMedGoogle Scholar
  28. Lacombe ML, Wallet V, Troll H, Veron M (1990) Functional cloning of a nucleoside diphosphate kinase from Dictyostelium discoideum. J Biol Chem 265:10012–10018PubMedGoogle Scholar
  29. Lacombe ML, Milon L, Munier A, Mehus JG, Lambeth DO (2000) The human Nm23/nucleoside diphosphate kinases. J Bioenerg Biomembr 32:247–258CrossRefPubMedGoogle Scholar
  30. Lakso M, Steeg PS, Westphal H (1992) Embryonic expression of nm23 during mouse organogenesis. Cell Growth Differ 3:873–879PubMedGoogle Scholar
  31. Landry M, Calas A (2002) Immunohistochemistry and in situ hybridization: interest of their various combinations for cytofunctional approaches of central and peripheral neurons. In: Carmignoto G, Merighi A (eds) Cellular and molecular methods in neurobiology. Springer, Berlin Heidleberg New York, pp 10-20Google Scholar
  32. Lawson SN, Biscoe TJ (1979) Development of mouse dorsal root ganglia: an autoradiographic and quantitative study. J Neurocytol 8:265–274CrossRefPubMedGoogle Scholar
  33. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148PubMedCrossRefGoogle Scholar
  34. Lombardi D, Sacchi A, D'Agostino G, Tibursi G (1995) The association of the Nm23-M1 protein and beta-tubulin correlates with cell differentiation. Exp Cell Res 217:267–271CrossRefPubMedGoogle Scholar
  35. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189CrossRefPubMedGoogle Scholar
  36. Luskin MB (1998) Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J Neurobiol 36:221–233CrossRefPubMedGoogle Scholar
  37. Massé K, Dabernat S, Bourbon PM, Larou M, Amrein L, Barraud P, Perel Y, Camara M, Landry M, Lacombe ML, Daniel JY (2002) Characterization of the nm23-M2, nm23-M3 and nm23-M4 mouse genes: comparison with their human orthologs. Gene 296:87–97CrossRefPubMedGoogle Scholar
  38. Mehus JG, Deloukas P, Lambeth DO (1999) NME6: a new member of the nm23/nucleoside diphosphate kinase gene family located on human chromosome 3p21.3. Hum Genet 104:454–459CrossRefPubMedGoogle Scholar
  39. Menezes JR, Smith CM, Nelson KC, Luskin MB (1995) The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol Cell Neurosci 6:496–508CrossRefPubMedGoogle Scholar
  40. Mesnildrey S, Agou F, Karlsson A, Bonne DD, Veron M (1998) Coupling between catalysis and oligomeric structure in nucleoside diphosphate kinase. J Biol Chem 273:4436–4442CrossRefPubMedGoogle Scholar
  41. Milon L, Rousseau-Merck MF, Munier A, Erent M, Lascu I, Capeau J, Lacombe ML (1997) nm23-H4, a new member of the family of human nm23/nucleoside diphosphate kinase genes localised on chromosome 16p13. Hum Genet 99:550–557CrossRefPubMedGoogle Scholar
  42. Munier A, Feral C, Milon L, Pinon VP, Gyapay G, Capeau J, Guellaen G, Lacombe ML (1998) A new human nm23 homologue (nm23-H5) specifically expressed in testis germinal cells. FEBS Lett 434:289–294CrossRefPubMedGoogle Scholar
  43. Munoz-Dorado J, Inouye M, Inouye S (1990) Nucleoside diphosphate kinase from Myxococcus xanthus. I. Cloning and sequencing of the gene. J Biol Chem 265:2702–2706PubMedGoogle Scholar
  44. Murphy M, Reid K, Brown MA, Bartlett PF (1993) Involvement of leukemia inhibitory factor and nerve growth factor in the development of dorsal root ganglion neurons. Development 117:1173–1182PubMedGoogle Scholar
  45. Otero AS (1997) Copurification of vimentin, energy metabolism enzymes, and a MER5 homolog with nucleoside diphosphate kinase. Identification of tissue-specific interactions. J Biol Chem 272:14690–14694CrossRefPubMedGoogle Scholar
  46. Otero AS (2000) NM23/nucleoside diphosphate kinase and signal transduction. J Bioenerg Biomembr 32:269–275CrossRefPubMedGoogle Scholar
  47. Ouatas T, Abdallah B, Gasmi L, Bourdais J, Postel E, Mazabraud A (1997) Three different genes encode NM23/nucleoside diphosphate kinases in Xenopus laevis. Gene 194:215–225CrossRefPubMedGoogle Scholar
  48. Ouatas T, Selo M, Sadji Z, Hourdry J, Denis H, Mazabraud A (1998) Differential expression of nucleoside diphosphate kinases (NDPK/NM23) during Xenopus early development. Int J Dev Biol 42:43–52PubMedGoogle Scholar
  49. Parks RE Jr, Agarwal RP (1973) Nucleoside diphosphokinases. In: Boyer PD (ed)The enzymes, vol 8, 3rd edn. Academic, New York, pp 307–334Google Scholar
  50. Pinon VP, 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 246:355–367CrossRefPubMedGoogle Scholar
  51. 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 261:478–480PubMedCrossRefGoogle Scholar
  52. Postel EH, Berberich SJ, Rooney JW, Kaetzel DM (2000) Human NM23/nucleoside diphosphate kinase regulates gene expression through DNA binding to nuclease-hypersensitive transcriptional elements. J Bioenerg Biomembr 32:277–284CrossRefPubMedGoogle Scholar
  53. Price J, Thurlow L (1988) Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development 104:473–482PubMedGoogle Scholar
  54. Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176PubMedCrossRefGoogle Scholar
  55. Reid CB, Liang I, Walsh C (1995) Systematic widespread clonal organization in cerebral cortex. Neuron 15:299–310CrossRefPubMedGoogle Scholar
  56. Reymond A, Volorio S, Merla G, Al-Maghtheh M, Zuffardi O, Bulfone A, Ballabio A, Zollo M (1999) Evidence for interaction between human PRUNE and nm23-H1 NDPKinase. Oncogene 18:7244–7252CrossRefPubMedGoogle Scholar
  57. Shimada N, Ishikawa N, Munakata Y, Toda T, Watanabe K, Kimura N (1993) A second form (beta isoform) of nucleoside diphosphate kinase from rat. Isolation and characterization of complementary and genomic DNA and expression. J Biol Chem 268:2583–2589PubMedGoogle Scholar
  58. Smith CM, Luskin MB (1998) Cell cycle length of olfactory bulb neuronal progenitors in the rostral migratory stream. Dev Dyn 213:220–227CrossRefPubMedGoogle Scholar
  59. Stahl JA, Leone A, Rosengard AM, Porter L, King CR, Steeg PS (1991) Identification of a second human nm23 gene, nm23-H2. Cancer Res 51:445–449PubMedGoogle Scholar
  60. Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, Sobel ME (1988a) Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 80:200–204PubMedCrossRefGoogle Scholar
  61. Steeg PS, Bevilacqua G, Pozzatti R, Liotta LA, Sobel ME (1988b) Altered expression of NM23, a gene associated with low tumor metastatic potential, during adenovirus 2 Ela inhibition of experimental metastasis. Cancer Res 48:6550–6554PubMedGoogle Scholar
  62. Stewart J, Rodaros D (1999) The effects of gonadal hormones on the development and expression of the stimulant effects of morphine in male and female rats. Behav Brain Res 102:89–98CrossRefPubMedGoogle Scholar
  63. Stewart RR, Hoge GJ, Zigova T, Luskin MB (2002) Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABA(A) receptors. J Neurobiol 50:305–322CrossRefPubMedGoogle Scholar
  64. 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 158:364–379CrossRefPubMedGoogle Scholar
  65. Tsuiki H, Nitta M, Furuya A, Hanai N, Fujiwara T, Inagaki M, Kochi M, Ushio Y, Saya H, Nakamura H (2000) A novel human nucleoside diphosphate (NDP) kinase, Nm23-H6, localizes in mitochondria and affects cytokinesis. J Cell Biochem 76:254–269CrossRefGoogle Scholar
  66. 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 309:358–362CrossRefPubMedGoogle Scholar
  67. 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 U S A 92:7435–7439PubMedCrossRefGoogle Scholar
  68. Walsh C, Cepko CL (1988) Clonally related cortical cells show several migration patterns. Science 241:1342–1345PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Lilian Amrein
    • 1
  • Perrine Barraud
    • 1
  • Jean-Yves Daniel
    • 1
  • Yves Pérel
    • 1
  • Marc Landry
    • 2
  1. 1.EA DRED 483, Laboratoire de Biologie de la Différenciation et du DéveloppementUniversité Victor SégalenBordeaux CedexFrance
  2. 2.INSERM E 358, Institut Francois MagendieUniversité Bordeaux 2Bordeaux CedexFrance

Personalised recommendations