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Learning about the functions of NME/NM23: lessons from knockout mice to silencing strategies

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Abstract

The human NME gene family (also known as NM23) comprises ten genes that are involved in diverse physiological and pathological processes including proliferation, differentiation, development, ciliary functions, and metastasis. For the moment, only the NME1, NME2, and NME7 genes have been inactivated in transgenic knockout mice, as well as a double NME1–NME2 gene knockout. Mice lacking NME1 or NME2 grow to adulthood without health problems, although NME1 −/− mice have modest growth retardation. Double knockout NME1 −/−NME2 −/− mice, by contrast, are highly hypotrophic and die at birth from profound anemia due to impaired erythroblast development. Evidence for a metastasis suppressor function of NME1 in vivo comes from crossing NME1 −/− mice with mice prone to develop hepatocellular carcinoma; the double transgenic mice present a higher incidence of lung metastases. Silencing of NME1 by siRNA interference has confirmed this function by conferring a “metastatic phenotype” on non-invasive human epithelial cancer cell lines. This function is specific to NME1 and is not observed when the NME2 is silenced. The data indicate that NME1 loss is causally involved at the early stages of the metastatic cascade. NME2 −/− mice and NME2 silencing experiments reveal a specific role of NME2 in activation of heterotrimeric G proteins and of KCa3.1 channel in T cells, pointing to a role of NME2 as a histidine phosphotransferase. Regarding NME7, consistent with its expression in axonemal structures, NME7 −/− mice present lesions similar to primary ciliary dyskinesia. This review summarizes the recent data obtained by knockout and silencing of NME/NM23 genes that provide mechanistic insights into their respective roles in physiology and pathology.

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References

  • Aktary Z, Chapman K, Lam L, Lo A, Ji C, Graham K, Cook L, Li L, Mackey JR, Pasdar M (2010) Plakoglobin interacts with and increases the protein levels of metastasis suppressor Nm23-H2 and regulates the expression of Nm23-H1. Oncogene 29:2118–2129

    Article  PubMed  CAS  Google Scholar 

  • Arnaud-Dabernat S, Bourbon PM, Dierich A, Le Meur M, Daniel JY (2003) Knockout mice as model systems for studying nm23/NDP kinase gene functions. Application to the nm23-M1 gene. J Bioenerg Biomembr 35:19–30

    Article  PubMed  CAS  Google Scholar 

  • Atfi A, Djelloul S, Chastre E, Davis R, Gespach C (1997) Evidence for a role of Rho-like GTPases and stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK) in transforming growth factor beta-mediated signaling. J Biol Chem 272:1429–1432

    Article  PubMed  CAS  Google Scholar 

  • Bakalian S, Marshall JC, Faingold D, Logan P, Antecka E, Burnier MN Jr (2007) Expression of nm23-H1 in uveal melanoma. Melanoma Res 17:284–290

    Article  PubMed  CAS  Google Scholar 

  • Bilitou A, Ohnuma S (2010) The role of cell cycle in retinal development: cyclin-dependent kinase inhibitors co-ordinate cell-cycle inhibition, cell-fate determination and differentiation in the developing retina. Dev Dynam 239:727–736

    Article  CAS  Google Scholar 

  • Bilitou A, Watson J, Gartner A, Ohnuma S (2009) The NM23 family in development. Mol Cell Biochem 329:17–33

    Article  PubMed  CAS  Google Scholar 

  • Boissan M, Wendum D, Arnaud-Dabernat S, Munier A, Debray M, Lascu I, Daniel JY, Lacombe ML (2005) Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma. J Natl Canc Inst 97:836–845

    Article  CAS  Google Scholar 

  • Boissan M, Dabernat S, Peuchant E, Schlattner U, Lascu I, Lacombe ML (2009) The mammalian Nm23/NDPK family: from metastasis control to cilia movement. Mol Cell Biochem 329:51–62

    Article  PubMed  CAS  Google Scholar 

  • Boissan M, De Wever O, Lizarraga F, Wendum D, Poincloux R, Chignard N, Desbois-Mouthon C, Dufour S, Nawrocki-Raby B, Birembaut P, Bracke M, Chavrier P, Gespach C, Lacombe ML (2010) Implication of metastasis suppressor NM23-H1 in maintaining adherens junctions and limiting the invasive potential of human cancer cells. Canc Res 70:7710–7722

    Article  CAS  Google Scholar 

  • Bowden ET, Onikoyi E, Slack R, Myoui A, Yoneda T, Yamada KM, Mueller SC (2006) Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp Cell Res 312:1240–1253

    Article  PubMed  CAS  Google Scholar 

  • Brooks TA, Hurley LH (2010) Targeting MYC Expression through G-Quadruplexes. Genes Cancer 1:641–649

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Choi YJ, Cho SK, Hwang KC, Park C, Kim JH, Park SB, Hwang S (2009) Nm23-M5 mediates round and elongated spermatid survival by regulating GPX-5 levels. FEBS Lett 583:1292–1298

    Article  PubMed  CAS  Google Scholar 

  • Chowdhury D, Beresford PJ, Zhu P, Zhang D, Sung JS, Demple B, Perrino FW, Lieberman J (2006) The exonuclease TREX1 is in the SET complex and acts in concert with NM23-H1 to degrade DNA during granzyme A-mediated cell death. Mol Cell 23:133–142

    Article  PubMed  CAS  Google Scholar 

  • Conery AR, Sever S, Harlow E (2010) Nucleoside diphosphate kinase Nm23-H1 regulates chromosomal stability by activating the GTPase dynamin during cytokinesis. Proc Natl Acad Sci U S A 107:15461–15466

    Article  PubMed  CAS  Google Scholar 

  • Cuello F, Schulze RA, Heemeyer F, Meyer HE, Lutz S, Jakobs KH, Niroomand F, Wieland T (2003) Activation of heterotrimeric G proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gbeta subunits. Complex formation of NDPK B with Gbeta gamma dimers and phosphorylation of His-266 IN Gbeta. J Biol Chem 278:7220–7226

    Article  PubMed  CAS  Google Scholar 

  • Curtis CD, Likhite VS, McLeod IX, Yates JR, Nardulli AM (2007) Interaction of the tumor metastasis suppressor nonmetastatic protein 23 homologue H1 and estrogen receptor alpha alters estrogen-responsive gene expression. Canc Res 67:10600–10607

    Article  CAS  Google Scholar 

  • Desvignes T, Pontarotti P, Fauvel C, Bobe J (2009) Nme protein family evolutionary history, a vertebrate perspective. BMC Evol Biol 9:256

    Article  PubMed  Google Scholar 

  • Dexheimer TS, Carey SS, Zuohe S, Gokhale VM, Hu X, Murata LB, Maes EM, Weichsel A, Sun D, Meuillet EJ, Montfort WR, Hurley LH (2009) NM23-H2 may play an indirect role in transcriptional activation of c-myc gene expression but does not cleave the nuclease hypersensitive element III1. Mol Canc Therapeut 8:1363–1377

    Article  CAS  Google Scholar 

  • Di L, Srivastava S, Zhdanova O, Sun Y, Li Z, Skolnik EY (2010) Nucleoside diphosphate kinase B knock-out mice have impaired activation of the K+ channel KCa3.1, resulting in defective T cell activation. J Biol Chem 285:38765–38771

    Article  PubMed  CAS  Google Scholar 

  • Duran MC, Vega F, Moreno-Bueno G, Artiga MJ, Sanchez L, Palacios J, Ridley A, Timms JF (2008) Characterisation of tumoral markers correlated with ErbB2 (HER2/Neu) overexpression and metastasis in breast cancer. Proteomics Clin Appl 2:1313–1326

    Article  PubMed  CAS  Google Scholar 

  • Duriez B, Duquesnoy P, Escudier E, Bridoux AM, Escalier D, Rayet I, Marcos E, Vojtek AM, Bercher JF, Amselem S (2007) A common variant in combination with a nonsense mutation in a member of the thioredoxin family causes primary ciliary dyskinesia. Proc Natl Acad Sci U S A 104:3336–3341

    Article  PubMed  CAS  Google Scholar 

  • Empereur S, Djelloul S, Di Gioia Y, Bruyneel E, Mareel M, Van Hengel J, Van Roy F, Comoglio P, Courtneidge S, Paraskeva C, Chastre E, Gespach C (1997) Progression of familial adenomatous polyposis (FAP) colonic cells after transfer of the src or polyoma middle T oncogenes: cooperation between src and HGF/Met in invasion. Br J Cancer 75:241–250

    Article  PubMed  CAS  Google Scholar 

  • Esufali S, Bapat B (2004) Cross-talk between Rac1 GTPase and dysregulated Wnt signaling pathway leads to cellular redistribution of beta-catenin and TCF/LEF-mediated transcriptional activation. Oncogene 23:8260–8271

    Article  PubMed  CAS  Google Scholar 

  • Evans RJ, Schwarz N, Nagel-Wolfrum K, Wolfrum U, Hardcastle AJ, Cheetham ME (2010) The retinitis pigmentosa protein RP2 links pericentriolar vesicle transport between the Golgi and the primary cilium. Hum Mol Genet 19:1358–1367

    Article  PubMed  CAS  Google Scholar 

  • Fan Z, Beresford PJ, Oh DY, Zhang D, Lieberman J (2003) Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell 112:659–672

    Article  PubMed  CAS  Google Scholar 

  • Fodde R, Brabletz T (2007) Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19:150–158

    Article  PubMed  CAS  Google Scholar 

  • Frame MC (2004) Newest findings on the oldest oncogene; how activated src does it. J Cell Sci 117:989–998

    Article  PubMed  CAS  Google Scholar 

  • Garinis GA, Manolis EN, Spanakis NE, Patrinos GP, Peros G, Menounos PG (2003) High frequency of concomitant nm23-H1 and E-cadherin transcriptional inactivation in primary non-inheriting colorectal carcinomas. J Mol Med 81:256–263

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hauck CR, Hsia DA, Puente XS, Cheresh DA, Schlaepfer DD (2002) FRNK blocks v-Src-stimulated invasion and experimental metastases without effects on cell motility or growth. EMBO J 21:6289–6302

    Article  PubMed  CAS  Google Scholar 

  • Hippe HJ, Wolf NM, Abu-Taha I, Mehringer R, Just S, Lutz S, Niroomand F, Postel EH, Katus HA, Rottbauer W, Wieland T (2009) The interaction of nucleoside diphosphate kinase B with Gbetagamma dimers controls heterotrimeric G protein function. Proc Natl Acad Sci U S A 106:16269–16274

    Article  PubMed  CAS  Google Scholar 

  • Hippe HJ, Abu-Taha I, Wolf NM, Katus HA, Wieland T (2011) Through scaffolding and catalytic actions nucleoside diphosphate kinase B differentially regulates basal and beta-adrenoceptor-stimulated cAMP synthesis. Cell Signal 23:579–585

    Article  PubMed  CAS  Google Scholar 

  • Hlubek F, Spaderna S, Jung A, Kirchner T, Brabletz T (2004) Beta-catenin activates a coordinated expression of the proinvasive factors laminin-5 gamma2 chain and MT1-MMP in colorectal carcinomas. Int J Canc 108:321–326

    Article  CAS  Google Scholar 

  • Horak CE, Lee JH, Elkahloun AG, Boissan M, Dumont S, Maga TK, Arnaud-Dabernat S, Palmieri D, Stetler-Stevenson WG, Lacombe ML, Meltzer PS, Steeg PS (2007) Nm23-H1 suppresses tumor cell motility by down-regulating the lysophosphatidic acid receptor EDG2. Canc Res 67:7238–7246

    Article  CAS  Google Scholar 

  • Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ (2006) A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Gene Dev 20:2673–2686

    Article  PubMed  CAS  Google Scholar 

  • Hsu T, Adereth Y, Kose N, Dammai V (2006) Endocytic function of von Hippel-Lindau tumor suppressor protein regulates surface localization of fibroblast growth factor receptor 1 and cell motility. J Biol Chem 281:12069–12080

    Article  PubMed  CAS  Google Scholar 

  • Ikeda T (2010) NDP kinase 7 is a conserved microtubule-binding protein preferentially expressed in ciliated cells. Cell Struct Funct 35:23–30

    Article  PubMed  CAS  Google Scholar 

  • Jung H, Seong HA, Ha H (2007) NM23-H1 tumor suppressor and its interacting partner STRAP activate p53 function. J Biol Chem 282:35293–35307

    Article  PubMed  CAS  Google Scholar 

  • Jung H, Seong HA, Ha H (2008) Direct interaction between NM23-H1 and macrophage migration inhibitory factor (MIF) is critical for alleviation of MIF-mediated suppression of p53 activity. J Biol Chem 283:32669–32679

    Article  PubMed  CAS  Google Scholar 

  • Kadono Y, Okada Y, Namiki M, Seiki M, Sato H (1998) Transformation of epithelial Madin-Darby canine kidney cells with p60(v-src) induces expression of membrane-type 1 matrix metalloproteinase and invasiveness. Canc Res 58:2240–2244

    CAS  Google Scholar 

  • Kaetzel DM, Zhang Q, Yang M, McCorkle JR, Ma D, Craven RJ (2006) Potential roles of 3′-5′ exonuclease activity of NM23-H1 in DNA repair and malignant progression. J Bioenerg Biomembr 38:163–167

    Article  PubMed  CAS  Google Scholar 

  • Kapetanovich L, Baughman C, Lee TH (2005) Nm23H2 facilitates coat protein complex II assembly and endoplasmic reticulum export in mammalian cells. Mol Biol Cell 16:835–848

    Article  PubMed  CAS  Google Scholar 

  • Kartagener M, Horlacher A (1936) Situs viscerum inversus und Polyposis nasi in einem Falle familiaerer Bronchiektasien. Bietr Klin Tuberk 87:331–333

    Article  Google Scholar 

  • Kim HD, Youn B, Kim TS, Kim SH, Shin HS, Kim J (2009) Regulators affecting the metastasis suppressor activity of Nm23-H1. Mol Cell Biochem 329:167–173

    Article  PubMed  CAS  Google Scholar 

  • Klumpp S, Krieglstein J (2009) Reversible phosphorylation of histidine residues in proteins from vertebrates. Sci Signal 2:pe13

    Article  PubMed  Google Scholar 

  • Kopitz C, Gerg M, Bandapalli OR, Ister D, Pennington CJ, Hauser S, Flechsig C, Krell HW, Antolovic D, Brew K, Nagase H, Stangl M, von Weyhern CW, Brucher BL, Brand K, Coussens LM, Edwards DR, Kruger A (2007) Tissue inhibitor of metalloproteinases-1 promotes liver metastasis by induction of hepatocyte growth factor signaling. Canc Res 67:8615–8623

    Article  CAS  Google Scholar 

  • Kotelevets L, Noe V, Bruyneel E, Myssiakine E, Chastre E, Mareel M, Gespach C (1998) Inhibition by platelet-activating factor of Src- and hepatocyte growth factor-dependent invasiveness of intestinal and kidney epithelial cells. Phosphatidylinositol 3′-kinase is a critical mediator of tumor invasion. J Biol Chem 273:14138–14145

    Article  PubMed  CAS  Google Scholar 

  • Kotelevets L, van Hengel J, Bruyneel E, Mareel M, van Roy F, Chastre E (2005) Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J 19:115–117

    PubMed  CAS  Google Scholar 

  • Lacombe ML, Milon L, Munier A, Mehus JG, Lambeth DO (2000) The human Nm23/nucleoside diphosphate kinases. J Bioenerg Biomembr 32:247–258

    Article  PubMed  CAS  Google Scholar 

  • Lee HY, Lee H (1999) Inhibitory activity of nm23-H1 on invasion and colonization of human prostate carcinoma cells is not mediated by its NDP kinase activity. Canc Lett 145:93–99

    Article  CAS  Google Scholar 

  • Lee JH, Marshall JC, Steeg PS, Horak CE (2009) Altered gene and protein expression by Nm23-H1 in metastasis suppression. Mol Cell Biochem 329:141–148

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Nie CJ, Hu L, Qin Y, Liu HB, Zeng TT, Chen L, Fu L, Deng W, Chen SP, Jia WH, Zhang C, Xie D, Guan XY (2010) Characterization of a novel mechanism of genomic instability involving the SEI1/SET/NM23H1 pathway in esophageal cancers. Canc Res 70:5695–5705

    Article  CAS  Google Scholar 

  • Ma W, Chen J, Xue X, Wang Z, Liu H, Wang T, Bai Y, Tang SC, Zhou Q (2008) Alteration in gene expression profile and biological behavior in human lung cancer cell line NL9980 by nm23-H1 gene silencing. Biochem Biophys Res Commun 371:425–430

    Article  PubMed  CAS  Google Scholar 

  • Majumder R, Krishnan KS (2010) Synaptic vesicle recycling: genetic and cell biological studies. J Neurogenet 24:146–157

    Article  PubMed  CAS  Google Scholar 

  • Marshall WF (2008) The cell biological basis of ciliary disease. J Cell Biol 180:17–21

    Article  PubMed  CAS  Google Scholar 

  • 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 296:87–97

    Article  PubMed  Google Scholar 

  • McDermott WG, Boissan M, Lacombe ML, Steeg PS, Horak CE (2008) Nm23-H1 homologs suppress tumor cell motility and anchorage independent growth. Clin Exp Metastasis 25:131–138

    Article  PubMed  CAS  Google Scholar 

  • Miller JH, Funchain P, Clendenin W, Huang T, Nguyen A, Wolff E, Yeung A, Chiang JH, Garibyan L, Slupska MM, Yang H (2002) Escherichia coli strains (ndk) lacking nucleoside diphosphate kinase are powerful mutators for base substitutions and frameshifts in mismatch-repair-deficient strains. Genetics 162:5–13

    PubMed  CAS  Google Scholar 

  • Mochizuki T, Bilitou A, Waters CT, Hussain K, Zollo M, Ohnuma S (2009) Xenopus NM23-X4 regulates retinal gliogenesis through interaction with p27Xic1. Neural Dev 4:1

    Article  PubMed  Google Scholar 

  • Munier A, Serres C, Kann ML, Boissan M, Lesaffre C, Capeau J, Fouquet JP, Lacombe ML (2003) Nm23/NDP kinases in human male germ cells: role in spermiogenesis and sperm motility? Exp Cell Res 289:295–306

    Article  PubMed  CAS  Google Scholar 

  • Nakahara H, Howard L, Thompson EW, Sato H, Seiki M, Yeh Y, Chen WT (1997) Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc Natl Acad Sci U S A 94:7959–7964

    Article  PubMed  CAS  Google Scholar 

  • Nallamothu G, Woolworth JA, Dammai V, Hsu T (2008) Awd, the homolog of metastasis suppressor gene Nm23, regulates Drosophila epithelial cell invasion. Mol Cell Biol 28:1964–1973

    Article  PubMed  CAS  Google Scholar 

  • Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Canc 9:274–284

    Article  CAS  Google Scholar 

  • Niitsu N, Nakamine H, Okamoto M (2011) Expression of nm23-H1 is associated with poor prognosis in peripheral T-cell lymphoma, not otherwise specified. Clin Canc Res (in press)

  • Nordman J, Wright A (2008) The relationship between dNTP pool levels and mutagenesis in an Escherichia coli NDP kinase mutant. Proc Natl Acad Sci U S A 105:10197–10202

    Article  PubMed  CAS  Google Scholar 

  • Otero AS (2000) NM23/nucleoside diphosphate kinase and signal transduction. J Bioenerg Biomembr 32:269–275

    Article  PubMed  CAS  Google Scholar 

  • Otsuki Y, Tanaka M, Yoshii S, Kawazoe N, Nakaya K, Sugimura H (2001) Tumor metastasis suppressor nm23H1 regulates Rac1 GTPase by interaction with Tiam1. Proc Natl Acad Sci U S A 98:4385–4390

    Article  PubMed  CAS  Google Scholar 

  • Palacios F, Schweitzer JK, Boshans RL, D’Souza-Schorey C (2002) ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat Cell Biol 4:929–936

    Article  PubMed  CAS  Google Scholar 

  • Palmieri D, Horak CE, Lee JH, Halverson DO, Steeg PS (2006) Translational approaches using metastasis suppressor genes. J Bioenerg Biomembr 38:151–161

    Article  PubMed  CAS  Google Scholar 

  • Parks RE Jr, Agarwal RP (1973) Nucleoside diphosphokinases. In: Boyer PD (ed) The enzymes. Academic, New York, pp 307–334

    Google Scholar 

  • Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K, Broadbent T, Sarkar S, Burt RW, Jones DA (2009) A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137:623–634

    Article  PubMed  CAS  Google Scholar 

  • Postel EH (2003) Multiple biochemical activities of NM23/NDP kinase in gene regulation. J Bioenerg Biomembr 35:31–40

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Postel EH, Wohlman I, Zou X, Juan T, Sun N, D’Agostin D, Cuellar M, Choi T, Notterman DA, La Perle KM (2009) Targeted deletion of Nm23/nucleoside diphosphate kinase A and B reveals their requirement for definitive erythropoiesis in the mouse embryo. Dev Dynam 238:775–787

    Article  CAS  Google Scholar 

  • Prakash T, Sharma VK, Adati N, Ozawa R, Kumar N, Nishida Y, Fujikake T, Takeda T, Taylor TD (2010) Expression of conjoined genes: another mechanism for gene regulation in eukaryotes. PLoS ONE 5:e13284

    Article  PubMed  Google Scholar 

  • Rowe RG, Weiss SJ (2008) Breaching the basement membrane: who, when and how? Trends Cell Biol 18:560–574

    Article  PubMed  CAS  Google Scholar 

  • Sabeh F, Shimizu-Hirota R, Weiss SJ (2009) Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 185:11–19

    Article  PubMed  CAS  Google Scholar 

  • Sadek CM, Jimenez A, Damdimopoulos AE, Kieselbach T, Nord M, Gustafsson JA, Spyrou G, Davis EC, Oko R, van der Hoorn FA, Miranda-Vizuete A (2003) Characterization of human thioredoxin-like 2. A novel microtubule-binding thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem 278:13133–13142

    Article  PubMed  CAS  Google Scholar 

  • Schwahn U, Lenzner S, Dong J, Feil S, Hinzmann B, van Duijnhoven G, Kirschner R, Hemberger M, Bergen AA, Rosenberg T, Pinckers AJ, Fundele R, Rosenthal A, Cremers FP, Ropers HH, Berger W (1998) Positional cloning of the gene for X-linked retinitis pigmentosa 2. Nat Genet 19:327–332

    Article  PubMed  CAS  Google Scholar 

  • Seong HA, Jung H, Ha H (2007) NM23-H1 tumor suppressor physically interacts with serine-threonine kinase receptor-associated protein, a transforming growth factor-beta (TGF-beta) receptor-interacting protein, and negatively regulates TGF-beta signaling. J Biol Chem 282:12075–12096

    Article  PubMed  CAS  Google Scholar 

  • Shen R, Wheeler LJ, Mathews CK (2006) Molecular interactions involving Escherichia coli nucleoside diphosphate kinase. J Bioenerg Biomembr 38:255–259

    Article  PubMed  CAS  Google Scholar 

  • Srivastava S, Li Z, Ko K, Choudhury P, Albaqumi M, Johnson AK, Yan Y, Backer JM, Unutmaz D, Coetzee WA, Skolnik EY (2006) Histidine phosphorylation of the potassium channel KCa3.1 by nucleoside diphosphate kinase B is required for activation of KCa3.1 and CD4 T cells. Mol Cell 24:665–675

    Article  PubMed  CAS  Google Scholar 

  • Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, Sobel ME (1988) Evidence for a novel gene associated with low tumor metastatic potential. J Natl Canc Inst 80:200–204

    Article  CAS  Google Scholar 

  • Steeg PS, Horak CE, Miller KD (2008) Clinical-translational approaches to the Nm23-H1 metastasis suppressor. Clin Canc Res 14:5006–5012

    Article  CAS  Google Scholar 

  • Sutnar A, Pesta M, Liska V, Treska V, Skalicky T, Kormunda S, Topolcan O, Cerny R, Holubec L Jr (2007) Clinical relevance of the expression of mRNA of MMP-7, MMP-9, TIMP-1, TIMP-2 and CEA tissue samples from colorectal liver metastases. Tumour Biol 28:247–252

    Article  PubMed  CAS  Google Scholar 

  • Takahashi M, Tsunoda T, Seiki M, Nakamura Y, Furukawa Y (2002) Identification of membrane-type matrix metalloproteinase-1 as a target of the beta-catenin/Tcf4 complex in human colorectal cancers. Oncogene 21:5861–5867

    Article  PubMed  CAS  Google Scholar 

  • Thakur RK, Kumar P, Halder K, Verma A, Kar A, Parent JL, Basundra R, Kumar A, Chowdhury S (2009) Metastases suppressor NM23-H2 interaction with G-quadruplex DNA within c-MYC promoter nuclease hypersensitive element induces c-MYC expression. Nucleic Acids Res 37:172–183

    Article  PubMed  CAS  Google Scholar 

  • Timmons L, Shearn A (2000) Role of AWD/nucleoside diphosphate kinase in Drosophila development. J Bioenerg Biomembr 32:293–300

    Article  PubMed  CAS  Google Scholar 

  • Tokarska-Schlattner M, Boissan M, Munier A, Borot C, Mailleau C, Speer O, Schlattner U, Lacombe ML (2008) The nucleoside diphosphate kinase D (NM23-H4) binds the inner mitochondrial membrane with high affinity to cardiolipin and couples nucleotide transfer with respiration. J Biol Chem 283:26198–26207

    Article  PubMed  CAS  Google Scholar 

  • Valentijn LJ, Koster J, Versteeg R (2006) Read-through transcript from NM23-H1 into the neighboring NM23-H2 gene encodes a novel protein, NM23-LV. Genomics 87:483–489

    Article  PubMed  CAS  Google Scholar 

  • Vogel P, Read R, Hansen GM, Freay LC, Zambrowicz BP, Sands AT (2010a) Situs inversus in Dpcd/Poll−/−, Nme7−/−, and Pkd1l1−/− mice. Vet Pathol 47:120–131

    Article  PubMed  CAS  Google Scholar 

  • Vogel P, Hansen G, Fontenot G, Read R (2010b) Tubulin tyrosine ligase-like 1 deficiency results in chronic rhinosinusitis and abnormal development of spermatid flagella in mice. Vet Pathol 47:703–712

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F (2008) Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 133:340–353

    Article  PubMed  CAS  Google Scholar 

  • Xie KM, Hou XF, Li MQ, Li DJ (2010) NME1 at the human maternal-fetal interface downregulates titin expression and invasiveness of trophoblast cells via MAPK pathway in early pregnancy. Reproduction 139:799–808

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Jarrett SG, Craven R, Kaetzel DM (2009) YNK1, the yeast homolog of human metastasis suppressor NM23, is required for repair of UV radiation- and etoposide-induced DNA damage. Mutat Res 660:74–78

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Institut National de la Santé et de la Recherche Médicale (INSERM) and by the Université Pierre et Marie Curie, grants (to M.L.L.) from the Groupement des Entreprises Françaises contre le Cancer (GEFLUC), and from the Association pour la Recherche contre le Cancer (ARC) and a fellowship (M.B.) from the Ligue Nationale contre le Cancer.

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The authors have no potential conflicts of interest to disclose.

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Correspondence to Mathieu Boissan or Marie-Lise Lacombe.

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This article is published as part of the special issue on NDPK research.

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Boissan, M., Lacombe, ML. Learning about the functions of NME/NM23: lessons from knockout mice to silencing strategies. Naunyn-Schmiedeberg's Arch Pharmacol 384, 421–431 (2011). https://doi.org/10.1007/s00210-011-0649-3

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  • DOI: https://doi.org/10.1007/s00210-011-0649-3

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