9
Views
64
CrossRef citations to date
0
Altmetric
Gene Expression

Nm23-H1 Metastasis Suppressor Expression Level Influences the Binding Properties, Stability, and Function of the Kinase Suppressor of Ras1 (KSR1) Erk Scaffold in Breast Carcinoma Cells

, , , &
Pages 1379-1388 | Received 26 Jul 2004, Accepted 16 Nov 2004, Published online: 27 Mar 2023

REFERENCES

  • An, W., R. Schnur, L. Neckers, and M. Blagosklonny. 1997. Depletion of p185erbB2, Raf-1 and mutant p53 proteins by geldanamycin derivatives correlates with antiproliferative activity. Cancer Chemother. Pharmacol. 40:60–64.
  • Anselmo, A., R. Bumeister, J. Thomas, and M. White. 2002. Critical contribution of linker proteins to Raf kinase activation. J. Biol. Chem. 277:5940–5943.
  • Baba, H., T. Urano, K. Okada, K. Furukawa, E. Nakayama, H. Tanaka, K. Iwasaki, and H. Shiku. 1995. Two isotypes of murine nm23/nucleoside diphosphate kinase, nm23-M1 and nm23-M2, are involved in metastatic suppression of a murine melanoma line. Cancer Res. 55:1977–1981.
  • Baillat, G., S. Gaillard, F. Castets, and A. Monneron. 2002. Interactions of phocein with nucleoside diphosphate kinase, Eps15, and dynamin I. J. Biol. Chem. 277:18961–18966.
  • Basso, A., D. Solit, P. Munster, and N. Rosen. 2002. Ansamycin antibiotics inhibit Akt activation and cyclin D expression in breast cancer cells that overexpress HER2. Oncogene 21:1159–1166.
  • Bell, B., H. Xing, K. Yan, N. Gautam, and A. Muslin. 1999. KSR-1 binds to G-protein bg subunits and inhibits bg-induced mitogen activated protein kinase activation. J. Biol. Chem. 274:7982–7986.
  • Bhujwalla, Z., E. Aboagye, R. Gilles, V. Chack, C. Mendola, and J. Backer. 1999. Nm23-transfected MDA-MB-435 human breast carcinoma cells form tumors with altered phospholipid metabolism and pH: a 31P nuclear magnetic resonance study in vivo and in vitro. Magn. Reson. Med. 41:897–903.
  • Bonvini, P., T. Gastaldi, B. Falini, and A. Rosolen. 2002. Nucleophosmin-anaplastic lymphoma kinase (NPM-ALK), a novel Hsp90-client tyrosine kinase: down-regulation of NPM-ALK expression and tyrosine phosphorylation in ALK+ CD30+ lymphoma cells by the Hsp90 antagonist 17-allylamino,17-demethoxygeldanamycin. Cancer Res. 62:1559–1566.
  • Brennan, J., D. Volle, O. V. Chaika, and R. Lewis. 2002. Phosphorylation regulates the nucleocytoplasmic distribution of kinase suppressor of Ras. J. Biol. Chem. 277:5369–5377.
  • Caligo, M., G. Cipollini, A. Berti, P. Viacava, P. Collecchi, and G. Bevilacqua. 1997. NM23 gene-expression in human breast carcinomas—loss of correlation with cell-proliferation in the advanced phase of tumor progression. Int. J. Cancer 74:102–111.
  • Cuello, F., R. Schulze, F. Heemeyer, H. Meyer, S. Lutz, K. Jakobs, F. Niroomand, and T. Wieland. 2003. Activation of heterotrimeric G proteins by a high energy phosphate transfer via nucleoside diphosphate kinase (NDPK) B and Gβ subunits. J. Biol. Chem. 278:7220–7226.
  • Du, J., and G. Hannon. 2002. The centrosomal kinase Aurora-A/STK15 interacts with putative tumor suppressor NM23-H1. Nucleic Acids Res. 30:5465–5475.
  • Elion, E. 2001. The Ste5 scaffold. J. Cell Sci. 114:3967–3978.
  • Fan, Z., P. Beresford, D. Oh, D. Zhang, and J. Lieberman. 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.
  • Fishbach, M., and J. Settleman. 2003. Specific biochemical inactivation of oncogenic ras proteins by nucleoside diphosphate kinase. Cancer Res. 63:4089–4094.
  • Fournier, H., S. Dupe-Manet, D. Bouvard, M. Laconbe, C. Marie, M. Block, and C. Albiges-Rizo. 2002. Integrin cytoplasmic domain-associated protein 1a (ICAP-1a) interacts directly with the metastasis suppressor nm23-H2, and both proteins are targeted to newly formed cell adhesion sites upon integrin engagement. J. Biol. Chem. 277:20895–20902.
  • Fukuda, M., A. Ishii, Y. Yasutomo, N. Shimada, N. Ishikawa, N. Hanai, N. Nagara, T. Irimura, G. Nicolson, and N. Kimura. 1996. Metastatic potential of rat mammary adenocarcinoma cells associated with decreased expression of nucleoside diphosphate kinase/nm23: reduction by transfection of NDP kinase a isoform, an nm23-H2 gene homolog. Int. J. Cancer 65:531–537.
  • Goodall, R., H. Dawkins, P. Robbins, E. Hahnel, M. Sarna, R. Hahnel, J. Papadimitriou, J. Harvey, and G. Sterrett. 1994. Evaluation of the expression levels of nm23-H1 RNA in primary breast cancer, benign breast disease, axillary lymph nodes and normal breast tissue. Pathology 26:423–428.
  • Hartsough, M., D. Morrison, M. Salerno, D. Palmieri, T. Ouatas, M. Mair, J. Patrick, and P. Steeg. 2002. Nm23-H1 metastasis suppressor phosphorylation of kinase suppressor of ras (KSR), via a histidine protein kinase pathway. J. Biol. Chem. 277:32389–32399.
  • Hendrix, M., E. Seftor, D. Kirschmann, and R. Seftor. 2000. Can breast cancer cells undergo vasculogenic mimicry. Br. Cancer Res. 2:417–422.
  • Isaacs, J., W. Xu, and L. Neckers. 2003. Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell 3:213–217.
  • Johnson, J., S. Decker, D. Zaharevitz, L. Rubenstein, J. Vendetti, S. Schepartz, S. Kalyandrug, M. Christian, S. Arbuck, M. Hollingshead, and E. Sausville. 2001. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer 84:1424–1431.
  • Kantor, J. D., B. McCormick, P. S. Steeg, and B. R. Zetter. 1993. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res. 53:1971–1973.
  • Kornfield, K., D. Hom, and H. Horvitz. 1995. The ksr-1 gene encodes a novel protein kinase involved in Ras-mediated signaling in C. elegans. Cell 83:903–913.
  • Leone, A., U. Flatow, C. R. King, M. A. Sandeen, I. M. K. Margulies, L. A. Liotta, and P. S. Steeg. 1991. Reduced tumor incidence, metastatic potential, and cytokine responsiveness of nm23-transfected melanoma cells. Cell 65:25–35.
  • Leone, A., U. Flatow, K. VanHoutte, and P. S. Steeg. 1993. 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.
  • Lintig, F. V., A. Dreilinger, N. Varki, A. Wallace, D. Casteel, and G. Boss. 2000. Ras activation in human breast cancer. Breast Cancer Res. Treat. 62:51–62.
  • Lombardi, D., A. Sacchi, G. D'Agostino, and G. Tibursi. 1995. The association of the Nm23-M1 protein and beta-tubulin correlates with cell differentiation. Exp. Cell Res. 217:267–271.
  • Lozano, J., R. Xing, Z. Cai, H. Jensen, C. Trempus, W. Mark, R. Cannon, and R. Kolesnick. 2003. Deficiency of kinase suppressor of ras1 prevents oncogenic ras signaling in mice. Cancer Res. 63:4232–4238.
  • Luo, J., and J. Benovic. 2003. G protein-coupled receptor kinase interaction with Hsp90 mediates kinase maturation. J. Biol. Chem. 278:50908–50914.
  • MacDonald, N., J. Freije, M. Stracke, R. Manrow, and P. Steeg. 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.
  • Mahanty, S., Y. Wang, F. Farley, and E. Elion. 1999. Nuclear shuttling of yeast scaffold Ste5 is required for its recruitment to the plasma membrane and activation of the mating MAPK cascade. Cell 98:501–512.
  • Maloney, A., and P. Workman. 2002. HSP90 as a new therapeutic target for cancer therapy: the story unfolds. Expert Opin. Biol. Ther. 2:3–24.
  • Maniotis, A., R. Folberg, A. Hess, E. Seftor, L. Gardner, J. Pe'er, J. Trent, P. Meltzer, and M. Hendrix. 1999. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 155:739–752.
  • Matheny, S., C. Chen, R. Kortum, G. Razidlo, R. Lewis, and M. White. 2004. Ras regulates assembly of mitogenic signalling complexes throughout the effector protein IMP. Nature 427:256–260.
  • Miele, M. E., A. D. L. Rosa, J. H. Lee, D. J. Hicks, J. U. Dennis, P. S. Steeg, and D. R. Welch. 1997. Suppression of human melanoma metastasis following introduction of chromosome 6 is independent of NME1 (nm23). Clin. Exp. Metastasis 15:259–265.
  • Miyakis, S., G. Sourvinos, and D. Spandidos. 1998. Differential expression and mutation of the ras family genes in human breast cancer. Biochem. Biophys. Res. Commun. 251:609–612.
  • Miyazaki, H., M. Fukuda, Y. Ishijima, A. Negishi, R. Hirayama, N. Ishikawa, T. Amagasa, and N. Kimura. 1999. Overexpression of nm23-H2/NDP kinase B in a human oral squamous cell carcinoma cell line results in reduced metastasis, differentiated phenotype in the metastatic site, and growth factor-independent proliferative activity in culture. Clin. Cancer Res. 5:4301–4307.
  • Morrison, D. 2001. KSR: a MAPK scaffold of the ras pathway. J. Cell Sci. 114:1609–1612.
  • Muller, J., S. Ory, T. Copeland, H. Piwnica-Worms, and D. Morrison. 2001. C-TAK1 regulates ras signaling by phosphorylating the MAPK scaffold, KSR. Mol. Cell 8:983–993.
  • Nahta, R., G. Hortobagyi, and F. Esteva. 2003. Novel pharmacological approaches in the treatment of breast cancer. Expert Opin. Investig. Drugs 12:909–921.
  • Nguyen, A., W. Burack, J. Stock, R. Kortum, O. Chaika, M. Afkarian, W. Muller, K. Murphy, D. Morrison, R. Lewis, J. McNeish, and A. Shaw. 2002. Kinase suppressor of Ras (KSR) is a scaffold which facilitates mitogen-activated protein kinase activation in vivo. Mol. Cell. Biol. 22:3035–3045.
  • Nguyen, D., S. Desai, A. Chen, T. Weiser, and D. Schrump. 2000. Modulation of metastasis phenotypes of non-small cell lung cancer cells by 17-allylamino 17-demethoxy geldanamycin. Ann. Thorac. Surg. 70:1853–1860.
  • Nosaka, K., M. Kawahara, M. Masuda, Y. Satomi, and H. Nishino. 1998. Association of nucleoside diphosphate kinase nm23-H2 with human telomeres. Biochem. Biophys. Res. Comm. 243:342–348.
  • Ohmachi, M., C. Rocheleau, D. Church, E. Lambie, T. Schedl, and M. Sundaram. 2002. C. elegans ksr-1 and ksr-2 have both unique and redundant functions and are required for MPK-1 ERK phosphorylation. Curr. Biol. 12:427–433.
  • Ory, S., M. Zhou, T. Conrads, T. Veenstra, and D. Morrison. 2003. Protein phosphatase 2A positively regulates Ras signaling by dephosphorylating KSR1 and Raf-1 on critical 14-3-3 binding sites. Curr. Biol. 13:1356–1364.
  • Otero, A. 1997. Copurification of vimentin, energy metabolism enzymes and a MER5 homolog with nucleoside diphosphate kinase. Identification of tissue-specific interactions. J. Biol. Chem. 272:14690–14694.
  • Otsuki, Y., M. Tanaka, S. Yoshii, N. Kawazoe, K. Nakaya, and H. Sugimura. 2001. Tumor metastasis suppressor nm23H1 regulates Rac GTPase by interaction with Tiam1. Proc. Natl. Acad. Sci. USA 98:4385–4390.
  • Ouatas, T., D. Halverson, and P. Steeg. 2003. Dexamethasone and medroxyprogesterone acetate elevate Nm23-H1 metastasis suppressor expression in metastatic human breast carcinoma cells: new uses for old compounds. Clin. Cancer Res. 9:3763–3772.
  • Palacios, F., J. Schweitzer, R. Boshans, and C. D'Souza-Schorey. 2002. ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4:929–936.
  • Paravicini, G., M. Steinmayr, E. André, and M. Becker-André. 1996. The metastasis suppressor candidate nucleoside diphosphate kinase Nm23 specifically interacts with members of the ROR/RZR nuclear orphan receptor subfamily. Biochem. Biophys. Res. Commun. 227:82–87.
  • Parhar, R. S., Y. Shi, M. Zou, N. R. Farid, P. Ernst, and S. Al-Sedairy. 1995. Effects of cytokine mediated modulation of Nm23 expression on the invasion and metastatic behavior of B16F10 melanoma cells. Int. J. Cancer 60:204–210.
  • Postel, E. 2003. Multiple biochemical activities of NM23/NDP kinase in gene regulation. J. Bioenerg. Biomembr. 35:31–40.
  • Postel, E., and B. Abramczyk. 2003. Escherichia coli nucleoside diphosphate kinase is a uracil-processing DNA repair nuclease. Proc. Natl. Acad. Sci. USA 100:13247–13252.
  • Reymond, A., S. Volorio, G. Merla, M. Al-Maghtheh, O. Zuffardi, A. Bulfone, A. Ballabio, and M. Zollo. 1999. Evidence for interaction between human PRUNE and nm23-H1 NDPKinase. Oncogene 18:7244–7252.
  • Roy, F., G. Laberge, M. Douziech, D. Ferland-McCollough, and M. Therrien. 2002. KSR is a scaffold required for activation of the ERK/MAPK module. Genes Dev. 16:427–438.
  • Roymans, D., K. Vissenberg, C. DeJonghe, R. W. G. Engler, N. Kimura, B. Grobben, P. Claes, J. Verbelen, C. VanBroeckhoven, and H. Slegers. 2001. Identification of the tumor metastasis suppressor Nm23-H1/Nm23-R1 as a constitutent of the centrosome. Exp. Cell Res. 262:145–153.
  • Roymans, D., R. Willems, K. Vissenberg, C. DeJonghe, B. Groben, P. Claes, I. Lascu, D. V. Bockstaele, J. Verbelen, C. VanBroeckhoven, and H. Slegers. 2000. Nucleoside diphosphate kinase b (Nm23-R1/NDPKb) is associated with intermediate filaments and becomes upregulated upon cAMP-induced differentiation of rat C6 glioma. Exp. Cell Res. 261:127–138.
  • Russell, R., A. Pedersen, J. Kantor, K. Geisinger, R. Long, N. Zbieranski, A. Townsend, B. Shelton, N. Brunner, and T. Kute. 1998. Relationship of nm23 to proteolytic factors, proliferation and motility in breast cancer tissues and cell lines. Br. J. Cancer 78:710–717.
  • Sausville, E., Y. Elsayed, M. Monga, and G. Kim. 2003. Signal transduction-directed cancer treatments. Annu. Rev. Pharmacol. Toxicol. 43:199–231.
  • Schondorf, T., A. Andrack, D. Niederacher, A. Scharl, M. Becker, H. Engel, and U. Gohring. 1999. H-ras gene amplification or mutation is not common in human primary breast cancer. Oncol. Rep. 6:1029–1033.
  • Sellappan, S., R. Grijalva, X. Zhou, W. Yang, M. B. Eli, G. Mills, and D. Yu. 2004. Lineage infidelity of MDA-MB-435 cells: expression of melanocyte proteins in a breast cancer cell line. Cancer Res. 64:3479–3485.
  • Siddiqui-Jain, A., C. Grand, D. Bearss, and L. Hurley. 2002. Direct evidence for a G-quadruplex in a promoter region and its targeting with a samll molecule to repress c-MTC transcription. Proc. Natl. Acad. Sci. USA 99:11593–11598.
  • Steeg, P. 2003. Metastasis suppressors alter the signal transduction of cancer cells. Nat. Cancer Rev. 3:55–63.
  • Stewart, S., M. Sundaram, Y. Zhang, J. Lee, M. Han, and K. Guan. 1999. Kinase suppressor of ras forms a multiprotein signaling complex and modulates MEK localization. Mol. Cell. Biol. 19:5523–5534.
  • Subramanian, C., M. Cotter, and E. Robertson. 2001. Epstein-Barr virus nuclear protein EBNA-3C interacts with the human metastatic suppressor Nm23-H1: a molecular link to cancer metastasis. Nat. Med. 7:350–355.
  • Sundaram, M., and M. Han. 1995. The C. elegans ksr-1 gene encodes a novel Raf-related kinase involved in Ras-mediated signal transduction. Cell 83:889–901.
  • Suzuki, E., T. Ota, K. Tsukuda, A. Okita, K. Matsuoka, M. Murakami, H. Doihara, and N. Shimizu. 2004. nm23-H1 reduces in vitro cell migration and the liver metastatic potential of colon cancer cells by regulating myosin light chain phosphorylation. Int. J. Cancer 108:207–211.
  • Tagashira, H., K. Hamazaki, N. Tanaka, C. Gao, and M. Namba. 1998. Reduced metastatic potential and c-myc overexpression of colon adenocarcinoma cells (Colon 26 line) transfected with nm23-R2 rat nucleoside diphosphate kinase a isoform. Int. J. Mol. Med. 2:65–68.
  • Therrien, M., H. Chang, N. Solomon, F. Karim, D. Wassarman, and G. Rubin. 1995. KSR, a novel protein kinase required for RAS signal transduction. Cell 83:879–888.
  • Toulas, C., J. Mihura, C. de Balincourt, B. Marques, E. Marek, G. Soula, H. Roche, and G. Favre. 1996. Potential prognostic value in human breast cancer of cytosolic Nme1 protein detection using an original hen specific antibody. Br. J. Cancer 73:630–635.
  • Tseng, Y., D. Vincent, J. Zhu, A. Adeyinka, J. Moyers, P. Watson, and C. Kahn. 2001. Regulation of growth and tumorigenicity of breast cancer cells by the low molecular weight GTPase Rad and Nm23. Cancer Res. 61:2071–2079.
  • Wagner, P., and N.-D. Vu. 2000. Histidine to aspartate phosphotransferase activity of nm23 protein: phosphorylation of aldolase C on Asp 319. Biochem. J. 346:623–630.
  • Wagner, P., and N.-D. Vu. 1995. Phosphorylation of ATP-citrate lyase by nucleoside diphosphate kinase. J. Biol. Chem. 270:21758–21764.
  • Webb, C., C. Hose, S. Koochekpour, M. Jeffers, M. Oskarsson, E. Sausville, A. Monks, and G. VandWoude. 2000. The geldanamycins are potent inhibitors of the hepatocyte growth factor/scatter factor-Met-urokinase plasminogen activator-pasmin proteolytic network. Cancer Res. 60:342–349.
  • Xing, H., C. Cordon-Cardo, X. Deng, W. Tong, L. Campodonico, Z. Fuks, and R. Kolesnick. 2003. Pharmacologic inactivation of kinase suppressor of ras-1 abrogates ras-mediated pancreatic cancer. Nat. Med. 9:1267–1268.
  • Xing, H., and R. Kolesnick. 2001. Kinase suppressor of ras signals through Thr269 of c-Raf-1. J. Biol. Chem. 276:9733–9741.
  • Xu, J., L. Liu, F. Deng, L. Timmons, E. Hersperger, P. Steeg, M. Veron, and A. Shearn. 1996. Rescue of the awd mutant phenotype by expression of human Nm23/NDP kinase in Drosophila. Dev. Biol. 177:544–557.
  • Yaguchi, H., N. Ohkura, T. Tsukada, and K. Yamaguchi. 2002. Menin, the multiple endocrine neoplasia type 1 gene product, exhibits GTP-hydrolyzing activity in the presence of the tumor metastasis suppressor nm23. J. Biol. Chem. 277:38197–38204.
  • Yan, F., and B. Polk. 2001. Kinase suppressor of ras is necessary for tumor necrosis factor a activation of extracellular signal-regulated kinase/mitogen-activated protein kinase in intestinal epithelial cells. Cancer Res. 61:963–989.
  • Yoder, J., H. Chong, K.-L. Guan, and M. Han. 2004. Modulation of KSR activity in Caenorhabditis elegans by Zn ions, PAR-1 kinase and PP2A phosphatase. EMBO J. 23:1–9.
  • Zhu, J., Y.-H. Tseng, J. Kantor, C. Rhodes, B. Zetter, J. Moyers, and C. Kahn. 1999. Interaction of the Ras-related protein associated with diabetes Rad and the putative tumor metastasis suppressor NM23 provides a novel mechanism of GTPase regulation. Proc. Natl. Acad. Sci. USA 96:14911–14918.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.