The metastasis suppressor, Ndrg-1: A new ally in the fight against cancer

Carcinogenesis

Volumn 27, Issue 12, 2006, Pages 2355-2366

  Kovacevic, Zaklina ^a   Richardson, Des R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOPICOLINALDEHYDE THIOSEMICARBAZONE; ANDROGEN; BIS 2 PYRIDYLKETONE 4,4 DIMETHYL 3 THIOSEMICARBAZONE; IRINOTECAN; IRON; IRON CHELATING AGENT; N MYC DOWNSTREAM REGULATED PROTEIN 1; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN;

ADVANCED CANCER; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER INVASION; CANCER MORTALITY; CELL LEVEL; CELLULAR DISTRIBUTION; CLINICAL TRIAL; COLON CANCER; CORRELATION ANALYSIS; DOWN REGULATION; EXOCYTOSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE OVEREXPRESSION; GENE TARGETING; GLEASON SCORE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; IRON METABOLISM; LIPID METABOLISM; LIPOGENESIS; LUNG CANCER; METASTASIS; MOTOR NEUROPATHY; MYELINATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SENSORY NEUROPATHY; STRESS; TISSUE DISTRIBUTION; TUMOR GROWTH; TUMOR MODEL;

BREAST NEOPLASMS; CELL CYCLE PROTEINS; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 8; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; IRON CHELATING AGENTS; MALE; MUSCLE PROTEINS; NEOPLASM METASTASIS; NEOPLASMS; NERVE TISSUE PROTEINS; PROSTATIC NEOPLASMS; PROTEINS;

EID: 33845358660     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl146     Document Type: Review

References (80)

1. Welch,D.R. and Tomasovic,S.P. (1985) Implications of tumor progression on clinical oncology. Clin. Exp. Metastasis, 3, 151-188.
2. Shevde,L.A. and Welch,D.R. (2003) Metastasis suppressor pathways - an evolving paradigm. Cancer Lett., 198, 1-20.
3. Welch,D.R. and Rinker-Schaeffer,C.W. (1999) What defines a useful marker of metastasis in human cancer? J. Natl Cancer Inst., 91, 1351-1353.
4. Welch,D.R. and Hunter,K.W. (2003) A new member of the growing family of metastasis suppressors identified in prostate cancer. J. Natl Cancer Inst., 95, 839-841.
5. Bandyopadhyay,S., Pai,S.K., Gross,S.C. et al. (2003) The Drg-1 gene suppresses tumor metastasis in prostate cancer. Cancer Res., 63, 1731-1736.
6. Bandyopadhyay,S., Pai,S.K., Hirota,S. et al. (2004) Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene, 23, 5675-5681.
7. Guan,R.J., Ford,H.L., Fu,Y., Li,Y., Shaw,L.M. and Pardee,A.B. (2000) Drg-1 as a differentiation-related, putative metastatic suppressor gene in human colon cancer. Cancer Res., 60, 749-755.
8. Li,J. and Kretzner,L. (2003) The growth-inhibitory Ndrg1 gene is a Myc negative target in human neuroblastomas and other cell types with overexpressed N- or c-myc. Mol. Cell Biochem., 250, 91-105.
9. Qu,X., Zhai,Y., Wei,H., Zhang,C., Xing,G., Yu,Y. and He,F. (2002) Characterization and expression of three novel differentiation-related genes belong to the human NDRG gene family. Mol. Cell Biochem., 229, 35-44.
10. Zhou,R.H., Kokame,K., Tsukamoto,Y., Yutani,C., Kato,H. and Miyata,T. (2001) Characterization of the human NDRG gene family: A newly identified member, NDRG4, is specifically expressed in brain and heart. Genomics, 73, 86-97.
11. Shimono,A., Okuda,T. and Kondoh,H. (1999) N-myc-dependent repression of ndr1, a gene identified by direct subtraction of whole mouse embryo cDNAs between wild type and N-myc mutant. Mech. Dev., 83, 39-52.
12. Lin,T.M. and Chang,C. (1997) Cloning and characterization of TDD5, an androgen target gene that is differentially repressed by testosterone and dihydrotestosterone. Proc. Natl Acad. Sci. USA, 94, 4988-4993.
13. Krauter-Canham,R., Bronner,R., Evrard,J.L., Hahne,G., Friedt,W. and Steinmetz,A. (1997) A transmitting tissue- and pollen-expressed protein from sunflower with sequence similarity to the human RTP protein. Plant Sci., 129, 191-202.
14. Kokame,K., Kato,H. and Miyata,T. (1996) Homocysteine-respondent genes in vascular endothelial cells identified by differential display analysis. GRP78/BiP and novel genes. J. Biol. Chem., 271, 29659-29665.
15. Cui,D.X., Zhang,L., Yan,X.J. et al. (2005) A microarray-based gastric carcinoma prewarning system. World J. Gastroenterol., 11, 1273-1282.
16. van Belzen,N., Dinjens,W.N., Diesveld,M.P., Groen,N.A., van der Made,A.C., Nozawa,Y., Vlietstra,R., Trapman,J. and Bosman,F.T. (1997) A novel gene which is up-regulated during colon epithelial cell differentiation and down-regulated in colorectal neoplasms. Lab. Invest., 77, 85-92.
17. Ulrix,W., Swinnen,J.V., Heyns,W. and Verhoeven,G. (1999) The differentiation-related gene 1, Drg1, is markedly upregulated by androgens in LNCaP prostatic adenocarcinoma cells. FEBS Lett., 455, 23-26.
18. Zhou,D., Salnikow,K. and Costa,M. (1998) Cap43, a novel gene specifically induced by Ni2+ compounds. Cancer Res., 58, 2182-2189.
19. Salnikow,K., Kluz,T., Costa,M., Piquemal,D., Demidenko,Z.N., Xie,K. and Blagosklonny,M.V. (2002) The regulation of hypoxic genes by calcium involves c-Jun/AP-1, which cooperates with hypoxia-inducible factor 1 in response to hypoxia. Mol. Cell Biol., 22, 1734-1741.
20. Le,N.T. and Richardson,D.R. (2004) Iron chelators with high antiproliferative activity up-regulate the expression of a growth inhibitory and metastasis suppressor gene: A link between iron metabolism and proliferation. Blood, 104, 2967-2975.
21. Kurdistani,S.K., Arizti,P., Reimer,C.L., Sugrue,M.M., Aaronson,S.A. and Lee,S.W. (1998) Inhibition of tumor cell growth by RTP/rit42 and its responsiveness to p53 and DNA damage. Cancer Res., 58, 4439-4444.
22. Kim,Y.H., Girard,L., Giacomini,C.P., Wang,P., Hernandez-Boussard,T., Tibshirani,R., Minna,J.D. and Pollack,J.R. (2006) Combined microarray analysis of small cell lung cancer reveals altered apoptotic balance and distinct expression signatures of MYC family gene amplification. Oncogene, 25, 130-138.
23. Williams,K., Fernandez,S., Stien,X., Ishii,K., Love,H.D., Lau,Y.F., Roberts,R.L. and Hayward,S.W. (2005) Unopposed c-MYC expression in benign prostatic epithelium causes a cancer phenotype. Prostate, 63, 369-384.
24. Agarwala,K.L., Kokame,K., Kato,H. and Miyata,T. (2000) Phosphorylation of RTP, an ER stress-responsive cytoplasmic protein. Biochem. Biophys. Res. Commun., 272, 641-647.
25. Sugiki,T., Murakami,M., Taketomi,Y., Kikuchi-Yanoshita,R. and Kudo,I. (2004) N-myc downregulated gene 1 is a phosphorylated protein in mast cells. Biol. Pharm. Bull., 27, 624-627.
26. Quandt,K., Frech,K., Karas,H., Wingender,E. and Werner,T. (1995) MatInd and MatInspector: New fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res., 23, 4878-4884.
27. Shaw,E., McCue,L.A., Lawrence,C.E. and Dordick,J.S. (2002) Identification of a novel class in the alpha/beta hydrolase fold superfamily: The N-myc differentiation-related proteins. Proteins, 47, 163-168.
28. Lachat,P., Shaw,P., Gebhard,S., van Belzen,N., Chaubert,P. and Bosman,F.T. (2002) Expression of NDRG1, a differentiation-related gene, in human tissues. Histochem. Cell Biol., 118, 399-408.
29. Piquemal,D., Joulia,D., Balaguer,P., Basset,A., Marti,J. and Commes,T. (1999) Differential expression of the RTP/Drg1/Ndr1 gene product in proliferating and growth arrested cells. Biochim. Biophys. Acta, 1450, 364-373.
30. Sugiki,T., Taketomi,Y., Kikuchi-Yanoshita,R., Murakami,M. and Kudo,I. (2004) Association of N-myc downregulated gene 1 with heat-shock cognate protein 70 in mast cells. Biol. Pharm. Bull., 27, 628-633.
31. Kose,S., Furuta,M., Koike,M., Yoneda,Y. and Imamoto,N. (2005) The 70-kD heat shock cognate protein (hsc70) facilitates the nuclear export of the import receptors. J. Cell Biol., 171, 19-25.
32. Liang,S.X. and Richardson,D.R. (2003) The effect of potent iron chelators on the regulation of p53: Examination of the expression, localization and DNA-binding activity of p53 and the transactivation of WAF1. Carcinogenesis, 24, 1601-1614.
33. Le,N.T. and Richardson,D.R. (2003) Potent iron chelators increase the mRNA levels of the universal cyclin-dependent kinase inhibitor p21(CIP1/ WAF1), but paradoxically inhibit its translation: A potential mechanism of cell cycle dysregulation. Carcinogenesis, 24, 1045-1058.
34. Fritsche,M., Haessler,C. and Brandner,G. (1993) Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene, 8, 307-318.
35. Gomez-Casero,E., Navarro,M., Rodriguez-Puebla,M.L., Larcher,F., Paramio,J.M., Conti,C.J. and Jorcano,J.L. (2001) Regulation of the differentiation-related gene Drg-1 during mouse skin carcinogenesis. Mol. Carcinog., 32, 100-109.
36. Hunter,M., Angelicheva,D., Tournev,I., Ingley,E., Chan,D.C., Watts,G.F., Kremensky,I. and Kalaydjieva,L. (2005) NDRG1 interacts with APO A-I and A-II and is a functional candidate for the HDL-C QTL on 8q24. Biochem. Biophys. Res. Commun., 332, 982-992.
37. Kalaydjieva,L., Gresham,D., Gooding,R. et al. (2000) N-myc downstream-regulated gene 1 is mutated in hereditary motor and sensory neuropathy-Lom. Am. J. Hum. Genet., 67, 47-58.
38. Masuda,K., Ono,M., Okamoto,M. et al. (2003) Downregulation of Cap43 gene by von Hippel-Lindau tumor suppressor protein in human renal cancer cells. Int. J. Cancer, 105, 803-810.
39. Okuda,T., Higashi,Y., Kokame,K., Tanaka,C., Kondoh,H. and Miyata,T. (2004) Ndrg1-deficient mice exhibit a progressive demyelinating disorder of peripheral nerves. Mol. Cell Biol., 24, 3949-3956.
40. Shah,M.A., Kemeny,N., Hummer,A., Drobnjak,M., Motwani,M., Cordon-Cardo,C., Gonen,M. and Schwartz,G.K. (2005) Drg1 expression in 131 colorectal liver metastases: Correlation with clinical variables and patient outcomes. Clin. Cancer Res., 11, 3296-3302.
41. Bandyopadhyay,S., Pai,S.K., Hirota,S. et al. (2004) PTEN up-regulates the tumor metastasis suppressor gene Drg-1 in prostate and breast cancer. Cancer Res., 64, 7655-7660.
42. Taketomi,Y., Sugiki,T., Saito,T. et al. (2003) Identification of NDRG1 as an early inducible gene during in vitro maturation of cultured mast cells. Biochem. Biophys. Res. Commun., 306, 339-346.
43. Kim,K.T., Ongusaha,P.P., Hong,Y.K., Kurdistani,S.K., Nakamura,M., Lu,K.P. and Lee,S.W. (2004) Function of Drg1/Rit42 in p53-dependent mitotic spindle checkpoint. J. Biol. Chem., 279, 38597-38602.
44. Rodgers,G.M. and Conn,M.T. (1990) Homocysteine, an atherogenic stimulus, reduces protein C activation by arterial and venous endothelial cells. Blood, 75, 895-901.
45. Rees,M.M. and Rodgers,G.M. (1993) Homocysteinemia: Association of a metabolic disorder with vascular disease and thrombosis. Thromb. Res., 71, 337-359.
46. Cangul,H (2004) Hypoxia upregulates the expression of the NDRG1 gene leading to its overexpression in various human cancers. BMC Genet., 5, 27.
47. Salnikow,K., Blagosklonny,M.V., Ryan,H., Johnson,R. and Costa,M. (2000) Carcinogenic nickel induces genes involved with hypoxic stress. Cancer Res., 60, 38-41.
48. Semenza,G.L. (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol., 15, 551-578.
49. Greijer,A.E., van der Groep,P., Kemming,D., Shvarts,A., Semenza,G.L., Meijer,G.A., van de Wiel,M.A., Belien,J.A., van Diest,P.J. and van der Wall,E. (2005) Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J. Pathol., 206, 291-304.
50. Ivan,M., Kondo,K., Yang,H., Kim,W., Valiando,J., Ohh,M., Salic,A., Asara,J.M., Lane,W.S. and Kaelin,W.G.,Jr. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: Implications for O2 sensing. Science, 292, 464-468.
51. Eguchi,H., Ikuta,T., Tachibana,T., Yoneda,Y. and Kawajiri,K. (1997) A nuclear localization signal of human aryl hydrocarbon receptor nuclear translocator/hypoxia-inducible factor 1beta is a novel bipartite type recognized by the two components of nuclear pore-targeting complex. J. Biol. Chem., 272, 17640-17647.
52. Caro,J. (2001) Hypoxia regulation of gene transcription. High Alt. Med. Biol., 2, 145-154.
53. Chen,B., Nelson,D.M. and Sadovsky,Y. (2006) N-myc down-regulated gene 1 modulates the response of term human trophoblasts to hypoxic injury. J. Biol. Chem., 281, 2764-2772.
54. Stein,S., Thomas,E.K., Herzog,B., Westfall,M.D., Rocheleau,J.V., Jackson,R.S.,2nd, Wang,M. and Liang,P. (2004) NDRG1 is necessary for p53-dependent apoptosis. J. Biol. Chem., 279, 48930-48940.
55. Unoki,M. and Nakamura,Y. (2001) Growth-suppressive effects of BPOZ and EGR2, two genes involved in the PTEN signaling pathway. Oncogene, 20, 4457-4465.
56. Davies,M.A., Kim,S.J., Parikh,N.U., Dong,Z., Bucana,C.D. and Gallick,G.E. (2002) Adenoviral-mediated expression of MMAC/PTEN inhibits proliferation and metastasis of human prostate cancer cells. Clin. Cancer Res., 8, 1904-1914.
57. Henriksson,M. and Luscher,B. (1996) Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv. Cancer Res., 68, 109-182.
58. Maruyama,Y., Ono,M., Kawahara,A., Yokoyama,T., Basaki,Y., Kage,M., Aoyagi,S., Kinoshita,H. and Kuwano,M. (2006) Tumor growth suppression in pancreatic cancer by a putative metastasis suppressor gene Cap43/NDRG1/ Drg-1 through modulation of angiogenesis. Cancer Res., 66, 6233-6242.
59. Liu,Y.N., Lee,W.W., Wang,C.Y., Chao,T.H., Chen,Y. and Chen,J.H. (2005) Regulatory mechanisms controlling human E-cadherin gene expression. Oncogene, 24, 8277-8290.
60. Caruso,R.P., Levinson,B., Melamed,J. et al. (2004) Altered N-myc downstream-regulated gene 1 protein expression in African-American compared with caucasian prostate cancer patients. Clin. Cancer Res., 10, 222-227.
61. Folkman,J. (1974) Tumor angiogensis: Role in regulation of tumor growth. Symp. Soc. Dev. Biol., 30, 43-52.
62. Motwani,M., Sirotnak,F.M., She,Y., Commes,T. and Schwartz,G.K. (2002) Drg1, a novel target for modulating sensitivity to CPT-11 in colon cancer cells. Cancer Res., 62, 3950-3955.
63. Shah,M.A., Kortmansky,J., Motwani,M. et al. (2005) A phase I clinical trial of the sequential combination of irinotecan followed by flavopiridol. Clin. Cancer Res., 11, 3836-3845.
64. Yoshizumi,T., Ohta,T., Ninomiya,I., Terada,I., Fushida,S., Fujimura,T., Nishimura,G., Shimizu,K., Yi,S. and Miwa,K. (2004) Thiazolidinedione, a peroxisome proliferator-activated receptor-gamma ligand, inhibits growth and metastasis of HT-29 human colon cancer cells through differentiation-promoting effects. Int. J. Oncol., 25, 631-639.
65. Fotovati,A., Fujii,T., Yamaguchi,M., Kage,M., Shirouzu,K., Oie,S., Basaki,Y., Ono,M., Yamana,H. and Kuwano,M. (2006) 17Beta-estradiol induces down-regulation of Cap43/NDRG1/Drg-1, a putative differentiation-related and metastasis suppressor gene, in human breast cancer cells. Clin. Cancer Res., 12, 3010-3018.
66. Wang,Z., Wang,F., Wang,W.Q., Gao,Q., Wei,W.L., Yang,Y. and Wang,G.Y. (2004) Correlation of N-myc downstream-regulated gene 1 overexpression with progressive growth of colorectal neoplasm. World J. Gastroenterol., 10, 550-554.
67. Cangul,H., Salnikow,K., Yee,H., Zagzag,D., Commes,T. and Costa,M. (2002) Enhanced expression of a novel protein in human cancer cells: A potential aid to cancer diagnosis. Cell Biol. Toxicol., 18, 87-96.
68. Dong,Z., Arnold,R.J., Yang,Y., Park,M.H., Hrncirova,P., Mechref,Y., Novotny,M.V. and Zhang,J.T. (2005) Modulation of differentiationrelated gene 1 expression by cell cycle blocker mimosine, revealed by proteomic analysis. Mol. Cell Proteomics, 4, 993-1001.
69. Richardson,D.R. and Ponka,P. (1997) The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim. Biophys. Acta, 1331, 1-40.
70. Richardson,D.R. (2005) Molecular mechanisms of iron uptake by cells and the use of iron chelators for the treatment of cancer. Curr. Med. Chem., 12, 2711-2729.
71. Boldt,D.H. (1999) New perspectives on iron: An introduction. Am. J. Med. Sci., 318, 207-212.
72. Atkin,C.L., Thelander,L., Reichard,P. and Lang,G. (1973) Iron and free radical in ribonucleotide reductase. Exchange of iron and Mossbauer spectroscopy of the protein B2 subunit of the Escherichia coli enzyme. J. Biol. Chem., 248, 7464-7472.
73. Kalinowski,D.S. and Richardson,D.R. (2005) The evolution of iron chelators for the treatment of iron overload disease and cancer. Pharmacol. Rev., 57, 547-583.
74. Richardson,D.R. (2002) Iron chelators as therapeutic agents for the treatment of cancer. Crit. Rev. Oncol. Hematol., 42, 267-281.
75. Chaston,T.B., Watts,R.N., Yuan,J. and Richardson,D.R. (2004) Potent antitumor activity of novel iron chelators derived from di-2-pyridylketone isonicotinoyl hydrazone involves fenton-derived free radical generation. Clin. Cancer Res., 10, 7365-7374.
76. Becker,E.M., Lovejoy,D.B., Greer,J.M., Watts,R. and Richardson,D.R. (2003) Identification of the di-pyridyl ketone isonicotinoyl hydrazone (PKIH) analogues as potent iron chelators and anti-tumour agents. Br. J. Pharmacol., 138, 819-830.
77. Yuan,J., Lovejoy,D.B. and Richardson,D.R. (2004) Novel di-2-pyridylderived iron chelators with marked and selective antitumor activity: In vitro and in vivo assessment. Blood, 104, 1450-1458.
78. Finch,R.A., Liu,M., Grill,S.P., Rose,W.C., Loomis,R., Vasquez,K.M., Cheng,Y. and Sartorelli,A.C. (2000) Triapine (3-aminopyridine-2-carboxaldehyde- thiosemicarbazone): A potent inhibitor of ribonucleotide reductase activity with broad spectrum antitumor activity. Biochem. Pharmacol., 59, 983-991.
79. Wadler,S., Makower,D., Clairmont,C., Lambert,P., Fehn,K. and Sznol,M. (2004) Phase I and pharmacokinetic study of the ribonucleotide reductase inhibitor, 3-aminopyridine-2-carboxaldehyde thiosemicarbazone, administered by 96-hour intravenous continuous infusion. J. Clin. Oncol., 22, 1553-1563.
80. Kulp,K.S. and Vulliet,P.R. (1996) Mimosine blocks cell cycle progression by chelating iron in asynchronous human breast cancer cells. Toxicol. Appl. Pharmacol., 139, 356-364.