Proteolytic cleavage and truncation of NDRG1 in human prostate cancer cells, but not normal prostate epithelial cells

Bioscience Reports

Volumn 33, Issue 3, 2013, Pages 451-461

  Ghalayini, Mohammad K ^a   Dong, Qihan ^a,b   Richardson, Des R ^a   Assinder, Stephen J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF WESTERN SYDNEY   (Australia)

Author keywords

CAP43; DRG1; NDR1; NDRG1; Prostate cancer; TDD5

Indexed keywords

FETUIN; GLYCOSIDASE; NDRG1 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; ISOPROTEIN; N-MYC DOWNSTREAM-REGULATED GENE 1 PROTEIN; SIGNAL PEPTIDE;

AMINO TERMINAL SEQUENCE; AMPLICON; ARTICLE; CANCER CELL; CELL LYSATE; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; MALE; MOLECULAR WEIGHT; PROSTATE CANCER; PROSTATE EPITHELIUM; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; WESTERN BLOTTING; AMINO ACID SEQUENCE; CHEMISTRY; GLYCOSYLATION; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PHOSPHORYLATION; PROSTATE; PROSTATE TUMOR; TUMOR CELL LINE;

PHOS;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; EPITHELIAL CELLS; GLYCOSYLATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROSTATE; PROSTATIC NEOPLASMS; PROTEIN ISOFORMS; PROTEOLYSIS;

EID: 84879671984     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20130042     Document Type: Article

References (50)

1. Shaw, E., McCue, L. A., Lawrence, C. E. and Dordick, J. S. (2002) Identification of a novel class in the α/β hydrolase fold superfamily: The N-myc differentiation-related proteins. Proteins Struct. Funct. Bioinf. 47, 163-168 (Pubitemid 34263330)
2. 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 (Pubitemid 34187673)
3. Cher, M. L., Bova, G. S., Moore, D. H., Small, E. J., Carroll, P. R., Pin, S. S., Epstein, J. I., Isaacs, W. B. and Jensen, R. H. (1996) Genetic alterations in untreated metastases and androgen-independent prostate cancer detected by comparative genomic hybridization and allelotyping. Cancer Res. 56, 3091-3102 (Pubitemid 26199756)
4. 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 (Pubitemid 28450049)
5. 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 - Mol. Cell Res. 1450, 364-373 (Pubitemid 29295486)
6. Angst, E., Dawson, D. W., Stroka, D., Gloor, B., Park, J., Candinas, D., Reber, H. A., Hines, O. J. and Eibl, G. (2011) N-myc downstream regulated gene-1 expression correlates with reduced pancreatic cancer growth and increased apoptosis in vitro and in vivo. Surgery 149, 614-624
7. 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
8. 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 (Pubitemid 30094577)
9. Bandyopadhyay, S., Pai, S. K., Hirota, S., Hosobe, S., Takano, Y., Saito, K., Piquemal, D., Commes, T., Watabe, M., Gross, S. C. et al. (2004) Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene 23, 5675-5681 (Pubitemid 39093045)
10. Bandyopadhyay, S., Pai, S. K., Hirota, S., Hosobe, S., Tsukada, T., Miura, K., Takano, Y., Saito, K., Commes, T., Piquemal, D. et al. (2004) PTEN up-regulates the tumor metastasis suppressor gene Drg-1 in prostate and breast cancer. Cancer Res. 64, 7655-7660 (Pubitemid 39446890)
11. Zhao, G., Chen, J., Deng, Y., Gao, F., Zhu, J., Feng, Z., Lv, X. and Zhao, Z. (2011) Identification of NDRG1-regulated genes associated with invasive potential in cervical and ovarian cancer cells. Biochem. Biophys. Res. Commun. 408, 154-159
12. Bandyopadhyay, S., Pai, S. K., Gross, S. C., Hirota, S., Hosobe, S., Miura, K., Saito, K., Commes, T., Hayashi, S., Watabe, M. et al. (2003) The Drg-1 gene suppresses tumor metastasis in prostate cancer. Cancer Res. 63, 1731-1736 (Pubitemid 36460828)
13. Chen, Z., Zhang, D., Yue, F., Zheng, M., Kovacevic, Z. and Richardson, D. R. (2012) The iron chelators Dp44mT and DFO inhibit TGFβ-induced epithelial-mesenchymal transition via up-regulation of N-myc downstream regulated gene 1 (NDRG1). J. Biol. Chem. 287, 17016-17028
14. Kovacevic, Z., Chikhani, S., Lui, G. Y., Sivagurunathan, S. and Richardson, D. R. (2013) The iron-regulated metastasis suppressor NDRG1 targets NEDD4L, PTEN, and SMAD4 and inhibits the PI3K and Ras signaling pathways. Antioxid. Redox Signal. 18, 874-887
15. 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 (Pubitemid 30420691)
16. Murakami, Y., Hosoi, F., Izumi, H., Maruyama, Y., Ureshino, H., Watari, K., Kohno, K., Kuwano, M. and Ono, M. (2010) Identification of sites subjected to serine/threonine phosphorylation by SGK1 affecting N-myc downstream-regulated gene 1 (NDRG1)/Cap43-dependent suppression of angiogenic CXC chemokine expression in human pancreatic cancer cells. Biochem. Biophys. Res. Commun. 396, 376-381
17. McCaig, C., Potter, L., Abramczyk, O. and Murray, J. T. (2011) Phosphorylation of NDRG1 is temporally and spatially controlled during the cell cycle. Biochem. Biophys. Res. Commun. 411, 227-234
18. Banz, V. M., Medová, M., Keogh, A., Furer, C., Zimmer, Y., Candinas, D. and Stroka, D. (2009) Hsp90 transcriptionally and post-translationally regulates the expression of NDRG1 and maintains the stability of its modifying kinase GSK3β. Biochim. Biophys. Acta - Mol. Cell Res. 1793, 1597-1603
19. Kovacevic, Z., Chikhani, S., Lovejoy, D. B. and Richardson, D. R. (2011) Novel thiosemicarbazone iron chelators induce up-regulation and phosphorylation of the metastasis suppressor N-myc down-stream regulated gene 1: a new strategy for the treatment of pancreatic cancer. Mol. Pharmacol. 80, 598-609
20. Kovacevic, Z., Sivagurunathan, S., Mangs, H., Chikhani, S., Zhang, D. and Richardson, D. R. (2011) The metastasis suppressor, N-myc downstream regulated gene 1 (NDRG1), upregulates p21 via p53-independent mechanisms. Carcinogenesis 32, 732-740
21. Masuda, K., Ono, M., Okamoto, M., Morikawa, W., Otsubo, M., Migita, T., Tsuneyoshi, M., Okuda, H., Shuin, T., Naito, S. 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 (Pubitemid 36706104)
22. Murray, J. T., Campbell, D. G., Morrice, N., Auld, G. C., Shpiro, N., Marquez, R., Peggie, M., Bain, J., Bloomberg, G. B., Grahammer, F. et al. (2004) Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem. J. 384, 477-488 (Pubitemid 40018961)
23. Sibold, S., Roh, V., Keogh, A., Studer, P., Tiffon, C., Angst, E., Vorburger, S. A., Weimann, R., Candinas, D. and Stroka, D. (2007) Hypoxia increases cytoplasmic expression of NDRG1, but is insufficient for its membrane localization in human hepatocellular carcinoma. FEBS Lett. 581, 989-994 (Pubitemid 46282732)
24. Tu, L. C., Yan, X., Hood, L. and Lin, B. (2007) Proteomics analysis of the interactome of N-myc downstream regulated gene 1 and its interactions with the androgen response program in prostate cancer cells. Mol. Cell. Proteomics 6, 575-588 (Pubitemid 46630091)
25. Bandyopadhyay, S., Wang, Y., Zhan, R., Pai, S. K., Watabe, M., Iiizumi, M., Furuta, E., Mohinta, S., Liu, W., Hirota, S. et al. (2006) The tumor metastasis suppressor gene Drg-1 down-regulates the expression of activating transcription factor 3 in prostate cancer. Cancer Res. 66, 11983-11990 (Pubitemid 46094212)
26. Assinder, S. J., Au, E., Dong, Q. and Winnick, C. (2010) A novel splice variant of the β-tropomyosin (TPM2) gene in prostate cancer. Mol. Carcinog. 49, 525-531
27. Hidetaka, K. (2009) Phos-tag Western blotting for detecting stoichiometric protein phosphorylation in cells. Protocol Exch., doi:10.1038/nprot.2009.170
28. 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 (Pubitemid 41694660)
29. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K. and Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5, 749-757
30. Zauner, G., Koeleman, C. A. M., Deelder, A. and Wuhrer, M. (2010) Protein glycosylation analysis by HILIC-LC-MS of proteinase K-generated N-and O-glycopeptides. J. Sep. Sci. 33, 903-910
31. Cangul, H. (2004) Hypoxia upregulates the expression of the NDRG1 gene leading to its overexpression in various human cancers. BMC Genetics 5, 27
32. Kokame, K., Kato, H. and Miyata, T. (1996) Homocysteine-respondent genes in vascular endothelial cells identified by differential display analysis. J. Biol. Chem. 271, 29659-29665 (Pubitemid 26389590)
33. 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 (Pubitemid 35352125)
34. Nishie, A., Masuda, K., Otsubo, M., Migita, T., Tsuneyoshi, M., Kohno, K., Shuin, T., Naito, S., Ono, M. and Kuwano, M. (2001) High expression of the Cap43 gene in infiltrating macrophages of human renal cell carcinomas. Clin. Cancer Res. 7, 2145-2151 (Pubitemid 32994855)
35. Park, H., Adams, M. A., Lachat, P., Bosman, F., Pang, S. C. and Graham, C. H. (2000) Hypoxia induces the expression of a 43-kDa protein (PROXY-1) in normal and malignant cells. Biochem. Biophys. Res. Commun. 276, 321-328
36. 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 (Pubitemid 29322774)
37. Arya, M., Bott, S. R., Shergill, I. S., Ahmed, H. U., Williamson, M. and Patel, H. R. (2006) The metastatic cascade in prostate cancer. Surg. Oncol. 15, 117-128 (Pubitemid 46241866)
38. Pulukuri, S. M., Gorantla, B., Knost, J. A. and Rao, J. S. (2009) Frequent loss of cystatin E/M expression implicated in the progression of prostate cancer. Oncogene 28, 2829-2838
39. Bjartell, A., Paju, A., Zhang, W.-M., Gadaleanu, V., Hansson, J., Landberg, G. and Stenman, U.-H. (2005) Expression of tumor-associated trypsinogens (TAT-1 and TAT-2) in prostate cancer. Prostate 64, 29-39 (Pubitemid 40734736)
40. Darmoul, D., Marie, J., Devaud, H., Gratio, V. and Laburthe, M. (2001) Initiation of human colon cancer cell proliferation by trypsin acting at protease-activated receptor-2. Br. J. Cancer 85, 772-779 (Pubitemid 32929479)
41. Hotakainen, K., Bjartell, A., Sankila, A., Järvinen, R., Paju, A., Rintala, E., Haglund, C. and Stenman, U. H. (2006) Differential expression of trypsinogen and tumor-associated trypsin inhibitor (TATI) in bladder cancer. Int. J. Oncol. 28, 95-101
42. Miyata, S., Koshikawa, N., Higashi, S., Miyagi, Y., Nagashima, Y., Yanoma, S., Kato, Y., Yasumitsu, H. and Miyazaki, K. (1999) Expression of trypsin in human cancer cell lines and cancer tissues and Its tight binding to soluble form of Alzheimer amyloid precursor protein in culture. J. Biochem. 125, 1067-1076 (Pubitemid 29332988)
43. Paju, A., Sorsa, T., Tervahartiala, T., Koivunen, E., Haglund, C., Leminen, A., Wahlstrom, T., Salo, T. and Stenman, U. H. (2001) The levels of trypsinogen isoenzymes in ovarian tumour cyst fluids are associated with promatrix metalloproteinase-9 but not promatrix metalloproteinase-2 activation. Br. J. Cancer 84, 1363-1371 (Pubitemid 32522105)
44. Sorsa, T., Salo, T., Koivunen, E., Tyynelä, J., Konttinen, Y. T., Bergmann, U., Tuuttila, A., Niemi, E., Teronen, O., Heikkilä, P. et al. (1997) Activation of type IV procollagenases by human tumor-associated trypsin-2. J. Biol. Chem. 272, 21067-21074 (Pubitemid 27373964)
45. Chaffer, C. L. and Weinberg, R. A. (2011) A perspective on cancer cell metastasis. Science 331, 1559-1564
46. Hanahan, D. and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
47. Kuefer, R., Hofer, M. D., Gschwend, J. E., Pienta, K. J., Sanda, M. G., Chinnaiyan, A. M., Rubin, M. A. and Day, M. L. (2003) The role of an 80 kDa fragment of E-cadherin in the metastatic progression of prostate cancer. Clin. Cancer Res. 9, 6447-6452 (Pubitemid 38031832)
48. Noe, V., Fingleton, B., Jacobs, K., Crawford, H. C., Vermeulen, S., Steelant, W., Bruyneel, E., Matrisian, L. M. and Mareel, M. (2001) Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J. Cell Sci. 114, 111-118 (Pubitemid 32120080)
49. Rios-Doria, J., Day, K. C., Kuefer, R., Rashid, M. G., Chinnaiyan, A. M., Rubin, M. A. and Day, M. L. (2003) The role of calpain in the proteolytic cleavage of E-cadherin in prostate and mammary epithelial cells. J. Biol. Chem. 278, 1372-1379 (Pubitemid 36790823)
50. Takino, T., Koshikawa, N., Miyamori, H., Tanaka, M., Sasaki, T., Okada, Y., Seiki, M. and Sato, H. (2003) Cleavage of metastasis suppressor gene product KiSS-1 protein/metastin by matrix metalloproteinases. Oncogene 22, 4617-4626 (Pubitemid 36976435)