Nicotinamide phosphoribosyltransferase promotes epithelial-to-mesenchymal transition as a soluble factor independent of its enzymatic activity

Journal of Biological Chemistry

Volumn 289, Issue 49, 2014, Pages 34189-34204

  Soncini, Debora ^a   Caffa, Irene ^a   Zoppoli, Gabriele ^c,d   Cea, Michele ^a,e   Cagnetta, Antonia ^e   Passalacqua, Mario ^b   Mastracci, Luca ^b,f   Boero, Silvia ^f   Montecucco, Fabrizio ^a,g   Sociali, Giovanna ^b   Lasigliè, Denise ^a   Damonte, Patrizia ^a   Grozio, Alessia ^b   Mannino, Elena ^b   Poggi, Alessandro ^f   D'Agostino, Vito G ^h   Monacelli, Fiammetta ^a   Provenzani, Alessandro ^h   Odetti, Patrizio ^a,f   Ballestrero, Alberto ^a,f   Bruzzone, Santina ^b   Nencioni, Alessio ^a,f   more..

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c JULES BORDET INSTITUTE   (Belgium)

^d NATIONAL CANCER INSTITUTE   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF GENOA   (Italy)

^g UNIVERSITY OF GENEVA   (Switzerland)

^h UNIVERSITY OF TRENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; BIOCHEMISTRY; BIOSYNTHESIS; CELLS; ENZYME ACTIVITY; MAMMALS;

ENZYMATIC ACTIVITIES; HUMAN BREAST CANCER; HUMAN MALIGNANCIES; MAMMARY EPITHELIAL CELLS; METASTATIC POTENTIAL; NICOTINAMIDE MONONUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; THERAPEUTIC STRATEGY;

DISEASES;

CD24 ANTIGEN; CD45 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; NERVE CELL ADHESION MOLECULE; NICOTINAMIDE NUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; PROGESTERONE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VIMENTIN; CYTOKINE; ERBB2 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE, HUMAN; SMALL INTERFERING RNA; TGFB1 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; BASAL LIKE BREAST CANCER; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER STAGING; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; CELL PROLIFERATION; DEFICIENCY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

MAMMALIA;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NAD; NEOPLASM PROTEINS; NEOPLASM STAGING; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84918577739     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.594721     Document Type: Article

References (52)

1. Imai, S., and Guarente, L. (2014) NAD and sirtuins in aging and disease. Trends Cell Biol. 24, 464-471
2. Guarente, L. (2011) Franklin H. Epstein lecture: sirtuins, aging, and medicine. N. Engl. J. Med. 364, 2235-2244
3. Santidrian, A. F., Matsuno-Yagi, A., Ritland, M., Seo, B. B., LeBoeuf, S. E., Gay, L. J., Yagi, T., and Felding-Habermann, B. (2013) Mitochondrial complex I activity and NAD+/NADH balance regulate breast cancer progression. J. Clin. Invest. 123, 1068-1081
4. Shackelford, R. E., Mayhall, K., Maxwell, N. M., Kandil, E., and Coppola, D. (2013) Nicotinamide phosphoribosyltransferase in malignancy: a review. Genes Cancer 4, 447-456
5. Menssen, A., Hydbring, P., Kapelle, K., Vervoorts, J., Diebold, J., Lüscher, B., Larsson, L. G., and Hermeking, H. (2012) The c-MYC oncoprotein, the NAMPT enzyme, the SIRT1-inhibitor DBC1, and the SIRT1 deacetylase form a positive feedback loop. Proc. Natl. Acad. Sci. U.S.A. 109, E187-196
6. Leary, R. J., Lin, J. C., Cummins, J., Boca, S., Wood, L. D., Parsons, D. W., Jones, S., Sjöblom, T., Park, B. H., Parsons, R., Willis, J., Dawson, D., Willson, J. K., Nikolskaya, T., Nikolsky, Y., Kopelovich, L., Papadopoulos, N., Pennacchio, L. A., Wang, T. L., Markowitz, S. D., Parmigiani, G., Kinzler, K. W., Vogelstein, B., and Velculescu, V. E. (2008) Integrated analysis of homozygous deletions, focal amplifications, and sequence alterations in breast and colorectal cancers. Proc. Natl. Acad. Sci. U.S.A. 105, 16224-16229
7. Roxanis, I. (2013) Occurrence and significance of epithelial-mesenchymal transition in breast cancer. J. Clin. Pathol. 66, 517-521
8. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
9. Biganzoli, L., Wildiers, H., Oakman, C., Marotti, L., Loibl, S., Kunkler, I., Reed, M., Ciatto, S., Voogd, A. C., Brain, E., Cutuli, B., Terret, C., Gosney, M., Aapro, M., and Audisio, R. (2012) Management of elderly patients with breast cancer: updated recommendations of the International Society of Geriatric Oncology (SIOG) and European Society of Breast Cancer Specialists (EUSOMA). Lancet Oncol. 13, e148-160
10. van den Brandt, P. A., Spiegelman, D., Yaun, S. S., Adami, H. O., Beeson, L., Folsom, A. R., Fraser, G., Goldbohm, R. A., Graham, S., Kushi, L., Marshall, J. R., Miller, A. B., Rohan, T., Smith-Warner, S. A., Speizer, F. E., Willett, W. C., Wolk, A., and Hunter, D. J. (2000) Pooled analysis of prospective cohort studies on height, weight, and breast cancer risk. Am. J. Epidemiol. 152, 514-527
11. Noto, H., Goto, A., Tsujimoto, T., Osame, K., and Noda, M. (2013) Latest insights into the risk of cancer in diabetes. J. Diabetes Investig. 4, 225-232
12. DeSantis, C., Ma, J., Bryan, L., and Jemal, A. (2014) Breast cancer statistics, 2013. CA-Cancer J. Clin. 64, 52-62
13. Ferlay, J., Parkin, D. M., and Steliarova-Foucher, E. (2010) Estimates of cancer incidence and mortality in Europe in 2008. Eur. J. Cancer 46, 765-781
14. Curtis, C., Shah, S. P., Chin, S. F., Turashvili, G., Rueda, O. M., Dunning, M. J., Speed, D., Lynch, A. G., Samarajiwa, S., Yuan, Y., Gräf, S., Ha, G., Haffari, G., Bashashati, A., Russell, R., McKinney, S., METABRIC Group, Langerød, A., Green, A., Provenzano, E., Wishart, G., Pinder, S., Watson, P., Markowetz, F., Murphy, L., Ellis, I., Purushotham, A., Børresen-Dale, A. L., Brenton, J. D., Tavaré, S., Caldas, C., and Aparicio, S. (2012) The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346-352
15. Vichai, V., and Kirtikara, K. (2006) Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat. Protoc. 1, 1112-1116
16. van der Veer, E., Ho, C., O'Neil, C., Barbosa, N., Scott, R., Cregan, S. P., and Pickering, J. G. (2007) Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J. Biol. Chem. 282, 10841-10845
17. Cea, M., Cagnetta, A., Fulciniti, M., Tai, Y. T., Hideshima, T., Chauhan, D., Roccaro, A., Sacco, A., Calimeri, T., Cottini, F., Jakubikova, J., Kong, S. Y., Patrone, F., Nencioni, A., Gobbi, M., Richardson, P., Munshi, N., and Anderson, K. C. (2012) Targeting NAD+ salvage pathway induces autophagy in multiple myeloma cells via mTORC1 and extracellular signalregulated kinase (ERK1/2) inhibition. Blood 120, 3519-3529
18. Bruzzone, S., Fruscione, F., Morando, S., Ferrando, T., Poggi, A., Garuti, A., D'Urso, A., Selmo, M., Benvenuto, F., Cea, M., Zoppoli, G., Moran, E., Soncini, D., Ballestrero, A., Sordat, B., Patrone, F., Mostoslavsky, R., Uccelli, A., and Nencioni, A. (2009) Catastrophic NAD+ depletion in activated T lymphocytes through NAMPT inhibition reduces demyelination and disability in EAE. PLoS ONE, e7897
19. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A. A., Kim, S., Wilson, C. J., Lehár, J., Kryukov, G. V., Sonkin, D., Reddy, A., Liu, M., Murray, L., Berger, M. F., Monahan, J. E., Morais, P., Meltzer, J., Korejwa, A., Jané-Valbuena, J., Mapa, F. A., Thibault, J., Bric-Furlong, E., Raman, P., Shipway, A., Engels, I. H., Cheng, J., Yu, G. K., Yu, J., Aspesi, P., Jr., de Silva, M., Jagtap, K., Jones, M. D., Wang, L., Hatton, C., Palescandolo, E., Gupta, S., Mahan, S., Sougnez, C., Onofrio, R. C., Liefeld, T., MacConaill, L., Winckler, W., Reich, M., Li, N., Mesirov, J. P., Gabriel, S. B., Getz, G., Ardlie, K., Chan, V., Myer, V. E., Weber, B. L., Porter, J., Warmuth, M., Finan, P., Harris, J. L., Meyerson, M., Golub, T. R., Morrissey, M. P., Sellers, W. R., Schlegel, R., and Garraway, L. A. (2012) The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607
20. Lee, Y. C., Yang, Y. H., Su, J. H., Chang, H. L., Hou, M. F., and Yuan, S. S. (2011) High visfatin expression in breast cancer tissue is associated with poor survival. Cancer Epidemiol. Biomark. Prev. 20, 1892-1901
21. Parker, J. S., Mullins, M., Cheang, M. C., Leung, S., Voduc, D., Vickery, T., Davies, S., Fauron, C., He, X., Hu, Z., Quackenbush, J. F., Stijleman, I. J., Palazzo, J., Marron, J. S., Nobel, A. B., Mardis, E., Nielsen, T. O., Ellis, M. J., Perou, C. M., and Bernard, P. S. (2009) Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol. 27, 1160-1167
22. Prat, A., Parker, J. S., Karginova, O., Fan, C., Livasy, C., Herschkowitz, J. I., He, X., and Perou, C. M. (2010) Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res. 12, R68
23. Mantovani, A., Marchesi, F., Porta, C., Sica, A., and Allavena, P. (2007) Inflammation and cancer: breast cancer as a prototype. Breast 16, S27-33
24. Grivennikov, S. I., Greten, F. R., and Karin, M. (2010) Immunity, inflammation, and cancer. Cell 140, 883-899
25. Lamouille, S., Xu, J., and Derynck, R. (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196
26. Li, Y., Zhang, Y., Dorweiler, B., Cui, D., Wang, T., Woo, C. W., Brunkan, C. S., Wolberger, C., Imai, S., and Tabas, I. (2008) Extracellular NAMPT promotes macrophage survival via a nonenzymatic interleukin-6/STAT3 signaling mechanism. J. Biol. Chem. 283, 34833-34843
27. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008) The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715
28. Maeda, M., Johnson, K. R., and Wheelock, M. J. (2005) Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J. Cell Sci. 118, 873-887
29. Lehmann, B. D., Bauer, J. A., Chen, X., Sanders, M. E., Chakravarthy, A. B., Shyr, Y., and Pietenpol, J. A. (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Invest. 121, 2750-2767
30. Rongvaux, A., Shea, R. J., Mulks, M. H., Gigot, D., Urbain, J., Leo, O., and Andris, F. (2002) Pre-B-cell colony-enhancing factor, whose expression is up-regulated in activated lymphocytes, is a nicotinamide phosphoribosyltransferase, a cytosolic enzyme involved in NAD biosynthesis. Eur. J. Immunol. 32, 3225-3234
31. Bogan, K. L., and Brenner, C. (2008) Nicotinic acid, nicotinamide, and nicotinamide riboside: a molecular evaluation of NAD+ precursor vitamins in human nutrition. Annu. Rev. Immunol. 28, 115-130
32. Hasmann, M., and Schemainda, I. (2003) FK866, a highly specific noncompetitive inhibitor of nicotinamide phosphoribosyltransferase, represents a novel mechanism for induction of tumor cell apoptosis. Cancer Res. 63, 7436-7442
33. Olesen, U. H., Christensen, M. K., Björkling, F., Jäättelä, M., Jensen, P. B., Sehested, M., and Nielsen, S. J. (2008) Anticancer agent CHS-828 inhibits cellular synthesis of NAD. Biochem. Biophys. Res. Commun. 367, 799-804
34. Cerna, D., Li, H., Flaherty, S., Takebe, N., Coleman, C. N., and Yoo, S. S. (2012) Inhibition of nicotinamide phosphoribosyltransferase (NAMPT) activity by small molecule GMX1778 regulates reactive oxygen species (ROS)-mediated cytotoxicity in a p53-and nicotinic acid phosphoribosyltransferase1 (NAPRT1)-dependent manner. J. Biol. Chem. 287, 22408-22417
35. Magnone, M., Bauer, I., Poggi, A., Mannino, E., Sturla, L., Brini, M., Zocchi, E., De Flora, A., Nencioni, A., and Bruzzone, S. (2012) NAD+ levels control Ca2+ store replenishment and mitogen-induced increase of cytosolic Ca2+ by cyclic ADP-ribose-dependent TRPM2 channel gating in human T lymphocytes. J. Biol. Chem. 287, 21067-21081
36. Grozio, A., Sociali, G., Sturla, L., Caffa, I., Soncini, D., Salis, A., Raffaelli, N., De Flora, A., Nencioni, A., and Bruzzone, S. (2013) CD73 protein as a source of extracellular precursors for sustained NAD+ biosynthesis in FK866-treated tumor cells. J. Biol. Chem. 288, 25938-25949
37. Liu, P., Li, H., Cepeda, J., Xia, Y., Kempf, J. A., Ye, H., Zhang, L. Q., and Ye, S. Q. (2009) Regulation of inflammatory cytokine expression in pulmonary epithelial cells by pre-B-cell colony-enhancing factor via a nonenzymatic and AP-1-dependent mechanism. J. Biol. Chem. 284, 27344-27351
38. Wang, T., Zhang, X., Bheda, P., Revollo, J. R., Imai, S., and Wolberger, C. (2006) Structure of NAMPT/PBEF/visfatin, a mammalian NAD+ biosynthetic enzyme. Nat. Struct. Mol. Biol. 13, 661-662
39. Revollo, J. R., Körner, A., Mills, K. F., Satoh, A., Wang, T., Garten, A., Dasgupta, B., Sasaki, Y., Wolberger, C., Townsend, R. R., Milbrandt, J., Kiess, W., and Imai, S. (2007) NAMPT/PBEF/Visfatin regulates insulin secretion in β cells as a systemic NAD biosynthetic enzyme. Cell Metab. 6, 363-375
40. Adya, R., Tan, B. K., Punn, A., Chen, J., and Randeva, H. S. (2008) Visfatin induces human endothelial VEGF and MMP-2/9 production via MAPK and PI3K/Akt signalling pathways: novel insights into visfatin-induced angiogenesis. Cardiovasc. Res. 78, 356-365
41. Jia, S. H., Li, Y., Parodo, J., Kapus, A., Fan, L., Rotstein, O. D., and Marshall, J. C. (2004) Pre-B cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis. J. Clin. Invest. 113, 1318-1327
42. Moschen, A. R., Kaser, A., Enrich, B., Mosheimer, B., Theurl, M., Niederegger, H., and Tilg, H. (2007) Visfatin, an adipocytokine with proinflammatory and immunomodulating properties. J. Immunol. 178, 1748-1758
43. Montecucco, F., Cea, M., Cagnetta, A., Damonte, P., Nahimana, A., Ballestrero, A., Del Rio, A., Bruzzone, S., and Nencioni, A. (2013) Nicotinamide phosphoribosyltransferase as a target in inflammation-related disorders. Curr. Top. Med. Chem. 13, 2930-2938
44. Tsouma, I., Kouskouni, E., Demeridou, S., Boutsikou, M., Hassiakos, D., Chasiakou, A., Hassiakou, S., and Baka, S. (2014) Correlation of visfatin levels and lipoprotein lipid profiles in women with polycystic ovary syndrome undergoing ovarian stimulation. Gynecol. Endocrinol. 30, 516-519
45. de Luis, D. A., Aller, R., Gonzalez Sagrado, M., Conde, R., Izaola, O., and de la Fuente, B. (2013) Serum visfatin levels and metabolic syndrome criteria in obese female subjects. Diabetes Metab. Res. Rev. 29, 576-581
46. Dalamaga, M., Archondakis, S., Sotiropoulos, G., Karmaniolas, K., Pelekanos, N., Papadavid, E., and Lekka, A. (2012) Could serum visfatin be a potential biomarker for postmenopausal breast cancer? Maturitas 71, 301-308
47. Reddy, P. S., Umesh, S., Thota, B., Tandon, A., Pandey, P., Hegde, A. S., Balasubramaniam, A., Chandramouli, B. A., Santosh, V., Rao, M. R., Kondaiah, P., and Somasundaram, K. (2008) PBEF1/NAmPRTase/Visfatin: a potential malignant astrocytoma/glioblastoma serum marker with prognostic value. Cancer Biol. Ther. 7, 663-668
48. Fazeli, M. S., Dashti, H., Akbarzadeh, S., Assadi, M., Aminian, A., Keramati, M. R., and Nabipour, I. (2013) Circulating levels of novel adipocytokines in patients with colorectal cancer. Cytokine 62, 81-85
49. Chang, Y. H., Chang, D. M., Lin, K. C., Shin, S. J., and Lee, Y. J. (2011) Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome and cardiovascular diseases: a meta-analysis and systemic review. Diabetes Metab. Res. Rev. 27, 515-527
50. Bruzzone, S., Parenti, M. D., Grozio, A., Ballestrero, A., Bauer, I., Del Rio, A., and Nencioni, A. (2013) Rejuvenating sirtuins: the rise of a new family of cancer drug targets. Curr. Pharm. Des. 19, 614-623
51. Santidrian, A. F., LeBoeuf, S. E., Wold, E. D., Ritland, M., Forsyth, J. S., and Felding, B. H. (2014) Nicotinamide phosphoribosyltransferase can affect metastatic activity and cell adhesive functions by regulating integrins in breast cancer. DNA Repair S1568-7864, 00222-00225
52. Imai, S. (2010) A possibility of nutriceuticals as an anti-aging intervention: activation of sirtuins by promoting mammalian NAD biosynthesis. Pharmacol. Res. 62, 42-47