Antiangiogenic effects of N6-isopentenyladenosine, an endogenous isoprenoid end product, mediated by AMPK activation

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1132-1144

  Pisanti, Simona ^a   Picardi, Paola ^a   Ciaglia, Elena ^a   Margarucci, Luigi ^a   Ronca, Roberto ^b   Giacomini, Arianna ^b   Malfitano, Anna Maria ^a   Casapullo, Agostino ^a   Laezza, Chiara ^c   Gazzerro, Patrizia ^a   Bifulco, Maurizio ^a  

^a UNIVERSITY OF SALERNO   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c CNR   (Italy)

Author keywords

AMP mimetic; Cancer progression; Endothelial cells; Mevalonate pathway

Indexed keywords

5 IODOTUBERCIDIN; 6 N (3,3 DIMETHYLALLYL)ADENOSINE; ADENOSINE KINASE; ADENYLATE KINASE; ISOPENTENYL DIPHOSPHATE; ANGIOGENESIS INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CHEMICAL STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DOSE TIME EFFECT RELATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; TUMOR GROWTH; UMBILICAL VEIN ENDOTHELIAL CELL; AMP-MIMETIC; CANCER GROWTH; METABOLISM; MEVALONATE PATHWAY; NEOVASCULARIZATION (PATHOLOGY); PHOSPHORYLATION;

AMP-MIMETIC; CANCER PROGRESSION; ENDOTHELIAL CELLS; MEVALONATE PATHWAY;

AMP-ACTIVATED PROTEIN KINASES; ANGIOGENESIS INHIBITORS; CHROMATOGRAPHY, LIQUID; ENZYME ACTIVATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISOPENTENYLADENOSINE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; TANDEM MASS SPECTROMETRY;

EID: 84899543582     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-238238     Document Type: Article

References (58)

1. Faust, J. R., and Dice, J. F. (1991) Evidence for isopentenyladenine modification on a cell cycle-regulated protein. J. Biol. Chem. 266, 9961-9970
2. Bifulco, M., Malfitano, A. M., Proto, M. C., Santoro, A., Caruso, M. G., and Laezza, C. (2008) Biological and pharmacological roles of N6-isopentenyladenosine: an emerging anticancer drug. Anticancer Agents Med. Chem. 8, 200-204
3. Laezza, C., Malfitano, A. M., Di Matola, T., Ricchi, P., and Bifulco, M. (2010) Involvement of Akt/NF-κB pathway in N6-isopentenyladenosine-induced apoptosis in human breast cancer cells. Mol. Carcinog. 49, 892-901
4. Burns, D. M., Rodi, C. P., and Agris, P. F. (1976) Natural occurrence of an inhibitor of mammalian cell growth in human and mouse cells of normal and tumor origin. Cancer Biochem. Biophys. 1, 269-280
5. Laezza, C., Migliaro, A., Cerbone, R., Tedesco, I., Santillo, M., Garbi, C., and Bifulco, M. (1997) N6-isopentenyladenosine affects cAMP-dependent microfilament organization in FRTL-5 thyroid cells. Exp. Cell Res. 234, 178-182
6. Laezza, C., Notarnicola, M., Caruso, M. G., Messa, C., Macchia, M., Bertini, S., Minutolo, F., Portella, G., Fiorentino, L., Stingo, S., and Bifulco, M. (2006) N6-isopentenyladenosine arrests tumor cell proliferation by inhibiting farnesyl diphosphate synthase and protein prenylation. FASEB J. 20, 412-418
7. Laezza, C., Caruso, M. G., Gentile, T., Notarnicola, M., Malfitano, A. M., Di Matola, T., Messa, C., Gazzerro, P., and Bifulco, M. (2009) N6-isopentenyladenosine inhibits cell proliferation and induces apoptosis in a human colon cancer cell line DLD1. Int. J. Cancer 124, 1322-1329
8. Spinola, M., Colombo, F., Falvella, F. S., and Dragani, T. A. (2007) N6-isopentenyladenosine: a potential therapeutic agent for a variety of epithelial cancers. Int. J. Cancer 120, 2744-2748
9. Carmeliet, P. (2003) Angiogenesis in health and disease. Nat. Med. 9, 653-660
10. Potente, M., Gerhardt, H., and Carmeliet, P. (2011) Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887
11. Hardie, D. G., Hawley, S. A., and Scott, J. W. (2006) AMPactivated protein kinase-development of the energy sensor concept. J. Physiol. 574, 7-15
12. Zou, M. H., and Wu, Y. (2008) AMP-Activated protein kinase activation as a strategy for protecting vascular endothelial function. Clin. Exp. Pharmacol. Physiol. 35, 535-545
13. Morrow, V. A., Foufelle, F., Connell, J. M., Petrie, J. R., Gould, G. W., and Salt, I. P. (2003) Direct activation of AMP-Activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. J. Biol. Chem. 278, 31629-31639
14. Ewart, M. A., Kohlhaas, C. F., and Salt, I. P. (2008) Inhibition of tumor necrosis factor α-stimulated monocyte adhesion to human aortic endothelial cells by AMP activated protein kinase. Arterioscler. Thromb. Vasc. Biol. 28, 2255-2257
15. Gaskin, F. S., Kamada, K., Yusof, M., Durante, W., Gross, G., and Korthuis, R. J. (2009) AICAR preconditioning prevents postischemic leukocyte rolling and adhesion: role of KATP channels and heme oxygenase. Microcirculation 16, 167-176
16. Liu, X. M., Peyton, K. J., Shebib, A. R., Wang, H., Korthuis, R. J., and Durante, W. (2011) Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival. Am. J. Physiol. Heart Circ. Physiol. 300, H84-H93
17. Reihill, J. A., Ewart, M. A., and Salt, I. P. (2011) The role of AMP-Activated protein kinase in the functional effects of vascular endothelial growth factor-A and -B in human aortic endothelial cells. Vasc. Cell 3, 9
18. Peyton, K. J., Liu, X. M., Yu, Y., Yates, B., and Durante, W. (2012) Activation of AMP-Activated protein kinase inhibits the proliferation of human endothelial cells. J. Pharmacol. Exp. Ther. 342, 827-834
19. Theodoropoulou, S., Brodowska, K., Kayama, M., Morizane, Y., Miller, J.W., Gragoudas, E. S., and Vavvas, D. G. (2013) Aminoimidazole carboxamide ribonucleotide (AICAR) inhibits the growth of retinoblastoma in vivo by decreasing angiogenesis and inducing apoptosis. PLoS ONE 8, e52852
20. Pisanti, S., Picardi, P., Prota, L., Proto, M. C., Laezza, C., McGuire, P. G., Morbidelli, L., Gazzerro, P., Ziche, M., Das, A., and Bifulco, M. (2011) Genetic and pharmacologic inactivation of cannabinoid CB1 receptor inhibits angiogenesis. Blood 117, 5541-5550
21. Bucci, M., Cantalupo, A., Vellecco, V., Panza, E., Monti, M.C., Zampella, A., and Ianaro, A.,and Cirino, G. (2013) Perthamide C inhibits eNOS and iNOS expression and has immunomodulating activity in vivo. PLoS ONE 8, e57801
22. Laezza, C., Pisanti, S., Crescenzi, E., and Bifulco, M. (2006) Anandamide inhibits Cdk2 and activates Chk1 leading to cell cycle arrest in human breast cancer cells. FEBS Lett. 580, 6076-6082
23. Santoro, A., Pisanti, S., Grimaldi, C., Izzo, A. A., Borrelli, F., Proto, M. C., Malfitano, A. M., Gazzerro, P., Laezza, C., and Bifulco, M. (2009) Rimonabant inhibits human colon cancer cell growth and reduces the formation of precancerous lesions in the mouse colon. Int. J. Cancer 125, 996-1003
24. Laezza, C., Pisanti, S., Malfitano, A. M., and Bifulco, M. (2008) The anandamide analog, Met-F-AEA, controls human breast cancer cell migration via the RHOA/RHO kinase signaling pathway. Endocr. Relat. Cancer 15, 965-974
25. Coltrini, D., Di Salle, E., Ronca, R., Belleri, M., Testini, C., and Presta, M. (2013) Matrigel plug assay: evaluation of the angiogenic response by reverse transcription-quantitative PCR. Angiogenesis 16, 469-477
26. Ronca, R., Alessi, P., Coltrini, D., Di Salle, E., Giacomini, A., Leali, D., Corsini, M., Belleri, M., Tobia, C., Garlanda, C., Bonomi, E., Tardanico, R., Vermi, W., and Presta, M. (2013) Long pentraxin-3 as an epithelial-stromal fibroblast growth factor-Targeting inhibitor in prostate cancer. J. Pathol. 230, 228-238
27. Auchampach, J,A. (2007) Adenosine receptors and angiogenesis. Circ. Res. 101, 1075-1077
28. Ciaglia, E., Pisanti, S., Picardi, P., Laezza, C., Malfitano, A.M., D'Alessandro, A., Gazzerro, P., Vitale, M., Carbone, E., and Bifulco, M. (2013) N6-isopentenyladenosine, an endogenous isoprenoid end product, directly affects cytotoxic and regulatory functions of human NK cells through FDPS modulation. [E-pub ahead of print]. J. Leukoc. Biol. doi: 10.1189/jlb.0413190
29. Divekar, A. Y., Slocum, H. K., and Hakala, M. T. (1974) N6-(delta2-isopentenyl)adenosine 5=-monophosphate: formation and effect on purine metabolism in cellular and enzymatic systems. Mol. Pharmacol. 10, 529-543
30. Mok, D. W., and Mok, M. C. (2001) Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 89-118
31. Golovko, A., Hjälm, G., Sitbon, F., and Nicander, B. (2000) Cloning of a human tRNA isopentenyl transferase. Gene 258, 85-93
32. Sinclair, C. J., Powell, A. E., Xiong, W., LaRivière, C. G., Baldwin, S. A., Cass, C. E., Young, J. D., and Parkinson, F. E. (2001) Nucleoside transporter subtype expression: effects on potency of adenosine kinase inhibitors. Br. J. Pharmacol. 134, 1037-1044
33. Lee, D. H., Lee, T. H., Jung, C. H., and Kim, Y. H. (2012) Wogonin induces apoptosis by activating the AMPK and p53 signaling pathways in human glioblastoma cells. Cell. Signal. 24, 2216-2225
34. Corton, J. M., Gillespie, J. G., Hawley, S. A., and Hardie, D. G. (1995) 5-Aminoimidazole-4-carboxamide ribonucleoside: a specific method for activating AMP-Activated protein kinase in intact cells? Eur. J. Biochem. 229, 558-565
35. Ouchi, N., Kobayashi, H., Kihara, S., Kumada, M., Sato, K., Inoue, T., Funahashi, T., and Walsh, K. (2004) Adiponectin stimulates angiogenesis by promoting cross-Talk between AMPactivated protein kinase and Akt signaling in endothelial cells. J. Biol. Chem. 279, 1304-1309
36. Stahmann, N., Woods, A., Spengler, K., Heslegrave, A., Bauer, R., Krause, S., Viollet, B.,Carling, D., and Heller, R. (2010) Activation of AMP-Activated protein kinase by vascular endothelial growth factor mediates endothelial angiogenesis independently of nitric-oxide synthase. J. Biol. Chem. 285, 10638-10652
37. Su, K. H., Yu, Y. B., Hou, H. H., Zhao, J. F., Kou, Y. R., Cheng, L. C., Shyue, S. K., and Lee, T. S. (2012) AMP-Activated protein kinase mediates erythropoietin-induced activation of endothelial nitric oxide synthase. J. Cell. Physiol. 227, 3053-3062
38. Nagata, D., Mogi, M., and Walsh, K. (2003) AMP-Activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem. 278, 31000-31006
39. Kanellis, J., Kandane, R. K., Etemadmoghadam, D., Fraser, S. A., Mount, P. F., Levidiotis, V., Kemp, B. E., and Power, D. A. (2006) Activators of the energy sensing kinase AMPK inhibit random cell movement and chemotaxis in U937 cells. Immunol. Cell Biol. 84, 6-12
40. Ruscica, M., Dozio, E., Steffani, L., Passafaro, L., Mazzer, M., Castellano, J. M., Motta, M., Tena-Sempere, M., and Magni, P. (2011) Role of the energy sensor adenosine monophosphateactivated protein kinase in the regulation of immature gonadotropin releasing hormone neuron migration. J. Endocrinol. Invest. 34, e362-e368
41. Esfahanian, N., Shakiba, Y., Nikbin, B., Soraya, H., Maleki-Dizaji, N., Ghazi-Khansari, M., and Garjani, A. (2012) Effect of metformin on the proliferation, migration, and MMP-2 and -9 expression of human umbilical vein endothelial cells. Mol. Med. Report 5, 1068-1074
42. Morizane, Y., Thanos, A., Takeuchi, K., Murakami, Y., Kayama, M., Trichonas, G., Miller, J., Foretz, M., Viollet, B., and Vavvas, D. G. (2011) AMP-Activated protein kinase suppresses matrix metalloproteinase-9 expression in mouse embryonic fibroblasts. J. Biol. Chem. 286, 16030-16038
43. Laplante, M., and Sabatini, D. M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293
44. Theodoropoulou, S., Kolovou, P. E., Morizane, Y., Kayama, M., Nicolaou, F., Miller, J. W., Gragoudas, E., Ksander, B. R., and Vavvas, D. G. (2010) Retinoblastoma cells are inhibited by aminoimidazole carboxamide ribonucleotide (AICAR) partially through activation of AMP-dependent kinase. FASEB J. 24, 2620-2630
45. Chen, M. B., Shen, W. X., Yang, Y., Wu, X. Y., Gu, J. H., and Lu, P. H. (2011) Activation of AMP-Activated protein kinase is involved in vincristine-induced cell apoptosis in B16 melanoma cell. J. Cell. Physiol. 226, 1915-1925
46. Chen, M. B., Wu, X. Y., Gu, J. H., Guo, Q. T., Shen, W. X., and Lu, P. H. (2011) Activation of AMP-Activated protein kinase contributes to doxorubicin-induced cell death and apoptosis in cultured myocardial H9c2 cells. Cell. Biochem. Biophys. 60, 311-322
47. Vakana, E., Altman, J. K., Glaser, H., Donato, N. J., and Platanias, L. C. (2011) Antileukemic effects of AMPK activators on BCR-ABL-expressing cells. Blood 118, 6399-6402
48. Zheng, Q. Y., Jin, F. S., Yao, C., Zhang, T., Zhang, G. H., and Ai, X. (2012) Ursolic acid-induced AMP-Activated protein kinase (AMPK) activation contributes to growth inhibition and apoptosis in human bladder cancer T24 cells. Biochem. Biophys. Res. Commun. 419, 741-747
49. Lee, C.W., Wong, L.L., Tse, E.Y., Liu, H.F., Leong, V.Y., Lee, J.M., Hardie, D.G., Ng, I. O., and Ching, Y. P. (2012) AMPK promotes p53 acetylation via phosphorylation and inactivation of SIRT1 in liver cancer cells. Cancer Res.72, 4394-4404
50. Sanli, T., Steinberg, G.R., Singh, G., and Tsakiridis, T. (2013) AMP-Activated protein kinase (AMPK) beyond metabolism: a novel genomic stress sensor participating in the DNA damage response pathway. [E-pub ahead of print.] Cancer Biol. Ther. 10.4161/cbt.26726
51. Folkman, J. (2006) Angiogenesis. Annu. Rev. Med. 57, 1-18
52. Simó, R., Carrasco, E., García-Ramírez, M., and Hernández, C. (2006) Angiogenic and antiangiogenic factors in proliferative diabetic retinopathy. Curr. Diabetes Rev. 2, 71-98
53. Göransson, O., McBride, A., Hawley, S. A., Ross, F. A., Shpiro, N., Foretz, M., Viollet, B., Hardie, D. G., and Sakamoto, K. (2007) Mechanism of action of A-769662, a valuable tool for activation of AMP-Activated protein kinase. J. Biol. Chem. 282, 32549-32560
54. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M. F., Goodyear, L. J., and Moller, D. E. (2001) Role of AMP-Activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108, 1167-1174
55. Landman, G. W., Kleefstra, N., van Hateren, K. J., Groenier, K. H., Gans, R. O., and Bilo, H. J. (2010) Metformin associated with lower cancer mortality in type 2 diabetes: ZODIAC-16. Diabetes Care 33, 322-326
56. Meisse, D., Van de Casteele, M., Beauloye, C., Hainault, I., Kefas, B. A., Rider, M. H., Foufelle, F., and Hue, L. (2002) Sustained activation of AMP-Activated protein kinase induces c-Jun N-Terminal kinase activation and apoptosis in liver cells. FEBS Lett. 526, 38-42
57. Yung, M. M., Chan, D. W., Liu, V. W., Yao, K. M., and Ngan, H. Y. (2013) Activation of AMPK inhibits cervical cancer cell growth through AKT/FOXO3a/FOXM1 signaling cascade. BMC Cancer 13, 327-335
58. Laezza, C., Fiorentino, L., Pisanti, S., Gazzerro, P., Caraglia, M., Portella, G., Vitale, M., and Bifulco, M. (2008) Lovastatin induces apoptosis of k-ras-Transformed thyroid cells via inhibition of ras farnesylation and by modulating redox state. J. Mol. Med. (Berl.) 86, 1341-1351