Toluquinol, a marine fungus metabolite, is a new angiosuppresor that interferes the Akt pathway

Biochemical Pharmacology

Volumn 85, Issue 12, 2013, Pages 1727-1740

  García Caballero, Melissa ^a,b   Marí Beffa, Manuel ^a   Cañedo, Librada ^c   Medina, Miguel Ángel ^a,b   Quesada, Ana R ^a,b  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c Instituto Biomar SA   (Spain)

Author keywords

2 Methylhydroquinone; Angiogenesis; Cancer; Marine compounds; Toluquinol

Indexed keywords

ANGIOGENESIS INHIBITOR; CASPASE; FIBROBLAST GROWTH FACTOR; FUNGAL EXTRACT; METHYLBENZOQUINOL; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CAPILLARY TUBE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; GROWTH INHIBITION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; TUMOR CELL;

ANGIOGENESIS INHIBITORS; ANIMALS; CATTLE; CELL MOVEMENT; CELLS, CULTURED; CHICK EMBRYO; DOSE-RESPONSE RELATIONSHIP, DRUG; HEK293 CELLS; HT29 CELLS; HUMANS; HYDROQUINONES; PENICILLIUM; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 84878840937     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.04.007     Document Type: Article

References (50)

1. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 5 2011 646 674
2. A.R. Quesada, M.Á. Medina, R. Muñoz-Chápuli, and Á.L. Ponce Do not say ever never more: the ins and outs of antiangiogenic therapies Curr Pharm Des 16 35 2010 3932 3957
3. G.M. Cragg, and D.J. Newman Medicinals for the millennia: the historical record Ann N Y Acad Sci 953 2001 3 25 (Pubitemid 34072972)
4. J. Bérdy Bioactive microbial metabolites J Antibiot (Tokyo) 58 1 2005 1 26
5. I. Bhatnagar, and S.K. Kim Immense essence of excellence: marine microbial bioactive compounds Mar Drugs 8 10 2010 2673 2701
6. J.F. Imhoff, A. Labes, and J. Wiese Bio-mining the microbial treasures of the ocean: new natural products Biotechnol Adv 29 5 2011 468 482
7. S.T. Carey, and M.S.R. Nair Metabolites of pyrenomycetes. 10. Isolation of para-toluquinone and toluquinol from nectria-erubescens Lloydia 42 2 1979 231
8. J. Huang, A.R. Putnam, G.M. Werner, S.K. Mishra, and C. Whitenack Herbicidal metabolites from a soil-dwelling fungus (Scopulariopis brumptii) Weed Sci 37 1989 123 128
9. C. Cárdenas, A.R. Quesada, and M.A. Medina Evaluation of the anti-angiogenic effect of aloe-emodin Cell Mol Life Sci 63 2006 3083 3089 (Pubitemid 46072310)
10. S. Rodríguez-Nieto, M. González-Iriarte, R. Carmona, R. Muñoz-Chápuli, M.A. Medina, and A.R. Quesada Antiangiogenic activity of aeroplysinin-1, a brominated compound isolated from a marine sponge FASEB J 16 2 2002 261 263
11. V.S. Pribluda, E.R. Gubish Jr., T.M. Lavallee, A. Treston, G.M. Swartz, and S.J. Green 2-Methoxyestradiol: an endogenous antiangiogenic and antiproliferative drug candidate Cancer Metastasis Rev 19 1-2 2000 173 179 (Pubitemid 32004707)
12. M. García-Caballero, M. Marí-Beffa, M.A. Medina, and A.R. Quesada Dimethylfumarate inhibits angiogenesis in vitro and in vivo: a possible role for its antipsoriatic effect? J Invest Dermatol 131 6 2011 1347 1355
13. T.C. Tran, B. Sneed, J. Haider, D. Blavo, A. White, and T. Aiyejorun Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish Cancer Res 67 23 2007 11386 11392 (Pubitemid 350248566)
14. I. Arnaoutova, and H.K. Kleinman In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract Nat Protoc 5 4 2010 628 635
15. R. Muñoz-Chápuli, A.R. Quesada, and M.A. Medina Angiogenesis and signal transduction in endothelial cells Cell Mol Life Sci 61 17 2004 2224 2243 (Pubitemid 39280120)
16. N.D. Lawson, and B.M. Weinstein In vivo imaging of embryonic vascular development using transgenic zebrafish Dev Biol 248 2 2002 307 318 (Pubitemid 35002091)
17. P.E. Bayliss, K.L. Bellavance, G.G. Whitehead, J.M. Abrams, S. Aegerter, and H.S. Robbins Chemical modulation of receptor signaling inhibits regenerative angiogenesis in adult zebrafish Nat Chem Biol 2 5 2006 265 273
18. C.C. Huang, N.D. Lawson, B.M. Weinstein, and S.L. Johnson reg6 is required for branching morphogenesis during blood vessel regeneration in zebrafish caudal fins Dev Biol 264 1 2003 263 274 (Pubitemid 37393462)
19. T.P. Fan, J.C. Yeh, K.W. Leung, P.Y. Yue, and R.N. Wong Angiogenesis: from plants to blood vessels Trends Pharmacol Sci 27 6 2006 297 309 (Pubitemid 43850005)
20. B.E. Cavell, S.S. Syed Alwi, A. Donlevy, and G. Packham Anti-angiogenic effects of dietary isothiocyanates: mechanisms of action and implications for human health Biochem Pharmacol 81 3 2011 327 336
21. J.W. Blunt, B.R. Copp, M.H. Munro, P.T. Northcote, and M.R. Prinsep Marine natural products Nat Prod Rep 28 2011 196 268
22. M.E. Castro, M. González-Iriarte, A.F. Barrero, N. Salvador-Tormo, R. Muñoz-Chápuli, and M.A. Medina Study of puupehenone and related compounds as inhibitors of angiogenesis Int J Cancer 110 1 2004 31 38 (Pubitemid 38507201)
23. J. Ma, X. Xin, L. Meng, L. Tong, L. Lin, and M. Geng The marine-derived oligosaccharide sulfate (MdOS), a novel multiple tyrosine kinase inhibitor, combats tumor angiogenesis both in vitro and in vivo PLoS ONE 3 11 2008 e3774
24. A.S. Rothmeier, I. Ischenko, J. Joore, D. Garczarczyk, R. Fürst, and C.J. Bruns Investigation of the marine compound spongistatin 1 links the inhibition of PKCalpha translocation to nonmitotic effects of tubulin antagonism in angiogenesis FASEB J 23 2009 1127 1137
25. B. Martínez-Poveda, A.R. Quesada, and M.A. Medina Hypericin in the dark inhibits key steps of angiogenesis in vitro Eur J Pharmacol 516 2005 97 103 (Pubitemid 40799344)
26. A. López-Jiménez, M. García-Caballero, M.A. Medina, and A.R. Quesada Anti-angiogenic properties of carnosol and carnosic acid, two major dietary compounds from rosemary Eur J Nutr 52 1 2013 85 95
27. Y.H. Kim, E.K. Shin, D.H. Kim, H.H. Lee, J.H. Park, and J.K. Kim Antiangiogenic effect of licochalcone A Biochem Pharmacol 80 8 2010 1152 1159
28. C. Fortes, J.A. García-Vilas, A.R. Quesada, and M.A. Medina Evaluation of the anti-angiogenic potential of hydroxytyrosol and tyrosol, two bio-active phenolic compounds of extra virgin olive oil, in endothelial cell cultures Food Chem 134 2012 134 140
29. K. Igura, T. Ohta, Y. Kuroda, and K. Kaji Resveratrol and quercetin inhibit angiogenesis in vitro Cancer Lett 171 1 2001 11 16 (Pubitemid 32727351)
30. C. Cárdenas, A.R. Quesada, and M.A. Medina Evaluation of the anti-angiogenic effect of aloe-emodin Cell Mol Life Sci 63 24 2006 3083 3089 (Pubitemid 46072310)
31. X. Bai, F. Cerimele, M. Ushio-Fukai, M. Waqas, P.M. Campbell, and B. Govindarajan Honokiol, a small molecular weight natural product, inhibits angiogenesis in vitro and tumor growth in vivo J Biol Chem 278 37 2003 35501 35507 (Pubitemid 37102321)
32. P. Cuevas, I. Sanchez, R.M. Lozano, and G. Gimenez-Gallego Dobesilate is an angiogenesis inhibitor Eur J Med Res 10 9 2005 369 372 (Pubitemid 41358532)
33. I.S. Fernández, P. Cuevas, J. Angulo, P. López-Navajas, A. Canales-Mayordomo, and R. González-Corrochano Gentisic acid, a compound associated with plant defense and a metabolite of aspirin, heads a new class of in vivo fibroblast growth factor inhibitors J Biol Chem 285 15 2010 11714 11729
34. S. Rodríguez-Nieto, M.A. Medina, and A.R. Quesada A re-evaluation of fumagillin selectivity towards endothelial cells Anticancer Res 21 2001 3457 3460 (Pubitemid 34224252)
35. H.U. Simon, A. Haj-Yehia, and F. Levi-Schaffer Role of reactive oxygen species (ROS) in apoptosis induction Apoptosis 5 2000 415 418 (Pubitemid 32162623)
36. M. Murata, M. Tsujikawa, and S. Kawanishi Oxidative DNA damage by minor metabolites of toluene may lead to carcinogenesis and reproductive dysfunction Biochem Biophys Res Commun 261 2 1999 478 483 (Pubitemid 29392501)
37. C.E. Whibley, K.L. McPhail, R.A. Keyzers, M.F. Maritz, V.D. Leaner, and M.J. Birrer Reactive oxygen species mediated apoptosis of esophageal cancer cells induced by marine triprenyl toluquinones and toluhydroquinones Mol Cancer Ther 6 9 2007 2535 2543 (Pubitemid 47480419)
38. B. Martínez-Poveda, R. Muñoz-Chápuli, S. Rodríguez-Nieto, J.M. Quintela, A. Fernández, and M.A. Medina IB05204, a dichloropyridodithienotriazine, inhibits angiogenesis in vitro and in vivo Mol Cancer Ther 6 2007 2675 2685 (Pubitemid 350058148)
39. J.C. Yeh, T. Cindrova-Davies, M. Belleri, L. Morbidelli, N. Miller, and C.W. Cho The natural compound n-butylidenephthalide derived from the volatile oil of Radix Angelica sinensis inhibits angiogenesis in vitro and in vivo Angiogenesis 14 2 2011 187 197
40. C.H. Yi, and J. Yuan The Jekyll and Hyde functions of caspases Dev Cell 16 2009 21 34
41. K. Kessenbrock, V. Plaks, and Z. Werb Matrix metalloproteinases: regulators of the tumor microenvironment Cell 141 2010 52 67
42. J. Fang, Y. Shing, D. Wiederschain, L. Yan, C. Butterfield, and G. Jackson Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model Proc Natl Acad Sci USA 97 2000 3884 3889 (Pubitemid 30226056)
43. T. Itoh, M. Tanioka, H. Yoshida, T. Yoshioka, H. Nishimoto, and S. Itohara Reduced angiogenesis and tumor progression in gelatinase A-deficient mice Cancer Res 58 1998 1048 1051 (Pubitemid 28182477)
44. J.Q. Cheng, C.W. Lindsley, G.Z. Cheng, H. Yang, and S.V. Nicosia The Akt/PKB pathway: molecular target for cancer drug discovery Oncogene 24 50 2005 7482 7492 (Pubitemid 41637988)
45. B.H. Jiang, and L.Z. Liu AKT signaling in regulating angiogenesis Curr Cancer Drug Targets 8 1 2008 19 26
46. B. Martínez-Poveda, A.R. Quesada, and M.A. Medina Hyperforin, a bio-active compound of St, John's Wort, is a new inhibitor of angiogenesis targeting several key steps of the process Int J Cancer 117 5 2005 775 780 (Pubitemid 41598828)
47. J. Angulo, C. Peiró, T. Romacho, A. Fernández, B. Cuevas, and R. González-Corrochano Inhibition of vascular endothelial growth factor (VEGF)-induced endothelial proliferation, arterial relaxation, vascular permeability and angiogenesis by dobesilate Eur J Pharmacol 667 1-3 2011 153 159
48. P. Cuevas, and J.M. Arrazola Therapeutic response of rosacea to dobesilate Eur J Med Res 10 10 2005 454 456 (Pubitemid 41614706)
49. M.L. Ribeiro, A.I. Seres, A.M. Carneiro, M. Stur, A. Zourdani, and P. Caillon Effect of calcium dobesilate on progression of early diabetic retinopathy: a randomised double-blind study Graefes Arch Clin Exp Ophthalmol 244 2006 1591 1600 (Pubitemid 44830817)
50. P. Cuevas, F. Carceller, J. Angulo, R. González-Corrochano, A. Cuevas-Bourdier, and G. Giménez-Gallego Antiglioma effects of a new, low molecular mass, inhibitor of fibroblast growth factor Neurosci Lett 491 1 2011 1 7