AICAR inhibits cancer cell growth and triggers cell-type distinct effects on OXPHOS biogenesis, oxidative stress and Akt activation

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 6, 2011, Pages 707-718

  Jose, Caroline ^a,b   Hébert Chatelain, Etienne ^a,b   Bellance, Nadège ^a,b   Larendra, Anaïs ^a,b   Su, Melser ^a,b   Nouette Gaulain, Karine ^a,b   Rossignol, Rodrigue ^a,b  

^a Laboratoire Maladies Rares Génétique et Métabolisme Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

AICAR; Mitochondrion; Oxidative phosphorylation; Tumor

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; HYPOXIA INDUCIBLE FACTOR 1; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL MEMBRANE POTENTIAL; CELL PROLIFERATION; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; EMBRYO CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN STABILITY; UPREGULATION;

EID: 79955623949     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2010.12.002     Document Type: Article

References (58)

1. A. Isidoro, M. Martinez, P.L. Fernandez, A.D. Ortega, G. Santamaria, M. Chamorro, J.C. Reed, and J.M. Cuezva Alteration of the bioenergetic phenotype of mitochondria is a hallmark of breast, gastric, lung and oesophageal cancer Biochem J 378 2004 17 20 (Pubitemid 38299539)
2. X.L. Zu, and M. Guppy Cancer metabolism: facts, fantasy, and fiction Biochem Biophys Res Commun 313 2004 459 465 (Pubitemid 38021849)
3. R. Moreno-Sanchez, S. Rodriguez-Enriquez, A. Marin-Hernandez, and E. Saavedra Energy metabolism in tumor cells FEBS J 274 2007 1393 1418 (Pubitemid 46333738)
4. F. Weinberg, and N.S. Chandel Mitochondrial metabolism and cancer Ann NY Acad Sci 1177 2009 66 73
5. K. Smolkova, L. Plecita-Hlavata, N. Bellance, G. Benard, R. Rossignol, and P. Jezek Waves of gene regulation suppress and then restore oxidative phosphorylation in cancer cells Int J Biochem Cell Biol 2010
6. M. Guppy, P. Leedman, X. Zu, and V. Russell Contribution by different fuels and metabolic pathways to the total ATP turnover of proliferating MCF-7 breast cancer cells Biochem J 364 2002 309 315 (Pubitemid 34538975)
7. S. Rodriguez-Enriquez, L. Carreno-Fuentes, J.C. Gallardo-Perez, E. Saavedra, H. Quezada, A. Vega, A. Marin-Hernandez, V. Olin-Sandoval, M.E. Torres-Marquez, and R. Moreno-Sanchez Oxidative phosphorylation is impaired by prolonged hypoxia in breast and possibly in cervix carcinoma Int J Biochem Cell Biol 2010
8. L. Reitzer, B. Wice, and D. Kennel Evidence that glutamine, not sugar, is the major energy source for cultured Hela cells JBC 254 1979 2669 2676 (Pubitemid 9196102)
9. E. Hervouet, A. Cizkova, J. Demont, A. Vojtiskova, P. Pecina, N.L. Franssen-van Hal, J. Keijer, H. Simonnet, R. Ivanek, S. Kmoch, C. Godinot, and J. Houstek HIF and reactive oxygen species regulate oxidative phosphorylation in cancer Carcinogenesis 29 2008 1528 1537
10. N. Bellance, G. Benard, F. Furt, H. Begueret, K. Smolkova, E. Passerieux, J.P. Delage, J.M. Baste, P. Moreau, and R. Rossignol Bioenergetics of lung tumors: alteration of mitochondrial biogenesis and respiratory capacity Int J Biochem Cell Biol 41 2009 2566 2577
11. M. Sanchez-Arago, M. Chamorro, and J.M. Cuezva Selection of cancer cells with repressed mitochondria triggers colon cancer progression Carcinogenesis 31 2010 567 576
12. P. Acebo, D. Giner, P. Calvo, A. Blanco-Rivero, A.D. Ortega, P.L. Fernandez, G. Roncador, E. Fernandez-Malave, M. Chamorro, and J.M. Cuezva Cancer abolishes the tissue type-specific differences in the phenotype of energetic metabolism Transl Oncol 2 2009 138 145
13. E. Hervouet, J. Demont, P. Pecina, A. Vojtiskova, J. Houstek, H. Simonnet, and C. Godinot A new role for the von Hippel-Lindau tumor suppressor protein: stimulation of mitochondrial oxidative phosphorylation complex biogenesis Carcinogenesis 26 2005 531 539 (Pubitemid 41214141)
14. L. Galluzzi, N. Larochette, N. Zamzami, and G. Kroemer Mitochondria as therapeutic targets for cancer chemotherapy Oncogene 25 2006 4812 4830 (Pubitemid 44192089)
15. S. Rodriguez-Enriquez, A. Marin-Hernandez, J.C. Gallardo-Perez, L. Carreno-Fuentes, and R. Moreno-Sanchez Targeting of cancer energy metabolism Mol Nutr Food Res 53 2009 29 48
16. P.L. Pedersen Tumor mitochondria and the bioenergetics of cancer cells Prog Exp Tumor Res 22 1978 190 274
17. N. Bellance, P. Lestienne, and R. Rossignol Mitochondria: from bioenergetics to the metabolic regulation of carcinogenesis Front Biosci 14 2009 4015 4034
18. S. Rodriguez-Enriquez, J.C. Gallardo-Perez, A. Aviles-Salas, A. Marin-Hernandez, L. Carreno-Fuentes, V. Maldonado-Lagunas, and R. Moreno-Sanchez Energy metabolism transition in multi-cellular human tumor spheroids J Cell Physiol 216 2008 189 197 (Pubitemid 351813110)
19. J.M. Cuezva, G. Chen, A.M. Alonso, A. Isidoro, D.E. Misek, S.M. Hanash, and D.G. Beer The bioenergetic signature of lung adenocarcinomas is a molecular marker of cancer diagnosis and prognosis Carcinogenesis 25 2004 1157 1163 (Pubitemid 38968043)
20. J.M. Cuezva, M. Krajewska, M.L. de Heredia, S. Krajewski, G. Santamaria, H. Kim, J.M. Zapata, H. Marusawa, M. Chamorro, and J.C. Reed The bioenergetic signature of cancer: a marker of tumor progression Cancer Res 62 2002 6674 6681 (Pubitemid 35364137)
21. R. Rossignol, R. Gilkerson, R. Aggeler, K. Yamagata, S.J. Remington, and R.A. Capaldi Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells Cancer Res 64 2004 985 993 (Pubitemid 38176901)
22. K. Smolkova, N. Bellance, F. Scandurra, E. Genot, E. Gnaiger, L. Plecita-Hlavata, P. Jezek, and R. Rossignol Mitochondrial bioenergetic adaptations of breast cancer cells to aglycemia and hypoxia J Bioenerg Biomembr 42 2010 55 67
23. L.H. Stockwin, S.X. Yu, S. Borgel, C. Hancock, T.L. Wolfe, L.R. Phillips, M.G. Hollingshead, and D.L. Newton Sodium dichloroacetate selectively targets cells with defects in the mitochondrial ETC Int J Cancer 2010
24. T.J. Schulz, R. Thierbach, A. Voigt, G. Drewes, B. Mietzner, P. Steinberg, A.F. Pfeiffer, and M. Ristow Induction of oxidative metabolism by mitochondrial frataxin inhibits cancer growth: Otto Warburg revisited J Biol Chem 281 2006 977 981
25. M. Lagouge, C. Argmann, Z. Gerhart-Hines, H. Meziane, C. Lerin, F. Daussin, N. Messadeq, J. Milne, P. Lambert, P. Elliott, B. Geny, M. Laakso, P. Puigserver, and J. Auwerx Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha Cell 127 2006 1109 1122 (Pubitemid 44894520)
26. C. Canto, Z. Gerhart-Hines, J.N. Feige, M. Lagouge, L. Noriega, J.C. Milne, P.J. Elliott, P. Puigserver, and J. Auwerx AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity Nature 458 2009 1056 1060
27. W.W. Winder, B.F. Holmes, D.S. Rubink, E.B. Jensen, M. Chen, and J.O. Holloszy Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle J Appl Physiol 88 2000 2219 2226 (Pubitemid 30453931)
28. L. Yu, and S.J. Yang AMP-activated protein kinase mediates activity-dependent regulation of peroxisome proliferator-activated receptor gamma coactivator-1alpha and nuclear respiratory factor 1 expression in rat visual cortical neurons Neuroscience 169 2010 23 38
29. G.K. McConell, G.P. Ng, M. Phillips, Z. Ruan, S.L. Macaulay, and G.D. Wadley Central role of nitric oxide synthase in AICAR and caffeine-induced mitochondrial biogenesis in L6 myocytes J Appl Physiol 108 2010 589 595
30. K.S. Persons, V.J. Eddy, S. Chadid, R. Deoliveira, A.K. Saha, and R. Ray Anti-growth effect of 1, 25-dihydroxyvitamin D3-3-bromoacetate alone or in combination with 5-amino-imidazole-4-carboxamide-1-beta-4-ribofuranoside in pancreatic cancer cells Anticancer Res 30 2010 1875 1880
31. J. Woodard, and L.C. Platanias AMP-activated kinase (AMPK)-generated signals in malignant melanoma cell growth and survival Biochem Biophys Res Commun 398 2010 135 139
32. S.Y. Yu, D.W. Chan, V.W. Liu, and H.Y. Ngan Inhibition of cervical cancer cell growth through activation of upstream kinases of AMP-activated protein kinase Tumour Biol 30 2009 80 85
33. T.J. Guan, F.J. Qin, J.H. Du, L. Geng, Y.Y. Zhang, and M. Li AICAR inhibits proliferation and induced S-phase arrest, and promotes apoptosis in CaSki cells Acta Pharmacol Sin 28 2007 1984 1990 (Pubitemid 350198343)
34. J.H. Jung, J.O. Lee, J.H. Kim, S.K. Lee, G.Y. You, S.H. Park, J.M. Park, E.K. Kim, P.G. Suh, J.K. An, and H.S. Kim Quercetin suppresses HeLa cell viability via AMPK-induced HSP70 and EGFR down-regulation J Cell Physiol 223 2010 408 414
35. C. Garcia-Garcia, C. Fumarola, N. Navaratnam, D. Carling, and A. Lopez-Rivas AMPK-independent down-regulation of cFLIP and sensitization to TRAIL-induced apoptosis by AMPK activators Biochem Pharmacol 79 2010 853 863
36. R. Rattan, S. Giri, A.K. Singh, and I. Singh 5-Aminoimidazole-4- carboxamide-1-beta-D-ribofuranoside inhibits cancer cell proliferation in vitro and in vivo via AMP-activated protein kinase J Biol Chem 280 2005 39582 39593 (Pubitemid 41713917)
37. T.K. Sengupta, G.M. Leclerc, T.T. Hsieh-Kinser, G.J. Leclerc, I. Singh, and J.C. Barredo Cytotoxic effect of 5-aminoimidazole-4-carboxamide-1-beta-4- ribofuranoside (AICAR) on childhood acute lymphoblastic leukemia (ALL) cells: implication for targeted therapy Mol Cancer 6 2007 46
38. D. Guo, I.E. Hildebrandt, R.M. Prins, H. Soto, M.M. Mazzotta, J. Dang, J. Czernin, J.Y. Shyy, A.D. Watson, M. Phelps, C.G. Radu, T.F. Cloughesy, and P.S. Mischel The AMPK agonist AICAR inhibits the growth of EGFRvIII-expressing glioblastomas by inhibiting lipogenesis Proc Natl Acad Sci USA 106 2009 12932 12937
39. J. Zhou, W. Huang, R. Tao, S. Ibaragi, F. Lan, Y. Ido, X. Wu, Y.O. Alekseyev, M.E. Lenburg, G.F. Hu, and Z. Luo Inactivation of AMPK alters gene expression and promotes growth of prostate cancer cells Oncogene 28 2009 1993 2002
40. X. Xiang, A.K. Saha, R. Wen, N.B. Ruderman, and Z. Luo AMP-activated protein kinase activators can inhibit the growth of prostate cancer cells by multiple mechanisms Biochem Biophys Res Commun 321 2004 161 167 (Pubitemid 39055618)
41. P. Mukherjee, T.J. Mulrooney, J. Marsh, D. Blair, T.C. Chiles, and T.N. Seyfried Differential effects of energy stress on AMPK phosphorylation and apoptosis in experimental brain tumor and normal brain Mol Cancer 7 2008 37
42. P. Baumann, S. Mandl-Weber, B. Emmerich, C. Straka, and R. Schmidmaier Activation of adenosine monophosphate activated protein kinase inhibits growth of multiple myeloma cells Exp Cell Res 313 2007 3592 3603 (Pubitemid 47404540)
43. R.Y. Su, Y. Chao, T.Y. Chen, D.Y. Huang, and W.W. Lin 5-Aminoimidazole-4-carboxamide riboside sensitizes TRAIL- and TNF{alpha}-induced cytotoxicity in colon cancer cells through AMP-activated protein kinase signaling Mol Cancer Ther 6 2007 1562 1571 (Pubitemid 46954023)
44. Y.M. Kim, J.T. Hwang, D.W. Kwak, Y.K. Lee, and O.J. Park Involvement of AMPK signaling cascade in capsaicin-induced apoptosis of HT-29 colon cancer cells Ann NY Acad Sci 1095 2007 496 503
45. M. Saitoh, K. Nagai, K. Nakagawa, T. Yamamura, S. Yamamoto, and T. Nishizaki Adenosine induces apoptosis in the human gastric cancer cells via an intrinsic pathway relevant to activation of AMP-activated protein kinase Biochem Pharmacol 67 2004 2005 2011 (Pubitemid 38591388)
46. K. Sai, D. Yang, H. Yamamoto, H. Fujikawa, S. Yamamoto, T. Nagata, M. Saito, T. Yamamura, and T. Nishizaki A(1) adenosine receptor signal and AMPK involving caspase-9/-3 activation are responsible for adenosine-induced RCR-1 astrocytoma cell death Neurotoxicology 27 2006 458 467 (Pubitemid 43867776)
47. J.V. Swinnen, A. Beckers, K. Brusselmans, S. Organe, J. Segers, L. Timmermans, F. Vanderhoydonc, L. Deboel, R. Derua, E. Waelkens, E. De Schrijver, T. Van de Sande, A. Noel, F. Foufelle, and G. Verhoeven Mimicry of a cellular low energy status blocks tumor cell anabolism and suppresses the malignant phenotype Cancer Res 65 2005 2441 2448 (Pubitemid 40490156)
48. C. Rocher, J.W. Taanman, D. Pierron, B. Faustin, G. Benard, R. Rossignol, M. Malgat, L. Pedespan, and T. Letellier Influence of mitochondrial DNA level on cellular energy metabolism: implications for mitochondrial diseases J Bioenerg Biomembr 40 2008 59 67
49. E. Borenfreund, and J.A. Puerner Toxicity determined in vitro by morphological alterations and neutral red absorption Toxicol Lett 24 1985 119 124 (Pubitemid 15103513)
50. K. Nouette-Gaulain, N. Bellance, B. Prevost, E. Passerieux, C. Pertuiset, O. Galbes, K. Smolkova, F. Masson, S. Miraux, J.P. Delage, T. Letellier, R. Rossignol, X. Capdevila, and F. Sztark Erythropoietin protects against local anesthetic myotoxicity during continuous regional analgesia Anesthesiology 110 2009 648 659
51. G. Benard, N. Bellance, D. James, P. Parrone, H. Fernandez, T. Letellier, and R. Rossignol Mitochondrial bioenergetics and structural network organization J Cell Sci 120 2007 838 848 (Pubitemid 46523485)
52. R.J. Youle, and M. Karbowski Mitochondrial fission in apoptosis Nat Rev Mol Cell Biol 6 2005 657 663 (Pubitemid 41081269)
53. W.J. Ryves, and A.J. Harwood The interaction of glycogen synthase kinase-3 (GSK-3) with the cell cycle Prog Cell Cycle Res 5 2003 489 495
54. M. Monk, and C. Holding Human embryonic genes re-expressed in cancer cells Oncogene 20 2001 8085 8091 (Pubitemid 34028332)
55. D. Kukidome, T. Nishikawa, K. Sonoda, K. Imoto, K. Fujisawa, M. Yano, H. Motoshima, T. Taguchi, T. Matsumura, and E. Araki Activation of AMP-activated protein kinase reduces hyperglycemia-induced mitochondrial reactive oxygen species production and promotes mitochondrial biogenesis in human umbilical vein endothelial cells Diabetes 55 2006 120 127 (Pubitemid 43343306)
56. R.L. Elstrom, D.E. Bauer, M. Buzzai, R. Karnauskas, M.H. Harris, D.R. Plas, H. Zhuang, R.M. Cinalli, A. Alavi, C.M. Rudin, and C.B. Thompson Akt stimulates aerobic glycolysis in cancer cells Cancer Res 64 2004 3892 3899 (Pubitemid 38697301)
57. R. Dixon, J. Gourzis, D. McDermott, J. Fujitaki, P. Dewland, and H. Gruber AICA-riboside: safety, tolerance, and pharmacokinetics of a novel adenosine-regulating agent J Clin Pharmacol 31 1991 342 347
58. S. Wei, S.K. Kulp, and C.S. Chen Energy restriction as an antitumor target of thiazolidinediones J Biol Chem 285 2010 9780 9791