Molecular mechanisms of fenofibrate-induced metabolic catastrophe and glioblastoma cell death

Molecular and Cellular Biology

Volumn 35, Issue 1, 2015, Pages 182-198

  Wilk, Anna ^a,b   Wyczechowska, Dorota ^a,b   Zapata, Adriana ^a,b   Dean, Matthew ^a,b   Mullinax, Jennifer ^c   Marrero, Luis ^b   Parsons, Christopher ^b   Peruzzi, Francesca ^a,b   Culicchia, Frank ^b   Ocho, Augusto ^b   Grabacka, Maja ^d   Reiss, Krzysztof ^a,b  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Louisville School of Medicine   (United States)

^d UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE MONOPHOSPHATE DEAMINASE; ADENOSINE TRIPHOSPHATE; FENOFIBRATE; MAMMALIAN TARGET OF RAPAMYCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ANTINEOPLASTIC AGENT; OXYGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DEATH; CYTOTOXICITY; FATTY ACID OXIDATION; FEMALE; GLIOBLASTOMA; GLYCOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; RESPIRATORY CHAIN; ANIMAL; ASTROCYTE; BRAIN NEOPLASMS; CANCER TRANSPLANTATION; CYTOLOGY; ELECTRON TRANSPORT; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NUDE MOUSE; OXYGEN CONSUMPTION; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

MAMMALIA;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTINEOPLASTIC AGENTS; ASTROCYTES; BRAIN NEOPLASMS; CELL DEATH; CELL LINE, TUMOR; ELECTRON TRANSPORT; FEMALE; FENOFIBRATE; GLIOBLASTOMA; GLYCOLYSIS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, NUDE; MITOCHONDRIA; NEOPLASM TRANSPLANTATION; OXYGEN; OXYGEN CONSUMPTION; PPAR ALPHA; SIGNAL TRANSDUCTION;

EID: 84920046789     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00562-14     Document Type: Article

References (61)

1. Cemeus C, Zhao TT, Barrett GM, Lorimer IA, Dimitroulakos J. 2008. Lovastatin enhances gefitinib activity in glioblastoma cells irrespective of EGFRvIII and PTEN status. J Neurooncol 90:9-17. http://dx.doi.org/10.1007/s11060-008-9627-0.
2. Egerod FL, Nielsen HS, Iversen L, Thorup I, Storgaard T, Oleksiewicz MB. 2005. Biomarkers for early effects of carcinogenic dual-acting PPAR agonists in rat urinary bladder urothelium in vivo. Biomarkers 10:295-309. http://dx.doi.org/10.1080/13547500500218682.
3. Grabacka M, Placha W, Plonka PM, Pajak S, Urbanska K, Laidler P, Slominski A. 2004. Inhibition of melanoma metastases by fenofibrate. Arch Dermatol Res 296:54-58. http://dx.doi.org/10.1007/s00403-004-0479-y.
4. Grabacka M, Reiss K. 2008. Anticancer properties of PPARalpha- effects on cellular metabolism and inflammation. PPAR Res 2008:930705. http://dx.doi.org/10.1155/2008/930705.
5. Panigrahy D, Kaipainen A, Huang S, Butterfield CE, Barnes CM, Fannon M, Laforme AM, Chaponis DM, Folkman J, Kieran MW. 2008. PPARalpha agonist fenofibrate suppresses tumor growth through direct and indirect angiogenesis inhibition. Proc Natl Acad Sci U S A 105:985-990. http://dx.doi.org/10.1073/pnas.0711281105.
6. Saidi SA, Holland CM, Charnock-Jones DS, Smith SK. 2006. In vitro and in vivo effects of the PPAR-alpha agonists fenofibrate and retinoic acid in endometrial cancer. Mol Cancer 5:13. http://dx.doi.org/10.1186/1476-4598-5-13.
7. Yanae M, Tsubaki M, Satou T, Itoh T, Imano M, Yamazoe Y, Nishida S. 2011. Statin-induced apoptosis via the suppression of ERK1/2 and Akt activation by inhibition of the geranylgeranyl-pyrophosphate biosynthesis in glioblastoma. J Exp Clin Cancer Res 30:74. http://dx.doi.org/10.1186/1756-9966-30-74.
8. Gardette V, Bongard V, Dallongeville J, Arveiler D, Bingham A, Ruidavets JB, Amouyel P, Haas B, Ducimetiere P, Ferrieres J. 2009. Ten-year all-cause mortality in presumably healthy subjects on lipidlowering drugs (from the Prospective Epidemiological Study of Myocardial Infarction [PRIME] prospective cohort). Am J Cardiol 103:381-386. http://dx.doi.org/10.1016/j.amjcard.2008.09.092.
9. Shigeto T, Yokoyama Y, Xin B, Mizunuma H. 2007. Peroxisome proliferator- activated receptor alpha and gamma ligands inhibit the growth of human ovarian cancer. Oncol Rep 18:833-840. http://dx.doi.org/10.3892/or.18.4.833.
10. Yokoyama Y, Xin B, Shigeto T, Mizunuma H. 2011. Combination of ciglitazone, a peroxisome proliferator-activated receptor gamma ligand, and cisplatin enhances the inhibition of growth of human ovarian cancers. J Cancer Res Clin Oncol 137:1219-1228. http://dx.doi.org/10.1007/s00432-011-0993-1.
11. Strakova N, Ehrmann J, Bartos J, Malikova J, Dolezel J, Kolar Z. 2005. Peroxisome proliferator-activated receptors (PPAR) agonists affect cell viability, apoptosis and expression of cell cycle related proteins in cell lines of glial brain tumors. Neoplasma 52:126-136.
12. Grabacka M, Plonka PM, Urbanska K, Reiss K. 2006. Peroxisome proliferator- activated receptor alpha activation decreases metastatic potential of melanoma cells in vitro via down-regulation of Akt. Clin Cancer Res 12: 3028-3036. http://dx.doi.org/10.1158/1078-0432.CCR-05-2556.
13. Drukala J, Urbanska K, Wilk A, Grabacka M, Wybieralska E, Del Valle L, Madeja Z, Reiss K. 2010. ROS accumulation and IGF-IR inhibition contribute to fenofibrate/PPARalpha-mediated inhibition of glioma cell motility in vitro. Mol Cancer 9:159. http://dx.doi.org/10.1186/1476-4598-9-159.
14. Urbanska K, Pannizzo P, Grabacka M, Croul S, Del Valle L, Khalili K, Reiss K. 2008. Activation of PPARalpha inhibits IGF-I-mediated growth and survival responses in medulloblastoma cell lines. Int J Cancer 123: 1015-1024. http://dx.doi.org/10.1002/ijc.23588.
15. Wilk A, Urbanska K, Grabacka M, Mullinax J, Marcinkiewicz C, Impastato D, Estrada JJ, Reiss K. 2012. Fenofibrate-induced nuclear translocation of FoxO3A triggers Bim-mediated apoptosis in glioblastoma cells in vitro. Cell Cycle 11:2660-2671. http://dx.doi.org/10.4161/cc.21015.
16. Sterba J, Valik D, Mudry P, Kepak T, Pavelka Z, Bajciova V, Zitterbart K, Kadlecova V, Mazanek P. 2006. Combined biodifferentiating and antiangiogenic oral metronomic therapy is feasible and effective in relapsed solid tumors in children: single-center pilot study. Onkologie 29: 308-313. http://dx.doi.org/10.1159/000093474.
17. Zapletalova D, Andre N, Deak L, Kyr M, Bajciova V, Mudry P, Dubska L, Demlova R, Pavelka Z, Zitterbart K, Skotakova J, Husek K, Martincekova A, Mazanek P, Kepak T, Doubek M, Kutnikova L, Valik D, Sterba J. 2012. Metronomic chemotherapy with the COMBAT regimen in advanced pediatric malignancies: a multicenter experience. Oncology 82: 249-260. http://dx.doi.org/10.1159/000336483.
18. Grabacka M, Pierzchalska M, Reiss K. 2013. Peroxisome proliferator activated receptor α ligands as anticancer drugs targeting mitochondrial metabolism. Curr Pharm Biotechnol 14:342-356. http://dx.doi.org/10.2174/1389201011314030009.
19. Ahmed W, Ziouzenkova O, Brown J, Devchand P, Francis S, Kadakia M, Kanda T, Orasanu G, Sharlach M, Zandbergen F, Plutzky J. 2007. PPARs and their metabolic modulation: new mechanisms for transcriptional regulation? J Intern Med 262:184-198. http://dx.doi.org/10.1111/j.1365-2796.2007.01825.x.
20. Araki H, Tamada Y, Imoto S, Dunmore B, Sanders D, Humphrey S, Nagasaki M, Doi A, Nakanishi Y, Yasuda K, Tomiyasu Y, Tashiro K, Print C, Charnock-Jones DS, Kuhara S, Miyano S. 2009. Analysis of PPARalpha-dependent and PPARalpha-independent transcript regulation following fenofibrate treatment of human endothelial cells. Angiogenesis 12:221-229. http://dx.doi.org/10.1007/s10456-009-9142-8.
21. Finck BN, Kelly DP. 2002. Peroxisome proliferator-activated receptor alpha (PPARalpha) signaling in the gene regulatory control of energy metabolism in the normal and diseased heart. J Mol Cell Cardiol 34:1249-1257. http://dx.doi.org/10.1006/jmcc.2002.2061.
22. Randle PJ. 1998. Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab Rev 14:263-283. http://dx.doi.org/10.1002/(SICI)1099-0895(199812)14:4<263::AID-DMR233>3.0.CO;2-C.
23. Wolfe RR. 1998. Metabolic interactions between glucose and fatty acids in humans. Am J Clin Nutr 67:519S-526S.
24. Beckner ME, Gobbel GT, Abounader R, Burovic F, Agostino NR, Laterra J, Pollack IF. 2005. Glycolytic glioma cells with active glycogen synthase are sensitive to PTEN and inhibitors of PI3K and gluconeogenesis. Lab Invest 85:1457-1470. http://dx.doi.org/10.1038/labinvest.3700355.
25. Jelluma N, Yang X, Stokoe D, Evan GI, Dansen TB, Haas-Kogan DA. 2006. Glucose withdrawal induces oxidative stress followed by apoptosis in glioblastoma cells but not in normal human astrocytes. Mol Cancer Res 4:319-330. http://dx.doi.org/10.1158/1541-7786.MCR-05-0061.
26. Marie SK, Shinjo SM. 2011. Metabolism and brain cancer. Clinics (Sao Paulo) 66(Suppl 1):S33-S43. http://dx.doi.org/10.1590/S1807-59322011001300005.
27. Warburg O. 1956. On the origin of cancer cells. Science 123:309-314. http://dx.doi.org/10.1126/science.123.3191.309.
28. Warburg O. 1956. On respiratory impairment in cancer cells. Science 124:269-270.
29. Dell' Antone P. 2012. Energy metabolism in cancer cells: how to explain the Warburg and Crabtree effects? Med Hypotheses 79:388-392. http://dx.doi.org/10.1016/j.mehy.2012.06.002.
30. Gamerdinger M, Clement AB, Behl C. 2007. Cholesterol-like effects of selectiveCOXinhibitors and fibrates on cellular membranes and amyloidbeta production. Mol Pharmacol 72:141-151. http://dx.doi.org/10.1124/mol.107.034009.
31. Nadanaciva S, Dykens JA, Bernal A, Capaldi RA, Will Y. 2007. Mitochondrial impairment by PPAR agonists and statins identified via immunocaptured OXPHOS complex activities and respiration. Toxicol Appl Pharmacol 223:277-287. http://dx.doi.org/10.1016/j.taap.2007.06.003.
32. Zungu M, Felix R, Essop MF. 2006. Wy-14,643 and fenofibrate inhibit mitochondrial respiration in isolated rat cardiac mitochondria. Mitochondrion 6:315-322. http://dx.doi.org/10.1016/j.mito.2006.09.001.
33. Valentinis B, Reiss K, Baserga R. 1998. Insulin-like growth factor-Imediated survival from anoikis: role of cell aggregation and focal adhesion kinase. J Cell Physiol 176:648-657.
34. Gualco E, Urbanska K, Perez-Liz G, Sweet T, Peruzzi F, Reiss K, Del Valle L. 2010. IGF-IR-dependent expression of survivin is required for T-antigen-mediated protection from apoptosis and proliferation of neural progenitors. Cell Death Differ 17:439-451. http://dx.doi.org/10.1038/cdd.2009.146.
35. Vu-Dac N, Schoonjans K, Kosykh V, Dallongeville J, Fruchart JC, Staels B, Auwerx J. 1995. Fibrates increase human apolipoprotein A-II expression through activation of the peroxisome proliferator-activated receptor. J Clin Invest 96:741-750. http://dx.doi.org/10.1172/JCI118118.
36. Troiano L, Ferraresi R, Lugli E, Nemes E, Roat E, Nasi M, Pinti M, Cossarizza A. 2007. Multiparametric analysis of cells with different mitochondrial membrane potential during apoptosis by polychromatic flow cytometry. Nat Protoc 2:2719-2727. http://dx.doi.org/10.1038/nprot.2007.405.
37. Wybieralska E, Szpak K, Gorecki A, Bonarek P, Miekus K, Drukala J, Majka M, Reiss K, Madeja Z, Czyz J. 2011. Fenofibrate attenuates contact-stimulated cell motility and gap junctional coupling in DU-145 human prostate cancer cell populations. Oncol Rep 26:447-453. http://dx.doi.org/10.3892/or.2011.1321.
38. Whitaker-Menezes D, Martinez-Outschoorn UE, Flomenberg N, Birbe RC, Witkiewicz AK, Howell A, Pavlides S, Tsirigos A, Ertel A, Pestell RG, Broda P, Minetti C, Lisanti MP, Sotgia F. 2011. Hyperactivation of oxidative mitochondrial metabolism in epithelial cancer cells in situ: visualizing the therapeutic effects of metformin in tumor tissue. Cell Cycle 10:4047-4064. http://dx.doi.org/10.4161/cc.10.23.18151.
39. Martin-Castillo B, Vazquez-Martin A, Oliveras-Ferraros C, Menendez JA. 2010. Metformin and cancer: doses, mechanisms and the dandelion and hormetic phenomena. Cell Cycle 9:1057-1064. http://dx.doi.org/10.4161/cc.9.6.10994.
40. El-Sisi A, Hegazy S, El-Khateeb E. 2013. Effects of three different fibrates on intrahepatic cholestasis experimentally induced in rats. PPAR Res 2013:781348. http://dx.doi.org/10.1155/2013/781348.
41. Kawamata H, Tachibana M, Fujimori T, Imai Y. 2006. Differentiationinducing therapy for solid tumors. Curr Pharm Des 12:379-385. http://dx.doi.org/10.2174/138161206775201947.
42. Kruczynski A, Pasteels J, Rombaut K, Salmon I, Camby I, Limouzy A, Delsol G, Brotchi J, Kiss R. 1995. The characterization of nuclear-DNA content, the proliferative activity and the immunohistochemical expression of gfap, vim, leu-7, s-100, p53 and cathepsin-d in human glioblastoma multiformes (hgbms) versus human gbm cell-lines grafted into the brains of nude-mice. Int J Oncol 6:473-481.
43. Qu J, Rizak JD, Fan Y, Guo X, Li J, Huma T, Ma Y. 2014. Establishment and partial characterization of a human tumor cell line, GBM-HSF, from a glioblastoma multiforme. Hum Cell 27:129-136. http://dx.doi.org/10.1007/s13577-013-0086-3.
44. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME. 2007. Molecular targets of glioma invasion. Cell Mol Life Sci 64:458-478. http://dx.doi.org/10.1007/s00018-007-6342-5.
45. Terzis AJ, Niclou SP, Rajcevic U, Danzeisen C, Bjerkvig R. 2006. Cell therapies for glioblastoma. Expert Opin Biol Ther 6:739-749. http://dx.doi.org/10.1517/14712598.6.8.739.
46. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, MirimanoffRO, Cairncross JG, Janzer RC, Stupp R. 2005. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997-1003. http://dx.doi.org/10.1056/NEJMoa043331.
47. Stupp R, Weber DC. 2005. The role of radio- and chemotherapy in glioblastoma. Onkologie 28:315-317. http://dx.doi.org/10.1159/000085575.
48. Wen PY, Yung WK, Lamborn KR, Dahia PL, Wang Y, Peng B, Abrey LE, Raizer J, Cloughesy TF, Fink K, Gilbert M, Chang S, Junck L, SchiffD, Lieberman F, Fine HA, Mehta M, Robins HI, DeAngelis LM, Groves MD, Puduvalli VK, Levin V, Conrad C, Maher EA, Aldape K, Hayes M, Letvak L, Egorin MJ, Capdeville R, Kaplan R, Murgo AJ, Stiles C, Prados MD. 2006. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08. Clin Cancer Res 12:4899-4907. http://dx.doi.org/10.1158/1078-0432.CCR-06-0773.
49. Saurav A, Kaushik M, Mohiuddin SM. 2012. Fenofibric acid for hyperlipidemia. Expert Opin Pharmacother 13:717-722. http://dx.doi.org/10.1517/14656566.2012.658774.
50. Carew JS, Nawrocki ST, Cleveland JL. 2007. Modulating autophagy for therapeutic benefit. Autophagy 3:464-467. http://dx.doi.org/10.4161/auto.4311.
51. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gelinas C, Fan Y, Nelson DA, Jin S, White E. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10:51-64. http://dx.doi.org/10.1016/j.ccr.2006.06.001.
52. Kondo Y, Kanzawa T, Sawaya R, Kondo S. 2005. The role of autophagy in cancer development and response to therapy. Nat Rev 5:726-734. http://dx.doi.org/10.1038/nrc1692.
53. Shimizu S, Takehara T, Hikita H, Kodama T, Tsunematsu H, Miyagi T, Hosui A, Ishida H, Tatsumi T, Kanto T, Hiramatsu N, Fujita N, Yoshimori T, Hayashi N. 2011. Inhibition of autophagy potentiates the antitumor effect of the multikinase inhibitor sorafenib in hepatocellular carcinoma. Int J Cancer 131:548-557. http://dx.doi.org/10.1002/ijc.26374.
54. Bahar FG, Ohura K, Ogihara T, Imai T. 2012. Species difference of esterase expression and hydrolase activity in plasma. J Pharm Sci 101: 3979-3988. http://dx.doi.org/10.1002/jps.23258.
55. Najib J. 2002. Fenofibrate in the treatment of dyslipidemia: a review of the data as they relate to the new suprabioavailable tablet formulation. Clin Ther 24:2022-2050. http://dx.doi.org/10.1016/S0149-2918(02)80095-9.
56. Guichard S, Terret C, Hennebelle I, Lochon I, Chevreau P, Fretigny E, Selves J, Chatelut E, Bugat R, Canal P. 1999. CPT-11 converting carboxylesterase and topoisomerase activities in tumour and normal colon and liver tissues. Br J Cancer 80:364-370. http://dx.doi.org/10.1038/sj.bjc.6690364.
57. Redinbo MR, Potter PM. 2005. Mammalian carboxylesterases: from drug targets to protein therapeutics. Drug Discov Today 10:313-325. http://dx.doi.org/10.1016/S1359-6446(05)03383-0.
58. Na K, Lee EY, Lee HJ, Kim KY, Lee H, Jeong SK, Jeong AS, Cho SY, Kim SA, Song SY, Kim KS, Cho SW, Kim H, Paik YK. 2009. Human plasma carboxylesterase 1, a novel serologic biomarker candidate for hepatocellular carcinoma. Proteomics 9:3989-3999. http://dx.doi.org/10.1002/pmic.200900105.
59. Tang X, Wu H, Wu Z, Wang G, Wang Z, Zhu D. 2008. Carboxylesterase 2 is downregulated in colorectal cancer following progression of the disease. Cancer Invest 26:178-181. http://dx.doi.org/10.1080/07357900701560786.
60. Frezza C, Cipolat S, Scorrano L. 2007. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc 2:287-295. http://dx.doi.org/10.1038/nprot.2006.478.
61. Pacifici M, Delbue S, Ferrante P, Jeansonne D, Kadri F, Nelson S, Velasco-Gonzalez C, Zabaleta J, Peruzzi F. 2013. Cerebrospinal fluid miRNA profile in HIV-encephalitis. J Cell Physiol 228:1070-1075. http://dx.doi.org/10.1002/jcp.24254.