ROS accumulation and IGF-IR inhibition contribute to fenofibrate/PPARα -mediated inhibition of Glioma cell motility in vitro

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Drukala, Justyna ^c   Urbanska, Katarzyna ^b   Wilk, Anna ^a   Grabacka, Maja ^d   Wybieralska, Ewa ^c   Del Valle, Luis ^a   Madeja, Zbigniew ^c   Reiss, Krzysztof ^a  

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

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; FENOFIBRATE; INSULIN RECEPTOR SUBSTRATE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA AGONIST; REACTIVE OXYGEN METABOLITE; SCAVENGER; SOMATOMEDIN C RECEPTOR; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOACCUMULATION; CANCER INHIBITION; CELL FUNCTION; CELL MOTILITY; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; FETUS; GLIOMA CELL; HORMONE ACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; NUCLEOTIDE METABOLISM; SIGNAL TRANSDUCTION; BIOSYNTHESIS; BRAIN TUMOR; CELL MOTION; DRUG ANTAGONISM; GLIOMA; METABOLISM; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; BASE SEQUENCE; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FENOFIBRATE; GLIOMA; HUMANS; PPAR ALPHA; REACTIVE OXYGEN SPECIES; RECEPTOR, IGF TYPE 1; RNA, SMALL INTERFERING;

EID: 77953657756     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-159     Document Type: Article

References (68)

1. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME. Molecular targets of glioma invasion. Cell Mol Life Sci 2007, 64:458-478.
2. Terzis AJ, Niclou SP, Rajcevic U, Danzeisen C, Bjerkvig R. Cell therapies for glioblastoma. Expert Opin Biol Ther 2006, 6:739-749.
3. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005, 352:997-1003.
4. Stupp R, Weber DC. The role of radio- and chemotherapy in glioblastoma. Onkologie 2005, 28:315-317.
5. Wen PY, Yung WK, Lamborn KR, Dahia PL, Wang Y, Peng B, Abrey LE, Raizer J, Cloughesy TF, Fink K, et al. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08. Clin Cancer Res 2006, 12:4899-4907.
6. Trojan J, Cloix JF, Ardourel MY, Chatel M, Anthony DD. Insulin-like growth factor type I biology and targeting in malignant gliomas. Neuroscience 2007, 145:795-811.
7. Hau P, Jachimczak P, Schlingensiepen R, Schulmeyer F, Jauch T, Steinbrecher A, Brawanski A, Proescholdt M, Schlaier J, Buchroithner J, et al. Inhibition of TGF-beta2 with AP 12009 in recurrent malignant gliomas: from preclinical to phase I/II studies. Oligonucleotides 2007, 17:201-212.
8. Ishii N, Maier D, Merlo A, Tada M, Sawamura Y, Diserens AC, Van Meir EG. Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol 1999, 9:469-479.
9. Louis DN. Molecular pathology of malignant gliomas. Annu Rev Pathol 2006, 1:97-117.
10. Resnicoff M, Tjuvajev J, Rotman HL, Abraham D, Curtis M, Aiken R, Baserga R. Regression of C6 rat brain tumors by cells expressing an antisense insulin-like growth factor I receptor RNA. J Exp Ther Oncol 1996, 1:385-389.
11. D'Ambrosio C, Ferber A, Resnicoff M, Baserga R. A soluble insulin-like growth factor I receptor that induces apoptosis of tumor cells in vivo and inhibits tumorigenesis. Cancer Res 1996, 56:4013-4020.
12. Urbanska K, Pannizzo P, Grabacka M, Croul S, Del Valle L, Khalili K, Reiss K. Activation of PPARalpha inhibits IGF-I-mediated growth and survival responses in medulloblastoma cell lines. Int J Cancer 2008, 123:1015-1024.
13. Grabacka M, Placha W, Plonka PM, Pajak S, Urbanska K, Laidler P, Slominski A. Inhibition of melanoma metastases by fenofibrate. Arch Dermatol Res 2004, 296:54-58.
14. Grabacka M, Plonka PM, Urbanska K, Reiss K. Peroxisome proliferator-activated receptor alpha activation decreases metastatic potential of melanoma cells in vitro via down-regulation of Akt. Clin Cancer Res 2006, 12:3028-3036.
15. Panigrahy D, Kaipainen A, Huang S, Butterfield CE, Barnes CM, Fannon M, Laforme AM, Chaponis DM, Folkman J, Kieran MW. PPARalpha agonist fenofibrate suppresses tumor growth through direct and indirect angiogenesis inhibition. Proc Natl Acad Sci USA 2008, 105:985-990. 2242705, 18199835.
16. Grabacka M, Reiss K. Anticancer Properties of PPARalpha-Effects on Cellular Metabolism and Inflammation. PPAR Res 2008, 2008:930705. 2396219, 18509489.
17. Holland CM, Saidi SA, Evans AL, Sharkey AM, Latimer JA, Crawford RA, Charnock-Jones DS, Print CG, Smith SK. Transcriptome analysis of endometrial cancer identifies peroxisome proliferator-activated receptors as potential therapeutic targets. Mol Cancer Ther 2004, 3:993-1001.
18. Saidi SA, Holland CM, Charnock-Jones DS, Smith SK. In vitro and in vivo effects of the PPAR-alpha agonists fenofibrate and retinoic acid in endometrial cancer. Mol Cancer 2006, 5:13. 1475879, 16569247.
19. Thuillier P, Anchiraico GJ, Nickel KP, Maldve RE, Gimenez-Conti I, Muga SJ, Liu KL, Fischer SM, Belury MA. Activators of peroxisome proliferator-activated receptor-alpha partially inhibit mouse skin tumor promotion. Mol Carcinog 2000, 29:134-142.
20. Issemann I, Green S. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature 1990, 347:645-650.
21. Ahmed W, Ziouzenkova O, Brown J, Devchand P, Francis S, Kadakia M, Kanda T, Orasanu G, Sharlach M, Zandbergen F, Plutzky J. PPARs and their metabolic modulation: new mechanisms for transcriptional regulation?. J Intern Med 2007, 262:184-198.
22. Staels B, Van Tol A, Fruchart JC, Auwerx J. Effects of hypolipidemic drugs on the expression of genes involved in high density lipoprotein metabolism in the rat. Isr J Med Sci 1996, 32:490-498.
23. Steiner G. Fenofibrate for cardiovascular disease prevention in metabolic syndrome and type 2 diabetes mellitus. Am J Cardiol 2008, 102:28L-33L.
24. Jiao HL, Ye P, Zhao BL. Protective effects of green tea polyphenols on human HepG2 cells against oxidative damage of fenofibrate. Free Radic Biol Med 2003, 35:1121-1128.
25. Nishimura J, Dewa Y, Muguruma M, Kuroiwa Y, Yasuno H, Shima T, Jin M, Takahashi M, Umemura T, Mitsumori K. Effect of fenofibrate on oxidative DNA damage and on gene expression related to cell proliferation and apoptosis in rats. Toxicol Sci 2007, 97:44-54.
26. Pollak MN, Schernhammer ES, Hankinson SE. Insulin-like growth factors and neoplasia. Nat Rev Cancer 2004, 4:505-518.
27. Reiss K, Valentinis B, Tu X, Xu SQ, Baserga R. Molecular markers of IGF-I-mediated mitogenesis. Exp Cell Res 1998, 242:361-372.
28. Korohoda W, Golda J, Sroka J, Wojnarowicz A, Jochym P, Madeja Z. Chemotaxis of Amoeba proteus in the developing pH gradient within a pocket-like chamber studied with the computer assisted method. Cell Motil Cytoskeleton 1997, 38:38-53.
29. Czyz J, Madeja Z, Irmer U, Korohoda W, Hulser DF. Flavonoid apigenin inhibits motility and invasiveness of carcinoma cells in vitro. Int J Cancer 2005, 114:12-18.
30. Sroka J, Antosik A, Czyz J, Nalvarte I, Olsson JM, Spyrou G, Madeja Z. Overexpression of thioredoxin reductase 1 inhibits migration of HEK-293 cells. Biol Cell 2007, 99:677-687.
31. Vu-Dac N, Schoonjans K, Kosykh V, Dallongeville J, Fruchart JC, Staels B, Auwerx J. Fibrates increase human apolipoprotein A-II expression through activation of the peroxisome proliferator-activated receptor. J Clin Invest 1995, 96:741-750. 185258, 7635967.
32. Yang S, Chintapalli J, Sodagum L, Baskin S, Malhotra A, Reiss K, Meggs LG. Activated IGF-1R inhibits hyperglycemia-induced DNA damage and promotes DNA repair by homologous recombination. Am J Physiol Renal Physiol 2005, 289:F1144-1152.
33. Cossarizza A, Salvioli S. Flow cytometric analysis of mitochondrial membrane potential using JC-1. Curr Protoc Cytom 2001, Chapter 9:Unit 9 14.
34. Goto M, Holgersson J, Kumagai-Braesch M, Korsgren O. The ADP/ATP ratio: A novel predictive assay for quality assessment of isolated pancreatic islets. Am J Transplant 2006, 6:2483-2487.
35. Guvakova MA. Insulin-like growth factors control cell migration in health and disease. Int J Biochem Cell Biol 2007, 39:890-909.
36. Urbanska K, Trojanek J, Del Valle L, Eldeen MB, Hofmann F, Garcia-Echeverria C, Khalili K, Reiss K. Inhibition of IGF-I receptor in anchorage-independence attenuates GSK-3beta constitutive phosphorylation and compromises growth and survival of medulloblastoma cell lines. Oncogene 2007, 26:2308-2317.
37. Scatena R, Bottoni P, Giardina B. Mitochondria, PPARs, and Cancer: Is Receptor-Independent Action of PPAR Agonists a Key?. PPAR Res 2008, 2008:256251. 2464819, 18645611.
38. Warburg O. On respiratory impairment in cancer cells. Science 1956, 124:269-270.
39. Li N, Brun T, Cnop M, Cunha DA, Eizirik DL, Maechler P. Transient oxidative stress damages mitochondrial machinery inducing persistent beta-cell dysfunction. J Biol Chem 2009, 28(284(35)):23602-12.
40. Monsalve M, Borniquel S, Valle I, Lamas S. Mitochondrial dysfunction in human pathologies. Front Biosci 2007, 12:1131-1153.
41. Husain M, Meggs LG, Vashistha H, Simoes S, Griffiths KO, Kumar D, Mikulak J, Mathieson PW, Saleem MA, Del Valle L, et al. Inhibition of p66ShcA longevity gene rescues podocytes from HIV-1-induced oxidative stress and apoptosis. J Biol Chem 2009, 284:16648-16658. 2713565, 19383602.
42. Garcia-Echeverria C, Pearson MA, Marti A, Meyer T, Mestan J, Zimmermann J, Gao J, Brueggen J, Capraro HG, Cozens R, et al. In vivo antitumor activity of NVP-AEW541-A novel, potent, and selective inhibitor of the IGF-IR kinase. Cancer Cell 2004, 5:231-239.
43. Hewish M, Chau I, Cunningham D. Insulin-like growth factor 1 receptor targeted therapeutics: novel compounds and novel treatment strategies for cancer medicine. Recent Pat Anticancer Drug Discov 2009, 4:54-72.
44. Andrews DW, Resnicoff M, Flanders AE, Kenyon L, Curtis M, Merli G, Baserga R, Iliakis G, Aiken RD. Results of a pilot study involving the use of an antisense oligodeoxynucleotide directed against the insulin-like growth factor type I receptor in malignant astrocytomas. J Clin Oncol 2001, 19:2189-2200.
45. Schlingensiepen KH, Fischer-Blass B, Schmaus S, Ludwig S. Antisense therapeutics for tumor treatment: the TGF-beta2 inhibitor AP 12009 in clinical development against malignant tumors. Recent Results Cancer Res 2008, 177:137-150.
46. Baserga R, Hongo A, Rubini M, Prisco M, Valentinis B. The IGF-I receptor in cell growth, transformation and apoptosis. Biochim Biophys Acta 1997, 1332:F105-126.
47. Resnicoff M, Abraham D, Yutanawiboonchai W, Rotman HL, Kajstura J, Rubin R, Zoltick P, Baserga R. The insulin-like growth factor I receptor protects tumor cells from apoptosis in vivo. Cancer Res 1995, 55:2463-2469.
48. Valentinis B, Morrione A, Peruzzi F, Prisco M, Reiss K, Baserga R. Anti-apoptotic signaling of the IGF-I receptor in fibroblasts following loss of matrix adhesion. Oncogene 1999, 18:1827-1836.
49. Wang JY, Del Valle L, Gordon J, Rubini M, Romano G, Croul S, Peruzzi F, Khalili K, Reiss K. Activation of the IGF-IR system contributes to malignant growth of human and mouse medulloblastomas. Oncogene 2001, 20:3857-3868.
50. Valentinis B, Reiss K, Baserga R. Insulin-like growth factor-I-mediated survival from anoikis: role of cell aggregation and focal adhesion kinase. J Cell Physiol 1998, 176:648-657.
51. Perer ES, Madan AK, Shurin A, Zakris E, Romeguera K, Pang Y, Beech DJ. Insulin-like growth factor I receptor antagonism augments response to chemoradiation therapy in colon cancer cells. J Surg Res 2000, 94:1-5.
52. Turner BC, Haffty BG, Narayanan L, Yuan J, Havre PA, Gumbs AA, Kaplan L, Burgaud JL, Carter D, Baserga R, Glazer PM. Insulin-like growth factor-I receptor overexpression mediates cellular radioresistance and local breast cancer recurrence after lumpectomy and radiation. Cancer Res 1997, 57:3079-3083.
53. Zandi E, Chen Y, Karin M. Direct phosphorylation of IkappaB by IKKalpha and IKKbeta: discrimination between free and NF-kappaB-bound substrate. Science 1998, 281:1360-1363.
54. Gamerdinger M, Clement AB, Behl C. Cholesterol-like effects of selective COX inhibitors and fibrates on cellular membranes and amyloid-{beta} production. Mol Pharmacol 2007,
55. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
56. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gelinas C, Fan Y, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64. 2857533, 16843265.
57. Shaw RJ. Glucose metabolism and cancer. Curr Opin Cell Biol 2006, 18:598-608.
58. Matoba S, Kang JG, Patino W, Wragg A, Boehm M, Gavrilova O, Hurley P, Bunz F, Hwang PM. p53 regulates mitochondrial respiration. Science 2006, 312:1650-1653.
59. Finck BN, Kelly DP. 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 2002, 34:1249-1257.
60. Randle PJ. Regulatory interactions between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab Rev 1998, 14:263-283.
61. Wolfe RR. Metabolic interactions between glucose and fatty acids in humans. Am J Clin Nutr 1998, 67:519S-526S.
62. Beckner ME, Gobbel GT, Abounader R, Burovic F, Agostino NR, Laterra J, Pollack IF. Glycolytic glioma cells with active glycogen synthase are sensitive to PTEN and inhibitors of PI3K and gluconeogenesis. Lab Invest 2005, 85:1457-1470.
63. Scatena R, Bottoni P, Vincenzoni F, Messana I, Martorana GE, Nocca G, De Sole P, Maggiano N, Castagnola M, Giardina B. Bezafibrate induces a mitochondrial derangement in human cell lines: a PPAR-independent mechanism for a peroxisome proliferator. Chem Res Toxicol 2003, 16:1440-1447.
64. Jiao HL, Zhao BL. Cytotoxic effect of peroxisome proliferator fenofibrate on human HepG2 hepatoma cell line and relevant mechanisms. Toxicol Appl Pharmacol 2002, 185:172-179.
65. Raha S, Myint AT, Johnstone L, Robinson BH. Control of oxygen free radical formation from mitochondrial complex I: roles for protein kinase A and pyruvate dehydrogenase kinase. Free Radic Biol Med 2002, 32:421-430.
66. Nakatani T, Tsuboyama-Kasaoka N, Takahashi M, Miura S, Ezaki O. Mechanism for peroxisome proliferator-activated receptor-alpha activator-induced up-regulation of UCP2 mRNA in rodent hepatocytes. J Biol Chem 2002, 277:9562-9569.
67. Pecqueur C, Bui T, Gelly C, Hauchard J, Barbot C, Bouillaud F, Ricquier D, Miroux B, Thompson CB. Uncoupling protein-2 controls proliferation by promoting fatty acid oxidation and limiting glycolysis-derived pyruvate utilization. Faseb J 2008, 22:9-18.
68. Friedl P, Noble PB, Zanker KS. Lymphocyte locomotion in three-dimensional collagen gels. Comparison of three quantitative methods for analysing cell trajectories. J Immunol Methods 1993, 165:157-165.