Inhibition of in vivo glioma growth and invasion by peroxisome proliferator-activated receptor γ agonist treatment

Molecular Pharmacology

Volumn 70, Issue 5, 2006, Pages 1524-1533

  Grommes, Christian ^a   Landreth, Gary E ^a   Sastre, Magdalena ^c   Beck, Martina ^c   Feinstein, Douglas L ^e   Jacobs, Andreas H ^f   Schlegel, Uwe ^d   Heneka, Michael T ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c UNIVERSITY HOSPITAL BONN   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^f UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; KI 67 ANTIGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA AGONIST; PIOGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; GLIOMA; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADMINISTRATION, ORAL; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BRAIN NEOPLASMS; BROMODEOXYURIDINE; CASPASE 3; CELL PROLIFERATION; CELL SURVIVAL; DNA, NEOPLASM; GLIOMA; HUMANS; KI-67 ANTIGEN; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; NEOPLASM INVASIVENESS; NEOPLASMS, EXPERIMENTAL; PPAR GAMMA; RATS; RATS, SPRAGUE-DAWLEY; THIAZOLIDINEDIONES; TREATMENT OUTCOME; TUMOR BURDEN;

EID: 33751159640     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.106.022194     Document Type: Article

References (46)

1. Berge K, Tronstad KJ, Flindt EN, Rasmussen TH, Madsen L, Kristiansen K, and Berge RK (2001) Tetradecylthioacetic acid inhibits growth of rat glioma cells ex vivo and in vivo via PPAR-dependent and PPAR-independent pathways. Carcinogenesis 22:1747-1755.
2. Brockman JA, Gupta RA, and Dubois RN (1998) Activation of PPARgamma leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology 115:1049-1055.
3. Brown DC and Gatter KC (2002) Ki67 protein: the immaculate deception? Histopathology 40:2-11.
4. Chang TH and Szabo E (2000) Induction of differentiation and apoptosis by ligands of peroxisome proliferator-activated receptor gamma in non-small cell lung cancer. Cancer Res 60:1129-1138.
5. Chattopadhyay N, Singh DP, Heese O, Godbole MM, Sinohara T, Black PM, and Brown EM (2000) Expression of peroxisome proliferator-activated receptors (PPARS) in human astrocytic cells: PPARgamma as inducers of apoptosis. J Neurosci Res 61:67-74.
6. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, and Evans RM (2001) PPARgamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat Med 7:48-52.
7. Choe G, Park JK, Jouben-Steele L, Kremen TJ, Liau LM, Vinters HV, Cloughesy TF, and Mischel PS (2002) Active matrix metalloproteinase 9 expression is associated with primary glioblastoma subtype. Clin Cancer Res 8:2894-2901.
8. Cullingford TE, Bhakoo K, Peuchen S, Dolphin CT, Patel R, and Clark JB (1998) Distribution of mRNAs encoding the peroxisome proliferator-activated receptor alpha, beta and gamma and the retinoid X receptor alpha, beta and gamma in rat central nervous system. J Neurochem 70:1366-1375.
9. Davies SJ, Fitch MT, Memberg SP, Hall AK, Raisman G, and Silver J (1997) Regeneration of adult axons in white matter tracts of the central nervous system. Nature (Lond) 390:680-683.
10. Elstner E, Muller C, Koshizuka K, Williamson EA, Park D, Asou H, Shintaku P, Said JW, Heber D, and Koeffler HP (1998) Ligands for peroxisome proliferator-activated receptorgamma and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc Natl Acad Sci USA 95:8806-8811.
11. Fajas L, Egler V, Reiter R, Miard S, Lefebvre AM, and Auwerx J (2003) PPARgamma controls cell proliferation and apoptosis in an RB-dependent manner. Oncogene 22:4186-4193.
12. Forsyth PA, Wong H, Laing TD, Rewcastle NB, Morris DG, Muzik H, Leco KJ, Johnston RN, Brasher PM, Sutherland G, et al. (1999) Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas. Br J Cancer 79:1828-1835.
13. Grommes C, Landreth GE, and Heneka MT (2004) Antineoplastic effects of peroxisome proliferator-activated receptor gamma agonists. Lancet Oncol 5:419-429.
14. Grommes C, Landreth GE, Schlegel U, and Heneka MT (2005) The nonthiazolidinedione tyrosine-based peroxisome proliferator-activated receptor γ ligand GW7845 induces apoptosis and limits migration and invasion of rat and human glioma cells. J Pharmacol Exp Ther 313:806-813.
15. Guan YF, Zhang YH, Breyer RM, Davis L, and Breyer MD (1999) Expression of peroxisome proliferator-activated receptor gamma (PPARgamma) in human transitional bladder cancer and its role in inducing cell death. Neoplasia 1:330-339.
16. Herndon ME and Lander AD (1990) A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron 4:949-961.
17. Kato M, Nagaya T, Fujieda M, Saito K, Yoshida J, and Seo H (2002) Expression of PPARgamma and its ligand-dependent growth inhibition in human brain tumor cell lines. Jpn J Cancer Res 93:660-666.
18. Kim YS, Han CY, Kim SW, Kim JH, Lee SK, Jung DJ, Park SY, Kang H, Choi HS, Lee JW, et al. (2001) The orphan nuclear receptor small heterodimer partner as a novel coregulator of nuclear factor-κb in oxidized low density lipoprotein-treated macrophage cell line RAW 264.7. J Biol Chem 276:33736-33740.
19. Kleihues P, Louis DN, Scheithauer BW, Rorke LB, Reifenberger G, Burger PC, and Cavenee WK (2002) The WHO classification of tumors of the nervous system. J Neuropathol Exp Neurol 61:215-225; discussion 226-9.
20. König JFR and Klippel RA (1963) The Rat Brain: A Stereotaxic Atlas of the Forebrain and Lower Parts of the Brainstem. Williams and Wilkins, Baltimore, MD.
21. Krajewski S, Kiwit JC, and Wechsler W (1986) RG2 glioma growth in rat cerebellum after subdural implantation. J Neurosurg 65:222-229.
22. Kubota T, Koshizuka K, Williamson EA, Asou H, Said JW, Holden S, Miyoshi I, and Koeffler HP (1998) Ligand for peroxisome proliferator-activated receptor gamma (troglitazone) has potent antitumor effect against human prostate cancer both in vitro and in vivo. Cancer Res 58:3344-3352.
23. Lakka SS, Rajan M, Gondi C, Yanamandra N, Chandrasekar N, Jasti SL, Adachi Y, Siddique K, Gujrati M, Olivero W, et al. (2002) Adenovirus-mediated expression of antisense MMP-9 in glioma cells inhibits tumor growth and invasion. Oncogene 21:8011-8019.
24. Lemberger T, Desvergne B, and Wahli W (1996) Peroxisome proliferator-activated receptors: a nuclear receptor signaling pathway in lipid physiology. Annu Rev Cell Dev Biol 12:335-363.
25. McDonald DR, Bamberger ME, Combs CK, and Landreth GE (1998) beta-Amyloid fibrils activate parallel mitogen-activated protein kinase pathways in microglia and THP1 monocytes. J Neurosci 18:4451-4460.
26. Motomura W, Okumura T, Takahashi N, Obara T, and Kohgo Y (2000) Activation of peroxisome proliferator-activated receptor gamma by troglitazone inhibits cell growth through the increase of p27KiP1 in human pancreatic carcinoma cells. Cancer Res 60:5558-5564.
27. Mueller E, Sarraf P, Tontonoz P, Evans RM, Martin KJ, Zhang M, Fletcher C, Singer S, and Spiegelman BM (1998) Terminal differentiation of human breast cancer through PPAR gamma. Mol Cell 1:465-470.
28. Nieder C, Grosu AL, Astner S, and Molls M (2005) Treatment of unresectable glioblastoma multiforme. Anticancer Res 25:4605-4610.
29. Parkins CS, Darling JL, Gill SS, Revesz T, and Thomas DG (1991) Cell proliferation in serial biopsies through human malignant brain tumours: measurement using Ki67 antibody labelling. Br J Neurosurg 5:289-298.
30. Perez-Ortiz JM, Tranque P, Vaquero CF, Domingo B, Molina F, Calvo S, Jordan J, Cena V, and Llopis J (2004) Glitazones differentially regulate primary astrocyte and glioma cell survival. Involvement of reactive oxygen species and peroxisome proliferator-activated receptor-γ. J Biol Chem 279:8976-8985.
31. r 92,000 type IV collagenase in human brain tumors. Cancer Res 53:2208-2211.
32. Reardon DA, Rich JN, Friedman HS, and Bigner DD (2006) Recent advances in the treatment of malignant astrocytoma. J Clin Oncol 24:1253-1265.
33. Redgate ES, Deutsch M, and Boggs SS (1991) Time of death of CNS tumor-bearing rats can be reliably predicted by body weight-loss patterns. Lab Anim Sci 41:269-273.
34. Sakamoto J, Kimura H, Moriyama S, Odaka H, Momose Y, Sugiyama Y, and Sawada H (2000) Activation of human peroxisome proliferator-activated receptor (PPAR) subtypes by pioglitazone. Biochem Biophys Res Commun 278:704-711.
35. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB, Holden SA, Chen LB, Singer S, Fletcher C, et al. (1998) Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med 4:1046-1052.
36. Sato H, Ishihara S, Kawashima K, Moriyama N, Suetsugu H, Kazumori H, Okuyama T, Rumi MA, Fukuda R, Nagasue N, et al. (2000) Expression of peroxisome proliferator-activated receptor (PPAR)gamma in gastric cancer and inhibitory effects of PPARgamma agonists. Br J Cancer 83:1394-1400.
37. Schabitz WR, Li F, Irie K, Sandage BW Jr, Locke KW, and Fisher M (1999) Synergistic effects of a combination of low-dose basic fibroblast growth factor and citicoline after temporary experimental focal ischemia. Stroke 30:427-431; discussion 431-2.
38. Sottocornola E, Colombo I, Vergani V, Taraboletti G, and Berra B (1998) Increased tumorigenicity and invasiveness of C6 rat glioma cells transfected with the human alpha-2,8 sialyltransferase cDNA. Invasion Metastasis 18:142-154.
39. Stander M, Naumann U, Dumitrescu L, Heneka M, Loschmann P, Gulbins E, Dichgans J, and Weller M (1998) Decorin gene transfer-mediated suppression of TGF-beta synthesis abrogates experimental malignant glioma growth in vivo. Gene Ther 5:1187-1194.
40. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996.
41. Tontonoz P, Singer S, Forman BM, Sarraf P, Fletcher JA, Fletcher CD, Brun RP, Mueller E, Altiok S, Oppenheim H, et al. (1997) Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator- activated receptor gamma and the retinoid X receptor. Proc Natl Acad Sci USA 94:237-241.
42. Torp SH (2002) Diagnostic and prognostic role of Ki67 immunostaining in human astrocytomas using four different antibodies. Clin Neuropathol 21:252-257.
43. Vitellaro-Zuccarello L, Meroni A, Amadeo A, and De Biasi S (2001) Chondroitin sulfate proteoglycans in the rat thalamus: expression during postnatal development and correlation with calcium-binding proteins in adults. Cell Tissue Res 306:15-26.
44. Wang M, Wise SC, Leff T, and Su TZ (1999) Troglitazone, an antidiabetic agent, inhibits cholesterol biosynthesis through a mechanism independent of peroxisome proliferator-activated receptor-gamma. Diabetes 48:254-260.
45. Willson TM, Brown PJ, Sternbach DD, and Henke BR (2000) The PPARs: from orphan receptors to drug discovery. J Med Chem 43:527-550.
46. Zander T, Kraus JA, Grommes C, Schlegel U, Feinstein D, Klockgether T, Landreth G, Koenigsknecht J, and Heneka MT (2002) Induction of apoptosis in human and rat glioma by agonists of the nuclear receptor PPARgamma. J Neurochem 81:1052-1060.