Transferrin-receptor-mediated iron accumulation controls proliferation and glutamate release in glioma cells

Journal of Molecular Medicine

Volumn 87, Issue 2, 2009, Pages 153-167

  Chirasani, S R ^a   Markovic, D S ^a,f   Synowitz, M ^b   Eichler, S A ^a   Wisniewski, P ^c   Kaminska, B ^c   Otto, A ^a   Wanker, E ^a   Schafer M ^d   Chiarugi, P ^e   Meier, J C ^a   Kettenmann, H ^a   Glass, R ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF FLORENCE   (Italy)

^f Helios Klinikum   (Germany)

Author keywords

ETS; Free radicals; Glioma; Neuro oncology; Neuroscience; Oxidative stress

Indexed keywords

GLUTAMIC ACID; IRON; MITOGEN ACTIVATED PROTEIN KINASE; P21 ACTIVATED KINASE; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE; TRANSFERRIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CANCER GROWTH; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; FEMALE; GLIOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL NECROSIS; NONHUMAN; OXIDATION REDUCTION REACTION; RAT; RECEPTOR DOWN REGULATION; TUMOR VOLUME; TUMOR XENOGRAFT;

ANIMALS; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; GLIOMA; GLUTAMATES; GREEN FLUORESCENT PROTEINS; HUMANS; IRON; MICE; MICE, INBRED C57BL; MICE, NUDE; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; NEOPLASM TRANSPLANTATION; OXIDATION-REDUCTION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEIN C-ETS-1; RATS; RATS, WISTAR; RECEPTORS, TRANSFERRIN; SIGNAL TRANSDUCTION;

EID: 58549111579     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-008-0414-3     Document Type: Article

References (46)

1. LS Terada 2006 Specificity in reactive oxidant signaling: think globally, act locally J Cell Biol 174 5 615 623
2. EA Veal AM Day BA Morgan 2007 Hydrogen peroxide sensing and signaling Mol Cell 26 1 1 14
3. SP Hussain LJ Hofseth CC Harris 2003 Radical causes of cancer Nat Rev Cancer 3 4 276 285
4. V Martin F Herrera G Garcia-Santos I Antolin J Rodriguez-Blanco C Rodriguez 2007 Signaling pathways involved in antioxidant control of glioma cell proliferation Free Radic Biol Med 42 11 1715 1722
5. Kleihues P, Burger PC, Scheithauer BW (1996) Histological typing of the tumours of the central nervous system, 2nd edn. Springer, Stuttgart
6. EC Holland 2000 Glioblastoma multiforme: the terminator Proc Natl Acad Sci USA 97 12 6242 6244
7. EC Holland 2001 Gliomagenesis: genetic alterations and mouse models Nat Rev Genet 2 2 120 129
8. T Takano JH Lin G Arcuino Q Gao J Yang M Nedergaard 2001 Glutamate release promotes growth of malignant gliomas Nat Med 7 9 1010 1015
9. H Sontheimer 2003 Malignant gliomas: perverting glutamate and ion homeostasis for selective advantage Trends Neurosci 26 10 543 549
10. L Recht CO Torres TW Smith V Raso TW Griffin 1990 Transferrin receptor in normal and neoplastic brain tissue: implications for brain-tumor immunotherapy J Neurosurg 72 6 941 945
11. DR Richardson 2002 Iron chelators as therapeutic agents for the treatment of cancer Crit Rev Oncol Hematol 42 3 267 281
12. L Zecca MB Youdim P Riederer JR Connor RR Crichton 2004 Iron, brain ageing and neurodegenerative disorders Nat Rev Neurosci 5 11 863 873
13. PG Cavanaugh L Jia Y Zou GL Nicolson 1999 Transferrin receptor overexpression enhances transferrin responsiveness and the metastatic growth of a rat mammary adenocarcinoma cell line Breast Cancer Res Treat 56 3 203 217
14. MH Sieweke H Tekotte J Frampton T Graf 1996 MafB is an interaction partner and repressor of Ets-1 that inhibits erythroid differentiation Cell 85 1 49 60
15. G Marziali E Perrotti R Ilari V Lulli EM Coccia R Moret LC Kuhn U Testa A Battistini 2002 Role of Ets-1 in transcriptional regulation of transferrin receptor and erythroid differentiation Oncogene 21 52 7933 7944
16. D Owen LC Kuhn 1987 Noncoding 3 sequences of the transferrin receptor gene are required for mRNA regulation by iron Embo J 6 5 1287 1293
17. AD Sharrocks 2001 The ETS-domain transcription factor family Nat Rev Mol Cell Biol 2 11 827 837
18. G Kitange M Kishikawa T Nakayama S Naito M Iseki S Shibata 1999 Expression of the Ets-1 proto-oncogene correlates with malignant potential in human astrocytic tumors Mod Pathol 12 6 618 626
19. J Dittmer 2003 The biology of the Ets1 proto-oncogene Mol Cancer 2 29
20. D Kita T Takino M Nakada T Takahashi J Yamashita H Sato 2001 Expression of dominant-negative form of Ets-1 suppresses fibronectin-stimulated cell adhesion and migration through down-regulation of integrin alpha5 expression in U251 glioma cell line Cancer Res 61 21 7985 7991
21. J Meier R Grantyn 2004 A gephyrin-related mechanism restraining glycine receptor anchoring at GABAergic synapses J Neurosci 246 1398 1405
22. I Ferrer 1999 Neurons and their dendrites in frontotemporal dementia Dement Geriatr Cogn Disord 10 Suppl 1 55 60
23. Eichler SA, Kirischuk S, Juttner R, Legendre P, Lehmann TN, Gloveli T, Grantyn R, Meier JC (2008) Glycinergic tonic inhibition of hippocampal neurons with depolarising GABAergic transmission elicits histopathological signs of temporal lobe epilepsy. J Cell Mol Med doi: 10.1111/j.1582-4934.2008.00357.x
24. A Castegna M Aksenov M Aksenova V Thongboonkerd JB Klein WM Pierce R Booze WR Markesbery DA Butterfield 2002 Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1 Free Radic Biol Med 33 4 562 571
25. F Petrat H de Groot U Rauen 2001 Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells Biochem J 356 Pt 1 61 69
26. RI Geran NH Greenberg MM Macdonald BJ Abbott 1977 Modified protocol for the testing of new synthetics in the L1210 lymphoid leukemia murine model in the DR&D program, DCT, NCI Natl Cancer Inst Monogr 45 151 153
27. M Nakada J Yamashita Y Okada H Sato 1999 Ets-1 positively regulates expression of urokinase-type plasminogen activator (uPA) and invasiveness of astrocytic tumors J Neuropathol Exp Neurol 58 4 329 334
28. HL Sun YN Liu YT Huang SL Pan DY Huang JH Guh FY Lee SC Kuo CM Teng 2007 YC-1 inhibits HIF-1 expression in prostate cancer cells: contribution of Akt/NF-kappaB signaling to HIF-1alpha accumulation during hypoxia Oncogene 26 3941 3951
29. CJ Mattia JD Adams Jr.SC Bondy 1993 Free radical induction in the brain and liver by products of toluene catabolism Biochem Pharmacol 46 1 103 110
30. P Chiarugi ML Taddei N Schiavone L Papucci E Giannoni T Fiaschi S Capaccioli G Raugei G Ramponi 2004 LMW-PTP is a positive regulator of tumor onset and growth Oncogene 23 22 3905 3914
31. A Ostman C Hellberg FD Bohmer 2006 Protein-tyrosine phosphatases and cancer Nat Rev Cancer 6 4 307 320
32. E Giannoni G Raugei P Chiarugi G Ramponi 2006 A novel redox-based switch: LMW-PTP oxidation enhances Grb2 binding and leads to ERK activation Biochem Biophys Res Commun 348 2 367 373
33. V Martin F Herrera P Carrera-Gonzalez G Garcia-Santos I Antolin J Rodriguez-Blanco C Rodriguez 2006 Intracellular signaling pathways involved in the cell growth inhibition of glioma cells by melatonin Cancer Res 66 2 1081 1088
34. N Nath S Wang V Betts E Knudsen S Chellappan 2003 Apoptotic and mitogenic stimuli inactivate Rb by differential utilization of p38 and cyclin-dependent kinases Oncogene 22 38 5986 5994
35. BP Zhou Y Liao W Xia B Spohn MH Lee MC Hung 2001 Cytoplasmic localization of p21Cip1/WAF1 by Akt-induced phosphorylation in HER-2/neu-overexpressing cells Nat Cell Biol 3 3 245 252
36. T Szatmari K Lumniczky S Desaknai S Trajcevski EJ Hidvegi H Hamada G Safrany 2006 Detailed characterization of the mouse glioma 261 tumor model for experimental glioblastoma therapy Cancer Sci 97 6 546 553
37. MW Hentze LC Kuhn 1996 Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress Proc Natl Acad Sci USA 93 16 8175 8182
38. MC McGahan J Harned M Mukunnemkeril M Goralska L Fleisher JB Ferrell 2005 Iron alters glutamate secretion by regulating cytosolic aconitase activity Am J Physiol Cell Physiol 288 5 C1117 C1124
39. S Segerer F Eitner Y Cui KL Hudkins CE Alpers 2002 Cellular injury associated with renal thrombotic microangiopathy in human immunodeficiency virus-infected macaques J Am Soc Nephrol 13 2 370 378
40. K Xing A Raza S Lofgren MR Fernando YS Ho MF Lou 2007 Low molecular weight protein tyrosine phosphatase (LMW-PTP) and its possible physiological functions of redox signaling in the eye lens Biochim Biophys Acta 1774 5 545 555
41. SK Pandey XX Yu LM Watts MD Michael KW Sloop AR Rivard TA Leedom VP Manchem L Samadzadeh RA McKay BP Monia S Bhanot 2007 Reduction of low molecular weight protein-tyrosine phosphatase expression improves hyperglycemia and insulin sensitivity in obese mice J Biol Chem 282 19 14291 14299
42. H Suyama T Igishi H Sano S Matsumoto Y Shigeoka H Nakanishi M Endo N Burioka Y Hitsuda E Shimizu 2004 ERK activation and subsequent RB phosphorylation are important determinants of the sensitivity to paclitaxel in lung adenocarcinoma cells Int J Oncol 24 6 1499 1504
43. DJ Fernandes CE Ravenhall T Harris T Tran R Vlahos AG Stewart 2004 Contribution of the p38MAPK signalling pathway to proliferation in human cultured airway smooth muscle cells is mitogen-specific Br J Pharmacol 142 7 1182 1190
44. FJ Renton TM Jeitner 1996 Cell cycle-dependent inhibition of the proliferation of human neural tumor cell lines by iron chelators Biochem Pharmacol 51 11 1553 1561
45. TM Jeitner FJ Renton 1996 Inhibition of the proliferation of human neural neoplastic cell lines by cysteamine Cancer Lett 103 1 85 90
46. P Basset J Zwiller MO Revel G Vincendon 1985 Growth promotion of transformed cells by iron in serum-free culture Carcinogenesis 6 3 355 359