Preferential Iron Trafficking Characterizes Glioblastoma Stem-like Cells

Cancer Cell

Volumn 28, Issue 4, 2015, Pages 441-455

  Schonberg, David L ^a   Miller, Tyler E ^a   Wu, Qiulian ^a   Flavahan, William A ^a   Das, Nupur K ^a   Hale, James S ^a   Hubert, Christopher G ^a   Mack, Stephen C ^a   Jarrar, Awad M ^a   Karl, Robert T ^b   Rosager, Ann Mari ^c   Nixon, Anne M ^f   Tesar, Paul J ^b   Hamerlik, Petra ^d   Kristensen, Bjarne W ^c   Horbinski, Craig ^e   Connor, James R ^f   Fox, Paul L ^a   Lathia, Justin D ^a   Rich, Jeremy N ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

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

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^e UNIVERSITY OF KENTUCKY   (United States)

^f PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXM1; TRANSFERRIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; IRON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER STEM CELL; CONTROLLED STUDY; ENHANCER REGION; EPIGENETICS; GENE EXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VIVO STUDY; IRON TRANSPORT; MITOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA SEQUENCE; TISSUE SPECIFICITY; TUMOR CELL; TUMOR GENE; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; BRAIN TUMOR; CANCER TRANSPLANTATION; CELL CULTURE; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN NEOPLASMS; CELLS, CULTURED; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; FERRITINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HUMANS; IRON; MICE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; RECEPTORS, TRANSFERRIN; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; TRANSFERRIN;

EID: 84944043452     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.09.002     Document Type: Article

References (54)

1. Akhtar-Zaidi B., Cowper-Sal-lari R., Corradin O., Saiakhova A., Bartels C.F., Balasubramanian D., Myeroff L., Lutterbaugh J., Jarrar A., Kalady M.F., et al. Epigenomic enhancer profiling defines a signature of colon cancer. Science 2012, 336:736-739.
2. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
3. Bao S., Wu Q., Sathornsumetee S., Hao Y., Li Z., Hjelmeland A.B., Shi Q., McLendon R.E., Bigner D.D., Rich J.N. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006, 66:7843-7848.
4. Cao Y., Lathia J.D., Eyler C.E., Wu Q., Li Z., Wang H., McLendon R.E., Hjelmeland A.B., Rich J.N. Erythropoietin Receptor Signaling Through STAT3 Is Required For Glioma Stem Cell Maintenance. Genes Cancer 2010, 1:50-61.
5. Chen J., Li Y., Yu T.-S., McKay R.M., Burns D.K., Kernie S.G., Parada L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488:522-526.
6. Coffman L.G., Parsonage D., D'Agostino R., Torti F.M., Torti S.V. Regulatory effects of ferritin on angiogenesis. Proc. Natl. Acad. Sci. USA 2009, 106:570-575.
7. Connor J.R., Boeshore K.L., Benkovic S.A., Menzies S.L. Isoforms of ferritin have a specific cellular distribution in the brain. J. Neurosci. Res. 1994, 37:461-465.
8. Corradin O., Saiakhova A., Akhtar-Zaidi B., Myeroff L., Willis J., Cowper-Sal lari R., Lupien M., Markowitz S., Scacheri P.C. Combinatorial effects of multiple enhancer variants in linkage disequilibrium dictate levels of gene expression to confer susceptibility to common traits. Genome Res. 2014, 24:1-13.
9. Daniels T.R., Delgado T., Rodriguez J.A., Helguera G., Penichet M.L. The transferrin receptor part I: biology and targeting with cytotoxic antibodies for the treatment of cancer. Clin. Immunol. 2006, 121:144-158.
10. Daniels T.R., Delgado T., Helguera G., Penichet M.L. The transferrin receptor part II: targeted delivery of therapeutic agents into cancer cells. Clin. Immunol. 2006, 121:159-176.
11. de Arriba Zerpa G.A., Saleh M.C., Fernández P.M., Guillou F., Espinosa de los Monteros A., de Vellis J., Zakin M.M., Baron B. Alternative splicing prevents transferrin secretion during differentiation of a human oligodendrocyte cell line. J. Neurosci. Res. 2000, 61:388-395.
12. Eyler C.E., Wu Q., Yan K., MacSwords J.M., Chandler-Militello D., Misuraca K.L., Lathia J.D., Forrester M.T., Lee J., Stamler J.S., et al. Glioma stem cell proliferation and tumor growth are promoted by nitric oxide synthase-2. Cell 2011, 146:53-66.
13. Flavahan W.A., Wu Q., Hitomi M., Rahim N., Kim Y., Sloan A.E., Weil R.J., Nakano I., Sarkaria J.N., Stringer B.W., et al. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat. Neurosci. 2013, 16:1373-1382.
14. Gilbert M.R., Liu Y., Neltner J., Pu H., Morris A., Sunkara M., Pittman T., Kyprianou N., Horbinski C. Autophagy and oxidative stress in gliomas with IDH1 mutations. Acta Neuropathol. 2014, 127:221-233.
15. Gong A.-H., Wei P., Zhang S., Yao J., Yuan Y., Zhou A.-D., Lang F.F., Heimberger A.B., Rao G., Huang S. FoxM1 drives a feed-forward STAT3-activation signaling loop that promotes the self-renewal and tumorigenicity of glioblastoma stem-like cells. Cancer Res. 2015, 75:2337-2348.
16. Hjelmeland A.B., Wu Q., Wickman S., Eyler C., Heddleston J., Shi Q., Lathia J.D., Macswords J., Lee J., McLendon R.E., Rich J.N. Targeting A20 decreases glioma stem cell survival and tumor growth. PLoS Biol. 2010, 8:e1000319.
17. Hjelmeland A.B., Wu Q., Heddleston J.M., Choudhary G.S., MacSwords J., Lathia J.D., McLendon R., Lindner D., Sloan A., Rich J.N. Acidic stress promotes a glioma stem cell phenotype. Cell Death Differ. 2011, 18:829-840.
18. Hodgson J.G., Yeh R.-F., Ray A., Wang N.J., Smirnov I., Yu M., Hariono S., Silber J., Feiler H.S., Gray J.W., et al. Comparative analyses of gene copy number and mRNA expression in glioblastoma multiforme tumors and xenografts. Neuro-oncol. 2009, 11:477-487.
19. Holtkamp N., Afanasieva A., Elstner A., van Landeghem F.K.H., Könneker M., Kuhn S.A., Kettenmann H., von Deimling A. Brain slice invasion model reveals genes differentially regulated in glioma invasion. Biochem. Biophys. Res. Commun. 2005, 336:1227-1233.
20. Huang J., Simcox J., Mitchell T.C., Jones D., Cox J., Luo B., Cooksey R.C., Boros L.G., McClain D.A. Iron regulates glucose homeostasis in liver and muscle via AMP-activated protein kinase in mice. FASEB J. 2013, 27:2845-2854.
21. Iwasaki K., Hailemariam K., Tsuji Y. PIAS3 interacts with ATF1 and regulates the human ferritin H gene through an antioxidant-responsive element. J. Biol. Chem. 2007, 282:22335-22343.
22. Joshi K., Banasavadi-Siddegowda Y., Mo X., Kim S.-H., Mao P., Kig C., Nardini D., Sobol R.W., Chow L.M.L., Kornblum H.I., et al. MELK-dependent FOXM1 phosphorylation is essential for proliferation of glioma stem cells. Stem Cells 2013, 31:1051-1063.
23. Kikyo N., Hagiwara K., Fujisawa M., Kikyo N., Yazaki Y., Okabe T. Purification of a cell growth factor from a human lung cancer cell line: its relationship with ferritin. J. Cell. Physiol. 1994, 161:106-110.
24. Kim E., Kim M., Woo D.-H., Shin Y., Shin J., Chang N., Oh Y.T., Kim H., Rheey J., Nakano I., et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell 2013, 23:839-852.
25. Koorts A.M., Levay P.F., Becker P.J., Viljoen M. Pro- and anti-inflammatory cytokines during immune stimulation: modulation of iron status and red blood cell profile. Mediators Inflamm. 2011, 2011:716301.
26. Kuhn D.E., Baker B.D., Lafuse W.P., Zwilling B.S. Differential iron transport into phagosomes isolated from the RAW264.7 macrophage cell lines transfected with Nramp1Gly169 or Nramp1Asp169. J. Leukoc. Biol. 1999, 66:113-119.
27. Kwak E.L., Larochelle D.A., Beaumont C., Torti S.V., Torti F.M. Role for NF-kappa B in the regulation of ferritin H by tumor necrosis factor-alpha. J. Biol. Chem. 1995, 270:15285-15293.
28. Lane D.J.R., Mills T.M., Shafie N.H., Merlot A.M., Saleh Moussa R., Kalinowski D.S., Kovacevic Z., Richardson D.R. Expanding horizons in iron chelation and the treatment of cancer: role of iron in the regulation of ER stress and the epithelial-mesenchymal transition. Biochim. Biophys. Acta 2014, 1845:166-181.
29. Lathia J.D., Gallagher J., Heddleston J.M., Wang J., Eyler C.E., Macswords J., Wu Q., Vasanji A., McLendon R.E., Hjelmeland A.B., Rich J.N. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010, 6:421-432.
30. Leitner D.F., Connor J.R. Functional roles of transferrin in the brain. Biochim. Biophys. Acta 2012, 1820:393-402.
31. Li Z., Bao S., Wu Q., Wang H., Eyler C., Sathornsumetee S., Shi Q., Cao Y., Lathia J., McLendon R.E., et al. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009, 15:501-513.
32. Liu M., Dai B., Kang S.-H., Ban K., Huang F.-J., Lang F.F., Aldape K.D., Xie T.X., Pelloski C.E., Xie K., et al. FoxM1B is overexpressed in human glioblastomas and critically regulates the tumorigenicity of glioma cells. Cancer Res. 2006, 66:3593-3602.
33. Liu X., Madhankumar A.B., Slagle-Webb B., Sheehan J.M., Surguladze N., Connor J.R. Heavy chain ferritin siRNA delivered by cationic liposomes increases sensitivity of cancer cells to chemotherapeutic agents. Cancer Res. 2011, 71:2240-2249.
34. Mencalha A.L., Binato R., Ferreira G.M., Du Rocher B., Abdelhay E. Forkhead box M1 (FoxM1) gene is a new STAT3 transcriptional factor target and is essential for proliferation, survival and DNA repair of K562 cell line. PLoS ONE 2012, 7:e48160.
35. Nandal A., Ruiz J.C., Subramanian P., Ghimire-Rijal S., Sinnamon R.A., Stemmler T.L., Bruick R.K., Philpott C.C. Activation of the HIF prolyl hydroxylase by the iron chaperones PCBP1 and PCBP2. Cell Metab. 2011, 14:647-657.
36. Peyssonnaux C., Zinkernagel A.S., Schuepbach R.A., Rankin E., Vaulont S., Haase V.H., Nizet V., Johnson R.S. Regulation of iron homeostasis by the hypoxia-inducible transcription factors (HIFs). J. Clin. Invest. 2007, 117:1926-1932.
37. Pham C.G., Bubici C., Zazzeroni F., Papa S., Jones J., Alvarez K., Jayawardena S., De Smaele E., Cong R., Beaumont C., et al. Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell 2004, 119:529-542.
38. Recalcati S., Taramelli D., Conte D., Cairo G. Nitric oxide-mediated induction of ferritin synthesis in J774 macrophages by inflammatory cytokines: role of selective iron regulatory protein-2 downregulation. Blood 1998, 91:1059-1066.
39. Ruddell R.G., Hoang-Le D., Barwood J.M., Rutherford P.S., Piva T.J., Watters D.J., Santambrogio P., Arosio P., Ramm G.A. Ferritin functions as a proinflammatory cytokine via iron-independent protein kinase C zeta/nuclear factor kappaB-regulated signaling in rat hepatic stellate cells. Hepatology 2009, 49:887-900.
40. Sauvageau M., Goff L.A., Lodato S., Bonev B., Groff A.F., Gerhardinger C., Sanchez-Gomez D.B., Hacisuleyman E., Li E., Spence M., et al. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. eLife 2013, 2:e01749.
41. Schober M., Fuchs E. Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-β and integrin/focal adhesion kinase (FAK) signaling. Proc. Natl. Acad. Sci. USA 2011, 108:10544-10549.
42. Shinojima N., Hossain A., Takezaki T., Fueyo J., Gumin J., Gao F., Nwajei F., Marini F.C., Andreeff M., Kuratsu J., Lang F.F. TGF-β mediates homing of bone marrow-derived human mesenchymal stem cells to glioma stem cells. Cancer Res. 2013, 73:2333-2344.
43. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
44. Stupp R., Hegi M.E., Mason W.P., van den Bent M.J., Taphoorn M.J.B., Janzer R.C., Ludwin S.K., Allgeier A., Fisher B., Belanger K., et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10:459-466. European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups, National Cancer Institute of Canada Clinical Trials GroupNational Cancer Institute of Canada Clinical Trials Group.
45. Torti S.V., Torti F.M. Iron and cancer: more ore to be mined. Nat. Rev. Cancer 2013, 13:342-355.
46. Venere M., Hamerlik P., Wu Q., Rasmussen R.D., Song L.A., Vasanji A., Tenley N., Flavahan W.A., Hjelmeland A.B., Bartek J., Rich J.N. Therapeutic targeting of constitutive PARP activation compromises stem cell phenotype and survival of glioblastoma-initiating cells. Cell Death Differ. 2014, 21:258-269.
47. Wang S., Bates J., Li X., Schanz S., Chandler-Militello D., Levine C., Maherali N., Studer L., Hochedlinger K., Windrem M., Goldman S.A. Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013, 12:252-264.
48. Wasserman W.W., Fahl W.E. Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA 1997, 94:5361-5366.
49. Wrighting D.M., Andrews N.C. Interleukin-6 induces hepcidin expression through STAT3. Blood 2006, 108:3204-3209.
50. Wu K.-J., Polack A., Dalla-Favera R. Coordinated regulation of iron-controlling genes, H-ferritin and IRP2, by c-MYC. Science 1999, 283:676-679.
51. Yan K., Wu Q., Yan D.H., Lee C.H., Rahim N., Tritschler I., DeVecchio J., Kalady M.F., Hjelmeland A.B., Rich J.N. Glioma cancer stem cells secrete Gremlin1 to promote their maintenance within the tumor hierarchy. Genes Dev. 2014, 28:1085-1100.
52. Ye X.Z., Xu S.L., Xin Y.H., Yu S.C., Ping Y.F., Chen L., Xiao H.L., Wang B., Yi L., Wang Q.L., et al. Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway. J. Immunol. 2012, 189:444-453.
53. Zhang N., Wei P., Gong A., Chiu W.-T., Lee H.-T., Colman H., Huang H., Xue J., Liu M., Wang Y., et al. FoxM1 promotes β-catenin nuclear localization and controls Wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011, 20:427-442.
54. Zhao D., Pan C., Sun J., Gilbert C., Drews-Elger K., Azzam D.J., Picon-Ruiz M., Kim M., Ullmer W., El-Ashry D., et al. VEGF drives cancer-initiating stem cells through VEGFR-2/Stat3 signaling to upregulate Myc and Sox2. Oncogene 2014, 34:3107-3119.