Neural stem cells adopt tumorigenic properties by constitutively activated NF-κb and subsequent vegf up-regulation

Stem Cells and Development

Volumn 19, Issue 7, 2010, Pages 999-1015

  Kaus, Aljoscha ^a   Widera, Darius ^b   Kassmer, Susannah ^c   Peter, Jan ^d   Zaenker, Kurt ^e   Kaltschmidt, Christian ^b   Kaltschmidt, Barbara ^f  

^a YALE UNIVERSITY   (United States)

^b Department of Cell Biolog ^*  (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e UNIVERSITY OF WITTEN HERDECKE   (Germany)

^f BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; DNA; GLUTAMATE DECARBOXYLASE 67; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NESTIN; NEUROFILAMENT M PROTEIN; PROTEIN P53; VASCULOTROPIN; BIOLOGICAL MARKER; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER RESEARCH; CARCINOGENIC ACTIVITY; CELL CULTURE; CELL CYCLE; CELL DEATH; CELL ISOLATION; CELL PROLIFERATION; CHROMOSOME; CONTROLLED STUDY; GLIOMA; GROWTH FACTOR INDEPENDENT NEURAL STEM CELL; IMMUNOCYTOCHEMISTRY; METAPHASE; MICROARRAY ANALYSIS; MORPHOLOGY; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL DIFFERENTIATION; CULTURE TECHNIQUE; CYTOLOGY; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; STEM CELL; WISTAR RAT;

RATTUS;

ANIMALS; BIOLOGICAL MARKERS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; HUMANS; MICROARRAY ANALYSIS; NEURONS; NF-KAPPA B; PHENOTYPE; RATS; RATS, WISTAR; STEM CELLS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77954928427     PISSN: 15473287     EISSN: None     Source Type: Journal    
DOI: 10.1089/scd.2009.0416     Document Type: Article

References (62)

1. Eriksson PS, E Perfilieva, T Bjork-Eriksson, AM Alborn, C Nordborg, DA Peterson and FH Gage. (1998). Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317.
2. Nunes MC, NS Roy, HM Keyoung, RR Goodman, G McKhann II, L Jiang, J Kang, M Nedergaard and SA Goldman. (2003). Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9: 439-447.
3. Sakakibara S, Y Nakamura, T Yoshida, S Shibata, M Koike, H Takano, S Ueda, Y Uchiyama, T Noda and H Okano. (2002). RNAbinding protein Musashi family: roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc Natl Acad Sci USA 99: 15194-15199.
4. Lendahl U, LB Zimmerman and RD McKay. (1990). CNS stem cells express a new class of intermediate filament protein. Cell 60: 585-595.
5. Sakakibara S, T Imai, K Hamaguchi, M Okabe, J Aruga, K Nakajima, D Yasutomi, T Nagata, Y Kurihara, S Uesugi, T Miyata, M Ogawa, K Mikoshiba and H Okano. (1996). Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176: 230-242.
6. Pevny LH, S Sockanathan, M Placzek and R Lovell-Badge. (1998). A role for SOX1 in neural determination. Development 125: 1967-1978.
7. Brazel CY, TL Limke, JK Osborne, T Miura, J Cai, L Pevny and MS Rao. (2005). Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Aging Cell 4: 197-207.
8. Sanai N, A Alvarez-Buylla and MS Berger. (2005). Neural stem cells and the origin of gliomas. N Engl J Med 353: 811-822.
9. Uchida K, M Mukai, H Okano and T Kawase. (2004). Possible oncogenicity of subventricular zone neural stem cells: case report. Neurosurgery 55: 977-978.
10. Barami K. (2007). Biology of the subventricular zone in relation to gliomagenesis. J Clin Neurosci 14: 1143-1149.
11. Widera D, A Kaus, C Kaltschmidt and B Kaltschmidt. (2008). Neural stem cells, inflammation and NF-kappaB: basic principle of maintenance and repair or origin of brain tumours? J Cell Mol Med 12: 459-470.
12. Zhong W. (2003). Diversifying neural cells through order of birth and asymmetry of division. Neuron 37: 11-14.
13. Widera D, I Mikenberg, M Elvers, C Kaltschmidt and B Kaltschmidt. (2006). Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling. BMC Neurosci 7: 64.
14. Widera D, I Mikenberg, A Kaus, C Kaltschmidt and B Kaltschmidt. (2006). Nuclear Factor-kappaB controls the reaggregation of 3D neurosphere cultures in vitro. Eur Cell Mater 11: 76-84; discussion 85.
15. Karin M, Y Yamamoto and QM Wang. (2004). The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov 3: 17-26.
16. Widera D, I Mikenberg, B Kaltschmidt and C Kaltschmidt. (2006). Potential role of NF-kappaB in adult neural stem cells: the underrated steersman? Int J Dev Neurosci 24: 91-102.
17. Kaltschmidt B, D Widera and C Kaltschmidt. (2005). Signaling via NF-kappaB in the nervous system. Biochim Biophys Acta 1745: 287-299.
18. Hayden MS and S Ghosh. (2008). Shared principles in NF-kappaB signaling. Cell 132: 344-362.
19. Kumar A, Y Takada, AM Boriek and BB Aggarwal. (2004). Nuclear factor-kappaB: its role in health and disease. J Mol Med 82: 434-448.
20. Kim HJ, N Hawke and AS Baldwin. (2006). NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ 13: 738-747.
21. Aggarwal BB. (2004). Nuclear factor-kappaB: the enemy within. Cancer Cell 6: 203-208.
22. Nakanishi C and M Toi. (2005). Nuclear factor-kappaB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 5: 297-309.
23. Schwartz SA, A Hernandez and B Mark Evers. (1999). The role of NF-kappaB/IkappaB proteins in cancer: implications for novel treatment strategies. Surg Oncol 8: 143-153.
24. Gage FH. (2000). Mammalian neural stem cells. Science 287: 1433-1438.
25. Lie DC, H Song, SA Colamarino, GL Ming and FH Gage. (2004). Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44: 399-421.
26. Shah K, G Hsich and XO Breakefield. (2004). Neural precursor cells and their role in neuro-oncology. Dev Neurosci 26: 118-130.
27. Schwamborn J, A Lindecke, M Elvers, V Horejschi, M Kerick, M Rafigh, J Pfeiffer, M Prullage, B Kaltschmidt and C Kaltschmidt. (2003). Microarray analysis of tumor necrosis factor alpha induced gene expression in U373 human glioblastoma cells. BMC Genomics 4: 46.
28. Fridmacher V, B Kaltschmidt, B Goudeau, D Ndiaye, FM Rossi, J Pfeiffer, C Kaltschmidt, A Israel and S Memet. (2003). Forebrainspecific neuronal inhibition of nuclear factor-kappaB activity leads to loss of neuroprotection. J Neurosci 23: 9403-9408.
29. Sasaki Y, E Derudder, E Hobeika, R Pelanda, M Reth, K Rajewsky and M Schmidt-Supprian. (2006). Canonical NF-kappaB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity 24: 729-739.
30. Jin K, Y Zhu, Y Sun, XO Mao, L Xie and DA Greenberg. (2002). Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99: 11946-11950.
31. Graham V, J Khudyakov, P Ellis and L Pevny. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765.
32. Perrin FE, G Boisset, M Docquier, O Schaad, P Descombes and AC Kato. (2005). No widespread induction of cell death genes occurs in pure motoneurons in an amyotrophic lateral sclerosis mouse model. Hum Mol Genet 14: 3309-3320.
33. Shea TB and ML Beermann. (1999). Neuronal intermediate filament protein alpha-internexin facilitates axonal neurite elongation in neuroblastoma cells. Cell Motil Cytoskeleton 43: 322-333.
34. Lindefors N. (1993). Dopaminergic regulation of glutamic acid decarboxylase mRNA expression and GABA release in the striatum: a review. Prog Neuropsychopharmacol Biol Psychiatry 17: 887-903.
35. Ryan KM, MK Ernst, NR Rice and KH Vousden. (2000). Role of NF-kappaB in p53-mediated programmed cell death. Nature 404: 892-897.
36. Maurer MH, WK Tripps, RE Feldmann Jr and W Kuschinsky. (2003). Expression of vascular endothelial growth factor and its receptors in rat neural stem cells. Neurosci Lett 344: 165-168.
37. Chilov D, E Kukk, S Taira, M Jeltsch, J Kaukonen, A Palotie, V Joukov and K Alitalo. (1997). Genomic organization of human and mouse genes for vascular endothelial growth factor C. J Biol Chem 272: 25176-25183.
38. Wang Z, S Banerjee, Y Li, KM Rahman, Y Zhang and FH Sarkar. (2006). Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 66: 2778-2784.
39. Gottipati S, NL Rao and WP Fung-Leung. (2008). IRAK1: a critical signaling mediator of innate immunity. Cell Signal 20: 269-276.
40. Thacker J and MZ Zdzienicka. (2004). The XRCC genes: expanding roles in DNA double-strand break repair. DNA Repair (Amst) 3: 1081-1090.
41. Dehmelt L and S Halpain. (2005). The MAP2/Tau family of microtubule-associated proteins. Genome Biol 6: 204.
42. Priest B, GJ Kaczorowski and ML Garcia. (2006). Ion channel modulators: new targets and new indications for old targets. Curr Opin Drug Discov Devel 9: 587-594.
43. Hait WN and JM Yang. (2006). The individualization of cancer therapy: the unexpected role of p53. Trans Am Clin Climatol Assoc 117: 85-101; discussion 101.
44. Barrett AJ, MM Horowitz, BH Pollock, MJ Zhang, MM Bortin, GR Buchanan, BM Camitta, J Ochs, J Graham-Pole and PA Rowlings. (1994). Bone marrow transplants from HLA-identical siblings as compared with chemotherapy for children with acute lymphoblastic leukemia in a second remission. N Engl J Med 331: 1253-1258.
45. Zheng H, H Ying, H Yan, AC Kimmelman, DJ Hiller, AJ Chen, SR Perry, G Tonon, GC Chu, Z Ding, JM Stommel, KL Dunn, R Wiedemeyer, MJ You, C Brennan, YA Wang, KL Ligon, WH Wong, L Chin and RA DePinho. (2008). p53 and Pten control neural and glioma stem/progenitor cell renewal and differentiation. Nature 455: 1129-1133.
46. Wang Y, J Yang, H Zheng, GJ Tomasek, P Zhang, PE McKeever, EY Lee and Y Zhu. (2009). Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytic glioma in a murine model. Cancer Cell 15: 514-526.
47. Basseres DS and AS Baldwin. (2006). Nuclear factor-kappaB and inhibitor of kappaB kinase pathways in oncogenic initiation and progression. Oncogene 25: 6817-6830.
48. Freedman VH and SI Shin. (1974). Cellular tumorigenicity in nude mice: correlation with cell growth in semi-solid medium. Cell 3: 355-359.
49. Singh SK, ID Clarke, T Hide and PB Dirks. (2004). Cancer stem cells in nervous system tumors. Oncogene 23: 7267-7273.
50. Rosland GV, A Svendsen, A Torsvik, E Sobala, E McCormack, H Immervoll, J Mysliwietz, JC Tonn, R Goldbrunner, PE Lonning, R Bjerkvig and C Schichor. (2009). Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res 69: 5331-5339.
51. Hemmati HD, I Nakano, JA Lazareff, M Masterman-Smith, DH Geschwind, M Bronner-Fraser and HI Kornblum. (2003). Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100: 15178-15183.
52. Leung SY, ST Yuen, TL Chan, AS Chan, JW Ho, K Kwan, YW Fan, KN Hung, LP Chung and AH Wyllie. (2000). Chromosomal instability and p53 inactivation are required for genesis of glioblastoma but not for colorectal cancer in patients with germline mismatch repair gene mutation. Oncogene 19: 4079-4083.
53. Shishodia S and BB Aggarwal. (2004). Nuclear factor-kappaB: a friend or a foe in cancer? Biochem Pharmacol 68: 1071-1080.
54. Cuevas P, D Diaz-Gonzalez and M Dujovny. (2003). Glioma cellassociated sustained activation of the transcription factor, nuclear factor-kappa B, was inhibited by neomycin. Neurol Res 25: 271-274.
55. Hui AM, W Zhang, W Chen, D Xi, B Purow, GC Friedman and HA Fine. (2004). Agents with selective estrogen receptor (ER) modulator activity induce apoptosis in vitro and in vivo in ER-negative glioma cells. Cancer Res 64: 9115-9123.
56. Walton NM, GE Snyder, D Park, F Kobeissy, B Scheffler and DA Steindler. (2009). Gliotypic neural stem cells transiently adopt tumorigenic properties during normal differentiation. Stem Cells 27: 280-289.
57. Siebzehnrubl FA, I Jeske, D Muller, R Buslei, R Coras, E Hahnen, HB Huttner, D Corbeil, J Kaesbauer, T Appl, S von Horsten and I Blumcke. (2009). Spontaneous in vitro transformation of adult neural precursors into stem-like cancer cells. Brain Pathol 19: 399-408.
58. Norden AD, J Drappatz and PY Wen. (2008). Novel antiangiogenic therapies for malignant gliomas. Lancet Neurol 7: 1152-1160.
59. Ranieri G, R Patruno, E Ruggieri, S Montemurro, P Valerio and D Ribatti. (2006). Vascular endothelial growth factor (VEGF) as a target of bevacizumab in cancer: from the biology to the clinic. Curr Med Chem 13: 1845-1857.
60. Kelly JJ, Stechishin O, Chojnacki A, Lun X, Sun B, Senger DL, Forsyth P, Auer RN, Dunn JF, Cairncross JG, Parney IF and Weiss S. (2009). Proliferation of human glioblastoma stem cells occurs independently of exogenous mitogens. Stem Cells 27: 1722-1733.
61. Biswas DK, AP Cruz, E Gansberger and AB Pardee. (2000). Epidermal growth factor-induced nuclear factor kappa B activation: A major pathway of cell-cycle progression in estrogenreceptor negative breast cancer cells. Proc Natl Acad Sci USA 97: 8542-8547.
62. Biswas DK and JD Iglehart. (2006). Linkage between EGFR family receptors and nuclear factor kappaB (NF-kappaB) signaling in breast cancer. J Cell Physiol 209: 645-652.