Hedgehog/GLI1 regulates IGF dependent malignant behaviors in glioma stem cells

Journal of Cellular Physiology

Volumn 226, Issue 4, 2011, Pages 1118-1127

  Hsieh, Antony ^a   Ellsworth, Ron ^b   Hsieh, David ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; SOMATOMEDIN; TEMOZOLOMIDE; TRANSCRIPTION FACTOR GLI1;

ANGIOGENESIS; ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER RESISTANCE; CANCER STEM CELL; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CLONOGENESIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; GLIOBLASTOMA; GLIOMA CELL; GLIOMA STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

CELL PROLIFERATION; CELL SURVIVAL; DACARBAZINE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GLIOMA; HEDGEHOG PROTEINS; HUMANS; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-LIKE GROWTH FACTOR I; MAP KINASE SIGNALING SYSTEM; NEOPLASTIC STEM CELLS; RADIATION TOLERANCE; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

ERINACEIDAE;

EID: 79251492356     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22433     Document Type: Article

References (36)

1. Annabi B, Lachambre MP, Plouffe K, Sartelet H, Beliveau R. 2009. Modulation of invasive properties of CD133+ glioblastoma stem cells: A role for MT1-MMP in bioactive lysophospholipid signaling. Mol Carcinog 48:910-919.
2. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. 2006. Glioma stem cells promote radio resistance by preferential activation of the DNA damage response. Nature 444:756-760.
3. Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN. 2006. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843-7848.
4. Beier D, Hau P, Proescholdt M, Lohmeier A, Wischhusen J, Oefner PJ, Aigner L, Brawanski A, Bogdahn U, Beier CP. 2007. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res 67:4010-4015.
5. Beier D, Rohrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P, Proescholdt M, Brawanski A, Bogdahn U, Trampe-Kieslich A, Giebel B, Wischhusen J, Reifenberger G, Hau P, Beier CP. 2008. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 68:5706-5715.
6. Bigelow RL, Chari NS, Unden AB, Spurgers KB, Lee S, Roop DR, Toftgard R, McDonnell TJ. 2004. Transcriptional regulation of Bcl-2 mediated by the sonic hedgehog signaling pathway through GLI-1. J Biol Chem 279:1197-1205.
7. Bommer GT, Feng Y, Iura A, Giordano TJ, Kuick R, Kadikoy H, Sikorski D, Wu R, Cho KR, Fearon ER. 2010. IRS1 regulation by Wnt/beta-catenin signaling and varied contribution of IRS1 to the neoplastic phenotype. J Biol Chem 285:1928-1938.
8. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. 1999. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286:1358-1362.
9. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. 2007. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 17:165-172.
10. Das S, Harris LG, Metge BJ, Liu S, Riker AI, Samant RS, Shevde LA. 2009. The hedgehog pathway transcription factor GLI1 promotes malignant behavior of cancer cells by up-regulating osteopontin. J Biol Chem 284:22888-22897.
11. Dhillon AS, Hagan S, Rath O, Kolch W. 2007. MAP kinase signalling pathways in cancer. Oncogene 26:3279-3290.
12. Eramo A, Ricci-Vitiani L, Zeuner A, Pallini R, Lotti F, Sette G, Pilozzi E, Larocca LM, Peschle C, De Maria R. 2006. Chemotherapy resistance of glioblastoma stem cells. Cell Death Differ 13:1238-1241.
13. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA, Cavenee WK. 2007. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev 21:2683-2710.
14. Hagemann C, Meyer C, Stojic J, Eicker S, Gerngras S, Kuhnel S, Roosen K, Vince GH. 2006. High efficiency transfection of glioma cell lines and primary cells for overexpression and RNAi experiments. J Neurosci Methods 156:194-202.
15. Hirano H, Lopes MB, Laws ER, Jr., Asakura T, Goto M, Carpenter JE, Karns LR, VandenBerg SR. 1999. Insulin-like growth factor-1 content and pattern of expression correlates with histopathologic grade in diffusely infiltrating astrocytomas. Neuro-Oncol 1:109-119.
16. Ingham PW, McMahon AP. 2001. Hedgehog signaling in animal development: Paradigms and principles. Genes Dev 15:3059-3087.
17. Khandwala HM, McCutcheon IE, Flyvbjerg A, Friend KE. 2000. The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr Rev 21:215-244.
18. Kondo T, Setoguchi T, Taga T. 2004. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA 101:781-786.
19. Lauth M, Bergstrom A, Shimokawa T, Toftgard R. 2007. Inhibition of GLI-mediated transcription and tumor cell growth by small-molecule antagonists. Proc Natl Acad Sci USA 104:8455-8460.
20. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA. 2006. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9:391-403.
21. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. 2006. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:67.
22. Louro ID, Bailey EC, Li X, South LS, McKie-Bell PR, Yoder BK, Huang CC, Johnson MR, Hill AE, Johnson RL, Ruppert JM. 2002. Comparative gene expression profile analysis of GLI and c-MYC in an epithelial model of malignant transformation. Cancer Res 62:5867.
23. Mischel PS, Cloughesy TF. 2003. Targeted molecular therapy of GBM. Brain Pathol 13:52-61.
24. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. 2006. VEGF receptor signalling-In control of vascular function. Nat Rev Mol Cell Biol 7:359-371.
25. Parathath SR, Mainwaring LA, Fernandez LA, Campbell DO, Kenney AM. 2008. Insulin receptor substrate 1 is an effector of sonic hedgehog mitogenic signaling in cerebellar neural precursors. Development 135:3291-3300.
26. Reardon DA, Wen PY, Desjardins A, Batchelor TT, Vredenburgh JJ. 2008. Glioblastoma multiforme: An emerging paradigm of anti-VEGF therapy. Expert Opin Biol Ther 8:541-553.
27. Rininsland F, Johnson TR, Chernicky CL, Schulze E, Burfeind P, Ilan J. 1997. Suppression of insulin-like growth factor type I receptor by a triple-helix strategy inhibits IGF-I transcription and tumorigenic potential of rat C6 glioblastoma cells. Proc Natl Acad Sci USA 94:5854-5859.
28. Salmaggi A, Boiardi A, Gelati M, Russo A, Calatozzolo C, Ciusani E, Sciacca FL, Ottolina A, Parati EA, La Porta C, Alessandri G, Marras C, Croci D, De Rossi M. 2006. Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia 54:850-860.
29. Samani AA, Yakar S, LeRoith D, Brodt P. 2007. The role of the IGF system in cancer growth and metastasis: Overview and recent insights. Endocr Rev 28:20-47.
30. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. 2004. Identification of human brain tumour initiating cells. Nature 432:396-401.
31. Soroceanu L, Kharbanda S, Chen R, Soriano RH, Aldape K, Misra A, Zha J, Forrest WF, Nigro JM, Modrusan Z, Feuerstein BG, Phillips HS. 2007. Identification of IGF2 signaling through phosphoinositide-3-kinase regulatory subunit 3 as a growth-promoting axis in glioblastoma. Proc Natl Acad Sci USA 104:3466-3471.
32. Stecca B, Ruiz i Altaba A. 2005. Brain as a paradigm of organ growth: Hedgehog-Gli signaling in neural stem cells and brain tumors. J Neurobiol 64:476-490.
33. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO. 2005. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996.
34. Woods SA, McGlade CJ, Guha A. 2002. Phosphatidylinositol 3'-kinase and MAPK/ERK kinase 1/2 differentially regulate expression of vascular endothelial growth factor in human malignant astrocytoma cells. Neuro-Oncol 4:242-252.
35. Yoon JW, Kita Y, Frank DJ, Majewski RR, Konicek BA, Nobrega MA, Jacob H, Walterhouse D, Iannaccone P. 2002. Gene expression profiling leads to identification of GLI1-binding elements in target genes and a role for multiple downstream pathways in GLI1-induced cell transformation. J Biol Chem 277:5548-5555.
36. Zheng X, Shen G, Yang X, Liu W. 2007. Most C6 cells are cancer stem cells: Evidence from clonal and population analyses. Cancer Res 67:3691-3697.