InVivo RNAi Screen for BMI1 Targets Identifies TGF-β/BMP-ER Stress Pathways as Key Regulators of Neural- and Malignant Glioma-Stem Cell Homeostasis

Cancer Cell

Volumn 23, Issue 5, 2013, Pages 660-676

  Gargiulo, Gaetano ^a   Cesaroni, Matteo ^b   Serresi, Michela ^a   deVries, Nienke ^a   Hulsman, Danielle ^a   Bruggeman, SophiaW ^a   Lancini, Cesare ^a   VanLohuizen, Maarten ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; BMI1 PROTEIN; BONE MORPHOGENETIC PROTEIN; RNA; TRANSFORMING GROWTH FACTOR BETA; ATF3 PROTEIN, HUMAN; BMI1 PROTEIN, MOUSE; CBX7 PROTEIN, HUMAN; ONCOPROTEIN;

ARTICLE; CHROMATIN; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GLIOBLASTOMA; GLIOMA CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VIVO STUDY; NEURAL STEM CELL; PRIORITY JOURNAL; RNA INTERFERENCE; ANIMAL; CANCER STEM CELL; CELL NUCLEUS; CHEMISTRY; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL NUCLEUS; CHROMATIN; ENDOPLASMIC RETICULUM STRESS; GLIOBLASTOMA; HOMEOSTASIS; HUMANS; MICE; NEOPLASTIC STEM CELLS; NEURAL STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 1; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

MLCS; MLOWN;

EID: 84877836210     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.03.030     Document Type: Article

References (51)

1. Abdouh M., Facchino S., Chatoo W., Balasingam V., Ferreira J., Bernier G. BMI1 sustains human glioblastoma multiforme stem cell renewal. J.Neurosci. 2009, 29:8884-8896.
2. Anido J., Sáez-Borderías A., Gonzàlez-Juncà A., Rodón L., Folch G., Carmona M.A., Prieto-Sánchez R.M., Barba I., Martínez-Sáez E., Prudkin L., et al. TGF-β receptor inhibitors target the CD44(high)/Id1(high) glioma-initiating cell population in human glioblastoma. Cancer Cell 2010, 18:655-668.
3. Bachoo R.M., Maher E.A., Ligon K.L., Sharpless N.E., Chan S.S., You M.J., Tang Y., DeFrances J., Stover E., Weissleder R., et al. Epidermal growth factor receptor and Ink4a/Arf: convergent mechanisms governing terminal differentiation and transformation along the neural stem cell to astrocyte axis. Cancer Cell 2002, 1:269-277.
4. Barrett L.E., Granot Z., Coker C., Iavarone A., Hambardzumyan D., Holland E.C., Nam H.-S., Benezra R. Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 2012, 21:11-24.
5. Biddie S.C., John S., Sabo P.J., Thurman R.E., Johnson T.A., Schiltz R.L., Miranda T.B., Sung M.-H., Trump S., Lightman S.L., et al. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol. Cell 2011, 43:145-155.
6. Bric A., Miething C., Bialucha C.U., Scuoppo C., Zender L., Krasnitz A., Xuan Z., Zuber J., Wigler M., Hicks J., et al. Functional identification of tumor-suppressor genes through an invivo RNA interference screen in a mouse lymphoma model. Cancer Cell 2009, 16:324-335.
7. Bruggeman S.W.M., Valk-Lingbeek M.E., van der Stoop P.P.M., Jacobs J.J.L., Kieboom K., Tanger E., Hulsman D., Leung C., Arsenijevic Y., Marino S., van Lohuizen M. Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev. 2005, 19:1438-1443.
8. Bruggeman S.W.M., Hulsman D., Tanger E., Buckle T., Blom M., Zevenhoven J., van Tellingen O., van Lohuizen M. Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell 2007, 12:328-341.
9. Bruggeman S.W.M., Hulsman D., van Lohuizen M. Bmi1 deficient neural stem cells have increased integrin dependent adhesion to self-secreted matrix. Biochim. Biophys. Acta 2009, 1790:351-360.
10. Büschges R., Weber R.G., Actor B., Lichter P., Collins V.P., Reifenberger G. Amplification and expression of cyclin D genes (CCND1, CCND2 and CCND3) in human malignant gliomas. Brain Pathol. 1999, 9:435-442.
11. Cahoy J.D., Emery B., Kaushal A., Foo L.C., Zamanian J.L., Christopherson K.S., Xing Y., Lubischer J.L., Krieg P.A., Krupenko S.A., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J.Neurosci. 2008, 28:264-278.
12. Carro M.S., Lim W.K., Alvarez M.J., Bollo R.J., Zhao X., Snyder E.Y., Sulman E.P., Anne S.L., Doetsch F., Colman H., et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 2010, 463:318-325.
13. Chirasani S.R., Sternjak A., Wend P., Momma S., Campos B., Herrmann I.M., Graf D., Mitsiadis T., Herold-Mende C., Besser D., et al. Bone morphogenetic protein-7 release from endogenous neural precursor cells suppresses the tumourigenicity of stem-like glioblastoma cells. Brain 2010, 133:1961-1972.
14. Facchino S., Abdouh M., Chatoo W., Bernier G. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J.Neurosci. 2010, 30:10096-10111.
15. Fellmann C., Zuber J., McJunkin K., Chang K., Malone C.D., Dickins R.A., Xu Q., Hengartner M.O., Elledge S.J., Hannon G.J., Lowe S.W. Functional identification of optimized RNAi triggers using a massively parallel sensor assay. Mol. Cell 2011, 41:733-746.
16. Forzati F., Federico A., Pallante P., Abbate A., Esposito F., Malapelle U., Sepe R., Palma G., Troncone G., Scarfò M., et al. CBX7 is a tumor suppressor in mice and humans. J.Clin. Invest. 2012, 122:612-623.
17. Gargiulo G., Levy S., Bucci G., Romanenghi M., Fornasari L., Beeson K.Y., Goldberg S.M., Cesaroni M., Ballarini M., Santoro F., et al. NA-Seq: a discovery tool for the analysis of chromatin structure and dynamics during differentiation. Dev. Cell 2009, 16:466-481.
18. Holland E.C., Hively W.P., DePinho R.A., Varmus H.E. A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev. 1998, 12:3675-3685.
19. Huang X., Li X., Guo B. KLF6 induces apoptosis in prostate cancer cells through up-regulation of ATF3. J.Biol. Chem. 2008, 283:29795-29801.
20. Inoue K., Zama T., Kamimoto T., Aoki R., Ikeda Y., Kimura H., Hagiwara M. TNFalpha-induced ATF3 expression is bidirectionally regulated by the JNK and ERK pathways in vascular endothelial cells. Genes Cells 2004, 9:59-70.
21. Kang Y., Chen C.-R., Massagué J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 2003, 11:915-926.
22. Kimmelman A.C., Qiao R.F., Narla G., Banno A., Lau N., Bos P.D., Nuñez Rodriguez N., Liang B.C., Guha A., Martignetti J.A., et al. Suppression of glioblastoma tumorigenicity by the Kruppel-like transcription factor KLF6. Oncogene 2004, 23:5077-5083.
23. Kioussi C., Briata P., Baek S.H., Rose D.W., Hamblet N.S., Herman T., Ohgi K.A., Lin C., Gleiberman A., Wang J., et al. Identification of a Wnt/Dvl/beta-Catenin -> Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 2002, 111:673-685.
24. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 2009, 32:149-184.
25. Lee J., Son M.J., Woolard K., Donin N.M., Li A., Cheng C.H., Kotliarova S., Kotliarov Y., Walling J., Ahn S., et al. Epigenetic-mediated dysfunction of the bone morphogenetic protein pathway inhibits differentiation of glioblastoma-initiating cells. Cancer Cell 2008, 13:69-80.
26. Leung C., Lingbeek M., Shakhova O., Liu J., Tanger E., Saremaslani P., Van Lohuizen M., Marino S. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004, 428:337-341.
27. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., García-Verdugo J.M., Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 2000, 28:713-726.
28. Meacham C.E., Ho E.E., Dubrovsky E., Gertler F.B., Hemann M.T. Invivo RNAi screening identifies regulators of actin dynamics as key determinants of lymphoma progression. Nat. Genet. 2009, 41:1133-1137.
29. Molofsky A.V., Pardal R., Iwashita T., Park I.-K., Clarke M.F., Morrison S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003, 425:962-967.
30. Molofsky A.V., Slutsky S.G., Joseph N.M., He S., Pardal R., Krishnamurthy J., Sharpless N.E., Morrison S.J. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 2006, 443:448-452.
31. Nam H.-S., Benezra R. High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 2009, 5:515-526.
32. Ohm J.E., McGarvey K.M., Yu X., Cheng L., Schuebel K.E., Cope L., Mohammad H.P., Chen W., Daniel V.C., Yu W., et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 2007, 39:237-242.
33. Park D.M., Sathornsumetee S., Rich J.N. Medical oncology: treatment and management of malignant gliomas. Nat. Rev. Clin. Oncol. 2010, 7:75-77.
34. Pietersen A.M., Evers B., Prasad A.A., Tanger E., Cornelissen-Steijger P., Jonkers J., van Lohuizen M. Bmi1 regulates stem cells and proliferation and differentiation of committed cells in mammary epithelium. Curr. Biol. 2008, 18:1094-1099.
35. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580.
36. Schlesinger Y., Straussman R., Keshet I., Farkash S., Hecht M., Zimmerman J., Eden E., Yakhini Z., Ben-Shushan E., Reubinoff B.E., et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat. Genet. 2007, 39:232-236.
37. Scott C.L., Gil J., Hernando E., Teruya-Feldstein J., Narita M., Martínez D., Visakorpi T., Mu D., Cordon-Cardo C., Peters G., et al. Role of thechromobox protein CBX7 in lymphomagenesis. Proc. Natl. Acad. Sci. USA 2007, 104:5389-5394.
38. Seoane J. TGFbeta and cancer initiating cells. Cell Cycle 2009, 8:3787-3788.
39. Sparmann A., van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 2006, 6:846-856.
40. Stock K., Kumar J., Synowitz M., Petrosino S., Imperatore R., Smith E.S.J., Wend P., Purfürst B., Nuber U.A., Gurok U., et al. Neural precursor cells induce cell death of high-grade astrocytomas through stimulation of TRPV1. Nat. Med. 2012, Published online July 22, 2012. 10.1038/nm.2827.
41. Sun Y., Kong W., Falk A., Hu J., Zhou L., Pollard S., Smith A. CD133 (Prominin) negative human neural stem cells are clonogenic and tripotent. PLoS ONE 2009, 4:e5498.
42. Taketani K., Kawauchi J., Tanaka-Okamoto M., Ishizaki H., Tanaka Y., Sakai T., Miyoshi J., Maehara Y., Kitajima S. Key role of ATF3 in p53-dependent DR5 induction upon DNA damage of human colon cancer cells. Oncogene 2011, 31:2210-2221.
43. Thompson M.R., Xu D., Williams B.R.G. ATF3 transcription factorand its emerging roles in immunity and cancer. J.Mol. Med. 2009, 87:1053-1060.
44. van der Lugt N.M., Domen J., Linders K., van Roon M., Robanus-Maandag E., te Riele H., van der Valk M., Deschamps J., Sofroniew M., van Lohuizen M., et al. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 1994, 8:757-769.
45. Veeriah S., Brennan C., Meng S., Singh B., Fagin J.A., Solit D.B., Paty P.B., Rohle D., Vivanco I., Chmielecki J., et al. The tyrosine phosphatase PTPRD is a tumor suppressor that is frequently inactivated and mutated in glioblastoma and other human cancers. Proc. Natl. Acad. Sci. USA 2009, 106:9435-9440.
46. Verhaak R.G.W., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110. Cancer Genome Atlas Research Network.
47. Watabe T., Miyazono K. Roles of TGF-beta family signaling in stem cell renewal and differentiation. Cell Res. 2009, 19:103-115.
48. Widschwendter M., Fiegl H., Egle D., Mueller-Holzner E., Spizzo G., Marth C., Weisenberger D.J., Campan M., Young J., Jacobs I., Laird P.W. Epigenetic stem cell signature in cancer. Nat. Genet. 2007, 39:157-158.
49. Wimmer K., Zhu Xx X.-X., Rouillard J.M., Ambros P.F., Lamb B.J., Kuick R., Eckart M., Weinhäusl A., Fonatsch C., Hanash S.M. Combined restriction landmark genomic scanning and virtual genome scans identify a novel human homeobox gene, ALX3, that is hypermethylated in neuroblastoma. Genes Chromosomes Cancer 2002, 33:285-294.
50. Wu X., Nguyen B.-C., Dziunycz P., Chang S., Brooks Y., Lefort K., Hofbauer G.F.L., Dotto G.P. Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature 2010, 465:368-372.
51. Yan L., Della Coletta L., Powell K.L., Shen J., Thames H., Aldaz C.M., MacLeod M.C. Activation of the canonical Wnt/β-catenin pathway in ATF3-induced mammary tumors. PLoS ONE 2011, 6:e16515.