Olig2-Dependent Reciprocal Shift in PDGF and EGF Receptor Signaling Regulates Tumor Phenotype and Mitotic Growth in Malignant Glioma

Cancer Cell

Volumn 29, Issue 5, 2016, Pages 669-683

  Lu, Fanghui ^a,b   Chen, Ying ^c   Zhao, Chuntao ^b   Wang, Haibo ^b   He, Danyang ^d   Xu, Lingli ^b   Wang, Jincheng ^b   He, Xuelian ^b   Deng, Yaqi ^b   Lu, Ellen E ^b   Liu, Xue ^c   Verma, Ravinder ^b   Bu, Hong ^a   Drissi, Rachid ^b   Fouladi, Maryam ^b   Stemmer Rachamimov, Anat O ^e   Burns, Dennis ^d   Xin, Mei ^b   Rubin, Joshua B ^f   Bahassi, El Mustapha ^g   Canoll, Peter ^h   Holland, Eric C ⁱ   Lu, Q Richard ^b,j   more..

^a SICHUAN UNIVERSITY   (China)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c XIAMEN UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^h NewYork Presbyterian Hospital   (United States)

ⁱ UNIVERSITY OF WASHINGTON   (United States)

^j CHILDREN S HOSPITAL OF FUDAN UNIVERSITY   (China)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN 20; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; KI 67 ANTIGEN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR A; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE PIM 1; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR ALPHA; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOLUMINESCENCE; CANCER GROWTH; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL GROWTH; CELL PROLIFERATION; CELL SELF-RENEWAL; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; MACROGLIA; MITOSIS; MOUSE; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; WHITE MATTER; 129 MOUSE; ANIMAL; ASTROCYTE; C57BL MOUSE; CELL TRANSFORMATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; KNOCKOUT MOUSE; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL ANALYSIS; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PHENOTYPE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; SURVIVAL ANALYSIS;

EID: 84975263198     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2016.03.027     Document Type: Article

References (37)

1. 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.
2. Bhat K.P., Balasubramaniyan V., Vaillant B., Ezhilarasan R., Hummelink K., Hollingsworth F., Wani K., Heathcock L., James J.D., Goodman L.D., et al. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell 2013, 24:331-346.
3. Brennan C.W., Verhaak R.G., McKenna A., Campos B., Noushmehr H., Salama S.R., Zheng S., Chakravarty D., Sanborn J.Z., Berman S.H., et al. The somatic genomic landscape of glioblastoma. Cell 2013, 155:462-477.
4. Cai J., Chen Y., Cai W.H., Hurlock E.C., Wu H., Kernie S.G., Parada L.F., Lu Q.R. A crucial role for Olig2 in white matter astrocyte development. Development 2007, 134:1887-1899.
5. 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.
6. Cataldo V.D., Gibbons D.L., Perez-Soler R., Quintas-Cardama A. Treatment of non-small-cell lung cancer with erlotinib or gefitinib. N. Engl. J. Med. 2011, 364:947-955.
7. Cancer Genome Atlas Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455:1061-1068.
8. 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.
9. Friedmann-Morvinski D., Bushong E.A., Ke E., Soda Y., Marumoto T., Singer O., Ellisman M.H., Verma I.M. Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 2012, 338:1080-1084.
10. Glasgow S.M., Zhu W., Stolt C.C., Huang T.W., Chen F., LoTurco J.J., Neul J.L., Wegner M., Mohila C., Deneen B. Mutual antagonism between Sox10 and NFIA regulates diversification of glial lineages and glioma subtypes. Nat. Neurosci. 2014, 17:1322-1329.
11. Hayden E.C. Genomics boosts brain-cancer work. Nature 2010, 463:278.
12. Jansen M., Yip S., Louis D.N. Molecular pathology in adult gliomas: diagnostic, prognostic, and predictive markers. Lancet Neurol. 2010, 9:717-726.
13. Johnson B.E., Mazor T., Hong C., Barnes M., Aihara K., McLean C.Y., Fouse S.D., Yamamoto S., Ueda H., Tatsuno K., et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 2014, 343:189-193.
14. Joseph N.M., Phillips J., Dahiya S., Felicella M., Tihan T., Brat D.J., Perry A. Diagnostic implications of IDH1-R132H and OLIG2 expression patterns in rare and challenging glioblastoma variants. Mod. Pathol. 2013, 26:315-326.
15. Lei L., Sonabend A.M., Guarnieri P., Soderquist C., Ludwig T., Rosenfeld S., Bruce J.N., Canoll P. Glioblastoma models reveal the connection between adult glial progenitors and the proneural phenotype. PLoS One 2011, 6:e20041.
16. Ligon K.L., Alberta J.A., Kho A.T., Weiss J., Kwaan M.R., Nutt C.L., Louis D.N., Stiles C.D., Rowitch D.H. The oligodendroglial lineage marker OLIG2 is universally expressed in diffuse gliomas. J. Neuropathol. Exp. Neurol. 2004, 63:499-509.
17. Ligon K.L., Huillard E., Mehta S., Kesari S., Liu H., Alberta J.A., Bachoo R.M., Kane M., Louis D.N., Depinho R.A., et al. Olig2-regulated lineage-restricted pathway controls replication competence in neural stem cells and malignant glioma. Neuron 2007, 53:503-517.
18. Liu C., Sage J.C., Miller M.R., Verhaak R.G., Hippenmeyer S., Vogel H., Foreman O., Bronson R.T., Nishiyama A., Luo L., et al. Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 2011, 146:209-221.
19. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 2002, 109:75-86.
20. Meacham C.E., Morrison S.J. Tumour heterogeneity and cancer cell plasticity. Nature 2013, 501:328-337.
21. Mehta S., Huillard E., Kesari S., Maire C.L., Golebiowski D., Harrington E.P., Alberta J.A., Kane M.F., Theisen M., Ligon K.L., et al. The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma. Cancer Cell 2011, 19:359-371.
22. Meijer D.H., Sun Y., Liu T., Kane M.F., Alberta J.A., Adelmant G., Kupp R., Marto J.A., Rowitch D.H., Nakatani Y., et al. An amino terminal phosphorylation motif regulates intranuclear compartmentalization of Olig2 in neural progenitor cells. J. Neurosci. 2014, 34:8507-8518.
23. Nie Z., Hu G., Wei G., Cui K., Yamane A., Resch W., Wang R., Green D.R., Tessarollo L., Casellas R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012, 151:68-79.
24. Noah J.W., Severson W., Noah D.L., Rasmussen L., White E.L., Jonsson C.B. A cell-based luminescence assay is effective for high-throughput screening of potential influenza antivirals. Antiviral Res. 2007, 73:50-59.
25. Ohgaki H., Kleihues P. Epidemiology and etiology of gliomas. Acta Neuropathol. 2005, 109:93-108.
26. Ozawa T., Riester M., Cheng Y.K., Huse J.T., Squatrito M., Helmy K., Charles N., Michor F., Holland E.C. Most human non-GCIMP glioblastoma subtypes evolve from a common proneural-like precursor glioma. Cancer Cell 2014, 26:288-300.
27. Persson A.I., Petritsch C., Swartling F.J., Itsara M., Sim F.J., Auvergne R., Goldenberg D.D., Vandenberg S.R., Nguyen K.N., Yakovenko S., et al. Non-stem cell origin for oligodendroglioma. Cancer Cell 2010, 18:669-682.
28. Schonberg D.L., Lubelski D., Miller T.E., Rich J.N. Brain tumor stem cells: molecular characteristics and their impact on therapy. Mol. Aspects Med. 2014, 39:82-101.
29. Sonabend A.M., Bansal M., Guarnieri P., Lei L., Amendolara B., Soderquist C., Leung R., Yun J., Kennedy B., Sisti J., et al. The transcriptional regulatory network of proneural glioma determines the genetic alterations selected during tumor progression. Cancer Res. 2014, 74:1440-1451.
30. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
31. Suva M.L., Rheinbay E., Gillespie S.M., Patel A.P., Wakimoto H., Rabkin S.D., Riggi N., Chi A.S., Cahill D.P., Nahed B.V., et al. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 2014, 157:580-594.
32. Venkatesh H.S., Johung T.B., Caretti V., Noll A., Tang Y., Nagaraja S., Gibson E.M., Mount C.W., Polepalli J., Mitra S.S., et al. Neuronal activity promotes glioma growth through Neuroligin-3 secretion. Cell 2015, 161:803-816.
33. Verhaak R.G., 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.
34. Wang J., Wang H., Li Z., Wu Q., Lathia J.D., McLendon R.E., Hjelmeland A.B., Rich J.N. c-Myc is required for maintenance of glioma cancer stem cells. PLoS One 2008, 3:e3769.
35. Yu Y., Chen Y., Kim B., Wang H., Zhao C., He X., Liu L., Liu W., Wu L.M., Mao M., et al. Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 2013, 152:248-261.
36. Yue T., Xian K., Hurlock E., Xin M., Kernie S.G., Parada L.F., Lu Q.R. A critical role for dorsal progenitors in cortical myelination. J. Neurosci. 2006, 26:1275-1280.
37. Zhu X., Zuo H., Maher B.J., Serwanski D.R., LoTurco J.J., Lu Q.R., Nishiyama A. Olig2-dependent developmental fate switch of NG2 cells. Development 2012, 139:2299-2307.