ABCG1 maintains high-grade glioma survival in vitro and in vivo

Oncotarget

Volumn 7, Issue 17, 2016, Pages 23416-23424

  Chen, Yi Hsien ^a   Cimino, Patrick J ^a   Luo, Jingqin ^a   Dahiya, Sonika ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Brain tumor; ER stress; Glioblastoma; Glioma stem cell

Indexed keywords

ABC TRANSPORTER G1; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; SHORT HAIRPIN RNA; ABCG1 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL GLIOBLASTOMA; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN EXPRESSION; ANIMAL; BRAIN TUMOR; C57BL MOUSE; CANCER GRADING; CASE CONTROL STUDY; CELL PROLIFERATION; DRUG SCREENING; FOLLOW UP; GLIOMA; METABOLISM; PATHOLOGY; SURVIVAL RATE; TUMOR CELL CULTURE;

ADULT; ANIMALS; APOPTOSIS; ATP BINDING CASSETTE TRANSPORTER, SUB-FAMILY G, MEMBER 1; BIOMARKERS, TUMOR; BRAIN NEOPLASMS; CASE-CONTROL STUDIES; CELL PROLIFERATION; FOLLOW-UP STUDIES; GLIOMA; HUMANS; MALE; MICE; MICE, INBRED C57BL; NEOPLASM GRADING; SURVIVAL RATE; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84966472214     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8030     Document Type: Article

References (46)

1. Kesari S, Schiff D, Henson JW, Muzikansky A, Gigas DC, Doherty L, Batchelor TT, Longtine JA, Ligon KL, Weaver S, Laforme A, Ramakrishna N, Black PM, et al. Phase II study of temozolomide, thalidomide, and celecoxib for newly diagnosed glioblastoma in adults. Neuro Oncol. 2008; 10:300-308.
2. Werner MH, Phuphanich S, Lyman GH. The increasing incidence of malignant gliomas and primary central nervous system lymphoma in the elderly. Cancer. 1995; 76:1634-1642.
3. Baumann F, Bjeljac M, Kollias SS, Baumert BG, Brandner S, Rousson V, Yonekawa Y, Bernays RL. Combined thalidomide and temozolomide treatment in patients with glioblastoma multiforme. J Neurooncol. 2004; 67:191-200.
4. Balasubramaniyan V, Vaillant B, Wang S, Gumin J, Butalid ME, Sai K, Mukheef F, Kim SH, Boddeke HW, Lang F, Aldape K, Sulman EP, Bhat KP, et al. Aberrant mesenchymal differentiation of glioma stem-like cells: implications for therapeutic targeting. Oncotarget. 2015. doi: 10.18632/oncotarget.5219.
5. Daniele S, Costa B, Zappelli E, Da Pozzo E, Sestito S, Nesi G, Campiglia P, Marinelli L, Novellino E, Rapposelli S, Martini C. Combined inhibition of AKT/mTOR and MDM2 enhances Glioblastoma Multiforme cell apoptosis and differentiation of cancer stem cells. Sci Rep. 2015; 5:9956.
6. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature. 2004; 432:396-401.
7. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003; 63:5821-5828.
8. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006; 5:67.
9. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW, Holland EC. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell. 2009; 4:226-235.
10. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006; 444:756-760.
11. Golebiewska A, Bougnaud S, Stieber D, Brons NH, Vallar L, Hertel F, Klink B, Schrock E, Bjerkvig R, Niclou SP. Side population in human glioblastoma is non-tumorigenic and characterizes brain endothelial cells. Brain. 2013; 136:1462-1475.
12. Wang N, Lan D, Chen W, Matsuura F, Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc Natl Acad Sci USA 2004; 101:9774-9779.
13. Tarling EJ, Edwards PA. ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc Natl Acad Sci USA. 2011; 108:19719-19724.
14. Klucken J, Buchler C, Orso E, Kaminski WE, Porsch-Ozcurumez M, Liebisch G, Kapinsky M, Diederich W, Drobnik W, Dean M, Allikmets R, Schmitz G. ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc Natl Acad Sci USA. 2000; 97:817-822.
15. Kennedy MA, Barrera GC, Nakamura K, Baldan A, Tarr P, Fishbein MC, Frank J, Francone OL, Edwards PA. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab. 2005; 1:121-131.
16. Chen YH, McGowan LD, Cimino PJ, Dahiya S, Leonard JR, Lee da Y, Gutmann DH. Mouse low-grade gliomas contain cancer stem cells with unique molecular and functional properties. Cell Rep. 2015; 10:1899-1912.
17. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, Alexe G, Lawrence M, O'Kelly M, 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.
18. Reilly KM, Loisel DA, Bronson RT, McLaughlin ME, Jacks T. Nf1;Trp53 mutant mice develop glioblastoma with evidence of strain-specific effects. Nat Genetics. 2000; 26:109-113.
19. Gursel DB, Connell-Albert YS, Tuskan RG, Anastassiadis T, Walrath JC, Hawes JJ, Amlin-Van Schaick JC, Reilly KM. Control of proliferation in astrocytoma cells by the receptor tyrosine kinase/PI3K/AKT signaling axis and the use of PI 103 and TCN as potential anti-astrocytoma therapies. Neuro Oncol. 2011; 13:610-621.
20. Ozawa T, Riester M, Cheng YK, Huse JT, Squatrito M, Helmy K, Charles N, Michor F, Holland EC. Most human non-GCIMP glioblastoma subtypes evolve from a common proneural-like precursor glioma. Cancer Cell. 2014; 26:288-300.
21. Network CGAR. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008; 455:1061-1068.
22. Banerjee S, Byrd JN, Gianino SM, Harpstrite SE, Rodriguez FJ, Tuskan RG, Reilly KM, Piwnica-Worms DR, Gutmann DH. The neurofibromatosis type 1 tumor suppressor controls cell growth by regulating signal transducer and activator of transcription-3 activity in vitro and in vivo. Cancer Res. 2010; 70:1356-1366.
23. Zemp FJ, McKenzie BA, Lun X, Maxwell L, Reilly KM, McFadden G, Yong VW, Forsyth PA. Resistance to oncolytic myxoma virus therapy in nf1(-/-)/trp53(-/-) syngeneic mouse glioma models is independent of anti-viral type-I interferon. PloS One. 2013; 8:e65801.
24. Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013; 32:805-818.
25. Li J, Lee AS. Stress induction of GRP78/BiP and its role in cancer. Curr Mol Med. 2006; 6:45-54.
26. Bajenaru ML, Hernandez MR, Perry A, Zhu Y, Parada LF, Garbow JR, Gutmann DH. Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res. 2003; 63:8573-8577.
27. Aleidi SM, Howe V, Sharpe LJ, Yang A, Rao G, Brown AJ, Gelissen IC. The E3-ubiquitin ligases, HUWE1 and NEDD4-1, are involved in the post-translational regulation of the ABCG1 and ABCG4 lipid transporters. J Biol Chem. 2015.
28. Zhang H, Nie W, Zhang X, Zhang G, Li Z, Wu H, Shi Q, Chen Y, Ding Z, Zhou X, Yu R. NEDD4-1 regulates migration and invasion of glioma cells through CNrasGEF ubiquitination in vitro. PloS One. 2013; 8:e82789.
29. Dai B, Pieper RO, Li D, Wei P, Liu M, Woo SY, Aldape KD, Sawaya R, Xie K, Huang S. FoxM1B regulates NEDD4-1 expression, leading to cellular transformation and full malignant phenotype in immortalized human astrocytes. Cancer Res. 2010; 70:2951-2961.
30. Zhang P, de Gooijer MC, Buil LC, Beijnen JH, Li G, van Tellingen O. ABCB1 and ABCG2 restrict the brain penetration of a panel of novel EZH2-Inhibitors. Int J Cancer. 2015; 137:2007-2018.
31. Lin F, de Gooijer MC, Roig EM, Buil LC, Christner SM, Beumer JH, Wurdinger T, Beijnen JH, van Tellingen O. ABCB1, ABCG2, and PTEN determine the response of glioblastoma to temozolomide and ABT-888 therapy. Clin Cancer Res. 2014; 20:2703-2713.
32. Shi L, Wang Z, Sun G, Wan Y, Guo J, Fu X. miR-145 inhibits migration and invasion of glioma stem cells by targeting ABCG2. Neuromolecular Med. 2014; 16:517-528.
33. Gong W, Wang Z, Wan Y, Shi L, Zhou Y. Downregulation of ABCG2 protein inhibits migration and invasion in U251 glioma stem cells. Neuroreport. 2014; 25:625-632.
34. Bleau AM, Huse JT, Holland EC. The ABCG2 resistance network of glioblastoma. Cell Cycle. 2009; 8:2936-2944.
35. Mittapalli RK, Chung AH, Parrish KE, Crabtree D, Halvorson KG, Hu G, Elmquist WF, Becher OJ. ABCG2 and ABCB1 limit the efficacy of dasatinib in a PDGF-B driven brainstem glioma model. Mol Cancer Ther. 2016.
36. Suzuki K, Gerelchuluun A, Hong Z, Sun L, Zenkoh J, Moritake T, Tsuboi K. Celecoxib enhances radiosensitivity of hypoxic glioblastoma cells through endoplasmic reticulum stress. Neuro Oncol. 2013; 15:1186-1199.
37. Liu AJ, Wang SH, Chen KC, Kuei HP, Shih YL, Hou SY, Chiu WT, Hsiao SH, Shih CM. Evodiamine, a plant alkaloid, induces calcium/JNK-mediated autophagy and calcium/mitochondria-mediated apoptosis in human glioblastoma cells. Chem Biol Interact. 2013; 205:20-28.
38. Johnson DR, Galanis E. Medical management of high-grade astrocytoma: current and emerging therapies. Semin Oncol. 2014; 41:511-522.
39. Ciechomska IA, Gabrusiewicz K, Szczepankiewicz AA, Kaminska B. Endoplasmic reticulum stress triggers autophagy in malignant glioma cells undergoing cyclosporine a-induced cell death. Oncogene. 2013; 32:1518-1529.
40. Cho HY, Wang W, Jhaveri N, Lee DJ, Sharma N, Dubeau L, Schonthal AH, Hofman FM, Chen TC. NEO212, temozolomide conjugated to perillyl alcohol, is a novel drug for effective treatment of a broad range of temozolomideresistant gliomas. Mol Cancer Ther. 2014; 13:2004-2017.
41. Booth L, Roberts JL, Cruickshanks N, Grant S, Poklepovic A, Dent P. Regulation of OSU-03012 toxicity by ER stress proteins, ER stress-inducing drugs. Mol Cancer Ther. 2014; 13:2384-2398.
42. Lee da Y, Yeh TH, Emnett RJ, White CR, Gutmann DH. Neurofibromatosis-1 regulates neuroglial progenitor proliferation and glial differentiation in a brain regionspecific manner. Genes Dev. 2010; 24:2317-2329.
43. Kaul A, Chen YH, Emnett RJ, Dahiya S, Gutmann DH. Pediatric glioma-associated KIAA1549:BRAF expression regulates neuroglial cell growth in a cell type-specific and mTOR-dependent manner. Genes Dev. 2012; 26:2561-2566.
44. Dasgupta B, Gutmann DH. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation in vitro and in vivo. J Neurosci. 2005; 25:5584-5594.
45. Gross S, Piwnica-Worms D. Real-time imaging of ligandinduced IKK activation in intact cells and in living mice. Nat Methods. 2005; 2:607-614.
46. Pong WW, Walker J, Wylie T, Magrini V, Luo J, Emnett RJ, Choi J, Cooper ML, Griffith M, Griffith OL, Rubin JB, Fuller GN, Piwnica-Worms D, et al. F11R is a novel monocyte prognostic biomarker for malignant glioma. PloS One. 2013; 8:e77571.