Temozolomide resistance in glioblastoma occurs by miRNA-9-targeted PTCH1, independent of sonic hedgehog level

Oncotarget

Volumn 6, Issue 2, 2015, Pages 1190-1201

  Munoz, Jessian L ^a,b   Rodriguez Cruz, Vivian ^c   Ramkissoon, Shakti H ^d   Ligon, Keith L ^d   Greco, Steven J ^a   Rameshwar, Pranela ^a,b  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b The State University of New Jersey   (United States)

^c UNIVERSITY OF PUERTO RICO AT CAYEY   (Puerto Rico)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Glioblastoma; MicroRNA 9; P gp; PTCH; Temozolomide

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CASPASE 3; DICER; MESSENGER RNA; MICRORNA 9; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN PATCHED 1; SMOOTHENED PROTEIN; TEMOZOLOMIDE; VISMODEGIB; 3' UNTRANSLATED REGION; ABC TRANSPORTER; ABCB1 PROTEIN, HUMAN; ABCG2 PROTEIN, HUMAN; ALKYLATING AGENT; CELL SURFACE RECEPTOR; DACARBAZINE; MICRORNA; MIRN92 MICRORNA, HUMAN; MULTIDRUG RESISTANCE PROTEIN; PATCHED RECEPTORS; SHH PROTEIN, HUMAN; SONIC HEDGEHOG PROTEIN; TUMOR PROTEIN;

ARTICLE; CANCER RESISTANCE; CELL DEATH; CONTROLLED STUDY; DRUG SENSITIVITY; GENE REPRESSION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; GLIOMA CELL; HUMAN; HUMAN CELL; SIGNAL TRANSDUCTION; SONIC HEDGEHOG SIGNALING; TUMOR RECURRENCE; 3' UNTRANSLATED REGION; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN TUMOR; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; MICRORNAS; NEOPLASM PROTEINS; P-GLYCOPROTEINS; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84921824931     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2778     Document Type: Article

References (36)

1. Gaviani P, Silvani A, Lamperti E, Botturi A, Fariselli L, Simonetti G, Ferrari D, Salmaggi A. Rechallenge with temozolomide in recurrent glioma. Neurol Sci. 2011; 32:247-249.
2. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, Colman H, Chakravarti A, Pugh S, Won M, Jeraj R, Brown PD, Jaeckle KA, Schiff D, Stieber VW, Brackman DG, Werner-Wasik M, Tremont-Lukats IW, Sulman EP, Aldape KD, Curran WJ, Mehta MP. A Randomized Trial of Bevacizumab for Newly Diagnosed Glioblastoma. N Engl J Med. 2014; 370:699-708.
3. Mimeault M, Batra SK. Complex Oncogenic Signaling Networks Regulate Brain Tumor-Initiating Cells and Their Progenies: Pivotal Roles of Wild-Type EGFR, EGFRvIII Mutant and Hedgehog Cascades and Novel Multitargeted Therapies. Brain Pathol. 2011; 21:479-500.
4. McDowell KA, Riggins GJ, Gallia GL. Targeting the AKT pathway in glioblastoma. Curr Pharm Des. 2011; 17:2411-2420.
5. Bae GU, Domene S, Roessler E, Schachter K, Kang JS, Muenke M, Krauss RS. Mutations in CDON, Encoding a Hedgehog Receptor, Result in Holoprosencephaly and Defective Interactions with Other Hedgehog Receptors. Am J Hum Genet. 2011; 89:231-240.
6. Abe Y, Kita Y, Niikura T. Mammalian Gup1, a homolog of Saccharomyces cerevisiae glycerol uptake/transporter-1, acts as a negative regulator for N-terminal palmitoylation of Sonic-áhedgehog. FEBS J. 2008; 275:318-331.
7. Grover VK, Valadez JG, Bowman AB, Cooper MK. Lipid Modifications of Sonic Hedgehog Ligand Dictate Cellular Reception and Signal Response. PLoS ONE. 2011; 6:e21353.
8. Rahnama F, Shimokawa T, Lauth M, Finta C, Kogerman P, Teglund S, Toftgard R, Zaphiropoulos PG. Inhibition of GLI1 gene activation by Patched1. Biochem J. 2006; 394:19-26.
9. Thomas ZI, Gibson W, Sexton JZ, Aird KM, Ingram SM, Aldrich A, Lyerly HK, Devi GR, Williams KP. Targeting GLI1 expression in human inflammatory breast cancer cells enhances apoptosis and attenuates migration. Br J Cancer. 2011; 104:1575-1586.
10. Bartel DP. MicroRNAs: Target Recognition and Regulatory Functions. Cell. 2009; 136:215-233.
11. Cho WC. Exploiting the therapeutic potential of microRNAs in human cancer. Expert Opin Ther Targets. 2012; 16:345-350.
12. Ebert M, Sharp P. Roles for MicroRNAs in Conferring Robustness to Biological Processes. Cell. 2012; 149:515-524.
13. Feng W, Feng Y. MicroRNAs in neural cell development and brain diseases. Sci China Life Sci. 2011; 54:1103-1112.
14. Ferretti E, De Smaele E, Miele E, Laneve P, Po A, Pelloni M, Paganelli A, Di Marcotullio L, Caffarelli E, Screpanti I, Bozzoni I, Alberto G. Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 2008; 27:2616-2627.
15. Chen P, Price C, Li Z, Li Y, Cao D, Wiley A, He C, Gurbuxani S, Kunjamma RB, Huang H, Jiang X, Arnovitz S, Xo M, Hong GM, Elkahloun AG, Neilly MB, Wunderlich M, Larson RA, Le Beau MM, Mulloy JC, Liu PR, Rowley JD, Chen J. miR-9 is an essential oncogenic microRNA specifically overexpressed in mixed lineage leukemia-rearranged leukemia. Proc Natl Acad Sci. 2013; 110:11511-11516.
16. Yoo AS, Staahl BT, Chen L, Crabtree GR. MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature. 2009; 460:642-646.
17. Shibata M, Nakao H, Kiyonari H, Abe T, Aizawa S. MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J Neurosci. 2011; 31:3407-3422.
18. Munoz JL, Bliss SA, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P. Delivery of Functional Anti-miR-9 by Mesenchymal Stem Cell-derived Exosomes to Glioblastoma Multiforme Cells Conferred Chemosensitivity. Mol Ther Nucleic Acids. 2013; 2:e126.
19. Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL. The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J Neurosci. 2008; 28:14341-14346.
20. Gjorgieva D, Zaidman N, Bosnakovski D. Mesenchymal stem cells for anti-cancer drug delivery. Recent Pat Anticancer Drug Discov. 2013; 8:310-318.
21. Martinez-Quintanilla J, Bhere D, Heidari P, He D, Mahmood U, Shah K. Therapeutic Efficacy and Fate of Bimodal Engineered Stem Cells in Malignant Brain Tumors. STEM CELLS. 2013; 31:1706-1714.
22. Metz MZ, Gutova M, Lacey SF, Abramyants Y, Vo T, Gilchrist M, Tirughana R, Ghoda LY, Barish ME, Brown CE, Najbauer J, Potter PM, Portnow J, Synold TW, Aboody KS. Neural Stem Cell-Mediated Delivery of Irinotecan-Activating Carboxylesterases to Glioma: Implications for Clinical Use. Stem Cells Transl Med. 2013; 2:983-992.
23. Bijlsma MF, Roelink H. Non-cell-autonomous signaling by Shh in tumors: challenges and opportunities for therapeutic targets. Expert Opin Ther Targets. 2010; 14:693-702.
24. Ulasov IV, Nandi S, Dey M, Sonabend AM, Lesniak MS. Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy. Mol Med. 2011; 17:103-112.
25. Moraes RC, Zhang X, Harrington N, Fung JY, Wu MF, Hilsenbeck SG, Allred DC, Lewis MT. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development. 2007; 134:1231-1242.
26. Munoz JL, Rodriguez-Cruz V, Greco SJ, Nagula V, Scotto KW, Rameshwar P. Temozolomide Induces the Production of Epidermal Growth Factor to Regulate MDR1 Expression in Glioblastoma Cells. Mol Cancer Ther. 2014; 13:2399-2411.
27. Incardona JP, Lee JH, Robertson CP, Enga K, Kapur RP, Roelink H. Receptor-mediated endocytosis of soluble and membrane-tethered Sonic hedgehog by Patched-1. Proc Natl Acad Sci. 2000; 97:12044-12049.
28. Anglesio MS, Wang Y, Yang W, Senz J, Wan A, Heravi-Moussavi A, Salamanca C, Maines-Bandiera S, Huntsman DG, Morin GB. Cancer-associated somatic DICER1 hotspot mutations cause defective miRNA processing and reverse-strand expression bias to predominantly mature 3p strands through loss of 5p strand cleavage. J Pathol. 2013; 229:400-409.
29. Laneve P, Gioia U, Andriotto A, Moretti F, Bozzoni I, Caffarelli E. A minicircuitry involving REST and CREB controls miR-9-2 expression during human neuronal differentiation. Nucleic Acids Res. 2010; 38:6895-6905.
30. Coolen M, Thieffry D, Drivenes O, Becker T, Bally-Cuif L. miR-9 Controls the Timing of Neurogenesis through the Direct Inhibition of Antagonistic Factors. Dev Cell. 2012; 22:1052-1064.
31. Sims-Mourtada J, Izzo JG, Ajani J, Chao KSC. Sonic Hedgehog promotes multiple drug resistance by regulation of drug transport. Oncogene. 2007; 26:5674-5679.
32. Stanton BZ, Peng LF. Small-molecule modulators of the Sonic Hedgehog signaling pathway. Mol Biosyst. 2010; 6:44-54.
33. Zhang Y, Laterra J, Pomper MG. Hedgehog pathway inhibitor HhAntag691 is a potent inhibitor of ABCG2/BCRP and ABCB1/Pgp. Neoplasia. 2009; 11:96-101.
34. Aleynik A, Gernavage K, Mourad Y, Sherman L, Liu K, Gubenko Y, Rameshwar P. Stem cell delivery of therapies for brain disorders. Clin Transl Med. 2014; 3:24.
35. Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA, Greco SJ, Bryan M, Patel PS, Rameshwar P. Gap Junction-Mediated Import of MicroRNA from Bone Marrow Stromal Cells Can Elicit Cell Cycle Quiescence in Breast Cancer Cells. Cancer Res. 2011; 71:1550-1560.
36. Park JM, Munoz JL, Won BW, Bliss SA, Greco SJ, Patel SA, Kandouz M, Rameshwar P. Exogenous CXCL12 activates protein kinase C to phosphorylate connexin 43 for gap junctional intercellular communication among confluent breast cancer cells. Cancer Lett. 2013; 331:84-91.