ZNF-Mediated Resistance to Imatinib Mesylate in Gastrointestinal Stromal Tumor

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Rink, Lori ^a   Ochs, Michael F ^b   Zhou, Yan ^a   von Mehren, Margaret ^a   Godwin, Andrew K ^c,d  

^a FOX CHASE CANCER CENTER   (United States)

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

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF KANSAS CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN SERUM ALBUMIN; IMATINIB; MESSENGER RNA; SMALL INTERFERING RNA; SOMATOMEDIN BINDING PROTEIN 2; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA2; TUMOR PROTEIN; ZINC FINGER PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CHEMOSENSITIZATION; CHROMOSOME 19P; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; GASTROINTESTINAL STROMAL TUMOR; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LIBRARY; GENE LOCATION; GENE LOCUS; GENE SILENCING; GENE TARGETING; GENETIC SCREENING; HUMAN; HUMAN CELL; NEDD9 GENE; RASSF8 GENE; REPRESSOR GENE; RNA INTERFERENCE; SOMATOMEDIN BINDING PROTEIN 2 GENE; TRANSCRIPTION FACTOR RUNX2 GENE; TRANSFORMING GROWTH FACTOR BETA2 GENE; TUMOR GENE; ZINC FINGER GENE; ZINC FINGER PROTEIN 431 GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANTINEOPLASTIC AGENTS; BENZAMIDES; CELL ADHESION MOLECULES; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GASTROINTESTINAL STROMAL TUMORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE LIBRARY; GENETIC LOCI; HUMANS; INDOLES; PHOSPHOPROTEINS; PIPERAZINES; PROTEIN KINASE INHIBITORS; PYRIMIDINES; PYRROLES; RNA, SMALL INTERFERING; TRANSFORMING GROWTH FACTOR BETA3; ZINC FINGERS;

EID: 84872845470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054477     Document Type: Article

References (66)

1. Corless CL, Heinrich MC, (2008) Molecular Pathobiology of Gastrointestinal Stromal Sarcomas. Annu Rev Pathol 3: 557-586.
2. Mazur MT, Clark HB, (1983) Gastric stromal tumors. Reappraisal of histogenesis. Am J Surg Pathol 7: 507-519.
3. Sircar K, Hewlett BR, Huizinga JD, Chorneyko K, Berezin I, et al. (1999) Interstitial cells of Cajal as precursors of gastrointestinal stromal tumors. Am J Surg Pathol 23: 377-389.
4. Kindblom LG, Remotti HE, Aldenborg F, Meis-Kindblom JM, (1998) Gastrointestinal pacemaker cell tumor (GIPACT): gastrointestinal stromal tumors show phenotypic characteristics of the interstitial cells of Cajal. Am J Pathol 152: 1259-1269.
5. Heinrich MC, Corless CL, (2005) Gastric GI stromal tumors (GISTs): the role of surgery in the era of targeted therapy. J Surg Oncol 90: 195-207; discussion 207.
6. Subramanian S, West RB, Corless CL, Ou W, Rubin BP, et al. (2004) Gastrointestinal stromal tumors (GISTs) with KIT and PDGFRA mutations have distinct gene expression profiles. Oncogene 23: 7780-7790.
7. Tarn C, Merkel E, Canutescu AA, Shen W, Skorobogatko Y, et al. (2005) Analysis of KIT mutations in sporadic and familial gastrointestinal stromal tumors: therapeutic implications through protein modeling. Clin Cancer Res 11: 3668-3677.
8. Janeway KA, Kim SY, Lodish M, Nose V, Rustin P, et al. Defects in succinate dehydrogenase in gastrointestinal stromal tumors lacking KIT and PDGFRA mutations. Proc Natl Acad Sci U S A 108: 314-318.
9. Pantaleo MA, Astolfi A, Indio V, Moore R, Thiessen N, et al. (2011) SDHA loss-of-function mutations in KIT-PDGFRA wild-type gastrointestinal stromal tumors identified by massively parallel sequencing. J Natl Cancer Inst 103: 983-987.
10. Tarn C, Rink L, Merkel E, Flieder D, Pathak H, et al. (2008) Insulin-like growth factor 1 receptor is a potential therapeutic target for gastrointestinal stromal tumors. Proc Natl Acad Sci U S A 105: 8387-8392.
11. Belinsky MG, Rink L, Cai KQ, Ochs MF, Eisenberg B, et al. (2008) The insulin-like growth factor system as a potential therapeutic target in gastrointestinal stromal tumors. Cell Cycle 7: 2949-2955.
12. Chou A, Chen J, Clarkson A, Samra JS, Clifton-Bligh RJ, et al. (2012) Succinate dehydrogenase-deficient GISTs are characterized by IGF1R overexpression. Mod Pathol 25: 1307-1313.
13. El-Rifai W, Sarlomo-Rikala M, Andersson LC, Knuutila S, Miettinen M, (2000) DNA sequence copy number changes in gastrointestinal stromal tumors: tumor progression and prognostic significance. Cancer Res 60: 3899-3903.
14. Miettinen M, Lasota J, (2003) Gastrointestinal stromal tumors (GISTs): definition, occurrence, pathology, differential diagnosis and molecular genetics. Pol J Pathol 54: 3-24.
15. Corless CL, Fletcher JA, Heinrich MC, (2004) Biology of gastrointestinal stromal tumors. J Clin Oncol 22: 3813-3825.
16. Miettinen M, Lasota J, (2001) Gastrointestinal stromal tumors-definition, clinical, histological, immunohistochemical, and molecular genetic features and differential diagnosis. Virchows Arch 438: 1-12.
17. Demetri GD, (2002) GIST 1, chemotherapy 0, with a brand new hitter up next. Cancer Invest 20: 853-854.
18. Verweij J, van Oosterom A, Blay JY, Judson I, Rodenhuis S, et al. (2003) Imatinib mesylate (STI-571 Glivec, Gleevec) is an active agent for gastrointestinal stromal tumours, but does not yield responses in other soft-tissue sarcomas that are unselected for a molecular target. Results from an EORTC Soft Tissue and Bone Sarcoma Group phase II study. Eur J Cancer 39: 2006-2011.
19. Blanke CD, Demetri GD, von Mehren M, Heinrich MC, Eisenberg B, et al. (2008) Long-term results from a randomized phase II trial of standard- versus higher-dose imatinib mesylate for patients with unresectable or metastatic gastrointestinal stromal tumors expressing KIT. J Clin Oncol 26: 620-625.
20. Debiec-Rychter M, Sciot R, Le Cesne A, Schlemmer M, Hohenberger P, et al. (2006) KIT mutations and dose selection for imatinib in patients with advanced gastrointestinal stromal tumours. Eur J Cancer 42: 1093-1103.
21. Demetri GD, van Oosterom AT, Garrett CR, Blackstein ME, Shah MH, et al. (2006) Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 368: 1329-1338.
22. Rink L, Skorobogatko Y, Kossenkov AV, Belinsky MG, Pajak T, et al. (2009) Gene expression signatures and response to imatinib mesylate in gastrointestinal stromal tumor. Mol Cancer Ther 8: 2172-2182.
23. Taguchi T, Sonobe H, Toyonaga S, Yamasaki I, Shuin T, et al. (2002) Conventional and molecular cytogenetic characterization of a new human cell line, GIST-T1, established from gastrointestinal stromal tumor. Lab Invest 82: 663-665.
24. Tarn C, Skorobogatko YV, Taguchi T, Eisenberg B, von Mehren M, et al. (2006) Therapeutic effect of imatinib in gastrointestinal stromal tumors: AKT signaling dependent and independent mechanisms. Cancer Res 66: 5477-5486.
25. Eva A, Robbins KC, Andersen PR, Srinivasan A, Tronick SR, et al. (1982) Cellular genes analogous to retroviral onc genes are transcribed in human tumour cells. Nature 295: 116-119.
26. Godwin AK, Meister A, O'Dwyer PJ, Huang CS, Hamilton TC, et al. (1992) High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci U S A 89: 3070-3074.
27. Boutros M, Bras LP, Huber W, (2006) Analysis of cell-based RNAi screens. Genome Biol 7: R66.
28. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
29. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
30. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey RV, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and BioConductor. New York: Springer. pp. 397-420.
31. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I, (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284.
32. Carvalho BS, Irizarry RA, (2010) A framework for oligonucleotide microarray preprocessing. Bioinformatics 26: 2363-2367.
33. Chen X, Arciero CA, Wang C, Broccoli D, Godwin AK, (2006) BRCC36 is essential for ionizing radiation-induced BRCA1 phosphorylation and nuclear foci formation. Cancer Res 66: 5039-5046.
34. Frolov A, Chahwan S, Ochs M, Arnoletti JP, Pan ZZ, et al. (2003) Response markers and the molecular mechanisms of action of Gleevec in gastrointestinal stromal tumors. Mol Cancer Ther 2: 699-709.
35. Ouyang G, Liu M, Ruan K, Song G, Mao Y, et al. (2009) Upregulated expression of periostin by hypoxia in non-small-cell lung cancer cells promotes cell survival via the Akt/PKB pathway. Cancer Lett 281: 213-219.
36. Ruan K, Bao S, Ouyang G, (2009) The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66: 2219-2230.
37. Strauss LG, Dimitrakopoulou-Strauss A, Koczan D, Pan L, Hohenberger P, (2012) Correlation of Dynamic PET and Gene Array Data in Patients with Gastrointestinal Stromal Tumors. ScientificWorldJournal 2012: 721313.
38. Duan Z, Choy E, Harmon D, Yang C, Ryu K, et al. (2009) ZNF93 increases resistance to ET-743 (Trabectedin; Yondelis) and PM00104 (Zalypsis) in human cancer cell lines. PLoS One 4: e6967.
39. Seyhan AA, Varadarajan U, Choe S, Liu W, Ryan TE, (2012) A genome-wide RNAi screen identifies novel targets of neratinib resistance leading to identification of potential drug resistant genetic markers. Mol Biosyst 8: 1553-1570.
40. Micci F, Skotheim RI, Haugom L, Weimer J, Eibak AM, et al. (2010) Array-CGH analysis of microdissected chromosome 19 markers in ovarian carcinoma identifies candidate target genes. Genes Chromosomes Cancer 49: 1046-1053.
41. Couch FJ, Gaudet MM, Antoniou AC, Ramus SJ, Kuchenbaecker KB, et al. (2012) Common variants at the 19p13.1 and ZNF365 loci are associated with ER subtypes of breast cancer and ovarian cancer risk in BRCA1 and BRCA2 mutation carriers. Cancer Epidemiol Biomarkers Prev 21: 645-657.
42. Stevens KN, Fredericksen Z, Vachon CM, Wang X, Margolin S, et al. (2012) 19p13.1 is a triple-negative-specific breast cancer susceptibility locus. Cancer Res 72: 1795-1803.
43. Hamilton AT, Huntley S, Tran-Gyamfi M, Baggott DM, Gordon L, et al. (2006) Evolutionary expansion and divergence in the ZNF91 subfamily of primate-specific zinc finger genes. Genome Res 16: 584-594.
44. Streit S, Michalski CW, Erkan M, Friess H, Kleeff J, (2009) Confirmation of DNA microarray-derived differentially expressed genes in pancreatic cancer using quantitative RT-PCR. Pancreatology 9: 577-582.
45. Shao R, Bao S, Bai X, Blanchette C, Anderson RM, et al. (2004) Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression. Mol Cell Biol 24: 3992-4003.
46. Tikhmyanova N, Little JL, Golemis EA, CAS proteins in normal and pathological cell growth control. Cell Mol Life Sci 67: 1025-1048.
47. Takeshita S, Kikuno R, Tezuka K, Amann E, (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294 (Pt 1):: 271-278.
48. Horiuchi K, Amizuka N, Takeshita S, Takamatsu H, Katsuura M, et al. (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14: 1239-1249.
49. Baril P, Gangeswaran R, Mahon PC, Caulee K, Kocher HM, et al. (2007) Periostin promotes invasiveness and resistance of pancreatic cancer cells to hypoxia-induced cell death: role of the beta4 integrin and the PI3k pathway. Oncogene 26: 2082-2094.
50. Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, et al. (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res 62: 5358-5364.
51. Bao S, Ouyang G, Bai X, Huang Z, Ma C, et al. (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5: 329-339.
52. Kudo Y, Ogawa I, Kitajima S, Kitagawa M, Kawai H, et al. (2006) Periostin promotes invasion and anchorage-independent growth in the metastatic process of head and neck cancer. Cancer Res 66: 6928-6935.
53. Pouyssegur J, Dayan F, Mazure NM, (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443.
54. Bristow RG, Hill RP, (2008) Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 8: 180-192.
55. Halatsch ME, Low S, Mursch K, Hielscher T, Schmidt U, et al. (2009) Candidate genes for sensitivity and resistance of human glioblastoma multiforme cell lines to erlotinib. Laboratory investigation. J Neurosurg 111: 211-218.
56. Natarajan M, Stewart JE, Golemis EA, Pugacheva EN, Alexandropoulos K, et al. (2006) HEF1 is a necessary and specific downstream effector of FAK that promotes the migration of glioblastoma cells. Oncogene 25: 1721-1732.
57. Kim M, Gans JD, Nogueira C, Wang A, Paik JH, et al. (2006) Comparative oncogenomics identifies NEDD9 as a melanoma metastasis gene. Cell 125: 1269-1281.
58. Zheng M, McKeown-Longo PJ, (2002) Regulation of HEF1 expression and phosphorylation by TGF-beta 1 and cell adhesion. J Biol Chem 277: 39599-39608.
59. Liu X, Elia AE, Law SF, Golemis EA, Farley J, et al. (2000) A novel ability of Smad3 to regulate proteasomal degradation of a Cas family member HEF1. Embo J 19: 6759-6769.
60. Sasaki T, Iwata S, Okano HJ, Urasaki Y, Hamada J, et al. (2005) Nedd9 protein, a Cas-L homologue, is upregulated after transient global ischemia in rats: possible involvement of Nedd9 in the differentiation of neurons after ischemia. Stroke 36: 2457-2462.
61. Martin-Rendon E, Hale SJ, Ryan D, Baban D, Forde SP, et al. (2007) Transcriptional profiling of human cord blood CD133+ and cultured bone marrow mesenchymal stem cells in response to hypoxia. Stem Cells 25: 1003-1012.
62. Thao le B, Vu HA, Yasuda K, Taniguchi S, Yagasaki F, et al. (2009) Cas-L was overexpressed in imatinib-resistant gastrointestinal stromal tumor cells. Cancer Biol Ther 8: 683-688.
63. Dupart JJ, Trent JC, Lee HY, Hess KR, Godwin AK, et al. (2009) Insulin-like growth factor binding protein-3 has dual effects on gastrointestinal stromal tumor cell viability and sensitivity to the anti-tumor effects of imatinib mesylate in vitro. Mol Cancer 8: 99.
64. Italiano A, Chen J, Zhang L, Hajdu M, Singer S, et al. (2012) Patterns of deregulation of insulin growth factor signalling pathway in paediatric and adult gastrointestinal stromal tumours. Eur J Cancer.
65. Ghosh P, Dahms NM, Kornfeld S, (2003) Mannose 6-phosphate receptors: new twists in the tale. Nat Rev Mol Cell Biol 4: 202-212.
66. Chang M, Kuo W, Chen R, Lu M, Tsai F, et al. (2008) IGFII/mannose 6-phosphate receptor activation induces metalloproteinase-9 matrix activity and increases plasminogen activator expression in H9c2 cardiomyoblast cells. J Mol Endocrinology 41: 65-74.