Identification of tyrosine kinase, HCK, and tumor suppressor, BIN1, as potential mediators of AHI-1 oncogene in primary and transformed CTCL cells

Blood

Volumn 113, Issue 19, 2009, Pages 4646-4655

  Kennah, Erin ^a,b   Ringrose, Ashley ^a   Zhou, Liang L ^a   Esmailzadeh, Sharmin ^a,b   Qian, Hong ^a   Su, Ming Wan ^b   Zhou, Youwen ^b   Jiang, Xiaoyan ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DASATINIB; MYC PROTEIN; PROTEIN TYROSINE KINASE; TUMOR SUPPRESSOR PROTEIN; AHI1 PROTEIN, HUMAN; BIN1 PROTEIN, HUMAN; HCK PROTEIN, HUMAN; HEMATOPOIETIC CELL KINASE; MESSENGER RNA; MYC PROTEIN, HUMAN; NUCLEAR PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR MARKER;

AHI 1 GENE; ARTICLE; BIN1 GENE; CELL TRANSFORMATION; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; DOWN REGULATION; ENZYME PHOSPHORYLATION; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE OVEREXPRESSION; HCK GENE; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; ONCOGENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEZARY SYNDROME; UPREGULATION; AGED; ALTERNATIVE RNA SPLICING; CLONOGENIC ASSAY; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENETICS; IMMUNOPRECIPITATION; LENTIVIRINAE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGED; AGED, 80 AND OVER; ALTERNATIVE SPLICING; BLOTTING, WESTERN; CELL TRANSFORMATION, NEOPLASTIC; COLONY-FORMING UNITS ASSAY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOPRECIPITATION; LENTIVIRUS; LYMPHOMA, T-CELL, CUTANEOUS; MALE; MIDDLE AGED; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-HCK; PROTO-ONCOGENE PROTEINS C-MYC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEZARY SYNDROME; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS;

EID: 66549109338     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-08-174037     Document Type: Article

References (50)

1. Klemke CD, Goerdt S, Schrama D, Becker JC. New insights into the molecular biology and targeted therapy of cutaneous T-cell lymphomas. J Dtsch Dermatol Ges. 2006;4:395-406.
2. Assaf C, Hummel M, Zemlin M, et al. Transition of Sezary syndrome into mycosis fungoides after complete clinical and molecular remission under extracorporeal photophoresis. J Clin Pathol. 2004;57:1325-1328. (Pubitemid 39611522)
3. Booken N, Gratchev A, Utikal J, et al. Sezary syndrome is a unique cutaneous T-cell lymphoma as identified by an expanded gene signature including diagnostic marker molecules CDO1 and DNM3. Leukemia. 2008;22:393-399. (Pubitemid 351250545)
4. Kari L, Loboda A, Nebozhyn M, et al. Classification and prediction of survival in patients with the leukemic phase of cutaneous T cell lymphoma. J Exp Med. 2003;197:1477-1488. (Pubitemid 36682545)
5. Olsen E, Vonderheid E, Pimpinelli N, et al. Revisions to the staging and classification of mycosis fungoides and Sezary syndrome: a proposal of the International Society for Cutaneous Lymphomas (ISCL) and the cutaneous lymphoma task force of the European Organization of Research and Treatment of Cancer (EORTC). Blood. 2007;110:1713-1722. (Pubitemid 47443880)
6. Willemze R, Jaffe ES, Burg G, et al. WHO-EORTC classification for cutaneous lymphomas. Blood. 2005;105:3768-3785.
7. Hwang ST, Janik JE, Jaffe ES, Wilson WH. Mycosis fungoides and Sezary syndrome. Lancet. 2008;371:945-957.
8. Hahtola S, Tuomela S, Elo L, et al. Th1 response and cytotoxicity genes are down-regulated in cutaneous T-cell lymphoma. Clin Cancer Res. 2006;12:4812-4821. (Pubitemid 44338565)
9. Jiang X, Hanna Z, Kaouass M, Girard L, Jolicoeur P. Ahi-1, a novel gene encoding a modular protein with WD40-repeat and SH3 domains, is targeted by the Ahi-1 and Mis-2 provirus integrations. J Virol. 2002;76:9046-9059. (Pubitemid 34919863)
10. Rechsteiner M, Rogers SW. PEST sequences and regulation by proteolysis. Trends Biochem Sci. 1996;21:267-271.
11. Ringrose A, Zhou Y, Pang E, et al. Evidence for an oncogenic role of AHI-1 in Sezary syndrome, a leukemic variant of human cutaneous T-cell lymphomas. Leukemia. 2006;20:1593-1601. (Pubitemid 44264103)
12. Lupas A. Coiled coils: new structures and new functions. Trends Biochem Sci. 1996;21:375-382. (Pubitemid 26338674)
13. Mason JM, Arndt KM. Coiled coil domains: stability, specificity, and biological implications. Chembiochem. 2004;5:170-176.
14. Jiang X, Zhao Y, Chan WY, et al. Deregulated expression in Ph+ human leukemias of AHI-1, a gene activated by insertional mutagenesis in mouse models of leukemia. Blood. 2004;103:3897-3904. (Pubitemid 38596311)
15. Zhou LL, Zhao Y, Ringrose A, et al. AHI-1 interacts with BCR-ABL and modulates BCR-ABL transforming activity and imatinib response of CML stem/progenitor cells. J Exp Med. 2008;205:2657-2671.
16. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A. 2001;98:31-36. (Pubitemid 32095858)
17. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3:Article3.
18. Jiang X, Saw KM, Eaves A, Eaves C. Instability of BCR-ABL gene in primary and cultured chronic myeloid leukemia stem cells. J Natl Cancer Inst. 2007;99:680-693. (Pubitemid 47073530)
19. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B. 1995;57:289-300.
20. Tracey L, Villuendas R, Dotor AM, et al. Mycosis fungoides shows concurrent deregulation of multiple genes involved in the TNF signaling pathway: an expression profile study. Blood. 2003;102:1042-1050. (Pubitemid 36917802)
21. Mao X, Orchard G, Vonderheid EC, et al. Heterogeneous abnormalities of CCND1 and RB1 in primary cutaneous T-cell lymphomas suggesting impaired cell cycle control in disease pathogenesis. J Invest Dermatol. 2006;126:1388-1395. (Pubitemid 43997923)
22. Carreno S, Gouze ME, Schaak S, Emorine LJ, Maridonneau-Parini I. Lack of palmitoylation redirects p59Hck from the plasma membrane to p61Hck-positive lysosomes. J Biol Chem. 2000;275:36223-36229. (Pubitemid 30841173)
23. Shah NP, Tran C, Lee FY, et al. Overriding imatinib resistance with a novel ABL kinase inhibitor. Science. 2004;305:399-401. (Pubitemid 38938156)
24. Druker BJ, Tamura S, Buchdunger E, et al. Effects of a selective inhibitor of the ABL tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med. 1996;2:561-566. (Pubitemid 26151518)
25. Sakamuro D, Elliott KJ, Wechsler-Reya R, Prendergast GC. BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat Genet. 1996;14:69-77. (Pubitemid 26301549)
26. Elliott K, Sakamuro D, Basu A, et al. Bin1 functionally interacts with Myc and inhibits cell proliferation via multiple mechanisms. Oncogene. 1999;18:3564-3573. (Pubitemid 29322381)
27. Pineda-Lucena A, Ho CS, Mao DY, et al. A structure-based model of the c-Myc/Bin1 protein interaction shows alternative splicing of Bin1 and c-Myc phosphorylation are key binding determinants. J Mol Biol. 2005;351:182-194. (Pubitemid 40967064)
28. Wechsler-Reya R, Sakamuro D, Zhang J, Duhadaway J, Prendergast GC. Structural analysis of the human BIN1 gene: evidence for tissue-specific transcriptional regulation and alternate RNA splicing. J Biol Chem. 1997;272:31453-31458. (Pubitemid 28013284)
29. Wechsler-Reya R, Elliott K, Herlyn M, Prendergast GC. The putative tumor suppressor BIN1 is a short-lived nuclear phosphoprotein, the localization of which is altered in malignant cells. Cancer Res. 1997;57:3258-3263. (Pubitemid 27351744)
30. Tajiri T, Liu X, Thompson PM, et al. Expression of a MYC N-interacting isoform of the tumor suppressor BIN1 is reduced in neuroblastomas with unfavorable biological features. Clin Cancer Res. 2003;9:3345-3355. (Pubitemid 37082729)
31. Capurso G, Lattimore S, Crnogorac-Jurcevic T, et al. Gene expression profiles of progressive pancreatic endocrine tumours and their liver metastases reveal potential novel markers and therapeutic targets. Endocr Relat Cancer. 2006;13:541-558. (Pubitemid 43886676)
32. Chang MY, Boulden J, Katz JB, et al. Bin1 ablation increases susceptibility to cancer during aging, particularly lung cancer. Cancer Res. 2007;67:7605-7612. (Pubitemid 47281352)
33. Chang MY, Boulden J, Sutanto-Ward E, et al. Bin1 ablation in mammary gland delays tissue remodeling and drives cancer progression. Cancer Res. 2007;67:100-107. (Pubitemid 46142764)
34. DuHadaway JB, Lynch FJ, Brisbay S, et al. Immunohistochemical analysis of Bin1/Amphiphysin II in human tissues: diverse sites of nuclear expression and losses in prostate cancer. J Cell Biochem. 2003;88:635-642. (Pubitemid 36158282)
35. Ge K, DuHadaway J, Du W, Herlyn M, Rodeck U, Prendergast GC. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc Natl Acad Sci U S A. 1999;96:9689-9694. (Pubitemid 29398793)
36. Ge K, Duhadaway J, Sakamuro D, Wechsler-Reya R, Reynolds C, Prendergast GC. Losses of the tumor suppressor BIN1 in breast carcinoma are frequent and reflect deficits in programmed cell death capacity. Int J Cancer. 2000;85:376-383. (Pubitemid 30030412)
37. Ge K, Minhas F, Duhadaway J, et al. Loss of heterozygosity and tumor suppressor activity of Bin1 in prostate carcinoma. Int J Cancer. 2000;86:155-161. (Pubitemid 30180808)
38. Wechsler-Reya RJ, Elliott KJ, Prendergast GC. A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol Cell Biol. 1998;18:566-575. (Pubitemid 28021067)
39. Gygi SP, Rochon Y, Franza BR, Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol. 1999;19:1720-1730. (Pubitemid 29098230)
40. Chen G, Gharib TG, Huang CC, et al. Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Proteomics. 2002;1:304-313.
41. Tian Q, Stepaniants SB, Mao M, et al. Integrated genomic and proteomic analyses of gene expression in Mammalian cells. Mol Cell Proteomics. 2004;3:960-969. (Pubitemid 40361231)
42. Corey SJ, Anderson SM. Src-related protein tyrosine kinases in hematopoiesis. Blood. 1999;93:1-14. (Pubitemid 29019382)
43. Stanglmaier M, Warmuth M, Kleinlein I, Reis S, Hallek M. The interaction of the Bcr-Abl tyrosine kinase with the Src kinase Hck is mediated by multiple binding domains. Leukemia. 2003;17:283-289. (Pubitemid 36266903)
44. Shivakrupa R, Radha V, Sudhakar C, Swarup G. Physical and functional interaction between Hck tyrosine kinase and guanine nucleotide exchange factor C3G results in apoptosis, which is independent of C3G catalytic domain. J Biol Chem. 2003;278:52188-52194. (Pubitemid 38035806)
45. Hu Y, Liu Y, Pelletier S, et al. Requirement of Src kinases Lyn, Hck and Fgr for BCR-ABL1-induced B-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet. 2004;36:453-461.
46. Hoshino K, Quintas-Cardama A, Yang H, Sanchez-Gonzalez B, Garcia-Manero G. Aberrant DNA methylation of the Src kinase Hck, but not of Lyn, in Philadelphia chromosome negative acute lymphocytic leukemia. Leukemia. 2007;21:906-911. (Pubitemid 46672065)
47. Radha V, Sudhakar C, Ray P, Swarup G. Induction of cytochrome c release and apoptosis by Hck-SH3 domain-mediated signalling requires caspase-3. Apoptosis. 2002;7:195-207. (Pubitemid 34633459)
48. Elliott K, Ge K, Du W, Prendergast GC. The c-Myc-interacting adaptor protein Bin1 activates a caspase-independent cell death program. Oncogene. 2000;19:4669-4684. (Pubitemid 30814874)
49. DuHadaway JB, Sakamuro D, Ewert DL, Prendergast GC. Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res. 2001;61:3151-3156. (Pubitemid 32691968)
50. Karni R, de Stanchina E, Lowe SW, Sinha R, Mu D, Krainer AR. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat Struct Mol Biol. 2007;14:185-193. (Pubitemid 46355578)