Extensive gene-specific translational reprogramming in a model of B cell differentiation and abl-dependent transformation

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Bates, Jamie G ^a,b   Salzman, Julia ^a,b   May, Damon ^c   Garcia, Patty B ^d   Hogan, Gregory J ^a,b   McIntosh, Martin ^c   Schlissel, Mark S ^d   Brown, Pat O ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c USA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; IMATINIB; MESSENGER RNA; RAPAMYCIN; PIPERAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTOME;

ACUTE LYMPHOCYTIC LEUKEMIA; ARTICLE; B LYMPHOCYTE; CANCER GROWTH; CELL ADHESION; CELL DIFFERENTIATION; CELL MATURATION; CELL TRANSFORMATION; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SPECIFIC TRANSLATIONAL REPROGRAMMING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NUCLEOTIDE SEQUENCE; PROTEOMICS; TRANSLATION INITIATION; TRANSLATION REGULATION; VIRUS ONCOGENE; CELL LINE; DNA MICROARRAY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY; POLYSOME; PRE B LYMPHOCYTE; PROTEIN SYNTHESIS; VIRUS CELL TRANSFORMATION;

B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE; CELL TRANSFORMATION, VIRAL; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENE PROTEINS V-ABL; PIPERAZINES; POLYRIBOSOMES; PRECURSOR CELLS, B-LYMPHOID; PROTEIN BIOSYNTHESIS; PYRIMIDINES; RNA, MESSENGER; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANSCRIPTOME;

EID: 84861714619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037108     Document Type: Article

References (107)

1. Abelson HT, Rabstein LS, (1970) Lymphosarcoma: virus-induced thymic-independent disease in mice. Cancer Res 30: 2213-2222.
2. Rosenberg N, Baltimore D, Scher CD, (1975) In vitro transformation of lymphoid cells by Abelson murine leukemia virus. Proc Natl Acad Sci U S A 72: 1932-1936.
3. Sklar MD, Shevach EM, Green I, Potter M, (1975) Transplantation and preliminary characterisation of lymphocyte surface markers of Abelson virus-induced lymphomas. Nature 253: 550-552.
4. Nowell PC, (1960) A minute chromosome in human chronic granulocytic leukemia. Science 132: 1497.
5. Rowley JD, (1973) Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 243: 290-293.
6. Shtivelman E, Lifshitz B, Gale RP, Canaani E, (1985) Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature 315: 550-554.
7. Kantarjian HM, Deisseroth A, Kurzrock R, Estrov Z, Talpaz M, (1993) Chronic myelogenous leukemia: a concise update. Blood 82: 691-703.
8. Lundell BI, McCarthy JB, Kovach NL, Verfaillie CM, (1996) Activation-dependent alpha5beta1 integrin-mediated adhesion to fibronectin decreases proliferation of chronic myelogenous leukemia progenitors and K562 cells. Blood 87: 2450-2458.
9. Lundell BI, McCarthy JB, Kovach NL, Verfaillie CM, (1997) Activation of beta1 integrins on CML progenitors reveals cooperation between beta1 integrins and CD44 in the regulation of adhesion and proliferation. Leukemia 11: 822-829.
10. Salesse S, Verfaillie CM, (2002) Mechanisms underlying abnormal trafficking and expansion of malignant progenitors in CML: BCR/ABL-induced defects in integrin function in CML. Oncogene 21: 8605-8611.
11. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, et al. (1996) Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 2: 561-566.
12. Druker BJ, (2008) Translation of the Philadelphia chromosome into therapy for CML. Blood 112: 4808-4817.
13. Weisberg E, Manley PW, Cowan-Jacob SW, Hochhaus A, Griffin JD, (2007) Second generation inhibitors of BCR-ABL for the treatment of imatinib-resistant chronic myeloid leukaemia. Nat Rev Cancer 7: 345-356.
14. Klein F, Feldhahn N, Harder L, Wang H, Wartenberg M, et al. (2004) The BCR-ABL1 kinase bypasses selection for the expression of a pre-B cell receptor in pre-B acute lymphoblastic leukemia cells. The Journal of experimental medicine 199: 673-685.
15. Trageser D, Iacobucci I, Nahar R, Duy C, von Levetzow G, et al. (2009) Pre-B cell receptor-mediated cell cycle arrest in Philadelphia chromosome-positive acute lymphoblastic leukemia requires IKAROS function. The Journal of experimental medicine 206: 1739-1753.
16. Muljo SA, Schlissel MS, (2003) A small molecule Abl kinase inhibitor induces differentiation of Abelson virus-transformed pre-B cell lines. Nat Immunol 4: 31-37.
17. Klug CA, Gerety SJ, Shah PC, Chen YY, Rice NR, et al. (1994) The v-abl tyrosine kinase negatively regulates NF-kappa B/Rel factors and blocks kappa gene transcription in pre-B lymphocytes. Genes Dev 8: 678-687.
18. Chen YY, Wang LC, Huang MS, Rosenberg N, (1994) An active v-abl protein tyrosine kinase blocks immunoglobulin light-chain gene rearrangement. Genes Dev 8: 688-697.
19. Hakansson P, Segal D, Lassen C, Gullberg U, Morse HC III, et al. (2004) Identification of genes differentially regulated by the P210 BCR/ABL1 fusion oncogene using cDNA microarrays. Exp Hematol 32: 476-482.
20. Jongen-Lavrencic M, Salesse S, Delwel R, Verfaillie CM, (2005) BCR/ABL-mediated downregulation of genes implicated in cell adhesion and motility leads to impaired migration toward CCR7 ligands CCL19 and CCL21 in primary BCR/ABL-positive cells. Leukemia: official journal of the Leukemia Society of America, Leukemia Research Fund, UK 19: 373-380.
21. Meric F, Hunt KK, (2002) Translation initiation in cancer: a novel target for therapy. Mol Cancer Ther 1: 971-979.
22. Zhang M, Fu W, Prabhu S, Moore JC, Ko J, et al. (2008) Inhibition of polysome assembly enhances imatinib activity against chronic myelogenous leukemia and overcomes imatinib resistance. Mol Cell Biol 28: 6496-6509.
23. Janes MR, Limon JJ, So L, Chen J, Lim RJ, et al. (2010) Effective and selective targeting of leukemia cells using a TORC1/2 kinase inhibitor. Nat Med 16: 205-213.
24. Ly C, Arechiga AF, Melo JV, Walsh CM, Ong ST, (2003) Bcr-Abl kinase modulates the translation regulators ribosomal protein S6 and 4E-BP1 in chronic myelogenous leukemia cells via the mammalian target of rapamycin. Cancer Res 63: 5716-5722.
25. Notari M, Neviani P, Santhanam R, Blaser BW, Chang JS, et al. (2006) A MAPK/HNRPK pathway controls BCR/ABL oncogenic potential by regulating MYC mRNA translation. Blood 107: 2507-2516.
26. Perrotti D, Calabretta B, (2004) Translational regulation by the p210 BCR/ABL oncoprotein. Oncogene 23: 3222-3229.
27. Prabhu S, Saadat D, Zhang M, Halbur L, Fruehauf JP, et al. (2007) A novel mechanism for Bcr-Abl action: Bcr-Abl-mediated induction of the eIF4F translation initiation complex and mRNA translation. Oncogene 26: 1188-1200.
28. Perrotti D, Calabretta B, (2002) Post-transcriptional mechanisms in BCR/ABL leukemogenesis: role of shuttling RNA-binding proteins. Oncogene 21: 8577-8583.
29. Hendrickson DG, Hogan DJ, McCullough HL, Myers JW, Herschlag D, et al. (2009) Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol 7: e1000238.
30. Schwanhausser B, Gossen M, Dittmar G, Selbach M, (2009) Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9: 205-209.
31. Gibbons JJ, Abraham RT, Yu K, (2009) Mammalian target of rapamycin: discovery of rapamycin reveals a signaling pathway important for normal and cancer cell growth. Semin Oncol 36 (Suppl 3): S3-S17.
32. Mamane Y, Petroulakis E, LeBacquer O, Sonenberg N, (2006) mTOR, translation initiation and cancer. Oncogene 25: 6416-6422.
33. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, et al. (2004) Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nature cell biology 6: 1122-1128.
34. Bhaskar PT, Hay N, (2007) The two TORCs and Akt. Developmental cell 12: 487-502.
35. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, et al. (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Molecular cell 22: 159-168.
36. Hamilton TL, Stoneley M, Spriggs KA, Bushell M, (2006) TOPs and their regulation. Biochem Soc Trans 34: 12-16.
37. Avni D, Biberman Y, Meyuhas O, (1997) The 5′ terminal oligopyrimidine tract confers translational control on TOP mRNAs in a cell type- and sequence context-dependent manner. Nucleic Acids Res 25: 995-1001.
38. Fogal V, Richardson AD, Karmali PP, Scheffler IE, Smith JW, et al. (2010) Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Molecular and cellular biology 30: 1303-1318.
39. McGee AM, Baines CP, (2010) Complement 1q-binding protein inhibits the mitochondrial permeability transition pore and protects against oxidative stress-induced death. The Biochemical journal 433: 119-125.
40. Iervolino A, Santilli G, Trotta R, Guerzoni C, Cesi V, et al. (2002) hnRNP A1 nucleocytoplasmic shuttling activity is required for normal myelopoiesis and BCR/ABL leukemogenesis. Mol Cell Biol 22: 2255-2266.
41. An WG, Schulte TW, Neckers LM, (2000) The heat shock protein 90 antagonist geldanamycin alters chaperone association with p210bcr-abl and v-src proteins before their degradation by the proteasome. Cell Growth Differ 11: 355-360.
42. Shiotsu Y, Neckers LM, Wortman I, An WG, Schulte TW, et al. (2000) Novel oxime derivatives of radicicol induce erythroid differentiation associated with preferential G(1) phase accumulation against chronic myelogenous leukemia cells through destabilization of Bcr-Abl with Hsp90 complex. Blood 96: 2284-2291.
43. Su IH, Basavaraj A, Krutchinsky AN, Hobert O, Ullrich A, et al. (2003) Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nature immunology 4: 124-131.
44. Kaul-Ghanekar R, Jalota A, Pavithra L, Tucker P, Chattopadhyay S, (2004) SMAR1 and Cux/CDP modulate chromatin and act as negative regulators of the TCRbeta enhancer (Ebeta). Nucleic acids research 32: 4862-4875.
45. Goebel P, Montalbano A, Ayers N, Kompfner E, Dickinson L, et al. (2002) High frequency of matrix attachment regions and cut-like protein x/CCAAT-displacement protein and B cell regulator of IgH transcription binding sites flanking Ig V region genes. Journal of immunology 169: 2477-2487.
46. Wang Z, Day N, Trifillis P, Kiledjian M, (1999) An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Molecular and cellular biology 19: 4552-4560.
47. Muto A, Hoshino H, Madisen L, Yanai N, Obinata M, et al. (1998) Identification of Bach2 as a B-cell-specific partner for small maf proteins that negatively regulate the immunoglobulin heavy chain gene 3′ enhancer. The EMBO journal 17: 5734-5743.
48. Hu H, Wang B, Borde M, Nardone J, Maika S, et al. (2006) Foxp1 is an essential transcriptional regulator of B cell development. Nature immunology 7: 819-826.
49. Jin ZX, Kishi H, Wei XC, Matsuda T, Saito S, et al. (2002) Lymphoid enhancer-binding factor-1 binds and activates the recombination-activating gene-2 promoter together with c-Myb and Pax-5 in immature B cells. J Immunol 169: 3783-3792.
50. Shaffer AL, Yu X, He Y, Boldrick J, Chan EP, et al. (2000) BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 13: 199-212.
51. Duy C, Yu JJ, Nahar R, Swaminathan S, Kweon SM, et al. (2010) BCL6 is critical for the development of a diverse primary B cell repertoire. The Journal of experimental medicine 207: 1209-1221.
52. Wang Y, Klumpp S, Amin HM, Liang H, Li J, et al. (2010) SSBP2 is an in vivo tumor suppressor and regulator of LDB1 stability. Oncogene 29: 3044-3053.
53. Madan V, Madan B, Brykczynska U, Zilbermann F, Hogeveen K, et al. (2009) Impaired function of primitive hematopoietic cells in mice lacking the Mixed-Lineage-Leukemia homolog MLL5. Blood 113: 1444-1454.
54. Ohya K, Kajigaya S, Kitanaka A, Yoshida K, Miyazato A, et al. (1999) Molecular cloning of a docking protein, BRDG1, that acts downstream of the Tec tyrosine kinase. Proceedings of the National Academy of Sciences of the United States of America 96: 11976-11981.
55. Miller SL, DeMaria JE, Freier DO, Riegel AM, Clevenger CV, (2005) Novel association of Vav2 and Nek3 modulates signaling through the human prolactin receptor. Molecular endocrinology 19: 939-949.
56. Miller SL, Antico G, Raghunath PN, Tomaszewski JE, Clevenger CV, (2007) Nek3 kinase regulates prolactin-mediated cytoskeletal reorganization and motility of breast cancer cells. Oncogene 26: 4668-4678.
57. Gomez TS, Billadeau DD, (2008) T cell activation and the cytoskeleton: you can't have one without the other. Advances in immunology 97: 1-64.
58. Spencer S, Dowbenko D, Cheng J, Li W, Brush J, et al. (1997) PSTPIP: a tyrosine phosphorylated cleavage furrow-associated protein that is a substrate for a PEST tyrosine phosphatase. The Journal of cell biology 138: 845-860.
59. Cousin H, Desimone DW, Alfandari D, (2008) PACSIN2 regulates cell adhesion during gastrulation in Xenopus laevis. Developmental biology 319: 86-99.
60. Seipel K, O'Brien SP, Iannotti E, Medley QG, Streuli M, (2001) Tara, a novel F-actin binding protein, associates with the Trio guanine nucleotide exchange factor and regulates actin cytoskeletal organization. Journal of cell science 114: 389-399.
61. Tsai IC, Amack JD, Gao ZH, Band V, Yost HJ, et al. (2007) A Wnt-CKIvarepsilon-Rap1 pathway regulates gastrulation by modulating SIPA1L1, a Rap GTPase activating protein. Developmental cell 12: 335-347.
62. Hu J, Teng J, Ding N, He M, Sun Y, et al. (2008) FAAP, a novel murine protein, is involved in cell adhesion through regulating vinculin-paxillin association. Frontiers in bioscience: a journal and virtual library 13: 7123-7131.
63. Lundell BI, McCarthy JB, Kovach NL, Verfaillie CM, (1997) Activation of beta1 integrins on CML progenitors reveals cooperation between beta1 integrins and CD44 in the regulation of adhesion and proliferation. Leukemia: official journal of the Leukemia Society of America, Leukemia Research Fund, UK 11: 822-829.
64. Mayne M, Moffatt T, Kong H, McLaren PJ, Fowke KR, et al. (2004) CYFIP2 is highly abundant in CD4+ cells from multiple sclerosis patients and is involved in T cell adhesion. European journal of immunology 34: 1217-1227.
65. Olsen PH, Ambros V, (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Developmental biology 216: 671-680.
66. Nottrott S, Simard MJ, Richter JD, (2006) Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nature structural & molecular biology 13: 1108-1114.
67. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223.
68. Schieke SM, Phillips D, McCoy JP Jr, Aponte AM, Shen RF, et al. (2006) The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J Biol Chem 281: 27643-27652.
69. Kim JH, Chu SC, Gramlich JL, Pride YB, Babendreier E, et al. (2005) Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood 105: 1717-1723.
70. Raj L, Ide T, Gurkar AU, Foley M, Schenone M, et al. (2011) Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475: 231-234.
71. Yap TA, Sandhu SK, Carden CP, de Bono JS, (2011) Poly(ADP-ribose) polymerase (PARP) inhibitors: Exploiting a synthetic lethal strategy in the clinic. CA: a cancer journal for clinicians 61: 31-49.
72. Svitkin YV, Ovchinnikov LP, Dreyfuss G, Sonenberg N, (1996) General RNA binding proteins render translation cap dependent. Embo J 15: 7147-7155.
73. Krecic AM, Swanson MS, (1999) hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol 11: 363-371.
74. Gorre ME, Ellwood-Yen K, Chiosis G, Rosen N, Sawyers CL, (2002) BCR-ABL point mutants isolated from patients with imatinib mesylate-resistant chronic myeloid leukemia remain sensitive to inhibitors of the BCR-ABL chaperone heat shock protein 90. Blood 100: 3041-3044.
75. Hsu LY, Lauring J, Liang HE, Greenbaum S, Cado D, et al. (2003) A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity 19: 105-117.
76. Jin ZX, Kishi H, Wei XC, Matsuda T, Saito S, et al. (2002) Lymphoid enhancer-binding factor-1 binds and activates the recombination-activating gene-2 promoter together with c-Myb and Pax-5 in immature B cells. Journal of immunology 169: 3783-3792.
77. Green M, Gandhi MK, Camilleri E, Marlton P, Lea R, et al. (2009) High levels of BACH2 associated with lower levels of BCL2 transcript abundance in t(14;18)(q21;q34) translocation positive non-Hodgkin's lymphoma. Leukemia research 33: 731-734.
78. Ochiai K, Katoh Y, Ikura T, Hoshikawa Y, Noda T, et al. (2006) Plasmacytic transcription factor Blimp-1 is repressed by Bach2 in B cells. The Journal of biological chemistry 281: 38226-38234.
79. Wang Z, Goldstein A, Zong RT, Lin D, Neufeld EJ, et al. (1999) Cux/CDP homeoprotein is a component of NF-muNR and represses the immunoglobulin heavy chain intronic enhancer by antagonizing the bright transcription activator. Molecular and cellular biology 19: 284-295.
80. Lazorchak AS, Schlissel MS, Zhuang Y, (2006) E2A and IRF-4/Pip promote chromatin modification and transcription of the immunoglobulin kappa locus in pre-B cells. Mol Cell Biol 26: 810-821.
81. Schlissel MS, (2004) Regulation of activation and recombination of the murine Igkappa locus. Immunological reviews 200: 215-223.
82. de Pooter RF, Kee BL, (2010) E proteins and the regulation of early lymphocyte development. Immunological reviews 238: 93-109.
83. Feldhahn N, Klein F, Mooster JL, Hadweh P, Sprangers M, et al. (2005) Mimicry of a constitutively active pre-B cell receptor in acute lymphoblastic leukemia cells. The Journal of experimental medicine 201: 1837-1852.
84. Schlissel MS, Corcoran LM, Baltimore D, (1991) Virus-transformed pre-B cells show ordered activation but not inactivation of immunoglobulin gene rearrangement and transcription. The Journal of experimental medicine 173: 711-720.
85. Spaargaren M, Beuling EA, Rurup ML, Meijer HP, Klok MD, et al. (2003) The B cell antigen receptor controls integrin activity through Btk and PLCgamma2. The Journal of experimental medicine 198: 1539-1550.
86. Skorski T, Bellacosa A, Nieborowska-Skorska M, Majewski M, Martinez R, et al. (1997) Transformation of hematopoietic cells by BCR/ABL requires activation of a PI-3k/Akt-dependent pathway. The EMBO journal 16: 6151-6161.
87. Skorski T, Kanakaraj P, Nieborowska-Skorska M, Ratajczak MZ, Wen SC, et al. (1995) Phosphatidylinositol-3 kinase activity is regulated by BCR/ABL and is required for the growth of Philadelphia chromosome-positive cells. Blood 86: 726-736.
88. Sengupta A, Arnett J, Dunn S, Williams DA, Cancelas JA, (2010) Rac2 GTPase deficiency depletes BCR-ABL+ leukemic stem cells and progenitors in vivo. Blood 116: 81-84.
89. Renshaw MW, Lea-Chou E, Wang JY, (1996) Rac is required for v-Abl tyrosine kinase to activate mitogenesis. Current biology: CB 6: 76-83.
90. Skorski T, Wlodarski P, Daheron L, Salomoni P, Nieborowska-Skorska M, et al. (1998) BCR/ABL-mediated leukemogenesis requires the activity of the small GTP-binding protein Rac. Proceedings of the National Academy of Sciences of the United States of America 95: 11858-11862.
91. Bassermann F, Jahn T, Miething C, Seipel P, Bai RY, et al. (2002) Association of Bcr-Abl with the proto-oncogene Vav is implicated in activation of the Rac-1 pathway. The Journal of biological chemistry 277: 12437-12445.
92. Geier JK, Schlissel MS, (2006) Pre-BCR signals and the control of Ig gene rearrangements. Semin Immunol 18: 31-39.
93. Kurzrock R, Kantarjian HM, Druker BJ, Talpaz M, (2003) Philadelphia chromosome-positive leukemias: from basic mechanisms to molecular therapeutics. Annals of internal medicine 138: 819-830.
94. Nilsson J, Sengupta J, Frank J, Nissen P, (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO reports 5: 1137-1141.
95. Psatha MI, Razi M, Koffer A, Moss SE, Sacks DB, et al. (2007) Targeting of calcium:calmodulin signals to the cytoskeleton by IQGAP1. Cell calcium 41: 593-605.
96. Meng X, Krokhin O, Cheng K, Ens W, Wilkins JA, (2007) Characterization of IQGAP1-containing complexes in NK-like cells: evidence for Rac 2 and RACK1 association during homotypic adhesion. Journal of proteome research 6: 744-750.
97. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, et al. (2012) The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature.
98. Bazzoni G, Carlesso N, Griffin JD, Hemler ME, (1996) Bcr/Abl expression stimulates integrin function in hematopoietic cell lines. The Journal of clinical investigation 98: 521-528.
99. Li Y, Clough N, Sun X, Yu W, Abbott BL, et al. (2007) Bcr-Abl induces abnormal cytoskeleton remodeling, beta1 integrin clustering and increased cell adhesion to fibronectin through the Abl interactor 1 pathway. Journal of cell science 120: 1436-1446.
100. Bendall SC, Hughes C, Stewart MH, Doble B, Bhatia M, et al. (2008) Prevention of amino acid conversion in SILAC experiments with embryonic stem cells. Molecular & cellular proteomics: MCP 7: 1587-1597.
101. Keller A, Backes C, Al-Awadhi M, Gerasch A, Kuntzer J, et al. (2008) GeneTrailExpress: a web-based pipeline for the statistical evaluation of microarray experiments. BMC Bioinformatics 9: 552.
102. Edgar R, Domrachev M, Lash AE, (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic acids research 30: 207-210.
103. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical chemistry 74: 5383-5392.
104. MacLean B, Eng JK, Beavis RC, McIntosh M, (2006) General framework for developing and evaluating database scoring algorithms using the TANDEM search engine. Bioinformatics 22: 2830-2832.
105. Han DK, Eng J, Zhou H, Aebersold R, (2001) Quantitative profiling of differentiation-induced microsomal proteins using isotope-coded affinity tags and mass spectrometry. Nature biotechnology 19: 946-951.
106. May D, Law W, Fitzgibbon M, Fang Q, McIntosh M, (2009) Software platform for rapidly creating computational tools for mass spectrometry-based proteomics. Journal of proteome research 8: 3212-3217.
107. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A statistical model for identifying proteins by tandem mass spectrometry. Analytical chemistry 75: 4646-4658.