Higher gene expression variability in the more aggressive subtype of chronic lymphocytic leukemia

Genome Medicine

Volumn 7, Issue 1, 2015, Pages

  Ecker, Simone ^a   Pancaldi, Vera ^a   Rico, Daniel ^a   Valencia, Alfonso ^a  

^a Structural Biology and Biocomputing Programme   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CANCER CLASSIFICATION; CANCER GROWTH; CANCER PROGNOSIS; CANCER RESISTANCE; CELL COMMUNICATION; CELL CYCLE; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; MAJOR CLINICAL STUDY; PATIENT CODING; PREDICTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84939150742     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-014-0125-z     Document Type: Article

References (76)

1. Elowitz MB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science. 2002;297:1183-6.
2. Carey LB, van Dijk D, Sloot PMA, Kaandorp JA, Segal E. Promoter sequence determines the relationship between expression level and noise. PLoS Biol. 2013;11:e1001528.
3. Geva-Zatorsky N, Rosenfeld N, Itzkovitz S, Milo R, Sigal A, Dekel E, et al. Oscillations and variability in the p53 system. Mol Sys Biol. 2006;2:2006.0033.
4. Ashall L, Horton CA, Nelson DE, Paszek P, Harper CV, Sillitoe K, et al. Pulsatile simulation determines timing and specificity of NF-kB-dependent transcription. Science. 2009;324:242-6.
5. Paszek P, Ryan S, Ashall L, Sillitoe K, Harper CV, Spiller DG, et al. Population robustness arising from cellular heterogeneity. Proc Natl Acad Sci U S A. 2010;107:11644-9.
6. Lehner B. Genes confer similar robustness to environmental, stochastic, and genetic perturbations in yeast. PLoS One. 2010;5:e9035.
7. Tirosh I, Reikhav S, Levy AA, Barkai N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science. 2009;324:659-62.
8. Basehoar AD, Zanton SJ, Pugh BF. Identification and distinct regulation of yeast TATA box-containing genes. Cell. 2004;116:699-709.
9. Choi JK, Kim Y-J. Intrinsic variability of gene expression encoded in nucleosome positioning sequences. Nat Genet. 2009;41:498-503.
10. Salari R, Wojtowicz D, Zheng J, Levens D, Pilpel Y, Przytycka TM. Teasing apart translational and transcriptional components of stochastic variations in eukaryotic gene expression. PLoS Comput Biol. 2012;8:e1002644.
11. Dong D, Shao X, Deng N, Zhang Z. Gene expression variations are predictive for stochastic noise. Nucleic Acids Res. 2011;39:403-13.
12. Lehner B, Kaneko K. Fluctuation and response in biology. Cell Mol Life Sci. 2011;68:1005-10.
13. Marusyk A, Polyak K. Tumor heterogeneity: causes and consequences. Biochim Biophys Acta. 2011;1805:1-28.
14. Meacham CE, Morrison SJ. Tumour heterogeneity and cancer cell plasticity. Nature. 2013;501:328-37.
15. Brock A, Chang H, Huang S. Non-genetic heterogeneity-a mutation-independent driving force for the somatic evolution of tumours. Nat Rev Genet. 2009;10:336-42.
16. Almendro V, Cheng Y-K, Randles A, Itzkovitz S, Marusyk A, Ametller E, et al. Inference of tumor evolution during chemotherapy by computational modeling and in situ analysis of genetic and phenotypic cellular diversity. Cell Rep. 2014;6:514-27.
17. Marusyk A, Almendro V, Polyak K. Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer. 2012;12:323-34.
18. Landau DA, Carter SL, Stojanov P, McKenna A, Stevenson K, Lawrence MS, et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell. 2013;152:714-26.
19. Ho JWK, Stefani M, Dos Remedios CG, Charleston MA. Differential variability analysis of gene expression and its application to human diseases. Bioinformatics. 2008;24:i390-8.
20. Hulse AM, Cai JJ. Genetic variants contribute to gene expression variability in humans. Genetics. 2013;193:95-108.
21. Fabris S, Mosca L, Todoerti K, Cutrona G, Lionetti M, Intini D, et al. Molecular and transcriptional characterization of 17p loss in B-cell chronic lymphocytic leukemia. Genes Chromosom Cancer. 2008;47:781-93.
22. Kulis M, Heath S, Bibikova M, Queirós AC, Navarro A, Clot G, et al. Epigenomic analysis detects widespread gene-body DNA hypomethylation in chronic lymphocytic leukemia. Nat Genet. 2012;44:1236-42.
23. Hamblin BTJ, Davis Z, Gardiner A, Oscier DG, Stevenson FK. Unmutated IgVH genes are associated with a more aggressive form of chronic lymphocytic leukemia. Blood. 1999;94:1848-54.
24. Ferreira PG, Jares P, Rico D, Gomez-Lopez G, Martinez-Trillos A, Villamor N, et al. Transcriptome characterization by RNA sequencing identifies a major molecular and clinical subdivision in chronic lymphocytic leukemia. Genome Res. 2013;24:212-26.
25. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-64.
26. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20:307-15.
27. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics. 2008;24:1547-8.
28. McCall MN, Irizarry RA. Thawing frozen robust multi-array analysis (fRMA). BMC Bioinformatics. 2011;12:369.
29. Haslinger C, Schweifer N, Stilgenbauer S, Döhner H, Lichter P, Kraut N, et al. Microarray gene expression profiling of B-cell chronic lymphocytic leukemia subgroups defined by genomic aberrations and VH mutation status. J Clin Oncol. 2004;22:3937-49.
30. Alemu EY, Carl JW, Corrada Bravo H, Hannenhalli S. Determinants of expression variability. Nucleic Acids Res. 2014;42:3503-14.
31. Loader C. Local Regression and Likelihood, vol. 42. New York: Springer; 1999.
32. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol. 1995;57:289-300.
33. Smyth GK. Limma: Linear Models for Microarray Data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinforma Comput Biol Solut Using R Bioconductor. New York: Springer; 2005. p. 397-420.
34. Jaffe AE, Murakami P, Lee H, Leek JT, Fallin MD, Feinberg AP, et al. Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol. 2012;41:200-9.
35. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
36. Lefebvre C, Rajbhandari P, Alvarez MJ, Bandaru P, Lim WK, Sato M, et al. A human B-cell interactome identifies MYB and FOXM1 as master regulators of proliferation in germinal centers. Mol Syst Biol. 2010;6:377.
37. Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. Int AAAI Conference on Weblogs and Social Media; 2009.
38. Blondel VD, Guillaume J, Lefebvre E. Fast unfolding of communities in large networks. J Stat Mech. 2008;P10008:1-12.
39. Breiman L. Random forests. Mach Learn. 2001;45:5-32.
40. R Development Core Team. R. A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2008.
41. Van Kampen N. Stochastic Processes in Physics and Chemistry. Amsterdam: North-Holland Personal Library; 2007.
42. Kaern M, Elston TC, Blake WJ, Collins JJ. Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet. 2005;6:451-64.
43. Klein U, Tu Y, Stolovitzky GA, Mattioli M, Cattoretti G, Husson H, et al. Gene expression profiling of B cell chronic lymphocytic leukemia reveals a homogeneous phenotype related to memory B cells. J Exp Med. 2001;194:1625-38.
44. Rosenwald A, Alizadeh AA, Widhopf G, Simon R, Davis RE, Yu X, et al. Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J Exp Med. 2001;194:1639-47.
45. Koivunen J, Aaltonen V, Peltonen J. Protein kinase C (PKC) family in cancer progression. Cancer Lett. 2006;235:1-10.
46. Ruvolo PP, Deng X, Carr BK, May WS. A functional role for mitochondrial protein kinase C in Bcl2 phosphorylation and suppression of apoptosis. J Biol Chem. 1998;273:25436-42.
47. Segil N, Roberts SB, Heintz N. Mitotic phosphorylation of the Oct-1 homeodomain and regulation of Oct-1 DNA binding activity. Science. 1991;254:1814-6.
48. Lee L, Stollar E, Chang J, Gu J, Brien RO, Ladbury J, et al. Expression of the Oct-1 transcription factor and characterization of its interactions. Biochemistry. 2001;40:6580-8.
49. Shatz M, Liscovitch M. Caveolin-1 and cancer multidrug resistance: coordinate regulation of pro-survival proteins? Leuk Res. 2004;28:907-8.
50. Engelman JA, Zhang X, Galbiati F, Volonte D, Sotgia F, Pestell RG, et al. Molecular genetics of the caveolin gene family: implications for human cancers, diabetes, Alzheimer disease, and muscular dystrophy. Am J Hum Genet. 1998;63:1578-87.
51. Gilling CE, Mittal AK, Chaturvedi NK, Iqbal J, Aoun P, Bierman PJ, et al. Lymph node-induced immune tolerance in chronic lymphocytic leukaemia: a role for caveolin-1. Br J Haematol. 2012;158:216-31.
52. Pede V, Rombout A, Vermeire J, Naessens E, Mestdagh P, Robberecht N, et al. CLL cells respond to B-Cell receptor stimulation with a microRNA/mRNA signature associated with MYC activation and cell cycle progression. PLoS One. 2013;8:e60275.
53. Damle RN, Temburni S, Calissano C, Yancopoulos S, Banapour T, Sison C, et al. CD38 expression labels an activated subset within chronic lymphocytic leukemia clones enriched in proliferating B cells. Blood. 2007;110:3352-9.
54. Meixner A, Karreth F, Kenner L, Wagner EF. JunD regulates lymphocyte proliferation and T helper cell cytokine expression. EMBO J. 2004;23:1325-35.
55. Weitzman JB, Fiette L, Matsuo K, Yaniv M. JunD protects cells from p53-dependent senescence and apoptosis. Mol Cell. 2000;6:1109-19.
56. Eferl R, Wagner EF. AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer. 2003;3:859-68.
57. Xu LL, Warren MK, Rose WL, Gong W, Wang JM. Human recombinant monocyte chemotactic protein and other C-C chemokines bind and induce directional migration of dendritic cells in vitro. J Leukoc Biol. 1996;60:365-71.
58. Wolter S, Doerrie A, Weber A, Schneider H, Hoffmann E, von der Ohe J, et al. c-Jun controls histone modifications, NF-kappaB recruitment, and RNA polymerase II function to activate the ccl2 gene. Mol Cell Biol. 2008;28:4407-23.
59. Lee C-K, Smith E, Gimeno R, Gertner R, Levy DE. STAT1 affects lymphocyte survival and proliferation partially independent of its role downstream of IFN-y. J Immunol. 2000;164:1286-92.
60. Frank DA, Mahajan S, Ritz J. B lymphocytes from patients with chronic lymphocytic leukemia contain signal transducer and activator of transcription (STAT) 1 and STAT3 constitutively phosphorylated on serine residues. J Clin Invest. 1997;100:3140-8.
61. Vallat L, Magdele H, Kruhoffer M, Sabatier L, Orntoft TF, Delic J. The resistance of B-CLL cells to DNA damage - induced apoptosis defined by DNA microarrays. Blood. 2003;101:4598-606.
62. Pelengaris S, Khan M, Evan G. c-MYC: more than just a matter of life and death. Nat Rev Cancer. 2002;2:764-76.
63. Dominguez-Sola D, Ying CY, Grandori C, Ruggiero L, Chen B, Li M, et al. Non-transcriptional control of DNA replication by c-Myc. Nature. 2007;448:445-51.
64. Lüscher B. Function and regulation of the transcription factors of the Myc/Max/Mad network. Gene. 2001;277:1-14.
65. Nilsson JA, Cleveland JL. Myc pathways provoking cell suicide and cancer. Oncogene. 2003;22:9007-21.
66. Rana S, Munawar M, Shahid A, Malik M, Ullah H, Fatima W, et al. Deregulated expression of circadian clock and clock-controlled cell cycle genes in chronic lymphocytic leukemia. Mol Biol Rep. 2014;41:95-103.
67. Wierstra I, Alves J. FOXM1, a typical proliferation-associated transcription factor. Biol Chem. 2007;388:1257-74.
68. Mencalha AL, Binato R, Ferreira GM, Du Rocher B, Abdelhay E. Forkhead box M1 (FoxM1) gene is a new STAT3 transcriptional factor target and is essential for proliferation, survival and DNA repair of K562 cell line. PLoS One. 2012;7:e48160.
69. Shupnik MA. Crosstalk between steroid receptors and the c-Src-receptor tyrosine kinase pathways: implications for cell proliferation. Oncogene. 2004;23:7979-89.
70. Fa S, Lambert B, Wennborg A. Identification of progression markers in B-CLL by gene expression profiling. Exp Hematol. 2005;33:883-93.
71. Sardet C, Vidal M, Cobrinik D, Geng Y, Onufryk C, Chen A, et al. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc Natl Acad Sci U S A. 1995;92:2403-7.
72. Bruey J-M, Kantarjian H, Ma W, Estrov Z, Yeh C, Donahue A, et al. Circulating Ki-67 index in plasma as a biomarker and prognostic indicator in chronic lymphocytic leukemia. Leuk Res. 2010;34:1320-4.
73. Obermann EC, Went P, Tzankov A, Pileri SA, Hofstaedter F, Marienhagen J, et al. Cell cycle phase distribution analysis in chronic lymphocytic leukaemia: a significant number of cells reside in early G1-phase. J Clin Pathol. 2007;60:794-7.
74. Oakes CC, Claus R, Gu L, Assenov Y, Hüllein J, Zucknick M, et al. Evolution of DNA methylation is linked to genetic aberrations in chronic lymphocytic leukemia. Cancer Discov. 2014;4:348-61.
75. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature. 2009;459:428-32.
76. Landau DA, Clement K, Ziller MJ, Boyle P, Fan J, Gu H, et al. Locally Disordered Methylation Forms the Basis of Intratumor Methylome Variation in Chronic Lymphocytic Leukemia. Cancer Cell. 2014;26:813-25.