Inorganic Arsenic-induced cellular transformation is coupled with genome wide changes in chromatin structure, transcriptome and splicing patterns

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Riedmann, Caitlyn ^a   Ma, Ye ^a   Melikishvili, Manana ^a   Godfrey, Steven Grason ^a   Zhang, Zhou ^b   Chen, Kuey Chu ^a   Rouchka, Eric C ^c   Fondufe Mittendorf, Yvonne N ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c University of Louisville   (United States)

Author keywords

Arsenic; Chromatin; Gene expression; Genome wide; Splicing

Indexed keywords

ARSENITE SODIUM; MICRORNA; TRANSCRIPTOME; ARSENOUS ACID DERIVATIVE; CHROMATIN; NUCLEOSOME; SODIUM DERIVATIVE;

ADAPTATION; ARTICLE; BEAS 2B CELL LINE; CELL DIFFERENTIATION; CELL TRANSFORMATION; CHROMATIN STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENETIC REGULATION; GENOME ANALYSIS; HELA CELL LINE; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; SIGNAL TRANSDUCTION; SPLICING DEFECT; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; APOPTOSIS; CELL LINE; CELL PROLIFERATION; CHEMISTRY; CHROMATIN; DNA FRAGMENTATION; DRUG EFFECTS; METABOLISM; NUCLEOSOME; RNA SPLICING;

APOPTOSIS; ARSENITES; CELL LINE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CHROMATIN; DNA FRAGMENTATION; EPITHELIAL-MESENCHYMAL TRANSITION; HELA CELLS; HUMANS; MICRORNAS; NUCLEOSOMES; RNA SPLICING; SIGNAL TRANSDUCTION; SODIUM COMPOUNDS; TRANSCRIPTOME;

EID: 84925298860     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1295-9     Document Type: Article

References (74)

1. States JC, Srivastava S, Chen Y, Barchowsky A. Arsenic and cardiovascular disease. Tox Sci Off J Soc Toxicol. 2009;107(2):312-23.
2. Tapio S, Grosche B. Arsenic in the aetiology of cancer. Mutat Res. 2006;612(3):215-46.
3. Dangleben NL, Skibola CF, Smith MT. Arsenic immunotoxicity: a review. Environ Health Global Access Sci Source. 2013;12(1):73.
4. He J, Wang M, Jiang Y, Chen Q, Xu S, Xu Q, et al. Chronic arsenic exposure and angiogenesis in human bronchial epithelial cells via the ROS/miR-199a-5p/HIF-1alpha/COX-2 pathway. Environ Health Perspect. 2014;122(3):255-61.
5. Hubaux R, Becker-Santos DD, Enfield KS, Rowbotham D, Lam S, Lam WL, et al. Molecular features in arsenic-induced lung tumors. Mol Cancer. 2013;12:20.
6. Kitchin KT, Conolly R. Arsenic-induced carcinogenesis-oxidative stress as a possible mode of action and future research needs for more biologically based risk assessment. Chem Res Toxicol. 2010;23(2):327-35.
7. Rossman TG. Mechanism of arsenic carcinogenesis: an integrated approach. Mutat Res. 2003;533(1-2):37-65.
8. Klein CB, Leszczynska J, Hickey C, Rossman TG. Further evidence against a direct genotoxic mode of action for arsenic-induced cancer. Toxicol Appl Pharmacol. 2007;222(3):289-97.
9. Arita A, Costa M. Epigenetics in metal carcinogenesis: nickel, arsenic, chromium and cadmium. Metallomics Integrated Biometal Sci. 2009;1(3):222-8.
10. Ren X, McHale CM, Skibola CF, Smith AH, Smith MT, Zhang L. An emerging role for epigenetic dysregulation in arsenic toxicity and carcinogenesis. Environ Health Perspect. 2011;119(1):11-9.
11. Hernandez-Castro B, Doniz-Padilla LM, Salgado-Bustamante M, Rocha D, Ortiz-Perez MD, Jimenez-Capdeville ME, et al. Effect of arsenic on regulatory T cells. J Clin Immunol. 2009;29(4):461-9.
12. Stueckle TA, Lu Y, Davis ME, Wang L, Jiang BH, Holaskova I, et al. Chronic occupational exposure to arsenic induces carcinogenic gene signaling networks and neoplastic transformation in human lung epithelial cells. Toxicol Appl Pharmacol. 2012;261(2):204-16.
13. Tokar EJ, Diwan BA, Waalkes MP. Arsenic exposure transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ Health Perspect. 2010;118(1):108-15.
14. Wang X, Son YO, Chang Q, Sun L, Hitron JA, Budhraja A, et al. NADPH oxidase activation is required in reactive oxygen species generation and cell transformation induced by hexavalent chromium. Toxicol Sci Off J Soc Toxicol. 2011;123(2):399-410.
15. Sun H, Clancy HA, Kluz T, Zavadil J, Costa M. Comparison of gene expression profiles in chromate transformed BEAS-2B cells. PLoS One. 2011;6(3):e17982.
16. O'Hara KA, Vaghjiani RJ, Nemec AA, Klei LR, Barchowsky A. Cr (VI)-stimulated STAT3 tyrosine phosphorylation and nuclear translocation in human airway epithelial cells requires Lck. Biochemical J. 2007;402(2):261-9.
17. Chen H, Kluz T, Zhang R, Costa M. Hypoxia and nickel inhibit histone demethylase JMJD1A and repress Spry2 expression in human bronchial epithelial BEAS-2B cells. Carcinogenesis. 2010;31(12):2136-44.
18. Cai T, Li X, Ding J, Luo W, Li J, Huang C. A cross-talk between NFAT and NF-kappaB pathways is crucial for nickel-induced COX-2 expression in Beas-2B cells. Curr Cancer Drug Targets. 2011;11(5):548-59.
19. Lewis DR, Southwick JW, Ouellet-Hellstrom R, Rench J, Calderon RL. Drinking water arsenic in Utah: a cohort mortality study. Environ Health Perspect. 1999;107(5):359-65.
20. Steinmaus C, Yuan Y, Bates MN, Smith AH. Case-control study of bladder cancer and drinking water arsenic in the western United States. Am J Epidemiol. 2003;158(12):1193-201.
21. Tokar EJ, Person RJ, Sun Y, Perantoni AO, Waalkes MP. Chronic exposure of renal stem cells to inorganic arsenic induces a cancer phenotype. Chem Res Toxicol. 2013;26(1):96-105.
22. Nagata S. Apoptotic DNA fragmentation. Exp Cell Res. 2000;256(1):12-8.
23. Nalabothula N, McVicker G, Maiorano J, Martin R, Pritchard JK, Fondufe-Mittendorf YN. The chromatin architectural proteins HMGD1 and H1 bind reciprocally and have opposite effects on chromatin structure and gene regulation. BMC Genomics. 2014;15:92.
24. Woodcock CL, Skoultchi AI, Fan Y. Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res Int J Molecular Supramolecular Evol Aspects Chromosome Biol. 2006;14(1):17-25.
25. Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, Kraus WL. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science. 2008;319(5864):819-21.
26. Ragab A, Thompson EC, Travers AA. High mobility group proteins HMGD and HMGZ interact genetically with the Brahma chromatin remodeling complex in Drosophila. Genetics. 2006;172(2):1069-78.
27. Zhou X, Sun X, Cooper KL, Wang F, Liu KJ, Hudson LG. Arsenite interacts selectively with zinc finger proteins containing C3H1 or C4 motifs. J Biol Chem. 2011;286(26):22855-63.
28. Sun X, Zhou X, Du L, Liu W, Liu Y, Hudson LG, et al. Arsenite binding-induced zinc loss from PARP-1 is equivalent to zinc deficiency in reducing PARP-1 activity, leading to inhibition of DNA repair. Toxicol Appl Pharmacol. 2014;274(2):313-8.
29. Hays AM, Lantz RC, Rodgers LS, Sollome JJ, Vaillancourt RR, Andrew AS, et al. Arsenic-induced decreases in the vascular matrix. Toxicol Pathol. 2008;36(6):805-17.
30. Posey T, Weng T, Chen Z, Chintagari NR, Wang P, Jin N, et al. Arsenic-induced changes in the gene expression of lung epithelial L2 cells: implications in carcinogenesis. BMC Genomics. 2008;9:115.
31. Mi H, Muruganujan A, Thomas PD. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res. 2013;41(Database issue):D377-86.
32. States JC, Barchowsky A, Cartwright IL, Reichard JF, Futscher BW, Lantz RC. Arsenic toxicology: translating between experimental models and human pathology. Environ Health Perspect. 2011;119(10):1356-63.
33. Zhou X, Sun X, Mobarak C, Gandolfi AJ, Burchiel SW, Hudson LG, et al. Differential binding of monomethylarsonous acid compared to arsenite and arsenic trioxide with zinc finger peptides and proteins. Chem Res Toxicol. 2014;27(4):690-8.
34. Flight RM, Harrison BJ, Mohammad F, Bunge MB, Moon LD, Petruska JC, et al. categoryCompare, an analytical tool based on feature annotations. Front Genet. 2014;5:98.
35. Trabosh VA, Divito KA, DA B, Simbulan-Rosenthal CM, Rosenthal DS. Sequestration of E12/E47 and suppression of p27KIP1 play a role in Id2-induced proliferation and tumorigenesis. Carcinogenesis. 2009;30(7):1252-9.
36. Nik AM, Reyahi A, Ponten F, Carlsson P. Foxf2 in intestinal fibroblasts reduces numbers of Lgr5 (+) stem cells and adenoma formation by inhibiting Wnt signaling. Gastroenterology. 2013;144(5):1001-11.
37. Kong PZ, Yang F, Li L, Li XQ, Feng YM. Decreased FOXF2 mRNA expression indicates early-onset metastasis and poor prognosis for breast cancer patients with histological grade II tumor. PLoS One. 2013;8(4):e61591.
38. Wang Y, Zhou Y, Graves DT. FOXO transcription factors: their clinical significance and regulation. BioMed Res Int. 2014;2014:925350.
39. Kobayashi W, Ozawa M. The transcription factor LEF-1 induces an epithelial-mesenchymal transition in MDCK cells independent of beta-catenin. Biochem Biophys Res Commun. 2013;442(1-2):133-8.
40. Dai W, Wang F, He L, Lin C, Wu S, Chen P, et al. Genistein inhibits hepatocellular carcinoma cell migration by reversing the epithelial-mesenchymal transition: Partial mediation by the transcription factor NFAT. Mol Carcinog 2013, Nov 14. doi:10.1002/mc.22100.
41. Zheng R, Blobel GA. GATA transcription factors and cancer. Genes Cancer. 2010;1(12):1178-88.
42. Zabuawala T, Taffany DA, Sharma SM, Merchant A, Adair B, Srinivasan R, et al. An ets2-driven transcriptional program in tumor-associated macrophages promotes tumor metastasis. Cancer Res. 2010;70(4):1323-33.
43. Mok SC, Bonome T, Vathipadiekal V, Bell A, Johnson ME, Wong KK, et al. A gene signature predictive for outcome in advanced ovarian cancer identifies a survival factor: microfibril-associated glycoprotein 2. Cancer Cell. 2009;16(6):521-32.
44. Albig AR, Becenti DJ, Roy TG, Schiemann WP. Microfibril-associate glycoprotein-2 (MAGP-2) promotes angiogenic cell sprouting by blocking notch signaling in endothelial cells. Microvasc Res. 2008;76(1):7-14.
45. Miyamoto A, Lau R, Hein PW, Shipley JM, Weinmaster G. Microfibrillar proteins MAGP-1 and MAGP-2 induce Notch1 extracellular domain dissociation and receptor activation. J Biol Chem. 2006;281(15):10089-97.
46. Sharma S, Salehi F, Scheithauer BW, Rotondo F, Syro LV, Kovacs K. Role of MGMT in tumor development, progression, diagnosis, treatment and prognosis. Anticancer Res. 2009;29(10):3759-68.
47. Yang S, Yan HL, Tao QF, Yuan SX, Tang GN, Yang Y, et al. Low CADM2 expression predicts high recurrence risk of hepatocellular carcinoma patients after hepatectomy. J Cancer Res Clin Oncol. 2014;140(1):109-16.
48. Severson PL, Tokar EJ, Vrba L, Waalkes MP, Futscher BW. Coordinate H3K9 and DNA methylation silencing of ZNFs in toxicant-induced malignant transformation. Epigenetics Off J DNA Methylation Soc. 2013;8(10):1080-8.
49. Qiu C, Wang D, Wang E, Cui Q. An upstream interacting context based framework for the computational inference of microRNA functions. Mol BioSyst. 2012;8(5):1492-8.
50. Xu Y, Tokar EJ, Person RJ, Orihuela RG, Ngalame NN, Waalkes MP. Recruitment of normal stem cells to an oncogenic phenotype by noncontiguous carcinogen-transformed epithelia depends on the transforming carcinogen. Environ Health Perspect. 2013;121(8):944-50.
51. Lee MY, Shen MR. Epithelial-mesenchymal transition in cervical carcinoma. Am J Transl Res. 2012;4(1):1-13.
52. Li J, Zhou BP. Activation of β-catenin and AKT pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer. 2011;11:49.
53. Xiao W, Zhou S, Hu H, Li H, He G, Liu Y, et al. Nogo-B promotes the epithelial-mesenchymal transition in HeLa cervical cancer cells via Fibulin-5. Oncol Rep. 2013;29(1):109-16.
54. Banno K, Iida M, Yanokura M, Kisu I, Iwata T, Tominaga E, et al. MicroRNA in cervical cancer: OncomiRs and tumor suppressor miRs in diagnosis and treatment. ScientificWorldJournal. 2014, doi:10.1155/2014/178075.
55. Tian X, Zhang S, Liu HM, Zhang YB, Blair CA, Mercola D, et al. Histone lysine-specific methyltransferases and demethylases in carcinogenesis: new targets for cancer therapy and prevention. Curr Cancer Drug Targets. 2013;13(5):558-79.
56. Chervona Y, Arita A, Costa M. Carcinogenic metals and the epigenome: understanding the effect of nickel, arsenic, and chromium. Metallomics Integrated Biometal Sci. 2012;4(7):619-27.
57. Chanda S, Dasgupta UB, Guhamazumder D, Gupta M, Chaudhuri U, Lahiri S, et al. DNA hypermethylation of promoter of gene p53 and p16 in arsenic-exposed people with and without malignancy. Toxicol Sci Off J Soc Toxicol. 2006;89(2):431-7.
58. Liang YJ, Wang QY, Zhou CX, Yin QQ, He M, Yu XT, et al. MiR-124 targets Slug to regulate epithelial-mesenchymal transition and metastasis of breast cancer. Carcinogenesis. 2013;34(3):713-22.
59. Lu Y, Lu J, Li X, Zhu H, Fan X, Zhu S, et al. MiR-200a inhibits epithelial-mesenchymal transition of pancreatic cancer stem cell. BMC Cancer. 2014;14:85.
60. Ye F, Tang H, Liu Q, Xie X, Wu M, Liu X, et al. miR-200b as a prognostic factor in breast cancer targets multiple members of RAB family. J Transl Med. 2014;12:17.
61. Ding XM. MicroRNAs: regulators of cancer metastasis and epithelial-mesenchymal transition (EMT). Chinese J Cancer. 2014;33(3):140-7.
62. Chen DQ, Pan BZ, Huang JY, Zhang K, Cui SY, De W, et al. HDAC 1/4-mediated silencing of microRNA-200b promotes chemoresistance in human lung adenocarcinoma cells. Oncotarget 2014.
63. Shukla S, Oberdoerffer S. Co-transcriptional regulation of alternative pre-mRNA splicing. Biochim Biophys Acta. 2012;1819(7):673-83.
64. Tilgner H, Knowles DG, Johnson R, Davis CA, Chakrabortty S, Djebali S, et al. Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs. Genome Res. 2012;22(9):1616-25.
65. Zhao R, Hou Y, Xue P, Woods CG, Fu J, Feng B, et al. Long isoforms of NRF1 contribute to arsenic-induced antioxidant response in human keratinocytes. Environ Health Perspect. 2011;119(1):56-62.
66. Zhang Y, Beezhold K, Castranova V, Shi X, Chen F. Characterization of an alternatively spliced GADD45alpha, GADD45alpha1 isoform, in arsenic-treated epithelial cells. Mol Carcinog. 2009;48(5):454-64.
67. Mastrangelo AM, Marone D, Laido G, De Leonardis AM, De Vita P. Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity. Plant Sci Int J Experimental Plant Biol. 2012;185-186:40-9.
68. Zhou GB, Zhang J, Wang ZY, Chen SJ, Chen Z. Treatment of acute promyelocytic leukaemia with all-trans retinoic acid and arsenic trioxide: a paradigm of synergistic molecular targeting therapy. Philos Trans R Soc Lond B Biol Sci. 2007;362(1482):959-71.
69. Teves SS, Henikoff S. Salt fractionation of nucleosomes for genome-wide profiling. Methods Mol Biol. 2012;833:421-32.
70. Collins JA, Schandi CA, Young KK, Vesely J, Willingham MC. Major DNA fragmentation is a late event in apoptosis. J Histochemist Cytochemist Off J Histochemist Soc. 1997;45(7):923-34.
71. Shi L, Jones WD, Jensen RV, Harris SC, Perkins RG, Goodsaid FM, et al. The balance of reproducibility, sensitivity, and specificity of lists of differentially expressed genes in microarray studies. BMC Bioinformatics. 2008;9 Suppl 9:S10.
72. Mi H, Muruganujan A, Casagrande JT, Thomas PD. Large-scale gene function analysis with the PANTHER classification system. Nat Protoc. 2013;8(8):1551-66.
73. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27-30.
74. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-50.