Pulmonary gene and microRNA expression changes in mice exposed to benzo(a)pyrene by oral gavage

Toxicology

Volumn 285, Issue 3, 2011, Pages 133-141

  Halappanavar, Sabina ^a   Wu, Dongmei ^a   Williams, Andrew ^a   Kuo, Byron ^a   Godschalk, Roger W ^b   Van Schooten, Frederik J ^b   Yauk, Carole Lyn ^a  

^a HEALTH CANADA   (Canada)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

B cell receptor signalling; Gene expression; MicroRNA; Polycyclic aromatic hydrocarbon

Indexed keywords

BENZO[A]PYRENE; MESSENGER RNA; MICRORNA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; IMMUNOTOXICITY; LIVER; LUNG; LUNG CANCER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA SYNTHESIS; UPREGULATION;

ADMINISTRATION, ORAL; ANIMALS; BENZO(A)PYRENE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; GENE EXPRESSION PROFILING; LUNG; MALE; MICE; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA;

MUS;

EID: 79957824357     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.04.011     Document Type: Article

References (57)

1. Alvo M., Liu Z., Williams A., Yauk C. Testing for mean and correlation changes in microarray experiments: an application for pathway analysis. BMC Bioinformatics 2010, 11:60.
2. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 1995, 57:289-300.
3. Bice D.E., Harris D.L., Hill J.O., Muggenburg B.A. Local and systemic immunity following localized deposition of antigen in the lung. Chest 1979, 75:246-248.
4. Bice D.E., Harris D.L., Schnizlein C.T., Mauderly J.L. Methods to evaluate the effects of toxic materials deposited in the lung on immunity in lung-associated lymph nodes. Drug and Chemical Toxicology 1979, 2:35-47.
5. Bolstad B.M., Irizarry R.A., Astrand M., Speed T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics (Oxford, England) 2003, 19:185-193.
6. Boysen G., Hecht S.S. Analysis of DNA and protein adducts of benzo[a]pyrene in human tissues using structure-specific methods. Mutation Research 2003, 543:17-30.
7. Calin G.A., Ferracin M., Cimmino A., Di Leva G., Shimizu M., Wojcik S.E., Iorio M.V., Visone R., Sever N.I., Fabbri M., Iuliano R., Palumbo T., Pichiorri F., Roldo C., Garzon R., Sevignani C., Rassenti L., Alder H., Volinia S., Liu C.G., Kipps T.J., Negrini M., Croce C.M. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. The New England Journal of Medicine 2005, 353:1793-1801.
8. Cannell I.G., Bushell M. Regulation of Myc by miR-34c: a mechanism to prevent genomic instability?. Cell Cycle 2010, (Georgetown, Tex 9).
9. Cannell I.G., Kong Y.W., Bushell M. How do microRNAs regulate gene expression?. Biochemical Society Transactions 2008, 36:1224-1231.
10. Castro D.J., Lohr C.V., Fischer K.A., Pereira C.B., Williams D.E. Lymphoma and lung cancer in offspring born to pregnant mice dosed with dibenzo[a,l]pyrene: the importance of in utero vs. lactational exposure. Toxicology and Applied Pharmacology 2008, 233:454-458.
11. Conney A.H. Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons: G.H.A. Clowes Memorial Lecture. Cancer Research 1982, 42:4875-4917.
12. Cui X., Qiu J.T.H.J., Blades N.J., Churchill G.A. Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 2005, 59-75. (Oxford, England).
13. Cummins J.M., He Y., Leary R.J., Pagliarini R., Diaz L.A., Sjoblom T., Barad O., Bentwich Z., Szafranska A.E., Labourier E., Raymond C.K., Roberts B.S., Juhl H., Kinzler K.W., Vogelstein B., Velculescu V.E. The colorectal microRNAome. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:3687-3692.
14. De Abrew K.N., Kaminski N.E., Thomas R.S. An integrated genomic analysis of aryl hydrocarbon receptor-mediated inhibition of B-cell differentiation. Toxicological Sciences 2010, 118:454-469.
15. Fabian M.R., Sonenberg N., Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annual Review of Biochemistry 2010, 79:351-379.
16. Friedman R.C., Farh K.K., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Research 2009, 19:92-105.
17. Gelboin H.V. Benzo[alpha]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiological Reviews 1980, 60:1107-1166.
18. Godschalk R.W., Maas L.M., Van Zandwijk N., van't Veer L.J., Breedijk A., Borm P.J., Verhaert J., Kleinjans J.C., van Schooten F.J. Differences in aromatic-DNA adduct levels between alveolar macrophages and subpopulations of white blood cells from smokers. Carcinogenesis 1998, 19:819-825.
19. Gunning W.T., Kramer P.M., Lubet R.A., Steele V.E., End D.W., Wouters W., Pereira M.A. Chemoprevention of benzo(a)pyrene-induced lung tumors in mice by the farnesyltransferase inhibitor R115777. Clinical Cancer Research 2003, 9:1927-1930.
20. Harrigan J.A., Vezina C.M., McGarrigle B.P., Ersing N., Box H.C., Maccubbin A.E., Olson J.R. DNA adduct formation in precision-cut rat liver and lung slices exposed to benzo[a]pyrene. Toxicological Sciences 2004, 77:307-314.
21. Harrigan J.A., McGarrigle B.P., Sutter T.R., Olson J.R. Tissue specific induction of cytochrome P450 (CYP) 1A1 and 1B1 in rat liver and lung following in vitro (tissue slice) and in vivo exposure to benzo(a)pyrene. Toxicology In Vitro 2006, 20:426-438.
22. Hockley S.L., Arlt V.M., Brewer D., Giddings I., Phillips D.H. Time- and concentration-dependent changes in gene expression induced by benzo(a)pyrene in two human cell lines, MCF-7 and HepG2. BMC Genomics 2006, 7:260.
23. Hockley S.L., Arlt V.M., Jahnke G., Hartwig A., Giddings I., Phillips D.H. Identification through microarray gene expression analysis of cellular responses to benzo(a)pyrene and its diol-epoxide that are dependent or independent of p53. Carcinogenesis 2008, 29:202-210.
24. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 2009, 4:44-57.
25. IARC Certain polycyclic aromatic hydrocarbons and heterocyclic compounds. IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Man 1973, International Agency for Research on Cancer (IARC), Lyon, France, pp. 91-136.
26. Jackson R.J., Standart N. How do microRNAs regulate gene expression?. Science's STKE 2007, re1.
27. Kaltreider H.B., Kyselka L., Salmon S.E. Immunology of the lower respiratory tract. II. The plaque-forming response of canine lymphoid tissues to sheep erythrocytes after intrapulmonary or intravenous immunization. The Journal of Clinical Investigation 1974, 54:263-270.
28. Katiyar S.K., Agarwal R., Mukhtar H. Protective effects of green tea polyphenols administered by oral intubation against chemical carcinogen-induced forestomach and pulmonary neoplasia in A/J mice. Cancer Letters 1993, 73:167-172.
29. Kerr M.K. Design considerations for efficient and effective microarray studies. Biometrics 2003, 59:822-828.
30. Kerr M.K., Churchill G.A. Statistical design and the analysis of gene expression microarray data. Genetical Research 2007, 89:509-514.
31. Keshava C., Whipkey D., Weston A. Transcriptional signatures of environmentally relevant exposures in normal human mammary epithelial cells: benzo[a]pyrene. Cancer Letters 2005, 221:201-211.
32. Levin W., Wood A., Chang R., Ryan D., Thomas P., Yagi H., Thakker D., Vyas K., Boyd C., Chu S.Y., Conney A., Jerina D. Oxidative metabolism of polycyclic aromatic hydrocarbons to ultimate carcinogens. Drug Metabolism Reviews 1982, 13:555-580.
33. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
34. Li Z., Fuscoe J.C., Chen T. MicroRNAs and their predicted target messenger RNAs are deregulated by exposure to a carcinogenic dose of comfrey in rat liver. Environmental and Molecular Mutagenesis 2011, doi:10.1002/em.20645.
35. Martensson I.L., Almqvist N., Grimsholm O., Bernardi A.I. The pre-B cell receptor checkpoint. FEBS Letters 2010, 584:2572-2579.
36. Masten S.A., Shiverick K.T. The Ah receptor recognizes DNA binding sites for the B cell transcription factor, BSAP: a possible mechanism for dioxin-mediated alteration of CD19 gene expression in human B lymphocytes. Biochemical and Biophysical Research Communications 1995, 212:27-34.
37. Merkerova M., Belickova M., Bruchova H. Differential expression of microRNAs in hematopoietic cell lineages. European Journal of Haematology 2008, 81:304-310.
38. Moffat I.D., Boutros P.C., Celius T., Linden J., Pohjanvirta R., Okey A.B. microRNAs in adult rodent liver are refractory to dioxin treatment. Toxicological Sciences 2007, 99:470-487.
39. Mott J.L., Kobayashi S., Bronk S.F., Gores G.J. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 2007, 26:6133-6140.
40. Near R.I., Matulka R.A., Mann K.K., Gogate S.U., Trombino A.F., Sherr D.H. Regulation of preB cell apoptosis by aryl hydrocarbon receptor/transcription factor-expressing stromal/adherent cells. Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine (New York, N.Y.) 1999, 221:242-252.
41. Pelkonen O., Nebert D.W. Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis. Pharmacological Reviews 1982, 34:189-222.
42. Pfaffl M.W., Horgan G.W., Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 2002, 30:e36.
43. Savage K.J., Monti S., Kutok J.L., Cattoretti G., Neuberg D., De Leval L., Kurtin P., Dal Cin P., Ladd C., Feuerhake F., Aguiar R.C., Li S., Salles G., Berger F., Jing W., Pinkus G.S., Habermann T., Dalla-Favera R., Harris N.L., Aster J.C., Golub T.R., Shipp M.A. The molecular signature of mediastinal large B-cell lymphoma differs from that of other diffuse large B-cell lymphomas and shares features with classical Hodgkin lymphoma. Blood 2003, 102:3871-3879.
44. Sempere L.F., Liu X., Dmitrovsky E. Tumor-suppressive microRNAs in lung cancer: diagnostic and therapeutic opportunities. TheScientificWorldJournal 2009, 9:626-628.
45. Shi Z., Dragin N., Miller M.L., Stringer K.F., Johansson E., Chen J., Uno S., Gonzalez F.J., Rubio C.A., Nebert D.W. Oral benzo[a]pyrene-induced cancer: two distinct types in different target organs depend on the mouse Cyp1 genotype. International Journal of Cancer 2010, 120:2334-2350.
46. Sulentic C.E., Holsapple M.P., Kaminski N.E. Aryl hydrocarbon receptor-dependent suppression by 2,3,7,8-tetrachlorodibenzo-p-dioxin of IgM secretion in activated B cells. Molecular Pharmacology 1998, 53:623-629.
47. TRDC R: A Language and Environment for Statistical Computing 2004.
48. Vaziri C., Faller D.V. A benzo[a]pyrene-induced cell cycle checkpoint resulting in p53-independent G1 arrest in 3T3 fibroblasts. The Journal of Biological Chemistry 1997, 272:2762-2769.
49. Vogel C.F., Li W., Sciullo E., Newman J., Hammock B., Reader J.R., Tuscano J., Matsumura F. Pathogenesis of aryl hydrocarbon receptor-mediated development of lymphoma is associated with increased cyclooxygenase-2 expression. The American Journal of Pathology 2007, 171:1538-1548.
50. Vorderstrasse B.A., Kerkvliet N.I. 2,3,7,8-Tetrachlorodibenzo-p-dioxin affects the number and function of murine splenic dendritic cells and their expression of accessory molecules. Toxicology and Applied Pharmacology 2001, 171:117-125.
51. Wattenberg L.W., Leong J.L. Inhibition of the carcinogenic action of benzo(a)pyrene by flavones. Cancer Research 1970, 30:1922-1925.
52. Wu H., Kerr K.M., Cui X., Churchill G.A. MAANOVA: A Software Package for the Analysis of Spotted cDNA Microarray Experiments 2003, pp. 313-341.
53. Xiao C., Calado D.P., Galler G., Thai T.H., Patterson H.C., Wang J., Rajewsky N., Bender T.P., Rajewsky K. miR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 2007, 131:146-159.
54. Yanaihara N., Caplen N., Bowman E., Seike M., Kumamoto K., Yi M., Stephens R.M., Okamoto A., Yokota J., Tanaka T., Calin G.A., Liu C.G., Croce C.M., Harris C.C. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006, 9:189-198.
55. Yauk C.L., Jackson K., Malowany M., Williams A. Lack of change in microRNA expression in adult mouse liver following treatment with benzo(a)pyrene despite robust mRNA transcriptional response. Mutation Research 2010, doi:10.1016/j.mrgentox.2010.02.012.
56. Zhao J.J., Lin J., Lwin T., Yang H., Guo J., Kong W., Dessureault S., Moscinski L.C., Rezania D., Dalton W.S., Sotomayor E., Tao J., Cheng J.Q. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood 2010, 115:2630-2639.
57. Zienolddiny S., Ryberg D., Svendsrud D.H., Eilertsen E., Skaug V., Hewer A., Phillips D.H., te Riele H., Haugen A. Msh2 deficiency increases susceptibility to benzo[a]pyrene-induced lymphomagenesis. International Journal of Cancer 2006, 118:2899-2902.