Cell cycle changes mediated by the p53/miR-34c axis are involved in the malignant transformation of human bronchial epithelial cells by benzo[a]pyrene

Toxicology Letters

Volumn 225, Issue 2, 2014, Pages 275-284

  Han, Zhuyu ^a   Zhang, Ying ^b   Xu, Yuan ^a,c   Ji, Jie ^a   Xu, Wenchao ^a,c   Zhao, Yue ^a,c   Luo, Fei ^a,c   Wang, Bairu ^a,c   Bian, Qian ^b   Liu, Qizhan ^a,c  

^a NANJING MEDICAL UNIVERSITY   (China)

^b JIANGSU PROVINCIAL CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^c Nanjing Medical University   (China)

Author keywords

Benzo a pyrene (BaP); Cell cycle; Malignant transformation; MiR 34c; P53

Indexed keywords

BENZO[A]PYRENE; CYCLIN D; MICRORNA; MICRORNA 34A; MICRORNA 34C; PROTEIN P53; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ARTICLE; BRONCHUS; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL MIGRATION; CELL TRANSFORMATION; COLONY FORMATION; EPITHELIUM CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; MALIGNANT TRANSFORMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION;

BENZO[A]PYRENE (BAP); CELL CYCLE; MALIGNANT TRANSFORMATION; MIR-34C; P53;

BENZO(A)PYRENE; CELL CYCLE; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN D1; EPITHELIAL CELLS; GENE SILENCING; HUMANS; MICRORNAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84892446850     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.12.008     Document Type: Article

References (57)

1. An W.C., Li X.M. Phosphate adsorption characteristics at the sediment-water interface and phosphorus fractions in Nansi Lake, China, and its main inflow rivers. Environmental Monitoring and Assessment 2009, 148:173-184.
2. Anna L., Holmila R., Kovacs K., Gyorffy E., Gyori Z., Segesdi J., Minarovits J., Soltesz I., Kostic S., Csekeo A., Husgafvel-Pursiainen K., Schoket B. Relationship between TP53 tumour suppressor gene mutations and smoking-related bulky DNA adducts in a lung cancer study population from Hungary. Mutagenesis 2009, 24:475-480.
3. Aylon Y., Oren M. Living with p53, dying of p53. Cell 2007, 130:597-600.
4. Bommer G.T., Gerin I., Feng Y., Kaczorowski A.J., Kuick R., Love R.E., Zhai Y., Giordano T.J., Qin Z.S., Moore B.B., MacDougald O.A., Cho K.R., Fearon E.R. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Current Biology 2007, 17:1298-1307.
5. Caino M.C., Oliva J.L., Jiang H., Penning T.M., Kazanietz M.G. Benzo[a]pyrene-7,8-dihydrodiol promotes checkpoint activation and G2/M arrest in human bronchoalveolar carcinoma H358 cells. Molecular Pharmacology 2007, 71:744-750.
6. Calin G.A., Croce C.M. MicroRNA-cancer connection: the beginning of a new tale. Cancer Research 2006, 66:7390-7394.
7. Chang T.C., Wentzel E.A., Kent O.A., Ramachandran K., Mullendore M., Lee K.H., Feldmann G., Yamakuchi M., Ferlito M., Lowenstein C.J., Arking D.E., Beer M.A., Maitra A., Mendell J.T. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Molecular Cell 2007, 26:745-752.
8. Chen S., Nguyen N., Tamura K., Karin M., Tukey R.H. The role of the Ah receptor and p38 in benzo[a]pyrene-7,8-dihydrodiol and benzo[a]pyrene-7,8-dihydrodiol-9,10-epoxide-induced apoptosis. The Journal of Biological Chemistry 2003, 278:19526-19533.
9. Chen W., Xu X., Bai L., Padilla M.T., Gott K.M., Leng S., Tellez C.S., Wilder J.A., Belinsky S.A., Scott B.R., Lin Y. Low-dose gamma-irradiation inhibits IL-6 secretion from human lung fibroblasts that promotes bronchial epithelial cell transformation by cigarette-smoke carcinogen. Carcinogenesis 2012, 33:1368-1374.
10. Cheng A.M., Byrom M.W., Shelton J., Ford L.P. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Research 2005, 33:1290-1297.
11. Corney D.C., Flesken-Nikitin A., Godwin A.K., Wang W., Nikitin A.Y. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Research 2007, 67:8433-8438.
12. Cox A.D., Der C.J. Biological assays for cellular transformation. Methods in Enzymology 1994, 238:277-294.
13. DeCastro A.J., Dunphy K.A., Hutchinson J., Balboni A.L., Cherukuri P., Jerry D.J., DiRenzo J. MiR203 mediates subversion of stem cell properties during mammary epithelial differentiation via repression of DeltaNP63alpha and promotes mesenchymal-to-epithelial transition. Cell Death & Disease 2013, 4:e514.
14. Ding J., Ning B., Gong W., Wen W., Wu K., Liang J., He G., Huang S., Sun W., Han T., Huang L., Cao G., Wu M., Xie W., Wang H. Cyclin D1 induction by benzo[a]pyrene-7,8-diol-9,10-epoxide via the phosphatidylinositol 3-kinase/Akt/MAPK- and p70s6k-dependent pathway promotes cell transformation and tumorigenesis. The Journal of Biological Chemistry 2009, 284:33311-33319.
15. Dreij K., Rhrissorrakrai K., Gunsalus K.C., Geacintov N.E., Scicchitano D.A. Benzo[a]pyrene diol epoxide stimulates an inflammatory response in normal human lung fibroblasts through a p53 and JNK mediated pathway. Carcinogenesis 2010, 31:1149-1157.
16. Du H.J., Tang N., Liu B.C., You B.R., Shen F.H., Ye M., Gao A., Huang C. Benzo[a]pyrene-induced cell cycle progression is through ERKs/cyclin D1 pathway and requires the activation of JNKs and p38 mapk in human diploid lung fibroblasts. Molecular and Cellular Biochemistry 2006, 287:79-89.
17. Duan Z., Choy E., Harmon D., Liu X., Susa M., Mankin H., Hornicek F. MicroRNA-199a-3p is downregulated in human osteosarcoma and regulates cell proliferation and migration. Molecular Cancer Therapeutics 2011, 10:1337-1345.
18. Evans C.D., LaDow K., Schumann B.L., Savage R.E., Caruso J., Vonderheide A., Succop P., Talaska G. Effect of arsenic on benzo[a]pyrene DNA adduct levels in mouse skin and lung. Carcinogenesis 2004, 25:493-497.
19. Feng Z., Zhang C., Wu R., Hu W. Tumor suppressor p53 meets microRNAs. Journal of Molecular Cell Biology 2011, 3:44-50.
20. Garzon R., Fabbri M., Cimmino A., Calin G.A., Croce C.M. MicroRNA expression and function in cancer. Trends in Molecular Medicine 2006, 12:580-587.
21. Guimaraes D.P., Hainaut P. TP53: a key gene in human cancer. Biochimie 2002, 84:83-93.
22. He L., He X., Lim L.P., de Stanchina E., Xuan Z., Liang Y., Xue W., Zender L., Magnus J., Ridzon D., Jackson A.L., Linsley P.S., Chen C., Lowe S.W., Cleary M.A., Hannon G.J. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447:1130-1134.
23. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death and Differentiation 2010, 17:193-199.
24. IARC Pharmaceuticals. Volume 100A. A Review of Human Carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans/World Health Organization 2012, 1-401. International Agency for Research on Cancer.
25. Javeri A., Ghaffarpour M., Taha M.F., Houshmand M. Downregulation of miR-34a in breast tumors is not associated with either p53 mutations or promoter hypermethylation while it correlates with metastasis. Medical Oncology 2013, 30:413.
26. Kastan M.B. Wild-type p53: tumors can't stand it. Cell 2007, 128:837-840.
27. Kato M., Slack F.J. microRNAs: small molecules with big roles - C. elegans to human cancer. Biology of the cell/under the auspices of the European Cell Biology Organization 2008, 100:71-81.
28. Kim J.K., Diehl J.A. Nuclear cyclin D1: an oncogenic driver in human cancer. Journal of Cellular Physiology 2009, 220:292-296.
29. Lai T.J., Tsai Y.Y., Cheng Y.W., Chiang C.C., Lee H., Chou M.C., Chang J.H. An association between BPDE-like DNA adduct levels and P53 gene mutation in pterygium. Molecular Vision 2006, 12:1687-1691.
30. Laposa R.R., Feeney L., Crowley E., de Feraudy S., Cleaver J.E. p53 suppression overwhelms DNA polymerase eta deficiency in determining the cellular UV DNA damage response. DNA Repair 2007, 6:1794-1804.
31. Leger C., Drobetsky E.A. Modulation of the DNA damage response in UV-exposed human lymphoblastoid cells through genetic-versus functional-inactivation of the p53 tumor suppressor. Carcinogenesis 2002, 23:1631-1639.
32. Li D., Wang Q., Liu C., Duan H., Zeng X., Zhang B., Li X., Zhao J., Tang S., Li Z., Xing X., Yang P., Chen L., Zeng J., Zhu X., Zhang S., Zhang Z., Ma L., He Z., Wang E., Xiao Y., Zheng Y., Chen W. Aberrant expression of miR-638 contributes to benzo(a)pyrene-induced human cell transformation. Toxicological Sciences 2012, 125:382-391.
33. Li Y., Xu Y., Ling M., Yang Y., Wang S., Li Z., Zhou J., Wang X., Liu Q. mot-2-Mediated cross talk between nuclear factor-B and p53 is involved in arsenite-induced tumorigenesis of human embryo lung fibroblast cells. Environmental Health Perspectives 2010, 118:936-942.
34. Ling M., Li Y., Xu Y., Pang Y., Shen L., Jiang R., Zhao Y., Yang X., Zhang J., Zhou J., Wang X., Liu Q. Regulation of miRNA-21 by reactive oxygen species-activated ERK/NF-kappaB in arsenite-induced cell transformation. Free Radical Biology & Medicine 2012, 52:1508-1518.
35. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
36. Ma L., Li N., He X., Zhang Q. miR-449b and miR-34c on inducing down-regulation of cell cycle-related proteins and cycle arrests in SKOV3-ipl cell, an ovarian cancer cell line. Beijing da xue xue bao Yi xue ban=Journal of Peking University Health Sciences 2011, 43:129-133.
37. Maier A., Schumann B.L., Chang X., Talaska G., Puga A. Arsenic co-exposure potentiates benzo[a]pyrene genotoxicity. Mutation Research 2002, 517:101-111.
38. Mukherjee J.J., Sikka H.C. Attenuation of BPDE-induced p53 accumulation by TPA is associated with a decrease in stability and phosphorylation of p53 and downregulation of NFkappaB activation: role of p38 MAP kinase. Carcinogenesis 2006, 27:631-638.
39. Nekanti U., Dastidar S., Venugopal P., Totey S., Ta M. Increased proliferation and analysis of differential gene expression in human Wharton's jelly-derived mesenchymal stromal cells under hypoxia. International Journal of Biological Sciences 2010, 6:499-512.
40. Pang Y., Lai Y., Xiao Y., Li W., Ma R., Wang Q., Wei Q., Lin Y., Li D., Tang S., Chen L., Yang P., Li Z., Wu D., Lin Z., Chen W. Metabolic activation of benzo(a)pyrene enhanced transformation of human bronchial epithelium cell HBETR. Wei sheng yan jiu=Journal of Hygiene Research 2009, 38:645-648.
41. Pang Y., Xu Y., Li H., Li Y., Zhao Y., Jiang R., Shen L., Zhou J., Wang X., Liu Q. The inhibition of HIF-2alpha on the ATM/Chk-2 pathway is involved in the promotion effect of arsenite on benzo(a)pyrene-induced cell transformation. Toxicology Letters 2013, 218:105-117.
42. Pietsch E.C., Sykes S.M., McMahon S.B., Murphy M.E. The p53 family and programmed cell death. Oncogene 2008, 27:6507-6521.
43. Schar P. Spontaneous DNA damage, genome instability, and cancer - when DNA replication escapes control. Cell 2001, 104:329-332.
44. Shen Y.L., Jiang Y.G., Greenlee A.R., Zhou L.L., Liu L.H. MicroRNA expression profiles and miR-10a target in anti-benzo[a] pyrene-7,8-diol-9,10-epoxide-transformed human 16HBE cells. Biomedical and Environmental Sciences: BES 2009, 22:14-21.
45. Solhaug A., Ovrebo S., Mollerup S., Lag M., Schwarze P.E., Nesnow S., Holme J.A. Role of cell signaling in B[a]P-induced apoptosis: characterization of unspecific effects of cell signaling inhibitors and apoptotic effects of B[a]P metabolites. Chemico-Biological Interactions 2005, 151:101-119.
46. Tellez C.S., Juri D.E., Do K., Bernauer A.M., Thomas C.L., Damiani L.A., Tessema M., Leng S., Belinsky S.A. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Research 2011, 71:3087-3097.
47. Teodoro J.G., Evans S.K., Green M.R. Inhibition of tumor angiogenesis by p53: a new role for the guardian of the genome. Journal of Molecular Medicine (Berlin) 2007, 85:1175-1186.
48. Wang A., Gu J., Judson-Kremer K., Powell K.L., Mistry H., Simhambhatla P., Aldaz C.M., Gaddis S., MacLeod M.C. Response of human mammary epithelial cells to DNA damage induced by BPDE: involvement of novel regulatory pathways. Carcinogenesis 2003, 24:225-234.
49. Wei J., Shi Y., Zheng L., Zhou B., Inose H., Wang J., Guo X.E., Grosschedl R., Karsenty G. miR-34s inhibit osteoblast proliferation and differentiation in the mouse by targeting SATB2. Journal of Cell Biology 2012, 197:509-521.
50. Wester P.W., Muller J.J., Slob W., Mohn G.R., Dortant P.M., Kroese E.D. Carcinogenic activity of benzo[a]pyrene in a 2 year oral study in Wistar rats. Food and Chemical Toxicology 2012, 50:927-935.
51. Xu Y., Li Y., Pang Y., Ling M., Shen L., Jiang R., Zhao Y., Zhou J., Wang X., Liu Q. Blockade of p53 by HIF-2alpha, but not HIF-1alpha, is involved in arsenite-induced malignant transformation of human bronchial epithelial cells. Archives of Toxicology 2012, 86:947-959.
52. Xue W., Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicology and Applied Pharmacology 2005, 206:73-93.
53. Yan C. Post-translational modification of p53 by ubiquitin. Methods in Molecular Biology 2010, 647:305-315.
54. Yohena T., Yoshino I., Takenaka T., Ohba T., Kouso H., Osoegawa A., Hamatake M., Oda S., Kuniyoshi Y., Maehara Y. Relationship between the loss of heterozygosity and tobacco smoking in pulmonary adenocarcinoma. Oncology Research 2007, 16:333-339.
55. Zhao J., Lammers P., Torrance C.J., Bader A.G. TP53-independent function of miR-34a via HDAC1 and p21. Molecular Therapy 2013.
56. Zhao Y., Xu Y., Li Y., Xu W., Luo F., Wang B., Pang Y., Xiang Q., Zhou J., Wang X., Liu Q. NF-kappaB-mediated inflammation leading to EMT via miR-200c is involved in cell transformation induced by cigarette smoke extract. Toxicological Sciences 2013.
57. Zheng T., Meng X., Wang J., Chen X., Yin D., Liang Y., Song X., Pan S., Jiang H., Liu L. PTEN- and p53-mediated apoptosis and cell cycle arrest by FTY720 in gastric cancer cells and nude mice. Journal of Cellular Biochemistry 2010, 111:218-228.