Arsenic exposure perturbs epithelial-mesenchymal cell transition and gene expression in a collagen gel assay

Toxicological Sciences

Volumn 116, Issue 1, 2010, Pages 273-285

  Lencinas, Alejandro ^a   Broka, Derrick M ^a   Konieczka, Jay H ^b   Klewer, Scott E ^c   Antin, Parker B ^a   Camenisch, Todd D ^a   Runyan, Raymond B ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Cardiac toxicity; Cytoscape; EMT; Heart development; Interactome; Microarray

Indexed keywords

ALPHA ACTININ 1; ARSENITE SODIUM; BETA TUBULIN 3; BIOLOGICAL MARKER; CD81 ANTIGEN; COLLAGEN GEL; COLONY STIMULATING FACTOR 2 RECEPTOR BETA; GROWTH ARREST SPECIFIC PROTEIN 7; HEPATOCYTE NUCLEAR FACTOR 3BETA; MYOSIN HEAVY CHAIN 1; MYOSIN HEAVY CHAIN 11; NEUROBLASTOMA RAS VIRAL PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; UNCLASSIFIED DRUG; ARSENIC; COLLAGEN; PRIMER DNA;

ANIMAL CELL; ARTICLE; ATRIOVENTRICULAR CANAL; CARDIOTOXICITY; CELL ADHESION; CHICK EMBRYO; CONTROLLED STUDY; CYTOSKELETON; DNA FRAGMENTATION; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HEART DEVELOPMENT; MICROARRAY ANALYSIS; NONHUMAN; ANIMAL; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; MESODERM; NICK END LABELING; NUCLEOTIDE SEQUENCE; TOXICITY;

ANIMALS; ARSENIC; BASE SEQUENCE; CHICK EMBRYO; COLLAGEN; DNA PRIMERS; EPITHELIAL CELLS; GENE EXPRESSION; IN SITU NICK-END LABELING; MESODERM;

EID: 77954371879     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq086     Document Type: Article

References (77)

1. Aggarwal, M., Wangikar, P. B., Sarkar, S. N., Rao, G. S., Kumar, D., Dwivedi, P., and Malik, J. K. (2007). Effects of low-level arsenic exposure on the developmental toxicity of anilofos in rats. J. Appl. Toxicol. 7, 255-261.
2. Alexander, S. M., Jackson, K. J., Bushnell, K. M., and McGuire, P. G. (1997). Spatial and temporal expression of the 72-kDa type IV collagenase (MMP-2) correlates with development and differentiation of valves in the embryonic avian heart. Dev. Dyn. 3, 261-268.
3. Arnoux, V., Come, C., Kusewitt, D. F., Hudson, L. G., and Savagner, P. (2005). Cutaneous wound reepithelialization: a partial and reversible EMT. In Rise and Fall of Epithelial Phenotype: Concepts of Epithelial-Mesenchymal Transition (P. Savagner, Ed.), pp. 111-134. Eurekah.com and Kluwer Academic/Plenum Publishers, New York.
4. Bates, M. N., Smith, A. H., and Hypenhay-Rich, C. (1992). Arsenic ingestion and internal cancer: a review. Am. J. Epidemiol. 1, 462-476.
5. Bolstad, B. M., Irizarry, R. A., Astrand, M., and Speed, T. P. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193.
6. Boyer, A. S., Ayerinskas, I. I., Vincent, E. B., McKinney, L., Weeks, D. L., and Runyan, R. B. (1999a). Complementary activities of TGFß2 and 3 in epithelial mesenchymal transformation in the embryonic heart. Dev. Biol. 208, 500-520.
7. Boyer, A. S., Ayerinskas, I. I., Vincent, E. B., McKinney, L. A., Weeks, D. L., and Runyan, R. B. (1999b). TGF beta 2 and TGF beta 3 have separate and sequential activities during epithelial-mesenchymal cell transformation in the embryonic heart. Developmental Biology 208, 530-545.
8. Boyer, A. S., Erickson, C. P., and Runyan, R. B. (1999c). Epithelialmesenchymal transformation in the embryonic heart is mediated through distinct pertussis toxin-sensitive and TGF beta signal transduction mechanisms. Dev. Dyn. 214, 81-91.
9. Brown, C. B., Boyer, A. S., Runyan, R. B., and Barnett, J. V. (1996). Antibodies to the type II TGF beta receptor block cell activation and migration during atrioventricular cushion transformation in the heart. Dev. Biol. 174, 248-257.
10. Campanaro, S., Picelli, S., Toregrossa, R., Colluto, L., Ceol, M., Del Prete, D., D'Angelo, A., Valle, G., and Anglani, F. (2007). Genes involved in TGFß1-driven epithelial-mesenchymal transition of renal epithelial cells are topologically related in the human interactome map. BMC Genomics 8, 383. doi:10.1186/1471-2164-8-383
11. Chang, C. P., Neilson, J. R., Bayle, J. H., Gestwicki, J. E., Kuo, A., Stankunas, K., Graef, I. A., and Crabtree, G. R. (2004). A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell 118, 649-663.
12. Chen, C. J., Chen, C. W., Wu, M. M., and Kuo, T. L. (1992). Cancer potential in liver, lung, bladder and kidney due to ingested inorganic arsenic in drinking water. Br. J. Cancer 66, 888-892.
13. Chen, C. J., Chuang, Y. C., Lin, T. M., and Wu, H. Y. (1985). Malignant neoplasms among residents of a blackfoot disease-endemic area in Taiwan: high-arsenic artesian well water and cancers. Cancer Res. 45, 5895-5899.
14. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., et al. (2007). Integration of biological networks and gene expression data using cytoscape. Nat. Protoc. 2, 2366-2382.
15. Dor, Y., Klewer, S. E., McDonald, J. A., Keshet, E., and Camenisch, T. D. (2003). VEGF modulates early heart valve formation. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 271, 202-208.
16. Enciso, J. M., Gratzinger, D., Camenisch, T. D., Canosa, S., Pinter, E., and Madri, J. A. (2003). Elevated glucose inhibits VEGF-A-mediated endocardial cushion formation: modulation by PECAM-1 and MMP-2. J. Cell Biol. 160, 605-615.
17. Engel, R. R., and Smith, A. H. (1994). Arsenic in drinking water and mortality from vascular disease: an ecologic analysis in 30 counties in the United States. Arch. Environ. Health 49, 418-427.
18. Fumal, I., Pierard-Franchimont, C., and Pierard, G. E. (2005). Arsenical keratoses and carcinomas. Rev. Med. Liege 60, 217-221.
19. Futschik, M. E., and Crompton, T. (2005). OLIN: optimized normalization, visualization and quality testing of two-channel microarray data. Bioinformatics 21, 1724-1726.
20. Graham-Evans, B., Cohly, H. H., Yu, H., and Tchounwou, P. B. (2004). Arsenic-induced genotoxic and cytotoxic effects in human keratinocytes, melanocytes and dentritic cells. Int. J. Environ. Res. Public Health 1, 83-89.
21. Hays, A. M., Lantz, R. C., Rodgers, L. S., Sollome, J. J., Vaillancourt, R. R., Andrew, A. S., Hamilton, J. W., and Camenisch, T. D. (2008). Arsenicinduced decreases in the vascular matrix. Toxicol. Pathol. 36, 805-817.
22. He, W., Greenwell, R. J., Brooks, D. M., Calderón-Garcidueñas, L., Beall, H. D., and Coffin, J. D. (2007). Arsenic exposure in pregnant mice disrupts placental vasculogenesis and causes spontaneous abortion. Toxicol. Sci. 99, 244-253.
23. Hill, D. S., Wlodarczyk, B. J., and Finnell, R. H. (2008). Reproductive consequences of oral arsenate exposure during pregnancy in a mouse model. Birth Defects Res. B 83, 40-47.
24. Ivanova, V. N., and Heia, T. K. (2006). Sodium arsenite accelerates TRAILmediated apoptosis in melanoma cells through upregulation of TRAIL-R1/R2 surface levels and downregulation of cFLIP expression. Exp. Cell Res. 312, 4120-4138.
25. Iwasaka, C., Tanaka, K., Abe, M., and Sato, Y. (1996). Ets-1 regulates angiogenesis by inducing the expression of urokinase-type plasminogen activator and matrix metalloproteinase-1 and the migration of vascular endothelial cells. J. Cell. Physiol. 169, 522-531.
26. Kao, Y. H., Yu, C. L., Chang, L. W., and Yu, H. S. (2003). Low concentrations of arsenic induce vascular endothelial growth factor and nitric oxide release and stimulate angiogenesis in vitro. Chem. Res. Toxicol. 16, 460-468.
27. Kestler, H. A., Müller, A., Kraus, J. M., Buchholz, M., Gress, T. M., Liu, H., Kane, D. W., Zeeberg, B. R., and Weinstein, J. N. (2008). VennMaster: areaproportional Euler diagrams for functional GO analysis of microarrays. BMC Genomics 29, 67.
28. Killcoyne, S., Carter, G. W., Smith, J., and Boyle, J. (2009). Cytoscape: a community-based framework for network modeling. Methods Mol. Biol. 563, 219-239.
29. Klymkowsky, M. W., and Savagner, P. (2009). Epithelial-mesenchymal transition: a cancer researcher's conceptual friend and foe. Am. J. Pathol. 174, 1588-1593.
30. Konieczka, J. H., Drew, K., Pine, A., Belasco, K., Davey, S., Yatskievych, T. A., Bonneau, R., and Antin, P. B. (2009). BioNetBuilder 2.0: bringing systems biology to chicken and other model organism. BMC Genomics 10, S6.
31. Krug, E. L., Mjaatvedt, C. H., and Markwald, R. R. (1987). Extracellular matrix from embryonic myocardium elicits an early morphogenetic event in cardiac endothelial differentiation. Dev Biol. 120, 348-355.
32. Li, C. H., and Loch-Caruso, R. (2007). Sodium arsenite inhibits migration of extravillous trophoblast cells in vitro. Reprod. Toxicol. 24, 296-302.
33. Lohrig, K., Müller, B., Davydova, J., Leister, D., and Wolters, D. A. (2009). Phosphorylation site mapping of soluble proteins: bioinformatical filtering reveals potential plastidic phosphoproteins in Arabidopsis thaliana. Planta 229, 1123-1134.
34. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell Stem Cell 5, 511-512.
35. Markwald, R. R., Fitzharris, T. P., and Manasek, F. J. (1977). Structural development of endocardial cushions. American Journal of Anatomy 148, 85-119.
36. McKeown, S. J., Lee, V. M., Bronner-Fraser, M., Newgreen, D. F., and Farlie, P. G. (2005). Sox10 overexpression induces neural crest-like cells from all dorsoventral levels of the neural tube but inhibits differentiation. Dev. Dyn. 233, 430-444.
37. Mercado-Pimentel, M. E., and Runyan, R. B. (2007). Multiple transforming growth factor-beta isoforms and receptors function during epithelial-mesenchymal cell transformation in the embryonic heart. Cells Tissues Organs 185, 146-156.
38. Milton, A. H., Smith, W., Rahman, B., Hasan, Z., Kulsum, U., Dear, K., Rakibuddin, M., and Ali, A. (2005). Chronic arsenic exposure and adverse pregnancy outcomes in Bangladesh. Epidemiology 16, 82-86.
39. Mjaatvedt, C. H., and Markwald, R. R. (1989). Induction of an epithelialmesenchymal transition by an in vivo adheron-like complex. Dev Biol. 136, 118-128.
40. Morandi, E., Severini, C., Quercioli, D., D'Ario, G., Perdichizzi, S., Capri, M., Farruggia, G., Mascolo, M. G., Horn, W., Vaccari, M., et al. (2008). Gene expression time-series analysis of camptothecin effects in U87-MG and DBTRG-05 glioblastoma cell lines. Mol. Cancer 11, 66.
41. Mousa, S. A., O'Connor, L., Rossman, T. G., and Block, E. (2007). Proangiogenesis action of arsenic and its reversal by selenium-derived compounds. Carcinogenesis 28, 962-967.
42. Murgo, A. J., McBee, W. L., and Cheson, B. D. (2000). Clinical trials referral resource. Clinical trials with arsenic trioxide. Oncology 2, 215-216; passim.
43. Nakaya, Y., and Sheng, G. (2008). Epithelial to mesenchymal transition during gastrulation: an embryological view. Dev. Growth Differ 50, 755.
44. Namgung, U., and Xia, Z. (2000). Arsenite-induced apoptosis in cortical neurons is mediated by c-Jun N-terminal protein kinase 3 and p38 mitogenactivated protein kinase. J. Nuerosci. 20, 6442-6451.
45. Olsen, C. E., Liguori, A. E., Zong, Y., Lantz, R. C., Burgess, J. L., and Boitano, S. (2008). Arsenic upregulates MMP-9 and inhibits wound repair in human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L293-L302.
46. Person, A. D., Klewer, S. E., and Runyan, R. B. (2005). Cell biology of cardiac cushion development. Int. Rev. Cytol. 243, 287-335.
47. Petrick, J. S., Blachere, F. M., Selmin, O., and Lantz, R. C. (2009). Inorganic arsenic as a developmental toxicant: in utero exposure and alterations in the developing rat lungs. Mol. Nutr. Food Res. 53, 583-591.
48. Potts, J. D., Dagle, J. M., Walder, J. A., Weeks, D. L., and Runyan, R. B. (1991). Epithelial-mesenchymal transformation of embryonic cardiac endothelial cells is inhibited by a modified antisense oligodeoxynucleotide to transforming growth factor beta 3. Proc. Natl. Acad. Sci. U.S.A. 88, 1516-1520.
49. Potts, J. D., and Runyan, R. B. (1989). Epithelial-mesenchymal cell transformation in the embryonic heart can be mediated, in part, by transforming growth factor β. Dev. Biol. 134, 392-401.
50. Potts, J. D., Vincent, E. B., Runyan, R. B., and Weeks, D. L. (1992). Sense and antisense TGF beta 3 mRNA levels correlate with cardiac valve induction. Dev. Dyn. 193, 340-345.
51. Rahman, A., Vahter, M., Ekström, E. C., Rahman, M., Golam Mustafa, A. H., Wahed, M. A., Yunus, M., and Persson, L. A. (2007). Association of arsenic exposure during pregnancy with fetal loss and infant death: a cohort study in Bangladesh. Am. J. Epidemiol. 165, 1389-1396.
52. Rea, M. A., Gregg, J. P., Qin, Q., Phillips, M. A., and Rice, R. H. (2003). Global alteration of gene expression in human keratinocytes by inorganic arsenic. Carcinogenesis 24, 747-756.
53. Rudge, C. V., Rollin, H. B., Nogueira, C. M., Thomassen, Y., Rudge, M. C., and Odland, J. (2009). The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J. Environ. Monit. 11, 1322-1330.
54. Runyan, R. B., and Markwald, R. R. (1983). Invasion of mesenchyme into three-dimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue. Dev. Biol. 95, 108-114.
55. Sarkar, F. H., Li, Y., Wang, Z., and Kong, D. (2009). Pancreatic cancer stem cells and EMT in drug resistance and metastasis. Minerva Chir. 64, 489-500.
56. Smith, A. H., Hopenhayn-Rich, C., Bates, M. N., Goeden, H. M., Hertz-Picciotto, I., Duggan, H. M., Wood, R., Kosnett, M. J., and Smith, M. T. (1992). Cancer risks from arsenic in drinking water. Environ. Health Perspect. 97, 259-267.
57. Smith, A. H., Lingas, E. O., and Rahman, M. (2000). Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull. World Health Organ. 78, 1093-1103.
58. Smyth, G. K., Yang, Y. H., and Speed, T. (2003). Statistical issues in cDNA microarray data analysis. Methods Mol. Biol. 224, 111-136.
59. Soucy, N. V., Ihnat, M. A., Kamat, C. D., Hess, L., Post, M. J., Klei, L. R., Clark, C., and Barchowsky, A. (2003). Arsenic stimulates angiogenesis and tumorigenesis in vivo. Toxicol. Sci. 76, 271-279.
60. Straub, A. C., Klei, L. R., Stolz, D. B., and Barchowsky, A. (2009). Arsenic requires sphingosine-1-phosphate type 1 receptors to induce angiogenic genes and endothelial cell remodeling. Am. J. Pathol. 174, 1949-1958.
61. Su, S. C., Mendoza, E. A., Kwak, H. I., and Bayless, K. J. (2008). Molecular profile of endothelial invasion of three-dimensional collagen matrices: insights into angiogenic sprout induction in wound healing. Am. J. Physiol. Cell Physiol. 295, C1215-C1229.
62. Tavares, A. L. P., Mercado-Pimentel, M. E., Runyan, R. B., and Kitten, G. T. (2006). TGF-mediated RhoA expression is necessary for epithelialmesenchymal transition in the embryonic chick heart. Dev. Dyn. 235, 1589-1598.
63. Timmerman, L. A., Grego-Bessa, J., Raya, A., Bertrán, E., Pérez-Pomares, J. M., Díez, J., Aranda, S., Palomo, S., McCormick, F., Izpisúa-Belmonte, J. C., et al. (2003). Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18, 99-115.
64. Tomasavic, S. P., and Welch, D. R. (1986). Heat stress proteins and experimental cancer metastasis. International Journal Hyperthermia 2, 253-266.
65. Trouba, K. J., Wauson, E. M., and Vorce, R. L. (2000). Sodium arsenite inhibits terminal differentiation of murine C3H 10T1/2 preadipocytes. Toxicol. Appl. Pharmacol. 168, 25-35.
66. Valentine, J. L., Kang, H. K., and Spivey, G. (1979). Arsenic levels in human blood, urine, and hair in response to exposure via drinking water. Environ. Res. 20, 24-32.
67. Wang, Z., and Rossman, T. G. (1995). The carcinogenicity of arsenic. In: Toxicology of Metals (L.W. Chang, Ed.), pp. 221-229. Lewis, Boca Raton, FL.
68. Wei, L. H., Lai, K. P., Chen, C. A., Cheng, C. H., Huang, Y. J., Chou, C. H., Kuo, M. L., and Hsieh, C. Y. (2005). Arsenic trioxide prevents radiationenhanced tumor invasiveness and inhibits matrix metalloproteinase-9 through downregulation of nuclear factor kappaB. Oncogene 24, 390-398.
69. Wendler, C. C., and Rivkees, S. A. (2006). Sphingosine-1-phosphate inhibits cell migration and endothelial to mesenchymal cell transformation during cardiac development. Dev. Biol. 291, 264-277.
70. Wu, M. M., Kuo, T. L., Hwang, Y. H., and Chen, C. J. (1989). Dose-response relation between arsenic concentration in well water and mortality from cancers and vascular disease. Am. J. Epidemiol. 130, 1123-1132.
71. Wu, Y., Moser, M., Bautch, V. L., and Patterson, C. (2003). HoxB5 is an upstream transcriptional switch for differentiation of the vascular endothelium from precursor cells. Mol. Cell Biol. 23, 5680-5691.
72. Yancy, S. L., Shelden, E. A., Gilmont, R. R., and Welsh, M. J. (2005). Sodium arsenite exposure alters cell migration, focal adhesion localization and decreases tyrosine phosphorylation of focal adhesion kinase in H9C2 myoblasts. Toxicol. Sci. 84, 278-286.
73. Yang, J., and Weinberg, R. A. (2008). Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829.
74. Yeung, N., Cline, M. S., Kuchinsky, A., Smoot, M. E., and Bader, G. D. (2008). Exploring biological networks with Cytoscape software. Curr. Protoc. Bioinformatics 23, 8.13.1-8.13.20.
75. Yu, H. S., Liao, W. T., and Chai, C. Y. (2006). Arsenic carcinogenesis in the skin. J. Biomed. Sci. 13, 657-666.
76. Zeisberg, E. M., Tarnavski, O., Zeisberg, M., Dorfman, A. L., McMullen, J. R., Gustafsson, E., Chandraker, A., Yuan, X., Pu, W. T., Roberts, A. B., et al. (2007). Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med. 13, 952-961.
77. Zhou, Z., Ran, Y. L., Hu, H., Pan, J., Li, Z. F., Chen, L. Z., Sun, L. C., Peng, L., Zhao, X. L., Yu, L., et al. (2008). TM4SF3 promotes esophageal carcinoma metastasis via upregulating ADAM12m expression. Clin. Exp. Metastasis 25, 537-548.