In vitro systems toxicology approach to investigate the effects of repeated cigarette smoke exposure on human buccal and gingival organotypic epithelial tissue cultures

References

• Ackermann M, Strimmer K. (2009). A general modular framework for gene set enrichment analysis. BMC Bioinformatics 10:47
   PubMed Web of Science ®Google Scholar
• Andrian E, Grenier D, Rouabhia M. (2004). In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect Immun 72:4689–98
   PubMed Web of Science ®Google Scholar
• Aufderheide M, Scheffler S, Mohle N, et al. (2011). Analytical in vitro approach for studying cyto- and genotoxic effects of particulate airborne material. Anal Bioanal Chem 401:3213–20
   PubMed Web of Science ®Google Scholar
• Autrup H, Seremet T, Arenholt D, et al. (1985). Metabolism of benzo[a]pyrene by cultured rat and human buccal mucosa cells. Carcinogenesis 6:1761–5
   PubMedGoogle Scholar
• Balharry D, Sexton K, Berube KA. (2008). An in vitro approach to assess the toxicity of inhaled tobacco smoke components: nicotine, cadmium, formaldehyde and urethane. Toxicology 244:66–76
   PubMed Web of Science ®Google Scholar
• Banerjee AG, Bhattacharyya I, Vishwanatha JK. (2005). Identification of genes and molecular pathways involved in the progression of premalignant oral epithelia. Mol Cancer Ther 4:865–75
   PubMed Web of Science ®Google Scholar
• Bolstad BM, Irizarry RA, Astrand M, Speed TP. (2003). A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193
   PubMed Web of Science ®Google Scholar
• Boyle JO, Gumus ZH, Kacker A, et al. (2010). Effects of cigarette smoke on the human oral mucosal transcriptome. Cancer Prev Res (Phila) 3:266–78
   PubMed Web of Science ®Google Scholar
• Ceder R, Merne M, Staab CA, et al. (2007). The application of normal, SV40 T-antigen-immortalised and tumour-derived oral keratinocytes, under serum-free conditions, to the study of the probability of cancer progression as a result of environmental exposure to chemicals. Altern Lab Anim 35:621–39
   PubMed Web of Science ®Google Scholar
• Chakraborti S, Mandal M, Das S, et al. (2003). Regulation of matrix metalloproteinases: an overview. Mol Cell Biochem 253:269–85
   PubMed Web of Science ®Google Scholar
• Chen YK, Hsue SS, Lin LM. (2005). Expression of p63 protein and mRNA in oral epithelial dysplasia. J Oral Pathol Med 34:232–9
   PubMed Web of Science ®Google Scholar
• Chinnathambi S, Tomanek-Chalkley A, Ludwig N, et al. (2003). Recapitulation of oral mucosal tissues in long-term organotypic culture. Anat Rec A Discov Mol Cell Evol Biol 270:162–74
   PubMedGoogle Scholar
• Combes RD. (2004). The use of human cells in biomedical research and testing. Altern Lab Anim 32:43–9
   PubMedGoogle Scholar
• Dabija-Wolter G, Bakken V, Cimpan MR, et al. (2013). In vitro reconstruction of human junctional and sulcular epithelium. J Oral Pathol Med 42:396–404
   PubMed Web of Science ®Google Scholar
• Dwivedi N, Chandra S, Kashyap B, et al. (2013). Suprabasal expression of Ki-67 as a marker for the severity of oral epithelial dysplasia and oral squamous cell carcinoma. Contemp Clin Dent 4:7–12
   PubMedGoogle Scholar
• Efron B, Tibshirani R. (2007). On testing the significance of sets of genes. Ann Appl Stat 1:107–29
   Web of Science ®Google Scholar
• Gautier L, Cope L, Bolstad BM, Irizarry RA. (2004). Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20:307–15
   PubMed Web of Science ®Google Scholar
• Gebel S, Lichtner RB, Frushour B, et al. (2013). Construction of a computable network model for DNA damage, autophagy, cell death, and senescence. Bioinform Biol Insights 7:97–117
   Google Scholar
• Gemmell E, Carter CL, Seymour GJ. (2001). Chemokines in human periodontal disease tissues. Clin Exp Immunol 125:134–41
   PubMed Web of Science ®Google Scholar
• Giaretti W, Maffei M, Pentenero M, et al. (2012a). Genomic aberrations in normal appearing mucosa fields distal from oral potentially malignant lesions. Cell Oncol (Dordr) 35:43–52
   PubMedGoogle Scholar
• Giaretti W, Pentenero M, Gandolfo S, Castagnola P. (2012b). Chromosomal instability, aneuploidy and routine high-resolution DNA content analysis in oral cancer risk evaluation. Future Oncol 8:1257–71
   PubMedGoogle Scholar
• Gonzalez-Suarez I, Sewer A, Walker P, et al. (2014). Systems biology approach for evaluating the biological impact of environmental toxicants in vitro. Chem Res Toxicol 27:367–76
   PubMed Web of Science ®Google Scholar
• Gower AC, Steiling K, Brothers JF, II et al. (2011). Transcriptomic studies of the airway field of injury associated with smoking-related lung disease. Proc Am Thorac Soc 8:173–9
   PubMedGoogle Scholar
• Hansson A, Bloor BK, Haig Y, et al. (2001). Expression of keratins in normal, immortalized and malignant oral epithelia in organotypic culture. Oral Oncol 37:419–30
   PubMedGoogle Scholar
• Hatakeyama S, Yaegashi T, Takeda Y, Kunimatsu K. (2007). Localization of bromodeoxyuridine-incorporating, p63- and p75(NGFR)-expressing cells in the human gingival epithelium. J Oral Sci 49:287–91
   PubMedGoogle Scholar
• Hedberg JJ, Grafstrom RC, Vondracek M, et al. (2001). Micro-array chip analysis of carbonyl-metabolising enzymes in normal, immortalised and malignant human oral keratinocytes. Cell Mol Life Sci 58:1719–26
   PubMed Web of Science ®Google Scholar
• Hoeng J, Deehan R, Pratt D, et al. (2012). A network-based approach to quantifying the impact of biologically active substances. Drug Discov Today 17:413–18
   PubMed Web of Science ®Google Scholar
• Hoeng J, Talikka M, Martin F, et al. (2013). Case study: the role of mechanistic network models in systems toxicology. Drug Discov Today 19:183–92
   PubMed Web of Science ®Google Scholar
• Homann N, Karkkainen P, Koivisto T, et al. (1997). Effects of acetaldehyde on cell regeneration and differentiation of the upper gastrointestinal tract mucosa. J Natl Cancer Inst 89:1692–7
   PubMedGoogle Scholar
• Huang W, Sherman BT, Lempicki RA. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57
   PubMed Web of Science ®Google Scholar
• International Organization for Standardization. (2010). ISO 3402: 1999 – Tobacco and tobacco products – Atmosphere for conditioning and testing, 4th ed. Geneva: ISO
   Google Scholar
• Iskandar AR, Martin F, Talikka M, et al. (2013). Systems approaches evaluating the perturbation of xenobiotic metabolism in response to cigarette smoke exposure in nasal and bronchial tissues. Biomed Res Int 2013:512086
   PubMed Web of Science ®Google Scholar
• Jones KB, Klein OD. (2013). Oral epithelial stem cells in tissue maintenance and disease: the first steps in a long journey. In J Oral Sci 5:121–9
   Google Scholar
• Khan I, Agarwal P, Thangjam GS, et al. (2011). Role of TGF-beta and BMP7 in the pathogenesis of oral submucous fibrosis. Growth Factors 29:119–27
   PubMed Web of Science ®Google Scholar
• Kim SG, Chae CH, Cho BO, et al. (2006). Apoptosis of oral epithelial cells in oral lichen planus caused by upregulation of BMP-4. J Oral Pathol Med 35:37–45
   PubMedGoogle Scholar
• Klausner M, Ayehunie S, Breyfogle BA, et al. (2007). Organotypic human oral tissue models for toxicological studies. Toxicol In Vitro 21:938–49
   PubMed Web of Science ®Google Scholar
• Kupfer DM, White VL, Jenkins MC, Burian D. (2010). Examining smoking-induced differential gene expression changes in buccal mucosa. BMC Med Genomics 3:24
   PubMedGoogle Scholar
• Liu Y, Sundqvist K, Belinsky SA, et al. (1993). Metabolism and macromolecular interaction of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in cultured explants and epithelial cells of human buccal mucosa. Carcinogenesis 14:2383–8
   PubMedGoogle Scholar
• Marcelo CL, Peramo A, Ambati A, Feinberg SE. (2012). Characterization of a unique technique for culturing primary adult human epithelial progenitor/“stem cells”. BMC Dermatol 12:8
   PubMedGoogle Scholar
• Martin F, Thomson TM, Sewer A, et al. (2012). Assessment of network perturbation amplitudes by applying high-throughput data to causal biological networks. BMC Syst Biol 6:54
   PubMed Web of Science ®Google Scholar
• Mathis C, Poussin C, Weisensee D, et al. (2013). Human bronchial epithelial cells exposed in vitro to cigarette smoke at the air-liquid interface resemble bronchial epithelium from human smokers. Am J Physiol Lung Cell Mol Physiol 304:L489–503
   PubMed Web of Science ®Google Scholar
• Maunders H, Patwardhan SR, Phillips J, et al. (2007). Human bronchial epithelial cell transcriptome: gene expression changes following acute exposure to whole cigarette smoke in vitro. Am J Physiol Lung Cell Mol Physiol 292:L1248–56
   PubMed Web of Science ®Google Scholar
• Mezentsev A, Amundson SA. (2011). Global gene expression responses to low- or high-dose radiation in a human three-dimensional tissue model. Radiat Res 175:677–88
   PubMed Web of Science ®Google Scholar
• Mostefaoui Y, Claveau I, Ross G, Rouabhia M. (2002). Tissue structure, and IL-1beta, IL-8, and TNF-alpha secretions after contact by engineered human oral mucosa with dentifrices. J Clin Periodontol 29:1035–41
   PubMed Web of Science ®Google Scholar
• Moyes DL, Runglall M, Murciano C, et al. (2010). A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe 8:225–35
   PubMed Web of Science ®Google Scholar
• Noutomi Y, Oga A, Uchida K, et al. (2006). Comparative genomic hybridization reveals genetic progression of oral squamous cell carcinoma from dysplasia via two different tumourigenic pathways. J Pathol 210:67–74
   PubMedGoogle Scholar
• Office of the Surgeon General US. (2004). The Health Consequences of Smoking: A Report of the Surgeon General. Atlanta, GA: Centers for Disease Control and Prevention (US)
   Google Scholar
• Paszkiewicz GM, Timm EA, Jr Mahoney MC, et al. (2008). Increased human buccal cell autofluorescence is a candidate biomarker of tobacco smoking. Cancer Epidemiol Biomarkers Prev 17:239–44
   PubMedGoogle Scholar
• Pentenero M, Giaretti W, Navone R, et al. (2009). DNA aneuploidy and dysplasia in oral potentially malignant disorders: association with cigarette smoking and site. Oral Oncol 45:887–90
   PubMedGoogle Scholar
• Port JL, Yamaguchi K, Du B, et al. (2004). Tobacco smoke induces CYP1B1 in the aerodigestive tract. Carcinogenesis 25:2275–81
   PubMedGoogle Scholar
• Proia NK, Paszkiewicz GM, Nasca MA, et al. (2006). Smoking and smokeless tobacco-associated human buccal cell mutations and their association with oral cancer – a review. Cancer Epidemiol Biomarkers Prev 15:1061–77
   PubMed Web of Science ®Google Scholar
• R Development Core Team. (2010). R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing
   Google Scholar
• R Development Core Team. (2012). R: a language and environment for statistical computing. With complete agglomeration and Euclidean distance metrics. Vienna, Austria: R Foundation for Statistical Computing
   Google Scholar
• Rowat JS, Squier CA. (1986). Rates of epithelial cell proliferation in the oral mucosa and skin of the tamarin monkey (Saguinus fuscicollis). J Dental Res 65:1326–31
   PubMedGoogle Scholar
• Rubini C, Artese L, Zizzi A, et al. (2011). Immunohistochemical expression of vascular endothelial growth factor (VEGF) in different types of odontogenic cysts. Clin Oral Investig 15:757–61
   PubMed Web of Science ®Google Scholar
• Sasco AJ, Secretan MB, Straif K. (2004). Tobacco smoking and cancer: a brief review of recent epidemiological evidence. Lung Cancer 45:S3–9
   PubMed Web of Science ®Google Scholar
• Schlage WK, Westra JW, Gebel S, et al. (2011). A computable cellular stress network model for non-diseased pulmonary and cardiovascular tissue. BMC Syst Biol 5:168
   PubMed Web of Science ®Google Scholar
• Smyth GK. (2004). Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:Article 3
   Google Scholar
• Spira A, Beane JE, Shah V, et al. (2007). Airway epithelial gene expression in the diagnostic evaluation of smokers with suspect lung cancer. Nat Med 13:361–6
   PubMed Web of Science ®Google Scholar
• Spivack SD, Hurteau GJ, Jain R, et al. (2004). Gene-environment interaction signatures by quantitative mRNA profiling in exfoliated buccal mucosal cells. Cancer Res 64:6805–13
   PubMed Web of Science ®Google Scholar
• Sridhar S, Schembri F, Zeskind J, et al. (2008). Smoking-induced gene expression changes in the bronchial airway are reflected in nasal and buccal epithelium. BMC Genomics 9:259
   PubMedGoogle Scholar
• Steiling K, Ryan J, Brody JS, Spira A. (2008). The field of tissue injury in the lung and airway. Cancer Prev Res (Phila) 1:396–403
   PubMed Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102:15545–50
   PubMed Web of Science ®Google Scholar
• Talikka M, Kostadinova R, Xiang Y, et al. (2014). The response of human respiratory organotypic cultures to repeated cigarette smoke exposure. Int J Toxicol [submitted]
   Google Scholar
• Terada M, Izumi K, Ohnuki H, et al. (2012). Construction and characterization of a tissue-engineered oral mucosa equivalent based on a chitosan-fish scale collagen composite. J Biomed Mater Res B Appl Biomater 100:1792–802
   PubMedGoogle Scholar
• Thomson TM, Sewer A, Martin F, et al. (2013). Quantitative assessment of biological impact using transcriptomic data and mechanistic network models. Toxicol Appl Pharmacol 273:863–78
   Google Scholar
• Toruner GA, Ulger C, Alkan M, et al. (2004). Association between gene expression profile and tumor invasion in oral squamous cell carcinoma. Cancer Genet Cytogenet 154:27–35
   PubMed Web of Science ®Google Scholar
• Vincenti MP, White LA, Schroen DJ, et al. (1996). Regulating expression of the gene for matrix metalloproteinase-1 (collagenase): mechanisms that control enzyme activity, transcription, and mRNA stability. Crit Rev Eukaryot Gene Expr 6:391–411
   PubMed Web of Science ®Google Scholar
• Vondracek M, Weaver DA, Sarang Z, et al. (2002). Transcript profiling of enzymes involved in detoxification of xenobiotics and reactive oxygen in human normal and simian virus 40 T antigen-immortalized oral keratinocytes. Int J Cancer 99:776–82
   PubMed Web of Science ®Google Scholar
• Vondracek M, Xi Z, Larsson P, et al. (2001). Cytochrome P450 expression and related metabolism in human buccal mucosa. Carcinogenesis 22:481–8
   PubMed Web of Science ®Google Scholar
• Walle T, Walle UK, Sedmera D, Klausner M. (2006). Benzo[A]pyrene-induced oral carcinogenesis and chemoprevention: studies in bioengineered human tissue. Drug Metab Dispos 34:346–50
   PubMed Web of Science ®Google Scholar
• Wang Y, Rotem E, Andriani F, Garlick JA. (2001). Smokeless tobacco extracts modulate keratinocyte and fibroblast growth in organotypic culture. J Dent Res 80:1862–6
   PubMed Web of Science ®Google Scholar
• Warnakulasuriya S, Dietrich T, Bornstein MM, et al. (2010). Oral health risks of tobacco use and effects of cessation. Int Dent J 60:7–30
   PubMed Web of Science ®Google Scholar
• Warnes GR, Bolker B, Bonebakker L, et al. (2012). gplots: Various R programming tools for plotting data (comprehensive R archive network). R package version 2.8.0. Available at: http://cran.r-project.org/web/packages/gplots/index.html webcite
   Google Scholar
• Watanabe S, Sato K, Okazaki Y, et al. (2009). Activation of PI3K-AKT pathway in oral epithelial dysplasia and early cancer of tongue. Bull Tokyo Dent Coll 50:125–33
   PubMedGoogle Scholar
• Westfall MD, Pietenpol JA. (2004). p63: molecular complexity in development and cancer. Carcinogenesis 25:857–64
   PubMed Web of Science ®Google Scholar
• Westra JW, Schlage WK, Frushour BP, et al. (2011). Construction of a computable cell proliferation network focused on non-diseased lung cells. BMC Syst Biol 5:105
   PubMed Web of Science ®Google Scholar
• Westra JW, Schlage WK, Hengstermann A, et al. (2013). A modular cell-type focused inflammatory process network model for non-diseased pulmonary tissue. Bioinform Biol Insights 7:167–92
   PubMedGoogle Scholar
• Winn DM. (2001). Tobacco use and oral disease. J Dent Educ 65:306–12
   PubMedGoogle Scholar
• Wu C, Irizarry R. (2005). with contributions from Macdonald J, Genry J. gcrma: background adjustment using sequence information. 2.2.0 edition
   Google Scholar
• Yu CC, Woods AL, Levison DA. (1992). The assessment of cellular proliferation by immunohistochemistry: a review of currently available methods and their applications. Histochem J 24:121–31
   PubMedGoogle Scholar
• Zhang L, Rosin MP. (2001). Loss of heterozygosity: a potential tool in management of oral premalignant lesions? J Oral Pathol Med 30:513–20
   PubMedGoogle Scholar