A review of co-culture models to study the oral microenvironment and disease

References

• Dale BA, Fredericks LP. Antimicrobial peptides in the oral environment: expression and function in health and disease. Curr Issues Mol Biol. 2005;7:119–12.
   PubMed Web of Science ®Google Scholar
• Souza LR, Oliveira MVM, Basile JR, et al. Anatomical and physiopathological aspects of oral cavity and oropharynx components related to oropharyngeal dysphagia. In: Seminars in Dysphagia. InTech; 2015. doi:10.5772/60766.
   Google Scholar
• Squier CA, Kremer MJ. Biology of oral mucosa and esophagus. J Natl Cancer Inst Monogr. 2001;29:7–15.
   PubMedGoogle Scholar
• Schoen MH, Freed JR. Prevention of dental disease: caries and periodontal disease. Annu Rev Public Health. 1981;2:71–92.
   Web of Science ®Google Scholar
• Kilian M, Chapple ILC, Hannig M, et al. The oral microbiome – an update for oral healthcare professionals. Bdj. 2016;221:657–666.
   Google Scholar
• Kriebel K, Hieke C, Müller-Hilke B, et al. Oral biofilms from symbiotic to pathogenic interactions and associated disease - Connection of periodontitis and rheumatic arthritis by peptidylarginine deiminase. Front Microbiol. 2018;9(JAN):1–14.
   Google Scholar
• Zarco MF, Vess TJ, Ginsburg GS. The oral microbiome in health and disease and the potential impact on personalized dental medicine. Oral Dis. 2012;18:109–120.
   PubMed Web of Science ®Google Scholar
• Kumar B, Kashyap N, Avinash a, et al. The composition, function and role of saliva in maintaining oral health: a review. Int J Contemp Dent Med Rev. 2017; 1–6.
   Google Scholar
• Anderson AC, Rothballer M, Altenburger MJ, et al. In-vivo shift of the microbiota in oral biofilm in response to frequent sucrose consumption. Sci Rep. 2018;8:14202.
   Web of Science ®Google Scholar
• Carter M, Shieh JC. Guide to research techniques in neuroscience. 2010.
   Google Scholar
• Goers L, Freemont P, Polizzi KM. Co-culture systems and technologies: taking synthetic biology to the next level. J R Soc Interface. 2014;11. DOI:10.1098/rsif.2014.0065
   Web of Science ®Google Scholar
• Science Direct. ScienceDirect.com | science, health and medical journals, full text articles and books. [cited 2019 Jul 4]. Availabe from: http://www.sciencedirect.com/
   Google Scholar
• ProQuest. ProQuest | databases, EBooks and technology for research. [cited 2019 Jul 4]. Available from: https://www.proquest.com/
   Google Scholar
• Directory of Open Access Journals. Directory of open access journals (DOAJ). doi:10.5260/chara.18.3.25.
   Google Scholar
• Pan Y, Teng D, Burke AC, et al. Oral bacteria modulate invasion and induction of apoptosis in HEp-2 cells by Pseudomonas aeruginosa. Microb Pathog. 2009;46:73–79.
   Web of Science ®Google Scholar
• Stathopoulou PG, Benakanakere MR, Galicia JC, et al. Epithelial cell pro-inflammatory cytokine response differs across dental plaque bacterial species. J Clin Periodontol. 2010;37:24–29.
   PubMed Web of Science ®Google Scholar
• Saito a, Inagaki S, Ishihara K. Differential ability of periodontopathic bacteria to modulate invasion of human gingival epithelial cells by Porphyromonas gingivalis. Microb Pathog. 2009;47:329–333.
   Web of Science ®Google Scholar
• Fteita D, Könönen E, Gürsoy M, et al. Quorum sensing molecules regulate epithelial cytokine response and biofilm-related virulence of three Prevotella species. Anaerobe. 2018;54:128–135.
   Web of Science ®Google Scholar
• Yee M, Kim S, Sethi P, et al. Porphyromonas gingivalis stimulates IL-6 and IL-8 secretion in GMSM-K, HSC-3 and H413 oral epithelial cells. Anaerobe. 2014;28:62–67.
   Web of Science ®Google Scholar
• Marsh PD, Zaura E. Dental biofilm: ecological interactions in health and disease. J Clin Periodontol. 2017;44:S12–22.
   PubMed Web of Science ®Google Scholar
• Palmer RJ. Composition and development of oral bacterial communities. Periodontol 2000. 2014;64:20–39.
   PubMed Web of Science ®Google Scholar
• Mintz KP, Fives-Taylor PM. Adhesion of Actinobacillus actinomycetemcomitans to a human oral cell line. Infect Immun. 1994;62:3672–3678. [cited 2019 Nov 25]. Available: http://www.ncbi.nlm.nih.gov/pubmed/8063383
   Web of Science ®Google Scholar
• Fives-Taylor P, Meyer D, Mintz K. Characteristics of Actinobacillus actinomycetemcomitans invasion of and adhesion to cultured epithelial cells. Adv Dent Res. 1995;9:55–62.
   Google Scholar
• Yilmaz O, Watanabe K, Lamont RJ. Involvement of integrins in fimbriae-mediated binding and invasion by Porphyromonas gingivalis. Cell Microbiol. 2002;4:305–314.
   PubMed Web of Science ®Google Scholar
• Yilmaz O, Young PA, Lamont RJ, et al. Gingival epithelial cell signalling and cytoskeletal responses to Porphyromonas gingivalis invasion. Microbiology. 2003;149:2417–2426.
   PubMed Web of Science ®Google Scholar
• Han YW, Shi W, Huang GT, et al. Interactions between periodontal bacteria and human oral epithelial cells: fusobacterium nucleatum adheres to and invades epithelial cells. Infect Immun. 2000;68:3140–3146.
   PubMed Web of Science ®Google Scholar
• Gursoy UK, Kononen E, Uitto VJ. Prevotella intermedia ATCC 25611 targets host cell lamellipodia in epithelial cell adhesion and invasion. Oral Microbiol Immunol. 2009;24:304–309.
   Google Scholar
• Dabija-Wolter G, Cimpan M-R, Costea DE, et al. Fusobacterium nucleatum enters normal human oral fibroblasts In Vitro. J Periodontol. 2009;80:1174–1183.
   Web of Science ®Google Scholar
• Bodet C, Chandad F, Grenier D. Modulation of cytokine production by Porphyromonas gingivalis in a macrophage and epithelial cell co-culture model. Microbes Infect. 2005;7:448–456.
   PubMed Web of Science ®Google Scholar
• Bodet C, Chandad F, Grenier D. Inflammatory responses of a macrophage/epithelial cell co-culture model to mono and mixed infections with Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia. Microbes Infect. 2006;8:27–35.
   PubMed Web of Science ®Google Scholar
• Bates AM, Fischer CL, Abhyankar VP, et al. Matrix metalloproteinase response of dendritic cell, gingival epithelial keratinocyte, and T-cell transwell Co-Cultures treated with Porphyromonas gingivalis Hemagglutinin-B. Int J Mol Sci. 2018;19:3923.
   Web of Science ®Google Scholar
• Diaz PI, Rogers AH. The effect of oxygen on the growth and physiology of Porphyromonas gingivalis. Oral Microbiol Immunol. 2004;19:88–94.
   Google Scholar
• Sancilio S, Di Giacomo V, Di Giulio M, et al. Biological responses of human gingival fibroblasts (HGFs) in an innovative co-culture model with Streptococcus mitis to thermosets coated with a silver polysaccharide antimicrobial system. PLoS One. 2014;9:e96520.
   PubMed Web of Science ®Google Scholar
• Giulio MD, D’Ercole S, Zara S, et al. Streptococcus mitis/human gingival fibroblasts co-culture: the best natural association in answer to the 2-hydroxyethyl methacrylate release. Apmis. 2012;120:139.
   Web of Science ®Google Scholar
• Grande R, Pacella S, Di Giulio M, et al. NF-kB mediated down-regulation of collagen synthesis upon HEMA (2-hydroxyethyl methacrylate) treatment of primary human gingival fibroblast/Streptococcus mutans co-cultured cells. Clin Oral Investig. 2015;19:841–849.
   Web of Science ®Google Scholar
• Mah W, Jiang G, Olver D, et al. Human gingival fibroblasts display a non-fibrotic phenotype distinct from skin fibroblasts in three-dimensional cultures. PLoS One. 2014;9:e90715.
   Web of Science ®Google Scholar
• Turabelidze a, Guo S, Chung AY, et al. Intrinsic differences between oral and skin keratinocytes. PLoS One. 2014;9:e101480.
   Web of Science ®Google Scholar
• Discher DE. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310:1139–1143.
   PubMed Web of Science ®Google Scholar
• Engler AJ, Sen S, Sweeney LH, et al. Matrix elasticity directs stem cell lineage specification supplementary Information. Cell. 2006;126(VN):677–689.
   Google Scholar
• Cukierman E. Taking cell-matrix adhesions to the third dimension. Science. 2001;294:1708–1712.
   PubMed Web of Science ®Google Scholar
• Dongari-Bagtzoglou a, Kashleva H. Development of a highly reproducible three-dimensional organotypic model of the oral mucosa. Nat Protoc. 2006;1:2012–2018.
   PubMed Web of Science ®Google Scholar
• Schaller M, Zakikhany K, Naglik JR, et al. Models of oral and vaginal candidiasis based on in vitro reconstituted human epithelia. Nat Protoc. 2007;1:2767–2773.
   Web of Science ®Google Scholar
• Yadev NP, Murdoch C, Saville SP, et al. Evaluation of tissue engineered models of the oral mucosa to investigate oral candidiasis. Microb Pathog. 2011;50:278–285.
   PubMed Web of Science ®Google Scholar
• Pinnock a, Murdoch C, Moharamzadeh K, et al. Characterisation and optimisation of organotypic oral mucosal models to study Porphyromonas gingivalis invasion. Microbes Infect. 2014;16:310–319.
   PubMed Web of Science ®Google Scholar
• Park J, Shokeen B, Haake SK, et al. Characterization of Fusobacterium nucleatum ATCC 23726 adhesins involved in strain-specific attachment to Porphyromonas gingivalis. Int J Oral Sci. 2016;8:138–144.
   Web of Science ®Google Scholar
• Gursoy UK, Pöllänen M, Könönen E, et al. Biofilm formation enhances the oxygen tolerance and invasiveness of Fusobacterium nucleatum in an oral mucosa culture model. J Periodontol. 2010;81:1084–1091.
   PubMed Web of Science ®Google Scholar
• Bao K, Akguel B, Bostanci N. Establishment and characterization of immortalized gingival epithelial and fibroblastic cell lines for the development of organotypic cultures. Cells Tissues Organs. 2014;199:228–237.
   Web of Science ®Google Scholar
• Sakolish CM, Esch MB, Hickman JJ, et al. Modeling barrier tissues In Vitro: methods, achievements, and challenges. EBioMedicine. 2016;5:30–39.
   Web of Science ®Google Scholar
• Merne M, Syrjäne S. The mesenchymal substrate influences the epithelial phenotype in a three-dimensional cell culture. Arch Dermatol Res. 2003;295:190–198.
   Web of Science ®Google Scholar
• Gursoy UK, Könönen E. Understanding the roles of gingival beta-defensins. J Oral Microbiol. 2012;4. DOI:10.3402/jom.v4i0.15127
   Google Scholar
• Duval K, Grover H, Han LH, et al. Modeling physiological events in 2D vs. 3D cell culture. Physiology. 2017;32:266–277.
   PubMed Web of Science ®Google Scholar
• Moharamzadeh K, Colley H, Murdoch C, et al. Tissue-engineered oral mucosa. J Dent Res. 2012;91:642–650.
   PubMed Web of Science ®Google Scholar
• Aas JA, Paster BJ, Stokes LN, et al. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol. 2005;43(5721):LP–5732.
   Google Scholar
• Hall CW, Mah TF. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 2017;41:276–301.
   PubMed Web of Science ®Google Scholar
• Millhouse E, Jose a, Sherry L, et al. Development of an in vitro periodontal biofilm model for assessing antimicrobial and host modulatory effects of bioactive molecules. BMC Oral Health. 2014;14:80.
   PubMed Web of Science ®Google Scholar
• Belibasakis GN, Thurnheer T, Bostanci N. Interleukin-8 responses of multi-layer gingival epithelia to subgingival biofilms: role of the “red complex” species. PLoS One. 2013;8:e81581.
   PubMed Web of Science ®Google Scholar
• Dickinson BC, Moffatt CE, Hagerty D, et al. Interaction of oral bacteria with gingival epithelial cell multilayers. Mol Oral Microbiol. 2011;26:210–220.
   PubMed Web of Science ®Google Scholar
• Khalaf H, Palm E, Bengtsson T. Cellular response mechanisms in Porphyromonas gingivalis Infection. In: Periodontitis - a useful reference. 2017. p. 45–68.
   Google Scholar
• Wang H-Y, Cheng J-W, Yu H-Y, et al. Efficacy of a novel antimicrobial peptide against periodontal pathogens in both planktonic and polymicrobial biofilm states. Acta Biomater. 2015;25:150–161.
   PubMed Web of Science ®Google Scholar
• La VD, Howell AB, Grenier D. Anti-Porphyromonas gingivalis and anti-inflammatory activities of a-type cranberry proanthocyanidins. Antimicrob Agents Chemother. 2010;54:1778LP–1784.
   Web of Science ®Google Scholar
• Zhou Y, Guan X, Zhu W, et al. Capsaicin inhibits Porphyromonas gingivalis growth, biofilm formation, gingivomucosal inflammatory cytokine secretion, and in vitro osteoclastogenesis. Eur J Clin Microbiol Infect Dis. 2014;33:211–219.
   Web of Science ®Google Scholar
• Matsui a, Jin JO, Johnston CD, et al. Pathogenic bacterial species associated with endodontic infection evade innate immune control by disabling neutrophils. Infect Immun. 2014;82:4068–4079.
   PubMed Web of Science ®Google Scholar
• Ramage G, Lappin DF, Millhouse E, et al. The epithelial cell response to health and disease associated oral biofilm models. J Periodontal Res. 2017;52:325–333.
   Web of Science ®Google Scholar
• Subbiahdoss G, Kuijer R, W Grijpma D, et al. Microbial biofilm growth vs. Tissue integration: “The race for the surface” experimentally studied. 2009.
   Google Scholar
• Dwidar M, Leung BM, Yaguchi T, et al. Patterning bacterial communities on epithelial cells. PLoS One. 2013;8:e67165.
   Web of Science ®Google Scholar
• Guggenheim B, Gmür R, Galicia JC, et al. In vitro modeling of host-parasite interactions: the “subgingival” biofilm challenge of primary human epithelial cells. BMC Microbiol. 2009;9:280.
   Web of Science ®Google Scholar
• Thurnheer T, Belibasakis GN, Bostanci N. Colonisation of gingival epithelia by subgingival biofilms in vitro: role of “red complex” bacteria. Arch Oral Biol. 2014;59:977–986.
   PubMed Web of Science ®Google Scholar
• Chin MYH, Busscher HJ, Evans R, et al. Early biofilm formation and the effects of antimicrobial agents on orthodontic bonding materials in a parallel plate flow chamber. Eur J Orthod. 2005;28:1–7.
   Web of Science ®Google Scholar
• Rath H, Stumpp SN, Stiesch M. Development of a flow chamber system for the reproducible in vitro analysis of biofilm formation on implant materials. PLoS One. 2017;12:e0172095.
   Web of Science ®Google Scholar
• Tolker-Nielsen T, Sternberg C. Growing and analyzing biofilms in flow chambers. Curr Protoc Microbiol. 2011;21:1B.2.1–1B.2.17.
   Google Scholar
• Crusz SA, Popat R, Rybtke MT, et al. Bursting the bubble on bacterial biofilms: a flow cell methodology. Biofouling. 2012;28:835–842.
   PubMed Web of Science ®Google Scholar
• Bao K, Papadimitropoulos a, Akgül B, et al. Establishment of an oral infection model resembling the periodontal pocket in a perfusion bioreactor system. Virulence. 2015;6:265–273.
   Google Scholar
• Bao K, Belibasakis GN, Selevsek N, et al. Proteomic profiling of host-biofilm interactions in an oral infection model resembling the periodontal pocket. Sci Rep. 2015;5:15999.
   Google Scholar
• Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67:1716–1725.
   PubMed Web of Science ®Google Scholar
• Shanahan F, Van Sinderen D, O’Toole PW, et al. Feeding the microbiota: transducer of nutrient signals for the host. Gut. 2017;66:1709–1717.
   PubMed Web of Science ®Google Scholar
• Tilg H, Adolph TE, Gerner RR, et al. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33:954–964.
   PubMed Web of Science ®Google Scholar
• Bahrami B, Child MW, Macfarlane S, et al. Adherence and cytokine induction in Caco-2 cells by bacterial populations from a three-stage continuous-culture model of the large intestine. Appl Environ Microbiol. 2011;77:2934–2942.
   Web of Science ®Google Scholar
• Park GS, Park MH, Shin W, et al. Emulating host-microbiome ecosystem of human gastrointestinal tract in Vitro. Stem Cell Rev Rep. 2017;13:321–334.
   Web of Science ®Google Scholar
• Payne AN, Zihler a, Chassard C, et al. Advances and perspectives in in vitro human gut fermentation modeling. Trends Biotechnol. 2012;30:17–25.
   PubMed Web of Science ®Google Scholar
• Monnappa AK, Bari W, Choi SY, et al. Investigating the responses of human epithelial cells to predatory bacteria. Sci Rep. 2016;6:33485.
   PubMed Web of Science ®Google Scholar
• Shaban L, Chen Y, Fasciano AC, et al. a 3D intestinal tissue model supports Clostridioides difficile germination, colonization, toxin production and epithelial damage. Anaerobe. 2018;50:85–92.
   Web of Science ®Google Scholar
• Dosh RH, Jordan-Mahy N, Sammon C, et al. Tissue engineering laboratory models of the small intestine. Tissue Eng - Part B Rev. 2018;24:98–111.
   PubMed Web of Science ®Google Scholar
• Fatehullah a, Tan SH, Barker N. Organoids as an in vitro model of human development and disease. Nat Cell Biol. 2016;18:246–254.
   PubMed Web of Science ®Google Scholar
• Bartfeld S, Bayram T, Van De Wetering M, et al. In vitro expansion of human gastric epithelial stem cells and their responses to bacterial infection. Gastroenterology. 2015;148:126–136.e6.
   Web of Science ®Google Scholar
• Trujillo-de Santiago G, Lobo-Zegers MJ, Montes-Fonseca SL, et al. Gut-microbiota-on-a-chip: an enabling field for physiological research. Microphysiol Syst. 2018;1:1.
   Google Scholar
• Anonye BO, Hassall J, Patient J, et al. Probing Clostridium difficile infection in complex human gut cellular models. Front Microbiol. 2019;10(APR):1–15.
   Google Scholar
• Rosenthal M, Goldberg D, Aiello a, et al. Skin microbiota: microbial community structure and its potential association with health and disease. Infect Genet Evol. 2011;11:839–848.
   PubMed Web of Science ®Google Scholar
• Rademacher F, Simanski M, Gläser R, et al. Skin microbiota and human 3D skin models. Exp Dermatol. 2018;27:489–494.
   PubMed Web of Science ®Google Scholar
• Klicks J, von Molitor E, Ertongur-Fauth T, et al. In vitro skin three-dimensional models and their applications. J Cell Biotechnol. 2017;3:21–39.
   Google Scholar
• El Ghalbzouri a, Commandeur S, Rietveld MH, et al. Replacement of animal-derived collagen matrix by human fibroblast-derived dermal matrix for human skin equivalent products. Biomaterials. 2009;30:71–78.
   Web of Science ®Google Scholar
• Anderson MJ, Parks PJ, Peterson ML. A mucosal model to study microbial biofilm development and anti-biofilm therapeutics. J Microbiol Methods. 2013;92:201–208.
   PubMed Web of Science ®Google Scholar
• Parashar a, Parashar S, Zingade a, et al. Interspecies communication in oral biofilm: an ocean of information. Oral Sci Int. 2015;12:37–42.
   Web of Science ®Google Scholar