New Gene Markers for Metabolic Processes and Homeostasis in Porcine Buccal Pouch Mucosa during Cells Long Term-Cultivation-A Primary Culture Approach
Language English Country Switzerland Media electronic
Document type Journal Article
PubMed
29596348
PubMed Central
PMC5979461
DOI
10.3390/ijms19041027
PII: ijms19041027
Knihovny.cz E-resources
- Keywords
- homeostasis, metabolic process, oral mucosa,
- MeSH
- Epithelial Cells cytology metabolism MeSH
- Homeostasis * MeSH
- Cells, Cultured MeSH
- Humans MeSH
- Swine MeSH
- Gene Expression Regulation * MeSH
- Mouth Mucosa cytology metabolism MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
The oral mucosal tissue is a compound structure composed of morphologically and physiologically different cell types. The morphological modification involves genetically determined lifespan, which may be recognized as the balance between cell survival and apoptosis. Although the biochemical processes and pathways in oral mucosa, with special regards to drug transport, delivery, and metabolism, are well known, the cellular physiological homeostasis in this tissue requires further investigation. The porcine buccal pouch mucosal cells (BPMCs) collected from 20 pubertal crossbred Landrace gilts, were used in this study. Immediately after recovery, the oral mucosa was separated micro-surgically, and treated enzymatically. The dispersed cells were transferred into primary in vitro culture systems for a long-term cultivation of 30 days. After each step of in vitro culture (IVC), the cells were collected for isolation of total RNA at 24 h, 7, 15, and 30 days of IVC. While the expression was analyzed for days 7, 15, and 30, the 24th hour was used as a reference for outcome calibration. The gene expression profile was determined using Affymetrix microarray assays and necessary procedures. In results, we observed significant up-regulation of SCARB1, PTGS2, DUSP5, ITGB3, PLK2, CCL2, TGFB1, CCL8, RFC4, LYN, ETS1, REL, LIF, SPP1, and FGER1G genes, belonging to two ontological groups, namely "positive regulation of metabolic process", and "regulation of homeostatic process" at 7 day of IVC as compared to down-regulation at days 15 and 30. These findings suggest that the metabolic processes and homeostatic regulations are much more intense in porcine mucosal cells at day 7 of IVC. Moreover, the increased expression of marker genes, for both of these ontological groups, may suggest the existence of not only "morphological lifespan" during tissue keratinization, but also "physiological checkpoint" dedicated to metabolic processes in oral mucosa. This knowledge may be useful for preclinical experiments with drugs delivery and metabolism in both animals and humans.
Department of Anatomy Poznań University of Medical Science 6 Święcickiego St 60 781 Poznań Poland
Department of Histology and Embryology Wrocław University of Medical Sciences 50 367 Wrocław Poland
Department of Oral Rehabilitation Poznań University of Medical Sciences 61 701 Poznań Poland
Department of Oral Surgery Poznań University of Medical Sciences 61 701 Poznań Poland
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Borys S., Khozmi R., Kranc W., Bryja A., Dyszkiewicz-Konwińska M., Jeseta M., Kempisty B. Recent findings of the types of programmed cell death. Adv. Cell Biol. 2017;5:43–49. doi: 10.1515/acb-2017-0004. DOI
Bryja A., Dyszkiewicz-Konwińska M., Budna J., Ciesiółka S., Kranc W., Borys S., Jeseta M., Urbaniak O., Bukowska D., Antosik P., et al. Expression of cell mitotic progression proteins and keratinocyte markers in porcine buccal pouch mucosal cells during short-term, real-time primary culture. J. Biol. Regul. Homeost. Agents. 2017;31:297–309. PubMed
Bryja A., Dyszkiewicz-Konwińska M., Budna J., Kranc W., Chachuła A., Borys S., Ciesiółka S., Ciesiółka J., Prylinski M., Prylinski D., et al. The biomedical aspects of oral mucosal epithelial cell culture in mammals. J. Biol. Regul. Homeost. Agents. 2017;31:81–85. PubMed
Bryja A., Dyszkiewicz-Konwińska M., Chachuła A., Ciesiółka S., Kranc W., Bukowska D., Antosik P., Bruska M., Nowicki M., Zabel M., et al. Differential expression and distribution of cytokeratins and vimentin in buccal pouch mucosal cells during real-time cell proliferation: Research based on a porcine model. J. Biol. Regul. Homeost. Agents. 2016;30:951–960. PubMed
Kranc W., Celichowski P., Budna J., Khozmi R., Bryja A., Ciesiółka S., Rybska M., Borys S., Jeseta M., Bukowska D., et al. Positive Regulation of Macromolecule Metabolic Process Belongs to the Main Mechanisms Crucial for Porcine Ooocytes Maturation. Adv. Cell Biol. 2017;5:15–31. doi: 10.1515/acb-2017-0002. DOI
Nawrocki M.J., Budna J., Celichowski P., Khozmi R., Bryja A., Kranc W., Borys S., Ciesiółka S., Ciesiółka S., Jeseta M., et al. Analysis of fructose and mannose—Regulatory peptides signaling pathway in porcine epithelial oviductal cells (OECs) primary cultured long-term in vitro. Adv. Cell Biol. 2017;5:129–135. doi: 10.1515/acb-2017-0011. DOI
Nawrocki M.J., Celichowski P., Budna J., Bryja A., Kranc W., Ciesiółka S., Borys S., Knap S., Jeseta M., Khozmi R., et al. The blood vessels development, morphogenesis and blood circulation are three ontologic groups highly up-regulated in porcine oocytes before in vitro maturation. Adv. Cell Biol. 2017;5:135–142. doi: 10.1515/acb-2017-0012. DOI
Sawada A., Wakabayashi N., Ona M., Suzuki T. Viscoelasticity of Human Oral Mucosa. J. Dent. Res. 2011;90:590–595. doi: 10.1177/0022034510396881. PubMed DOI
Chen J., Ahmad R., Li W., Swain M., Li Q. Biomechanics of oral mucosa. J. R. Soc. Interface. 2015;12:20150325. doi: 10.1098/rsif.2015.0325. PubMed DOI PMC
Bryja A., Dyszkiewicz-Konwińska M., Budna J., Kranc W., Chachuła A., Ciesiółka S., Sumelka E., Krajecki M., Bukowska D., Antosik P., et al. Carcinogenesis in mammalian oral mucosa from the perspective of biomedical research. Med. Weter. 2017;73:82–87. doi: 10.21521/mw.5641. DOI
Rolin G., Placet V., Jacquet E., Tauzin H., Robin S., Pazart L., Viennet C., Saas P., Muret P., Binda D., et al. Development and characterization of a human dermal equivalent with physiological mechanical properties. Skin Res. Technol. 2012;18:251–258. doi: 10.1111/j.1600-0846.2011.00564.x. PubMed DOI
Davis N.G., Phillips A., Becker D.L. Connexin dynamics in the privileged wound healing of the buccal mucosa. Wound Repair Regen. 2013;21:571–578. doi: 10.1111/wrr.12054. PubMed DOI
Guzmán-Uribe D., Alvarado-Estrada K.N., Pierdant-Pérez M., Torres-Álvarez B., Sánchez-Aguilar J.M., Rosales-Ibáñez R. Oral mucosa: An alternative epidermic cell source to develop autologous dermal-epidermal substitutes from diabetic subjects. J. Appl. Oral Sci. 2017;25:186–195. doi: 10.1590/1678-77572016-0217. PubMed DOI PMC
Dyszkiewicz-Konwińska M., Bryja A., Jopek K., Budna J., Bukowska D., Antosik P., Bruska M., Nowicki M., Zabel M., Kempisty B. Expression of connexins in porcine buccal pouch mucosa cells during real-time long-term cells proliferation in vitro—A primary culture approache. J. Biol. Regul. Homeost. Agents. 2017;31:567–577. PubMed
Huveneers S., Truong H., Danen E.H.J. Integrins: Signaling, disease, and therapy. Int. J. Radiat. Biol. 2007;83:743–751. doi: 10.1080/09553000701481808. PubMed DOI
Li R., Pendergast A.M. Arg kinase regulates epithelial cell polarity by targeting β1-integrin and small GTPase pathways. Curr. Biol. 2011;21:1534–1542. doi: 10.1016/j.cub.2011.08.023. PubMed DOI PMC
Lee J.L., Streuli C.H. Integrins and epithelial cell polarity. J. Cell Sci. 2014;127:3217–3225. doi: 10.1242/jcs.146142. PubMed DOI PMC
Akhtar N., Streuli C.H. An integrin–ILK–microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat. Cell Biol. 2013;15:17–27. doi: 10.1038/ncb2646. PubMed DOI PMC
Lee M., Vasioukhin V. Cell polarity and cancer—Cell and tissue polarity as a non-canonical tumor suppressor. J. Cell Sci. 2008;121:1141–1150. doi: 10.1242/jcs.016634. PubMed DOI
Feigin M.E., Muthuswamy S.K. Polarity proteins regulate mammalian cell-cell junctions and cancer pathogenesis. Curr. Opin. Cell Biol. 2009;21:694–700. doi: 10.1016/j.ceb.2009.07.003. PubMed DOI PMC
Zovein A.C., Luque A., Turlo K.A., Hofmann J.J., Yee K.M., Becker M.S., Fassler R., Mellman I., Lane T.F., LuisaIruela-Arispe M., et al. β1 Integrin Establishes Endothelial Cell Polarity and Arteriolar Lumen Formation via a Par3-Dependent Mechanism. Dev. Cell. 2010;18:39–51. doi: 10.1016/j.devcel.2009.12.006. PubMed DOI PMC
Yu W., Datta A., Leroy P., O’Brien L.E., Mak G., Jou T.S., Matlin K.S., Mostov K.E., Zegers M.M. 1-Integrin Orients Epithelial Polarity via Rac1 and Laminin. Mol. Biol. Cell. 2004;16:433–445. doi: 10.1091/mbc.E04-05-0435. PubMed DOI PMC
Gómez-Lamarca M.J., Cobreros-Reguera L., Ibáñez-Jiménez B., Palacios I.M., Martín-Bermudo M.D. Integrins regulate epithelial cell differentiation by modulating Notch activity. J. Cell Sci. 2014;127:4667–4678. doi: 10.1242/jcs.153122. PubMed DOI PMC
Sarrazy V., Datta A., Leroy P., O’Brien L.E., Mak G., Jou T.S., Matlin K.S., Mostov K.E., Zegers M.M. Integrins αvβ5 and αvβ3 promote latent TGF-β1 activation by human cardiac fibroblast contraction. Cardiovasc. Res. 2014;102:407–417. doi: 10.1093/cvr/cvu053. PubMed DOI PMC
Li W., Zhang B., Li H., Zhao C., Zhong Y., Sun J., Lv S. TGF β1 Mediates Epithelial Mesenchymal Transition via β6 Integrin Signaling Pathway in Breast Cancer. Cancer Investig. 2014;32:409–415. doi: 10.3109/07357907.2014.933235. PubMed DOI
Diegelmann R.F., Evans M.C. Wound healing: An overview of acute, fibrotic and delayed healing. Front. Biosci. 2004;9:283–289. doi: 10.2741/1184. PubMed DOI
Massagué J. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 2012;13:616–630. doi: 10.1038/nrm3434. PubMed DOI PMC
Cirillo N., Hassona Y., Celentano A., Lim K.P., Manchella S., Parkinson E.K., Prime S.S. Cancer-associated fibroblasts regulate keratinocyte cell–cell adhesion via TGF-β-dependent pathways in genotype-specific oral cancer. Carcinogenesis. 2017;38:76–85. doi: 10.1093/carcin/bgw113. PubMed DOI
Kamath V., Krishnamurthy S., Satelur K., Rajkumar K. Transforming growth factor-β1 and TGF-β2 act synergistically in the fibrotic pathway in oral submucous fibrosis: An immunohistochemical observation. Indian J. Med. Paediatr. Oncol. 2015;36:111. doi: 10.4103/0971-5851.158842. PubMed DOI PMC
Maria S., Kamath V., Satelur K., Rajkumar K. Evaluation of transforming growth factor beta1 gene in oral submucous fibrosis induced in Sprague-Dawley rats by injections of areca nut and pan masala (commercial areca nut product) extracts. J. Cancer Res. Ther. 2016;12:379. PubMed
Rajalalitha P., Vali S. Molecular pathogenesis of oral submucous fibrosis—A collagen metabolic disorder. J. Oral Pathol. Med. 2005;34:321–328. doi: 10.1111/j.1600-0714.2005.00325.x. PubMed DOI
Yang H., Fang L., Zhan R., Hegarty J.M., Ren J., Hsiai T.K., Gleeson J.G., Miller Y.I., Trejo J., Chi N.C. Polo-like kinase 2 regulates angiogenic sprouting and blood vessel development. Dev. Biol. 2015;404:49–60. doi: 10.1016/j.ydbio.2015.05.011. PubMed DOI PMC
Lowell C. Src-family kinases: Rheostats of immune cell signaling. Mol. Immunol. 2004;41:631–643. doi: 10.1016/j.molimm.2004.04.010. PubMed DOI
Xu Y., Harder K.W., Huntington N.D., Hibbs M.L., Tarlinton D.M. Lyn Tyrosine Kinase: Accentuating the Positive and the Negative. Immunity. 2005;22:9–18. doi: 10.1016/j.immuni.2004.12.004. PubMed DOI
Lim Y.J., Koo J.E., Hong E.H., Park Z.Y., Lim K.M., Bae O.N., Lee J.Y. A Src-family-tyrosine kinase, Lyn, is required for efficient IFN-β expression in pattern recognition receptor, RIG-I, signal pathway by interacting with IPS-1. Cytokine. 2015;72:63–70. doi: 10.1016/j.cyto.2014.12.008. PubMed DOI
Chen D., Yang K., Zhang G., Mei J., Xiang L. Screen and analysis of key disease genes for precancerous lesions of oral buccal mucosa induced by DMBA in golden hamsters. Oncol. Lett. 2011;2:265–271. doi: 10.3892/ol.2010.228. PubMed DOI PMC
Garrett-Sinha L.A. Review of Ets1 structure, function, and roles in immunity. Cell. Mol. Life Sci. 2013;70:3375–3390. doi: 10.1007/s00018-012-1243-7. PubMed DOI PMC
Mayeux J., Skaug B., Luo W., Russell L.M., John S., Saelee P., Abbasi H., Li Q.-Z., Garrett-Sinha L.A., Satterthwaite A.B. Genetic Interaction between Lyn, Ets1, and Btk in the Control of Antibody Levels. J. Immunol. 2015;195:1955–1963. doi: 10.4049/jimmunol.1500165. PubMed DOI PMC
Oikawa T., Yamada T. Molecular biology of the Ets family of transcription factors. Gene. 2003;303:11–34. doi: 10.1016/S0378-1119(02)01156-3. PubMed DOI
Vairaktaris E., Spyridonidou S., Goutzanis L., Vylliotis A., Lazaris A., Donta I., Perrea D., Yapijakis C., Patsouris E. Diabetes and oral oncogenesis. Anticancer Res. 2007;27:4185–4193. PubMed
Vairaktaris E., Spyridonidou S., Papakosta V., Vylliotis A., Lazaris A., Perrea D., Yapijakis C., Patsouris E. The hamster model of sequential oral oncogenesis. Oral Oncol. 2008;44:315–324. doi: 10.1016/j.oraloncology.2007.08.015. PubMed DOI
Wang D., Dubois R.N. Prostaglandins and cancer. Gut. 2006;55:115–122. doi: 10.1136/gut.2004.047100. PubMed DOI PMC
Yip-Schneider M.T., Barnard D.S., Billings S.D., Cheng L., Heilman D.K., Lin A., Marshall S.J., Crowell P.L., Marshall M.S., Sweeney C.J. Cyclooxygenase-2 expression in human pancreatic adenocarcinomas. Carcinogenesis. 2000;21:139–146. doi: 10.1093/carcin/21.2.139. PubMed DOI
Lee L.M., Pan C.C., Cheng C.J., Chi C.W., Liu T.Y. Expression of cyclooxygenase-2 in prostate adenocarcinoma and benign prostatic hyperplasia. Anticancer Res. 2001;21:1291–1294. PubMed
Byatnal A.A., Byatnal A., Sen S., Guddattu V., Solomon M.C. Cyclooxygenase-2—An Imperative Prognostic Biomarker in Oral Squamous Cell Carcinoma—An Immunohistochemical Study. Pathol. Oncol. Res. 2015;21:1123–1131. doi: 10.1007/s12253-015-9940-9. PubMed DOI
Seyedmajidi M., Shafaee S., Siadati S., Khorasani M., Bijani A., Ghasemi N. Cyclo-oxygenase-2 expression in oral squamous cell carcinoma. J. Cancer Res. Ther. 2014;10:1024. doi: 10.4103/0973-1482.138205. PubMed DOI
Mauro A., Lipari L., Leone A., Tortorici S., Burruano F., Provenzano S., Gerbino A., Buscemi M. Expression of cyclooxygenase-1 and cyclooxygenase-2 in normal and pathological human oral mucosa. Folia Histochem. Cytobiol. 2011;48:555–563. doi: 10.2478/v10042-010-0066-3. PubMed DOI
Huang D.W., Sherman B.T., Tan Q., Kir J., Liu D., Bryant D., Guo Y., Stephens R., Baseler M.W., Lane H.C., et al. DAVID Bioinformatics Resources: Expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res. 2007;35:W169–W175. doi: 10.1093/nar/gkm415. PubMed DOI PMC
Von Mering C., Jensen L.J., Snel B., Hooper S.D., Krupp M., Foglierini M., Jouffre N., Huynen M.A., Bork P. STRING: Known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res. 2005;33:D433–D437. doi: 10.1093/nar/gki005. PubMed DOI PMC
Kamburov A., Pentchev K., Galicka H., Wierling C., Lehrach H., Herwig R. ConsensusPathDB: Toward a more complete picture of cell biology. Nucleic Acids Res. 2011;39:D712–D717. doi: 10.1093/nar/gkq1156. PubMed DOI PMC
Walter W., Sánchez-Cabo F., Ricote M. GOplot: An R package for visually combining expression data with functional analysis: Fig. 1. Bioinformatics. 2015;31:2912–2914. doi: 10.1093/bioinformatics/btv300. PubMed DOI