ORIGINAL RESEARCH
Selective changes in expression of integrin α-subunits in the intestinal epithelial Caco-2 cells under conditions of hypoxia and microcirculation
1 National Research University Higher School of Economics, Moscow, Russia
2 Art photonics GmbH, Berlin, Germany
Correspondence should be addressed: Diana V. Maltseva
Vavilova, 7, Moscow, 117321; moc.liamg@avestlamd
Funding: the study was supported by the Ministry of Science and Higher Education of the Russian Federation, project ID RFMEFI61719X0056.
Acknowledgement: the authors express their appreciation to the Center for Collective Use "Human Proteome" (IBMC) for the opportunity to use the equipment for proteome analysis, and to the Center for Precision Genome Editing and Genetic Technologies for Biomedicine of the Pirogov Russian National Research Medical University (Moscow, Russia) for the opportunity to use the molecular biology technologies.
Author contribution: Maltseva DV — working with cultured cells, molecular biology research, data analysis, manuscript writing; Poloznikov AA — proteomic and transcriptomic analysis data processing, bioinformatics analysis, functional analysis of genes, statistical analysis, manuscript writing, study management; Artyushenko VG — interpreting the study results, manuscript reviewing.
Compliance with ethical standards: the study was carried out in accordance with the World Medical Association Declaration of Helsinki.
- Bartfeld S. Modeling infectious diseases and host-microbe interactions in gastrointestinal organoids. Dev Biol. Academic Press; 2016; 420 (2): 262–70.
- Cummins EP, Crean D. Hypoxia and inflammatory bowel disease. Microbes Infect. Elsevier Masson; 2017; 19 (3): 210–21.
- Ward JBJ, Keely SJ, Keely SJ. Oxygen in the regulation of intestinal epithelial transport. J Physiol. John Wiley & Sons, Ltd; 2014; 592 (12): 2473–89.
- Pavlacky J, Polak J. Technical feasibility and physiological relevance of hypoxic cell culture models. Front Endocrinol (Lausanne). Frontiers; 2020; 11: 57.
- Poloznikov AA, Zakhariants AA, Nikulin S V, Smirnova NA, Hushpulian DM, Gaisina IN, et al. Structure-activity relationship for branched oxyquinoline HIF activators: Effect of modifications to phenylacetamide “tail”. Biochimie. 2017; 133: 74–9.
- Muñoz-Sánchez J, Chánez-Cárdenas ME. The use of cobalt chloride as a chemical hypoxia model. J Appl Toxicol. 2019; 39 (4): 556–70.
- Lopez-Sánchez LM, Jimenez C, Valverde A, Hernandez V, Peñarando J, Martinez A, et al. CoCl2, a mimic of hypoxia, induces formation of polyploid giant cells with stem characteristics in colon cancer. Maki CG, editor. PLoS One. Public Library of Science; 2014; 9 (6): e99143.
- Makarova JA, Shkurnikov MU, Wicklein D, Lange T, Samatov TR, Turchinovich AA, et al. Intracellular and extracellular microRNA: An update on localization and biological role. Prog Histochem Cytochem. Urban & Fischer; 2016; 51 (3–4): 33–49.
- Turchinovich А, Samatov TR, Tonevitsky AG, Burwinkel B. Circulating miRNAs: cell-cell communication function? Front Genet. 2013; 4 (June): 119.
- Nersisyan S, Shkurnikov M, Turchinovich A, Knyazev E, Tonevitsky A. Integrative analysis of miRNA and mRNA sequencing data reveals potential regulatory mechanisms of ACE2 and TMPRSS2. PLoS One. 2020; 15 (7 July).
- Sakharov D, Maltseva D, Knyazev E, Nikulin S, Poloznikov A, Shilin S, et al. Towards embedding Caco-2 model of gut interface in a microfluidic device to enable multi-organ models for systems biology. BMC Syst Biol. BioMed Central; 2019; 13 (S1): 19.
- Shah P, Jogani V, Bagchi T, Misra A. Role of Caco-2 cell monolayers in prediction of intestinal drug absorption. Biotechnol Prog. American Chemical Society (ACS); 2006; 22 (1): 186–98.
- Lenaerts K, Bouwman FG, Lamers WH, Renes J, Mariman EC. Comparative proteomic analysis of cell lines and scrapings of the human intestinal epithelium. BMC Genomics. BioMed Central; 2007; 8 (1): 91.
- Ölander M, Wiśniewski JR, Matsson P, Lundquist P, Artursson P. The proteome of filter-grown Caco-2 cells with a focus on proteins involved in drug disposition. J Pharm Sci. Elsevier; 2016; 105 (2): 817–27.
- Beaulieu J-F. Integrins and human intestinal cell functions [Internet]. Front Biosci. 1999.
- Maltseva D, Raygorodskaya M, Knyazev E, Zgoda V, Tikhonova O, Zaidi S, et al. Knockdown of the α5 laminin chain affects differentiation of colorectal cancer cells and their sensitivity to chemotherapy. Biochimie. Elsevier; 2020; 174: 107–16.
- Carvalho BS, Irizarry RA. A framework for oligonucleotide microarray preprocessing. Bioinformatics. Oxford Academic; 2010; 26 (19): 2363–7.
- Yoav B, Yosef H. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc. 1995; 57 (1): 289–300.
- Nersisyan S, Shkurnikov M, Poloznikov A, Turchinovich A, Burwinkel B, Anisimov N, et al. A post-processing algorithm for miRNA microarray data. Int J Mol Sci. Multidisciplinary Digital Publishing Institute; 2020; 21 (4): 1228.
- Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. Nature Publishing Group; 2009; 4 (1): 44–57.
- Karagkouni D, Paraskevopoulou MD, Chatzopoulos S, Vlachos IS, Tastsoglou S, Kanellos I, et al. DIANA-TarBase v8: a decade-long collection of experimentally supported miRNA–gene interactions. Nucleic Acids Res. Oxford Academic; 2018; 46 (D1): D239–45.
- Sticht C, De La Torre C, Parveen A, Gretz N. miRWalk: An online resource for prediction of microRNA binding sites. Campbell M, editor. PLoS One. Public Library of Science; 2018; 13 (10): e0206239.
- Hinske LC, França GS, Torres HAM, Ohara DT, Lopes-Ramos CM, Heyn J, et al. miRIAD — integrating microRNA inter- and intragenic data. Database. Oxford Academic; 2014; 2014.
- Basson MD, Modlin IM, Madri JA. Human enterocyte (Caco-2) migration is modulated in vitro by extracellular matrix composition and epidermal growth factor. J Clin Invest. American Society for Clinical Investigation; 1992; 90 (1): 15–23.
- Gerasimenko T, Nikulin S, Zakharova G, Poloznikov A, Petrov V, Baranova A, et al. Impedance spectroscopy as a tool for monitoring performance in 3D models of epithelial tissues. Front Bioeng Biotechnol. Frontiers; 2020; 7: 474.
- Benita Y, Kikuchi H, Smith AD, Zhang MQ, Chung DC, Xavier RJ. An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res. 2009; 37 (14): 4587–602.
- Karginov F V, Hannon GJ. Remodeling of Ago2-mRNA interactions upon cellular stress reflects miRNA complementarity and correlates with altered translation rates. Genes Dev. Cold Spring Harbor Laboratory Press; 2013; 27 (14): 1624–32.
- Balakrishnan I, Yang X, Brown J, Ramakrishnan A, Torok-Storb B, Kabos P, et al. Genome-wide analysis of miRNA-mRNA interactions in marrow stromal cells. Stem Cells. John Wiley & Sons, Ltd; 2014; 32 (3): 662–73.
- Steiman-Shimony A, Shtrikman O, Margalit H. Assessing the functional association of intronic miRNAs with their host genes. RNA. Cold Spring Harbor Laboratory Press; 2018; 24 (8): 991–1004.
- Calvo Anguiano G, Lugo Trampe J, Camacho A, Said Fernández S, Mercado Hernández R, Zomosa Signoret V, et al. Comparison of specific expression profile in two in vitro hypoxia models. Exp Ther Med. Spandidos Publications; 2018; 15 (6): 4777–84.
- Zhigalova N, Artemov A, Mazur AM, Prokhortchouk EB. Transcriptome sequencing revealed differences in the response of renal cancer cells to hypoxia and CoCl2 treatment. F1000Research. F1000 Research Limited; 2015; 4: 1518.
- Chen C, Xue S, Zhang J, Chen W, Gong D, Zheng J, et al. DNA-methylation-mediated repression of miR-766-3p promotes cell proliferation via targeting SF2 expression in renal cell carcinoma. Int J Cancer. John Wiley & Sons, Ltd; 2017; 141 (9): 1867–78.
- You Y, Que K, Zhou Y, Zhang Z, Zhao X, Gong J, et al. MicroRNA- 766-3p inhibits tumour progression by targeting Wnt3a in hepatocellular carcinoma. Moleucles and Cells. Korean Society for Molecular and Cellular Biology; 41 (9): 830–41.
- Hu G, Wang C, Wang H, Wang Y, Hu S, Cao Z, et al. Long noncoding RNA CCAT2 functions as a competitive endogenous RNA to regulate FOXC1 expression by sponging miR-23b-5p in lung adenocarcinoma. J Cell Biochem. John Wiley & Sons, Ltd; 2019; 120 (5): 7998–8007.
- Takada Y, Ye X, Simon S. The integrins. Genome Biol. 2007; 8 (5): 215.
- Heise T, Dersch P. Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc Natl Acad Sci U S A. National Academy of Sciences; 2006; 103 (9): 3375–80.
- Isberg RR, Leong JM. Multiple β1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. Cell Press; 1990; 60 (5): 861–71.
- Zeitouni NE, Dersch P, Naim HY, von Köckritz-Blickwede M. Hypoxia decreases invasin-mediated Yersinia enterocolitica internalization into Caco-2 cells. Karhausen J, editor. PLoS One. Public Library of Science; 2016; 11 (1): e0146103.