Matrigel Basement Membrane Matrix influences expression of microRNAs in cancer cell lines
Abstract
Matrigel is a medium rich in extracellular matrix (ECM) components used for three-dimensional cell culture and is known to alter cellular phenotypes and gene expression. microRNAs (miRNAs) are small, non-coding RNAs that regulate gene expression and have roles in cancer. While miRNA profiles of numerous cell lines cultured on plastic have been reported, the influence of Matrigel-based culture on cancer cell miRNA expression is largely unknown. This study investigated the influence of Matrigel on the expression of miRNAs that might facilitate ECM-associated cancer cell growth. We performed miRNA profiling by microarray using two colon cancer cell lines (SW480 and SW620), identifying significant differential expression of miRNAs between cells cultured in Matrigel and on plastic. Many of these miRNAs have previously been implicated in cancer-related processes. A common Matrigel-induced miRNA signature comprised of up-regulated miR-1290 and miR-210 and down-regulated miR-29b and miR-32 was identified using RT-qPCR across five epithelial cancer cell lines (SW480, SW620, HT-29, A549 and MDA-MB-231). Experimental modulation of these miRNAs altered expression of their known target mRNAs involved in cell adhesion, proliferation and invasion, in colon cancer cell lines. Furthermore, ITGA5 was identified as a novel putative target of miR-32 that may facilitate cancer cell interactions with the ECM. We propose that culture of cancer cell lines in Matrigel more accurately recapitulates miRNA expression and function in cancer than culture on plastic and thus is a valuable approach to the in vitro study of miRNAs.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Various cancer cell lines grown in 2D and 3D culture often display different gene expression profiles, especially many genes that play a role in proliferation, angiogenesis, migration, invasion, and chemosensitivity.
“Various cancer cell lines grown in 2D and 3D culture often display different gene expression profiles, especially many genes that play a role in proliferation, angiogenesis, migration, invasion, and chemosensitivity. 17,40”
From Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors (2014) · cites this paper as [40]
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714 · see citing works
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome Biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 13,133 · see citing works
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829 · see citing works
limma: Linear Models for Microarray Data
Smyth, G. K. (2005) · Statistics for Biology and Health · doi:10.1007/0-387-29362-0_23 · Cited by 5,796 · see citing works
Combinatorial microRNA target predictions
Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., et al. (2005) · Nature Genetics · doi:10.1038/ng1536 · Cited by 4,603 · see citing works
Prediction of Mammalian MicroRNA Targets
Lewis, B. P., Shih, I.-H., Jones-Rhoades, M. W., Bartel, D. P., & Burge, C. B. (2003) · Cell · doi:10.1016/s0092-8674(03)01018-3 · Cited by 4,333 · see citing works
MicroRNA targets in Drosophila
Enright, A. J., John, B., Gaul, U., Tuschl, T., Sander, C., & Marks, D. S. (2003) · Genome Biology · doi:10.1186/gb-2003-5-1-r1 · Cited by 3,597 · see citing works
Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Gentleman, R. C., Carey, V. J., Huber, W. K., Irizarry, R. A., & Dudoit, S. (2005) · Statistics in the health sciences · doi:10.1007/0-387-29362-0 · Cited by 3,470 · see citing works
The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation
Chen, J., Mandel, E. M., Thomson, J. M., Wu, Q., Callis, T. E., Hammond, S. M., Conlon, F. L., & Wang, D.-Z. (2005) · Nature Genetics · doi:10.1038/ng1725 · Cited by 2,763 · see citing works
microRNAs as oncogenes and tumor suppressors
Zhang, B., Pan, X., Cobb, G. P., & Anderson, T. A. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.08.028 · Cited by 2,755 · see citing works
Normalization of cDNA microarray data
Smyth, G. K., & Speed, T. (2003) · Methods · doi:10.1016/s1046-2023(03)00155-5 · Cited by 1,871 · see citing works
Role of integrins in cell invasion and migration
Hood, J. D., & Cheresh, D. A. (2002) · Nature reviews. Cancer · doi:10.1038/nrc727 · Cited by 1,781 · see citing works
Matrigel: Basement membrane matrix with biological activity
Kleinman, H. K., & Martin, G. R. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.05.004 · Cited by 1,673 · see citing works
How does the extracellular matrix direct gene expression?
Bissell, M. J., Hall, H. G., & Parry, G. (1982) · Journal of Theoretical Biology · doi:10.1016/0022-5193(82)90388-5 · Cited by 1,522 · see citing works
Cheng, A. M. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki200 · Cited by 1,420 · see citing works
Use of within-array replicate spots for assessing differential expression in microarray experiments
Smyth, G. K., Michaud, J., & Scott, H. S. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti270 · Cited by 1,406 · see citing works
Three-dimensional culture models of normal and malignant breast epithelial cells
Lee, G. Y., Kenny, P. A., Lee, E. H., & Bissell, M. J. (2007) · Nature Methods · doi:10.1038/nmeth1015 · Cited by 1,336 · see citing works
Kim, S., Turnbull, J. E., & Guimond, S. E. (2011) · Journal of Endocrinology · doi:10.1530/joe-10-0377 · Cited by 1,166 · see citing works
Kenny, P. A., Lee, G. Y., Myers, C. A., Neve, R. M., Semeiks, J. R., Spellman, P. T., Lorenz, K., Lee, E. H., Barcellos‐Hoff, M. H., PETERSEN, O. W., et al. (2008) · eScholarship (California Digital Library) · Cited by 1,039 · see citing works
MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype
Blenkiron, C., Goldstein, L. D., Thorne, N., Spiteri, I., Chin, S., Dunning, M., Barbosa‐Morais, N. L., Teschendorff, A. E., Green, A. R., Ellis, I. O., et al. (2007) · Genome biology · doi:10.1186/gb-2007-8-10-r214 · Cited by 955 · see citing works
Spandidos, A., Wang, X., Wang, H., & Seed, B. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1005 · Cited by 900 · see citing works
A custom microarray platform for analysis of microRNA gene expression
Thomson, J. M., Parker, J. S., Perou, C. M., & Hammond, S. M. (2004) · Nature Methods · doi:10.1038/nmeth704 · Cited by 742 · see citing works
Ambs, S., Prueitt, R. L., Yi, M., Hudson, R. S., Howe, T. M., Petrocca, F., Wallace, T. A., Liu, C., Volinia, S., Calin, G. A., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0144 · Cited by 705 · see citing works
hsa-miR-210 Is Induced by Hypoxia and Is an Independent Prognostic Factor in Breast Cancer
Camps, C., Buffa, F. M., Colella, S., Moore, J., Sotiriou, C. P., Sheldon, H., Harris, A. L., Gleadle, J., & Ragoussis, J. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1755 · Cited by 658 · see citing works
Revisiting the principles of microRNA target recognition and mode of action
Brodersen, P., & Voinnet, O. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2619 · Cited by 657 · see citing works
MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis
Pichiorri, F., Suh, S.-S., Ladetto, M., Kuehl, M., Palumbo, T., Drandi, D., Taccioli, C., Zanesi, N., Alder, H., Hagan, J. P., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806202105 · Cited by 563 · see citing works
Practical Aspects of microRNA Target Prediction
Witkos, T. M., Kościańska, E., & Krzyżosiak, W. J. (2011) · Current Molecular Medicine · doi:10.2174/156652411794859250 · Cited by 463 · see citing works
Hakkinen, K. M., Harunaga, J. S., Doyle, A. D., & Yamada, K. M. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0273 · Cited by 344 · see citing works
Härmä, V., Virtanen, J., Mäkelä, R., Happonen, A., Mpindi, J.-P., Knuuttila, M., Kohonen, P., Lötjönen, J., Kallioniemi, O., & Nees, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010431 · Cited by 344 · see citing works
The role of integrin binding sites in fibronectin matrix assembly in vivo
Leiß, M., Beckmann, K., Girós, A., Costell, M., & Fässler, R. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.06.001 · Cited by 296 · see citing works
miR‐210: More than a silent player in hypoxia
Devlin, C. M., Greco, S., Martelli, F., & Ivan, M. (2011) · IUBMB Life · doi:10.1002/iub.427 · Cited by 289 · see citing works
Fridman, R., Giaccone, G., Kanemoto, T., Martin, G. R., Gazdar, A. F., & Mulshine, J. L. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.17.6698 · Cited by 255 · see citing works
Renal Medullary MicroRNAs in Dahl Salt-Sensitive Rats
Liu, Y., Taylor, N. E., Lü, L., Usa, K., Cowley, A. W., Ferreri, N. R., Yeo, N. C., & Liang, M. (2010) · Hypertension · doi:10.1161/hypertensionaha.109.144428 · Cited by 235 · see citing works
Multiple uses of basement membrane‐like matrix (BME/Matrigel) in vitro and in vivo with cancer cells
Benton, G., Kleinman, H. K., George, J., & Arnaoutova, I. (2010) · International Journal of Cancer · doi:10.1002/ijc.25781 · Cited by 220 · see citing works
β 1 integrin function in vivo: Adhesion, migration and more
Brakebusch, C., & Fässler, R. (2005) · Cancer and Metastasis Reviews · doi:10.1007/s10555-005-5132-5 · Cited by 210 · see citing works
Analysis of cDNA microarray images
Yang, J. Y. H. (2001) · Briefings in Bioinformatics · doi:10.1093/bib/2.4.341 · Cited by 208 · see citing works
Tsuchiya, S., Fujiwara, T., Sato, F., Shimada, Y., Tanaka, E. I., Sakai, Y., Shimizu, K., & Tsujimoto, G. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.170852 · Cited by 203 · see citing works
Qiao, Y., Liang, L., Guo, W., Zha, R., Tian, Q., Huang, S., Yao, J., Ding, J., Bao, M., Ge, C., et al. (2010) · Hepatology · doi:10.1002/hep.24614 · Cited by 175 · see citing works
Evolution of microRNA expression during human bronchial squamous carcinogenesis
Mascaux, C., Laes, J., Anthoine, G., et al. (2008) · European Respiratory Journal · doi:10.1183/09031936.00084108 · Cited by 145 · see citing works
Extracellular matrix and HIF‐1 signaling: The role of prolidase
Surażyński, A., Donald, S. P., Cooper, S. K., Whiteside, M. A., Salnikow, K., Liu, Y., & Phang, J. M. (2007) · International Journal of Cancer · doi:10.1002/ijc.23263 · Cited by 114 · see citing works
Villarreal, G., Oh, D., Kang, M. H., & Rhee, D. J. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-6165 · Cited by 109 · see citing works
Cross-talk between miR-29 and Transforming Growth Factor-Betas in Trabecular Meshwork Cells
Luna, C., Li, G., Qiu, J., et al. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-6448 · Cited by 97 · see citing works
Spencer, V. A., Xu, R., & Bissell, M. J. (2008) · eScholarship (California Digital Library) · Cited by 79 · see citing works
Genovesi, L. A., Carter, K. W., Gottardo, N. G., Giles, K. M., & Dallas, P. B. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023935 · Cited by 50 · see citing works
Self-citationIntegrins and extracellular matrix: a novel mechanism of multidrug resistance
Elliott, T., & Sethi, T. (2002) · Expert Review of Anticancer Therapy · doi:10.1586/14737140.2.4.449 · Cited by 46 · see citing works
The Use of Matrigel to Facilitate the Establishment of Human Cancer Cell Lines as Xenografts
Mullen, P. (2003) · Humana Press eBooks · doi:10.1385/1-59259-406-9:287 · Cited by 45 · see citing works
The cell surface receptor FGFRL1 forms constitutive dimers that promote cell adhesion
Rieckmann, T., Kotevic, I., & Trüeb, B. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2007.10.029 · Cited by 44 · see citing works
Fukushima, K., Murata, M., Hachisuga, M., Tsukimori, K., Seki, H., Takeda, S., Asanoma, K., & Wake, N. (2008) · Placenta · doi:10.1016/j.placenta.2008.01.006 · Cited by 43 · see citing works
Effects of microRNA-29 family members on proliferation and invasion of gastric cancer cell lines
Lang, N., Liu, M., Tang, Q., et al. (2010) · 癌症:英文版 · doi:10.5732/cjc.009.10597 · Cited by 40 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Edmondson, R., Broglie, J. J., Adcock, A. F., & Yang, L. (2014) · ASSAY and Drug Development Technologies · doi:10.1089/adt.2014.573 · Cited by 2,515 · see citing works
Polysaccharide matrices used in 3D in vitro cell culture systems
Diekjürgen, D., & Grainger, D. W. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.06.020 · Cited by 125 · see citing works
Bridging the gap between tumor-on-chip and clinics: a systematic review of 15 years of studies
Bouquerel, C., Dubrova, A., Hofer, I., Phan, D. T. T., Bernheim, M., Ladaigue, S., Cavaniol, C., Maddalo, D., Cabel, L., Mechta-Grigoriou, F., et al. (2023) · Lab on a Chip · doi:10.1039/d3lc00531c · Cited by 58 · see citing works
Optimized delivery of siRNA into 3D tumor spheroid cultures in situ
Morgan, R. G., Chambers, A. C., Legge, D. N., Coles, S. J., Greenhough, A., & Williams, A. C. (2018) · Scientific Reports · doi:10.1038/s41598-018-26253-3 · Cited by 47 · see citing works
- Authors
- Price, K. J., Tsykin, A., Giles, K. M., Sladic, R. T., Epis, M. R., Ganss, R., Goodall, G. J., & Leedman, P. J.
- Affiliations
- The University of Western Australia (AU)
- South Australia Pathology (AU)
- Corresponding author
- Leedman, Peter J.
- Venue
- Biochemical and Biophysical Research Communications
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 427
- Issue
- 2
- Pages
- 343-348
- ISSN
- 0006-291X (ISSN-L)
- OpenAlex
- W2059490699
- Cited by
- 49
- References
- 50
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 4 · 2020: 8 · 2019: 6 · 2018: 6 · 2017: 3 · 2016: 3 · 2015: 1 · 2014: 6 · 2013: 2
- FWCI
- 0.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biochemical and Biophysical Research Communications (publishedVersion)
- PubMed (publishedVersion)
- UWA Profiles and Research Repository (University of Western Australia) (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Funders
- University of Western Australia
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- Matrigel, extracellular matrix, microRNA expression, colon cancer cell lines, miR-1290, miR-210, miR-29b, miR-32, integrin alpha5, cell adhesion, cell proliferation, cell invasion
- MeSH terms
- Cell Adhesion, Cell Transformation, Neoplastic, Collagen, Drug Combinations, Extracellular Matrix, Humans, Laminin, Neoplasm Invasiveness, Proteoglycans, Gene Expression Regulation, Neoplastic, Cell Culture Techniques, Oligonucleotide Array Sequence Analysis, MicroRNAs, Cell Line, Tumor, Cell Proliferation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review