Insights into amebiasis using a human 3D-intestinal model.
Entamoeba histolytica
3D-intestinal model
inflammation
secretome
transcriptome
Journal
Cellular microbiology
ISSN: 1462-5822
Titre abrégé: Cell Microbiol
Pays: India
ID NLM: 100883691
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
25
09
2019
revised:
27
01
2020
accepted:
04
03
2020
pubmed:
17
3
2020
medline:
7
8
2021
entrez:
17
3
2020
Statut:
ppublish
Résumé
Entamoeba histolytica is the causative agent of amebiasis, an infectious disease targeting the intestine and the liver in humans. Two types of intestinal infection are caused by this parasite: silent infection, which occurs in the majority of cases, and invasive disease, which affects 10% of infected persons. To understand the intestinal pathogenic process, several in vitro models, such as cell cultures, human tissue explants or human intestine xenografts in mice, have been employed. Nevertheless, our knowledge on the early steps of amebic intestinal infection and the molecules involved during human-parasite interaction is scarce, in part due to limitations in the experimental settings. In the present work, we took advantage of tissue engineering approaches to build a three-dimensional (3D)-intestinal model that is able to replicate the general characteristics of the human colon. This system consists of an epithelial layer that develops tight and adherens junctions, a mucus layer and a lamina propria-like compartment made up of collagen containing macrophages and fibroblast. By means of microscopy imaging, omics assays and the evaluation of immune responses, we show a very dynamic interaction between E. histolytica and the 3D-intestinal model. Our data highlight the importance of several virulence markers occurring in patients or in experimental models, but they also demonstrate the involvement of under described molecules and regulatory factors in the amoebic invasive process.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13203Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Aggarwal, S., Ahuja, V., & Paul, J. (2017). Attenuated GABAergic signaling in intestinal epithelium contributes to pathogenesis of ulcerative colitis. Digestive Diseases and Sciences, 62, 2768-2779.
Ando-Akatsuka, Y., Yonemura, S., Itoh, M., Furuse, M., & Tsukita, S. (1999). Differential behavior of E-cadherin and occludin in their colocalization with ZO-1 during the establishment of epithelial cell polarity. Journal of Cellular Physiology, 179, 115-125.
Artym, V. V., & Matsumoto, K. (2010). Imaging cells in three-dimensional collagen matrix. Current Protocols in Cell Biology, 10, 1-20.
Bacikova, D., & Horowitz, D. S. (2005). Genetic and functional interaction of evolutionarily conserved regions of the Prp18 protein and the U5 snRNA. Molecular and Cellular Biology, 25, 2107-2116.
Bansal, D., Ave, P., Kerneis, S., Frileux, P., Boche, O., Baglin, A. C., … Labruyère, E. (2009). An ex-vivo human intestinal model to study Entamoeba histolytica pathogenesis. PLoS Neglected Tropical Diseases, 3, e551.
Barondes, S. H., Cooper, D. N., Gitt, M. A., & Leffler, H. (1994). Galectins. Structure and function of a large family of animal lectins. The Journal of Biological Chemistry, 269, 20807-20810.
Behrens, I., Stenberg, P., Artursson, P., & Kissel, T. (2001). Transport of lipophilic drug molecules in a new mucus-secreting cell culture model based on HT29-MTX cells. Pharmaceutical Research, 18, 1138-1145.
Bennett, V., & Chen, L. (2001). Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Current Opinion in Cell Biology, 13, 61-67.
Blazquez, S., Guigon, G., Weber, C., Syan, S., Sismeiro, O., Coppee, J. Y., … Guillén, N. (2008). Chemotaxis of Entamoeba histolytica towards the pro-inflammatory cytokine TNF is based on PI3K signalling, cytoskeleton reorganization and the Galactose/N-acetylgalactosamine lectin activity. Cellular Microbiology, 10, 1676-1686.
Bouameur, J. E., Favre, B., & Borradori, L. (2014). Plakins, a versatile family of cytolinkers: Roles in skin integrity and in human diseases. The Journal of Investigative Dermatology, 134, 885-894.
Bretscher, A., Osborn, M., Wehland, J., & Weber, K. (1981). Villin associates with specific microfilamentous structures as seen by immunofluorescence microscopy on tissue sections and cells microinjected with villin. Experimental Cell Research, 135, 213-219.
Brightbill, H. D., Libraty, D. H., Krutzik, S. R., Yang, R. B., Belisle, J. T., Bleharski, J. R., … Modlin, R. L. (1999). Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science, 285, 732-736.
Calandra, T., & Roger, T. (2003). Macrophage migration inhibitory factor: A regulator of innate immunity. Nature Reviews. Immunology, 3, 791-800.
Cheng, Z., Bai, Y., Wang, P., Wu, Z., Zhou, L., Zhong, M., … Mao, H. (2017). Identification of long noncoding RNAs for the detection of early stage lung squamous cell carcinoma by microarray analysis. Oncotarget, 8, 13329-13337.
Choi, D. S., Kim, D. K., Kim, Y. K., & Gho, Y. S. (2013). Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics, 13, 1554-1571.
Choi, D. S., Yang, J. S., Choi, E. J., Jang, S. C., Park, S., Kim, O. Y., … Gho, Y. S. (2012). The protein interaction network of extracellular vesicles derived from human colorectal cancer cells. Journal of Proteome Research, 11, 1144-1151.
Ciobanasu, C., Faivre, B., & Le Clainche, C. (2012). Actin dynamics associated with focal adhesions. International journal of cell biology, 2012, 941292.
Comai, L. (2004). Mechanism of RNA polymerase I transcription. Advances in Protein Chemistry, 67, 123-155.
Cornick, S., Moreau, F., Gaisano, H. Y., & Chadee, K. (2017). Entamoeba histolytica-induced mucin exocytosis is mediated by VAMP8 and is critical in mucosal innate host defense. MBio, 8(5), pii: e01323-17.
Cox, J., & Mann, M. (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology, 26, 1367-1372.
Cseh, A. M., Fabian, Z., Sumegi, B., & Scorrano, L. (2017). Poly(adenosine diphosphate-ribose) polymerase as therapeutic target: lessons learned from its inhibitors. Oncotarget, 8, 50221-50239.
Da Violante, G., Zerrouk, N., Richard, I., Frendo, J. L., Zhiri, A., Li-Khuan, R., … Arnaud, P. (2004). Short term Caco-2/TC7 cell culture: comparison between conventional 21-d and a commercially available 3-d system. Biological & Pharmaceutical Bulletin, 27, 1986-1992.
Daigneault, M., Preston, J. A., Marriott, H. M., Whyte, M. K., & Dockrell, D. H. (2010). The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLoS One, 5, e8668.
de Chaumont, F., Dallongeville, S., Chenouard, N., Herve, N., Pop, S., Provoost, T., … Olivo-Marin, J. C. (2012). Icy: an open bioimage informatics platform for extended reproducible research. Nature Methods, 9, 690-696.
Delacour, D., Salomon, J., Robine, S., & Louvard, D. (2016). Plasticity of the brush border - the yin and yang of intestinal homeostasis. Nature Reviews. Gastroenterology & Hepatology, 13, 161-174.
Diamond, L. S., Harlow, D. R., & Cunnick, C. C. (1978). A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Transactions of the Royal Society of Tropical Medicine and Hygiene, 72, 431-432.
Dobin, A., & Gingeras, T. R. (2015). Mapping RNA-seq Reads with STAR. Current Protocols in Bioinformatics, 51, 11-19.
Dutton, J. S., Hinman, S. S., Kim, R., Wang, Y., & Allbritton, N. L. (2019). Primary cell-derived intestinal models: Recapitulating physiology. Trends in Biotechnology, 37, 744-760.
Elston, R., & Inman, G. J. (2012). Crosstalk between p53 and TGF-beta Signalling. Journal of Signal Transduction, 2012, 294097.
Engeland, K. (2018). Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM. Cell Death and Differentiation, 25, 114-132.
Faust, D. M., & Guillen, N. (2012). Virulence and virulence factors in Entamoeba histolytica, the agent of human amoebiasis. Microbes and Infection, 14, 1428-1441.
Galluzzi, L., Diotallevi, A., & Magnani, M. (2017). Endoplasmic reticulum stress and unfolded protein response in infection by intracellular parasites. Future Sci OA, 3, FSO198.
Geraldo, S., Simon, A., & Vignjevic, D. M. (2013). Revealing the cytoskeletal organization of invasive cancer cells in 3D. Journal of Visualized Experiments, 80, e50763.
Giai Gianetto, Q., Combes, F., Ramus, C., Bruley, C., Coute, Y., & Burger, T. (2016). Calibration plot for proteomics: A graphical tool to visually check the assumptions underlying FDR control in quantitative experiments. Proteomics, 16, 29-32.
Hahne, J. C., & Valeri, N. (2018). Non-coding RNAs and resistance to anticancer drugs in gastrointestinal tumors. Frontiers in Oncology, 8, 226.
Hamers, A. A., Uleman, S., van Tiel, C. M., Kruijswijk, D., van Stalborch, A. M., Huveneers, S., … van 't Veer, C. (2014). Limited role of nuclear receptor Nur77 in Escherichia coli-induced peritonitis. Infection and Immunity, 82, 253-264.
Hernandez-Nava, E., Cuellar, P., Nava, P., Chavez-Munguia, B., Schnoor, M., Orozco, E., & Betanzos, A. (2017). Adherens junctions and desmosomes are damaged by Entamoeba histolytica: Participation of EhCPADH complex and EhCP112 protease. Cellular Microbiology, 19. https://doi.org/10.1111/cmi.12761.e12761
Hilgendorf, C., Spahn-Langguth, H., Regardh, C. G., Lipka, E., Amidon, G. L., & Langguth, P. (2000). Caco-2 versus Caco-2/HT29-MTX co-cultured cell lines: permeabilities via diffusion, inside- and outside-directed carrier-mediated transport. Journal of Pharmaceutical Sciences, 89, 63-75.
Huang, Z., Wang, Z., Long, S., Jiang, H., Chen, J., Zhang, J., & Dong, L. (2014). A 3-D artificial colon tissue mimic for the evaluation of nanoparticle-based drug delivery system. Molecular Pharmaceutics, 11, 2051-2061.
Huston, C. D., Houpt, E. R., Mann, B. J., Hahn, C. S., & Petri, W. A., Jr. (2000). Caspase 3-dependent killing of host cells by the parasite Entamoeba histolytica. Cellular Microbiology, 2, 617-625.
Jalili-Firoozinezhad, S., Gazzaniga, F. S., Calamari, E. L., Camacho, D. M., Fadel, C. W., Bein, A., … Ingber, D. E. (2019). A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nature Biomedical Engineering, 3, 520-531.
Kamarainen, M., Heiskala, K., Knuutila, S., Heiskala, M., Winqvist, O., & Andersson, L. C. (2003). RELP, a novel human REG-like protein with up-regulated expression in inflammatory and metaplastic gastrointestinal mucosa. The American Journal of Pathology, 163, 11-20.
Kim, H. J., Li, H., Collins, J. J., & Ingber, D. E. (2016). Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. Proceedings of the National Academy of Sciences of the United States of America, 113, E7-E15.
Kopitar-Jerala, N. (2017). The role of interferons in inflammation and inflammasome activation. Frontiers in Immunology, 8, 873.
Kruse, J. P., & Gu, W. (2009). Modes of p53 regulation. Cell, 137, 609-622.
Lago, M., Monteil, V., Douche, T., Guglielmini, J., Criscuolo, A., Maufrais, C., … Norel, F. (2017). Proteome remodelling by the stress sigma factor RpoS/sigma(S) in Salmonella: identification of small proteins and evidence for post-transcriptional regulation. Scientific Reports, 7, 2127.
Lee, E., Schiller, L. R., & Fordtran, J. S. (1988). Quantification of colonic lamina propria cells by means of a morphometric point-counting method. Gastroenterology, 94, 409-418.
Leopold Wager, C. M., Arnett, E., & Schlesinger, L. S. (2019). Macrophage nuclear receptors: Emerging key players in infectious diseases. PLoS Pathogens, 15, e1007585.
Leroy, A., Lauwaet, T., De Bruyne, G., Cornelissen, M., & Mareel, M. (2000). Entamoeba histolytica disturbs the tight junction complex in human enteric T84 cell layers. FASEB Journal, 14, 1139-1146.
Lesuffleur, T., Barbat, A., Luccioni, C., Beaumatin, J., Clair, M., Kornowski, A., … Zweibaum, A. (1991). Dihydrofolate reductase gene amplification-associated shift of differentiation in methotrexate-adapted HT-29 cells. The Journal of Cell Biology, 115, 1409-1418.
Li, E., Stenson, W. F., Kunz-Jenkins, C., Swanson, P. E., Duncan, R., & Stanley, S. L., Jr. (1994). Entamoeba histolytica interactions with polarized human intestinal Caco-2 epithelial cells. Infection and Immunity, 62, 5112-5119.
Li, N., Wang, D., Sui, Z., Qi, X., Ji, L., Wang, X., & Yang, L. (2013). Development of an improved three-dimensional in vitro intestinal mucosa model for drug absorption evaluation. Tissue Engineering. Part C, Methods, 19, 708-719.
Liao, Y., Smyth, G. K., & Shi, W. (2014). featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923-930.
Liberzon, A., Birger, C., Thorvaldsdottir, H., Ghandi, M., Mesirov, J. P., & Tamayo, P. (2015). The molecular signatures database (MSigDB) hallmark gene set collection. Cell Systems, 1, 417-425.
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
Low, E. N. D., Mokhtar, N. M., Wong, Z., & Raja Ali, R. A. (2019). Colonic mucosal transcriptomic changes in patients with long-duration ulcerative colitis revealed colitis-associated cancer pathways. Journal of Crohn's & Colitis, 13, 755-763.
MacMicking, J. D. (2012). Interferon-inducible effector mechanisms in cell-autonomous immunity. Nature Reviews. Immunology, 12, 367-382.
Majoros, A., Platanitis, E., Kernbauer-Holzl, E., Rosebrock, F., Muller, M., & Decker, T. (2017). Canonical and Non-Canonical Aspects of JAK-STAT Signaling: Lessons from Interferons for Cytokine Responses. Frontiers in Immunology, 8, 29.
Mamuya, F. A., & Duncan, M. K. (2012). aV integrins and TGF-beta-induced EMT: a circle of regulation. Journal of Cellular and Molecular Medicine, 16, 445-455.
Marie, C., & Petri, W. A., Jr. (2014). Regulation of virulence of Entamoeba histolytica. Annual Review of Microbiology, 68, 493-520.
Marie, C., Verkerke, H. P., Theodorescu, D., & Petri, W. A. (2015). A whole-genome RNAi screen uncovers a novel role for human potassium channels in cell killing by the parasite Entamoeba histolytica. Scientific Reports, 5, 13613.
Marquay Markiewicz, J., Syan, S., Hon, C. C., Weber, C., Faust, D., & Guillen, N. (2011). A proteomic and cellular analysis of uropods in the pathogen Entamoeba histolytica. PLoS Neglected Tropical Diseases, 5, e1002.
Medema, R. H., & Macurek, L. (2012). Checkpoint control and cancer. Oncogene, 31, 2601-2613.
Monroy, V. S., Flores, M. O., Villalba-Magdaleno, J. D., Garcia, C. G., & Ishiwara, D. G. (2010). Entamoeba histolytica: Differential gene expression during programmed cell death and identification of early pro- and anti-apoptotic signals. Experimental Parasitology, 126, 497-505.
Moonah, S. N., Abhyankar, M. M., Haque, R., & Petri, W. A., Jr. (2014). The macrophage migration inhibitory factor homolog of Entamoeba histolytica binds to and immunomodulates host macrophages. Infection and Immunity, 82, 3523-3530.
Mortimer, L., Moreau, F., Cornick, S., & Chadee, K. (2015). The NLRP3 inflammasome is a pathogen sensor for invasive Entamoeba histolytica via activation of alpha5beta1 integrin at the macrophage-amebae intercellular junction. PLoS Pathogens, 11, e1004887.
Murray-Zmijewski, F., Slee, E. A., & Lu, X. (2008). A complex barcode underlies the heterogeneous response of p53 to stress. Nature Reviews. Molecular Cell Biology, 9, 702-712.
Nagafuchi, A., & Takeichi, M. (1988). Cell binding function of E-cadherin is regulated by the cytoplasmic domain. The EMBO Journal, 7, 3679-3684.
Nagaraja, S., & Ankri, S. (2018). Utilization of different omic approaches to unravel stress response mechanisms in the parasite Entamoeba histolytica. Frontiers in Cellular and Infection Microbiology, 8, 19.
Nakada-Tsukui, K., & Nozaki, T. (2016). Immune response of amebiasis and immune evasion by Entamoeba histolytica. Frontiers in Immunology, 7, 175.
Natoli, M., Leoni, B. D., D'Agnano, I., Zucco, F., & Felsani, A. (2012). Good Caco-2 cell culture practices. Toxicology In Vitro, 26, 1243-1246.
Navabi, N., McGuckin, M. A., & Linden, S. K. (2013). Gastrointestinal cell lines form polarized epithelia with an adherent mucus layer when cultured in semi-wet interfaces with mechanical stimulation. PLoS One, 8, e68761.
Ohshima, K., Kanto, K., Hatakeyama, K., Ide, T., Wakabayashi-Nakao, K., Watanabe, Y., … Mochizuki, T. (2014). Exosome-mediated extracellular release of polyadenylate-binding protein 1 in human metastatic duodenal cancer cells. Proteomics, 14, 2297-2306.
Pageot, L. P., Perreault, N., Basora, N., Francoeur, C., Magny, P., & Beaulieu, J. F. (2000). Human cell models to study small intestinal functions: recapitulation of the crypt-villus axis. Microscopy Research and Technique, 49, 394-406.
Pelaseyed, T., Bergstrom, J. H., Gustafsson, J. K., Ermund, A., Birchenough, G. M., Schutte, A., … Hansson, G. C. (2014). The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunological Reviews, 260, 8-20.
Perdomo, D., Baron, B., Rojo-Dominguez, A., Raynal, B., England, P., & Guillen, N. (2013). The alpha-helical regions of KERP1 are important in Entamoeba histolytica adherence to human cells. Scientific Reports, 3, 1171.
Perdomo, D., Manich, M., Syan, S., Olivo-Marin, J. C., Dufour, A. C., & Guillen, N. (2016). Intracellular traffic of the lysine and glutamic acid rich protein KERP1 reveals features of endomembrane organization in Entamoeba histolytica. Cellular Microbiology, 18, 1134-1152.
Petrey, A. C., & de la Motte, C. A. (2017). The extracellular matrix in IBD: A dynamic mediator of inflammation. Current Opinion in Gastroenterology, 33, 234-238.
Petri, W. A., Jr., Haque, R., & Mann, B. J. (2002). The bittersweet interface of parasite and host: lectin-carbohydrate interactions during human invasion by the parasite Entamoeba histolytica. Annual Review of Microbiology, 56, 39-64.
Pineda, E., & Perdomo, D. (2017). Entamoeba histolytica under oxidative stress: What countermeasure mechanisms are in place? Cell, 6, pii: E44.
Ploper, D., & De Robertis, E. M. (2015). The MITF family of transcription factors: Role in endolysosomal biogenesis, Wnt signaling, and oncogenesis. Pharmacological Research, 99, 36-43.
Quintana-Hayashi, M. P., & Lindén, S. K. (2018). Differentiation of gastrointestinal cell lines by culture in semi-wet interface. Methods in Molecular Biology, 1817, 41-46.
Ralston, K. S., & Petri, W. A., Jr. (2011). Tissue destruction and invasion by Entamoeba histolytica. Trends in Parasitology, 27, 254-263.
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015). limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research, 43, e47.
Roychaudhuri, R., Yang, M., Hoshi, M. M., & Teplow, D. B. (2009). Amyloid beta-protein assembly and Alzheimer disease. The Journal of Biological Chemistry, 284, 4749-4753.
Sano, R., & Reed, J. C. (2013). ER stress-induced cell death mechanisms. Biochimica et Biophysica Acta, 1833, 3460-3470.
Schroder, K., Hertzog, P. J., Ravasi, T., & Hume, D. A. (2004). Interferon-gamma: An overview of signals, mechanisms and functions. Journal of Leukocyte Biology, 75, 163-189.
Schroder, M., & Kaufman, R. J. (2005). The mammalian unfolded protein response. Annual Review of Biochemistry, 74, 739-789.
Seigneur, M., Mounier, J., Prevost, M. C., & Guillen, N. (2005). A lysine- and glutamic acid-rich protein, KERP1, from Entamoeba histolytica binds to human enterocytes. Cellular Microbiology, 7, 569-579.
Seydel, K. B., Li, E., Swanson, P. E., & Stanley, S. L., Jr. (1997). Human intestinal epithelial cells produce proinflammatory cytokines in response to infection in a SCID mouse-human intestinal xenograft model of amebiasis. Infection and Immunity, 65, 1631-1639.
Shen, X. M., Okuno, T., Milone, M., Otsuka, K., Takahashi, K., Komaki, H., … Engel, A. G. (2016). Mutations causing slow-channel myasthenia reveal that a valine ring in the channel pore of muscle AChR is optimized for stabilizing channel gating. Human Mutation, 37, 1051-1059.
Huang da, W., Sherman, B. T., & Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4, 44-57.
Shin, W., & Kim, H. J. (2018). Intestinal barrier dysfunction orchestrates the onset of inflammatory host-microbiome cross-talk in a human gut inflammation-on-a-chip. Proceedings of the National Academy of Sciences of the United States of America, 115, E10539-e10547.
Shirley, D. T., Farr, L., Watanabe, K., & Moonah, S. (2018). A review of the global burden, new diagnostics, and current therapeutics for amebiasis. Open Forum Infectectious Diseases, 5, ofy161.
Smith, J. A. (2018). Regulation of cytokine production by the unfolded protein response; Implications for infection and autoimmunity. Frontiers in Immunology, 9, 422.
Srinivasan, B., Kolli, A. R., Esch, M. B., Abaci, H. E., Shuler, M. L., & Hickman, J. J. (2015). TEER measurement techniques for in vitro barrier model systems. Journal of Laboratory Automation, 20, 107-126.
Stepanov, G. A., Filippova, J. A., Komissarov, A. B., Kuligina, E. V., Richter, V. A., & Semenov, D. V. (2015). Regulatory role of small nucleolar RNAs in human diseases. BioMed Research International, 2015, 206849.
St-Pierre, J., Moreau, F., Cornick, S., Quach, J., Begum, S., Aracely Fernandez, L., … Chadee, K. (2017). The macrophage cytoskeleton acts as a contact sensor upon interaction with Entamoeba histolytica to trigger IL-1beta secretion. PLoS Pathogens, 13, e1006592.
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., … Mesirov, J. P. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America, 102, 15545-15550.
Sun, C. C., Li, S. J., Li, G., Hua, R. X., Zhou, X. H., & Li, D. J. (2016). Long intergenic noncoding RNA 00511 acts as an oncogene in non-small-cell lung cancer by binding to EZH2 and suppressing p57. Molecular Therapy-Nucleic Acids, 5, e385.
Sun, H. Q., Kwiatkowska, K., Wooten, D. C., & Yin, H. L. (1995). Effects of CapG overexpression on agonist-induced motility and second messenger generation. The Journal of Cell Biology, 129, 147-156.
Thibeaux, R., Ave, P., Bernier, M., Morcelet, M., Frileux, P., Guillen, N., & Labruyere, E. (2014). The parasite Entamoeba histolytica exploits the activities of human matrix metalloproteinases to invade colonic tissue. Nature Communications, 5, 5142.
Thibeaux, R., Dufour, A., Roux, P., Bernier, M., Baglin, A. C., Frileux, P., … Labruyère, E. (2012). Newly visualized fibrillar collagen scaffolds dictate Entamoeba histolytica invasion route in the human colon. Cellular Microbiology, 14, 609-621.
Thibeaux, R., Weber, C., Hon, C. C., Dillies, M. A., Ave, P., Coppee, J. Y., … Guillén, N. (2013). Identification of the virulence landscape essential for Entamoeba histolytica invasion of the human colon. PLoS Pathogens, 9, e1003824.
Tyanova, S., Temu, T., & Cox, J. (2016). The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nature Protocols, 11, 2301-2319.
Ujang, J. A., Kwan, S. H., Ismail, M. N., Lim, B. H., Noordin, R., & Othman, N. (2016). Proteome analysis of excretory-secretory proteins of Entamoeba histolytica HM1:IMSS via LC-ESI-MS/MS and LC-MALDI-TOF/TOF. Clinical Proteomics, 13, 33.
Ulm, H., Wilmes, M., Shai, Y., & Sahl, H. G. (2012). Antimicrobial host defensins-Specific antibiotic activities and innate defense modulation. Frontiers in Immunology, 3, 249.
Vizcaino, J. A., Csordas, A., Del-Toro, N., Dianes, J. A., Griss, J., Lavidas, I., … Hermjakob, H. (2016). 2016 update of the PRIDE database and its related tools. Nucleic Acids Research, 44, 11033.
Wang, Y., Kim, R., Gunasekara, D. B., Reed, M. I., DiSalvo, M., Nguyen, D. L., … Allbritton, N. L. (2018). Formation of human colonic crypt array by application of chemical gradients across a shaped epithelial monolayer. Cellular and Molecular Gastroenterology and Hepatology, 5, 113-130.
Wessel, D., & Flugge, U. I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Analytical Biochemistry, 138, 141-143.
Wieczorek, S., Combes, F., Lazar, C., Giai Gianetto, Q., Gatto, L., Dorffer, A., … Burger, T. (2017). DAPAR & ProStaR: Software to perform statistical analyses in quantitative discovery proteomics. Bioinformatics, 33, 135-136.
Wu, D., & Smyth, G. K. (2012). Camera: A competitive gene set test accounting for inter-gene correlation. Nucleic Acids Research, 40, e133.
Yang, D., Chen, Q., Chertov, O., & Oppenheim, J. J. (2000). Human neutrophil defensins selectively chemoattract naive T and immature dendritic cells. Journal of Leukocyte Biology, 68, 9-14.
Yano, T., Kanoh, H., Tamura, A., & Tsukita, S. (2017). Apical cytoskeletons and junctional complexes as a combined system in epithelial cell sheets. Annals of the New York Academy of Sciences, 1405, 32-43.
Ye, D., Dawson, K. A., & Lynch, I. (2015). A TEM protocol for quality assurance of in vitro cellular barrier models and its application to the assessment of nanoparticle transport mechanisms across barriers. Analyst, 140, 83-97.
Yu, M., Li, W., Wang, Q., Wang, Y., & Lu, F. (2018). Circadian regulator NR1D2 regulates glioblastoma cell proliferation and motility. Oncogene, 37, 4838-4853.