دورية أكاديمية

Plakins are involved in the regulation of centrosome position in polarized epithelial cells.

التفاصيل البيبلوغرافية
العنوان: Plakins are involved in the regulation of centrosome position in polarized epithelial cells.
المؤلفون: Geay J; Université de Paris, CEA/INSERM/AP-HP, Institut de Recherche Saint Louis, UMR976, HIPI, CytoMorpho Lab, Hopital Saint Louis, Paris, France., Margaron Y; Université Grenoble-Alpes, CEA/INRA/CNRS, Interdisciplinary Research Institute of Grenoble, UMR5168, LPCV, CytoMorpho Lab, Grenoble, France., Gentien D; Université PSL, Department of Translational Research, Institut Curie, Genomics Platform, Paris, France., Reyal F; Université Paris Cité, Université PSL, INSERM U932, Breast Gynecological and Reconstructive Surgery, Institut Curie, Paris, France., Puisieux A; Université Claude Bernard Lyon 1, Cancer Research Center of Lyon, INSERM 1052, CNRS 5286, Centre Léon Bérard, Lyon, France.; Université PSL, Institut Curie, Université Versailles Saint-Quentin, CNRS UMR 3666, INSERM U1143, Paris, France., Blanchoin L; Université de Paris, CEA/INSERM/AP-HP, Institut de Recherche Saint Louis, UMR976, HIPI, CytoMorpho Lab, Hopital Saint Louis, Paris, France.; Université Grenoble-Alpes, CEA/INRA/CNRS, Interdisciplinary Research Institute of Grenoble, UMR5168, LPCV, CytoMorpho Lab, Grenoble, France., Guyon L; Université Grenoble Alpes, CEA/INSERM, Interdisciplinary Research Institute of Grenoble, BioSanté UMR_S 1292, Grenoble, France., Théry M; Université de Paris, CEA/INSERM/AP-HP, Institut de Recherche Saint Louis, UMR976, HIPI, CytoMorpho Lab, Hopital Saint Louis, Paris, France.; Université Grenoble-Alpes, CEA/INRA/CNRS, Interdisciplinary Research Institute of Grenoble, UMR5168, LPCV, CytoMorpho Lab, Grenoble, France.
المصدر: Biology of the cell [Biol Cell] 2024 Jul; Vol. 116 (7), pp. e2400048. Date of Electronic Publication: 2024 Jun 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Wiley-Blackwell Country of Publication: England NLM ID: 8108529 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1768-322X (Electronic) Linking ISSN: 02484900 NLM ISO Abbreviation: Biol Cell Subsets: MEDLINE
أسماء مطبوعة: Publication: 2012- : Chichester : Wiley-Blackwell
Original Publication: Ivry sur Seine France : Publié par la Société française de microscopie électronique avec le concours du Centre national de la recherche scientifique et de l'Institute national de la santé et de la recherche médicale, [1981-
مواضيع طبية MeSH: Centrosome*/metabolism , Epithelial Cells*/metabolism , Cell Polarity* , Epithelial-Mesenchymal Transition* , Plakins*/metabolism , Plakins*/genetics, Humans ; Female ; Breast Neoplasms/metabolism ; Breast Neoplasms/pathology ; Breast Neoplasms/genetics ; Cell Line, Tumor ; Microtubules/metabolism
مستخلص: Background Information: The control of epithelial cell polarity is key to their function. Its dysregulation is a major cause of tissue transformation. In polarized epithelial cells,the centrosome is off-centred toward the apical pole. This asymmetry determines the main orientation of the microtubule network and intra-cellular traffic. However, the mechanism regulating centrosome positioning at the apical pole of polarized epithelial cells is still poorly undertood.
Results: In this study we used transcriptomic data from breast cancer cells to identify molecular changes associated with the different stages of tumour transformation. We correlated these changes with variations in centrosome position or with cell progression along the epithelial-to-mesenchymal transition (EMT), a process that involves centrosome repositioning. We found that low levels of epiplakin, desmoplakin and periplakin correlated with centrosome mispositioning in cells that had progressed through EMT or tissue transformation. We further tested the causal role of these plakins in the regulation of centrosome position by knocking down their expression in a non-tumorigenic breast epithelial cell line (MCF10A). The downregulation of periplakin reduced the length of intercellular junction, which was not affected by the downregulation of epiplakin or desmoplakin. However, down-regulating any of them disrupted centrosome polarisation towards the junction without affecting microtubule stability.
Conclusions: Altogether, these results demonstrated that epiplakin, desmoplakin and periplakin are involved in the maintenance of the peripheral position of the centrosome close to inter-cellular junctions. They also revealed that these plakins are downregulated during EMT and breast cancer progression, which are both associated with centrosome mispositioning.
Significance: These results revealed that the down-regulation of plakins and the consequential centrosome mispositioning are key signatures of disorganised cytoskeleton networks, inter-cellular junction weakening, shape deregulation and the loss of polarity in breast cancer cells. These metrics could further be used as a new readouts for early phases of tumoral development.
(© 2024 The Author(s). Biology of the Cell published by Wiley‐VCH GmbH on behalf of Société Française des Microscopies and Société de Biologie Cellulaire de France.)
References: Aho, S., Li, K., Ryoo, Y., McGee, C., Ishida‐Yamamoto, A., Uitto, J. & Klement, J. F. (2004) Periplakin gene targeting reveals a constituent of the cornified cell envelope dispensable for normal mouse development. Molecular and Cellular Biology, 24, 6410–6418.
Aho, S., Lupo, J., Coly, P.‐A., Sabine, A., Castellazzi, M., Morand, P., Sergeant, A., Manet, E., Boyer, V. & Gruffat, H. (2009) Characterization of the ubinuclein protein as a new member of the nuclear and adhesion complex components (NACos). Biology of the Cell, 101, 319–334.
Azioune, A., Carpi, N., Tseng, Q., Théry, M. & Piel, M. (2010) Protein micropatterns: a direct printing protocol using deep UVs. Methods in Cell Biology, 97, 133–146.
Barlan, K. & Gelfand, V. I. (2017) Microtubule‐based transport and the distribution, tethering, and organization of organelles. Cold Spring Harbor Perspectives in Biology, 9, a025817.
Bouameur, J. E., Favre, B. & Borradori, L. (2014) Plakins, a versatile family of cytolinkers: roles in skin integrity and in human diseases. Journal of Investigative Dermatology, 134, 885–894.
Brabletz, T., Kalluri, R., Nieto, M. A. & Weinberg, R. A. (2018) EMT in cancer. Nature Reviews Cancer, 18, 128–134.
Broussard, J. A., Koetsier, J. L., Hegazy, M. & Green, K. J. (2021) Desmosomes polarize and integrate chemical and mechanical signaling to govern epidermal tissue form and function. Current Biology, 31, 3275–3291.e5.
Burute, M., Thery, M. & Théry, M. (2012) Spatial segregation between cell‐cell and cell‐matrix adhesions. Current Opinion in Cell Biology, 24, 628–636.
Burute, M., Prioux, M., Blin, G., Truchet, S., Letort, G., Tseng, Q., Bessy, T., Lowell, S., Young, J., Filhol, O., Théry, M. (2017) Polarity reversal by centrosome repositioning primes cell scattering during epithelial‐to‐mesenchymal transition. Developmental Cell, 40, 168–184.
Chun, M. G. H. & Hanahan, D. (2010) Genetic deletion of the desmosomal component desmoplakin promotes tumor microinvasion in a mouse model of pancreatic neuroendocrine carcinogenesis. PLoS Genetics, 6, e1001120.
Darwich, A. S., Aslam, U., Ashcroft, D. M. & Rostami‐Hodjegan, A. (2014) Meta‐analysis of the turnover of intestinal epithelia in preclinical animal species and humans. Drug Metabolism and Disposition, 42, 2016–2022.
Dash, C. S. K., Behera, A. K., Dehuri, S. & Ghosh, A. (2023) An outliers detection and elimination framework in classification task of data mining. Decision Analytics Journal, 6, 100164.
Dent, R., Hanna, W. M., Trudeau, M., Rawlinson, E., Sun, P. & Narod, S. A. (2009) Pattern of metastatic spread in triple‐negative breast cancer. Breast Cancer Research and Treatment, 115, 423–428.
Ebnet, K., Kummer, D., Steinbacher, T., Singh, A., Nakayama, M. & Matis, M. (2018) Regulation of cell polarity by cell adhesion receptors. Seminars in Cell & Developmental Biology, 81, 2–12.
Fustaino, V., Presutti, D., Colombo, T., Cardinali, B., Papoff, G., Brandi, R., Bertolazzi, P., Felici, G. & Ruberti, G. (2017) Characterization of epithelial‐mesenchymal transition intermediate/hybrid phenotypes associated to resistance to EGFR inhibitors in non‐small cell lung cancer cell lines. Oncotarget, 8, 103340–103363.
Gallicano, G. I., Bauer, C. & Fuchs, E. (2001) Rescuing desmoplakin function in extra‐embryonic ectoderm reveals the importance of this protein in embryonic heart, neuroepithelium, skin and vasculature. Development (Cambridge, England), 128, 929–941.
Gan, Z., Ding, L., Burckhardt, C. J., Lowery, J., Zaritsky, A., Sitterley, K., Mota, A., Costigliola, N., Starker, C. G., Voytas, D. F., Tytell, J., Goldman, R. D., & Danuser, G. (2016) Vimentin intermediate filaments template microtubule networks to enhance persistence in cell polarity and directed migration. Cell Systems, 3, 252–263.e8.
Haupt, A. & Minc, N. (2018) How cells sense their own shape—mechanisms to probe cell geometry and their implications in cellular organization and function. Journal of Cell Science, 131, jcs214015.
Hinck, L., Näthke, I. & Na, I. (2014) Changes in cell and tissue organization in cancer of the breast and colon. Current Opinion in Cell Biology, 26, 87–95.
Hu, L., Huang, Z., Wu, Z., Ali, A. & Qian, A. (2018) Mammalian plakins, giant cytolinkers: versatile biological functions and roles in cancer. International Journal of Molecular Sciences, 19, 974.
Huang, D. 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.
Huang, R. Y.‐J., Guilford, P. & Thiery, J. P. (2012) Early events in cell adhesion and polarity during epithelial‐mesenchymal transition. Journal of Cell Science 4417–4422.
Hudis, C. A. & Gianni, L. (2011) Triple‐negative breast cancer: an unmet medical need. The Oncologist, 16, 1–11.
Jang, M. H., Kim, H. J., Kim, E. J., Chung, Y. R. & Park, S. Y. (2015) Expression of epithelial‐mesenchymal transition‐related markers in triple‐negative breast cancer: ZEB1 as a potential biomarker for poor clinical outcome. Human Pathology, 46, 1267–1274.
Jefferson, J. J., Leung, C. L. & Liem, R. K. H. (2004) Plakins: Goliaths that link cell junctions and the cytoskeleton. Nature Reviews Molecular Cell Biology, 5, 542–553.
Jimenez, A. J., Schaeffer, A., De Pascalis, C., Letort, G., Vianay, B., Bornens, M., Piel, M., Blanchoin, L. & Théry, M. (2021) Acto‐myosin network geometry defines centrosome position. Current Biology, 31, 1206–1220.e5.
Jung, H.‐Y. Y., Fattet, L., Tsai, J. H., Kajimoto, T., Chang, Q., Newton, A. C. & Yang, J. (2019) Apical–basal polarity inhibits epithelial–mesenchymal transition and tumour metastasis by PAR‐complex‐mediated SNAI1 degradation. Nature Cell Biology, 21, 359–371.
Kokado, M., Okada, Y., Miyamoto, T., Yamanaka, O. & Saika, S. (2016) Effects of epiplakin‐knockdown in cultured corneal epithelial cells. BMC Research Notes, 9, 1–5.
Lambert, A. W. & Weinberg, R. A. (2021) Linking EMT programmes to normal and neoplastic epithelial stem cells. Nature Reviews Cancer, 21, 325–338.
Lechler, T. & Fuchs, E. (2007) Desmoplakin: an unexpected regulator of microtubule organization in the epidermis. Journal of Cell Biology, 176, 147–154.
Leduc, C. & Etienne‐Manneville, S. (2017) Regulation of microtubule‐associated motors drives intermediate filament network polarization. Journal of Cell Biology, 216, 1689–1703.
Lee, M. & Vasioukhin, V. (2008) Cell polarity and cancer—cell and tissue polarity as a non‐canonical tumor suppressor. Journal of Cell Science, 121, 1141–1150.
Lehmann, B. D., Bauer, J. A., Chen, X., Sanders, M. E., Chakravarthy, A. B., Shyr, Y. & Pietenpol, J. A. (2011) Identification of human triple‐negative breast cancer subtypes and preclinical models for selection of targeted therapies. Journal of Clinical Investigation, 121, 2750–2767.
Lerebours, F., Vacher, S., Guinebretiere, J. M., Rondeau, S., Caly, M., Gentien, D., Van Laere, S., Bertucci, F., de la Grange, P., Bièche, L., et al. (2021) Hemoglobin overexpression and splice signature as new features of inflammatory breast cancer? Journal of Advanced Research, 28, 77–85.
Li, R. & Gundersen, G. G. (2008) Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nature Reviews Molecular Cell Biology, 9, 860–873.
Liem, R. K. H. (2016) Cytoskeletal integrators: the spectrin superfamily. Cold Spring Harbor Perspectives in Biology, 8, a018259.
Liu, J., Welm, B., Boucher, K. M., Ebbert, M. T. W. & Bernard, P. S. (2012) TRIM29 functions as a tumor suppressor in nontumorigenic breast cells and invasive ER+ breast cancer. American Journal of Pathology, 180, 839–847.
Lord, S. J., Velle, K. B., Mullins, R. D. & Fritz‐Laylin, L. K. (2020) SuperPlots: communicating reproducibility and variability in cell biology. Journal of Cell Biology, 219, e202001064.
Lu, S., Liu, Y., Tian, S., He, Y. & Dong, W. (2023) KIFC3 regulates progression of hepatocellular carcinoma via EMT and the AKT/mTOR pathway. Experimental Cell Research, 426, 113564.
Lüönd, F., Sugiyama, N., Bill, R., Bornes, L., Hager, C., Tang, F., Santacroce, N., Beisel, C., Ivanek, R., Bürglin, T., Tiede, S., van Rheenen, J. & Christofori, G. (2021) Distinct contributions of partial and full EMT to breast cancer malignancy. Developmental Cell, 56, 3203–3221.e11.
Morel, A.‐P., Hinkal, G. W., Thomas, C., Fauvet, F., Courtois‐Cox, S., Wierinckx, A., Devouassoux‐Shisheboran, M., Treilleux, I., Tissier, A., Gras, B., Pourchet, J., Puisieux, I., Browne, G. J., Spicer, D. B., Lachuer, J., Ansieau, S. & Puisieux, A. (2012) EMT inducers catalyze malignant transformation of mammary epithelial cells and drive tumorigenesis towards claudin‐low tumors in transgenic mice. PLoS Genetics, 8, e1002723.
Moreno‐Bueno, G., Portillo, F. & Cano, A. (2008) Transcriptional regulation of cell polarity in EMT and cancer. Oncogene, 27, 6958–6969.
Muthuswamy, S. K. & Xue, B. (2012) Cell polarity as a regulator of cancer cell behavior plasticity. Annual Review of Cell and Developmental Biology, 28, 599–625.
Noordstra, I., Liu, Q., Nijenhuis, W., Hua, S., Jiang, K. Baars, M., Remmelzwaal, S., Martin, M., Kapitein, L. C. & Akhmanova, A. (2016) Control of apico‐basal epithelial polarity by the microtubule minus‐end binding protein CAMSAP3 and spectraplakin ACF7. Journal of Cell Science, 129, 4278–4288.
Okumura, R. & Takeda, K. (2017) Roles of intestinal epithelial cells in the maintenance of gut homeostasis. Experimental & Molecular Medicine, 49, e338.
Oriolo, A. S., Wald, F. A., Ramsauer, V. P. & Salas, P. J. I. (2007) Intermediate filaments: a role in epithelial polarity. Experimental Cell Research, 313, 2255–2264.
Peglion, F. & Etienne‐Manneville, S. (2024) Cell polarity changes in cancer initiation and progression. Journal of Cell Biology, 223, 1–15.
Prechova, M., Korelova, K. & Gregor, M. (2023) Plectin. Current Biology, 33, R128–R130.
R Core Team (2022) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Rodriguez‐Fraticelli, A. E., Auzan, M., Alonso, M. a, Bornens, M. & Martin‐Belmonte, F. (2012) Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis. Journal of Cell Biology, 198, 1011–1023.
Rody, A., Karn, T., Liedtke, C., Pusztai, L., Ruckhaeberle, E., Hanker, L., Gaetje, R., Solbach, C., Ahr, A., Metzler, D., Schmidt, M., Müller, V., Holtrich, U. & Kaufmann, M. (2011) A clinically relevant gene signature in triple negative and basal‐like breast cancer. Breast Cancer Research. 13, R97.
Roignot, J., Peng, X. & Mostov, K. (2013) Polarity in mammalian epithelial morphogenesis. Cold Spring Harbor Perspectives in Biology, 5, 1–16.
Saitoh, M. (2018) JB special review‐cellular plasticity in epithelial homeostasis and diseases: involvement of partial EMT in cancer progression. Journal of Biochemistry, 164, 257–264.
Sarrió, D., Rodriguez‐Pinilla, S. M., Hardisson, D., Cano, A., Moreno‐Bueno, G. & Palacios, J. (2008) Epithelial‐mesenchymal transition in breast cancer relates to the basal‐like phenotype. Cancer Research, 68, 989–997.
Schaedel, L., Lorenz, C., Schepers, A. V., Klumpp, S. & Köster, S. (2021) Vimentin intermediate filaments stabilize dynamic microtubules by direct interactions. Nature Communications, 12, 3799.
Schöck, F. & Perrimon, N. (2002) Molecular mechanisms of epithelial morphogenesis. Annual Review of Cell and Developmental Biology, 18, 463–493.
Sevilla, L. M., Nachat, R., Groot, K. R., Klement, J. F., Uitto, J., Djian, P., Määttä, A. & Watt, F. M. (2007) Mice deficient in involucrin, envoplakin, and periplakin have a defective epidermal barrier. Journal of Cell Biology, 179, 1599–1612.
Sonnenberg, A. & Liem, R. K. H. (2007) Plakins in development and disease. Experimental Cell Research, 313, 2189–2203.
Spazierer, D., Fuchs, P., Pröll, V., Janda, L., Oehler, S., Fischer, I., Hauptmann, R. & Wiche, G. (2003) Epiplakin gene analysis in mouse reveals a single exon encoding a 725‐kDa protein with expression restricted to epithelial tissues. Journal of Biological Chemistry, 278, 31657–31666.
Sternemalm, J., Geimer, S., Frikstad, K. A. M., Schink, K. O., Stokke, T. & Patzke, S. (2015) CSPP‐L associates with the desmosome of polarized epithelial cells and is required for normal spheroid formation. PLoS ONE, 10, 1–19.
Su, J., Morgani, S. M., David, C. J., Wang, Q., Er, E. E., Huang, Y.‐H., Basnet, H., Zou, Y., Shu, W., Soni, R. K., Hendrickson, R. C., Hadjantonakis, A. K. & Massagué, J. (2020) TGF‐β orchestrates fibrogenic and developmental EMTs via the RAS effector RREB1. Nature, 577, 566–571.
Suárez‐Fariñas, M., Dhingra, N., Gittler, J., Shemer, A., Cardinale, I., de Guzman Strong, C., Krueger, J. G. & Guttman‐Yassky, E. (2013) Intrinsic atopic dermatitis shows similar TH2 and higher TH17 immune activation compared with extrinsic atopic dermatitis. Journal of Allergy and Clinical Immunology, 132, 361–370.
Suozzi, K. C., Wu, X. & Fuchs, E. (2012) Spectraplakins: master orchestrators of cytoskeletal dynamics. Journal of Cell Biology, 197, 465–475.
Taube, J. H., Herschkowitz, J. I., Komurov, K., Zhou, A. Y., Gupta, S., Yang, J., Hartwell, K., Onder, T. T., Gupta, P. B., Evans, K. W., Hollier, B. G., Ram, P. T., Lander, E. S., Rosen, J. M., Weinberg, R. A. & Mani, S. A. (2010) Core epithelial‐to‐mesenchymal transition interactome gene‐expression signature is associated with claudin‐low and metaplastic breast cancer subtypes. Proceedings of the National Academy of Sciences of the United States of America, 107, 15449–15454.
Tortosa, E., Galjart, N., Avila, J. & Sayas, C. L. (2013) MAP1B regulates microtubule dynamics by sequestering EB1/3 in the cytosol of developing neuronal cells. The EMBO Journal, 32, 1293–1306.
Toya, M., Kobayashi, S., Kawasaki, M., Shioi, G., Kaneko, M., Ishiuchi, T., Misaki, K., Meng, W. & Takeichi, M. (2016) CAMSAP3 orients the apical‐to‐basal polarity of microtubule arrays in epithelial cells. Proceedings of the National Academy of Sciences of the United States of America, 113, 332–337.
Tsai, J. H. & Yang, J. (2013) Epithelial‐mesenchymal plasticity in carcinoma metastasis. Genes & Development, 27, 2192–2206.
Tseng, Q., Duchemin‐Pelletier, E., Deshiere, A., Balland, M., Guillou, H., Filhol, O. & Théry, M. (2012) Spatial organization of the extracellular matrix regulates cell‐cell junction positioning. Proceedings of the National Academy of Sciences of the United States of America, 109, 1506–1511.
Uhler, C. & Shivashankar, G. V. (2017) Regulation of genome organization and gene expression by nuclear mechanotransduction. Nature Reviews Molecular Cell Biology, 18, 717–727.
Wesley, T., Berzins, S., Kannourakis, G. & Ahmed, N. (2021) The attributes of plakins in cancer and disease: perspectives on ovarian cancer progression, chemoresistance and recurrence. Cell Communication and Signaling, 19, 1–21.
Whitford, M. K. M. & McCaffrey, L. (2023) Polarity in breast development and cancer. Elsevier.
Wirtz‐Peitz, F., Nishimura, T. & Knoblich, J. A. (2008) Linking cell cycle to asymmetric division: aurora‐a phosphorylates the par complex to regulate numb localization. Cell, 135, 161–173.
Wodarz, A. & Näthke, I. (2007) Cell polarity in development and cancer. Nature Cell Biology, 9, 1016–1024.
Wu, X., Kodama, A. & Fuchs, E. (2008) ACF7 regulates cytoskeletal‐focal adhesion dynamics and migration and has ATPase activity. Cell, 135, 137–148.
Wu, X., Shen, Q. T., Oristian, D. S., Lu, C. P., Zheng, Q., Wang, H. W. & Fuchs, E. (2011) Skin stem cells orchestrate directional migration by regulating microtubule‐ACF7 connections through GSK3β. Cell, 144, 341–352.
Yao, T., Hu, W., Chen, J., Shen, L., Yu, Y., Tang, Z., Zang, G., Zhang, Y. & Chen, X. (2022) Collagen XV mediated the epithelial‐mesenchymal transition to inhibit hepatocellular carcinoma metastasis. Journal of Gastrointestinal Oncology, 13, 2472–2484.
Zhong, P., Shu, R., Wu, H., Liu, Z., Shen, X. & Hu, Y. (2021) Low KRT15 expression is associated with poor prognosis in patients with breast invasive carcinoma. Experimental and Therapeutic Medicine, 21, 305.
معلومات مُعتمدة: 771599 International ERC_ European Research Council; 780458 International ERC_ European Research Council
المشرفين على المادة: 0 (Plakins)
تواريخ الأحداث: Date Created: 20240608 Date Completed: 20240712 Latest Revision: 20240712
رمز التحديث: 20240712
DOI: 10.1111/boc.202400048
PMID: 38850178
قاعدة البيانات: MEDLINE
الوصف
تدمد:1768-322X
DOI:10.1111/boc.202400048