Ectopic expression of matrix metalloproteinases and filopodia extension via JNK activation are involved in the invasion of blood tumor cells in Drosophila mxc mutant.
Drosophila
JNK
filopodia
hemocyte
invasion
tumor
Journal
Genes to cells : devoted to molecular & cellular mechanisms
ISSN: 1365-2443
Titre abrégé: Genes Cells
Pays: England
ID NLM: 9607379
Informations de publication
Date de publication:
Oct 2023
Oct 2023
Historique:
revised:
12
08
2023
received:
07
07
2023
accepted:
12
08
2023
pubmed:
24
8
2023
medline:
24
8
2023
entrez:
24
8
2023
Statut:
ppublish
Résumé
Drosophila mxc
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
709-726Subventions
Organisme : Japan Society for the Promotion of Science
ID : Grant-in-Aid for Scientific Research(C)/17K07500
Informations de copyright
© 2023 The Authors. Genes to Cells published by Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd.
Références
Amack, J. D. (2021). Cellular dynamics of EMT: Lessons from live in vivo imaging of embryonic development. Cell Communication and Signaling: CCS, 19, 79. https://doi.org/10.1186/s12964-021-00761-8
Araki, M., Kurihara, M., Kinoshita, S., Awane, R., Sato, T., Ohkawa, Y., & Inoue, Y. H. (2019). Anti-tumour effects of antimicrobial peptides, components of the innate immune system, against haematopoietic tumours in Drosophila mxc mutants. Disease Models & Mechanisms, 12, dmm037721. https://doi.org/10.1242/dmm.037721
Armstrong, A. J., Marengo, M. S., Oltean, S., Kemeny, G., Bitting, R. L., Turnbull, J. D., Herold, C. I., Marcom, P. K., George, D. J., & Garcia-Blanco, M. A. (2011). Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Molecular Cancer Research, 9, 997-1007. https://doi.org/10.1158/1541-7786
Banerjee, U., Girard, J. R., Goins, L. M., & Spratford, C. M. (2019). Drosophila as a genetic model for hematopoiesis. Genetics, 211, 367-417. https://doi.org/10.1534/genetics.118.300223
Benhra, N., Barrio, L., Muzzopappa, M., & Milán, M. (2018). Chromosomal instability induces cellular invasion in epithelial tissues. Developmental Cell, 47, 161-174.e4. https://doi.org/10.1016/j.devcel.2018.08.021
Chen, P. C., Tang, C. H., Lin, L. W., Tsai, C. H., Chu, C. Y., Lin, T. H., & Huang, Y. L. (2017). Thrombospondin-2 promotes prostate cancer bone metastasis by the up-regulation of matrix metalloproteinase-2 through down-regulating miR-376c expression. Journal of Hematology & Oncology, 10, 33. https://doi.org/10.1186/s13045-017-0390-6
Evans, C. J., Hartenstein, V., & Banerjee, U. (2003). Thicker than blood: Conserved mechanisms in Drosophila and vertebrate hematopoiesis. Developmental Cell, 5, 673-690. https://doi.org/10.1016/s1534-5807(03)00335-6
Fares, J., Fares, M. Y., Khachfe, H. H., Salhab, H. A., & Fares, Y. (2020). Molecular principles of metastasis: A hallmark of cancer revisited. Signal Transduction and Targeted Therapy, 5, 28. https://doi.org/10.1038/s41392-020-0134-x
Gateff, E. (1994). Tumor-suppressor genes, hematopoietic malignancies and other hematopoietic disorders of Drosophila melanogaster. Annals of the New York Academy of Sciences, 712, 260-279. https://doi.org/10.1111/j.1749-6632
Gobin, E., Bagwell, K., Wagner, J., Mysona, D., Sandirasegarane, S., Smith, N., Bai, S., Sharma, A., Schleifer, R., & She, J. X. (2019). A pan-cancer perspective of matrix metalloproteases (MMP) gene expression profile and their diagnostic/prognostic potential. BMC Cancer, 19, 581. https://doi.org/10.1186/s12885-019-5768-0
Han, D. S., & Lee, E. O. (2022). Sp1 plays a key role in vasculogenic mimicry of human prostate cancer cells. International Journal of Molecular Sciences, 23, 1321. https://doi.org/10.3390/ijms23031321
Holz, A., Bossinger, B., Strasser, T., Janning, W., & Klapper, R. (2003). The two origins of hemocytes in Drosophila. Development, 130, 4955-4962. https://doi.org/10.1242/dev.00702
Jabłońska-Trypuć, A., Matejczyk, M., & Rosochacki, S. (2016). Matrix metalloproteinases (MMPs), the main extracellular matrix (ECM) enzymes in collagen degradation, as a target for anticancer drugs. Journal of Enzyme Inhibition and Medicinal Chemistry, 31, 177-183. https://doi.org/10.3109/14756366.2016
Javelaud, D., Laboureau, J., Gabison, E., Verrecchia, F., & Mauviel, A. (2003). Disruption of basal JNK activity differentially affects key fibroblast functions important for wound healing. The Journal of Biological Chemistry, 278, 24624-24628. https://doi.org/10.1074/jbc.M301942200
Jia, Q., Liu, Y., Liu, H., & Li, S. (2014). Mmp1 and Mmp2 cooperatively induce Drosophila fat body cell dissociation with distinct roles. Scientific Reports, 4, 7535. https://doi.org/10.1038/srep07535
Jiang, W. G., Sanders, A. J., Katoh, M., Ungefroren, H., Gieseler, F., Prince, M., Thompson, S. K., Zollo, M., Spano, D., Dhawan, P., Sliva, D., Subbarayan, P. R., Sarkar, M., Honoki, K., Fujii, H., Georgakilas, A. G., Amedei, A., Niccolai, E., Amin, A., … Santini, D. (2015). Tissue invasion and metastasis: Molecular, biological and clinical perspectives. Seminars in Cancer Biology, 35, S244-S275. https://doi.org/10.1016/j.semcancer.2015.03.008
Jung, S. H., Evans, C. J., Uemura, C., & Banerjee, U. (2005). The Drosophila lymph gland as a developmental model of hematopoiesis. Development, 132, 2521-2533. https://doi.org/10.1242/dev.01837
Kanda, H., Shimamura, R., Koizumi-Kitajima, M., & Okano, H. (2019). Degradation of extracellular matrix by matrix metalloproteinase 2 is essential for the establishment of the blood-brain barrier in Drosophila. iScience, 16, 218-229. https://doi.org/10.1016/j.isci.2019.05.027
Karamanou, K., Franchi, M., Onisto, M., Passi, A., Vynios, D. H., & Brézillon, S. (2020). Evaluation of lumican effects on morphology of invading breast cancer cells, expression of integrins and downstream signaling. The FEBS Journal, 287, 4862-4880. https://doi.org/10.1111/febs.15289
Kinoshita, S., Takarada, K., Kinoshita, Y., & Inoue, Y. H. (2022). Drosophila hemocytes recognize lymph gland tumors of mxc mutants and activate the innate immune pathway in a reactive oxygen species-dependent manner. Biology Open, 11, bio059523. https://doi.org/10.1242/bio.059523
Kurihara, M., Komatsu, K., Awane, R., & Inoue, Y. H. (2020). Loss of histone locus bodies in the mature hemocytes of larval lymph gland result in hyperplasia of the tissue in mxc mutants of Drosophila. International Journal of Molecular Sciences, 21, 1586. https://doi.org/10.3390/ijms21051586
Kurihara, M., Takarada, K., & Inoue, Y. H. (2020). Enhancement of leukemia-like phenotypes in Drosophila mxc mutant larvae due to activation of the RAS-MAP kinase cascade possibly via down-regulation of DE-cadherin. Genes to Cells, 25, 757-769. https://doi.org/10.1111/gtc.12811
Kurucz, E., Márkus, R., Zsámboki, J., Folkl-Medzihradszky, K., Darula, Z., Vilmos, P., Udvardy, A., Krausz, I., Lukacsovich, T., Gateff, E., Zettervall, C. J., Hultmark, D., & Andó, I. (2007). Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr Biol, 17, 649-654. https://doi.org/10.1016/j.cub.2007.02.041
LaFever, K. S., Wang, X., Page-McCaw, P., Bhave, G., & Page-McCaw, A. (2017). Both Drosophila matrix metalloproteinases have released and membrane-tethered forms but have different substrates. Scientific Reports, 7, 44560. https://doi.org/10.1038/srep44560
Lee, E. Y. H. P., & Muller, W. J. (2010). Oncogenes and tumor suppressor genes. Cold Spring Harbor Perspectives in Biology, 2, a003236. https://doi.org/10.1101/cshperspect.a003236
Lin, Y. C., Tsai, P. H., Lin, C. Y., Cheng, C. H., Lin, T. H., Lee, K. P. H., Huang, K. Y., Chen, S. H., Hwang, J. J., Kandaswami, C. C., & Lee, M. T. (2013). Impact 6of flavonoids on matrix metalloproteinase secretion and invadopodia formation in highly invasive A431-III cancer cells. PLoS One, 8, e71903. https://doi.org/10.1371/journal.pone.0071903
Longjohn, M. N., Phan, H. D., & Christian, S. L. (2022). Culturing suspension cancer cell lines. Methods in Molecular Biology, 2508, 9-17. https://doi.org/10.1007/978-1-0716-2376-3_2
Lu, W., & Kang, Y. (2019). Epithelial-mesenchymal plasticity in cancer progression and metastasis. Developmental Cell, 49, 361-374. https://doi.org/10.1016/j.devcel.2019.04.010
Melcarne, C., Lemaitre, B., & Kurant, E. (2019). Phagocytosis in Drosophila: From molecules and cellular machinery to physiology. Insect Biochemistry and Molecular Biology, 109, 1-12. https://doi.org/10.1016/j.ibmb.2019.04.002
Mendes, O., Kim, H. T., Lungu, G., & Stoica, G. (2007). MMP2 role in breast cancer brain metastasis development and its regulation by TIMP2 and ERK1/2. Clinical & Experimental Metastasis, 24, 341-351. https://doi.org/10.1007/s10585-007-9071-0
Miles, W. O., Dyson, N. J., & Walker, J. A. (2011). Modeling tumor invasion and metastasis in Drosophila. Disease Models & Mechanisms, 4, 753-761. https://doi.org/10.1242/dmm.006908
Mori, S., Chang, J. T., Andrechek, E. R., Matsumura, N., Baba, T., Yao, G., Kim, J. W., Gatza, M., Murphy, S., & Nevins, J. R. (2009). Anchorage-independent cell growth signature identifies tumors with metastatic potential. Oncogene, 28, 2796-2805. https://doi.org/10.1038/onc.2009.139
Niland, S., Riscanevo, A. X., & Eble, J. A. (2021). Matrix metalloproteinases shape the tumor microenvironment in cancer progression. International Journal of Molecular Sciences, 23, 146. https://doi.org/10.3390/ijms23010146
Oka, S., Hirai, J., Yasukawa, T., Nakahara, Y., & Inoue, Y. H. (2015). A correlation of reactive oxygen species accumulation by depletion of superoxide dismutases with age-dependent impairment in the nervous system and muscles of Drosophila adults. Biogerontology, 16, 485-501. https://doi.org/10.1007/s10522-015-9570-3
Pagliarini, R. A., & Xu, T. (2003). A genetic screen in Drosophila for metastatic behavior. Science, 302, 1227-1231. https://doi.org/10.1126/science.1088474
Paluch, E. K., Aspalter, I. M., & Sixt, M. (2016). Focal adhesion-independent cell migration. Annual Review of Cell and Developmental Biology, 32, 469-490. https://doi.org/10.1146/annurev-cellbio-111315-125341
Parsons, B., & Foley, E. (2013). The Drosophila platelet-derived growth factor and vascular endothelial growth factor-receptor related (Pvr) protein ligands Pvf2 and Pvf3 control hemocyte viability and invasive migration. The Journal of Biological Chemistry, 288, 20173-20183. https://doi.org/10.1074/jbc.M113.483818
Parvy, J. P., Yu, Y., Dostalova, A., Kondo, S., Kurjan, A., Bulet, P., Lemaître, B., Vidal, M., & Cordero, J. B. (2019). The antimicrobial peptide defensin cooperates with tumour necrosis factor to drive tumour cell death in Drosophila. eLife, 8, e45061. https://doi.org/10.7554/eLife.45061
Petrie, R. J., & Yamada, K. M. (2012). At the leading edge of three-dimensional cell migration. Journal of Cell Science, 125, 5917-5926. https://doi.org/10.1242/jcs.093732
Remillieux-Leschelle, N., Santamaria, P., & Randsholt, N. B. (2002). Regulation of larval hematopoiesis in Drosophila melanogaster: A role for the multi sex combs gene. Genetics, 162, 1259-1274. https://doi.org/10.1093/genetics/162.3.1259
Santamaría, P., & Randsholt, N. B. (1995). Characterization of a region of the X chromosome of Drosophila including multi sex combs (mxc), a Polycomb group gene which also functions as a tumour suppressor. Molecular & General Genetics, 246, 282-290. https://doi.org/10.1007/BF00288600
Shrestha, R., & Gateff, E. (1982). Ultrastructure and cytochemistry of the cell types in the larval hematopoietic organs and hemolymph of Drosophila melanogaster. Development, Growth & Differentiation, 24, 65-82. https://doi.org/10.1111/j.1440-169X.1982.00065.x
Si-Tu, J., Cai, Y., Feng, T., Yang, D., Yuan, S., Yang, X., He, S., Li, Z., Wang, Y., Tang, Y., Ye, C., & Li, Z. (2019). Upregulated circular RNA circ-102004 that promotes cell proliferation in prostate cancer. International Journal of Biological Macromolecules, 122, 1235-1243. https://doi.org/10.1016/j.ijbiomac.2018.09.076
Sopko, R., Foos, M., Vinayagam, A., Zhai, B., Binari, R., Hu, Y., Randklev, S., Perkins, L. A., Gygi, S. P., & Perrimon, N. (2014). Combining genetic perturbations and proteomics to examine kinase-phosphatase networks in Drosophila embryos. Developmental Cell, 31(1), 114-127.
Srivastava, A., Pastor-Pareja, J. C., Igaki, T., Pagliarini, R., & Xu, T. (2007). Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proceedings of the National Academy of Sciences of the United States of America, 104, 2721-2726. https://doi.org/10.1073/pnas.0611666104
Stefanidakis, M., Karjalainen, K., Jaalouk, D. E., Gahmberg, C. G., O'Brien, S., Pasqualini, R., Arap, W., & Koivunen, E. (2009). Role of leukemia cell invadosome in extramedullary infiltration. Blood, 114, 3008-3017. https://doi.org/10.1182/blood-2008-04-148643
Uhlirova, M., & Bohmann, D. (2006). JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. The EMBO Journal, 25, 5294-5304. https://doi.org/10.1038/sj.emboj.7601401
Vicente-Manzanares, M., Ma, X., Adelstein, R. S., & Horwitz, A. R. (2009). Non-muscle myosin II takes centre stage in cell adhesion and migration. Nature Reviews. Molecular Cell Biology, 10, 778-790. https://doi.org/10.1038/nrm2786
Voutouri, C., Kirkpatrick, N. D., Chung, E., Mpekris, F., Baish, J. W., Munn, L. L., Fukumura, D., Stylianopoulos, T., & Jain, R. K. (2019). Experimental and computational analyses reveal dynamics of tumor vessel cooption and optimal treatment strategies. Proceedings of the National Academy of Sciences of the United States of America, 116, 2662-2671. https://doi.org/10.1073/pnas.1818322116
Whiteley, A. E., Price, T. T., Cantelli, G., & Sipkins, D. A. (2021). Leukaemia: a model metastatic disease. Nature Reviews. Cancer, 21, 461-475. https://doi.org/10.1038/s41568-021-00355-z
Winkler, J., Abisoye-Ogunniyan, A., Metcalf, K. J., & Werb, Z. (2020). Concepts of extracellular matrix remodelling in tumour progression and metastasis. Nature Communications, 11, 5120. https://doi.org/10.1038/s41467-020-18794-x
Yang, S. A., Portilla, J. M., Mihailovic, S., Huang, Y. C., & Deng, W. M. (2019). Oncogenic notch triggers neoplastic tumorigenesis in a transition-zone-like tissue microenvironment. Developmental Cell, 49, 461-472. https://doi.org/10.1016/j.devcel.2019.03.015
Yasothornsrikul, S., Davis, W. J., Cramer, G., Kimbrell, D. A., & Dearolf, C. R. (1997). Viking: Identification and characterization of a second type IV collagen in Drosophila. Gene, 198, 17-25. https://doi.org/10.1016/s0378-1119(97)00274-6
Zhu, S., Chen, R., Soba, P., & Jan, Y. N. (2019). JNK signaling coordinates with ecdysone signaling to promote pruning of Drosophila sensory neuron dendrites. Development, 146, dev163592. https://doi.org/10.1242/dev.163592