Entamoeba histolytica and Entamoeba dispar: Morphological and Behavioral Differences Induced by Fibronectin through GTPases Activation and Actin-Binding Proteins.
Actin cytoskeleton
adhesion
displacement
invasive capacity
migration
movement
small GTPases
Journal
The Journal of eukaryotic microbiology
ISSN: 1550-7408
Titre abrégé: J Eukaryot Microbiol
Pays: United States
ID NLM: 9306405
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
16
12
2019
revised:
19
02
2020
accepted:
26
03
2020
pubmed:
18
4
2020
medline:
22
6
2021
entrez:
18
4
2020
Statut:
ppublish
Résumé
Early steps of tissue invasion by Entamoeba histolytica are mediated by adhesion and migration through matrix components such as fibronectin with the participation of the actin cytoskeleton. Striking differences in their produced structures, movement, and migration were found. These observations suggest differential changes in their ability to organize the actin cytoskeleton and, therefore, to modify its morphology after adhesion to fibronectin. To understand these observations, we explore deeper the cytoskeleton pathway of E. histolytica compared to Entamoeba dispar, analyzing the activation and involvement of actin cytoskeleton regulatory proteins such as small GTPases (Rho, Rac1 and Cdc42), myosin IB, paxillin, alpha-actinin, and ARP2/3 during interaction with fibronectin. Results showed a higher activation of Rac1 in E. histolytica compared to E. dispar, while Cdc42 and RhoA were equally activated in both amebae; besides, variations in the amount of myosin IB, paxillin, and ARP2/3 were detected among these species, coinciding and reflected in formation of lamellipodia in E. histolytica and filopodia in E. dispar. These could partially explain the higher invasive capacity of E. histolytica compared to E. dispar, due to its pleomorphic ability, high motility, migration, activation, and abundance of proteins involved in the cytoskeleton arrangement.
Substances chimiques
Fibronectins
0
Microfilament Proteins
0
Protozoan Proteins
0
GTP Phosphohydrolases
EC 3.6.1.-
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
491-504Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2020 International Society of Protistologists.
Références
Addis, M. F., Rappelli, P., Delogu, G., Carta, F., Cappuccinelli, P. & Fiori, P. L. 1998. Cloning and molecular characterization of a cDNA clone coding for Trichomonas vaginalis alpha-actinin and intracellular localization of the protein. Infect. Immun., 66:4924-4931.
Aguilar-Rojas, A., Olivo-Marin, J. C. & Guillen, N. 2016. The motility of Entamoeba histolytica: finding ways to understand intestinal amoebiasis. Curr. Opin. Microbiol., 34:24-30. https://doi.org/10.1016/j.mib.2016.07.016
Ali, I. K., Mondal, U., Roy, S., Haque, R., Petri Jr, W. A. & Clark, C. G. 2007. Evidence for a link between parasite genotype and outcome of infection with Entamoeba histolytica. J. Clin. Microbiol., 45:285-289. https://doi.org/10.1128/JCM.01335-06
Ali, I. K., Solaymani-Mohammadi, S., Akhter, J., Roy, S., Gorrini, C., Calderaro, A., Parker, S. K., Haque, R., Petri Jr, W. A. & Clark, C. G. 2008. Tissue invasion by Entamoeba histolytica: evidence of genetic selection and/or DNA reorganization events in organ tropism. PLoS Negl. Trop Dis., 2:e219. https://doi.org/10.1371/journal.pntd.0000219
Bosch, D. E. & Siderovski, D. P. 2015. Entamoeba histolytica RacC selectively engages p21-activated kinase effectors. Biochemistry, 54:404-412. https://doi.org/10.1021/bi501226f
Brakebusch, C. & Fässler, R. 2003. The integrin-actin connection, an eternal love affair. EMBO J., 22:2324-2333.
Campellone, K. G. & Welch, M. D. 2010. A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol., 11:237-251. https://doi.org/10.1038/nrm2867
Campos-Parra, A. D., Hernández-Cuevas, N. A., Hernandez-Rivas, R. & Vargas, M. 2010. EhNCABP166: a nucleocytoplasmic actin-binding protein from Entamoeba histolytica. Mol. Biochem. Parasitol., 172:19-30. https://doi.org/10.1016/j.molbiopara.2010.03.010
de la Cruz, O. H., Muñiz-Lino, M., Guillén, N., Weber, C., Marchat, L. A., López-Rosas, I., Ruíz-García, E., Astudillo-de la Vega, H., Fuentes-Mera, L., Álvarez-Sánchez, E., Mendoza-Hernández, G. & López-Camarillo, C. 2014. Proteomic profiling reveals that EhPC4 transcription factor induces cell migration through up-regulation of the 16-kDa actin-binding protein EhABP16 in Entamoeba histolytica. J. Proteomics., 111:46-58. https://doi.org/10.1016/j.jprot.2014.03.041
De Jong, K. L., MacLeod, H. C., Norton, P. R. & Petersen, N. O. 2006. Fibronectin organization under and near cells. Eur. Biophys. J., 35:695-708. https://doi.org/10.1007/s00249-006-0081-7
Diamond, L. S., Clark, C. G. & Cunnick, C. C. 1995. YI-S, a casein-free medium for axenic cultivation of Entamoeba histolytica, related Entamoeba, Giardia intestinalis and Trichomonas vaginalis. J. Eukaryot. Microbiol., 42:277-278.
Diamond, L. S., Harlow, D. R. & Cunnick, C. C. 1978. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg., 72:431-432.
Dufour, A. C., Olivo-Marin, J. C. & Guillen, N. 2015. Amoeboid movement in protozoan pathogens. Semin. Cell Dev. Biol., 46:128-134. https://doi.org/10.1016/j.semcdb.2015.10.010
Eitaki, M., Yamamori, T., Meike, S., Yasui, H. & Inanami, O. 2012. Vincristine enhances amoeboid-like motility via GEF-H1/RhoA/ROCK/Myosin light chain signaling in MKN45 cells. BMC Cancer, 469:1-12. https://doi.org/10.1186/1471-2407-12-469
Espinosa-Cantellano, M., Castañón-Gutiérrez, G. & Martínez-Palomo, A. 1997. In vivo pathogenesis of Entamoeba dispar. Arch. Med. Res., 28:204-206.
Feick, P., Haas, S. R., Singer, M. V. & Böcker, U. 2006. Low-dose exposure of intestinal epithelial cells to formaldehyde results in MAP kinase activation and molecular alteration of the focal adhesion protein paxillin. Toxicology, 219:60-72. https://doi.org/10.1016/j.tox.2005.11.004
Fife, C. M., McCarroll, J. A. & Kavallaris, M. 2014. Movers and shakers: cell cytoskeleton in cancer metastasis. Br. J. Pharmacol., 171:5507-5523. https://doi.org/10.1111/bph.12704
Flores-Robles, D., Rosales, C., Rosales-Encina, J. L. & Talamás-Rohana, P. 2003. Entamoeba histolytica: a beta 1 integrin-like fibronectin receptor assembles a signaling complex similar to those of mammalian cells. Exp. Parasitol., 103:8-15.
Giannone, G., Dubin-Thaler, B. J., Rossier, O., Cai, Y., Chaga, O., Jiang, G., Beaver, W., Döbereiner, H. G., Freund, Y., Borisy, G. & Sheetz, M. P. 2007. Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell, 128:561-575. https://doi.org/10.1016/j.cell.2006.12.039
Goley, E. D. & Welch, M. D. 2006. The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol., 7:713-726. https://doi.org/10.1038/nrm2026
Haga, R. B. & Ridley, A. J. 2016. Rho GTPases: regulation and roles in cancer cell biology. Small GTPases, 7:207-221. https://doi.org/10.1080/21541248.2016.1232583
Hall, A. 2012. Rho family GTPases. Biochem. Soc. Trans., 40:1378-1382. https://doi.org/10.1042/BST20120103
Hasan, M. M., Teixeira, J. E. & Huston, C. D. 2018. Invadosome-mediated human extracellular matrix degradation by Entamoeba histolytica. Infect. Immun., pii:e00287-18. https://doi.org/10.1128/IAI.00287-18
Herrera-Martínez, M., Hernández-Ramírez, V. I., Lagunes-Guillén, A. E., Chávez-Munguía, B. & Talamás-Rohana, P. 2013. Actin, RhoA, and Rab11 participation during encystment in Entamoeba invadens. Biomed. Res. Int., https://doi.org/10.1155/2013/919345
Innocenti, M. 2018. New insights into the formation and the function of lamellipodia and ruffles in mesenchymal cell migration. Cell Adh. Migr., 12:401-416. https://doi.org/10.1080/19336918.2018.1448352
Kato, K., Makiuchi, T., Cheng, X. & Tachibana, H. 2017. Comparison of hemolytic activity of the intermediate subunit of Entamoeba histolytica and Entamoeba dispar lectins. PLoS ONE, 12:e0181864. https://doi.org/10.1371/journal.pone.0181864
Kim, M. C., Whisler, J., Silberberg, Y. R., Kamm, R. D. & Asada, H. H. 2015. Cell invasion dynamics into a three dimensional extracellular matrix fibre network. PLoS Comput. Biol., 11:e1004535. https://doi.org/10.1371/journal.pcbi.1004535
Kirchner, J., Kam, Z., Tzur, G., Bershadsky, A. D. & Geiger, B. 2003. Live-cell monitoring of tyrosine phosphorylation in focal adhesions following microtubule disruption. J. Cell Sci., 116:975-986.
Leroy, A., Mareel, M., De Bruyne, G., Bailey, G. & Nelis, H. 1994-1995. Metastasis of Entamoeba histolytica compared to colon cancer: one more step in invasion. Invasion Metastasis, 14:177-191.
Machacek, M., Hodgson, L., Welch, C., Elliott, H., Pertz, O., Nalbant, P., Abell, A., Johnson, G. L., Hahn, K. M. & Danuser, G. 2009. Coordination of Rho GTPase activities during cell protrusion. Nature, 461:99-103. https://doi.org/10.1038/nature08242
Manich, M., Hernandez-Cuevas, N., Ospina-Villa, J. D., Syan, S., Marchat, L. A., Olivo-Marin, J. C. & Guillén, N. 2018. Morphodynamics of the actin-rich cytoskeleton in Entamoeba histolytica. Front Cell. Infect. Microbiol., 8:179. https://doi.org/10.3389/fcimb.2018.00179
Marion, S., Wilhelm, C., Voigt, H., Bacri, J. C. & Guillén, N. 2004. Overexpression of myosin IB in living Entamoeba histolytica enhances cytoplasm viscosity and reduces phagocytosis. J. Cell Sci., 117:3271-3279. https://doi.org/10.1242/jcs.01178
Meza, I. 2000. Extracellular matrix-induced signaling in Entamoeba histolytica: its role in invasiveness. Parasitol. Today, 16:23-28. https://doi.org/10.1016/s0169-4758(99)01586-0
Meza, I., Talamás-Rohana, P. & Vargas, M. A. 2006. The cytoskeleton of Entamoeba histolytica: structure, function, and regulation by signaling pathways. Arch. Med. Res., 37:234-243. https://doi.org/10.1016/j.arcmed.2005.09.008
Mullins, R. D., Heuser, J. A. & Pollard, T. D. 1998. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl Acad. Sci. USA, 95:6181-6186. https://doi.org/10.1073/pnas.95.11.6181
Münter, S., Way, M. & Frischknecht, F. 2006. Signaling during pathogen infection. Sci STKE., 335:1-14. https://doi.org/10.1126/stke.3352006re5
Orozco, E., Benitez-Bibriesca, L. & Hernandez, R. 1994. Invasion and metastasis mechanisms in Entamoeba histolytica and cancer cells. Some common cellular and molecular features. Mutat. Res., 305:229-239. https://doi.org/10.1016/0027-5107(94)90243-7
Otey, C. A. & Carpen, O. 2004. Alpha-actinin revisited: a fresh look at an old player. Cell Motil. Cytoskeleton, 58:104-111. https://doi.org/10.1002/cm.20007
Pollard, T. D. 2016. Actin and actin-binding proteins. Cold Spring Harb. Perspect. Biol., pii: a018226. https://doi.org/10.1101/cshperspect.a018226
Ríos, A., Hernández-Ramírez, V. I., Moguel, M., Zárate Bahena, A. I., Rosales-Encina, J. L., Vargas, M. A. & Talamás-Rohana, P. 2008. Participation of Rho, ROCK-2, and GAP activities during actin microfilament rearrangements in Entamoeba histolytica induced by fibronectin signaling. Cell Biol. Int., 32:984-1000. https://doi.org/10.1016/j.cellbi.2008.04.016
Rottner, K., Hänisch, J. & Campellone, K. G. 2010. WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends Cell Biol., 20:650-661. https://doi.org/10.1016/j.tcb.2010.08.014
Rotty, J. D., Wu, C. & Bear, J. E. 2013. New insights into the regulation and cellular functions of the ARP2/3 complex. Nat. Rev. Mol. Cell Biol., 14:7-12. https://doi.org/10.1038/nrm3492
Ruoslahti, E., Hayman, E. G., Pierschbacher, M. & Engvall, E. 1982. Fibronectin: purification, immunochemical properties, and biological activities. Methods Enzymol., 82:803-831. https://doi.org/10.1016/0076-6879(82)82103-4
Schulte, W. & Scholze, H. 1989. Action of the major protease from Entamoeba histolytica on proteins of the extracellular matrix. J. Protozool., 36:538-543. https://doi.org/10.1111/j.1550-7408.1989.tb01092.x
Sengupta, K., Hernández-Ramírez, V. I., Rosales-Encina, J. L., Mondragón, R., Garibay-Cerdenares, O. L., Flores-Robles, D., Javier-Reyna, R., Pertuz, S. & Talamás-Rohana, P. 2009. Physical, structural, and functional properties of the beta1 integrin-like fibronectin receptor (beta1EhFNR) in Entamoeba histolytica. Infect. Genet. Evol., 9:962-970. https://doi.org/10.1016/j.meegid.2009.06.020
Sierra-López, F., Baylón-Pacheco, L., Espíritu-Gordillo, P., Lagunes-Guillén, A., Chávez-Munguía, B. & Rosales-Encina, J. L. 2018. Influence of micropatterned grill lines on Entamoeba histolytica trophozoites morphology and migration. Front Cell. Infect. Microbiol., 8:295. https://doi.org/10.3389/fcimb.2018.00295
Talamás-Lara, D., Chávez-Munguía, B., González-Robles, A., Talamás-Rohana, P., Salazar-Villatoro, L., Durán-Díaz, Á. & Martínez-Palomo, A. 2014. Erythrophagocytosis in Entamoeba histolytica and Entamoeba dispar: a comparative study. Biomed. Res. Int., https://doi.org/10.1155/2014/626259
Talamás-Lara, D., Talamás-Rohana, P., Fragoso-Soriano, R. J., Espinosa-Cantellano, M., Chávez-Munguía, B., González-Robles, A. & Martínez-Palomo, A. 2015. Cell-matrix interactions of Entamoeba histolytica and E. dispar. A comparative study by electron-, atomic force- and confocal microscopy. Exp. Cell Res., 337:226-233. https://doi.org/10.1016/j.yexcr.2015.07.030
Talamás-Rohana, P. & Meza, I. 1988. Interaction between pathogenic amebas and fibronectin: substrate degradation and changes in cytoskeleton organization. J. Cell Biol., 106:1787-1794. https://doi.org/10.1083/jcb.106.5.1787
Talamás-Rohana, P. & Ríos, A. 2000. Actin stress fibers in Entamoeba histolytica induced by fibronectin. Arch. Med. Res., 31:S131-S133. https://doi.org/10.1016/s0188-4409(00)00190-9
Ti, S. C., Jurgenson, C. T., Nolen, B. J. & Pollard, T. D. 2011. Structural and biochemical characterization of two binding sites for nucleation-promoting factor WASp-VCA on Arp2/3 complex. Proc. Natl Acad. Sci. USA, 108:E463-E471. https://doi.org/10.1073/pnas.1100125108
Tsuruta, D. & Jones, J. C. 2003. The vimentin cytoskeleton regulates focal contact size and adhesion of endothelial cells subjected to shear stress. J. Cell Sci., 116:4977-4984. https://doi.org/10.1242/jcs.00823
Vázquez, J., Franco, E., Reyes, G. & Meza, I. 1995. Characterization of adhesion plates induced by interaction of Entamoeba histolytica trophozoites with fibronectin. Cell Motil. Cytoskeleton, 32:37-45.
Voigt, H. & Guillén, N. 1999. New insights into the role of the cytoskeleton in phagocytosis of Entamoeba histolytica. Cell. Microbiol., 1:195-203. https://doi.org/10.1046/j.1462-5822.1999.00021.x
Warner, H., Wilson, B. J. & Caswell, P. T. 2019. Control of adhesion and protrusion in cell migration by Rho GTPases. Curr. Opin. Cell Biol., 56:64-70. https://doi.org/10.1016/j.ceb.2018.09.003
Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M. & Barton, G. J. 2009. Jalview Version 2- a multiple sequence alignment editor and analysis workbench. Bioinformatics, 25:1189-1191. https://doi.org/10.1093/bioinformatics/btp033
Wilson, I. W., Weedall, G. D. & Hall, N. 2012. Host-parasite interactions in Entamoeba histolytica and Entamoeba dispar: what have we learned from their genomes? Parasite Immunol., 34:90-99. https://doi.org/10.1111/j.1365-3024.2011.01325.x
Zimerman, B., Volberg, T. & Geiger, B. 2004. Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil. Cytoskeleton, 58:143-159. https://doi.org/10.1002/cm.20005