Abstract
Entamoeba histolytica, the etiological agent of amebiasis interacts with and feeds on the gut microbiota. Several studies have emphasized the close relationship between E. histolytica and the bacteria and its impact on the parasite’s pathogenesis. In this work we present an integrated omics analysis of the effect of E. coli and other bacteria on the resistance of E. histolytica to oxidative stress.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- GAPDH:
-
Glyceraldehyde-3-phosphate dehydrogenase putative
- HKB:
-
Heat killed bacteria
- HKBOS:
-
Heat killed bacteria exposed to oxidative stress
- LB:
-
Live bacteria
- LRR:
-
Leucine rich repeat proteins
- MDH:
-
Malate dehydrogenase
- OS:
-
Oxidative stress
- OX:
-
Oxidized proteins
- OX-RAC:
-
Resin assisted capture of oxidized proteins
- NS:
-
Nitrosative stress
References
Bansal, D., Sehgal, R., Chawla, Y., Mahajan, R. C., & Malla, N. (2004). In vitro activity of antiamoebic drugs against clinical isolates of Entamoeba histolytica and Entamoeba dispar. Annals of Clinical Microbiology and Antimicrobials, 3, 27. https://doi.org/10.1186/1476-0711-3-27.
Bhattacharya, A., Ghildyal, R., Prasad, J., Bhattacharya, S., & Diamond, L. S. (1992). Modulation of a surface antigen of Entamoeba histolytica in response to bacteria. Infection and Immunity, 60(4), 1711–1713.
Bracha, R., Kobiler, D., & Mirelman, D. (1982). Attachment and ingestion of bacteria by trophozoites of Entamoeba histolytica. Infection and Immunity, 36(1), 396–406.
Bracha, R., & Mirelman, D. (1984). Virulence of Entamoeba histolytica trophozoites. Effects of bacteria, microaerobic conditions, and metronidazole. Journal of Experimental Medicine, 160(2), 353–368.
Ehrenkaufer, G. M., Haque, R., Hackney, J. A., Eichinger, D. J., & Singh, U. (2007). Identification of developmentally regulated genes in Entamoeba histolytica: Insights into mechanisms of stage conversion in a protozoan parasite. Cellular Microbiology, 9(6), 1426–1444. https://doi.org/10.1111/j.1462-5822.2006.00882.x.
Gilchrist, C. A., Petri, S. E., Schneider, B. N., Reichman, D. J., Jiang, N., Begum, S., … Petri, W. A., Jr. (2016). Role of the gut microbiota of children in diarrhea due to the protozoan parasite Entamoeba histolytica. The Journal of Infectious Diseases, 213(10), 1579–1585. https://doi.org/10.1093/infdis/jiv772 (jiv772 [pii]).
Hernandez Ceruelos, A., Romero-Quezada, L. C., Ruvalcaba Ledezma, J. C., & Lopez Contreras, L. (2019). Therapeutic uses of metronidazole and its side effects: An update. European Review for Medical and Pharmacological Sciences, 23(1), 397–401. https://doi.org/10.26355/eurrev_201901_16788.
Hertzberger, R., Arents, J., Dekker, H. L., Pridmore, R. D., Gysler, C., Kleerebezem, M., et al. (2014). H(2)O(2) production in species of the Lactobacillus acidophilus group: A central role for a novel NADH-dependent flavin reductase. Applied and Environment Microbiology, 80(7), 2229–2239. https://doi.org/10.1128/AEM.04272-13.
Hinshaw, D. B., Miller, M. T., Omann, G. M., Beals, T. F., & Hyslop, P. A. (1993). A cellular model of oxidant-mediated neuronal injury. Brain Research, 615(1), 13–26. https://doi.org/10.1016/0006-8993(93)91110-e.
Iyer, L. R., Verma, A. K., Paul, J., & Bhattacharya, A. (2019). Phagocytosis of gut bacteria by Entamoeba histolytica. Frontiers in Cellular and Infection Microbiology, 9, 34. https://doi.org/10.3389/fcimb.2019.00034.
Jeelani, G., & Nozaki, T. (2016). Entamoeba thiol-based redox metabolism: A potential target for drug development. Molecular and Biochemical Parasitology, 206(1–2), 39–45. https://doi.org/10.1016/j.molbiopara.2016.01.004.
Jung, T., Hohn, A., & Grune, T. (2014). The proteasome and the degradation of oxidized proteins: Part II—Protein oxidation and proteasomal degradation. Redox Biology, 2, 99–104. https://doi.org/10.1016/j.redox.2013.12.008.
Kim, J. G., Park, S. J., Sinninghe Damste, J. S., Schouten, S., Rijpstra, W. I., Jung, M. Y., et al. (2016). Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proceedings of the National Academy of Sciences of the United States of America, 113(28), 7888–7893. https://doi.org/10.1073/pnas.1605501113.
Lofmark, S., Edlund, C., & Nord, C. E. (2010). Metronidazole is still the drug of choice for treatment of anaerobic infections. Clinical Infectious Diseases, 50(Suppl 1), S16–S23. https://doi.org/10.1086/647939.
Lu, J., & Holmgren, A. (2014). The thioredoxin antioxidant system. Free Radical Biology and Medicine, 66, 75–87. https://doi.org/10.1016/j.freeradbiomed.2013.07.036.
Marie, C., & Petri, W. A., Jr. (2014). Regulation of virulence of Entamoeba histolytica. Annual Review of Microbiology, 68, 493–520. https://doi.org/10.1146/annurev-micro-091313-103550.
Mendoza-Macias, C. L., Barrios-Ceballos, M. P., de la Pena, L. P., Rangel-Serrano, A., Anaya-Velazquez, F., Mirelman, D., et al. (2009). Entamoeba histolytica: Effect on virulence, growth and gene expression in response to monoxenic culture with Escherichia coli 055. Experimental Parasitology, 121(2), 167–174. https://doi.org/10.1016/j.exppara.2008.10.011.
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. https://doi.org/10.3389/fcimb.2018.00019.
Nirujogi, R. S., Muthusamy, B., Kim, M. S., Sathe, G. J., Lakshmi, P. T., Kovbasnjuk, O. N., … Jabbour, R. E. (2017). Secretome analysis of diarrhea-inducing strains of Escherichia coli. Proteomics, 17(6). https://doi.org/10.1002/pmic.201600299.
Paniagua, G. L., Monroy, E., Garcia-Gonzalez, O., Alonso, J., Negrete, E., & Vaca, S. (2007). Two or more enteropathogens are associated with diarrhoea in Mexican children. Annals of Clinical Microbiology and Antimicrobials, 6, 17. https://doi.org/10.1186/1476-0711-6-17.
Santi-Rocca, J., Smith, S., Weber, C., Pineda, E., Hon, C. C., Saavedra, E., et al. (2012). Endoplasmic reticulum stress-sensing mechanism is activated in Entamoeba histolytica upon treatment with nitric oxide. PLoS ONE, 7(2), e31777. https://doi.org/10.1371/journal.pone.0031777.
Sawa, A., Khan, A. A., Hester, L. D., & Snyder, S. H. (1997). Glyceraldehyde-3-phosphate dehydrogenase: Nuclear translocation participates in neuronal and nonneuronal cell death. Proceedings of the National Academy of Sciences of the United States of America, 94(21), 11669–11674. https://doi.org/10.1073/pnas.94.21.11669.
Scher, J. U., Sczesnak, A., Longman, R. S., Segata, N., Ubeda, C., Bielski, C., … Littman, D. R. (2013). Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife, 2, e01202. https://doi.org/10.7554/eLife.01202.
Schweighoffer, E., Nys, J., Vanes, L., Smithers, N., & Tybulewicz, V. L. J. (2017). TLR4 signals in B lymphocytes are transduced via the B cell antigen receptor and SYK. Journal of Experimental Medicine, 214(5), 1269–1280. https://doi.org/10.1084/jem.20161117.
Shahi, P., Trebicz-Geffen, M., Nagaraja, S., Alterzon-Baumel, S., Hertz, R., Methling, K., … Ankri, S. (2016). Proteomic identification of oxidized proteins in Entamoeba histolytica by resin-assisted capture: Insights into the role of arginase in resistance to oxidative stress. PLoS Neglected Tropical Diseases, 10(1), e0004340. https://doi.org/10.1371/journal.pntd.0004340.
Sharma, A. (2010). Virulence mechanisms of Tannerella forsythia. Periodontology 2000, 54, 106–116.
Sharma, A., Sojar, H. T., Glurich, I., Honma, K., Kuramitsu, H. K., & Genco, R. J. (1998). Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037. Infection and immunity, 66, 5703–5710.
Shaulov, Y., Shimokawa, C., Trebicz-Geffen, M., Nagaraja, S., Methling, K., Lalk, M., … Ankri, S. (2018). Escherichia coli mediated resistance of Entamoeba histolytica to oxidative stress is triggered by oxaloacetate. PLoS Pathogens, 14(10), e1007295. https://doi.org/10.1371/journal.ppat.1007295.
Shenton, D., Smirnova, J. B., Selley, J. N., Carroll, K., Hubbard, S. J., Pavitt, G. D., … Grant, C. M. (2006). Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. Journal of Biological Chemistry, 281(39), 29011–29021. https://doi.org/10.1074/jbc.M601545200.
Silvestre, A., Plaze, A., Berthon, P., Thibeaux, R., Guillen, N., & Labruyere, E. (2015). In Entamoeba histolytica, a BspA family protein is required for chemotaxis toward tumour necrosis factor. Microbial Cell, 2(7), 235–246. https://doi.org/10.15698/mic2015.07.214.
Stanley, S. L., Jr., and Reed, S. L. (2001). Microbes and microbial toxins: Paradigms for microbial-mucosal interactions. VI. Entamoeba histolytica: Parasite-host interactions. The American Journal of Physiology: Gastrointestinal and Liver Physiology, 280(6), G1049–G1054. https://doi.org/10.1152/ajpgi.2001.280.6.g1049.
Thomas, P. D., Campbell, M. J., Kejariwal, A., Mi, H., Karlak, B., Daverman, R., et al. (2003). PANTHER: A library of protein families and subfamilies indexed by function. Genome Research, 13(9), 2129–2141. https://doi.org/10.1101/gr.772403.
Turkeltaub, J. A., McCarty, T. R., & Hotez, P. J. (2015). The intestinal protozoa: Emerging impact on global health and development. Current Opinion in Gastroenterology, 31(1), 38–44. https://doi.org/10.1097/MOG.0000000000000135.
Valen, G., Sonden, A., Vaage, J., Malm, E., & Kjellstrom, B. T. (1999). Hydrogen peroxide induces endothelial cell atypia and cytoskeleton depolymerization. Free Radical Biology and Medicine, 26(11–12), 1480–1488. https://doi.org/10.1016/s0891-5849(99)00009-x.
Varet, H., Shaulov, Y., Sismeiro, O., Trebicz-Geffen, M., Legendre, R., Coppee, J. Y., et al. (2018). Enteric bacteria boost defences against oxidative stress in Entamoeba histolytica. Scientific Reports, 8(1), 9042. https://doi.org/10.1038/s41598-018-27086-w.
Vaure, C., & Liu, Y. (2014). A comparative review of toll-like receptor 4 expression and functionality in different animal species. Frontiers in immunology, 5, 316.
Verma, A. K., Verma, R., Ahuja, V., and Paul, J. (2012). Real-time analysis of gut flora in Entamoeba histolytica infected patients of Northern India. BMC Microbiology, 12, 183. https://doi.org/10.1186/1471-2180-12-183 (-2180-12-183 [pii]).
Wittner, M., and Rosenbaum, R. M. (1970). Role of bacteria in modifying virulence of Entamoeba histolytica. Studies of amebae from axenic cultures. The American Journal of Tropical Medicine and Hygiene, 19(5), 755–761. https://doi.org/10.4269/ajtmh.1970.19.755.
Yanai, T., & Okamoto, J. (1952). Relationship between the number of Escherichia coli in stools and the infectivity of rats to Entamoeba histolytica in the experimental infection of the amoebae. Kitasato Archives of Experimental Medicine, 25(1), 67–68.
Acknowledgements and Funding
We would like to acknowledge the assistance of Ms. Shruti Nagaraja in the preparation of Fig. 3.1.
This study was supported by grants from the Israel Science Foundation (260/16), the US-Israel Binational Science Foundation (2015211), the Niedersachsen-Israel ZN3454 program and the European ERA-NET Infect-ERA program AMOEBAC (Israel Ministry of Health Grant 031L000).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this paper
Cite this paper
Shaulov, Y., Ankri, S. (2020). Integrative Omics Analysis of the Effect of Bacteria on the Resistance of Entamoeba histolytica to Oxidative Stress. In: Guillen, N. (eds) Eukaryome Impact on Human Intestine Homeostasis and Mucosal Immunology. Springer, Cham. https://doi.org/10.1007/978-3-030-44826-4_3
Download citation
DOI: https://doi.org/10.1007/978-3-030-44826-4_3
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-44825-7
Online ISBN: 978-3-030-44826-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)