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Heat Shock Proteins in Parasitic Flatworms

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Heat Shock Proteins in Veterinary Medicine and Sciences

Part of the book series: Heat Shock Proteins ((HESP,volume 12))

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Abstract

During the entire life cycle, parasitic flatworms experience great changes in growth environment in aspects of temperature, nutrient, pH, and immune responses. They have evolved to have multiple mechanisms to survive these stresses, and one is to orchestrate expression of heat shock proteins (HSP), a conserved protein family that plays a crucial role in maintenance of protein homeostasis. These parasites encode a considerable number of hsp genes, some which lack typical domains/motifs or are expressed in a secretory pattern via multiple secretory pathways. Flatworm HSP has been shown to offer protection from stress-induced damages as well as to be immunogenic and immunomodulative, rendering them to play a role in parasite development and modulation of immune responses. Due to the immunogenic and immunomodulative properties, some flatworm HSP have been demonstrated to be promising diagnostic and vaccine candidates. Using nanotechnology, development of effective HSP-targeting antagonists is of high veterinary interest. It will allow us to use these small molecules to pinpoint a role of flatworm HSP during parasitism, which in turn aids us to better control parasite transmission.

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References

  • Batulan, Z., Pulakazhi Venu, V. K., Li, Y., Koumbadinga, G., Alvarez-Olmedo, D. G., Shi, C., & O’Brien, E. R. (2016). Extracellular release and signaling by heat shock protein 27: Role in modifying vascular inflammation. Frontiers in Immunology, 7, 285.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolhassani, A., & Rafati, S. (2008). Heat-shock proteins as powerful weapons in vaccine development. Expert Review of Vaccines, 7, 1185–1199.

    Article  CAS  PubMed  Google Scholar 

  • Buck, A. H., Coakley, G., Simbari, F., McSorley, H. J., Quintana, J. F., Le Bihan, T., Kumar, S., Abreu-Goodger, C., Lear, M., Harcus, Y., et al. (2014). Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity. Nature Communications, 5, 5488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao, X., Fu, Z., Zhang, M., Han, Y., Han, H., Han, Q., Lu, K., Hong, Y., & Lin, J. (2016). iTRAQ-based comparative proteomic analysis of excretory-secretory proteins of schistosomula and adult worms of Schistosoma japonicum. Journal of Proteomics, 138, 30–39.

    Article  CAS  PubMed  Google Scholar 

  • Carra, S., Alberti, S., Arrigo, P. A., Benesch, J. L., Benjamin, I. J., Boelens, W., Bartelt-Kirbach, B., Brundel, B., Buchner, J., Bukau, B., et al. (2017). The growing world of small heat shock proteins: From structure to functions. Cell Stress & Chaperones, 22, 601–611.

    Article  CAS  Google Scholar 

  • Cass, C. L., Johnson, J. R., Califf, L. L., Xu, T., Hernandez, H. J., Stadecker, M. J., Yates, J. R., 3rd, & Williams, D. L. (2007). Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology, 155, 84–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaiyadet, S., Sotillo, J., Smout, M., Cantacessi, C., Jones, M. K., Johnson, M. S., Turnbull, L., Whitchurch, C. B., Potriquet, J., Laohaviroj, M., et al. (2015). Carcinogenic liver Fluke secretes extracellular vesicles that promote Cholangiocytes to adopt a tumorigenic phenotype. Journal of Infectious Diseases, 212, 1636–1645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chebotareva, N., Bobkova, I., & Shilov, E. (2017). Heat shock proteins and kidney disease: Perspectives of HSP therapy. Cell Stress & Chaperones, 22, 319–343.

    Article  CAS  Google Scholar 

  • Cheng, G., Luo, R., Hu, C., Lin, J., Bai, Z., Zhang, B., & Wang, H. (2013). TiO2-based phosphoproteomic analysis of schistosomes: Characterization of phosphorylated proteins in the different stages and sex of Schistosoma japonicum. Journal of Proteome Research, 12, 729–742.

    Article  CAS  PubMed  Google Scholar 

  • Chung, E. J., Jeong, Y. I., Lee, M. R., Kim, Y. J., Lee, S. E., Cho, S. H., Lee, W. J., Park, M. Y., & Ju, J. W. (2017). Heat shock proteins 70 and 90 from Clonorchis sinensis induce Th1 response and stimulate antibody production. Parasites & Vectors, 10, 118.

    Article  Google Scholar 

  • Cloutier, P., & Coulombe, B. (2013). Regulation of molecular chaperones through post-translational modifications: Decrypting the chaperone code. Biochimica et Biophysica Acta, 1829, 443–454.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cwiklinski, K., de la Torre-Escudero, E., Trelis, M., Bernal, D., Dufresne, P. J., Brennan, G. P., O’Neill, S., Tort, J., Paterson, S., Marcilla, A., et al. (2015). The extracellular vesicles of the Helminth Pathogen, Fasciola hepatica: Biogenesis pathways and Cargo molecules involved in Parasite Pathogenesis. Molecular and Cellular Probes, 14, 3258–3273.

    Article  CAS  Google Scholar 

  • Duan, M. M., Xu, R. M., Yuan, C. X., Li, Y. Y., Liu, Q., Cheng, G. F., Lin, J. J., & Feng, X. G. (2015). SjHSP70, a recombinant Schistosoma japonicum heat shock protein 70, is immunostimulatory and induces protective immunity against cercarial challenge in mice. Parasitology Research, 114, 3415–3429.

    Article  PubMed  Google Scholar 

  • Egger, B., Lapraz, F., Tomiczek, B., Muller, S., Dessimoz, C., Girstmair, J., Skunca, N., Rawlinson, K. A., Cameron, C. B., Beli, E., et al. (2015). A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Current Biology, 25, 1347–1353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feder, M. E., & Hofmann, G. E. (1999). Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annual Review of Physical Chemistry, 61, 243–282.

    Article  CAS  Google Scholar 

  • Fromm, B., Worren, M. M., Hahn, C., Hovig, E., & Bachmann, L. (2013). Substantial loss of conserved and gain of novel MicroRNA families in flatworms. Molecular Biology and Evolution, 30, 2619–2628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He, S., Yang, L., Lv, Z., Hu, W., Cao, J., Wei, J., Sun, X., Yang, J., Zheng, H., & Wu, Z. (2010). Molecular and functional characterization of a mortalin-like protein from Schistosoma japonicum (SjMLP/hsp70) as a member of the HSP70 family. Parasitology Research, 107, 955–966.

    Article  PubMed  Google Scholar 

  • Huang, F., Dang, Z., Suzuki, Y., Horiuchi, T., Yagi, K., Kouguchi, H., Irie, T., Kim, K., & Oku, Y. (2016). Analysis on Gene Expression Profile in Oncospheres and Early Stage Metacestodes from Echinococcus multilocularis. PLoS Neglected Tropical Diseases, 10, e0004634.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishida, K., Varrecchia, M., Knudsen, G. M., & Jolly, E. R. (2014). Immunolocalization of anti-hsf1 to the acetabular glands of infectious schistosomes suggests a non-transcriptional function for this transcriptional activator. PLoS Neglected Tropical Diseases, 8, e3051.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jee, H. (2016). Size dependent classification of heat shock proteins: a mini-review. Journal of Exercise Rehabilitation, 12, 255–259.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolinski, T., Marek-Trzonkowska, N., Trzonkowski, P., & Siebert, J. (2016). Heat shock proteins (HSPs) in the homeostasis of regulatory T cells (Tregs). Central European Journal of Immunology, 41, 317–323.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouguchi, H., Matsumoto, J., Katoh, Y., Suzuki, T., Oku, Y., & Yagi, K. (2010). Echinococcus multilocularis: Two-dimensional Western blotting method for the identification and expression analysis of immunogenic proteins in infected dogs. Experimental Parasitology, 124, 238–243.

    Article  CAS  PubMed  Google Scholar 

  • Koziol, U., Iriarte, A., Castillo, E., Soto, J., Bello, G., Cajarville, A., Roche, L., & Marin, M. (2009). Characterization of a putative hsp70 pseudogene transcribed in protoscoleces and adult worms of Echinococcus granulosus. Gene, 443, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Lantner, F., Ziv, E., Ram, D., & Schechter, I. (1998). Different forms of the mRNA encoding the heat-shock transcription factor are expressed during the life cycle of the parasitic helminth Schistosoma mansoni. European Journal of Biochemistry, 253, 390–398.

    Article  CAS  PubMed  Google Scholar 

  • Lardans, V., Ram, D., Lantner, F., Ziv, E., & Schechter, I. (2001). Differences in DNA-sequence recognition between the DNA-binding domain fragment and the full-length molecule of the heat-shock transcription factor of schistosome. Biochimica et Biophysica Acta, 1519, 230–234.

    Article  CAS  PubMed  Google Scholar 

  • Liu, F., Cui, S. J., Hu, W., Feng, Z., Wang, Z. Q., & Han, Z. G. (2009). Excretory/secretory proteome of the adult developmental stage of human blood fluke, Schistosoma japonicum. Molecular & Cellular Proteomics, 8, 1236–1251.

    Article  CAS  Google Scholar 

  • Luo, R., Zhou, C., Lin, J., Yang, D., Shi, Y., & Cheng, G. (2012). Identification of in vivo protein phosphorylation sites in human pathogen Schistosoma japonicum by a phosphoproteomic approach. Journal of Proteomics, 75, 868–877.

    Article  CAS  PubMed  Google Scholar 

  • Mambula, S. S., & Calderwood, S. K. (2006). Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. Journal of Immunology, 177, 7849–7857.

    Article  CAS  Google Scholar 

  • Mambula, S. S., Stevenson, M. A., Ogawa, K., & Calderwood, S. K. (2007). Mechanisms for Hsp70 secretion: Crossing membranes without a leader. Methods, 43, 168–175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez, J., Perez-Serrano, J., Bernadina, W. E., & Rodriguez-Caabeiro, F. (1999). Echinococcus granulosus: In vitro effects of ivermectin and praziquantel on hsp60 and hsp70 levels. Experimental Parasitology, 93, 171–180.

    Article  CAS  PubMed  Google Scholar 

  • Mathieson, W., & Wilson, R. A. (2010). A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: The miracidium, hatch fluid and secretions. International Journal for Parasitology, 40, 617–628.

    Article  CAS  PubMed  Google Scholar 

  • Merckelbach, A., Wager, M., & Lucius, R. (2003). Analysis of cDNAs coding for immunologically dominant antigens from an oncosphere-specific cDNA library of Echinococcus multilocularis. Parasitology Research, 90, 493–501.

    Article  PubMed  Google Scholar 

  • Mitchell, K. M., Mutapi, F., & Woolhouse, M. E. (2008). The predicted impact of immunosuppression upon population age-intensity profiles for schistosomiasis. Parasite Immunology, 30, 462–470.

    Article  CAS  PubMed  Google Scholar 

  • Mulvenna, J., Moertel, L., Jones, M. K., Nawaratna, S., Lovas, E. M., Gobert, G. N., Colgrave, M., Jones, A., Loukas, A., & McManus, D. P. (2010). Exposed proteins of the Schistosoma japonicum tegument. International Journal for Parasitology, 40, 543–554.

    Article  CAS  PubMed  Google Scholar 

  • Mutapi, F., Bourke, C., Harcus, Y., Midzi, N., Mduluza, T., Turner, C. M., Burchmore, R., & Maizels, R. M. (2011). Differential recognition patterns of Schistosoma haematobium adult worm antigens by the human antibodies IgA, IgE, IgG1 and IgG4. Parasite Immunology, 33, 181–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O'Brien, D., & van Oosten-Hawle, P. (2016). Regulation of cell-non-autonomous proteostasis in metazoans. Essays in Biochemistry, 60, 133–142.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira, A. S., Cavalcanti, M. G., Zingali, R. B., Lima-Filho, J. L., & Chaves, M. E. (2015). Isoforms of Hsp70-binding human LDL in adult Schistosoma mansoni worms. Parasitology Research, 114, 1145–1152.

    Article  PubMed  Google Scholar 

  • Perez-Morales, D., & Espinoza, B. (2015). The role of small heat shock proteins in parasites. Cell Stress & Chaperones, 20, 767–780.

    Article  CAS  Google Scholar 

  • Prodromou, C. (2016). Mechanisms of Hsp90 regulation. The Biochemical Journal, 473, 2439–2452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauvage, F., Messaoudi, S., Fattal, E., Barratt, G., & Vergnaud-Gauduchon, J. (2017). Heat shock proteins and cancer: How can nanomedicine be harnessed? Journal of Controlled Release, 248, 133–143.

    Article  CAS  PubMed  Google Scholar 

  • Scott, J. C., & McManus, D. P. (1999). Identification of novel 70-kDa heat shock protein-encoding cDNAs from Schistosoma japonicum. International Journal for Parasitology, 29, 437–444.

    Article  CAS  PubMed  Google Scholar 

  • Shrestha, L., Bolaender, A., Patel, H. J., & Taldone, T. (2016). Heat Shock Protein (HSP) Drug discovery and development: Targeting heat shock proteins in disease. Current Topics in Medicinal Chemistry, 16, 2753–2764.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sotillo, J., Pearson, M., Becker, L., Mulvenna, J., & Loukas, A. (2015). A quantitative proteomic analysis of the tegumental proteins from Schistosoma mansoni schistosomula reveals novel potential therapeutic targets. International Journal for Parasitology, 45, 505–516.

    Article  CAS  PubMed  Google Scholar 

  • Tsai, I. J., Zarowiecki, M., Holroyd, N., Garciarrubio, A., Sanchez-Flores, A., Brooks, K. L., Tracey, A., Bobes, R. J., Fragoso, G., Sciutto, E., et al. (2013). The genomes of four tapeworm species reveal adaptations to parasitism. Nature, 496, 57–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vacirca, D., Perdicchio, M., Campisi, E., Delunardo, F., Ortona, E., Margutti, P., Teggi, A., Gottstein, B., & Siracusano, A. (2011). Favourable prognostic value of antibodies anti-HSP20 in patients with cystic echinococcosis: A differential immunoproteomic approach. Parasite Immunology, 33, 193–198.

    Article  CAS  PubMed  Google Scholar 

  • Van Hellemond, J. J., Retra, K., Brouwers, J. F., van Balkom, B. W., Yazdanbakhsh, M., Shoemaker, C. B., & Tielens, A. G. (2006). Functions of the tegument of schistosomes: Clues from the proteome and lipidome. International Journal for Parasitology, 36, 691–699.

    Article  PubMed  Google Scholar 

  • Wang, S., Luo, Y., Xiao, L., Luo, X., Gao, S., Dou, Y., Zhang, H., Guo, A., Meng, Q., Hou, J., et al. (2016a). Comparative genomics reveals adaptive evolution of Asian tapeworm in switching to a new intermediate host. Nature Communications, 7, 12845.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Wang, J., Liang, Y., Ni, H., Shi, L., Xu, C., Zhou, Y., Su, Y., Mou, X., Chen, D., & Mao, C. (2016b). Schistosoma japonicum HSP60-derived peptide SJMHE1 suppresses delayed-type hypersensitivity in a murine model. Parasites & Vectors, 9, 147.

    Article  Google Scholar 

  • Wang, X., Zhou, S., Chi, Y., Wen, X., Hoellwarth, J., He, L., Liu, F., Wu, C., Dhesi, S., Zhao, J., et al. (2009a). CD4+CD25+ Treg induction by an HSP60-derived peptide SJMHE1 from Schistosoma japonicum is TLR2 dependent. European Journal of Immunology, 39, 3052–3065.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Cheng, Z., Lu, X., & Tang, C. (2009b). Echinococcus multilocularis: Proteomic analysis of the protoscoleces by two-dimensional electrophoresis and mass spectrometry. Experimental Parasitology, 123, 162–167.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Xiao, D., Shen, Y., Han, X., Zhao, F., Li, X., Wu, W., Zhou, H., Zhang, J., & Cao, J. (2015). Proteomic analysis of the excretory/secretory products and antigenic proteins of Echinococcus granulosus adult worms from infected dogs. BMC Veterinary Research, 11, 119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Weinreb, O., Dovrat, A., Dunia, I., Benedetti, E. L., & Bloemendal, H. (2001). UV-A-related alterations of young and adult lens water-insoluble alpha-crystallin, plasma membranous and cytoskeletal proteins. European Journal of Biochemistry, 268, 536–543.

    Article  CAS  PubMed  Google Scholar 

  • Yang, J., Yang, L., Lv, Z., Wang, J., Zhang, Q., Zheng, H., & Wu, Z. (2012). Molecular cloning and characterization of a HSP70 gene from Schistosoma japonicum. Parasitology Research, 110, 1785–1793.

    Article  PubMed  Google Scholar 

  • Yang, L. L., Lv, Z. Y., Hu, S. M., He, S. J., Li, Z. Y., Zhang, S. M., Zheng, H. Q., Li, M. T., Yu, X. B., Fung, M. C., & Wu, Z. D. (2009). Schistosoma japonicum: Proteomics analysis of differentially expressed proteins from ultraviolet-attenuated cercariae compared to normal cercariae. Parasitology Research, 105, 237–248.

    Article  PubMed  Google Scholar 

  • Zheng, Y. (2013). Strategies of Echinococcus species responses to immune attacks: Implications for therapeutic tool development. International Immunopharmacology, 17, 495–501.

    Article  CAS  PubMed  Google Scholar 

  • Zheng, Y., Guo, X., Su, M., Guo, A., Ding, J., Yang, J., Xiang, H., Cao, X., Zhang, S., Ayaz, M., & Luo, X. (2017). Regulatory effects of Echinococcus multilocularis extracellular vesicles on RAW264.7 macrophages. Veterinary Parasitology, 235, 29–36.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, L., Liu, J., Dao, J., Lu, K., Li, H., Gu, H., Feng, X., & Cheng, G. (2016). Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite-host interactions. Scientific Reports, 6, 25885.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The study was financially supported by grants from the National Natural Science Foundation of China (31201900, 31702224, U1703104 and 31472185), Central State Public-interest Scientific Institution Basal Research Fund (1610312016017) and the National Key Basic Research Program (973 program) of China (2015CB150300).

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Authors and Affiliations

  1. State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, CAAS, Lanzhou, China

    Yadong Zheng, Xiaola Guo, Jin’en Wu & Jing Yang

  2. Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, China

    Yadong Zheng

  3. Department of Ophthalmology, Shanghai Ninth People’s Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China

    Xiaoliang Jin

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  1. Yadong Zheng
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  2. Xiaola Guo
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  3. Jin’en Wu
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  4. Jing Yang
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  5. Xiaoliang Jin
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Correspondence to Yadong Zheng .

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Editors and Affiliations

  1. Professor, Department of Medicine and Director, Precision Therapeutics Proteogenomics Diagnostic Center, Eleanor N. Dana Cancer Center University of Toledo College of Medicine and Life Sciences, Toledo, USA

    Alexzander A. A. Asea

  2. Visiting Scientist Professor, Department of Experimental Radiation Oncology, The University of Texas MD Anderson Cancer Center, Houston, USA

    Punit Kaur

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Zheng, Y., Guo, X., Wu, J., Yang, J., Jin, X. (2017). Heat Shock Proteins in Parasitic Flatworms. In: Asea, A., Kaur, P. (eds) Heat Shock Proteins in Veterinary Medicine and Sciences. Heat Shock Proteins, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-319-73377-7_11

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