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Heat shock protein 70 (Hsp70) in Schistosoma mansoni and its role in decreased adult worm sensitivity to praziquantel

Published online by Cambridge University Press:  04 March 2020

Iman F. Abou-El-Naga Open the ORCID record for Iman F. Abou-El-Naga [Opens in a new window]
Iman F. Abou-El-Naga*
Affiliation:
Medical Parasitology Department, Faculty of Medicine, Alexandria University, Alexandria, Egypt
*
Author for correspondence: Iman F. Abou-El-Naga, E-mail: imanabouelnaga@hotmail.com
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Abstract

Schistosoma mansoni is the most common species causing schistosomiasis. It has a complex life cycle involving a vertebrate definitive host and a snail intermediate host of the genus Biomphalaria. Each stage encounters a plethora of environmental stresses specially heat stress. Another sort of stress arises from repeated exposure of the parasite to praziquantel (PZQ), the only drug used for treatment, which leads to the development of resistance in the fields and the labs. Heat shock protein 70 (Hsp70) is found in different developmental stages of S. mansoni. It is immunogenic and regulate cercarial invasion besides its chaperone function. In the Biomphalaria/S. mansoni interaction, epigenetic modulations of the Hsp70 gene underscore the susceptibility phenotype of the snail. Hsp70 is up-regulated in adult S. mansoni with decreased sensitivity to PZQ. This could be due to the induction of oxidative and endoplasmic reticulum stress, induction of apoptosis, exposure to the stressful drug pressure and increase influx of calcium ions. Up-regulation of Hsp70 might help the worm to survive the schistosomicidal effect of the drug mainly by dealing with misfolded proteins, inhibition of apoptosis, induction of autophagy, up-regulation of the P-glycoprotein transporter and attenuation of the signalling from G protein coupled receptors.

Keywords

ApoptosisBiomphalariaenvironmental stressglobal warmingHsp70praziquantel resistanceSchistosoma mansoni
Type
Review Article
Information
Parasitology , Volume 147 , Issue 6 , May 2020 , pp. 634 - 642
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Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Abou-El-Naga, IF (2015) Demographic, socioeconomic and environmental changes affecting circulation of neglected tropical diseases in Egypt. Asian Pacific Journal of Tropical Medicine 8, 881–888.CrossRefGoogle ScholarPubMed
Abou-El-Naga, IF (2018) Towards elimination of schistosomiasis after 5000 years of endemicity in Egypt. Acta Tropica 181, 112–121.CrossRefGoogle ScholarPubMed
Abou-El-Naga, IF and Radwan, EH (2012) Defense response of susceptible and resistant Biomphalaria alexandrina snails against Schistosoma mansoni infection. Revista de Biologia Tropica 60, 1195–1204.Google ScholarPubMed
Abou-El-Naga, IF, Amer, EI, Boulos, LM, El-Faham, MH, Abou Seada, NM and Younis, SS (2019) Biological and proteomic studies of Schistosoma mansoni with decreased sensitivity to praziquantel. Comparative Immunology, Microbiology and Infectious Diseases 66, 101341.CrossRefGoogle ScholarPubMed
Aragon, AD, Imani, RA, Blackburn, VR and Cunningham, C (2008) Microarray based analysis of temperature and oxidative stress induced messenger RNA in Schistosoma mansoni. Molecular and Biochemical Parasitology 162, 134–141.CrossRefGoogle ScholarPubMed
Aragon, AD, Imani, RA, Blackburn, VR, Cupit, PM, Melman, SD, Goronga, T, Webb, T, Loker, ES and Cunningham, C (2009) Towards an understanding of the mechanism of action of praziquantel. Molecular and Biochemical Parasitology 164, 57–65.CrossRefGoogle ScholarPubMed
Arican-Goktas, HD, Ittiprasert, W, Bridger, JM and Knight, M (2014) Differential spatial repositioning of activated genes in Biomphalaria glabrata snails infected with Schistosoma mansoni. PLOS Neglected Tropical Diseases 8, e3013.CrossRefGoogle ScholarPubMed
Bais, S, Berry, CT, Liu, X, Ruthel, G, Freedman, BD and Greenberg, RM (2018) Atypical pharmacology of schistosome TRPA1-like ion channels. PLOS Neglected Tropical Diseases 12, e0006495.CrossRefGoogle ScholarPubMed
Berriman, M, Haas, BJ, LoVerde, PT, Wilson, RA, Dillon, GP, Cerqueira, GC, Mashiyama, ST, Al-Lazikani, B, Andrade, LF, Ashton, PD, Aslett, MA, Bartholomeu, DC, Blandin, G, Caffrey, CR, Coghlan, A, Coulson, R, Day, TA, Delcher, A, DeMarco, R, Djikeng, A, Eyre, T, Gamble, JA, Ghedin, E, Gu, Y, Hertz-Fowler, C, Hirai, H, Hirai, Y, Houston, R, Ivens, A, Johnston, DA, Lacerda, D, Macedo, CD, McVeigh, P, Ning, Z, Oliveira, G, Overington, JP, Parkhill, J, Pertea, M, Pierce, RJ, Protasio, AV, Quail, MA, Rajandream, MA, Rogers, J, Sajid, M, Salzberg, SL, Stanke, M, Tivey, AR, White, O, Williams, DL, Wortman, J, Wu, W, Zamanian, M, Zerlotini, A, Fraser-Liggett, CM, Barrell, BG and El-Sayed, NM (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460, 352–358.CrossRefGoogle ScholarPubMed
Biyani, N, Singh, AK, Mandal, S, Chawla, B and Madhubala, R (2011) Differential expression of proteins in antimony-susceptible and -resistant isolates of Leishmania donovani. Molecular and Biochemical Parasitology 179, 91–99.CrossRefGoogle ScholarPubMed
Bolhassani, A and Rafati, S (2008) Heat-shock proteins as powerful weapons in vaccine development. Expert Review of Vaccines 7, 1185–1199.CrossRefGoogle ScholarPubMed
Bolhassani, A and Rafati, S (2013) Mini-chaperones: potential immuno-stimulators in vaccine design. Human Vaccines and Immunotherapeutics 9, 153–161.CrossRefGoogle ScholarPubMed
Calavas, D and Martin, PM (2014) Schistosomiasis in cattle in Corsica, France. Emerging Infectious Diseases 20, 2163–2164.CrossRefGoogle ScholarPubMed
Campbell-Lendrum, D, Manga, L, Bagayoko, M and Sommerfeld, J (2015) Climate change and vector-borne diseases: what are the implications for public health research and policy? Philosophical Transaction of the Royal Society London B: Biological Science 370, 20130552.CrossRefGoogle ScholarPubMed
Chan, JD, Cupit, PM, Gunaratne, GS, Mc Corvy, JD, Yang, Y and Stoltz, K (2017) The anthelmintic praziquantel is a human serotoninergic G-protein-coupled receptor ligand. Nat Communications 8, 1910.CrossRefGoogle ScholarPubMed
Cioli, D and Pica-Mattoccia, L (2003) Praziquantel. Parasitology Research 90, S3–S9.CrossRefGoogle ScholarPubMed
Coelho, JR and Bezerra, FS (2006) The effects of temperature change on the infection rate of Biomphalaria glabrata with Schistosoma mansoni. Memorias do Instituto Oswaldo Cruz 101, 223–224.CrossRefGoogle ScholarPubMed
Couto, FF, Coelho, PM, Araujo, N, Kusel, JR, Katz, N, Jannotti-Passos, LK and Mattos, AC (2011) Schistosoma mansoni: a method for inducing resistance to praziquantel using infected Biomphalaria glabrata snails. Memorias do Instituto Oswaldo Cruz 106, 153–157.CrossRefGoogle ScholarPubMed
De Maio, A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock (Augusta, Ga.) 11, 1–12.CrossRefGoogle ScholarPubMed
De Maio, A (2011) Extracellular heat shock proteins, cellular export vesicles and the stress observation system: a form of communication during injury, infection, and cell damage. Cell Stress and Chaperones 16, 235–249.CrossRefGoogle ScholarPubMed
de Paula, RG, de Magalhães Ornelas, AM, Morais, ER, de Souza Gomes, M, de Paula Aguiar, D, Magalhães, LG and Rodrigues, V (2015) Proteasome stress responses in Schistosoma mansoni. Parasitology Research 114, 1747–1760.CrossRefGoogle ScholarPubMed
Duan, MM, Xu, RM, Yuan, CX, Li, YY, Liu, Q, Cheng, GF, Lin, JJ and Feng, XG (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.CrossRefGoogle ScholarPubMed
El-Bassiouni, EA, Helmy, MH, Saad, EI, El-NabiKamel, MA, Abdel-Meguid, E and Hussein, HS (2007) Modulation of the antioxidant defence in different developmental stages of Schistosoma mansoni by praziquantel and artemether. British Journal of Biomedical Science 64, 168–174.CrossRefGoogle ScholarPubMed
El-Kenawy, EA, El-Kott, AF and Hasan, MS (2008) Heat shock protein expression independently predicts survival outcome in schistosomiasis-associated urinary bladder cancer. The International Journal of Biological Markers 23, 214–218.CrossRefGoogle Scholar
Fernández-Fernández, MR, Gragera, M, Ochoa-Ibarrola, L, Quintana-Gallardo, L and Valpuesta, JM (2017) Hsp70 – a master regulator in protein degradation. FEBS Letters 591, 2648–2660.CrossRefGoogle ScholarPubMed
Fogarty, CE, Zhao, M, McManus, DP, Duke, MG, Cummins, SF and Wang, T (2019) Comparative study of excretory-secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata. Parasite and Vectors 12, 452.CrossRefGoogle ScholarPubMed
Gees, M, Colsoul, B and Nilius, B (2010) The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harb Perspective in Biology 2, a003962.Google ScholarPubMed
Gehrmann, M, Radons, J, Molls, M and Multhoff, G (2008) The therapeutic implications of clinically applied modifiers of heat shock protein 70 (Hsp70) expression by tumor cells. Cell Stress & Chaperones 13, 1–10.CrossRefGoogle ScholarPubMed
Giri, BR and Roy, B (2016) Praziquantel induced oxidative stress and apoptosis-like cell death in Raillietina echinobothrida. Acta Tropica 159, 50–57.CrossRefGoogle ScholarPubMed
Gorman, AM, Healy, SJ, Jäger, R and Samali, A (2012) Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacology and Therapeutics 134, 306–316.CrossRefGoogle ScholarPubMed
Grabe, K and Haas, W (2004) Navigation within host tissues: cercariae orientate towards dark after penetration. Parasitology Research 93, 111–113.CrossRefGoogle Scholar
Greenberg, RM (2005) Are Ca2+ channels targets of praziquantel action? International Journal for Parasitology 35, 1–9.CrossRefGoogle ScholarPubMed
Greenberg, RM and Doenhoff, MJ (2017) Chemotherapy and drug resistance in schistosomiasis and other trematode and cestode infections. In Mayers, D, Sobel, J, Ouellette, M, Kaye, K and Marchaim, D (eds), Antimicrobial Drug Resistance. Cham: Springer, pp. 705–734.CrossRefGoogle Scholar
Gryseels, B (2012) Schistosomiasis. Infectious Disease Clinics of North America 26, 383–397.CrossRefGoogle ScholarPubMed
Gryseels, B, Polman, K, Clerinx, J and Kestens, L (2006) Human schistosomiasis. The Lancet 368, 1106–1118.CrossRefGoogle ScholarPubMed
Hammouda, NA, Abou El Naga, IF, El-Temsahi, MM and Sharaf, IA (1994) Schistosoma mansoni: a comparative study on two cercarial transformation methods. Journal of the Egyptian Society of Parasitology 24, 479–486.Google ScholarPubMed
Hara, Y, Wakamori, M, Ishii, M, Maeno, E, Nishida, M, Yoshida, T, Yamada, H, Shimizu, S, Mori, E, Kudoh, J, Shimizu, N, Kurose, H, Okada, Y, Imoto, K and Mori, Y (2002) LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Molecular Cell 9, 163–173.CrossRefGoogle ScholarPubMed
He, S, Yang, L, Lv, Z, Hu, W, Cao, J, Wei, J, Sun, X, Yang, J, Zheng, H and 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.CrossRefGoogle ScholarPubMed
Hedstrom, RC, Culpepper, J, Harrison, RA, Agabian, N and Newport, G (1987) A major immunogen in Schistosoma mansoni infections is homologous to the heat-shock protein hsp90. Journal of Experimental Medicine 165, 1430–1435.CrossRefGoogle Scholar
Hedstrom, R, Culpepper, J, Schinski, V, Agabian, N and Newport, G (1988) Schistosome heat-shock proteins are immunologically distinct host-like antigens. Molecular and Biochemical Parasitology 29, 275–282.CrossRefGoogle ScholarPubMed
Hines-Kay, J, Cupit, PM, Sanchez, MC, Rosenberg, GH, Hanelt, B and Cunningham, C (2012) Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Molecular and Biochemical Parasitology 186, 87–94.CrossRefGoogle ScholarPubMed
Hsu, WL and Yoshioka, T (2015) Role of TRP channels in the induction of heat shock proteins (Hsps) by heating skin. Biophysics (Nagoya-shi Japan) 11, 25–32.Google ScholarPubMed
Hurowitz, EH, Melnyk, JM, Chen, YJ, Kouros-Mehr, H, Simon, MI and Shizuya, HM (2000) Genomic characterization of the human heterotrimeric G protein alpha, beta, and gamma subunit genes. DNA Research 7, 111–120.CrossRefGoogle ScholarPubMed
Ishida, K and Jolly, ER (2016) Hsp70 may be a molecular regulator of schistosome host invasion. PLOS Neglected Tropical Diseases 10, e0004986.CrossRefGoogle ScholarPubMed
Ishida, Y and Nagata, K (2009) Autophagy eliminates a specific species of misfolded procollagen and plays a protective role in cell survival against ER stress. Autophagy 5, 1217–1219.CrossRefGoogle Scholar
Ishida, K, Varrecchia, M, Knudsen, GM and Jolly, ER (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.CrossRefGoogle ScholarPubMed
Ismail, MM, Taha, SA, Farghaly, AM and el-Azony, AS (1994) Laboratory induced resistance to praziquantel in experimental schistosomiasis. Journal of the Egyptian Society of Parasitology 24, 685–695.Google ScholarPubMed
Ittiprasert, W and Knight, M (2012) Reversing the resistance phenotype of the Biomphalaria glabrata snail host Schistosoma mansoni infection by temperature modulation. PLOS Pathogens 8, e1002677.CrossRefGoogle ScholarPubMed
Ittiprasert, W, Nene, R, Miller, A, Raghavan, N, Lewis, F, Hodgson, J and Knight, M (2009) Schistosoma mansoni infection of juvenile Biomphalaria glabrata induces a differential stress response between resistant and susceptible snails. Experimental Parasitology 123, 203–211.CrossRefGoogle ScholarPubMed
Jeremias, WJ, Araújo, FMG, Queiroz, FR, Pais, FSM, Mattos, ACA, Salim, ACM, Coelho, PMZ, Oliveira, GC, Kusel, JR, Guerra-Sá, R, Coimbra, RS and Babá, ÉH (2017) Comparative sequence analysis reveals regulation of genes in developing schistosomula of Schistosoma mansoni exposed to host portal serum. PLOS One 12, e0178829.CrossRefGoogle ScholarPubMed
Joly, AL, Wettstein, G, Mignot, G, Ghiringhelli, F and Garrido, C (2010) Dual role of heat shock proteins as regulators of apoptosis and innate immunity. Journal of Innate Immunity 2, 238–247.CrossRefGoogle ScholarPubMed
Kabatereine, NB, Brooker, S, Tukahebwa, EM, Kazibwe, F and Onapa, AW (2004) Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control. Tropical Medicine and Internal Health 9, 372–380.CrossRefGoogle ScholarPubMed
Kalinda, C, Chimbari, M and Mukaratirwa, S (2017) Implications of changing temperatures on the growth, fecundity and survival of intermediate host snails of schistosomiasis: a systematic review. International Journal of Environmental Research and Public Health 14, E80.CrossRefGoogle ScholarPubMed
Kanamura, HY, Hancock, K, Rodrigues, V and Damian, RT (2002) Schistosoma mansoni heat shock protein 70 elicits an early humoral immune response in S. mansoni infected baboons. Memorias do Instituto Oswaldo Cruz 97, 711–716.CrossRefGoogle ScholarPubMed
Kasinathan, RS, Sharma, LK, Cunningham, C, Webb, TR and Greenberg, RM (2014) Inhibition or knockdown of ABC transporters enhances susceptibility of adult and juvenile schistosomes to praziquantel. PLOS Neglected Tropical Diseases 8, e3265.CrossRefGoogle ScholarPubMed
Kimura, K, Tanaka, N, Nakamura, N, Takano, S and Ohkuma, S (2007) Knockdown of mitochondrial heat shock protein 70 promotes progeria-like phenotypes in Caenorhabditis elegans. The Journal of Biological Chemistry 282, 5910–5918.CrossRefGoogle ScholarPubMed
Knight, M, Arican-Goktas, HD, Ittiprasert, W, Odoemelam, EC, Miller, AN and Bridger, JM (2014) Schistosomes and snails: a molecular encounter. Frontiers in Genetics 5, 230.CrossRefGoogle ScholarPubMed
Knight, M, Elhelu, O, Smith, M, Haugen, B, Miller, A, Raghavan, N, Wellman, C, Cousin, C, Dixon, F, Mann, V, Rinaldi, G, Ittiprasert, W and Brindley, PJ (2015) Susceptibility of snails to infection with schistosomes is influenced by temperature and expression of heat shock proteins. Epidemiology (Sunnyvale) 5, 189.Google ScholarPubMed
Knight, M, Ittiprasert, W, Arican-Goktas, HD and Bridger, JM (2016) Epigenetic modulation, stress and plasticity in susceptibility of the snail host, Biomphalaria glabrata, to Schistosoma mansoni infection. International Journal for Parasitology 46, 389–394.CrossRefGoogle ScholarPubMed
Knudsen, GM, Medzihradszky, KF, Lim, KC, Hansell, E and McKerrow, JH (2005) Proteomic analysis of Schistosoma mansoni cercarial secretions. Molecular and Cellular Proteomics 4, 1862–1875.CrossRefGoogle ScholarPubMed
Kumar, S, Stokes, J III, Singh, UP, Scissum Gunn, K, Acharya, A, Manne, U and Mishra, M (2016) Targeting Hsp70: a possible therapy for cancer. Cancer Letters 374, 156–166.CrossRefGoogle ScholarPubMed
Kusel, JR, Al-Adhami, BH and Doenhoff, MJ (2007) The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitology 134, 1477–1526.CrossRefGoogle ScholarPubMed
Lim, WK, Kanelakis, KC and Neubig, RR (2013) Regulation of G protein signaling by the 70 kDa heat shock protein. Cellular Signalling 25, 389–396.CrossRefGoogle Scholar
Liu, T, Daniels, CK and Cao, S (2012) Comprehensive review on the HSC70 functions, interactions with related molecules and involvement in clinical diseases and therapeutic potential. Pharmacology and Therapeutics 136, 354–374.CrossRefGoogle ScholarPubMed
Loverde, PT (1998) Do antioxidants play a role in schistosome host-parasite interactions? Parasitology Today 14, 284–289.CrossRefGoogle ScholarPubMed
Mambula, SS and Calderwood, SK (2006) Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. The Journal of Immunology 177, 7849–7857.CrossRefGoogle ScholarPubMed
Masamba, P, Adenowo, AF, Oyinloye, BE and Kappo, AP (2016) Universal stress proteins as new targets for environmental and therapeutic interventions of schistosomiasis. International Journal of Environmental Research and Public Health 13, E972.CrossRefGoogle ScholarPubMed
Mathieson, W, Castro-Borges, W and Wilson, RA (2011) The proteasome-ubiquitin pathway in the Schistosoma mansoni egg has development- and morphology specific characteristics. Molecular and Biochemical Parasitology 175, 118–125.CrossRefGoogle ScholarPubMed
Mayer, MP and Bukau, B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and Molecular Life Sciences 62, 670–684.CrossRefGoogle ScholarPubMed
Morais, ER, Oliveira, KC, Magalhães, LG, Moreira, EB, Verjovski Almeida, S and Rodrigues, V (2013) Effects of curcumin on the parasite Schistosoma mansoni: a transcriptomic approach. Molecular and Biochemical Parasitology 187, 91–97.CrossRefGoogle ScholarPubMed
Morgan, JA, Dejong, RJ, Snyder, SD, Mkoji, GM, Loker, ES and Andrews, P (2001) Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology 123, 211–228.CrossRefGoogle ScholarPubMed
Moseley, P (2000) Stress proteins and the immune response. Immunopharmacology 48, 299–302.CrossRefGoogle ScholarPubMed
Nelson, MK, Cruz, BC, Buena, KL, Nguyen, H and Sullivan, JT (2016) Effects of abnormal temperature and starvation on the internal defense system of the schistosome-transmitting snail Biomphalaria glabrata. Journal of Invertebrate Pathology 138, 18–23.CrossRefGoogle ScholarPubMed
Neumann, S, Zin, E, Lantner, F and Schechter, I (1993) Regulation of HSP70 gene expression during the life cycle of the parasitic helminth Schistosoma mansoni. European Journal of Biochemistry 212, 589–596.CrossRefGoogle ScholarPubMed
Onile, OS, Calder, B, Soares, NC, Anumudu, CI and Blackburn, JM (2017) Quantitative label-free proteomic analysis of human urine to identify novel candidate protein biomarkers for schistosomiasis. PLOS Neglected Tropical Diseases 11, e0006045. https://doi.org/10.1371/journal.pntd.0006045.CrossRefGoogle ScholarPubMed
Park, SK and Marchant, JS (2020) The journey to discovering a flatworm target of praziquantel: a long TRP. Trends in Parasitology 36, 182–194.CrossRefGoogle ScholarPubMed
Park, SK, Gunaratne, GS, Chulkov, EG, Moehring, F, McCusker, P, Dosa, PI, Chan, JD, Stucky, CL and Marchant, JS (2019) The anthelmintic drug praziquantel activates a schistosome transient receptor potential channel. The Journal of Biological Chemistry 294, 18873–18880.CrossRefGoogle ScholarPubMed
Pereira-Júnior, OS, Pereira, RV, Silva, CS, Castro-Borges, W, Sá, RG, Cabral, FJ, Silva, SH, Soares, CS, Morais, ER, Moreira, EB, Magalhães, LG, de Paula, FM and Rodrigues, V (2013) Investigation on the 19S ATPase proteasome subunits (Rpt1-6) conservation and their differential gene expression in Schistosoma mansoni. Parasitology Research 112, 235–242.CrossRefGoogle ScholarPubMed
Pereira, C, Fallon, PG, Cornette, J, Capron, A, Doenhoff, MJ and Pierce, RJ (1998) Alterations in cytochrome-c oxidase expression between praziquantel-resistant and susceptible strains of Schistosoma mansoni. Parasitology 117, 63–73.CrossRefGoogle ScholarPubMed
Pereira, AS, Cavalcanti, MG, Zingali, RB, Lima-Filho, JL and Chaves, ME (2015) Isoforms of Hsp70-binding human LDL in adult Schistosoma mansoni worms. Parasitology Research 114, 1145–1152.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L, Orsini, T, Basso, A, Festucci, A, Liberti, P, Guidi, A, Marcatto-Maggi, AL, Nobre-Santana, S, Troiani, AR, Cioli, D and Valle, C (2008) Schistosoma mansoni: lack of correlation between praziquantel-induced intra-worm calcium influx and parasite death. Experimental Parasitology 119, 332–335.CrossRefGoogle ScholarPubMed
Pockley, AG, Muthana, M and Calderwood, SK (2008) The dual immunoregulatory roles of stress proteins. Trends in Biochemical Sciences 33, 71–79.CrossRefGoogle ScholarPubMed
Prole, DL and Taylor, CW (2011) Identification of intracellular and plasma membrane calcium channel homologues in pathogenic parasites. PLOS One 6, e26218.CrossRefGoogle ScholarPubMed
Protasio, AV, Tsai, IJ, Babbage, A, Nichol, S, Hunt, M, Aslett, MA, De Silva, N, Velarde, GS, Anderson, TJ, Clark, RC, Davidson, C, Dillon, GP, Holroyd, NE, LoVerde, PT, Lloyd, C, McQuillan, J, Oliveira, G, Otto, TD, Parker-Manuel, SJ, Quail, MA, Wilson, RA, Zerlotini, A, Dunne, DW and Berriman, M (2012) A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLOS Neglected Tropical Diseases 6, e1455.CrossRefGoogle ScholarPubMed
Richards, CS (1970) Genetics of a molluscan vector of schistosomiasis. Nature 227, 806–810.CrossRefGoogle ScholarPubMed
Routsias, JG and Tzioufas, AG (2006) The role of chaperone proteins in autoimmunity. Annals of the New York Academy of Science 1088, 52–64.CrossRefGoogle ScholarPubMed
Sanchez, MC, Cupit, PM, Bu, L and Cunningham, C (2019) Transcriptomic analysis of reduced sensitivity to praziquantel in Schistosoma mansoni. Molecular and Biochemical Parasitology 228, 6–15.CrossRefGoogle ScholarPubMed
Shonhai, A, Maier, AG, Przyborski, JM and Blatch, GL (2011) Intracellular protozoan parasites of humans: the role of molecular chaperones in development and pathogenesis. Protein and Peptide Letters 18, 143–157.CrossRefGoogle ScholarPubMed
Sotillo, J, Pearson, M, Potriquet, J, Becker, L, Pickering, D, Mulvenna, J and Loukas, A (2016) Extracellular vesicles secreted by Schistosoma mansoni contain protein vaccine candidates. International Journal for Parasitology 46, 1–5.CrossRefGoogle ScholarPubMed
Specht, HM, Ahrens, N, Blankenstein, C, Duell, T, Fietkau, R, Gaipl, US, Günther, C, Gunther, S, Habl, G, Hautmann, H, Hautmann, M, Huber, RM, Molls, M, Offner, R, Rödel, C, Rödel, F, Schütz, M, Combs, SE and Multhoff, G (2015) Heat shock protein 70 (Hsp70) peptide activated natural killer (NK) cells for the treatment of patients with non-small cell lung cancer (NSCLC) after radiochemotherapy (RCTx) – from preclinical studies to a clinical phase II trial. Frontiers in Immunology 6, 162.CrossRefGoogle ScholarPubMed
Stensgaard, AS, Vounatsou, P, Sengupta, ME and Utzinger, J (2019) Schistosomes, snails and climate change: current trends and future expectations. Acta Tropica 190, 257–268.CrossRefGoogle ScholarPubMed
Stirewalt, MA (1954) Effect of snail maintenance temperatures on development of Schistosoma mansoni. Experimental Parasitology 3, 504–516.CrossRefGoogle ScholarPubMed
Swindell, WR, Huebner, M and Weber, AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8, 125.CrossRefGoogle ScholarPubMed
Tempone, AJ, Bianconi, ML and Rumjanek, FD (1997) The interaction of human LDL with the tegument of adult Schistosoma mansoni. Molecular and Cellular Biochemistry 177, 139–144.CrossRefGoogle ScholarPubMed
Tiroli-Cepeda, AO and Ramos, CH (2011) An overview of the role of molecular chaperones in protein homeostasis. Protein and Peptide Letters 18, 101–109.CrossRefGoogle ScholarPubMed
Ushioda, R, Miyamoto, A, Inoue, M, Watanabe, S, Okumura, M, Maegawa, KI, Uegaki, K, Fujii, S, Fukuda, Y, Umitsu, M, Takagi, J, Inaba, K, Mikoshiba, K and Nagata, K (2016) Redox-assisted regulation of Ca2+ homeostasis in the endoplasmic reticulum by disulfide reductase ERdj5. Proceedings of the National Academy of Sciences of the United States of America 113, E6055–E6063.CrossRefGoogle ScholarPubMed
Walker, AJ (2011) Insights into the functional biology of schistosomes. Parasites and Vectors 4, 203.CrossRefGoogle ScholarPubMed
World Health Organization (1993) The Control of Schistosomiasis: Second Report of WHO Expert Committee. WHO Technical Report Series No. 830. Geneva, Switzerland: World Health Organization.Google Scholar
Xiao, SH, Mei, JY and Jiao, PY (2009) The in vitro effect of mefloquine and praziquantel against juvenile and adult Schistosoma japonicum. Parasitology Research 106, 237–246.CrossRefGoogle ScholarPubMed
Xin, Y, Yin, F, Qi, S, Shen, L, Xu, Y, Luo, L, Lan, L and Yin, Z (2013) Parthenolide reverses doxorubicin resistance in human lung carcinoma A549 cells by attenuating NF-κB activation and HSP70 up-regulation. Toxicology Letters 221, 73–82.CrossRefGoogle ScholarPubMed
Yokota, S and Fujii, N (2010) Immunomodulatory activity of extracellular heat shock proteins and their autoantibodies. Microbiology and Immunology 54, 299–307.Google ScholarPubMed
You, H, McManus, DP, Hu, W, Smout, MJ, Brindley, PJ and Gobert, GN (2013) Transcriptional responses of in vivo praziquantel exposure in schistosomes identifies a functional role for calcium signalling pathway member CamKII. PLOS Pathogens 9, e1003254.CrossRefGoogle ScholarPubMed
Zahoor, Z, Davies, AJ, Kirk, RS, Rollinson, D and Walker, AJ (2010) Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host. Biomphalaria glabrata. Cell Stress and Chaperones 15, 639–650.CrossRefGoogle ScholarPubMed