Biochemical and biophysical methodologies open the road for effective schistosomiasis therapy and vaccination

Biochimica et Biophysica Acta - General Subjects

Volumn 1861, Issue 1, 2017, Pages 3613-3620

  El Ridi, Rashika ^a   Tallima, Hatem ^a,b   Migliardo, Federica ^c  

^a CAIRO UNIVERSITY   (Egypt)

^b The American University in Cairo   (Egypt)

^c UNIVERSITY OF MESSINA   (Italy)

Author keywords

Arachidonic acid; Elastic incoherent and quasi elastic neutron scattering; Hydrogen bond barrier; Neutral sphingomyelinase; Schistosoma; Sphingomyelin

Indexed keywords

3,3' (1,4 PHENYLENE)BIS[N [4 (4,5 DIHYDRO 1H IMIDAZOL 2 YL)PHENYL]ACRYLAMIDE]; ARACHIDONIC ACID; CHOLESTEROL; CURCUMIN; GLUTATHIONE; MANUMYCIN; METHYL BETA CYCLODEXTRIN; PRAZIQUANTEL; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; TETRASPANIN;

ARTICLE; BIOCHEMISTRY; BIOPHYSICS; BIOSYNTHESIS; BLEACHING; COMBINATION CHEMOTHERAPY; DRUG CYTOTOXICITY; DRUG EFFICACY; ENZYME ACTIVATION; FLUORESCENCE; HEALTH PROGRAM; HUMAN; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; IMMUNE EVASION; IN VITRO STUDY; IN VIVO STUDY; INTEGUMENT; LIPID BILAYER; MONOTHERAPY; NEUTRON SCATTERING; NONHUMAN; PARASITE DEATH; PARASITE VIABILITY; PRIORITY JOURNAL; QUASI ELASTIC NEUTRON SCATTERING; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SCHISTOSOMICIDE; TEMPERATURE; VACCINATION; ANIMAL; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; PROCEDURES; SCHISTOSOMA;

ANIMALS; BIOCHEMISTRY; BIOPHYSICS; IMMUNE EVASION; SCHISTOSOMA; SCHISTOSOMIASIS; VACCINATION;

EID: 84963974164     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2016.03.036     Document Type: Article

References (87)

1. [1] Utzinger, J., N'goran, E.K., Caffrey, C.R., Keiser, J., From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Trop. 120:Suppl. 1 (2011), S121–S137.
2. [2] Adenowo, A.F., Oyinloye, B.E., Ogunyinka, B.I., Kappo, A.P., Impact of human schistosomiasis in sub-Saharan Africa. Braz. J. Infect. Dis. 19 (2015), 196–205.
3. [3] King, C.H., It's time to dispel the myth of “asymptomatic” schistosomiasis. PLoS Negl. Trop. Dis., 9, 2015, e0003504.
4. [4] Kusel, J.R., Al-Adhami, B.H., Doenhoff, M.J., The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitology 134 (2007), 1477–1526.
5. [5] Keating, J.H., Wilson, R.A., Skelly, P.J., No overt cellular inflammation around intravascular schistosomes in vivo. J. Parasitol. 92 (2006), 1365–1369.
6. [6] Hockley, D.J., McLaren, D.J., Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. Int. J. Parasitol. 3 (1973), 13–25.
7. [7] Hockley, D.J., Ultrastructure of the tegument of Schistosoma. Adv. Parasitol. 11 (1973), 233–305.
8. [8] Mclaren, D.J., Hockley, D.J., Blood flukes have a double outer membrane. Nature 269 (1977), 147–149.
9. [9] Igetei, J.E., Liddell, S., El-Faham, M., Doenhoff, M.J., Purification of a chymotrypsin-like enzyme present on adult Schistosoma mansoni worms from infected mice and its characterization as a host carboxylesterase. Parasitology, 2016 (in print).
10. [10] Wilson, R.A., Barnes, P.E., An in vitro investigation of dynamic processes occurring in the schistosome tegument, using compounds known to disrupt secretory processes. Parasitology 68 (1974), 259–270.
11. [11] Skelly, P.J., Shoemaker, C.B., The Schistosoma mansoni host-interactive tegument forms from vesicle eruptions of a cyton network. Parasitology 122 (2001), 67–73.
12. [12] Skelly, P.J., Wilson, R.A., Making sense of the schistosome surface. Adv. Parasitol. 63 (2006), 185–284 Review.
13. [13] Leow, C.Y., Willis, C., Hofmann, A., Jones, M.K., Structure–function analysis of apical membrane-associated molecules of the tegument of schistosome parasites of humans: prospects for identification of novel targets for parasite control. Br. J. Pharmacol. 172 (2015), 1653–1663.
14. [14] Kruger, F.J., Wolmarans, C.T., Host cellular components adhering to the tegument of schistosomes from cattle, buffalo, hippopotamus and lechwe. Onderstepoort J. Vet. Res. 57 (1990), 137–139.
15. [15] Dean, D.A., Decreased binding of cytotoxic antibody by developing Schistosoma mansoni. Evidence for a surface change independent of host antigen adsorption and membrane turnover. J. Parasitol. 63 (1977), 418–426.
16. [16] Lawson, B.W., Bickle, Q.D., Taylor, M.G., Mechanisms involved in the loss of antibody-mediated adherence of macrophages to lung-stage schistosomula of Schistosoma mansoni in vitro. Parasitology 106 (1993), 463–469.
17. [17] Abath, F.G., Werkhauser, R.C., The tegument of Schistosoma mansoni: functional and immunological features. Parasite Immunol. 18 (1996), 15–20.
18. [18] Pearce, E.J., James, S.L., Post lung-stage schistosomula of Schistosoma mansoni exhibit transient susceptibility to macrophage-mediated cytotoxicity in vitro that may relate to late phase killing in vivo. Parasite Immunol. 8 (1986), 513–527.
19. [19] Pearce, E.J., Basch, D.P., Sher, A., Evidence that the reduced surface antigenicity of developing Schistosoma mansoni schistosomula is due to antigen shedding rather than host molecule acquisition. Parasite Immunol. 8 (1986), 79–94.
20. [20] Dessein, A., Samuelson, J.C., Butterworth, A.E., Hogan, M., Sherry, B.A., Vadas, M.A., David, J.R., Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82 (1981), 357–374.
21. [21] Foley, M., Kusel, J.R., Garland, P.B., Fluorescence recovery after photobleaching: applications to parasite surface membranes. Parasitol. Today 2 (1986), 318–320.
22. [22] Foley, M., Kusel, J.R., Garland, P.B., Changes in the organization of the surface membrane upon transformation of cercariae to schistosomula of the helminth parasite Schistosoma mansoni. Parasitology 96 (1988), 85–97.
23. [23] Foley, M., MacGregor, A.N., Kusel, J.R., Garland, P.B., Downie, T., Moore, I., The lateral diffusion of lipid probes in the surface membrane of Schistosoma mansoni. J. Cell Biol. 103 (1986), 807–818.
24. [24] Kusel, J.R., Gordon, J.F., Biophysical studies of the schistosome surface and their relevance to its properties under immune and drug attack. Parasite Immunol. 11 (1989), 431–451.
25. [25] Furlong, S.T., Caulfield, J.P., Schistosoma mansoni: synthesis and release of phospholipids, lysophospholipids, and neutral lipids by schistosomula. Exp. Parasitol. 69 (1989), 65–77.
26. [26] Furlong, S.T., Thibault, K.S., Morbelli, L.M., Quinn, J.J., Rogers, R.A., Uptake and compartmentalization of fluorescent lipid analogs in larval Schistosoma mansoni. J. Lipid Res. 36 (1995), 1–12.
27. [27] Brouwers, J.F., Smeenk, I.M., van Golde, L.M., Tielens, A.G., The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni. Mol. Biochem. Parasitol. 88 (1997), 175–185.
28. [28] Retra, K., deWalick, S., Schmitz, M., Yazdanbakhsh, M., Tielens, A.G., Brouwers, J.F., Hellemond, J.J.van, The tegumental surface membranes of Schistosoma mansoni are enriched in parasite-specific phospholipid species. Int. J. Parasitol. 45 (2015), 629–636.
29. [29] El Ridi, R., Mohamed, S.H., Tallima, H., Incubation of Schistosoma mansoni lung-stage schistosomula in corn oil exposes their surface membrane antigenic specificities. J. Parasitol. 89 (2003), 1064–1067.
30. [30] Simons, K., Ikonen, E., How cells handle cholesterol. Science 290 (2000), 1721–1726.
31. [31] Allan, D., Payares, G., Evans, W.H., The phospholipid and fatty acid composition of Schistosoma mansoni and of its purified tegumental membrane. Mol. Biochem. Parasitol. 23 (1987), 123–128.
32. [32] de Meyer, F., Smit, B., Effect of cholesterol on the structure of a phospholipid bilayer. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 3654–3658.
33. [33] Krause, M.R., Regen, S.L., The structural role of cholesterol in cell membranes: from condensed bilayers to lipid rafts. Acc. Chem. Res. 47 (2014), 3512–3521.
34. [34] Mahammad, S., Parmryd, I., Cholesterol depletion using methyl-β-cyclodextrin. Methods Mol. Biol. 1232 (2015), 91–102.
35. [35] Castanho, M.A., Coutinho, A., Prieto, M.J., Absorption and fluorescence spectra of polyene antibiotics in the presence of cholesterol. J. Biol. Chem. 267 (1992), 204–209.
36. [36] Muller, C.P., Stephany, D.A., Winkler, D.F., Hoeg, J.M., Demosky, S.J. Jr., Wunderlich, J.R., Filipin as a flow microfluorometry probe for cellular cholesterol. Cytometry 5 (1984), 42–54.
37. [37] El Ridi, R., Tallima, H., Mohamed, S.H., Montash, M., Depletion of Schistosoma mansoni lung-stage schistosomula cholesterol by methyl-beta-cyclodextrin dramatically increases specific antibody binding to surface membrane antigens. J. Parasitol. 90 (2004), 727–732.
38. [38] Tallima, H., El Ridi, R., Methyl-beta-cyclodextrin treatment and filipin staining reveal the role of cholesterol in surface membrane antigen sequestration of Schistosoma mansoni and S. haematobium lung-stage larvae. J. Parasitol. 91 (2005), 720–725.
39. [39] Tallima, H., Hamada, M., El Ridi, R., Evaluation of cholesterol content and impact on antigen exposure in the outer lipid bilayer of adult schistosomes. Parasitology 134 (2007), 1775–1783.
40. [40] Bernardo, K., Krut, O., Wiegmann, K., Kreder, D., Micheli, M., Schäfer, R., Sickman, A., Schmidt, W.E., Schröder, J.M., Meyer, H.E., Sandhoff, K., Krönke, M., Purification and characterization of a magnesium-dependent neutral sphingomyelinase from bovine brain. J. Biol. Chem. 275 (2000), 7641–7647.
41. [41] Huwiler, A., Kolter, T., Pfeilschifter, J., Sandhoff, K., Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta 1485 (2000), 63–99.
42. [42] Worgall, T.S., Johnson, R.A., Seo, T., Gierens, H., Deckelbaum, R.J., Unsaturated fatty acid-mediated decreases in sterol regulatory element-mediated gene transcription are linked to cellular sphingolipid metabolism. J. Biol. Chem. 277 (2002), 3878–3885.
43. [43] Tallima, H., Salah, M., El Ridi, R., In vitro and in vivo effects of unsaturated fatty acids on Schistosoma mansoni and S. haematobium lung-stage larvae. J. Parasitol. 91 (2005), 1094–1102.
44. [44] El Ridi, R., Tallima, H., Equilibrium in lung schistosomula sphingomyelin breakdown and biosynthesis allows very small molecules, but not antibody, to access proteins at the host–parasite interface. J. Parasitol. 92 (2006), 730–737.
45. [45] Puchtler, H., Meloan, S.N., On the chemistry of formaldehyde fixation and its effects on immunohistochemical reactions. Histochemistry 82 (1985), 201–204.
46. [46] Kiernan, J.A., Formaldehyde, formalin, paraformaldehyde and glutaraldehyde: what they are and what they do. Microbiol. Today 8 (2000), 8–12.
47. [47] Arenz, C., Thutewohl, M., Block, O., Waldmann, H., Altenbach, H.J., Giannis, A., Manumycin a and its analogues are irreversible inhibitors of neutral sphingomyelinase. Chembiochem 2 (2001), 141–143.
48. [48] Clarke, C.J., Hannun, Y.A., Neutral sphingomyelinases and nSMase2: bridging the gaps. Biochim. Biophys. Acta 1758 (2006), 1893–1901.
49. [49] Gault, C.R., Obeid, L.M., Hannun, Y.A., An overview of sphingolipid metabolism: from synthesis to breakdown. Adv. Exp. Med. Biol. 688 (2010), 1–23.
50. [50] Mombelli, E., Morris, R., Taylor, W., Fraternali, F., Hydrogen-bonding propensities of sphingomyelin in solution and in a bilayer assembly: a molecular dynamics study. Biophys. J. 84 (2003), 1507–1517.
51. [51] Oborina, E.M., Yappert, M.C., Effect of sphingomyelin versus dipalmitoyl phosphatidylcholine on the extent of lipid oxidation. Chem. Phys. Lipids 123 (2003), 223–232.
52. [52] Migliardo, F., Tallima, H., El Ridi, R., Rigidity and resistance of larval- and adult schistosomes-medium interface. Biochem. Biophys. Res. Commun. 446 (2014), 255–260.
53. [53] Migliardo, F., Tallima, H., El Ridi, R., Is there a sphingomyelin-based hydrogen bond barrier at the mammalian host-schistosome parasite interface?. Cell Biochem. Biophys. 68 (2014), 359–367.
54. [54] Volino, F., Dianoux, A.J., Organic liquids. Structures Dynamics and Chemical Properties, 1978, John Wiley and Sons Ltd, New York.
55. [55] Yoshimura, S., Banno, Y., Nakashima, S., Hayashi, K., Yamakawa, H., Sawada, M., et al. Inhibition of neutral sphingomyelinase activation and ceramide formation by glutathione in hypoxic PC12 cell death. J. Neurochem. 73 (1999), 675–683.
56. [56] Berriman, M., Haas, B.J., LoVerde, P.T., et al. The genome of the blood fluke Schistosoma mansoni. Nature 460 (2009), 352–358.
57. [57] Tallima, H., Al-Halbosiy, M.F., El Ridi, R., Enzymatic activity and immunolocalization of Schistosoma mansoni and Schistosoma haematobium neutral sphingomyelinase. Mol. Biochem. Parasitol. 178 (2011), 23–28.
58. [58] El Ridi, R., Tallima, H., Solving the riddle of the lung-stage schistosomula paved the way to a novel remedy and an efficacious vaccine for schistosomiasis. El Ridi, Rashika, (eds.) Parasitic Diseases — Schistosomiasis, 2013, 179–202 (http://www.intechopen.com/books/parasitic-diseases-schistosomiasis/solving-the-riddle-of-the-lung-stage-schistosomula-paved-the-way-to-a-novel-remedy-and-an-efficaciou).
59. [59] Young, N.D., Jex, A.R., Li, B., et al. Whole-genome sequence of Schistosoma haematobium. Nat. Genet. 44 (2012), 221–225.
60. [60] El Ridi, R., Aboueldahab, M., Tallima, H., Salah, M., Mahana, N., Fawzi, S., Mohamed, S.H., Fahmy, O.M., In vitro and in vivo activities of arachidonic acid against Schistosoma mansoni and Schistosoma haematobium. Antimicrob. Agents Chemother. 54 (2010), 3383–3389.
61. [61] El Ridi, R., Tallima, H., Salah, M., Aboueldahab, M., Fahmy, O.M., Halbosiy, M.F., Mahmoud, S.S., Efficacy and mechanism of action of arachidonic acid in the treatment of hamsters infected with Schistosoma mansoni or Schistosoma haematobium. Int. J. Antimicrob. Agents 39 (2012), 232–239.
62. [62] Tallima, H., Hadley, K., El Ridi, R., Praziquantel and arachidonic acid combination — an innovative approach to the treatment of schistosomiasis. Amidou, S., (eds.) An Overview of Tropical Diseases, 2015, InTech, Croatia, 145–172 ( http://www.intechopen.com/books/an-overview-of-tropical-diseases/praziquantel-and-arachidonic-acid-combination-an-innovative-approach-to-the-treatment-of-schistosomi).
63. [63] Selim, S., El Sagheer, O., El Amir, A., Barakat, R., Hadley, K., Bruins, M.J., El Ridi, R., Efficacy and safety of arachidonic acid for treatment of Schistosoma mansoni-infected children in Menoufiya, Egypt. Am.J.Trop. Med. Hyg. 91 (2014), 973–981.
64. [64] Barakat, R., Abou El-Ela, N.E., Sharaf, S., El Sagheer, O., Selim, S., Tallima, H., Bruins, M.J., Hadley, K.B., El Ridi, R., Efficacy and safety of arachidonic acid for treatment of school-age children in Schistosoma mansoni high-endemicity regions. Am.J.Trop. Med. Hyg. 92 (2015), 797–804.
65. [65] William, S., Botros, S., Ismail, M., Farghally, A., Day, T.A., Bennett, J.L., Praziquantel-induced tegumental damage in vitro is diminished in schistosomes derived from praziquantel-resistant infections. Parasitology 122 (2001), 63–66.
66. [66] Wu, M., Harvey, K.A., Ruzmetov, N., Welch, Z.R., Sech, L., Jackson, K., Stillwell, W., Zaloga, G.P., Siddiqui, R.A., Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway. Int. J. Cancer 117 (2005), 340–348.
67. [67] Mondal, S., Mandal, C., Sangwan, R., Chandra, S., Mandal, C., Withanolide D induces apoptosis in leukemia by targeting the activation of neutral sphingomyelinase-ceramide cascade mediated by synergistic activation of c-Jun N-terminal kinase and p38 mitogen-activated protein kinase. Mol. Cancer, 9, 2010, 239.
68. [68] Mondal, S., Roy, S., Maity, R., Mallick, A., Sangwan, R., Misra-Bhattacharya, S., Mandal, C., Withanolide D, carrying the baton of Indian rasayana herb as a lead candidate of antileukemic agent in modern medicine. Adv. Exp. Med. Biol. 749 (2012), 295–312.
69. [69] Park, B., Lee, Y.M., Kim, J.S., Her, Y., Kang, J.H., Oh, S.H., Kim, H.M., Neutral sphingomyelinase 2 modulates cytotoxic effects of protopanaxadiol on different human cancer cells. BMC Complement. Altern. Med., 13, 2013, 194.
70. [70] Shakor, A.B., Atia, M., Ismail, I.A., Alshehri, A., El-Refaey, H., Kwiatkowska, K., Sobota, A., Curcumin induces apoptosis of multidrug-resistant human leukemia HL60 cells by complex pathways leading to ceramide accumulation. Biochim. Biophys. Acta 2014 (1841), 1672–1682.
71. [71] Tseng, T.H., Shen, C.H., Huang, W.S., Chen, C.N., Liang, W.H., Lin, T.H., Kuo, H.C., Activation of neutral-sphingomyelinase, MAPKs, and p75 NTR-mediating caffeic acid phenethyl ester-induced apoptosis in C6 glioma cells. J. Biomed. Sci., 21, 2014, 61.
72. [72] Truman, J.P., García-Barros, M., Obeid, L.M., Hannun, Y.A., Evolving concepts in cancer therapy through targeting sphingolipid metabolism. Biochim. Biophys. Acta 1841 (2014), 1174–1188.
73. [73] Romero-Ramírez, L., García-Álvarez, I., Casas, J., Barreda-Manso, M.A., Yanguas-Casás, N., Nieto-Sampedro, M., Fernández-Mayoralas, A., New oleyl glycoside as anti-cancer agent that targets on neutral sphingomyelinase. Biochem. Pharmacol. 97 (2015), 158–172.
74. [74] Ganley-Leal, L.M., Guarner, J., Todd, C.W., Da'Dara, A.A., Freeman, G.L. Jr., Boyer, A.E., Harn, D.A., Secor, W.E., Comparison of Schistosoma mansoni irradiated cercariae and Sm23 DNA vaccines. Parasite Immunol. 27 (2005), 341–349.
75. [75] Pearson, M.S., Pickering, D.A., McSorley, H.J., Bethony, J.M., Tribolet, L., Dougall, A.M., Hotez, P.J., Loukas, A., Enhanced protective efficacy of a chimeric form of the schistosomiasis vaccine antigen Sm-TSP-2. PLoS Negl. Trop. Dis., 6, 2012, e1564.
76. [76] Pinheiro, C.S., Ribeiro, A.P., Cardoso, F.C., Martins, V.P., Figueiredo, B.C., Assis, N.R., Morais, S.B., Caliari, M.V., Loukas, A., Oliveira, S.C., A multivalent chimeric vaccine composed of Schistosoma mansoni SmTSP-2 and Sm29 was able to induce protection against infection in mice. Parasite Immunol. 36 (2014), 303–312.
77. [77] Stephenson, R., You, H., McManus, D.P., Toth, I., Schistosome vaccine adjuvants in preclinical and clinical research. Vaccines (Basel) 2 (2014), 654–685.
78. [78] Sotillo, J., Pearson, M., Potriquet, J., Becker, L., Pickering, D., Mulvenna, J., Loukas, A., Extracellular vesicles secreted by Schistosoma mansoni contain protein vaccine candidates. Int. J. Parasitol. 46 (2016), 1–5.
79. [79] 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., Dalton, J.P., Robinson, M.W., The extracellular vesicles of the helminth pathogen, Fasciola hepatica: biogenesis pathways and cargo molecules involved in parasite pathogenesis. Mol. Cell. Proteomics 14 (2015), 3258–3273.
80. [80] Knudsen, G.M., Medzihradszky, K.F., Lim, K.C., Hansell, E., McKerrow, J.H., Proteomic analysis of Schistosoma mansoni cercarial secretions. Mol. Cell. Proteomics 4 (2005), 1862–1875.
81. [81] Curwen, R.S., Ashton, P.D., Sundaralingam, S., Wilson, R.A., Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Mol. Cell. Proteomics 5 (2006), 835–844.
82. [82] El Ridi, R., Tallima, H., Schistosoma mansoni ex vivo lung-stage larvae excretory-secretory antigens as vaccine candidates against schistosomiasis. Vaccine 27 (2009), 666–673.
83. [83] Riveau, G., Deplanque, D., Remoué, F., Schacht, A.M., Vodougnon, H., Capron, M., Thiry, M., Martial, J., Libersa, C., Capron, A., Safety and immunogenicity of rSh28GST antigen in humans: phase 1 randomized clinical study of a vaccine candidate against urinary schistosomiasis. PLoS Negl. Trop. Dis., 6, 2012, e1704.
84. [84] Tendler, M., Almeida, M., Simpson, A., Development of the Brazilian anti schistosomiasis vaccine based on the recombinant fatty acid binding protein Sm14 plus GLA-SE adjuvant. Front. Immunol., 6, 2015, 218.
85. [85] Molehin, A.J., Rojo, J.U., Siddiqui, S.Z., Gray, S.A., Carter, D., Siddiqui, A.A., Development of a schistosomiasis vaccine. Expert Rev. Vaccines, 2015 (in press).
86. [86] Tallima, H., El Ridi, R., Schistosoma mansoni glyceraldehyde 3-phosphate dehydrogenase is a lung-stage schistosomula surface membrane antigen. Folia Parasitol. 55 (2008), 180–186.
87. [87] El Ridi, R., Othman, A.A., McManus, D.P., Editorial: the schistosomiasis vaccine — it is time to stand up. Front. Immunol., 6, 2015, 390.