Insulin growth factor inhibitor as a potential new anti-schistosoma drug: An in vivo experimental study

Gryseels, 2006, Human schistosomiasis, Lancet, 368, 1106, 10.1016/S0140-6736(06)69440-3 Doenhoff, 2006, Praziquantel for the treatment of schistosomiasis: its use for control in areas with endemic disease and prospects for drug resistance, Expert Rev. Anti Infect. Ther., 4, 199, 10.1586/14787210.4.2.199 DeMarco, 2009, Schistosomes: proteomics studies for potential novel vaccines and drug targets, Drug Discov. Today, 14, 472, 10.1016/j.drudis.2009.01.011 Schacke, 1994, Molecular cloning of a tyrosine kinase gene from the marine sponge Geodia cydonium: a new member belonging to the receptor tyrosine kinase class II family, Mol. Membr. Biol., 11, 101, 10.3109/09687689409162227 Khayath, 2007, Diversification of the insulin receptor family in the helminth parasite Schistosoma mansoni, FEBS J., 274, 659, 10.1111/j.1742-4658.2006.05610.x Skellys, 1994, Cloning, characterization, and functional expression of cDNAs encoding glucose transporter proteins from the human parasite schistosoma mansoni, J. Biol. Chem., 269, 4247, 10.1016/S0021-9258(17)41770-4 You, 2010, Cloning and characterisation of Schistosoma japonicum insulin receptors, PLoS One, 5, 1, 10.1371/journal.pone.0009868 Ahier, 2008, Insulin receptors and glucose uptake in the human parasite Schistosoma mansoni, Parasite, 15, 573, 10.1051/parasite/2008154573 Gouignard, 2012, Schistosoma mansoni: structural and biochemical characterization of two distinct Venus Kinase Receptors, Exp. Parasitol., 132, 32, 10.1016/j.exppara.2011.05.007 Vanderstraete, 2013, Dual targeting of insulin and Venus Kinase Receptors of Schistosoma mansoni for novel anti-schistosome therapy, PLoS Negl. Trop. Dis., 7, 1, 10.1371/journal.pntd.0002226 Liang, 1987, Laboratory cultivation of schistosome vector snails and maintenance of schistosome life cycles, Proceeding 1st Sino-American Symp., 34 Deutsch, 2004, Tyrosine kinase inhibitor AG1024 exerts antileukaemic effects on STI571-resistant Bcr-Abl expressing cells and decreases AKT phosphorylation, Br. J. Cancer, 91, 1735, 10.1038/sj.bjc.6602190 Gonnert, 1977, Praziquantel, a new board-spectrum antischistosomal agent, Z. Parasitenkd., 52, 129, 10.1007/BF00389899 De Oliveira, 2014, Anthelmintic activity in vitro and in vivo of Baccharis trimera (Less) DC against immature and adult worms of Schistosoma mansoni, Exp. Parasitol., 139, 63, 10.1016/j.exppara.2014.02.010 Attallah, 1999, Immunochemical characterization and diagnostic potential of a 63-kilodalton Schistosoma antigen, Am. J. Trop. Med. Hyg., 60, 493, 10.4269/ajtmh.1999.60.493 U. of Minnesota, Euthanasia Guidelines, (2009). http://www.ahc.umn.edu/rar/euthanasia.html. Pellegrino, 1962, New approach to the screening of drugs in experimental Schistosomiasis mansoni in mice, Am. J. Trop. Med. Hyg., 11, 201, 10.4269/ajtmh.1962.11.201 Cheever, 1968, Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues, Bull. World Heal. Organ., 39, 328 Reitman, 1957, A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases, Am. J. Clin. Pathol., 28, 56, 10.1093/ajcp/28.1.56 Von Lichtenberg, 1962, Host response to eggs of S. mansoni. I. Granuloma formation in the unsensitized laboratory mouse, Am. J. Pathol., 41, 711 James, 1990, Sirius red histophotometry and spectrophotometry of sections in the assessment of the collagen content of liver tissue and its application in growing rat liver, Liver, 10, 1, 10.1111/j.1600-0676.1990.tb00428.x Chen, 2013, Liraglutide ameliorates glycometabolism and insulin resistance through the upregulation of GLUT4 in diabetic KKAy mice, Int. J. Mol. Med., 32, 892, 10.3892/ijmm.2013.1453 Qi, 1999, Blockade of type β transforming growth factor signaling prevents liver fibrosis and dysfunction in the rat, Proc. Natl. Acad. Sci. U. S. A., 96, 2345, 10.1073/pnas.96.5.2345 Elshal, 2015, The multi-kinase inhibitor pazopanib targets hepatic stellate cell activation and apoptosis alleviating progression of liver fibrosis, Naunyn. Schmiedebergs Arch. Pharmacol., 1293, 10.1007/s00210-015-1157-7 WHO, Schistosomiasis Factsheet 2015, Updat. January 2017. (n.d.). http://www.who.int/mediacentre/factsheets/fs115/en/ (Accessed 1 January 2017). Mcmanus, 2008, Current status of vaccines for Schistosomiasis, Clin. Microbiol. Rev., 21, 225, 10.1128/CMR.00046-07 Giboda, 1992, Modification of tissue egg load in Schistosomiasis mansoni as a tool for morbidity reduction, Mitt. Österr. Ges. Tropenmed. Parasitol., 14, 89 Levitzki, 2006, Tyrphostins and other tyrosine kinase inhibitors, Annu. Rev. Biochem., 75, 93, 10.1146/annurev.biochem.75.103004.142657 von Willebrand, 2003, The tyrphostin AG1024 accelerates the degradation of phosphorylated forms of retinoblastoma protein (pRb) and restores pRb tumor suppressive function in melanoma cells, Cancer Res., 63, 1420 Camirand, 2005, Inhibition of insulin-like growth factor-1 receptor signaling enhances growth-inhibitory and proapoptotic effects of gefitinib (Iressa) in human breast cancer cells, Breast Cancer Res., 7, 570, 10.1186/bcr1028 Camirand, 2004, Co-targeting IGF-1R and c-kit: synergistic inhibition of proliferation and induction of apoptosis in H 209 small cell lung cancer cells, Br. J. Cancer, 90, 1825, 10.1038/sj.bjc.6601682 Párrizas, 1997, Specific inhibition of insulin-like growth factor-1 and insulin receptor tyrosine kinase activity and biological function by tyrphostins, Endocrinology, 138, 14271433, 10.1210/endo.138.4.5092 Saule, 2005, Host glucose metabolism mediates T4 and IL-7 action on Schistosoma mansoni development, J. Parasitol., 91, 737, 10.1645/GE-3402.1 Thabet, 2008, Decreased basal non-insulin-stimulated glucose uptake by diaphragm in streptozotocin-induced diabetic mice infected with Schistosoma mansoni, Parasitol. Res., 103, 595, 10.1007/s00436-008-1016-2 Hulstijn, 2011, Parasitological and morphological study of Schistosoma mansoni and diabetes mellitus in mice, Exp. Parasitol., 129, 42, 10.1016/j.exppara.2011.05.017 You, 2012, The insulin receptor is a transmission blocking veterinary vaccine target for zoonotic Schistosoma japonicum, Int. J. Parasitol., 42, 801, 10.1016/j.ijpara.2012.06.002 El-Lakkany, 2012, Anti-inflammatory/anti-fibrotic effects of the hepatoprotective silymarin and the schistosomicide praziquantel against Schistosoma mansoni-induced liver fibrosis, Parasite Vectors, 5, 9, 10.1186/1756-3305-5-9 Vicogne, 2003, An unusual receptor tyrosine kinase of Schistosoma mansoni contains a Venus flytrap module, Mol. Biochem. Parasitol., 126, 51, 10.1016/S0166-6851(02)00249-9 Ahier, 2009, A new family of receptor tyrosine kinases with a venus flytrap binding domain in insects and other invertebrates activated by aminoacids, PLoS One, 4, e5651, 10.1371/journal.pone.0005651 Vanderstraete, 2014, Venus kinase receptors control reproduction in the platyhelminth parasite schistosoma mansoni, PLoS Pathog., 10, 1005798, 10.1371/journal.ppat.1004138 You, 2015, Suppression of the insulin receptors in adult Schistosoma japonicum impacts on parasite growth and development: further evidence of vaccine potential, PLoS Negl. Trop. Dis., 9, 10.1371/journal.pntd.0003730 Hulstijn, 2001, Lower faecal egg excretion in chemically-induced diabetic mice infected with schistosoma mansoni due to impaired egg maturation, Mem Inst Oswaldo Cruz, Rio Janeiro, 96, 393, 10.1590/S0074-02762001000300020 Hulstijn, 2003, Morphological changes in the reproductive organs of male and female Schistosoma mansoni worms caused by streptozotocin, a drug used to induce diabetes mellitus, Parasitology, 126, 53, 10.1017/S0031182002002512 Giboda, 1994, Schistosoma mansoni eggs as a target for praziquantel: efficacy of oral application in mice, J. Trop. Med. Hyg., 97, 98 Mduluza, 2001, The impact of repeated treatment with praziquantel of schistosomiasis in children under six years of age living in an endemic area for schistosoma haematobium infection, Mem. Inst. Oswaldo Cruz Rio Janeiro, 96, 157, 10.1590/S0074-02762001000900024 Doenhoff, 2008, Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis, Curr. Opin. Infect. Dis., 21, 659, 10.1097/QCO.0b013e328318978f Wu, 2011, New insight into praziquantel against various developmental stages of schistosomes, Parasitol. Res., 109, 1501, 10.1007/s00436-011-2670-3 Liang, 2011, New insight into the antifibrotic effects of praziquantel on mice in infection with schistosoma japonicum, PLoS One, 6, 10.1371/journal.pone.0020247 Sabah, 1986, Schistosoma mansoni: chemotherapy of infections of different ages, Exp. Parasitol., 61, 294, 10.1016/0014-4894(86)90184-0 Pica-Mattoccia, 2004, Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment, Int. J. Parasitol., 34, 527, 10.1016/j.ijpara.2003.12.003 Doenhoff, 2009, Praziquantel: its use in control of schistosomiasis in sub Saharan Africa and current research needs, Parasitology, 136, 1825, 10.1017/S0031182009000493 Blum, 2000, Substrate competitive inhibitors of IGF-1 receptor kinase, Biochemistry, 39, 15705, 10.1021/bi001516y Shaheen, 1989, Effect of praziquantel on some aspect of carbohydrate metabolism in mice infected with Schistosoma mansoni, Pharmacol. Res., 21, 263, 10.1016/S1043-6618(89)80004-0 Zaccone, 2003, Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes, Eur. J. Immunol., 33, 1439, 10.1002/eji.200323910 Zaccone, 2009, Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice, Eur. J. Immunol., 39, 1098, 10.1002/eji.200838871 Chen, 2013, Association of previous schistosome infection with diabetes and metabolic syndrome: a cross-sectional study in rural China, J. Clin. Endocrinol. Metab., 98, 283, 10.1210/jc.2012-2517 Shen, 2015, The potential long-term effect of previous schistosome infection reduces the risk of metabolic syndrome among Chinese men, Parasite Imunol., 37, 333, 10.1111/pim.12187 Gelmedin, 2015, Re-positioning protein-kinase inhibitors against schistosomiasis, Futur. Med. Chem., 7, 737, 10.4155/fmc.15.31 Andrade, 2009, Schistosomiasis and liver fibrosis, Parasite Immunol., 31, 656, 10.1111/j.1365-3024.2009.01157.x Burke, 2009, Immunopathogenesis of human schistosomiasis, Parasite Immunol., 31, 163, 10.1111/j.1365-3024.2009.01098.x Wilson, 2007, Immunopathology of schistosomiasis, Immunol. Cell Biol., 85, 148, 10.1038/sj.icb.7100014 Farah, 2000, Repeated exposure induces periportal fibrosis in Schistosoma mansoni-infected baboons: role of TGF-beta and IL-4, J. Immunol., 164, 5337, 10.4049/jimmunol.164.10.5337 Gressner, 2006, Modern pathogenetic concepts of liver fibrosis suggest stellate cells and TGF-β as major players and therapeutic targets, J. Cell. Mol. Med., 10, 76, 10.1111/j.1582-4934.2006.tb00292.x Morcos, 1985, Reversal of hepatic fibrosis after praziquantel therapy of murine schistosomiasis, Am. J. Trop. Med. Hyg., 34, 314, 10.4269/ajtmh.1985.34.314 Frenzel, 1999, Evidence for a long-term effect of a single dose of praziquantel on Schistosoma mansoni-induced hepatosplenic lesions in northern Uganda, Am. J. Trop. Med. Hyg., 60, 927, 10.4269/ajtmh.1999.60.927 Berhe, 2008, Reversibility of schistosomal periportal thickening/fibrosis after praziquantel therapy: a twenty-six month follow-up study in Ethiopia, Am. J. Trop. Med. Hyg., 78, 228, 10.4269/ajtmh.2008.78.228