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Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Review Article

Unveiling the Potential of Purinergic Signaling in Schistosomiasis Treatment

Author(s): Nathália Ferreira Oliveira and Claudia Lucia Martins Silva*

Volume 21, Issue 3, 2021

Published on: 24 September, 2020

Page: [193 - 204] Pages: 12

DOI: 10.2174/1568026620666200924115113

Price: $65

Abstract

Schistosomiasis is a neglected tropical disease. It is related to long-lasting granulomatous fibrosis and inflammation of target organs, and current sub-optimal pharmacological treatment creates global public health concerns. Intravascular worms and eggs release antigens and extracellular vesicles that target host endothelial cells, modulate the immune system, and stimulate the release of damageassociated molecular patterns (DAMPs). ATP, one of the most studied DAMPs, triggers a cascade of autocrine and paracrine actions through purinergic P2X and P2Y receptors, which are shaped by ectonucleotidases (CD39). Both P2 receptor families, and in particular P2Y1, P2Y2, P2Y12, and P2X7 receptors, have been attracting increasing interest in several inflammatory diseases and drug development. Current data obtained from the murine model unveiled a CD39-ADP-P2Y1/P2Y12 receptors signaling pathway linked to the liver and mesenteric exacerbations of schistosomal inflammation. Therefore, we proposed that members of this purinergic signaling could be putative pharmacological targets to reduce schistosomal morbidity.

Keywords: Purinergic signaling, Schistosomiasis, Endothelial cell, Inflammation, Macrophage, Microbiome, Extracellular vesicle, ATP, P2Y receptor.

Graphical Abstract

[1]
McManus, D.P.; Dunne, D.W.; Sacko, M.; Utzinger, J.; Vennervald, B.J.; Zhou, X-N. Schistosomiasis. Nat. Rev. Dis. Primers, 2018, 4(1), 13.
[http://dx.doi.org/10.1038/s41572-018-0013-8] [PMID: 30093684]
[2]
Butrous, G. Schistosome infection and its effect on pulmonary circulation. Glob. Cardiol. Sci. Pract., 2019, 2019(1), 5.
[http://dx.doi.org/10.21542/gcsp.2019.5] [PMID: 31024947]
[3]
World Health Organization (WHO). http://www.who.int/schistosomiasis/en/2020
[4]
Osakunor, D.N.M.; Woolhouse, M.E.J.; Mutapi, F. Paediatric schistosomiasis: What we know and what we need to know. PLoS Negl. Trop. Dis., 2018, 12(2)e0006144
[http://dx.doi.org/10.1371/journal.pntd.0006144] [PMID: 29420537]
[5]
King, C.H. Health metrics for helminth infections. Acta Trop., 2015, 141(Pt B), 150-160.
[http://dx.doi.org/10.1016/j.actatropica.2013.12.001] [PMID: 24333545]
[6]
Mutapi, F.; Maizels, R.; Fenwick, A.; Woolhouse, M. Human schistosomiasis in the post mass drug administration era. Lancet Infect. Dis., 2017, 17(2), e42-e48.
[http://dx.doi.org/10.1016/S1473-3099(16)30475-3] [PMID: 27988094]
[7]
Boissier, J.; Moné, H.; Mitta, G.; Bargues, M.D.; Molyneux, D.; Mas-Coma, S. Schistosomiasis reaches Europe. Lancet Infect. Dis., 2015, 15(7), 757-758.
[http://dx.doi.org/10.1016/S1473-3099(15)00084-5] [PMID: 26122434]
[8]
Gryseels, B.; Polman, K.; Clerinx, J.; Kestens, L. Human schistosomiasis. Lancet, 2006, 368(9541), 1106-1118.
[http://dx.doi.org/10.1016/S0140-6736(06)69440-3] [PMID: 16997665]
[9]
Colley, D.G.; Secor, W.E. Immunology of human schistosomiasis. Parasite Immunol., 2014, 36(8), 347-357.
[http://dx.doi.org/10.1111/pim.12087] [PMID: 25142505]
[10]
Pearce, E.J.; MacDonald, A.S. The immunobiology of schistosomiasis. Nat. Rev. Immunol., 2002, 2(7), 499-511.
[http://dx.doi.org/10.1038/nri843] [PMID: 12094224]
[11]
Barsoum, R.S.; Esmat, G.; El-Baz, T. Human schistosomiasis: clinical perspective: review J. Adv. Res., 2013, 4(5), 433-444.
[http://dx.doi.org/10.1016/j.jare.2013.01.005] [PMID: 25685450]
[12]
Barrenho, E.; Miraldo, M.; Smith, P.C. Does global drug innovation correspond to burden of disease? The neglected diseases in developed and developing countries. Health Econ., 2019, 28(1), 123-143.
[http://dx.doi.org/10.1002/hec.3833] [PMID: 30417950]
[13]
Melman, S.D.; Steinauer, M.L.; Cunningham, C.; Kubatko, L.S.; Mwangi, I.N.; Wynn, N.B.; Mutuku, M.W.; Karanja, D.M.S.; Colley, D.G.; Black, C.L.B.; Secor, W.E.; Mkoji, G.M.; Loker, E.S. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl. Trop. Dis., 2009, 3(8)e504
[http://dx.doi.org/10.1371/journal.pntd.0000504] [PMID: 19688043]
[14]
Thomas, C.M.; Timson, D.J. The mechanism of action of praziquantel: six hypotheses. Curr. Top. Med. Chem., 2018, 18(18), 1575-1584.
[http://dx.doi.org/10.2174/1568026618666181029143214] [PMID: 30370849]
[15]
Masimirembwa, C.M.; Hasler, J.A. Characterisation of praziquantel metabolism by rat liver microsomes using cytochrome P450 inhibitors. Biochem. Pharmacol., 1994, 48(9), 1779-1783.
[http://dx.doi.org/10.1016/0006-2952(94)90464-2] [PMID: 7980647]
[16]
Rajman, I.; Knapp, L.; Morgan, T.; Masimirembwa, C. African genetic diversity: implications for cytochrome P450-mediated drug metabolism and drug development. EBioMedicine, 2017, 17, 67-74.
[http://dx.doi.org/10.1016/j.ebiom.2017.02.017] [PMID: 28237373]
[17]
Burnstock, G. The therapeutic potential of purinergic signalling. Biochem. Pharmacol., 2018, 151, 157-165.
[http://dx.doi.org/10.1016/j.bcp.2017.07.016] [PMID: 28735873]
[18]
Jacobson, K.A.; Boeynaems, J.M. P2Y nucleotide receptors: promise of therapeutic applications. Drug Discov. Today, 2010, 15(13-14), 570-578.
[http://dx.doi.org/10.1016/j.drudis.2010.05.011] [PMID: 20594935]
[19]
Burnstock, G.; Verkhratsky, A. Evolutionary origins of the purinergic signalling system. Acta Physiol, (Oxf), 2009, 195, 415-447.
[http://dx.doi.org/10.1111/j.1748-1716.2009.01957.x]
[20]
Verkhratsky, A.; Burnstock, G. Biology of purinergic signalling: its ancient evolutionary roots, its omnipresence and its multiple functional significance. BioEssays, 2014, 36(7), 697-705.
[http://dx.doi.org/10.1002/bies.201400024] [PMID: 24782352]
[21]
Burnstock, G. Purinergic signalling: from discovery to current developments. Exp. Physiol., 2014, 99(1), 16-34.
[http://dx.doi.org/10.1113/expphysiol.2013.071951] [PMID: 24078669]
[22]
Burnstock, G. Purinoceptors: ontogeny and phylogeny. Drug Dev. Res., 1996, 39, 204-242.
[http://dx.doi.org/10.1002/(SICI)1098-2299(199611/12)39:3/4<204::AID-DDR2>3.0.CO;2-V]
[23]
Berriman, M.; Haas, B.J.; LoVerde, P.T.; Wilson, R.A.; Dillon, G.P.; Cerqueira, G.C.; Mashiyama, S.T.; Al-Lazikani, B.; Andrade, L.F.; Ashton, P.D.; Aslett, M.A.; Bartholomeu, D.C.; Blandin, G.; Caffrey, C.R.; Coghlan, A.; Coulson, R.; Day, T.A.; Delcher, A.; DeMarco, R.; Djikeng, A.; Eyre, T.; Gamble, J.A.; Ghedin, E.; Gu, Y.; Hertz-Fowler, C.; Hirai, H.; Hirai, Y.; Houston, R.; Ivens, A.; Johnston, D.A.; Lacerda, D.; Macedo, C.D.; McVeigh, P.; Ning, Z.; Oliveira, G.; Overington, J.P.; Parkhill, J.; Pertea, M.; Pierce, R.J.; Protasio, A.V.; Quail, M.A.; Rajandream, M.A.; Rogers, J.; Sajid, M.; Salzberg, S.L.; Stanke, M.; Tivey, A.R.; White, O.; Williams, D.L.; Wortman, J.; Wu, W.; Zamanian, M.; Zerlotini, A.; Fraser-Liggett, C.M.; Barrell, B.G.; El-Sayed, N.M. The genome of the blood fluke Schistosoma mansoni. Nature, 2009, 460(7253), 352-358.
[http://dx.doi.org/10.1038/nature08160] [PMID: 19606141]
[24]
Zhou, Y.; Zheng, H.; Chen, Y.; Zhang, L.; Wang, K.; Guo, J.; Huang, Z. The schistosoma japonicum genome sequencing and functional analysis consortium. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature, 2009, 460, 345-351.
[http://dx.doi.org/10.1038/nature08140]
[25]
Young, N.D.; Jex, A.R.; Li, B.; Liu, S.; Yang, L.; Xiong, Z.; Li, Y.; Cantacessi, C.; Hall, R.S.; Xu, X.; Chen, F.; Wu, X.; Zerlotini, A.; Oliveira, G.; Hofmann, A.; Zhang, G.; Fang, X.; Kang, Y.; Campbell, B.E.; Loukas, A.; Ranganathan, S.; Rollinson, D.; Rinaldi, G.; Brindley, P.J.; Yang, H.; Wang, J.; Wang, J.; Gasser, R.B. Whole-genome sequence of Schistosoma haematobium. Nat. Genet., 2012, 44(2), 221-225.
[http://dx.doi.org/10.1038/ng.1065] [PMID: 22246508]
[26]
Silva, L.L.; Marcet-Houben, M.; Nahum, L.A.; Zerlotini, A.; Gabaldón, T.; Oliveira, G. The Schistosoma mansoni phylome: using evolutionary genomics to gain insight into a parasite’s biology. BMC Genomics, 2012, 13, 617.
[http://dx.doi.org/10.1186/1471-2164-13-617] [PMID: 23148687]
[27]
Zerlotini, A.; Aguiar, E.R.; Yu, F.; Xu, H.; Li, Y.; Young, N.D.; Gasser, R.B.; Protasio, A.V.; Berriman, M.; Roos, D.S.; Kissinger, J.C.; Oliveira, G. SchistoDB: an updated genome resource for the three key schistosomes of humans. Nucleic Acids Res., 2013, 41(Database issue), D728-D731.
[PMID: 23161692]
[28]
Ferreira, L.G.; Oliva, G.; Andricopulo, A.D. Target-based molecular modeling strategies for schistosomiasis drug discovery. Future Med. Chem., 2015, 7(6), 753-764.
[http://dx.doi.org/10.4155/fmc.15.21] [PMID: 25996068]
[29]
Serrão, V.H.B.; Pereira, H.D.; de Souza, J.R.T.; Romanello, L. Schistosoma mansoni purine and pyrimidine biosynthesis: structures and kinetic experiments in the search for the best therapeutic target. Curr. Pharm. Des., 2017, 23(45)
[http://dx.doi.org/10.2174/1381612823666171011100532] [PMID: 29022512]
[30]
Senft, A.W.; Crabtree, G.W. Purine metabolism in the schistosomes: potential targets for chemotherapy. Pharmacol. Ther., 1983, 20(3), 341-356.
[http://dx.doi.org/10.1016/0163-7258(83)90031-1] [PMID: 6412258]
[31]
Levy, M.G.; Read, C.P. Relation of tegumentary phosphohydrolase to purine and pyrimidine transport in Schistosoma mansoni. J. Parasitol., 1975, 61(4), 648-656.
[http://dx.doi.org/10.2307/3279457] [PMID: 170394]
[32]
Levy, M.G.; Read, C.P. Purine and pyrimidine transport in Schistosoma mansoni. J. Parasitol., 1975, 61(4), 627-632.
[http://dx.doi.org/10.2307/3279455] [PMID: 1165547]
[33]
Dovey, H.F.; McKerrow, J.H.; Wang, C.C. Action of tubercidin and other adenosine analogs on Schistosoma mansoni schistosomules. Mol. Biochem. Parasitol., 1985, 16(2), 185-198.
[http://dx.doi.org/10.1016/0166-6851(85)90086-6] [PMID: 3929087]
[34]
Bhardwaj, R.; Skelly, P.J. Purinergic signaling and immune modulation at the schistosome surface? Trends Parasitol., 2009, 25(6), 256-260.
[http://dx.doi.org/10.1016/j.pt.2009.03.004] [PMID: 19423396]
[35]
Da’dara, A.A.; Bhardwaj, R.; Skelly, P.J. Schistosome apyrase SmATPDase1, but not SmATPDase2, hydrolyses exogenous ATP and ADP. Purinergic Signal., 2014, 10(4), 573-580.
[http://dx.doi.org/10.1007/s11302-014-9416-5] [PMID: 24894599]
[36]
Elzoheiry, M.; Da’dara, A.A.; deLaforcade, A.M.; El-Beshbishi, S.N.; Skelly, P.J. The essential ectoenzyme SmNPP5 from the human intravascular parasite schistosoma mansoni is an ADPase and a potent inhibitor of platelet aggregation. Thromb. Haemost., 2018, 118(6), 979-989.
[http://dx.doi.org/10.1055/s-0038-1641715] [PMID: 29669386]
[37]
Vasconcelos, E.G.; Nascimento, P.S.; Meirelles, M.N.; Verjovski-Almeida, S.; Ferreira, S.T. Characterization and localization of an ATP-diphosphohydrolase on the external surface of the tegument of Schistosoma mansoni. Mol. Biochem. Parasitol., 1993, 58(2), 205-214.
[http://dx.doi.org/10.1016/0166-6851(93)90042-V] [PMID: 8479445]
[38]
Mendes, R.G.; Gusmão, M.A.; Maia, A.C. Detoni, Mde.L.; Porcino, G.N.; Soares, T.V.; Juliano, M.A.; Juliano, L.; Coelho, P.M.Z.; Lenzi, H.L.; Faria-Pinto, P.; Vasconcelos, E.G. Immunostimulatory property of a synthetic peptide belonging to the soluble ATP diphosphohydrolase isoform (SmATPDase 2) and immunolocalisation of this protein in the Schistosoma mansoni egg. Mem. Inst. Oswaldo Cruz, 2011, 106(7), 808-813.
[http://dx.doi.org/10.1590/S0074-02762011000700005] [PMID: 22124552]
[39]
Maia, A.C.; Detoni, M.L.; Porcino, G.N.; Soares, T.V.; do Nascimento Gusmão, M.A.; Fessel, M.R.; Marques, M.J.; Souza, M.A.; Coelho, P.M.Z.; Estanislau, J.A.G.; da Costa Rocha, M.O.; de Oliveira Santos, M.; Faria-Pinto, P.; Vasconcelos, E.G. Occurrence of a conserved domain in ATP diphosphohydrolases from pathogenic organisms associated to antigenicity in human parasitic diseases. Dev. Comp. Immunol., 2011, 35(10), 1059-1067.
[http://dx.doi.org/10.1016/j.dci.2011.03.026] [PMID: 21527274]
[40]
Oliveira, S.D.; Oliveira, N.F.; Meyer-Fernandes, J.R.; Savio, L.E.; Ornelas, F.G.; Ferreira, Z.S.; Coutinho-Silva, R.; Silva, C.L.M. Increased expression of NTPDases 2 and 3 in mesenteric endothelial cells during schistosomiasis favors leukocyte adhesion through P2Y1 receptors. Vascul. Pharmacol., 2016, 82, 66-72.
[http://dx.doi.org/10.1016/j.vph.2016.02.005] [PMID: 26924460]
[41]
Crabtree, G.W.; Senft, A.W. Pathways of nucleotide metabolism in schistosoma mansoni. V. Adenosine cleavage enzyme and effects of purine analogues on adenosine metabolism in vitro. Biochem. Pharmacol., 1974, 23(3), 649-660.
[http://dx.doi.org/10.1016/0006-2952(74)90630-3] [PMID: 4822748]
[42]
Stegman, R.J.; Senft, A.W.; Brown, P.R.; Parks, R.E., Jr Pathways of nucleotide metabolism in Schistosoma mansoni. IV. Incorporation of adenosine analogs in vitro. Biochem. Pharmacol., 1973, 22(4), 459-468.
[http://dx.doi.org/10.1016/0006-2952(73)90287-6] [PMID: 4691875]
[43]
Romanello, L.; Bachega, J.F.; Cassago, A.; Brandão-Neto, J.; DeMarco, R.; Garratt, R.C.; Pereira, H.D. Adenosine kinase from Schistosoma mansoni: structural basis for the differential incorporation of nucleoside analogues. Acta Crystallogr. D Biol. Crystallogr., 2013, 69(Pt 1), 126-136.
[http://dx.doi.org/10.1107/S0907444912044800] [PMID: 23275171]
[44]
Dovey, H.F.; McKerrow, J.H.; Wang, C.C. Purine salvage in Schistosoma mansoni schistosomules. Mol. Biochem. Parasitol., 1984, 11, 157-167.
[http://dx.doi.org/10.1016/0166-6851(84)90062-8] [PMID: 6431283]
[45]
Senft, A.W.; , Miech; , R.P.; , Brown; , F.R.; , Senft; , D.G. Purine metabolism in Schistosoma mansoni. Int. J. Parasitol., 1972, 2, 249-260.
[http://dx.doi.org/10.1016/0020-7519(72)90013-6]
[46]
Angelucci, F.; Basso, A.; Bellelli, A.; Brunori, M.; Pica Mattoccia, L.; Valle, C. The anti-schistosomal drug praziquantel is an adenosine antagonist. Parasitology, 2007, 134(Pt 9), 1215-1221.
[http://dx.doi.org/10.1017/S0031182007002600] [PMID: 17428352]
[47]
da Silva, S.P.; Noël, F. Time course of the effect of praziquantel on Schistosoma mansoni attachment in vitro: comparison with its effects on worm length and motility. Parasitol. Res., 1995, 81(7), 543-548.
[http://dx.doi.org/10.1007/BF00932019] [PMID: 7479644]
[48]
Kohn, A.B.; Anderson, P.A.; Roberts-Misterly, J.M.; Greenberg, R.M. Schistosome calcium channel beta subunits. Unusual modulatory effects and potential role in the action of the antischistosomal drug praziquantel. J. Biol. Chem., 2001, 276(40), 36873-36876.
[http://dx.doi.org/10.1074/jbc.C100273200] [PMID: 11500482]
[49]
Castilho, M.S.; Postigo, M.P.; Pereira, H.M.; Oliva, G.; Andricopulo, A.D. Structural basis for selective inhibition of purine nucleoside phosphorylase from Schistosoma mansoni: kinetic and structural studies. Bioorg. Med. Chem., 2010, 18(4), 1421-1427.
[http://dx.doi.org/10.1016/j.bmc.2010.01.022] [PMID: 20129792]
[50]
Muller, W.A. Transendothelial migration: unifying principles from the endothelial perspective. Immunol. Rev., 2016, 273(1), 61-75.
[http://dx.doi.org/10.1111/imr.12443] [PMID: 27558328]
[51]
Wilson, R.A. Virulence factors of schistosomes. Microbes Infect., 2012, 14(15), 1442-1450.
[http://dx.doi.org/10.1016/j.micinf.2012.09.001] [PMID: 22982150]
[52]
Schramm, G.; Haas, H. Th2 immune response against Schistosoma mansoni infection. Microbes Infect., 2010, 12(12-13), 881-888.
[http://dx.doi.org/10.1016/j.micinf.2010.06.001] [PMID: 20542135]
[53]
Wilson, R.A.; Coulson, P.S. Immune effector mechanisms against schistosomiasis: looking for a chink in the parasite’s armour. Trends Parasitol., 2009, 25(9), 423-431.
[http://dx.doi.org/10.1016/j.pt.2009.05.011] [PMID: 19717340]
[54]
Jacobs, W.; van Dam, G.; Bogers, J.; Deelder, A.; Van Marck, E. Schistosomal granuloma modulation. I. Schistosoma mansoni worm antigens CAA and CCA prime egg-antigen-induced hepatic granuloma formation. Parasitol. Res., 1999, 85(1), 7-13.
[http://dx.doi.org/10.1007/s004360050499] [PMID: 9950221]
[55]
Cutts, L.; Wilson, R.A. The protein antigens secreted in vivo by adult male Schistosoma mansoni. Parasitology, 1997, 114(Pt 3), 245-255.
[http://dx.doi.org/10.1017/S0031182096008438] [PMID: 9075344]
[56]
Al-Sherbiny, M.; el Ridi, R.; Guirguis, N.I.; Dean, D.A. Identification and characterization of Schistosoma mansoni antigens recognized by T and B lymphocytes of humans with early active intestinal and/or urinary schistosomiasis. Int. J. Parasitol., 1995, 25(1), 113-121.
[http://dx.doi.org/10.1016/0020-7519(94)E0067-W] [PMID: 7541026]
[57]
Silva, C.L.M. Endothelial cells as targets of the intravascular parasitic disease schistosomiasis.Vascular responses to pathogens; Gavins, F.N.E; Stokes, K.Y., Ed.; Eds.; Academic Press: London, 2015, pp. 195-208.
[58]
Maizels, R.M.; Smits, H.H.; McSorley, H.J. Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity, 2018, 49(5), 801-818.
[http://dx.doi.org/10.1016/j.immuni.2018.10.016] [PMID: 30462997]
[59]
Motran, C.C.; Silvane, L.; Chiapello, L.S.; Theumer, M.G.; Ambrosio, L.F.; Volpini, X.; Celias, D.P.; Cervi, L. Cervi1, L. Helminth infections: recognition and modulation of the immune response by innate immune cells. Front. Immunol., 2018, 9, 664.
[http://dx.doi.org/10.3389/fimmu.2018.00664] [PMID: 29670630]
[60]
Hams, E.; Aviello, G.; Fallon, P.G. The schistosoma granuloma: friend or foe? Front. Immunol., 2013, 4, 89.
[http://dx.doi.org/10.3389/fimmu.2013.00089] [PMID: 23596444]
[61]
Dunne, D.W.; Cooke, A. A worm’s eye view of the immune system: consequences for evolution of human autoimmune disease. Nat. Rev. Immunol., 2005, 5(5), 420-426.
[http://dx.doi.org/10.1038/nri1601] [PMID: 15864275]
[62]
Jacobs, W.; Bogers, J.; Deelder, A.; Wéry, M.; Van Marck, E. Adult Schistosoma mansoni worms positively modulate soluble egg antigen-induced inflammatory hepatic granuloma formation in vivo. Stereological analysis and immunophenotyping of extracellular matrix proteins, adhesion molecules, and chemokines. Am. J. Pathol., 1997, 150(6), 2033-2045.
[PMID: 9176396]
[63]
Ritter, M.; Gross, O.; Kays, S.; Ruland, J.; Nimmerjahn, F.; Saijo, S.; Tschopp, J.; Layland, L.E.; Prazeres da Costa, C. Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc. Natl. Acad. Sci. USA, 2010, 107(47), 20459-20464.
[http://dx.doi.org/10.1073/pnas.1010337107] [PMID: 21059925]
[64]
Zerr, M.; Hechler, B.; Freund, M.; Magnenat, S.; Lanois, I.; Cazenave, J-P.; Léon, C.; Gachet, C. Major contribution of the P2Y1receptor in purinergic regulation of TNFα-induced vascular inflammation. Circulation, 2011, 123(21), 2404-2413.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.110.002139] [PMID: 21576651]
[65]
Seye, C.I.; Yu, N.; Jain, R.; Kong, Q.; Minor, T.; Newton, J.; Erb, L.; González, F.A.; Weisman, G.A. The P2Y2 nucleotide receptor mediates UTP-induced vascular cell adhesion molecule-1 expression in coronary artery endothelial cells. J. Biol. Chem., 2003, 278(27), 24960-24965.
[http://dx.doi.org/10.1074/jbc.M301439200] [PMID: 12714597]
[66]
Jacobs, W.; Bogers, J.J.; Timmermans, J.P.; Deelder, A.M.; Van Marck, E.A. Adhesion molecules in intestinal Schistosoma mansoni infection. Parasitol. Res., 1998, 84(4), 276-280.
[http://dx.doi.org/10.1007/s004360050395] [PMID: 9569091]
[67]
Figliuolo da Paz, V.R.; Figueiredo-Vanzan, D.; Dos Santos Pyrrho, A. Interaction and involvement of cellular adhesion molecules in the pathogenesis of Schistosomiasis mansoni. Immunol. Lett., 2019, 206, 11-18.
[http://dx.doi.org/10.1016/j.imlet.2018.11.011] [PMID: 30503821]
[68]
Schwartz, C.; Fallon, P.G. Schistosoma “eggs-iting” the host: granuloma formation and egg excretion. Front. Immunol., 2018, 9, 2492.
[http://dx.doi.org/10.3389/fimmu.2018.02492] [PMID: 30459767]
[69]
Wilson, M.S.; Mentink-Kane, M.M.; Pesce, J.T.; Ramalingam, T.R.; Thompson, R.; Wynn, T.A. Immunopathology of schistosomiasis. Immunol. Cell Biol., 2007, 85(2), 148-154.
[http://dx.doi.org/10.1038/sj.icb.7100014] [PMID: 17160074]
[70]
Fallon, P.G.; Richardson, E.J.; McKenzie, G.J.; McKenzie, A.N. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol., 2000, 164(5), 2585-2591.
[http://dx.doi.org/10.4049/jimmunol.164.5.2585] [PMID: 10679097]
[71]
de Jesus, A.R.; Magalhães, A.; Miranda, D.G.; Miranda, R.G.; Araújo, M.I.; de Jesus, A.A.; Silva, A.; Santana, L.B.; Pearce, E.; Carvalho, E.M. Association of type 2 cytokines with hepatic fibrosis in human Schistosoma mansoni infection. Infect. Immun., 2004, 72(6), 3391-3397.
[http://dx.doi.org/10.1128/IAI.72.6.3391-3397.2004] [PMID: 15155645]
[72]
Taylor, J.J.; Mohrs, M.; Pearce, E.J. Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. J. Immunol., 2006, 176(10), 5839-5847.
[http://dx.doi.org/10.4049/jimmunol.176.10.5839] [PMID: 16670290]
[73]
Deaton, A.M.; Cook, P.C.; De Sousa, D.; Phythian-Adams, A.T.; Bird, A.; MacDonald, A.S. A unique DNA methylation signature defines a population of IFN-γ/IL-4 double-positive T cells during helminth infection. Eur. J. Immunol., 2014, 44(6), 1835-1841.
[http://dx.doi.org/10.1002/eji.201344098] [PMID: 24578067]
[74]
la Sala, A.; Ferrari, D.; Di Virgilio, F.; Idzko, M.; Norgauer, J.; Girolomoni, G. Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol., 2003, 73(3), 339-343.
[http://dx.doi.org/10.1189/jlb.0802418] [PMID: 12629147]
[75]
Burnstock, G.; Ralevic, V. Purinergic signaling and blood vessels in health and disease. Pharmacol. Rev., 2013, 66(1), 102-192.
[http://dx.doi.org/10.1124/pr.113.008029] [PMID: 24335194]
[76]
Lohman, A.W.; Billaud, M.; Isakson, B.E. Mechanisms of ATP release and signalling in the blood vessel wall. Cardiovasc. Res., 2012, 95(3), 269-280.
[http://dx.doi.org/10.1093/cvr/cvs187] [PMID: 22678409]
[77]
Idzko, M.; Ferrari, D.; Eltzschig, H.K. Nucleotide signalling during inflammation. Nature, 2014, 509(7500), 310-317.
[http://dx.doi.org/10.1038/nature13085] [PMID: 24828189]
[78]
Coddou, C.; Yan, Z.; Obsil, T.; Huidobro-Toro, J.P.; Stojilkovic, S.S. Activation and regulation of purinergic P2X receptor channels. Pharmacol. Rev., 2011, 63(3), 641-683.
[http://dx.doi.org/10.1124/pr.110.003129] [PMID: 21737531]
[79]
Jacobson, K.A.; Paoletta, S.; Katritch, V.; Wu, B.; Gao, Z-G.; Zhao, Q.; Stevens, R.C.; Kiselev, E. Nucleotides acting at P2Y receptors: connecting structure and function. Mol. Pharmacol., 2015, 88(2), 220-230.
[http://dx.doi.org/10.1124/mol.114.095711] [PMID: 25837834]
[80]
Rafehi, M.; Müller, C.E. Tools and drugs for uracil nucleotideactivated P2Y receptors. Pharmacol. Ther., 2018, 190, 24-80.
[http://dx.doi.org/10.1016/j.pharmthera.2018.04.002] [PMID: 29660366]
[81]
Jankowski, V.; van der Giet, M.; Mischak, H.; Morgan, M.; Zidek, W.; Jankowski, J. Dinucleoside polyphosphates: strong endogenous agonists of the purinergic system. Br. J. Pharmacol., 2009, 157(7), 1142-1153.
[http://dx.doi.org/10.1111/j.1476-5381.2009.00337.x] [PMID: 19563527]
[82]
Fraga, H.; Fontes, R. Enzymatic synthesis of mono and dinucleoside polyphosphates. Biochim. Biophys. Acta, 2011, 1810(12), 1195-1204.
[http://dx.doi.org/10.1016/j.bbagen.2011.09.010] [PMID: 21978831]
[83]
Lazarowski, E.R. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal., 2012, 8(3), 359-373.
[http://dx.doi.org/10.1007/s11302-012-9304-9] [PMID: 22528679]
[84]
Lazarowski, E.R.; Boucher, R.C.; Harden, T.K. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol., 2003, 64(4), 785-795.
[http://dx.doi.org/10.1124/mol.64.4.785] [PMID: 14500734]
[85]
Robson, S.C.; Sévigny, J.; Zimmermann, H. The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signal., 2006, 2(2), 409-430.
[http://dx.doi.org/10.1007/s11302-006-9003-5] [PMID: 18404480]
[86]
Jacobson, K.A.; Müller, C.E. Medicinal chemistry of adenosine, P2Y and P2X receptors. Neuropharmacology, 2016, 104, 31-49.
[http://dx.doi.org/10.1016/j.neuropharm.2015.12.001] [PMID: 26686393]
[87]
von Kügelgen, I.; Hoffmann, K. Pharmacology and structure of P2Y receptors. Neuropharmacology, 2016, 104, 50-61.
[http://dx.doi.org/10.1016/j.neuropharm.2015.10.030] [PMID: 26519900]
[88]
Fuentes, E.; Palomo, I. Extracellular ATP metabolism on vascular endothelial cells: A pathway with pro-thrombotic and anti-thrombotic molecules. Vascul. Pharmacol., 2015, 75, 1-6.
[http://dx.doi.org/10.1016/j.vph.2015.05.002] [PMID: 25989108]
[89]
Gao, Z.G.; Verzijl, D.; Zweemer, A.; Ye, K.; Göblyös, A.; Ijzerman, A.P.; Jacobson, K.A. Functionally biased modulation of A(3) adenosine receptor agonist efficacy and potency by imidazoquinolinamine allosteric enhancers. Biochem. Pharmacol., 2011, 82(6), 658-668.
[http://dx.doi.org/10.1016/j.bcp.2011.06.017] [PMID: 21718691]
[90]
Vecchio, E.A.; Baltos, J-A.; Nguyen, A.T.N.; Christopoulos, A.; White, P.J.; May, L.T. New paradigms in adenosine receptor pharmacology: allostery, oligomerization and biased agonism. Br. J. Pharmacol., 2018, 175(21), 4036-4046.
[http://dx.doi.org/10.1111/bph.14337] [PMID: 29679502]
[91]
Ciruela, F.; Casadó, V.; Rodrigues, R.J.; Luján, R.; Burgueño, J.; Canals, M.; Borycz, J.; Rebola, N.; Goldberg, S.R.; Mallol, J.; Cortés, A.; Canela, E.I.; López-Giménez, J.F.; Milligan, G.; Lluis, C.; Cunha, R.A.; Ferré, S.; Franco, R. Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers. J. Neurosci., 2006, 26(7), 2080-2087.
[http://dx.doi.org/10.1523/JNEUROSCI.3574-05.2006] [PMID: 16481441]
[92]
Baltos, J-A.; Gregory, K.J.; White, P.J.; Sexton, P.M.; Christopoulos, A.; May, L.T. Quantification of adenosine A(1) receptor biased agonism: Implications for drug discovery. Biochem. Pharmacol., 2016, 99, 101-112.
[http://dx.doi.org/10.1016/j.bcp.2015.11.013] [PMID: 26581123]
[93]
Baltos, J-A.; Paoletta, S.; Nguyen, A.T.N.; Gregory, K.J.; Tosh, D.K.; Christopoulos, A.; Jacobson, K.A.; May, L.T. Structure-activity analysis of biased agonism at the human adenosine A3 receptor. Mol. Pharmacol., 2016, 90(1), 12-22.
[http://dx.doi.org/10.1124/mol.116.103283] [PMID: 27136943]
[94]
North, R.A. Molecular physiology of P2X receptors. Physiol. Rev., 2002, 82(4), 1013-1067.
[http://dx.doi.org/10.1152/physrev.00015.2002] [PMID: 12270951]
[95]
Guo, C.; Masin, M.; Qureshi, O.S.; Murrell-Lagnado, R.D. Evidence for functional P2X4/P2X7 heteromeric receptors. Mol. Pharmacol., 2007, 72(6), 1447-1456.
[http://dx.doi.org/10.1124/mol.107.035980] [PMID: 17785580]
[96]
Virginio, C.; MacKenzie, A.; North, R.A.; Surprenant, A. Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J. Physiol., 1999, 519(Pt 2), 335-346.
[http://dx.doi.org/10.1111/j.1469-7793.1999.0335m.x] [PMID: 10457053]
[97]
Pippel, A.; Stolz, M.; Woltersdorf, R.; Kless, A.; Schmalzing, G.; Markwardt, F. Localization of the gate and selectivity filter of the full-length P2X7 receptor. Proc. Natl. Acad. Sci. USA, 2017, 114(11), E2156-E2165.
[http://dx.doi.org/10.1073/pnas.1610414114] [PMID: 28235784]
[98]
Agboh, K.C.; Webb, T.E.; Evans, R.J.; Ennion, S.J. Functional characterization of a P2X receptor from Schistosoma mansoni. J. Biol. Chem., 2004, 279(40), 41650-41657.
[http://dx.doi.org/10.1074/jbc.M408203200] [PMID: 15292267]
[99]
Raouf, R.; Blais, D.; Séguéla, P. High zinc sensitivity and pore formation in an invertebrate P2X receptor. Biochim. Biophys. Acta, 2005, 1669(2), 135-141.
[http://dx.doi.org/10.1016/j.bbamem.2005.01.009] [PMID: 15893516]
[100]
Ijzerman, A.P.; Fredholm, B.; Jacobson, K.A.; Linden, J.; Müeller, C.; Frenguelli, B. Adenosine receptors (version 2019.4) in the IUPHAR/BPS Guide to Pharmacology Database. Structure-activity Relat. Aden. Recept., 2019, 2019, 4. (2019)
[101]
Zimmermann, H.; Zebisch, M.; Sträter, N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal., 2012, 8(3), 437-502.
[http://dx.doi.org/10.1007/s11302-012-9309-4] [PMID: 22555564]
[102]
Alexander, S.P.H.; Christopoulos, A.; Davenport, A.P.; Kelly, E.; Mathie, A.; Peters, J.A.; Veale, E.L.; Armstrong, J.F.; Faccenda, E.; Harding, S.D.; Pawson, A.J.; Sharman, J.L.; Southan, C.; Davies, J.A. CGTP Collaborators. (2019) The Concise guide to pharmacology 2019/20: G protein-coupled receptors. Br. J. Pharmacol., 2019, 176(S1), S21-S141.
[103]
Volonté, C.; Amadio, S.; D’Ambrosi, N.; Colpi, M.; Burnstock, G. P2 receptor web: complexity and fine-tuning. Pharmacol. Ther., 2006, 112(1), 264-280.
[http://dx.doi.org/10.1016/j.pharmthera.2005.04.012] [PMID: 16780954]
[104]
Zhou, Z.; Matsumoto, T.; Jankowski, V.; Pernow, J.; Mustafa, S.J.; Duncker, D.J.; Merkus, D. Uridine adenosine tetraphosphate and purinergic signaling in cardiovascular system: An update. Pharmacol. Res., 2019, 141, 32-45.
[http://dx.doi.org/10.1016/j.phrs.2018.12.009] [PMID: 30553823]
[105]
Abbracchio, M.P.; Burnstock, G.; Boeynaems, J-M.; Barnard, E.A.; Boyer, J.L.; Kennedy, C.; Knight, G.E.; Fumagalli, M.; Gachet, C.; Jacobson, K.A.; Weisman, G.A. International union of pharmacology lviii: update on the p2y g protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev., 2006, 58(3), 281-341.
[http://dx.doi.org/10.1124/pr.58.3.3] [PMID: 16968944]
[106]
Choi, R.C.Y.; Simon, J.; Tsim, K.W.K.; Barnard, E.A. Constitutive and agonist-induced dimerizations of the P2Y1 receptor: relationship to internalization and scaffolding. J. Biol. Chem., 2008, 283(16), 11050-11063.
[http://dx.doi.org/10.1074/jbc.M709266200] [PMID: 18270199]
[107]
Vuerich, M.; Robson, S.C.; Longhi, M.S. Ectonucleotidases in intestinal and hepatic inflammation. Front. Immunol., 2019, 10, 507.
[http://dx.doi.org/10.3389/fimmu.2019.00507] [PMID: 30941139]
[108]
Allard, B.; Longhi, M.S.; Robson, S.C.; Stagg, J. The ectonucleotidases CD39 and CD73: Novel checkpoint inhibitor targets. Immunol. Rev., 2017, 276(1), 121-144.
[http://dx.doi.org/10.1111/imr.12528] [PMID: 28258700]
[109]
Regateiro, F.S.; Howie, D.; Nolan, K.F.; Agorogiannis, E.I.; Greaves, D.R.; Cobbold, S.P.; Waldmann, H. Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-β. Eur. J. Immunol., 2011, 41(10), 2955-2965.
[http://dx.doi.org/10.1002/eji.201141512] [PMID: 21770045]
[110]
Aird, W.C. Endothelium in health and disease. Pharmacol. Rep., 2008, 60(1), 139-143.
[PMID: 18276995]
[111]
Rothermel, A.L.; Wang, Y.; Schechner, J.; Mook-Kanamori, B.; Aird, W.C.; Pober, J.S.; Tellides, G.; Johnson, D.R. Endothelial cells present antigens in vivo. BMC Immunol., 2004, 5, 5.
[http://dx.doi.org/10.1186/1471-2172-5-5] [PMID: 15113397]
[112]
Pober, J.S.; Sessa, W.C. Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol., 2007, 7(10), 803-815.
[http://dx.doi.org/10.1038/nri2171] [PMID: 17893694]
[113]
Cook-Mills, J.M.; Deem, T.L. Active participation of endothelial cells in inflammation. J. Leukoc. Biol., 2005, 77(4), 487-495.
[http://dx.doi.org/10.1189/jlb.0904554] [PMID: 15629883]
[114]
Vila, E.; Salaices, M. Cytokines and vascular reactivity in resistance arteries. Am. J. Physiol. Heart Circ. Physiol., 2005, 288(3), H1016-H1021.
[http://dx.doi.org/10.1152/ajpheart.00779.2004] [PMID: 15706038]
[115]
Silva, C.L.M. Endothelial cells as targets of the intravascular parasitic disease schistosomiasis. In: Vascular Responses to Pathogens; Gavins, F., Ed.; Elsevier Inc.: Amsterdam, 2015; pp. 195-207.
[116]
Oliveira, S.D.; Quintas, L.E.; Amaral, L.S.; Noël, F.; Farsky, S.H.; Silva, C.L. Increased endothelial cell-leukocyte interaction in murine schistosomiasis: possible priming of endothelial cells by the disease. PLoS One, 2011, 6(8)e23547
[http://dx.doi.org/10.1371/journal.pone.0023547] [PMID: 21853150]
[117]
Silva, C.L.; Morel, N.; Lenzi, H.L.; Noël, F. Increased reactivity to 5-hydroxytryptamine of portal veins from mice infected with Schistosoma mansoni. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 1998, 120(3), 417-423.
[http://dx.doi.org/10.1016/S1095-6433(98)10041-7] [PMID: 9787826]
[118]
Oliveira, S.D.; Coutinho-Silva, R.; Silva, C.L. Endothelial P2X7 receptors’ expression is reduced by schistosomiasis. Purinergic Signal., 2013, 9(1), 81-89.
[http://dx.doi.org/10.1007/s11302-012-9332-5] [PMID: 22987361]
[119]
Oliveira, S.D.; Silva, C.L.M. Schistosomiasis differentially affects vasoconstrictor responses: up-regulation of 5-HT receptor-mediated aorta contraction. Mem. Inst. Oswaldo Cruz, 2011, 106(4), 456-460.
[http://dx.doi.org/10.1590/S0074-02762011000400012] [PMID: 21739034]
[120]
Sotillo, J.; Robinson, M.W.; Kimber, M.J.; Cucher, M.; Ancarola, M.E.; Nejsum, P.; Marcilla, A.; Eichenberger, R.M.; Tritten, L. The protein and microRNA cargo of extracellular vesicles from parasitic helminths - current status and research priorities. Int. J. Parasitol., 2020, 50(9), 635-645.
[http://dx.doi.org/10.1016/j.ijpara.2020.04.010] [PMID: 32652128]
[121]
Wang, L.; Karlsson, L.; Moses, S.; Hultgårdh-Nilsson, A.; Andersson, M.; Borna, C.; Gudbjartsson, T.; Jern, S.; Erlinge, D. P2 receptor expression profiles in human vascular smooth muscle and endothelial cells. J. Cardiovasc. Pharmacol., 2002, 40(6), 841-853.
[http://dx.doi.org/10.1097/00005344-200212000-00005] [PMID: 12451317]
[122]
Lyubchenko, T.; Woodward, H.; Veo, K.D.; Burns, N.; Nijmeh, H.; Liubchenko, G.A.; Stenmark, K.R.; Gerasimovskaya, E.V. P2Y1 and P2Y13 purinergic receptors mediate Ca2+ signaling and proliferative responses in pulmonary artery vasa vasorum endothelial cells. Am. J. Physiol. Cell Physiol., 2011, 300(2), C266-C275.
[http://dx.doi.org/10.1152/ajpcell.00237.2010] [PMID: 20962269]
[123]
Yamamoto, K.; Korenaga, R.; Kamiya, A.; Qi, Z.; Sokabe, M.; Ando, J. P2X(4) receptors mediate ATP-induced calcium influx in human vascular endothelial cells. Am. J. Physiol. Heart Circ. Physiol., 2000, 279(1), H285-H292.
[http://dx.doi.org/10.1152/ajpheart.2000.279.1.H285] [PMID: 10899068]
[124]
Liu, C.; Mather, S.; Huang, Y.; Garland, C.J.; Yao, X. Extracellular ATP facilitates flow-induced vasodilatation in rat small mesenteric arteries. Am. J. Physiol. Heart Circ. Physiol., 2004, 286(5), H1688-H1695.
[http://dx.doi.org/10.1152/ajpheart.00576.2003] [PMID: 14715503]
[125]
Chen, Q.; Yang, Y.; Hou, J.; Shu, Q.; Yin, Y.; Fu, W.; Han, F.; Hou, T.; Zeng, C.; Nemeth, E.; Linzmeier, R.; Ganz, T.; Fang, X. Increased gene copy number of DEFA1/DEFA3 worsens sepsis by inducing endothelial pyroptosis. Proc. Natl. Acad. Sci. USA, 2019, 116(8), 3161-3170.
[http://dx.doi.org/10.1073/pnas.1812947116] [PMID: 30718392]
[126]
M., Palmetshofer, A., Kaczmarek, E., Koziak, K., Stroka, D., Grey, S.T., Stuhlmeier, K.M., Robson, S.C. Extracellular ATP and ADP activate transcription factor NF-κB and induce endothelial cell apoptosis. Biochem. Biophys. Res. Commun., 1998, 139(7), 822-829.
[127]
Thimm, D.; Knospe, M.; Abdelrahman, A.; Moutinho, M.; Alsdorf, B.B.; von Kügelgen, I.; Schiedel, A.C.; Müller, C.E. Characterization of new G protein-coupled adenine receptors in mouse and hamster. Purinergic Signal., 2013, 9(3), 415-426.
[http://dx.doi.org/10.1007/s11302-013-9360-9] [PMID: 23608776]
[128]
Jacobs, W.; Van de Vijver, K.; Deelder, A.; Van Marck, E. Morphometrical and immunopathological dissection of the hepatic Schistosoma haematobium granuloma in the murine host. Parasite, 1998, 5(4), 299-306.
[http://dx.doi.org/10.1051/parasite/1998054299] [PMID: 9879552]
[129]
Ritter, D.M.; McKerrow, J.H. Intercellular adhesion molecule 1 is the major adhesion molecule expressed during schistosome granuloma formation. Infect. Immun., 1996, 64(11), 4706-4713.
[http://dx.doi.org/10.1128/IAI.64.11.4706-4713.1996] [PMID: 8890229]
[130]
Soliman, K.; El-Ansary, A.; Mohamed, A.M. Effect of carnosine administration on metabolic parameters in bilharzia-infected hamsters. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2001, 129(1), 157-164.
[http://dx.doi.org/10.1016/S1096-4959(01)00332-3] [PMID: 11337259]
[131]
Zuccarini, M.; Giuliani, P.; Buccella, S.; Di Liberto, V.; Mudò, G.; Belluardo, N.; Carluccio, M.; Rossini, M.; Condorelli, D.F.; Rathbone, M.P.; Caciagli, F.; Ciccarelli, R.; Di Iorio, P. Modulation of the TGF-β1-induced epithelial to mesenchymal transition (EMT) mediated by P1 and P2 purine receptors in MDCK cells. Purinergic Signal., 2017, 13(4), 429-442.
[http://dx.doi.org/10.1007/s11302-017-9571-6] [PMID: 28616713]
[132]
Barron, L.; Wynn, T.A. Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. Eur. J. Immunol., 2011, 41(9), 2509-2514.
[http://dx.doi.org/10.1002/eji.201141869] [PMID: 21952807]
[133]
Maizels, R.M.; Pearce, E.J.; Artis, D.; Yazdanbakhsh, M.; Wynn, T.A. Regulation of pathogenesis and immunity in helminth infections. J. Exp. Med., 2009, 206(10), 2059-2066.
[http://dx.doi.org/10.1084/jem.20091903] [PMID: 19770272]
[134]
Rutitzky, L.I.; Hernandez, H.J.; Stadecker, M.J. Th1-polarizing immunization with egg antigens correlates with severe exacerbation of immunopathology and death in schistosome infection. Proc. Natl. Acad. Sci. USA, 2001, 98(23), 13243-13248.
[http://dx.doi.org/10.1073/pnas.231258498] [PMID: 11606762]
[135]
Herbert, D.R.; Hölscher, C.; Mohrs, M.; Arendse, B.; Schwegmann, A.; Radwanska, M.; Leeto, M.; Kirsch, R.; Hall, P.; Mossmann, H.; Claussen, B.; Förster, I.; Brombacher, F. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity, 2004, 20(5), 623-635.
[http://dx.doi.org/10.1016/S1074-7613(04)00107-4] [PMID: 15142530]
[136]
Lopez-Castejón, G.; Baroja-Mazo, A.; Pelegrín, P. Novel macrophage polarization model: from gene expression to identification of new anti-inflammatory molecules. Cell. Mol. Life Sci., 2011, 68(18), 3095-3107.
[http://dx.doi.org/10.1007/s00018-010-0609-y] [PMID: 21188461]
[137]
Geissmann, F.; Manz, M.G.; Jung, S.; Sieweke, M.H.; Merad, M.; Ley, K. Development of monocytes, macrophages, and dendritic cells. Science, 2010, 327(5966), 656-661.
[http://dx.doi.org/10.1126/science.1178331] [PMID: 20133564]
[138]
Naito, M. Macrophage differentiation and function in health and disease. Pathol. Int., 2008, 58(3), 143-155.
[http://dx.doi.org/10.1111/j.1440-1827.2007.02203.x] [PMID: 18251777]
[139]
Van den Bossche, J.; O’Neill, L.A.; Menon, D. Macrophage immunometabolism: where are we (Going)? Trends Immunol., 2017, 38(6), 395-406.
[http://dx.doi.org/10.1016/j.it.2017.03.001] [PMID: 28396078]
[140]
Savio, L.E.B.; de Andrade Mello, P.; da Silva, C.G.; Coutinho-Silva, R. The P2X7 Receptor in Inflammatory Diseases: Angel or Demon? Front. Pharmacol., 2018, 9, 52.
[http://dx.doi.org/10.3389/fphar.2018.00052] [PMID: 29467654]
[141]
Giuliani, A.L.; Sarti, A.C.; Falzoni, S.; Di Virgilio, F. The P2X7 Receptor-Interleukin-1 Liaison. Front. Pharmacol., 2017, 8, 123.
[http://dx.doi.org/10.3389/fphar.2017.00123] [PMID: 28360855]
[142]
Lister, M.F.; Sharkey, J.; Sawatzky, D.A.; Hodgkiss, J.P.; Davidson, D.J.; Rossi, A.G.; Finlayson, K. The role of the purinergic P2X7 receptor in inflammation. J. Inflamm. (Lond.), 2007, 4, 5.
[http://dx.doi.org/10.1186/1476-9255-4-5] [PMID: 17367517]
[143]
Oliveira, S.D.; Nanini, H.F.; Savio, L.E.; Waghabi, M.C.; Silva, C.L.; Coutinho-Silva, R. Macrophage P2X7 receptor function is reduced during schistosomiasis: putative role of TGF- β1. Mediators Inflamm., 2014, 2014134974
[http://dx.doi.org/10.1155/2014/134974] [PMID: 25276050]
[144]
Welter-Stahl, L.; da Silva, C.M.; Schachter, J.; Persechini, P.M.; Souza, H.S.; Ojcius, D.M.; Coutinho-Silva, R. Expression of purinergic receptors and modulation of P2X7 function by the inflammatory cytokine IFNgamma in human epithelial cells. Biochim. Biophys. Acta, 2009, 1788(5), 1176-1187.
[http://dx.doi.org/10.1016/j.bbamem.2009.03.006] [PMID: 19306841]
[145]
Lenzi, H.L.; Pacheco, R.G.; Pelajo-Machado, M.; Panasco, M.S.; Romanha, W.S.; Lenzi, J.A. Immunological system and Schistosoma mansoni: co-evolutionary immunobiology. What is the eosinophil role in parasite-host relationship? Mem. Inst. Oswaldo Cruz, 1997, 92(Suppl. 2), 19-32.
[http://dx.doi.org/10.1590/S0074-02761997000800005] [PMID: 9698912]
[146]
Spencer, L.A.; Bonjour, K.; Melo, R.C.; Weller, P.F. Eosinophil secretion of granule-derived cytokines. Front. Immunol., 2014, 5, 496.
[http://dx.doi.org/10.3389/fimmu.2014.00496] [PMID: 25386174]
[147]
Davies, S.J.; Smith, S.J.; Lim, K.C.; Zhang, H.; Purchio, A.F.; McKerrow, J.H.; West, D.B. In vivo imaging of tissue eosinophilia and eosinopoietic responses to schistosome worms and eggs. Int. J. Parasitol., 2005, 35(8), 851-859.
[http://dx.doi.org/10.1016/j.ijpara.2005.02.017] [PMID: 15950229]
[148]
Neves, J.S.; Perez, S.A.; Spencer, L.A.; Melo, R.C.; Reynolds, L.; Ghiran, I.; Mahmudi-Azer, S.; Odemuyiwa, S.O.; Dvorak, A.M.; Moqbel, R.; Weller, P.F. Eosinophil granules function extracellularly as receptor-mediated secretory organelles. Proc. Natl. Acad. Sci. USA, 2008, 105(47), 18478-18483.
[http://dx.doi.org/10.1073/pnas.0804547105] [PMID: 19017810]
[149]
Savio, L.E.B.; de Andrade Mello, P.; Figliuolo, V.R.; de Avelar Almeida, T.F.; Santana, P.T.; Oliveira, S.D.S.; Silva, C.L.M.; Feldbrügge, L.; Csizmadia, E.; Minshall, R.D.; Longhi, M.S.; Wu, Y.; Robson, S.C.; Coutinho-Silva, R. CD39 limits P2X7 receptor inflammatory signaling and attenuates sepsis-induced liver injury. J. Hepatol., 2017, 67(4), 716-726.
[http://dx.doi.org/10.1016/j.jhep.2017.05.021] [PMID: 28554875]
[150]
Jacob, F.; Pérez Novo, C.; Bachert, C.; Van Crombruggen, K. Purinergic signaling in inflammatory cells: P2 receptor expression, functional effects, and modulation of inflammatory responses. Purinergic Signal., 2013, 9(3), 285-306.
[http://dx.doi.org/10.1007/s11302-013-9357-4] [PMID: 23404828]
[151]
Muniz, V.S.; Baptista-Dos-Reis, R.; Benjamim, C.F.; Mata-Santos, H.A.; Pyrrho, A.S.; Strauch, M.A.; Melo, P.A.; Vicentino, A.R.; Silva-Paiva, J.; Bandeira-Melo, C.; Weller, P.F.; Figueiredo, R.T.; Neves, J.S. Purinergic P2Y12 Receptor Activation in Eosinophils and the Schistosomal Host Response. PLoS One, 2015, 10(10)e0139805
[http://dx.doi.org/10.1371/journal.pone.0139805] [PMID: 26448282]
[152]
Abbracchio, MP; Boeynaems, JM; Boyer, JL; Burnstock, G; Ceruti, S; Fumagalli, M; Gachet, C; Hills, R; Humphries, RG; Inoue, K; Jacobson, KA; Kennedy, C; King, BF; Lecca, D; Miras-Portugal, MT; Müller, CE; Ralevic, V; Weisman, GA P2Y receptors (version 2019.4) in the IUPHAR/BPS Guide to Pharmacology Database. IUPHAR/BPS Guide to Pharmacology, 2019, 2019(4)
[153]
Schuchardt, M.; Tölle, M.; van der Giet, M. P2Y purinoceptors as potential emerging therapeutical target in vascular disease. Curr. Pharm. Des., 2012, 18(37), 6169-6180.
[http://dx.doi.org/10.2174/138161212803582504] [PMID: 23004340]

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