The essential schistosome tegumental ectoenzyme SmNPP5 can block NAD-induced T cell apoptosis

References

• Colley DG, Bustinduy AL, Secor WE, et al. Human schistosomiasis. Lancet. 2014;383:2253–2264.
   PubMed Web of Science ®Google Scholar
• Steinmann P, Keiser J, Bos R, et al. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006;6:411–425.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Schistosomiasis fact sheet. [ cited 2019 Oct 24]; Available from: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis
   Google Scholar
• Wilson RA. The saga of schistosome migration and attrition. Parasitology. 2009;136:1581–1592.
   PubMed Web of Science ®Google Scholar
• King CH, Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chronic Illn. 2008;4:65–79.
   PubMedGoogle Scholar
• Bhardwaj R, Skelly PJ. Purinergic signaling and immune modulation at the schistosome surface? Trends Parasitol. 2009;25:256–260.
   PubMed Web of Science ®Google Scholar
• Da’dara A, Skelly PJ. Manipulation of vascular function by blood flukes? Blood Rev. 2011;25:175–179.
   PubMed Web of Science ®Google Scholar
• Hewitson JP, Grainger JR, Maizels RM. Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol. 2009;167:1–11.
   PubMed Web of Science ®Google Scholar
• Mebius MM, van Genderen PJJ, Urbanus RT, et al. Interference with the host haemostatic system by schistosomes. PLoSPathog. 2013;9:e1003781.
   Web of Science ®Google Scholar
• McSorley HJ, Maizels RM. Helminth infections and host immune regulation. Clin Microbiol Rev. 2012;25:585–608.
   PubMed Web of Science ®Google Scholar
• Bhardwaj R, Krautz-Peterson G, Da’dara A, et al. Tegumental phosphodiesterase SmNPP-5 is a virulence factor for schistosomes. Infect Immun. 2011;79:4276–4284.
   PubMed Web of Science ®Google Scholar
• Elzoheiry M, Da’dara AA, deLaforcade AM, et al. The essential ectoenzyme SmNPP5 from the human intravascular parasite Schistosoma mansoni is an ADPase and a potent inhibitor of platelet aggregation. Thromb Haemost. 2018;118:979–989.
   PubMed Web of Science ®Google Scholar
• Ziegler M, Niere M. NAD+ surfaces again. Biochem J. 2004;382:e5–6.
   PubMedGoogle Scholar
• Koch-Nolte F, Fischer S, Haag F, et al. Compartmentation of NAD+-dependent signaling. FEBS Lett. 2011;585:1651–1656.
   PubMed Web of Science ®Google Scholar
• Adriouch S, Haag F, Boyer O, et al. Extracellular NAD+: a danger signal hindering regulatory T cells. Microbes Infect. 2012;14:1284–1292.
   PubMed Web of Science ®Google Scholar
• Rissiek B, Haag F, Boyer O, et al. ADP-ribosylation of P2X7: a matter of life and death for regulatory T cells and natural killer T cells. Curr Top Microbiol Immunol. 2015;384:107–126.
   PubMed Web of Science ®Google Scholar
• Haag F, Adriouch S, Brass A, et al. Extracellular NAD and ATP: partners in immune cell modulation. Purinergic Signal. 2007;3:71–81.
   PubMed Web of Science ®Google Scholar
• Adriouch S, Hubert S, Pechberty S, et al. NAD+ released during inflammation participates in T cell homeostasis by inducing ART2-mediated death of naive T cells in vivo. J Immunol. 2007;179:186–194.
   PubMed Web of Science ®Google Scholar
• Seman M, Adriouch S, Scheuplein F. Immunity CK. NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity. 2003;19:571–582.
   PubMed Web of Science ®Google Scholar
• Scheuplein F, Schwarz N, Adriouch S, et al. NAD+ and ATP released from injured cells induce P2X7-dependent shedding of CD62L and externalization of phosphatidylserine by murine T cells. J Immunol. 2009;182:2898–2908.
   PubMed Web of Science ®Google Scholar
• Hubert S, Rissiek B, Klages K, et al. Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2X7 pathway. J Exp Med. 2010;207:2561–2568.
   PubMed Web of Science ®Google Scholar
• Tang C-L, Gao Y-R, Wang L-X, et al. Role of regulatory T cells in Schistosoma-mediated protection against Type 1 diabetes. Mol Cell Endocrinol. 2019;491:110434.
   PubMed Web of Science ®Google Scholar
• Zhou S, Jin X, Chen X, et al. Heat shock protein 60 in eggs specifically induces Tregs and reduces liver immunopathology in mice with Schistosomiasis Japonica. PLoS ONE. 2015;10:e0139133–17.
   PubMed Web of Science ®Google Scholar
• Deterre P, Gelman L, Gary-Gouy H, et al. Coordinated regulation in human T cells of nucleotide-hydrolyzing ecto-enzymatic activities, including CD38 and PC-1. Possible role in the recycling of nicotinamide adenine dinucleotide metabolites. J Immunol. 1996;157:1381–1388.
   PubMed Web of Science ®Google Scholar
• Gorelik A, Randriamihaja A, Illes K, et al. A key tyrosine substitution restricts nucleotide hydrolysis by the ectoenzyme NPP5. Febs J. 2017;284:3718–3726.
   PubMed Web of Science ®Google Scholar
• Goodrich SP, Muller-Steffner H, Osman A, et al. Production of calcium-mobilizing metabolites by a novel member of the ADP-ribosyl cyclase family expressed in Schistosoma mansoni. Biochemistry. 2005;44:11082–11097.
   PubMed Web of Science ®Google Scholar
• Kuhn I, Kellenberger E, Schuber F, et al. Schistosoma mansoni NAD+ catabolizing enzyme: identification of key residues in catalysis. Biochim Biophys Acta. 2013;1834:2520–2527.
   Google Scholar
• Ramalho-Pinto FJ, Gazzinelli G, Howells RE, et al. Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomulein vitro. Exp Parasitol. 1974;36:360–372.
   PubMed Web of Science ®Google Scholar
• Basch PF. Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J Parasitol. 1981;67:179–185.
   PubMed Web of Science ®Google Scholar
• Muller HM, Muller CD, Schuber F. NAD+glycohydrolase, an ecto-enzyme of calf spleen cells. Biochem J. 1983;212:459–464.
   PubMed Web of Science ®Google Scholar
• Ali TH, El-Ghonemy DH. Purification and characterization of the enzymes involved in nicotinamide adenine dinucleotide degradation by Penicillium brevicompactum NRC 829. 3 Biotech. 2016;6:34.
   PubMedGoogle Scholar
• Da’dara AA, Skelly P. Gene suppression in schistosomes using RNAi. Methods Mol Bio. 2015;2015(1201):143–164.
   Google Scholar
• Da’dara AA, Bhardwaj R, Ali YBM, et al. Schistosome tegumental ecto-apyrase (SmATPDase1) degrades exogenous pro-inflammatory and pro-thrombotic nucleotides. PeerJ. 2014;2:e316.
   PubMed Web of Science ®Google Scholar
• Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008;3:1101–1108.
   PubMed Web of Science ®Google Scholar
• Lee C-Y, Everse J. Studies on the properties of 1,N6-ethenoadenine derivatives of various coenzymes. Arch Biochem Biophys. 1973;157:83–90.
   PubMed Web of Science ®Google Scholar
• Adriouch S, Ohlrogge W, Haag F, et al. Rapid induction of naive T Cell apoptosis by ecto-nicotinamide adenine dinucleotide: requirement for Mono(ADP-ribosyl)transferase 2 and a downstream effector. J Immunol. 2001;167:196–203.
   PubMed Web of Science ®Google Scholar
• Kahl S, Nissen M, Girisch R, et al. Metalloprotease-mediated shedding of enzymatically active mouse ecto-ADP-ribosyltransferase ART2.2 upon T cell activation. J Immunol. 2000;165:4463–4469.
   PubMed Web of Science ®Google Scholar
• Tang C-L, Lei J-H, Wang T, et al. Effect of CD4+ CD25+ regulatory T cells on the immune evasion of Schistosoma japonicum. Parasitol Res. 2011;108:477–480.
   PubMed Web of Science ®Google Scholar
• Tang C-L, Xie Y-P, Yu W-H, et al. Effects of regulatory T cells on glyceraldehyde-3-phosphate dehydrogenase vaccine efficacy against Schistosoma japonicum. Acta Trop. 2019;202:105239.
   PubMed Web of Science ®Google Scholar
• Turner JD, Jenkins GR, Hogg KG, et al. CD4+CD25+ regulatory cells contribute to the regulation of colonic Th2 granulomatous pathology caused by schistosome infection. PLoS Negl Trop Dis. 2011;5:e1269–11.
   PubMed Web of Science ®Google Scholar
• Velavan TP, Ojurongbe O. Regulatory T Cells and Parasites. J Biomed Biotechnol. 2011;2011:1–8.
   Google Scholar
• Layland LE, Mages J, Loddenkemper C, et al. Prazeres da Costa CU. Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J Immunol. 2010;184:713–724.
   PubMed Web of Science ®Google Scholar
• Rofatto HK, Tararam CA, Borges WC, et al. Characterization of phosphodiesterase-5 as a surface protein in the tegument of Schistosoma mansoni. Mol Biochem Parasitol. 2009;166:32–41.
   PubMed Web of Science ®Google Scholar
• Muller-Steffner H, Jacques SA, Kuhn I, et al. Efficient inhibition of SmNACE by coordination complexes Is abolished by S. mansoni sequestration of metal. ACS Chem Biol. 2017;12:1787–1795.
   PubMed Web of Science ®Google Scholar
• Mesquita I, Varela P, Belinha A, et al. Exploring NAD+ metabolism in host-pathogen interactions. Cell Mol Life Sci. 2016;73:1225–1236.
   PubMed Web of Science ®Google Scholar
• Lebrun I, Marques-Porto R, Pereira AS, et al. Bacterial toxins: an overview on bacterial proteases and their action as virulence factors. Mini Rev Med Chem. 2009;9:820–828.
   PubMed Web of Science ®Google Scholar
• Simon NC, Aktories K, Barbieri JT. Novel bacterial ADP-ribosylating toxins: structure and function. Nat Rev Microbiol. 2014;12:599–611.
   PubMed Web of Science ®Google Scholar
• Hsieh CL, Huang HM, Hsieh SY, et al. NAD-glycohydrolase depletes intracellular NAD+ and inhibits acidification of autophagosomes to enhance multiplication of Group A Streptococcus in endothelial cells. Front Microbiol. 2018;9:161–211.
   PubMed Web of Science ®Google Scholar
• Sun J, Siroy A, Lokareddy RK, et al. The tuberculosis necrotizing toxin kills macrophages by hydrolyzing NAD. Nat Struct Mol Bio. 2015;22:672–678.
   Google Scholar
• Tak U, Vlach J, Garza-Garcia A, et al. The tuberculosis necrotizing toxin is an NAD+ and NADP+ glycohydrolase with distinct enzymatic properties. J Biol Chem. 2019;294:3024–3036.
   PubMed Web of Science ®Google Scholar
• Hancz D, Westerlund E, Bastiat-Sempe B, et al. Inhibition of inflammasome-dependent Interleukin 1β production by Streptococcal NAD+-glycohydrolase: evidence for extracellular activity. mBio. 2017;8:470–515.
   Web of Science ®Google Scholar
• Westerlund E, Valfridsson C, Yi DX, et al. The secreted virulence factor NADase of group A Streptococcus inhibits P2X7 receptor-mediated release of IL-1β. Front Immunol. 2019;10:1–12.
   PubMed Web of Science ®Google Scholar
• Pétriacq P, Ton J, Patrit O, et al. NAD acts as an integral regulator of multiple defense layers. Plant Physiol. 2016;172:1465–1479.
   PubMed Web of Science ®Google Scholar
• Abdelsamad N, Regmi H, Desaeger J, et al. Nicotinamide adenine dinucleotide induced resistance against root-knot nematode Meloidogyne hapla is based on increased tomato basal defense. J Nematol. 2019;51:1–10.
   PubMed Web of Science ®Google Scholar
• Wan L, Essuman K, Anderson RG, et al. TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. Science. 2019;365:799–803.
   PubMed Web of Science ®Google Scholar