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Research Paper

Apyrase decreases phage induction and Shiga toxin release from E. coli O157:H7 and has a protective effect during infection

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Article: 2122667 | Received 16 May 2022, Accepted 02 Sep 2022, Published online: 22 Sep 2022

References

  • Tarr PI, Gordon CA, Chandler WL. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 2005;365:1073–14. doi:10.1016/S0140-6736(05)71144-2.
  • Freedman SB, Xie J, Neufeld MS, Hamilton WL, Hartling L, Tarr PI, Alberta Provincial Pediatric Enteric Infection Team, Nettel-Aguirre A, Chuck A, Lee B, et al. Shiga toxin-producing Escherichia coli infection, antibiotics, and risk of developing hemolytic uremic syndrome: a meta-analysis. Clin Infect Dis. 2016;62:1251–1258. doi:10.1093/cid/ciw099.
  • McKee ML, O’Brien AD. Investigation of enterohemorrhagic Escherichia coli O157:H7 adherence characteristics and invasion potential reveals a new attachment pattern shared by intestinal E. coli. Infect Immun. 1995;63:2070–2074. doi:10.1128/iai.63.5.2070-2074.1995.
  • Matussek A, Einemo IM, Jogenfors A, Löfdahl S, Löfgren S. Shiga toxin-producing Escherichia coli in diarrheal stool of Swedish children: evaluation of polymerase chain reaction screening and duration of Shiga toxin shedding. J Pediatric Infect Dis Soc. 2016;5:147–151. doi:10.1093/jpids/piv003.
  • Yamasaki E, Watahiki M, Isobe J, Sata T, Nair GB, Kurazono H. Quantitative detection of Shiga toxins directly from stool specimens of patients associated with an outbreak of enterohemorrhagic Escherichia coli in Japan–quantitative Shiga toxin detection from stool during EHEC outbreak. Toxins (Basel). 2015;7:4381–4389. doi:10.3390/toxins7104381.
  • Malyukova I, Murray KF, Zhu C, Boedeker E, Kane A, Patterson K, Peterson JR, Donowitz M, Kovbasnjuk O. Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis. Am J Physiol Gastrointest Liver Physiol. 2009;296:G78–92. doi:10.1152/ajpgi.90347.2008.
  • Bekassy ZD, Calderon Toledo C, Leoj G, Kristoffersson A, Leopold SR, Perez MT, Karpman D. Intestinal damage in enterohemorrhagic Escherichia coli infection. Pediatr Nephrol. 2011;26:2059–2071. doi:10.1007/s00467-010-1616-9.
  • Calderon Toledo C, Arvidsson I, Karpman D. Cross-reactive protection against enterohemorrhagic Escherichia coli infection by enteropathogenic E. coli in a mouse model. Infect Immun. 2011;79:2224–2233. doi:10.1128/IAI.01024-10.
  • Rodríguez-Rubio L, Haarmann N, Schwidder M, Muniesa M, Schmidt H. Bacteriophages of Shiga toxin-producing Escherichia coli and their contribution to pathogenicity. Pathogens. 2021;10:404. doi:10.3390/pathogens10040404.
  • Galkin VE, Yu X, Bielnicki J, Ndjonka D, Bell CE, Egelman EH. Cleavage of bacteriophage lambda cI repressor involves the RecA C-terminal domain. J Mol Biol. 2009;385:779–787. doi:10.1016/j.jmb.2008.10.081.
  • Aertsen A, Van Houdt R, Vanoirbeek K, Michiels CW. An SOS response induced by high pressure in Escherichia coli. J Bacteriol. 2004;186:6133–6141. doi:10.1128/jb.186.18.6133-6141.2004.
  • Sperandio V, Torres AG, Giron JA, Kaper JB. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J Bacteriol. 2001;183:5187–5197. doi:10.1128/jb.183.17.5187-5197.2001.
  • Berger M, Aijaz I, Berger P, Dobrindt U, Koudelka G. Transcriptional and translational inhibitors block SOS response and Shiga toxin expression in enterohemorrhagic Escherichia coli. Sci Rep. 2019;9:18777. doi:10.1038/s41598-019-55332-2.
  • Fuchs S, Mühldorfer I, Donohue-Rolfe A, Kerényi M, Emödy L, Alexiev R, Nenkov P, Hacker J. Influence of RecA onin vivovirulence and Shiga toxin 2 production inEscherichia colipathogens. Microb Pathog. 1999;27:13–23. doi:10.1006/mpat.1999.0279.
  • Johansson KE, Ståhl AL, Arvidsson I, Loos S, Tontanahal A, Rebetz J, Chromek M, Kristoffersson A-C, Johannes L, Karpman D. Shiga toxin signals via ATP and its effect is blocked by purinergic receptor antagonism. Sci Rep. 2019;9:14362. doi:10.1038/s41598-019-50692-1.
  • Ståhl AL, Arvidsson I, Johansson KE, Chromek M, Rebetz J, Loos S, Kristoffersson A-C, Békássy ZD, Mörgelin M, Karpman D. A novel mechanism of bacterial toxin transfer within host blood cell-derived microvesicles. PLoS Pathog. 2015;11:e1004619. doi:10.1371/journal.ppat.1004619.
  • Proietti M, Perruzza L, Scribano D, Pellegrini G, D’Antuono R, Strati F, Raffaelli M, Gonzalez SF, Thelen M, Hardt W-D, et al. ATP released by intestinal bacteria limits the generation of protective IgA against enteropathogens. Nat Commun. 2019;10:250. doi:10.1038/s41467-018-08156-z.
  • Mempin R, Tran H, Chen C, Gong H, Kim Ho K, Lu S. Release of extracellular ATP by bacteria during growth. BMC Microbiol. 2013;13:301. doi:10.1186/1471-2180-13-301.
  • Inami A, Kiyono H, Kurashima Y. ATP as a pathophysiologic mediator of bacteria-host crosstalk in the gastrointestinal tract. Int J Mol Sci. 2018;19:2371. doi:10.3390/ijms19082371.
  • Knowles AF. The GDA1_CD39 superfamily: nTPDases with diverse functions. Purinergic Signal. 2011;7:21–45. doi:10.1007/s11302-010-9214-7.
  • Calderon Toledo C, Rogers TJ, Svensson M, Tati R, Fischer H, Svanborg C, Karpman D. Shiga toxin-mediated disease in MyD88-deficient mice infected with Escherichia coli O157:H7. Am J Pathol. 2008;173:1428–1439. doi:10.2353/ajpath.2008.071218.
  • Vuerich M, Robson SC, Longhi MS. Ectonucleotidases in intestinal and hepatic inflammation. Front Immunol. 2019;10:507. doi:10.3389/fimmu.2019.00507.
  • Cauwels A, Rogge E, Vandendriessche B, Shiva S, Brouckaert P. Extracellular ATP drives systemic inflammation, tissue damage and mortality. Cell Death Dis. 2014;5:e1102. doi:10.1038/cddis.2014.70.
  • Wan P, Liu X, Xiong Y, Ren Y, Chen J, Lu N, Guo Y, Bai A. Extracellular ATP mediates inflammatory responses in colitis via P2 x 7 receptor signaling. Sci Rep. 2016;6:19108. doi:10.1038/srep19108.
  • Wu X, Ren J, Chen G, Wu L, Song X, Li G, Deng Y, Wang G, Gu G, Li J. Systemic blockade of P2X7 receptor protects against sepsis-induced intestinal barrier disruption. Sci Rep. 2017;7:4364. doi:10.1038/s41598-017-04231-5.
  • Zoja C, Buelli S, Morigi M. Shiga toxin-associated hemolytic uremic syndrome: pathophysiology of endothelial dysfunction. Pediatr Nephrol. 2010;25:2231–2240. doi:10.1007/s00467-010-1522-1.
  • Karpman D, Papadopoulou D, Nilsson K, Sjögren AC, Mikaelsson C, Lethagen S. Platelet activation by Shiga toxin and circulatory factors as a pathogenetic mechanism in the hemolytic uremic syndrome. Blood. 2001;97:3100–3108. doi:10.1182/blood.v97.10.3100.
  • Ghosh SA, Polanowska-Grabowska RK, Fujii J, Obrig T, Gear AR. Shiga toxin binds to activated platelets. J Thromb Haemost. 2004;2:499–506. doi:10.1111/j.1538-7933.2004.00638.x.
  • Ståhl AL, Sartz L, Karpman D. Complement activation on platelet-leukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood. 2011;117:5503–5513. doi:10.1182/blood-2010-09-309161.
  • Oury C, Wera O. P2X1: a unique platelet receptor with a key role in thromboinflammation. Platelets. 2021;32:902–908. doi:10.1080/09537104.2021.1902972.
  • Bayliss J, Delarosa S, Wu J, Peterson JR, Eboda ON, Su GL, Hemmila M, Krebsbach PH, Cederna PS, Wang SC, et al. Adenosine triphosphate hydrolysis reduces neutrophil infiltration and necrosis in partial-thickness scald burns in mice. J Burn Care Res. 2014;35:54–61. doi:10.1097/BCR.0b013e31829b36d6.
  • Bayliss JM, Levi B, Wu J, Wang SC, Su GL, Xi C. Apyrase elicits host antimicrobial responses and resolves infection in burns. J Burn Care Res. 2016;37:e501–e7. doi:10.1097/bcr.0000000000000335.
  • Patents J. ADP’ase-enhanced apyrase therapy for wounds, microbial infection, sepsis, and heterotopic ossification. 2014. Oct 29. https://patents.justia.com/patent/20170333532.
  • Roberts V, Campbell DJ, Lu B, Chia J, Cowan PJ, Dwyer KM. The differential effect of apyrase treatment and hCD39 overexpression on chronic renal fibrosis after ischemia-reperfusion injury. Transplantation. 2017;101:e194–e204. doi:10.1097/tp.0000000000001679.
  • Crunkhorn S. Cardiovascular drugs: engineered apyrase averts clot formation. Nat Rev Drug Discov. 2014;13:724–725. doi:10.1038/nrd4444.
  • Iversen H, LA-L TM, Aspholm M, LP A, Lindback T, Commensal E. coli Stx2 lysogens produce high levels of phages after spontaneous prophage induction. Front Cell Infect Microbiol. 2015;5:5. doi:10.3389/fcimb.2015.00005.
  • Aijaz I, Koudelka GB. Cheating, facilitation and cooperation regulate the effectiveness of phage-encoded exotoxins as antipredator molecules. Microbiologyopen. 2019;8:e00636. doi:10.1002/mbo3.636.
  • Tontanahal A, Arvidsson I, Karpman D. Annexin induces cellular uptake of extracellular vesicles and delays disease in Escherichia coli O157:H7 infection. Microorganisms. 2021;9:1143. doi:10.3390/microorganisms9061143.