Desialylation of platelets by pneumococcal neuraminidase a induces ADP-dependent platelet hyperreactivity

Infection and Immunity

Volumn 86, Issue 10, 2018, Pages

  Kullaya, Vesla ^a,b   De Jonge, Marien I ^a   Langereis, Jeroen D ^a   Van Der Gaast De Jongh, Christa E ^a,b   Büll, Christian ^a   Adema, Gosse J ^a   Lefeber, Dirk ^a   Cremers, Amelieke J ^a   Mmbaga, Blandina T ^b   De Groot, Phillip G ^c   De Mast, Quirijn ^a   Van Der Ven, Andre J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b KILIMANJARO CHRISTIAN MEDICAL CENTRE   (Tanzania)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Desialylation; Nana; Platelets; Sialic acid; Streptococcus pneumoniae

Indexed keywords

ADENOSINE DIPHOSPHATE; APYRASE; COLLAGEN RELATED PEPTIDE XL; FIBRINOGEN; GLYCOPROTEIN; NEURAMINIDASE A; OSELTAMIVIR; PADGEM PROTEIN; PEPTIDE; SIALIC ACID; SIALIDASE INHIBITOR; THROMBIN RECEPTOR ACTIVATION PEPTIDE; TICAGRELOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; N ACETYLNEURAMINIC ACID; SIALIDASE;

ADULT; ARTICLE; CELL INTERACTION; COHORT ANALYSIS; CONTROLLED STUDY; DESIALYLATION; EX VIVO STUDY; HUMAN; HUMAN CELL; LEUKOCYTE; NONHUMAN; PLATELET COUNT; PLATELET REACTIVITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIALYLATION; SIGNAL TRANSDUCTION; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTE MEMBRANE; BLOOD; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PNEUMOCOCCAL INFECTION;

ADENOSINE DIPHOSPHATE; BACTERIAL PROTEINS; BLOOD PLATELETS; HOST-PATHOGEN INTERACTIONS; HUMANS; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; PLATELET AGGREGATION; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE;

EID: 85052799536     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00213-18     Document Type: Article

References (51)

1. Kadioglu A, Andrew PW. 2004. The innate immune response to pneumococcal lung infection: The untold story. Trends Immunol 25:143-149. https://doi.org/10.1016/j.it.2003.12.006.
2. Arman M, Krauel K, Tilley DO, Weber C, Cox D, Greinacher A, Kerrigan SW, Watson SP. 2014. Amplification of bacteria-induced platelet activation is triggered by Fc-RIIA, integrin -Iib-3, and platelet factor 4. Blood 123: 3166-3174. https://doi.org/10.1182/blood-2013-11-540526.
3. Keane C, Tilley D, Cunningham A, Smolenski A, Kadioglu A, Cox D, Jenkinson HF, Kerrigan SW. 2010. Invasive Streptococcus pneumoniae trigger platelet activation via Toll-like receptor 2. J Thromb Haemost 8:2757-2765. https://doi.org/10.1111/j.1538-7836.2010.04093.x.
4. de Stoppelaar SF, Claushuis TAM, Schaap MCL, Hou B, van der Poll T, Nieuwland R, van 't Veer C. 2016. Toll-like receptor signalling is not involved in platelet response to Streptococcus pneumoniae in vitro or in vivo. PLoS One 11: 0156977. https://doi.org/10.1371/journal.pone.0156977.
5. Brogly N, Devos P, Boussekey N, Georges H, Chiche A, Leroy O. 2007. Impact of thrombocytopenia on outcome of patients admitted to ICU for severe community-acquired pneumonia. J Infect 55:136 -140. https://doi.org/10.1016/j.jinf.2007.01.011.
6. Vieira-de-Abreu A, Campbell RA, Weyrich AS, Zimmerman GA. 2012. Platelets: Versatile effector cells in hemostasis, inflammation, and the immune continuum. Semin Immunopathol 34:5-30. https://doi.org/10.1007/s00281-011-0286-4.
7. Semple JW, Italiano JE, Freedman J. 2011. Platelets and the immune continuum. Nat Rev Immunol 11:264-274. https://doi.org/10.1038/nri2956.
8. Schrottmaier WC, Kral JB, Badrnya S, Assinger A. 2015. Aspirin and P2Y12 inhibitors in platelet-mediated activation of neutrophils and monocytes. Thromb Haemost 114:478-489. https://doi.org/10.1160/TH14-11-0943.
9. Rae N, Finch S, Chalmers JD. 2016. Cardiovascular disease as a complication of community-acquired pneumonia. Curr Opin Pulm Med 22: 212-218. https://doi.org/10.1097/MCP.0000000000000261.
10. Trappetti C, Kadioglu A, Carter M, Hayre J, Iannelli F, Pozzi G, Andrew PW, Oggioni M. 2009. Sialic acid: A preventable signal for pneumococcal biofilm formation, colonization, and invasion of the host. J Infect Dis 199:1497-1505. https://doi.org/10.1086/598483.
11. Brittan JL, Buckeridge TJ, Finn A, Kadioglu A, Jenkinson HF. 2012. Pneumococcal neuraminidase A: An essential upper airway colonization factor for Streptococcus pneumoniae. Mol Oral Microbiol 27:270 -283. https://doi.org/10.1111/j.2041-1014.2012.00658.x.
12. Crook M. 1991. Sialic acid: Its importance to platelet function in health and disease. Platelets 2:1-10. https://doi.org/10.3109/09537109109005496.
13. Madoff MA, Ebbe S, Baldini M. 1964. Sialic acid of human blood platelets. J Clin Invest 43:870-877. https://doi.org/10.1172/JCI104972.
14. Grozovsky R, Begonja AJ, Liu K, Visner G, Hartwig JH, Falet H, Hoffmeister KM. 2015. The Ashwell-Morell receptor regulates hepatic thrombopoietin production via JAK2-STAT3 signaling. Nat Med 21:47-54. https://doi.org/10.1038/nm.3770.
15. Zhang X-H, Wang Q-M, Zhang J-M, Feng F-E, Wang F-R, Chen H, Han W, Xu L, Liu K, Huang X. 2015. Desialylation is associated with apoptosis and phagocytosis of platelets in patients with prolonged isolated thrombocytopenia after allo-HSCT. J Hematol Oncol 8:116. https://doi.org/10.1186/s13045-015-0216-3.
16. Grewal PK, Aziz PV, Uchiyama S, Rubio GR, Lardone RD, Le D, Varki NM, Nizet V, Marth JD. 2013. Inducing host protection in pneumococcal sepsis by preactivation of the Ashwell-Morell receptor. Proc Natl Acad Sci U S A 110:20218-20223. https://doi.org/10.1073/pnas.1313905110.
17. Xu G, Kiefel MJ, Wilson JC, Andrew PW, Oggioni MR, Taylor GL. 2011. Three Streptococcus pneumoniae sialidases: Three different products. J Am Chem Soc 133:1718 -1721. https://doi.org/10.1021/ja110733q.
18. Gualdi L, Hayre JK, Gerlini A, Bidossi A, Colomba L, Trappetti C, Pozzi G, Docquier J, Andrew P, Ricci S, Oggioni MR. 2012. Regulation of neuraminidase expression in Streptococcus pneumoniae. BMC Microbiol 12:200. https://doi.org/10.1186/1471-2180-12-200.
19. Gut H, Xu G, Taylor GL, Walsh MA. 2011. Structural basis for Streptococcus pneumoniae NanA inhibition by influenza antivirals zanamivir and oseltamivir carboxylate. J Mol Biol 409:496 -503. https://doi.org/10.1016/j.jmb.2011.04.016.
20. Xu Z, von Grafenstein S, Walther E, Fuchs JE, Liedl KR, Sauerbrei A, Schmidtke M. 2016. Sequence diversity of NanA manifests in distinct enzyme kinetics and inhibitor susceptibility. Sci Rep 6:25169. https://doi.org/10.1038/srep25169.
21. Nieswandt B, Bergmeier W, Eckly A, Schulte V, Ohlmann P, Cazenave J-P, Zirngibl H, Offermanns S, Gachet C. 2001. Evidence for cross-talk between glycoprotein VI and Gi-coupled receptors during collageninduced platelet aggregation. Blood 97:3829 -3835. https://doi.org/10.1182/blood.V97.12.3829.
22. Greenberg J, Packham MA, Cazenave JP, Reimers HJ, Mustard JF. 1975 Effects on platelet function of removal of platelet sialic acid by neuraminidase. Lab Invest 32:476-484.
23. Dörr K, Kilch T, Kappel S, Alansary D, Schwär G, Niemeyer BA, Peinelt C. 2016. Cell type-specific glycosylation of Orai1 modulates store-operated Ca 2-entry. Sci Signal 9: 25. https://doi.org/10.1126/scisignal.aaa9913.
24. Varga-Szabo D, Braun A, Nieswandt B. 2011. STIM and Orai in platelet function. Cell Calcium 50:270 -278. https://doi.org/10.1016/j.ceca.2011.04.002.
25. De Marco L, Girolami A, Russell S, Ruggeri ZM. 1985. Interaction of asialo von Willebrand factor with glycoprotein Ib induces fibrinogen binding to the glycoprotein IIb/IIIa complex and mediates platelet aggregation. J Clin Invest 75:1198 -1203. https://doi.org/10.1172/JCI111816.
26. Iyú D, Glenn JR, White AE, Fox SC, van Giezen H, Nylander S, Heptinstall S. 2011. Mode of action of P2Y12 antagonists as inhibitors of platelet function. Thromb Haemost 105:96 -106.
27. Harfenist E, Packham M, Mustard J. 1984. Effects of variant gamma chains and sialic acid content of fibrinogen upon its interactions with ADP-stimulated human and rabbit platelets. Blood 64:1163-1168.
28. Park K, Gerndt SJ, Cooper SL. 1986. The effect of fibrinogen sialic acid residues on ex vivo platelet deposition on biomaterials. Thromb Res 43:293-302. https://doi.org/10.1016/0049-3848(86)90149-0.
29. Jenne CN, Kubes P. 2015. Platelets in inflammation and infection. Platelets 26:286 -292. https://doi.org/10.3109/09537104.2015.1010441.
30. Kral JB, Schrottmaier WC, Salzmann M, Assinger A. 2016. Platelet interaction with innate immune cells. Transfus Med Hemother 43:78-88. https://doi.org/10.1159/000444807.
31. Thomas MR, Storey RF. 2015. The role of platelets in inflammation. Thromb Haemost 114:449-458. https://doi.org/10.1160/TH14-12-1067.
32. Cangemi R, Casciaro M, Rossi E, Calvieri C, Bucci T, Calabrese CM, Taliani G, Falcone M, Palange P, Bertazzoni G, Farcomeni A, Grieco S, Pignatelli P, Violi F, Albanese F, Biliotti E, Carnevale R, Catasca E, Celestini A, Esvan R, Fazi L, Marinelli P, Mordenti M, Napoleone L, Palumbo Pastori Perri Proietti M, Capparuccia MR, Russo A, Russo R, Sarallo V, Salvatori G, Scarpellini MG, Ullo I. 2014. Platelet activation is associated with myocardial infarction in patients with pneumonia. J Am Coll Cardiol 64: 1917-1925. https://doi.org/10.1016/j.jacc.2014.07.985.
33. Chen G-Y, Chen X, King S, Cavassani KA, Cheng J, Zheng X, Yu H, Qu J, Fang D, Wu W, Bai X-F, Liu J-Q, Woodiga SA, Chen C, Sun L, Hogaboam CM, Kunkel SL, Zheng P, Liu Y. 2011. Amelioration of sepsis by inhibiting sialidase-mediated disruption of the CD24-SiglecG interaction. Nat Biotechnol 29:428-435. https://doi.org/10.1038/nbt.1846.
34. Li J, van der Wal DE, Zhu G, Xu M, Yougbare I, Ma L, Vadasz B, Carrim N, Grozovsky R, Ruan M, Zhu L, Zeng Q, Tao L, Zhai Z-M, Peng J, Hou M, Leytin V, Freedman J, Hoffmeister KM, Ni H. 2015. Desialylation is a mechanism of Fc-independent platelet clearance and a therapeutic target in immune thrombocytopenia. Nat Commun 6:7737. https://doi.org/10.1038/ncomms8737.
35. Paulson JC, Kawasaki N. 2011. Sialidase inhibitors DAMPen sepsis. Nat Biotechnol 29:406-407. https://doi.org/10.1038/nbt.1859.
36. Jansen AJG, Peng J, Zhao H-G, Hou M, Ni H. 2015. Sialidase inhibition to increase platelet counts: A new treatment option for thrombocytopenia. Am J Hematol 90:E94 -E95. https://doi.org/10.1002/ajh.23953.
37. Furman MI, Barnard MR, Krueger LA, Fox ML, Shilale EA, Lessard DM, Marchese P, Frelinger AL, Goldberg RJ, Michelson AD. 2001. Circulating monocyte-platelet aggregates are an early marker of acute myocardial infarction. J Am Coll Cardiol 38:1002-1006. https://doi.org/10.1016/S0735-1097(01)01485-1.
38. Varki A. 2008. Sialic acids in human health and disease. Trends Mol Med 14:351-360. https://doi.org/10.1016/j.molmed.2008.06.002.
39. Bennett JS, Vilaire G. 1979. Exposure of platelet fibrinogen receptors by ADP and epinephrine. J Clin Invest 64:1393-1401. https://doi.org/10.1172/JCI109597.
40. Zhong X, Kriz R, Seehra J, Kumar R. 2004. N-linked glycosylation of platelet P 2 Y 12 ADP receptor is essential for signal transduction but not for ligand binding or cell surface expression. FEBS Lett 562:111-117. https://doi.org/10.1016/S0014-5793(04)00191-7.
41. Kunicki TJ, Cheli Y, Moroi M, Furihata K. 2005. The influence of N-linked glycosylation on the function of platelet glycoprotein VI. Blood 106: 2744-2749. https://doi.org/10.1182/blood-2005-04-1454.
42. Nguyen KA, Hamzeh-Cognasse H, Palle S, Anselme-Bertrand I, Arthaud C-A, Chavarin P, Pozzetto B, Garraud O, Cognasse F. 2014. Role of Siglec-7 in apoptosis in human platelets. PLoS One 9: 106239. https://doi.org/10.1371/journal.pone.0106239.
43. Cognasse F, Nguyen KA, Damien P, McNicol A, Pozzetto B, Hamzeh- Cognasse H, Garraud O. 2015. The inflammatory role of platelets via their TLRs and Siglec receptors. Front Immunol 6:83. https://doi.org/10.3389/fimmu.2015.00083.
44. King SJ, Hippe KR, Weiser JN. 2006. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol 59:961-974. https://doi.org/10.1111/j.1365-2958.2005.04984.x.
45. Burghout P, Bootsma HJ, Kloosterman TG, Bijlsma JJE, de Jongh CE, Kuipers OP, Kuipers OPM. 2007. Search for genes essential for pneumococcal transformation: The RADA DNA repair protein plays a role in genomic recombination of donor DNA. J Bacteriol 189:6540-6550. https://doi.org/10.1128/JB.00573-07.
46. Cremers AJH, Meis JF, Walraven G, Van Der Gaast-De Jongh CE, Ferwerda G, Hermans PWM. 2014. Effects of 7-valent pneumococcal conjugate 1 vaccine on the severity of adult 2 bacteremic pneumococcal pneumonia. Vaccine 32:3989 -3994. https://doi.org/10.1016/j.vaccine.2014.04.089.
47. Cremers AJH, Mobegi FM, De Jonge MI, Van Hijum SAFT, Meis JF, Hermans PWM, Ferwerda G, Bentley SD, Zomer AL. 2015. The postvaccine microevolution of invasive Streptococcus pneumoniae. Sci Rep 5:14952. https://doi.org/10.1038/srep14952.
48. Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. https://doi.org/10.1093/nar/gkh340.
49. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671- 675. https://doi.org/10.1038/nmeth.2089.
50. Tunjungputri RN, van der Ven AJ, Riksen N, Rongen G, Tacke S, van den Berg TNA, Fijnheer R, Gomes ME, Dinarello CA, van de Veerdonk FL, Gasem M, Netea MG, Joosten LAB, De Groot PG, de Mast Q. 2015. Differential effects of platelets and platelet inhibition by ticagrelor on TLR2- And TLR4-mediated inflammatory responses. Thromb Haemost 113:1035-1045. https://doi.org/10.1160/TH14-07-0579.
51. Tunjungputri RN, van de Heijden W, Urbanus RT, de Groot PG, van der Ven A, de Mast Q. 2017. Higher platelet reactivity and platelet-monocyte complex formation in Gram-positive sepsis compared to Gram-negative sepsis. Platelets 28:595-601. https://doi.org/10.1080/09537104.2016.1252837.