NBEAL2 deficiency increases organ damage but does not affect host defense during Gram-negative pneumonia-derived sepsis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 38, Issue 8, 2018, Pages 1772-1784

  Claushuis, Theodora A M ^d   De Stoppelaar, Sacha F ^a   De Vos, Alex F ^a   Grootemaat, Anita E ^c,d   Van Der Wel, Nicole N ^c,d   Roelofs, Joris J T H ^b   Ware, Jerry ^e   Van'T Veer, Cornelis ^a   Van Der Poll, Tom ^a,c  

^a Center for Experimental and Molecular Medicine   (Netherlands)

^b Department of Pathology ^*  (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF ARKANSAS AT LITTLE ROCK   (United States)

Author keywords

Endotoxemia; Gray platelet syndrome; Infection; Neutrophils; Sepsis

Indexed keywords

NBEAL2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ADHESION RECEPTOR; CD11B ANTIGEN; GELATINASE B; LCN2 PROTEIN, MOUSE; MMP9 PROTEIN, MOUSE; NBEAL2 PROTEIN, MOUSE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PANCREATIC ELASTASE; PEROXIDASE; PLASMA PROTEIN; THROMBIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL PNEUMONIA; BACTERIUM COLONY; C57BL 6 MOUSE; CONTROLLED STUDY; EXPERIMENTAL SEPSIS; FEMALE; HOST RESISTANCE; IN VIVO STUDY; KLEBSIELLA PNEUMONIAE; LEUKOCYTE; MALE; MOUSE; NBEAL2 DEFICIENCY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; STAPHYLOCOCCUS INFECTION; ANIMAL; BLOOD; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; GENETICS; GRAY PLATELET SYNDROME; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; KLEBSIELLA INFECTION; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MONOCYTE; MULTIPLE ORGAN FAILURE; NEUTROPHIL; PATHOGENICITY; SEPSIS; THROMBOCYTE; THROMBOCYTE TRANSFUSION;

ANIMALS; BLOOD PLATELETS; BLOOD PROTEINS; CD11B ANTIGEN; DISEASE MODELS, ANIMAL; FEMALE; GRAY PLATELET SYNDROME; HOST-PATHOGEN INTERACTIONS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIPOCALIN-2; MALE; MATRIX METALLOPROTEINASE 9; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; MULTIPLE ORGAN FAILURE; NEUTROPHILS; PANCREATIC ELASTASE; PEROXIDASE; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PLATELET TRANSFUSION; PNEUMONIA, BACTERIAL; SEPSIS;

EID: 85055604549     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.118.311332     Document Type: Article

References (42)

1. Middleton EA, Weyrich AS, Zimmerman GA. Platelets in pulmonary immune responses and inflammatory lung diseases. Physiol Rev. 2016;96:1211-1259. doi: 10.1152/physrev.00038.2015.
2. de Jong JS, Dekker LR. Platelets and cardiac arrhythmia. Front Physiol. 2010;1:166. doi: 10.3389/fphys.2010.00166.
3. Nurden AT, Nurden P. Should any genetic defect affecting α-granules in platelets be classified as gray platelet syndrome? Am J Hematol. 2016;91:714-718. doi: 10.1002/ajh.24359.
4. Drouin A, Favier R, Massé JM, Debili N, Schmitt A, Elbim C, Guichard J, Adam M, Gougerot-Pocidalo MA, Cramer EM. Newly recognized cellular abnormalities in the gray platelet syndrome. Blood. 2001;98:1382-1391.
5. Chedani H, Dupuy E, Massé JM, Cramer EM. Neutrophil secretory defect in the gray platelet syndrome: a new case. Platelets. 2006;17:14-19. doi: 10.1080/09537100500165601.
6. White JG, Brunning RD. Neutrophils in the gray platelet syndrome. Platelets. 2004;15:333-340. doi: 10.1080/09537100410001714872.
7. Sowerby JM, Thomas DC, Clare S, et al. NBEAL2 is required for neutrophil and NK cell function and pathogen defense. J Clin Invest. 2017;127:3521-3526. doi: 10.1172/JCI91684.
8. Drube S, Grimlowski R, Deppermann C, et al. The neurobeachin-like 2 protein regulates mast cell homeostasis. J Immunol. 2017;199:2948-2957. doi: 10.4049/jimmunol.1700556.
9. Kovach MA, Standiford TJ. The function of neutrophils in sepsis. Curr Opin Infect Dis. 2012;25:321-327. doi: 10.1097/QCO.0b013e3283528c9b.
10. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11:519-531. doi: 10.1038/nri3024.
11. de Stoppelaar SF, van 't Veer C, Claushuis TA, Albersen BJ, Roelofs JJ, van der Poll T. Thrombocytopenia impairs host defense in gram-negative pneumonia-derived sepsis in mice. Blood. 2014;124:3781-3790. doi: 10.1182/blood-2014-05-573915.
12. van den Boogaard FE, Schouten M, de Stoppelaar SF, Roelofs JJ, Brands X, Schultz MJ, van't Veer C, van der Poll T. Thrombocytopenia impairs host defense during murine Streptococcus pneumoniae pneumonia. Crit Care Med. 2015;43:e75-e83. doi: 10.1097/CCM.0000000000000853.
13. Kang CI, Song JH, Chung DR, et al; Korean Network for Study of Infectious Diseases (KONSID). Risk factors and pathogenic significance of severe sepsis and septic shock in 2286 patients with gram-negative bac-teremia. J Infect. 2011;62:26-33. doi: 10.1016/j.jinf.2010.10.010.
14. Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the offense with a strong defense. Microbiol Mol Biol Rev. 2016;80:629-661. doi: 10.1128/MMBR.00078-15.
15. Kanaji T, Russell S, Ware J. Amelioration of the macrothrombocyto-penia associated with the murine Bernard-Soulier syndrome. Blood. 2002;100:2102-2107. doi: 10.1182/blood-2002-03-0997.
16. Hommes TJ, van Lieshout MH, van 't Veer C, Florquin S, Bootsma HJ, Hermans PW, de Vos AF, van der Poll T. Role of nucleotide-binding oligomerization domain-containing (NOD) 2 in host defense during pneumococcal pneumonia. PLoS One. 2015;10:e0145138. doi: 10.1371/journal.pone.0145138.
17. de Boer JD, Van't Veer C, Stroo I, van der Meer AJ, de Vos AF, van der Zee JS, Roelofs JJ, van der Poll T. Protease-activated receptor-2 deficient mice have reduced house dust mite-evoked allergic lung inflammation. Innate Immun. 2014;20:618-625. doi: 10.1177/1753425913503387.
18. Boulaftali Y, Hess PR, Getz TM, Cholka A, Stolla M, Mackman N, Owens AP III, Ware J, Kahn ML, Bergmeier W. Platelet ITAM signaling is critical for vascular integrity in inflammation. J Clin Invest. 2013;123:908-916. doi: 10.1172/JCI65154.
19. Brinkmann V, Abu Abed U, Goosmann C, Zychlinsky A. Immunodetection of NETs in paraffin-embedded tissue. Front Immunol. 2016;7:513. doi: 10.3389/fimmu.2016.00513.
20. Deppermann C, Cherpokova D, Nurden P, et al. Gray platelet syndrome and defective thrombo-inflammation in nbeal2-deficient mice. J Clin Invest. 2013;123:3331-3342.
21. Kahr WH, Lo RW, Li L, Pluthero FG, Christensen H, Ni R, Vaezzadeh N, Hawkins CE, Weyrich AS, Di Paola J, Landolt-Marticorena C, Gross PL. Abnormal megakaryocyte development and platelet function in Nbeal2(-/-) mice. Blood. 2013;122:3349-3358. doi: 10.1182/blood-2013-04-499491.
22. Gunay-Aygun M, Falik-Zaccai TC, Vilboux T, et al. NBEAL2 is mutated in gray platelet syndrome and is required for biogenesis of platelet α-granules. Nat Genet. 2011;43:732-734. doi: 10.1038/ng.883.
23. Xiong H, Carter RA, Leiner IM, Tang YW, Chen L, Kreiswirth BN, Pamer EG. Distinct contributions of neutrophils and CCR2+ monocytes to pulmonary clearance of different klebsiella pneumoniae strains. Infect Immun. 2015;83:3418-3427. doi: 10.1128/IAI.00678-15.
24. Papayannopoulos V. Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol. 2018;18:134-147. doi: 10.1038/nri. 2017.105.
25. Claushuis TA, de Stoppelaar SF, Stroo I, Roelofs JJ, Ottenhoff R, van der Poll T, Van't Veer C. Thrombin contributes to protective immunity in pneumonia-derived sepsis via fibrin polymerization and platelet-neutrophil interactions. J Thromb Haemost. 2017;15:744-757. doi: 10.1111/jth.13625.
26. Greco E, Lupia E, Bosco O, Vizio B, Montrucchio G. Platelets and multi-organ failure in sepsis. Int J Mol Sci. 2017;18:2200.
27. Levi M, van der Poll T. Coagulation and sepsis. Thromb Res. 2017;149:38-44. doi: 10.1016/j.thromres.2016.11.007.
28. Thomas MR, Storey RF. Effect of P2Y12 inhibitors on inflammation and immunity. Thromb Haemost. 2015;114:490-497.
29. Mayer L, Jasztal M, Pardo M, et al. Nbeal2 interacts with Dock7, Sec16a, and Vac14. Blood. 2018;131:1000-1011. doi: 10.1182/blood-2017-08-800359.
30. Gunay-Aygun M, Zivony-Elboum Y, Gumruk F, et al. Gray platelet syndrome: natural history of a large patient cohort and locus assignment to chromosome 3p. Blood. 2010;116:4990-5001. doi: 10.1182/blood-2010-05-286534.
31. Belaaouaj A, McCarthy R, Baumann M, Gao Z, Ley TJ, Abraham SN, Shapiro SD. Mice lacking neutrophil elastase reveal impaired host defense against gram negative bacterial sepsis. Nat Med. 1998;4:615-618.
32. Aratani Y, Kura F, Watanabe H, Akagawa H, Takano Y, Suzuki K, Maeda N, Koyama H. Differential host susceptibility to pulmonary infections with bacteria and fungi in mice deficient in myeloperoxidase. J Infect Dis. 2000;182:1276-1279. doi: 10.1086/315843.
33. Kolaczkowska E, Jenne CN, Surewaard BG, Thanabalasuriar A, Lee WY, Sanz MJ, Mowen K, Opdenakker G, Kubes P. Molecular mechanisms of NET formation and degradation revealed by intravi-tal imaging in the liver vasculature. Nat Commun. 2015;6:6673. doi: 10.1038/ncomms7673.
34. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol. 2005;77:598-625. doi: 10.1189/jlb.1204697.
35. Wong CH, Jenne CN, Petri B, Chrobok NL, Kubes P. Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat Immunol. 2013;14:785-792. doi: 10.1038/ni.2631.
36. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13:463-469. doi: 10.1038/nm1565.
37. Claushuis TAM, de Vos AF, Nieswandt B, Boon L, Roelofs J, de Boer OJ, van 't Veer CJ, van der Poll T. Platelet glycoprotein VI aids in local immunity during gram-negative pneumonia derived sepsis. Blood. 2018;131:864-876.
38. Kasper B, Brandt E, Brandau S, Petersen F. Platelet factor 4 (CXC chemokine ligand 4) differentially regulates respiratory burst, survival, and cytokine expression of human monocytes by using distinct signaling pathways. J Immunol. 2007;179:2584-2591.
39. Scheuerer B, Ernst M, Dürrbaum-Landmann I, Fleischer J, Grage-Griebenow E, Brandt E, Flad HD, Petersen F. The CXC-chemokine platelet factor 4 promotes monocyte survival and induces monocyte differentiation into macrophages. Blood. 2000;95:1158-1166.
40. de Stoppelaar SF, Van't Veer C, Roelofs JJ, Claushuis TA, de Boer OJ, Tanck MW, Hoogendijk AJ, van der Poll T. Platelet and endothelial cell P-selectin are required for host defense against Klebsiella pneumoniae-induced pneumosepsis. J Thromb Haemost. 2015;13:1128-1138. doi: 10.1111/ jth.12893.
41. Deppermann C, Kraft P, Volz J, Schuhmann MK, Beck S, Wolf K, Stegner D, Stoll G, Nieswandt B. Platelet secretion is crucial to prevent bleeding in the ischemic brain but not in the inflamed skin or lung in mice. Blood. 2017;129:1702-1706. doi: 10.1182/blood-2016-12-750711.
42. Guerrero JA, Bennett C, van der Weyden L, McKinney H, Chin M, Nurden P, McIntyre Z, Cambridge EL, Estabel J, Wardle-Jones H, Speak AO, Erber WN, Rendon A, Ouwehand WH, Ghevaert C. Gray platelet syndrome: proinflammatory megakaryocytes and α-granule loss cause myelofibro-sis and confer metastasis resistance in mice. Blood. 2014;124:3624-3635. doi: 10.1182/blood-2014-04-566760.